Importance of insulin resistance to vascular repair and regeneration

Free Radical Biology and Medicine

Volumn 60, Issue , 2013, Pages 246-263

  Cubbon, Richard M ^a   Mercer, Ben N ^a   Sengupta, Anshuman ^a   Kearney, Mark T ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Diabetes mellitus; Free radicals; Growth factor; Insulin resistance; Nitric oxide; Reactive oxygen species; Vascular repair

Indexed keywords

ADIPONECTIN; ALDOSTERONE; ANGIOTENSIN II; ANGIOTENSIN RECEPTOR; C REACTIVE PROTEIN; CD133 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN; GLUCOSE TRANSPORTER 4; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HYPOXIA INDUCIBLE FACTOR 1BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN RECEPTOR; LIVER X RECEPTOR; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PLASMINOGEN ACTIVATOR INHIBITOR 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SOMATOMEDIN C RECEPTOR; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; VASCULOTROPIN A; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ADAPTIVE IMMUNITY; ANGIOGENESIS; APOPTOSIS; ATHEROSCLEROSIS; AUTOPHOSPHORYLATION; BIOAVAILABILITY; BLOOD CLOTTING; CARDIOVASCULAR MORTALITY; CARDIOVASCULAR RISK; COST EFFECTIVENESS ANALYSIS; DYSLIPIDEMIA; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIAL DYSFUNCTION; ENDOTHELIAL PROGENITOR CELL; ENZYME ACTIVITY; FIBRINOLYSIS; GENETIC TRANSCRIPTION; HEART MUSCLE REVASCULARIZATION; HUMAN; HYPERGLYCEMIA; HYPERTENSION; INSULIN RESISTANCE; INTRACELLULAR SIGNALING; METABOLIC SYNDROME X; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; OBESITY; OXIDATIVE STRESS; PARTICLE SIZE; PERCUTANEOUS CORONARY INTERVENTION; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; VASCULAR SMOOTH MUSCLE;

ANIMALS; DIABETES COMPLICATIONS; HUMANS; INSULIN; INSULIN RESISTANCE; METABOLIC SYNDROME X; MICE; NITRIC OXIDE; OBESITY; REGENERATION; VASCULAR DISEASES;

MURINAE;

EID: 84875926487     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.02.028     Document Type: Review

References (278)

1. Emerging Risk Factors Collaboration S.R. Seshasai, and S. Kaptoge Diabetes mellitus, fasting glucose, and risk of cause-specific death N. Engl. J. Med. 364 2011 829 841
2. G.L. Booth, M.K. Kapral, K. Fung, and J.V. Tu Relation between age and cardiovascular disease in men and women with diabetes compared with non-diabetic people: a population-based retrospective cohort study Lancet 368 2006 29 36
3. The DECODE Study Group Is the current definition for diabetes relevant to mortality risk from all causes and cardiovascular and noncardiovascular diseases? Diabetes Care 26 2003 688 696
4. The International Diabetes Federation. URL: 〈http://www.idf.org/ diabetesatlas/5e/the-global-burden〉. Accessed 6 September 2012.
5. A.M. From, C.L. Leibson, F. Bursi, M.M. Redfield, S.A. Weston, and S.J. Jacobsen Diabetes in heart failure: prevalence and impact on outcome in the population Am. J. Med. 119 2006 591 599
6. Ovbiagele B., Markovic D., Fonarow G.C. Recent US patterns and predictors of prevalent diabetes among acute myocardial infarction patients. Cardiol. Res. Pract.20111456152011.
7. Cubbon R.M., Adams B., Rajwani A., Mercer B.N., Patel P.A., Gherardi G., et al. Diabetes mellitus is associated with adverse prognosis in chronic heart failure of ischaemic and non-ischaemic aetiology. Diabetes Vasc. Dis. Res. (in press);.
8. Cubbon R.M., Wheatcroft S.B., Grant P.J., Gale C.P., Barth J.H., Sapsford R.J., et al. Temporal trends in mortality of patients with diabetes mellitus suffering acute myocardial infarction: a comparison of over 3000 patients between 1995 and 2003. Eur. Heart J.28540-5452007.
9. M. Lenzen, L. Ryden, J. Ohrvik, M. Bartnik, K. Malmberg, and W. Scholte op Reimer Diabetes known or newly detected, but not impaired glucose regulation, has a negative influence on 1-year outcome in patients with coronary artery disease: a report from the Euro Heart Survey on diabetes and the heart Eur. Heart J. 27 2006 2969 2974
10. R. Ross Atherosclerosis - an inflammatory disease N. Engl. J. Med. 340 1999 115 126
11. S.M. Grundy, H.B. Brewer Jr., J.I. Cleeman, S.C. Smith Jr., C. Lenfant for the Conference Participants Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association Conference on Scientific Issues Related to Definition Circulation 109 2004 433 438
12. P.J. Kuhlencordt, R. Gyurko, F. Han, M. Scherrer-Crosbie, T.H. Aretz, and R. Hajjar Accelerated atherosclerosis, aortic aneurysm formation, and ischemic heart disease in apolipoprotein E/endothelial nitric oxide synthase double-knockout mice Circulation 104 2001 448 454
13. B.M. Balletshofer, K. Rittig, M.D. Enderle, A. Volk, E. Maerker, and S. Jacob Endothelial dysfunction is detectable in young normotensive first-degree relatives of subjects with type 2 diabetes in association with insulin resistance Circulation 101 2000 1780 1784
14. S. Makimattila, M.L. Liu, J. Vakkilainen, A. Schlenzka, S. Lahdenpera, and M. Syvanne Impaired endothelium-dependent vasodilation in type 2 diabetes: relation to LDL size, oxidized LDL, and antioxidants Diabetes Care 22 1999 973 981
15. I.L. Williams, P.J. Chowienczyk, S.B. Wheatcroft, A. Patel, R. Sherwood, and A. Momin Effect of fat distribution on endothelial-dependent and endothelial-independent vasodilatation in healthy humans Diabetes Obes. Metab. 8 2006 296 301
16. J. Kim, M. Montagnani, K.K. Koh, and M.J. Quon Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms Circulation 113 2006 1888 1904
17. M. Cimini, S. Fazel, S. Zhuo, M. Xaymardan, H. Fujii, and R.D. Weisel c-kit dysfunction impairs myocardial healing after infarction Circulation 116 2007 I77 82
18. G. Foteinos, Y. Hu, Q. Xiao, B. Metzler, and Q. Xu Rapid endothelial turnover in atherosclerosis-prone areas coincides with stem cell repair in apolipoprotein E-deficient mice Circulation 117 2008 1856 1863
19. S. Dimmeler Regulation of bone marrow-derived vascular progenitor cell mobilization and maintenance Arterioscler. Thromb. Vasc. Biol 30 2010 1088 1093
20. E. Van Belle, C. Bauters, T. Asahara, and J.M. Isner Endothelial regrowth after arterial injury: from vascular repair to therapeutics Cardiovasc. Res. 38 1998 54 68
21. A. Zampetaki, J.P. Kirton, and Q. Xu Vascular repair by endothelial progenitor cells Cardiovasc. Res. 78 2008 413 421
22. E. Torsney, and Q. Xu Resident vascular progenitor cells J. Mol. Cell. Cardiol. 50 2011 304 311
23. M.K. Hagensen, M.K. Raarup, M.B. Mortensen, T. Thim, J.R. Nyengaard, and E. Falk Circulating endothelial progenitor cells do not contribute to regeneration of endothelium after murine arterial injury Cardiovasc. Res 93 2012 223 231
24. M.K. Hagensen, J. Shim, E. Falk, and J.F. Bentzon Flanking recipient vasculature, not circulating progenitor cells, contributes to endothelium and smooth muscle in murine allograft vasculopathy Arterioscler. Thromb. Vasc. Biol. 31 2011 808 813
25. M.K. Hagensen, J. Shim, T. Thim, E. Falk, and J.F. Bentzon Circulating endothelial progenitor cells do not contribute to plaque endothelium in murine atherosclerosis Circulation 121 2010 898 905
26. S. Rupp, M. Koyanagi, M. Iwasaki, J. Bauer, S. von Gerlach, and D. Schranz Characterization of long-term endogenous cardiac repair in children after heart transplantation. Eur. Heart J. 29 2008 1867 1872
27. S. Jiang, L. Walker, M. Afentoulis, D.A. Anderson, L. Jauron-Mills, and C.L. Corless Transplanted human bone marrow contributes to vascular endothelium Proc. Natl. Acad. Sci. USA 101 2004 16891 16896
28. M. Potente, H. Gerhardt, and P. Carmeliet Basic and therapeutic aspects of angiogenesis Cell 146 2011 873 887
29. M. Heil, I. Eitenmuller, T. Schmitz-Rixen, and W. Schaper Arteriogenesis versus angiogenesis: similarities and differences J. Cell. Mol. Med. 10 2006 45 55
30. S. Wedgwood, C.J. Mitchell, J.R. Fineman, and S.M. Black Developmental differences in the shear stress-induced expression of endothelial NO synthase: changing role of AP-1 Am. J. Physiol. Lung Cell. Mol. Physiol. 284 2003 L650 L662
