Skip to main content

Hemodynamic Forces, Exercise, and Angiogenesis

  • Conference paper
Therapeutic Angiogenesis

Part of the book series: Ernst Schering Research Foundation Workshop 28 ((SCHERING FOUND,volume 28))

Abstract

It is generally acknowledged that training results in capillary growth in skeletal muscle, with the extent of growth varying according to length and type of training. There is also growth of arterioles and expansion of the whole vascular bed, as indicated by increased maximal conductance. Surprisingly, in the heart, training results in capillary growth almost predominantly in young animals, while growth of arterioles and enlargement of large vessels occurs in adults, even when not accompanied by capillary growth (see Hudlická et al. 1992). There is no doubt that the changes in capillary supply are due at least in part to growth of endothelial cells, which was demonstrated by [3H]thymidine incorporation in capillary nuclei in the hearts of animals trained by swimming (Man-dache et al. 1973). Although there is no parallel evidence in skeletal muscles, increased capillarization demonstrated either by histochemical techniques which depict specifically capillary endothelium, or by electron microscopy, thus revealing all anatomically present vessels, are the result of growth of new vessels.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
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, Hang J, Wells ML, McGee FD, Montani JP (1995) Long-term electrical stimulation of rabbit skeletal muscle increases growth of paired arteries and veins. Am J Physiol 38:H717–724

    Google Scholar 

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

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Annex BH, Torgan CE, Lin P, Taylor DA, Thompson MA, Peters KG, Kraus WE (1998) Induction and maintenance of increased VEGF protein by chronic motor nerve Stimulation in skeletal muscle. Am J Physiol 274:H860–867

    PubMed  CAS  Google Scholar 

  • Anversa P, Beghi PC, Levicky V, McDonald SL, Kikkawa Y (1982) Morphometry of right ventricular hypertrophy induced by strenuous exercise in rat. Am J Physiol 243:H850–861

    Google Scholar 

  • Anversa P, Levicky V, Beghi C, McDonald SL, Kikkawa Y (1983) Morphometry of exercise-induced right ventricular hypertrophy in the rat. Circ Res 52:57–64

    Article  PubMed  CAS  Google Scholar 

  • Anversa P, Beghi C, Kikkawa Y, O1ivetti G (1986) Myocardial infarction in rats. Infarct size, myocyte hypertrophy and capillary growth. Circ Res 58:26–37

    Article  PubMed  CAS  Google Scholar 

  • Armstrong RB, Laughlin MH (1983) Blood flows within and among rat muscles as a function of time during high speed treadmill exercise. J Physiol (Lond) 344:189–208

    CAS  Google Scholar 

  • Bell RD, Rasmussen RL (1974) Exercise and the myocardial capillary-fiber ratio during growth. Growth 38:237–244

    PubMed  CAS  Google Scholar 

  • Ben Ezra D (1978) Neovasculogenic ability of prostaglandins,growth factors and synthetic chemoattractants. Am J Ophthalmol 86:455–461

    Google Scholar 

  • Bloor CM, White FC, Sanders TM (1984) Effects of exercise on collateral development in myocardial ischemia in pigs. J Appl Physiol 56:656–665

    Article  PubMed  CAS  Google Scholar 

  • Breen EC, Johnson EC, Wagner H, Tseng HM, Sung LA, Wagner PD (1996) Angiogenic growth factor mRNA responses in muscle to a single bout of exercise. J Appl Physiol 81:355–361

    PubMed  CAS  Google Scholar 

  • Breisch EA, White FC, Nimmo LE, McKirnan MD, Bloor CM (1986) Exercise-induced cardiac hypertrophy, a correlation of blood flow and microvas-culature. J Appl Physiol 60:1259–1267

    PubMed  CAS  Google Scholar 

  • Brown MD, Hudlická O (1991) Capillary supply and cardiac performance in the rabbit after chronic dobutamine treatment. Cardiovasc Res 25:909–915

    Article  PubMed  CAS  Google Scholar 

  • Brown MD, Hudlická O (1995) Vascular conductance and capillary supply in heart and skeletal muscle in response to altered activity. Microcirculation 2:98

    Google Scholar 

  • Brown MD, Cotter M, Hudlická O, Vrbova G (1976) The effect of different patterns of muscle activity on capillary density, mechanical properties and structure of slow and fast rabbit muscles. Pflugers Arch 361:241–250

    Article  PubMed  CAS  Google Scholar 

  • Brown MD, Cleasby MJ, Hudlická O (1990) Capillary supply of hypertro-phied rat hearts after chronic treatment with the bradycardic agent alinidine. J Physiol (Lond) 427:40P

    Google Scholar 

  • Brown MD, Davies MK, Hudlická O, Townsend P (1994) Long-term bradycardia by electrical pacing: a new method for studying heart rate reduction. Cardiovasc Res 28:1774–1779

