FOXM1 promotes invasion and migration of colorectal cancer cells partially dependent on HSPA5 transactivation

Oncotarget

Volumn 7, Issue 18, 2016, Pages 26480-26495

  Luo, Xiaoyong ^a   Yao, Jinke ^c   Nie, Peipei ^d   Yang, Zhiyuan ^a   Feng, Hongbo ^a   Chen, Pinjia ^a   Shi, Xinpeng ^a   Zou, Zhengzhi ^b  

^a ZHENGZHOU UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^c SUN YAT SEN UNIVERSITY   (China)

^d GUANGZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Colorectal cancer; FOXM1; HSPA5; Invasion; Migration

Indexed keywords

GELATINASE A; GELATINASE B; GLUCOSE REGULATED PROTEIN 78; HEPATOCYTE NUCLEAR FACTOR 3; X BOX BINDING PROTEIN 1; FORKHEAD BOX PROTEIN M1; FOXM1 PROTEIN, HUMAN; HEAT SHOCK PROTEIN; MOLECULAR CHAPERONE GRP78;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; FOXM1 GENE; GENE; GENETIC ASSOCIATION; HSPA5 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; UPREGULATION; XBP1 GENE; CELL MOTION; COLORECTAL TUMOR; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRANSCRIPTION INITIATION; TUMOR CELL LINE; TUMOR INVASION;

CELL LINE, TUMOR; CELL MOVEMENT; COLORECTAL NEOPLASMS; FORKHEAD BOX PROTEIN M1; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAT-SHOCK PROTEINS; HUMANS; NEOPLASM INVASIVENESS; TRANSCRIPTIONAL ACTIVATION;

EID: 84967102076     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8419     Document Type: Article

References (53)

