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Changes in the Organization of the Smooth Muscle Cells in Rat Vein Grafts

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Abstract

Mechanical tensile stress in vein grafts increases suddenly under the influence of arterial blood pressure. In this study, we examined the influence of increased tensile stress on the organization of the smooth muscle cells (SMCs) in the neointima and media of the rat vein grafts. An autogenous jugular vein was grafted into the abdominal aorta of the rat, and changes in the organization of the vein graft SMCs were studied by observing the distribution of SMC actin filaments and nuclei at 3 min and 1, 5, 10, and 30 days after surgery. In a normal jugular vein, the average wall circumferential tensile stress was ~ 3 kPa at an internal pressure of 3 mm Hg. The SMCs, that contained long, slender actin filamentous bundles, were oriented mainly in the circumferential direction of the vessel, and constituted a 2- to 3-cell-thick medial layer underneath the endothelium. In a vein graft, the wall circumferential tensile stress suddenly increased by ~ 140 times compared with the control level. In response to this suddenly increased stress, the SMC layer was stretched into a structure with scattered pores and disrupted SMC actin filamentous bundles within 3 min. This initial change was followed by a rapid reduction in the density of the SMC nuclei and actin filaments within 1 day and progressive SMC proliferation, that was associated with medial thickening and a change in the SMC orientation from 5 to 30 days. Further studies showed that a local inflation of normal jugular veins to 120 mm Hg for 3 min induced a similar change as found in the vein grafts, whereas the organization of the SMCs was not significantly changed in vein-vein grafts, that did not experience a change in tensile stress. These results suggested that increased tensile stress contributed to the initial damage of the SMCs and played a role in the regulation of medial SMC remodeling in vein grafts. © 1998 Biomedical Engineering Society.

PAC98: 8722-q, 8745-k

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REFERENCES

  1. Adams, A. E., and J. R. Pringle. Staining of actin with fluorochrome-conjugated phalloidin. Meth. Enzym.194:729- 729, 1991.

    Google Scholar 

  2. Angelini, G. D., A. J. Bryan, H. M. Williams, R. Morgan, and A. C. Newby. Distention promotes platelet and leukocyte adhesion and reduces short-term patency in pig arteriovenous bypass grafts. J. Thorac. Cardiovasc. Surg.99:433-439, 1990.

    Google Scholar 

  3. Batellier, J., M. Wassef, R. Merval, M. Duriez, and A. Tedgui. Protection from atherosclerosis in vein grafts by a rigid external support. Arteriosclerosis Thrombosis13:379- 384, 1993.

    Google Scholar 

  4. Berceli, S. A., H. S. Borovetz, R. A. Sheppeck, H. H. Moosa, V. S. Warty, M. A. Armany, and I. M. Herman. Mechanisms of vein graft atherosclerosis: LDL metabolism and endothelial actin reorganization. J. Vascular Surg.13:336-47, 1991.

    Google Scholar 

  5. Boerboom, L. E., G. N. Olinger, T. Z. Liu, E. R. Rodriguez, V. J. Ferrans, and A. H. Kissebah. Histologic, morphometric, and biochemical evolution of vein grafts in nonhuman primate model. I. Sequential changes within the first three months. J. Thorac. Cardiovasc. Surg.99:97-106, 1990.

    Google Scholar 

  6. Bryan, A. J., and G. D. Angelini. The biology of saphenous vein graft occlusion: etiology and strategies for prevention. Curr. Opinion Cardiol.9:641-649, 1994.

    Google Scholar 

  7. Canver, C. C. Conduit options in coronary artery bypass surgery. Chest108:1150-1155, 1995.

    Google Scholar 

  8. Cassimeris, L., H. McNeill, and S. H. Zigmond. Chemoattractant-stimulated polymorphonuclear leukocytes contain two populations of actin filaments that differ in their spacial distributions and relative stabilities. J. Cell Biol.110:1067-1075, 1990.

    Google Scholar 

  9. Chobanian, A. V. 1989 Corcoran lecture: adaptive and maladaptive responses of the arterial wall to hypertension. Hypertension15:666-674, 1990.

