PI3K signaling in arterial diseases: Non redundant functions of the PI3K isoforms

Advances in Biological Regulation

Volumn 59, Issue , 2015, Pages 4-18

  Lupieri, Adrien ^a   Smirnova, Natalia ^a   Malet, Nicole ^a   Gayral, Stéphanie ^a   Laffargue, Muriel ^a  

^a UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

Atherosclerosis; Endothelial cells; Inflammation; Phosphoinositide 3 kinases; Restenosis; Smooth muscle cells

Indexed keywords

ISOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE;

ANIMAL; CARDIOVASCULAR DISEASE; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CARDIOVASCULAR DISEASES; HUMANS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION;

EID: 84942551306     PISSN: 22124926     EISSN: None     Source Type: Book Series    
DOI: 10.1016/j.jbior.2015.06.002     Document Type: Review

References (162)

1. Abedi H., Zachary I. Signalling mechanisms in the regulation of vascular cell migration. Cardiovasc. Res. 1995, 30:544-556.
2. Ait-Oufella H., Herbin O., Bouaziz J.D., Binder C.J., Uyttenhove C., Laurans L., et al. B cell depletion reduces the development of atherosclerosis in mice. J. Exp. Med. 2010, 207:1579-1587.
3. Ait-Oufella H., Salomon B.L., Potteaux S., Robertson A.K., Gourdy P., Zoll J., et al. Natural regulatory T cells control the development of atherosclerosis in mice. Nat. Med. 2006, 12:178-180.
4. Aki S., Yoshioka K., Okamoto Y., Takuwa N., Takuwa Y. Phosphatidylinositol 3-kinase class II alpha-isoform PI3K-C2alpha is required for transforming growth factor beta-induced Smad signaling in endothelial cells. J. Biol. Chem. 2015, 290:6086-6105.
5. Ali K., Bilancio A., Thomas M., Pearce W., Gilfillan A.M., Tkaczyk C., et al. Essential role for the p110delta phosphoinositide 3-kinase in the allergic response. Nature 2004, 431:1007-1011.
6. Ali K., Camps M., Pearce W.P., Ji H., Ruckle T., Kuehn N., et al. Isoform-specific functions of phosphoinositide 3-kinases: p110 delta but not p110 gamma promotes optimal allergic responses in vivo. J. Immunol. 2008, 180:2538-2544.
7. Ammirati E., Moroni F., Magnoni M., Camici P.G. The role of T and B cells in human atherosclerosis and atherothrombosis. Clin. Exp. Immunol. 2015, 179:173-187.
8. Anderson K.E., Boyle K.B., Davidson K., Chessa T.A., Kulkarni S., Jarvis G.E., et al. CD18-dependent activation of the neutrophil NADPH oxidase during phagocytosis of Escherichia coli or Staphylococcus aureus is regulated by class III but not class I or II PI3Ks. Blood 2008, 112:5202-5211.
9. Andreo U., Guo L., Chirieac D.V., Tuyama A.C., Montenont E., Brodsky J.L., et al. Insulin-stimulated degradation of apolipoprotein B100: roles of class II phosphatidylinositol-3-kinase and autophagy. PLoS One 2013, 8:e57590.
10. Anzinger J.J., Chang J., Xu Q., Barthwal M.K., Bohnacker T., Wymann M.P., et al. Murine bone marrow-derived macrophages differentiated with GM-CSF become foam cells by PI3Kgamma-dependent fluid-phase pinocytosis of native LDL. J. Lipid Res. 2012, 53:34-42.
11. Asahara T., Bauters C., Pastore C., Kearney M., Rossow S., Bunting S., et al. Local delivery of vascular endothelial growth factor accelerates reendothelialization and attenuates intimal hyperplasia in balloon-injured rat carotid artery. Circulation 1995, 91:2793-2801.
12. Azam M.A., Yoshioka K., Ohkura S., Takuwa N., Sugimoto N., Sato K., et al. Ca2+-independent, inhibitory effects of cyclic adenosine 5'-monophosphate on Ca2+ regulation of phosphoinositide 3-kinase C2alpha, Rho, and myosin phosphatase in vascular smooth muscle. J. Pharmacol. Exp. Ther. 2007, 320:907-916.
13. Beer-Hammer S., Zebedin E., von Holleben M., Alferink J., Reis B., Dresing P., et al. The catalytic PI3K isoforms p110gamma and p110delta contribute to B cell development and maintenance, transformation, and proliferation. J. Leukoc. Biol. 2010, 87:1083-1095.
14. Bergamini G., Bell K., Shimamura S., Werner T., Cansfield A., Muller K., et al. A selective inhibitor reveals PI3Kgamma dependence of T(H)17 cell differentiation. Nat. Chem. Biol. 2012, 8:737.
15. Berger S.B., Romero X., Ma C., Wang G., Faubion W.A., Liao G., et al. SLAM is a microbial sensor that regulates bacterial phagosome functions in macrophages. Nat. Immunol. 2010, 11:920-927.
16. Biswas K., Yoshioka K., Asanuma K., Okamoto Y., Takuwa N., Sasaki T., et al. Essential role of class II phosphatidylinositol-3-kinase-C2alpha in sphingosine 1-phosphate receptor-1-mediated signaling and migration in endothelial cells. J. Biol. Chem. 2013, 288:2325-2339.
