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
International Journal of Oncology
Join Editorial Board Propose a Special Issue
Print ISSN: 1019-6439 Online ISSN: 1791-2423
Journal Cover
August-2023 Volume 63 Issue 2

Full Size Image

Cover Legend PDF

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
August-2023 Volume 63 Issue 2

Full Size Image

Cover Legend PDF

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

Deactivation of glycogen synthase kinase-3β by heat shock‑inducible tumor small protein attenuates hyperthermia‑induced pro‑migratory activity in colorectal cancer cells

  • Authors:
    • Keita Koizumi
    • Takahiro Domoto
    • Toshinari Minamoto
    • Kazuhito Satomura
    • Hideo Nakajima
  • View Affiliations / Copyright

    Affiliations: Department of Oncology, Ageo Central General Hospital, Ageo, Saitama 362‑8588, Japan, Divison of Translational and Clinical Oncology, Cancer Research Institute, Kanazawa University, Kanazawa, Ishikawa 920‑0934, Japan, Department of Oral Medicine and Stomatology, Tsurumi University School of Dental Medicine, Yokohama, Kanagawa 230‑8501, Japan
  • Article Number: 92
    |
    Published online on: June 23, 2023
       https://doi.org/10.3892/ijo.2023.5540
  • 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

Hyperthermia is a promising approach for improving cancer treatment in combination with chemotherapy, radiotherapy and/or immunotherapy; however, its molecular mechanisms remain unclear. Although heat shock proteins (HSPs) are involved in hyperthermia via antigen presentation and immune activation, major HSPs including HSP90 are associated with cancer progression via tumor cell migration and metastasis. The present study showed that heat shock‑inducible tumor small protein (HITS) could counteract the pro‑migratory effects of HSPs in colorectal cancer (CRC) cells, which represents a novel function. Western blotting analysis revealed that overexpression of HITS increased the protein level of glycogen synthase kinase‑3β (GSK3β) phosphorylated (p) at the serine 9 (pGSK3βS9; inactive form) in HCT 116, RKO and SW480 CRC cells. GSK3βS9 phosphorylation was reported to suppress migration in some cancer types; therefore, by using the wound healing assay, the present study revealed that HITS overexpression decreased the migration activity of CRC cells. Induction of HITS transcription was observed at 12 and 18 h after heat shock (HS) by using semi‑quantitative reverse transcription‑PCR analysis, followed by increased levels of pGSK3βS9 protein at 24 and 30 h in CRC cells in western blotting. Thus, HS induced not only HSPs to promote cell migration, but also HITS to counteract the migratory activity of these HSPs in CRC cells. HITS knockdown in CRC cells subject to HS showed increased cell migration in wound healing assay, which was decreased by the GSK3β inhibitor AR‑A014418, confirming the anti‑migratory effect of HITS via the deactivation of GSK3β. The present findings indicated that the deactivation of GSK3β sufficiently offset the pro‑migratory effect of hyperthermia via major HSPs in CRC.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

View References

1 

Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA and Jemal A: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68:394–424. 2018. View Article : Google Scholar : PubMed/NCBI

2 

Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A and Bray F: Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 71:209–249. 2021. View Article : Google Scholar : PubMed/NCBI

3 

Leporrier J, Maurel J, Chiche L, Bara S, Segol P and Launoy G: A population-based study of the incidence, management and prognosis of hepatic metastases from colorectal cancer. Br J Surg. 93:465–474. 2006. View Article : Google Scholar : PubMed/NCBI

4 

Zarour LR, Anand S, Billingsley KG, Bisson WH, Cercek A, Clarke MF, Coussens LM, Gast CE, Geltzeiler CB, Hansen L, et al: Colorectal cancer liver metastasis: Evolving paradigms and future directions. Cell Mol Gastroenterol Hepatol. 3:163–173. 2017. View Article : Google Scholar : PubMed/NCBI

5 

Dillekås H, Rogers MS and Straume O: Are 90% of deaths from cancer caused by metastases? Cancer Med. 8:5574–5576. 2019. View Article : Google Scholar : PubMed/NCBI

6 

Chow FC and Chok KS: Colorectal liver metastases: An update on multidisciplinary approach. World J Hepatol. 11:150–172. 2019. View Article : Google Scholar : PubMed/NCBI

