Axl is essential for VEGF-A-dependent activation of PI3K/Akt

EMBO Journal

Volumn 31, Issue 7, 2012, Pages 1692-1703

  Ruan, Guo Xiang ^a   Kazlauskas, Andrius ^a  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

Author keywords

Angiogenesis; Axl; PI3K; VEGF A; VEGFR 2

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN AXL; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ARTICLE; BLOOD VESSEL PERMEABILITY; ENDOTHELIUM CELL; ENZYME ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS;

AMINO ACID MOTIFS; ANIMALS; CELL MOVEMENT; ENDOTHELIAL CELLS; FIBROBLAST GROWTH FACTOR 2; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

MUS;

EID: 84859432817     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.21     Document Type: Article

References (54)

1. Ackah E, Yu J, Zoellner S, Iwakiri Y, Skurk C, Shibata R, Ouchi N, Easton RM, Galasso G, Birnbaum MJ, Walsh K, Sessa WC (2005) Akt1/protein kinase Balpha is critical for ischemic and VEGFmediated angiogenesis. J Clin Invest 115: 2119-2127 (Pubitemid 41134153)
2. Braunger J, Schleithoff L, Schulz AS, Kessler H, Lammers R, Ullrich A, Bartram CR, Janssen JW (1997) Intracellular signaling of the Ufo/Axl receptor tyrosine kinase is mediated mainly by a multisubstrate docking-site. Oncogene 14: 2619-2631 (Pubitemid 27283101)
3. Brown DM, Kaiser PK, Michels M, Soubrane G, Heier JS, Kim RY, Sy JP, Schneider S (2006) Ranibizumab versus verteporfin for neovascular age-related macular degeneration. N Engl J Med 355: 1432-1444 (Pubitemid 44511558)
4. 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 (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439 (Pubitemid 26102719)
5. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H, Scholz D, Acker T, DiPalma T, Dewerchin M, Noel A, Stalmans I, Barra A, Blacher S, Vandendriessche T, Ponten A et al (2001) Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 7: 575-583 (Pubitemid 32448325)
6. Cross MJ, Dixelius J, Matsumoto T, Claesson-Welsh L (2003) VEGFreceptor signal transduction. Trends Biochem Sci 28: 488-494
7. Cully M, You H, Levine AJ, Mak TW (2006) Beyond PTEN mutations: the PI3K pathway as an integrator of multiple inputs during tumorigenesis. Nat Rev Cancer 6: 184-192 (Pubitemid 43292562)
8. Dance M, Montagner A, Yart A, Masri B, Audigier Y, Perret B, Salles JP, Raynal P (2006) The adaptor protein Gab1 couples the stimulation of vascular endothelial growth factor receptor-2 to the activation of phosphoinositide 3-kinase. J Biol Chem 281: 23285-23295
9. Eliceiri BP, Paul R, Schwartzberg PL, Hood JD, Leng J, Cheresh DA (1999) Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell 4: 915-924 (Pubitemid 30054898)
10. Ferrara N (2009) VEGF-A: a critical regulator of blood vessel growth. Eur Cytokine Netw 20: 158-163
11. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380: 439-442 (Pubitemid 26102720)
12. Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9: 669-676 (Pubitemid 36749215)
13. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16: 4604-4613 (Pubitemid 26272112)
14. Gallicchio M, Mitola S, Valdembri D, Fantozzi R, Varnum B, Avanzi GC, Bussolino F (2005) Inhibition of vascular endothelial growth factor receptor 2-mediated endothelial cell activation by Axl tyrosine kinase receptor. Blood 105: 1970-1976 (Pubitemid 40731780)
15. Holland SJ, Pan A, Franci C, Hu Y, Chang B, Li W, Duan M, Torneros A, Yu J, Heckrodt TJ, Zhang J, Ding P, Apatira A, Chua J, Brandt R, Pine P, Goff D, Singh R, Payan DG, Hitoshi Y (2010) R428, a selective small molecule inhibitor of Axl kinase, blocks tumor spread and prolongs survival in models of metastatic breast cancer. Cancer Res 70: 1544-1554
