Key role of PI3Kγ in monocyte chemotactic protein-1-mediated amplification of PDGF-induced aortic smooth muscle cell migration

British Journal of Pharmacology

Volumn 166, Issue 5, 2012, Pages 1643-1653

  Fougerat, A ^a   Smirnova, N F ^a   Gayral, S ^a   Malet, N ^a   Hirsch, E ^b   Wymann, M P ^c   Perret, B ^a   Martinez, L O ^a   Douillon, M ^a   Laffargue, M ^a  

^a Université de Toulouse   (France)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

aortic smooth muscle cells; chemokines; migration; PI3K ; platelet derived growth factor

Indexed keywords

CHEMOKINE RECEPTOR CCR2; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN KINASE B;

ANIMAL CELL; AORTA; ARTICLE; AUTOCRINE EFFECT; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER;

ANIMALS; AORTA, THORACIC; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CCL2; CLASS IB PHOSPHATIDYLINOSITOL 3-KINASE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCYTES, SMOOTH MUSCLE; PLATELET-DERIVED GROWTH FACTOR; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, CCR2; RECOMBINANT PROTEINS; SWINE;

EID: 84862741643     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2012.01866.x     Document Type: Article

References (53)

1. Baudhuin LM, Jiang Y, Zaslavsky A, Ishii I, Chun J, Xu Y, (2004). S1P3-mediated Akt activation and cross-talk with platelet-derived growth factor receptor (PDGFR). FASEB J 18: 341-343.
2. Biswas P, Delfanti F, Bernasconi S, Mengozzi M, Cota M, Polentarutti N, et al,. (1998). Interleukin-6 induces monocyte chemotactic protein-1 in peripheral blood mononuclear cells and in the U937 cell line. Blood 91: 258-265.
3. Bogdanov VY, Poon M, Taubman MB, (1998). Platelet-derived growth factor-specific regulation of the JE promoter in rat aortic smooth muscle cells. J Biol Chem 273: 24932-24938.
4. Bondeva T, Pirola L, Bulgarelli-Leva G, Rubio I, Wetzker R, Wymann MP, (1998). Bifurcation of lipid and protein kinase signals of PI3Kgamma to the protein kinases PKB and MAPK. Science 282: 293-296.
5. Boring L, Gosling J, Cleary M, Charo IF, (1998). Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 394: 894-897.
6. Ciraolo E, Iezzi M, Marone R, Marengo S, Curcio C, Costa C, et al,. (2008). Phosphoinositide 3-kinase p110beta activity: key role in metabolism and mammary gland cancer but not development. Sci Signal 1: ra3.
7. Condliffe AM, Davidson K, Anderson KE, Ellson CD, Crabbe T, Okkenhaug K, et al,. (2005). Sequential activation of class IB and class IA PI3K is important for the primed respiratory burst of human but not murine neutrophils. Blood 106: 1432-1440.
8. Del Prete A, Vermi W, Dander E, Otero K, Barberis L, Luini W, et al,. (2004). Defective dendritic cell migration and activation of adaptive immunity in PI3Kgamma-deficient mice. EMBO J 23: 3505-3515.
9. Denger S, Jahn L, Wende P, Watson L, Gerber SH, Kubler W, et al,. (1999). Expression of monocyte chemoattractant protein-1 cDNA in vascular smooth muscle cells: induction of the synthetic phenotype: a possible clue to SMC differentiation in the process of atherogenesis. Atherosclerosis 144: 15-23.
10. Egashira K, Zhao Q, Kataoka C, Ohtani K, Usui M, Charo IF, et al,. (2002). Importance of monocyte chemoattractant protein-1 pathway in neointimal hyperplasia after periarterial injury in mice and monkeys. Circ Res 90: 1167-1172.
11. Fernandez-Hernando C, Jozsef L, Jenkins D, Di Lorenzo A, Sessa WC, (2009). Absence of Akt1 reduces vascular smooth muscle cell migration and survival and induces features of plaque vulnerability and cardiac dysfunction during atherosclerosis. Arterioscler Thromb Vasc Biol 29: 2033-2040.
12. Force T, Kyriakis JM, Avruch J, Bonventre JV, (1991). Endothelin, vasopressin, and angiotensin II enhance tyrosine phosphorylation by protein kinase C-dependent and -independent pathways in glomerular mesangial cells. J Biol Chem 266: 6650-6656.
13. Fougerat A, Gayral S, Gourdy P, Schambourg A, Ruckle T, Schwarz MK, et al,. (2008). Genetic and pharmacological targeting of phosphoinositide 3-kinase-gamma reduces atherosclerosis and favors plaque stability by modulating inflammatory processes. Circulation 117: 1310-1317.
14. Goncharova EA, Ammit AJ, Irani C, Carroll RG, Eszterhas AJ, Panettieri RA, et al,. (2002). PI3K is required for proliferation and migration of human pulmonary vascular smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 283: L354-L363.