17. Boyle D.L., Kim H.R., Topolewski K., Bartok B., Firestein G.S. Novel phosphoinositide 3-kinase delta,gamma inhibitor: potent anti-inflammatory effects and joint protection in models of rheumatoid arthritis. J. Pharmacol. Exp. Ther. 2014, 348:271-280.
18. Braun-Dullaeus R.C., Mann M.J., Seay U., Zhang L., von Der Leyen H.E., Morris R.E., et al. Cell cycle protein expression in vascular smooth muscle cells in vitro and in vivo is regulated through phosphatidylinositol 3-kinase and mammalian target of rapamycin. Arterioscler. Thromb. Vasc. Biol. 2001, 21:1152-1158.
19. Burke J.E., Williams R.L. Dynamic steps in receptor tyrosine kinase mediated activation of class IA phosphoinositide 3-kinases (PI3K) captured by H/D exchange (HDX-MS). Adv. Biol. Regul. 2013, 53:97-110.
20. Cai X., Srivastava S., Sun Y., Li Z., Wu H., Zuvela-Jelaska L., et al. Tripartite motif containing protein 27 negatively regulates CD4 T cells by ubiquitinating and inhibiting the class II PI3K-C2beta. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:20072-20077.
21. Cain R.J., Vanhaesebroeck B., Ridley A.J. The PI3K p110alpha isoform regulates endothelial adherens junctions via Pyk2 and Rac1. J. Cell Biol. 2010, 188:863-876.
22. Caligiuri G., Nicoletti A., Poirier B., Hansson G.K. Protective immunity against atherosclerosis carried by B cells of hypercholesterolemic mice. J. Clin. Investig. 2002, 109:745-753.
23. Canobbio I., Stefanini L., Cipolla L., Ciraolo E., Gruppi C., Balduini C., et al. Genetic evidence for a predominant role of PI3Kbeta catalytic activity in ITAM- and integrin-mediated signaling in platelets. Blood 2009, 114:2193-2196.
24. Chaabane C., Otsuka F., Virmani R., Bochaton-Piallat M.L. Biological responses in stented arteries. Cardiovasc. Res. 2013, 99:353-363.
25. Chang J.D., Sukhova G.K., Libby P., Schvartz E., Lichtenstein A.H., Field S.J., et al. Deletion of the phosphoinositide 3-kinase p110gamma gene attenuates murine atherosclerosis. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:8077-8082.
26. Chavakis E., Carmona G., Urbich C., Gottig S., Henschler R., Penninger J.M., et al. Phosphatidylinositol-3-kinase-gamma is integral to homing functions of progenitor cells. Circ. Res. 2008, 102:942-949.
27. Ciraolo E., Iezzi M., Marone R., Marengo S., Curcio C., Costa C., et al. Phosphoinositide 3-kinase p110beta activity: key role in metabolism and mammary gland cancer but not development. Sci. Signal. 2008, 1:ra3.
28. Clayton E., Bardi G., Bell S.E., Chantry D., Downes C.P., Gray A., et al. A crucial role for the p110delta subunit of phosphatidylinositol 3-kinase in B cell development and activation. J. Exp. Med. 2002, 196:753-763.
29. Collmann E., Bohnacker T., Marone R., Dawson J., Rehberg M., Stringer R., et al. Transient targeting of phosphoinositide 3-kinase acts as a roadblock in mast cells' route to allergy. J. Allergy Clin. Immunol. 2013, 132:959-968.
30. Cosemans J.M., Munnix I.C., Wetzker R., Heller R., Jackson S.P., Heemskerk J.W. Continuous signaling via PI3K isoforms beta and gamma is required for platelet ADP receptor function in dynamic thrombus stabilization. Blood 2006, 108:3045-3052.
31. De Meyer G.R., Grootaert M.O., Michiels C.F., Kurdi A., Schrijvers D.M., Martinet W. Autophagy in vascular disease. Circ. Res. 2015, 116:468-479.
32. Diaz-Munoz M.D., Osma-Garcia I.C., Iniguez M.A., Fresno M. Cyclooxygenase-2 deficiency in macrophages leads to defective p110gamma PI3K signaling and impairs cell adhesion and migration. J. Immunol. 2013, 191:395-406.
33. Dimmeler S., Aicher A., Vasa M., Mildner-Rihm C., Adler K., Tiemann M., et al. HMG-CoA reductase inhibitors (statins) increase endothelial progenitor cells via the PI 3-kinase/Akt pathway. J. Clin. Investig. 2001, 108:391-397.
34. Dimmeler S., Fleming I., Fisslthaler B., Hermann C., Busse R., Zeiher A.M. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999, 399:601-605.
35. Doukas J., Eide L., Stebbins K., Racanelli-Layton A., Dellamary L., Martin M., et al. Aerosolized phosphoinositide 3-kinase gamma/delta inhibitor TG100-115 [3-[2,4-diamino-6-(3-hydroxyphenyl)pteridin-7-yl]phenol] as a therapeutic candidate for asthma and chronic obstructive pulmonary disease. J. Pharmacol. Exp. Ther. 2009, 328:758-765.
36. Durand C.A., Hartvigsen K., Fogelstrand L., Kim S., Iritani S., Vanhaesebroeck B., et al. Phosphoinositide 3-kinase p110 delta regulates natural antibody production, marginal zone and B-1 B cell function, and autoantibody responses. J. Immunol. 2009, 183:5673-5684.
