Docking protein gab1 is an essential component of postnatal angiogenesis after ischemia via HGF/c-met signaling

Circulation Research

Volumn 108, Issue 6, 2011, Pages 664-675

  Shioyama, Wataru ^a   Nakaoka, Yoshikazu ^a   Higuchi, Kaori ^a   Minami, Takashi ^c   Taniyama, Yoshiaki ^b   Nishida, Keigo ^d   Kidoya, Hiroyasu ^e   Sonobe, Takashi ^f   Naito, Hisamichi ^e   Arita, Yoh ^a   Hashimoto, Takahiro ^a   Kuroda, Tadashi ^a   Fujio, Yasushi ^h   Shirai, Mikiyasu ^f   Takakura, Nobuyuki ^e   Morishita, Ryuichi ^b   Yamauchi Takihara, Keiko ^a   Kodama, Tatsuhiko ^a,c   Hirano, Toshio ^d,i,j   Mochizuki, Naoki ^g   Komuro, Issei ^a   more..

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b Department of Clinical Gene Therapy ^*  (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d Institute of Physical and Chemical Research   (Japan)

^e OSAKA UNIVERSITY   (Japan)

^f Departments of Cardiac Physiology   (Japan)

^g NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^h OSAKA UNIVERSITY   (Japan)

ⁱ JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^j OSAKA UNIVERSITY   (Japan)

more..

Author keywords

angiogenesis; endothelial cells; Gab1; growth factors; signal transduction

Indexed keywords

BINDING PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; GRB2 ASSOCIATED BINDER 1 PROTEIN; GRB2 ASSOCIATED BINDER 2 PROTEIN; KRUPPEL LIKE FACTOR 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 7; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE P85; PROTEIN TYROSINE PHOSPHATASE SHP 2; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE EXPRESSION; GENE TRANSFER; HINDLIMB; HUMAN; HUMAN CELL; ISCHEMIA; LIMB BLOOD FLOW; LIMB ISCHEMIA; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TISSUE NECROSIS; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION;

ANIMALS; ANIMALS, NEWBORN; ARTERIES; CARRIER PROTEINS; CLASS IA PHOSPHATIDYLINOSITOL 3-KINASE; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION; HEPATOCYTE GROWTH FACTOR; HINDLIMB; HUMANS; ISCHEMIA; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHOPROTEINS; PHOSPHORYLATION; REGIONAL BLOOD FLOW; SH2 DOMAIN-CONTAINING PROTEIN TYROSINE PHOSPHATASES; SIGNAL TRANSDUCTION; TYROSINE;

EID: 79953063307     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.232223     Document Type: Article

References (40)

