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
Experimental and Therapeutic Medicine
Join Editorial Board Propose a Special Issue
Print ISSN: 1792-0981 Online ISSN: 1792-1015
Journal Cover
July-2023 Volume 26 Issue 1

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
July-2023 Volume 26 Issue 1

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

  • Supplementary Files
    • Supplementary_Data.pdf
Article

5‑aminiolevulinic acid induces a radiodynamic effect with enhanced delayed reactive oxygen species production under hypoxic conditions in lymphoma cells: An in vitro study

  • Authors:
    • Kohei Suzuki
    • Junkoh Yamamoto
    • Keita Toh
    • Ryo Miyaoka
  • View Affiliations / Copyright

    Affiliations: Department of Neurosurgery, University of Occupational and Environmental Health, Kitakyushu, Fukuoka 807‑8555, Japan
  • Article Number: 360
    |
    Published online on: June 7, 2023
       https://doi.org/10.3892/etm.2023.12059
  • 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

Primary central nervous system lymphoma (PCNSL) is a rare and aggressive type of intracranial tumor. However, PCNSL is radiosensitive; thus, whole‑brain radiotherapy (WBRT) is often selected as an alternative consolidation therapy. WBRT‑related delayed neurotoxicity can affect the quality of life of the elderly. 5‑aminolevulinic acid (ALA) is a natural precursor of heme and has been widely used as a live molecular fluorescence marker in brain tumor surgery. Experimental studies have demonstrated that combination therapy with 5‑ALA and ionizing irradiation (IR), denoted radiodynamic therapy (RDT), resulted in tumor suppression in cancer, including glioma, melanoma, colorectal cancer, prostate cancer, breast cancer and lung cancer; however, to the best of our knowledge, this method has not been investigated in lymphoma. The present study aimed to investigate the radiodynamic effect of 5‑ALA on lymphoma cells in vitro. The synthesis of 5‑ALA‑induced protoporphyrin IX (PpIX) was assessed under normal and hypoxic conditions in lymphoma cells (Raji, HKBML and TK). Subsequently, the radiodynamic effect of 5‑ALA was evaluated using a colony formation assay and reactive oxygen species (ROS) production after RDT was examined using flow cytometry. Finally, the mitochondrial density in the lymphoma cells was evaluated. Lymphoma cells exhibited a high accumulation of 5‑ALA‑induced PpIX in the flow cytometric analysis, and a decrease in the surviving fraction under IR in cells with 5‑ALA treatment compared with cells not treated with 5‑ALA in the colony formation assay under normal and hypoxic conditions. Although ROS production 12 h after IR was increased compared with that immediately after IR (0 h), pretreatment with 5‑ALA enhanced the delayed ROS production in each lymphoma cell line under normoxic conditions. Raji and TK cells exhibited an increase in ROS production 12 h after IR compared with that at 0 h in the 5‑ALA‑untreated cells under hypoxic conditions. Raji, HKBML and TK cells exhibited an increase in ROS production 12 h after IR compared with that at 0 h in the 5‑ALA‑treated cells, while TK cells exhibited enhancement of ROS production 12 h after IR in 5‑ALA‑treated cells compared with 5‑ALA‑untreated cells under hypoxic conditions. Other studies have demonstrated that impaired mitochondria damaged by IR produce ROS via the metabolic process, then damage the rest of the surrounding normal mitochondria, consequently propagating oxidative stress within tumor cells and leading to cell death. Thus, we hypothesized that the propagating oxidative stress after IR was associated with mitochondrial density in tumor cells. Namely, high accumulation of 5‑ALA‑indcued PpIX may promote ROS production in mitochondria of tumor cells after IR, and suppress the cell surviving fraction via the propagation of oxidative stress. In the colony formation assay, Raji cell colony formation was suppressed by RDT with 5‑ALA. Simultaneously, the mitochondrial density in the Raji cells was higher than that in other cell lines. Pretreatment with 5‑ALA enhanced delayed ROS production after IR in lymphoma cells under normoxic conditions. Under hypoxic conditions, only TK cells exhibited enhancement of ROS production 12 h after IR in the 5‑ALA‑treated group compared with the 5‑ALA‑untreated group. Although further studies evaluating the effect of hypoxic conditions in lymphoma cells are needed, the results suggested that RDT with 5‑ALA could suppress colony formation under normal and hypoxic conditions in lymphoma cells. Therefore, RDT with 5‑ALA is a potential treatment option for PCNSL.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

