Wall remodeling during luminal expansion of mesenteric arterial collaterals in the rat.

Wall remodeling associated with rapid luminal enlargement of collateral mesenteric arteries in rats was investigated 1 and 4 weeks after creation of a collateral pathway by ligating three to four sequential arteries. Paired observations were made of inner diameters of collateral and normal arteries in the same animals. Arterial blood flow was measured at the final observation. Sections of arteries were processed for morphological measurements. After 4 weeks, inner arterial diameter was increased more at the beginning (63 +/- 6%) than the end (25 +/- 9%) of the collateral pathway. At 1 and 4 weeks, respectively, cross-sectional areas of collateral relative to normal arteries were increased by 46 +/- 5% and 59 +/- 13% (lumen), 55 +/- 8% and 65 +/- 14% (media), and 89 +/- 18% and 60 +/- 31% (intima). The wall expansion during luminal enlargement resulted in a normal medial thickness:luminal radius relationship. At 1 week postligation, wall shear rate remained elevated and endothelial but not smooth muscle hyperplasia had occurred (intimal nuclei: 40 +/- 1.7 collateral versus 24 +/- 3.0 normal; medial nuclei: 42 +/- 6.8 collateral versus 37 +/- 2.1 normal). At 4 weeks, wall shear rate in collaterals was similar to normal arteries, and smooth muscle hyperplasia had taken place (medial nuclei: 84 +/- 9.4 collateral versus 44 +/- 4.7 normal). The data demonstrate that wall expansion associated with rapid luminal enlargement of these collaterals involves hyperplasia of both endothelial and smooth muscle cells; however, smooth muscle proliferation does not occur until after wall shear rate is reduced. The specific cellular adaptations that occur during collateral development may depend on the level of wall shear and shear-dependent modulation of endothelial growth factors.

[1]  B L Langille,et al.  Monocyte adhesion and changes in endothelial cell number, morphology, and F-actin distribution elicited by low shear stress in vivo. , 1993, The American journal of pathology.

[2]  H. Masuda,et al.  Difference in dilatation between endothelium-preserved and -desquamated segments in the flow-loaded rat common carotid artery. , 1992, Arteriosclerosis and thrombosis : a journal of vascular biology.

[3]  N K Hollenberg,et al.  "Tissue need" and limb collateral arterial growth. Skeletal contractile power and perfusion during collateral development in the rat. , 1992, Circulation research.

[4]  W. Casscells.  Smooth muscle cell growth factors. , 1991, Progress in growth factor research.

[5]  N. Resnick,et al.  Hemodynamic forces are complex regulators of endothelial gene expression , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[6]  C. Peiró,et al.  Influence of endothelium on cultured vascular smooth muscle cell proliferation. , 1995, Hypertension.

[7]  J. Angus,et al.  Reactivity of canine isolated epicardial collateral coronary arteries. Relation to vessel structure. , 1991, Circulation research.

[8]  S. Diamond,et al.  Constitutive NOS expression in cultured endothelial cells is elevated by fluid shear stress. , 1995, The American journal of physiology.

[9]  A. Hassid,et al.  Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. , 1989, The Journal of clinical investigation.

[10]  R M Lehman,et al.  Mechanism of enlargement of major cerebral collateral arteries in rabbits. , 1991, Stroke.

[11]  W. Schaper,et al.  The collateral circulation of the heart. , 1988, Progress in cardiovascular diseases.

[12]  K. Pritchard,et al.  Chronic exercise in dogs increases coronary vascular nitric oxide production and endothelial cell nitric oxide synthase gene expression. , 1994, Circulation research.

[13]  S Amerini,et al.  Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. , 1994, The Journal of clinical investigation.

[14]  Robert M. Nerem,et al.  Hemodynamics and Vascular Endothelial Biology , 1993, Journal of cardiovascular pharmacology.

[15]  S. Grinstein,et al.  Proton conductance of the plasma membrane: properties, regulation, and functional role. , 1993, The American journal of physiology.

[16]  H. Bohlen,et al.  Maturation of the rat intestinal microvasculature from juvenile to early adult life. , 1990, The American journal of physiology.

[17]  S Glagov,et al.  Shear stress regulation of artery lumen diameter in experimental atherogenesis. , 1987, Journal of vascular surgery.

[18]  B L Langille,et al.  Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. , 1986, Science.