    Article  PubMed  CAS  Google Scholar 

  • Brown MD, Hudlická O, Makki RF, Weiss JB (1995a) Low-molecular-mass endothelial cell-stimulating angiogenic factor in relation to capillary growth induced in rat skeletal muscle by low-frequency electrical stimulation. Int J Microcirc 15:111–116

    Article  CAS  Google Scholar 

  • Brown MD, Davies M, Hudlická O, Townsend P (1995b) Capillary density and performance in bradycardially paced infarcted pig hearts. J Mol Cell Cardiol 27:A91

    Google Scholar 

  • Brown MD, Walter HJ, Hansen-Smith FM, Hudlická O, Egginton S (1998) Lack of involvement of basic fibroblast growth factor (FGF-2) in capillary growth in skeletal muscles exposed to long-term contractile activity. Angio-genesis 2:81–21

    CAS  Google Scholar 

  • Buttrick PM, Malhotra A, Factor S, Greenen D, Scheuer J (1988) Effect of chronic dobutamine administration on hearts of normal and hypertensive rats. Circ Res 63:173–181

    Article  PubMed  CAS  Google Scholar 

  • Chandrasherkhar Y, Anand IS (1991) Exercise as a coronary protective factor. Am Heart J 122:1723–1739

    Article  Google Scholar 

  • Clyne CAC, Mears H, Weiler RO, O’Donnell TF (1985) Calf muscle adaptation to peripheral vascular disease. Cardiovasc Res 19:507–512

    Article  PubMed  CAS  Google Scholar 

  • Daemmgen JW, Gross GJ (1985) AQ-AH 208, a new bradycardic agent, increases coronary collateral blood flow to ischemic myocardium. J Cardiovasc Pharmacol 7:1048–1054

    Article  PubMed  CAS  Google Scholar 

  • Dawson JM (1987) Responses of the microcirculation in metabolically different skeletal muscles to increased and reduced blood flow. PhD thesis, University of Birmingham

    Google Scholar 

  • Dawson JM, Hudlická O (1989) The effect of long-term activity on the mi-crovasculature of rat glycolytic skeletal muscle. Int J Microcirc 8:53–59

    CAS  Google Scholar 

  • Dawson JM, Hudlická O (1990) Changes in the microcirculation in slow and fast skeletal muscles with long-term limitation of blood supply. Cardiovasc Res 24:390–395

    Article  PubMed  CAS  Google Scholar 

  • Dawson JM, Hudlická O (1993) Can changes in microcirculation explain capillary growth in skeletal muscle? Int J Exp Pathol 74:65–71

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dawson JM, Okyayuz-Baklouti I, Hudlická O (1990) Skeletal muscle microcirculation: the effects of limited blood supply and treatment with torbafylline. Int J Microcirc 9:385–400

    CAS  Google Scholar 

  • Delp MM, Laughlin MH (1997) Time course of enhanced endothelium-mediated dilation in the aorta of trained rats. Med Sci Sports Exerc 29:1454–1461

    Article  PubMed  CAS  Google Scholar 

  • Duling BR, Dejardins C (1987) Capillary hematocrit — what does it mean? NIPS 2:66–69

    Google Scholar 

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

    Google Scholar 

  • Egginton S, Hudlická O (1999) Early changes in performance, blood flow and capillary fine structure in rat fast muscles induced by electrical stimulation. J Physiol (Lond) 515:265–275

    Article  CAS  Google Scholar 

  • Egginton S, Hudlická O, Brown MD, Graciotti L, Granata AL (1996) In vivo pericyte-endothelial cell interaction during angiogenesis in adult cardiac and skeletal muscle. Microvasc Res 51:213–228

    Article  PubMed  CAS  Google Scholar 

  • Esbjornsson M, Jansson E, Sundberg CJ, Sylven C, Eiken O, Nygren A, Kai-jser L (1993) Muscle fiber types and enzyme activities after training with local leg ischaemia in man. Acta Physiol Scand 148:233–241

    Article  PubMed  CAS  Google Scholar 

  • Firoozan S, Forfar JC (1996) Exercise training and the coronary collateral circulation: is its value underestimated in man? Eur Heart J 17:1791–1795

    Article  PubMed  CAS  Google Scholar 

  • Froelicher VF (1972) Animal studies of effect of chronic exercise on the heart and atherosclerosis. Am Heart J 84:496–506

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Fulgenzi G, Graciotti L, Collis MG, Hudlická O (1998) The effect of alpha-1 adrenoceptor antagonist prazosin on capillary supply, blood flow and performance in a rat model of chronic muscle ischaemia. Eur J Vasc Endovasc Surg 16:71–77

    Article  PubMed  CAS  Google Scholar 

  • Glaser SP (1997) Effects of zatebradine (ULFS 49CL), a sinus node inhibi-tor,on heart rate and exercise duration in chronic stable angina pectoris. Am J Cardiol 79:1401–1404