37. Dutra R.C., Cola M., Leite D.F., Bento A.F., Claudino R.F., Nascimento A.F., et al. Inhibitor of PI3Kgamma ameliorates TNBS-induced colitis in mice by affecting the functional activity of CD4+CD25+FoxP3+ regulatory T cells. Br. J. Pharmacol. 2011, 163:358-374.
38. Falasca M., Maffucci T. Regulation and cellular functions of class II phosphoinositide 3-kinases. Biochem. J. 2012, 443:587-601.
39. Fougerat A., Gayral S., Gourdy P., Schambourg A., Ruckle T., Schwarz M.K., et al. Genetic and pharmacological targeting of phosphoinositide 3-kinase-gamma reduces atherosclerosis and favors plaque stability by modulating inflammatory processes. Circulation 2008, 117:1310-1317.
40. Fougerat A., Smirnova N., Gayral S., Malet N., Hirsch E., Wymann M., et al. Key role of PI3Kgamma in monocyte chemotactic protein-1-mediated amplification of PDGF-induced aortic smooth muscle cell migration. Br. J. Pharmacol. 2012, 166:1643-1653.
41. Franco I., Gulluni F., Campa C.C., Costa C., Margaria J.P., Ciraolo E., et al. PI3K class II alpha controls spatially restricted endosomal PtdIns3P and Rab11 activation to promote primary cilium function. Dev. Cell 2014, 28:647-658.
42. Frostegard J., Ulfgren A.K., Nyberg P., Hedin U., Swedenborg J., Andersson U., et al. Cytokine expression in advanced human atherosclerotic plaques: dominance of pro-inflammatory (Th1) and macrophage-stimulating cytokines. Atherosclerosis 1999, 145:33-43.
43. Fukao T., Koyasu S. PI3K and negative regulation of TLR signaling. Trends Immunol. 2003, 24:358-363.
44. Gaidarov I., Smith M.E., Domin J., Keen J.H. The class II phosphoinositide 3-kinase C2alpha is activated by clathrin and regulates clathrin-mediated membrane trafficking. Mol. Cell 2001, 7:443-449.
45. Gayral S., Garnotel R., Castaing-Berthou A., Blaise S., Fougerat A., Berge E., et al. Elastin-derived peptides potentiate atherosclerosis through the immune Neu1-PI3Kgamma pathway. Cardiovasc. Res. 2014, 102:118-127.
46. Ghigo A., Damilano F., Braccini L., Hirsch E. PI3K inhibition in inflammation: toward tailored therapies for specific diseases. Bioessays 2010, 32:185-196.
47. Gilio K., Munnix I.C., Mangin P., Cosemans J.M., Feijge M.A., van der Meijden P.E., et al. Non-redundant roles of phosphoinositide 3-kinase isoforms alpha and beta in glycoprotein VI-induced platelet signaling and thrombus formation. J. Biol. Chem. 2009, 284:33750-33762.
48. Gratacap M.P., Guillermet-Guibert J., Martin V., Chicanne G., Tronchere H., Gaits-Iacovoni F., et al. Regulation and roles of PI3Kbeta, a major actor in platelet signaling and functions. Adv. Enzyme Regul. 2011, 51:106-116.
49. Graupera M., Guillermet-Guibert J., Foukas L.C., Phng L.K., Cain R.J., Salpekar A., et al. Angiogenesis selectively requires the p110alpha isoform of PI3K to control endothelial cell migration. Nature 2008, 453:662-666.
50. Graupera M., Potente M. Regulation of angiogenesis by PI3K signaling networks. Exp. Cell Res. 2013, 319:1348-1355.
51. Gruen M., Rose C., Konig C., Gajda M., Wetzker R., Brauer R. Loss of phosphoinositide 3-kinase gamma decreases migration and activation of phagocytes but not T cell activation in antigen-induced arthritis. BMC Musculoskelet. Disord. 2010, 11:63.
52. Gu H., Saito K., Klaman L.D., Shen J., Fleming T., Wang Y., et al. Essential role for Gab2 in the allergic response. Nature 2001, 412:186-190.
53. Guha M., Mackman N. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J. Biol. Chem. 2002, 277:32124-32132.
54. Guidetti G.F., Torti M. The small GTPase Rap1b: a bidirectional regulator of platelet adhesion receptors. J. Signal Transduct. 2012, 2012:412089.
55. Guillermet-Guibert J., Bjorklof K., Salpekar A., Gonella C., Ramadani F., Bilancio A., et al. 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. 2008, 105:8292-8297.
56. Hafizi S., Chester A.H., Yacoub M.H. Molecular mechanisms of vascular smooth muscle cell growth. Curr. Opin. Cardiol. 1997, 12:495-503.
57. Hagensen M.K., Raarup M.K., Mortensen M.B., Thim T., Nyengaard J.R., Falk E., et al. Circulating endothelial progenitor cells do not contribute to regeneration of endothelium after murine arterial injury. Cardiovasc. Res. 2012, 93:223-231.
58. Hagensen M.K., Shim J., Thim T., Falk E., Bentzon J.F. Circulating endothelial progenitor cells do not contribute to plaque endothelium in murine atherosclerosis. Circulation 2010, 121:898-905.
