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Biomechanics of skeletal muscle capillaries: Hemodynamic resistance, endothelial distensibility, and pseudopod formation

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Abstract

The objective of this study was to investigate the structure of capillaries in rat skeletal muscle and their mechanical properties over a wide range of transmural pressures. Capillaries were fixed at controlled pressures and studied with intravital and electron microscopy. Capillary lumen dimensions depend on the local transmural pressure, with irregular and partially collapsed cross-sections at low transmural pressures and circular cross-sections at elevated pressures. The average circumferential wall stress is a nonlinear function of the circumferential stretch. Elevation of the transcapillary pressure serves to increase the endothelial surface area exposed to the lumen and to the basement membrane while the average endothelial thickness and cell volume decrease. The number of vesicles in the endothelium and their average size decrease with the stretching of the endothelial cell. The balance of membrane area measurements on the vesicles and on the cell surface show that the total membrane surface is conserved at all pressures, and the vesicles become unfolded during stretching of the endothelial cells. This suggests that the vesicle membrane serves as a reservoir for the increase of endothelial surface membrane area during capillary distension. Under normal or elevated capillary pressure, virtually no evidence for pseudopod formation by the endothelial cells was detected. If the capillary transmural pressure was reduced to zero in the presence of autologous plasma for periods of about 10 min, limited evidence for pseudopods in less than 10% of the capillary sections was seen. If the muscle capillaries were perfused with plasmalyte and fixed at low pressures, all capillaries exhibited pseudopod formation. Addition of plasma proteins prevented most pseudopod formations. Endothelial pseudopods are depleted of vesicles and form sheet-like projections. Once pseudopods are formed at low pressure, they cannot readily be unfolded by elevation of the capillary transmural pressure. Pseudopods appear to consist of a crosslinked actin matrix and may have a strong effect on the resistance to blood flow in capillaries. These results may be relevant with respect to capillary blood flow at low pressures.

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References

  1. Abbas, B., S. P. Hume, J. S. McCullough, D. J. Wilson, P. C. Stewart, and K. E. Carr. Early morphological changes in blood capillaries of mouse duodenal villi induced by X-irradiation.J. Submicrosc. Cyto. Pathol. 22:609–614, 1990.

    CAS  Google Scholar 

  2. Azuma, T., and S. Oka. Mechanical equilibrium of blood vessel walls.Am. J. Physiol. 221:1310–1318, 1971.

    PubMed  CAS  Google Scholar 

  3. Baez, S., H. Lamport, and A. Baez. Pressure effects in living microscopic vessels. In: Flow Properties of Blood, edited by A. L. Copley and G. Stainsby. London: Pergamon, 1960, pp. 122–136.

    Google Scholar 

  4. Bagge, U., B. Amundson, and C. Lauritzen. White blood cell deformability and plugging of skeletal muscle capillaries in hemorrhagic shock.Acta Physiol. Scand. 108:158–163, 1980.

    Article  Google Scholar 

  5. Baldwin, A. L., and A. W. Gore. Simultaneous measurement of capillary distensibility and hydraulic conductance.Microvasc. Res. 38:1–22, 1989.

    Article  PubMed  CAS  Google Scholar 

  6. Barroso-Aranda, J., G. W. Schmid-Schönbein, B. W. Zweifach, and R. L. Engler. Granulocytes and no-reflow phenomenon in irreversible hemorrhagic shock.Circ. Res. 63:437–447, 1988.

    PubMed  CAS  Google Scholar 

  7. Bundgaard, M., P. Hagman, and C. Crone. The three-dimensional organization of plasmalemmal vesicular profiles in the endothelium of rat heart capillaries.Microvasc. Res. 25:358–368, 1983.

    Article  PubMed  CAS  Google Scholar 

  8. Del Zoppo, G. J., G. W. Schmid-Schönbein, E. Mori, B. R. Copeland, and C.-M. Chang. Polymorphonuclear leukocytes occlude capillaries following middle cerebral artery occlusion and reperfusion.Stroke 22:1276–1283, 1991.