View References

1 

Han CH and Batchelor TT: Diagnosis and management of primary central nervous system lymphoma. Cancer. 123:4314–4324. 2017.PubMed/NCBI View Article : Google Scholar

2 

Siegal T and Bairey O: Primary CNS lymphoma in the elderly: The challenge. Acta Haematol. 141:138–145. 2019.PubMed/NCBI View Article : Google Scholar

3 

Ferreri AJ and Marturano E: Primary CNS lymphoma. Best Pract Res Clin Haematol. 25:119–130. 2012.PubMed/NCBI View Article : Google Scholar

4 

Calimeri T, Steffanoni S, Gagliardi F, Chiara A and Ferreri AJM: Erratum to ‘How we treat primary central nervous system lymphoma’: [ESMO Open Volume 6, Issue 4, August 2021, 100213]. ESMO Open. 6(100326)2021.PubMed/NCBI View Article : Google Scholar

5 

Ishizuka M, Abe F, Sano Y, Takahashi K, Inoue K, Nakajima M, Kohda T, Komatsu N, Ogura S and Tanaka T: Novel development of 5-aminolevurinic acid (ALA) in cancer diagnoses and therapy. Int Immunopharmacol. 11:358–365. 2011.PubMed/NCBI View Article : Google Scholar

6 

Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F and Reulen HJ: ALA-Glioma Study group. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: A randomised controlled multicentre phase III trial. Lancet Oncol. 7:392–401. 2006.PubMed/NCBI View Article : Google Scholar

7 

Stummer W, Holling M, Bendok BR, Vogelbaum MA, Cox A, Renfrow SL, Widhalm G, Ezrin A, DeSena S, Sackman ML and Wyse JW: The NXDC-MEN-301 Study on 5-ALA for meningiomas surgery: An innovative study design for the assessing the benefit of intra-operative fluorescence imaging. Brain Sci. 12(1044)2022.PubMed/NCBI View Article : Google Scholar

8 

Kiesel B, Millesi M, Woehrer A, Furtner J, Bavand A, Roetzer T, Mischkulnig M, Wolfsberger S, Preusser M, Knosp E and Widhalm G: 5-ALA-induced fluorescence as a marker for diagnostic tissue in stereotactic biopsies of intracranial lymphomas: Experience in 41 patients. Neurosurg Focus. 44(E7)2018.PubMed/NCBI View Article : Google Scholar

9 

Takahashi J and Misawa M: Characterization of reactive oxygen species generated by protoporphyrin IX under X-ray irradiation. Radiat Phys Chem. 78:889–898. 2009.

10 

Ueta K, Yamamoto J, Tanaka T, Nakano Y, Kitagawa T and Nishizawa S: 5-Aminolevulinic acid enhances mitochondrial stress upon ionizing irradiation exposure and increases delayed production of reactive oxygen species and cell death in glioma cells. Int J Mol Med. 39:387–398. 2017.PubMed/NCBI View Article : Google Scholar

11 

Yamamoto J, Ogura S, Shimajiri S, Nakano Y, Akiba D, Kitagawa T, Ueta K, Tanaka T and Nishizawa S: 5-aminolevulinic acid-induced protoporphyrin IX with multi-dose ionizing irradiation enhances host antitumor response and strongly inhibits tumor growth in experimental glioma in vivo. Mol Med Rep. 11:1813–1819. 2015.PubMed/NCBI View Article : Google Scholar

12 

Yamamoto J, Ogura S, Tanaka T, Kitagawa T, Nakano Y, Saito T, Takahashi M, Akiba D and Nishizawa S: Radiosensitizing effect of 5-aminolevulinic acid-induced protoporphyrin IX in glioma cells in vitro. Oncol Rep. 27:1748–1752. 2012.PubMed/NCBI View Article : Google Scholar

