GIV/Girdin is a central hub for profibrogenic signalling networks during liver fibrosis

Nature Communications

Volumn 5, Issue , 2014, Pages

  Lopez Sanchez, Inmaculada ^a   Dunkel, Ying ^a   Roh, Yoon Seok ^a   Mittal, Yash ^a   De Minicis, Samuele ^a   Muranyi, Andrea ^b   Singh, Shalini ^b   Shanmugam, Kandavel ^b   Aroonsakool, Nakon ^a   Murray, Fiona ^a   Ho, Samuel B ^c   Seki, Ekihiro ^a   Brenner, David A ^a   Ghosh, Pradipta ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; G ALPHA INTERACTING VESICLE ASSOCIATED PROTEIN; GUANINE; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMAD PROTEIN; TRANSCRIPTION FACTOR FKHR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; CCDC88A PROTEIN, HUMAN; COLLAGEN; GIRDIN PROTEIN, MOUSE; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; VESICULAR TRANSPORT PROTEIN;

COLLAGEN; PROTEIN; SIGNALING;

ARTICLE; CELL ACTIVATION; DISEASE COURSE; FIBROGENESIS; HUMAN; HUMAN CELL; LIVER FIBROSIS; LIVER INJURY; PROTEIN EXPRESSION; STELLATE CELL; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL LINE; GENETICS; HEPATIC STELLATE CELL; LIVER CIRRHOSIS; MALE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; CELL LINE; COLLAGEN; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEPATIC STELLATE CELLS; HUMANS; LIVER CIRRHOSIS; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION; VESICULAR TRANSPORT PROTEINS;

EID: 84904673615     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5451     Document Type: Article

References (64)

