Structural basis for activation of trimeric Gi proteins by multiple growth factor receptors via GIV/Girdin

Molecular Biology of the Cell

Volumn 25, Issue 22, 2014, Pages 3654-3671

  Lin, Changsheng ^a,d   Ear, Jason ^a,e   Midde, Krishna ^a   Lopez Sanchez, Inmaculada ^a   Aznar, Nicolas ^a   Garcia Marcos, Mikel ^b,f   Kufareva, Irina ^c   Abagyan, Ruben ^c   Ghosh, Pradipta ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d GLADSTONE INSTITUTES   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ARGININE; GROWTH FACTOR; GROWTH FACTOR RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; LEUCINE; MUTANT PROTEIN; PHOSPHOTYROSINE; PROTEIN GIRDIN; PROTEIN GIV; PROTEIN KINASE B; PROTEIN SH2; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; CCDC88A PROTEIN, HUMAN; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; GNAI3 PROTEIN, HUMAN; PROTEIN BINDING; VESICULAR TRANSPORT PROTEIN;

ARTICLE; AUTOPHOSPHORYLATION; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; PLASTICITY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TUMOR INVASION; AMINO ACID SEQUENCE; ANIMAL; CELL MOTION; CHEMICAL STRUCTURE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; HELA CELL LINE; METABOLISM; MOLECULAR GENETICS; PROTEIN DOMAIN; PROTEIN FOLDING; STRUCTURAL HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CELL MOVEMENT; GENE EXPRESSION REGULATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; HELA CELLS; HUMANS; MICROFILAMENT PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY, PROTEIN; VESICULAR TRANSPORT PROTEINS;

EID: 84908587141     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-05-0978     Document Type: Article

References (82)

1. Abagyan RA, Batalov S (1997). Do aligned sequences share the same fold? J Mol Biol 273, 355-368.
2. Abagyan R, Batalov S, Cardozo T, Totrov M, Webber J, Zhou Y (1997). Homology modeling with internal coordinate mechanics: deformation zone mapping and improvements of models via conformational search. Proteins Suppl 1, 29-37.
3. Abagyan R, Totrov M (1994). Biased probability Monte Carlo conformational searches and electrostatic calculations for peptides and proteins. J Mol Biol 235, 983-1002.
4. Abagyan R, Totrov M, Kuznetsov DA (1994). ICM: a new method for protein modeling and design: applications to docking and structure prediction from the distorted native conformation. J Comp Chem 15, 488-506.
5. Arold ST, Ulmer TS, Mulhern TD, Werner JM, Ladbury JE, Campbell ID, Noble ME (2001). The role of the Src homology 3-Src homology 2 interface in the regulation of Src kinases. J Biol Chem 276, 17199-17205.
6. Bairstow SF, Ling K, Anderson RA (2005). Phosphatidylinositol phosphate kinase type Igamma directly associates with and regulates Shp-1 tyrosine phosphatase. J Biol Chem 280, 23884-23891.
7. Batzer AG, Rotin D, Urena JM, Skolnik EY, Schlessinger J (1994). Hierarchy of binding sites for Grb2 and Shc on the epidermal growth factor receptor. Mol Cell Biol 14, 5192-5201.
8. Beas AO, Taupin V, Teodorof C, Nguyen LT, Garcia-Marcos M, Farquhar MG (2012). Galphas promotes EEA1 endosome maturation and shuts down proliferative signaling through interaction with GIV (Girdin). Mol Biol Cell 23, 4623-4634.
9. Cardozo T, Batalov S, Abagyan R (2000). Estimating local backbone structural deviation in homology models. Comput Chem 24, 13-31.
10. Cardozo T, Totrov M, Abagyan R (1995). Homology modeling by the ICM method. Proteins 23, 403-414.
11. Chen P, Gupta K, Wells A (1994a). Cell movement elicited by epidermal growth factor receptor requires kinase and autophosphorylation but is separable from mitogenesis. J Cell Biol 124, 547-555.
12. Chen P, Xie H, Sekar MC, Gupta K, Wells A (1994b). Epidermal growth factor receptor-mediated cell motility: phospholipase C activity is required, but mitogen-activated protein kinase activity is not sufficient for induced cell movement. J Cell Biol 127, 847-857.