59. Hansson G.K., Hermansson A. The immune system in atherosclerosis. Nat. Immunol. 2011, 12:204-212.
60. Harada K., Truong A.B., Cai T., Khavari P.A. The class II phosphoinositide 3-kinase C2beta is not essential for epidermal differentiation. Mol. Cell Biol. 2005, 25:11122-11130.
61. Harris D.P., Vogel P., Wims M., Moberg K., Humphries J., Jhaver K.G., et al. Requirement for class II phosphoinositide 3-kinase C2alpha in maintenance of glomerular structure and function. Mol. Cell Biol. 2011, 31:63-80.
62. Harris M.B., Ju H., Venema V.J., Liang H., Zou R., Michell B.J., et al. Reciprocal phosphorylation and regulation of endothelial nitric-oxide synthase in response to bradykinin stimulation. J. Biol. Chem. 2001, 276:16587-16591.
63. Harris S.J., Ciuclan L., Finan P.M., Wymann M.P., Walker C., Westwick J., et al. Genetic ablation of PI3Kgamma results in defective IL-17RA signalling in T lymphocytes and increased IL-17 levels. Eur. J. Immunol. 2012, 42:3394-3404.
64. Hawkins P.T., Stephens L.R. PI3K signalling in inflammation. Biochim. Biophys. Acta 2015, 1851:882-897.
65. Haylock-Jacobs S., Comerford I., Bunting M., Kara E., Townley S., Klingler-Hoffmann M., et al. PI3Kdelta drives the pathogenesis of experimental autoimmune encephalomyelitis by inhibiting effector T cell apoptosis and promoting Th17 differentiation. J. Autoimmun. 2011, 36:278-287.
66. Haynes M.P., Sinha D., Russell K.S., Collinge M., Fulton D., Morales-Ruiz M., et al. Membrane estrogen receptor engagement activates endothelial nitric oxide synthase via the PI3-kinase-Akt pathway in human endothelial cells. Circ. Res. 2000, 87:677-682.
67. Heller R., Chang Q., Ehrlich G., Hsieh S.N., Schoenwaelder S.M., Kuhlencordt P.J., et al. Overlapping and distinct roles for PI3Kbeta and gamma isoforms in S1P-induced migration of human and mouse endothelial cells. Cardiovasc. Res. 2008, 80:96-105.
68. Hers I. Insulin-like growth factor-1 potentiates platelet activation via the IRS/PI3Kalpha pathway. Blood 2007, 110:4243-4252.
69. Hirsch E., Bosco O., Tropel P., Laffargue M., Calvez R., Altruda F., et al. Resistance to thromboembolism in PI3Kgamma-deficient mice. FASEB J. 2001, 15:2019-2021.
70. Hirsch E., Katanaev V.L., Garlanda C., Azzolino O., Pirola L., Silengo L., et al. Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation. Science (New York, NY) 2000, 287:1049-1053.
71. Holy E.W., Jakob P., Eickner T., Camici G.G., Beer J.H., Akhmedov A., et al. PI3K/p110alpha inhibition selectively interferes with arterial thrombosis and neointima formation, but not re-endothelialization: potential implications for drug-eluting stent design. Eur. Heart J. 2014, 35:808-820.
72. Igarashi J., Michel T. Sphingosine 1-phosphate and isoform-specific activation of phosphoinositide 3-kinase beta. Evidence for divergence and convergence of receptor-regulated endothelial nitric-oxide synthase signaling pathways. J. Biol. Chem. 2001, 276:36281-36288.
73. Ii M., Takenaka H., Asai J., Ibusuki K., Mizukami Y., Maruyama K., et al. Endothelial progenitor thrombospondin-1 mediates diabetes-induced delay in reendothelialization following arterial injury. Circ. Res. 2006, 98:697-704.
74. Itoh Y., Toriumi H., Yamada S., Hoshino H., Suzuki N. Resident endothelial cells surrounding damaged arterial endothelium reendothelialize the lesion. Arterioscler. Thromb. Vasc. Biol. 2010, 30:1725-1732.
75. Iwakura A., Luedemann C., Shastry S., Hanley A., Kearney M., Aikawa R., et al. Estrogen-mediated, endothelial nitric oxide synthase-dependent mobilization of bone marrow-derived endothelial progenitor cells contributes to reendothelialization after arterial injury. Circulation 2003, 108:3115-3121.
76. Jaber N., Zong W.X. Class III PI3K Vps34: essential roles in autophagy, endocytosis, and heart and liver function. Ann. N. Y. Acad. Sci. 2013, 1280:48-51.
77. Jackson S.F., Schoenwaelder S.M. Type I phosphoinositide 3-kinases: potential antithrombotic targets?. Cell Mol. Life Sci. 2006, 63:1085-1090.
78. Jackson S.P., Schoenwaelder S.M. PI 3-Kinase p110beta regulation of platelet integrin alpha(IIb)beta3. Curr. Top. Microbiol. Immunol. 2010, 346:203-224.
79. Jackson S.P., Schoenwaelder S.M. Antithrombotic phosphoinositide 3-kinase beta inhibitors in humans: a 'shear' delight!. J. Thromb. Haemost. 2012, 10:2123-2126.
