Type-2 diabetic Lepr db/db mice show a defective microvascular phenotype under basal conditions and an impaired response to angiogenesis gene therapy in the setting of limb ischemia

Frontiers in Bioscience

Volumn 12, Issue 6, 2007, Pages 2003-2012

  Emanueli, Costanza ^a,b   Caporali, Andrea ^a   Krankel, Nicolle ^a,b   Cristofaro, Brunella ^a   Van Linthout, Sophie ^b,d   Madeddu, Paolo ^a,b,c  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

^c IRCCS MULTIMEDICA   (Italy)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Akt; Angiogenesis; Apoptosis; eNOS; Gene therapy; Leprdb db mice; Limb ischemia; Tissue kallikrein; Type 2 diabetes

Indexed keywords

MURINAE; MUS;

CELL SURFACE RECEPTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; LEPTIN RECEPTOR; PROTEIN KINASE B; TISSUE KALLIKREIN; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL; ARTICLE; C57BL MOUSE; CAPILLARY; DIABETIC ANGIOPATHY; GENE THERAPY; GENETICS; HUMAN; ISCHEMIA; LEG; METABOLISM; MOUSE; MOUSE MUTANT; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; SKELETAL MUSCLE; VASCULARIZATION;

ANIMALS; CAPILLARIES; DIABETES MELLITUS, TYPE 2; DIABETIC ANGIOPATHIES; GENE THERAPY; HUMANS; ISCHEMIA; LOWER EXTREMITY; MICE; MICE, INBRED C57BL; MICE, OBESE; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE TYPE III; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, CELL SURFACE; TISSUE KALLIKREINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 36049044373     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/2205     Document Type: Article

References (42)

1. W.B. Kannel & L. McGee: Diabetes and cardiovascular disease: the Framingham study. JAMA 241, 2035-2038 (1979) (Pubitemid 9228506)
2. A.F. Amos, D.I. Mc Carty & P. Zimmet: The rising global burden of diabetes and its complications: estimates and projections by 2010. Diabet Med 14, S5-S85 (1997)
3. P. Zimmet , K.G. Alberti & J. Shaw: Global and social implications of the diabetes epidemics. Nature 414, 762-787 (2001)
4. X. Haffner: Coronary heart disease in patients with diabetes. N Engl J Med 342, 1040-1042 (2000)
5. A. Rivard, M. Silver, D. Chen, M. Kearney, M. Magner, B. Annex, K. Peters & J.M. Isner: Rescue of diabetesrelated impairment of angiogenesis by intramuscular gene therapy with adeno-VEGF. Am J Pathol 154:355-363 (1999) (Pubitemid 29094086)
6. Y. Taniyama, R. Morishita, K. Hiraoka, M. Aoki, H. Nakagami, K. Yamasaki, K Matsumoto, T. Nakamura, Y. Kaneda & T. Togihara: Therapeutic angiogenesis induced by human hepatocyte growth factor gene in rat diabetic hind limb ischaemia model: molecular mechanisms of delayed angiogenesis in diabetes. Circulation 104, 2344-2350 (2001) (Pubitemid 33049519)
7. G.C. Schatteman, H.D. Hanlon, C. Jiao , S. G. Dodds & B.A. Christy: Blood-derived angioblasts accelerate bloodflow restoration in diabetic mice. J Clin Invest 106, 571-578 (2000) (Pubitemid 30666390)
8. C. Emanueli, M.B. Salis, A. Pinna, T. Stacca, A. F. Milia, A. Spano, J. Chao, L. Chao, L. Sciola, & P. Madeddu: Prevention of diabetes-induced microangiopathy by human tissue kallikrein gene transfer. Circulation 106, 993-999 (2002) (Pubitemid 34925336)
9. C. Emanueli, G. Graiani, M.B. Salis, S. Gadau, E. Desortes & P. Madeddu: Prophylactic gene therapy with human tissue kallikrein ameliorates limb ischaemia recovery in type 1 diabetic mice. Diabetes 53, 1096-1103 (2004) (Pubitemid 38436624)
10. M. Simons & J.A. Ware: Therapeutic angiogenesis in cardiovascular disease. Nat Rev Drug Discov 2:863-871 (2003) (Pubitemid 37407792)
11. A.M. Madiehe, S. Hebert, T.D. Mitchell & R.B.S. Harris: Strain-dependent stimulation of growth in leptintreated obese db/db mice. Endocrinology 143, 3875-3883 (2002) (Pubitemid 35244367)
12. Y. Zhang, R. Proenca, M. Maffei, M. Barone, L. Leopold & J.M. Friedman: Positional cloning of the mouse obese gene and its human homologue. Nature (Lond)372, 425-432 (1994) (Pubitemid 24365442)
13. M. Aizawa-Abe M, Y. Ogawa Y., H. Masuzaki, K. Ebihara, N. Satoh, H. Iwai, N. Matsuoka, T. Hayashi, K. Hosoda, G. Inoue, Y. Yoshimasa & K. Nakao: Pathophysiological role of leptin in obesity-related hypertension. J Clin Invest 105, 1243-1252 (2000) (Pubitemid 30266077)
14. N.S. Gibran, Y.C. Jang, F.F. Isik, D.G. Greenhalgh, L.A, Muffley, R.A. Underwood, M.L. Usui, J. Larsen, D.G. Smith, N. Bunnett, J.C. Ansel & J.E. Olerud: Diminished neuropeptide levels contribute to the impaired healing response associated with diabetes mellitus. J Surg Res 108, 122-128 (2002) (Pubitemid 35373824)
15. Z. Wang, Y.T. Zhou, T. Kakuma, Y. Lee, S.P. Kalra, P.S., W. Pan & R.H. Unger : Leptin resistance of adipocytes in obesity: role of suppressors of cytokine signalling. Biochem Biophys Res Commun 277, 20-26 (2000)
16. P. Madeddu, A. Pinna, B. Salis, G. Graiani & C. Emanueli. Prophylactic gene therapy with tissue kallkrein ameliorates the post-ischaemic recovery of diabetic limbs. Impaired angiogenesis response to limb ischaemia in genetically type 2 diabetic mice is corrected by gene therapy with tissue kallikrein or activated Akt-B kinase. Diabetologia 46: (Suppl 2)(2003)
17. S. Schiekofer, G. Galasso, K. Sato, B.J. Kraus & K. Walsh: 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(8), 1603-9 (2005) (Pubitemid 41098928)
18. C. Emanueli, A. Minasi, A. Zacheo, J. Chao, L. Chao, M.B. Salis, S. Straino, M.G. Tozzi, R. Smith, L. Gaspa, G. Bianchini,; F. Stillo, M.C. Capogrossi & P. Madeddu: Local delivery of human tissue kallikrein gene accelerates spontaneous angiogenesis in mouse model of hindlimb ischaemia. Circulation 103, 125-132 (2001) (Pubitemid 32050447)
19. C. Emanueli, MB Salis, S Van Linthout, M. Meloni, E. Desortes, J-S. Silvestre, M. Clergue, C.D. Figueroa, S. Gadau, G. Condorelli & P. Madeddu: Role of Akt/protein kinase B (Akt-B)and endothelial nitric oxide synthase (eNOS)in muscular neovascularization induced by tissue kallikrein gene transfer. Circulation 110, 1638-1644 (2004) (Pubitemid 39297987)
20. S.H. Snyder & S.R. Jaffrey: Vessels vivified by Akt acting on NO synthase. Nat. Cell Biol 1, E95-E96 (1999)
21. Y. Fujio, T. Nguyen, D. Wencker, R.N. Kitsis & K. Walsh: Akt promotes survival of cardiomyocytes in vitro and protects against ischaemia-reperfusion injury in mouse heart. Circulation 101, 660-667 (2000) (Pubitemid 30094738)
22. C. Emanueli, M.B. Salis, A. Pinna, G. Graiani, L. Manni L & P. Madeddu: Nerve growth factor promotes angiogenesis and arteriogenesis in ischaemic hindlimbs. Circulation 106, 2257-2262 (2002) (Pubitemid 35222222)