7 

Ganesh K, Stadler ZK, Cercek A, Mendelsohn RB, Shia J, Segal NH and Diaz LA Jr: Immunotherapy in colorectal cancer: rationale, challenges and potential. Nat Rev Gastroenterol Hepatol. 16:361–375. 2019. View Article : Google Scholar : PubMed/NCBI

8 

Van der Jeught K, Xu HC, Li YJ, Lu XB and Ji G: Drug resistance and new therapies in colorectal cancer. World J Gastroenterol. 24:3834–3848. 2018. View Article : Google Scholar : PubMed/NCBI

9 

George TJ, Franke AJ, Chakravarthy AB, Das P, Dasari A, El-Rayes BF, Hong TS, Kinsella TJ, Landry JC, Lee JJ, et al: National Cancer Institute (NCI) state of the science: Targeted radiosensitizers in colorectal cancer. Cancer. 125:2732–2746. 2019.PubMed/NCBI

10 

Hettinga JV, Konings AW and Kampinga HH: Reduction of cellular cisplatin resistance by hyperthermia-a review. Int J Hyperthermia. 13:439–457. 1997. View Article : Google Scholar : PubMed/NCBI

11 

Yagawa Y, Tanigawa K, Kobayashi Y and Yamamoto M: Cancer immunity and therapy using hyperthermia with immunotherapy, radiotherapy, chemotherapy, and surgery. J Cancer Metastasis Treat. 3:218–230. 2017. View Article : Google Scholar

12 

Vassos N and Piso P: Metastatic colorectal cancer to the peritoneum: Current treatment options. Curr Treat Options Oncol. 19:492018. View Article : Google Scholar : PubMed/NCBI

13 

Dayanc BE, Beachy SH, Ostberg JR and Repasky EA: Dissecting the role of hyperthermia in natural killer cell mediated anti-tumor responses. Int J Hyperthermia. 24:41–56. 2008. View Article : Google Scholar : PubMed/NCBI

14 

Tsan MF and Gao B: Heat shock proteins and immune system. J Leukoc Biol. 85:905–910. 2009. View Article : Google Scholar : PubMed/NCBI

15 

Ciocca DR and Calderwood SK: Heat shock proteins in cancer: Diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones. 10:86–103. 2005. View Article : Google Scholar : PubMed/NCBI

16 

Boroumand N, Saghi H, Avan A, Bahreyni A, Ryzhikov M, Khazaei M and Hassanian SM: Therapeutic potency of heat-shock protein-90 pharmacological inhibitors in the treatment of gastrointestinal cancer, current status and perspectives. J Pharm Pharmacol. 70:151–158. 2018. View Article : Google Scholar : PubMed/NCBI

17 

Nakajima H, Ishigaki Y, Xia QS, Ikeda T, Yoshitake Y, Yonekura H, Nojima T, Tanaka T, Umehara H, Tomosugi N, et al: Induction of HITS, a newly identified family with sequence similarity 107 protein (FAM107B), in cancer cells by heat shock stimulation. Int J Oncol. 37:583–593. 2010. View Article : Google Scholar : PubMed/NCBI

18 

Liu Q, Zhao XY, Bai RZ, Liang SF, Nie CL, Yuan Z, Wang CT, Wu Y, Chen LJ and Wei YQ: Induction of tumor inhibition and apoptosis by a candidate tumor suppressor gene DRR1 on 3p21.1. Oncol Rep. 22:1069–1075. 2009.PubMed/NCBI

19 

Schmidt MV, Schülke JP, Liebl C, Stiess M, Avrabos C, Bock J, Wochnik GM, Davies HA, Zimmermann N, Scharf SH, et al: Tumor suppressor down-regulated in renal cell carcinoma 1 (DRR1) is a stress-induced actin bundling factor that modulates synaptic efficacy and cognition. Proc Natl Acad Sci USA. 108:17213–17218. 2011. View Article : Google Scholar : PubMed/NCBI

20 

Nakajima H, Koizumi K, Tanaka T, Ishigaki Y, Yoshitake Y, Yonekura H, Sakuma T, Fukushima T, Umehara H, Ueno S, et al: Loss of HITS (FAM107B) expression in cancers of multiple organs: Tissue microarray analysis. Int J Oncol. 41:1347–1357. 2012. View Article : Google Scholar : PubMed/NCBI