13. Cismowski MJ, Ma C, Ribas C, Xie X, Spruyt M, Lizano JS, Lanier SM, Duzic E (2000). Activation of heterotrimeric G-protein signaling by a ras-related protein. Implications for signal integration. J Biol Chem 275, 23421-23424.
14. Cismowski MJ, Takesono A, Bernard ML, Duzic E, Lanier SM (2001). Receptor-independent activators of heterotrimeric G-proteins. Life Sci 68, 2301-2308.
15. Daub H, Weiss FU, Wallasch C, Ullrich A (1996). Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 379, 557-560.
16. Decker SJ (1993). Transmembrane signaling by epidermal growth factor receptors lacking autophosphorylation sites. J Biol Chem 268, 9176-9179.
17. Dunker AK, Silman I, Uversky VN, Sussman JL (2008). Function and structure of inherently disordered proteins. Curr Opin Struct Biol 18, 756-764.
18. Dyson HJ, Wright PE (2002). Coupling of folding and binding for unstructured proteins. Curr Opin Struct Biol 12, 54-60.
19. Dyson HJ, Wright PE (2005). Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6, 197-208.
20. Enomoto A, Asai N, Namba T, Wang Y, Kato T, Tanaka M, Tatsumi H, Taya S, Tsuboi D, Kuroda K, et al. (2009). Roles of disrupted-in-schizophrenia 1-interacting protein girdin in postnatal development of the dentate gyrus. Neuron 63, 774-787.
21. Enomoto A, Murakami H, Asai N, Morone N, Watanabe T, Kawai K, Murakumo Y, Usukura J, Kaibuchi K, Takahashi M (2005). Akt/PKB regulates actin organization and cell motility via Girdin/APE. Dev Cell 9, 389-402.
22. Garcia-Marcos M, Ear J, Farquhar MG, Ghosh P (2011a). A GDI (AGS3) and a GEF (GIV) regulate autophagy by balancing G protein activity and growth factor signals. Mol Biol Cell 22, 673-686.
23. Garcia-Marcos M, Ghosh P, Ear J, Farquhar MG (2010). 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.
24. Garcia-Marcos M, Ghosh P, Farquhar MG (2009). 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.
25. Garcia-Marcos M, Jung BH, Ear J, Cabrera B, Carethers JM, Ghosh P (2011b). Expression of GIV/Girdin, a metastasis-related protein, predicts patient survival in colon cancer. FASEB J 25, 590-599.
26. Garcia-Marcos M, Kietrsunthorn PS, Pavlova Y, Adia MA, Ghosh P, Farquhar MG (2012). 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.
27. Ghosh P, Beas AO, Bornheimer SJ, Garcia-Marcos M, Forry EP, Johannson C, Ear J, Jung BH, Cabrera B, Carethers JM, et al. (2010). A Gαi-GIV molecular complex binds epidermal growth factor receptor and determines whether cells migrate or proliferate. Mol Biol Cell 21, 2338-2354.
28. Ghosh P, Garcia-Marcos M, Bornheimer SJ, Farquhar MG (2008). Activation of Galphai3 triggers cell migration via regulation of GIV. J Cell Biol 182, 381-393.
29. Ghosh P, Garcia-Marcos M, Farquhar MG (2011). GIV/Girdin is a rheostat that fine-tunes growth factor signals during tumor progression. Cell Adh Migr 5, 237-248.
30. Gill GN, Kawamoto T, Cochet C, Le A, Sato JD, Masui H, McLeod C, Mendelsohn J (1984). Monoclonal anti-epidermal growth factor receptor antibodies which are inhibitors of epidermal growth factor binding and antagonists of epidermal growth factor binding and antagonists of epidermal growth factor-stimulated tyrosine protein kinase activity. J Biol Chem 259, 7755-7760.
31. Gonnet GH, Cohen MA, Benner SA (1992). Exhaustive matching of the entire protein sequence database. Science 256, 1443-1445.
