Epithelial-to-mesenchymal transition and ovarian tumor progression induced by tissue transglutaminase

Cancer Research

Volumn 69, Issue 24, 2009, Pages 9192-9201

  Shao, Minghai ^a   Cao, Liyun ^a   Shen, Changyu ^a   Satpathy, Minati ^a   Chelladurai, Bhadrani ^a   Bigsby, Robert M ^a,b   Nakshatri, Harikrishna ^a,b   Matei, Daniela ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MATRIGEL; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE ANTIBODY; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INVASION; CELL INVASION; CELL TRANSFORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM CELL; FEMALE; GENE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MESENCHYME CELL; METASTASIS; METASTASIS POTENTIAL; MOUSE; NONHUMAN; OVARY CARCINOMA; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; TUMOR XENOGRAFT;

ANIMALS; ASCITES; CADHERINS; CELL LINE, TUMOR; DISEASE PROGRESSION; EPITHELIAL CELLS; FEMALE; HOMEODOMAIN PROTEINS; HUMANS; MESODERM; MICE; MICE, INBRED BALB C; MICE, NUDE; NF-KAPPA B; OVARIAN NEOPLASMS; PERITONEAL NEOPLASMS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; TRANSGLUTAMINASES; TRANSPLANTATION, HETEROLOGOUS;

EID: 73649115337     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-1257     Document Type: Article

References (50)

