STAT3 protein up-regulates Gα-interacting vesicle-associated protein (GIV)/girdin expression, and GIV enhances STAT3 activation in a positive feedback loop during wound healing and tumor invasion/metastasis

Journal of Biological Chemistry

Volumn 287, Issue 50, 2012, Pages 41667-41683

  Dunkel, Ying ^a   Ong, Andrew ^a   Notani, Dimple ^a   Mittal, Yash ^a   Lam, Michael ^a   Mi, Xiaoyi ^b   Ghosh, Pradipta ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CHINA MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL PROCESS; BREAST CARCINOMAS; CANCER INVASION; CANCER PATIENTS; FEEDBACK REGULATION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; IMMUNOHISTOCHEMICAL ANALYSIS; POSITIVE FEEDBACK LOOP; PROTEIN SIGNALING; SIGNAL TRANSDUCERS; SIGNALING PATHWAYS; THERAPEUTIC TARGETS; TRANSCRIPTIONAL ACTIVATIONS; TUMOR ANGIOGENESIS; TUMOR INVASION; TUMOR METASTASIS; WOUND HEALING;

AMINO ACIDS; BIOCHEMISTRY; CHEMICAL ACTIVATION; DISEASES; NUCLEOTIDES; PATHOLOGY; POSITIVE IONS; REPAIR; TRANSCRIPTION; TRANSCRIPTION FACTORS; TUMORS;

ACTIVATION ANALYSIS;

G ALPHA INTERACTING VESICLE ASSOCIATED PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN TYROSINE KINASE; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOREGULATION; BINDING SITE; BREAST CARCINOMA; CANCER INVASION; CLINICAL ARTICLE; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; METASTASIS; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION; WOUND HEALING;

BREAST NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HELA CELLS; HUMANS; MICROFILAMENT PROTEINS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM PROTEINS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; UP-REGULATION; VESICULAR TRANSPORT PROTEINS; WOUND HEALING;

GREAT ISLAND VIRUS;

EID: 84871275879     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.390781     Document Type: Article

References (65)

