Arteriogenesis: Role of nitric oxide

Endothelium: Journal of Endothelial Cell Research

Volumn 10, Issue 4-5, 2003, Pages 207-216

  Prior, B M ^a   Lloyd, P G ^a   Ren, J ^a   Li, Z ^a   Yang, H T ^a   Laughlin, M H ^a,b,c   Terjung, R L ^a,b,c  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

Author keywords

Conductance; Exercise training; Fibroblast growth factor 2; Peripheral arterial occlusive disease; Shear stress; Vascular endothelial growth factor

Indexed keywords

ANGIOGENIC FACTOR; ARGININE; FIBROBLAST GROWTH FACTOR 2; HEPARIN; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; VASCULOTROPIN;

ADRENERGIC ACTIVITY; ANGIOGENESIS; BLOOD FLOW; CELL FUNCTION; COLLATERAL CIRCULATION; DIET SUPPLEMENTATION; DRUG EFFICACY; DRUG MEGADOSE; DRUG RESPONSE; ENDOTHELIUM CELL; EXERCISE; FEMORAL ARTERY; HUMAN; INTERMITTENT CLAUDICATION; NONHUMAN; OXYGEN TRANSPORT; PERIPHERAL ISCHEMIA; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PRIORITY JOURNAL; REVIEW; SHEAR STRESS; SIGNAL TRANSDUCTION; SIMULATION;

EID: 0346998272     PISSN: 10623329     EISSN: None     Source Type: Journal    
DOI: 10.1080/10623320390246388     Document Type: Review

References (73)