32. Gschwind A, Fischer OM, Ullrich A (2004). The discovery of receptor tyrosine kinases: targets for cancer therapy. Nat Rev Cancer 4, 361-370.
33. Haan S, Hemmann U, Hassiepen U, Schaper F, Schneider-Mergener J, Wollmer A, Heinrich PC, Grotzinger J (1999). Characterization and binding specificity of the monomeric STAT3-SH2 domain. J Biol Chem 274, 1342-1348.
34. Helin K, Velu T, Martin P, Vass WC, Allevato G, Lowy DR, Beguinot L (1991). The biological activity of the human epidermal growth factor receptor is positively regulated by its C-terminal tyrosines. Oncogene 6, 825-832.
35. Iakoucheva LM, Brown CJ, Lawson JD, Obradovic Z, Dunker AK (2002). Intrinsic disorder in cell-signaling and cancer-associated proteins. J Mol Biol 323, 573-584.
36. Iakoucheva LM, Radivojac P, Brown CJ, O'Connor TR, Sikes JG, Obradovic Z, Dunker AK (2004). The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res 32, 1037-1049.
37. Jiang P, Enomoto A, Jijiwa M, Kato T, Hasegawa T, Ishida M, Sato T, Asai N, Murakumo Y, Takahashi M (2008). An actin-binding protein Girdin regulates the motility of breast cancer cells. Cancer Res 68, 1310-1318.
38. Keilhack H, Tenev T, Nyakatura E, Godovac-Zimmermann J, Nielsen L, Seedorf K, Bohmer FD (1998). Phosphotyrosine 1173 mediates binding of the protein-tyrosine phosphatase SHP-1 to the epidermal growth factor receptor and attenuation of receptor signaling. J Biol Chem 273, 24839-24846.
39. Kitamura T, Asai N, Enomoto A, Maeda K, Kato T, Ishida M, Jiang P, Watanabe T, Usukura J, Kondo T, et al. (2008). Regulation of VEGF-mediated angiogenesis by the Akt/PKB substrate Girdin. Nat Cell Biol 10, 329-337.
40. Lane JR, Henderson D, Powney B, Wise A, Rees S, Daniels D, Plumpton C, Kinghorn I, Milligan G (2008). Antibodies that identify only the active conformation of G(i) family G protein alpha subunits. FASEB J 22, 1924-1932.
41. Lee MJ, Dohlman HG (2008). Coactivation of G protein signaling by cell-surface receptors and an intracellular exchange factor. Curr Biol 18, 211-215.
42. Liebmann C, Bohmer FD (2000). Signal transduction pathways of G protein-coupled receptors and their cross-talk with receptor tyrosine kinases: lessons from bradykinin signaling. Curr Med Chem 7, 911-943.
43. Lin C, Ear J, Pavlova Y, Mittal Y, Kufareva I, Ghassemian M, Abagyan R, Garcia-Marcos M, Ghosh P (2011). Tyrosine phosphorylation of the Galpha-interacting protein GIV promotes activation of phosphoinositide 3-kinase during cell migration. Sci Signal 4, ra64.
44. Liu BA, Shah E, Jablonowski K, Stergachis A, Engelmann B, Nash PD (2011). The SH2 domain-containing proteins in 21 species establish the provenance and scope of phosphotyrosine signaling in eukaryotes. Sci Signal 4, ra83.
45. Lopez-Sanchez I, Dunkel Y, Roh YS, Mittal Y, De Minicis S, Muranyi A, Singh S, Shanmugam K, Aroonsakool N, Murray F, et al. (2014). GIV/Girdin is a central hub for profibrogenic signalling networks during liver fibrosis. Nat Commun 5, 4451.
46. Lowes VL, Ip NY, Wong YH (2002). Integration of signals from receptor tyrosine kinases and g protein-coupled receptors. Neuro-Signals 11, 5-19.
47. Luttrell LM (2006). Transmembrane signaling by G protein-coupled receptors. Methods Mol Biol 332, 3-49.
48. Luttrell LM, Daaka Y, Lefkowitz RJ (1999). Regulation of tyrosine kinase cascades by G-protein-coupled receptors. Curr Opin Cell Biol 11, 177-183.
