C-Cbl inhibits angiogenesis and tumor growth by suppressing activation of PLCγ1

Oncogene

Volumn 30, Issue 19, 2011, Pages 2198-2206

  Meyer, R D ^a   Husain, D ^a   Rahimi, N ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

angiogenesis; c Cbl; PLC gammal; ubiquitination; VEGFR 2

Indexed keywords

CBL PROTEIN; PHOSPHOLIPASE C GAMMA1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE INACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RETINA NEOVASCULARIZATION; TUMOR GROWTH; TUMOR VASCULARIZATION;

ANIMALS; CELL DIVISION; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; HUMANS; MICE; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHOLIPASE C GAMMA; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-CBL; SIGNAL TRANSDUCTION; TYROSINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

MUS;

EID: 79955811775     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.597     Document Type: Article

References (37)

1. Adams RH, Alitalo K. (2007). Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8: 464-478. (Pubitemid 46823443)
2. Fukumura D, Jain RK. (2007). Tumor microvasculature and microenvironment: Targets for anti-angiogenesis and normalization. Microvasc Res 74: 72-84. (Pubitemid 350051025)
3. Fang D, Liu Y-C. (2001). Proteolysis-independent regulation of PI3K by Cbl-b-mediated ubiquitination in T cells. Nat Immunol 2: 870-875.
4. Feshchenko EA, Langdon WY, Tsygankov AY. (1998). Fyn, Yes, and Syk phosphorylation sites in c-Cbl map to the same tyrosine residues that become phosphorylated in activated T cells. J Biol Chem 273: 8323-8331. (Pubitemid 28168891)
5. Folkman J. (1990). What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst 82: 4-6. (Pubitemid 20020880)
6. Funakoshi T, Birsner AE, D'Amato RJ. (2006). Antiangiogenic effect of oral 2-methoxyestradiol on choroidal neovascularization in mice. Exp Eye Res 83: 1102-1107. (Pubitemid 44397030)
7. Graham LJ, Stoica BA, Shapiro M, DeBell KE, Rellahan B, Laborda J et al. (1998). Sequences surrounding the Src-homology 3 domain of phospholipase C gamma-1 increase the domain's association with Cbl. Biochem Biophys Res Commun 249: 537-541. (Pubitemid 28431789)
8. Graham LJ, Veri M-C, DeBell KE, Noviello C, Rawat R, Jen S et al. (2003). 70Z/3 Cbl induces PLC gamma1 activation in T lymphocytes via an alternate Lat- and Slp-76-independent signaling mechanism. Oncogene 22: 2493-2503. (Pubitemid 36560732)
9. Hochstrasser M. (2009). Origin and function of ubiquitin-like proteins. Nature 458: 422-429.
10. Husain D, Meyer R, Mehta M, Pfeifer WM, Chou E, Navruzbekov G et al. (2010). Role of c-Cbl Dependent Regulation of Phospholipase C gamma 1 Activation in Experimental Choroidal Neovasculariza-tion. Invest Ophthalmol Vis Sci 51: 6803-6809.
11. Ji Q-S, Winnier GE, Niswender KD, Horstman D, Wisdom R, Magnusen MA et al. (1997). Essential role of the tyrosine kinase substrate phospholipase C-gamma1 inmammalian growth and development. Proc Natl Acad Sci USA 94: 2999-3003. (Pubitemid 27157253)
12. Lawson ND, Mugford JW, Diamond BA, Weinstein BM. (2003). phospholipase C gamma-1 is required downstream of vascular endothelial growth factor during arterial development. Genes Dev 17: 1346-1351. (Pubitemid 36666004)
13. Liao H-J, Kume T, McKay C, Xu M-J, Ihle JN, Carpenter G. (2002). Absence of erythrogenesis and vasculogenesis in Plc gamma-deficient mice. J Biol Chem 277: 9335-9341. (Pubitemid 34953017)
14. Meyer RD, Latz C, Rahimi N. (2003). Recruitment and activation of PLCg1 by vascular endothelial growth factor receptor-2 are required for tubulogenesis and differentiation of endothelial cells. J Biol Chem 278: 16347-16355. (Pubitemid 36799761)
15. Meyer RD, Sacks DB, Rahimi N. (2008). IQGAP1-dependent signaling pathway regulates endothelial cell proliferation and angiogenesis. PLoS One 3: e3848.
