Thymosin beta 4 induces colon cancer cell migration and clinical metastasis via enhancing ILK/IQGAP1/Rac1 signal transduction pathway

Cancer Letters

Volumn 308, Issue 2, 2011, Pages 162-171

  Tang, Mei Chuan ^a   Chan, Li Chuan ^a   Yeh, Yi Chen ^a   Chen, Cheng Yu ^a   Chou, Teh Ying ^a   Wang, Wei Shu ^a   Su, Yeu ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

ILK; IQGAP1; Migration; Rac1; Thymosin 4 (T 4)

Indexed keywords

INTEGRIN LINKED KINASE; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1; RAC1 PROTEIN; THYMOSIN BETA4;

ANIMAL CELL; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER TISSUE; CELL MIGRATION; CELL STRAIN SW480; COLON CANCER; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL MOVEMENT; COLONIC NEOPLASMS; HUMANS; MICE; NEOPLASM METASTASIS; PROTEIN-SERINE-THREONINE KINASES; RAC1 GTP-BINDING PROTEIN; RAS GTPASE-ACTIVATING PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; THYMOSIN; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 80051817916     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.05.001     Document Type: Article

References (49)

1. Hannappel E., Leibold W. Biosynthesis rates and content of thymosin beta 4 in cell lines. Arch. Biochem. Biophys. 1985, 240:236-241.
2. Mannherz H., Hannappel E. The beta-thymosins: intracellular and extracellular activities of a versatile actin binding protein family. Cell Motil. Cytoskel. 2009, 66:839-851.
3. Huff T., Muller C.S., Otto A.M., Netzker R., Hannappel E. beta-Thymosins, small acidic peptides with multiple functions. Int. J. Biochem. Cell Biol. 2001, 33:205-220.
4. Sosne G., Qiu P., Kurpakus-Wheater M. Thymosin beta-4 and the Eye. Ann. N.Y. Acad. Sci. 2007, 1112:114-122.
5. Ballweber E., Huff T., Humeny A., Bonk T., Becker C., Müller C.S., Mannherz H.G., Hannappel E. Thymosin beta(4) serves as a glutaminyl substrate of transglutaminase: labeling with fluorescent dansylcadaverine does not abolish interaction with G-actin. FEBS Lett. 1999, 464:14-20.
6. Sosne G., Hafeez S., Greenberry A.L., Kurpakus-Wheater M. Thymosin beta 4 promotes human conjunctival epithelial cell migration. Curr. Eye Res. 2002, 24:268-273.
7. Wang W.S., Chen P.M., Su Y. Colorectal carcinoma: from tumorigenesis to treatment. Cell Mol. Life Sci. 2006, 63:663-671.
8. Wang W.S., Chen P.M., Hsiao H.L., Wang H.S., Liang W.Y., Su Y. Overexpression of the thymosin beta-4 gene is associated with increased invasion of SW480 colon carcinoma cells and the distant metastasis of human colorectal carcinoma. Oncogene 2004, 23:6666-6671.
9. Smart N., Rossdeutsch A., Riley P. Thymosin beta 4 and angiogenesis: modes of action and therapeutic potential. Angiogenesis 2007, 10:229-241.
10. Yamazaki D., Kurisu S., Takenawa T. Regulation of cancer cell motility through actin reorganization. Cancer Sci. 2005, 96:379-386.
11. Takenawa T., Miki H. WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 2001, 114:1801-1809.
12. Jaffe A.B., Hall A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 2005, 21:247-269.
13. Kuhn T.B., Meberg P.J., Brown M.D., Bernstein B.W., Minamide L.S., Jensen J.R., Okada K., Soda E.A., Bamburg J.R. Regulating actin dynamics in neuronal growth cones by ADF/cofilin and rho family GTPases. J. Neurobiol. 2000, 44:126-144.
14. Yoganathan N., Yee A., Zhang Z., Leung D., Yan J., Fazli L., Kojic D.L., Costello P.C., Jabali M., Dedhar S. Integrin-linked kinase, a promising cancer therapeutic target: biochemical and biological properties,. Pharmacol. Ther. 2002, 93:233-242.