23. A. Papapetropoulos, D. Foulton, K. Mahboubi, R.G. Kalb, D.S. O'Connor, F. Li, D.O.C. Altieri & W.C. Sessa: Angiopoietin-1 inhibits endothelial cell apoptosis via the Akt/surviving pathway. J Biol Chem 275, 9102-9105 (2000) (Pubitemid 30185122)
24. W. Kim, S.O. Moon, M.J. Sung, S.H. Kim, S. Lee, J.N. So & S.K. Park: Angiogenic role of adrenomedullin through activation of Akt, mitogen-activated protein kinase, and focal adhesion kinase in endothelial cells. FASEB J 17, 1937-1939 (2003)
25. J-S. Silvestre, R. Tamarat, T.G. Ebrahimian, A. Le-Roux, M. Clergue, F. Emmanuel, M. Duriez, B. Schwartz, D. Branellec & B. I. Lévy: Vascular endothelial growth factor-B promotes in vivo angiogenesis. Circ Res 93, 114-123 (2003) (Pubitemid 36919698)
26. N. Ouchi, H. Kobayashi, S. Kihara, M. Kumada, K. Sato, T. Inoue, T. Funahashi & K. Walsh: Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signalling in endothelial cells. J Biol Chem 279, 1304-1309 (2004) (Pubitemid 38082655)
27. Y. Kureishi, Z. Luo, I. Shiojima, A. Bialik, D. Fulton, D.J. Lefer, W.C. Sessa & K. Walsh: The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals. Nat Med 6, 1004-1010 (2000)
28. J Chao, L Jin , LM Chen, V.C. Chen, L. Chao: Systemic and portal vein delivery of human kallikrein gene reduces blood pressure in hypertensive rats. Hum Gene Ther 7, 901-911 (1996) (Pubitemid 26169655)
29. A Bellacosa, TO Chan, NN Ahmed, K. Datta, S. Malstrom, D. Stokoe, F. McCormick, J. Feng & P. Tsichlis: Akt activation by growth factors is a multiple-step process: the role of the PH domain. Oncogene 17, 313-325 (1998) (Pubitemid 28383008)
30. P. Madeddu, M.V. Varoni, D. Palomba, C. Emanueli, M.P. Demontis, N. Glorioso, P. Dessì-Fulgheri, R. Sarzani& V. Anania: Cardiovascular phenotype of a mouse strain with disruption of bradykinin B2-receptor gene. Circulation 96, 3570-3578 (1997) (Pubitemid 27513435)
31. P. Zimmet, E.J. Boyko, G.R. Collier & M. de Courten: Etiology of the metabolic syndrome: potential role of insulin resistance, leptin resistance, and other players. Ann NY Acad Sci 892, 25-44 (1999)
32. C. Vecchione, A. Maffei, S. Colella, A. Aretini, R. Poulet, G. Frati, M.T. Gentile, L. Fratta, V. Trimarco, B. Trimarco & G. Lembo: Leptin effect on endothelial nitric oxide is mediated through Akt-endothelial nitric oxide synthase phosphorylation pathway. Diabetes 51, 168-173 (2002) (Pubitemid 34517994)
33. B. Cohen, D. Barman, Y. Levy, I. Goldberg, E. Fridman, J. Kopolovic & M. Rubinstein: Leptin induces angiopoietin-2 expression in adipose tissue. J Biol Chem 276, 7697-7700 (2001)
34. D Rizzoni, E Porteri, D Guelfi D, M.L. Muiesan, U, Valentini, A. Cimino, A. Girelli, L. Rodella, R. Bianchi, I. Sleiman & E. Agabiti Rosei: Structural alterations in subcutaneous small arteries of normotensive and hypertensive patients with non-insulin-dependent diabetes mellitus. Circulation 103, 1238-1244 (2001) (Pubitemid 32221346)
35. T. Murohara, T. Asahara, M. Silver, C. Bauters, H. Masuda, C. Kalka, M. Kearney, D. Chen, D. Chen, J.F. Syme& z.ast;, M.C. Fishman, P.L. Huang & J.M. Isner: Nitric Oxide Synthase Modulates Angiogenesis in Response to Tissue Ischaemia. J Clin Invest 101(11), 2567-2578 (1998) (Pubitemid 28270451)
36. A. Aicher, C. Heeschen, C. Mildner-Rihm, C. Urbich, C. Ihling, K. Technau-Ihling, A.M. Zeiher & S. Dimmeler: Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nature Medicine 9, 1370-1376 (2003) (Pubitemid 37466185)
37. M. Potente, C. Urbich, K-I. c Sasaki, W.K. Hofmann, C. Heeschen, A. Aicher, R. Kollipara, R.A. DePinho, A. M. Zeiher & S. Dimmeler: Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J. Clin. Invest. 115, 2382-2392 (2005) (Pubitemid 41266200)
38. M. Potente, B. Fisslthaler, R. Busse & I. Fleming: 11, 12-Epoxyeicosatrienoic acid-induced inhibition of FOXO factors promotes endothelial proliferation by down-regulating p27Kip1. J Biol Chem .278(32):29619-29125 (2003)
39. MB Harris, H Ju, VJ Venema, H. Liang, R. Zou, B.J. Michell, Z-P. Chen, B.E. Kemp & R.C. Venema: Reciprocal phosphorylation and regulation of endothelial nitric-oxide synthase in response to bradykinin stimulation. J Biol Chem 276, 16587-16591 (2001)
40. K. Minai, T. Matsumoto, H. Horie, N. Ohira , H. Takashima, H. Yokohama & M. Kinoshita: Bradykinin stimulates the release of tissue plasminogen activator in human coronary circulation: effects of angiotensinconverting enzyme inhibitors. J Am Coll Cardiol 37, 1565-1570 (2001)
41. I. Shiojima & K. Walsh: Role of Akt in vascular homeostastasis and angiogenesis. Circ Res 90, 1243-50 (2002) (Pubitemid 34787405)
42. S. Gadau, C. Emanueli, S. Van Linthout, G. Graiani, M. Todaro, M. Meloni, I. Campesi, G. Invernici, F. Spillmann, K. Ward & P. Madeddu: Benfotiamine accelerates the healing of ischaemic diabetic limbs in mice through protein kinase B/Akt-mediated potentiation of angiogenesis and inhibition of apoptosis. Diabetologia 49, 405-420 (2006) (Pubitemid 43185412)