1. Ghosh, P., Garcia-Marcos, M., and Farquhar, M. G. (2011) GIV/Girdin is a rheostat that fine-tunes growth factor signals during tumor progression. Cell Adh. Migr. 5, 237-248
2. Ghosh, P., Beas, A. O., Bornheimer, S. J., Garcia-Marcos, M., Forry, E. P., Johannson, C., Ear, J., Jung, B. H., Cabrera, B., Carethers, J. M., and Farquhar, M. G. (2010) A Gαi-GIV molecular complex binds epidermal growth factor receptor and determines whether cells migrate or proliferate. Mol. Biol. Cell 21, 2338-2354
3. Ghosh, P., Garcia-Marcos, M., Bornheimer, S. J., and Farquhar, M. G. (2008) Activation of Gαi3 triggers cell migration via regulation of GIV. J. Cell Biol. 182, 381-393
4. Yamaguchi, M., Suyari, O., Nagai, R., and Takahashi, M. (2010) dGirdin a new player of Akt /PKB signaling in Drosophila melanogaster. Front. Biosci. 15, 1164-1171
5. Puseenam, A., Yoshioka, Y., Nagai, R., Hashimoto, R., Suyari, O., Itoh, M., Enomoto, A., Takahashi, M., and Yamaguchi, M. (2009) A novel Drosophila Girdin-like protein is involved in Akt pathway control of cell size. Exp. Cell Res. 315, 3370-3380
6. Bradshaw, N. J., and Porteous, D. J. (2012) DISC1-binding proteins in neural development, signalling and schizophrenia. Neuropharmacology 62, 1230-1241
7. Enomoto, A., Asai, N., Namba, T., Wang, Y., Kato, T., Tanaka, M., Tatsumi, H., Taya, S., Tsuboi, D., Kuroda, K., Kaneko, N., Sawamoto, K., Miyamoto, R., Jijiwa, M., Murakumo, Y., Sokabe, M., Seki, T., Kaibuchi, K., and Takahashi, M. (2009) Roles of disrupted-in-schizophrenia 1-interacting protein girdin in postnatal development of the dentate gyrus. Neuron 63, 774-787
8. Miyake, H., Maeda, K., Asai, N., Shibata, R., Ichimiya, H., Isotani-Sakakibara, M., Yamamura, Y., Kato, K., Enomoto, A., Takahashi, M., and Murohara, T. (2011) The actin-binding protein Girdin and its Akt-mediated phosphorylation regulate neointima formation after vascular injury. Circ. Res. 108, 1170-1179
9. Garcia-Marcos, M., Ear, J., Farquhar, M. G., and Ghosh, P. (2011) A GDI (AGS3) and a GEF (GIV) regulate autophagy by balancing G protein activity and growth factor signals. Mol. Biol. Cell 22, 673-686
10. Kitamura, T., Asai, N., Enomoto, A., Maeda, K., Kato, T., Ishida, M., Jiang, P., Watanabe, T., Usukura, J., Kondo, T., Costantini, F., Murohara, T., and Takahashi, M. (2008) Regulation of VEGF-mediated angiogenesis by the Akt/PKB substrate Girdin. Nat. Cell Biol. 10, 329-337 (Pubitemid 351331020)
11. Enomoto, A., Murakami, H., Asai, N., Morone, N., Watanabe, T., Kawai, K., Murakumo, Y., Usukura, J., Kaibuchi, K., and Takahashi, M. (2005) Akt/PKB regulates actin organization and cell motility via Girdin/APE. Dev. Cell 9, 389-402 (Pubitemid 41235808)
12. Garcia-Marcos, M., Jung, B. H., Ear, J., Cabrera, B., Carethers, J. M., and Ghosh, P. (2011) Expression of GIV/Girdin, a metastasis-related protein, predicts patient survival in colon cancer. FASEB J. 25, 590-599
13. Jiang, P., Enomoto, A., Jijiwa, M., Kato, T., Hasegawa, T., Ishida, M., Sato, T., Asai, N., Murakumo, Y., and Takahashi, M. (2008) An actin-binding protein Girdin regulates the motility of breast cancer cells. Cancer Res. 68, 1310-1318 (Pubitemid 351346837)
14. Garcia-Marcos, M., Ghosh, P., and Farquhar, M. G. (2009) GIV is a non-receptor GEF for Gαi with a unique motif that regulates Akt signaling. Proc. Natl. Acad. Sci. U.S.A. 106, 3178-3183
15. Liu, C., Zhang, Y., Xu, H., Zhang, R., Li, H., Lu, P., and Jin, F. (2012) Girdin protein: a new potential distant metastasis predictor of breast cancer. Med. Oncol. 29, 1554-1560
16. Ling, Y., Jiang, P., Cui, S. P., Ren, Y. L., Zhu, S. N., Yang, J. P., Du, J., Zhang, Y., Liu, J. Y., and Zhang, B. (2011) Clinical implications for girdin protein expression in breast cancer. Cancer Invest. 29, 405-410