    PubMed  Google Scholar 

  9. Drenkhahn, D., and J. Wagner. Stress fibers in the splenic sinus endothelium in-situ: Molecular structure, relationship to the extracellular matrix, and contractility.J. Cell. Biol. 102:1738–1747, 1986.

    Article  Google Scholar 

  10. Ellis, C. G., O. Mathieu-Costell, R. F. Potter, I. C. Mac-Donald, and A. C. Groom. Effect of sacromere length on total capillary length in skeletal muscle: In-vivo evidence for longitudinal stretching of capillaries.Microvasc. Res. 40: 63–72, 1990.

    Article  PubMed  CAS  Google Scholar 

  11. Engler, R. L., G. W. Schmid-Schönbein, and R. S. Pavelec. Leukocyte capillary plugging in myocardial ischemia and reperfusion in the dog.Am. J. Pathol. 111:98–111, 1983.

    PubMed  CAS  Google Scholar 

  12. Frøkjær-Jensen, J. The plasmalemmal vesicular system in capillary endothelium. Conventional electron microscopic (EM) thin sections compared with the picture arising from ultrathin (≈140 Å) serial sectioning.Prog. Appl. Microcirc. 1:17–34, 1983.

    Google Scholar 

  13. Frøkjær-Jensen, J., and U. S. Ryan. Reorganization of the plasmalemmal vesicular system during shape changes of endothelial cells in culture.Int. J. Microcirc. Clin. Exp. 3: 362, 1984.

    Google Scholar 

  14. Gidlöf, A., D. H. Lewis, and F. Hammersen. The effect of prolonged total ischemia on the ultrastructure of human skeletal muscle capillaries: A morphometric analysis.Int. J. Microcirc. Clin. Exp. 7:67–86, 1987.

    Google Scholar 

  15. Gidlöf, A., D. H. Lewis, and F. Hammersen. Fine structure of the human skeletal muscle capillary: A morphometric analysis.Int. J. Microcirc. Clin. Exp. 7:43–66, 1987.

    Google Scholar 

  16. Hammersen, F., and E. Hammersen. The ultrastructure of endothelial gap-formation and leukocyte emigration.Prog. Appl. Microcirc. 12:1–34, 1987.

    Google Scholar 

  17. Hammersen, F., and E. Hammersen. The ultrastructure of microvascular endothelial cell reactions to various stimuli.Prog. Appl. Microcirc. 6:91–108, 1984.

    Google Scholar 

  18. Hochberger, A. I., and B. W. Zweifach. Analysis of critical closing pressure in the perfused rabbit ear.Am. J. Physiol. 214:962–968, 1968.

    PubMed  CAS  Google Scholar 

  19. Johansson, B. R. Quantitative ultrastructural morphometry of blood capillary endothelium in skeletal muscle.Microvasc. Res. 17:107–117, 118–130, 1979.

    Article  PubMed  CAS  Google Scholar 

  20. Komatsu, H., A. Koo, E. Chan, M. Inoue, N. Kaplowitz, and P. H. Guth. Hepatic microvascular ‘no reflow’ induced by ischemia-reperfusion in the rat: Role of superoxide free radicals.Gastroenterology 96:A266, 1989.

    Google Scholar 

  21. Korthius, R. J., and D. N. Granger. Ischemia-reperfusion injury: Role of oxygen radicals. In: Physiology of Oxygen Radicals, edited by A. E. Taylor, S. Matalon, and P. A. Ward. Bethesda: American Physiological Society, 1986, pp. 217–250.

    Google Scholar 

  22. Lee, J. The morphometry and mechanical properties of skeletal muscle capillaries. University of California, San Diego, La Jolla, California, Ph.D. Dissertation, 1990.

    Google Scholar 

  23. Lee, S. Y., and G. W. Schmid-Schönbein. Pulsatile pressure and flow in the skeletal muscle microcirculation.J. Biomech. Eng. 112:437–443, 1990.

    PubMed  CAS  Google Scholar 

  24. Lewis, D. H. Microcirculation and ischemia. In: Induced Skeletal Muscle Ischemia in Man, edited by D. H. Lewis. Basel: Karger, 1982, pp. 25–32.

    Google Scholar 

  25. Lübbers, D. W., G. Hauck, H. Weigelt, and K. Addicks. Contractile properties of frog capillaries tested by electrical stimulation.Bibl. Anat. 17:3–10, 1979.

    PubMed  Google Scholar 

  26. Majno, G. Ultrastructure of the vascular membrane. In: Handbook of Physiology, edited by Hamilton and Dow, Washington: American Physiological Society, 1965, pp. 2293–2375.

    Google Scholar 

  27. Mazzoni, M. C., P. Borgström, M. Intaglietta, and K. E. Arfors. Lumenal narrowing and endothelial cell swelling in skeletal muscle capillaries during hemorrhagic shock.Circ. Shock 29:27–39, 1989.

    PubMed  CAS  Google Scholar 

  28. Mazzoni, M. C., T. C. Skalak, and G. W. Schmid-Schönbein. The effect of skeletal muscle fiber deformation on lymphatic volume.Am. J. Physiol. 259:H1860-H1868, 1990.

    PubMed  CAS  Google Scholar 

  29. Milne, W. E. Numerical solution of differential equations. New York: Wiley, 1953, 371 pp.

    Google Scholar 

  30. Murphy, M., and P. C. Johnson. Possible contribution of basement membrane to the structural rigidity of capillaries.Microvasc. Res. 9:242–245, 1975.

    Article  PubMed  CAS  Google Scholar 

  31. Palade, G. E., and R. R. Bruns. Structural modulations of plasmalemmal vesicles.J. Cell Biol. 37:633–653, 1968.

    Article  PubMed  CAS  Google Scholar 

  32. Palade, G. E., M. Simionescu, and N. Simionescu. Structural aspects of the permeability of the microvascular endothelium.Acta Physiol. Scand. Suppl. 463:11–32, 1979.

    PubMed  CAS  Google Scholar 

  33. Philpott, D. E., I. A. Popova, K. Kato, J. Stevenson, J. Miquel, and W. Sapp. Morphological and biochemical examination of Cosmos 1887 rat heart tissue: Part I—Ultrastructure.FASEB J. 4:73–78, 1990.

    PubMed  CAS  Google Scholar 

  34. Ragan, D. M. S., E. E. Schmidt, I. C. MacDonald, and A. C. Groom. Spontaneous cyclic contractions of the capillary wall in-vivo, impeding red cell flow: A quantitative analysis.Microvasc. Res. 36:13–30, 1988.

    Article  PubMed  CAS  Google Scholar 

  35. Renkin, E. M. Capillary transport of macromolecules: Pores and other endothelial pathways.J. Appl. Physiol. 58: 315–325, 1985.

    PubMed  CAS  Google Scholar 

  36. Renkin, E. M., and F. E. Curry. Endothelial permeability: Pathways and modulations. In: Endothelium, edited by Fishman. New York Academy of Science Series, 1982, pp. 248–259.

    Google Scholar 

  37. Ryan, U. Macrophage like properties of endothelial cells.News Physiol. Sci. 3:93–96, 1988.

    Google Scholar 

  38. Sato, M., M. J. Levesque, and R. M. Nerem. Micropipette aspiration of cultured bovine aortic endothelial cells exposed to shear stress.Arteriosclerosis 7:276–286, 1987.

    PubMed  CAS  Google Scholar 

  39. Schmid-Schönbein, G. W. Rheology of leukocytes. In: Handbook of Bioengineering, edited by R. Skalak and S. Chien. New York: McGraw Hill, 1987, pp. 13.1–13.25.

    Google Scholar 

  40. Schmid-Schönbein, G. W., and H. Murakami. Blood flow in contracting arterioles.Int. J. Microcirc. Clin. Exp., 4: 311–328, 1985.

    PubMed  Google Scholar 

  41. Schmid-Schönbein, G. W., Y. Y. Shih, and S. Chien. Morphometry of human leukocytes.Blood 56:866–875, 1980.

    PubMed  Google Scholar 

  42. Schmid-Schönbein, G. W., and R. Skalak. Continuum mechanical model of leukocytes during protopod formation.J. Biomech. Eng. 106:10–18, 1984.

    Article  PubMed  Google Scholar 

  43. Schmid-Schönbein, G. W., R. Skalak, K.-L. P. Sung, and S. Chien. Human leukocytes in the active state. In: White Blood Cells, Morphology and Rheology as Related to Function, edited by U. Bagge G. V. R. Born, and P. Gaehtgens. The Hague: Martinus Nijhoff, 1982, pp. 21–31.

    Google Scholar 

  44. Shepro, D., and P. A. D'Amore. Physiology and biochemistry of the vascular well endothelium. In: Handbook of Physiology, edited by E. M. Renkin and C. C. Michel. Bethesda: American Physiological Society, Section 2, Volume IV, Microcirculation Part 1, 1984, pp. 103–164.

    Google Scholar 

  45. Simionescu, M., and N. Simionescu. Ultrastructure of the microvascular wall: Functional correlations. In: Handbook of Physiology, edited by E. M. Renkin and C. C. Michel. Bethesda, Maryland: American Physiological Society, Section 2, Volume IV, Microcirculation Part 1, 1984, pp. 41–101.

    Google Scholar 

  46. Skalak, T. C., and G. W. Schmid-Schönbein. Viscoelastic properties of microvessels in rate spinotrapezius muscle.J. Biomech. Eng. 108:193–199, 1986.

    PubMed  CAS  Google Scholar 

  47. Smaje, L. H., P. A. Fraser, and G. Clough. The distensibility of single capillaries and venules in the cat mesentery.Microvasc. Res. 20:358–370, 1980.

    Article  PubMed  CAS  Google Scholar 

  48. Sutton, D. W., and G. W. Schmid-Schönbein. Hemodynamics at low flow in the resting, vasodilated rat skeletal muscle.Am. J. Physiol. 257:H1419-H1427, 1989.

    PubMed  CAS  Google Scholar 

  49. Swayne, G. T. G., L. H. Smaje, and D. H. Bergel. Distensibility of single capillaries and venules in the rat and frog mesentery.Int. J. Microcirc. Clin. Exp. 8:25–42, 1989.

    PubMed  CAS  Google Scholar 

  50. Underwood, E. Quantitative Stereology. Reading, MA: Addison-Wesley, 1970, 274 pp.

    Google Scholar 

  51. Valerius, N. H., O. Stendahl, J. H. Hartwig, and T. P. Stossel. Distribution of actin/binding protein and myosin in polymorphonuclear leukocytes during locomotion and phagocytosis.Cell 24:195–202, 1981.

    Article  PubMed  CAS  Google Scholar 

  52. Wagner, R. C., and J. R. Casley-Smith. Endothelial vesicles.Microvasc. Res. 21:267–298, 1981.

    Article  PubMed  CAS  Google Scholar 

  53. Weigelt, H., and D. W. Lübbers. The fine adjustment of capillary blood flow through excitation of the capillary wall. In: Oxygen Transport to Tissue, edited by D. W. Lübbers, H. Acker, E. Leniger-Follert, and T. K. Goldstick. New York: Plenum Press, 1984, pp. 731–737.

    Google Scholar 

  54. Wolff, J. On the meaning of vesiculation in capillary endothelium.Angiologica 4:64–68, 1967.

    PubMed  CAS  Google Scholar 

  55. Zweifach, B. W. A micro-manipulative study of blood capillaries.Anat. Rec. 59:83–108, 1934.

    Article  Google Scholar 

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  1. Jye Lee

    Present address: Department of Medical Technology, Chang Gung Medical College, 33332 Kwei-San, Tao-Yuan, Taiwan, R.O.C.

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  1. Institute for Biomedical Engineering, University of California-San Diego, 92093-4012, La Jolla, CA, U.S.A.

    Jye Lee & Geert W. Schmid-Schönbein

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Lee, J., Schmid-Schönbein, G.W. Biomechanics of skeletal muscle capillaries: Hemodynamic resistance, endothelial distensibility, and pseudopod formation. Ann Biomed Eng 23, 226–246 (1995). https://doi.org/10.1007/BF02584425

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