16. Holland SJ, Powell MJ, Franci C, Chan EW, Friera AM, Atchison RE, McLaughlin J, Swift SE, Pali ES, Yam G, Wong S, Lasaga J, Shen MR, Yu S, Xu W, Hitoshi Y, Bogenberger J, Nor JE, Payan DG, Lorens JB (2005) Multiple roles for the receptor tyrosine kinase axl in tumor formation. Cancer Res 65: 9294-9303 (Pubitemid 41507996)
17. Holmes K, Roberts OL, Thomas AM, Cross MJ (2007) Vascular endothelial growth factor receptor-2: structure, function, intracellular signalling and therapeutic inhibition. Cell Signal 19: 2003-2012 (Pubitemid 47354167)
18. Im E, Kazlauskas A (2006) Regulating angiogenesis at the level of PtdIns-4, 5-P2. EMBO J 25: 2075-2082
19. Im E, Kazlauskas A (2007) Src family kinases promote vessel stability by antagonizing the Rho/ROCK pathway. J Biol Chem 282: 29122-29129 (Pubitemid 350043365)
20. Im E, Motiejunaite R, Aranda J, Park EY, Federico L, Kim TI, Clair T, Stracke ML, Smyth S, Kazlauskas A (2010) Phospholipase Cgamma activation drives increased production of autotaxin in endothelial cells and lysophosphatidic acid-dependent regression. Mol Cell Biol 30: 2401-2410
21. Kazlauskas A, Cooper JA (1989) Autophosphorylation of the PDGF receptor in the kinase insert region regulates interactions with cell proteins. Cell 58: 1121-1133 (Pubitemid 19238189)
22. Kerbel RS (2008) Tumor angiogenesis. N Engl J Med 358: 2039-2049 (Pubitemid 351656458)
23. Klinghoffer RA, Duckworth B, Valius M, Cantley L, Kazlauskas A (1996) Platelet-derived growth factor-dependent activation of phosphatidylinositol 3-kinase is regulated by receptor binding of SH2-domain-containing proteins which influence Ras activity. Mol Cell Biol 16: 5905-5914 (Pubitemid 26315112)
24. Knock GA, Snetkov VA, Shaifta Y, Drndarski S, Ward JP, Aaronson PI (2008) Role of src-family kinases in hypoxic vasoconstriction of rat pulmonary artery. Cardiovasc Res 80: 453-462
25. Kypta RM, Goldberg Y, Ulug ET, Courtneidge SA (1990) Association between the PDGF receptor and members of the src family of tyrosine kinases. Cell 62: 481-492
26. Laramee M, Chabot C, Cloutier M, Stenne R, Holgado-Madruga M, Wong AJ, Royal I (2007) The scaffolding adapter Gab1 mediates vascular endothelial growth factor signaling and is required for endothelial cell migration and capillary formation. J Biol Chem 282: 7758-7769 (Pubitemid 47093597)
27. Li Y, Ye X, Tan C, Hongo JA, Zha J, Liu J, Kallop D, Ludlam MJ, Pei L (2009) Axl as a potential therapeutic target in cancer: role of Axl in tumor growth, metastasis and angiogenesis. Oncogene 28: 3442-3455
28. Lim YC, Luscinskas FW (2006) Isolation and culture of murine heart and lung endothelial cells for in vitro model systems. Methods Mol Biol 341: 141-154
29. Lu Q, Gore M, Zhang Q, Camenisch T, Boast S, Casagranda F, Lai C, Skinner MK, Klein R, Matsushima GK, Earp HS, Goff SP, Lemke G (1999) Tyro-3 family receptors are essential regulators of mammalian spermatogenesis. Nature 398: 723-728 (Pubitemid 29197652)
30. Manalo DJ, Rowan A, Lavoie T, Natarajan L, Kelly BD, Ye SQ, Garcia JG, Semenza GL (2005) Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105: 659-669 (Pubitemid 40070750)
31. Matsumoto T, Bohman S, Dixelius J, Berge T, Dimberg A, Magnusson P, Wang L, Wikner C, Qi JH, Wernstedt C, Wu J, Bruheim S, Mugishima H, Mukhopadhyay D, Spurkland A, Claesson-Welsh L (2005) VEGF receptor-2 Y951 signaling and a role for the adapter molecule TSAd in tumor angiogenesis. EMBO J 24: 2342-2353 (Pubitemid 41032586)
32. Matsumoto T, Claesson-Welsh L (2001) VEGF receptor signal transduction. Sci STKE 2001: re21
33. McCloskey P, Fridell YW, Attar E, Villa J, Jin Y, Varnum B, Liu ET (1997) GAS6 mediates adhesion of cells expressing the receptor tyrosine kinase Axl. J Biol Chem 272: 23285-23291 (Pubitemid 27392465)
34. Melaragno MG, Fridell YW, Berk BC (1999) The Gas6/Axl system: a novel regulator of vascular cell function. Trends Cardiovasc Med 9: 250-253