15. Grassia G, Maddaluno M, Guglielmotti A, Mangano G, Biondi G, Maffia P, et al,. (2009). The anti-inflammatory agent bindarit inhibits neointima formation in both rats and hyperlipidaemic mice. Cardiovasc Res 84: 485-493.
16. Gu L, Okada Y, Clinton SK, Gerard C, Sukhova GK, Libby P, et al,. (1998). Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell 2: 275-281.
17. Guillermet-Guibert J, Bjorklof K, Salpekar A, Gonella C, Ramadani F, Bilancio A, et al,. (2008). The p110beta isoform of phosphoinositide 3-kinase signals downstream of G protein-coupled receptors and is functionally redundant with p110gamma. Proc Natl Acad Sci U S A 105: 8292-8297.
18. Guzman-Hernandez ML, Vazquez-Macias A, Carretero-Ortega J, Hernandez-Garcia R, Garcia-Regalado A, Hernandez-Negrete I, et al,. (2009). Differential inhibitor of Gbetagamma signaling to AKT and ERK derived from phosducin-like protein: effect on sphingosine 1-phosphate-induced endothelial cell migration and in vitro angiogenesis. J Biol Chem 284: 18334-18346.
19. Hannigan M, Zhan L, Li Z, Ai Y, Wu D, Huang CK, (2002). Neutrophils lacking phosphoinositide 3-kinase gamma show loss of directionality during N-formyl-Met-Leu-Phe-induced chemotaxis. Proc Natl Acad Sci U S A 99: 3603-3608.
20. Hayes IM, Jordan NJ, Towers S, Smith G, Paterson JR, Earnshaw JJ, et al,. (1998). Human vascular smooth muscle cells express receptors for CC chemokines. Arterioscler Thromb Vasc Biol 18: 397-403.
21. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B, (1998). A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A 95: 2509-2514.
22. Heller R, Chang Q, Ehrlich G, Hsieh SN, Schoenwaelder SM, Kuhlencordt PJ, et al,. (2008). Overlapping and distinct roles for PI3Kbeta and gamma isoforms in S1P-induced migration of human and mouse endothelial cells. Cardiovasc Res 80: 96-105.
23. Hirsch E, Katanaev VL, Garlanda C, Azzolino O, Pirola L, Silengo L, et al,. (2000). Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation. Science 287: 1049-1053.
24. Horvath C, Welt FG, Nedelman M, Rao P, Rogers C, (2002). Targeting CCR2 or CD18 inhibits experimental in-stent restenosis in primates: inhibitory potential depends on type of injury and leukocytes targeted. Circ Res 90: 488-494.
25. Hsieh HL, Tung WH, Wu CY, Wang HH, Lin CC, Wang TS, et al,. (2009). Thrombin induces EGF receptor expression and cell proliferation via a PKC(delta)/c-Src-dependent pathway in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 29: 1594-1601.
26. Irani C, Goncharova EA, Hunter DS, Walker CL, Panettieri RA, Krymskaya VP, (2002). Phosphatidylinositol 3-kinase but not tuberin is required for PDGF-induced cell migration. Am J Physiol Lung Cell Mol Physiol 282: L854-L862.
27. Jia S, Liu Z, Zhang S, Liu P, Zhang L, Lee SH, et al,. (2008). Essential roles of PI(3)K-p110beta in cell growth, metabolism and tumorigenesis. Nature 454: 776-779.
28. Jones GE, Prigmore E, Calvez R, Hogan C, Dunn GA, Hirsch E, et al,. (2003). Requirement for PI 3-kinase gamma in macrophage migration to MCP-1 and CSF-1. Exp Cell Res 290: 120-131.
29. Kalmes A, Daum G, Clowes AW, (2001). EGFR transactivation in the regulation of SMC function. Ann N Y Acad Sci 947: 42-54; discussion 54-45.
30. Kranzhofer R, Clinton SK, Ishii K, Coughlin SR, Fenton JW 2nd, Libby P, (1996). Thrombin potently stimulates cytokine production in human vascular smooth muscle cells but not in mononuclear phagocytes. Circ Res 79: 286-294.
31. Laffargue M, Raynal P, Yart A, Peres C, Wetzker R, Roche S, et al,. (1999). An epidermal growth factor receptor/Gab1 signaling pathway is required for activation of phosphoinositide 3-kinase by lysophosphatidic acid. J Biol Chem 274: 32835-32841.
32. Leeb-Lundberg LM, Song XH, (1991). Bradykinin and bombesin rapidly stimulate tyrosine phosphorylation of a 120-kDa group of proteins in Swiss 3T3 cells. J Biol Chem 266: 7746-7749.
33. Liu B, Poon M, Taubman MB, (2006). PDGF-BB enhances monocyte chemoattractant protein-1 mRNA stability in smooth muscle cells by downregulating ribonuclease activity. J Mol Cell Cardiol 41: 160-169.
34. Ma J, Wang Q, Fei T, Han JD, Chen YG, (2007). MCP-1 mediates TGF-beta-induced angiogenesis by stimulating vascular smooth muscle cell migration. Blood 109: 987-994.
