Effects of aging on the collateral circulation, and therapeutic implications

Circulation

Volumn 125, Issue 25, 2012, Pages 3211-3219

  Epstein, Stephen E ^a   Lassance Soares, Roberta M ^a   Faber, James E ^b   Burnett, Mary Susan ^a  

^a WASHINGTON HOSPITAL CENTER   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

aging; collateral circulation; eNOS; rarefaction

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; MICRORNA; SILDENAFIL; TADALAFIL;

AGING; ARTERY BLOOD FLOW; ARTERY DIAMETER; ARTERY OCCLUSION; CELL FUNCTION; COLLATERAL CIRCULATION; ENZYME INHIBITION; HEMATOPOIETIC STEM CELL; HEREDITY; HUMAN; MICROVASCULAR ISCHEMIA; NONHUMAN; OUTCOME ASSESSMENT; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; STEM CELL MOBILIZATION;

AGING; ANIMALS; COLLATERAL CIRCULATION; CORONARY ARTERY DISEASE; HUMANS; SIGNAL TRANSDUCTION;

EID: 84863195535     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.111.079038     Document Type: Review

References (56)

1. Mukherjee D, Bhatt DL, Roe MT, Patel V, Ellis SG. Direct myocardial revascularization and angiogenesis-how many patients might be eligible? Am J Cardiol. 1999;84:598-600. (Pubitemid 29408596)
2. Zhang H, Prabhakar P, Sealock R, Faber JE. Wide genetic variation in the native pial collateral circulation is a major determinant of variation in severity of stroke. J Cereb Blood Flow Metab. 2010;30:923-934.
3. Chalothorn D, Faber JE. Strain-dependent variation in native collateral function in mouse hindlimb. Physiol Genomics. 2010;42:469-479.
4. Chalothorn D, Zhang H, Smith JE, Edwards JC, Faber JE. Chloride intracellular channel-4 is a determinant of native collateral formation in skeletal muscle and brain. Circ Res. 2009;2:105.
5. Meier P, Gloekler S, Zbinden R, Beckh S, de Marchi SF, Zbinden S, Wustmann K, Billinger M, Vogel R, Cook S, Wenaweser P, Togni M, Windecker S, Meier B, Seiler C. Beneficial effect of recruitable col-laterals: a 10-year follow-up study in patients with stable coronary artery disease undergoing quantitative collateral measurements. Circulation. 2007;116:975-983. (Pubitemid 47329562)
6. Losordo DW, Henry TD, Davidson C, Sup Lee J, Costa MA, Bass T, Mendelsohn F, Fortuin FD, Pepine CJ, Traverse JH, Amrani D, Ewenstein BM, Riedel N, Story K, Barker K, Povsic TJ, Harrington RA, Schatz RA; ACT34-CMI Investigators. Intramyocardial, autologous CD34+ cell therapy for refractory angina. Circ Res. 2011;109:428-436.
7. Traverse JH, Henry TD, Ellis SG, Pepine CJ, Willerson JT, Zhao DX, Forder JR, Byrne BJ, Hatzopoulos AK, Penn MS, Perin EC, Baran KW, Chambers J, Lambert C, Raveendran G, Simon DI, Vaughan DE, Simpson LM, Gee AP, Taylor DA, Cogle CR, Thomas JD, Silva GV, Jorgenson BC, Olson RE, Bowman S, Francescon J, Geither C, Handberg E, Smith DX, Baraniuk S, Piller LB, Loghin C, Aguilar D, Richman S, Zierold C, Bettencourt J, Sayre SL, Vojvodic RW, Skarlatos SI, Gordon DJ, Ebert RF, Kwak M, Moyé LA, Simari RD; Cardiovascular Cell Therapy ResearchNetwork. Effect of intracoronary delivery of autologous bone marrow mononuclear cells 2 to 3 weeks following acute myocardial infarction on left ventricular function: the LateTIME randomized trial. JAMA. 2011;306:2110-2119.
8. Kinnaird T, Stabile E, Zbinden S, Burnett MS, Epstein SE. Cardiovascular risk factors impair native collateral development and may impair efficacy of therapeutic interventions. Cardiovasc Res. 2008;78:257-264. (Pubitemid 351556098)
