p70 S6 kinase drives ovarian cancer metastasis through multicellular spheroid-peritoneum interaction and P-cadherin/β1 integrin signaling activation

Oncotarget

Volumn 5, Issue 19, 2014, Pages 9133-9149

  Man Ip, Carman Ka ^a   Yung, Susan ^a   Chan, Tak Mao ^a   Tsao, Sai Wah ^a   Wong, Alice Sze Tsai ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Adhesion; Metastasis; P cadherin; p70S6K; 1 integrin

Indexed keywords

BETA1 INTEGRIN; GLYCOSYLTRANSFERASE; LYSINE; P CADHERIN; PROTEIN ST6GAL I; REGULATOR PROTEIN; S6 KINASE; SERINE; UNCLASSIFIED DRUG; CADHERIN; CATENIN; DELTA CATENIN; LEUKOCYTE ANTIGEN; SIALYLTRANSFERASE; SMALL INTERFERING RNA; ST6GAL1 PROTEIN, HUMAN;

ARTICLE; CELL ADHESION; CELL COMMUNICATION; CELL INTERACTION; ENZYME INDUCTION; ENZYME SPECIFICITY; GOLGI COMPLEX; HUMAN; HUMAN CELL; IN VIVO STUDY; MESOTHELIUM CELL; MULTICELLULAR SPHEROID; OVARY CANCER; PERITONEUM; PERITONEUM METASTASIS; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIALYLATION; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; TUMOR SEEDING; TUMOR SPHEROID; UPREGULATION; ANIMAL; BIOSYNTHESIS; CYTOLOGY; FEMALE; GENETICS; METABOLISM; METASTASIS; MORTALITY; MOUSE; NONOBESE DIABETIC MOUSE; OVARY TUMOR; PATHOLOGY; PROGNOSIS; RNA INTERFERENCE; SCID MOUSE; TUMOR CELL CULTURE;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD29; CADHERINS; CATENINS; CELL ADHESION; FEMALE; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM METASTASIS; OVARIAN NEOPLASMS; PERITONEUM; PROGNOSIS; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIALYLTRANSFERASES; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED;

EID: 84910070048     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2362     Document Type: Article

References (55)

