Hypoxia/reoxygenation-experienced cancer cell migration and metastasis are regulated by Rap1-and Rac1-GTPase activation via the expression of thymosin beta-4

Oncotarget

Volumn 6, Issue 12, 2015, Pages 9820-9833

  Lee, Jae Wook ^a   Ryu, Yun Kyoung ^a   Ji, Young Hoon ^b   Kang, Joo Hyun ^b   Moon, Eun Yi ^a  

^a Sejong University   (South Korea)

^b Korea Institute of Radiation and Medical Science   (South Korea)

Author keywords

Cancer cell migration; Rac1 GTPase; Rap1 GTPase; Thymosin beta 4; Tumor metastasis

Indexed keywords

4 AMINO 6 [2 [[4 (DIETHYLAMINO) 1 METHYLBUTYL]AMINO] 6 METHYL 4 PYRIMIDINYL] 2 METHYLQUINOLINE; 8 (4 CHLOROPHENYLTHIO)ADENOSINE 3' ,5' CYCLIC MONOPHOSPHATE; HYDROLASE INHIBITOR; RAC1 PROTEIN; RAP1 PROTEIN; THYMOSIN BETA4; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; UNCLASSIFIED DRUG; AMINOQUINOLINE DERIVATIVE; GUANOSINE TRIPHOSPHATASE; NEUROPEPTIDE; OXYGEN; PYRIMIDINE DERIVATIVE; RAC1 PROTEIN, HUMAN; RAC1 PROTEIN, MOUSE; TELOMERE BINDING PROTEIN; TERF2IP PROTEIN, HUMAN; THYMOSIN; THYMOSIN BETA(4);

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CELL MIGRATION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; GENE EXPRESSION; HELA CELL LINE; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MALE; METASTASIS INHIBITION; MOLECULAR INTERACTION; MOUSE; NONHUMAN; REOXYGENATION; TRANSGENIC MOUSE; ANIMAL; C57BL MOUSE; CELL HYPOXIA; CELL MOTION; CHEMISTRY; EXPERIMENTAL MELANOMA; GENE EXPRESSION REGULATION; METABOLISM; METASTASIS; SIGNAL TRANSDUCTION; TUMOR CELL LINE; TUMOR MICROENVIRONMENT; TWO HYBRID SYSTEM;

AMINOQUINOLINES; ANIMALS; CELL HYPOXIA; CELL LINE, TUMOR; CELL MOVEMENT; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GTP PHOSPHOHYDROLASES; HELA CELLS; HUMANS; MALE; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; NEOPLASM METASTASIS; NEUROPEPTIDES; OXYGEN; PYRIMIDINES; RAC1 GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; TELOMERE-BINDING PROTEINS; THYMOSIN; TUMOR MICROENVIRONMENT; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84929591055     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3218     Document Type: Article

References (49)

