Capillary growth, ultrastructure remodelling and exercise training in skeletal muscle of essential hypertensive patients

Acta Physiologica

Volumn 214, Issue 2, 2015, Pages 210-220

  Gliemann, L ^a   Buess, R ^b   Nyberg, M ^a   Hoppeler, H ^b   Odriozola, A ^b   Thaning, P ^c   Hellsten, Y ^a   Baum, O ^b   Mortensen, S P ^c,d  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF BERN   (Switzerland)

^c International Center for Research and Research Training in Endocrine Disruption of Male Reproduction and Child Health   (Denmark)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Capillaries; Cardiovascular disease; High blood pressure; Physical activity; Vascular remodelling

Indexed keywords

THROMBOSPONDIN 1; TISSUE INHIBITOR OF METALLOPROTEINASE 1; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR; VEGFA PROTEIN, HUMAN;

AEROBIC EXERCISE; ANGIOGENESIS; ARTICLE; BLOOD VESSEL PARAMETERS; CAPILLARY AREA; CAPILLARY BASEMENT MEMBRANE THICKNESS; CAPILLARY DENSITY; CAPILLARY GROWTH; CAPILLARY LUMEN AREA; CAPILLARY TO FIBER RATIO; CLINICAL ARTICLE; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; ESSENTIAL HYPERTENSION; EXERCISE; FEMALE; HUMAN; MICROVASCULATURE; MORPHOMETRICS; MUSCLE BIOPSY; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; SYSTOLIC BLOOD PRESSURE; TRANSMISSION ELECTRON MICROSCOPY; VASTUS LATERALIS MUSCLE; BLOOD PRESSURE; CAPILLARY; HYPERTENSION; METABOLISM; PHYSIOLOGY; ULTRASTRUCTURE;

BLOOD PRESSURE; CAPILLARIES; HUMANS; HYPERTENSION; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84929292477     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12501     Document Type: Article

References (52)

1. Altman, D.G. 1980. Statistics and ethics in medical research: III How large a sample? Br Med J 281, 1336-1338.
2. Andersen, P. & Henriksson, J. 1977. Capillary supply of the quadriceps femoris muscle of man: adaptive response to exercise. J Physiol 270, 677-690.
3. Baum, O., Djonov, V., Ganster, M., Widmer, M. & Baumgartner, I. 2005. Arteriolization of capillaries and FGF-2 upregulation in skeletal muscles of patients with chronic peripheral arterial disease. Microcirculation 12, 527-537.
4. Baum, O., Ganster, M., Baumgartner, I., Nieselt, K. & Djonov, V. 2007. Basement membrane remodeling in skeletal muscles of patients with limb ischemia involves regulation of matrix metalloproteinases and tissue inhibitor of matrix metalloproteinases. J Vasc Res 44, 202-213.
5. Baum, O., Vieregge, M., Koch, P., Gul, S., Hahn, S., Huber-Abel, F.A.M., Pries, A.R. & Hoppeler, H. 2013. Phenotype of capillaries in skeletal muscle of nNOS-knockout mice. Am J Physiol Regul Integr Comp Physiol 304, R1175-R1182.
6. Conway, J. 1984. Hemodynamic aspects of essential hypertension in humans. Physiol Rev 64, 617-660.
7. Cornelissen, V.A. & Fagard, R.H. 2005. Effects of endurance training on blood pressure, blood pressure-regulating mechanisms, and cardiovascular risk factors. Hypertension 46, 667-675.
8. Debbabi, H., Uzan, L., Mourad, J.J., Safar, M. & Levy, B.I. 2006. Increased skin capillary density in treated essential hypertensive patients. Am J Hypertens 19, 477-483.
9. Egginton, S. 2009. Invited review: activity-induced angiogenesis. Pflugers Arch 457, 963-977.
10. Fagard, R.H. & Cornelissen, V.A. 2007. Effect of exercise on blood pressure control in hypertensive patients. Eur J Cardiovasc Prev Rehabil 14, 12-17.
11. Ferrara, N. 2001. Role of vascular endothelial growth factor in regulation of physiological angiogenesis. Am J Physiol Cell Physiol 280, C1358-C1366.
12. Folkman, J. 1976. The vascularization of tumors. Sci Am 234, 58-73.
13. Gliemann, L., Olesen, J., Biensø, R.S., Schmidt, J., Akerstrom, T., Nyberg, M., Lindqvist, A., Bangsbo, J. & Hellsten, Y. 2014. Resveratrol modulates the angiogenic response to exercise training in skeletal muscle of aged men. Am J Physiol Heart Circ Physiol 307, H1111-H1119.
14. Greene, A.S. & Amaral, S.L. 2002. Microvascular angiogenesis and the renin-angiotensin system. Curr Hypertens Rep 4, 56-62.
15. Greene, A.S., Tonellato, P.J., Zhang, Z., Lombard, J.H. & Cowley, A.W. 1992. Effect of microvascular rarefaction on tissue oxygen delivery in hypertension. Am J Physiol 262, H1486-H1493.
16. Guilbert, J.J. 2003. The world health report 2002 - reducing risks, promoting healthy life. Educ Health (Abingdon) 16, 230.
17. Gustafsson, T., Puntschart, A., Kaijser, L., Jansson, E. & Sundberg, C.J. 1999. Exercise-induced expression of angiogenesis-related transcription and growth factors in human skeletal muscle. Am J Physiol 276, H679-H685.
18. Gustafsson, T., Knutsson, A., Puntschart, A., Kaijser, L., Nordqvist, A.S., Sundberg, C.J. & Jansson, E. 2002. Increased expression of vascular endothelial growth factor in human skeletal muscle in response to short-term one-legged exercise training. Pflugers Arch 444, 752-759.
19. Hansen, A.H., Nielsen, J.J., Saltin, B. & Hellsten, Y. 2010. Exercise training normalizes skeletal muscle vascular endothelial growth factor levels in patients with essential hypertension. J Hypertens 28, 1176-1185.
20. Hellsten, Y., Jensen, L., Thaning, P., Nyberg, M. & Mortensen, S. 2012b. Impaired formation of vasodilators in peripheral tissue in essential hypertension is normalized by exercise training: role of adenosine and prostacyclin. J Hypertens 30, 2007-2014.
21. Henrich, H.A., Romen, W., Heimgärtner, W., Hartung, E. & Bäumer, F. 1988. Capillary rarefaction characteristic of the skeletal muscle of hypertensive patients. Klin Wochenschr 66, 54-60.
22. Hernández, N., Torres, S.H., Finol, H.J. & Vera, O. 1999. Capillary changes in skeletal muscle of patients with essential hypertension. Anat Rec 256, 425-432.
23. Høier, B., Nordsborg, N., Andersen, S., Jensen, L., Nybo, L., Bangsbo, J. & Hellsten, Y. 2012. Pro- and anti-angiogenic factors in human skeletal muscle in response to acute exercise and training. J Physiol 590, 595-606.
24. Høier, B., Walker, M., Passos, M., Walker, P.J., Green, A., Bangsbo, J., Askew, C.D. & Hellsten, Y. 2013. Angiogenic response to passive movement and active exercise in individuals with peripheral arterial disease. J Appl Physiol 115, 1777-1787.
25. Hoppeler, H., Howald, H., Conley, K., Lindstedt, S.L., Claassen, H., Vock, P. & Weibel, E.R. 1985. Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol 59, 320-327.
26. Jones, W.S., Duscha, B.D., Robbins, J.L., Duggan, N.N., Regensteiner, J.G., Kraus, W.E., Hiatt, W.R., Dokun, A.O. & Annex, B.H. 2012. 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.
27. Malek, M.H. & Olfert, I.M. 2009. Global deletion of thrombospondin-1 increases cardiac and skeletal muscle capillarity and exercise capacity in mice. Exp Physiol 94, 749-760.
28. Melo, R.M., Martinho, E. & Michelini, L.C. 2003. Training-induced, pressure-lowering effect in SHR: wide effects on circulatory profile of exercised and nonexercised muscles. Hypertension 42, 851-857.
29. Milkiewicz, M., Hudlicka, O., Verhaeg, J., Egginton, S. & Brown, M.D. 2003. Differential expression of Flk-1 and Flt-1 in rat skeletal muscle in response to chronic ischaemia: favourable effect of muscle activity. Clin Sci (Lond) 105, 473-482.
30. Millauer, B., Wizigmann-Voos, S., Schnürch, H., Martinez, R., Møller, N.P., Risau, W. & Ullrich, A. 1993. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 72, 835-846.
31. Mortensen, S.P., Nyberg, M., Gliemann, L., Thaning, P., Saltin, B. & Hellsten, Y. 2014. Exercise training modulates functional sympatholysis and alpha-adrenergic vasoconstrictor responsiveness in hypertensive and normotensive individuals. J Physiol 592, 3063-3073. doi: 10.1113/jphysiol.2014.273722.
32. Nyberg, M., Gliemann, L., Thaning, P., Hellsten, Y. & Mortensen, S.P. 2012. Role of nitric oxide and prostanoids in the regulation of leg blood flow and blood pressure in humans with essential hypertension: effect of high-intensity aerobic training. J Physiol 590, 1481-1494.
33. Olfert, I.M. & Birot, O. 2011. Importance of anti-angiogenic factors in the regulation of skeletal muscle angiogenesis. Microcirculation 18, 316-330.
34. Olfert, I.M., Breen, E.C., Mathieu-Costello, O. & Wagner, P.D. 2001. Skeletal muscle capillarity and angiogenic mRNA levels after exercise training in normoxia and chronic hypoxia. J Appl Physiol 91, 1176-1184.
35. Olfert, I.M., Breen, E.C., Gavin, T.P. & Wagner, P.D. 2006. Temporal thrombospondin-1 mRNA response in skeletal muscle exposed to acute and chronic exercise. Growth Factors 24, 253-259.
36. Olfert, I.M., Howlett, R.A., Tang, K., Dalton, N.D., Gu, Y., Peterson, K.L., Wagner, P.D. & Breen, E.C. 2009. Muscle-specific VEGF deficiency greatly reduces exercise endurance in mice. J Physiol 587, 1755-1767.
37. Olfert, I.M., Howlett, R.A., Wagner, P.D. & Breen, E.C. 2010. Myocyte vascular endothelial growth factor is required for exercise-induced skeletal muscle angiogenesis. Am J Physiol Regul Integr Comp Physiol 299, R1059-R1067.
38. Perk, J., De Backer, G., Gohlke, H., Graham, I., Reiner, Z., Verschuren, M., Albus, C., Benlian, P., Boysen, G., Cifkova, R. et al. 2012. European Guidelines on cardiovascular disease prevention in clinical practice (version 2012). Eur Heart J 33, 1635-1701.
39. Peterson, C.M., Jones, R.L., Esterly, J.A., Wantz, G.E. & Jackson, R.L. 1980. Changes in basement membrane thickening and pulse volume concomitant with improved glucose control and exercise in patients with insulin-dependent diabetes mellitus. Diabetes Care 3, 586-589.
40. Plouët, J., Schilling, J. & Gospodarowicz, D. 1989. Isolation and characterization of a newly identified endothelial cell mitogen produced by AtT-20 cells. EMBO J 8, 3801-3806.
41. Prior, B.M., Yang, H.T. & Terjung, R.L. 2004. What makes vessels grow with exercise training? J Appl Physiol 97, 1119-1128.
42. Ridnour, L.A., Isenberg, J.S., Espey, M.G., Thomas, D.D., Roberts, D.D. & Wink, D.A. 2005. Nitric oxide regulates angiogenesis through a functional switch involving thrombospondin-1. Proc Natl Acad Sci USA 102, 13147-13152.
43. Rogers, M.W., Probst, M.M., Gruber, J.J., Berger, R. & Boone, J.B. 1996. Differential effects of exercise training intensity on blood pressure and cardiovascular responses to stress in borderline hypertensive humans. J Hypertens 14, 1369-1375.
44. Schiffrin, E.L. 2012. Vascular remodeling in hypertension: mechanisms and treatment. Hypertension 59, 367-374.
45. Shapiro, S.S. & Wilk, M.B. 1965. An analysis of variance test for normality (complete samples). Biometrika 52, 591-611.
46. Su, W., Gao, F., Lu, J., Wu, W., Zhou, G. & Lu, S. 2012. Levels of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 mRNAs in patients with primary hypertension or hypertension-induced atherosclerosis. J Int Med Res 40, 986-994.
47. Tan, E.C., Ter Laak, H.J., Hopman, M.T., van Goor, H. & Goris, R.J. 2012. Impaired oxygen utilization in skeletal muscle of CRPS I patients. J Surg Res 173, 145-152.
48. Tang, K., Breen, E.C., Gerber, H.-P., Ferrara, N.M.A. & Wagner, P.D. 2004. Capillary regression in vascular endothelial growth factor-deficient skeletal muscle. Physiol Genomics 18, 63-69.
49. Tayebjee, M.H., Nadar, S., Blann, A.D., Gareth Beevers, D., MacFadyen, R.J. & Lip, G.Y.H. 2004. Matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 in hypertension and their relationship to cardiovascular risk and treatment: a substudy of the Anglo-Scandinavian Cardiac Outcomes Trial (ASCOT). Am J Hypertens 17, 764-769.
50. Uitto, J., Perejda, A.J., Grant, G.A., Rowold, E.A., Kilo, C. & Williamson, J.R. 1982. Glycosylation of human glomerular basement membrane collagen: increased content of hexose in ketoamine linkage and unaltered hydroxylysine-O-glycosides in patients with diabetes. Connect Tissue Res 10, 287-296.
51. Weibel, E.R. 1979. Stereological Methods. Practical Methods for Biological Morphometry. Academic Press, London.
52. Williams, J.L., Weichert, A., Zakrzewicz, A., Da Silva-Azevedo, L., Pries, A.R., Baum, O. & Egginton, S. 2006. Differential gene and protein expression in abluminal sprouting and intraluminal splitting forms of angiogenesis. Clin Sci (Lond) 110, 587-595.