49. Margolis BL, Lax I, Kris R, Dombalagian M, Honegger AM, Howk R, Givol D, Ullrich A, Schlessinger J (1989). All autophosphorylation sites of epidermal growth factor (EGF) receptor and HER2/neu are located in their carboxyl-terminal tails. Identification of a novel site in EGF receptor. J Biol Chem 264, 10667-10671.
50. Marinissen MJ, Gutkind JS (2001). G-protein-coupled receptors and signaling networks: emerging paradigms. Trends Pharmacol Sci 22, 368-376.
51. Marty C, Ye RD (2010). Heterotrimeric G protein signaling outside the realm of seven transmembrane domain receptors. Mol Pharmacol 78, 12-18.
52. Mills GB, Moolenaar WH (2003). The emerging role of lysophosphatidic acid in cancer. Nat Rev 3, 582-591.
53. Mittal Y, Pavlova Y, Garcia-Marcos M, Ghosh P (2011). Src homology domain 2-containing protein-tyrosine phosphatase-1 (SHP-1) binds and dephosphorylates G(alpha)-interacting, vesicle-associated protein (GIV)/Girdin and attenuates the GIV-phosphatidylinositol 3-kinase (PI3K)-Akt signaling pathway. J Biol Chem 286, 32404-32415.
54. Miyake H, Maeda K, Asai N, Shibata R, Ichimiya H, Isotani-Sakakibara M, Yamamura Y, Kato K, Enomoto A, Takahashi M, et al. (2011). The actin-binding protein Girdin and its Akt-mediated phosphorylation regulate neointima formation after vascular injury. Circ Res 108, 1170-1179.
55. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A (2002). A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20, 87-90.
56. Natarajan K, Berk BC (2006). Crosstalk coregulation mechanisms of G protein-coupled receptors and receptor tyrosine kinases. Methods Mol Biol 332, 51-77.
57. Okabayashi Y, Kido Y, Okutani T, Sugimoto Y, Sakaguchi K, Kasuga M (1994). Tyrosines 1148 and 1173 of activated human epidermal growth factor receptors are binding sites of Shc in intact cells. J Biol Chem 269, 18674-18678.
58. Okutani T, Okabayashi Y, Kido Y, Sugimoto Y, Sakaguchi K, Matuoka K, Takenawa T, Kasuga M (1994). Grb2/Ash binds directly to tyrosines 1068 and 1086 and indirectly to tyrosine 1148 of activated human epidermal growth factor receptors in intact cells. J Biol Chem 269, 31310-31314.
59. Ostrom RS, Gregorian C, Drenan RM, Xiang Y, Regan JW, Insel PA (2001). Receptor number and caveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J Biol Chem 276, 42063-42069.
60. Piiper A, Zeuzem S (2004). Receptor tyrosine kinases are signaling intermediates of G protein-coupled receptors. Curr Pharm Des 10, 3539-3545.
61. Poppleton H, Sun H, Fulgham D, Bertics P, Patel TB (1996). Activation of Gsalpha by the epidermal growth factor receptor involves phosphorylation. J Biol Chem 271, 6947-6951.
62. Porteous D, Millar K (2009). How DISC1 regulates postnatal brain development: girdin gets in on the AKT. Neuron 63, 711-713.
63. Puseenam A, Yoshioka Y, Nagai R, Hashimoto R, Suyari O, Itoh M, Enomoto A, Takahashi M, Yamaguchi M (2009). A novel Drosophila Girdin-like protein is involved in Akt pathway control of cell size. Exp Cell Res 315, 3370-3380.
64. Rose PW, Beran B, Bi C, Bluhm WF, Dimitropoulos D, Goodsell DS, Prlic A, Quesada M, Quinn GB, Westbrook JD, et al. (2011). The RCSB Protein Data Bank: redesigned web site and web services. Nucleic Acids Res 39, D392-D401.
65. Sakaguchi K, Okabayashi Y, Kido Y, Kimura S, Matsumura Y, Inushima K, Kasuga M (1998). Shc phosphotyrosine-binding domain dominantly interacts with epidermal growth factor receptors and mediates Ras activation in intact cells. Mol Endocrinol 12, 536-543.