1. Friedman, S. L. Mechanisms of hepatic fibrogenesis. Gastroenterology 134, 1655-1669 (2008). (Pubitemid 351615417)
2. Pinzani, M., Gesualdo, L., Sabbah, G. M. & Abboud, H. E. Effects of plateletderived growth factor and other polypeptide mitogens on DNA synthesis and growth of cultured rat liver fat-storing cells. J. Clin. Invest. 84, 1786-1793 (1989). (Pubitemid 20016182)
3. Gressner, A. M., Weiskirchen, R., Breitkopf, K. & Dooley, S. Roles of TGF-beta in hepatic fibrosis. Front. Biosci. 7, d793-d807 (2002).
4. Svegliati-Baroni, G. et al. Bile acids induce hepatic stellate cell proliferation via activation of the epidermal growth factor receptor. Gastroenterology 128, 1042-1055 (2005). (Pubitemid 40523554)
5. Yoshiji, H. et al. Vascular endothelial growth factor and receptor interaction is a prerequisite for murine hepatic fibrogenesis. Gut. 52, 1347-1354 (2003). (Pubitemid 37026470)
6. Svegliati-Baroni, G. et al. Insulin and insulin-like growth factor-1 stimulate proliferation and type I collagen accumulation by human hepatic stellate cells: differential effects on signal transduction pathways. Hepatology (Baltimore, Md) 29, 1743-1751 (1999). (Pubitemid 29247048)
7. Seki, E. et al. CCR1 and CCR5 promote hepatic fibrosis in mice. J. Clin. Invest. 119, 1858-1870 (2009).
8. Chow, E. K. et al. TLR agonists regulate PDGF-B production and cell proliferation through TGF-beta/type I IFN crosstalk. EMBO J. 24, 4071-4081 (2005). (Pubitemid 41752876)
9. Parsons, C. J., Takashima, M. & Rippe, R. A. Molecular mechanisms of hepatic fibrogenesis. J. Gastroenterol. Hepatol. 22(Suppl 1), S79-S84 (2007). (Pubitemid 46848998)
10. Adachi, M. et al. The forkhead transcription factor FoxO1 regulates proliferation and transdifferentiation of hepatic stellate cells. Gastroenterology 132, 1434-1446 (2007). (Pubitemid 46627569)
11. Son, G., Hines, I. N., Lindquist, J., Schrum, L. W. & Rippe, R. A. Inhibition of phosphatidylinositol 3-kinase signaling in hepatic stellate cells blocks the progression of hepatic fibrosis. Hepatology (Baltimore, Md) 50, 1512-1523 (2009).
12. Solis-Herruzo, J. A. et al. G proteins are involved in the suppression of collagen alpha 1 (I) gene expression in cultured rat hepatic stellate cells. Cell Signal 10, 173-183 (1998). (Pubitemid 28156068)
13. Liu, X., Sun, S. Q., Hassid, A. & Ostrom, R. S. cAMP inhibits transforming growth factor-beta-stimulated collagen synthesis via inhibition of extracellular signal-regulated kinase 1/2 and Smad signaling in cardiac fibroblasts. Mol. Pharmacol. 70, 1992-2003 (2006). (Pubitemid 44771915)
14. Ghosh, A. K., Yuan, W., Mori, Y. & Varga, J. Smad-dependent stimulation of type I collagen gene expression in human skin fibroblasts by TGF-beta involves functional cooperation with p300/CBP transcriptional coactivators. Oncogene 19, 3546-3555 (2000). (Pubitemid 30487452)
15. Kitamura, T. et al. Regulation of VEGF-mediated angiogenesis by the Akt/PKB substrate Girdin. Nat. Cell Biol. 10, 329-337 (2008). (Pubitemid 351331020)
16. Garcia-Marcos, M., Ghosh, P. & Farquhar, M. G. GIV is a nonreceptor GEF for G alpha I with a unique motif that regulates Akt signaling. Proc. Natl Acad. Sci. USA 106, 3178-3183 (2009).
17. Lin, C. et al. Tyrosine phosphorylation of the Galpha-interacting protein GIV promotes activation of phosphoinositide 3-kinase during cell migration. Sci. Signal 4, ra64 (2011).
18. Jiang, P. et al. An actin-binding protein Girdin regulates the motility of breast cancer cells. Cancer Res. 68, 1310-1318 (2008). (Pubitemid 351346837)
19. Ghosh, P., Garcia-Marcos, M., Bornheimer, S. J. & Farquhar, M. G. Activation of Galphai3 triggers cell migration via regulation of GIV. J. Cell Biol. 182, 381-393 (2008).
20. Lopez-Sanchez, I. et al. Protein kinase C-theta (PKCtheta) phosphorylates and inhibits the guanine exchange factor, GIV/Girdin. Proc. Natl Acad. Sci. USA 110, 5510-5515 (2013).