1. Satpathy M, Cao L, Pincheira R, et al. Enhanced peritoneal ovarian tumor dissemination by tissue transglutaminase. Cancer Res 2007;67:7194-202.
2. Mann AP, Verma A, Sethi G, et al. Overexpression of tissue transglutaminase leads to constitutive activation of nuclear factor-κB in cancer cells: delineation of a novel pathway. Cancer Res 2006;66:8788-95.
3. Pincus JH, Waelsch H. The specificity of transglutaminase. II. Structural requirements of the amine substrate. Arch Biochem Biophys 1968;126:44-52.
4. Matei D, Graeber TG, Baldwin RL, Karlan BY, Rao J, Chang DD. Gene expression in epithelial ovarian carcinoma. Oncogene 2002;21:6289-98.
5. Fesus L, Piacentini M. Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci 2002;27:534-9.
6. Verma A, Guha S, Wang H, et al. Tissue transglutaminase regulates focal adhesion kinase/AKT activation by modulating PTEN expression in pancreatic cancer cells. Clin Cancer Res 2008;14:1997-2005.
7. Satpathy M, Shao M, Emerson R, Donner DB, Matei D. Tissue transglutaminase regulates MMP-2 in ovarian cancer by modulating CREB activity. J Biol Chem 2009; 284:15390-9.
8. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002;2:442-54.
9. Yamashita S, Miyagi C, Fukada T, Kagara N, Che YS, Hirano T. Zinc transporter LIVI controls epithelial-mesenchymal transition in zebrafish gastrula organizer. Nature 2004;429:298-302.
10. Nagar B, Overduin M, Ikura M, Rini JM. Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature 1996;380:360-4.
11. Shapiro L, Fannon AM, Kwong PD, et al. Structural basis of cell-cell adhesion by cadherins. Nature 1995;374: 327-37.
12. Nagafuchi A, Shirayoshi Y, Okazaki K, Yasuda K, Takeichi M. Transformation of cell adhesion properties by exogenously introduced E-cadherin cDNA. Nature 1987;329:341-3.
13. Patel DJ, Gumbiner BM. Cell-cell recognition. Zipping together a cell adhesion interface. Nature 1995; 374:306-7.
14. Cavey M, Rauzi M, Lenne PF, Lecuit T. A two-tiered mechanism for stabilization and immobilization of Ecadherin. Nature 2008;453:751-6.
15. Perl AK, Wilgenbus P, Dahl U, Semb H, Christofori G. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 1998;392:190-3.
16. Kuphal S, Bosserhoff AK. Influence of the cytoplasmic domain of E-cadherin on endogenous N-cadherin expression in malignant melanoma. Oncogene 2006;25: 248-59.
17. Kim JB, Islam S, Kim YJ, et al. N-Cadherin extracellular repeat 4 mediates epithelial to mesenchymal transition and increased motility. J Cell Biol 2000;151:1193-206.
18. Nieman MT, Prudoff RS, Johnson KR, Wheelock MJ. N-cadherin promotes motility in human breast cancer cells regardless of their E-cadherin expression. J Cell Biol 1999;147:631-44.
19. Graff JR, Herman JG, Lapidus RG, et al. E-cadherin expression is silenced by DNA hypermethylation in human breast and prostate carcinomas. Cancer Res 1995; 55:5195-9.
20. Hajra KM, Chen DY, Fearon ER. The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res 2002;62:1613-8.
21. Moreno-Bueno G, Cubillo E, Sarrio D, et al. Genetic profiling of epithelial cells expressing E-cadherin repressors reveals a distinct role for Snail, Slug, and E47 factors in epithelial-mesenchymal transition. Cancer Res 2006;66:9543-56.
22. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 2007;7:415-28.
23. Boyer B, Roche S, Denoyelle M, Thiery JP. Src and Ras are involved in separate pathways in epithelial cell scattering. EMBO J 1997;16:5904-13.
24. Rodier JM, Valles AM, Denoyelle M, Thiery JP, Boyer B. pp60c-src is a positive regulator of growth factor-induced cell scattering in a rat bladder carcinoma cell line. J Cell Biol 1995;131:761-73.
25. Grille SJ, Bellacosa A, Upson J, et al. The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res 2003;63:2172-8.
26. Zhou BP, Deng J, Xia W, et al. Dual regulation of Snail by GSK-3β-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 2004;6: 931-40.
27. Chua HL, Bhat-Nakshatri P, Clare SE, Morimiya A, Badve S, Nakshatri H. NF-κB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene 2007;26: 711-24.
28. Fuchs BC, Fujii T, Dorfman JD, et al. Epithelialto-mesenchymal transition and integrin-linked kinase mediate sensitivity to epidermal growth factor receptor inhibition in human hepatoma cells. Cancer Res 2008;68: 2391-9.
29. Li Y, Yang J, Dai C, Wu C, Liu Y. Role for integrinlinked kinase in mediating tubular epithelial to mesenchymal transition and renal interstitial fibrogenesis. J Clin Invest 2003;112:503-16.
30. Akimov SS, Krylov D, Fleischman LF, Belkin AM. Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J Cell Biol 2000;148:825-38.
31. Tucholski J, Lesort M, Johnson GV. Tissue transglutaminase is essential for neurite outgrowth in human neuroblastoma SH-SY5Y cells. Neuroscience 2001;102: 481-91.
32. DiFeo A, Narla G, Camacho-Vanegas O, et al. Ecadherin is a novel transcriptional target of the KLF6 tumor suppressor. Oncogene 2006;25:6026-31.
33. Sodek KL, Ringuette MJ, Brown TJ. Compact spheroid formation by ovarian cancer cells is associated with contractile behavior and an invasive phenotype. Int J Cancer 2008;124:2060-70.
34. Cao L, Petrusca DN, Satpathy M, Nakshatri H, Petrache I, Matei D. Tissue transglutaminase protects epithelial ovarian cancer cells from cisplatin induced apoptosis by promoting cell survival signaling. Carcinogenesis 2008;29:1893-900.
35. Julien S, Puig I, Caretti E, et al. Activation of NF-κB by Akt upregulates Snail expression and induces epithelium mesenchyme transition. Oncogene 2007;26:7445-56.
36. Olmeda D, Jorda M, Peinado H, Fabra A, Cano A. Snail silencing effectively suppresses tumour growth and invasiveness. Oncogene 2007;26:1862-74.
37. Tothill RW, Tinker AV, George J, et al. Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin Cancer Res 2008;14: 5198-208.
38. Hurt EM, Saykally JN, Anose BM, Kalli KR, Sanders MM. Expression of the ZEB1 (δEF1) transcription factor in human: additional insights. Mol Cell Biochem 2008; 318:89-99.
39. Cheng GZ, Chan J, Wang Q, Zhang W, Sun CD, Wang LH. Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion, and resistance to paclitaxel. Cancer Res 2007;67:1979-87.
40. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008;22:894-907.
41. Burleson KM, Hansen LK, Skubitz AP. Ovarian carcinoma spheroids disaggregate on type I collagen and invade live human mesothelial cell monolayers. Clin Exp Metastasis 2004;21:685-97.
42. Park SH, Cheung LW, Wong AS, Leung PC. Estrogen regulates Snail and Slug in the down-regulation of Ecadherin and induces metastatic potential of ovarian cancer cells through estrogen receptor α. Mol Endocrinol 2008;22:2085-98.
43. Ahmed N, Maines-Bandiera S, Quinn MA, Unger WG, Dedhar S, Auersperg N. Molecular pathways regulating EGF-induced epithelio-mesenchymal transition in human ovarian surface epithelium. Am J Physiol Cell Physiol 2006;290:C1532-42.
44. Duong TD, Erickson CA. MMP-2 plays an essential role in producing epithelial-mesenchymal transformations in the avian embryo. Dev Dyn 2004;229:42-53.
45. Shaw TJ, Senterman MK, Dawson K, Crane CA, Vanderhyden BC. Characterization of intraperitoneal, orthotopic, and metastatic xenograft models of human ovarian cancer. Mol Ther 2004;10:1032-42.
46. Fu X, Hoffman RM. Human ovarian carcinoma metastatic models constructed in nude mice by orthotopic transplantation of histologically-intact patient specimens. Anticancer Res 1993;13:283-6.
47. Sengupta S, Kim KS, Berk MP, et al. Lysophosphatidic acid downregulates tissue inhibitor of metalloproteinases, which are negatively involved in lysophosphatidic acid-induced cell invasion. Oncogene 2007;26: 2894-901.
48. Tom BH, Rutzky LP, Oyasu R, Tomita JT, Goldenberg DM, Kahan BD. Human colon adenocarcinoma cells. II. Tumorigenic and organoid expression in vivo and in vitro. J Natl Cancer Inst 1977;58:1507-12.
49. Hwang JY, Mangala LS, Fok JY, et al. Clinical and biological significance of tissue transglutaminase in ovarian carcinoma. Cancer Res 2008;68:5849-58.
50. Verma A, Wang H, Manavathi B, et al. Increased expression of tissue transglutaminase in pancreatic ductal adenocarcinoma and its implications in drug resistance and metastasis. Cancer Res 2006;66:10525-33.