21 

Domoto T, Pyko IV, Furuta T, Miyashita K, Uehara M, Shimasaki T, Nakada M and Minamoto T: Glycogen synthase kinase-3β is a pivotal mediator of cancer invasion and resistance to therapy. Cancer Sci. 107:1363–1372. 2016. View Article : Google Scholar : PubMed/NCBI

22 

Domoto T, Uehara M, Bolidong D and Minamoto T: Glycogen synthase kinase 3β in cancer biology and treatment. Cells. 9:13882020. View Article : Google Scholar : PubMed/NCBI

23 

Beurel E, Grieco SF and Jope RS: Glycogen synthase kinase-3 (GSK3): Regulation, actions, and diseases. Pharmacol Ther. 148:114–131. 2015. View Article : Google Scholar : PubMed/NCBI

24 

Turano M, Costabile V, Cerasuolo A, Duraturo F, Liccardo R, Delrio P, Pace U, Rega D, Dodaro CA, Milone M, et al: Characterisation of mesenchymal colon tumour-derived cells in tumourspheres as a model for colorectal cancer progression. Int J Oncol. 53:2379–2396. 2018.PubMed/NCBI

25 

Kazi A, Xiang S, Yang H, Delitto D, Trevino J, Jiang RHY, Ayaz M, Lawrence HR, Kennedy P and Sebti SM: GSK3 suppression upregulates β-catenin and c-Myc to abrogate KRas-dependent tumors. Nat Commun. 9:51542018. View Article : Google Scholar : PubMed/NCBI

26 

Yoshino Y, Suzuki M, Takahashi H and Ishioka C: Inhibition of invasion by glycogen synthase kinase-3 beta inhibitors through dysregulation of actin re-organisation via down-regulation of WAVE2. Biochem Biophys Res Commun. 464:275–280. 2015. View Article : Google Scholar : PubMed/NCBI

27 

Chikano Y, Domoto T, Furuta T, Sabit H, Kitano-Tamura A, Pyko IV, Takino T, Sai Y, Hayashi Y, Sato H, et al: Glycogen synthase kinase 3β sustains invasion of glioblastoma via the focal adhesion kinase, Rac1, and c-Jun N-terminal kinase-mediated pathway. Mol Cancer Ther. 14:564–574. 2015. View Article : Google Scholar : PubMed/NCBI

28 

Kitano A, Shimasaki T, Chikano Y, Nakada M, Hirose M, Higashi T, Ishigaki Y, Endo Y, Takino T, Sato H, et al: Aberrant glycogen synthase kinase 3β is involved in pancreatic cancer cell invasion and resistance to therapy. PLoS One. 8:e552892013. View Article : Google Scholar : PubMed/NCBI

29 

Shakoori A, Ougolkov A, Yu ZW, Zhang B, Modarressi MH, Billadeau DD, Mai M, Takahashi Y and Minamoto T: Deregulated GSK3β activity in colorectal cancer: Its association with tumor cell survival and proliferation. Biochem Biophys Res Commun. 334:1365–1373. 2005. View Article : Google Scholar : PubMed/NCBI

30 

Kawauchi T, Chihama K, Nabeshima Y and Hoshino M: The in vivo roles of STEF/Tiam1, Rac1 and JNK in cortical neuronal migration. EMBO J. 22:4190–4201. 2003. View Article : Google Scholar : PubMed/NCBI

31 

Gayet J, Zhou XP, Duval A, Rolland S, Hoang JM, Cottu P and Hamelin R: Extensive characterization of genetic alterations in a series of human colorectal cancer cell lines. Oncogene. 20:5025–5032. 2001. View Article : Google Scholar : PubMed/NCBI

32 

Ahmed D, Eide PW, Eilertsen IA, Danielsen SA, Eknæs M, Hektoen M, Lind GE and Lothe RA: Epigenetic and genetic features of 24 colon cancer cell lines. Oncogenesis. 2:e712013. View Article : Google Scholar : PubMed/NCBI

33 

Mai W, Miyashita K, Shakoori A, Zhang B, Yu ZW, Takahashi Y, Motoo Y, Kawakami K and Minamoto T: Detection of active fraction of GSK3β in cancer cells by nonradioisotopic in vitro kinase assay. Oncology. 71:297–305. 2006. View Article : Google Scholar : PubMed/NCBI

