Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Biomedical Reports
Join Editorial Board Propose a Special Issue
Print ISSN: 2049-9434 Online ISSN: 2049-9442
Journal Cover
February-2024 Volume 20 Issue 2

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
February-2024 Volume 20 Issue 2

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Review Open Access

Regulation of cancer stem cells and immunotherapy of glioblastoma (Review)

  • Authors:
    • Аleksandra Kosianova
    • Oleg Pak
    • Igor Bryukhovetskiy
  • View Affiliations / Copyright

    Affiliations: Medical Center, School of Medicine and Life Science, Far Eastern Federal University, Vladivostok 690091, Russian Federation
    Copyright: © Kosianova et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 24
    |
    Published online on: December 19, 2023
       https://doi.org/10.3892/br.2023.1712
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Glioblastoma (GB) is one of the most adverse diagnoses in oncology. Complex current treatment results in a median survival of 15 months. Resistance to treatment is associated with the presence of cancer stem cells (CSCs). The present review aimed to analyze the mechanisms of CSC plasticity, showing the particular role of β‑catenin in regulating vital functions of CSCs, and to describe the molecular mechanisms of Wnt‑independent increase of β‑catenin levels, which is influenced by the local microenvironment of CSCs. The present review also analyzed the reasons for the low effectiveness of using medication in the regulation of CSCs, and proposed the development of immunotherapy scenarios with tumor cell vaccines, containing heterogenous cancer cells able of producing a multidirectional antineoplastic immune response. Additionally, the possibility of managing lymphopenia by transplanting hematopoietic stem cells from a healthy sibling and using clofazimine or other repurposed drugs that reduce β‑catenin concentration in CSCs was discussed in the present study.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

View References

1 

Herrlinger U: News on the horizon in glioblastoma therapy. ESMO Open. 5(e000601)2020.PubMed/NCBI View Article : Google Scholar

2 

Schaff LR and Mellinghoff IK: Glioblastoma and other primary brain malignancies in adults: A review. JAMA. 329:574–587. 2023.PubMed/NCBI View Article : Google Scholar

3 

Delavar A, Wali AR, Santiago-Dieppa DR, Al Jammal OM, Kidwell RL and Khalessi AA: Racial and ethnic disparities in brain tumor survival by age group and tumor type. Br J Neurosurg. 36:705–711. 2022.PubMed/NCBI View Article : Google Scholar

4 

Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, et al: Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-Year analysis of the EORTC-NCIC trial. Lancet Oncol. 10:459–466. 2009.PubMed/NCBI View Article : Google Scholar

5 

Luo C, Song K, Wu S, Hameed NUF, Kudulaiti N, Xu H, Qin ZY and Wu JS: The prognosis of glioblastoma: A large, multifactorial study. Br J Neurosurg. 35:555–561. 2021.PubMed/NCBI View Article : Google Scholar

6 

Yabo YA, Niclou SP and Golebiewska A: Cancer cell heterogeneity and plasticity: A paradigm shift in glioblastoma. Neuro Oncol. 24:669–682. 2022.PubMed/NCBI View Article : Google Scholar

7 

Bikfalvi A, da Costa CA, Avril T, Barnier JV, Bauchet L, Brisson L, Cartron PF, Castel H, Chevet E, Chneiweiss H, et al: Challenges in glioblastoma research: Focus on the tumor microenvironment. Trends Cancer. 9:9–27. 2023.PubMed/NCBI View Article : Google Scholar

8 

Huang M, Zhang D, Wu JY, Xing K, Yeo E, Li C, Zhang L, Holland E, Yao L, Qin L, et al: Wnt-mediated endothelial transformation into mesenchymal stem cell-like cells induces chemoresistance in glioblastoma. Sci Transl Med. 12(eaay7522)2020.PubMed/NCBI View Article : Google Scholar

9 

Barzegar Behrooz A, Talaie Z, Jusheghani F, Łos MJ, Klonisch T and Ghavami S: Wnt and PI3K/Akt/mTOR survival pathways as therapeutic targets in glioblastoma. Int J Mol Sci. 23(1353)2022.PubMed/NCBI View Article : Google Scholar

10 

Behrooz AB and Syahir A: Could we address the interplay between CD133, Wnt/β-catenin, and TERT signaling pathways as a potential target for glioblastoma therapy? Front Oncol. 11(642719)2021.PubMed/NCBI View Article : Google Scholar

11 

Crunkhorn S: Targeting drug-resistant glioblastoma. Nat Rev Drug Discov. 21(711)2022.PubMed/NCBI View Article : Google Scholar

12 

Precilla DS, Kuduvalli SS, Purushothaman M, Marimuthu P, Muralidharan AR and Anitha TS: Wnt/β-catenin antagonists: Exploring new avenues to trigger old drugs in alleviating glioblastoma multiforme. Curr Mol Pharmacol. 15:338–360. 2022.PubMed/NCBI View Article : Google Scholar

13 

Yuan B, Wang G, Tang X, Tong A and Zhou L: Immunotherapy of glioblastoma: Recent advances and future prospects. Hum Vaccin Immunother. 18(2055417)2022.PubMed/NCBI View Article : Google Scholar

14 

Youngblood MW, Stupp R and Sonabend AM: Role of Resection in glioblastoma management. Neurosurg Clin N Am. 32:9–22. 2021.PubMed/NCBI View Article : Google Scholar

15 

De Biase G, Garcia DP, Bohnen A and Quiñones-Hinojosa A: Perioperative management of patients with glioblastoma. Neurosurg Clin N Am. 32:1–8. 2021.PubMed/NCBI View Article : Google Scholar

16 

Lu VM, Goyal A, Graffeo CS, Perry A, Burns TC, Parney IF, Quinones-Hinojosa A and Chaichana KL: Survival benefit of maximal resection for glioblastoma reoperation in the temozolomide era: A meta-analysis. World Neurosurg. 127:31–37. 2019.PubMed/NCBI View Article : Google Scholar

17 

Robin AM, Lee I and Kalkanis SN: Reoperation for recurrent glioblastoma multiforme. Neurosurg Clin N Am. 28:407–428. 2017.PubMed/NCBI View Article : Google Scholar

18 

Liang C, Gong J, Zhang B, Meng Z, Li M and Guo Y: Multiple subtentorial metastasis in diffuse midline glioma receiving tumor treating fields: A case report and literature review. Ann Transl Med. 9(1604)2021.PubMed/NCBI View Article : Google Scholar

19 

Chen J, Shi Q, Li S, Zhao Y and Huang H: Clinical characteristics of glioblastoma with metastatic spinal dissemination. Ann Palliat Med. 11:506–512. 2022.PubMed/NCBI View Article : Google Scholar

20 

Shah AH, Mahavadi A, Di L, Sanjurjo A, Eichberg DG, Borowy V, Figueroa J, Luther E, de la Fuente MI, Semonche A, et al: Survival benefit of lobectomy for glioblastoma: Moving towards radical supramaximal resection. J Neurooncol. 148:501–508. 2020.PubMed/NCBI View Article : Google Scholar

21 

Ryan JT, Nakayama M, Gleeson I, Mannion L, Geso M, Kelly J, Ng SP and Hardcastle N: Functional brain imaging interventions for radiation therapy planning in patients with glioblastoma: A systematic review. Radiat Oncol. 17(178)2022.PubMed/NCBI View Article : Google Scholar

22 

Ylanan AMD, Pascual JSG, Cruz-Lim EMD, Ignacio KHD, Cañal JPA and Khu KJO: Intraoperative radiotherapy for glioblastoma: A systematic review of techniques and outcomes. J Clin Neurosci. 93:36–41. 2021.PubMed/NCBI View Article : Google Scholar

