Skip to main content
SpringerLink
Log in

Angiogenesis in Skeletal Muscle

  • Chapter
Book cover Molecular, Cellular, and Clinical Aspects of Angiogenesis

Part of the book series: NATO ASI Series ((NSSA,volume 285))

  • 65 Accesses

Abstract

Growth of vessels in normal adult skeletal muscles occurs during development, cold exposure, increased activity, administration of certain hormones, and increased physical activity (such as endurance exercise or chronic electrical stimulation). It always starts as growth of capillaries, with growth of larger vessels following later, or sometimes not at all: in endurance training growth of capillaries is not accompanied by growth of larger vessels, while a long-term increase in activity due to electrical stimulation leads to growth of the whole vascular bed (demonstrated by increased capillarization, corrosion casts, number of arterioles and maximal conductance measurements. One factor involved in capillary growth in stimulated muscles is the greater shear stress accompanying an increased velocity of flow, as similar growth was found in animals where long-term increase in blood flow was induced by the alpha1 blocker prazosin. Increased shear stress damaged the luminal glycocalyx and also caused a release of prostaglandins. These appear to mediate capillary growth as simultaneous administration of indomethacin decreased incorporation of bromodeoxyuridine into capillary-linked nuclei and attenuated capillary growth. In addition, distortion of the capillary basement membrane by increased capillary wall tension, and by continuous stretching and relaxation of surrounding muscle fibres,may also involved. Long-term muscle stretch due to extirpation of agonists induced capillary growth, but without an increase in blood flow. Disturbance of the basement membrane may lead to release of growth factors. While the evidence for the involvement of bFGF was negative, a low molecular weight angiogenic factor (ESAF) was demonstrated in both stimulated and stretched muscles. Capillary growth in stimulated muscles may also be enhanced by pericyte withdrawal as there was significantly less of capillary perimeter covered by pericytes in muscles with demonstrated capillary growth. Thus mechanical factors acting both from luminal and abluminal side can initiate capillary growth in skeletal muscle by activating either prostaglandins, ESAF or possibly other growth factors, but not bFGF.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Adair TH, Gay WJ, Montani J-P. Growth regulation of the vascular system; evidence for a metabolic hypothesis. Am.J. Physiol. 259, R393–404, 1990.

    PubMed  CAS  Google Scholar 

  • Andersen P, Henriksson J. Capillary supply of the quadriceps femoris muscle of man: adaptive response to exercise. J. Physiol, Lond. 270: 677–690, 1977.

    PubMed  CAS  Google Scholar 

  • Ando J, Nomura H, Kamiya A. The effect of fluid shear stress on the migration and proliferation of cultured endothelial cells. Microvasc. Res. 33: 62–70, 1987.

    Article  PubMed  CAS  Google Scholar 

  • Atherton GW, Cabric M, James NT. Stereological analyses of capillaries in muscles of dystrophic mice. Virchows Arch. A Pathol. Anat. 397: 347–382, 1982.

    Article  CAS  Google Scholar 

  • Bischoff J. Approaches to studying the adhesion molecules in angiogenesis. Trends in Cell. Biol. 5: 69–74, 1995.

    Article  CAS  Google Scholar 

  • Brodai P, Ingjer F, Hermansen L. Capillary supply of skeletal muscles fibres in untrained and endurance-trained men. Am. J. Physiol. 232 (Heart Circ. Physiol. 1): H705-H712, 1977.

    Google Scholar 

  • Brown LC, Messick FC, Kok MP, Hamilton IG, Girard PR. Fluid flow stimulates metalloproteinase production and deposition into extracellular matrix of endothelial cells. FASEB J. 9: A617, 1995.

    Google Scholar 

  • Brown MD, Cotter MA, Hudlicka O, Vrbova G. The effects of different patterns of muscle activity on capillary density, mechanical properties and structure of slow and fast rabbit muscles. Pfluegers Arch. 361: 241–250, 1976.

    Article  CAS  Google Scholar 

  • Brown MD, Egginton S, Hudlicka O. Changes in capillary endothelial cell glycocalyx in rat skeletal muscles during chronic electrical stimulation. Int. J. Microcirc: Clin. Exper. 11:447, 1992a.

    Google Scholar 

  • Brown MD, Egginton S, Walter HJ, Hudlicka O. Increased capillary supply and localization of basic fibroblast growth factor in rat fast skeletal muscle after stretch-induced overload. Int. J. Microcirc: Clin. Exper. 11: S181, 1992b.