34 

Shakoori A, Mai W, Miyashita K, Yasumoto K, Takahashi Y, Ooi A, Kawakami K and Minamoto T: Inhibition of GSK-3β activity attenuates proliferation of human colon cancer cells in rodents. Cancer Sci. 98:1388–1393. 2007. View Article : Google Scholar : PubMed/NCBI

35 

Mai W, Kawakami K, Shakoori A, Kyo S, Miyashita K, Yokoi K, Jin MJ, Shimasaki T, Motoo Y and Minamoto T: Deregulated glycogen synthase kinase 3β sustains gastrointestinal cancer cells survival by modulating human telomerase reverse transcriptase and telomerase. Clin Cancer Res. 15:6810–6819. 2009. View Article : Google Scholar : PubMed/NCBI

36 

Turunen SP, Tatti-Bugaeva O and Lehti K: Membrane-type matrix metalloproteases as diverse effectors of cancer progression. Biochim Biophys Acta Mol Cell Res. 1864:1974–1988. 2017. View Article : Google Scholar : PubMed/NCBI

37 

Ning Q, Gan YH, Shi RR and Meng JH: Effects of HDAC4 on IL-1β-induced matrix metalloproteinase expression regulated partially through the WNT3A/β-catenin pathway. Chin Med J (Engl). 134:963–970. 2021. View Article : Google Scholar : PubMed/NCBI

38 

Tu Y, Tian Y, Wu Y and Cui S: Clinical significance of heat shock proteins in gastric cancer following hyperthermia stress: Indications for hyperthermic intraperitoneal chemoperfusion therapy. Oncol Lett. 15:9385–9391. 2018.PubMed/NCBI

39 

Grimmig T, Moll EM, Kloos K, Thumm R, Moench R, Callies S, Kreckel J, Vetterlein M, Pelz J, Polat B, et al: Upregulated heat shock proteins after hyperthermic chemotherapy point to induced cell survival mechanisms in affected tumor cells from peritoneal carcinomatosis. Cancer Growth Metastasis. 10:11790644177305592017. View Article : Google Scholar : PubMed/NCBI

40 

Chen JS, Hsu YM, Chen CC, Chen LL, Lee CC and Huang TS: Secreted heat shock protein 90α induces colorectal cancer cell invasion through CD91/LRP-1 and NF-κB-mediated integrin αV expression. J Biol Chem. 285:25458–25466. 2010. View Article : Google Scholar : PubMed/NCBI

41 

Song D, Guo M, Xu S, Song X, Bai B, Li Z, Chen J, An Y, Nie Y, Wu K, et al: HSP90-dependent PUS7 overexpression facilitates the metastasis of colorectal cancer cells by regulating LASP1 abundance. J Exp Clin Cancer Res. 40:1702021. View Article : Google Scholar : PubMed/NCBI

42 

Sims JD, McCready J and Jay DG: Extracellular heat shock protein (HSP)70 and HSP90α assist in matrix metalloproteinase-2 activation and breast cancer cell migration and invasion. PLoS One. 6:e188482011. View Article : Google Scholar : PubMed/NCBI

43 

Guo W, Reigan P, Siegel D, Zirrolli J, Gustafson D and Ross D: Formation of 17-allylamino-demethoxygeldanamycin (17-AAG) hydroquinone by NAD(P)H:quinone oxidoreductase 1: Role of 17-AAG hydroquinone in heat shock protein 90 inhibition. Cancer Res. 65:10006–10015. 2005. View Article : Google Scholar : PubMed/NCBI

44 

Bhat R, Xue Y, Berg S, Hellberg S, Ormö M, Nilsson Y, Radesäter AC, Jerning E, Markgren PO, Borgegård T, et al: Structural insights and biological effects of glycogen synthase kinase 3-specific inhibitor AR-A014418. J Biol Chem. 278:45937–45945. 2003. View Article : Google Scholar : PubMed/NCBI

45 

John JK, Paraiso KH, Rebecca VW, Cantini LP, Abel EV, Pagano N, Meggers E, Mathew R, Krepler C, Izumi V, et al: GSK3β inhibition blocks melanoma cell/host interactions by downregulating N-cadherin expression and decreasing FAK phosphorylation. J Invest Dermatol. 132:2818–2827. 2012. View Article : Google Scholar : PubMed/NCBI

