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The Blood Vasculature as an Adaptive System: Role of Mechanical Sensing

  • Timothy W. Secomb
  • Axel R. Pries

Abstract

The vascular system consists of an extensive network of conduits that carry blood to all parts of the body. The metabolic requirements of tissues, including oxygen demand, vary spatially and temporally. In order to meet these varying requirements, the vascular system must have the ability to adjust and control blood flow in space and time. Centrally driven neural and hormonal signals modulate flow at the whole-organ or regional level. Local modulation of blood flow is achieved by responses of individual microvessels to stimuli that they experience. The responses include acute changes of diameter achieved by alterations in the contractile state of smooth muscle in vessel walls (flow regulation), and long-term changes of vascular dimensions achieved by structural alterations in the vessel walls and by addition or loss of vascular segments (structural adaptation). Here, current understanding of these processes is reviewed, with emphasis on the role of vascular responses to mechanical stresses, i.e., wall shear stress resulting from blood flow and circumferential wall stress resulting from intravascular pressure, and the importance of these responses in flow regulation and structural adaptation. It is concluded that the blood vasculature is a sensitive adaptive system, in which mechanical sensing plays an important role in coordinating vascular responses.

Keywords

Wall Shear Stress Vessel Diameter Flow Resistance Vascular Response Fluid Shear Stress 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Bakker EN, Der Meulen ET, Spaan JA, VanBavel E (2000) Organoid culture of cannulated rat resistance arteries: effect of serum factors on vasoactivity and remodeling. Am J Physiol Heart Circ Physiol 278: H1233–H1240PubMedGoogle Scholar
  2. Bassingthwaighte JB, King RB, Roger SA (1989) Fractal nature of regional myocardial blood flow heterogeneity. Circ Res 65: 578–590PubMedCrossRefGoogle Scholar
  3. Bayliss WM (1902) On the local reactions of the arterial wall to changes of internal pressure. J Physiol (Lond) 28: 220–231Google Scholar
  4. Caro CG, Pedley TJ, Schroter RC, Seed WA (1978) The Mechanics of the Circulation. Oxford University Press, OxfordGoogle Scholar
  5. Cornelissen AJ, Dankelman J, VanBavel E, Stassen HG, Spaan JA (2000) Myogenic reactivity and resistance distribution in the coronary arterial tree: a model study. Am J Physiol Heart Circ Physiol 278: H1490–H1499PubMedGoogle Scholar
  6. Damiano ER (1998) The effect of the endothelial-cell glycocalyx on the motion of red blood cells through capillaries. Microvasc Res 55: 77–91PubMedCrossRefGoogle Scholar
  7. Davies PF (1995) Flow-mediated endothelial me-chanotransduction. Physiol Rev 75: 519–560PubMedGoogle Scholar
  8. Davis MJ, Hill MA (1999) Signaling mechanisms underlying the vascular myogenic response. Physiol Rev 79: 387–423PubMedGoogle Scholar
  9. Desjardins C, Duling BR (1990) Heparinase treatment suggests a role for the endothelial cell glycocalyx in regulation of capillary hematocrit. Am J Physiol 258: H647–H654PubMedGoogle Scholar
  10. Duling BR, Berne RM (1970) Propagated vasodilation in the microcirculation of the hamster cheek pouch. Circ Res 26: 163–170PubMedCrossRefGoogle Scholar
  11. Fann JI, Sokoloff MH, Sams GE, Yun KL, Kosek JC, Miller DC (1990) The reversibility of canine vein-graft arterialization. Circulation 82: IV9–18PubMedGoogle Scholar
  12. Folkow B (1949) Intravascular pressure as a factor regulating the tone of the small vessels. Acta Physiol Scand 17: 289–310PubMedCrossRefGoogle Scholar
  13. Folkow B (1987) Structure and function of the arteries in hypertension. Am Heart J 114: 938–948PubMedCrossRefGoogle Scholar
  14. Hacking WJG, VanBavel E, Spaan JAE (1996) Shear stress is not sufficient to control growth of vascular networks: a model study. Am J Physiol 270: H364–H375PubMedGoogle Scholar
  15. Haidekker MA, L’Heureux N, Frangos JA (2000) Fluid shear stress increases membrane fluidity in endothelial cells: a study with DCVJ fluorescence. Am J Physiol Heart Circ Physiol 278: H1401–H1406PubMedGoogle Scholar
  16. Jackson WF (1987) Arteriolar oxygen reactivity: where is the sensor? Am J Physiol 253: H1120–H1126PubMedGoogle Scholar
  17. Jackson WF (2000) Hypoxia does not activate ATP-sensitive K + channels in arteriolar muscle cells. Microcirculation 7: 137–145PubMedGoogle Scholar
  18. Johnson PC (1980) The myogenic response. In: Bohr DF, Somlyo AP, Sparks HV, Jr.: Handbook of Physiology, Section 2, The Cardiovascular System, Vol. II: Vascular Smooth Muscle. American Physiological Society, Bethesda, MD, 409–442Google Scholar
  19. Kamiya A, Bukhari R, Togawa T (1984) Adaptive regulation of wall shear stress optimizing vascular tree function. Bull Math Biol 46: 127–137PubMedGoogle Scholar
  20. Koller A, Kaley G (1990) Endothelium regulates skeletal muscle microcirculation by a blood flow velocity sensing mechanism. Am J Physiol 258: H916–H920PubMedGoogle Scholar
  21. Kuo L, Davis MJ, Chilian WM (1990) Endothelium-dependent, flow-induced dilation of isolated coronary arterioles. Am J Physiol 259: H1063–H1070PubMedGoogle Scholar
  22. Kuo L, Hein TW (2002) Mechanism of shear-stress induced coronary microvascular dilation. In: Barth FG, Humphrey JAC, Secomb TW (eds) Sensors and Sensing in Biology and Engineering. Springer, Wien New YorkGoogle Scholar
  23. LaBarbera M (1990) Principles of design of fluid transport systems in zoology. Science 249: 992–1000PubMedCrossRefGoogle Scholar
  24. Langille BL, O’Donnell F (1986) Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science 231: 405–407PubMedCrossRefGoogle Scholar
  25. Mayrovitz HN, Roy J (1983) Microvascular blood flow: evidence indicating a cubic dependence on arteriolar diameter. Am J Physiol 245: H1031–H1038PubMedGoogle Scholar
  26. Murray CD (1926) The physiological principle of minimum work. I. The vascular system and the cost of blood volume. Proc Natl Acad Sci USA 12: 207–214PubMedCrossRefGoogle Scholar
  27. Pries AR, Reglin B, Secomb TW (2001) Structural adaptation of microvascular networks: functional roles of adaptive responses. Am J Physiol Heart Circ Physiol 281: H1015–H1025PubMedGoogle Scholar
  28. Pries AR, Secomb TW, Gaehtgens P (1995a) Design principles of vascular beds. Circ Res 77: 1017–1023PubMedCrossRefGoogle Scholar
  29. Pries AR, Secomb TW, Gaehtgens P (1995b) Structure and hemodynamics of microvascular networks: heterogeneity and correlations. Am J Physiol 269: H1713–H1722PubMedGoogle Scholar
  30. Pries AR, Secomb TW, Gaehtgens P (1998) Structural adaptation and stability of microvascular networks: theory and simulations. Am J Physiol 275: H349–H360PubMedGoogle Scholar
  31. Pries AR, Secomb TW, Gaehtgens P (1999) Structural autoregulation of terminal vascular beds: vascular adaptation and development of hypertension. Hypertension 33: 153–161PubMedCrossRefGoogle Scholar
  32. Pries AR, Secomb TW, Gaehtgens P (2000) The endothelial surface layer. Pflügers Arch 440: 653–666PubMedCrossRefGoogle Scholar
  33. Pries AR, Secomb TW, Gaehtgens P, Gross JF (1990) Blood flow in microvascular networks. Experiments and simulation. Circ Res 67: 826–834PubMedCrossRefGoogle Scholar
  34. Pries AR, Secomb TW, Gessner T, Sperandio MB, Gross JF, Gaehtgens P (1994) Resistance to blood flow in microvessels in vivo. Circ Res 75: 904–915PubMedCrossRefGoogle Scholar
  35. Rodbard S (1975) Vascular caliber. Cardiology 60: 4–49PubMedCrossRefGoogle Scholar
  36. Schretzenmayr A (1933) Über kreislaufregulatorische Vorgänge an den grossen Arterien bei der Muskelarbeit. Pflügers Arch Ges Physiol 232: 743–748CrossRefGoogle Scholar
  37. Secomb TW, Hsu R, Pries AR (2001) Effect of the endothelial surface layer on transmission of fluid shear stress to endothelial cells. Biorheology 38: 143–150PubMedGoogle Scholar
  38. Secomb TW, Pries AR (2002) Information transfer in microvascular networks. Microcirculation (in press) Segal SS, Jacobs TL (2001) Role of endothelial cell conduction in ascending vasodilation and exercise hyperemia in hamster skeletal muscle. J Physiol 536: 937–946Google Scholar
  39. Skalak TC, Price RJ (1996) The role of mechanical stresses in microvascular remodeling. Microcirculation 3: 143–165PubMedCrossRefGoogle Scholar
  40. Tulis DA, Unthank JL, Prewitt RL (1998) Flow-induced arterial remodeling in rat mesenteric vasculature. Am J Physiol 274: H874–H882Google Scholar
  41. Vink H, Duling BR (1996) Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ Res 79: 581–589PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2003

Authors and Affiliations

  • Timothy W. Secomb
  • Axel R. Pries

There are no affiliations available

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