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From the Departments of Medicine (Cardiology) and Biomedical
Research,*
St. Elizabeth's Medical Center, Tufts University
School of Medicine, Boston, Massachusetts, and Department of Medicine
(Cardiology),
Duke University, Durham,
North Carolina
Diabetes is a major risk factor for coronary and peripheral artery
diseases. Although diabetic patients often present with advanced forms
of these diseases, it is not known whether the compensatory
mechanisms to vascular ischemia are affected in this condition.
Accordingly, we sought to determine whether diabetes could: 1)
impair the development of new collateral vessel formation in response
to tissue ischemia and 2) inhibit cytokine-induced therapeutic
neovascularization. Hindlimb ischemia was created by femoral artery
ligation in nonobese diabetic mice (NOD mice,
n = 20) and in control C57 mice
(n = 20). Hindlimb perfusion was evaluated by
serial laser Doppler studies after the surgery. In NOD mice,
measurement of the Doppler flow ratio between the ischemic and the
normal limb indicated that restoration of perfusion in the ischemic
hindlimb was significantly impaired. At day 14 after surgery,
Doppler flow ratio in the NOD mice was 0.49 ± 0.04
versus 0.73 ± 0.06 for the C57 mice
(P 
0.005). This impairment in blood flow
recovery persisted throughout the duration of the study with Doppler
flow ratio values at day 35 of 0.50 ± 0.05 versus
0.90 ± 0.07 in the NOD and C57 mice, respectively
(P 0.001). CD31 immunostaining confirmed the
laser Doppler data by showing a significant reduction in capillary
density in the NOD mice at 35 days after surgery (302 ± 4
capillaries/mm2 versus 782 ± 78 in C57
mice (P 0.005). The reduction in
neovascularization in the NOD mice was the result of a lower level of
vascular endothelial growth factor (VEGF) in the ischemic
tissues, as assessed by Northern blot, Western blot and
immunohistochemistry. The central role of VEGF was confirmed by showing
that normal levels of neovascularization (compared with C57) could be
achieved in NOD mice that had been supplemented for this growth factor
via intramuscular injection of an adenoviral vector encoding for VEGF.
We conclude that 1) diabetes impairs endogenous neovascularization of
ischemic tissues; 2) the impairment in new blood vessel formation
results from reduced expression of VEGF; and 3) cytokine
supplementation achieved by intramuscular adeno-VEGF gene transfer
restores neovascularization in a mouse model of diabetes.
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E. Chou, I. Suzuma, K. J. Way, D. Opland, A. C. Clermont, K. Naruse, K. Suzuma, N. L. Bowling, C. J. Vlahos, L. P. Aiello, et al. Decreased Cardiac Expression of Vascular Endothelial Growth Factor and Its Receptors in Insulin-Resistant and Diabetic States: A Possible Explanation for Impaired Collateral Formation in Cardiac Tissue Circulation, January 22, 2002; 105(3): 373 - 379. [Abstract] [Full Text] [PDF]
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 K.S. MOULTON Plaque Angiogenesis: Its Functions and Regulation Cold Spring Harb Symp Quant Biol, January 1, 2002; 67(0): 471 - 482. [Abstract] [PDF]
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 Z S Kyriakides, S Psychari, N Chrysomallis, M Georgiadis, E Sbarouni, and D T Kremastinos Type II diabetes does not prevent the recruitment of collateral vessels and the normal reduction of myocardial ischaemia on repeated balloon inflations during angioplasty Heart, January 1, 2002; 87(1): 61 - 66. [Abstract] [Full Text] [PDF]
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 S. B. Freedman and J. M. Isner Therapeutic Angiogenesis for Coronary Artery Disease Ann Intern Med, January 1, 2002; 136(1): 54 - 71. [Abstract] [Full Text] [PDF]
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P. Porcu, C. Emanueli, M. Kapatsoris, J. Chao, L. Chao, and P. Madeddu Reversal of Angiogenic Growth Factor Upregulation by Revascularization of Lower Limb Ischemia Circulation, January 1, 2002; 105(1): 67 - 72. [Abstract] [Full Text] [PDF]
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Y. Taniyama, R. Morishita, K. Hiraoka, M. Aoki, H. Nakagami, K. Yamasaki, K. Matsumoto, T. Nakamura, Y. Kaneda, and T. Ogihara Therapeutic Angiogenesis Induced by Human Hepatocyte Growth Factor Gene in Rat Diabetic Hind Limb Ischemia Model: Molecular Mechanisms of Delayed Angiogenesis in Diabetes Circulation, November 6, 2001; 104(19): 2344 - 2350. [Abstract] [Full Text] [PDF]
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S. Takeshita, H. Tomiyama, N. Yokoyama, Y. Kawamura, T. Furukawa, Y. Ishigai, T. Shibano, T. Isshiki, and T. Sato Angiotensin-converting enzyme inhibition improves defective angiogenesis in the ischemic limb of spontaneously hypertensive rats Cardiovasc Res, November 1, 2001; 52(2): 314 - 320. [Abstract] [Full Text] [PDF]
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 D. A. Elson, G. Thurston, L. E. Huang, D. G. Ginzinger, D. M. McDonald, R. S. Johnson, and J. M. Arbeit Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor-1{alpha} Genes & Dev., October 1, 2001; 15(19): 2520 - 2532. [Abstract] [Full Text] [PDF]
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R Tabibiazar and S.G Rockson Angiogenesis and the ischaemic heart Eur. Heart J., June 1, 2001; 22(11): 903 - 918. [PDF]
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 Z. T. Bloomgarden European Association for the Study of Diabetes Annual Meeting, 2000: Pathogenesis of type 2 diabetes, vascular disease, and neuropathy Diabetes Care, June 1, 2001; 24(6): 1115 - 1119. [Full Text]
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 D. Simovic, J. M. Isner, A. H. Ropper, A. Pieczek, and D. H. Weinberg Improvement in Chronic Ischemic Neuropathy After Intramuscular phVEGF165 Gene Transfer in Patients With Critical Limb Ischemia Arch Neurol, May 1, 2001; 58(5): 761 - 768. [Abstract] [Full Text] [PDF]
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L. E. Benjamin Glucose, VEGF-A, and Diabetic Complications Am. J. Pathol., April 1, 2001; 158(4): 1181 - 1184. [Full Text] [PDF]
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J. Waltenberger Impaired collateral vessel development in diabetes: potential cellular mechanisms and therapeutic implications Cardiovasc Res, February 16, 2001; 49(3): 554 - 560. [Abstract] [Full Text] [PDF]
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 C. Kalka, H. Tehrani, B. Laudenberg, P. R. Vale, J. M. Isner, T. Asahara, and J. F. Symes VEGF gene transfer mobilizes endothelial progenitor cells in patients with inoperable coronary disease Ann. Thorac. Surg., September 1, 2000; 70(3): 829 - 834. [Abstract] [Full Text] [PDF]
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 A. W. Griffioen and G. Molema Angiogenesis: Potentials for Pharmacologic Intervention in the Treatment of Cancer, Cardiovascular Diseases, and Chronic Inflammation Pharmacol. Rev., June 1, 2000; 52(2): 237 - 268. [Abstract] [Full Text] [PDF]
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G. Walter, E. R. Barton, and H. L. Sweeney Noninvasive measurement of gene expression in skeletal muscle PNAS, May 9, 2000; 97(10): 5151 - 5155. [Abstract] [Full Text] [PDF]
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P. Sinnaeve, O. Varenne, D. Collen, and S. Janssens Gene therapy in the cardiovascular system: an update Cardiovasc Res, December 1, 1999; 44(3): 498 - 506. [Abstract] [Full Text] [PDF]
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C. Kalka, H. Masuda, T. Takahashi, W. M. Kalka-Moll, M. Silver, M. Kearney, T. Li, J. M. Isner, and T. Asahara Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization PNAS, March 28, 2000; 97(7): 3422 - 3427. [Abstract] [Full Text] [PDF]
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 S. C. FRANCIS, M. K. RAIZADA, A. A. MANGI, L. G. MELO, V. J. DZAU, P. R. VALE, J. M. ISNER, D. W. LOSORDO, J. CHAO, M. J. KATOVICH, et al. Genetic targeting for cardiovascular therapeutics: are we near the summit or just beginning the climb? Physiol Genomics, December 21, 2001; 7(2): 79 - 94. [Abstract] [Full Text] [PDF]
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