35. Mehrhof FB, Schmidt-Ullrich R, Dietz R, Scheidereit C, (2005). Regulation of vascular smooth muscle cell proliferation: role of NF-kappaB revisited. Circ Res 96: 958-964.
36. Mori E, Komori K, Yamaoka T, Tanii M, Kataoka C, Takeshita A, et al,. (2002). Essential role of monocyte chemoattractant protein-1 in development of restenotic changes (neointimal hyperplasia and constrictive remodeling) after balloon angioplasty in hypercholesterolemic rabbits. Circulation 105: 2905-2910.
37. Orr AW, Hastings NE, Blackman BR, Wamhoff BR, (2009). Complex regulation and function of the inflammatory smooth muscle cell phenotype in atherosclerosis. J Vasc Res 47: 168-180.
38. Patrucco E, Notte A, Barberis L, Selvetella G, Maffei A, Brancaccio M, et al,. (2004). PI3Kgamma modulates the cardiac response to chronic pressure overload by distinct kinase-dependent and -independent effects. Cell 118: 375-387.
39. Poon M, Hsu WC, Bogdanov VY, Taubman MB, (1996). Secretion of monocyte chemotactic activity by cultured rat aortic smooth muscle cells in response to PDGF is due predominantly to the induction of JE/MCP-1. Am J Pathol 149: 307-317.
40. Radhakrishnan Y, Maile LA, Ling Y, Graves LM, Clemmons DR, (2008). Insulin-like growth factor-I stimulates Shc-dependent phosphatidylinositol 3-kinase activation via Grb2-associated p85 in vascular smooth muscle cells. J Biol Chem 283: 16320-16331.
41. Rott D, Zhu J, Zhou YF, Burnett MS, Zalles-Ganley A, Epstein SE, (2003). IL-6 is produced by splenocytes derived from CMV-infected mice in response to CMV antigens, and induces MCP-1 production by endothelial cells: a new mechanistic paradigm for infection-induced atherogenesis. Atherosclerosis 170: 223-228.
42. Sako H, Miura S, Iwata A, Nishikawa H, Kawamura A, Matsuo K, et al,. (2008). Changes in CCR2 chemokine receptor expression and plasma MCP-1 concentration after the implantation of bare metal stents versus sirolimus-eluting stents in patients with stable angina. Intern Med 47: 7-13.
43. Spinetti G, Wang M, Monticone R, Zhang J, Zhao D, Lakatta EG, (2004). Rat aortic MCP-1 and its receptor CCR2 increase with age and alter vascular smooth muscle cell function. Arterioscler Thromb Vasc Biol 24: 1397-1402.
44. Tanimoto T, Lungu AO, Berk BC, (2004). Sphingosine 1-phosphate transactivates the platelet-derived growth factor beta receptor and epidermal growth factor receptor in vascular smooth muscle cells. Circ Res 94: 1050-1058.
45. Taubman MB, Rollins BJ, Poon M, Marmur J, Green RS, Berk BC, et al,. (1992). JE mRNA accumulates rapidly in aortic injury and in platelet-derived growth factor-stimulated vascular smooth muscle cells. Circ Res 70: 314-325.
46. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, et al,. (2001). Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 70: 535-602.
47. Vecchione C, Patrucco E, Marino G, Barberis L, Poulet R, Aretini A, et al,. (2005). Protection from angiotensin II-mediated vasculotoxic and hypertensive response in mice lacking PI3Kgamma. J Exp Med 201: 1217-1228.
48. Voisin L, Foisy S, Giasson E, Lambert C, Moreau P, Meloche S, (2002). EGF receptor transactivation is obligatory for protein synthesis stimulation by G protein-coupled receptors. Am J Physiol Cell Physiol 283: C446-C455.
49. Wymann MP, Zvelebil M, Laffargue M, (2003). Phosphoinositide 3-kinase signalling-which way to target? Trends Pharmacol Sci 24: 366-376.
50. Wysocki SJ, Zheng MH, Smith A, Lamawansa MD, Iacopetta BJ, Robertson TA, et al,. (1996). Monocyte chemoattractant protein-1 gene expression in injured pig artery coincides with early appearance of infiltrating monocyte/macrophages. J Cell Biochem 62: 303-313.
51. Zargham R, (2008). Preventing restenosis after angioplasty: a multistage approach. Clin Sci (Lond) 114: 257-264.
52. Zhong L, Chen WQ, Ji XP, Zhang M, Zhao YX, Yao GH, et al,. (2008). Dominant-negative mutation of monocyte chemoattractant protein-1 prevents vulnerable plaques from rupture in rabbits independent of serum lipid levels. J Cell Mol Med 12: 2362-2371.
53. Zhou L, Takayama Y, Boucher P, Tallquist MD, Herz J, (2009). LRP1 regulates architecture of the vascular wall by controlling PDGFRbeta-dependent phosphatidylinositol 3-kinase activation. PLoS One 4: e6922.