13 

Kitagawa T, Yamamoto J, Tanaka T, Nakano Y, Akiba D, Ueta K and Nishizawa S: 5-Aminolevulinic acid strongly enhances delayed intracellular production of reactive oxygen species (ROS) generated by ionizing irradiation: Quantitative analyses and visualization of intracellular ROS production in glioma cells in vitro. Oncol Rep. 33:583–590. 2015.PubMed/NCBI View Article : Google Scholar

14 

Takahashi J, Murakami M, Mori T and Iwahashi H: Verification of radiodynamic therapy by medical linear accelerator using a mouse melanoma tumor model. Sci Rep. 8(2728)2018.PubMed/NCBI View Article : Google Scholar

15 

Yamada K, Murayama Y, Kamada Y, Arita T, Kosuga T, Konishi H, Morimura R, Shiozaki A, Kuriu Y, Ikoma H, et al: Radiosensitizing effect of 5-aminolevulinic acid in colorectal cancer in vitro and in vivo. Oncol Lett. 17:5132–5138. 2019.PubMed/NCBI View Article : Google Scholar

16 

Miyake M, Tanaka N, Hori S, Ohnishi S, Takahashi H, Fujii T, Owari T, Ohnishi K, Iida K, Morizawa Y, et al: Dual benefit of supplementary oral 5-aminolevulinic acid to pelvic radiotherapy in a syngenic prostate cancer model. Prostate. 79:340–351. 2019.PubMed/NCBI View Article : Google Scholar

17 

Kaneko T, Tominaga M, Kouzaki R, Hanyu A, Ueshima K, Yamada H, Suga M, Yamashita T, Okimoto T and Uto Y: Radiosensitizing effect of 5-aminolevulinic acid and protoporphyrin IX on Carbon-ion beam irradiation. Anticancer Res. 38:4313–4317. 2018.PubMed/NCBI View Article : Google Scholar

18 

Yang DM, Cvetkovic D, Chen L and Ma CC: Therapeutic effects of in-vivo radiodynamic therapy (RDT) for lung cancer treatment: A combination of 15MV photons and 5-aminolevulinic acid (5-ALA). Biomed Phys Eng Express. 8(1088/2057-1976/ac9b5c)2022.PubMed/NCBI View Article : Google Scholar

19 

Wang J, Valdez A and Chen Y: Evaluation of automated Wes system as an analytical and characterization tool to support monoclonal antibody drug product development. J Pharm Biomed Anal. 139:263–268. 2017.PubMed/NCBI View Article : Google Scholar

20 

Baddela VS, Sharma A, Michaelis M and Vanselow J: HIF1 driven transcriptional activity regulates steroidogenesis and proliferation of bovine granulosa cells. Sci Rep. 10(3906)2020.PubMed/NCBI View Article : Google Scholar

21 

Prall F, Maletzki C and Linnebacher M: Microdensitometry of osteopontin as an immunohistochemical prognostic biomarker in colorectal carcinoma tissue microarrays: Potential and limitations of the method in ‘biomarker pathology’. Histopathology. 61:823–832. 2012.PubMed/NCBI View Article : Google Scholar

22 

Yamamori T, Yasui H, Yamazumi M, Wada Y, Nakamura Y, Nakamura H and Inanami O: Ionizing radiation induces mitochondrial reactive oxygen species production accompanied by upregulation of mitochondrial electron transport chain function and mitochondrial content under control of the cell cycle checkpoint. Free Radic Biol Med. 53:260–270. 2012.PubMed/NCBI View Article : Google Scholar

23 

Saenko Y, Cieslar-Pobuda A, Skonieczna M and Rzeszowska-Wolny J: Changes of reactive oxygen and nitrogen species and mitochondrial functioning in human K562 and HL60 cells exposed to ionizing radiation. Radiat Res. 180:360–366. 2013.PubMed/NCBI View Article : Google Scholar

24 

Dupin C, Sutter J, Amintas S, Derieppe MA, Lalanne M, Coulibaly S, Guyon J, Daubon T, Boutin J, Blouin JM, et al: An orthotopic model of glioblastoma is resistant to radiodynamic therapy with 5-AminoLevulinic acid. Cancers (Basel). 14(4244)2022.PubMed/NCBI View Article : Google Scholar