9. Faber JE, Dai X, Lucitti J. Genetic and environmental mechanisms controlling formation and maintenance of the native collateral circulation. In: I. E Deindl IE, Schaper W, eds. Arteriogenesis-Molecular Regulation, Pathophysiology and Therapeutics. Achen, Germany: Shaker Verlag; 2011.
10. Mac Gabhann F, Peirce SM. Collateral capillary arterialization following arteriolar ligation in murine skeletal muscle. Microcirculation. 2010;17: 333-347.
11. Chalothorn D, Faber JE. Formation and maturation of the native cerebral collateral circulation. J Mol Cell Cardiol. 2010;49:251-259.
12. Maxwell MP Hearse DJ, Yellon DM. Species variation in the coronary collateral circulation during regional myocardial ischaemia: a critical determinant of the rate of evolution and extent of myocardial infarction. Cardiovascular Res. 1987;21:737-746. (Pubitemid 17144243)
13. Clayton JA, Chalothorn D, Faber JE. Vascular endothelial growth factor-A specifies formation of native collaterals and regulates collateral growth in ischemia. Circ Res. 2008;103:1027-1036.
14. Wang S, Zhang H, Dai X, Sealock R, Faber JE. Genetic architecture underlying variation in extent and remodeling of the collateral circulation. Circ Res. 2010;107:558-568.
15. Goldstein RE, Michaelis LL, Morrow AG, Epstein SE. Coronary collateral function in patients without occlusive coronary artery disease. Circulation. 1975;51:118-125.
16. Wustmann K, Zbinden S, Windecker S, Meier B, Seiler C. Is there functional collateral flow during vascular occlusion in angiographically normal coronary arteries? Circulation. 2003;107:2213-2220. (Pubitemid 36547215)
17. Rivard A, Fabre JE, Silver M, Chen D, Murohara T, Kearney M, Magner M, Asahara T, Isner JM. Age-dependent impairment of angiogenesis. Circulation. 1999;99:111-120. (Pubitemid 29035965)
18. Bosch-Marce M, Okuyama H, Wesley JB, Sarkar K, Kimura H, Liu YV, Zhang H, Strazza M, Rey S, Savino L, Zhou YF, McDonald KR, Na Y, Vandiver S, Rabi A, Shaked Y, Kerbel R, Lavallee T, Semenza GL. Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia. Circ Res. 2007;101:1310-1318. (Pubitemid 350294648)
19. Wang J, Peng X, Lassance-Soares RM, Najafi AH, Alderman LO, Sood S, Xue Z, Chan R, Faber JE, Epstein SE, Burnett MS. Aging-induced collateral dysfunction: impaired responsiveness of collaterals and susceptibility to apoptosis via dysfunctional eNOS signaling. J Cardiovasc Transl Res. 2011;6:779-789.
20. Faber JE, Zhang H, Lassance-Soares RM, Prabhakar P, Najafi AH, Burnett MS, Epstein SE. Aging causes collateral rarefaction and increased severity of ischemic injury in multiple tissues. Arterioscler Thromb Vasc Biol. 2011;31:1748-1756.
21. Sonntag WE, Lynch CD, Cooney PT, Hutchins PM. Decreases in cerebral microvasculature with age are associated with the decline in growth hormone and insulin-like growth factor 1. Endocrinology. 1997;138: 3515-3520. (Pubitemid 27345707)
22. Heil M, Schaper W. Influence of mechanical, cellular, and molecular factors on collateral artery growth (arteriogenesis). Circ Res. 2004;95: 449-458. (Pubitemid 39180925)
23. Sampath R, Kukielka GL, Smith CW, Eskin SG, McIntire LV. Shear stress-mediated changes in the expression of leukocyte adhesion receptors on human umbilical vein endothelial cells in vitro. Ann Biomed Eng. 1995;23:247-256.
24. Lee CW, Stabile E, Kinnaird T, Shou M, Devaney JM, Epstein SE, Burnett MS. Temporal patterns of gene expression after acute hindlimb ischemia in mice: insights into the genomic program for collateral vessel development. J Am Coll Cardiol. 2004;43:474-482. (Pubitemid 38167711)
25. Arras M, Ito WD, Scholz D, Winkler B, Schaper J, Schaper W. Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. J Clin Invest. 1998;101:40-50. (Pubitemid 28058901)