1. Brown JM. The hypoxic cell: a target for selective cancer therapy-eighteenth Bruce F. Cain memorial award lecture. Cancer Res. 1999; 59:5863-5870.
2. Cho WK, Seong YR, Lee YH, Kim MJ, Hwang KS, Yoo J, Choi S, Jung CR, Im DS. Oncolytic effects of adenovirus mutant capable of replicating in hypoxic and normoxic regions of solid tumor. Mol Ther. 2004; 10:938-949.
3. Folkman J. What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst. 1990;82:4-6.
4. Oh JM, Moon EY. Actin-sequestering protein, thymosin beta-4, induces paclitaxel resistance through ROS/HIF-1alpha stabilization in HeLa human cervical tumor cells. Life Sci. 2010; 87:286-293.
5. Hockel M, Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst. 2001; 93:266-276.
6. Harris AL. Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer. 2002; 2:38-47.
7. Dewhirst MW, Cao Y, Moeller B. Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response. Nat Rev Cancer. 2008; 8:425-437.
8. Mahabeleshwar GH, Kundu GC. Tyrosine kinase p56lck regulates cell motility and nuclear factor kappaB-mediated secretion of urokinase type plasminogen activator through tyrosine phosphorylation of IkappaBalpha following hypoxia/reoxygenation. J Biol Chem. 2003; 278:52598-52612.
9. Binker MG, Binker-Cosen AA, Richards D, Gaisano HY, de Cosen RH, Cosen-Binker LI. Hypoxia-reoxygenation increase invasiveness of PANC-1 cells through Rac1/MMP-2. Biochem Biophys Res Commun. 2010; 393:371-376.
10. Bacac M, Stamenkovic I. Metastatic cancer cell. Annual review of pathology. 2008; 3:221-247.
11. Chen H, Bernstein BW, Bamburg JR. Regulating actinfilament dynamics in vivo. Trends Biochem Sci. 2000; 25:19-23.
12. Yamazaki D, Kurisu S, Takenawa T. Regulation of cancer cell motility through actin reorganization. Cancer Sci. 2005; 96:379-386.
13. Bailey CL, Kelly P, Casey PJ. Activation of Rap1 promotes prostate cancer metastasis. Cancer Res. 2009; 69:4962-4968.
14. Burnham CA, Shokoples SE, Tyrrell GJ. Rac1, RhoA, and Cdc42 participate in HeLa cell invasion by group B streptococcus. FEMS Microbiol Lett. 2007; 272:8-14.
15. Takai Y, Sasaki T, Matozaki T. Small GTP-binding proteins. Physiol Rev. 2001; 81:153-208.
16. Kometani K, Ishida D, Hattori M, Minato N. Rap1 and SPA-1 in hematologic malignancy. Trends Mol Med. 2004; 10:401-408.
17. Kitayama H, Sugimoto Y, Matsuzaki T, Ikawa Y, Noda M. A ras-related gene with transformation suppressor activity. Cell. 1989; 56:77-84.
18. Singer SJ, Kupfer A. The directed migration of eukaryotic cells. Ann Rev Cell Biol. 1986; 2:337-365.
19. Fukumoto Y, Kaibuchi K, Hori Y, Fujioka H, Araki S, Ueda T, Kikuchi A, Takai Y. Molecular cloning and characterization of a novel type of regulatory protein (GDI) for the rho proteins, ras p21-like small GTP-binding proteins. Oncogene. 1990; 5:1321-1328.
20. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci U S A. 2004; 101:7618-7623.
21. Takahashi M, Rikitake Y, Nagamatsu Y, Hara T, Ikeda W, Hirata K, Takai Y. Sequential activation of Rap1 and Rac1 small G proteins by PDGF locally at leading edges of NIH3T3 cells. Genes Cells. 2008; 13:549-569.
22. Jenei V, Andersson T, Jakus J, Dib K. E3B1, a human homologue of the mouse gene product Abi-1, sensitizes activation of Rap1 in response to epidermal growth factor. Exp Cell Res. 2005; 310:463-473.
23. Arthur WT, Quilliam LA, Cooper JA. Rap1 promotes cell spreading by localizing Rac guanine nucleotide exchange factors. J Cell Biol. 2004; 167:111-122.
24. Maillet M, Robert SJ, Cacquevel M, Gastineau M, Vivien D, Bertoglio J, Zugaza JL, Fischmeister R, Lezoualc'h F. Crosstalk between Rap1 and Rac regulates secretion of sAPPalpha. Nat Cell Biol. 2003; 5:633-639.
25. Valles AM, Beuvin M, Boyer B. Activation of Rac1 by paxillin-Crk-DOCK180 signaling complex is antagonized by Rap1 in migrating NBT-II cells. J Biol Chem. 2004; 279:44490-44496.