80. Jackson S.P., Schoenwaelder S.M., Goncalves I., Nesbitt W.S., Yap C.L., Wright C.E., et al. PI 3-kinase p110beta: a new target for antithrombotic therapy. Nat. Med. 2005, 11:507-514.
81. Jeziorska M., McCollum C., Woolley D.E. Mast cell distribution, activation, and phenotype in atherosclerotic lesions of human carotid arteries. J. Pathol. 1997, 182:115-122.
82. Jones G.E., Prigmore E., Calvez R., Hogan C., Dunn G.A., Hirsch E., et al. Requirement for PI 3-kinase gamma in macrophage migration to MCP-1 and CSF-1. Exp. Cell Res. 2003, 290:120-131.
83. Jou S.T., Carpino N., Takahashi Y., Piekorz R., Chao J.R., Wang D., et al. Essential, nonredundant role for the phosphoinositide 3-kinase p110delta in signaling by the B-cell receptor complex. Mol. Cell Biol. 2002, 22:8580-8591.
84. Kaartinen M., Penttila A., Kovanen P.T. Mast cells of two types differing in neutral protease composition in the human aortic intima. Demonstration of tryptase- and tryptase/chymase-containing mast cells in normal intimas, fatty streaks, and the shoulder region of atheromas. Arterioscler. Thromb. 1994, 14:966-972.
85. Kaplan D.R., Whitman M., Schaffhausen B., Pallas D.C., White M., Cantley L., et al. Common elements in growth factor stimulation and oncogenic transformation: 85 kd phosphoprotein and phosphatidylinositol kinase activity. Cell 1987, 50:1021-1029.
86. Kaplan-Albuquerque N., Garat C., Desseva C., Jones P.L., Nemenoff R.A. Platelet-derived growth factor-BB-mediated activation of Akt suppresses smooth muscle-specific gene expression through inhibition of mitogen-activated protein kinase and redistribution of serum response factor. J. Biol. Chem. 2003, 278:39830-39838.
87. Kim S., Garcia A., Jackson S.P., Kunapuli S.P. Insulin-like growth factor-1 regulates platelet activation through PI3-Kalpha isoform. Blood 2007, 110:4206-4213.
88. Kraft S., Kinet J.P. New developments in FcepsilonRI regulation, function and inhibition. Nat. Rev. Immunol. 2007, 7:365-378.
89. Laffargue M., Calvez R., Finan P., Trifilieff A., Barbier M., Altruda F., et al. Phosphoinositide 3-kinase gamma is an essential amplifier of mast cell function. Immunity 2002, 16:441-451.
90. Laurent P.A., Severin S., Gratacap M.P., Payrastre B. Class I PI 3-kinases signaling in platelet activation and thrombosis: PDK1/Akt/GSK3 axis and impact of PTEN and SHIP1. Adv. Biol. Regul. 2014, 54:162-174.
91. Laurent P.A., Severin S., Hechler B., Vanhaesebroeck B., Payrastre B., Gratacap M.P. Platelet PI3Kbeta and GSK3 regulate thrombus stability at a high shear rate. Blood 2015, 125:881-888.
92. Levine B., Mizushima N., Virgin H.W. Autophagy in immunity and inflammation. Nature 2011, 469:323-335.
93. Li H., Li J., Li Y., Singh P., Cao L., Xu L.J., et al. Sonic hedgehog promotes autophagy of vascular smooth muscle cells. Am. J. Physiol. 2012, 303:H1319-H1331.
94. Lian L., Wang Y., Draznin J., Eslin D., Bennett J.S., Poncz M., et al. The relative role of PLCbeta and PI3Kgamma in platelet activation. Blood 2005, 106:110-117.
95. Lin H.H., Chen Y.H., Yet S.F., Chau L.Y. After vascular injury, heme oxygenase-1/carbon monoxide enhances re-endothelialization via promoting mobilization of circulating endothelial progenitor cells. J. Thromb. Haemost. 2009, 7:1401-1408.
96. Lockman K., Hinson J.S., Medlin M.D., Morris D., Taylor J.M., Mack C.P. Sphingosine 1-phosphate stimulates smooth muscle cell differentiation and proliferation by activating separate serum response factor co-factors. J. Biol. Chem. 2004, 279:42422-42430.
97. Luo L., Wall A.A., Yeo J.C., Condon N.D., Norwood S.J., Schoenwaelder S., et al. Rab8a interacts directly with PI3Kgamma to modulate TLR4-driven PI3K and mTOR signalling. Nat. Commun. 2014, 5:4407.
98. Luscher T.F., Steffel J., Eberli F.R., Joner M., Nakazawa G., Tanner F.C., et al. Drug-eluting stent and coronary thrombosis: biological mechanisms and clinical implications. Circulation 2007, 115:1051-1058.
99. Maiellaro K., Taylor W.R. The role of the adventitia in vascular inflammation. Cardiovasc. Res. 2007, 75:640-648.
100. Major A.S., Fazio S., Linton M.F. B-lymphocyte deficiency increases atherosclerosis in LDL receptor-null mice. Arterioscler. Thromb. Vasc. Biol. 2002, 22:1892-1898.
101. Martin V., Guillermet-Guibert J., Chicanne G., Cabou C., Jandrot-Perrus M., Plantavid M., et al. Deletion of the p110beta isoform of phosphoinositide 3-kinase in platelets reveals its central role in Akt activation and thrombus formation in vitro and in vivo. Blood 2010, 115:2008-2013.
