Pim1 kinase promotes angiogenesis through phosphorylation of endothelial nitric oxide synthase at Ser-633

Cardiovascular Research

Volumn 109, Issue 1, 2016, Pages 141-150

  Chen, Ming ^a   Yi, Bing ^a   Zhu, Ni ^a   Wei, Xin ^a   Zhang, Guan Xin ^a,b   Huang, Shengdong ^b   Sun, Jianxin ^a,b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Angiogenesis; Diabetes; eNOS; Phosphorylation; Pim1

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; NITRIC OXIDE; PROTEIN KINASE PIM 1; SERINE; VASCULOTROPIN; NOS3 PROTEIN, MOUSE; PIM1 PROTEIN, MOUSE; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; ARTICLE; ASSAY; CELL MIGRATION; CONTROLLED STUDY; DIABETES MELLITUS; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; EX VIVO STUDY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; VASCULAR RING; ANIMAL; C57BL MOUSE; CELL CULTURE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; ENDOTHELIAL CELLS; HUMANS; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-PIM-1; SERINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84959912477     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv250     Document Type: Article

References (43)

1. Fleming I. Molecular mechanisms underlying the activation of eNOS. Pflugers Arch 2010; 459: 793-806
2. Qian J, Fulton D. Post-translational regulation of endothelial nitric oxide synthase in vascular endothelium. Front Physiol 2013; 4: 347
3. Musicki B, Burnett AL. Endothelial dysfunction in diabetic erectile dysfunction. Int J Impot Res 2007; 19: 129-138
4. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 1999; 399: 597-601
5. Fleming I, Fisslthaler B, Dimmeler S, Kemp BE, Busse R. Phosphorylation of Thr(495) regulates Ca(2+)/calmodulin-dependent endothelial nitric oxide synthase activity. Circ Res 2001; 88: E68-E75
6. Fulton D, Ruan L, Sood SG, Li C, Zhang Q, Venema RC. Agonist-stimulated endothelial nitric oxide synthase activation and vascular relaxation. Role of eNOS phosphorylation at Tyr83. Circ Res 2008; 102: 497-504
7. Michell BJ, Harris MB, Chen ZP, Ju H, Venema VJ, Blackstone MA, Huang W, Venema RC, Kemp BE. Identification of regulatory sites of phosphorylation of the bovine endothelial nitric-oxide synthase at serine 617 and serine 635. J Biol Chem 2002; 277: 42344-42351
8. Loot AE, Schreiber JG, Fisslthaler B, Fleming I. Angiotensin II impairs endothelial function via tyrosine phosphorylation of the endothelial nitric oxide synthase. J Exp Med 2009; 206: 2889-2896
9. Luo Z, Fujio Y, Kureishi Y, Rudic RD, Daumerie G, Fulton D, Sessa WC, Walsh K. Acute modulation of endothelial Akt/PKB activity alters nitric oxide-dependent vasomotor activity in vivo. J Clin Invest 2000; 106: 493-499
10. Chen Z, Peng IC, Sun W, Su MI, Hsu PH, Fu Y, Zhu Y, DeFea K, Pan S, Tsai MD, Shyy JY. AMP-activated protein kinase functionally phosphorylates endothelial nitric oxide synthase Ser633. Circ Res 2009; 104: 496-505
11. Boo YC, Hwang J, Sykes M, Michell BJ, Kemp BE, Lum H, Jo H. Shear stress stimulates phosphorylation of eNOS at Ser(635) by a protein kinase A-dependent mechanism. Am J Physiol Heart Circ Physiol 2002; 283: H1819-H1828
12. Xiao Z, Wang T, Qin H, Huang C, Feng Y, Xia Y. Endoplasmic reticulum Ca2+ release modulates endothelial nitric-oxide synthase via extracellular signal-regulated kinase (ERK) 1/2-mediated serine 635 phosphorylation. J Biol Chem 2011; 286: 20100-20108
