Diabetes impairs the vascular recruitment of normal stem cells by oxidant damage, reversed by increases in pAMPK, Heme Oxygenase-1, and Adiponectin

Stem Cells

Volumn 27, Issue 2, 2009, Pages 399-407

  Sambuceti, Glanmario ^a,b,h   Morbelli, Silvia ^a   Vanella, Luca ^c   Kusmic, Claudia ^d   Marini, Cecilia ^d   Massollo, Michela ^a   Augerl, Carla ^a   Corselli, Mirko ^e   Ghersl, Chiara ^a   Chiavarina, Barbara ^e   Rodella, Luigi F ^g   L'abbate, Antonio ^f   Drummond, George ^c   Abraham, Nader G ^c   Frassoni, Francesco ^e  

^a UNIVERSITY OF GENOA   (Italy)

^b Advanced Biotechnology Center   (Italy)

^c NEW YORK MEDICAL COLLEGE   (United States)

^d CNR   (Italy)

^e UNIVERSITY OF GENOA   (Italy)

^f SCUOLA SUPERIORE SANT ANNA   (Italy)

^g UNIVERSITY OF BRESCIA   (Italy)

^h UNIVERSITY OF GENOA   (Italy)

Author keywords

CD31; Endothelial progenitor cells; HO 1; NO; pAMPK; Vascular repair

Indexed keywords

ADIPONECTIN; ANTIOXIDANT; CD31 ANTIGEN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEME OXYGENASE 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PROTOPORPHYRIN COBALT; THROMBOMODULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; BLOOD VESSEL WALL; CELL KINETICS; CONTROLLED STUDY; DIABETES MELLITUS; ENDOTHELIUM CELL; ENDOTHELIUM LESION; GENE EXPRESSION; MALE; NONHUMAN; OXIDATION; PLASMA CLEARANCE; RAT; STEM CELL;

ADIPONECTIN; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTIGENS, CD31; BLOTTING, WESTERN; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; ENDOTHELIAL CELLS; HEME OXYGENASE-1; IMMUNOHISTOCHEMISTRY; MALE; NITRIC OXIDE SYNTHASE TYPE III; PROTOPORPHYRINS; RATS; RATS, SPRAGUE-DAWLEY; STEM CELLS; THROMBOMODULIN;

ANIMALIA; PHOS; RATTUS;

EID: 62549120373     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2008-0800     Document Type: Article

References (52)

