Abstract
We have previously shown that monocytes adhere to the vascular wall during collateral vessel growth (arteriogenesis) and capillary sprouting (angiogenesis). In this study we investigated the association of monocyte accumulation with both the production of the cytokines-basic fibroblast growth factor (bFGF) and TNF-alpha-and vessel proliferation in the rabbit after femoral artery occlusion. In particular, we studied the effects of an increase in monocyte recruitment by LPS on capillary density as well as collateral and peripheral conductance after 7 d of occlusion. Monocytes accumulated around day 3 in collateral arteries when maximal proliferation was observed, and stained strongly for bFGF and TNF-alpha. In the lower limb where angiogenesis was shown to be predominant, macrophage accumulation was also closely associated with maximal proliferation (around day 7). LPS treatment significantly increased capillary density (424+/-26.1 n/mm2 vs. 312+/-20.7 n/mm2; P < 0.05) and peripheral conductance (109+/-33.8 ml/min/100 mmHg vs. 45+/-6.8 ml/min/100 mmHg; P < 0.05) as compared with untreated animals after 7 d of occlusion. These results indicate that monocyte activation plays a major role in angiogenesis and collateral artery growth.
Full Text
The Full Text of this article is available as a PDF (817.5 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Arras M., Höche A., Bohle R., Eckert P., Riedel W., Schaper J. Tumor necrosis factor-alpha in macrophages of heart, liver, kidney, and in the pituitary gland. Cell Tissue Res. 1996 Jul;285(1):39–49. doi: 10.1007/s004410050618. [DOI] [PubMed] [Google Scholar]
- Bastagli L., Lazzarotto T., Caldarera C. M., Guarnieri C., Ventura C., Pepe G., Puddu P. Presence of basic fibroblast growth factor in cultured rat cardiomyocytes and its release in culture medium. Ann N Y Acad Sci. 1995 Mar 27;752:417–421. doi: 10.1111/j.1749-6632.1995.tb17449.x. [DOI] [PubMed] [Google Scholar]
- Berse B., Brown L. F., Van de Water L., Dvorak H. F., Senger D. R. Vascular permeability factor (vascular endothelial growth factor) gene is expressed differentially in normal tissues, macrophages, and tumors. Mol Biol Cell. 1992 Feb;3(2):211–220. doi: 10.1091/mbc.3.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Birdsall H. H., Green D. M., Trial J., Youker K. A., Burns A. R., MacKay C. R., LaRosa G. J., Hawkins H. K., Smith C. W., Michael L. H. Complement C5a, TGF-beta 1, and MCP-1, in sequence, induce migration of monocytes into ischemic canine myocardium within the first one to five hours after reperfusion. Circulation. 1997 Feb 4;95(3):684–692. doi: 10.1161/01.cir.95.3.684. [DOI] [PubMed] [Google Scholar]
- Clauss M., Grell M., Fangmann C., Fiers W., Scheurich P., Risau W. Synergistic induction of endothelial tissue factor by tumor necrosis factor and vascular endothelial growth factor: functional analysis of the tumor necrosis factor receptors. FEBS Lett. 1996 Jul 29;390(3):334–338. doi: 10.1016/0014-5793(96)00690-4. [DOI] [PubMed] [Google Scholar]
- Cortese R., Monaci P., Luzzago A., Santini C., Bartoli F., Cortese I., Fortugno P., Galfrè G., Nicosia A., Felici F. Selection of biologically active peptides by phage display of random peptide libraries. Curr Opin Biotechnol. 1996 Dec;7(6):616–621. doi: 10.1016/s0958-1669(96)80072-3. [DOI] [PubMed] [Google Scholar]
- Dvorak H. F., Brown L. F., Detmar M., Dvorak A. M. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol. 1995 May;146(5):1029–1039. [PMC free article] [PubMed] [Google Scholar]