    Article  Google Scholar 

  • Gray SD, Renkin EM (1978) Microvascular supply in relation to fiber metabolic type in mixed skeletal muscle of rabbits. Microvasc Res 16:406–425

    Article  PubMed  CAS  Google Scholar 

  • Gross GJ, Daemmgen JW (1987) Effect of the new specific bradycardial agent AQ-A39 (Falipamil) on coronary collateral blood flow in dogs. J Cardiovasc Pharmacol 10:123–127

    Article  PubMed  CAS  Google Scholar 

  • Gute D, Laughlin MH, Amann JF (1994) Regional changes in capillary supply in skeletal muscle of interval-sprint and low-intensity, endurance-trained rats. Microcirculation 1:183–193

    Article  PubMed  CAS  Google Scholar 

  • Gute D, Fraga C, Laughlin MH, Amann JF (1996) Regional changes in capillary supply in skeletal muscle of high-intensity endurance-trained rats. J Appl Physiol 81:619–616

    PubMed  CAS  Google Scholar 

  • Hammarsten J, Bylund-Fellenius NC, Holm J, Schersten T, Krotkiewski M (1980) Capillary supply and muscle fiber types in patients with intermittent claudication: relationship between morphology and metabolism. Eur J Clin Invest 10:301–305

    Article  PubMed  CAS  Google Scholar 

  • Hang J, Kong L, Gu J-W, Adair TH (1995) VEGF gene expression is upregu-lated in electrically stimulated rat skeletal muscle. Am J Physiol 269:H1827-H1831

    PubMed  CAS  Google Scholar 

  • Hansen-Smith FM, Hudlická O, Egginton S (1996) In vivo angiogenesis in adult rat skeletal muscle: early changes in capillary network architecture and ultrastructure. Cell Tissue Res 286:123–136

    Article  PubMed  CAS  Google Scholar 

  • Hansen-Smith FM, Egginton S, Hudlická O (1998) Growth of arterioles in chronically stimulated adult skeletal muscle. Microcirculation 5:49–59

    PubMed  CAS  Google Scholar 

  • Heaton WH, Marr KC, Capurro NL, Goldstein RE, Epstein SE (1978) Beneficial effect of physical training on blood flow to myocardium perfused by chronic collaterals in the exercising dog. Circulation 57:575–581

    Article  PubMed  CAS  Google Scholar 

  • Henriksson J, Nygaard E, Andersson J, Eklöf B (1980) Enzyme activities, fiber types and capillarization in calf muscles of patients with intermittent claudication. Scand J Clin Lab Invest 40:361–369

    Article  PubMed  CAS  Google Scholar 

  • Hester RL, Duling B (1988) Red cell velocity during functional hyperemia: implications for rheology and oxygen transport. Am J Physiol 255:H236–244

    PubMed  CAS  Google Scholar 

  • Ho KW, Roy RR, Taylor JF, Heusner WW, Van Huss WD (1983) Differential effects of running and weight-lifting on the rat coronary arterial tree. Med Sci Sports Exerc 15:472–477

    PubMed  CAS  Google Scholar 

  • Hogan RD, Hirschmann L (1984) Arteriolar proliferation in the rat cremaster muscle as a long-term autoregulatory response to reduced perfusion. Mi-crovasc Res 27:290–296

    Article  CAS  Google Scholar 

  • Hoppeler H, Desplanches D (1992) Muscle structural modifications in hypoxia. Int J Sports Med 143 [Suppl 1]:S166–168

    Article  Google Scholar 

  • Hudlická O (1975) Uptake of substrates in slow and fast muscles in situ. Mi-crovasc Res 10:17–28

    Article  Google Scholar 

  • Hudlická O (1991) What makes blood vessels grow? J Physiol (Lond) 444:1–24

    Google Scholar 

  • Hudlická O (1994) Mechanical factors involved in the growth of the heart and its blood vessels. Cell Mol Biol Res 40:143–152

    PubMed  Google Scholar 

  • Hudlická O (1998) Is physiological angiogenesis in skeletal muscle regulated by changes in microcirculation? Microcirculation 5:7–23

    PubMed  Google Scholar 

  • Hudlická O, Brown MD (1993) Physical forces in angiogenesis. In: Rubanyi G (ed) Mechanoreception by the vascular wall. Futura, Mount Kisco, p197–241

    Google Scholar 

  • Hudlická O, Brown MD (1996) Postnatal growth of the heart and its blood vessels. J Vasc Res 33:266–287

    Article  PubMed  Google Scholar 

  • Hudlická O, Egginton S (1994) Early changes in muscle blood flow and performance induced by chronic electrical stimulation of rat fast muscles. J Physiol (Lond) 477:37P

