Angiogenic response to passive movement and active exercise in individuals with peripheral arterial disease

Journal of Applied Physiology

Volumn 115, Issue 12, 2013, Pages 1777-1787

  Hoier, B ^a   Walker, M ^b   Passos, M ^a,c   Walker, P J ^d,e   Green, A ^d   Bangsbo, J ^a   Askew, C D ^b   Hellsten, Y ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF THE SUNSHINE COAST   (Australia)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

Author keywords

Capillary; Intermittent claudication; Microdialysis; Skeletal muscle; Vascular endothelial growth factor

Indexed keywords

ANGIOPOIETIN 2; MESSENGER RNA; THROMBOSPONDIN 1; VASCULOTROPIN; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1;

AGED; ANGIOGENESIS; ARTICLE; CAPILLARY; CASE CONTROL STUDY; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; EXERCISE; FEMALE; GENETICS; HUMAN; INTERMITTENT CLAUDICATION; MALE; METABOLISM; MICRODIALYSIS; MIDDLE AGED; PATHOPHYSIOLOGY; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; SKELETAL MUSCLE;

CAPILLARY; INTERMITTENT CLAUDICATION; MICRODIALYSIS; SKELETAL MUSCLE; VASCULAR ENDOTHELIAL GROWTH FACTOR;

AGED; ANGIOPOIETIN-2; CASE-CONTROL STUDIES; EXERCISE; FEMALE; HUMANS; MALE; MIDDLE AGED; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; PERIPHERAL ARTERIAL DISEASE; RNA, MESSENGER; THROMBOSPONDIN 1; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84891275461     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00979.2013     Document Type: Article

References (56)