26. Hertzog M, van Heijenoort C, Didry D, Gaudier M, Coutant J, Gigant B, Didelot G, Preat T, Knossow M, Guittet E, Carlier MF. The beta-thymosin/WH2 domain; structural basis for the switch from inhibition to promotion of actin assembly. Cell. 2004; 117:611-623.
27. Safer D, Elzinga M, Nachmias VT. Thymosin beta 4 and Fx, an actin-sequestering peptide, are indistinguishable. J Biol Chem. 1991; 266:4029-4032.
28. Sun HQ, Kwiatkowska K, Yin HL. Actin monomer binding proteins. Curr Opin Cell Biol. 1995; 7:102-110.
29. Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, Condeelis JS. Cofilin promotes actin polymerization and defines the direction of cell motility. Science. 2004; 304:743-746.
30. Huff T, Muller CS, Otto AM, Netzker R, Hannappel E. beta-Thymosins, small acidic peptides with multiple functions. Int J Biochem Cell Biol. 2001; 33:205-220.
31. Low TL, Goldstein AL. Chemical characterization of thymosin beta 4. J Biol Chem. 1982; 257:1000-1006.
32. Low TL, Hu SK, Goldstein AL. Complete amino acid sequence of bovine thymosin beta 4: a thymic hormone that induces terminal deoxynucleotidyl transferase activity in thymocyte populations. Proc Natl Acad Sci U S A. 1981; 78:1162-1166.
33. Brakebusch C, Fassler R. Beta 1 integrin function in vivo:adhesion, migration and more. Cancer Meta Rev. 2005; 24:403-411.
34. Zvaifler NJ. Relevance of the stroma and epithelial-mesenchymal transition (EMT) for the rheumatic diseases. Arthritis Res Ther. 2006; 8:210.
35. Goldstein AL. Thymosin beta4: a new molecular target for antitumor strategies. J Natl Cancer Inst. 2003; 95:1646-1647.
36. Oh JM, Ryoo IJ, Yang Y, Kim HS, Yang KH, Moon EY. Hypoxia-inducible transcription factor (HIF)-1 alpha stabilization by actin-sequestering protein, thymosin beta-4 (TB4) in Hela cervical tumor cells. Cancer Lett. 2008; 264:29-35.
37. Moon EY, Im YS, Ryu YK, Kang JH. Actin-sequestering protein, thymosin beta-4, is a novel hypoxia responsive regulator. Clin Exp Metastasis. 2010; 27:601-609.
38. Huang HC, Hu CH, Tang MC, Wang WS, Chen PM, Su Y. Thymosin beta4 triggers an epithelial-mesenchymal transition in colorectal carcinoma by upregulating integrin-linked kinase. Oncogene. 2007; 26:2781-2790.
39. Wang WS, Chen PM, Hsiao HL, Ju SY, Su Y. Overexpression of the thymosin beta-4 gene is associated with malignant progression of SW480 colon cancer cells. Oncogene. 2003; 22:3297-3306.
40. Wang WS, Chen PM, Hsiao HL, Wang HS, Liang WY, 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.
41. Ryu YK, Lee YS, Lee GH, Song KS, Kim YS, Moon EY. Regulation of glycogen synthase kinase-3 by thymosin beta-4 is associated with gastric cancer cell migration. Int J Cancer. 2012; 131:2067-2077.
42. Bos JL, de Rooij J, Reedquist KA. Rap1 signalling:adhering to new models. Nat Rev Mol Cell Biol. 2001; 2:369-377.
43. Carmona G, Gottig S, Orlandi A, Scheele J, Bauerle T, Jugold M, Kiessling F, Henschler R, Zeiher AM, Dimmeler S, Chavakis E. Role of the small GTPase Rap1 for integrin activity regulation in endothelial cells and angiogenesis. Blood. 2009; 113:488-497.
44. Tang MC, Chan LC, Yeh YC, Chen CY, Chou TY, Wang WS, Su Y. Thymosin beta 4 induces colon cancer cell migration and clinical metastasis via enhancing ILK/IQGAP1/Rac1 signal transduction pathway. Cancer Lett. 2011; 308:162-171.
45. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer. 2003; 3:11-22.
46. Franke B, Akkerman JW, Bos JL. Rapid Ca2+-mediated activation of Rap1 in human platelets. EMBO J. 1997; 16:252-259.
47. Spaargaren M, Bischoff JR. Identification of the guanine nucleotide dissociation stimulator for Ral as a putative effector molecule of R-ras, H-ras, K-ras, and Rap. Proc Natl Acad Sci U S A. 1994; 91:12609-12613.
48. Gietz D, St Jean A, Woods RA, Schiestl RH. Improved method for high efficiency transformation of intact yeast cells. Nucl Acids Res. 1992; 20:1425.
49. Oh SY, Song JH, Gil JE, Kim JH, Yeom YI, Moon EY. ERK activation by thymosin-beta-4 (TB4) overexpression induces paclitaxel-resistance. Exp Cell Res. 2006; 312:1651-1657.