1. Bahia L, Aguiar LG, Villela N et al. Relationship between adipokines, inflammation, and vascular reactivity in lean controls and obese subjects with metabolic syndrome. Clinics 2006;61:433-440.
2. Kruger AL, Peterson S, Turkseven S et al. D-4F induces heme oxygenase- 1 and extracellular superoxide dismutase, decreases endothelial cell sloughing, and improves vascular reactivity in rat model of diabetes. Circulation 2005; 111:3126 -3134.
3. Abraham NG, Kushida T, McClung J el al. Heme oxygenase-1 attenuates glucose-mediated cell growth arrest and apoptosis in human microvessel endothelial cells. Circ Res 2003;93:507-514.
4. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995;1:27-31.
5. Esper RJ, Vilarino JO. Machado RA et al. Endothelial dysfunction in normal and abnormal glucose metabolism. Adv Cardiol 2008:45:17-43.
6. Urbich C, Dimmeler S. Endothelial progenitor cells: Characterization and role in vascular biology. Circ Res 2004:95:343-353.
7. Fadini GP. Miorin M, Facco M et al. Circulating endothelial progenitor cells are reduced in peripheral vascular complications of type 2 diabetes mellitus. .1 Am Coll Cardiol 2005;45:1449-1457.
8. Tepper OM, Galiano RD, Capla JM et al. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 2002; 106:2781-2786.
9. Heeschen C. Lehmann R, Honold J et al. Profoundly reduced neovascularization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation 2004; 109: 1615-1622.
10. Nakagami H, Kaneda Y, Ogihara T et al. Endothelial dysfunction in hvperglvcemia as a trigger of atherosclerosis. Curr Diabetes Rev 2005; 159-63.
11. Wright E Jr. Seism-Bacon JL, Glass LC. Oxidative stress in type 2 diabetes: The role of fasting and postprandial glycaemia. Int J Clin Pract 2006;60:308-314.
12. Dimmeler S, Fleming I, Fisslthaler B et al. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999;399:601-605.
13. Morange PE, Simon C, Alessi MC et al. Endothelial cell markers and the risk of coronary heart disease: The Prospective Epidemiological Study of Myocardial Infarction (PRIME) study. Circulation 2004; 109:1343-1348.
14. Li D, Mehta JL. 3-hydroxy-3-melhylglulary 1 coenzyme A reductase inhibitors protect against oxidized low-density lipoprotein-induced endothelial dysfunction. Endothelium 2003;10:17-21.
15. Asija A, Peterson S, Stec DE et al. Targeting endothelial cells with heme oxygenase-1 gene using VE-cadherin promoter attenuates hyperglyce- mia-mediated cell injury and apoptosis. Antiox Redox Signal 2007; 12: 2065-2074.
16. Peterson SJ. Husney D, Kruger AL et al. Long-term treatment with the apolipoprotein A1 mimetic peptide increases antioxidants and vascular repair in type I diabetic rats. J Pharmacol Exp Ther 2007;322:514-520.
17. L'Abbate A, Neglia D. Vecoli C et al Beneficial effect of heme oxygenase-1 expression on myocardial ischemia-reperfusion involves an increase in adiponectin in mildly diabetic rats. Am J Phyisiol Heart Circ Physiol 2007;293:H3532-H3541
18. Li M, Kim DH, Tsenovoy PL et al. Treatment of obese diabetic mice with a heme oxygenase inducer reduces visceral and subcutaneous adiposity, increases adiponectin levels, and improves insulin sensitivity and glucose tolerance. Diabetes 2008;57:1526-1535.
19. Kim DH, Burgess AP, Li M et al. Heme oxygenase-mediated increases in adiponectin decrease fat content and inflammatory cytokines tumor necrosis factor-alpha and interleukin-6 in Zucker rats and reduce adipo- genesis in human mesenchymal stem cells. J Pharmacol Exp Ther 2008; 325:833-840.
20. Abraham NG. Tsenovoy PL, McClung .1 et al Heme oxygenase: A target gene for anti-diabetic and obesity. Curr Pharm Des 2008; 14:412-421.
21. Lin HV. Kim JY. Pocai A et al. Adiponectin resistance exacerbates insulin resistance in insulin receptor transgenic/knockout mice. Diabetes 2007;56:1969-1976.
22. Lin Y, Berg AH, Iyengar P et al. The hyperglycemia-induced inflammatory response in adipocytes: The role of reactive oxygen species. J Biol Chem 2005;280:4617-4626.
23. Arita Y, Kihara S. Ouchi N et al. Paradoxical decrease of an adipose- specific protein, adiponectin, in obesity. Biochem Biophys Res Commun 1999;257:79-83.
24. Weyer C, Funahashi T. Tanaka S et al. Hypoadiponectinemia in obesity and type 2 diabetes: Close association with insulin resistance and hyper- insulinemia. J Clin Endocrinol Metab 2001;86:1930-1935.
25. Hopkins TA. Ouchi N, Shibata R et al. Adiponectin actions in the cardiovascular system. Cardiovasc Res 2007;74:11-18.
26. Di Noia MA. Van Driesche S, Palmieri F et al. Heme oxygenase-1 enhances renal mitochondrial transport carriers and cytochrome C oxidase activity in experimental diabetes. J Biol Chem 2006;281:15687-15693.
27. Hardie DC. Minireview: The AMP-activated protein kinase cascade: The key sensor of cellular energy status. Endocrinology 2003;144:5179-5183.
28. Hardie DG. AMP-activated protein kinase as a drug target. Annu Rev Pharmacol Toxicol 2007;47:185-210.
29. Skurk C. Maatz H, Kim HS et al. The Akt-regulated forkhead transcription factor FOX03a controls endothelial cell viability through modulation of the caspase-8 inhibitor FLIP. J Biol Chem 2004;279:1513-1525.
30. Masiello P, Broca C, Gross R et al. Experimental NIDDM: Development of a new model in adult rats administered streptozotocin and nicotinamide. Diabetes 1998;47:224-229.
31. Barbash IM, Chouraqui P, Baron J et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: Feasibility, cell migration, and body distribution. Circulation 2003; 108: 863-868.
32. Abraham NG, Rezzani R, Rodella L et al. Overexpression of human heme oxygenase-1 attenuates endothelial cell sloughing in experimental diabetes. Am J Physiol Heart Circ Physiol 2004;287:H2468-H2477.
33. Peterson SJ, Drummond G, Kim DH et al. L-4F treatment reduces adiposity, increases adiponectin levels, and improves insulin sensitivity in obese mice. J Lipid Res 2008;49:1658-1669.
34. Vasa M, Fichtlschcrcr S, Aicher A et al. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 2001;89:E1-E7.
35. Popov D, Hasu M. Costache G et al. Capillary and aortic endothelia interact in situ with nonenzymatically glycated albumin and develop specific alterations in early experimental diabetes. Acta Diabetol 1997; 34:285-293.
36. Ishikawa K, Sugawara D. Goto J et al. Heme oxygenase-1 inhibits atherogenesis in Watanabe heritable hyperlipidemic rabbits. Circulation 2001;104:1831-1836.
37. Sandusky G, Berg DT, Richardson MA et al. Modulation of thrombomodulin-dependent activation of human protein C through differential expression of endothelial Smads. J Biol Chem 2002;277:49815-49819.
38. Laszik ZG. Zhou XJ, Ferrell GL et al. Down-regulation of endothelial expression of endothelial cell protein C receptor and thrombomodulin in coronary atherosclerosis. Am J Pathol 2001;159:797-802.
39. Yamada S, Ito T, Adachi J et al. Decreased arterial responses in WHHL rabbits, an animal model of spontaneous hypercholesterolemia and atherosclerosis. Exp Anim 2002;51:493-499.
40. Andreotti F, Porto I, Crea F et al. Inflammatory gene polymorphisms and ischaemic heart disease: Review of population association studies. Heart 2002;87:107-112.
41. Waugb JM, Li-Hawkins J, Yuksel E et al. Thrombomodulin overexpression to limit neointima formation. Circulation 2000;102:332-337.
42. Loomans CJ, de Koning EJ, Staal FJ et al Endothelial progenitor cell dysfunction: A novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 2004;53:195-199.
43. Duda DG, Fukumura D, Jain RK. Role of eNOS in neovascularization: NO for endothelial progenitor cells. Trends Mol Med 2004; 10:143-145.
44. Fukumura D. Jain RK. Role of nitric oxide in angiogenesis and microcirculation in tumors. Cancer Metastasis Rev 1998;17:77-89.
45. Gallagher KA, Liu ZJ. Xiao M et al. Diabetic impairments in NO-mediated endothelial progenitor cell mobilization and homing are reversed bv hyper- oxia and SDF-1 alpha. J Clin Invest 2007;117:1249-1259.
46. Grosser N, Hemmerle A, Berndt G et al. The antioxidant defense protein heme oxygenase 1 is a novel target for statins in endothelial cells. Free Radic Biol Med 2004;37:2064-2071.
47. Turkseven S, Kruger A, Mingone CJ et al. Antioxidant mechanism of heme oxygenase-1 involves an increase in superoxide dismutase and catalase in experimental diabetes. Am J Physiol Heart Circ Physiol 2005;289:H701-H707.
48. Abraham NG, Kappas A. Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev 2008;60:79-127.
49. Ouchi N, Kobayashi H, Kihara S et al. Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. J Biol Chem 2004;279:1304-1309.
50. Chen ZP, Mitchelhill KI. Michell BJ et al. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett 1999;443:285-289.
51. Janlzen F, Konemann S, Wolff B et al. Isoprenoid depletion by statins antagonizes cytokine-induced down-regulation of endothelial nitric oxide expression and increases NO synthase activity in human umbilical vein endothelial cells. J Physiol Pharmacol 2007;58:503-514.
52. Hill JM, Zalos G, Halcox JP el al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 2003; 348:593-600.