1. Siegel R, Naishadham D and Jemal A. Cancer statistics, 2012. CA Cancer J Clin. 2012; 62:10-29.
2. Ip CK and Wong AS. Exploiting p70 S6 kinase as a target for ovarian cancer. Expert Opin Ther Targets. 2012; 16:619-630.
3. Altomare DA, Wang HQ, Skele KL, De Rienzo A, Klein-Szanto AJ, Godwin AK and Testa JR. AKT and mTOR phosphorylation is frequently detected in ovarian cancer and can be targeted to disrupt ovarian tumor cell growth. Oncogene. 2004; 23:5853-5857.
4. Zhou HY and Wong AST. Activation of p70(S6K) induces expression of matrix metalloproteinase 9 associated with hepatocyte growth factor-mediated invasion in human ovarian cancer cells. Endocrinology. 2006; 147:2557-2566.
5. Castellvi J, Garcia A, Rojo F, Ruiz-Marcellan C, Gil A, Baselga J and Cajal SRY. Phosphorylated 4E binding protein 1: A hallmark of cell signaling that correlates with survival in ovarian cancer. Cancer. 2006; 107:1801-1811.
6. Pon YL, Zhou HY, Cheung ANY, Ngan HYS and WongAST. p70 S6 kinase promotes epithelial to mesenchymal transition through Snail induction in ovarian cancer cells. Cancer Res. 2008; 68:6524-6532.
7. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell. 2002; 110:673-687.
8. Sundfeldt K. Cell-cell adhesion in the normal ovary and ovarian tumors of epithelial origin; an exception to the rule. Mol Cell Endocrinol. 2003; 202:89-96.
9. Elmasri WM, Casagrande G, Hoskins E, Kimm D and KohnEC. Cell adhesion in ovarian cancer. Cancer Treat Res. 2009; 149:297-318.
10. Sowter HM, Corps AN and Smith SK. Hepatocyte growth factor (HGF) in ovarian epithelial tumour fluids stimulates the migration of ovarian carcinoma cells. Int J Cancer. 1999; 83:476-480.
11. Sawada K, Radjabi AR, Shinomiya N, Kistner E, KennyH, Becker AR, Turkyilmaz MA, Salgia R, Yamada SD, VandeWoude GF, Tretiakova MS and Lengyel E. c-Met overexpression is a prognostic factor in ovarian cancer and an effective target for inhibition of peritoneal dissemination and invasion. Cancer Res. 2007; 67:1670-1679.
12. Wong AS, Pelech SL, Woo MM, Yim G, Rosen B, EhlenT, Leung PC and Auersperg N. Coexpression of hepatocyte growth factor-Met: an early step in ovarian carcinogenesis? Oncogene. 2001; 20:1318-1328.
13. Wong AST, Roskelley CD, Pelech S, Miller D, LeungPCK and Auersperg N. Progressive changes in Met-dependent signaling in a human ovarian surface epithelial model of malignant transformation. Exp Cell Res. 2004; 299:248-256.
14. Moser TL, Pizzo SV, Bafetti LM, Fishman DA and StackMS. Evidence for preferential adhesion of ovarian epithelial carcinoma cells to type I collagen mediated by the alpha2beta1 integrin. Int J Cancer. 1996; 67:695-701.
15. Wilson AP. Mesothelial cells stimulate the anchorage-independent growth of human ovarian tumour cells. BrJCancer. 1989; 59:876-882.
16. Tozer EC, Hughes PE and Loftus JC. Ligand binding and affinity modulation of integrins. Biochem Cell Biol. 1996; 74:785-798.
17. Bellis SL. Variant glycosylation: an underappreciated regulatory mechanism for beta1 integrins. Biochim Biophys Acta. 2004; 1663:52-60.
18. Semel AC, Seales EC, Singhal A, Eklund EA, Colley KJ and Bellis SL. Hyposialylation of integrins stimulates the activity of myeloid fibronectin receptors. J Biol Chem. 2002; 277:32830-32836.
19. Seales EC, Jurado GA, Singhal A and Bellis SL. Ras oncogene directs expression of a differentially sialylated, functionally altered beta1 integrin. Oncogene. 2003; 22:7137-7145.
20. Shaw TJ, Senterman MK, Dawson K, Crane CA and Vanderhyden BC. Characterization of intraperitoneal, orthotopic, and metastatic xenograft models of human cancer. Mol Ther. 2004; 10:1032-1042.