66. Savage CR Jr, Cohen S (1972). Epidermal growth factor and a new derivative. Rapid isolation procedures and biological and chemical characterization. J Biol Chem 247, 7609-7611.
67. Schafer B, Gschwind A, Ullrich A (2004). Multiple G-protein-coupled receptor signals converge on the epidermal growth factor receptor to promote migration and invasion. Oncogene 23, 991-999.
68. Schlessinger J (1994). SH2/SH3 signaling proteins. Curr Opin Genet Dev 4, 25-30.
69. Schlessinger J, Lemmon MA (2003). SH2 and PTB domains in tyrosine kinase signaling. Sci STKE 2003 RE12.
70. Shyu YJ, Suarez CD, Hu CD (2008). Visualization of ternary complexes in living cells by using a BiFC-based FRET assay. Nat Protocols 3, 1693-1702.
71. Siderovski DP, Willard FS (2005). The GAPs, GEFs, and GDIs of heterotrimeric G-protein alpha subunits. Int J Biol Sci 1, 51-66.
72. Songyang Z, Shoelson SE, Chaudhuri M, Gish G, Pawson T, Haser WG, King F, Roberts T, Ratnofsky S, Lechleider RJ, et al. (1993). SH2 domains recognize specific phosphopeptide sequences. Cell 72, 767-778.
73. Songyang Z, Shoelson SE, McGlade J, Olivier P, Pawson T, Bustelo XR, Barbacid M, Sabe H, Hanafusa H, Yi T, et al. (1994). Specific motifs recognized by the SH2 domains of Csk, 3BP2, fps/fes, GRB-2, HCP, SHC, Syk, and Vav. Mol Cell Biol 14, 2777-2785.
74. Sorkin A, Helin K, Waters CM, Carpenter G, Beguinot L (1992). Multiple autophosphorylation sites of the epidermal growth factor receptor are essential for receptor kinase activity and internalization. Contrasting significance of tyrosine 992 in the native and truncated receptors. J Biol Chem 267, 8672-8678.
75. Sorkin A, Waters C, Overholser KA, Carpenter G (1991). Multiple autophosphorylation site mutations of the epidermal growth factor receptor. Analysis of kinase activity and endocytosis. J Biol Chem 266, 8355-8362.
76. Sun H, Seyer JM, Patel TB (1995). A region in the cytosolic domain of the epidermal growth factor receptor antithetically regulates the stimulatory and inhibitory guanine nucleotide-binding regulatory proteins of adenylyl cyclase. Proc Natl Acad Sci USA 92, 2229-2233.
77. Tall GG, Krumins AM, Gilman AG (2003). Mammalian Ric-8A (synembryn) is a heterotrimeric Galpha protein guanine nucleotide exchange factor. J Biol Chem 278, 8356-8362.
78. Walton GM, Chen WS, Rosenfeld MG, Gill GN (1990). Analysis of deletions of the carboxyl terminus of the epidermal growth factor receptor reveals self-phosphorylation at tyrosine 992 and enhanced in vivo tyrosine phosphorylation of cell substrates. J Biol Chem 265, 1750-1754.
79. Wang Y, Kaneko N, Asai N, Enomoto A, Isotani-Sakakibara M, Kato T, Asai M, Murakumo Y, Ota H, Hikita T, et al. (2011). Girdin is an intrinsic regulator of neuroblast chain migration in the rostral migratory stream of the postnatal brain. J Neurosci 31, 8109-8122.
80. Wang H, Misaki T, Taupin V, Eguchi A, Ghosh P, Farquhar MG (2014). GIV/Girdin links vascular endothelial growth factor signaling to Akt survival signaling in podocytes independent of nephrin. J Am Soc Nephrol, ASN.2013090985.
81. Williams KP, Shoelson SE (1993). Cooperative self-assembly of SH2 domain fragments restores phosphopeptide binding. Biochemistry 32, 11279-11284.
82. Yamaguchi M, Suyari O, Nagai R, Takahashi M (2010). dGirdin a new player of Akt /PKB signaling in Drosophila melanogaster. Front Biosci 15, 1164-1171.