15. Hannigan G., Troussard A.A., Dedhar S. Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat. Rev. Cancer 2005, 5:51-63.
16. McDonald P.C., Fielding A.B., Dedhar S. Integrin-linked kinase - essential roles in physiology and cancer biology. J. Cell Sci. 2008, 121:3121-3132.
17. Persad S., Dedhar S. The role of integrin-linked kinase (ILK) in cancer progression. Cancer Metast. Rev. 2003, 22:375-384.
18. Nakrieko K.A., Welch I., Dupuis H., Bryce D., Pajak A., St Arnaud R., Dedhar S., D'Souza S.J., Dagnino L. Impaired hair follicle morphogenesis and polarized keratinocyte movement upon conditional inactivation of integrin-linked kinase in the epidermis. Mol. Biol. Cell 2008, 19:1462-1473.
19. Huang H.C., Hu C.H., Tang M.C., Wang W.S., Chen P.M., Su Y. Thymosin beta4 triggers an epithelial-mesenchymal transition in colorectal carcinoma by upregulating integrin-linked kinase. Oncogene 2007, 26:2781-2790.
20. Mataraza J.M., Briggs M.W., Li Z., Entwistle A., Ridley A.J., Sacks D.B. IQGAP1 promotes cell motility and invasion. J. Biol. Chem. 2003, 278:41237-41245.
21. Smart N., Scambler P.J., Riley P.R. A rapid and sensitive assay for quantification of siRNA efficiency and specificity. Biol. Proced. Online 2005, 7:1-7.
22. Lien C.Y., Lee O.K., Su Y. Cbfb enhances the osteogenic differentiation of both human and mouse mesenchymal stem cells induced by Cbfa-1 via reducing its ubiquitination-mediated degradation. Stem Cells 2007, 25:1462-1468.
23. Guo L., Yu W., Li X., Zhao G., Liang J., He P., Wang K., Zhou P., Jiang Y., Zhao M. Targeting of integrin-linked kinase with a small interfering RNA suppresses progression of experimental proliferative vitreoretinopathy. Exp. Eye Res. 2008, 87:551-560.
24. Wang W.S., Chen P.M., Hsiao H.L., Ju S.Y., Su Y. Overexpression of the thymosin beta-4 gene is associated with malignant progression of SW480 colon cancer cells. Oncogene 2003, 22:3297-3306.
25. Wong K., Mohammadi S., Isberg R. Disruption of RhoGDI and RhoA regulation by a Rac1 specificity switch mutant. J. Biol. Chem. 2006, 281:40379-40388.
26. Salhia B., Tran N.L., Chan A., Wolf A., Nakada M., Rutka F., Ennis M., McDonough W.S., Berens M.E., Symons M., Rutka J.T. The guanine nucleotide exchange factors trio, Ect2, and Vav3 mediate the invasive behavior of glioblastoma. Am. J. Pathol. 2008, 173:1828-1838.
27. Minard M.E., Herynk M.H., Collard J.G., Gallick G.E. The guanine nucleotide exchange factor Tiam1 increases colon carcinoma growth at metastatic sites in an orthotopic nude mouse model. Oncogene 2005, 24:2568-2573.
28. Gao Y., Dickerson J.B., Guo F., Zheng J., Zheng Y. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc. Natl. Acad. Sci. USA 2004, 101:7618-7623.
29. Fan Y., Gong Y., Ghosh P.K., Graham L.M., Fox P.L. Spatial coordination of actin polymerization and ILK-Akt2 activity during endothelial cell migration. Dev. Cell. 2009, 16:661-674.
30. Brown M.D., Sacks D.B. IQGAP1 in cellular signaling: bridging the GAP. Trends Cell. Biol. 2006, 16:242-249.
31. Dobreva I., Fielding A., Foster L.J., Dedhar S. Mapping the integrin-linked kinase interactome using SILAC. J. Proteome Res. 2008, 7:1740-1749.
32. Nabeshima K., Shimao Y., Inoue T., Koono M. Immunohistochemical analysis of IQGAP1 expression in human colorectal carcinomas: its overexpression in carcinomas and association with invasion fronts. Cancer Lett. 2002, 176:101-109.