1. Askew CD, Green S, Walker PJ, Kerr GK, Green AA, Williams AD, Febbraio MA. Skeletal muscle phenotype is associated with exercise tolerance in patients with peripheral arterial disease. J Vasc Surg 41: 802-807, 2005.
2. Bongrazio M, Da Silva-Azevedo L, Bergmann EC, Baum O, Hinz B, Pries AR, Zakrzewicz A. Shear stress modulates the expression of thrombospondin-1 and CD36 in endothelial cells in vitro and during shear stress-induced angiogenesis in vivo. Int J Immunopathol Pharmacol 19: 35-48, 2006.
3. Breen EC, Johnson EC, Wagner H, Tseng HM, Sung LA, Wagner PD. Angiogenic growth factor mRNA responses in muscle to a single bout of exercise. J Appl Physiol 81: 355-361, 1996.
4. Choksy S, Pockley AG, Wajeh YE, Chan P. VEGF and VEGF receptor expression in human chronic critical limb ischaemia. Eur J Vasc Endovasc Surg 28: 660-669, 2004.
5. Dawson JM, Hudlicka O. The effects of long term administration of prazosin on the microcirculation in skeletal muscles. Cardiovasc Res 23: 913-920, 1989.
6. Duscha BD, Robbins JL, Jones WS, Kraus WE, Lye RJ, Sanders JM, Allen JD, Regensteiner JG, Hiatt WR, Annex BH. Angiogenesis in skeletal muscle precede improvements in peak oxygen uptake in peripheral artery disease patients. Arterioscler Thromb Vasc Biol 31: 2742-2748, 2011.
7. Egginton S. Invited review: Activity-induced angiogenesis. Pflügers Arch 457: 963-977, 2009.
8. Folkman J. The role of angiogenesis in tumor growth. Semin Cancer Biol 3: 65-71, 1992.
9. Gavin TP, Ruster RS, Carrithers JA, Zwetsloot KA, Kraus RM, Evans CA, Knapp DJ, Drew JL, McCartney JS, Garry JP, Hickner RC. No difference in the skeletal muscle angiogenic response to aerobic exercise training between young and aged men. J Physiol 585: 231-239, 2007.
10. Gupta K, Gupta P, Wild R, Ramakrishnan S, Hebbel RP. Binding and displacement of vascular endothelial growth factor (VEGF) by thrombospondin: Effect on human microvascular endothelial cell proliferation and angiogenesis. Angiogenesis 3: 147-158, 1999.
11. Gustafsson T, Ameln H, Fischer H, Sundberg CJ, Timmons JA, Jansson E. VEGF-A splice variants and related receptor expression in human skeletal muscle following submaximal exercise. J Appl Physiol 98: 2137-2146, 2005.
12. Gustafsson T, Puntschart A, Kaijser L, Jansson E, Sundberg CJ. Exercise-induced expression of angiogenesis-related transcription and growth factors in human skeletal muscle. Am J Physiol Heart Circ Physiol 276: H679-H685, 1999.
13. Gustafsson T, Rundqvist H, Norrbom J, Rullman E, Jansson E, Sundberg CJ. The influence of physical training on the angiopoietin and VEGF-A systems in human skeletal muscle. J Appl Physiol 103: 1012- 1020, 2007.
14. Hammarsten J, Bylund-Fellenius AC, Holm J, Schersten T, Krotkiewski M. Capillary supply and muscle fibre types in patients with intermittent claudication: Relationships between morphology and metabolism. Eur J Clin Invest 10: 301-305, 1980.
15. Hansen AH, Nielsen JJ, Saltin B, Hellsten Y. Exercise training normalizes skeletal muscle vascular endothelial growth factor levels in patients with essential hypertension. J Hypertens 28: 1176-1185, 2010.
16. Hellsten Y, Nielsen JJ, Lykkesfeldt J, Bruhn M, Silveira L, Pilegaard H, Bangsbo J. Antioxidant supplementation enhances the exercise-induced increase in mitochondrial uncoupling protein 3 and endothelial nitric oxide synthase mRNA content in human skeletal muscle. Free Radic Biol Med 43: 353-361, 2007.
17. Hellsten Y, Rufener N, Nielsen JJ, Hoier B, Krustrup P, Bangsbo J. Passive leg movement enhances interstitial VEGF protein, endothelial cell proliferation, and eNOS mRNA content in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 294: R975-R982, 2008.
18. Hiscock N, Fischer CP, Pilegaard H, Pedersen BK. Vascular endothelial growth factor mRNA expression and arteriovenous balance in response to prolonged, submaximal exercise in humans. Am J Physiol Heart Circ Physiol 285: H1759-H1763, 2003.