31. E. Demicheva, M. Hecker, and T. Korff Stretch-induced activation of the transcription factor activator protein-1 controls monocyte chemoattractant protein-1 expression during arteriogenesis Circ. Res 103 2008 477 484
32. C. Coulon, M. Georgiadou, C. Roncal, K. De Bock, T. Langenberg, and P. Carmeliet From vessel sprouting to normalization Arterioscler. Thromb. Vasc. Biol. 30 2010 2331 2336
33. H.K. Eltzschig, and P. Carmeliet Hypoxia and inflammation N. Engl. J. Med. 364 2011 656 665
34. Y. Cao Adipose tissue angiogenesis as a therapeutic target for obesity and metabolic diseases Nat. Rev. Drug Discovery 9 2010 107 115
35. P. Carmeliet, and R.K. Jain Molecular mechanisms and clinical applications of angiogenesis Nature 473 2011 298 307
36. H.P. Hammes, Y. Feng, F. Pfister, and M. Brownlee Diabetic retinopathy: targeting vasoregression Diabetes 60 2011 9 16
37. L Jakobsson, K Bentley, and Gerhardt H. VEGFRs and Notch: a dynamic collaboration in vascular patterning Biochem. Soc. Trans. 37 2009 1233 1236
38. T. Asahara, T. Murohara, A. Sullivan, M. Silver, R. van der Zee, and T. Li Isolation of putative progenitor endothelial cells for angiogenesis Science 275 1997 964 966
39. M. Vasa, S. Fichtlscherer, K. Adler, A. Aicher, H. Martin, and A.M. Zeiher Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease Circulation 103 2001 2885 2890
40. + cells identifies a population of functional endothelial precursors Blood 95 2000 952 958
41. N. Werner, S. Kosiol, T. Schiegl, P. Ahlers, K. Walenta, and A. Link Circulating endothelial progenitor cells and cardiovascular outcomes N. Engl. J. Med. 353 2005 999 1007
42. K.K. Hirschi, D.A. Ingram, and M.C. Yoder Assessing identity, phenotype, and fate of endothelial progenitor cells Arterioscler. Thromb. Vasc. Biol. 28 2008 1584 1595
43. M. Prokopi, G. Pula, U. Mayr, C. Devue, J. Gallagher, and Q. Xiao Proteomic analysis reveals presence of platelet microparticles in endothelial progenitor cell cultures Blood 114 2009 723 732
44. J. Hur, C.H. Yoon, H.S. Kim, J.H. Choi, H.J. Kang, and K.K. Hwang Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis Arterioscler. Thromb. Vasc. Biol. 24 2004 288 293
45. J.M. Hill, G. Zalos, J.P.J. Halcox, W.H. Schenke, M.A. Waclawiw, and A.A. Quyyumi Circulating endothelial progenitor cells, vascular function, and cardiovascular risk N. Engl. J. Med. 348 2003 593 600
46. J. Hur, H.M. Yang, C.H. Yoon, C.S. Lee, K.W. Park, and J.H. Kim Identification of a novel role of T cells in postnatal vasculogenesis Circulation 116 2007 1671 1682
47. + cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors Exp. Hematol 35 2007 1109 1118
48. + hematopoietic precursors. Arterioscler Thromb. Vasc. Biol 27 2007 1572 1579
49. J.A. Mund, M.L. Estes, M.C. Yoder, D.A. Ingram, and J. Case Flow cytometric identification and functional characterization of immature and mature circulating endothelial cells Arterioscler. Thromb. Vasc. Biol. 32 2012 1045 1053
50. K.i. Ishigami, S. Uemura, Y. Morikawa, T. Soeda, S Okayama, and T Nishida Long-term follow-up of neointimal coverage of Sirolimus-eluting stents evaluation with optical coherence tomography Circ. J. 73 2009 2300 2307
51. A. Rivard, M. Silver, D. Chen, M. Kearney, M. Magner, and B. Annex Rescue of diabetes-related impairment of angiogenesis by intramuscular gene therapy with adeno-VEGF Am. J. Pathol. 154 1999 355 363
52. M.B. Kahn, N.Y. Yuldasheva, R.M. Cubbon, J. Smith, S.T. Rashid, and H. Viswambharan Insulin resistance impairs circulating angiogenic progenitor cell function and delays endothelial regeneration Diabetes 60 2011 1295 1303
53. Y.L. Chen, C.L. Chang, C.K. Sun, C.J. Wu, T.H. Tsai, and S.Y. Chung Impact of obesity control on circulating level of endothelial progenitor cells and angiogenesis in response to ischemic stimulation J. Transl. Med. 10 2012 86
54. R.M. Cubbon, S.R. Murgatroyd, C. Ferguson, T.S. Bowen, M. Rakobowchuk, and V. Baliga Human exercise-induced circulating progenitor cell mobilization is nitric oxide-dependent and is blunted in South Asian men Arterioscler. Thromb. Vasc. Biol. 30 2010 878 884
55. G.P. Fadini, M. Miorin, M. Facco, S. Bonamico, I. Baesso, and F. Grego Circulating endothelial progenitor cells are reduced in peripheral vascular complications of type 2 diabetes mellitus J. Am. Coll. Cardiol 45 2005 1449 1457
56. M. Ii, H. Takenaka, J. Asai, K. Ibusuki, Y. Mizukami, and K. Maruyama Endothelial progenitor thrombospondin-1 mediates diabetes-induced delay in reendothelialization following arterial injury Circ. Res. 98 2006 697 704
57. D.A. Ingram, I.Z. Lien, L.E. Mead, M. Estes, D.N. Prater, and E. Derr-Yellin In vitro hyperglycemia or a diabetic intrauterine environment reduces neonatal endothelial colony-forming cell numbers and function Diabetes 57 2008 724 731
58. G. Assmann, R. Guerra, G. Fox, P. Cullen, H. Schulte, and D. Willett Harmonizing the definition of the metabolic syndrome: comparison of the criteria of the Adult Treatment Panel III and the International Diabetes Federation in United States American and European populations Am. J. Cardiol. 99 2007 541 548
59. R. Noor, U. Shuaib, C.X. Wang, K. Todd, U. Ghani, and B. Schwindt High-density lipoprotein cholesterol regulates endothelial progenitor cells by increasing eNOS and preventing apoptosis Atherosclerosis 192 2007 92 99
60. V. Petoumenos, G. Nickenig, and N. Werner High-density lipoprotein exerts vasculoprotection via endothelial progenitor cells J. Cell. Mol. Med. 13 2009 4623 4635
61. F. Rossi, C. Bertone, F. Montanile, F. Miglietta, C. Lubrano, and L. Gandini HDL cholesterol is a strong determinant of endothelial progenitor cells in hypercholesterolemic subjects Microvasc. Res. 80 2010 274 279
62. D. Seetharam, C. Mineo, A.K. Gormley, L.L. Gibson, W. Vongpatanasin, and K.L. Chambliss High-density lipoprotein promotes endothelial cell migration and reendothelialization via scavenger receptor-B type I Circ. Res. 98 2006 63 72
63. Y. Feng, M. van Eck, E. Van Craeyveld, F. Jacobs, V. Carlier, and S. Van Linthout Critical role of scavenger receptor-B1-expressing bone marrow-derived endothelial progenitor cells in the attenuation of allograft vasculopathy after human apo A-I transfer Blood 113 2009 755 764
64. J. Chen, X. Cui, A. Zacharek, H. Jiang, C. Roberts, and C. Zhang Niaspan increases angiogenesis and improves functional recovery after stroke Ann. Neurol 62 2007 49 58
65. A.J. Murphy, M. Akhtari, S. Tolani, T. Pagler, N. Bijl, and C.L. Kuo ApoE regulates hematopoietic stem cell proliferation, monocytosis, and monocyte accumulation in atherosclerotic lesions in mice J. Clin. Invest. 121 2011 4138 4149
66. M. Westerterp, S. Gourion-Arsiquaud, A. Murphy, A. Shih, S. Cremers, and R. Levine Regulation of hematopoietic stem and progenitor cell mobilization by cholesterol efflux pathways Cell Stem Cell 11 2012 195 206
67. A. Noghero, A. Perino, G. Seano, E. Saglio, G.L. Sasso, and F. Veglio Liver X receptor activation reduces angiogenesis by impairing lipid raft localization and signaling of vascular endothelial growth factor receptor-2 Arterioscler. Thromb. Vasc. Biol. 32 2012 2280 2288
68. S. Hazra, A. Rasheed, A. Bhatwadekar, X. Wang, L.C. Shaw, and M. Patel Liver X receptor modulates diabetic retinopathy outcome in a mouse model of streptozotocin-induced diabetes Diabetes 61 2012 3270 3279
69. C. Besler, T.F. Luscher, and U. Landmesser Molecular mechanisms of vascular effects of high-density lipoprotein: alterations in cardiovascular disease EMBO Mol. Med. 4 2012 251 268
70. P.J. Barter, M. Caulfield, M. Eriksson, S.M. Grundy, J.J.P. Kastelein, and M. Komajda Effects of torcetrapib in patients at high risk for coronary events N. Engl. J. Med. 357 2007 2109 2122