35. Miles AA, Miles EM (1952) Vascular reactions to histamine, histamine-liberator and leukotaxine in the skin of guinea-pigs. J Physiol 118: 228-257
36. Nishijima K, Ng YS, Zhong L, Bradley J, Schubert W, Jo N, Akita J, Samuelsson SJ, Robinson GS, Adamis AP, Shima DT (2007) Vascular endothelial growth factor-A is a survival factor for retinal neurons and a critical neuroprotectant during the adaptive response to ischemic injury. Am J Pathol 171: 53-67 (Pubitemid 47339226)
37. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L (2006) VEGF receptor signalling-in control of vascular function. Nat Rev Mol Cell Biol 7: 359-371
38. Ory DS, Neugeboren BA, Mulligan RC (1996) A stable humanderived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes. Proc Natl Acad Sci USA 93: 11400-11406 (Pubitemid 26347133)
39. Pandya NM, Dhalla NS, Santani DD (2006) Angiogenesis-a new target for future therapy. Vascul Pharmacol 44: 265-274
40. Phung TL, Ziv K, Dabydeen D, Eyiah-Mensah G, Riveros M, Perruzzi C, Sun J, Monahan-Earley RA, Shiojima I, Nagy JA, Lin MI, Walsh K, Dvorak AM, Briscoe DM, Neeman M, SessaWC, Dvorak HF, Benjamin LE (2006) Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 10: 159-170 (Pubitemid 44175906)
41. Qiao Y, Molina H, Pandey A, Zhang J, Cole PA (2006) Chemical rescue of a mutant enzyme in living cells. Science 311: 1293-1297 (Pubitemid 43334720)
42. Rahimi N (2006) VEGFR-1 and VEGFR-2: two non-identical twins with a unique physiognomy. Front Biosci 11: 818-829 (Pubitemid 43262905)
43. Rahimi N, Kazlauskas A (1999) A role for cadherin-5 in regulation of vascular endothelial growth factor receptor 2 activity in endothelial cells. Mol Biol Cell 10: 3401-3407 (Pubitemid 29489570)
44. Rodriguez LG, Wu X, Guan JL (2005) Wound-healing assay. Methods Mol Biol 294: 23-29
45. Rogers MS, Birsner AE, D'Amato RJ (2007) The mouse cornea micropocket angiogenesis assay. Nat Protoc 2: 2545-2550
46. Rohde CM, Schrum J, Lee AW (2004) A juxtamembrane tyrosine in the colony stimulating factor-1 receptor regulates ligand-induced Src association, receptor kinase function, and down-regulation. J Biol Chem 279: 43448-43461 (Pubitemid 39390644)
47. Rosenfeld PJ, Brown DM, Heier JS, Boyer DS, Kaiser PK, Chung CY, Kim RY (2006) Ranibizumab for neovascular age-related macular degeneration. N Engl J Med 355: 1419-1431 (Pubitemid 44511557)
48. Rothlin CV, Ghosh S, Zuniga EI, Oldstone MB, Lemke G (2007) TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 131: 1124-1136 (Pubitemid 350235020)
49. Six I, Kureishi Y, Luo Z, Walsh K (2002) Akt signaling mediates VEGF/VPF vascular permeability in vivo. FEBS Lett 532: 67-69 (Pubitemid 35375868)
50. Songyang Z, Carraway KLI, Eck MJ, Harrison SC, Feldman RA, Mohammadi M, Schlessinger J, Hubbard SR, Smith DP, Eng C, Lorenzo MJ, Ponder BAJ, Mayer BJ, Cantley LC (1995) Catalytic specificity of protein-tyrosine kinases is critical for selective signalling. Nature 373: 536-539
51. Varnum BC, Young C, Elliott G, Garcia A, Bartley TD, Fridell YW, Hunt RW, Trail G, Clogston C, Toso RJ, Yanagihara D, Bennett L, Sylber M, Merewether LA, Tseng A, Escobar E, Liu ET, Yamane HK (1995) Axl receptor tyrosine kinase stimulated by the vitamin K-dependent protein encoded by growth-arrest-specific gene 6. Nature 373: 623-626
52. Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, Heldin CH (1994) Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J Biol Chem 269: 26988-26995 (Pubitemid 24332901)
53. Whitehead JP, Clark SF, Urso B, James DE (2000) Signalling through the insulin receptor. Curr Opin Cell Biol 12: 222-228 (Pubitemid 30142570)
54. Wybenga-Groot LE, Baskin B, Ong SH, Tong J, Pawson T, Sicheri F (2001) Structural basis for autoinhibition of the Ephb2 receptor tyrosine kinase by the unphosphorylated juxtamembrane region. Cell 106: 745-757 (Pubitemid 32900665)