Gα12 inhibits α2β1 integrin-mediated Madin-Darby canine kidney cell attachment and migration on collagen-I and blocks tubulogenesis

Molecular Biology of the Cell

Volumn 20, Issue 21, 2009, Pages 4596-4610

  Kong, Tianqing ^a   Xu, Daosong ^b   Yu, Wanfeng ^a   Takakura, Ayumi ^a   Boucher, Ilene ^a   Tran, Mei ^a   Kreidberg, Jordan A ^c   Shah, Jagesh ^a   Zhou, Jing ^a   Denker, Bradley M ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; G PROTEIN ALPHA 12; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; LIGAND; PAXILLIN; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN TYROSINE KINASE; RHO KINASE; THROMBIN; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL ADHESION; CELL MIGRATION; CELL POLARITY; CELL SPREADING; CELL STRAIN; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME INHIBITION; EPITHELIUM CELL; FOCAL ADHESION; GENE ACTIVATION; GENE SILENCING; IMMUNOFLUORESCENCE; INHIBITION KINETICS; LAMELLIPODIUM; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; THREE DIMENSIONAL IMAGING;

ANIMALS; CELL ADHESION; CELL LINE; CELL MOVEMENT; COLLAGEN TYPE I; DOGS; ENZYME ACTIVATION; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; HUMANS; INTEGRIN ALPHA2BETA1; KIDNEY TUBULES; PAXILLIN; PSEUDOPODIA; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 73949114220     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-03-0220     Document Type: Article

References (48)