19. Hoffner L, Nielsen JJ, Langberg H, Hellsten Y. Exercise but not prostanoids enhance levels of vascular endothelial growth factor and other proliferative agents in human skeletal muscle interstitium. J Physiol 550: 217-225, 2003.
20. Hoier B, Nordsborg N, Andersen S, Jensen L, Nybo L, Bangsbo J, Hellsten Y. Pro- and anti-angiogenic factors in human skeletal muscle in response to acute exercise and training. J Physiol 590: 595-606, 2012.
21. Hoier B, Olsen K, Nyberg M, Bangsbo J, Hellsten Y. Contraction induced secretion of VEGF from skeletal muscle cells is mediated by adenosine. Am J Physiol Heart Circ Physiol 299: H857-H862, 2010.
22. Hoier B, Passos M, Bangsbo J, Hellsten Y. Intense intermittent exercise provides weak stimulus for VEGF secretion and capillary growth in skeletal muscle. Exp Physiol 98: 585-597, 2013.
23. Hoier B, Prats C, Qvortrup K, Pilegaard H, Bangsbo J, Hellsten Y. Subcellular localization and mechanism of secretion of vascular endothelial growth factor in human skeletal muscle. FASEB J 27: 3496-3504, 2013.
24. Hoier B, Rufener N, Bojsen-Moller J, Bangsbo J, Hellsten Y. The effect of passive movement training on angiogenic factors and capillary growth in human skeletal muscle. J Physiol 588: 3833-3845, 2010.
25. Iruela-Arispe ML, Lombardo M, Krutzsch HC, Lawler J, Roberts DD. Inhibition of angiogenesis by thrombospondin-1 is mediated by 2 independent regions within the type 1 repeats. Circulation 100: 1423- 1431, 1999.
26. Jensen L, Schjerling P, Hellsten Y. Regulation of VEGF and bFGF mRNA expression and other proliferative compounds in skeletal muscle cells. Angiogenesis 7: 255-267, 2004.
27. Jones WS, Duscha BD, Robbins JL, Duggan NN, Regensteiner JG, Kraus WE, Hiatt WR, Dokun AO, Annex BH. Alteration in angiogenic and anti-angiogenic forms of vascular endothelial growth factor-A in skeletal muscle of patients with intermittent claudication following exercise training. Vasc Med 17: 94-100, 2012.
28. Kanno S, Oda N, Abe M, Saito S, Hori K, Handa Y, Tabayashi K, Sato Y. Establishment of a simple and practical procedure applicable to therapeutic angiogenesis. Circulation 99: 2682-2687, 1999.
29. Kendall RL, Thomas KA. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci U S A 90: 10705-10709, 1993.
30. Lloyd PG, Prior BM, Yang HT, Terjung RL. Angiogenic growth factor expression in rat skeletal muscle in response to exercise training. Am J Physiol Heart Circ Physiol 284: H1668-H1678, 2003.
31. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton D, McClain J, Aldrich TH, Papadopoulos N, Daly TJ, Davis S, Sato TN, Yancopoulos GD. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277: 55-60, 1997.
32. Makitie J. Skeletal muscle capillaries in intermittent claudication. Arch Pathol Lab Med 101: 500-503, 1977.
33. Malek MH, Olfert IM. Global deletion of thrombospondin-1 increases cardiac and skeletal muscle capillarity and exercise capacity in mice. Exp Physiol 94: 749-760, 2009.
34. Mortensen SP, Askew CD, Walker M, Nyberg M, Hellsten Y. The hyperaemic response to passive leg movement is dependent on nitric oxide: A new tool to evaluate endothelial nitric oxide function. J Physiol 590: 4391-4400, 2012.
35. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 13: 9-22, 1999.
36. Nordsborg N, Mohr M, Pedersen LD, Nielsen JJ, Langberg H, Bangsbo J. Muscle interstitial potassium kinetics during intense exhaustive exercise: Effect of previous arm exercise. Am J Physiol Regul Integr Comp Physiol 285: R143-R148, 2003.
37. Nyberg M, Blackwell JR, Damsgaard R, Jones AM, Hellsten Y, Mortensen SP. Lifelong physical activity prevents an age-related reduction in arterial and skeletal muscle nitric oxide bioavailability in humans. J Physiol 590: 5361-5370, 2012.
38. Olfert IM, Breen EC, Gavin TP, Wagner PD. Temporal thrombospondin- 1 mRNA response in skeletal muscle exposed to acute and chronic exercise. Growth Factors 24: 253-259, 2006.
39. Olfert IM, Howlett RA, Wagner PD, Breen EC. Myocyte vascular endothelial growth factor is required for exercise-induced skeletal muscle angiogenesis. Am J Physiol Regul Integr Comp Physiol 299: R1059- R1067, 2010.
40. Palmer-Kazen U, Religa P, Wahlberg E. Exercise in patients with intermittent claudication elicits signs of inflammation and angiogenesis. Eur J Vasc Endovasc Surg 38: 689-696, 2009.
41. Palmer-Kazen U, Wariaro D, Luo F, Wahlberg E. Vascular endothelial cell growth factor and fibroblast growth factor 2 expression in patients with critical limb ischemia. J Vasc Surg 39: 621-628, 2004.
42. Pilegaard H, Ordway GA, Saltin B, Neufer PD. Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol Endocrinol Metab 279: E806-E814, 2000.
43. Richardson RS, Wagner H, Mudaliar SR, Henry R, Noyszewski EA, Wagner PD. Human VEGF gene expression in skeletal muscle: Effect of acute normoxic and hypoxic exercise. Am J Physiol Heart Circ Physiol 277: H2247-H2252, 1999.
44. Rissanen TT, Vajanto I, Hiltunen MO, Rutanen J, Kettunen MI, Niemi M, Leppanen P, Turunen MP, Markkanen JE, Arve K, Alhava E, Kauppinen RA, Yla-Herttuala S. Expression of vascular endothelial growth factor and vascular endothelial growth factor receptor-2 (KDR/ Flk-1) in ischemic skeletal muscle and its regeneration. Am J Pathol 160: 1393-1403, 2002.
45. Rivilis I, Milkiewicz M, Boyd P, Goldstein J, Brown MD, Egginton S, Hansen FM, Hudlicka O, Haas TL. Differential involvement of MMP-2 and VEGF during muscle stretch- versus shear stress-induced angiogenesis. Am J Physiol Heart Circ Physiol 283: H1430-H1438, 2002.
46. Robbins JL, Jones WS, Duscha BD, Allen JD, Kraus WE, Regensteiner JG, Hiatt WR, Annex BH. Relationship between leg muscle capillary density and peak hyperemic blood flow with endurance capacity in peripheral artery disease. J Appl Physiol 111: 81-86, 2011.
47. Rullman E, Rundqvist H, Wagsater D, Fischer H, Eriksson P, Sundberg CJ, Jansson E, Gustafsson T. A single bout of exercise activates matrix metalloproteinase in human skeletal muscle. J Appl Physiol 102: 2346-2351, 2007.
48. Ryan NA, Zwetsloot KA, Westerkamp LM, Hickner RC, Pofahl WE, Gavin TP. Lower skeletal muscle capillarization and VEGF expression in aged vs. young men. J Appl Physiol 100: 178 -185, 2006.
49. Schlager O, Giurgea A, Schuhfried O, Seidinger D, Hammer A, Groger M, Fialka-Moser V, Gschwandtner M, Koppensteiner R, Steiner S. Exercise training increases endothelial progenitor cells and decreases asymmetric dimethylarginine in peripheral arterial disease: A randomized controlled trial. Atherosclerosis 217: 240-248, 2011.
50. Tsurumi Y, Murohara T, Krasinski K, Chen D, Witzenbichler B, Kearney M, Couffinhal T, Isner JM. Reciprocal relation between VEGF and NO in the regulation of endothelial integrity. Nat Med 3: 879-886, 1997.
51. Tuomisto TT, Rissanen TT, Vajanto I, Korkeela A, Rutanen J, Yla-Herttuala S. HIF-VEGF-VEGFR-2, TNF-alpha and IGF pathways are upregulated in critical human skeletal muscle ischemia as studied with DNA array. Atherosclerosis 174: 111-120, 2004.
52. Wagner PD. The critical role of VEGF in skeletal muscle angiogenesis and blood flow. Biochem Soc Trans 39: 1556-1559, 2011.
53. Waltenberger J, Mayr U, Pentz S, Hombach V. Functional upregulation of the vascular endothelial growth factor receptor KDR by hypoxia. Circulation 94: 1647-1654, 1996.
54. Williams JL, Cartland D, Hussain A, Egginton S. A differential role for nitric oxide in two forms of physiological angiogenesis in mouse. J Physiol 570: 445-454, 2006.
55. Williams JL, Weichert A, Zakrzewicz A, Da Silva-Azevedo L, Pries AR, Baum O, and Egginton S. Differential gene and protein expression in abluminal sprouting and intraluminal splitting forms of angiogenesis. Clin Sci (Lond) 110: 587-595, 2006.
56. Wood RE, Sanderson BE, Askew CD, Walker PJ, Green S, Stewart IB. Effect of training on the response of plasma vascular endothelial growth factor to exercise in patients with peripheral arterial disease. Clin Sci (Lond) 111: 401-409, 2006.