Arteriogenesis: A focus on signal transduction cascades and transcription factors

Summary

In recent years intensive investigations have been performed to unravel the molecular mechanisms of collateral artery growth (arteriogenesis), a process designed by nature to compensate the devastating consequences of major arterial occlusions. Currently, a variety of gene products as well as signal transduction pathways involved in arteriogenesis have been identified. However, it is still not clear how the progression of cellular signals evoked by an increased blood flow and therefore mechanical stress proceeds. Literature research identified the transcription factors early growth response-1 (Egr-1) as well as serum response factor (SRF) and myocardin-related transcription factors (MRTFs) as liaisons connecting the key pathways of arteriogenesis, i.e.the Rho-kinase pathway and the MEK/ERK pathway, with each other as well as with downstream genes.

Keywords

Arteriogenesis - Rho-kinase - MEK/ERK - serum response factor - Egr-1

• References

• 1 Schaper W. Introduction. In: Arteriogenesis. Boston, Dordrecht, London: Kluwer Academic Publishers; 2004: 1-10.
• 2 Fulton WFM. The Coronary Arteries Springfield. Illinois: Charles C. Thomas; 1965
• 3 Schaper W, DeBrabander M, Lewi P. DNA-synthesis and mitoses in coronary collateral vessels of the dog. Circ Res 1971; 28: 671-679.
• 4 Arras M, Ito WD, Scholz D. et al. Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. J Clin Invest 1998; 101: 41-50.
• 5 Wolf C, Cai JW, Vosschulte R. et al. Vascular remodeling and altered protein expression during growth of coronary collateral arteries. J Mol Cell Cardiol 1998; 30: 2291-2305.
• 6 Lloyd PG, Yang HT, Terjung RL. Arteriogenesis and angiogenesis in rat ischemic hindlimb: role of nitric oxide. Am J Physiol Heart Circ Physiol 2001; 281: H2528-H2538.
• 7 Hoefer IE, van Royen N, Rectenwald JE. et al. Direct evidence for tumor necrosis factor-alpha signaling in arteriogenesis. Circulation 2002; 105: 1639-1641.
• 8 Busch HJ, Buschmann IR, Mies G, Bode C, Hossmann KA. Arteriogenesis in hypoperfused rat brain. J Cereb Blood Flow Metab 2003; 23: 621-628.
• 9 Pipp F, Boehm S, Cai WJ. et al. Elevated fluid shear stress enhances postocclusive collateral artery growth and gene expression in the pig hind limb. Arterioscler Thromb Vasc Biol 2004; 24: 1664-1668.
• 10 Deindl E, Zaruba MM, Brunner S. et al. G-CSF administration after myocardial infarction in mice attenuates late ischemic cardiomyopathy by enhanced arteriogenesis. FASEB J 2006; 7: 956-958.
• 11 Ito WD, Arras M, Scholz D. et al. Angiogenesis but not collateral growth is associated with ischemia after femoral artery occlusion. Am J Physiol 1997; 273: H1255-H1265.
• 12 Deindl E, Buschmann I, Hoefer IE. et al. Role of ischemia and hypoxia-inducible genes in arteriogenesis after femoral artery occlusion in the rabbit. Circ Res 2001; 89: 779-786.
• 13 Scholz D, Ziegelhoeffer T, Helisch A. et al. Contribution of arteriogenesis and angiogenesis to postocclusive hindlimb perfusion in mice. J Mol Cell Cardiol 2002; 34: 775-787.
• 14 Helisch A, Wagner S, Khan N. et al. Impact of mouse strain differences in innate hindlimb collateral vasculature. Arterioscler Thromb Vasc Biol 2006; 26: 520-526.
• 15 Deindl E, Helisch A, Scholz D. et al. Role of hypoxia/ ischemia/VEGF-A and strain differences. In: Arteriogenesis. Boston, Dordrecht, London: Kluwer Academic Publishers; 2004: 115-129. Thromb Vasc Biol 2004; 24: 1664-1668.
• 16 Resnick N, Einav S, Chen-Konak L. et al. Hemodynamic forces as a stimulus for arteriogenesis. Endothelium 2003; 10: 197-206.
• 17 Schaper W, Pipp F, Scholz D. et al. Physical forces and their translation into molecular mechanisms. In: Arteriogenesis. Boston, Dordrecht, London: Kluwer Academic Publishers; 2004
• 18 Kojda G, Hambrecht R. Molecular mechanisms of vascular adaptations to exercise. Physical activity as an effective antioxidant therapy? Cardiovasc Res 2005; 67: 187-197.
• 19 Eitenmuller I, Volger O, Kluge A. et al. The range of adaptation by collateral vessels after femoral artery occlusion. Circ Res 2006; 99: 656-662.
• 20 Boengler K, Pipp F, Broich K. et al. Identification of differentially expressed genes like cofilin2 in growing collateral arteries. Biochem Biophys Res Commun 2003; 17: 751-756.
