Role of tissue transglutaminase 2 in the acquisition of a mesenchymal-like phenotype in highly invasive A431 tumor cells

Molecular Cancer

Volumn 10, Issue , 2011, Pages

  Lin, Chun Yu ^a,c   Tsai, Pei Hsun ^a   Kandaswami, Chithan C ^b   Chang, Geen Dong ^a   Cheng, Chia Hsiung ^c   Huang, Chang Jen ^a,c   Lee, Ping Ping ^c   Hwang, Jiuan Jiuan ^d   Lee, Ming Ting ^a,c  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b Castle Hills Health   (United States)

^c INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^d NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

Epithelial mesenchymal transition; Matrix metalloproteinase; Migration; NF B; PI3K Akt; Snail; Tissue transglutaminase

Indexed keywords

GELATINASE B; GLYCOGEN SYNTHASE KINASE 3BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN KINASE B; TISSUE TRANSGLUTAMINASE 2; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG; ONCOPROTEIN; TISSUE TRANSGLUTAMINASE 2, HUMAN;

ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CELL INVASION; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; MESENCHYME CELL; MOLECULAR DYNAMICS; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; TUMOR CELL; UPREGULATION; AGED; FEMALE; GENETIC TRANSFECTION; GENETICS; HUMAN; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

GASTROPODA;

AGED, 80 AND OVER; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; MATRIX METALLOPROTEINASE 9; NEOPLASM INVASIVENESS; NEOPLASMS; NF-KAPPA B; ONCOGENE PROTEIN V-AKT; PHENOTYPE; PHOSPHATIDYLINOSITOL 3-KINASES; SIGNAL TRANSDUCTION; TRANSFECTION; TRANSGLUTAMINASES;

EID: 79960556702     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-10-87     Document Type: Article

References (45)

1. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002, 2:442-454. 10.1038/nrc822, 12189386.
2. Thiery JP. Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol 2003, 15:740-746. 10.1016/j.ceb.2003.10.006, 14644200.
3. Yilmaz M, Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev 2009, 28:15-33. 10.1007/s10555-008-9169-0, 19169796.
4. Iwatsuki M, Mimori K, Yokobori T, Ishi H, Beppu T, Nakamori S, Baba H, Mori M. Epithelial-mesenchymal transition in cancer development and its clinical significance. Cancer Sci 2010, 101:293-299. 10.1111/j.1349-7006.2009.01419.x, 19961486.
5. Huber MA, Kraut N, Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 2005, 17:548-558. 10.1016/j.ceb.2005.08.001, 16098727.
6. Guarino M. Epithelial-mesenchymal transition and tumour invasion. Int J Biochem Cell Biol 2007, 39:2153-2160. 10.1016/j.biocel.2007.07.011, 17825600.
7. Peinado H, Portillo F, Cano A. Transcriptional regulation of cadherins during development and carcinogenesis. Int J Dev Biol 2004, 48:365-375. 10.1387/ijdb.041794hp, 15349812.
8. Fesus L, Szondy Z. Transglutaminase 2 in the balance of cell death and survival. FEBS Lett 2005, 579:3297-3302. 10.1016/j.febslet.2005.03.063, 15943974.
9. Fesus L, Piacentini M. Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci 2002, 27:534-539. 10.1016/S0968-0004(02)02182-5, 12368090.
10. Lorand L, Graham RM. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 2003, 4:140-156. 10.1038/nrm1014, 12563291.
11. Collighan RJ, Griffin M. Transglutaminase 2 cross-linking of matrix proteins: biological significance and medical applications. Amino Acids 2009, 36:659-670. 10.1007/s00726-008-0190-y, 18982407.
12. Ientile R, Caccamo D, Griffin M. Tissue transglutaminase and the stress response. Amino Acids 2007, 33:385-394. 10.1007/s00726-007-0517-0, 17390097.
13. Verma A, Mehta K. Transglutaminase-mediated activation of nuclear transcription factor-kappaB in cancer cells: a new therapeutic opportunity. Curr Cancer Drug Targets 2007, 7:559-565. 10.2174/156800907781662275, 17896921.
14. Mehta K. High levels of transglutaminase expression in doxorubicin-resistant human breast carcinoma cells. Int J Cancer 1994, 58:400-406. 10.1002/ijc.2910580316, 7914183.
15. Verma A, Mehta K. Tissue transglutaminase-mediated chemoresistance in cancer cells. Drug Resist Updat 2007, 10:144-151. 10.1016/j.drup.2007.06.002, 17662645.
16. Verma A, Wang H, Manavathi B, Fok JY, Mann AP, Kumar R, Mehta K. Increased expression of tissue transglutaminase in pancreatic ductal adenocarcinoma and its implications in drug resistance and metastasis. Cancer Res 2006, 66:10525-10533. 10.1158/0008-5472.CAN-06-2387, 17079475.
17. 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, 29:1893-1900. 10.1093/carcin/bgn158, 2556973, 18667446.
18. Hwang JY, Mangala LS, Fok JY, Lin YG, Merritt WM, Spannuth WA, Nick AM, Fiterman DJ, Vivas-Mejia PE, Deavers MT, et al. Clinical and biological significance of tissue transglutaminase in ovarian carcinoma. Cancer Res 2008, 68:5849-5858. 10.1158/0008-5472.CAN-07-6130, 2547344, 18632639.
19. Herman JF, Mangala LS, Mehta K. Implications of increased tissue transglutaminase (TG2) expression in drug-resistant breast cancer (MCF-7) cells. Oncogene 2006, 25:3049-3058. 10.1038/sj.onc.1209324, 16449978.
20. Kim DS, Park SS, Nam BH, Kim IH, Kim SY. Reversal of drug resistance in breast cancer cells by transglutaminase 2 inhibition and nuclear factor-kappaB inactivation. Cancer Res 2006, 66:10936-10943. 10.1158/0008-5472.CAN-06-1521, 17108131.
21. Verma A, Guha S, Diagaradjane P, Kunnumakkara AB, Sanguino AM, Lopez-Berestein G, Sood AK, Aggarwal BB, Krishnan S, Gelovani JG, Mehta K. Therapeutic significance of elevated tissue transglutaminase expression in pancreatic cancer. Clin Cancer Res 2008, 14:2476-2483. 10.1158/1078-0432.CCR-07-4529, 18413840.
22. Han JA, Park SC. Reduction of transglutaminase 2 expression is associated with an induction of drug sensitivity in the PC-14 human lung cancer cell line. J Cancer Res Clin Oncol 1999, 125:89-95. 10.1007/s004320050247, 10190315.
23. Shao M, Cao L, Shen C, Satpathy M, Chelladurai B, Bigsby RM, Nakshatri H, Matei D. Epithelial-to-mesenchymal transition and ovarian tumor progression induced by tissue transglutaminase. Cancer Res 2009, 69:9192-9201. 10.1158/0008-5472.CAN-09-1257, 19951993.