- Fràter-Schröder M., Risau W., Hallmann R., Gautschi P., Böhlen P. Tumor necrosis factor type alpha, a potent inhibitor of endothelial cell growth in vitro, is angiogenic in vivo. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5277–5281. doi: 10.1073/pnas.84.15.5277. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goto F., Goto K., Weindel K., Folkman J. Synergistic effects of vascular endothelial growth factor and basic fibroblast growth factor on the proliferation and cord formation of bovine capillary endothelial cells within collagen gels. Lab Invest. 1993 Nov;69(5):508–517. [PubMed] [Google Scholar]
- Iijima K., Yoshikawa N., Connolly D. T., Nakamura H. Human mesangial cells and peripheral blood mononuclear cells produce vascular permeability factor. Kidney Int. 1993 Nov;44(5):959–966. doi: 10.1038/ki.1993.337. [DOI] [PubMed] [Google Scholar]
- Ito W. D., Arras M., Scholz D., Winkler B., Htun P., Schaper W. Angiogenesis but not collateral growth is associated with ischemia after femoral artery occlusion. Am J Physiol. 1997 Sep;273(3 Pt 2):H1255–H1265. doi: 10.1152/ajpheart.1997.273.3.H1255. [DOI] [PubMed] [Google Scholar]
- Ito W. D., Arras M., Winkler B., Scholz D., Schaper J., Schaper W. Monocyte chemotactic protein-1 increases collateral and peripheral conductance after femoral artery occlusion. Circ Res. 1997 Jun;80(6):829–837. doi: 10.1161/01.res.80.6.829. [DOI] [PubMed] [Google Scholar]
- Lazarous D. F., Scheinowitz M., Shou M., Hodge E., Rajanayagam S., Hunsberger S., Robison W. G., Jr, Stiber J. A., Correa R., Epstein S. E. Effects of chronic systemic administration of basic fibroblast growth factor on collateral development in the canine heart. Circulation. 1995 Jan 1;91(1):145–153. doi: 10.1161/01.cir.91.1.145. [DOI] [PubMed] [Google Scholar]
- Leibovich S. J., Polverini P. J., Shepard H. M., Wiseman D. M., Shively V., Nuseir N. Macrophage-induced angiogenesis is mediated by tumour necrosis factor-alpha. Nature. 1987 Oct 15;329(6140):630–632. doi: 10.1038/329630a0. [DOI] [PubMed] [Google Scholar]
- Lupia E., Montrucchio G., Battaglia E., Modena V., Camussi G. Role of tumor necrosis factor-alpha and platelet-activating factor in neoangiogenesis induced by synovial fluids of patients with rheumatoid arthritis. Eur J Immunol. 1996 Aug;26(8):1690–1694. doi: 10.1002/eji.1830260804. [DOI] [PubMed] [Google Scholar]
- Mackay F., Loetscher H., Stueber D., Gehr G., Lesslauer W. Tumor necrosis factor alpha (TNF-alpha)-induced cell adhesion to human endothelial cells is under dominant control of one TNF receptor type, TNF-R55. J Exp Med. 1993 May 1;177(5):1277–1286. doi: 10.1084/jem.177.5.1277. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Neumann B., Machleidt T., Lifka A., Pfeffer K., Vestweber D., Mak T. W., Holzmann B., Krönke M. Crucial role of 55-kilodalton TNF receptor in TNF-induced adhesion molecule expression and leukocyte organ infiltration. J Immunol. 1996 Feb 15;156(4):1587–1593. [PubMed] [Google Scholar]
- Patrick C. W., Jr, McIntire L. V. Shear stress and cyclic strain modulation of gene expression in vascular endothelial cells. Blood Purif. 1995;13(3-4):112–124. doi: 10.1159/000170194. [DOI] [PubMed] [Google Scholar]
- Polverini P. J., Cotran P. S., Gimbrone M. A., Jr, Unanue E. R. Activated macrophages induce vascular proliferation. Nature. 1977 Oct 27;269(5631):804–806. doi: 10.1038/269804a0. [DOI] [PubMed] [Google Scholar]