102. Mountford J.K., Petitjean C., Putra H.W., McCafferty J.A., Setiabakti N.M., Lee H., et al. The class II PI 3-kinase, PI3KC2alpha, links platelet internal membrane structure to shear-dependent adhesive function. Nat. Commun. 2015, 6:6535.
103. Nakazawa G., Otsuka F., Nakano M., Vorpahl M., Yazdani S.K., Ladich E., et al. The pathology of neoatherosclerosis in human coronary implants bare-metal and drug-eluting stents. J. Am. Coll. Cardiol. 2011, 57:1314-1322.
104. Nashed B.F., Zhang T., Al-Alwan M., Srinivasan G., Halayko A.J., Okkenhaug K., et al. Role of the phosphoinositide 3-kinase p110delta in generation of type 2 cytokine responses and allergic airway inflammation. Eur. J. Immunol. 2007, 37:416-424.
105. Nylander S., Kull B., Bjorkman J.A., Ulvinge J.C., Oakes N., Emanuelsson B.M., et al. Human target validation of phosphoinositide 3-kinase (PI3K)beta: effects on platelets and insulin sensitivity, using AZD6482 a novel PI3Kbeta inhibitor. J. Thromb. Haemost. 2012, 10:2127-2136.
106. Oak J.S., Deane J.A., Kharas M.G., Luo J., Lane T.E., Cantley L.C., et al. Sjogren's syndrome-like disease in mice with T cells lacking class 1A phosphoinositide-3-kinase. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:16882-16887.
107. Okkenhaug K. Signaling by the phosphoinositide 3-kinase family in immune cells. Annu. Rev. Immunol. 2013, 31:675-704.
108. Okkenhaug K., Bilancio A., Farjot G., Priddle H., Sancho S., Peskett E., et al. Impaired B and T cell antigen receptor signaling in p110delta PI 3-kinase mutant mice. Science (New York, NY) 2002, 297:1031-1034.
109. Okkenhaug K., Patton D.T., Bilancio A., Garcon F., Rowan W.C., Vanhaesebroeck B. The p110delta isoform of phosphoinositide 3-kinase controls clonal expansion and differentiation of Th cells. J. Immunol. 2006, 177:5122-5128.
110. Omori S.A., Cato M.H., Anzelon-Mills A., Puri K.D., Shapiro-Shelef M., Calame K., et al. Regulation of class-switch recombination and plasma cell differentiation by phosphatidylinositol 3-kinase signaling. Immunity 2006, 25:545-557.
111. Owens G.K., Kumar M.S., Wamhoff B.R. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 2004, 84:767-801.
112. Park S.J., Kang S.J., Virmani R., Nakano M., Ueda Y. In-stent neoatherosclerosis: a final common pathway of late stent failure. J. Am. Coll. Cardiol. 2012, 59:2051-2057.
113. Patton D.T., Garden O.A., Pearce W.P., Clough L.E., Monk C.R., Leung E., et al. Cutting edge: the phosphoinositide 3-kinase p110 delta is critical for the function of CD4+CD25+Foxp3+ regulatory T cells. J. Immunol. 2006, 177:6598-6602.
114. Paulhe F., Perret B., Chap H., Iberg N., Morand O., Racaud-Sultan C. Phosphoinositide 3-kinase C2alpha is activated upon smooth muscle cell migration and regulated by alpha(v)beta(3) integrin engagement. Biochem. Biophys. Res. Commun. 2002, 297:261-266.
115. Potente M., Urbich C., Sasaki K., Hofmann W.K., Heeschen C., Aicher A., et al. Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J. Clin. Investig. 2005, 115:2382-2392.
116. Puri K.D., Doggett T.A., Douangpanya J., Hou Y., Tino W.T., Wilson T., et al. Mechanisms and implications of phosphoinositide 3-kinase delta in promoting neutrophil trafficking into inflamed tissue. Blood 2004, 103:3448-3456.
117. Puri K.D., Doggett T.A., Huang C.Y., Douangpanya J., Hayflick J.S., Turner M., et al. The role of endothelial PI3Kgamma activity in neutrophil trafficking. Blood 2005, 106:150-157.
118. Qiao J.H., Tripathi J., Mishra N.K., Cai Y., Tripathi S., Wang X.P., et al. Role of macrophage colony-stimulating factor in atherosclerosis: studies of osteopetrotic mice. Am. J. Pathol. 1997, 150:1687-1699.
119. Rajavashisth T., Qiao J.H., Tripathi S., Tripathi J., Mishra N., Hua M., et al. Heterozygous osteopetrotic (op) mutation reduces atherosclerosis in LDL receptor- deficient mice. J. Clin. Investig. 1998, 101:2702-2710.
120. Ramadani F., Bolland D.J., Garcon F., Emery J.L., Vanhaesebroeck B., Corcoran A.E., et al. The PI3K isoforms p110alpha and p110delta are essential for pre-B cell receptor signaling and B cell development. Sci. Signal. 2010, 3:ra60.
121. Rodriguez-Borlado L., Barber D.F., Hernandez C., Rodriguez-Marcos M.A., Sanchez A., Hirsch E., et al. Phosphatidylinositol 3-kinase regulates the CD4/CD8 T cell differentiation ratio. J. Immunol. 2003, 170:4475-4482.