23 

Khan L, Soliman H, Sahgal A, Perry J, Xu W and Tsao MN: External beam radiation dose escalation for high grade glioma. Cochrane Database Syst Rev. 5(CD011475)2020.PubMed/NCBI View Article : Google Scholar

24 

Barbarite E, Sick JT, Berchmans E, Bregy A, Shah AH, Elsayyad N and Komotar RJ: The role of brachytherapy in the treatment of glioblastoma multiforme. Neurosurg Rev. 40:195–211. 2017.PubMed/NCBI View Article : Google Scholar

25 

Vogelius IR and Bentzen SM: Proton vs photon radiation therapy for glioblastoma: Maximizing information from trial. Neuro Oncol. 24:849–850. 2022.PubMed/NCBI View Article : Google Scholar

26 

Malouff TD, Seneviratne DS, Ebner DK, Stross WC, Waddle MR, Trifiletti DM and Krishnan S: Boron Neutron capture therapy: A review of clinical applications. Front Oncol. 11(601820)2021.PubMed/NCBI View Article : Google Scholar

27 

Laprie A, Tensaouti F and Cohen-Jonathan Moyal E: Radiation dose intensification for glioblastoma. Cancer Radiother. 26:894–898. 2022.PubMed/NCBI View Article : Google Scholar : (In French).

28 

Tan AC, Ashley DM, López GY, Malinzak M, Friedman HS and Khasraw M: Management of glioblastoma: State of the art and future directions. CA Cancer J Clin. 70:299–312. 2020.PubMed/NCBI View Article : Google Scholar

29 

Woodroffe RW, Zanaty M, Soni N, Mott SL, Helland LC, Pasha A, Maley J, Dhungana N, Jones KA, Monga V and Greenlee JDW: Survival after reoperation for recurrent glioblastoma. J Clin Neurosci. 73:118–124. 2020.PubMed/NCBI View Article : Google Scholar

30 

Zakaria R and Weinberg JS: Challenges associated with reoperation in patients with glioma. Neurosurg Clin N Am. 32:129–135. 2021.PubMed/NCBI View Article : Google Scholar

31 

Mathen P, Rowe L, Mackey M, Smart D, Tofilon P and Camphausen K: Radiosensitizers in the temozolomide era for newly diagnosed glioblastoma. Neurooncol Pract. 7:268–276. 2020.PubMed/NCBI View Article : Google Scholar

32 

Herrlinger U, Tzaridis T, Mack F, Steinbach JP, Schlegel U, Sabel M, Hau P, Kortmann RD, Krex D, Grauer O, et al: Lomustine-temozolomide combination therapy versus standard temozolomide therapy in patients with newly diagnosed glioblastoma with methylated MGMT promoter (CeTeG/NOA-09): A randomised, open-label, phase 3 trial. Lancet. 393:678–688. 2019.PubMed/NCBI View Article : Google Scholar

33 

Hwang K, Lee JH, Kim SH, Go KO, Ji SY, Han JH and Kim CY: The combination PARP inhibitor olaparib with temozolomide in an experimental glioblastoma model. In Vivo. 35:2015–2023. 2021.PubMed/NCBI View Article : Google Scholar

34 

Nguyen TTT, Zhang Y, Shang E, Shu C, Torrini C, Zhao J, Bianchetti E, Mela A, Humala N, Mahajan A, et al: HDAC inhibitors elicit metabolic reprogramming by targeting super-enhancers in glioblastoma models. J Clin Invest. 130:3699–3716. 2020.PubMed/NCBI View Article : Google Scholar

35 

Bindra RS: Penetrating the brain tumor space with DNA damage response inhibitors. Neuro Oncol. 22:1718–1720. 2020.PubMed/NCBI View Article : Google Scholar

36 

Zhao J, Yang S, Cui X, Wang Q, Yang E, Tong F, Hong B, Xiao M, Xin L, Xu C, et al: A novel compound EPIC-0412 reverses temozolomide resistance via inhibiting DNA repair/MGMT in glioblastoma. Neuro Oncol. 25:857–870. 2023.PubMed/NCBI View Article : Google Scholar

37 

Goel NJ, Bird CE, Hicks WH and Abdullah KG: Economic implications of the modern treatment paradigm of glioblastoma: An analysis of global cost estimates and their utility for cost assessment. J Med Econ. 24:1018–1024. 2021.PubMed/NCBI View Article : Google Scholar

38 

Lauko A, Lo A, Ahluwalia MS and Lathia JD: Cancer cell heterogeneity & plasticity in glioblastoma and brain tumors. Semin Cancer Biol. 82:162–175. 2022.PubMed/NCBI View Article : Google Scholar

39 

Oliver L, Lalier L, Salaud C, Heymann D, Cartron PF and Vallette FM: Drug resistance in glioblastoma: Are persisters the key to therapy? Cancer Drug Resist. 3:287–301. 2020.PubMed/NCBI View Article : Google Scholar

40 

Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, et al: Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 17:98–110. 2010.PubMed/NCBI View Article : Google Scholar

41 

Steponaitis G and Tamasauskas A: Mesenchymal and proneural subtypes of glioblastoma disclose branching based on GSC associated signature. Int J Mol Sci. 22(4964)2021.PubMed/NCBI View Article : Google Scholar

42 

Brennan CW, Verhaak RG, McKenna A, Campos B, Noushmehr H, Salama SR, Zheng S, Chakravarty D, Sanborn JZ, Berman SH, et al: The somatic genomic landscape of glioblastoma. Cell. 155:462–477. 2013.PubMed/NCBI View Article : Google Scholar

43 

Melhem JM, Detsky J, Lim-Fat MJ and Perry JR: Updates in IDH-wildtype glioblastoma. Neurotherapeutics. 19:1705–1723. 2022.PubMed/NCBI View Article : Google Scholar

44 

French R and Pauklin S: Epigenetic regulation of cancer stem cell formation and maintenance. Int J Cancer. 148:2884–2897. 2021.PubMed/NCBI View Article : Google Scholar

45 

Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P and Ellison DW: The 2016 World Health Organization classification of tumors of the central nervous system: A summary. Acta Neuropathol. 131:803–820. 2016.PubMed/NCBI View Article : Google Scholar

46 

Capper D, Stichel D, Sahm F, Jones DTW, Schrimpf D, Sill M, Schmid S, Hovestadt V, Reuss DE, Koelsche C, et al: Practical implementation of DNA methylation and copy-number-based CNS tumor diagnostics: The Heidelberg experience. Acta Neuropathol. 136:181–210. 2018.PubMed/NCBI View Article : Google Scholar

47 

Neftel C, Laffy J, Filbin MG, Hara T, Shore ME, Rahme GJ, Richman AR, Silverbush D, Shaw ML, Hebert CM, et al: An integrative model of cellular states, plasticity, and genetics for glioblastoma. Cell. 178:835–849.e21. 2019.PubMed/NCBI View Article : Google Scholar

48 

Garofano L, Migliozzi S, Oh YT, D'Angelo F, Najac RD, Ko A, Frangaj B, Caruso FP, Yu K, Yuan J, et al: Pathway-based classification of glioblastoma uncovers a mitochondrial subtype with therapeutic vulnerabilities. Nat Cancer. 2:141–156. 2021.PubMed/NCBI View Article : Google Scholar

49 

Hubert CG and Lathia JD: Seeing the GBM diversity spectrum. Nat Cancer. 2:135–137. 2021.PubMed/NCBI View Article : Google Scholar

50 

Richards LM, Whitley OKN, MacLeod G, Cavalli FMG, Coutinho FJ, Jaramillo JE, Svergun N, Riverin M, Croucher DC, Kushida M, et al: Gradient of developmental and injury response transcriptional states defines functional vulnerabilities underpinning glioblastoma heterogeneity. Nat Cancer. 2:157–173. 2021.PubMed/NCBI View Article : Google Scholar

