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

Journal of Vascular Surgery

Volumn 50, Issue 6, 2009, Pages 1412-1422

  Yan, Jinglian ^a   Tie, Guodong ^a   Park, Brian ^a   Yan, Yagai ^b   Nowicki, Philip T ^a   Messina, Louis M ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; STREPTOZOCIN; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY DISEASE; ARTICLE; BLOOD FLOW; CELL MIGRATION; CONTROLLED STUDY; CONVALESCENCE; ENDOTHELIUM CELL; EXCISION; FEMORAL ARTERY; GASTROCNEMIUS MUSCLE; HINDLIMB; INSULIN DEPENDENT DIABETES MELLITUS; LIMB ISCHEMIA; LIMB PERFUSION; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; STREPTOZOCIN DIABETES;

ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; CHEMOTAXIS; COLLATERAL CIRCULATION; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; ENDOTHELIAL CELLS; HINDLIMB; ISCHEMIA; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE STRESS; RECEPTORS, LEPTIN; RECOVERY OF FUNCTION; REGIONAL BLOOD FLOW; STEM CELLS; TIME FACTORS; TYROSINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 70649107812     PISSN: 07415214     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jvs.2009.08.007     Document Type: Article

References (34)

1. Brownlee M. The pathobiology of diabetic complications. A unifying hypothesis. Diabetes 54 (2005) 1615-1624
2. Mazzone T., Chait A., and Plutzky J. Cardiovascular disease risk in type 2 diabetes mellitus: insights from mechanistic studies. Lancet 371 (2008) 1800-1809
3. van Weel V., de Vries M., Voshol P., Verloop R., Eilers P., van Hinsbergh V., et al. Hypercholesterolemia reduces collateral artery growth more dominantly than hypergylcemia or insulin resistance in mice. Arterioscler Thrombv Vasc Biol 26 (2006) 1383-1390
4. Waters R., Terjung R., Peters K., and Annex B. Preclinical models of human peripheral arterial occlusive disease: implications for investigating therapeutic agents. J Appl Physiol 97 (2004) 773-780
5. Tamarat R., Silvestre J.S., Ricousse-Roussanne S.L., Barateau V., Lecomte-Raclet L., Clergue M., et al. Impairment in ischemia-induced neovascularization in diabetes. Bone marrow mononuclear cell dysfunction and therapeutic potential of placenta growth factor treatment. Am J Pathol 164 (2004) 457-466
6. Emanueli C., Caporali A., Krankel N., Cristofaro B., Van Linthout S., and Madeddu P. Type-2 diabetic Lepr (db/db) mice show defective microvascular phenotype under basal conditions and an impaired response to angiogenesis gene therapy in the setting of limb ischemia. Front Biosci 12 (2007) 2003-2012
7. Urbich C., and Dimmeler S. Endothelial progenitor cells. Characterization and role in vascular biology. Circ Res 95 (2004) 343-354
8. Asahara T., Murohara T., Sullivan A., Silver M., van der Zee R., Li T., et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275 (1997) 964-967
9. Takahashi T., Kalka C., Masuda H., Chen D., Silver M., Kearney M., et al. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5 (1999) 434-438
10. Gallagher K.A., Liu Z.J., Xiao M., Chen H.Y., Goldstein L.J., Buerk D.G., et al. Diabetic impairments in NO-mediated endothelial progenitor cell mobilization and homing are reversed by hyperoxia and SDF-1α. J Clin Invest 117 (2007) 1249-1259
11. Fadini G.P., Sartore S., Schiavon M., Albiero M., Baesso I., Cabrelle A., et al. Diabetes impairs progenitor cell mobilization after hindlimb ischemia-reperfusion injury in rats. Diabetologia 49 (2006) 3075-3084
12. Tepper O.M., Galiano R.D., Capla J.M., Kalka C., Gagne P.J., Jacobowitz G.R., et al. Human endothelial progenitor cells from type II diabetic patients exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 106 (2002) 2781-2786
13. Loomans C.J., de Koning E.J.P., Staal F.J.T., Rookmaaker M.B., Verseyden C., de Boer H.C., et al. Endothelial progenitor cell dysfunction-a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 53 (2004) 195-199