71. AIM-HIGH Investigators, W.E. Boden, and J.L. Probstfield Niacin in patients with low HDL cholesterol levels receiving intensive statin therapy N. Engl. J. Med. 365 2011 2255 2267
72. L. Liu, T. Wen, X.y. Zheng, D.G. Yang, S.P. Zhao, and D.Y. Xu Remnant-like particles accelerate endothelial progenitor cells senescence and induce cellular dysfunction via an oxidative mechanism Atherosclerosis 202 2009 405 414
73. E. Miller-Kasprzak, P. Bogdanski, D. Pupek-Musialik, and P.P. Jagodzinski Insulin resistance and oxidative stress influence colony-forming unit-endothelial cells capacity in obese patients Obesity 19 2011 736 742
74. Q. Xiao, S. Kiechl, S. Patel, F. Oberhollenzer, S. Weger, and A. Mayr Endothelial progenitor cells, cardiovascular risk factors, cytokine levels and atherosclerosis: results from a large population-based study PLoS ONE 2007 e975
75. T.S. Li, M. Kubo, K. Ueda, M. Murakami, M. Ohshima, and T. Kobayashi Identification of risk factors related to poor angiogenic potency of bone marrow cells from different patients Circulation 120 2009 S255 S261
76. W.X. Guo, Q.D. Yang, Y.H. Liu, X.Y. Xie, M. Wang, and R.C. Niu Palmitic and linoleic acids impair endothelial progenitor cells by inhibition of Akt/eNOS pathway Arch. Med. Res. 39 2008 434 442
77. M. Vasa, S. Fichtlscherer, A. Aicher, K. Adler, C. Urbich, and H. Martin Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease Circ. Res. 2001 e1 e7
78. - microparticles to endothelial progenitors as a novel marker of atherosclerosis in hypercholesterolemia Arterioscler. Thromb. Vasc. Biol. 26 2006 2530 2535
79. G. Croce, G. Passacquale, S. Necozione, C. Ferri, and G. Desideri Nonpharmacological treatment of hypercholesterolemia increases circulating endothelial progenitor cell population in adults Arterioscler. Thromb. Vasc. Biol. 2006 e38 e39
80. D. Tirziu, K.L. Moodie, Z.W. Zhuang, K. Singer, A. Helisch, and J.F. Dunn Delayed arteriogenesis in hypercholesterolemic mice Circulation 112 2005 2501 2509
81. F.S. Czepluch, A. Bergler, and J. Waltenberger Hypercholesterolaemia impairs monocyte function in CAD patients J. Intern. Med. 261 2007 201 204
82. P. Haddad, S. Dussault, J. Groleau, J. Turgeon, F. Maingrette, and A. Rivard Nox2-derived reactive oxygen species contribute to hypercholesterolemia- induced inhibition of neovascularization: effects on endothelial progenitor cells and mature endothelial cells Atherosclerosis 217 2011 340 349
83. I. Avraham-Davidi, Y. Ely, V.N. Pham, D. Castranova, M. Grunspan, and G. Malkinson ApoB-containing lipoproteins regulate angiogenesis by modulating expression of VEGF receptor 1 18 2012 967 973 Nat. Med. 18 2012 967 973
84. G. Tie, J. Yan, Y. Yang, B.D. Park, J.A. Messina, and R.L. Raffai Oxidized low-density lipoprotein induces apoptosis in endothelial progenitor cells by inactivating the phosphoinositide 3-kinase/Akt pathway J. Vasc. Res. 47 2010 519 530
85. T. Imanishi, C. Moriwaki, T. Hano, and I. Nishio Endothelial progenitor cell senescence is accelerated in both experimental hypertensive rats and patients with essential hypertension J. Hypertens 23 2005 1831 1837
86. T. Umemura, J. Soga, T. Hidaka, H. Takemoto, S. Nakamura, and D. Jitsuiki Aging and hypertension are independent risk factors for reduced number of circulating endothelial progenitor cells Am. J. Hypertens 21 2008 1203 1209
87. P. Delva, M. Degan, P. Vallerio, E. Arosio, P. Minuz, and G. Amen Endothelial progenitor cells in patients with essential hypertension J. Hypertens. 25 2007 127 132
88. C. Endtmann, T. Ebrahimian, T. Czech, O. Arfa, U. Laufs, and M. Fritz Angiotensin II impairs endothelial progenitor cell number and function in vitro and in vivo Hypertension 58 2011 394 403
89. T. Thum, K. Schmitter, F. Fleissner, V. Wiebking, B. Dietrich, and J.D. Widder Impairment of endothelial progenitor cell function and vascularization capacity by aldosterone in mice and humans Eur. Heart J. 32 2011 1275 1286
90. D.D. Chen, Y.G. Dong, H. Yuan, and A.F. Chen Endothelin 1 activation of endothelin A receptor/NADPH oxidase pathway and diminished antioxidants critically contribute to endothelial progenitor cell reduction and dysfunction in salt-sensitive hypertension Hypertension 59 2012 1037 1043
91. F. Michel, M.L. Ambroisine, M. Duriez, C. Delcayre, B.I. Levy, and J.S. Silvestre Aldosterone enhances ischemia-induced neovascularization through angiotensin II-dependent pathway Circulation 109 2004 1933 1937
92. V.C. Munk, L. Sanchez de Miguel, M. Petrimpol, N. Butz, A. Banfi, and U. Eriksson Angiotensin II induces angiogenesis in the hypoxic adult mouse heart in vitro through an AT2-B2 receptor pathway Hypertension 49 2007 1178 1185
93. G.J. Padfield, O. Tura, M.L.A. Haeck, A. Short, E. Freyer, and G.R. Barclay Circulating endothelial progenitor cells are not affected by acute systemic inflammation Am. J. Physiol. Heart Circ. Physiol. 298 2010 H2054 H2061
94. J. Grisar, D. Aletaha, C.W. Steiner, T. Kapral, S. Steiner, and D. Seidinger Depletion of endothelial progenitor cells in the peripheral blood of patients with rheumatoid arthritis Circulation 111 2005 204 211
95. H. Fujii, S.H. Li, P.E. Szmitko, P.W.M. Fedak, and S. Verma C-reactive protein alters antioxidant defenses and promotes apoptosis in endothelial progenitor cells Arterioscler. Thromb. Vasc. Biol. 26 2006 2476 2482
96. F.H. Seeger, J. Haendeler, D.H. Walter, U. Rochwalsky, J. Reinhold, and C. Urbich p38 mitogen-activated protein kinase downregulates endothelial progenitor cells Circulation 111 2005 1184 1191
97. S. Verma, M.A. Kuliszewski, S.H. Li, P.E. Szmitko, L. Zucco, and C.H. Wang C-reactive protein attenuates endothelial progenitor cell survival, differentiation, and function: further evidence of a mechanistic link between C-reactive protein and cardiovascular disease Circulation 109 2004 2058 2067
98. C.V. Desouza, F.G. Hamel, K. Bidasee, and K. O'Connell Role of inflammation and insulin resistance in endothelial progenitor cell dysfunction Diabetes 60 2011 1286 1294
99. A.B. Aurora, D. Biyashev, Y. Mirochnik, T.A. Zaichuk, C. Sanchez-Martinez, and M.A. Renault NF-κB balances vascular regression and angiogenesis via chromatin remodeling and NFAT displacement Blood 116 2010 475 484
100. Y. Hasegawa, T. Saito, T. Ogihara, Y. Ishigaki, T. Yamada, and J. Imai Blockade of the nuclear factor-κB pathway in the endothelium prevents insulin resistance and prolongs life spans/clinical perspective Circulation 125 2012 1122 1133
101. E. Stabile, M.S. Burnett, C. Watkins, T. Kinnaird, A. Bachis, and A. la Sala Impaired arteriogenic response to acute hindlimb ischemia in CD4-knockout mice Circulation 108 2003 205 210
102. Y. Wu, J.E. Ip, J. Huang, L. Zhang, K. Matsushita, and C.C. Liew Essential role of ICAM-1/CD18 in mediating EPC recruitment, angiogenesis, and repair to the infarcted myocardium Circ. Res. 99 2006 315 322
103. C.H. Yoon, J. Hur, I.Y. Oh, K.W. Park, T.Y. Kim, and J.H. Shin Intercellular adhesion molecule-1 is upregulated in ischemic muscle, which mediates trafficking of endothelial progenitor cells Arterioscler. Thromb. Vasc. Biol. 26 2006 1066 1072
104. M. Heil, T. Ziegelhoeffer, F. Pipp, S. Kostin, S. Martin, and M. Clauss Blood monocyte concentration is critical for enhancement of collateral artery growth Am. J. Physiol. Heart Circ. Physiol 283 2002 H2411 H2419
105. B. Schweighofer, J. Testori, C. Sturtzel, S. Sattler, H. Mayer, and O. Wagner The VEGF-induced transcriptional response comprises gene clusters at the crossroad of angiogenesis and inflammation Thromb. Haemostasis 102 2009 544 554
106. J.S. Silvestre, Z. Mallat, A. Tedgui, and B.I. Levy Post-ischaemic neovascularization and inflammation Cardiovasc. Res. 78 2008 242 249
107. J. Chang, Y. Li, Y. Huang, K.S.L. Lam, R.L.C. Hoo, and W.T. Wong Adiponectin prevents diabetic premature senescence of endothelial progenitor cells and promotes endothelial repair by suppressing the p38 MAP kinase/p16INK4A signaling pathway Diabetes 59 2010 2949 2959