    Google Scholar 

  • Hudlická O, Tyler KR (1984) The effect of long-term high frequency stimulation on capillary density and fiber types in rabbit fast muscles. J Physiol (Lond) 353:435–445

    Google Scholar 

  • Hudlická O, Dodd L, Renkin EM, Gray SD (1982) Early changes in fiber profile and capillary density in long-term stimulated muscles. Am J Physiol 243:H528–535

    PubMed  Google Scholar 

  • Hudlická O, Tyler KR, Wright AJA, Ziada AMAR (1984) Growth of capillaries in skeletal muscles. Prog Appl Microcirc 5:44–64

    Google Scholar 

  • Hudlická O, West D, Kumar S, El Khelly F, Wright AJA (1989) Can growth of capillaries in the heart and skeletal muscle be explained by the presence of an angiogenic factor? Br J Exp Pathol 70:237–246

    PubMed  Google Scholar 

  • Hudlická O, Brown MD, Egginton S (1992) Angiogenesis in skeletal and cardiac muscle. Physiol Rev 72:369–417

    PubMed  Google Scholar 

  • Hudlická O, Brown MD, Egginton S, Dawson JM (1994) Effect of long-term electrical stimulation on vascular supply and fatigue in chronically ischemic muscles. J Appl Physiol 77:1317–1324

    PubMed  Google Scholar 

  • Hudlická O, Brown MD, Walter H, Weiss JB, Bate A (1995) Factors involved in capillary growth in the heart. Mol Cell Biochem 147:57–68

    Article  PubMed  Google Scholar 

  • Hudlická O, Brown MD, Silgram H (1996) Role of nitric oxide in capillary proliferation in chronically stimulated rat skeletal muscle. Int J Microcirc 16(S1):P92

    Google Scholar 

  • Hudlická O, Brown MD, Egginton S (1998a) Angiogenesis: basic concepts and methodology. In: Halliday A, Hunt BJ, Poston L, Schachter M (eds) An introduction to vascular biology. Cambridge University Press, Cambridge, p3–19

    Google Scholar 

  • Hudlická O, Brown MD, Dawson JM (1998b) Growth and regression of capillaries in rabbit and rat skeletal muscles. J Physiol (Lond) 511P:158P

    Google Scholar 

  • Hughes RA, Hudlická O (1992) Changes in capillary ultrastructure, blood flow and muscle performance during development of collateral circulation in rat fast muscles. J Physiol (Lond) 452:115P

    Google Scholar 

  • Indolfi C, Goth B.D, Miyazaki S, Miura T, Schulz R, Ross J Jr (1991) Heart rate reduction improves myocardial ischemia in swine — role of interventricular blood flow redistribution. Am J Physiol 261:H910–917

    PubMed  CAS  Google Scholar 

  • Ingjer F (1979) Effects of endurance training on muscle fiber ATPase activity, capillary supply and mitochondrial content in man. J Physiol (Lond) 294:419–432

    CAS  Google Scholar 

  • Ito WD, Arras M, Scholz D, Winkler B, Htun P, Schaper W (1997) Angiogenesis but not collateral growth is associated with ischemia of the femoral artery occlusion. Am J Physiol 273:H1255–1265

    PubMed  CAS  Google Scholar 

  • Jacobs TB, Bell RD, McClements JD (1984) Exercise, age and the development of the myocardial vasculature. Growth 48:148–157

    PubMed  CAS  Google Scholar 

  • Jansson E, Johansson J, Sylven C, Kaijser L (1988) Calf muscle adaptation in intermittent claudication. Clin Physiol 8:17–29

    Article  PubMed  CAS  Google Scholar 

  • Jeal S, Brown MD, Hudlická O, Egginton S (1997) Involvement of vascular endothelial growth factor in capillary growth as a result of chronic electrical stimulation of skeletal muscle in conscious rats. J Physiol (Lond) 499:39P

    Google Scholar 

  • John HT, Warren R (1961) The stimulus to collateral circulation. Surgery 49:14–25

    PubMed  CAS  Google Scholar 

  • Kern MJ, Donohue TJ, Bach RG, Aguirre FV, Caracciolo EA, Ofili EO (1993) Quantitating coronary collateral flow velocity in patients during coronary angioplasty using a Doppler guide wire. Am J Cardiol 71:34D-40D

    Article  PubMed  CAS  Google Scholar 

  • Koller A, Kaley G (1996) Shear stress dependent regulation of vascular resistance in health and disease: role of endothelium. Endothelium 4:247–272

    Article  CAS  Google Scholar 

  • Lash JM (1994) Contribution of arterial feed vessels to skeletal muscle functional hyperemia. J Appl Physiol 76:1512–1519

    PubMed  CAS  Google Scholar 

  • Lash JM, Bohlen HG (1992) Functional adaptations of rat skeletal muscle arterioles to aerobic exercise training. J Appl Physiol 72:2052–2062

    PubMed  CAS  Google Scholar 

  • Laughlin MH, McAllister RM (1992) Exercise training-induced coronary vascular adaptation. J Appl Physiol 73:2209–2225

    PubMed  CAS  Google Scholar 

  • Laughlin MH, Armstrong RB (1982) Muscle blood flow distribution patterns as a function of running speed in rats. Am J Physiol 243:H296–306

    PubMed  CAS  Google Scholar 

  • Laughlin MH, Tomanek RJ (1987) Myocardial capillarity and maximal capillary diffusion capacity in exercise-trained dogs. J Appl Physiol 63:1481–1486

    PubMed  CAS  Google Scholar 

  • Laughlin MH, Korthuis RJ, Sexton WL, Armstrong RB (1988) Regional blood flow capacity and exercise hyperemia in high intensity trained rats. J Appl Physiol 64:2420–2427

    PubMed  CAS  Google Scholar 

  • Leon AS, Bloor CM (1968) Effects of exercise and its cessation on the heart and its blood supply. J Appl Physiol 24:485–490

    PubMed  CAS  Google Scholar 

  • Liang CS, Turtle RR, Hood WB Jr, Gavras H (1979) Conditioning effects of chronic infusion of dobutamine. Comparison with exercise training. J Clin Invest 64:613–619

    Article  PubMed  CAS  Google Scholar 

  • Libonati JR, Gaughan JP, Hefner CA, Gow A, Paolone AM, Houser SR (1997) Reduced ischemic and reperfusion injury following exercise training. Med Sci Sports Exerc 29:809–816

    Google Scholar 

  • Mai JV, Edgerton VR, Barnard RJ (1970). Capillarity of red,white and intermediate muscle fibers in trained and untrained guinea pigs. Experientia 26:1222–1223

    Article  PubMed  CAS  Google Scholar 

  • Mall G, Mattfeldt T, Rieger P, Volk B, Frolov VA (1982) Morphometric analysis of the rabbit myocardium after chronic ethanol feeding — early capillary changes. Basic Res Cardiol 77:57–67

    Article  PubMed  CAS  Google Scholar 

  • Mandache E, Unge G, Appelgren LE, Ljungqvist A (1973) The proliferation activity of the heart tissues in various forms of experimental cardiac hyper-trophy studied by electron microscope autoradiography. Virchows Arch Cell Pathol 12:112–122

    CAS  Google Scholar 

  • Mattfeldt T, Mall G (1987) Growth of capillaries and myocardial cells in the normal rat heart. J Mol Cell Cardiol 19:1237–1246

    Article  PubMed  CAS  Google Scholar 

  • Mattfeldt T, Krämer KL, Zeitz R, Mall G (1986) Stereology of myocardial hypertrophy induced by physical exercise. Virchows Arch Pathol Anat His-topathol 409:473–484

    Article  CAS  Google Scholar 

  • Mathien GM, Terjung RL (1986) Influence of training following bilateral stenosis of the femoral artery in rats. Am J Physiol 250:H1050–1059

    PubMed  CAS  Google Scholar 

  • Mathien GM, Terjung RL (1990) Muscle blood flow in trained rats with peripheral arterial insufficiency. Am J Physiol 258:H759–765

    PubMed  CAS  Google Scholar 

  • McKirnan MD, Bloor CM (1994) Clinical significance of coronary vascular adaptations to exercise training. Med Sci Sports Exerc 26:1262–1268

    PubMed  CAS  Google Scholar 

  • Mellander S, Bjornberg G (1992) Regulation of vascular smooth muscle tone and capillary pressure. NIPS 7:113–119

    Google Scholar 

  • Michel G, Buchwald H, Schoenherr H (1972) Quantitative studies on the formation of cardiac muscle fibers and capillaries in various types of domestic and wild poultry. Anat Anz 132:382–388

    PubMed  CAS  Google Scholar 

  • Morris JN (1994) Exercise in the prevention of coronary heart disease: today’s best buy in public health. Med Sci Sports Exerc 26:807–814

    PubMed  CAS  Google Scholar 

  • Müller JM, Myers PR, Laughlin MH (1994) Vasodilator responses of coronary resistance arteries of exercise-trained pigs.Circulation 89:2308–2314

    Article  PubMed  Google Scholar 

  • Muronara T, Asahara T, Silver M, Bauters C, Masuda H, Kalka C, Kerney M, Chen D, Symes JF, Fishman MC, Huang PL, Isner JM (1998) Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 101:2567–2578

    Article  Google Scholar 

  • Myrhage R, Hudlická O (1978) 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

    Article  PubMed  CAS  Google Scholar 

  • Nellis SH, Liedtke AL (1982) Pressure dimensions in the terminal vascular bed of the myocardium determined by a new free motion technique. In: Till-manns H, Kubier W, Zebe H (eds) Microcirculation of the heart.Springer, Berlin Heidelberg New York, p 61–74