122. Roller A., Perino A., Dapavo P., Soro E., Okkenhaug K., Hirsch E., et al. Blockade of phosphatidylinositol 3-kinase PI3Kdelta or PI3Kgamma reduces IL-17 and ameliorates imiquimod-induced psoriasis-like dermatitis. J. Immunol. 2012, 189:4612-4620.
123. Sage A.P., Mallat Z. Multiple potential roles for B cells in atherosclerosis. Ann. Med. 2014, 46:297-303.
124. Salabei J.K., Cummins T.D., Singh M., Jones S.P., Bhatnagar A., Hill B.G. PDGF-mediated autophagy regulates vascular smooth muscle cell phenotype and resistance to oxidative stress. Biochem. J. 2013, 451:375-388.
125. Salabei J.K., Hill B.G. Implications of autophagy for vascular smooth muscle cell function and plasticity. Free Radic. Biol. Med. 2013, 65:693-703.
126. Sasaki T., Irie-Sasaki J., Jones R.G., Oliveira-dos-Santos A.J., Stanford W.L., Bolon B., et al. Function of PI3Kgamma in thymocyte development, T cell activation, and neutrophil migration. Sci. (New York, NY) 2000, 287:1040-1046.
127. Schoenwaelder S.M., Ono A., Sturgeon S., Chan S.M., Mangin P., Maxwell M.J., et al. Identification of a unique co-operative phosphoinositide 3-kinase signaling mechanism regulating integrin alpha IIb beta 3 adhesive function in platelets. J. Biol. Chem. 2007, 282:28648-28658.
128. Scott N.A., Cipolla G.D., Ross C.E., Dunn B., Martin F.H., Simonet L., et al. Identification of a potential role for the adventitia in vascular lesion formation after balloon overstretch injury of porcine coronary arteries. Circulation 1996, 93:2178-2187.
129. Senis Y.A., Atkinson B.T., Pearce A.C., Wonerow P., Auger J.M., Okkenhaug K., et al. Role of the p110delta PI 3-kinase in integrin and ITAM receptor signalling in platelets. Platelets 2005, 16:191-202.
130. Shi Y., O'Brien J.E., Fard A., Mannion J.D., Wang D., Zalewski A. Adventitial myofibroblasts contribute to neointimal formation in injured porcine coronary arteries. Circulation 1996, 94:1655-1664.
131. Shi Y., O'Brien J.E., Fard A., Zalewski A. Transforming growth factor-beta 1 expression and myofibroblast formation during arterial repair. Arterioscler. Thromb. Vasc. Biol. 1996, 16:1298-1305.
132. Smirnova N.F., Gayral S., Pedros C., Loirand G., Vaillant N., Malet N., et al. Targeting PI3Kgamma activity decreases vascular trauma-induced intimal hyperplasia through modulation of the Th1 response. J. Exp. Med. 2014, 211:1779-1792.
133. Srivastava S., Choudhury P., Li Z., Liu G., Nadkarni V., Ko K., et al. Phosphatidylinositol 3-phosphate indirectly activates KCa3.1 via 14 amino acids in the carboxy terminus of KCa3.1. Mol. Biol. Cell 2006, 17:146-154.
134. Srivastava S., Di L., Zhdanova O., Li Z., Vardhana S., Wan Q., et al. The class II phosphatidylinositol 3 kinase C2beta is required for the activation of the K+ channel KCa3.1 and CD4 T-cells. Mol. Biol. Cell 2009, 20:3783-3791.
135. Stephens L., Hawkins P. More paths to PI3Kgamma. PLoS Biol. 2013, 11:e1001594.
136. Steyers C.M., Miller F.J. Endothelial dysfunction in chronic inflammatory diseases. Int. J. Mol. Sci. 2014, 15:11324-11349.
137. Sturgeon S.A., Jones C., Angus J.A., Wright C.E. Advantages of a selective beta-isoform phosphoinositide 3-kinase antagonist, an anti-thrombotic agent devoid of other cardiovascular actions in the rat. Eur. J. Pharmacol. 2008, 587:209-215.
138. Suarez-Fueyo A., Rojas J.M., Cariaga A.E., Garcia E., Steiner B.H., Barber D.F., et al. Inhibition of PI3Kdelta reduces kidney infiltration by macrophages and ameliorates systemic lupus in the mouse. J. Immunol. 2014, 193:544-554.
139. Sun J., Sukhova G.K., Wolters P.J., Yang M., Kitamoto S., Libby P., et al. Mast cells promote atherosclerosis by releasing proinflammatory cytokines. Nat. Med. 2007, 13:719-724.
140. Toker A., Marmiroli S. Signaling specificity in the Akt pathway in biology and disease. Adv. Biol. Regul. 2014, 55:28-38.
141. Troutman T.D., Bazan J.F., Pasare C. Toll-like receptors, signaling adapters and regulation of the pro-inflammatory response by PI3K. Cell Cycle 2012, 11:3559-3567.
142. Tsuzuki M. Bone marrow-derived cells are not involved in reendothelialized endothelium as endothelial cells after simple endothelial denudation in mice. Basic Res. Cardiol. 2009, 104:601-611.