25 

Galadari S, Rahman A, Pallichankandy S and Thayyullathil F: Reactive oxygen species and cancer paradox: To promote or to suppress? Free Radic Biol Med. 104:144–164. 2017.PubMed/NCBI View Article : Google Scholar

26 

Owari T, Tanaka N, Nakai Y, Miyake M, Anai S, Kishi S, Mori S, Fujiwara-Tani R, Hojo Y, Mori T, et al: 5-Aminolevulinic acid overcomes hypoxia-induced radiation resistance by enhancing mitochondrial reactive oxygen species production in prostate cancer cells. Br J Cancer. 127:350–363. 2022.PubMed/NCBI View Article : Google Scholar

27 

Nordmann NJ and Michael AP: 5-Aminolevulinic acid radiodynamic therapy for treatment of high-grade gliomas: A systematic review. Clin Neurol Neurosurg. 201(106430)2021.PubMed/NCBI View Article : Google Scholar

28 

Krivoshapkin A, Gaytan A, Abdullaev O, Salim N, Sergeev G, Marmazeev I, Cesnulis E, Killeen T, Tyuryn V, Kiselev R, et al: Prospective comparative study of intraoperative balloon electronic brachytherapy versus resection with multidisciplinary adjuvant therapy for recurrent glioblastoma. Surg Neurol Int. 12(517)2021.PubMed/NCBI View Article : Google Scholar

29 

Pepper NB, Stummer W and Eich HT: The use of radiosensitizing agents in the therapy of glioblastoma multiforme-a comprehensive review. Strahlenther Onkol. 198:507–526. 2022.PubMed/NCBI View Article : Google Scholar

30 

Higgins GS, O'Cathail SM, Muschel RJ and McKenna WG: Drug radiotherapy combinations: Review of previous failures and reasons for future optimism. Cancer Treat Rev. 41:105–113. 2015.PubMed/NCBI View Article : Google Scholar

31 

Dhani N, Fyles A, Hedley D and Milosevic M: The clinical significance of hypoxia in human cancers. Semin Nucl Med. 45:110–121. 2015.PubMed/NCBI View Article : Google Scholar

32 

Ashton TM, McKenna WG, Kunz-Schughart LA and Higgins GS: Oxidative phosphorylation as an emerging target in cancer therapy. Clin Cancer Res. 24:2482–2490. 2018.PubMed/NCBI View Article : Google Scholar

33 

Ihata T, Nonoguchi N, Fujishiro T, Omura N, Kawabata S, Kajimoto Y and Wanibuchi M: The effect of hypoxia on photodynamic therapy with 5-aminolevulinic acid in malignant gliomas. Photodiagnosis Photodyn Ther. 40(103056)2022.PubMed/NCBI View Article : Google Scholar

34 

Castillo CA, Leon D, Ruiz MA, Albasanz JL and Martin M: Modulation of adenosine A1 and A2A receptors in C6 glioma cells during hypoxia: Involvement of endogenous adenosine. J Neurochem. 105:2315–2329. 2008.PubMed/NCBI View Article : Google Scholar

35 

Caro P, Kishan AU, Norberg E, Stanley IA, Chapuy B, Ficarro SB, Polak K, Tondera D, Gounarides J, Yin H, et al: Metabolic signatures uncover distinct targets in molecular subsets of diffuse large B cell lymphoma. Cancer Cell. 22:547–560. 2012.PubMed/NCBI View Article : Google Scholar

36 

Stadlbauer A, Marhold F, Oberndorfer S, Heinz G, Zimmermann M, Buchfelder M, Heynold E and Kinfe TM: Metabolic tumor microenvironment characterization of contrast enhancing brain tumors using physiologic MRI. Metabolites. 11(668)2021.PubMed/NCBI View Article : Google Scholar

37 

Norberg E, Lako A, Chen PH, Stanley IA, Zhou F, Ficarro SB, Chapuy B, Chen L, Rodig S, Shin D, et al: Differential contribution of the mitochondrial translation pathway to the survival of diffuse large B-cell lymphoma subsets. Cell Death Differ. 24:251–262. 2017.PubMed/NCBI View Article : Google Scholar

38 

Noble RA, Thomas H, Zhao Y, Herendi L, Howarth R, Dragoni I, Keun HC, Vellano CP, Marszalek JR and Wedge SR: Simultaneous targeting of glycolysis and oxidative phosphorylation as a therapeutic strategy to treat diffuse large B-cell lymphoma. Br J Cancer. 127:937–947. 2022.PubMed/NCBI View Article : Google Scholar

39 

Farrell C, Shi W, Bodman A and Olson JJ: Congress of neurological surgeons systematic review and evidence-based guidelines update on the role of emerging developments in the management of newly diagnosed glioblastoma. J Neurooncol. 150:269–359. 2020.PubMed/NCBI View Article : Google Scholar

40 

Averbeck D and Rodriguez-Lafrasse C: Role of mitochondria in radiation responses: Epigenetic, metabolic, and signaling impacts. Int J Mol Sci. 22(11047)2021.PubMed/NCBI View Article : Google Scholar

41 

Kam WW and Banati RB: Effects of ionizing radiation on mitochondria. Free Radic Biol Med. 65:607–619. 2013.PubMed/NCBI View Article : Google Scholar

42 

Tigano M, Vargas DC, Tremblay-Belzile S, Fu Y and Sfeir A: Nuclear sensing of breaks in mitochondrial DNA enhances immune surveillance. Nature. 591:477–481. 2021.PubMed/NCBI View Article : Google Scholar

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Suzuki K, Yamamoto J, Toh K and Miyaoka R: 5‑aminiolevulinic acid induces a radiodynamic effect with enhanced delayed reactive oxygen species production under hypoxic conditions in lymphoma cells: An <em>in vitro</em> study. Exp Ther Med 26: 360, 2023.
APA
Suzuki, K., Yamamoto, J., Toh, K., & Miyaoka, R. (2023). 5‑aminiolevulinic acid induces a radiodynamic effect with enhanced delayed reactive oxygen species production under hypoxic conditions in lymphoma cells: An <em>in vitro</em> study. Experimental and Therapeutic Medicine, 26, 360. https://doi.org/10.3892/etm.2023.12059
MLA
Suzuki, K., Yamamoto, J., Toh, K., Miyaoka, R."5‑aminiolevulinic acid induces a radiodynamic effect with enhanced delayed reactive oxygen species production under hypoxic conditions in lymphoma cells: An <em>in vitro</em> study". Experimental and Therapeutic Medicine 26.1 (2023): 360.
Chicago
Suzuki, K., Yamamoto, J., Toh, K., Miyaoka, R."5‑aminiolevulinic acid induces a radiodynamic effect with enhanced delayed reactive oxygen species production under hypoxic conditions in lymphoma cells: An <em>in vitro</em> study". Experimental and Therapeutic Medicine 26, no. 1 (2023): 360. https://doi.org/10.3892/etm.2023.12059
Copy and paste a formatted citation
x
Spandidos Publications style
Suzuki K, Yamamoto J, Toh K and Miyaoka R: 5‑aminiolevulinic acid induces a radiodynamic effect with enhanced delayed reactive oxygen species production under hypoxic conditions in lymphoma cells: An <em>in vitro</em> study. Exp Ther Med 26: 360, 2023.
APA
Suzuki, K., Yamamoto, J., Toh, K., & Miyaoka, R. (2023). 5‑aminiolevulinic acid induces a radiodynamic effect with enhanced delayed reactive oxygen species production under hypoxic conditions in lymphoma cells: An <em>in vitro</em> study. Experimental and Therapeutic Medicine, 26, 360. https://doi.org/10.3892/etm.2023.12059
MLA
Suzuki, K., Yamamoto, J., Toh, K., Miyaoka, R."5‑aminiolevulinic acid induces a radiodynamic effect with enhanced delayed reactive oxygen species production under hypoxic conditions in lymphoma cells: An <em>in vitro</em> study". Experimental and Therapeutic Medicine 26.1 (2023): 360.
Chicago
Suzuki, K., Yamamoto, J., Toh, K., Miyaoka, R."5‑aminiolevulinic acid induces a radiodynamic effect with enhanced delayed reactive oxygen species production under hypoxic conditions in lymphoma cells: An <em>in vitro</em> study". Experimental and Therapeutic Medicine 26, no. 1 (2023): 360. https://doi.org/10.3892/etm.2023.12059
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