    Google Scholar 

  • Odedra R, Weiss JB (1991) Low molecular weight angiogenesis factor. Pharmacol Ther 49:111–124

    Article  PubMed  CAS  Google Scholar 

  • Oltman CL, Parker JL, Laughlin MH (1995) Endothelium dependent vasodilation of proximal coronary arteries from exercise-trained pigs. J Appl Physiol 79:33–40

    PubMed  CAS  Google Scholar 

  • Pearce SC, Hudlická O (1995) Possible involvement of prostaglandins in capillary growth in chronically stimulated skeletal muscles. Microcirculation 2:98

    Google Scholar 

  • Pipili-Synetos E, Papageorgiou A, Sakkoula E, Sotiropoulou G, Fotsis T, Karakiulakis G, Maragoudakis ME (1995) Inhibition of angiogenesis, tumor-growth and metastasis by the NO-releasing vasodilators, isosorbide mononitrate and dinitrate. Br J Pharmacol 116:1829–1834

    Article  PubMed  CAS  Google Scholar 

  • Poupa O, Rakusan K, Ostadal B (1970) The effect of physical activity upon the heart of the vertebrates. Med Sport 4:202–235

    Google Scholar 

  • Price RJ, Owens GK, Skalak TC (1994) Immunohistochemical identification of arteriolar development using markers of smooth muscle differentiation -evidence that capillary arterialization proceeds from terminal arterioles. Circ Res 75:520–527

    Article  PubMed  CAS  Google Scholar 

  • Przyklenk K, Groom AC (1984) Can exercise promote neovascularisation in the transition zone of infarcted rat hearts? Can J Physiol Pharmacol 62:630–644

    Article  PubMed  CAS  Google Scholar 

  • Przyklenk K, Groom AC (1985) Effect of exercise frequency, intensity and duration on neovascularization in the transition zone of infarcted rat hearts. Can J Physiol Pharmacol 63:273–278

    Article  PubMed  CAS  Google Scholar 

  • Rakusan K, Wicker P (1990) Morphometry of the small arteries and arterioles in the rat heart: effects of chronic hypertension and exercise. Cardiovasc Res 24:278–284

    Article  PubMed  CAS  Google Scholar 

  • Rakusan K, Ostadal B, Wachtlová M (1971) The influence of muscular work on the capillary density in the heart and skeletal muscle of pigeon (Columbia livia dom). Can J Physiol Pharmacol 49:167–170

    Article  PubMed  CAS  Google Scholar 

  • Regensteiner JG (1997) Exercise in the treatment of claudication: assessment and treatment of functional impairment. Vasc Med 2:238–242

    PubMed  CAS  Google Scholar 

  • Richardson RS, Mudaliar SRD, Mathieu-Costello O, Wagner PD (1998) VEGF mRNA response to acute exercise following chronic training. Med Sci Sports Exerc 30:S50

    Google Scholar 

  • Roberts KC, Nixon C, Unthank JL, Lash JM (1997) Femoral artery ligation stimulates capillary growth and limits training-induced increases in oxidative capacity in rats. Microcirculation 4:253–260

    Article  PubMed  CAS  Google Scholar 

  • Saltin B, Gollnick PD (1983) Skeletal muscle adaptability: significance for metabolism and performance. In: Handbook of physiology, section 10: skeletal muscle. American Physiological Society, Bethesda, p 555–631

    Google Scholar 

  • Sanne H, Sivertsson R (1968) The effect of exercise on the development of collateral circulation after experimental occlusion of femoral artery in the cat. Acta Physiol Scand 73:257–263

    Article  PubMed  CAS  Google Scholar 

  • Sasayama S, Fujita M (1992) Recent insights into coronary collateral circulation. Circulation 85:1197–1204

    Article  PubMed  CAS  Google Scholar 

  • Schamhardt HC, Verdouw PD, Saxena PR (1981) Improvement of perfusion and function of ischemic porcine myocardium after reduction of heart rate by alinidine. J Cardiovasc Pharmacol 3:728–738

    Article  PubMed  CAS  Google Scholar 

  • Schantz P, Henriksson J, Jansson E (1983) Adaptation of human skeletal muscle to endurance training of long duration. Clin Physiol 3:141–151

    Article  PubMed  CAS  Google Scholar 

  • Schaper W (1971) The collateral circulation of the heart. North-Holland, Amsterdam

    Google Scholar 

  • Schaper W, Nienaber C, Gottwick M (1981) The importance of collateral circulation for myocardial survival. Acta Med Scand [Suppl] 657:29–34

    Google Scholar 

  • Sewell WH, Roth DR (1958) Basic observations on ability of newly formed capillaries to develop into collateral arteries. Surg Forum 9:227–229