17. Natsume, A., Kato, T., Kinjo, S., Enomoto, A., Toda, H., Shimato, S., Ohka, F., Motomura, K., Kondo, Y., Miyata, T., Takahashi, M., and Wakabayashi, T. (2012) Girdin maintains the stemness of glioblastoma stem cells. Oncogene 31, 2715-2724
18. Darnell, J. E. (2005) Validating Stat3 in cancer therapy. Nat. Med. 11, 595-596
19. Devarajan, E., and Huang, S. (2009) STAT3 as a central regulator of tumor metastases. Curr. Mol. Med. 9, 626-633
20. Dauer, D. J., Ferraro, B., Song, L., Yu, B., Mora, L., Buettner, R., Enkemann, S., Jove, R., and Haura, E. B. (2005) Stat3 regulates genes common to both wound healing and cancer. Oncogene 24, 3397-3408 (Pubitemid 40756241)
21. Gu, L., Dagvadorj, A., Lutz, J., Leiby, B., Bonuccelli, G., Lisanti, M. P., Addya, S., Fortina, P., Dasgupta, A., Hyslop, T., Bubendorf, L., and Nevalainen, M. T. (2010) Transcription factor Stat3 stimulates metastatic behavior of human prostate cancer cells in vivo, whereas Stat5b has a preferential role in the promotion of prostate cancer cell viability and tumor growth. The Am. J. Pathol. 176, 1959-1972
22. i/sinteracting protein found on COPI, endoplasmic reticulum-Golgi transport vesicles. J. Biol. Chem. 280, 22012-22020
23. Lin, C., Ear, J., Pavlova, Y., Mittal, Y., Kufareva, I., Ghassemian, M., Abagyan, R., Garcia-Marcos, M., and Ghosh, P. (2011) Tyrosine phosphorylation of the Gα-interacting protein GIV promotes activation of phosphoinositide 3-kinase during cell migration. Sci. Signal. 4, ra64
24. Garcia-Marcos, M., Kietrsunthorn, P. S., Pavlova, Y., Adia, M. A., Ghosh, P., and Farquhar, M. G. (2012) Functional characterization of the guanine nucleotide exchange factor (GEF) motif of GIV protein reveals a threshold effect in signaling. Proc. Natl. Acad. Sci. U.S.A. 109, 1961-1966
25. Mittal, Y., Pavlova, Y., Garcia-Marcos, M., and Ghosh, P. (2011) Src homology domain 2-containing protein-tyrosine phosphatase-1 (SHP-1) binds and dephosphorylates Gα-interacting, vesicle-associated protein (GIV)/Girdin and attenuates the GIV-phosphatidylinositol 3-kinase (PI3K)-Akt signaling pathway. J. Biol. Chem. 286, 32404-32415
26. Kumar, A., Choi, K. H., Renthal, W., Tsankova, N. M., Theobald, D. E., Truong, H. T., Russo, S. J., Laplant, Q., Sasaki, T. S., Whistler, K. N., Neve, R. L., Self, D. W., and Nestler, E. J. (2005) Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48, 303-314 (Pubitemid 41476363)
27. Park, O. K., Schaefer, L. K., Wang, W., and Schaefer, T. S. (2000) Dimer stability as a determinant of differential DNA binding activity of Stat3 isoforms. J. Biol. Chem. 275, 32244-32249
28. Niu, G., Wright, K. L., Huang, M., Song, L., Haura, E., Turkson, J., Zhang, S., Wang, T., Sinibaldi, D., Coppola, D., Heller, R., Ellis, L. M., Karras, J., Bromberg, J., Pardoll, D., Jove, R., and Yu, H. (2002) Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis. Oncogene 21, 2000-2008 (Pubitemid 34270888)
29. Dvorak, H. F. (1986) Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. New Engl. J. Med. 315, 1650-1659
30. Nuutila, K., Siltanen, A., Peura, M., Bizik, J., Kaartinen, I., Kuokkanen, H., Nieminen, T., Harjula, A., Aarnio, P., Vuola, J., and Kankuri, E. (2012) Human skin transcriptome during superficial cutaneous wound healing. Wound Repair Regen., doi: 10.1111/j.1524-475X.2012.00831.x
31. Feezor, R. J., Paddock, H. N., Baker, H. V., Varela, J. C., Barreda, J., Moldawer, L. L., Schultz, G. S., and Mozingo, D. W. (2004) Temporal patterns of gene expression in murine cutaneous burn wound healing. Physiol. Genomics 16, 341-348 (Pubitemid 38420054)
32. Band, V., Zajchowski, D., Swisshelm, K., Trask, D., Kulesa, V., Cohen, C., Connolly, J., and Sager, R. (1990) Tumor progression in four mammary epithelial cell lines derived from the same patient. Cancer Res. 50, 7351-7357