108. + monocytes in vitro J. Cell. Mol. Med 10 2006 459 469
109. P.H. Huang, J.S. Chen, H.Y. Tsai, Y.H. Chen, F.Y. Lin, and H.B. Leu Globular adiponectin improves high glucose-suppressed endothelial progenitor cell function through endothelial nitric oxide synthase dependent mechanisms J. Mol. Cell. Cardiol. 51 2011 109 119
110. N. Ouchi, H. Kobayashi, S. Kihara, M. Kumada, K. Sato, and T. Inoue Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells J. Biol. Chem. 279 2004 1304 1309
111. K. Sharma, S. RamachandraRao, G. Qiu, H.K. Usui, Y. Zhu, and S.R. Dunn Adiponectin regulates albuminuria and podocyte function in mice J. Clin. Invest. 118 2008 1645 1656
112. M.R. Schroeter, M. Leifheit, P. Sudholt, N.M. Heida, C. Dellas, and I. Rohm Leptin enhances the recruitment of endothelial progenitor cells into neointimal lesions after vascular injury by promoting integrin-mediated adhesion Circ. Res. 103 2008 536 544
113. R. Wolk, A. Deb, N.M. Caplice, and V.K. Somers Leptin receptor and functional effects of leptin in human endothelial progenitor cells Atherosclerosis 183 2005 131 139
114. M.R. Schroeter, S. Stein, N.M. Heida, M. Leifheit-Nestler, I.F. Cheng, and R. Gogiraju Leptin promotes the mobilization of vascular progenitor cells and neovascularization by NOX2-mediated activation of MMP9 Cardiovasc. Res. 93 2012 170 180
115. R. Cao, E. Brakenhielm, C. Wahlestedt, J. Thyberg, and Y. Cao Leptin induces vascular permeability and synergistically stimulates angiogenesis with FGF-2 and VEGF Proc. Natl. Acad. Sci. USA 98 2001 6390 6395
116. A. Bouloumie, H.C.A. Drexler, M. Lafontan, and R Busse Leptin, the product of Ob gene, promotes angiogenesis Circ. Res. 83 1998 1059 1066
117. K. Aronis, K. Diakopoulos, C. Fiorenza, J. Chamberland, and C. Mantzoros Leptin administered in physiological or pharmacological doses does not regulate circulating angiogenesis factors in humans Diabetologia 54 2011 2358 2367
118. Y. Sun, S. Chen, G. Song, L. Ren, L. Wei, and N. Liu Effect of visfatin on the function of endothelial progenitor cells in high-fat-fed obese rats and investigation of its mechanism of action Int. J. Mol. Med 30 2012 628
119. S. Vallejo, T. Romacho, J. Angulo, L.A. Villalobos, E. Cercas, and A. Leivas Visfatin impairs endothelium-dependent relaxation in rat and human mesenteric microvessels through nicotinamide phosphoribosyltransferase activity PLoS ONE 6 2011 e27299 2011
120. R. Adya, B.K. Tan, A. Punn, J. Chen, and H.S. Randeva Visfatin induces human endothelial VEGF and MMP-2/9 production via MAPK and PI3K/Akt signalling pathways: novel insights into visfatin-induced angiogenesis Cardiovasc. Res. 78 2008 356 365
121. J.W. Park, W.H. Kim, S.H. Shin, J.Y. Kim, M.R. Yun, and K.J. Park Visfatin exerts angiogenic effects on human umbilical vein endothelial cells through the mTOR signaling pathway Biochim. Biophys. Acta 1813 2011 763 771
122. Y.H. Bae, H.J. Park, S.R. Kim, J.Y. Kim, Y. Kang, and J.A. Kim Notch1 mediates visfatin-induced FGF-2 up-regulation and endothelial angiogenesis Cardiovasc. Res. 89 2011 436 445
123. F. Lovren, Y. Pan, P.C. Shukla, A. Quan, H. Teoh, and P.E. Szmitko Visfatin activates eNOS via Akt and MAP kinases and improves endothelial cell function and angiogenesis in vitro and in vivo: translational implications for atherosclerosis Am. J. Physiol. Endocrinol. Metab. 296 2009 E1440 E1449
124. H. Mu, R. Ohashi, S. Yan, H. Chai, H. Yang, and P. Lin Adipokine resistin promotes in vitro angiogenesis of human endothelial cells Cardiovasc. Res. 70 2006 146 157
125. Y. Cho, S.E. Lee, H.C. Lee, J. Hur, S. Lee, and S.W. Youn Adipokine resistin is a key player to modulate monocytes, endothelial cells, and smooth muscle cells, leading to progression of atherosclerosis in rabbit carotid artery J. Am. Coll. Cardiol. 57 2011 99 109
126. D.J. Schneider Abnormalities of coagulation, platelet function, and fibrinolysis associated with syndromes of insulin resistance Coron. Artery Dis. 16 2005 473 476
127. I. Mertens, A. Verrijken, J.J. Michiels, M. Van der Planken, J.B. Ruige, and L.F. Van Gaal Among inflammation and coagulation markers, PAI-1 is a true component of the metabolic syndrome Int. J. Obes. 30 2006 1308 1314
128. M. Ohki, Y. Ohki, M. Ishihara, C. Nishida, Y. Tashiro, and H. Akiyama Tissue type plasminogen activator regulates myeloid-cell dependent neoangiogenesis during tissue regeneration Blood 115 2010 4302 4312
129. S. Heymans, A. Luttun, D. Nuyens, G. Theilmeier, E. Creemers, and L. Moons Inhibition of plasminogen activators or matrix metalloproteinases prevents cardiac rupture but impairs therapeutic angiogenesis and causes cardiac failure Nat. Med. 5 1999 1135 1142
130. K. Bajou, A. Noel, R.D. Gerard, V. Masson, N. Brunner, and C. Holst-Hansen Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization Nat. Med. 4 1998 923 928
131. R.D. Starke, F. Ferraro, K.E. Paschalaki, N.H. Dryden, T.A.J. McKinnon, and R.E. Sutton Endothelial von Willebrand factor regulates angiogenesis Blood 117 2011 1071 1080
132. S.H. Alzahrani, and R.A. Ajjan Coagulation and fibrinolysis in diabetes Diabetes Vasc. Dis. Res. 7 2010 260 273
133. A. Sahni, A.A. Khorana, R.B. Baggs, H. Peng, and C.W. Francis FGF-2 binding to fibrin(ogen) is required for augmented angiogenesis Blood 107 2006 126 131
134. K. Abe, M. Shoji, J. Chen, A. Bierhaus, I. Danave, and C. Micko Regulation of vascular endothelial growth factor production and angiogenesis by the cytoplasmic tail of tissue factor Proc. Natl. Acad. Sci. USA 96 1999 8663 8668
135. A.T. Nurden Platelets, inflammation and tissue regeneration Thromb. Haemostasis 105 2011 S13 S33
136. E.R. Nuzzolo, M.G. Iachininoto, and L. Teofili Endothelial progenitor cells and thrombosis Thromb. Res. 129 2012 309 313
137. Y.H. Chen, S.J. Lin, F.Y. Lin, T.C. Wu, C.R. Tsao, and P.H. Huang High glucose impairs early and late endothelial progenitor cells by modifying nitric oxide related but not oxidative stress-mediated mechanisms Diabetes 56 2007 1559 1568
138. E. Larger, M. Marre, P. Corvol, and J.M. Gasc Hyperglycemia-induced defects in angiogenesis in the chicken chorioallantoic membrane model Diabetes 53 2004 752 761
139. J.X. Chen, and A. Stinnett Disruption of Ang-1/Tie-2 signaling contributes to the impaired myocardial vascular maturation and angiogenesis in type II diabetic mice Arterioscler. Thromb. Vasc. Biol 28 2008 1606 1613
140. D. Yao, T. Taguchi, T. Matsumura, R. Pestell, D. Edelstein, and I. Giardino High glucose increases angiopoietin-2 transcription in microvascular endothelial cells through methylglyoxal modification of mSin3A J. Biol. Chem. 282 2007 31038 31045
141. H.P. Hammes, J. Lin, P. Wagner, Y. Feng, F. vom Hagen, and T. Krzizok Angiopoietin-2 causes pericyte dropout in the normal retina: evidence for involvement in diabetic retinopathy Diabetes 53 2004 1104 1110
142. H. Singh, N.P.J. Brindle, and V.A Zammit High glucose and elevated fatty acids suppress signaling by the endothelium protective ligand angiopoietin-1 Microvasc. Res 79 2010 121 127
143. P. Geraldes, J. Hiraoka-Yamamoto, M. Matsumoto, A. Clermont, M. Leitges, and A. Marette Activation of PKC-[delta] and SHP-1 by hyperglycemia causes vascular cell apoptosis and diabetic retinopathy Nat. Med. 15 2009 1298 1306
144. M. Tanii, Y. Yonemitsu, T. Fujii, Y. Shikada, R.i. Kohno, and M. Onimaru Diabetic microangiopathy in ischemic limb is a disease of disturbance of the platelet-derived growth factor-BB/protein kinase C axis but not of impaired expression of angiogenic factors Circ. Res. 98 2006 55 62
145. G. Fadini, L. Pucci, R. Vanacore, I. Baesso, G. Penno, and A. Balbarini Glucose tolerance is negatively associated with circulating progenitor cell levels Diabetologia 50 2007 2156 2163
146. C.J.M. Loomans, E.J.P. de Koning, F.J.T. Staal, M.B. Rookmaaker, C. Verseyden, and H.C. de Boer Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes Diabetes 53 2004 195 199