21. Ghosh, P., Garcia-Marcos, M. & Farquhar, M. G. GIV/Girdin is a rheostat that fine-tunes growth factor signals during tumor progression. Cell Adh. Migr. 5, 237-248 (2011).
22. Dunkel, Y. et al. STAT3 protein up-regulates Galpha-interacting vesicleassociated protein (GIV)/Girdin expression, and GIV enhances STAT3 activation in a positive feedback loop during wound healing and tumor invasion/metastasis. J. Biol. Chem. 287, 41667-41683 (2012).
23. Albanis, E. & Friedman, S. L. Hepatic fibrosis. Pathogenesis and principles of therapy. Clin. Liver Dis. 5, 315-334 (2001). (Pubitemid 32472561)
24. Schuppan, D., Krebs, A., Bauer, M. & Hahn, E. G. Hepatitis C and liver fibrosis. Cell Death Differ. 10(Suppl 1), S59-S67 (2003). (Pubitemid 36511853)
25. Weiler-Normann, C., Herkel, J. & Lohse, A. W. Mouse models of liver fibrosis. Z. Gastroenterol. 45, 43-50 (2007). (Pubitemid 46202720)
26. Ghosh, P. et al. A G{alpha}i-GIV molecular complex binds epidermal growth factor receptor and determines whether cells migrate or proliferate. Mol. Biol. Cell 21, 2338-2354 (2010).
27. Wu, J., Kuncio, G. S. & Zern, M. A. in Liver Growth and Repair (eds S., Alastair. & D., Anne Mae.) 558-576 (Springer, 1998).
28. Moreira, R. K. Hepatic stellate cells and liver fibrosis. Arch. Pathol. Lab. Med. 131, 1728-1734 (2007). (Pubitemid 350077474)
29. Mederacke, I. et al. Fate tracing reveals hepatic stellate cells as dominant contributors to liver fibrosis independent of its aetiology. Nat. Commun. 4, 2823 (2013).
30. Yata, Y. et al. DNase I-hypersensitive sites enhance alpha1(I) collagen gene expression in hepatic stellate cells. Hepatology (Baltimore, Md) 37, 267-276 (2003). (Pubitemid 36152525)
31. Xu, L. et al. Human hepatic stellate cell lines, LX-1 and LX-2: new tools for analysis of hepatic fibrosis. Gut. 54, 142-151 (2005). (Pubitemid 40007234)
32. Enomoto, A. et al. Akt/PKB regulates actin organization and cell motility via Girdin/APE. Dev. Cell 9, 389-402 (2005). (Pubitemid 41235808)
33. Basu, A. & Haldar, S. The relationship between BcI2, Bax and p53: consequences for cell cycle progression and cell death. Mol. Hum. Reprod. 4, 1099-1109 (1998). (Pubitemid 28552792)
34. Wright, M. C. et al. Gliotoxin stimulates the apoptosis of human and rat hepatic stellate cells and enhances the resolution of liver fibrosis in rats. Gastroenterology 121, 685-698 (2001). (Pubitemid 32822584)
35. Elmore, S. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 35, 495-516 (2007). (Pubitemid 46911891)
36. Cong, M., Iwaisako, K., Jiang, C. & Kisseleva, T. Cell signals influencing hepatic fibrosis. Int. J. Hepatol. 2012, 158547 (2012).
37. Lane, J. R., Powney, B., Wise, A., Rees, S. & Milligan, G. G protein coupling and ligand selectivity of the D2L and D3 dopamine receptors. J. Pharmacol. Exp. Ther. 325, 319-330 (2008). (Pubitemid 351439159)
38. Chen, S. L. & Morgan, T. R. The natural history of hepatitis C virus (HCV) infection. Int. J. Med. Sci. 3, 47-52 (2006).
39. Vallet-Pichard, A. et al. FIB-4: an inexpensive and accurate marker of fibrosis in HCV infection. comparison with liver biopsy and fibrotest. Hepatology (Baltimore, Md) 46, 32-36 (2007). (Pubitemid 47171918)
40. Chou, R. & Wasson, N. Blood tests to diagnose fibrosis or cirrhosis in patients with chronic hepatitis C virus infection. Ann. Intern. Med. 159, 372 (2013).
41. Shah, R. et al. TGF-beta1 up-regulates the expression of PDGF-beta receptor mRNA and induces a delayed PI3K-, AKT-, and p70-dependent proliferative response in activated hepatic stellate cells.. Alcohol Clin. Exp. Res. 37, 1838-1848 (2013).
42. Messadi, D. V. et al. Effect of TGF-beta 1 on PDGF receptors expression in human scar fibroblasts. Front. Biosci. 3, a16-a22 (1998).
43. Ikuno, Y. & Kazlauskas, A. TGFbeta1-dependent contraction of fibroblasts is mediated by the PDGFalpha receptor. Invest. Ophthalmol. Vis. Sci. 43, 41-46 (2002). (Pubitemid 34032438)