24. Kumar A, Xu J, Brady S, Gao H, Yu D, Reuben J, Mehta K. Tissue transglutaminase promotes drug resistance and invasion by inducing mesenchymal transition in mammary epithelial cells. PLoS One 2010, 5:e13390. 10.1371/journal.pone.0013390, 2953521, 20967228.
25. Kao WT, Lin CY, Lee LT, Lee PP, Hung CC, Lin YS, Chen SH, Ke FC, Hwang JJ, Lee MT. Investigation of MMP-2 and -9 in a highly invasive A431 tumor cell sub-line selected from a Boyden chamber assay. Anticancer Res 2008, 28:2109-2120.
26. Chen SH, Lin CY, Lee LT, Chang GD, Lee PP, Hung CC, Kao WT, Tsai PH, Schally AV, Hwang JJ, Lee MT. Up-regulation of fibronectin and tissue transglutaminase promotes cell invasion involving increased association with integrin and MMP expression in A431 cells. Anticancer Res 2010, 30:4177-4186.
27. Lin CY, Tsai PH, Kandaswami CC, Lee PP, Huang CJ, Hwang JJ, Lee MT. Matrix metalloproteinase-9 cooperates with transcription factor Snail to induce epithelial-mesenchymal transition. cancer science 2011, 102:815-827. 10.1111/j.1349-7006.2011.01861.x, 21219539.
28. Giard DJ, Aaronson SA, Todaro GJ, Arnstein P, Kersey JH, Dosik H, Parks WP. In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. Journal of the National Cancer Institute 1973, 51:1417-1423.
29. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.
30. Schreiber E, Matthias P, Muller MM, Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res 1989, 17:6419. 10.1093/nar/17.15.6419, 318318, 2771659.
31. Grille SJ, Bellacosa A, Upson J, Klein-Szanto AJ, van Roy F, Lee-Kwon W, Donowitz M, Tsichlis PN, Larue L. The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res 2003, 63:2172-2178.
32. Papkoff J, Aikawa M. WNT-1 and HGF regulate GSK3 beta activity and beta-catenin signaling in mammary epithelial cells. Biochem Biophys Res Commun 1998, 247:851-858. 10.1006/bbrc.1998.8888, 9647782.
33. Bachelder RE, Yoon SO, Franci C, de Herreros AG, Mercurio AM. Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription: implications for the epithelial-mesenchymal transition. J Cell Biol 2005, 168:29-33. 2171685, 15631989.
34. Diehl JA, Cheng M, Roussel MF, Sherr CJ. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 1998, 12:3499-3511. 10.1101/gad.12.22.3499, 317244, 9832503.
35. Huber MA, Azoitei N, Baumann B, Grunert S, Sommer A, Pehamberger H, Kraut N, Beug H, Wirth T. NF-kappaB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression. J Clin Invest 2004, 114:569-581. 503772, 15314694.
36. Akimov SS, Belkin AM. Cell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin. Blood 2001, 98:1567-1576. 10.1182/blood.V98.5.1567, 11520809.
37. Chhabra A, Verma A, Mehta K. Tissue transglutaminase promotes or suppresses tumors depending on cell context. Anticancer Res 2009, 29:1909-1919.
38. Akimov SS, Krylov D, Fleischman LF, Belkin AM. Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J Cell Biol 2000, 148:825-838. 10.1083/jcb.148.4.825, 2169362, 10684262.
39. Verma A, Guha S, Wang H, Fok JY, Koul D, Abbruzzese J, Mehta K. Tissue transglutaminase regulates focal adhesion kinase/AKT activation by modulating PTEN expression in pancreatic cancer cells. Clin Cancer Res 2008, 14:1997-2005. 10.1158/1078-0432.CCR-07-1533, 18381937.
40. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890. 10.1016/j.cell.2009.11.007, 19945376.
41. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009, 119:1420-1428. 10.1172/JCI39104, 2689101, 19487818.
42. Orlowski RZ, Baldwin AS. NF-kappaB as a therapeutic target in cancer. Trends Mol Med 2002, 8:385-389. 10.1016/S1471-4914(02)02375-4, 12127724.
43. Mann AP, Verma A, Sethi G, Manavathi B, Wang H, Fok JY, Kunnumakkara AB, Kumar R, Aggarwal BB, Mehta K. Overexpression of tissue transglutaminase leads to constitutive activation of nuclear factor-kappaB in cancer cells: delineation of a novel pathway. Cancer Res 2006, 66:8788-8795. 10.1158/0008-5472.CAN-06-1457, 16951195.
44. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nat Rev Cancer 2007, 7:415-428. 10.1038/nrc2131, 17508028.
45. Hugo H, Ackland ML, Blick T, Lawrence MG, Clements JA, Williams ED, Thompson EW. Epithelial--mesenchymal and mesenchymal--epithelial transitions in carcinoma progression. J Cell Physiol 2007, 213:374-383. 10.1002/jcp.21223, 17680632.