147. L. Sibal, A. Aldibbiat, S. Agarwal, G. Mitchell, C. Oates, and S. Razvi Circulating endothelial progenitor cells, endothelial function, carotid intima-media thickness and circulating markers of endothelial dysfunction in people with type 1 diabetes without macrovascular disease or microalbuminuria Diabetologia 52 2009 1464 1473
148. T.G. Ebrahimian, C. Heymes, D. You, O. Blanc-Brude, B. Mees, and L. Waeckel NADPH oxidase-derived overproduction of reactive oxygen species impairs postischemic neovascularization in mice with type 1 diabetes Am. J. Pathol. 169 2006 719 728
149. M. Salis, G. Graiani, E. Desortes, R. Caldwell, P. Madeddu, and C. Emanueli Nerve growth factor supplementation reverses the impairment, induced by type 1 diabetes, of hindlimb post-ischaemic recovery in mice Diabetologia 47 2004 1055 1063
150. J.D. Luo, T.P. Hu, L. Wang, M.S. Chen, S.M. Liu, and A.F. Chen Sonic hedgehog improves delayed wound healing via enhancing cutaneous nitric oxide function in diabetes Am. J. Physiol. Endocrinol. Metab. 297 2009 E525 E531
151. L. Tie, X.J. Li, X. Wang, K.M. Channon, A.F. Chen, and GTP Endothelium-specific cyclohydrolase I overexpression accelerates refractory wound healing by suppressing oxidative stress in diabetes Am. J. Physiol. Endocrinol. Metab. 296 2009 E1423 E1429
152. J.M. van Golde, M.S. Ruiter, N.C. Schaper, S. Voo, J. Waltenberger, and W.H. Backes Impaired collateral recruitment and outward remodeling in experimental diabetes Diabetes 57 2008 2818 2823
153. K. Kinnunen, T. Puustjarvi, M. Terasvirta, P. Nurmenniemi, T. Heikura, and S. Laidinen Differences in retinal neovascular tissue and vitreous humour in patients with type 1 and type 2 diabetes Br. J. Ophthalmol. 93 2009 1109 1115
154. M. Jonas, E.R. Edelman, A. Groothuis, A.B. Baker, P. Seifert, and C. Rogers Vascular neointimal formation and signaling pathway activation in
155. J. Yan, G. Tie, B. Park, Y. Yan, P.T. Nowicki, and L.M. Messina Recovery from hind limb ischemia is less effective in type 2 than in type 1 diabetic mice: roles of endothelial nitric oxide synthase and endothelial progenitor cells J. Vasc. Surg. 50 2009 1412 1422
156. R.M. Cubbon, H. Viswambharan, V. Baliga, N. Yuldasheva, S. Stephen, and J. Askham Akt-gene-based restoration of Akt activity in endothelial progenitor cells from human subjects at high cardiovascular risk rescues vascular reparative capacity Heart 98 2012 A1
157. A. Belfiore, F. Frasca, G. Pandini, L. Sciacca, and R. Vigneri Insulin receptor isoforms and insulin receptor/insulin-like growth factor receptor hybrids in physiology and disease Endocr. Rev. 30 2009 586 623
158. T. Kondo, D. Vicent, K. Suzuma, M. Yanagisawa, G.L. King, and M. Holzenberger Knockout of insulin and IGF-1 receptors on vascular endothelial cells protects against retinal neovascularization J. Clin. Invest. 111 2003 1835 1842
159. T. Kondo, A. Hafezi-Moghadam, K. Thomas, D.D. Wagner, and C.R. Kahn Mice lacking insulin or insulin-like growth factor 1 receptors in vascular endothelial cells maintain normal blood-brain barrier Biochem. Biophys. Res. Commun. 317 2004 315 320
160. S.Y. Aghdam, S.A. Eming, S. Willenborg, B. Neuhaus, C.M. Niessen, and L. Partridge Vascular endothelial insulin/IGF-1 signaling controls skin wound vascularization Biochem. Biophys. Res. Commun. 421 2012 197 202
161. Z. He, D.M. Opland, K.J. Way, K. Ueki, N. Bodyak, and P.M. Kang Regulation of vascular endothelial growth factor expression and vascularization in the myocardium by insulin receptor and PI3K/Akt pathways in insulin resistance and ischemia Arterioscler. Thromb. Vasc. Biol. 26 2006 787 793
162. Y.s. Yoon, S. Uchida, O. Masuo, M. Cejna, J.S. Park, and H Gwon c., et al. Progressive attenuation of myocardial vascular endothelial growth factor expression is a seminal event in diabetic cardiomyopathy Circulation 111 2005 2073 2085
163. Z.Y. Jiang, Z. He, B.L. King, T. Kuroki, D.M. Opland, and K. Suzuma Characterization of multiple signaling pathways of insulin in the regulation of vascular endothelial growth factor expression in vascular cells and angiogenesis J. Biol. Chem 278 2003 31964 31971
164. Y. Maeno, Q. Li, K. Park, C. Rask-Madsen, B. Gao, and M. Matsumoto Inhibition of insulin signaling in endothelial cells by protein kinase C-induced phosphorylation of p85 subunit of phosphatidylinositol 3-kinase (PI3K) J. Biol. Chem. 287 2012 4518 4530
165. G.I. Welsh, L.J. Hale, V. Eremina, M. Jeansson, Y. Maezawa, and R. Lennon Insulin signaling to the glomerular podocyte is critical for normal kidney function Cell Metab. 12 2010 329 340
166. S. Han, C.P. Liang, T. DeVries-Seimon, M. Ranalletta, C.L. Welch, and K. Collins-Fletcher Macrophage insulin receptor deficiency increases ER stress-induced apoptosis and necrotic core formation in advanced atherosclerotic lesions Cell Metab. 3 2006 257 266
167. J. Baumgartl, S. Baudler, M. Scherner, V. Babaev, L. Makowski, and J. Suttles Myeloid lineage cell-restricted insulin resistance protects apolipoproteinE-deficient mice against atherosclerosis Cell Metab. 3 2006 247 256
168. J. Waltenberger, J. Lange, and A. Kranz Vascular endothelial growth factor-A induced chemotaxis of monocytes is attenuated in patients with diabetes mellitus Circulation 102 2000 185 190
169. V. Tchaikovski, S. Olieslagers, F. Bohmer, and J. Waltenberger Diabetes mellitus activates signal transduction pathways resulting in vascular endothelial growth factor resistance of human monocytes Circulation 120 2009 150 159
170. S. Olieslagers, E. Pardali, V. Tchaikovski, P. ten Dijke, and J. Waltenberger TGF-β1/ALK5-induced monocyte migration involves PI3K and p38 pathways and is not negatively affected by diabetes mellitus Cardiovasc. Res. 91 2011 510 518
171. H. Gehart, S. Kumpf, A. Ittner, and R. Ricci MAPK signalling in cellular metabolism: stress or wellness? EMBO Rep. 11 2010 834 840
172. Y.H. Lee, J. Giraud, R.J. Davis, and M.F. White c-Jun N-terminal kinase (JNK) mediates feedback inhibition of the insulin signaling cascade J. Biol. Chem. 278 2003 2896 2902
173. C. Miele, A. Riboulet, M.A. Maitan, F. Oriente, C. Romano, and P. Formisano Human glycated albumin affects glucose metabolism in L6 skeletal muscle cells by impairing insulin-induced insulin receptor substrate (IRS) signaling through a protein kinase C-alpha mediated mechanism J. Biol. Chem. 278 2003 47376 47387
174. Z. Gao, D. Hwang, F. Bataille, M. Lefevre, D. York, and M.J. Quon Serine phosphorylation of insulin receptor substrate 1 by inhibitor κB kinase complex J. Biol. Chem. 277 2002 48115 48121
175. Z. Gao, X. Zhang, A. Zuberi, D. Hwang, M.J. Quon, and M. Lefevre Inhibition of insulin sensitivity by free fatty acids requires activation of multiple serine kinases in 3T3-L1 adipocytes Mol. Endocrinol. 18 2004 2024 2034
176. J. Kim, D.C. Yeh, M. Ver, Y. Li, A. Carranza, and T.P. Conrads Phosphorylation of Ser24 in the pleckstrin homology domain of insulin receptor substrate-1 by mouse pelle-like kinase/interleukin-1 receptor-associated kinase J. Biol. Chem. 280 2005 23173 23183
177. M.T.A. Nguyen, H. Satoh, S. Favelyukis, J.L. Babendure, T. Imamura, and J.I. Sbodio JNK and tumor necrosis factor-alpha mediate free fatty acid-induced insulin resistance in 3T3-L1 adipocytes J. Biol. Chem. 280 2005 35361 35371
178. Y. Li, T.J. Soos, X. Li, J. Wu, M. DeGennaro, and X. Sun Protein kinase C-theta inhibits insulin signaling by phosphorylating IRS1 at Ser1101 J. Biol. Chem 279 2004 45304 45307
179. M. Yuan, N. Konstantopoulos, J. Lee, L. Hansen, Z.W. Li, and M. Karin Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of IKK-beta Science 293 2001 1673 1677
180. J. Hirosumi, G. Tuncman, L. Chang, C.Z. Gorgun, K.T. Uysal, and K. Maeda A central role for JNK in obesity and insulin resistance Nature 420 2002 333 336