1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015; 65:87-108.
2. Davila RE, Rajan E, Baron TH, Adler DG, Egan JV, Faigel DO, Gan SI, Hirota WK, Leighton JA, Lichtenstein D, Qureshi WA, Shen B, Zuckerman MJ, VanGuilder T, Fanelli RD. ASGE guideline: colorectal cancer screening and surveillance. Gastrointest Endosc. 2006; 63:546-557.
3. Koo CY, Muir KW, Lam EW. FOXM1: From cancer initiation to progression and treatment. Biochim Biophys Acta. 2012; 1819:28-37.
4. Myatt SS, Lam EW. The emerging roles of forkhead box (Fox) proteins in cancer. Nat Rev Cancer. 2007; 7:847-859.
5. Kong X, Li L, Li Z, Le X, Huang C, Jia Z, Cui J, Huang S, Wang L, Xie K. Dysregulated expression of FOXM1 isoforms drives progression of pancreatic cancer. Cancer Res. 2013; 73:3987-3996.
6. Yu G, Zhou A, Xue J, Huang C, Zhang X, Kang SH, Chiu WT, Tan C, Xie K, Wang J, Huang S. FoxM1 promotes breast tumorigenesis by activating PDGF-A and forming a positive feedback loop with the PDGF/AKT signaling pathway. Oncotarget. 2015; 6:11281-11294. doi: 10.18632/oncotarget.3596.
7. Laoukili J, Stahl M, Medema RH. FoxM1: at the crossroads of ageing and cancer. Biochim Biophys Acta. 2007; 1775:92-102.
8. Laoukili J, Kooistra MR, Bras A, Kauw J, Kerkhoven RM, Morrison A, Clevers H, Medema RH. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol. 2005; 7:126-136.
9. Wonsey DR, Follettie MT. Loss of the forkhead transcription factor FoxM1 causes centrosome amplification and mitotic catastrophe. Cancer Res. 2005; 65:5181-5189.
10. Zona S, Bella L, Burton MJ, Nestal DMG, Lam EW. FOXM1: an emerging master regulator of DNA damage response and genotoxic agent resistance. Biochim Biophys Acta. 2014; 1839:1316-1322.
11. Xu K, Liu X, Mao X, Xue L, Wang R, Chen L, Chu X. MicroRNA-149 suppresses colorectal cancer cell migration and invasion by directly targeting forkhead box transcription factor FOXM1. Cell Physiol Biochem. 2015; 35:499-515.
12. Chiu WT, Huang YF, Tsai HY, Chen CC, Chang CH, Huang SC, Hsu KF, Chou CY. FOXM1 confers to epithelial-mesenchymal transition, stemness and chemoresistance in epithelial ovarian carcinoma cells. Oncotarget. 2015; 6:2349-2365. doi: 10.18632/oncotarget.2957.
13. Li D, Wei P, Peng Z, Huang C, Tang H, Jia Z, Cui J, Le X, Huang S, Xie K. The critical role of dysregulated FOXM1-PLAUR signaling in human colon cancer progression and metastasis. Clin Cancer Res. 2013; 19:62-72.
14. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell. 2000; 101:249-258.
15. Abdel MM, Jagannathan S, Malek E, Sayed DM, Elgammal SA, Abd EH, Thabet NM, Driscoll JJ. Molecular chaperone GRP78 enhances aggresome delivery to autophagosomes to promote drug resistance in multiple myeloma. Oncotarget. 2015; 6:3098-3110. doi: 10.18632/oncotarget.3075.
16. Raiter A, Yerushalmi R, Hardy B. Pharmacological induction of cell surface GRP78 contributes to apoptosis in triple negative breast cancer cells. Oncotarget. 2014; 5:11452-11463. doi: 10.18632/oncotarget.2576.
17. Misra UK, Deedwania R, Pizzo SV. Binding of activated alpha2-macroglobulin to its cell surface receptor GRP78 in 1-LN prostate cancer cells regulates PAK-2-dependent activation of LIMK. J Biol Chem. 2005; 280:26278-26286.
18. Li Z, Zhang L, Zhao Y, Li H, Xiao H, Fu R, Zhao C, Wu H, Li Z. Cell-surface GRP78 facilitates colorectal cancer cell migration and invasion. Int J Biochem Cell Biol. 2013; 45:987-994.
19. Yao X, Liu H, Zhang X, Zhang L, Li X, Wang C, Sun S. Cell Surface GRP78 Accelerated Breast Cancer Cell Proliferation and Migration by Activating STAT3. Plos One. 2015; 10:e125634.
20. Zhang J, Jiang Y, Jia Z, Li Q, Gong W, Wang L, Wei D, Yao J, Fang S, Xie K. Association of elevated GRP78 expression with increased lymph node metastasis and poor prognosis in patients with gastric cancer. Clin Exp Metastasis. 2006; 23:401-410.
21. Chang YJ, Chiu CC, Wu CH, An J, Wu CC, Liu TZ, Wei PL, Huang MT. Glucose-regulated protein 78 (GRP78) silencing enhances cell migration but does not influence cell proliferation in hepatocellular carcinoma. Ann Surg Oncol. 2010; 17:1703-1709.
22. Arap MA, Lahdenranta J, Mintz PJ, Hajitou A, Sarkis AS, Arap W, Pasqualini R. Cell surface expression of the stress response chaperone GRP78 enables tumor targeting by circulating ligands. Cancer Cell. 2004; 6:275-284.
23. Raiter A, Vilkin A, Gingold R, Levi Z, Halpern M, Niv Y, Hardy B. The presence of anti-GRP78 antibodies in the serum of patients with colorectal carcinoma: a potential biomarker for early cancer detection. Int J Biol Markers. 2014; 29:e431-e435.
24. Zhao L, Ackerman SL. Endoplasmic reticulum stress in health and disease. Curr Opin Cell Biol. 2006; 18:444-452.
25. Vellanki RN, Zhang L, Volchuk A. OASIS/CREB3L1 is induced by endoplasmic reticulum stress in human glioma cell lines and contributes to the unfolded protein response, extracellular matrix production and cell migration. Plos One. 2013; 8:e54060.
26. Xia LM, Huang WJ, Wang B, Liu M, Zhang Q, Yan W, Zhu Q, Luo M, Zhou ZZ, Tian DA. Transcriptional up-regulation of FoxM1 in response to hypoxia is mediated by HIF-1. J Cell Biochem. 2009; 106:247-256.
27. Yusuf D, Butland SL, Swanson MI, Bolotin E, Ticoll A, Cheung WA, Zhang XY, Dickman CT, Fulton DL, Lim JS, Schnabl JM, Ramos OH, Vasseur-Cognet M, et al. The transcription factor encyclopedia. Genome Biol. 2012; 13:R24.
28. Dai B, Kang SH, Gong W, Liu M, Aldape KD, Sawaya R, Huang S. Aberrant FoxM1B expression increases matrix metalloproteinase-2 transcription and enhances the invasion of glioma cells. Oncogene. 2007; 26:6212-6219.
29. Yuan XP, Dong M, Li X, Zhou JP. GRP78 promotes the invasion of pancreatic cancer cells by FAK and JNK. Mol Cell Biochem. 2015; 398:55-62.
30. Huang SC, Ho CT, Lin-Shiau SY, Lin JK. Carnosol inhibits the invasion of B16/F10 mouse melanoma cells by suppressing metalloproteinase-9 through down-regulating nuclear factor-kappa B and c-Jun. Biochem Pharmacol. 2005; 69:221-232.
31. Hsieh YS, Chu SC, Yang SF, Chen PN, Liu YC, Lu KH. Silibinin suppresses human osteosarcoma MG-63 cell invasion by inhibiting the ERK-dependent c-Jun/AP-1 induction of MMP-2. Carcinogenesis. 2007; 28:977-987.
32. Song IS, Jeong YJ, Jeong SH, Heo HJ, Kim HK, Bae KB, Park YH, Kim SU, Kim JM, Kim N, Ko KS, Rhee BD, Han J. FOXM1-induced PRX3 Regulates Stemness and Survival of Colon Cancer Cells via Maintenance of Mitochondrial Function. Gastroenterology. 2015; 149:1006-16.e9.
33. Briest F, Berg E, Grass I, Freitag H, Kaemmerer D, Lewens F, Christen F, Arsenic R, Altendorf-Hofmann A, Kunze A, Sanger J, Knosel T, Siegmund B, Hummel M, Grabowski P. FOXM1: A novel drug target in gastroenteropancreatic neuroendocrine tumors. Oncotarget. 2015; 6:8185-8199. doi: 10.18632/oncotarget.3600.
34. Cook KL, Clarke R. Heat shock 70 kDa protein 5/glucose-regulated protein 78 "AMP"ing up autophagy. Autophagy. 2012; 8:1827-1829.
35. Kandala PK, Srivastava SK. Regulation of macroautophagy in ovarian cancer cells in vitro and in vivo by controlling glucose regulatory protein 78 and AMPK. Oncotarget. 2012; 3:435-449. doi: 10.18632/oncotarget.483.
36. Kang JM, Park S, Kim SJ, Kim H, Lee B, Kim J, Park J, Kim ST, Yang HK, Kim WH, Kim SJ. KIAA1324 Suppresses Gastric Cancer Progression by Inhibiting the Oncoprotein GRP78. Cancer Res. 2015; 75:3087-3097.
37. Bella L, Zona S, Nestal DMG, Lam EW. FOXM1: A key oncofoetal transcription factor in health and disease. Semin Cancer Biol. 2014; 29:32-39.
38. Park HJ, Gusarova G, Wang Z, Carr JR, Li J, Kim KH, Qiu J, Park YD, Williamson PR, Hay N, Tyner AL, Lau LF, Costa RH, Raychaudhuri P. Deregulation of FoxM1b leads to tumour metastasis. EMBO Mol Med. 2011; 3:21-34.
39. Xing X, Lai M, Wang Y, Xu E, Huang Q. Overexpression of glucose-regulated protein 78 in colon cancer. Clin Chim Acta. 2006; 364:308-315.
40. Wei PL, Kuo LJ, Wang W, Lin FY, Liu HH, How T, Ho YS, Huang MT, Wu CH, Chang YJ. Silencing of glucose-regulated protein 78 (GRP78) enhances cell migration through the upregulation of vimentin in hepatocellular carcinoma cells. Ann Surg Oncol. 2012; 19:S572-S579.
41. Takahashi H, Wang JP, Zheng HC, Masuda S, Takano Y. Overexpression of GRP78 and GRP94 is involved in colorectal carcinogenesis. Histol Histopathol. 2011; 26:663-671.
42. Misra UK, Gonzalez-Gronow M, Gawdi G, Wang F, Pizzo SV. A novel receptor function for the heat shock protein Grp78: silencing of Grp78 gene expression attenuates alpha2M*-induced signalling. Cell Signal. 2004; 16:929-938.
43. Zhao S, Li H, Wang Q, Su C, Wang G, Song H, Zhao L, Luan Z, Su R. The role of c-Src in the invasion and metastasis of hepatocellular carcinoma cells induced by association of cell surface GRP78 with activated alpha2M. BMC Cnacer. 2015; 15:389.
44. Zou ZZ, Nie PP, Li YW, Hou BX, Rui-Li, Shi XP, Ma ZK, Han BW, Luo XY. Synergistic induction of apoptosis by salinomycin and gefitinib through lysosomal and mitochondrial dependent pathway overcomes gefitinib resistance in colorectal cancer. Oncotarget. 2015. doi: 10.18632/oncotarget.5628.
45. Lee HK, Xiang C, Cazacu S, Finniss S, Kazimirsky G, Lemke N, Lehman NL, Rempel SA, Mikkelsen T, Brodie C. GRP78 is overexpressed in glioblastomas and regulates glioma cell growth and apoptosis. Neuro Oncol. 2008; 10:236-243.
46. van Schadewijk A, Van'T WE, Stolk J, Hiemstra PS. A quantitative method for detection of spliced X-box binding protein-1 (XBP1) mRNA as a measure of endoplasmic reticulum (ER) stress. Cell Stress Chaperones. 2012; 17:275-279.
47. Nie P, Hu W, Zhang T, Yang Y, Hou B, Zou Z. Synergistic Induction of Erlotinib-Mediated Apoptosis by Resveratrol in Human Non-Small-Cell Lung Cancer Cells by Down-Regulating Survivin and Up-Regulating PUMA. Cell Physiol Biochem. 2015; 35:2255-2271.
48. Lou YF, Zou ZZ, Chen PJ, Huang GB, Li B, Zheng DQ, Yu XR, Luo XY. Combination of gefitinib and DNA methylation inhibitor decitabine exerts synergistic anti-cancer activity in colon cancer cells. Plos One. 2014; 9:e97719.
49. Zou Z, Yuan Z, Zhang Q, Long Z, Chen J, Tang Z, Zhu Y, Chen S, Xu J, Yan M, Wang J, Liu Q. Aurora kinase A inhibition-induced autophagy triggers drug resistance in breast cancer cells. Autophagy. 2012; 8:1798-1810.
50. Mi YJ, Geng GJ, Zou ZZ, Gao J, Luo XY, Liu Y, Li N, Li CL, Chen YQ, Yu XY, Jiang J. Dihydroartemisinin inhibits glucose uptake and cooperates with glycolysis inhibitor to induce apoptosis in non-small cell lung carcinoma cells. Plos One. 2015; 10:e120426.
51. Jiang S, Zou Z, Nie P, Wen R, Xiao Y, Tang J. Synergistic Effects between mTOR Complex 1/2 and Glycolysis Inhibitors in Non-Small-Cell Lung Carcinoma Cells. Plos One. 2015; 10:e132880.
52. Li Q, Zhang N, Jia Z, Le X, Dai B, Wei D, Huang S, Tan D, Xie K. Critical role and regulation of transcription factor FoxM1 in human gastric cancer angiogenesis and progression. Cancer Res. 2009; 69:3501-3509.
53. Chang YJ, Huang YP, Li ZL, Chen CH. GRP78 knockdown enhances apoptosis via the down-regulation of oxidative stress and Akt pathway after epirubicin treatment in colon cancer DLD-1 cells. Plos One. 2012; 7:e35123.