• 21 Galbraith CG, Skalak R, Chien S. Shear stress induces spatial reorganization of the endothelial cell cytoskeleton. Cell Motil Cytoskel 1998; 40: 317-330.
• 22 Arber S, Barbayannis FA, Hanser H. et al. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 1998; 393: 805-809.
• 23 Toshima J, Toshima JY, Amano T. et al. Cofilin Phosphorylation by protein kinase testicular protein ki- nase 1 and its role in integrin-mediated actin reorganization and focal adhesion formation. Mol Biol Cell 2001; 12: 1131-1145.
• 24 Arai A, Spencer JA, Olson EN. STARS, a striated muscle activator of Rho signaling and serum response factor-dependent transcription. J Biol Chem 2002; 277: 24453-24459.
• 25 Troidl K, Troidl C, Eitenmueller I. et al. Intra-collateral adenoviral gene transfer of actin-binding Rho activating protein (ABRA) improves collateral conductance. Eur Heart J 2006; 27: 453 (Abstr).
• 26 Kuwahara K, Barrientos T, Pipes GC. et al. Musclespecific signaling mechanism that links actin dynamics to serum response factor. Mol Cell Biol 2005; 25: 3173-3181.
• 27 Sukhatme VP, Cao X, Chang LC. et al. A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization. Cell 1988; 53: 37-43.
• 28 Gashler A, Sukhatme VP. Early growth response protein 1 (Egr-1): prototype of a zinc-finger family of transcription factors. Prog Nucleic Acid Res Mol Biol 1995; 50: 191-224.
• 29 Guillemot L, Levy A, Raymondjean M. et al. Angiotensin II-induced transcriptional activation of the cyclin D1 gene is mediated by Egr-1 in CHO-AT(1A) cells. Biol Chem 2001; 276: 39394-39403.
• 30 Khachigian LM, Linder V, Williams AM. et al. Egr-1 induced endothelial gene expression: a common theme in vascular injury. Science 1996; 271: 1427-1431.
• 31 Khachigian LM, Collins T. Inducible expression of Egr-1-dependent genes. A paradigm of transcriptional activation in vascular endothelium. Circ Res 1997; 81: 457-461.
• 32 Silverman ES, Collins T. Pathways of Egr-1 mediated gene transcription in vascular biology. Am J Pathol 1999; 154: 665-670.
• 33 Fahmy RG, Khachigian LM. Antisense egr-1 RNA driven by the CMV promoter is an inhibitor of vascular smooth muscle cell proliferation and regrowth after injury. J Cell Biochem 2002; 84: 575-582.
• 34 Fahmy RG, Dass CR, Sun LQ. et al. Transcription factor Egr-1 supports FGF-dependent angiogenesis during neovascularization and tumor growth. Nat Med 2003; 8: 1026-1032.
• 35 Baron V, De Gregorio G, Krones-Herzig A. et al. Inhibition of Egr-1 expression reverses transformation of prostate cancer cells in vitro and in vivo. Oncogene 2003; 22: 4194-4204.
• 36 Deindl E, Ziegelhoeffer T, Vogel S. et al. Arteriogenesis is associated with an increased expression of the zink-finger transcription factor egr-1. Abstract book XIIth International Vascular Biology Meeting 2002; Abstract P51.
• 37 Sarateanu CS, Retuerto MA, Beckmann JT. et al. An Egr-1 master switch for arteriogenesis: studies in Egr-1 homozygous negative and wild-type animals. J Thorac Cardiovasc Surg 2006; 131: 138-145.
• 38 Lee YS, Jang HS, Kim JM. et al. Adenoviral-mediated delivery of early growth response factor-1 gene increases tissue perfusion in a murine model of hindlimb ischemia. Mol Ther 2005; 12: 328-336.
• 39 Day FL, Rafty LA, Chesterman CN. et al. Angiotensin II (ATII)-inducible platelet-derived growth factor A-chain gene expression is p42/44 extracellular signal- regulated kinase-1/2 and Egr-1-dependent and mediated via the ATII type 1 but not type 2 receptor. Induction by ATII antagonized by nitric oxide. J Biol Chem 1999; 274: 23726-23733.
• 40 Vogel S, Kubin T, von der Ahe D. et al. MEK hyperphosphorylation coincides with cell cycle shut down of cultured smooth muscle cells. J Cell Physiol 2006; 206: 25-34.
• 41 Allen LA, Terjung RL, Yang HT. Exogenous basic fibroblast growth factor increases collateral blood flow in female rats with femoral artery occlusion. J Cardiovasc Pharmacol 2006; 47: 146-154.
• 42 Horvath KA, Doukas J, Lu CY. et al. Myocardial function recovery after fibroblast growth factor 2 gene therapy as assessed by echocardiography and magnetic resonance imaging. Ann Thorac Surgery 2002; 74: 481-486.
• 43 Rajanayagam MA, Shou M, Thirumurti V. et al. Intracoronary basic fibroblast growth factor enhances myocardial collateral perfusion in dog. J Am Coll Cardiol 2000; 35: 519-526.