- Riese J., Zeller R., Dono R. Nucleo-cytoplasmic translocation and secretion of fibroblast growth factor-2 during avian gastrulation. Mech Dev. 1995 Jan;49(1-2):13–22. doi: 10.1016/0925-4773(94)00296-y. [DOI] [PubMed] [Google Scholar]
- Risau W. Mechanisms of angiogenesis. Nature. 1997 Apr 17;386(6626):671–674. doi: 10.1038/386671a0. [DOI] [PubMed] [Google Scholar]
- Schaper J., König R., Franz D., Schaper W. The endothelial surface of growing coronary collateral arteries. Intimal margination and diapedesis of monocytes. A combined SEM and TEM study. Virchows Arch A Pathol Anat Histol. 1976 Jun 22;370(3):193–205. doi: 10.1007/BF00427580. [DOI] [PubMed] [Google Scholar]
- Schaper W., Ito W. D. Molecular mechanisms of coronary collateral vessel growth. Circ Res. 1996 Nov;79(5):911–919. doi: 10.1161/01.res.79.5.911. [DOI] [PubMed] [Google Scholar]
- Shyy Y. J., Hsieh H. J., Usami S., Chien S. Fluid shear stress induces a biphasic response of human monocyte chemotactic protein 1 gene expression in vascular endothelium. Proc Natl Acad Sci U S A. 1994 May 24;91(11):4678–4682. doi: 10.1073/pnas.91.11.4678. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takeshita S., Zheng L. P., Brogi E., Kearney M., Pu L. Q., Bunting S., Ferrara N., Symes J. F., Isner J. M. Therapeutic angiogenesis. A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model. J Clin Invest. 1994 Feb;93(2):662–670. doi: 10.1172/JCI117018. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Unger E. F., Banai S., Shou M., Lazarous D. F., Jaklitsch M. T., Scheinowitz M., Correa R., Klingbeil C., Epstein S. E. Basic fibroblast growth factor enhances myocardial collateral flow in a canine model. Am J Physiol. 1994 Apr;266(4 Pt 2):H1588–H1595. doi: 10.1152/ajpheart.1994.266.4.H1588. [DOI] [PubMed] [Google Scholar]
- Wahl S. M., Hunt D. A., Wakefield L. M., McCartney-Francis N., Wahl L. M., Roberts A. B., Sporn M. B. Transforming growth factor type beta induces monocyte chemotaxis and growth factor production. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5788–5792. doi: 10.1073/pnas.84.16.5788. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wahl S. M., Wong H., McCartney-Francis N. Role of growth factors in inflammation and repair. J Cell Biochem. 1989 Jun;40(2):193–199. doi: 10.1002/jcb.240400208. [DOI] [PubMed] [Google Scholar]
- White F. C., Carroll S. M., Magnet A., Bloor C. M. Coronary collateral development in swine after coronary artery occlusion. Circ Res. 1992 Dec;71(6):1490–1500. doi: 10.1161/01.res.71.6.1490. [DOI] [PubMed] [Google Scholar]
- Wung B. S., Cheng J. J., Chao Y. J., Lin J., Shyy Y. J., Wang D. L. Cyclical strain increases monocyte chemotactic protein-1 secretion in human endothelial cells. Am J Physiol. 1996 Apr;270(4 Pt 2):H1462–H1468. doi: 10.1152/ajpheart.1996.270.4.H1462. [DOI] [PubMed] [Google Scholar]
- Yanagisawa-Miwa A., Uchida Y., Nakamura F., Tomaru T., Kido H., Kamijo T., Sugimoto T., Kaji K., Utsuyama M., Kurashima C. Salvage of infarcted myocardium by angiogenic action of basic fibroblast growth factor. Science. 1992 Sep 4;257(5075):1401–1403. doi: 10.1126/science.1382313. [DOI] [PubMed] [Google Scholar]
- van der Poll T., Coyle S. M., Kumar A., Barbosa K., Agosti J. M., Lowry S. F. Down-regulation of surface receptors for TNF and IL-1 on circulating monocytes and granulocytes during human endotoxemia: effect of neutralization of endotoxin-induced TNF activity by infusion of a recombinant dimeric TNF receptor. J Immunol. 1997 Feb 1;158(3):1490–1497. [PubMed] [Google Scholar]