1. Gu H, Neel BG. The "Gab" in signal transduction. Trends Cell Biol. 2003;13:122-130.
2. Wohrle FU, Daly RJ, Brummer T. Function, regulation and pathological roles of the Gab/DOS docking proteins. Cell Commun Signal. 2009;7:22.
3. Itoh M, Yoshida Y, Nishida K, Narimatsu M, Hibi M, Hirano T. Role of Gab1 in heart, placenta, and skin development and growth factor-and cytokine-induced extracellular signal-regulated kinase mitogen-activated protein kinase activation. Mol Cell Biol. 2000;20: 3695-3704. (Pubitemid 30243915)
4. Sachs M, Brohmann H, Zechner D, Muller T, Hulsken J, Walther I, Schaeper U, Birchmeier C, Birchmeier W. Essential role of Gab1 for signaling by the c-Met receptor in vivo. J Cell Biol. 2000;150: 1375-1384.
5. Gu H, Saito K, Klaman LD, Shen J, Fleming T, Wang Y, Pratt JC, Lin G, Lim B, Kinet JP, Neel BG. Essential role for Gab2 in the allergic response. Nature. 2001;412:186-190. (Pubitemid 32674715)
6. Wada T, Nakashima T, Oliveira-dos-Santos AJ, Gasser J, Hara H, Schett G, Penninger JM. The molecular scaffold Gab2 is a crucial component of RANK signaling and osteoclastogenesis. Nat Med. 2005;11:394-399. (Pubitemid 40562329)
7. Zhang Y, Diaz-Flores E, Li G, Wang Z, Kang Z, Haviernikova E, Rowe S, Qu CK, Tse W, Shannon KM, Bunting KD. Abnormal hematopoiesis in Gab2 mutant mice. Blood. 2007;110:116-124. (Pubitemid 47026826)
8. Seiffert M, Custodio JM, Wolf I, Harkey M, Liu Y, Blattman JN, Greenberg PD, Rohrschneider LR. Gab3-deficient mice exhibit normal development and hematopoiesis and are immunocompetent. Mol Cell Biol. 2003;23:2415-2424. (Pubitemid 36351023)
9. Bard-Chapeau EA, Yuan J, Droin N, Long S, Zhang EE, Nguyen TV, Feng GS. Concerted functions of Gab1 and Shp2 in liver regeneration and hepatoprotection. Mol Cell Biol. 2006;26:4664-4674. (Pubitemid 43877583)
10. Bard-Chapeau EA, Hevener AL, Long S, Zhang EE, Olefsky JM, Feng GS. Deletion of Gab1 in the liver leads to enhanced glucose tolerance and improved hepatic insulin action. Nat Med. 2005;11:567-571. (Pubitemid 40685981)
11. Nakaoka Y, Nishida K, Narimatsu M, Kamiya A, Minami T, Sawa H, Okawa K, Fujio Y, Koyama T, Maeda M, Sone M, Yamasaki S, Arai Y, Koh GY, Kodama T, Hirota H, Otsu K, Hirano T, Mochizuki N. Gab family proteins are essential for postnatal maintenance of cardiac function via neuregulin-1/ErbB signaling. J Clin Invest. 2007;117: 1771-1781. (Pubitemid 47036311)
12. Weng T, Mao F, Wang Y, Sun Q, Li R, Yang G, Zhang X, Luo J, Feng GS, Yang X. Osteoblastic molecular scaffold Gab1 is required for maintaining bone homeostasis. J Cell Sci. 2010;123:682-689.
13. Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003;9: 653-660. (Pubitemid 36749213)
14. Adams RH, Alitalo K. Molecular regulation of angiogenesis and lymp-hangiogenesis. Nat Rev Mol Cell Biol. 2007;8:464-478.
15. Mochizuki N. Vascular integrity mediated by vascular endothelial cadherin and regulated by sphingosine 1-phosphate and angiopoietin-1. Circ J. 2009;73:2183-2191.
16. Atkins GB, Jain MK. Role of Kruppel-like transcription factors in endo-thelial biology. Circ Res. 2007;100:1686-1695. (Pubitemid 46987860)
17. Parmar KM, Larman HB, Dai G, Zhang Y, Wang ET, Moorthy SN, Kratz JR, Lin Z, Jain MK, Gimbrone MA Jr, Garcia-Cardena G. Integration of flow-dependent endothelial phenotypes by Kruppel-like factor 2. J Clin Invest. 2006;116:49-58. (Pubitemid 43121790)
18. Nakaoka Y, Nishida K, Fujio Y, Izumi M, Terai K, Oshima Y, Sugiyama S, Matsuda S, Koyasu S, Yamauchi-Takihara K, Hirano T, Kawase I, Hirota H. Activation of gp130 transduces hypertrophic signal through interaction of scaffolding/docking protein Gab1 with tyrosine phosphatase SHP2 in cardiomyocytes. Circ Res. 2003;93: 221-229. (Pubitemid 36993233)
19. Nakaoka Y, Shioyama W, Kunimoto S, Arita Y, Higuchi K, Yamamoto K, Fujio Y, Nishida K, Kuroda T, Hirota H, Yamauchi-Takihara K, Hirano T, Komuro I, Mochizuki N. SHP2 mediates gp130-dependent cardiomyocyte hypertrophy via negative regulation of skeletal alpha-actin gene. J Mol Cell Cardiol. 2010;49:157-164.
