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
-
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 - Published online on: June 23, 2023 https://doi.org/10.3892/ijo.2023.5540
- Article Number: 92
This article is mentioned in:
Abstract
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
Tsan MF and Gao B: Heat shock proteins and immune system. J Leukoc Biol. 85:905–910. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
Zhang C, Li S and Zhao Z: β-Elemene promotes apoptosis induced by hyperthermia via inhibiting HSP70. Dis Markers. 2022:73130262022.PubMed/NCBI | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 | |
|
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 |