[19]  H. Inui,et al.  Differences in signal transduction between platelet-derived growth factor (PDGF) alpha and beta receptors in vascular smooth muscle cells. PDGF-BB is a potent mitogen, but PDGF-AA promotes only protein synthesis without activation of DNA synthesis. , 1994, The Journal of biological chemistry.

[20]  H. Inui,et al.  Molecular structure and transcriptional regulation of the gene for the platelet-derived growth factor alpha receptor in cultured vascular smooth muscle cells. , 1995, The Journal of clinical investigation.

[21]  H. Granger,et al.  Nitric oxide promotes DNA synthesis and cyclic GMP formation in endothelial cells from postcapillary venules. , 1993, Biochemical and biophysical research communications.

[22]  A. Clowes,et al.  Increased blood flow inhibits neointimal hyperplasia in endothelialized vascular grafts. , 1991, Circulation research.

[23]  A. Kamiya,et al.  Increase in endothelial cell density before artery enlargement in flow-loaded canine carotid artery. , 1989, Arteriosclerosis.

[24]  R. Nerem,et al.  Fluid shear stress stimulates platelet-derived growth factor expression in endothelial cells. , 1993, The American journal of physiology.

[25]  J. Anderson,et al.  Chronic collateral growth after femoral artery occlusion in the dog. , 1971, Journal of applied physiology.

[26]  T Togawa,et al.  Adaptive regulation of wall shear stress to flow change in the canine carotid artery. , 1980, The American journal of physiology.

[27]  B L Langille,et al.  Expression of ICAM-1 and VCAM-1 and monocyte adherence in arteries exposed to altered shear stress. , 1995, Arteriosclerosis, thrombosis, and vascular biology.

[28]  G. Owens,et al.  Control of hypertrophic versus hyperplastic growth of vascular smooth muscle cells. , 1989, The American journal of physiology.

[29]  C M Bloor,et al.  Coronary collateral development in swine after coronary artery occlusion. , 1992, Circulation research.

[30]  V. Dzau.  The role of mechanical and humoral factors in growth regulation of vascular smooth muscle and cardiac myocytes. , 1993, Current opinion in nephrology and hypertension.

[31]  Longland Cj.  The collateral circulation of the limb; Arris and Gale lecture delivered at the Royal College of Surgeons of England on 4th February, 1953. , 1953 .

[32]  H. Burkhart,et al.  Early collateral and microvascular adaptations to intestinal artery occlusion in rat. , 1996, The American journal of physiology.

[33]  H. Bohlen,et al.  Quantification of Intestinal Microvascular Growth During Maturation: Techniques and Observations , 1987, Circulation research.

[34]  J. Bevan,et al.  Flow-Dependent Regulation of Vascular Function , 1995, Clinical Physiology Series.

[35]  J. M. Lash,et al.  Early adaptations in collateral and microvascular resistances after ligation of the rat femoral artery. , 1995, Journal of applied physiology.

[36]  R. Dubey.  Vasodilator-derived nitric oxide inhibits fetal calf serum- and angiotensin-II-induced growth of renal arteriolar smooth muscle cells. , 1994, The Journal of pharmacology and experimental therapeutics.

[37]  J A Frangos,et al.  Shear stress increases endothelial platelet-derived growth factor mRNA levels. , 1991, The American journal of physiology.

[38]  W. Chilian,et al.  METHODS FOR ASSESSING CORONARY COLLATERAL GROWTH: INSIGHTS INTO MECHANISMS RESPONSIBLE FOR COLLATERAL DEVELOPMENT , 1992 .

[39]  B. L. Langille,et al.  Blood Flow-Induced Remodeling of the Artery Wall , 1995 .

[40]  P. Boutouyrie,et al.  Remodeling of the radial artery in response to a chronic increase in shear stress. , 1996, Hypertension.

[41]  J. M. Lash,et al.  Exercise training effects on collateral and microvascular resistances in rat model of arterial insufficiency. , 1995, The American journal of physiology.

[42]  B L Langille,et al.  Adaptations of carotid arteries of young and mature rabbits to reduced carotid blood flow. , 1989, The American journal of physiology.

[43]  A Kamiya,et al.  Effects of endothelial denudation in flow-induced arterial dilatation. , 1993, Frontiers of medical and biological engineering : the international journal of the Japan Society of Medical Electronics and Biological Engineering.