20. Caron C, Spring K, Laramee M, Chabot C, Cloutier M, Gu H, Royal I. Non-redundant roles of the Gab1 and Gab2 scaffolding adapters in VEGF-mediated signalling, migration, and survival of endothelial cells. Cell Signal. 2009;21:943-953.
21. Dance M, Montagner A, Yart A, Masri B, Audigier Y, Perret B, Salles JP, Raynal P. The adaptor protein Gab1 couples the stimulation of vascular endothelial growth factor receptor-2 to the activation of phosphoinositide 3-kinase. J Biol Chem. 2006;281:23285-23295.
22. Laramee M, Chabot C, Cloutier M, Stenne R, Holgado-Madruga M, Wong AJ, Royal I. The scaffolding adapter Gab1 mediates vascular endothelial growth factor signaling and is required for endothelial cell migration and capillary formation. J Biol Chem. 2007;282:7758-7769. (Pubitemid 47093597)
23. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA, Yanagisawa M. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev Biol. 2001;230:230-242. (Pubitemid 32171420)
24. Koyama T, Nakaoka Y, Fujio Y, Hirota H, Nishida K, Sugiyama S, Okamoto K, Yamauchi-Takihara K, Yoshimura M, Mochizuki S, Hori M, Hirano T, Mochizuki N. Interaction of scaffolding adaptor protein Gab1 with tyrosine phosphatase SHP2 negatively regulates IGF-I-dependent myogenic differentiation via the ERK1/2 signaling pathway. J Biol Chem. 2008;283:24234-24244.
25. Fahmy RG, Dass CR, Sun LQ, Chesterman CN, Khachigian LM. Transcription factor Egr-1 supports FGF-dependent angiogenesis during neovascularization and tumor growth. Nat Med. 2003;9: 1026-1032. (Pubitemid 37021782)
26. Khachigian LM. Early growth response-1 in cardiovascular pathobiology. Circ Res. 2006;98:186-191.
27. Lin Z, Kumar A, SenBanerjee S, Staniszewski K, Parmar K, Vaughan DE, Gimbrone MA Jr, Balasubramanian V, Garcia-Cardena G, Jain MK. Kruppel-like factor 2 (KLF2) regulates endothelial thrombotic function. Circ Res. 2005;96:e48-e57.
28. Meng S, Chen Z, Munoz-Antonia T, Wu J. Participation of both Gab1 and Gab2 in the activation of the ERK/MAPK pathway by epidermal growth factor. Biochem J. 2005;391:143-151. (Pubitemid 41445485)
29. Lock LS, Maroun CR, Naujokas MA, Park M. Distinct recruitment and function of Gab1 and Gab2 in Met receptor-mediated epithelial morphogenesis. Mol Biol Cell. 2002;13:2132-2146. (Pubitemid 34651497)
30. Maroun CR, Naujokas MA, Holgado-Madruga M, Wong AJ, Park M. The tyrosine phosphatase SHP-2 is required for sustained activation of extracellular signal-regulated kinase and epithelial morphogenesis downstream from the met receptor tyrosine kinase. Mol Cell Biol. 2000;20: 8513-8525.
31. Hayashi M, Kim SW, Imanaka-Yoshida K, Yoshida T, Abel ED, Eliceiri B, Yang Y, Ulevitch RJ, Lee JD. Targeted deletion of BMK1/ERK5 in adult mice perturbs vascular integrity and leads to endothelial failure. J Clin Invest. 2004;113:1138-1148. (Pubitemid 38544099)
32. Regan CP, Li W, Boucher DM, Spatz S, Su MS, Kuida K. Erk5 null mice display multiple extraembryonic vascular and embryonic cardiovascular defects. Proc Natl Acad Sci USA. 2002;99:9248-9253. (Pubitemid 34764599)
33. Sohn SJ, Sarvis BK, Cado D, Winoto A. ERK5 MAPK regulates embryonic angiogenesis and acts as a hypoxia-sensitive repressor of vascular endothelial growth factor expression. J Biol Chem. 2002;277: 43344-43351. (Pubitemid 35285722)
34. Nicoli S, Standley C, Walker P, Hurlstone A, Fogarty KE, Lawson ND. MicroRNA-mediated integration of haemodynamics and Vegf signalling during angiogenesis. Nature. 2010;464:1196-1200.
35. Bladt F, Riethmacher D, Isenmann S, Aguzzi A, Birchmeier C. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature. 1995;376:768-771.
36. Schmidt C, Bladt F, Goedecke S, Brinkmann V, Zschiesche W, Sharpe M, Gherardi E, Birchmeier C. Scatter factor/hepatocyte growth factor is essential for liver development. Nature. 1995;373:699-702.
37. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature. 1996;380:435-439. (Pubitemid 26102719)
38. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 1996;380:439-442. (Pubitemid 26102720)
39. Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothe-lium. Nature. 1995;376:66-70.
40. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 1995;376:62-66.