    Google Scholar 

  • Sexton WL, Laughlin MH (1994) Influence of endurance exercise training on distribution of vascular adaptations in rat skeletal muscle. Am J Physiol 266:H483–490

    PubMed  CAS  Google Scholar 

  • Sexton WL, Korthuis RJ, Laughlin MH (1988) High intensity exercise training increases vascular transport capacity of rat hindquarters. Am J Physiol 254:H274–278

    PubMed  CAS  Google Scholar 

  • Shammas NW, Moss AJ, Sullebarger JT, Gutierrez OH, Rocco TA (1993) Acquired coronary angiogenesis after myocardial infarction. Cardiology 83:212–216

    Article  PubMed  CAS  Google Scholar 

  • Sinoway LI, Shenberger J, Wilson J, McLaughlin D, Musch T, Zelis R (1987) A 30-day forearm work protocol increases maximal forearm blood flow. J Appl Physiol 62:1063–1067

    PubMed  CAS  Google Scholar 

  • Skalak TC, Price RJ (1996) Mechanical stresses in microvascular remodelling. Microcirculation 3:143–165

    Article  PubMed  CAS  Google Scholar 

  • Skorjanc D, Jaschinski FJ, Heine G, Perte D (1998) Sequential increases in capillarization and mitochondrial enzymes in low-frequency stimulated rabbit muscles. Am J Physiol 274:C810–818

    PubMed  CAS  Google Scholar 

  • Snell PG, Martin WH, Buckley JC, Blomqvist CG (1987) Maximal vascular leg conductance in trained and untrained men. J Appl Physiol 62:606–610

    PubMed  CAS  Google Scholar 

  • Spinale FG, Grine RC, Tempel GE, Crawford FA, Zile MR (1992) Alterations in the myocardial capillary vasculature accompany tachycardia induced cardiomyopathy. Basic Res Cardiol 87:65–79

    Article  PubMed  CAS  Google Scholar 

  • Sun D, Huang A, Koller A, Kaley G (1994) Short term daily exercise activity enhances endothelial NO synthesis in skeletal muscle arterioles of rats. J Appl Physiol 76:2241–2247

    PubMed  CAS  Google Scholar 

  • Tepperman J, Pearlman D (1961) Effects of exercise and anaemia on coronary arteries of small animals as revealed by the corrosion-cast technique. Circ Res 9:576–584

    Article  PubMed  CAS  Google Scholar 

  • Tharp GD, Wagner CT (1982) Chronic exercise and cardiac vascularization. Eur J Appl Physiol 48:97–104

    Article  CAS  Google Scholar 

  • Thomas DP (1985) Effects of acute and chronic exercise on myocardial ultrastructure. Med Sci Sports Exerc 17:546–553

    PubMed  CAS  Google Scholar 

  • Tillmanns H, Ikeda S, Hansen H, Sarma JS, Fauvel JH, Bing RJ (1974) Microcirculation in the ventricle of the dog and turtle. Circ Res 34:561–569

    Article  PubMed  CAS  Google Scholar 

  • Tillmanns H, Steinhausen M, Leinberger H, Thederan H, Kubier W (1981) Pressure measurement in the terminal vascular bed of the epimyocardium of rats and cats. Circ Res 49:1201–1211

    Article  Google Scholar 

  • Tillmanns H, Steinhausen M, Leinberger H, Thederan H, Kubier W (1982) The effect of coronary vasodilators on the microcirculation of the ventricular myocardium. In: Tillmanns H, Kubier W, Zebe H (eds) Microcirculation of the heart. Springer, Berlin Heidelberg New York, p 305–312

    Chapter  Google Scholar 

  • Tomanek RJ (1970) Effect of age and exercise on the extent of the myocardial capillary bed. Anat Rec 167:55–62

    Article  PubMed  CAS  Google Scholar 

  • Tomanek RJ (1994) Exercise induced coronary angiogenesis. Med Sci Sports Exerc 26:1245–1251

    PubMed  CAS  Google Scholar 

  • Tomoike H (1993) Functional aspects of collateral development in animal models. In: Schaper W, Schaper J (eds) Collateral circulation. Kluwer Academic, Boston, p 149–172

    Google Scholar 

  • Tornling G, Unge G, Skoog L, Ljungqvist A, Carlsson S, Adolfsson J (1978) Proliferative activity of myocardial capillary wall cells in dipyridamole treated rats. Cardiovasc Res 12:692–695

    Article  PubMed  CAS  Google Scholar 

  • Tsang GMK, Green MA, Crow A, Smith FCT, Beck S, Hudlicka O, Shearman CP (1994) Chronic muscle stimulation improves ischemic muscle performance in patients with peripheral vascular disease. Eur J Vasc Surg 8:419–422

    Article  PubMed  CAS  Google Scholar 

  • Unge G, Carlsson S, Ljungqvist A, Tornling G, Adolfsson J (1979) The proliferative activity of myocardial capillary wall cells in variously aged swimming-exercised rats. Acta Pathol Microbiol Scand [A] Pathol 87:15–17

