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(Circulation. 1999;99:111-120.)
© 1999 American Heart Association, Inc.
Basic Science Reports |
Age-Dependent Impairment of Angiogenesis
Presented in preliminary form as finalist presentation for the Melvin Marcus Young Investigator Award at the 70th Scientific Sessions of the American Heart Association, November 9–12, 1997, and published in abstract form (Circulation. 1997;96:I-J).
From the Departments of Medicine (Cardiology) and Biomedical Research, St. Elizabeth's Medical Center, Tufts University School of Medicine, Boston, Mass.
Correspondence to Jeffrey M. Isner, MD, St. Elizabeth's Medical Center, 736 Cambridge St, Boston, MA 02135. E-mail jisner{at}opal.tufts.edu
Background—The effect of aging on angiogenesis in ischemic vascular disease has not been studied. Accordingly, we investigated the hypothesis that angiogenesis is impaired as a function of age.
Methods and Results—Forty days after the resection of 1 femoral artery, collateral vessel development was significantly impaired in old (aged 4 to 5 years; n=7) versus young (aged 6 to 8 months; n=6) New Zealand White (NZW) rabbits on the basis of reduced hindlimb perfusion (ischemic: normal blood pressure ratio=0.58±0.05 versus 0.77±0.06; P<0.005), reduced number of angiographically visible vessels (angiographic score=0.48±0.05 versus 0.70±0.05; P<0.01), and lower capillary density in the ischemic limb (130.3±5.8/mm2 versus 171.4±9.5/mm2; P<0.001). Angiogenesis was also impaired in old (aged 2 years) versus young (aged 12 weeks) mice as shown by reduced hindlimb perfusion (measured by laser Doppler imaging) and lower capillary density (353.0±14.3/mm2 versus 713.3±63.4/mm2; P<0.01). Impaired angiogenesis in old animals was the result of impaired endothelial function (lower basal NO release and decreased vasodilation in response to acetylcholine) and a lower expression of vascular endothelial growth factor (VEGF) in ischemic tissues (by Northern blot, Western blot, and immunohistochemistry). When recombinant VEGF protein was administered to young and old rabbits, both groups exhibited a significant and similar increase in blood pressure ratio, angiographic score, and capillary density.
Conclusions—Angiogenesis responsible for collateral development in limb ischemia is impaired with aging; responsible mechanisms include age-related endothelial dysfunction and reduced VEGF expression. Advanced age, however, does not preclude augmentation of collateral vessel development in response to exogenous angiogenic cytokines.
Key Words: growth substances • endothelium • aging • angiogenesis
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 E. Sadoun and M. J. Reed Impaired Angiogenesis in Aging Is Associated with Alterations in Vessel Density, Matrix Composition, Inflammatory Response, and Growth Factor Expression J. Histochem. Cytochem., September 1, 2003; 51(9): 1119 - 1130. [Abstract] [Full Text] [PDF]
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T. Koike, R. B. Vernon, M. D. Gooden, E. Sadoun, and M. J. Reed Inhibited Angiogenesis in Aging: A Role for TIMP-2 J. Gerontol. A Biol. Sci. Med. Sci., September 1, 2003; 58(9): B798 - 805. [Abstract] [Full Text] [PDF]
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C. Patterson The Ponzo Effect: Endothelial Progenitor Cells Appear on the Horizon Circulation, June 24, 2003; 107(24): 2995 - 2997. [Full Text] [PDF]
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 Y. Ootaki, M. Yamaguchi, N. Yoshimura, S. Oka, M. Yoshida, and T. Hasegawa Vascular endothelial growth factor in children with congenital heart disease Ann. Thorac. Surg., May 1, 2003; 75(5): 1523 - 1526. [Abstract] [Full Text] [PDF]
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H. Masuda and T. Asahara Post-natal endothelial progenitor cells for neovascularization in tissue regeneration Cardiovasc Res, May 1, 2003; 58(2): 390 - 398. [Abstract] [Full Text] [PDF]
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N. van Royen, I. Hoefer, M. Bottinger, J. Hua, S. Grundmann, M. Voskuil, C. Bode, W. Schaper, I. Buschmann, and J.J. Piek Local Monocyte Chemoattractant Protein-1 Therapy Increases Collateral Artery Formation in Apolipoprotein E-Deficient Mice but Induces Systemic Monocytic CD11b Expression, Neointimal Formation, and Plaque Progression Circ. Res., February 7, 2003; 92(2): 218 - 225. [Abstract] [Full Text] [PDF]
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E. G. Lakatta Arterial and Cardiac Aging: Major Shareholders in Cardiovascular Disease Enterprises: Part III: Cellular and Molecular Clues to Heart and Arterial Aging Circulation, January 28, 2003; 107(3): 490 - 497. [Full Text] [PDF]
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J. M. Edelberg Auto Repair on the Aging Stem Cell Superhighway Sci. Aging Knowl. Environ., September 4, 2002; 2002(35): pe13 - 13. [Abstract] [Full Text]
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Z. S. Katusic Therapeutic Angiogenesis: New Indication for Endothelial NO Synthase Gene Transfer Arterioscler Thromb Vasc Biol, August 1, 2002; 22(8): 1254 - 1255. [Full Text] [PDF]
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J. L. Tuttle, T. L. Hahn, B. M. Sanders, F. A. Witzmann, S. J. Miller, M. C. Dalsing, and J. L. Unthank Impaired collateral development in mature rats Am J Physiol Heart Circ Physiol, July 1, 2002; 283(1): H146 - H155. [Abstract] [Full Text] [PDF]
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T. Krabatsch, R. Petzina, H. Hausmann, A. Koster, and R. Hetzer Factors influencing results and outcome after transmyocardial laser revascularization Ann. Thorac. Surg., June 1, 2002; 73(6): 1888 - 1892. [Abstract] [Full Text] [PDF]
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J. M. Edelberg, L. Tang, K. Hattori, D. Lyden, and S. Rafii Young Adult Bone Marrow-Derived Endothelial Precursor Cells Restore Aging-Impaired Cardiac Angiogenic Function Circ. Res., May 31, 2002; 90 (10): e89 - e93. [Abstract] [Full Text] [PDF]
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K. Przyklenk and P. Whittaker Reply J. Am. Coll. Cardiol., May 15, 2002; 39(10): 1701 - 1702. [Full Text] [PDF]
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S. Marchetti, C. Gimond, K. Iljin, C. Bourcier, K. Alitalo, J. Pouyssegur, and G. Pages Endothelial cells genetically selected from differentiating mouse embryonic stem cells incorporate at sites of neovascularization in vivo J. Cell Sci., May 15, 2002; 115(10): 2075 - 2085. [Abstract] [Full Text] [PDF]
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 D. G. Espinosa-Heidmann, I. Suner, E. P. Hernandez, W. D. Frazier, K. G. Csaky, and S. W. Cousins Age as an Independent Risk Factor for Severity of Experimental Choroidal Neovascularization Invest. Ophthalmol. Vis. Sci., May 1, 2002; 43(5): 1567 - 1573. [Abstract] [Full Text] [PDF]
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J. M. Edelberg, J. T. Jacobson, D. S. Gidseg, L. Tang, and D. J. Christini Enhanced myocyte-based biosensing of the blood-borne signals regulating chronotropy J Appl Physiol, February 1, 2002; 92(2): 581 - 585. [Abstract] [Full Text] [PDF]
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 S. Franco, I. Segura, H. H. Riese, and M. A. Blasco Decreased B16F10 Melanoma Growth and Impaired Vascularization in Telomerase-deficient Mice with Critically Short Telomeres Cancer Res., January 1, 2002; 62(2): 552 - 559. [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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T. Pohl, C. Seiler, M. Billinger, E. Herren, K. Wustmann, H. Mehta, S. Windecker, F. R. Eberli, and B. Meier Frequency distribution of collateral flow and factors influencing collateral channel development: Functional collateral channel measurement in 450 patients with coronary artery disease J. Am. Coll. Cardiol., December 1, 2001; 38(7): 1872 - 1878. [Abstract] [Full Text] [PDF]
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K. Przyklenk, G. Li, and P. Whittaker No loss in the in vivo efficacy of ischemic preconditioning in middle-aged and old rabbits J. Am. Coll. Cardiol., November 15, 2001; 38(6): 1741 - 1747. [Abstract] [Full Text] [PDF]
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P. Abete, N. Ferrara, F. Cacciatore, E. Sagnelli, M. Manzi, V. Carnovale, C. Calabrese, D. de Santis, G. Testa, G. Longobardi, et al. High level of physical activity preserves the cardioprotective effect of preinfarction angina in elderly patients J. Am. Coll. Cardiol., November 1, 2001; 38(5): 1357 - 1365. [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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A. S. Khan, C. D. Lynch, D. C. Sane, M. C. Willingham, and W. E. Sonntag Growth Hormone Increases Regional Coronary Blood Flow and Capillary Density in Aged Rats J. Gerontol. A Biol. Sci. Med. Sci., August 1, 2001; 56(8): B364 - 371. [Abstract] [Full Text] [PDF]
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C. Emanueli, M. B. Salis, T. Stacca, L. Gaspa, J. Chao, L. Chao, A. Piana, and P. Madeddu Rescue of Impaired Angiogenesis in Spontaneously Hypertensive Rats by Intramuscular Human Tissue Kallikrein Gene Transfer Hypertension, July 1, 2001; 38(1): 136 - 141. [Abstract] [Full Text] [PDF]
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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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M. Simons Therapeutic coronary angiogenesis: a fronte praecipitium a tergo lupi? Am J Physiol Heart Circ Physiol, May 1, 2001; 280(5): H1923 - H1927. [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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E. VASILE, Y. TOMITA, L. F. BROWN, O. KOCHER, and H. F. DVORAK Differential expression of thymosin {beta}-10 by early passage and senescent vascular endothelium is modulated by VPF/VEGF: evidence for senescent endothelial cells in vivo at sites of atherosclerosis FASEB J, February 1, 2001; 15(2): 458 - 466. [Abstract] [Full Text] [PDF]
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