21. Cheung LW, Mak AS, Cheung AN, Ngan HY, Leung PC and Wong AS. P-cadherin cooperates with insulin-like growth factor-1 receptor to promote metastatic signaling of gonadotropin-releasing hormone in ovarian cancer via p120 catenin. Oncogene. 2011; 30:2964-2974.
22. Gumbiner BM. Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol. 2005; 6:622-634.
23. Takeichi M. Morphogenetic roles of classic cadherins. Curr Opin Cell Biol. 1995; 7:619-627.
24. Burleson KM, Hansen LK and Skubitz AP. Ovarian carcinoma spheroids disaggregate on type I collagen and invade live human mesothelial cell monolayers. Clin Exp Metastasis. 2004; 21:685-697.
25. Muller-Klingspor V, Hefler L, Obermair A, Kaider A, Breitenecker G, Leodolte S and Kohlberger P. Prognostic value of beta1-integrin (=CD29) in serous adenocarcinomas of the ovary. Anticancer Res. 2001; 21:2185-2188.
26. Mitra AK, Sawada K, Tiwari P, Mui K, Gwin K and Lengyel E. Ligand-independent activation of c-Met by fibronectin and alpha(5)beta(1)-integrin regulates ovarian cancer invasion and metastasis. Oncogene. 2011; 30:1566-1576.
27. Cheung LW, Leung PC and Wong AS. Cadherin switching and activation of p120 catenin signaling are mediators of gonadotropin-releasing hormone to promote tumor cell migration and invasion in ovarian cancer. Oncogene. 2010; 29:2427-2440.
28. Buczek-Thomas JA, Chen N and Hasan T. Integrin-mediated adhesion and signalling in ovarian cancer cells. Cell Signal. 1998; 10:55-63.
29. Ouyang M, Lu S, Kim T, Chen CE, Seong J, LeckbandDE, Wang F, Reynolds AB, Schwartz MA and Wang Y. N-cadherin regulates spatially polarized signals through distinct p120ctn and beta-catenin-dependent signalling pathways. Nat Commun. 2013; 4:1589.
30. Mukoyama Y, Utani A, Matsui S, Zhou S, Miyachi Y and Matsuyoshi N. T-cadherin enhances cell-matrix adhesiveness by regulating beta1 integrin trafficking in cutaneoussquamous carcinoma cells. Genes Cells. 2007; 12:787-796.
31. Marsden M and DeSimone DW. Integrin-ECM interactions regulate cadherin-dependent cell adhesion and are required for convergent extension in Xenopus. Curr Biol. 2003; 13:1182-1191.
32. Martinez-Rico C, Pincet F, Thiery JP and Dufour S. Integrins stimulate E-cadherin-mediated intercellular adhesion by regulating Src-kinase activation and actomyosin contractility. J Cell Sci. 2010; 123:712-722.
33. Yano H, Mazaki Y, Kurokawa K, Hanks SK, Matsuda M and Sabe H. Roles played by a subset of integrin signaling molecules in cadherin-based cell-cell adhesion. J Cell Biol. 2004; 166:283-295.
34. Niessen CM and Gottardi CJ. Molecular components of the adherens junction. Biochim Biophys Acta. 2008; 1778:562-571.
35. Dall'Olio F. The sialyl-alpha2,6-lactosaminyl-structure: biosynthesis and functional role. Glycoconj J. 2000; 17:669-676.
36. Le Marer N, Laudet V, Svensson EC, Cazlaris H, VanHilleB, Lagrou C, Stehelin D, Montreuil J, Verbert A and Delannoy P. The c-Ha-ras oncogene induces increased expression of beta-galactoside alpha-2, 6-sialyltransferase in rat fibroblast (FR3T3) cells. Glycobiology. 1992; 2:49-56.
37. Svensson EC, Soreghan B and Paulson JC. Organization of the beta-galactoside alpha 2,6-sialyltransferase gene. Evidence for the transcriptional regulation of terminal glycosylation. J Biol Chem. 1990; 265:20863-20868.
38. Vandamme V, Cazlaris H, Le Marer N, Laudet V, LagrouC, Verbert A and Delannoy P. Comparison of sialyl-and alpha-1,3-galactosyltransferase activity in NIH3T3 cells transformed with ras oncogene: increased beta-galactoside alpha-2,6-sialyltransferase. Biochimie. 1992; 74:89-99.
39. Christie DR, Shaikh FM, Lucas JAt, Lucas JA 3rd and Bellis SL. ST6Gal-I expression in ovarian cancer cells promotes an invasive phenotype by altering integrin glycosylation and function. J Ovarian Res. 2008; 1:3.