    CAS  Google Scholar 

  • Valdivia E, Watson M (1960).Histologic alterations in muscles of guinea pigs during chronic hypoxia. Arch Pathol 69:199–208

    PubMed  CAS  Google Scholar 

  • Wachtlová M, Rakusan K, Poupa O (1965) The coronary terminal vascular bed in the heart of the hare (Lepus Europaeus) and the rabbit (Oryctolagus Do-mesticus). Physiol Bohemoslov 14:328–331

    PubMed  Google Scholar 

  • Wachtlová M, Rakusan K, Roth Z, Poupa O (1967) The terminal vascular bed of the myocardium in the wild rat (Rattus Norvegicus) and the laboratory rat (Rattus Norvegicus lab). Physiol Bohemoslov 16:548–554

    PubMed  Google Scholar 

  • Ware JA, Simons M (1997) Angiogenesis in ischemic heart disease. Nature Med 3:158–164

    Article  PubMed  CAS  Google Scholar 

  • White FC, Bloor CM (1995) Coronary growth, not angiogenesis, is the dominant response increasing coronary vascular bed cross-sectional area induced by exercise training. FASEB J 9:A909

    Google Scholar 

  • White FC, McKirnan M, Breisch EA, Guth BD, Liu Y-M, Bloor CM (1987) Adaptation of the left ventricle to exercise induced hypertrophy. J Appl Physiol 62:1097–1110

    Article  PubMed  CAS  Google Scholar 

  • White FC, Roth DM, Bloor CM (1990) Coronary vascular remodelling during chronic ischemia. Circulation 82 [Suppl IV]:378

    Google Scholar 

  • White FC, Bloor CM, McKirnan MD, Caroll SM (1998) Exercise training in swine promotes growth of arteriolar bed and capillary angiogenesis in heart. J Appl Physiol 85:1160–1168

    PubMed  CAS  Google Scholar 

  • Woodman CR, Muller JM, Laughlin MH, Price EM (1997) Induction of nitric oxide synthase mRNA in coronary resistance arteries isolated from exercise trained rats. Am J Physiol 273:H2575–2579

    PubMed  CAS  Google Scholar 

  • Wright AJA, Hudlická O (1981) Capillary growth and changes in heart performance induced by chronic bradycardial pacing in the rabbit. Circ Res 49:469–478

    Article  PubMed  CAS  Google Scholar 

  • Wyatt HL, Mitchell J (1978) Influence of physical conditioning and decondi-tioning on coronary vasculature of dogs. J Appl Physiol 215:619–625

    Google Scholar 

  • Xie Z, Gao M, Batra S, Koyama T (1997) The capillarity of left ventricular tissue of rats subjected to coronary artery occlusion. Cardiovasc Res 33:671–676

    Article  PubMed  CAS  Google Scholar 

  • Yang HT, Ogilvie RW, Terjung RL (1991) Low intensity training produces muscle adaptation in rats with femoral artery stenosis. J Appl Physiol 71:1822–1829

    PubMed  CAS  Google Scholar 

  • Zetterquist S (1970) Effect of active training on the nutritive blood flow in exercising ischemic legs. Scand J Clin Lab Invest 25:101–111

    Article  PubMed  CAS  Google Scholar 

  • Zheng W, Tomanek RJ (1998) VEGF is upregulated in bradycardia-induced coronary angiogenesis in rat. FASEB J 12:A71

    Google Scholar 

  • Zhou A-L, Egginton S (1998) Immunogold labelling of proliferating cells during skeletal muscle angiogenesis. J Vasc Res 35:386

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ziada AMAR, Hudlická O, Tyler KR (1989) The effect of long-term administration of a 1-blocker prazosin on capillary density in cardiac and skeletal muscle. Pflugers Arch 415:355–360

    Article  PubMed  CAS  Google Scholar 

  • Ziche M, Morbidelli L, Masini E, Amerini S, Granger HJ, Maggi CA, Geppetti P, Ledda F (1994) Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J Clin Invest 94:2036–2044

    Article  PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

J. A. Dormandy W. P. Dole G. M. Rubanyi

Rights and permissions

Reprints and permissions

Copyright information

© 1999 Springer-Verlag Berlin Heidelberg

About this paper

Cite this paper

Hudlická, O., Brown, M.D. (1999). Hemodynamic Forces, Exercise, and Angiogenesis. In: Dormandy, J.A., Dole, W.P., Rubanyi, G.M. (eds) Therapeutic Angiogenesis. Ernst Schering Research Foundation Workshop 28, vol 28. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-03776-8_6

Download citation

  • DOI: https://doi.org/10.1007/978-3-662-03776-8_6

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-662-03778-2

  • Online ISBN: 978-3-662-03776-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics