The art of arteriogenesis

Cell Biochemistry and Biophysics

Volumn 43, Issue 1, 2005, Pages 1-15

  Deindl, Elisabeth ^a,b   Schaper, Wolfgang ^b  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

Arteriogenesis; Cofilin; Collateral arteries; Fibroblast growth factor; Hypoxia; Mechanical forces; Monocytes; Stem cells; Urokinase plasminogen activator; Vascular endothelial growth factor

Indexed keywords

ANIMALIA;

EID: 23244453898     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1385/cbb:43:1:001     Document Type: Article

References (101)

1. Schaper, W., DeBrabander, M., and Lewi, P. (1971) DNA-synthesis and mitoses in coronary collateral vessels of the dog. Circ. Res. 28, 671-679.
2. Wolf, C., Cai, J. W., Vosschulte, R., et al. (1998) Vascular remodeling and altered protein expression during growth of coronary collateral arteries. J. Mol. Cell. Cardiol. 30, 2291-2305.
3. Scholz, D., Ziegelhoeffer, T., Helisch, A., et al. (2002) Contribution of arteriogenesis and angiogenesis to postocclusive hindlimb perfusion in mice. J. Mol. Cell. Cardiol. 34, 775-787.
4. Herzog, S., Sager, H., Khmelevski, E., Deylig, A., and Ito, W. D. (2002) Collateral arteries grow from preexisting anastomoses in the rat hindlimb. Am. J. Physiol. Heart Circ. Physiol. 283, H2012-H2020.
5. Ito, W. D., Arras, M., Winkler, B., Scholz, D., Schaper, J., and Schaper, W. (1997) Monocyte chemotactic protein-1 increases collateral and peripheral conductance after femoral artery occlusion. Circ. Res. 80, 829-837.
6. Schaper, W., Pipp, F., Scholz, D., et al. (2004) Physical forces and their translation into molecular mechanisms, in Arteriogenesis, (Schaper, W. and Schaper, J. eds.) Kluwer Academic, Boston, pp. 73-114.
7. Neufeld, G., Cohen, T., Gengrinovitch, S., and Poltorak, Z. (1999) Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 13, 9-22.
8. Fulton, W. F. M. (1965) The Coronary Arteries, Charles C. Thomas., Springfield, IL.
9. Schaper, W. and Schaper, J. (1993) Collateral Circulation - Heart, Brain, Kidney, Limbs. Kluwer Academic, Boston.
10. Paskins-Hurlburt, A. and Hollenberg, N. K. (1992) "Tissue need" and limb collateral arterial growth: skeletal contractile power and perfusion during collateral development in the rat. Circ. Res. 70, 546-553.
11. Henry, T. D., Annex, B. H., McKendall, G. R., et al. (2003) The VIVA trial: Vascular endothelial growth factor in Ischemia for Vascular Angiogenesis. Circulation 107, 1359-1365.
12. Makinen, K., Manninen, H., Hedman, M., et al. (2002) Increased vascularity detected by digital subtraction angiography after VEGF gene transfer to human lower limb artery: a randomized., placebo-controlled, double-blinded phase II study. Mol. Ther. 6, 127-133.
13. Rajagopalan, S., Mohler, E. R., 3rd., Lederman, R. J., et al. (2003) Regional angiogenesis with vascular endothelial growth factor in peripheral arterial disease: a phase II randomized, double-blind, controlled study of adenoviral delivery of vascular endothelial growth factor 121 in patients with disabling intermittent claudication. Circulation 108, 1933-1938.
14. Kastrup, J. (2003) Therapeutic angiogenesis in ischemic heart disease: gene or recombinant vascular growth factor protein therapy? Curr. Gene Ther. 3, 197-206.
15. Lee, C. W., Stabile, E., Kinnaird, T., et al. (2004) Temporal patterns of gene expression after acute hindlimb ischemia in mice: insights into the genomic program for collateral vessel development. J. Am. Coll. Cardiol. 43, 474-482.
16. Ito, W. D., Arras, M., Scholz, D., Winkler, B., Htun, P., and Schaper, W. (1997) Angiogenesis but not collateral growth is associated with ischemia after femoral artery occlusion. Am. J. Physiol. 273, H1255-H1265.
17. Deindl, E. and Schaper, W. (1999) Collateral and capillary formation - a comparison, in Therapeutic Angiogenesis, Ernst Schering Research Foundation - Workshop 28 (Dormandy, J. A., Dole, W. P., and Rubanyi, G. M., eds.), Springer, Berlin, pp. 67-86.
18. Deindl, E., Buschmann, I., Hoefer, I. E., et al. (2001) Role of ischemia and hypoxia-inducible genes in arteriogenesis after femoral artery occlusion in the rabbit. Circ. Res. 89, 779-786.
19. Deindl, E., Helisch, A., Scholz, D., Heil, M., Wagner, S., and Schaper, W. (2004) Role of hypoxia/ischemia/VEGF-A and strain differences, in Arteriogenesis, (Schaper, W. and Schaper, J., eds.) Kluwer Academic, Boston, pp. 115-130.
20. Scholz, D., Ito, W., Fleming, I., Deindl, E., Sauer, A., Wiesnet, M., Busse, R., Schaper, J., and Schaper, W. (2000) Ultrastructure and molecular histology of rabbit hindlimb collateral artery growth (arteriogenesis). Virchows Arch. 436, 257-270.
21. Arras, M., Ito, W. D., Scholz, D., Winkler, B., Schaper, J., and Schaper, W. (1998) Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. J. Clin. Invest. 101, 41-50.
22. Ziegelhoeffer, T., Fernandez, B., Kostin, S., et al. (2004) Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ. Res. 94, 230-238.
23. Busse, R. and Fleming. I. (2003) Regulation of endothelium-derived vasoactive autacoid production by hemodynamic forces. Trends Pharmacol. Sci. 24, 24-29.
24. Galbraith, C. G., Skalak, R., and Chien, S. (1998) Shear stress induces spatial reorganization of the endothelial cell cytoskeleton. Cell. Motil. Cytoskel. 40, 317-330.
25. Moon, A. and Drubin, D. G. (1995) The ADF/cofilin proteins: stimulus-responsive modulators of actin dynamics. Mol. Biol. Cell. 6, 1423-1431.
26. Theriot, J. A. (1997) Accelerating on a treadmill: ADF/cofilin promotes rapid actin turnover in the dynamic cytoskeleton. J. Cell Biol. 136, 1165-1168.
27. Yonezawa, N., Nishida, E., and Sakai, H. (1985) pH control of actin polymerization by cofilin. J. Biol. Chem. 260, 14,410-14,412.
28. Toshima, J., Toshima, J. Y., Amano, T., Yang, N., Narumiya, S., and Mizundo, K. (2001) Cofilin phosphorylation by protein kinase testicular protein kinase 1 and its role in integrin-mediated actin reorganization and focal adhesion formation. Mol. Biol. Cell 12, 1131-1145.
29. Arber, S., Barbayannis, F. A., Hanser, H., et al. (1998) Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393, 805-809.
30. Niwa, R., Nagata-Ohashi, K., Takeichi, M., Mizundo, K., and Uemura, T. (2002) Control of actin reorganization by slingshot, a family of phosphatases that dephosphorylate ADF/cofilin. Cell 108, 233-246.
31. Ono, S., Minami, N., Abe, H., and Obinata, T. (1994) Characterization of a novel cofilin isoform that is predominantely expressed in mammilian skeletal muscle. J. Biol. Chem. 269, 15,280-15,286.
32. Boengler, K., Pipp, F., Broich, K., Fernandez, B., Schaper, W., and Deindl, E. (2003) Identification of differentially expressed genes like cofilin2 in growing collateral arteries. Biochem. Biophys. Res. Commun. 17, 751-756.
33. Vartiainen, M. K., Mustonen, T., Mattila, P. K., et al. (2002) The three mouse actin-depolymerizing factor/cofilins evolved to fullfill cell-type-specific requirements for actin dynamics. Mol. Biol. Cell 13, 725-732.
34. Baird, A. and Klagsbrunn, M. (1991) The fibroblast growth factor family. Cancer Cells 3, 239-243.
35. Fernig, D. G. and Gallagher, J. T. (1994) Fibroblast growth factors and their receptors: an information network controlling tissue growth, morphogenesis and repair. Prog. Growth Factor Res. 5, 353-377.
36. Givol, D. and Yayon, A. (1992) Complexity of FGF receptors: genetic basis for structural diversity and functional specificity. FASEB J. 6, 3362-3369.
37. Partanen, J., Vainikka, S., Korhonen, J., Armstrong, E., and Alitalo, K. (1992) Diverse receptors for fibroblast growth factors. Prog. Growth Factors Res. 4, 69-83.
38. Schumacher, B., Pecher, P., von Specht, B. U., and Stegmann, T. (1998) Induction of neoangiogenesis in ischemic myocardium by human growth factors: first clinical results of a new treatment of coronary heart disease. Circulation 97, 645-650.
39. Unger, E. F., Banai, S., Shou, M., et al. (1994) Basic fibroblast growth factor enhances myocardial collateral flow in a canine model. Am. J. Physiol. 266, H1588-H1595.
40. Yang, H. T., Deschenes, M. R., Ogilvie, R. W., and Terjung, R. L. (1996) Basic fibroblast growth factor increases collateral blood flow in rats with femoral arterial ligation. Circ. Res. 79, 62-69.
41. Rajanayagam, M. A., Shou, M., Thirumurti, V., et al. (2000) Intracoronary basic fibroblast growth factor enhances myocardial collateral perfusion in dog. J. Am. Coll. Cardiol. 35, 519-526.
42. Horvath, K. A., Doukas, J., Lu, CY., et al. (2002) Myocardial function recovery after fibroblast growth factor 2 gene therapy as assessed by echocardiography and magnetic resonance imaging. Ann. Thorac. Surg. 74, 481-486.
43. Simons, M., Annex, B. H., Laham, R. J., et al. (2002) Pharmacological treatment of coronary artery disease with recombinant fibroblast growth factor-2: double-blind, randomized, controlled clinical trial. Circulation 105, 788-793.
44. Lederman, R. J., Mendelsohn, F. O., Anderson, R. D., et al. (2002) Therapeutic angiogenesis with recombinant fibroblast growth factor-2 for intermittent claudication (the TRAFFIC study): a randomised trial. Lancet 359, 2053-2058.
45. Burgess, W. H. and Maciag, T. (1989) The heparin-binding (fibroblast) growth factor family of proteins. Annu. Rev. Biochem. 58, 575-606.
46. Basilico, C. and Moscatelli, D. (1992) The FGF family of growth factors and oncogenes. Adv. Cancer Res. 59, 115-165.
47. Johnson, D. E. and Wiliams, L. T. (1993) Structural and functional diversity in the FGF receptor multigene family growth factors and oncogenes. Adv. Cancer Res. 60, 1-60.
48. Jin, Y., Pasumarthi, B. S., Bock, M. E., Lytras, A., Kardami, E., and Cattini, P. A. (1994) Cloning and expression of fibroblast growth factor receptor-1 isoforms in the mouse heart: evidence for isoform switching during heart development. J. Mol. Cell. Cardiol. 26, 1449-1459.
49. Wang, J.-K., Gao, G., and Goldfarb, M. (1994) Fibroblast growth factor receptors have different signaling and mitogenic potentials. Mol. Cell. Biol. 14, 181-188.
50. Abraham, J. A., Mergia, A., Whang, J. L., Tumola, A., Gospodarowicz, D., and Fiddes, J. C. (1986) Nucleotide sequence of a bovine clone encoding the angiogenic protein, basic fibroblast growth factor. Science 233, 545-548.
51. Muthukrishan, L., Warder, E., and McNeil, P. L. (1991) Basic fibroblast growth factor is efficiently released from cytosolic storage sites through plasma membrane disruptions of endothelial cells. J. Cell. Physiol. 148, 1-16.
52. McNeil, P. L., Muthukrishnan, W. E., and D'Amore, P. A. (1989) Growth factors are released by mechanically wounded endothelial cells. J. Cell Biol. 109, 811-821.
53. Mignatti, P., Morimoto, T., and Rifkin, D. B. (1992) Basic fibroblast growth factor, a protein devoid of of secretory signal sequence, is released by cells via a pathway independent of the endoplasmic reticulum-Golgi complex. J. Cell Physiol. 151, 81-93.
54. 3. J. Biol. Chem. 277, 23,453-23,458.
55. Prudovsky, I., Bagala, C., Tarantini, F., Mandinova, A., Bellum, S., and Maciag, T. (2002) The intracellular translocation of the components of the fibroblast growth factor 1 release complex precedes their assembly prior to export. J. Cell Biol. 158, 201-208.
56. Schlessinger, J. and Ullrich, A. (1992) Growth factor signaling by receptor tyrosine kinases. Neuron 9, 383-391.
57. Schlessinger, J., Lax, I., and Lemmon, M. (1995) Regulation of growth factor activation by proteoglycans: what is the role of the low affinity receptors? Cell 83, 357-360.
58. Friesel, R. and Maciag, T. (1999) Fibroblast growth factor prototype release and fibroblast growth factor receptor signaling. Thromb. Haemost. 82, 748-754.
59. Liekens, S., Neyts, J., Degréve, B., and De Clercq, E., (1997) The sulfonic acid polymers PAMPS [Poly(2-Acrylamido-2-Methyl-1-Propanesulfonoc Acid)] and related analogons are highly potent inhibitors of angiogenesis. Oncol. Res. 9, 173-181.
60. Deindl, E., Hoefer, I. E., Fernandez, B., Barancik, M., Heil, M., Strniskova, M., and Schaper, W. (2003) Involvement of the fibroblast growth factor system in adaptive and chemokine-induced arteriogenesis. Circ. Res. 92, 561-568.
61. Deindl, E., Fernandez, B., Ziegelhoeffer, T., and Schaper, W. (2001) Collateral artery growth is associated with an increased expression of Egr-1. FASEB J. 15, A1079.
62. Vogel, S., Kubin, T., Barancik, M., Deindl, E., von der Ahe, D., and Zimmermann, R. (2004) Signal transduction pathways in smooth muscle cells involved in arteriogenesis, in Arteriogenesis, (Schaper, W. and Schaper J., eds.) Kluwer Academic, Boston, pp. 213-232.
63. Schwachtgen, J. L., Houston, P., Campbell, C., Sukhatme, V., and Braddock, M. (1998) Fluid shear stress activation of egr-1 transcription in cultured human endothelial and epithelial cells is mediated via the extracellular signal-related kinase 1/2 mitogen-activated protein kinase pathway. J. Clin. Invest. 101, 2540-2549.
64. Collen, D. and Lijnen, H. R. (1991) Basic and clinical aspects of fibrinolysis and thrombolysis. Blood 78, 3114-3124.
65. Vassalli, J. D. (1994) The urokinase receptor. Fibrinolysis 8, 172-181.
66. Carmeliet, P. and Collen, D. (1996) Gene manipulation and transfer of the plasminogen system and coagulation system in mice. Semin. Thromb. Hemost. 22, 525-542.
67. Blasi, F., Conese, M., Moller, L. B., et al. (1994) The urokinase receptor: structure, regulation and inhibitor-mediated internalization. Fibrinolysis 8, 182-188.
68. Behrendt, N., Ronne, E., and Dano, K. (1995) The structure and function of the urokinase receptor, a membrane protein governing plasminogen activation on the cell surface. Biol. Chem. Hoppe Seyler 376, 269-279.
69. Gyetko, M. R., Todd, R. F. I., Wilkinson, C. C., and Sitrin, R. G. (1994) The urokinase receptor is required for human monocyte chemotaxis in vitro. J. Clin. Invest. 93, 1380-1387.
70. Sitrin, R. G., Todd, R. F., Albrecht, E., and Gyetko, M. R. (1996) The urokinase receptor (CD87) facilitates CD11b/CD18-mediated adhesion of human monocytes. J. Clin. Invest. 97, 1942-1951.
71. Waltz, D. A., Sailor, L. Z., and Chapman, H. A. (1993) Cytokines induce urokinase-dependent adhesion of human myeloid cells: a regulatory role for plasminogen activator inhibitors. J. Clin. Invest. 91, 1541-1552.
72. Rao, N. K., Shi, G. P., and Chapman, H. A. (1995) Urokinase receptor is a multifunctional protein: influence of receptor occupancy on macrophage gene expression. J. Clin. Invest. 96, 464-474.
73. Sitrin, R. G., Shollenberger, S. B., Stricter, R. M., and Gyetko, M. R. (1996) Endogenously produced urokinase amplifies tumor necrosis factor-secretion by THP-1 mononuclear phagocytes. J. Leukoc. Biol. 59, 302-311.
74. Cao, D., Mizukami, I. F., Garni-Wagner, B. A., et al. (1995) Human urokinase-type plasminogen activator primes neutrophils for superoxide anion release. J. Immunol. 154, 1817-1829.
75. Cai, W. J., Koltai, S., Kocsis, E., et al. (2003) Remodeling of the adventitia during coronary arteriogenesis. Am. J. Physiol. Heart Circ. Physiol. 284, H31-H40.
76. Deindl, E., Ziegelhoffer, T., Kanse, S. M., et al. (2003) Receptor-independent role of the urokinase-type plasminogen activator during arteriogenesis. FASEB J. 17, 1174-1176.
77. Carmeliet, P., Moons, L., Herbert, J.-M., et al. (1997) Urokinase-type but not tissue-type plasminogen activator mediates arterial neointima formation in mice. Circ. Res. 81, 829-839.
78. Syrovets, T., Rohwedder, A., Werchau, H., and Simmet, T. (1997) Plasmin triggers proinflammtory stimulation of human peripheral monocytes including cytokine expression. Naunyn Schmiedebergs Arch. Pharmacol. 312.
79. van Royen, N., Hoefer, I., Buschmann, I., et al. (2002) Exogenous application of transforming growth factor beta 1 stimulates arteriogenesis in the peripheral circulation. FASEB J. 16, 432-434.
80. Buschmann, I. R., Hoefer, I. E., van Royen, N., Katzer, E., Braun-Dulleaus, R., Heil, M., Kostin, S., Bode, C., and Schaper, W. (2001) GM-CSF: a strong arteriogenic factor acting by amplification of monocyte function. Atherosclerosis 159, 343-356.