51 

Ensenyat-Mendez M, Íñiguez-Muñoz S, Sesé B and Marzese DM: iGlioSub: An integrative transcriptomic and epigenomic classifier for glioblastoma molecular subtypes. BioData Min. 14(42)2021.PubMed/NCBI View Article : Google Scholar

52 

Wang LB, Karpova A, Gritsenko MA, Kyle JE, Cao S, Li Y, Rykunov D, Colaprico A, Rothstein JH, Hong R, et al: Proteogenomic and metabolomic characterization of human glioblastoma. Cancer Cell. 39:509–528.e20. 2021.PubMed/NCBI View Article : Google Scholar

53 

Drakulic D, Schwirtlich M, Petrovic I, Mojsin M, Milivojevic M, Kovacevic-Grujicic N and Stevanovic M: Current opportunities for targeting dysregulated neurodevelopmental signaling pathways in glioblastoma. Cells. 11(2530)2022.PubMed/NCBI View Article : Google Scholar

54 

Bonnet D and Dick JE: Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 3:730–737. 1997.PubMed/NCBI View Article : Google Scholar

55 

Walcher L, Kistenmacher AK, Suo H, Kitte R, Dluczek S, Strauß A, Blaudszun AR, Yevsa T, Fricke S and Kossatz-Boehlert U: Cancer stem cells-origins and biomarkers: Perspectives for targeted personalized therapies. Front Immunol. 11(1280)2020.PubMed/NCBI View Article : Google Scholar

56 

Bryukhovetskiy A, Shevchenko V, Kovalev S, Chekhonin V, Baklaushev V, Bryukhovetskiy I and Zhukova M: To the novel paradigm of proteome-based cell therapy of tumors: Through comparative proteome mapping of tumor stem cells and tissue-specific stem cells of humans. Cell Transplant. 23 (Suppl 1):S151–S170. 2014.PubMed/NCBI View Article : Google Scholar

57 

Bryukhovetskiy IS, Dyuizen IV, Shevchenko VE, Bryukhovetskiy AS, Mischenko PV, Milkina EV and Khotimchenko YS: Hematopoietic stem cells as a tool for the treatment of glioblastoma multiforme. Mol Med Rep. 14:4511–4520. 2016.PubMed/NCBI View Article : Google Scholar

58 

Couturier CP, Nadaf J, Li Z, Baig S, Riva G, Le P, Kloosterman DJ, Monlong J, Nkili Meyong A, Allache R, et al: Glioblastoma scRNA-seq shows treatment-induced, immune-dependent increase in mesenchymal cancer cells and structural variants in distal neural stem cells. Neuro Oncol. 24:1494–1508. 2022.PubMed/NCBI View Article : Google Scholar

59 

Wang X, Zhou R, Xiong Y, Zhou L, Yan X, Wang M, Li F, Xie C, Zhang Y, Huang Z, et al: Sequential fate-switches in stem-like cells drive the tumorigenic trajectory from human neural stem cells to malignant glioma. Cell Res. 31:684–702. 2021.PubMed/NCBI View Article : Google Scholar

60 

Mizrak D, Brittan M and Alison M: CD133: Molecule of the moment. J Pathol. 214:3–9. 2008.PubMed/NCBI View Article : Google Scholar

61 

Zheng Y, Wang L, Yin L, Yao Z, Tong R, Xue J and Lu Y: Lung cancer stem cell markers as therapeutic targets: An update on signaling pathways and therapies. Front Oncol. 12(873994)2022.PubMed/NCBI View Article : Google Scholar

62 

Park J, Kim SK, Hallis SP, Choi BH and Kwak MK: Role of CD133/NRF2 axis in the development of colon cancer stem cell-like properties. Front Oncol. 11(808300)2022.PubMed/NCBI View Article : Google Scholar

63 

Hefni AM, Sayed AM, Hussien MT, Abdalla AZ and Gabr AG: CD133 is an independent predictive and prognostic marker in metastatic breast cancer. Cancer Biomark. 35:207–215. 2022.PubMed/NCBI View Article : Google Scholar

64 

Gimple RC, Bhargava S, Dixit D and Rich JN: Glioblastoma stem cells: Lessons from the tumor hierarchy in a lethal cancer. Genes Dev. 33:591–609. 2019.PubMed/NCBI View Article : Google Scholar

65 

Beier CP and Beier D: CD133 negative cancer stem cells in glioblastoma. Front Biosci (Elite Ed). 3:701–710. 2011.PubMed/NCBI View Article : Google Scholar

66 

Wang Z, Zhang H, Xu S, Liu Z and Cheng Q: The adaptive transition of glioblastoma stem cells and its implications on treatments. Signal Transduct Target Ther. 6(124)2021.PubMed/NCBI View Article : Google Scholar

67 

Xie XP, Laks DR, Sun D, Ganbold M, Wang Z, Pedraza AM, Bale T, Tabar V, Brennan C, Zhou X and Parada LF: Quiescent human glioblastoma cancer stem cells drive tumor initiation, expansion, and recurrence following chemotherapy. Dev Cell. 57:32–46.e8. 2022.PubMed/NCBI View Article : Google Scholar

68 

Liu J, Gao L, Zhan N, Xu P, Yang J, Yuan F, Xu Y, Cai Q, Geng R and Chen Q: Hypoxia induced ferritin light chain (FTL) promoted epithelia mesenchymal transition and chemoresistance of glioma. J Exp Clin Cancer Res. 39(137)2020.PubMed/NCBI View Article : Google Scholar

69 

Gao L, Tong S, Liu J, Cai J, Ye Z, Zhou L, Song P, Li Z, Lei P, Wei H, et al: TMEM2 induces epithelial-mesenchymal transition and promotes resistance to temozolomide in GBM cells. Heliyon. 9(e16559)2023.PubMed/NCBI View Article : Google Scholar

70 

Zhang X, Wang X, Xu R, Ji J, Xu Y, Han M, Wei Y, Huang B, Chen A, Zhang Q, et al: YM155 decreases radiation-induced invasion and reverses epithelial-mesenchymal transition by targeting STAT3 in glioblastoma. J Transl Med. 16(79)2018.PubMed/NCBI View Article : Google Scholar

71 

Zhang X, Wang X, Xu R, Ji J, Xu Y, Han M, Wei Y, Huang B, Chen A, Zhang Q, et al: Correction to: YM155 decreases radiation-induced invasion and reverses epithelial-mesenchymal transition by targeting STAT3 in glioblastoma. J Transl Med. 19(407)2021.PubMed/NCBI View Article : Google Scholar

72 

Huang W, Zhang C, Cui M, Niu J and Ding W: Inhibition of bevacizumab-induced epithelial-mesenchymal transition by BATF2 overexpression involves the suppression of Wnt/β-catenin signaling in glioblastoma cells. Anticancer Res. 37:4285–4294. 2017.PubMed/NCBI View Article : Google Scholar

73 

Coelho BP, Fernandes CFL, Boccacino JM, Souza MCDS, Melo-Escobar MI, Alves RN, Prado MB, Iglesia RP, Cangiano G, Mazzaro GR and Lopes MH: Multifaceted WNT signaling at the crossroads between epithelial-mesenchymal transition and autophagy in glioblastoma. Front Oncol. 10(597743)2020.PubMed/NCBI View Article : Google Scholar

74 

Alkailani MI, Aittaleb M and Tissir F: WNT signaling at the intersection between neurogenesis and brain tumorigenesis. Front Mol Neurosci. 15(1017568)2022.PubMed/NCBI View Article : Google Scholar