    Google Scholar 

  • Brown MD, Walter HJ, Weiss JB, Hudlicka O. Growth factors in angiogenesis in skeletal muscle and heart. FASEB J. 7: A884,1993.

    Google Scholar 

  • Burch TG, Prewitt RL, Law PK. In vivo morphometric analysis of muscle microcirculation in dystrophic mice. Muscle & Nerve, 4: 420–424, 1981.

    Article  CAS  Google Scholar 

  • Capo LA, Sillau AH. The effect of hyperthyroidism on capillarity and oxygen capacity in rat soleus and gastrocnemius muscles. J. Physiol. Lond., 342: 1–14, 1983.

    PubMed  CAS  Google Scholar 

  • Clark ER, Clark EL. Microscopic observations on the extra endothelial cells of living mammalian blood vessels. Am. J. Anat. 66: 1–49, 1940.

    Article  Google Scholar 

  • Clausen JP, Trap-Jensen J. Effects of training on the distribution of cardiac output in patients with coronary artery disease. Circulation. 42: 611–624, 1970.

    PubMed  CAS  Google Scholar 

  • D’Amore P, Orlidge A. Growth factors and pericytes in microangiography. Diabete Metab. 14: 495–504, 1988.

    Google Scholar 

  • Davel LE, Miguez MM, De Lustig ES. Evidence that indomethacin inhibits lymphocyte-induced angiogenesis. Transplantation Baltimore. 39: 564–565 1985.

    CAS  Google Scholar 

  • Dawson JM, Tyler KR, Hudlicka O. A comparison of the microcirculation in rat fast glycolytic and slow oxidative muscles at rest and during contractions. Microvasc. Res. 33: 167–182, 1987.

    Article  PubMed  CAS  Google Scholar 

  • Dawson JM, Hudlicka O. Inhibition of capillary growth in skeletal muscle with GPA 1734. Int. J. Microcirc: Clin. Exper. 9: 134, 1990.

    Google Scholar 

  • Dawson JM, Hudlicka O. Can changes in microcirculation explain capillary growth in skeletal muscle? Int. J. Exp. Path. 74: 65–71, 1993.

    CAS  Google Scholar 

  • Egginton S. Effect of an anabolic hormone on striated muscle growth and performance. Pflugers Arch. 410: 349–355, 1987a.

    Article  PubMed  CAS  Google Scholar 

  • Egginton S. Effect of anabolic hormone on anaerobic capacity of rat striated muscle. Pflugers Arch. 410: 356–361, 1987b.

    Article  PubMed  CAS  Google Scholar 

  • Egginton S, Hudlicka O. The effect of long-term activation of glycolytic fibres in rat skeletal muscle on capillary supply and enzyme activities. J. Physiol. 409: 71P, 1989.

    Google Scholar 

  • Egginton S, Hudlicka O. Effect of long-term muscle overload on capillary supply, blood flow and performance in rat fast muscle. J. Physiol. 452: 9P, 1992.

    Google Scholar 

  • Egginton S, Hudlicka O, Brown MD. The possible role in angiogenesis of pericytes from chronically stimulated rat skeletal muscles. J. Physiol. 467: 43P, 1993.

    Google Scholar 

  • Fairney J, Egginton S. The effect of cold acclimation on muscle capillary supply in the Syrian hamster (Mesocricetus auratus). J. Physiol. 475: 61–62P, 1994.

    Google Scholar 

  • Form DH, Auerbach R. PGE2 and angiogenesis. Proc. Soc. Exp. Biol. Med. 172: 214–218, 1983.

    PubMed  CAS  Google Scholar 

  • Folkman J, Cotran R. Relation of vascular proliferation to tumor growth. Int. Rev. Exp. Pathol. 16: 207–248, 1976.

    PubMed  CAS  Google Scholar 

  • Fulgenzi G, Hudlicka O. The effect of alpha1 blocker prazosin on capillarization, blood flow and performance in ischaemic skeletal muscles. Int. J. Microcirc: Clin. Exper. 14: (S1), 229, 1994.

    Google Scholar 

  • Hansen-Smith FM, Carlson BM, Irwin KL. Revascularization of the freely grafted extensor digitorum longus muscle in the rat. Am. J. Anat. 158: 65–82, 1980.