13. Narlik-Grassow M, Blanco-Aparicio C, Carnero A. The PIM family of serine/threonine kinases in cancer. Med Res Rev 2014; 34: 136-159
14. Nawijn MC, Alendar A, Berns A. For better or for worse: the role of Pim oncogenes in tumorigenesis. Nat Rev Cancer 2011; 11: 23-34
15. Katare R, Caporali A, Zentilin L, Avolio E, Sala-Newby G, Oikawa A, Cesselli D, Beltrami AP, Giacca M, Emanueli C, Madeddu P. Intravenous gene therapy with PIM-1 via a cardiotropic viral vector halts the progression of diabetic cardiomyopathy through promotion of prosurvival signaling. Circ Res 2011; 108: 1238-1251
16. Trinh TB, Xiao Q, Pei D. Profiling the substrate specificity of protein kinases by on-bead screening of peptide libraries. Biochemistry 2013; 52: 5645-5655
17. Kobayashi K, Forte TM, Taniguchi S, Ishida BY, Oka K, Chan L. The db/db mouse, a model for diabetic dyslipidemia: molecular characterization and effects of Western diet feeding. Metabolism 2000; 49: 22-31
18. You B, Jiang YY, Chen S, Yan G, Sun J. The orphan nuclear receptor Nur77 suppresses endothelial cell activation through induction of IkappaBalpha expression. Circ Res 2009; 104: 742-749
19. Chen M, Yi B, Sun J. Inhibition of cardiomyocyte hypertrophy by protein arginine methyltransferase 5. J Biol Chem 2014; 289: 24325-24335
20. Zheng Q, Yuan Y, YiW, Lau WB, Wang Y, Wang X, Sun Y, Lopez BL, Christopher TA, Peterson JM, Wong GW, Yu S, Yi D, Ma XL. C1q/TNF-related proteins, a family of novel adipokines, induce vascular relaxation through the adiponectin receptor-1/AMPK/eNOS/nitric oxide signaling pathway. Arterioscler Thromb Vasc Biol 2011; 31: 2616-2623
21. Baker M, Robinson SD, Lechertier T, Barber PR, Tavora B, D'Amico G, Jones DT, Vojnovic B, Hodivala-Dilke K. Use of the mouse aortic ring assay to study angiogenesis. Nat Protoc 2012; 7: 89-104
22. Zippo A, De Robertis A, Serafini R, Oliviero S. PIM1-dependent phosphorylation of histone H3 at serine 10 is required for MYC-dependent transcriptional activation and oncogenic transformation. Nat Cell Biol 2007; 9: 932-944
23. Sun J, Liao JK. Induction of angiogenesis by heat shock protein 90 mediated by protein kinase Akt and endothelial nitric oxide synthase. Arterioscler Thromb Vasc Biol 2004; 24: 2238-2244
24. Lin YW, Beharry ZM, Hill EG, Song JH, Wang W, Xia Z, Zhang Z, Aplan PD, Aster JC, Smith CD, Kraft AS. A small molecule inhibitor of Pim protein kinases blocks the growth of precursor T-cell lymphoblastic leukemia/lymphoma. Blood 2010; 115: 824-833
25. Sun J, Liao JK. Functional interaction of endothelial nitric oxide synthase with a voltagedependent anion channel. Proc Natl Acad Sci USA 2002; 99: 13108-13113
26. Mount PF, Kemp BE, Power DA. Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J Mol Cell Cardiol 2007; 42: 271-279
27. Butt E, Bernhardt M, Smolenski A, Kotsonis P, Frohlich LG, Sickmann A, Meyer HE, Lohmann SM, Schmidt HH. Endothelial nitric-oxide synthase (type III) is activated and becomes calcium independent upon phosphorylation by cyclic nucleotidedependent protein kinases. J Biol Chem 2000; 275: 5179-5187
28. Boo YC, Sorescu GP, Bauer PM, Fulton D, Kemp BE, Harrison DG, Sessa WC, Jo H. Endothelial NO synthase phosphorylated at SER635 produces NO without requiring intracellular calcium increase. Free Radic Biol Med 2003; 35: 729-741
29. Willert M, Augstein A, Poitz DM, Schmeisser A, Strasser RH, Braun-Dullaeus RC. Transcriptional regulation of Pim-1 kinase in vascular smooth muscle cells and its role for proliferation. Basic Res Cardiol 2010; 105: 267-277