46 

Wu H, Hasan R, Zhang H, Gray J, Williams D, Miller M, Allen F, Lee V, Kelly T and Zhou GL: Phosphorylation regulates CAP1 (cyclase-associated protein 1) functions in the motility and invasion of pancreatic cancer cells. Sci Rep. 9:49252019. View Article : Google Scholar : PubMed/NCBI

47 

Zhou GL, Zhang H, Wu H, Ghai P and Field J: Phosphorylation of the cytoskeletal protein CAP1 controls its association with cofilin and actin. J Cell Sci. 127:5052–5065. 2014.PubMed/NCBI

48 

Rom S, Fan S, Reichenbach N, Dykstra H, Ramirez SH and Persidsky Y: Glycogen synthase kinase 3β inhibition prevents monocyte migration across brain endothelial cells via Rac1-GTPase suppression and down-regulation of active integrin conformation. Am J Pathol. 181:1414–1425. 2012. View Article : Google Scholar : PubMed/NCBI

49 

Yoeli-Lerner M, Chin YR, Hansen CK and Toker A: Akt/protein kinase B and glycogen synthase kinase-3β signaling pathway regulates cell migration through the NFAT1 transcription factor. Mol Cancer Res. 7:425–432. 2009. View Article : Google Scholar : PubMed/NCBI

50 

Zhao J, Xu J, Zhao J and Zhang R: EFEMP2 promotes colon cancer cell invasion and growth through the ERK1/2 signaling pathway. Int J Clin Exp Pathol. 12:851–856. 2019.PubMed/NCBI

51 

Rath T, Stöckle J, Roderfeld M, Tschuschner A, Graf J and Roeb E: Matrix metalloproteinase-13 is regulated by toll-like receptor-9 in colorectal cancer cells and mediates cellular migration. Oncol Lett. 2:483–488. 2011. View Article : Google Scholar : PubMed/NCBI

52 

Nakajima H and Koizumi K: Family with sequence similarity 107: A family of stress responsive small proteins with diverse functions in cancer and the nervous system (Review). Biomed Rep. 2:321–325. 2014. View Article : Google Scholar : PubMed/NCBI

53 

Kretzschmar A, Schülke JP, Masana M, Dürre K, Müller MB, Bausch AR and Rein T: The stress-inducible protein DRR1 exerts distinct effects on actin dynamics. Int J Mol Sci. 19:39932018. View Article : Google Scholar : PubMed/NCBI

54 

Guo J, Bian Y, Wang Y, Chen L, Yu A and Sun X: FAM107B is regulated by S100A4 and mediates the effect of S100A4 on the proliferation and migration of MGC803 gastric cancer cells. Cell Biol Int. 41:1103–1109. 2017. View Article : Google Scholar : PubMed/NCBI

55 

Allgöwer C, Kretz AL, von Karstedt S, Wittau M, Henne-Bruns D and Lemke J: Friend or foe: S100 proteins in cancer. Cancers (Basel). 12:20372020. View Article : Google Scholar : PubMed/NCBI

56 

Chen M, Bresnick AR and O'Connor KL: Coupling S100A4 to rhotekin alters Rho signaling output in breast cancer cells. Oncogene. 32:3754–3764. 2013. View Article : Google Scholar : PubMed/NCBI

57 

Huang CY, Wei PL, Chen WY, Chang WC and Chang YJ: Silencing heat shock protein 27 inhibits the progression and metastasis of colorectal cancer (CRC) by maintaining the stability of stromal interaction molecule 1 (STIM1) proteins. Cells. 7:2622018. View Article : Google Scholar : PubMed/NCBI

58 

Lin Y, Peng N, Zhuang H, Zhang D, Wang Y and Hua ZC: Heat shock proteins HSP70 and MRJ cooperatively regulate cell adhesion and migration through urokinase receptor. BMC Cancer. 14:6392014. View Article : Google Scholar : PubMed/NCBI

59 

Moser C, Lang SA, Kainz S, Gaumann A, Fichtner-Feigl S, Koehl GE, Schlitt HJ, Geissler EK and Stoeltzing O: Blocking heat shock protein-90 inhibits the invasive properties and hepatic growth of human colon cancer cells and improves the efficacy of oxaliplatin in p53-deficient colon cancer tumors in vivo. Mol Cancer Ther. 6:2868–2878. 2007. View Article : Google Scholar : PubMed/NCBI

60 

Hagn F, Lagleder S, Retzlaff M, Rohrberg J, Demmer O, Richter K, Buchner J and Kessler H: Structural analysis of the interaction between Hsp90 and the tumor suppressor protein p53. Nat Struct Mol Biol. 18:1086–1093. 2011. View Article : Google Scholar : PubMed/NCBI

61 

Lacey T and Lacey H: Linking hsp90′s role as an evolutionary capacitator to the development of cancer. Cancer Treat Res Commun. 28:1004002021. View Article : Google Scholar : PubMed/NCBI

62 

Dou F, Chang X and Ma D: Hsp90 maintains the stability and function of the Tau phosphorylating kinase GSK3β. Int J Mol Sci. 8:51–60. 2007. View Article : Google Scholar

63 

Banz VM, Medová M, Keogh A, Furer C, Zimmer Y, Candinas D and Stroka D: Hsp90 transcriptionally and post-translationally regulates the expression of NDRG1 and maintains the stability of its modifying kinase GSK3β. Biochim Biophys Acta. 1793:1597–1603. 2009. View Article : Google Scholar : PubMed/NCBI

64 

Tang W, Wu Y, Qi X, Yu R, Lu Z, Chen A, Fan X and Li J: PGK1-coupled HSP90 stabilizes GSK3β expression to regulate the stemness of breast cancer stem cells. Cancer Biol Med. 19:486–503. 2022. View Article : Google Scholar : PubMed/NCBI

65 

Muller P, Ruckova E, Halada P, Coates PJ, Hrstka R, Lane DP and Vojtesek B: C-terminal phosphorylation of Hsp70 and Hsp90 regulates alternate binding to co-chaperones CHIP and HOP to determine cellular protein folding/degradation balances. Oncogene. 32:3101–3110. 2013. View Article : Google Scholar : PubMed/NCBI

66 

Zhang C, Li S and Zhao Z: β-Elemene promotes apoptosis induced by hyperthermia via inhibiting HSP70. Dis Markers. 2022:73130262022.PubMed/NCBI

67 

Schwock J, Dhani N, Cao MP, Zheng J, Clarkson R, Radulovich N, Navab R, Horn LC and Hedley DW: Targeting focal adhesion kinase with dominant-negative FRNK or Hsp90 inhibitor 17-DMAG suppresses tumor growth and metastasis of SiHa cervical xenografts. Cancer Res. 69:4750–4759. 2009. View Article : Google Scholar : PubMed/NCBI

68 

Taiyab A and Rao ChM: HSP90 modulates actin dynamics: Inhibition of HSP90 leads to decreased cell motility and impairs invasion. Biochim Biophys Acta. 1813:213–221. 2011. View Article : Google Scholar : PubMed/NCBI

69 

Liu Z, Li H, He L, Xiang Y, Tian C, Li C, Tan P, Jing J, Tian Y, Du L, et al: Discovery of small-molecule inhibitors of the HSP90-calcineurin-NFAT pathway against glioblastoma. Cell Chem Biol. 26:352–365.e7. 2019. View Article : Google Scholar : PubMed/NCBI

70 

Lu C, Chen D, Zhang Z, Fang F, Wu Y, Luo L and Yin Z: Heat shock protein 90 regulates the stability of c-Jun in HEK293 Cells. Mol Cells. 24:210–214. 2007.PubMed/NCBI

71 

Stellas D, El Hamidieh A and Patsavoudi E: Monoclonal antibody 4C5 prevents activation of MMP2 and MMP9 by disrupting their interaction with extracellular HSP90 and inhibits formation of metastatic breast cancer cell deposits. BMC Cell Biol. 11:512010. View Article : Google Scholar : PubMed/NCBI

72 

Jia D, Rao W, Wang C, Jin C, Wang S, Chen D, Zhang M, Guo J, Chang Z and Liu J: Inhibition of B16 murine melanoma metastasis and enhancement of immunity by fever-range whole body hyperthermia. Int J Hyperthermia. 27:275–285. 2011. View Article : Google Scholar : PubMed/NCBI

73 

Byun YH, Gwak HS, Kwon JW, Song MK, Shin SH, Jo YH, Yoo H and Lee SH: Local recurrence of brain metastasis reduced by intra-operative hyperthermia treatment. Int J Hyperthermia. 35:168–175. 2019. View Article : Google Scholar : PubMed/NCBI

74 

Zhao J, Lv Y, Cai Y, Wei W, Yin C, Wang X, Hao Z, Shen C and Wang H: Hyperthermic carbon dioxide pneumoperitoneum reinforces the inhibition of 5-FU on the proliferation and invasion of colon cancer. Oncol Rep. 37:492–500. 2017. View Article : Google Scholar : PubMed/NCBI

75 

Kumar S, Stokes J III, Singh UP, Scissum Gunn K, Acharya A, Manne U and Mishra M: Targeting HSP70: A possible therapy for cancer. Cancer Lett. 374:156–166. 2016. View Article : Google Scholar : PubMed/NCBI

76 

Kryeziu K, Bruun J, Guren TK, Sveen A and Lothe RA: Combination therapies with HSP90 inhibitors against colorectal cancer. Biochim Biophys Acta Rev Cancer. 1871:240–247. 2019. View Article : Google Scholar : PubMed/NCBI

77 

Zhou L, Zhang M, Fu Q, Li J and Sun H: Targeted near infrared hyperthermia combined with immune stimulation for optimized therapeutic efficacy in thyroid cancer treatment. Oncotarget. 7:6878–6890. 2016. View Article : Google Scholar : PubMed/NCBI

78 

Vriend LEM, van den Tempel N, Oei AL, L'Acosta M, Pieterson FJ, Franken NAP, Kanaar R and Krawczyk PM: Boosting the effects of hyperthermia-based anticancer treatments by HSP90 inhibition. Oncotarget. 8:97490–97503. 2017. View Article : Google Scholar : PubMed/NCBI

79 

Daunys S, Matulis D and Petrikaitė V: Synergistic activity of HSP90 inhibitors and anticancer agents in pancreatic cancer cell cultures. Sci Rep. 9:161772019. View Article : Google Scholar : PubMed/NCBI

80 

Baran B, Mert Ozupek N, Yerli Tetik N, Acar E, Bekcioglu O and Baskin Y: Difference between left-sided and right-sided colorectal cancer: A focused review of literature. Gastroenterology Res. 11:264–273. 2018. View Article : Google Scholar : PubMed/NCBI

81 

de Vries NL, Swets M, Vahrmeijer AL, Hokland M and Kuppen PJ: The immunogenicity of colorectal cancer in relation to tumor development and treatment. Int J Mol Sci. 17:10302016. View Article : Google Scholar : PubMed/NCBI

82 

Picard E, Verschoor CP, Ma GW and Pawelec G: Relationships between immune landscapes, genetic subtypes and responses to immunotherapy in colorectal cancer. Front Immunol. 11:3692020. View Article : Google Scholar : PubMed/NCBI

83 

Zhang H, Du Y, Wang Z, Lou R, Wu J and Feng J: Integrated analysis of oncogenic networks in colorectal cancer identifies GUCA2A as a molecular marker. Biochem Res Int. 2019:64694202019. View Article : Google Scholar : PubMed/NCBI

84 

Mah WC, Thurnherr T, Chow PK, Chung AY, Ooi LL, Toh HC, Teh BT, Saunthararajah Y and Lee CG: Methylation profiles reveal distinct subgroup of hepatocellular carcinoma patients with poor prognosis. PLoS One. 9:e1041582014. View Article : Google Scholar : PubMed/NCBI

85 

Song MA, Tiirikainen M, Kwee S, Okimoto G, Yu H and Wong LL: Elucidating the landscape of aberrant DNA methylation in hepatocellular carcinoma. PLoS One. 8:e557612013. View Article : Google Scholar : PubMed/NCBI

86 

Kan S, Chai S, Chen W and Yu B: DNA methylation profiling identifies potentially significant epigenetically-regulated genes in glioblastoma multiforme. Oncol Lett. 18:1679–1688. 2019.PubMed/NCBI

87 

Parameswaran R, Ramakrishnan P, Moreton SA, Xia Z, Hou Y, Lee DA, Gupta K, deLima M, Beck RC and Wald DN: Repression of GSK3 restores NK cell cytotoxicity in AML patients. Nat Commun. 7:111542016. View Article : Google Scholar : PubMed/NCBI

88 

Cichocki F, Valamehr B, Bjordahl R, Zhang B, Rezner B, Rogers P, Gaidarova S, Moreno S, Tuininga K, Dougherty P, et al: GSK3 inhibition drives maturation of NK cells and enhances their antitumor activity. Cancer Res. 77:5664–5675. 2017. View Article : Google Scholar : PubMed/NCBI

89 

Noh KT, Son KH, Jung ID, Kang TH, Choi CH and Park YM: Glycogen synthase kinase-3β (GSK-3β) inhibition enhances dendritic cell-based cancer vaccine potency via suppression of interferon-γ-induced indoleamine 2,3-dioxygenase expression. J Biol Chem. 290:12394–12402. 2015. View Article : Google Scholar : PubMed/NCBI

90 

Taylor A, Harker JA, Chanthong K, Stevenson PG, Zuniga EI and Rudd CE: Glycogen synthase kinase 3 inactivation drives T-bet-mediated downregulation of co-receptor PD-1 to enhance CD8(+) cytolytic T cell responses. Immunity. 44:274–286. 2016. View Article : Google Scholar : PubMed/NCBI

91 

Grassilli E, Narloch R, Federzoni E, Ianzano L, Pisano F, Giovannoni R, Romano G, Masiero L, Leone BE, Bonin S, et al: Inhibition of GSK3B bypass drug resistance of p53-null colon carcinomas by enabling necroptosis in response to chemotherapy. Clin Cancer Res. 19:3820–3831. 2013. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Koizumi K, Domoto T, Minamoto T, Satomura K and Nakajima H: Deactivation of glycogen synthase kinase-3β by heat shock‑inducible tumor small protein attenuates hyperthermia‑induced pro‑migratory activity in colorectal cancer cells. Int J Oncol 63: 92, 2023.
APA
Koizumi, K., Domoto, T., Minamoto, T., Satomura, K., & Nakajima, H. (2023). Deactivation of glycogen synthase kinase-3β by heat shock‑inducible tumor small protein attenuates hyperthermia‑induced pro‑migratory activity in colorectal cancer cells. International Journal of Oncology, 63, 92. https://doi.org/10.3892/ijo.2023.5540
MLA
Koizumi, K., Domoto, T., Minamoto, T., Satomura, K., Nakajima, H."Deactivation of glycogen synthase kinase-3β by heat shock‑inducible tumor small protein attenuates hyperthermia‑induced pro‑migratory activity in colorectal cancer cells". International Journal of Oncology 63.2 (2023): 92.
Chicago
Koizumi, K., Domoto, T., Minamoto, T., Satomura, K., Nakajima, H."Deactivation of glycogen synthase kinase-3β by heat shock‑inducible tumor small protein attenuates hyperthermia‑induced pro‑migratory activity in colorectal cancer cells". International Journal of Oncology 63, no. 2 (2023): 92. https://doi.org/10.3892/ijo.2023.5540
Copy and paste a formatted citation
x
Spandidos Publications style
Koizumi K, Domoto T, Minamoto T, Satomura K and Nakajima H: Deactivation of glycogen synthase kinase-3β by heat shock‑inducible tumor small protein attenuates hyperthermia‑induced pro‑migratory activity in colorectal cancer cells. Int J Oncol 63: 92, 2023.
APA
Koizumi, K., Domoto, T., Minamoto, T., Satomura, K., & Nakajima, H. (2023). Deactivation of glycogen synthase kinase-3β by heat shock‑inducible tumor small protein attenuates hyperthermia‑induced pro‑migratory activity in colorectal cancer cells. International Journal of Oncology, 63, 92. https://doi.org/10.3892/ijo.2023.5540
MLA
Koizumi, K., Domoto, T., Minamoto, T., Satomura, K., Nakajima, H."Deactivation of glycogen synthase kinase-3β by heat shock‑inducible tumor small protein attenuates hyperthermia‑induced pro‑migratory activity in colorectal cancer cells". International Journal of Oncology 63.2 (2023): 92.
Chicago
Koizumi, K., Domoto, T., Minamoto, T., Satomura, K., Nakajima, H."Deactivation of glycogen synthase kinase-3β by heat shock‑inducible tumor small protein attenuates hyperthermia‑induced pro‑migratory activity in colorectal cancer cells". International Journal of Oncology 63, no. 2 (2023): 92. https://doi.org/10.3892/ijo.2023.5540
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