    Article  PubMed  CAS  Google Scholar 

  • Hansen-Smith FM, Hudlicka O. Ultrastructure of capillaries during angiogenesis in electrically stimulated rat extensor digitorum longs (EDL) muscle. FESAB J. 7: 1993.

    Google Scholar 

  • Hermansen L, Wachtlova M. Capillary density of skeletal muscle in well-trained and untrained men. J. Appl. Physiol. 30: 860–863, 1971.

    PubMed  CAS  Google Scholar 

  • Hoppeler H, Desplanches D. Muscle structural modifications in hypoxia. Int. J. Sports Med. 13:Suppl 1,S166–168,1992.

    Article  PubMed  Google Scholar 

  • Hoppeler H, Kleinert E, Schlegel C, Claassen H, Howald H, Kayar SR, Ceretelli P. Morphological adaptations of human skeletal muscle to chronic hypoxia. Int. J. Sports Med. 11:Suppl 1,53–59, 1990.

    Article  Google Scholar 

  • Hudlicka O. Uptake of substrates in slow and fast muscles in situ. Microvasc. Res. 10: 17–28, 1975.

    Article  PubMed  CAS  Google Scholar 

  • Hudlicka O. Review lecture: What makes blood vessels grow? J. Physiol. Lond. 444: 1–24, 1991.

    PubMed  CAS  Google Scholar 

  • Hudlicka O. Physiological mechanisms of angiogenesis. In Functionality of the endothelium in health and diseased states: A comprehensive review. Ed. G. Pastelin, R. Rubio, G. Ceballos & J. Suarez, Sociedad Mexicana de Cardiologia. Gobierno del Estado de Veracruz, p252–262, 1994.

    Google Scholar 

  • Hudlicka O, Brown MD. Physical Forces and Angiogenesis. In Mechanoreception by the Vascular Wall. Ed. G.M. Rubanyi, Futura Publishing Co Inc, Mount Kisco, NY, 1993.

    Google Scholar 

  • Hudlicka O, Brown M, Egginton S. Angiogenesis in skeletal and cardiac muscle. Physiol. Rev. 72: 369–669, 1992.

    PubMed  CAS  Google Scholar 

  • Hudlicka O, Dodd C, Renkin EM, Gray SD. Early changes in fiber profiles and capillary density in long-term stimulated muscles. Am. J. Physiol. 243 (Heart Circ. Physiol. 12): H528-H535, 1982.

    PubMed  CAS  Google Scholar 

  • Hudlicka O, Tyler KR, Wright AJA, Ziada AMAR. Growth of capillaries in skeletal muscles. Prog. Appl. Microcirc. 5: 44–61, 1984.

    Google Scholar 

  • Hudlicka O, Egginton S, Brown MD. Capillary diffusion distances — their importance for cardiac and skeletal muscle performance. News in Physiological Sciences, 3: 134–137, 1988.

    Google Scholar 

  • Ingber DE, Folkman J. How does extracellular matrix control capillary morphogenesis? Cell. 58: 803–305, 1989.

    Article  PubMed  CAS  Google Scholar 

  • Ingjer F. Effects of endurance training on muscle fibre ATP-ase activity, capillary supply and mitochondria in man. J. Physiol. Lond. 294: 419–432, 1979.

    PubMed  CAS  Google Scholar 

  • Knighton DR, Silver IA, Hunt TK. Regulation of wound-healing angiogenesis — effect of oxygen gradients and inspired oxygen concentration. Surgery St Louis, 90: 1981.

    Google Scholar 

  • Koller A, Kaley G. Prostaglandins mediate arteriolar dilatation to increased blood flow velocity in skeletal muscle microcirculation. Circ. Res. 67: 529–534, 1990.

    PubMed  CAS  Google Scholar 

  • Kuwabara T, Cogan, DG. Retinal vascular patterns. VI. Mural cells of the retinal capillaries. Arch. Ophthalmol. 69: 492–502, 1963.

    CAS  Google Scholar 

  • Laughlin MH, Armstrong RB. Muscular blood flow distribution patterns as a function of running speed in rats. Am. J. Physiol. 243 (Heart Circ. Physiol. 12): H296-H306, 1982

    PubMed  CAS  Google Scholar 

  • Maragoudakis ME, Sarmonika M, Panousta-Copoulu M. Inhibition of basement membrane biosynthesis prevents angiogenesis. J. Pharmacol. Exper. Therap. 244: 729–733, 1988.