33. Bresalier, R. S., Hujanen, E. S., Raper, S. E., Roll, F. J., Itzkowitz, S. H., Martin, G. R., and Kim, Y. S. (1987) An animal model for colon cancer metastasis: establishment and characterization of murine cell lines with enhanced liver-metastasizing ability. Cancer Res. 47, 1398-1406 (Pubitemid 17023214)
34. Liddle, F. J., Alvarez, J. V., Poli, V., and Frank, D. A. (2006) Tyrosine phosphorylation is required for functional activation of disulfide-containing constitutively active STAT mutants. Biochemistry 45, 5599-5605 (Pubitemid 43673190)
35. Yuan, Z. L., Guan, Y. J., Chatterjee, D., and Chin, Y. E. (2005) Stat3 dimerization regulated by reversible acetylation of a single lysine residue. Science 307, 269-273 (Pubitemid 40116244)
36. Diaz, N., Minton, S., Cox, C., Bowman, T., Gritsko, T., Garcia, R., Eweis, I., Wloch, M., Livingston, S., Seijo, E., Cantor, A., Lee, J. H., Beam, C. A., Sullivan, D., Jove, R., and Muro-Cacho, C. A. (2006) Activation of stat3 in primary tumors from high-risk breast cancer patients is associated with elevated levels of activated SRC and survivin expression. Clin. Cancer Res. 12, 20-28 (Pubitemid 43166171)
37. Morikawa, T., Baba, Y., Yamauchi, M., Kuchiba, A., Nosho, K., Shima, K., Tanaka, N., Huttenhower, C., Frank, D. A., Fuchs, C. S., and Ogino, S. (2011) STAT3 expression, molecular features, inflammation patterns, and prognosis in a database of 724 colorectal cancers. Clin. Cancer Res. 17, 1452-1462
38. Kusaba, T., Nakayama, T., Yamazumi, K., Yakata, Y., Yoshizaki, A., Inoue, K., Nagayasu, T., and Sekine, I. (2006) Activation of STAT3 is a marker of poor prognosis in human colorectal cancer. Oncol. Rep. 15, 1445-1451
39. Qiao, M., Iglehart, J. D., and Pardee, A. B. (2007) Metastatic potential of 21T human breast cancer cells depends on Akt/protein kinase B activation. Cancer Res. 67, 5293-5299 (Pubitemid 46997268)
40. Ma, X. T., Wang, S., Ye, Y. J., Du, R. Y., and Cui, Z. R. (2003) Relationship of Stat3 and its target gene products with malignancy in human colorectal carcinoma. Ai Zheng 22, 1135-1139
41. Xie, T. X., Wei, D., Liu, M., Gao, A. C., Ali-Osman, F., Sawaya, R., and Huang, S. (2004) Stat3 activation regulates the expression of matrix metalloproteinase-2 and tumor invasion and metastasis. Oncogene 23, 3550-3560 (Pubitemid 38658421)
42. Senft, C., Priester, M., Polacin, M., Schröder, K., Seifert, V., Kögel, D., and Weissenberger, J. (2011) Inhibition of the JAK-2/STAT3 signaling pathway impedes the migratory and invasive potential of human glioblastoma cells. J. Neurooncol. 101, 393-403
43. Yang, J., Chatterjee-Kishore, M., Staugaitis, S. M., Nguyen, H., Schlessinger, K., Levy, D. E., and Stark, G. R. (2005) Novel roles of unphosphorylated STAT3 in oncogenesis and transcriptional regulation. Cancer Res. 65, 939-947 (Pubitemid 40216455)
44. Yang, J., and Stark, G. R. (2008) Roles of unphosphorylated STATs in signaling. Cell Res. 18, 443-451 (Pubitemid 351498851)
45. Grivennikov, S. I., and Karin, M. (2010) Dangerous liaisons: STAT3 and NF-κB collaboration and crosstalk in cancer. Cytokine Growth Factor Rev. 21, 11-19
46. Kuraishy, A., Karin, M., and Grivennikov, S. I. (2011) Tumor promotion via injury- and death-induced inflammation. Immunity 35, 467-477
47. Lin, L., Deangelis, S., Foust, E., Fuchs, J., Li, C., Li, P. K., Schwartz, E. B., Lesinski, G. B., Benson, D., Lü, J., Hoyt, D., and Lin, J. (2010) A novel small molecule inhibits STAT3 phosphorylation and DNA binding activity and exhibits potent growth suppressive activity in human cancer cells. Mol. Cancer 9, 217
48. Turkson, J., and Jove, R. (2000) STAT proteins: novel molecular targets for cancer drug discovery. Oncogene 19, 6613-6626 (Pubitemid 32197700)