33. Hayashi H., Nabeshima K., Aoki M., Hamasaki M., Enatsu S., Yamauchi Y., Yamashita Y., Iwasaki H. Overexpression of IQGAP1 in advanced colorectal cancer correlates with poor prognosis: critical role in tumor invasion. Int. J. Cancer 2010, 126:2563-2574.
34. Bouquier N., Vignal E., Charrasse S., Weill M., Schmidt S., Leonetti J.P., Blangy A., Fort P. A cell active chemical GEF inhibitor selectively targets the Trio/RhoG/Rac1 signaling pathway. Chem. Biol. 2009, 16:657-666.
35. Bock-Marquette I., Saxena A., White M.D., Dimaio J.M., Srivastava D. Thymosin beta4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature 2004, 432:466-472.
36. Dong P., Nabeshima K., Nishimura N., Kawakami T., Hachisuga T., Kawarabayashi T., Iwasaki H. Overexpression and diffuse expression pattern of IQGAP1 at invasion fronts are independent prognostic parameters in ovarian carcinomas. Cancer Lett. 2006, 243:120-127.
37. White C.D., Brown M.D., Sacks D.B. IQGAPs in cancer: a family of scaffold proteins underlying tumorigenesis. FEBS Lett. 2009, 583:1817-1824.
38. Mateer S.C., Wang N., Bloom G.S. IQGAPs: integrators of the cytoskeleton, cell adhesion machinery, and signaling networks. Cell Motil. Cytoskel. 2003, 55:147-155.
39. Swart-Mataraza J.M., Li Z., Sacks D.B. IQGAP1 is a component of Cdc42 signaling to the cytoskeleton. J. Biol. Chem. 2002, 277:24753-24763.
40. Brill S., Li S., Lyman C.W., Church D.M., Wasmuth J.J., Weissbach L., Bernards A., Snijders A.J. The Ras GTPase-activating-protein-related human protein IQGAP2 harbors a potential actin binding domain and interacts with calmodulin and Rho family GTPases. Mol. Cell. Biol. 1996, 16:4869-4878.
41. Hart M.J., Callow M.G., Souza B., Polakis P. IQGAP1, a calmodulin-binding protein with a rasGAP-related domain, is a potential effector for cdc42Hs. EMBO J. 1996, 15:2997-3005.
42. Boulter E., Grall D., Cagnol S., Van Obberghen-Schilling E. Regulation of cell-matrix adhesion dynamics and Rac-1 by integrin linked kinase. FASEB J. 2006, 20:1489-1491.
43. Qian Y., Zhong X., Flynn D.C., Zheng J.Z., Qiao M., Wu C., Dedhar S., Shi X., Jiang B.H. ILK mediates actin filament rearrangements and cell migration and invasion through PI3K/Akt/Rac1 signaling. Oncogene 2005, 24:3154-3165.
44. Fukuda T., Chen K., Shi X., Wu C. PINCH-1 is an obligate partner of integrin-linked kinase(ILK) functioning in cell shape modulation, motility, and survival. J. Biol. Chem. 2003, 278:51324-51333.
45. Brieger A., Plotz G., Zeuzem S., Trojan J. Thymosin beta 4 expression and nuclear transport are regulated by hMLH1. Biochem. Biophys. Res. Commun. 2007, 364:731-736.
46. Bednarek R., Boncela J., Smolarczyk K., Cierniewska-Cieslak A., Wyroba E., Cierniewski C.S. Ku80 as a novel receptor for Thymosin beta 4 that mediates its intracellular activity different from g-actin sequestering. J. Biol. Chem. 2008, 283:1534-1544.
47. Steeg P.S. Tumor metastasis: mechanistic insights and clinical challenges. Nat. Med. 2006, 12:895-904.
48. Hage B., Meinel K., Baum I., Giehl K., Menke A. Rac 1 activation inhibits E-cadherin-mediated adherens junctions via binding to IQGAP 1 in pancreatic carcinoma cells. Cell Commun. Signal 2009, 7:23.
49. Ji P., Diederichs S., Wang W., Boing S., Metzger R., Schneider P.M., Tidow N., Brandt B., Buerger H., Bulk E., Thomas M., Berdel W.E., Serve H., Muller-Tidow C. MALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene 2003, 22:8031-8041.