44. Das, F. et al. Akt kinase targets association of CBP with SMAD 3 to regulate TGFbeta-induced expression of plasminogen activator inhibitor-1. J. Cell Physiol. 214, 513-527 (2008). (Pubitemid 350309008)
45. Garcia-Marcos, M., Ghosh, P., Ear, J. & Farquhar, M. G. A structural determinant that renders G alpha(i) sensitive to activation by GIV/girdin is required to promote cell migration. J. Biol. Chem. 285, 12765-12777 (2010).
46. Jia, Y. & Turek, J. J. Altered NF-kappaB gene expression and collagen formation induced by polyunsaturated fatty acids. J. Nutr. Biochem. 16, 500-506 (2005). (Pubitemid 41039224)
47. He, Z., Zhu, Y. & Jiang, H. Toll-like receptor 4 mediates lipopolysaccharide-induced collagen secretion by phosphoinositide3-kinase-Akt pathway in fibroblasts during acute lung injury. J. Recept. Signal Transduct. Res. 29, 119-125 (2009).
48. Guo, J. et al. Functional linkage of cirrhosis-predictive single nucleotide polymorphisms of Toll-like receptor 4 to hepatic stellate cell responses. Hepatology (Baltimore, Md) 49, 960-968 (2009).
49. Schwabe, R. F., Seki, E. & Brenner, D. A. Toll-like receptor signaling in the liver. Gastroenterology 130, 1886-1900 (2006). (Pubitemid 43668871)
50. Kisseleva, T. & Brenner, D. A. Mechanisms of fibrogenesis. Exp. Biol. Med. (Maywood) 233, 109-122 (2008). (Pubitemid 351231543)
51. Swaney, J. S. et al. Inhibition of cardiac myofibroblast formation and collagen synthesis by activation and overexpression of adenylyl cyclase. Proc. Natl Acad. Sci. USA 102, 437-442 (2005). (Pubitemid 40116785)
52. Kisseleva, T. & Brenner, D. A. Fibrogenesis of parenchymal organs. Proc. Am. Thorac. Soc. 5, 338-342 (2008). (Pubitemid 351520684)
53. Kolios, G., Valatas, V. & Kouroumalis, E. Role of Kupffer cells in the pathogenesis of liver disease. World J. Gastroenterol. 12, 7413-7420 (2006). (Pubitemid 46017736)
54. Chao, W., Liu, H. L., Zhou, W. G., Hanahan, D. J. & Olson, M. S. Regulation of platelet-activating factor receptor and platelet-activating factor receptormediated biological responses by cAMP in rat Kupffer cells. J. Biol. Chem. 265, 17576-17583 (1990).
55. Wang, H., Lafdil, F., Kong, X. & Gao, B. Signal transducer and activator of transcription 3 in liver diseases: a novel therapeutic target. Int. J. Biol. Sci. 7, 536-550 (2011).
56. Coulouarn, C. et al. Hepatocyte-stellate cell cross-talk in the liver engenders a permissive inflammatory microenvironment that drives progression in hepatocellular carcinoma. Cancer Res. 72, 2533-2542 (2012).
57. Garcia-Marcos, M. et al. Expression of GIV/Girdin, a metastasis-related protein, predicts patient survival in colon cancer. FASEB J. 25, 590-599 (2011).
58. Lane, J. R. et al. Antibodies that identify only the active conformation of G(i) family G protein alpha subunits. FASEB J. 22, 1924-1932 (2008). (Pubitemid 351811469)
59. Fukasawa, H. et al. Phosphorylation of podocalyxin (Ser415) Prevents RhoA and ezrin activation and disrupts its interaction with the actin cytoskeleton. Am. J. Pathol. 179, 2254-2265 (2011).
60. Taura, K. et al. Hepatic stellate cells secrete angiopoietin 1 that induces angiogenesis in liver fibrosis. Gastroenterology 135, 1729-1738 (2008).
61. Garcia-Marcos, M., Ear, J., Farquhar, M. G. & Ghosh, P. A GDI (AGS3) and a GEF (GIV) regulate autophagy by balancing G protein activity and growth factor signals. Mol. Biol. Cell 22, 673-686 (2011).
62. Luo, J. et al. A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat. Protoc. 2, 1236-1247 (2007). (Pubitemid 46908240)
63. Garcia-Marcos, M. et al. Functional characterization of the guanine nucleotide exchange factor (GEF) motif of GIV protein reveals a threshold effect in signaling. Proc. Natl Acad. Sci. USA 109, 1961-1966 (2012).
64. Ostrom, R. S. et al. Receptor number and caveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J. Biol. Chem. 276, 42063-42069 (2001).