16. Meyer RD, Singh A, Majnoun F, Latz C, Lashkari K, Rahimi N. (2004). Substitution of C-terminus of VEGFR-2 with VEGFR-1 promotes VEGFR-1 activation and endothelial cell proliferation. Oncogene 23: 5523-5531. (Pubitemid 39044063)
17. Miura-Shimura Y, Duan L, Rao NL, Reddi AL, Shimura H, Rottapel R et al. (2003). Cbl-mediated ubiquitinylation and negative regulation of Vav. J Biol Chem 278: 38495-38504. (Pubitemid 37221744)
18. Miyazaki T, Sanjay A, Neff L, Tanaka S, Horne WC, Baron R. (2004). Src kinase activity is essential for osteoclast function. J Biol Chem 279: 17660-17666. (Pubitemid 38560531)
19. Murphy MA, Schnall RG, Venter DJ, Barnett L, Bertoncello I, Thien CB et al. (1998). Tissue hyperplasia and enhanced T-cell signalling via ZAP-70 in c-Cbl-deficient mice. Mol Cell Biol 18: 4872-4882. (Pubitemid 28343071)
20. Naramura M, Jang IK, Kole H, Huang F, Haines D, Gu H. (2002). c-Cbl and Cbl-b regulate T cell responsiveness by promoting ligand-induced TCR down-modulation. Nat Immunol 3: 1192-1199. (Pubitemid 35469704)
21. 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.
22. Rahimi N. (2006). VEGFR-1 and VEGFR-2: two non-identical twins with a unique physiognomy. Front Biosci 11: 818-829. (Pubitemid 43262905)
23. Rahimi N, Dayanir V, Lashkari K. (2000). Receptor chimeras indicate that the vascular endothelial growth factor receptor-1 (VEGFR-1) modulates mitogenic activity of VEGFR-2 in endothelial cells. J Biol Chem 275: 16986-16992. (Pubitemid 30398939)
24. Rahimi N, Golde TE, Meyer RD. (2009). Identification of ligand-induced proteolytic cleavage and ectodomain shedding of VEGFR-1/FLT1 in leukemic cancer cells. Cancer Res 69: 2607-2614.
25. Ravid T, Hochstrasser M. (2008). Diversity of degradation signals in the ubiquitin-proteasome system. Nat Rev Mol Cell Biol 9: 679-690.
26. Rebecchi MJ, Pentyala SN. (2000). Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol Rev 80: 1291-1335.
27. Sakurai Y, Ohgimoto K, Kataoka Y, Yoshida N, Shibuya M. (2005). Essential role of Flk-1 (VEGF receptor 2) tyrosine residue 1173 in vasculogenesis in mice. Proc Natl Acad Sci USA 102: 1076-1081. (Pubitemid 40170728)
28. Schwartz AL, Ciechanover A. (2009). Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. Annu Rev Pharmacol Toxicol 49: 73-79.
29. Singh AJ, Meyer RD, Band H, Rahimi N. (2005). The carboxyl terminus of VEGFR-2 is required for PKC-mediated downregula-tion. Mol Biol Cell 16: 2106-2118. (Pubitemid 40471975)
30. Singh AJ, Meyer RD, Navruzbekov G, Shelke R, Duan L, Band H et al. (2007). A critical role for the E3-ligase activity of c-Cbl in VEGFR-2-mediated PLCgamma1 activation and angiogenesis. Proc Natl Acad Sci USA 104: 5413-5418. (Pubitemid 47175694)
31. Swaminathan G, Tsygankov AY. (2006). The Cbl family proteins: ring leaders in regulation of cell signaling. J Cell Physiol 209: 21-43. (Pubitemid 44318665)
32. Takahashi T, Yamaguchi S, Chida K, Shibuya M. (2001). A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLCg1 and DNA synthesis in vascular endothelial cells. EMBO J 20: 2768-2778. (Pubitemid 32938560)
33. Teckchandani AM, Panetti TS, Tsygankov AY. (2005). c-Cbl regulates migration of v-Abl-transformed NIH 3T3 fibroblasts via Rac1. Exp Cell Res 307: 247-258. (Pubitemid 40732750)
34. Thien CBF, Langdon WY. (2005). c-Cbl and Cbl-b ubiquitin ligases: substrate diversity and negative regulation of signaling responses. Biochem J 391: 153-165.
35. Woodman SE, Ashton AW, Schubert W, Lee H, Williams TM, Medina FA et al. (2003). Caveolin-1 knockout mice show an impaired angiogenic response to exogenous stimuli. Am J Pathol 162: 2059-2068. (Pubitemid 36613061)
36. Zeng H, Qin L, Zhao D, Tan X, Manseau EJ, Van Hoang M et al. (2006). Orphan nuclear receptor TR3/Nur77 regulates VEGF-A-induced angiogenesis through its transcriptional activity. J Exp Med 203: 719-729.
37. Zhang H, He Y, Dai S, Xu Z, Luo Y, Wan T et al. (2008). AIP1 functions as an endogenous inhibitor of VEGFR2-mediated signaling and inflammatory angiogenesis in mice. J Clin Invest 118: 3904-3916.