75 

Rajakulendran N, Rowland KJ, Selvadurai HJ, Ahmadi M, Park NI, Naumenko S, Dolma S, Ward RJ, So M, Lee L, et al: Wnt and Notch signaling govern self-renewal and differentiation in a subset of human glioblastoma stem cells. Genes Dev. 33:498–510. 2019.PubMed/NCBI View Article : Google Scholar

76 

Rim EY, Clevers H and Nusse R: The Wnt pathway: From signaling mechanisms to synthetic modulators. Annu Rev Biochem. 91:571–598. 2022.PubMed/NCBI View Article : Google Scholar

77 

Sareddy GR, Pratap UP, Viswanadhapalli S, Venkata PP, Nair BC, Krishnan SR, Zheng S, Gilbert AR, Brenner AJ, Brann DW and Vadlamudi RK: PELP1 promotes glioblastoma progression by enhancing Wnt/β-catenin signaling. Neurooncol Adv. 1(vdz042)2019.PubMed/NCBI View Article : Google Scholar

78 

Latour M, Her NG, Kesari S and Nurmemmedov E: WNT signaling as a therapeutic target for glioblastoma. Int J Mol Sci. 22(8428)2021.PubMed/NCBI View Article : Google Scholar

79 

Tang C, Guo J, Chen H, Yao CJ, Zhuang DX, Wang Y, Tang WJ, Ren G, Yao Y, Wu JS, et al: Gene mutation profiling of primary glioblastoma through multiple tumor biopsy guided by 1H-magnetic resonance spectroscopy. Int J Clin Exp Pathol. 8:5327–5335. 2015.PubMed/NCBI

80 

Morris LG, Ramaswami D and Chan TA: The FAT epidemic: A gene family frequently mutated across multiple human cancer types. Cell Cycle. 12:1011–1012. 2013.PubMed/NCBI View Article : Google Scholar

81 

Fargeas CA, Lorico A and Corbeil D: Commentary: Could we address the interplay between CD133, Wnt/β-catenin, and TERT signaling pathways as a potential target for glioblastoma therapy? Front Oncol. 11(712358)2021.PubMed/NCBI View Article : Google Scholar

82 

Shevchenko V, Arnotskaya N, Zaitsev S, Sharma A, Sharma HS, Bryukhovetskiy A, Pak O, Khotimchenko Y and Bryukhovetskiy I: Proteins of Wnt signaling pathway in cancer stem cells of human glioblastoma. Int Rev Neurobiol. 151:185–200. 2020.PubMed/NCBI View Article : Google Scholar

83 

Manoranjan B, Chokshi C, Venugopal C, Subapanditha M, Savage N, Tatari N, Provias JP, Murty NK, Moffat J, Doble BW and Singh SK: A CD133-AKT-Wnt signaling axis drives glioblastoma brain tumor-initiating cells. Oncogene. 39:1590–1599. 2020.PubMed/NCBI View Article : Google Scholar

84 

Jhanwar-Uniyal M, Wainwright JV, Mohan AL, Tobias ME, Murali R, Gandhi CD and Schmidt MH: Diverse signaling mechanisms of mTOR complexes: mTORC1 and mTORC2 in forming a formidable relationship. Adv Biol Regul. 72:51–62. 2019.PubMed/NCBI View Article : Google Scholar

85 

Shahcheraghi SH, Tchokonte-Nana V, Lotfi M, Lotfi M, Ghorbani A and Sadeghnia HR: Wnt/beta-catenin and PI3K/Akt/mTOR signaling pathways in glioblastoma: Two main targets for drug design: A review. Curr Pharm Des. 26:1729–1741. 2020.PubMed/NCBI View Article : Google Scholar

86 

Liu N, Guo XH, Liu JP and Cong YS: Role of telomerase in the tumor microenvironment. Clin Exp Pharmacol Physiol. 47:357–364. 2020.PubMed/NCBI View Article : Google Scholar

87 

Abad E, Graifer D and Lyakhovich A: DNA damage response and resistance of cancer stem cells. Сancer Lett. 474:106–117. 2020.PubMed/NCBI View Article : Google Scholar

88 

Fan D, Yue Q, Chen J, Wang C, Yu R, Jin Z, Yin S, Wang Q, Chen L, Liao X, et al: Reprogramming the immunosuppressive microenvironment of IDH1 wild-type glioblastoma by blocking Wnt signaling between microglia and cancer cells. Oncoimmunology. 10(1932061)2021.PubMed/NCBI View Article : Google Scholar

89 

Hao J, Han X, Huang H, Yu X, Fang J, Zhao J, Prayson RA, Bao S and Yu JS: Sema3C signaling is an alternative activator of the canonical WNT pathway in glioblastoma. Nat Commun. 14(2262)2023.PubMed/NCBI View Article : Google Scholar

90 

Montemurro N, Pahwa B, Tayal A, Shukla A, De Jesus Encarnacion M, Ramirez I, Nurmukhametov R, Chavda V and De Carlo A: Macrophages in recurrent glioblastoma as a prognostic factor in the synergistic system of the tumor microenvironment. Neurol Int. 15:595–608. 2023.PubMed/NCBI View Article : Google Scholar

91 

Chan MK, Chung JY, Tang PC, Chan AS, Ho JY, Lin TP, Chen J, Leung KT, To KF, Lan HY and Tang PM: TGF-β signaling networks in the tumor microenvironment. Cancer Lett. 550(215925)2022.PubMed/NCBI View Article : Google Scholar

92 

Yun EJ, Kim S, Hsieh JT and Baek ST: Wnt/β-catenin signaling pathway induces autophagy-mediated temozolomide-resistance in human glioblastoma. Cell Death Dis. 11(771)2020.PubMed/NCBI View Article : Google Scholar

93 

Matias D, Predes D, Niemeyer Filho P, Lopes MC, Abreu JG, Lima FRS and Moura Neto V: Microglia-glioblastoma interactions: New role for Wnt signaling. Biochim Biophys Acta Rev Cancer. 1868:333–340. 2017.PubMed/NCBI View Article : Google Scholar

94 

Tao W, Chu C, Zhou W, Huang Z, Zhai K, Fang X, Huang Q, Zhang A, Wang X, Yu X, et al: Dual role of WISP1 in maintaining glioma stem cells and tumor-supportive macrophages in glioblastoma. Nat Commun. 11(3015)2020.PubMed/NCBI View Article : Google Scholar

95 

Bayik D and Lathia JD: Cancer stem cell-immune cell crosstalk in tumor progression. Nat Rev Cancer. 21:526–536. 2021.PubMed/NCBI View Article : Google Scholar

96 

Omuro A: Immune-checkpoint inhibitors for glioblastoma: What have we learned? Arq Neuropsiquiatr. 80 (5 Suppl 1):S266–S269. 2022.PubMed/NCBI View Article : Google Scholar

97 

Verdugo E, Puerto I and Medina MÁ: An update on the molecular biology of glioblastoma, with clinical implications and progress in its treatment. Cancer Commun (Lond). 42:1083–1111. 2022.PubMed/NCBI View Article : Google Scholar

98 

Sautter L, Hofheinz R, Tuettenberg J, Grimm M, Vajkoczy P, Groden C, Schmieder K, Hochhaus A, Wenz F and Giordano FA: Open-label phase II evaluation of imatinib in primary inoperable or incompletely resected and recurrent glioblastoma. Oncology. 98:16–22. 2020.PubMed/NCBI View Article : Google Scholar

99 

Kim JY, Jo Y, Oh HK and Kim EH: Sorafenib increases tumor treating fields-induced cell death in glioblastoma by inhibiting STAT3. Am J Cancer Res. 10:3475–3486. 2020.PubMed/NCBI

100 

Alamón C, Dávila B, García MF, Sánchez C, Kovacs M, Trias E, Barbeito L, Gabay M, Zeineh N, Gavish M, et al: Sunitinib-containing carborane pharmacophore with the ability to inhibit tyrosine kinases receptors FLT3, KIT and PDGFR-β, exhibits powerful in vivo anti-glioblastoma activity. Cancers (Basel). 12(3423)2020.PubMed/NCBI View Article : Google Scholar

101 

Reardon DA, Desjardins A, Vredenburgh JJ, O'Rourke DM, Tran DD, Fink KL, Nabors LB, Li G, Bota DA, Lukas RV, et al: Rindopepimut with bevacizumab for patients with relapsed EGFRvIII-expressing glioblastoma (ReACT): Results of a double-blind randomized phase II trial. Clin Cancer Res. 26:1586–1594. 2020.PubMed/NCBI View Article : Google Scholar

102 

Padovan M, Eoli M, Pellerino A, Rizzato S, Caserta C, Simonelli M, Michiara M, Caccese M, Anghileri E, Cerretti G, et al: Depatuxizumab mafodotin (Depatux-M) plus temozolomide in recurrent glioblastoma patients: Real-world experience from a multicenter study of italian association of neuro-oncology (AINO). Cancers (Basel). 13(2773)2021.PubMed/NCBI View Article : Google Scholar

103 

Lassman AB, Pugh SL, Wang TJC, Aldape K, Gan HK, Preusser M, Vogelbaum MA, Sulman EP, Won M, Zhang P, et al: Depatuxizumab mafodotin in EGFR-amplified newly diagnosed glioblastoma: A phase III randomized clinical trial. Neuro Oncol. 25:339–350. 2023.PubMed/NCBI View Article : Google Scholar

104 

Cloughesy T, Finocchiaro G, Belda-Iniesta C, Recht L, Brandes AA, Pineda E, Mikkelsen T, Chinot OL, Balana C, Macdonald DR, et al: Randomized, double-blind, placebo-controlled, multicenter phase II study of onartuzumab plus bevacizumab versus placebo plus bevacizumab in patients with recurrent glioblastoma: efficacy, safety, and hepatocyte growth factor and O6-methylguanine-DNA methyltransferase biomarker analyses. J Clin Oncol. 35:343–351. 2017.PubMed/NCBI View Article : Google Scholar

105 

Cloughesy TF, Drappatz J, de Groot J, Prados MD, Reardon DA, Schiff D, Chamberlain M, Mikkelsen T, Desjardins A, Ping J, et al: Phase II study of cabozantinib in patients with progressive glioblastoma: Subset analysis of patients with prior antiangiogenic therapy. Neuro Oncol. 20:259–267. 2018.PubMed/NCBI View Article : Google Scholar

106 

Zhang T, Xin Q and Kang JM: Bevacizumab for recurrent glioblastoma: A systematic review and meta-analysis. Eur Rev Med Pharmacol Sci. 25:6480–6491. 2021.PubMed/NCBI View Article : Google Scholar

107 

Wen PY, Rodon JA, Mason W, Beck JT, DeGroot J, Donnet V, Mills D, El-Hashimy M and Rosenthal M: Phase I, open-label, multicentre study of buparlisib in combination with temozolomide or with concomitant radiation therapy and temozolomide in patients with newly diagnosed glioblastoma. ESMO Open. 5(e000673)2020.PubMed/NCBI View Article : Google Scholar

108 

Rosenthal M, Clement PM, Campone M, Gil-Gil MJ, DeGroot J, Chinot O, Idbaih A, Gan H, Raizer J, Wen PY, et al: Buparlisib plus carboplatin or lomustine in patients with recurrent glioblastoma: A phase Ib/II, open-label, multicentre, randomised study. ESMO Open. 5(e000672)2020.PubMed/NCBI View Article : Google Scholar

109 

Kaley TJ, Panageas KS, Pentsova EI, Mellinghoff IK, Nolan C, Gavrilovic I, DeAngelis LM, Abrey LE, Holland EC, Omuro A, et al: Phase I clinical trial of temsirolimus and perifosine for recurrent glioblastoma. Ann Clin Transl Neurol. 7:429–436. 2020.PubMed/NCBI View Article : Google Scholar

110 

Schiff D, Jaeckle KA, Anderson SK, Galanis E, Giannini C, Buckner JC, Stella P, Flynn PJ, Erickson BJ, Schwerkoske JF, et al: Phase 1/2 trial of temsirolimus and sorafenib in the treatment of patients with recurrent glioblastoma: North central cancer treatment group study/alliance N0572. Cancer. 124:1455–1463. 2018.PubMed/NCBI View Article : Google Scholar

111 

Lin Z, Xu H, Yang R, Li Z, Zheng H, Zhang Z, Peng J, Zhang X, Qi S, Liu Y and Huang G: Effective treatment of a BRAF V600E-mutant epithelioid glioblastoma patient by vemurafenib: a case report. Anticancer Drugs. 33:100–104. 2022.PubMed/NCBI View Article : Google Scholar

112 

Herrera-Rios D, Li G, Khan D, Tsiampali J, Nickel AC, Aretz P, Hewera M, Suwala AK, Jiang T, Steiger HJ, et al: A computational guided, functional validation of a novel therapeutic antibody proposes Notch signaling as a clinical relevant and druggable target in glioma. Sci Rep. 10(16218)2020.PubMed/NCBI View Article : Google Scholar

113 

Bogdahn U, Hau P, Stockhammer G, Venkataramana NK, Mahapatra AK, Suri A, Balasubramaniam A, Nair S, Oliushine V, Parfenov V, et al: Targeted therapy for high-grade glioma with the TGF-β2 inhibitor trabedersen: Results of a randomized and controlled phase IIb study. Neuro Oncol. 13:132–142. 2011.PubMed/NCBI View Article : Google Scholar

114 

Hadizadeh M, AminJafari A, Parvizpour S and Ghasemi S: Novel targets to overcome antiangiogenesis therapy resistance in glioblastoma multiforme: Systems biology approach and suggestion of therapy by galunisertib. Cell Biol Int. 46:1649–1660. 2022.PubMed/NCBI View Article : Google Scholar

115 

Wick A, Desjardins A, Suarez C, Forsyth P, Gueorguieva I, Burkholder T, Cleverly AL, Estrem ST, Wang S, Lahn MM, et al: Phase 1b/2a study of galunisertib, a small molecule inhibitor of transforming growth factor-beta receptor I, in combination with standard temozolomide-based radiochemotherapy in patients with newly diagnosed malignant glioma. Invest New Drugs. 38:1570–1579. 2020.PubMed/NCBI View Article : Google Scholar

116 

Hsu SY, Lee SC, Liu HC, Peng SF, Chueh FS, Lu TJ, Lee HT and Chou YC: Phenethyl isothiocyanate suppresses the proinflammatory cytokines in human glioblastoma cells through the PI3K/Akt/NF-κB signaling pathway in vitro. Oxid Med Cell Longev. 2022(2108289)2022.PubMed/NCBI View Article : Google Scholar

117 

Li S, He Y, Chen K, Sun J, Zhang L, He Y, Yu H and Li Q: RSL3 drives ferroptosis through NF-κB pathway activation and GPX4 depletion in glioblastoma. Oxid Med Cell Longev. 2021(2915019)2021.PubMed/NCBI View Article : Google Scholar

118 

Volmar MNM, Cheng J, Alenezi H, Richter S, Haug A, Hassan Z, Goldberg M, Li Y, Hou M, Herold-Mende C, et al: Cannabidiol converts NF-κB into a tumor suppressor in glioblastoma with defined antioxidative properties. Neuro Oncol. 23:1898–1910. 2021.PubMed/NCBI View Article : Google Scholar

119 

Navone SE, Guarnaccia L, Cordiglieri C, Crisà FM, Caroli M, Locatelli M, Schisano L, Rampini P, Miozzo M, La Verde N, et al: Aspirin affects tumor angiogenesis and sensitizes human glioblastoma endothelial cells to temozolomide, bevacizumab, and sunitinib, impairing vascular endothelial growth factor-related signaling. World Neurosurg. 120:e380–e391. 2018.PubMed/NCBI View Article : Google Scholar

120 

Kast RE: Adding high-dose celecoxib to increase effectiveness of standard glioblastoma chemoirradiation. Ann Pharm Fr. 79:481–488. 2021.PubMed/NCBI View Article : Google Scholar

121 

Yin D, Jin G, He H, Zhou W, Fan Z, Gong C, Zhao J and Xiong H: Celecoxib reverses the glioblastoma chemo-resistance to temozolomide through mitochondrial metabolism. Aging (Albany NY). 13:21268–21282. 2021.PubMed/NCBI View Article : Google Scholar

122 

Pantovic A, Bosnjak M, Arsikin K, Kosic M, Mandic M, Ristic B, Tosic J, Grujicic D, Isakovic A, Micic N, et al: In vitro antiglioma action of indomethacin is mediated via AMP-activated protein kinase/mTOR complex 1 signalling pathway. Int J Biochem Cell Biol. 83:84–96. 2017.PubMed/NCBI View Article : Google Scholar

123 

Allani SK, Weissbach H and Lopez Toledano MA: Sulindac induces differentiation of glioblastoma stem cells making them more sensitive to oxidative stress. Neoplasma. 65:376–388. 2018.PubMed/NCBI View Article : Google Scholar

124 

Qiu J, Shi Z and Jiang J: Cyclooxygenase-2 in glioblastoma multiforme. Drug Discov Today. 22:148–156. 2017.PubMed/NCBI View Article : Google Scholar

125 

Li H, Jiao S, Li X, Banu H, Hamal S and Wang X: Therapeutic effects of antibiotic drug tigecycline against cervical squamous cell carcinoma by inhibiting Wnt/β-catenin signaling. Biochem Biophys Res Commun. 467:14–20. 2015.PubMed/NCBI View Article : Google Scholar

126 

Wieland A, Trageser D, Gogolok S, Reinartz R, Höfer H, Keller M, Leinhaas A, Schelle R, Normann S, Klaas L, et al: Anticancer effects of niclosamide in human glioblastoma. Clin Cancer Res. 19:4124–4136. 2013.PubMed/NCBI View Article : Google Scholar

127 

Li H, Liu S, Jin R, Xu H, Li Y, Chen Y and Zhao G: Pyrvinium pamoate regulates MGMT expression through suppressing the Wnt/β-catenin signaling pathway to enhance the glioblastoma sensitivity to temozolomide. Cell Death Discov. 7(288)2021.PubMed/NCBI View Article : Google Scholar

128 

Liu Y, Fang S, Sun Q and Liu B: Anthelmintic drug ivermectin inhibits angiogenesis, growth and survival of glioblastoma through inducing mitochondrial dysfunction and oxidative stress. Biochem Biophys Res Commun. 480:415–421. 2016.PubMed/NCBI View Article : Google Scholar

129 

Hajikhani B, Nasiri MJ, Hosseini SS, Khalili F, Karimi-Yazdi M, Hematian A, Nojookambari NY, Goudarzi M, Dadashi M and Mirsaeidi M: Clofazimine susceptibility testing of Mycobacterium avium complex and Mycobacterium abscessus: A meta-analysis study. J Glob Antimicrob Resist. 26:188–193. 2021.PubMed/NCBI View Article : Google Scholar

130 

Park L, Wallace CE, Vasile G and Buckley C: A case of lepromatous leprosy with erythema nodosum leprosum. Cureus. 15(e33846)2023.PubMed/NCBI View Article : Google Scholar

131 

Ahmed K, Koval A, Xu J, Bodmer A and Katanaev VL: Towards the first targeted therapy for triple-negative breast cancer: Repositioning of clofazimine as a chemotherapy-compatible selective Wnt pathway inhibitor. Cancer Lett. 449:45–55. 2019.PubMed/NCBI View Article : Google Scholar

132 

Xu J, Koval A and Katanaev VL: Beyond TNBC: Repositioning of clofazimine against a broad range of Wnt-dependent cancers. Front Oncol. 10(602817)2020.PubMed/NCBI View Article : Google Scholar

133 

Keswani RK, Tian C, Peryea T, Girish G, Wang X and Rosania GR: Repositioning clofazimine as a macrophage-targeting photoacoustic contrast agent. Sci Rep. 6(23528)2016.PubMed/NCBI View Article : Google Scholar

134 

Trexel J, Yoon GS, Keswani RK, McHugh C, Yeomans L, Vitvitsky V, Banerjee R, Sud S, Sun Y, Rosania GR and Stringer KA: Macrophage-mediated clofazimine sequestration is accompanied by a shift in host energy metabolism. J Pharm Sci. 106:1162–1174. 2017.PubMed/NCBI View Article : Google Scholar

135 

Yoon GS, Sud S, Keswani RK, Baik J, Standiford TJ, Stringer KA and Rosania GR: Phagocytosed clofazimine biocrystals can modulate innate immune signaling by inhibiting TNFα and boosting IL-1RA secretion. Mol Pharm. 12:2517–2527. 2015.PubMed/NCBI View Article : Google Scholar

136 

Geribaldi-Doldán N, Fernández-Ponce C, Quiroz RN, Sánchez-Gomar I, Escorcia LG, Velásquez EP and Quiroz EN: The role of microglia in glioblastoma. Front Oncol. 10(603495)2021.PubMed/NCBI View Article : Google Scholar

137 

Castellani G, Croese T, Peralta Ramos JM and Schwartz M: Transforming the understanding of brain immunity. Science. 380(eabo7649)2023.PubMed/NCBI View Article : Google Scholar

138 

Rustenhoven J and Kipnis J: Brain borders at the central stage of neuroimmunology. Nature. 612:417–429. 2022.PubMed/NCBI View Article : Google Scholar : De Leo A, Ugolini A and Veglia F: Myeloid cells in glioblastoma microenvironment. Cells 10: 18, 2020.

139 

Lewellis SW and Knaut H: Attractive guidance: How the chemokine SDF1/CXCL12 guides different cells to different locations. Semin Cell Dev Biol. 23:333–340. 2012.PubMed/NCBI View Article : Google Scholar

140 

Giordano FA, Link B, Glas M, Herrlinger U, Wenz F, Umansky V, Brown JM and Herskind C: Targeting the post-irradiation tumor microenvironment in glioblastoma via inhibition of CXCL12. Cancers (Basel). 11(272)2019.PubMed/NCBI View Article : Google Scholar

141 

Wang S, Chen C, Li J, Xu X, Chen W and Li F: The CXCL12/CXCR4 axis confers temozolomide resistance to human glioblastoma cells via up-regulation of FOXM1. J Neurol Sci. 414(116837)2020.PubMed/NCBI View Article : Google Scholar

142 

Dolina JS, Van Braeckel-Budimir N, Thomas GD and Salek-Ardakani S: CD8+ T cell exhaustion in cancer. Front Immunol. 12(715234)2021.PubMed/NCBI View Article : Google Scholar

143 

Belk JA, Daniel B and Satpathy AT: Epigenetic regulation of T cell exhaustion. Nat Immunol. 23:848–860. 2022.PubMed/NCBI View Article : Google Scholar

144 

Yang T, Kong Z and Ma W: PD-1/PD-L1 immune checkpoint inhibitors in glioblastoma: Clinical studies, challenges and potential. Hum Vaccin Immunother. 17:546–553. 2021.PubMed/NCBI View Article : Google Scholar

145 

Arrieta VA, Dmello C, McGrail DJ, Brat DJ, Lee-Chang C, Heimberger AB, Chand D, Stupp R and Sonabend AM: Immune checkpoint blockade in glioblastoma: From tumor heterogeneity to personalized treatment. J Clin Invest. 133(e163447)2023.PubMed/NCBI View Article : Google Scholar

146 

Caramanna I, de Kort JM, Brandes AA, Taal W, Platten M, Idbaih A, Frenel JS, Wick W, Preetha CJ, Bendszus M, et al: Corticosteroids use and neurocognitive functioning in patients with recurrent glioblastoma: Evidence from European organization for research and treatment of cancer (EORTC) trial 26101. Neurooncol Pract. 9:310–316. 2022.PubMed/NCBI View Article : Google Scholar

147 

Pitter KL, Tamagno I, Alikhanyan K, Hosni-Ahmed A, Pattwell SS, Donnola S, Dai C, Ozawa T, Chang M, Chan TA, et al: Corticosteroids compromise survival in glioblastoma. Brain. 139:1458–1471. 2016.PubMed/NCBI View Article : Google Scholar

148 

Klement RJ and Champ CE: Corticosteroids compromise survival in glioblastoma in part through their elevation of blood glucose levels. Brain. 140(e16)2017.PubMed/NCBI View Article : Google Scholar

149 

Yovino S, Kleinberg L, Grossman SA, Narayanan M and Ford E: The etiology of treatment-related lymphopenia in patients with malignant gliomas: Modeling radiation dose to circulating lymphocytes explains clinical observations and suggests methods of modifying the impact of radiation on immune cells. Cancer Invest. 31:140–144. 2013.PubMed/NCBI View Article : Google Scholar

150 

Kut C and Kleinberg L: Radiotherapy, lymphopenia and improving the outcome for glioblastoma: A narrative review. Chin Clin Oncol. 12(4)2023.PubMed/NCBI View Article : Google Scholar

151 

Saito T, Sugiyama K, Hama S, Yamasaki F, Takayasu T, Nosaka R, Muragaki Y, Kawamata T and Kurisu K: Prognostic importance of temozolomide-induced neutropenia in glioblastoma, IDH-wildtype patients. Neurosurg Rev. 41:621–628. 2018.PubMed/NCBI View Article : Google Scholar

152 

Aboody KS, Brown A, Rainov NG, Bower KA, Liu S, Yang W, Small JE, Herrlinger U, Ourednik V, Black PM, et al: Neural stem cells display extensive tropism for pathology in adult brain: Evidence from intracranial gliomas. Proc Natl Acad Sci USA. 97:12846–12851. 2000.PubMed/NCBI View Article : Google Scholar

153 

Snyder EY, Park KI, Flax JD, Liu S, Rosario CM, Yandava BD and Aurora S: Potential of neural ‘stem-like’ cells for gene therapy and repair of the degenerating central nervous system. Adv Neurol. 72:121–132. 1997.PubMed/NCBI

154 

Bryukhovetskiy IS, Mischenko PV, Tolok EV, Zaitcev SV, Khotimchenko YS and Bryukhovetskiy AS: Directional migration of adult hematopoeitic progenitors to C6 glioma in vitro. Oncol Lett. 9:1839–1844. 2015.PubMed/NCBI View Article : Google Scholar

155 

Hass R, von der Ohe J and Dittmar T: Hybrid formation and fusion of cancer cells in vitro and in vivo. Cancers (Basel). 13(4496)2021.PubMed/NCBI View Article : Google Scholar

156 

Goldenberg DM: Horizontal transmission of malignancy by cell-cell fusion. Expert Opin Biol Ther. 12 (Suppl 1):S133–S139. 2012.PubMed/NCBI View Article : Google Scholar

157 

Sun Z, Wang L, Zhou Y, Dong L, Ma W, Lv L, Zhang J and Wang X: Glioblastoma stem cell-derived exosomes enhance stemness and tumorigenicity of glioma cells by transferring Notch1 protein. Cell Mol Neurobiol. 40:767–784. 2020.PubMed/NCBI View Article : Google Scholar

158 

Khan F, Pang L, Dunterman M, Lesniak MS, Heimberger AB and Chen P: Macrophages and microglia in glioblastoma: Heterogeneity, plasticity, and therapy. J Clin Invest. 133(e163446)2023.PubMed/NCBI View Article : Google Scholar

159 

Wang G, Zhong K, Wang Z, Zhang Z, Tang X, Tong A and Zhou L: Tumor-associated microglia and macrophages in glioblastoma: From basic insights to therapeutic opportunities. Front Immunol. 13(964898)2022.PubMed/NCBI View Article : Google Scholar

160 

Bryukhovetskiy IS, Mischenko PV, Tolok EV, Zaitcev SV, Khotimchenko YS and Bryukhovetskiy AS: Directional migration of adult hematopoeitic progenitors to C6 glioma in vitro. Oncol Lett. 9:1839–1844. 2015.PubMed/NCBI View Article : Google Scholar

161 

Lee-Six H, Øbro NF, Shepherd MS, Grossmann S, Dawson K, Belmonte M, Osborne RJ, Huntly BJP, Martincorena I, Anderson E, et al: Population dynamics of normal human blood inferred from somatic mutations. Nature. 561:473–478. 2018.PubMed/NCBI View Article : Google Scholar

162 

Jaiswal S: Clonal hematopoiesis and nonhematologic disorders. Blood. 136:1606–1614. 2020.PubMed/NCBI View Article : Google Scholar

163 

Kast RE, Hill QA, Wion D, Mellstedt H, Focosi D, Karpel-Massler G, Heiland T and Halatsch ME: Glioblastoma-synthesized G-CSF and GM-CSF contribute to growth and immunosuppression: Potential therapeutic benefit from dapsone, fenofibrate, and ribavirin. Tumour Biol. 39(1010428317699797)2017.PubMed/NCBI View Article : Google Scholar

164 

Bryukhovetskiy I, Manzhulo I, Mischenko P, Milkina E, Dyuizen I, Bryukhovetskiy A and Khotimchenko Y: Cancer stem cells and microglia in the processes of glioblastoma multiforme invasive growth. Oncol Lett. 12:1721–1728. 2016.PubMed/NCBI View Article : Google Scholar

165 

Zaitsev S, Sharma HS, Sharma A, Manzhulo I, Polevshchikov A, Kudriavtsev I, Khotimchenko Y, Pak O, Bryukhovetskiy A and Bryukhovetskiy I: Pro-inflammatory modification of cancer cells microsurroundings increases the survival rates for rats with low differentiated malignant glioma of brain. Int Rev Neurobiol. 151:253–279. 2020.PubMed/NCBI View Article : Google Scholar

166 

Choe JH, Watchmaker PB, Simic MS, Gilbert RD, Li AW, Krasnow NA, Downey KM, Yu W, Carrera DA, Celli A, et al: SynNotch-CAR T cells overcome challenges of specificity, heterogeneity, and persistence in treating glioblastoma. Sci Transl Med. 13(eabe7378)2021.PubMed/NCBI View Article : Google Scholar

167 

Meister H, Look T, Roth P, Pascolo S, Sahin U, Lee S, Hale BD, Snijder B, Regli L, Ravi VM, et al: Multifunctional mRNA-based CAR T cells display promising antitumor activity against glioblastoma. Clin Cancer Res. 28:4747–4756. 2022.PubMed/NCBI View Article : Google Scholar

168 

Maggs L, Cattaneo G, Dal AE, Moghaddam AS and Ferrone S: CAR T cell-based immunotherapy for the treatment of glioblastoma. Front Neurosci. 15(662064)2021.PubMed/NCBI View Article : Google Scholar