• 44 Unger EF, Banai S, Shou M. et al. Basic fibroblast growth factor enhances myocardial collateral flow in a canine model. Am J Physiol 1994; 266: H1588-H1595.
• 45 Yang HT, Deschenes MR, Ogilvie RW. et al. Basic fibroblast growth factor increases collateral blood flow in rats with femoral arterial ligation. Circ Res 1996; 79: 62-69.
• 46 Yang HT, Feng Y. bFGF increases collateral blood flow in aged rats with femoral artery ligation. Am J Physiol Heart Circ Physiol 2000; 278: H85-H93.
• 47 Sarker KP, Lee KY. L6 myoblast differentiation is modulated by Cdk5 via the PI3K-AKT-p70S6K signaling pathway. Oncogene 2004; 23: 6064-6070.
• 48 Boengler K, Pipp F, Fernandez B. et al. Arteriogenesis is associated with an induction of the cardiac ankyrin repeat protein (carp). Cardiovasc Res 2003; 59: 573-581.
• 49 Kanai H, Tanaka T, Aihara Y. et al. Transforming growth factor-beta/Smads signaling induces transcription of the cell type-restricted ankyrin repeat protein CARP gene through CAGA motif in vascular smooth muscle cells. Circ Res 2001; 88: 30-39.
• 50 Fan L, Sebe A, Peterfi Z. et al. Cell contact-dependent regulation of epithelial myofibroblast transition via the Rho-Rho kinase phospho-myosin pathway. Mol Biol Cell 2007; 18: 1083-1097.
• 51 van Royen N, Hoefer I, Buschmann I. et al. Exogenous application of transforming growth factor beta 1 stimulates arteriogenesis in the peripheral circulation. FASEB J 2002; 16: 432-434.
• 52 Thannickal VJ, Aldweib KD, Rajan T. et al. Upregulated expression of fibroblast growth factor (FGF) receptors by transforming growth factor-beta1 (TGFbeta1) mediates enhanced mitogenic responses to FGFs in cultured human lung fibroblasts. Biochem Biophys Res Commun 1998; 251: 437-441.
• 53 Deindl E, Hoefer IE, Fernandez B. et al. Involvement of the fibroblast growth factor system in adaptive and chemokine-induced arteriogenesis. Circ Res 2003; 92: 561-568.
• 54 Collen D, Lijnen HR. Basic and clinical aspects of fibrinolysis and thrombolysis. Blood 1991; 78: 3114-3124.
• 55 Syrovets T, Tippler B, Rieks M. et al. Plasmin Is a potent and specific chemoattractant for human peripheral monocytes acting via a cyclic guanosine monophosphate- dependent pathway. Blood 1997; 89: 4574-4583.
• 56 Gyetko MR, Todd RFI, Wilkinson CC. et al. The urokinase receptor is required for human monocyte chemotaxis in vitro. J Clin Invest 1994; 93: 1380-1387.
• 57 Sitrin RG, Todd RF, Albrecht E. et al. The urokinase receptor (CD87) facilitates CD11b/CD18-mediated adhesion of human monocytes. J Clin Invest 1996; 97: 1942-1951.
• 58 Waltz DA, Sailor LZ, Chapman HA. Cytokines induce urokinase-dependent adhesion of human myeloid cells. a regulatory role for plasminogen activator inhibitors. J Clin Invest 1993; 91: 1541-1552.
• 59 Rao NK, Shi GP, Chapman HA. Urokinase receptor is a multifunctional protein: influence of receptor occupancy on macrophage gene expression. J Clin Invest 1995; 96: 464-474.
• 60 Cai W, Vosschulte R, Afsah-Hedjri A. et al. Altered balance between extracellular proteolysis and antiproteolysis is associated with adaptive coronary arteriogenesis. J Mol Cell Cardiol 2000; 32: 997-1011.
• 61 Deindl E, Ziegelhoffer T, Kanse SM. et al. Receptor- independent role of the urokinase-type plasminogen activator during arteriogenesis. FASEB J 2003; 17: 1174-1176.
• 62 Scholz D, Ito W, Fleming I. et al. Ultrastructure and molecular histology of rabbit hindlimb collateral artery growth (arteriogenesis). Virchows Arch 2000; 436: 257-270.
• 63 Cernuda-Morollon E, Ridley AJ. Rho GTPases and leukocyte adhesion receptor expression and function in endothelial cells. Circ Res 2006; 98: 757-767.
• 64 Kim JS, Kim JG, Moon MY. et al. Transforming growth factor-beta1 regulates macrophage migration via RhoA. Blood 2006; 108: 1821-1829.
• 65 Busse R, Fleming I. Regulation of endothelium-derived vasoactive autacoid production by hemodynamic forces. Trends Pharmacol Sci 2003; 24: 24-29.
• 66 Hynes RO. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992; 102: 7-17.
• 67 Hynes RO, Bader BL, Hodivala-Dilke K. Integrins in vascular development. Braz J Med Biol Res 1999; 32: 501-510.
• 68 Fernandez B, Broich K. Cell-cell and cell-matrix interactions. In: Arteriogenesis. Boston, Dordrecht, London: Kluwer Academic Publishers; 2004: 173-189.
• 69 Grande JP. Role of transforming growth factor-beta in tissue injury and repair. Proc Soc Exp Biol Med 1997; 4: 27-40.