1. Alvarez, S. E., Seguin, L. R., Villarreal, R. S., Nahmias, C., and Ciuffo, G. M. (2008). Involvement of c-Src tyrosine kinase in SHP-1 phosphatase activation by Ang II AT2 receptors in rat fetal tissues. J. Cell. Biochem. 105, 703-711.
2. Arthur, W. T., and Burridge, K. (2001). RhoA inactivation by p190RhoGAP regulates cell spreading and migration by promoting membrane protrusion and polarity. Mol. Biol. Cell 12, 2711-2720.
3. Arthur, W. T., Petch, L. A., and Burridge, K. (2000). Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr. Biol. 10, 719-722.
4. Battini, L., Fedorova, E., Macip, S., Li, X., Wilson, P. D., and Gusella, G. L. (2006). Stable knockdown of polycystin-1 confers integrin- α2β1-mediated anoikis resistance. J. Am. Soc. Nephrol. 17, 3049-3058.
5. Boca, M., D'Amato, L., Distefano, G., Polishchuk, R. S., Germino, G. G., and Boletta, A. (2007). Polycystin-1 induces cell migration by regulating phosphatidylinositol 3-kinase-dependent cytoskeletal rearrangements and GSK3β-dependent cell cell mechanical adhesion. Mol. Biol. Cell 18, 4050-4061.
6. Buhl, A. M., Johnson, N. L., Dhanasekaran, N., and Johnson, G. L. (1995). Gα12 and Gα13 stimulate Rho-dependent stress fiber formation and focal adhesion assembly. J. Biol. Chem. 270, 24631-24634.
7. Chen, D., et al. (2004). Differential expression of collagen- and laminin-binding integrins mediates ureteric bud and inner medullary collecting duct cell tubulogenesis. Am. J. Physiol. Renal. Physiol. 287, F602-F611.
8. Dorsam, R. T., Kim, S., Jin, J., and Kunapuli, S. P. (2002). Coordinated signaling through both G12/13 and G(i) pathways is sufficient to activate GPIIb/IIIa in human platelets. J. Biol. Chem. 277, 47588-47595.
9. Earley, S., and Plopper, G. E. (2008). Phosphorylation of focal adhesion kinase promotes extravasation of breast cancer cells. Biochem. Biophys. Res. Commun. 366, 476-482.
10. Goulimari, P., Kitzing, T. M., Knieling, H., Brandt, D. T., Offermanns, S., and Grosse, R. (2005). Gα12/13 is essential for directed cell migration and localized Rho-Dia1 function. J. Biol. Chem. 280, 42242-42251.
11. Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687.
12. Joly, D., Morel, V., Hummel, A., Ruello, A., Nusbaum, P., Patey, N., Noel, L. H., Rousselle, P., and Knebelmann, B. (2003). β4 integrin and laminin 5 are aberrantly expressed in polycystic kidney disease: role in increased cell adhesion and migration. Am. J. Pathol. 163, 1791-1800.
13. Kelly, P., Casey, P. J., and Meigs, T. E. (2007). Biologic functions of the G12 subfamily of heterotrimeric G proteins: growth, migration, and metastasis. Biochemistry 46, 6677-6687.
14. Kelly, P., Moeller, B. J., Juneja, J., Booden, M. A., Der, C. J., Daaka, Y., Dewhirst, M. W., Fields, T. A., and Casey, P. J. (2006a). The G12 family of heterotrimeric G proteins promotes breast cancer invasion and metastasis. Proc. Natl. Acad. Sci. USA 103, 8173-8178.
15. Kelly, P., Stemmle, L. N., Madden, J. F., Fields, T. A., Daaka, Y., and Casey, P. J. (2006b). A role for the G12 family of heterotrimeric G proteins in prostate cancer invasion. J. Biol. Chem. 281, 26483-26490.
16. Khare, S., Holgren, C., and Samarel, A. M. (2006). Deoxycholic acid differentially regulates focal adhesion kinase phosphorylation: role of tyrosine phosphatase ShP2. Am. J. Physiol. Gastrointest. Liver Physiol. 291, G1100-G1112.
17. Kiyokawa, E., Hashimoto, Y., Kobayashi, S., Sugimura, H., Kurata, T., and Matsuda, M. (1998). Activation of Rac1 by a Crk SH3-binding protein, DOCK180. Genes Dev. 12, 3331-3336.
18. Kolesnikova, T. V., Mannion, B. A., Berditchevski, F., and Hemler, M. E. (2001). β1 integrins show specific association with CD98 protein in low density membranes. BMC Biochem. 2, 10.
19. Kozasa, T., Jiang, X., Hart, M. J., Sternweis, P. M., Singer, W. D., Gilman, A. G., Bollag, G., and Sternweis, P. C. (1998). p115 RhoGEF, a GTPase activating protein for Gα12 and Gα13. Science 280, 2109-2111.
20. Liao, Z., Seye, C. I., Weisman, G. A., and Erb, L. (2007). The P2Y2 nucleotide receptor requires interaction with α v integrins to access and activate G12. J. Cell Sci. 120, 1654-1662.
21. Lim, Y., Han, I., Jeon, J., Park, H., Bahk, Y. Y., and Oh, E. S. (2004). Phosphorylation of focal adhesion kinase at tyrosine 861 is crucial for Ras transformation of fibroblasts. J. Biol. Chem. 279, 29060-29065.
22. Ma, Y. C., Huang, J., Ali, S., Lowry, W., and Huang, X. Y. (2000). Src tyrosine kinase is a novel direct effector of G proteins. Cell 102, 635-646.
23. Meigs, T. E., Fedor-Chaiken, M., Kaplan, D. D., Brackenbury, R., and Casey, P. J. (2002). Gα12 and Gα13 negatively regulate the adhesive functions of cadherin. J. Biol. Chem. 277, 24594-24600.
24. Meyer, T. N., Hunt, J., Schwesinger, C., and Denker, B. M. (2003). Gα12 regulates epithelial cell junctions through Src tyrosine kinases. Am. J. Physiol. Cell Physiol. 285, C1281-C1293.
25. Meyer, T. N., Schwesinger, C., and Denker, B. M. (2002). Zonula occludens-1 is a scaffolding protein for signaling molecules. Gα12 directly binds to the Src homology 3 domain and regulates paracellular permeability in epithelial cells. J. Biol. Chem. 277, 24855-24858.