    Google Scholar 

  10. Davies, P. F., and S. C. Tripathi. Mechanical stress mechanisms and the cell. An endothelial paradigm. Circ. Res.72:239-245, 1993.

    Google Scholar 

  11. Donaldson, M. C., J. A. Mannick, and A. D. Whittemore. Causes of primary graft failure after in situ saphenous vein bypass grafting. J. Vasc. Surg.15:113-118, 1992.

    Google Scholar 

  12. Fath, K. A., R. W. Alexander, and P. Delafontaine. Abdominal coarctation increases insulin-like growth factor I mRNA levels in rat aorta. Circ. Res.72:271-277, 1993.

    Google Scholar 

  13. Fung, Y. C. Biodynamics: Circulation. New York: Springer, 1984, pp. 77-157.

    Google Scholar 

  14. Fung, Y. C., and S. Q. Liu. Changes of residual strains in arteries due to hypertrophy caused by aortic constriction. Circ. Res.65:1340-1349, 1989.

    Google Scholar 

  15. Fung, Y. C. Biomechanics: Motion, Flow, Stress, and Growth. New York: Springer, 1990, pp. 499-546.

    Google Scholar 

  16. Fung, Y. C., and S. Q. Liu. Changes of zero-stress state of rat pulmonary arteries in hypoxic hypertension. J. Appl. Physiol.70:2455-2470, 1991.

    Google Scholar 

  17. Fung, Y. C., and S. Q. Liu. Determination of the mechanical properties of the different layers of blood vessels in vivo. Proc. Natl. Acad. Sci. USA92:2169-2173, 1995.

    Google Scholar 

  18. Girard, H. Arterial pressure in chick embryo. Am. J. Physiol.224:454-460, 1973.

    Google Scholar 

  19. Grondin, C. M., and J. C. Thornton. The natural history of saphenous vein grafts. In: Coronary Artery Graft Disease. Mechanisms and Prevention, edited by T. F. Luscher, M. Turina, and E. Braunwald. Berlin: Springer, 1994, pp. 3-15.

    Google Scholar 

  20. Gundry, S. R., M. Jones, T. Ishihara, and V. J. Ferrans. Intraoperative trauma to human saphenous veins: scanning electron microscopic comparison of preparation techniques. Ann. Thorac. Surg.30:40-45, 1980.

    Google Scholar 

  21. Hamet, P., V. Hadrava, U. Kruppa, and J. Tremblay. Transforming growth factor b1 expression and effect in aortic smooth muscle cells from spontaneously hypertensive rats. Hypertension17:896-901, 1991.

    Google Scholar 

  22. Hartwig, J. H. Mechanisms of actin rearrangements mediating platelet activation. J. Cell Biol.118:1421-1442, 1992.

    Google Scholar 

  23. Hoch, J. R., V. K. Stark, D. A. Hullett, and W. D. Turnipseed. Vein graft intimal hyperplasia: Leukocytes and cytokine gene expression. Surgery116:463-471, 1994.

    Google Scholar 

  24. Hu, N., and E. B. Clark. Hemodynamics of the stage 12 to stage 29 chick embryo. Circ. Res.65:1665-1670, 1989.

    Google Scholar 

  25. Jang, I. K., and V. Fuster. Mechanisms of plaque formation and occlusion in venous coronary bypass grafts. In: Coronary Artery Graft Disease. Mechanisms and Prevention, edited by T. F. Luscher, M. Turina, and E. Braunwald. Berlin: Springer, 1994, pp. 42-50.

    Google Scholar 

  26. Kohler, T. R., T. R. Kirkman, and A. W. Clowes. The effect of rigid external support on vein graft adaptation to the arterial circulation. J. Vasc. Surg.9:277-285, 1989.

    Google Scholar 

  27. Langille, B. L., J. J. K. Graham, D. Kim, and A. I. Gotlieb. Dynamics of shear-induced redistribution of F-actin in endothelial cells in vivo. Arteriosclerosis Thrombosis11:1814- 1820, 1991.

    Google Scholar 

  28. Liu, S. Q., and Y. C. Fung. Relationship between hypertension, hypertrophy, and opening angle of zero-stress state of arteries following aortic constriction. J. Biomech. Eng.111:325-335, 1989.

    Google Scholar 

  29. Liu, S. Q., and Y. C. Fung. Changes in the structure and mechanical properties of pulmonary arteries in rats exposed to cigarette smoke. Am. Rev. Respir. Dis.148:768-777, 1993.

    Google Scholar 

  30. Liu, S. Q., and Y. C. Fung. Material coefficients of the strain energy function of pulmonary arteries in normal and cigarette smoke-exposed rats. J. Biomech.26:1261-1269, 1993.

    Google Scholar 

  31. Liu, S. Q., M. Yen, and Y. C. Fung. On measuring the third dimension of cultured endothelial cells. Proc. Natl. Acad. Sci. USA91:8782-8786, 1994.

    Google Scholar 

  32. Liu, S. Q., and Y. C. Fung. Indicial functions of arterial remodeling in response to locally altered blood pressure. Am. J. Physiol.270:H1323-H1333, 1996.

    Google Scholar 

  33. Liu, S. Q. Vein graft engineering. In: Advances in Bioengineering, ASME Proceedings, 1996, Vol. 33, pp. 473-474.

    Google Scholar 

  34. Liu, S. Q. Alterations in structure of elastic laminae of rat pulmonary arteries in hypoxic hypertension. J. Appl. Physiol.81:2147-2155, 1996.

    Google Scholar 

  35. Liu, S. Q. Regression of hypoxic hypertension-induced changes in elastic laminae of rat pulmonary arteries. J. Appl. Physiol.82:1677–1684, 1997.

    Google Scholar 

  36. Lyall, F., M. R. Deehan, I. A. Greer, F. Boswell, W. C. Brown, and G. T. McInners. Mechanical stretch increases proto-oncogene expression and phosphoinositide turnover in vascular smooth muscle cells. J. Hypert.12:1139-1145, 1994.

    Google Scholar 

  37. Metcalfe, M. J., G. Y. Lip, and H. J. Dargie. Factors influencing coronary artery bypass graft patency. Cardiovasc. Surg.2:679-85, 1994.

    Google Scholar 

  38. Mills, N. L., and C. T. Everson. Vein graft failure. Curr. Opinion Cardiology10:562-568, 1995.

    Google Scholar 

  39. Owens, G. K. Regulation of differentiation of vascular smooth muscle cells. Physiol. Rev.75:487-517, 1995.

    Google Scholar 

  40. Sarzani, R., G. Arnaldi, and A. V. Chobanian. Hypertensioninduced changes of platelet-derived growth factor receptor expression in rat aorta and heart. Hypertension17:888-895, 1991.

    Google Scholar 

  41. Small, J. V. Organization of actin in the leading edge of cultured cells: influence of osmium tetroxide and dehydration on the ultrastructure of actin meshworks. J. Cell Biol.91:694-694, 1981.

    Google Scholar 

  42. Sumpio, B. E., A. J. Banes, M. Buckley, and G. Johnson, Jr. Alterations in aortic endothelial cell morphology and cytoskeletal protein synthesis during cyclic tensional deformation. J. Vasc. Surg.7:130-138, 1988.

    Google Scholar 

  43. Theriot, J. A. Regulation of the actin cytoskeleton in living cells. Seminars Cell Biol.5:193-199, 1994.

    Google Scholar 

  44. Zar, J. H. Biostatistical Analysis. 2nd ed. Englewood Cliffs, NJ: Prentice Hall, 1984, pp. 162-184.

    Google Scholar 

  45. Zweep, H. P., S. Satoh, B. Van der Lei, W. I. L. J. Hinrichs, F. Dijk, J. Feijen, and C. R. H. Wildevuur. Degradation of a supporting prosthesis can optimize arterialization of autologous veins. Ann. Thorac. Surg.56:1117-1122, 1993.

    Google Scholar 

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Liu, S.Q., Fung, Y.C. Changes in the Organization of the Smooth Muscle Cells in Rat Vein Grafts. Annals of Biomedical Engineering 26, 86–95 (1998). https://doi.org/10.1114/1.52

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