181. T. Kubota, N. Kubota, M. Moroi, Y. Terauchi, T. Kobayashi, and K. Kamata Lack of insulin receptor substrate-2 causes progressive neointima formation in response to vessel injury Circulation 107 2003 3073 3080
182. J.D. Symons, S.L. McMillin, C. Riehle, J. Tanner, M. Palionyte, and E. Hillas Contribution of insulin and Akt1 signaling to endothelial nitric oxide synthase in the regulation of endothelial function and blood pressure Circ. Res. 104 2009 1085 1094
183. T. Kito, R. Shibata, M. Kondo, T. Yamamoto, H. Suzuki, and M. Ishii Nifedipine ameliorates ischemia-induced revascularization in diet-induced obese mice Am. J. Hypertens 25 2012 401 406
184. C.Y. Wang, H.H. Kim, Y. Hiroi, N. Sawada, S. Salomone, and L.E. Benjamin Obesity increases vascular senescence and susceptibility to ischemic injury through chronic activation of Akt and mTOR Sci. Signaling 2 2009 ra11
185. H. Miyauchi, T. Minamino, K. Tateno, T. Kunieda, H. Toko, and I. Komuro Akt negatively regulates the in vitro lifespan of human endothelial cells via a p53/p21-dependent pathway EMBO J. 23 2004 212 220
186. J.i. Nishi, T. Minamino, H. Miyauchi, A. Nojima, K. Tateno, and S. Okada Vascular endothelial growth factor receptor-1 regulates postnatal angiogenesis through inhibition of the excessive activation of Akt Circ. Res. 103 2008 261 268
187. E. Ackah, J. Yu, S. Zoellner, Y. Iwakiri, C. Skurk, and R. Shibata Akt1/protein kinase B-alpha is critical for ischemic and VEGF-mediated angiogenesis J. Clin. Invest 115 2005 2119 2127
188. C. Fernandez-Hernando, E. Ackah, J. Yu, Y. Suírez, T. Murata, and Y. Iwakiri Loss of Akt1 leads to severe atherosclerosis and occlusive coronary artery disease Cell Metab. 6 2007 446 457
189. Q.J. Zhang, W.L. Holland, L. Wilson, J.M. Tanner, D. Kearns, and J.M. Cahoon Ceramide mediates vascular dysfunction in diet-induced obesity by PP2A-mediated dephosphorylation of the eNOS-Akt complex Diabetes 61 2012 1848 1859
190. J.H. Lee, T. Palaia, and L. Ragolia Impaired insulin-mediated vasorelaxation in diabetic Goto-Kakizaki rats is caused by impaired Akt phosphorylation Am. J. Physiol. Cell Physiol. 296 2009 C327 C338
191. B.H. Jiang, J.Z. Zheng, M. Aoki, and P.K. Vogt Phosphatidylinositol 3-kinase signaling mediates angiogenesis and expression of vascular endothelial growth factor in endothelial cells Proc. Natl. Acad. Sci. USA 97 2000 1749 1753
192. E. Chavakis, G. Carmona, C. Urbich, S. Gottig, R. Henschler, and J.M. Penninger Phosphatidylinositol-3-kinase-gamma is integral to homing functions of progenitor cells Circ. Res. 102 2008 942 949
193. P. Madeddu, N. Kraenkel, L.S. Barcelos, M. Siragusa, P. Campagnolo, and A. Oikawa Phosphoinositide 3-kinase-gamma gene knockout impairs postischemic neovascularization and endothelial progenitor cell functions Arterioscler. Thromb. Vasc. Biol. 28 2008 68 76
194. Schleicher M., Yu J., Murata T., Derakhshan B., Atochin D., Qian L., et al. The Akt1-eNOS axis illustrates the specificity of kinase-substrate relationships in vivoSci. Signaling2ra41; 2009.
195. T. Murohara, T. Asahara, M. Silver, C. Bauters, H. Masuda, and C. Kalka Nitric oxide synthase modulates angiogenesis in response to tissue ischemia J. Clin. Invest. 101 1998 2567 2578
196. A. Aicher, C. Heeschen, C. Mildner-Rihm, C. Urbich, C. Ihling, and K. Technau-Ihling Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells Nat. Med. 9 2003 1370 1376
197. M.S. Segal, R. Shah, A. Afzal, C.M. Perrault, K. Chang, and A. Schuler Nitric oxide cytoskeletal-induced alterations reverse the endothelial progenitor cell migratory defect associated with diabetes Diabetes 55 2006 102 109
198. A. Ceriello, and E. Motz Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited Arterioscler. Thromb. Vasc. Biol. 24 2004 816 823
199. F. Giacco, and M. Brownlee Oxidative stress and diabetic complications Circ. Res. 107 2010 1058 1070
200. R.A. Benndorf, E. Schwedhelm, A. Gnann, R. Taheri, G. Kom, and M. Didie Isoprostanes inhibit vascular endothelial growth factor-induced endothelial cell migration, tube formation, and cardiac vessel sprouting in vitro, as well as angiogenesis in vivo via activation of the thromboxane A2 receptor: a potential link between oxidative stress and impaired angiogenesis Circ. Res 103 2008 1037 1046
201. D.A. Ingram, T.R. Krier, L.E. Mead, C. McGuire, D.N. Prater, and J. Bhavsar Clonogenic endothelial progenitor cells are sensitive to oxidative stress Stem Cells 25 2007 297 304
202. S.A. Sorrentino, F.H. Bahlmann, C. Besler, M. Muller, S. Schulz, and N. Kirchhoff Oxidant stress impairs in vivo reendothelialization capacity of endothelial progenitor cells from patients with type 2 diabetes mellitus: restoration by the peroxisome proliferator-activated receptor-{gamma} agonist rosiglitazone Circulation 116 2007 163 173
203. T. Thum, D. Fraccarollo, M. Schultheiss, S. Froese, P. Galuppo, and J.D. Widder Endothelial nitric oxide synthase uncoupling impairs endothelial progenitor cell mobilization and function in diabetes Diabetes 56 2007 666 674
204. D.J. Ceradini, D. Yao, R.H. Grogan, M.J. Callaghan, D. Edelstein, and M. Brownlee Decreasing intracellular superoxide corrects defective ischemia-induced new vessel formation in diabetic mice J. Biol. Chem. 283 2008 10930 10938
205. K. Schroder, A. Kohnen, A. Aicher, E.A. Liehn, T. Buchse, and S. Stein NADPH oxidase Nox2 is required for hypoxia-induced mobilization of endothelial progenitor cells Circ. Res. 105 2009 537 544
206. N. Urao, H. Inomata, M. Razvi, H.W. Kim, K. Wary, and R. McKinney Role of Nox2-based NADPH oxidase in bone marrow and progenitor cell function involved in neovascularization induced by hindlimb ischemia Circ. Res. 103 2008 212 220
207. M. Ushio-Fukai, Y. Tang, T. Fukai, S.I. Dikalov, Y. Ma, and M. Fujimoto Novel role of gp91phox-containing NAD(P)H oxidase in vascular endothelial growth factor-induced signaling and angiogenesis Circ. Res. 91 2002 1160 1167
208. L. Serrander, L. Cartier, K. Bedard, B. Banfi, B. Lardy, and O. Plastre NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation Biochem. J. 406 2007 105 114
209. K. Schroder, M. Zhang, S. Benkhoff, A. Mieth, R. Pliquett, and J. Kosowski Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase Circ. Res. 110 2012 1217 1225
210. S.M. Craige, K. Chen, Y. Pei, C. Li, and X. Huang Chen, et al. NADPH oxidase 4 promotes endothelial angiogenesis through endothelial nitric oxide synthase activation/clinical perspective Circulation 124 2011 731 740
211. M. Zhang, A.C. Brewer, K. Schroder, C.X.C. Santos, D.J. Grieve, and M. Wang NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis Proc. Natl. Acad. Sci. USA 107 2010 18121 18126
212. D. Meng, A. Mei, J. Liu, X. Kang, X. Shi, and R. Qian NADPH oxidase 4 mediates insulin-stimulated HIF-1a and VEGF expression, and angiogenesis in vitro. PLoS ONE e48393 2012
213. J. Li, J.J. Wang, Q. Yu, K. Chen, K. Mahadev, and S.X. Zhang Inhibition of reactive oxygen species by lovastatin downregulates vascular endothelial growth factor expression and ameliorates blood-retinal barrier breakdown in db/db mice: role of NADPH oxidase 4 Diabetes 59 2010 1528 1538
214. B. Lener, R. Koziel, H. Pircher, E. Hutter, R. Greussing, and D. Herndler-Brandstetter The NADPH oxidase Nox4 restricts the replicative lifespan of human endothelial cells Biochem. J. 423 2009 363 374
215. C. Kleinschnitz, H. Grund, K. Wingler, M.E. Armitage, E. Jones, and M. Mittal Post-stroke inhibition of induced NADPH oxidase type 4 prevents oxidative stress and neurodegeneration PLoS Biol 2010 e1000479
216. E.R. Duncan, P.A. Crossey, S. Walker, N. Anilkumar, L. Poston, and G. Douglas Effect of endothelium-specific insulin resistance on endothelial function in vivo Diabetes 57 2008 3307 3314
217. Sukumar P., Viswambharan H., Imrie H., Cubbon R.M., Yuldasheva N., Gage M., et al. Nox2 NADPH-oxidase has a critical role in insulin resistance-related endothelial cell dysfunction. Diabetes (in press).