26. Mitra, S. K., Hanson, D. A., and Schlaepfer, D. D. (2005). Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6, 56-68.
27. Nieswandt, B., Schulte, V., Zywietz, A., Gratacap, M. P., and Offermanns, S. (2002). Costimulation of Gi- and G12/G13-mediated signaling pathways induces integrin αIIb β3 activation in platelets. J. Biol. Chem. 277, 39493-39498.
28. O'Brien, L. E., Zegers, M. M., and Mostov, K. E. (2002). Opinion: Building epithelial architecture: insights from three-dimensional culture models. Nat. Rev. Mol. Cell Biol. 3, 531-537.
29. Pohl, M., Stuart, R. O., Sakurai, H., and Nigam, S. K. (2000). Branching morphogenesis during kidney development. Annu. Rev. Physiol. 62, 595-620.
30. Pollack, A. L., Runyan, R. B., and Mostov, K. E. (1998). Morphogenetic mechanisms of epithelial tubulogenesis: MDCK cell polarity is transiently rearranged without loss of cell-cell contact during scatter factor/hepatocyte growth factor-induced tubulogenesis. Dev. Biol. 204, 64-79.
31. Ren, X. D., Kiosses, W. B., and Schwartz, M. A. (1999). Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18, 578-585.
32. Rieken, S., Herroeder, S., Sassmann, A., Wallenwein, B., Moers, A., Offermanns, S., and Wettschureck, N. (2006). Lysophospholipids control integrin-dependent adhesion in splenic B cells through G(i) and G(12)/G(13) family G-proteins but not through G(q)/G(11). J. Biol. Chem. 281, 36985-36992.
33. Rigacci, S., Rovida, E., Dello Sbarba, P., and Berti, A. (2002). Low Mr phosphotyrosine protein phosphatase associates and dephosphorylates p125 focal adhesion kinase, interfering with cell motility and spreading. J. Biol. Chem. 277, 41631-41636.
34. Riobo, N. A., and Manning, D. R. (2005). Receptors coupled to heterotrimeric G proteins of the G12 family. Trends Pharmacol. Sci. 26, 146-154.
35. Sabath, E., Negoro, H., Beaudry, S., Paniagua, M., Angelow, S., Shah, J., Grammatikakis, N., Yu, A. S., and Denker, B. M. (2008). Gα12 regulates protein interactions within the MDCK cell tight junction and inhibits tight-junction assembly. J. Cell Sci. 121, 814-824.
36. Saelman, E. U., Keely, P. J., and Santoro, S. A. (1995). Loss of MDCK cell α2β1integrin expression results in reduced cyst formation, failure of hepatocyte growth factor/scatter factor-induced branching morphogenesis, and increased apoptosis. J. Cell Sci. 108(Pt 11), 3531-3540.
37. Wang, C. Z., Su, H. W., Hsu, Y. C., Shen, M. R., and Tang, M. J. (2006). A discoidin domain receptor 1/SHP-2 signaling complex inhibits α2β1-integrin-mediated signal transducers and activators of transcription 1/3 activation and cell migration. Mol. Biol. Cell 17, 2839-2852.
38. Wang, X. Q., and Frazier, W. A. (1998). The thrombospondin receptor CD47 (IAP) modulates and associates with α2β1 integrin in vascular smooth muscle cells. Mol. Biol. Cell 9, 865-874.
39. Wilson, P. D., Geng, L., Li, X., and Burrow, C. R. (1999). The PKD1 gene product, "polycystin-1," is a tyrosine-phosphorylated protein that colocalizes with α2β1-integrin in focal clusters in adherent renal epithelia. Lab. Invest. 79,1311-1323.
40. Xu, J., et al. (2003). Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 114, 201-214.
41. Yamaguchi, Y., Katoh, H., Mori, K., and Negishi, M. (2002). Gα(12) and Gα(13) interact with Ser/Thr protein phosphatase type 5 and stimulate its phosphatase activity. Curr. Biol. 12, 1353-1358.
42. Yamaguchi, Y., Katoh, H., and Negishi, M. (2003). N-terminal short sequences of α subunits of the G12 family determine selective coupling to receptors. J. Biol. Chem. 278, 14936-14939.
43. Yanamadala, V., Negoro, H., Gunaratnam, L., Kong, T., and Denker, B. M. (2007). Gα12 stimulates apoptosis in epithelial cells through JNK1-mediated Bcl-2 degradation and up-regulation of IkBα. J. Biol. Chem. 282, 24352-24363.
44. Yang, X. H., Richardson, A. L., Torres-Arzayus, M. I., Zhou, P., Sharma, C., Kazarov, A. R., Andzelm, M. M., Strominger, J. L., Brown, M., and Hemler, M. E. (2008). CD151 accelerates breast cancer by regulating α 6 integrin function, signaling, and molecular organization. Cancer Res. 68, 3204-3213.
45. Yuasa, T., Takakura, A., Denker, B. M., Venugopal, B., and Zhou, J. (2004). Polycystin-1L2 is a novel G-protein-binding protein. Genomics 84, 126-138.
46. Zhu, D., Kosik, K. S., Meigs, T. E., Yanamadala, V., and Denker, B. M. (2004). Gα12 directly interacts with PP2A: evidence for Gα12-stimulated PP2A phosphatase activity and dephosphorylation of microtubule-associated protein, tau. J. Biol. Chem. 279, 54983-54986.
47. Zhu, D., Tate, R. I., Ruediger, R., Meigs, T. E., and Denker, B. M. (2007). Domains necessary for Gα12 binding and stimulation of protein phosphatase-2A (PP2A): is Gα12 a novel regulatory subunit of PP2A? Mol. Pharmacol. 71, 1268-1276.
48. Zylstra, S., Chen, F. A., Ghosh, S. K., Repasky, E. A., Rao, U., Takita, H., and Bankert, R. B. (1986). Membrane-associated glycoprotein (gp 160) identified on human lung tumors by a monoclonal antibody. Cancer Res. 46, 6446-6451.