169 

Wang D, Starr R, Chang WC, Aguilar B, Alizadeh D, Wright SL, Yang X, Brito A, Sarkissian A, Ostberg JR, et al: Chlorotoxin-directed CAR T cells for specific and effective targeting of glioblastoma. Sci Transl Med. 12(eaaw2672)2020.PubMed/NCBI View Article : Google Scholar

170 

Agliardi G, Liuzzi AR, Hotblack A, De Feo D, Núñez N, Stowe CL, Friebel E, Nannini F, Rindlisbacher L, Roberts TA, et al: Intratumoral IL-12 delivery empowers CAR-T cell immunotherapy in a pre-clinical model of glioblastoma. Nat Commun. 12(444)2021.PubMed/NCBI View Article : Google Scholar

171 

Brown CE, Rodriguez A, Palmer J, Ostberg JR, Naranjo A, Wagner JR, Aguilar B, Starr R, Weng L, Synold TW, et al: Off-the-shelf, steroid-resistant, IL13Rα2-specific CAR T cells for treatment of glioblastoma. Neuro Oncol. 24:1318–1330. 2022.PubMed/NCBI View Article : Google Scholar

172 

Wang G, Zhang Z, Zhong K, Wang Z, Yang N, Tang X, Li H, Lu Q, Wu Z, Yuan B, et al: CXCL11-armed oncolytic adenoviruses enhance CAR-T cell therapeutic efficacy and reprogram tumor microenvironment in glioblastoma. Mol Ther. 31:134–153. 2023.PubMed/NCBI View Article : Google Scholar

173 

Ghouzlani A, Kandoussi S, Tall M, Reddy KP, Rafii S and Badou A: Immune checkpoint inhibitors in human glioma microenvironment. Front Immunol. 12(679425)2021.PubMed/NCBI View Article : Google Scholar

174 

Gatto L, Franceschi E, Di Nunno V, Maggio I, Lodi R and Brandes AA: Engineered CAR-T and novel CAR-based therapies to fight the immune evasion of glioblastoma: Gutta cavat lapidem. Expert Rev Anticancer Ther. 21:1333–1353. 2021.PubMed/NCBI View Article : Google Scholar

175 

Bryukhovetskiy I: Cell-based immunotherapy of glioblastoma multiforme. Oncol Lett. 23(133)2022.PubMed/NCBI View Article : Google Scholar

176 

Baharom F, Ramirez-Valdez RA, Khalilnezhad A, Khalilnezhad S, Dillon M, Hermans D, Fussell S, Tobin KKS, Dutertre CA, Lynn GM, et al: Systemic vaccination induces CD8+ T cells and remodels the tumor microenvironment. Cell. 185:4317–4332.e15. 2022.PubMed/NCBI View Article : Google Scholar

177 

Liau LM, Ashkan K, Brem S, Campian JL, Trusheim JE, Iwamoto FM, Tran DD, Ansstas G, Cobbs CS, Heth JA, et al: Association of autologous tumor lysate-loaded dendritic cell vaccination with extension of survival among patients with newly diagnosed and recurrent glioblastoma: A phase 3 prospective externally controlled cohort trial. JAMA Oncol. 9:112–121. 2023.PubMed/NCBI View Article : Google Scholar

178 

Keskin DB, Anandappa AJ, Sun J, Tirosh I, Mathewson ND, Li S, Oliveira G, Giobbie-Hurder A, Felt K, Gjini E, et al: Neoantigen vaccine generates intratumoral T cell responses in phase Ib glioblastoma trial. Nature. 565:234–239. 2019.PubMed/NCBI View Article : Google Scholar

179 

Chen KS, Reinshagen C, Van Schaik TA, Rossignoli F, Borges P, Mendonca NC, Abdi R, Simon B, Reardon DA, Wakimoto H and Shah K: Bifunctional cancer cell-based vaccine concomitantly drives direct tumor killing and antitumor immunity. Sci Transl Med. 15(eabo4778)2023.PubMed/NCBI View Article : Google Scholar

180 

Wang J, Weiss T, Neidert MC, Toussaint NC, Naghavian R, Sellés Moreno C, Foege M, Tomas Ojer P, Medici G, Jelcic I, et al: Vaccination with designed neopeptides induces intratumoral, cross-reactive CD4+ T-cell responses in glioblastoma. Clin Cancer Res. 28:5368–5382. 2022.PubMed/NCBI View Article : Google Scholar

181 

Yu TW, Chueh HY, Tsai CC, Lin CT and Qiu JT: Novel GM-CSF-based vaccines: One small step in GM-CSF gene optimization, one giant leap for human vaccines. Hum Vaccin Immunother. 12:3020–3028. 2016.PubMed/NCBI View Article : Google Scholar

182 

Li L, Zhou J, Dong X, Liao Q, Zhou D and Zhou Y: Dendritic cell vaccines for glioblastoma fail to complete clinical translation: Bottlenecks and potential countermeasures. Int Immunopharmacol. 109(108929)2022.PubMed/NCBI View Article : Google Scholar

183 

Liau LM, Ashkan K, Tran DD, Campian JL, Trusheim JE, Cobbs CS, Heth JA, Salacz M, Taylor S, D'Andre SD, et al: First results on survival from a large phase 3 clinical trial of an autologous dendritic cell vaccine in newly diagnosed glioblastoma. J Transl Med. 16(142)2018.PubMed/NCBI View Article : Google Scholar

184 

Zhu P, Li SY, Ding J, Fei Z, Sun SN, Zheng ZH, Wei D, Jiang J, Miao JL, Li SZ, et al: Combination immunotherapy of glioblastoma with dendritic cell cancer vaccines, anti-PD-1 and poly I:C. J Pharm Anal. 13:616–624. 2023.PubMed/NCBI View Article : Google Scholar

185 

Medikonda R, Dunn G, Rahman M, Fecci P and Lim M: A review of glioblastoma immunotherapy. J Neurooncol. 151:41–53. 2021.PubMed/NCBI View Article : Google Scholar

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Kosianova А, Pak O and Bryukhovetskiy I: Regulation of cancer stem cells and immunotherapy of glioblastoma (Review). Biomed Rep 20: 24, 2024.
APA
Kosianova, А., Pak, O., & Bryukhovetskiy, I. (2024). Regulation of cancer stem cells and immunotherapy of glioblastoma (Review). Biomedical Reports, 20, 24. https://doi.org/10.3892/br.2023.1712
MLA
Kosianova, А., Pak, O., Bryukhovetskiy, I."Regulation of cancer stem cells and immunotherapy of glioblastoma (Review)". Biomedical Reports 20.2 (2024): 24.
Chicago
Kosianova, А., Pak, O., Bryukhovetskiy, I."Regulation of cancer stem cells and immunotherapy of glioblastoma (Review)". Biomedical Reports 20, no. 2 (2024): 24. https://doi.org/10.3892/br.2023.1712
Copy and paste a formatted citation
x
Spandidos Publications style
Kosianova А, Pak O and Bryukhovetskiy I: Regulation of cancer stem cells and immunotherapy of glioblastoma (Review). Biomed Rep 20: 24, 2024.
APA
Kosianova, А., Pak, O., & Bryukhovetskiy, I. (2024). Regulation of cancer stem cells and immunotherapy of glioblastoma (Review). Biomedical Reports, 20, 24. https://doi.org/10.3892/br.2023.1712
MLA
Kosianova, А., Pak, O., Bryukhovetskiy, I."Regulation of cancer stem cells and immunotherapy of glioblastoma (Review)". Biomedical Reports 20.2 (2024): 24.
Chicago
Kosianova, А., Pak, O., Bryukhovetskiy, I."Regulation of cancer stem cells and immunotherapy of glioblastoma (Review)". Biomedical Reports 20, no. 2 (2024): 24. https://doi.org/10.3892/br.2023.1712
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team