218. A.J. Kowaltowski de Souza-Pinto N.C., Castilho R.F., Vercesi A.E. Mitochondria and reactive oxygen species Free Radic. Biol. Med. 47 2009 333 343
219. J. Szendroedi, E. Phielix, and M. Roden The role of mitochondria in insulin resistance and type 2 diabetes mellitus Nat. Rev. Endocrinol. 8 2012 92 103
220. R.B. Hamanaka, and N.S. Chandel Mitochondrial reactive oxygen species regulate hypoxic signaling Curr. Opin. Cell Biol. 21 2009 894 899
221. X. Lin, C.A. David, J.B. Donnelly, M. Michaelides, N.S. Chandel, and X. Huang A chemical genomics screen highlights the essential role of mitochondria in HIF-1 regulation Proc. Natl. Acad. Sci. USA 105 2008 174 179
222. H.J. Jung, J.S. Shim, J. Lee, Y.M. Song, K.C. Park, and S.H. Choi Terpestacin inhibits tumor angiogenesis by targeting UQCRB of mitochondrial complex III and suppressing hypoxia-induced reactive oxygen species production and cellular oxygen sensing J. Biol. Chem. 285 2010 11584 11595
223. S. Dai, Y. He, H. Zhang, L. Yu, T. Wan, and Z. Xu Endothelial-specific expression of mitochondrial thioredoxin promotes ischemia-mediated arteriogenesis and angiogenesis Arterioscler. Thromb. Vasc. Biol. 29 2009 495 502
224. T.J. Guzik, N.E.J. West, R. Pillai, D.P. Taggart, and K.M. Channon Nitric oxide modulates superoxide release and peroxynitrite formation in human blood vessels Hypertension 39 2002 1088 1094
225. D.H. Platt, M. Bartoli, A.B. El-Remessy, M. Al-Shabrawey, T. Lemtalsi, and D. Fulton Peroxynitrite increases VEGF expression in vascular endothelial cells via STAT3 Free Radic. Biol. Med. 39 2005 1353 1361
226. F.C. Sasso, D. Torella, O. Carbonara, G.M. Ellison, M. Torella, and M. Scardone Increased vascular endothelial growth factor expression but impaired vascular endothelial growth factor receptor signaling in the myocardium of type 2 diabetic patients with chronic coronary heart disease J. Am. Coll. Cardiol. 46 2005 827 834
227. H. Kajiwara, Z. Luo, A.J. Belanger, A. Urabe, K.A. Vincent, and G.Y. Akita A hypoxic inducible factor-1a hybrid enhances collateral development and reduces vascular leakage in diabetic rats J. Gene Med. 11 2009 390 400
228. G. Doronzo, I. Russo, L. Mattiello, G. Anfossi, A. Bosia, and M. Trovati Insulin activates vascular endothelial growth factor in vascular smooth muscle cells: influence of nitric oxide and of insulin resistance Eur. J. Clin. Invest. 34 2004 664 673
229. R. Nagahama, T. Matoba, K. Nakano, S. Kim-Mitsuyama, K. Sunagawa, and K. Egashira Nanoparticle-mediated delivery of pioglitazone enhances therapeutic neovascularization in a murine model of hindlimb ischemia Arterioscler. Thromb. Vasc. Biol. 32 2012 2427 2434
230. C. Treins, S. Giorgetti-Peraldi, J. Murdaca, G.L. Semenza, and E. Van Obberghen Insulin stimulates hypoxia-inducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway J. Biol. Chem. 277 2002 27975 27981
231. V. Poulaki, W. Qin, A.M. Joussen, P. Hurlbut, S.J. Wiegand, and J. Rudge Acute intensive insulin therapy exacerbates diabetic blood-retinal barrier breakdown via hypoxia-inducible factor-1a and VEGF. J Clin. Invest. 109 2002 805 815
232. S. Yim, S.M. Choi, Y. Choi, N. Lee, J. Chung, and H. Park Insulin and hypoxia share common target genes but not the hypoxia-inducible factor-1a J. Biol. Chem. 278 2003 38260 38268
233. H. Thangarajah, D. Yao, E.I. Chang, Y. Shi, L. Jazayeri, and I.N. Vial The molecular basis for impaired hypoxia-induced VEGF expression in diabetic tissues Proc. Natl. Acad. Sci. USA 106 2009 13505 13510
234. S.I. Chisalita, M.D. Nitert, and H.J. Arnqvist Characterisation of receptors for IGF-I and insulin; evidence for hybrid insulin/IGF-I receptor in human coronary artery endothelial cells Growth Horm. IGF Res 16 2006 258 266
235. S. Chisalita, and H. Arnqvist Expression and function of receptors for insulin-like growth factor-I and insulin in human coronary artery smooth muscle cells Diabetologia 48 2005 2155 2161
236. M.J. Khorsandi, J.A. Fagin, D. Giannella-Neto, J.S. Forrester, and B. Cercek Regulation of insulin-like growth factor-I and its receptor in rat aorta after balloon denudation: evidence for local bioactivity J. Clin. Invest. 90 1992 1926 1931
237. A. Cittadini, M. Monti, M. Castiello, E. D'Arco, G. Galasso, and D. Sorriento Insulin-like growth factor-1 protects from vascular stenosis and accelerates re-endothelialization in a rat model of carotid artery injury J. Thromb. Haemostasis 7 2009 1920 1928
238. H. Imrie, A. Abbas, H. Viswambharan, A. Rajwani, R.M. Cubbon, and M. Gage Vascular insulin-like growth factor-I resistance and diet-induced obesity Endocrinology 150 2009 4575 4582
239. H. Imrie, H. Viswambharan, P. Sukumar, A. Abbas, R.M. Cubbon, and N. Yuldasheva Novel role of the IGF-1 receptor in endothelial function and repair: studies in endothelium-targeted IGF-1 receptor transgenic mice Diabetes 61 2012 2359 2368
240. M. Grant, R. Mames, C. Fitzgerald, E. Ellis, M. Aboufriekha, and J. Guy Insulin-like growth factor I acts as an angiogenic agent in rabbit cornea and retina: comparative studies with basic fibroblast growth factor Diabetologia 36 1993 282 291
241. L.E.H. Smith, W. Shen, C. Perruzzi, S. Soker, F. Kinose, and X. Xu Regulation of vascular endothelial growth factor-dependent retinal neovascularization by insulin-like growth factor-1 receptor Nat. Med. 5 1999 1390 1395
242. S. Sukhanov, Y. Higashi, S.Y. Shai, C. Vaughn, J. Mohler, and Y. Li IGF-1 reduces inflammatory responses, suppresses oxidative stress, and decreases atherosclerosis progression in ApoE-deficient mice Arterioscler. Thromb. Vasc. Biol. 27 2007 2684 2690
243. T. Thum, S. Hoeber, S. Froese, I. Klink, D.O. Stichtenoth, and P. Galuppo Age-dependent impairment of endothelial progenitor cells is corrected by growth hormone mediated increase of insulin-like growth factor-1 Circ. Res 100 2007 434 443
244. B. Hynes, A.H.S. Kumar, J. O'Sullivan, C. Klein Buneker, A.L. Leblond, and S. Weiss Potent endothelial progenitor cell-conditioned media-related anti-apoptotic, cardiotrophic, and pro-angiogenic effects post-myocardial infarction are mediated by insulin-like growth factor-1 Eur. Heart J. 34 2013 782 789
245. C. Urbich, A. Aicher, C. Heeschen, E. Dernbach, W.K. Hofmann, and A.M. Zeiher Soluble factors released by endothelial progenitor cells promote migration of endothelial cells and cardiac resident progenitor cells J. Mol. Cell. Cardiol 39 2005 733 742
246. G.S. Johansson, S.I. Chisalita, and H.J. Arnqvist Human microvascular endothelial cells are sensitive to IGF-I but resistant to insulin at the receptor level Mol. Cell. Endocrinol 296 2008 58 63