26. Stabile E, Kinnaird T, la Sala A, Hanson SK, Watkins C, Campia U, Shou M, Zbinden S, Fuchs S, Kornfeld H, Epstein SE, Burnett MS. Cd8+T lymphocytes regulate the arteriogenic response to ischemia by infiltrating the site of collateral vessel development and recruiting CD4+ mononuclear cells through the expression of interleukin-16. Circulation. 2006; 113:118-124. (Pubitemid 43958496)
27. Ziegelhoeffer T, Fernandez B, Kostin S, Heil M, Voswinckel R, Helisch A, Schaper W. Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ Res. 2004;94:230-238. (Pubitemid 38197456)
28. Stabile E, Burnett MS, Watkins C, Kinnaird T, Bachis A, la Sala A, Miller JM, Shou M, Epstein SE, Fuchs S. Impaired arteriogenic response to acute hindlimb ischemia in CD4-knockout mice. Circulation. 2003; 108:205-210. (Pubitemid 36871304)
29. Kinnaird T, Stabile E, Burnett MS, Lee CW, Barr S, Fuchs S, Epstein SE. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res. 2004;94:678-685. (Pubitemid 38387752)
30. Wang M, Monticone RE, Lakatta EG. Arterial aging: a journey into subclinical arterial disease. Curr Opin Nephrol Hypertens. 2010;19: 201-207.
31. Kurotobi T, Sato H, Kinjo K, Nakatani D, Mizuno H, Shimizu M, Imai K, Hirayama A, Kodama K, Hori M; OACIS Group. Reduced collateral circulation to the infarct-related artery in elderly patients with acute myocardial infarction. J Am Coll Cardiol. 2004;44:28-34. (Pubitemid 38968451)
32. Schulz E, Jansen T, Wenzel P, Daiber A, Münzel T. Nitric oxide, tetrahydrobiopterin, oxidative stress, and endothelial dysfunction in hypertension. Antioxid Redox Signal. 2008;10:1115-1126. (Pubitemid 351451710)
33. Sun D, Huang A, Yan EH, Wu Z, Yan C, Kaminski PM, Oury TD, Wolin MS, Kaley G. Reduced release of nitric oxide to shear stress in mesenteric arteries of aged rats. Am J Physiol Heart Circ Physiol. 2004;286: H2249-H2256. (Pubitemid 38685240)
34. Dai X, Faber JE. eNOS deficiency causes collateral vessel rarefaction and impairs activation of a cell cycle gene network during arteriogenesis. Circ Res. 2010;106:1870-1881.
35. Csiszar A, Ungvari Z, Edwards JG, Kaminski P, Wolin MS, Koller A, Kaley G. Aging-induced phenotypic changes and oxidative stress impair coronary arteriolar function. Circ Res. 2002;90:1159-1166. (Pubitemid 34786900)
36. Yu J, deMuinck ED, Zhuang Z, Drinane M, Kauser K, Rubanyi GM, Qian HS, Murata T, Escalante B, Sessa WC. Endothelial nitric oxide synthase is critical for ischemic remodeling, mural cell recruitment, and blood flow reserve. Proc Natl Acad Sci USA. 2005;102:10999-11004. (Pubitemid 41105982)
37. Xin Y, Wang YM, Zhang H, Li J, Wang W, Wei YJ, Hu SS. Aging adversely impacts biological properties of human bone marrow-derived mesenchymal stem cells: implications for tissue engineering heart valve construction. Artif Organs. 2010;34:215-222.
38. Hoffmann J, Haendeler J, Aicher A, Rossig L, Vasa M, Zeiher AM, Dimmeler S. Aging enhances the sensitivity of endothelial cells toward apoptotic stimuli: important role of nitric oxide. Circ Res. 2001;89: 709-715. (Pubitemid 34627071)
39. Wink DA, Miranda KM, Espey MG, Pluta RM, Hewett SJ, Colton C, Vitek M, Feelisch M, Grisham MB. Mechanisms of the antioxidant effects of nitric oxide. Antioxid Redox Signal. 2001;3:203-213. (Pubitemid 32473337)
40. Landmesser U, Dikalov S, Price SR, McCann L, Fukai T, Holland SM, Mitch WE, Harrison DG. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest. 2003;111:1201-1209. (Pubitemid 36519937)
41. Sullivan JC, Loomis ED, Collins M, Imig JD, Inscho EW, Pollock JS. Age-related alterations in NOS and oxidative stress in mesenteric arteries from male and female rats. J Appl Physiol. 2004;97:1268-1274. (Pubitemid 39299340)
42. Dimmeler S, Fisslthaler B, Fleming I, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells via Akt-dependent phosphorylation. Nature. 1999;399:601-605.
43. Chen C-A, Druhan LJ, Varadharaj S, Chen Y-R, ZweierJL. Phosphorylation of endothelial nitric-oxide synthase regulates superoxide generation from the enzyme. J Biol Chem. 2008:283:27038-27047.
44. Schäfer A, Fraccarollo D, Pförtsch S, Flierl U, Vogt C, Pfrang J, Kobsar A, Renné T, Eigenthaler M, Ertl G, Bauersachs J. Improvement of vascular function by acute and chronic treatment with the PDE-5 inhibitor sildenafil in experimental diabetes mellitus. Br J Pharmacol. 2008;153: 886-893. (Pubitemid 351328925)
45. Miller SJ, Coppinger BJ, Zhou X, Unthank JL. Antioxidants reverse age-related collateral growth impairment. J Vasc Res. 2010;47:108-114.
46. Pandey AC, Semon J, Kaushal D, O'Sullivan RP, Glowacki J, Gimble JM, Bunnell BA. MicroRNA profiling reveals age dependent differential expression of nuclear factor kappa B and mitogen-activated protein kinase in adipose and bone marrow-derived human mesenchymal stem cells. Stem Cell Res Ther. 2011;2:49.
47. Weber M, Baker MB, Moore JP, Searles CD. MiR-21 is induced in endothelial cells by shear stress and modulates apoptosis and eNOS activity. Biochem Biophys Res Commun. 2010;393:643-648.
48. He L, He, X Lim LP, de Stanchina E, Xuan Z, Liang Y, Xue W, Zender L, Magnus J, Ridzon D, Jackson AL, Linsley PS, Chen C, Lowe SW, Cleary MA, Hannon GJ. A microRNA component of the p53 tumour suppressor network. Nature. 2007;447:1130-1134. (Pubitemid 47014436)
49. Chamorro-Jorganes A, Araldi E, Penalva LO, Sandhu D, Fernández- Hernando C, Suárez Y. MicroRNA-16 and MicroRNA-424 regulate cellautonomous angiogenic functions in endothelial cells via targeting vascular endothelial growth factor receptor-2 and fibroblast growth factor receptor-1. Arterioscler Thromb Vasc Biol. 2011;31:2595-2606.
50. Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, Richardson JA, Bassel-Duby R, Olson EN. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell. 2008;15: 261-271.
51. Bonauer A, Carmona G, Iwasaki M, Mione M, Koyanagi M, Fischer A, Burchfield J, Fox H, Doebele C, Ohtani K, Chavakis E, Potente M, Tjwa M, Urbich C, Zeiher AM, Dimmeler S. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science. 2009;324:1710-1713.
52. Liu LZ, Li C, Chen Q, Jing Y, Carpenter R, Jiang Y, Kung HF, Lai L, Jiang BH. MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1-expression. PLoS One. 2011;6:e19139.
53. Zhao T, Li J, Chen AF. Microrna-34a induces endothelial progenitor cell senescence and impedes its angiogenesis via suppressing silent information regulator 1. Am J Physiol Endocrinol Metab. 2010;299: E110-E116.
54. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, Teruya-Feldstein J, Reinhardt F, Onder TT, Valastyan S, Westermann F, Speleman F, Vandesompele J, Weinberg RA. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol. 2010;12:247-256.
55. Chang EI, Loh SA, Ceradini DJ, Chang EI, Lin SE, Bastidas N, Aarabi S, Chan DA, Freedman ML, Giaccia AJ, Gurtner GC. Age decreases endothelial progenitor cell recruitment through decreases in hypoxia-inducible factor 1alpha stabilization during ischemia. Circulation. 2007;116: 2818-2829. (Pubitemid 350291224)
56. Clough GF, Norman M. The microcirculation: a target for developmental priming. Microcirculation. 2011;18:286-297.