    CAS  Google Scholar 

  • Mellander S, Bjomberg J. Regulation of vascular smooth muscle tone and capillary pressure. NIPS 7: 113–119, 1992.

    Google Scholar 

  • Myrhage R, Hudlicka O. Capillary growth in chronically stimulated adult skeletal muscle as studied by intravital microscopy and histological methods in rabbits and rats. Microvasc. Res. 16: 73–90, 1978.

    Article  PubMed  CAS  Google Scholar 

  • Orlidge A, D’Amore PA. Inhibition of capillary endothelial cell growth by pericytes and smooth muscle cells. J. Cell Biol. 105:1455–1462, 1987.

    Article  PubMed  CAS  Google Scholar 

  • Pearce SC, Hudlicka O. Are prostaglandins involved in capillary growth in chronically stimulated skeletal muscles? Int. J. Microcirc. 14: 243, 1994.

    Google Scholar 

  • Pearce S, Hudlicka O, Egginton S. Early in activity-induced angiogenesis in rat skeletal muscles: incorporation of bromodeoxyuridine into cells of the interstitium. J. Physiol. 483P, 1995.

    Google Scholar 

  • Saltin B, Kiens B, Savard G, Pedersen PK. Role of hemoglobin and capillarization for oxygen delivery and extraction in muscle exercise. Acta Physiol. Scand. 128 Suppl 556: 21–32, 1986.

    Google Scholar 

  • Smith P. Effect of hypoxia upon the growth and sprouting activity of cultured aorti endothelium from the rat. J. Cell Sci. 92: 505–512, 1989.

    PubMed  Google Scholar 

  • Stingl J, Rhodin JAG. Early postnatal growth of skeletal muscle blood vessels of the rat. Cell & Tiss. Res. 275: 419–434, 1994.

    Article  CAS  Google Scholar 

  • Valdivia E. Total capillary bed in striated muscles of guinea pigs native to the Peruvian mountains. Am. J. Physiol. 194: 585–589, 1958.

    PubMed  CAS  Google Scholar 

  • Vanotti A, Magiday M. Untersuchungen zum Studium des TrainiertScin. V. Uber die Capillarisierung der trainierten Muskulatur. Arbeitsphysiologie 7: 615–622, 1934.

    Google Scholar 

  • Walter H, Hudlicka O. Expression of basic fibroblast growth factor (bFGF) in chronically stimulated skeletal muscles. Int. J. Microcirc: Clin. Exper. 11: 447, 1992.

    Google Scholar 

  • Wolff JR, Goerz CH, Bar TH, Gueldner FH. Common morphogenetic aspects of various organotypic microvascular patterns. Microvasc. Res. 10: 373–395, 1975.

    Article  PubMed  CAS  Google Scholar 

  • Ziada AMAR, Hudlicka O, Tyler KR, Wright AJA. The effect of long-term vasodilatation on capillary growth and performance in rabbit heart and skeletal muscle. Cardiovasc. Res. 18: 724–732, 1984.

    Article  PubMed  CAS  Google Scholar 

  • Ziche M, Jones J, Gullino PM. Role of prostaglandin E1 and copper in angiogenesis. J. Natl. Cancer Inst. 69: 475–482, 1982.

    PubMed  CAS  Google Scholar 

  • Zumstein A, Mathieu O, Howald H, Hoppeler H. Morphometric analysis of the capillary supply in skeletal muscles of trained and untrained subjects — its limitations in muscle biopsies. Pfluegers Arch. 397: 277–283, 1983.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology, University of Birmingham, Birmingham, B15 2TT, UK

    O. Hudlicka & S. Egginton

  2. Department of Sport and Exercise Sciences, University of Birmingham, Birmingham, B15 2TT, UK

    M. D. Brown

Authors
  1. O. Hudlicka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. D. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Egginton
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. University of Patras Medical School, Patras, Greece

    Michael E. Maragoudakis

Rights and permissions

Reprints and permissions

Copyright information

© 1996 Plenum Press, New York

About this chapter

Cite this chapter

Hudlicka, O., Brown, M.D., Egginton, S. (1996). Angiogenesis in Skeletal Muscle. In: Maragoudakis, M.E. (eds) Molecular, Cellular, and Clinical Aspects of Angiogenesis. NATO ASI Series, vol 285. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-0389-3_13

Download citation

  • DOI: https://doi.org/10.1007/978-1-4613-0389-3_13

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-8030-6

  • Online ISBN: 978-1-4613-0389-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation