Identification of PI3K regulatory subunit p55γ as a novel inhibitor of vascular smoothmuscle cell proliferation and neointimal formation

Cardiovascular Research

Volumn 105, Issue 1, 2015, Pages 75-85

  Li, Geng ^a   Xie, Ning ^a   Yao, Yuan ^a   Zhang, Yan ^a   Guo, Jiaojiao ^a   Feng, Yuanqing ^a   Lv, Fengxiang ^a   Xiao, Rui Ping ^a   Cao, Chun Mei ^a  

^a PEKING UNIVERSITY   (China)

Author keywords

Neointimal formation; P55 ; Restenosis; Vascular smooth muscle cell proliferation

Indexed keywords

MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE P55 GAMMA SUBUNIT; PLATELET DERIVED GROWTH FACTOR BB; PROTEIN BCL XL; PROTEIN MDM2; PROTEIN P21; PROTEIN P53; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; BCL2L1 PROTEIN, RAT; CYCLIN DEPENDENT KINASE INHIBITOR 1A; MDM2 PROTEIN, RAT; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; PIK3R3 PROTEIN, HUMAN; PROTEIN BCL X;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAROTID ARTERY INJURY; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE ACTIVATION; GENE OVEREXPRESSION; GENE SILENCING; IN VITRO STUDY; IN VIVO STUDY; MALE; NEOINTIMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RAT; RNA ANALYSIS; S PHASE CELL CYCLE CHECKPOINT; UBIQUITINATION; UPREGULATION; VASCULAR SMOOTH MUSCLE CELL; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL CYCLE CHECKPOINT; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; VASCULAR SMOOTH MUSCLE;

ANIMALS; BCL-X PROTEIN; CAROTID ARTERY INJURIES; CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; CELLS, CULTURED; CLASS IA PHOSPHATIDYLINOSITOL 3-KINASE; CYCLIN-DEPENDENT KINASE INHIBITOR P21; GENE KNOCKDOWN TECHNIQUES; HUMANS; MALE; MUSCLE, SMOOTH, VASCULAR; NEOINTIMA; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-MDM2; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84929086179     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvu235     Document Type: Article

References (41)

1. Braun-Dullaeus RC, Mann MJ, Dzau VJ. Cell cycle progression:newtherapeutic target for vascular proliferative disease. Circulation 1998;98:82-89.
2. Dzau VJ, Braun-Dullaeus RC, Sedding DG. Vascular proliferation and atherosclerosis: new perspectives and therapeutic strategies. Nat Med 2002;8:1249-1256.
3. Novak K. Cardiovascular disease increasing in developing countries. Nat Med 1998;4: 989-990.
4. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 1993; 362:801-809.
5. Clowes AW, Schwartz SM. Significance of quiescent smooth muscle migration in the injured rat carotid artery. Circ Res 1985;56:139-145.
6. Clowes AW, Reidy MA, Clowes MM. Kinetics of cellular proliferation after arterial injury. I. Smooth muscle growth in the absence of endothelium. Lab Invest 1983;49: 327-333.
7. Bunney TD, Katan M. Phosphoinositide signalling in cancer: beyond PI3 K and PTEN. Nat Rev Cancer 2010;10:342-352.
8. Morello F, Perino A, Hirsch E. Phosphoinositide 3-kinase signalling in the vascular system. Cardiovasc Res 2009;82:261-271.
9. Shiojima I, Walsh K. Regulation of cardiac growth and coronary angiogenesis by the Akt/ PKB signaling pathway. Genes Dev 2006;20:3347-3365.
10. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, Woscholski R, Parker PJ, Waterfield MD. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 2001;70:535-602.
11. Engelman JA, Luo J, Cantley LC. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 2006;7:606-619.
12. Inukai K, Funaki M, Anai M, Ogihara T, Katagiri H, Fukushima Y, Sakoda H, Onishi Y, Ono H, Fujishiro M, Abe M, Oka Y, Kikuchi M, Asano T. Five isoforms of the phosphatidylinositol 3-kinase regulatory subunit exhibit different associations with receptor tyrosine kinases and their tyrosine phosphorylations. FEBS Lett 2001;490:32-38.
13. Pons S, Asano T, Glasheen E, Miralpeix M, Zhang Y, Fisher TL, Myers MG Jr, Sun XJ, White MF. The structure and function of p55PIK reveal a new regulatory subunit for phosphatidylinositol 3-kinase. Mol Cell Biol 1995;15:4453-4465.
14. Vanhaesebroeck B, Leevers SJ, Panayotou G, Waterfield MD. Phosphoinositide 3-kinases: a conserved family of signal transducers. Trends Biochem Sci 1997;22:267-272.
15. Soroceanu L, Kharbanda S, Chen R, Soriano RH, Aldape K, Misra A, Zha J, Forrest WF, Nigro JM, Modrusan Z, Feuerstein BG, Phillips HS. Identification of IGF2 signaling through phosphoinositide-3-kinase regulatory subunit 3 as a growth-promoting axis in glioblastoma. Proc Natl Acad Sci USA 2007;104:3466-3471.
16. Zhang L, Huang J, Yang N, Greshock J, Liang S, Hasegawa K, Giannakakis A, Poulos N, O'Brien-Jenkins A, Katsaros D, Butzow R, Weber BL, Coukos G. Integrative genomic analysis of phosphatidylinositol 3-kinase family identifies PIK3R3 as a potential therapeutic target in epithelial ovarian cancer. Clin Cancer Res 2007;13:5314-5321.
17. Zhou J, Chen GB, Tang YC, Sinha RA, WuY, Yap CS, Wang G, Hu J, Xia X, Tan P, Goh LK, YenPM. Genetic and bioinformatic analyses of the expression and function of PI3 Kregulatory subunit PIK3R3 in an Asian patient gastric cancer library. BMC Med Genomics 2012; 5:34.
18. Wang G, Chen C, Yang R, Cao X, Lai S, Luo X, Feng Y, Xia X, Gong J, Hu J. p55PIK-PI3 K stimulates angiogenesis in colorectal cancer cell by activating NF-kappaB pathway. Angiogenesis 2013;16:561-573.
19. Wang G, Cao X, Lai S, Luo X, Feng Y, Xia X, Yen PM, Gong J, Hu J. PI3K stimulatesDNA synthesis and cell-cycle progression via its p55PIK regulatory subunit interaction with PCNA. Mol Cancer Ther 2013;12:2100-2109.
20. Xia X, Cheng A, Akinmade D, HamburgerAW. The N-terminal 24 amino acids of the p55 gamma regulatory subunit of phosphoinositide 3-kinase binds Rb and induces cell cycle arrest. Mol Cell Biol 2003;23:1717-1725.
21. Li Q, Li G, Lan X, Zheng M, Chen KH, Cao CM, Xiao RP. Receptor interacting protein 3 suppresses vascular smooth muscle cell growth by inhibition of the phosphoinositide 3-kinase-Akt axis. J Biol Chem 2010;285:9535-9544.
22. Cao CM, Zhang Y, Weisleder N, Ferrante C, Wang X, Lv F, Zhang Y, Song R, Hwang M, Jin L, Guo J, Peng W, Li G, Nishi M, Takeshima H, Ma J, Xiao RP. MG53 constitutes a primary determinant of cardiac ischemic preconditioning. Circulation 2010;121: 2565-2574.
23. Song R, PengW, Zhang Y, Lv F, WuHK, GuoJ, CaoY, Pi Y, Zhang X, Jin L, Zhang M, Jiang P, Liu F, Meng S, Zhang X, Jiang P, Cao CM, Xiao RP. Central role of E3 ubiquitin ligaseMG53 in insulin resistance and metabolic disorders. Nature 2013;494:375-379.
24. Brooks CL, GuW. p53 ubiquitination: Mdm2 and beyond. Mol Cell 2006;21:307-315.
25. Michael D, Oren M. The p53-Mdm2 module and the ubiquitin system. Semin Cancer Biol 2003;13:49-58.
26. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP, Sedivy JM, Kinzler KW, Vogelstein B. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 1998;282:1497-1501.
27. el-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW, Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell 1993;75:817-825.
28. Waga S, Hannon GJ, Beach D, Stillman B. The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature 1994;369:574-578.
29. Waga S, Stillman B. Cyclin-dependent kinase inhibitor p21 modulates the DNA primertemplate recognition complex. Mol Cell Biol 1998;18:4177-4187.
30. Deng Y, Wang J, Wang G, Jin Y, Luo X, Xia X, Gong J, Hu J. p55PIK transcriptionally activated by MZF1 promotes colorectal cancer cell proliferation. Biomed Res Int 2013;2013: 868131.
31. AndresV. Control of vascular cell proliferation and migration by cyclin-dependent kinase signalling: new perspectives and therapeutic potential. Cardiovasc Res 2004;63:11-21.
32. Scott S, O'Sullivan M, Hafizi S, Shapiro LM, Bennett MR. Human vascular smooth muscle cells from restenosis or in-stent stenosis sites demonstrate enhanced responses to p53: implications for brachytherapy and drug treatment for restenosis. Circ Res 2002;90: 398-404.
33. Radhakrishnan SK, Feliciano CS, Najmabadi F, Haegebarth A, Kandel ES, Tyner AL, Gartel AL. Constitutive expression of E2F-1 leads to p21-dependent cell cycle arrest in S phase of the cell cycle. Oncogene 2004;23:4173-4176.
34. ZhuH, Zhang L, WuS, Teraishi F, Davis JJ, Jacob D, Fang B. Induction of S-phase arrest and p21 overexpression by a small molecule 2[[3-(2, 3-dichlorophenoxy)propyl] amino] ethanol in correlation with activation of ERK. Oncogene 2004;23:4984-4992.
35. Li H, Telemaque S, Miller RE, Marsh JD. High glucose inhibits apoptosis induced by serum deprivation in vascular smooth muscle cells via upregulation of Bcl-2 and Bcl-xl. Diabetes 2005;54:540-545.
36. Chipuk JE, Bouchier-Hayes L, Kuwana T, Newmeyer DD, GreenDR. PUMA couples the nuclear and cytoplasmic proapoptotic function of p53. Science 2005;309:1732-1735.
37. Jung MS, Jin DH, Chae HD, Kang S, Kim SC, Bang YJ, Choi TS, Choi KS, ShinDY. Bcl-xL and E1B-19K proteins inhibit p53-induced irreversible growth arrest and senescence by preventing reactive oxygen species-dependent p38 activation. J Biol Chem 2004;279: 17765-17771.
38. Schoop RA, Kooistra K, Baatenburg De Jong RJ, Noteborn MH. Bcl-xL inhibits p53-but not apoptin-induced apoptosis in head and neck squamous cell carcinoma cell line. Int J Cancer 2004;109:38-42.
39. Garas SM, Huber P, Scott NA. Overview of therapies for prevention of restenosis after coronary interventions. Pharmacol Ther 2001;92:165-178.
40. Moussa I, Leon MB, Baim DS, O'Neill WW, Popma JJ, Buchbinder M, Midwall J, Simonton CA, Keim E, Wang P, Kuntz RE, Moses JW. Impact of sirolimus-eluting stents on outcome in diabetic patients: a SIRIUS (SIRolImUS-coated Bx Velocity balloon-expandable stent in the treatment of patients with de novo coronary artery lesions) substudy. Circulation 2004;109:2273-2278.
41. Sousa JE, Costa MA, Abizaid A, Abizaid AS, Feres F, Pinto IM, Seixas AC, Staico R, Mattos LA, Sousa AG, Falotico R, Jaeger J, Popma JJ, SerruysPW. Lack of neointimal proliferation after implantation of sirolimus-coated stents in human coronary arteries: a quantitative coronary angiography and three-dimensional intravascular ultrasound study. Circulation 2001;103:192-195.