49. Masciocchi, D., Gelain, A., Villa, S., Meneghetti, F., and Barlocco, D. (2011) Signal transducer and activator of transcription 3 (STAT3): a promising target for anticancer therapy. Future Med. Chem. 3, 567-597
50. Mankan, A. K., and Greten, F. R. (2011) Inhibiting signal transducer and activator of transcription 3: rationality and rationale design of inhibitors. Expert Opin. Investig. Drugs 20, 1263-1275
51. Page, B. D., Ball, D. P., and Gunning, P. T. (2011) Signal transducer and activator of transcription 3 inhibitors: a patent review. Expert Opin. Ther. Pat. 21, 65-83
52. Darnell, J. E., Jr. (1997) STATs and gene regulation. Science 277, 1630-1635
53. Cantwell, C. A., Sterneck, E., and Johnson, P. F. (1998) Interleukin-6-specific activation of the C/EBPδ gene in hepatocytes is mediated by Stat3 and Sp1. Mol. Cell. Biol. 18, 2108-2117 (Pubitemid 28152660)
54. Bousquet, C., Zatelli, M. C., and Melmed, S. (2000) Direct regulation of pituitary proopiomelanocortin by STAT3 provides a novel mechanism for immuno-neuroendocrine interfacing. J. Clin. Investig. 106, 1417-1425
55. Noonberg, S. B., Scott, G. K., Hunt, C. A., Hogan, M. E., and Benz, C. C. (1994) Inhibition of transcription factor binding to the HER2 promoter by triplex-forming oligodeoxyribonucleotides. Gene 149, 123-126
56. Kwon, H., Thierry-Mieg, D., Thierry-Mieg, J., Kim, H. P., Oh, J., Tunyaplin, C., Carotta, S., Donovan, C. E., Goldman, M. L., Tailor, P., Ozato, K., Levy, D. E., Nutt, S. L., Calame, K., and Leonard, W. J. (2009) Analysis of interleukin-21-induced Prdm1 gene regulation reveals functional cooperation of STAT3 and IRF4 transcription factors. Immunity 31, 941-952
57. Schiavone, D., Dewilde, S., Vallania, F., Turkson, J., Di Cunto, F., and Poli, V. (2009) The RhoU/Wrch1 Rho GTPase gene is a common transcriptional target of both the gp130/STAT3 and Wnt-1 pathways. Biochem. J. 421, 283-292
58. Walker, S. R., Nelson, E. A., Zou, L., Chaudhury, M., Signoretti, S., Richardson, A., and Frank, D. A. (2009) Reciprocal effects of STAT5 and STAT3 in breast cancer. Mol. Cancer Res. 7, 966-976
59. Lee, H., Deng, J., Kujawski, M., Yang, C., Liu, Y., Herrmann, A., Kortylewski, M., Horne, D., Somlo, G., Forman, S., Jove, R., and Yu, H. (2010) STAT3-induced S1PR1 expression is crucial for persistent STAT3 activation in tumors. Nat. Med. 16, 1421-1428
60. Niu, G., Wright, K. L., Ma, Y., Wright, G. M., Huang, M., Irby, R., Briggs, J., Karras, J., Cress, W. D., Pardoll, D., Jove, R., Chen, J., and Yu, H. (2005) Role of Stat3 in regulating p53 expression and function. Mol. Cell. Biol. 25, 7432-7440 (Pubitemid 41170107)
61. Armanious, H., Gelebart, P., Mackey, J., Ma, Y., and Lai, R. (2010) STAT3 upregulates the protein expression and transcriptional activity of β-catenin in breast cancer. Int. J. Clin. Exp. Pathol. 3, 654-664
62. Syed, Z. A., Yin, W., Hughes, K., Gill, J. N., Shi, R., and Clifford, J. L. (2011) HGF/c-met/Stat3 signaling during skin tumor cell invasion: indications for a positive feedback loop. BMC Cancer 11, 180
63. Sanz-Moreno, V., Gaggioli, C., Yeo, M., Albrengues, J., Wallberg, F., Viros, A., Hooper, S., Mitter, R., Féral, C. C., Cook, M., Larkin, J., Marais, R., Meneguzzi, G., Sahai, E., and Marshall, C. J. (2011) ROCK and JAK1 signaling cooperate to control actomyosin contractility in tumor cells and stroma. Cancer Cell 20, 229-245
64. Sano, S., Chan, K. S., and DiGiovanni, J. (2008) Impact of Stat3 activation upon skin biology: a dichotomy of its role between homeostasis and diseases. J. Dermatol. Sci. 50, 1-14 (Pubitemid 351249893)
65. Bromberg, J. (2002) Stat proteins and oncogenesis. J. Clin. Investig. 109, 1139-1142