30. Walpen T, Peier M, Haas E, Kalus I, Schwaller J, Battegay E, Humar R. Loss of pim1 imposes a hyperadhesive phenotype on endothelial cells. Cell Physiol Biochem 2012; 30: 1083-1096
31. Zippo A, De Robertis A, Bardelli M, Galvagni F, Oliviero S. Identification of Flk-1 target genes in vasculogenesis: Pim-1 is required for endothelial and mural cell differentiation in vitro. Blood 2004; 103: 4536-4544
32. Kawasaki K, Smith RS Jr., Hsieh CM, Sun J, Chao J, Liao JK. Activation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates nitric oxide-induced endothelial cell migration and angiogenesis. Mol Cell Biol 2003; 23: 5726-5737
33. Cen B, Xiong Y, Song JH, Mahajan S, DuPont R, McEachern K, DeAngelo DJ, Cortes JE, Minden MD, Ebens A, Mims A, LaRue AC, Kraft AS. The Pim-1 protein kinase is an important regulator of MET receptor tyrosine kinase levels and signaling. Mol Cell Biol 2014; 34: 2517-2532
34. Triggle CR, Ding H. A review of endothelial dysfunction in diabetes: a focus on the contribution of a dysfunctional eNOS. J Am Soc Hypertens 2010; 4: 102-115
35. Li Q, Atochin D, Kashiwagi S, Earle J, Wang A, Mandeville E, Hayakawa K, d'Uscio LV, Lo EH, Katusic Z, Sessa W, Huang PL. Deficient eNOS phosphorylation is a mechanism for diabetic vascular dysfunction contributing to increased stroke size. Stroke 2013; 44: 3183-3188
36. Zhong JC, Yu XY, Huang Y, Yung LM, LauC W, Lin SG. Apelin modulates aortic vascular tone via endothelial nitric oxide synthase phosphorylation pathway in diabetic mice. Cardiovasc Res 2007; 74: 388-395
37. Moore A, Shindikar A, Fomison-Nurse I, Riu F, Munasinghe PE, Ram TP, Saxena P, Coffey S, Bunton RW, Galvin IF, Williams MJ, Emanueli C, Madeddu P, Katare R. Rapid onset of cardiomyopathy in STZ-induced female diabetic mice involves the downregulation of pro-survival Pim-1. Cardiovasc Diabetol 2014; 13: 68
38. Borillo GA, Mason M, Quijada P, Volkers M, Cottage C, McGregor M, Din S, Fischer K, Gude N, Avitabile D, Barlow S, Alvarez R, Truffa S, Whittaker R, Glassy MS, Gustafsson AB, Miyamoto S, Glembotski CC, Gottlieb RA, Brown JH, Sussman M.A. Pim-1 kinase protects mitochondrial integrity in cardiomyocytes. Circ Res 2010; 106: 1265-1274
39. Din S, Mason M, Volkers M, Johnson B, Cottage CT, Wang Z, Joyo AY, Quijada P, Erhardt P, Magnuson NS, Konstandin MH, Sussman M.A. Pim-1 preserves mitochondrial morphology by inhibiting dynamin-related protein 1 translocation. Proc Natl Acad Sci USA 2013; 110: 5969-5974
40. Din S, Konstandin MH, Johnson B, Emathinger J, Volkers M, Toko H, Collins B, Ormachea L, Samse K, Kubli DA, De La Torre A, Kraft AS, Gustafsson AB, Kelly DP, Sussman M.A. Metabolic dysfunction consistent with premature aging results from deletion of Pim kinases. Circ Res 2014; 115: 376-387
41. Davidson SM, Duchen MR. Endothelial mitochondria: contributing to vascular function and disease. Circ Res 2007; 100: 1128-1141
42. Kolluru GK, Bir SC, Kevil CG. Endothelial dysfunction and diabetes: effects on angiogenesis, vascular remodeling, and wound healing. Int J Vasc Med 2012; 2012: 918267
43. Tu ML, Wang HQ, Sun XD, Chen LJ, Peng XC, Yuan YH, Li RM, Ruan XZ, Li DS, Xu YJ, Ke ZJ. Pim-1 is up-regulated by shear stress and is involved in shear stress-induced proliferation of rat mesenchymal stem cells. Life Sci 2011; 88: 233-238