81. Seiler, C., Pohl, T., Wustmann, K., Hutter, D., Nicolet, P. A., Windecker, S., Eberli, F. R., and Meier, B. (2001) Promotion of collateral growth by granulocyte-macrophage colony-stimulating factor in patients with coronary artery disease: a randomized, double-blind, placebo-controlled study. Circulation 23, 2012-2017.
82. Heil, M., Ziegelhoeffer, T., Wagner, S., Fernandez, B., Helisch, A., Martin, S., Tribulova, S., Kuziel, W. A., Bachmann, G., and Schaper, W. (2004) Collateral artery growth (arteriogenesis) after experimental arterial occlusion is impaired in mice lacking CC-chemokine receptor-2. Circ. Res. 94, 671-677.
83. Hoefer, I. E., van Royen, N., Rectenwald, J. E., et al. (2004) Arteriogenesis proceeds via ICAM-1/Mac-1-mediated mechanisms. Circ. Res. 94, 1179-1185.
84. van Royen, N., Voskuil, M., Hoefer, I., et al. (2004) CD44 regulates arteriogenesis in mice and is differentially expressed in patients with poor and good collateralization. Circulation 109, 1647-1652.
85. Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., Witzenbichler, B., Schatteman, G., and Isner, J. M. (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275, 964-967.
86. Shi, Q., Rafii, S., Wu, M. H., et al. (1998) Evidence for circulating bone marrow-derived endothelial cells. Blood 92, 362-367.
87. Orlic, D., Kajstura, J., Chimenti, S., et al. (2001) Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc. Natl. Acad. Sci. USA 98, 10,344-10,349.
88. Kalka, C., Masuda, H., Takahashi, T., et al. (2000) Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc. Natl. Acad. Sci. USA 97, 3422-3427.
89. Orlic, D., Kajstura, J., Chimenti, S., Bodine, D. M., Leri, A., and Anversa, P. (2001) Transplanted adult bone marrow cells repair myocardial infarcts in mice. Ann. NY Acad. Sci. 938, 221-229.
90. Kocher, A. A., Schuster, M. D., Szabolcs, M. J., et al. (2001) Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat. Med. 7, 430-436.
91. Shintani, S., Murohara, T., Ikeda, H., et al. (2001) Augmentation of postnatal neovascularization with autologous bone marrow transplantation. Circulation 103, 897-903.
92. Kawamoto, A., Gwon, H. C., Iwaguro, H., et al. (2001) Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103, 634-637.
93. Balsam, L. B., Wagers, A. J., Christensen, J. L., Kofidis, T., Weissman, I. L., and Robbins, R. C. (2004) Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428, 668-673.
94. Voswinckel, R., Ziegelhoeffer, T., Heil, M., et al. (2003) Circulating vascular progenitor cells do not contribute to compensatory lung growth. Circ. Res. 93, 372-379.
95. Beck, H., Voswinckel, R., Wagner, S., et al. (2003) Participation of bone marrow-derived cells in long-term repair processes after experimental stroke. J. Cereb. Blood Flow Metab. 23, 709-717.
96. Castro, R. F., Jackson, K. A., Goodell, M. A., Robertson, C. S., Liu, H., and Shine, H. D. (2002) Failure of bone marrow cells to transdifferentiate into neural cells in vivo. Science 297, 1299.
97. Wagers, A. J., Sherwood, R. I., Christensen, J. L., and Weissman, I. L. (2002) Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297, 2256-2259.
98. Rehman, J., Li, J., Orschell, C. M., and March, K. L. (2003) Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 107, 1164-1169.
99. Kinnaird, T., Stabile, E., Burnett, M. S., et al. (2004) Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 109, 1543-1549.
100. Boengler, K., Pipp, F., Fernandez, B., Ziegelhoeffer, T., Schaper, W., and Deindl, E. (2003) Arteriogenesis is associated with an induction of the cardiac ankyrin repeat protein (carp). Cardiovasc. Res. 59, 573-581.
101. Zimmermann, R., Boengler, K., Kampmann, A., et al. (2004) Expression profiling of growing arteries/hunting for new genes involved in arteriogenesis, in Arteriogenesis, (Schaper, W. and Schaper J., eds.) Kluwer Academic, Boston, pp. 233-252.