Arteriogenesis, a new concept of vascular adaptation in occlusive disease

The formation of collateral arteries as a process adaptive to arterial occlusion is now called ‘arteriogenesis’ to emphasize the difference to angiogenesis, the formation of capillaries by sprouting from pre-existent ones (W. Schaper, I. Buschmann. Cardiovasc Res 1999; 43: 835–7; I. Buschmann, W. Schaper. J Pathol 2000; 190: 338–42; D. Scholz et al. Virchows Arch 2000; 436: 257–70). The differences are that collaterals develop from pre-existing arterioles and that circulating monocytes adhere to endothelium that had been activated by the high shear stress generated by the large pressure differences between perfusion territories. Monocytes are the major producers of growth factors and of proteolytic enzymes that enable smooth muscle cells to migrate and divide. The nature of the growth factors remains uncertain. Neither FGF-1/2 nor VEGF is expressed on the transcriptional or translational level in collaterals proper and in the tissue surrounding them. Only FGF receptor 1 has a brief window of upregulation shortly after arterial occlusion. While transgenic overexpression of FGF-1 increases number and branching of arterioles, targeted disruption of FGF-1/2 does not negatively influence arteriogenesis. Cytokines that attract monocytes or prolong the life span of monocytes (MCP-1, GM CSF) are strong arteriogenic factors. Collateral vessels exhibit the same morphology whether they had formed in the heart, limbs or brain or in dogs, rabbits or mouse. They are tortuous because they also increase lengthwise in a restricted space. In animals larger than the mouse, they develop an intima, and initially, many arterioles participate in arteriogenesis, but only a few mature into large arterial channels which, when arterial occlusion had proceeded slowly enough, can replace the occluded artery to a significant proportion. Therapy with a single growth factor in animals with occluded femoral arteries significantly increases the speed of arteriogenesis but does not significantly increase the level of adaptation. It appears that the mastergene for arteriogenesis still awaits discovery.

[1]  J. Canty,et al.  Regional alterations in SR Ca2+-ATPase, phospholamban, and HSP-70 expression in chronic hibernating myocardium. , 1999, American journal of physiology. Heart and circulatory physiology.

[2]  W. Schaper,et al.  Vascular remodeling and altered protein expression during growth of coronary collateral arteries. , 1998, Journal of molecular and cellular cardiology.

[3]  W. Schaper,et al.  The endothelial surface of growing coronary collateral arteries. Intimal margination and diapedesis of monocytes , 1976, Virchows Archiv A.

[4]  W. Schaper,et al.  Pathophysiology of myocardial perfusion. , 1976, Pathobiology annual.

[5]  R. Bruzzone,et al.  Connections with connexins: the molecular basis of direct intercellular signaling. , 1996, European journal of biochemistry.

[6]  S. Epstein,et al.  Basic fibroblast growth factor enhances myocardial collateral flow in a canine model. , 1994, The American journal of physiology.

[7]  G. Semenza,et al.  Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. , 1994, The Journal of biological chemistry.

[8]  W. Schaper,et al.  Ultrastructure of ischemia-induced changes in the precapillary anastomotic network of the heart. , 1972, The American journal of cardiology.

[9]  W. Schaper,et al.  Quantification of Collateral Resistance in Acute and Chronic Experimental Coronary Occlusion in the Dog , 1976, Circulation research.

[10]  B. Feeley,et al.  Ex Vivo Antisense Oligonucleotides to Proliferating Cell Nuclear Antigen and Cdc2 Kinase Inhibit Graft Coronary Artery Disease , 2000, Circulation.

[11]  H. Dvorak,et al.  Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. , 1995, The American journal of pathology.

[12]  M. De Brabander,et al.  DNA Synthesis and Mitoses in Coronary Collateral Vessels of the Dog , 1971, Circulation research.

[13]  S. Schwartz The intima : A new soil. , 1999, Circulation research.

[14]  R. Ogilvie,et al.  Basic fibroblast growth factor increases collateral blood flow in rats with femoral arterial ligation. , 1996, Circulation research.

[15]  P. Carmeliet Mechanisms of angiogenesis and arteriogenesis , 2000, Nature Medicine.

[16]  W. Risau,et al.  Mechanisms of angiogenesis , 1997, Nature.

[17]  W. Schaper,et al.  Connexin37, not Cx40 and Cx43, is induced in vascular smooth muscle cells during coronary arteriogenesis. , 2001, Journal of molecular and cellular cardiology.

[18]  W. Schaper,et al.  Monocyte chemotactic protein-1 increases collateral and peripheral conductance after femoral artery occlusion. , 1997, Circulation research.

[19]  W. Schaper,et al.  DNA synthesis in coronary collaterals after coronary artery occlusion in conscious dog. , 1982, The American journal of physiology.

[20]  Dian Feng,et al.  Heterogeneity of the Angiogenic Response Induced in Different Normal Adult Tissues by Vascular Permeability Factor/Vascular Endothelial Growth Factor , 2000, Laboratory Investigation.

[21]  P. Carmeliet,et al.  Clotting Factors Build Blood Vessels , 2001, Science.

[22]  C. Bloor,et al.  Exercise Induced Coronary Collateral Development: A Comparison to Other Models of Myocardial Angiogenesis , 1992 .

[23]  I. Buschmann,et al.  Arteriogenesis, the good and bad of it. , 1999, European heart journal.

[24]  C. Basilico,et al.  Compensation by Fibroblast Growth Factor 1 (FGF1) Does Not Account for the Mild Phenotypic Defects Observed in FGF2 Null Mice , 2000, Molecular and Cellular Biology.

[25]  I. Buschmann,et al.  The pathophysiology of the collateral circulation (arteriogenesis) , 2000, The Journal of pathology.

[26]  W. Schaper,et al.  Altered balance between extracellular proteolysis and antiproteolysis is associated with adaptive coronary arteriogenesis. , 2000, Journal of molecular and cellular cardiology.

[27]  W. Schaper Tangential wall stress as a molding force in the development of collateral vessels in the canine heart , 1967, Experientia.

[28]  Takashi Nakamura,et al.  Collateral Circulation of the Heart Morphological and Functional Study on the Interarterial Coronary Anastomoses , 1963 .

[29]  B. Nilius,et al.  Blockers of volume-activated Cl− currents inhibit endothelial cell proliferation , 1995, Pflügers Archiv.

[30]  Gil Vm Hibernating myocardium. An incomplete adaptation to ischemia , 1998 .

[31]  Takayuki Asahara,et al.  Isolation of Putative Progenitor Endothelial Cells for Angiogenesis , 1997, Science.

[32]  W. Schaper,et al.  Angiogenesis but not collateral growth is associated with ischemia after femoral artery occlusion. , 1997, The American journal of physiology.

[33]  Imo E. Hoefer,et al.  Role of Ischemia and of Hypoxia-Inducible Genes in Arteriogenesis After Femoral Artery Occlusion in the Rabbit , 2001, Circulation research.

[34]  E. Unanue,et al.  Activated macrophages induce vascular proliferation , 1977, Nature.

[35]  J. Ware,et al.  Angiogenesis in ischemic heart disease , 1997, Nature Medicine.

[36]  R. Busse,et al.  Ultrastructure and molecular histology of rabbit hind-limb collateral artery growth (arteriogenesis) , 2000, Virchows Archiv.

[37]  W. Risau Differentiation of endothelium , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[38]  J. Ross,et al.  Comparison of Postpacing and Exercise‐induced Myocardial Dysfunction During Collateral Development in Conscious Dogs , 1982, Circulation.

[39]  W. Schaper,et al.  Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. , 1998, The Journal of clinical investigation.