14. Aicher A., Heeschen C., Mildner-Rihm C., Urbich C., Ihling C., Technau-Ihling K., et al. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 9 (2003) 1370-1376
15. Lloyd P., Yang H., and Terjung R. Arteriogenesis and angiogenesis in rat ischemic hindlimb: role of nitric oxide. Am J Physiol Heart Circ Physiol 281 (2001) H2528-H2538
16. Sorrentino S.A., Bahlmann F.H., Besler C., Muller M., Schulz S., Kirchhoff N., et al. Oxidative stress impairs in vivo reendothelialization capacity of endothelial progenitor cells from patients with Type 2 diabetes mellitus-restoration by the peroxisome proliferator-activated receptor-γ agonist rosiglitazone. Circulation 116 (2007) 163-173
17. Thum T., Fraccarollo D., Schultheiss M., Froese S., Galuppo P., Widder J., et al. Endothelial nitric oxide synthase uncoupling impairs endothelial progenitor cell mobilization and function in diabetes. Diabetes 56 (2007) 666-674
18. Rees D., and Alcolado J. Animal models of diabetes mellitus. Diabetes Med 22 (2005) 359-370
19. Hummel K., Dickie M., and Coleman D. Diabetes, a new mutation in the mouse. Science 153 (1966) 1127-1128
20. Tang G.L., Chang D.S., Sarkar R., Wang R., and Messina L.M. The effect of gradual or acute arterial occlusion on skeletal muscle blood flow, arteriogenesis, and inflammation in rat hindlimb ischemia. J Vasc Surg 41 (2005) 312-320
21. Schaper W., and Scholz D. Factors regulating arteriogenesis. Arterioscler Thromb Vasc Biol 23 (2003) 1143-1151
22. Schiekofer S., Glasso G., Sato K., Kraus B.J., and Walsh K. Impaired revascularization in a mouse model of type 2 diabetes is associated with dysregulation of a complex angiogenic-regulatory network. Arterioscler Thromb Vasc Biol 25 (2005) 1603-1609
23. Granger H., Goodman A., and Granger D. Role of resistance and exchange vessels in local microvascular control of skeletal muscle oxygenation in the dog. Circ Res 38 (1976) 379-385
24. Ito W., Arras M., Scholz D., Winkler B., Htun P., and Schaper W. Angiogenesis but not collateral growth is associated with ischemia after femoral artery occlusion. Am J Physiol Heart Circ Physiol 273 (1997) H1255-H1265
25. Fadini G., Sartore S., Albiero M., Baesso I., Murphy E., Menegolo M., et al. Number and function of endothelial progenitor cells as a marker of severity for diabetic vasculopathy. Arterioscler Thromb Vasc Biol 26 (2006) 2140-2146
26. Huang P.H., Sata M., Nishimatsu H., Sumi M., Hirata Y., and Nagai R. Pioglitazone ameliorates endothelial dysfunction and restores ischemia-induced angiogenesis in diabetic mice. Biomed Pharmacother 62 (2008) 46-52
27. Schatteman G.C., Hanlon H.D., Jiao C.H., Dodds S.G., and Christy B.A. Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice. J Clin Invest 106 (2000) 571-578
28. Kinnaird T., Stabile E., Burnett M., Shou M., Lee W., Barr S., et al. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 109 (2004) 1543-1549
29. Pittenger M., Mackay A., Beck S., Jaiswal R., Douglas R., Mosca J., et al. Multilineage potential of adult human mesenchymal stem cells. Science 284 (1999) 143-146
30. Kikutani H., and Makino S. The murine autoimmune diabetes model: NOD and related strains. Adv Immunol 51 (1992) 285-322
31. Leiter E. The genetics of diabetic susceptibility in mice. FASEB J 3 (1989) 2231-2241
32. Loffreda S., Yang S., Lin H., Karp C., Brengman M., Wang D., et al. Leptin regulates proinflammatory immune responses. FASEB J 12 (1998) 57-65
33. Martin-Romero C., Santos-Alvarez J., Goberna R., and Sánchez-Margalet V. Human leptin enhances activation and proliferation of human circulating T lymphocytes. Cell Immunol 199 (2000) 15-24
34. Stabile E., Kinnaird T., la Sala A., Hanson S., Watkins C., Campia U., et al. CD8+ T lymphocytes regulate the arteriogenic response to ischemia by infiltrating the site of collateral development and recruiting CD4+ mononuclear cells through expression of IL-16. Circulation 113 (2006) 118-124