40. Dall'Olio F and Chiricolo M. Sialyltransferases in cancer. Glycoconj J. 2001; 18:841-850.
41. Schultz MJ, Swindall AF, Wright JW, Sztul ES, Landen CN and Bellis SL. ST6Gal-I sialyltransferase confers cisplatin resistance in ovarian tumor cells. J Ovarian Res. 2013; 6:25.
42. Tang MK, Zhou HY, Yam JW and Wong AS. c-Met overexpression contributes to the acquired apoptotic resistance of nonadherent ovarian cancer cells through a cross talk mediated by phosphatidylinositol 3-kinase and extracellular signal-regulated kinase 1/2. Neoplasia. 2010; 12:128-138.
43. Zietarska M, Maugard CM, Filali-Mouhim A, Alam-FahmyM, Tonin PN, Provencher DM and Mes-Masson AM. Molecular description of a 3D in vitro model for the study of epithelial ovarian cancer (EOC). Mol Carcinog. 2007; 46:872-885.
44. Mabuchi S, Altomare DA, Cheung M, Zhang L, PoulikakosPI, Hensley HH, Schilder RJ, Ozols RF and Testa JR. RAD001 inhibits human ovarian cancer cell proliferation, enhances cisplatin-induced apoptosis, and prolongs survival in an ovarian cancer model. Clinical cancer research: an official journal of the American Association for Cancer Research. 2007; 13:4261-4270.
45. Mabuchi S, Altomare DA, Connolly DC, Klein-SzantoA, Litwin S, Hoelzle MK, Hensley HH, Hamilton TC and Testa JR. RAD001 (Everolimus) delays tumor onset and progression in a transgenic mouse model of ovarian cancer. Cancer Res. 2007; 67:2408-2413.
46. Takano M, Kikuchi Y, Kudoh K, Goto T, Furuya K, Kikuchi R, Kita T, Fujiwara K, Shiozawa T and AokiD. Weekly administration of temsirolimus for heavily pretreated patients with clear cell carcinoma of the ovary: a report of six cases. International journal of clinical oncology. 2011; 16:605-609.
47. Santiskulvong C, Konecny GE, Fekete M, Chen KY, KaramA, Mulholland D, Eng C, Wu H, Song M and Dorigo O. Dual targeting of phosphoinositide 3-kinase and mammalian target of rapamycin using NVP-BEZ235 as a novel therapeutic approach in human ovarian carcinoma. Clinical cancer research: an official journal of the American Association for Cancer Research. 2011; 17:2373-2384.
48. Huynh H, Teo CC and Soo KC. Bevacizumab and rapamycin inhibit tumor growth in peritoneal model of human ovarian cancer. Molecular cancer therapeutics. 2007; 6:2959-2966.
49. Piha-Paul SA, Wheler JJ, Fu S, Levenback C, Lu K, Falchook GS, Naing A, Hong DS, Tsimberidou AM and Kurzrock R. Advanced gynecologic malignancies treated with a combination of the VEGF inhibitor bevacizumab and the mTOR inhibitor temsirolimus. Oncotarget. 2014; 5:1846-1855.
50. Comas M, Toshkov I, Kuropatwinski KK, Chernova OB, Polinsky A, Blagosklonny MV, Gudkov AV and Antoch MP. New nanoformulation of rapamycin Rapatar extends lifespan in homozygous p53-/-mice by delaying carcinogenesis. Aging. 2012; 4:715-722.
51. Komarova EA, Antoch MP, Novototskaya LR, ChernovaOB, Paszkiewicz G, Leontieva OV, BlagosklonnyMV and Gudkov AV. Rapamycin extends lifespan and delays tumorigenesis in heterozygous p53+/-mice. Aging. 2012; 4:709-714.
52. Leontieva OV, Novototskaya LR, Paszkiewicz GM, Komarova EA, Gudkov AV and Blagosklonny MV. Dysregulation of the mTOR pathway in p53-deficient mice. Cancer biology & therapy. 2013; 14:1182-1188.
53. Romero I and Bast RC Jr. Minireview: human ovarian cancer: biology, current management, and paths to personalizing therapy. Endocrinology. 2012; 153:1593-1602.
54. Iwanicki MP, Davidowitz RA, Ng MR, Besser A, MuranenT, Merritt M, Danuser G, Ince TA and BruggeJS. Ovarian cancer spheroids use myosin-generated force to clear the mesothelium. Cancer Discov. 2011; 1:144-157.
55. Yung S, Li FK and Chan TM. Peritoneal mesothelial cell culture and biology. Perit Dial Int. 2006; 26:162-173.