143. Urbich C., Knau A., Fichtlscherer S., Walter D.H., Bruhl T., Potente M., et al. FOXO-dependent expression of the proapoptotic protein Bim: pivotal role for apoptosis signaling in endothelial progenitor cells. FASEB J. 2005, 19:974-976.
144. Van der Heiden K., Gijsen F.J., Narracott A., Hsiao S., Halliday I., Gunn J., et al. The effects of stenting on shear stress: relevance to endothelial injury and repair. Cardiovasc. Res. 2013, 99:269-275.
145. van Dop W.A., Marengo S., te Velde A.A., Ciraolo E., Franco I., ten Kate F.J., et al. The absence of functional PI3Kgamma prevents leukocyte recruitment and ameliorates DSS-induced colitis in mice. Immunol. Lett. 2010, 131:33-39.
146. Vanhaesebroeck B., Guillermet-Guibert J., Graupera M., Bilanges B. The emerging mechanisms of isoform-specific PI3K signalling. Nat. Rev. Mol. Cell Biol. 2010, 11:329-341.
147. Vanhaesebroeck B., Jones G.E., Allen W.E., Zicha D., Hooshmand-Rad R., Sawyer C., et al. Distinct PI(3)Ks mediate mitogenic signalling and cell migration in macrophages. Nat. Cell Biol. 1999, 1:69-71.
148. Vanhoutte P.M. Regeneration of the endothelium in vascular injury. Cardiovasc. Drugs Ther. 2010, 24:299-303. sponsored by the International Society of Cardiovascular Pharmacotherapy.
149. Vantler M., Jesus J., Leppanen O., Scherner M., Berghausen E.M., Mustafov L., et al. Class IA phosphatidylinositol 3-Kinase isoform p110alpha mediates vascular remodeling. Arterioscler. Thromb. Vasc. Biol. 2015, 35:1434-1444.
150. Walser R., Burke J.E., Gogvadze E., Bohnacker T., Zhang X., Hess D., et al. PKCbeta phosphorylates PI3Kgamma to activate it and release it from GPCR control. PLoS Biol. 2013, 11:e1001587.
151. Walter D.H., Rittig K., Bahlmann F.H., Kirchmair R., Silver M., Murayama T., et al. Statin therapy accelerates reendothelialization: a novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation 2002, 105:3017-3024.
152. Wang Y., Yoshioka K., Azam M.A., Takuwa N., Sakurada S., Kayaba Y., et al. Class II phosphoinositide 3-kinase alpha-isoform regulates Rho, myosin phosphatase and contraction in vascular smooth muscle. Biochem. J. 2006, 394:581-592.
153. Watanabe N., Nakajima H., Suzuki H., Oda A., Matsubara Y., Moroi M., et al. Functional phenotype of phosphoinositide 3-kinase p85alpha-null platelets characterized by an impaired response to GP VI stimulation. Blood 2003, 102:541-548.
154. Weiss-Haljiti C., Pasquali C., Ji H., Gillieron C., Chabert C., Curchod M.L., et al. Involvement of phosphoinositide 3-kinase gamma, Rac, and PAK signaling in chemokine-induced macrophage migration. J. Biol. Chem. 2004, 279:43273-43284.
155. Wymann M.P., Zvelebil M., Laffargue M. Phosphoinositide 3-kinase signalling-which way to target?. Trends Pharmacol. Sci. 2003, 24:366-376.
156. Yao Q., Renault M.A., Chapouly C., Vandierdonck S., Belloc I., Jaspard-Vinassa B., et al. Sonic hedgehog mediates a novel pathway of PDGF-BB-dependent vessel maturation. Blood 2014, 123:2429-2437.
157. Yoshioka K., Sugimoto N., Takuwa N., Takuwa Y. Essential role for class II phosphoinositide 3-kinase alpha-isoform in Ca2+-induced, Rho- and Rho kinase-dependent regulation of myosin phosphatase and contraction in isolated vascular smooth muscle cells. Mol. Pharmacol. 2007, 71:912-920.
158. Yoshioka K., Yoshida K., Cui H., Wakayama T., Takuwa N., Okamoto Y., et al. Endothelial PI3K-C2alpha, a class II PI3K, has an essential role in angiogenesis and vascular barrier function. Nat. Med. 2012, 18:1560-1569.
159. Zeng L., Xiao Q., Margariti A., Zhang Z., Zampetaki A., Patel S., et al. HDAC3 is crucial in shear- and VEGF-induced stem cell differentiation toward endothelial cells. J. Cell Biol. 2006, 174:1059-1069.
160. Zhang J., Banfic H., Straforini F., Tosi L., Volinia S., Rittenhouse S.E. A type II phosphoinositide 3-kinase is stimulated via activated integrin in platelets. A source of phosphatidylinositol 3-phosphate. J. Biol. Chem. 1998, 273:14081-14084.
161. Zhang T.T., Okkenhaug K., Nashed B.F., Puri K.D., Knight Z.A., Shokat K.M., et al. Genetic or pharmaceutical blockade of p110delta phosphoinositide 3-kinase enhances IgE production. J. Allergy Clin. Immunol. 2008, 122. 811-9 e2.
162. Zheng Y.H., Tian C., Meng Y., Qin Y.W., Du Y.H., Du J., et al. Osteopontin stimulates autophagy via integrin/CD44 and p38 MAPK signaling pathways in vascular smooth muscle cells. J. Cell Physiol. 2012, 227:127-135.