247. G. Li, E.J. Barrett, H. Wang, W. Chai, and Z. Liu Insulin at physiological concentrations selectively activates insulin but not insulin-like growth factor I (IGF-I) or insulin/IGF-I hybrid receptors in endothelial cells Endocrinology 146 2005 4690 4696
248. S.J. Sherajee, Y. Fujita, K. Rafiq, D. Nakano, H. Mori, and T. Masaki Aldosterone induces vascular insulin resistance by increasing insulin-like growth factor-1 receptor and hybrid receptor Arterioscler. Thromb. Vasc. Biol. 32 2012 257 263
249. A. Abbas, H. Imrie, H. Viswambharan, P. Sukumar, A. Rajwani, and R.M. Cubbon The insulin-like growth factor-1 receptor is a negative regulator of nitric oxide bioavailability and insulin sensitivity in the endothelium Diabetes 60 2011 2169 2178
250. D. Senthil, G. Ghosh Choudhury, B.K. Bhandari, and B.S. Kasinath The type 2 vascular endothelial growth factor receptor recruits insulin receptor substrate-1 in its signalling pathway Biochem. J. 368 2002 49 56
251. D. Feliers, X. Chen, N. Akis, G.G. Choudhury, M. Madaio, and B.S. Kasinath VEGF regulation of endothelial nitric oxide synthase in glomerular endothelial cells Kidney Int. 68 2005 1648 1659
252. M. Berdugo, C. Andrieu-Soler, M. Doat, Y. Courtois, D. BenEzra, and F. Behar-Cohen Downregulation of IRS-1 expression causes inhibition of corneal angiogenesis. Invest Ophthalmol. Visual Sci. 46 2005 4072 4078
253. J. Kling Safety signal dampens reception for mipomersen antisense Nat. Biotech. 28 2010 295 297
254. Tsukagawa E., Adachi H., Hirai Y., Enomoto M., Fukami A., Ogata K., et al. Independent association of elevated serum HGF levels with development of insulin resistance in a 10-year prospective study. Clin. Endocrinol. (in press);.
255. A. Fafalios, J. Ma, X. Tan, J. Stoops, J. Luo, and M.C. DeFrances A hepatocyte growth factor receptor (Met)-insulin receptor hybrid governs hepatic glucose metabolism Nat. Med. 17 2011 1577 1584
256. D.M. Breen, K.K. Chan, J.K. Dhaliwall, M.R. Ward, N. Al Koudsi, and L. Lam Insulin increases reendothelialization and inhibits cell migration and neointimal growth after arterial injury Arterioscler. Thromb. Vasc. Biol. 29 2009 1060 1066
257. L. Dong, L. Kang, L. Ding, Q. Chen, J. Bai, and R. Gu Insulin modulates ischemia-induced endothelial progenitor cell mobilization and neovascularization in diabetic mice Microvasc. Res. 82 2011 227 236
258. A. Langer, and W. Rogowski Systematic review of economic evaluations of human cell-derived wound care products for the treatment of venous leg and diabetic foot ulcers BMC Health Serv. Res. 9 2009 115
259. C.F. Cheng, D. Sahu, F. Tsen, Z. Zhao, J. Fan, and R. Kim A fragment of secreted Hsp90α carries properties that enable it to accelerate effectively both acute and diabetic wound healing in mice J. Clin. Invest. 121 2011 4348 4361
260. Y. Kusumanto, V. van Weel, N. Mulder, A. Smit, J. van den Dungen, and J. Hooymans Treatment with intramuscular vascular endothelial growth factor gene compared with placebo for patients with diabetes mellitus and critical limb ischemia: a double-blind randomized trial Hum. Gene Ther. 17 2006 683 691
261. L. Cao, P.R. Arany, J. Kim, J. Rivera-Feliciano, Y.S. Wang, and Z. He Modulating Notch signaling to enhance neovascularization and reperfusion in diabetic mice Biomaterials 31 2010 9048 9056
262. A. Al Haj Zen, A. Oikawa, M. Bazan-Peregrino, M. Meloni, C. Emanueli, and P Madeddu Inhibition of delta-like-4 mediated signaling impairs reparative angiogenesis after ischemia Circ. Res. 107 2010 283 293
263. Y. Nishimura, M. Ii, G. Qin, H. Hamada, J. Asai, and H. Takenaka CXCR4 antagonist AMD3100 accelerates impaired wound healing in diabetic mice J. Invest. Dermatol. 132 2012 711 720
264. H.R. Jin, W.J. Kim, J.S. Song, S. Piao, M.J. Choi, and M. Tumurbaatar Intracavernous delivery of a designed angiopoietin-1 variant rescues erectile function by enhancing endothelial regeneration in the streptozotocin-induced diabetic mouse Diabetes 60 2011 969 980
265. C.H. Cho, H.K. Sung, K.T. Kim, H.G. Cheon, G.T. Oh, and H.J. Hong COMP-angiopoietin-1 promotes wound healing through enhanced angiogenesis, lymphangiogenesis, and blood flow in a diabetic mouse model Proc. Natl. Acad. Sci. USA 103 2006 4946 4951
266. R. Gupta, J. Tongers, and D.W. Losordo Human studies of angiogenic gene therapy Circ. Res. 105 2009 724 736
267. J.X. Chen, and A. Stinnett Ang-1 gene therapy inhibits hypoxia-inducible factor-1a (HIF-1a)-prolyl-4-hydroxylase-2, stabilizes HIF-1a expression, and normalizes immature vasculature in db/db mice Diabetes 57 2008 3335 3343
268. S.M. Samuel, Y. Akita, D. Paul, M. Thirunavukkarasu, L. Zhan, and P.R. Sudhakaran Coadministration of adenoviral vascular endothelial growth factor and angiopoietin-1 enhances vascularization and reduces ventricular remodeling in the infarcted myocardium of type 1 diabetic rats Diabetes 59 2010 51 60
269. I.R. Botusan, V.G. Sunkari, O. Savu, A.I. Catrina, J. Grunler, and S. Lindberg Stabilization of HIF-1a is critical to improve wound healing in diabetic mice Proc. Natl. Acad. Sci. USA 105 2008 19426 19431
270. K. Sarkar, K. Fox-Talbot, C. Steenbergen, M. Bosch-Marce, and G.L. Semenza Adenoviral transfer of HIF-1a enhances vascular responses to critical limb ischemia in diabetic mice Proc. Natl. Acad. Sci. USA 106 2009 18769 18774
271. V. Jeevanantham, M. Butler, A. Saad, A. Abdel-Latif, E.K. Zuba-Surma, and B. Dawn Adult bone marrow cell therapy improves survival and induces long-term improvement in cardiac parameters/clinical perspective Circulation 126 2012 551 568
272. C.W. Siu, and H.F. Tse Cardiac regeneration: messages from CADUCEUS Lancet 379 2010 870 871
273. E. Marban, and K. Malliaras Mixed results for bone marrow-derived cell therapy for ischemic heart disease JAMA 308 2012 2405 2406
274. Asai J., Takenaka H., Ii M., Asahi M., Kishimoto S., Katoh N., et al. Topical application of ex vivo expanded endothelial progenitor cells promotes vascularisation and wound healing in diabetic mice. Int. Wound J. (in press).
275. E.J. Marrotte, D.D. Chen, J.S. Hakim, and A.F. Chen Manganese superoxide dismutase expression in endothelial progenitor cells accelerates wound healing in diabetic mice J. Clin. Invest. 120 2010 4207 4219
276. D. Lu, L. Zhang, H. Wang, Y. Zhang, J. Liu, and J. Xu Peroxisome proliferator activated receptor-g coactivator-1a (PGC-1a) enhances engraftment and angiogenesis of mesenchymal stem cells in diabetic hindlimb ischemia Diabetes 61 2012 1153 1159
277. + cells Invest. Ophthalmol. Visual Sci. 52 2011 5093 5104
278. D. Broqueres-You, C. Lere-Dean, T. Merkulova-Rainon, C.S. Mantsounga, D. Allanic, and P. Hainaud Ephrin-B2-activated peripheral blood mononuclear cells from diabetic patients restore diabetes-induced impairment of postischemic neovascularization Diabetes 61 2012 2621 2632