1. Alexander M.Y., Brosnan M.J., Hamilton C.A., Fennell J.P., Beattie E.C., Jardine E., Heistad D.D., and Dominiczak A.F. (2000) Gene transfer of endothelial nitric oxide synthase but not Cu/Zn superoxide dismutase restores nitric oxide availability in the SHRSP. Cardiovascular Research, 47, 609-617.
2. Asahara T., Bauters C., Zheng L.P., Takeshita S., Bunting S., Ferrara N., Symes J.F., and Isner J.M. (1995) Synergistic effect of vascular endothelial growth factor and basic fibroblast growth factor on angiogenesis in vivo. Circulation, 92, II365-II371.
3. Babaei S., Teichert-Kuliszewska K., Monge J.C., Mohamed F., Bendeck M.P., and Stewart D.J. (1998) Role of nitric oxide in the angiogenic response in vitro to basic fibroblast growth factor. Circulation Research, 82, 1007-1015.
4. Baffour R., Berman J., Garb J.L., Rhee S.W., Kaufman J., and Friedmann P. (1992) Enhanced angiogenesis and growth of collaterals by in vivo administration of recombinant basic fibroblast growth factor in a rabbit model of acute lower limb ischemia: Dose-response effect of basic fibroblast growth factor. Journal of Vascular Surgery, 16, 181-191.
5. Bauters C., Asahara T., Zheng L.P., Takeshita S., Bunting S., Ferrara N., Symes J.F., and Isner J.M. (1994) Physiological assessment of augmented vascularity induced by VEGF in ischemic rabbit hindlimb. American Journal of Physiology, 267, H1263-H1271.
6. Bauters C., Asahara T., Zheng L.P., Takeshita S., Bunting S., Ferrara N., Symes J.F., and Isner J.M. (1995a) Site-specific therapeutic angiogenesis after systemic administration of vascular endothelial growth factor. Journal of Vascular Surgery, 21, 314-325.
7. Bauters C., Asahara T., Zheng L.P., Takeshita S., Bunting S., Ferrara N., Symes J.F., and Isner J.M. (1995b) Recovery of disturbed endothelium-dependent flow in the collateral perfused rabbit ischemic hindlimb after administration of vascular endothelial growth factor [see comments]. Circulation, 91, 2802-2809.
8. Chleboun J.O., and Martins R.N. (1994) The development and enhancement of the collateral circulation in an animal model of lower limb ischemia. Australian and New Zealand Journal of Surgery, 64, 202-207.
9. Clarkson P., Adams M.R., Powe A.J., Donald A.E., McCredie R., Robinson J., McCarthy S.N., Keech A., Celermajer D.S., and Deanfield J.E. (1996) Oral L-arginine improves endothelium-dependent dilation in hypercholesterolemic young adults. Journal of Clinical Investigation, 97, 1989-1994.
10. Conrad M.C., Anderson J.L., and Garrett J.B. (1971) Chronic collateral growth after femoral artery occlusion in the dog. Journal of Applied Physiology, 31, 550-555.
11. Cuevas P., Carceller F., Ortega S., Zazo M., Nieto I., and Gimenez-Gallego G. (1991) Hypotensive activity of fibroblast growth factor. Science, 254, 1208-1210.
12. Ekelund U., and Mellander S. (1990) Role of endothelium-derived nitric oxide in the regulation of tonus in large-bore arterial resistance vessels, arterioles and veins in cat skeletal muscle. Acta Physiologica Scandinavia, 140, 301-309.
13. Fannon M., Forsten K.E., and Nugent M.A. (2000) Potentiation and inhibition of bFGF binding by heparin: A model for regulation of cellular response. Biochemistry, 39, 1434-1445.
14. Furchgott R.F., and Zawadzki J.V. (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288, 373-376.
15. Goligorsky M.S., Chen J., and Brodsky S. (2001) Workshop: Endothelial cell dysfunction leading to diabetic nephropathy: Focus on nitric oxide. Hypertension, 37, 744-748.
16. Gustafsson T., Puntschart A., Kaijser L., Jansson E., and Sundberg C.J. (1999) Exercise induced expression of angiogenesis-related transcription and growth factors in human skeletal muscle. American Journal of Physiology, 276, H679-H685.
17. Guzman R.J., Abe K., and Zarins C.K. (1997) Flow-induced arterial enlargement is inhibited by suppression of nitric oxide synthase activity in vivo. Surgery, 122, 273-279.
18. Herzog S., Sager H., Khmelevski E., Deylig A., and Ito W.D. (2002) Collateral arteries grow from preexisting anastomoses in the rat hindlimb. American Journal of Physiology Heart and Circulatory Physiology, 283, H2012-H2020.
19. Hester R.L., Eraslan A., and Saito Y. (1993) Differences in EDNO contribution to arteriolar diameters at rest and during functional dilation in striated muscle. American Journal of Physiology, 265, 146-151.
20. Hudlicka O., Brown M.D., and Silgram H. (2000) Inhibition of capillary growth in chronically stimulated rat muscles by N(G)-nitro-L-arginine, nitric oxide synthase inhibitor. Microvascular Research, 59, 45-51.
21. 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. American Journal of Physiology, 273, H1255-H1265.
22. Jasperse J.L., Woodman C.R., Price E.M., Hasser E.M., and Laughlin M.H. (1999) Hindlimb unweighting decreases ecNOS gene expression and endothelium-dependent dilation in rat soleus feed arteries. Journal of Applied Physiology, 87, 1476-1482.
23. John S., Delles C., Jacobi J., Schlaich M.P., Schneider M., Schmitz G., and Schmieder R.E. (2001) Rapid improvement of nitric oxide bioavailability after lipid-lowering therapy with cerivastatin within two weeks. Journal of the American College of Cardiology, 37, 1351-1358.
24. Korff T., and Augustin H.G. (1999) Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. Journal of Cell Science, 112, 3249-3258.
25. Ku D.D., Zaleski J.K., Liu S., and Brock T.A. (1993) Vascular endothelial growth factor induces EDRF-dependent relaxation in coronary arteries. American Journal of Physiology, 265, H586-H592.
26. Lash J.M., Nixon J.C., and Unthank J.L. (1995) Exercise training effects on collateral and microvascular resistances in rat model of arterial insufficiency. American Journal of Physiology, 268, H125-H137.
27. Laughlin M.H., and Armstrong R.B. (1982) Muscular blood flow distribution patterns as a function of running speed in rats. American Journal of Physiology, 243, H296-H306.
28. Laughlin M.H., Korthuis R.J., Duncker D.J., and Bache R.J. (1996) Control of blood flow to cardiac and skeletal muscle during exercise. In Handbook of Physiology: Exercise: Regulation and Integration of Multiple Systems (eds. L.B. Rowell and J.T. Shepherd). Oxford: Oxford University Press, pp. 705-769.
29. Laughlin M.H., Pollock J.S., Amann J.F., Hollis M.L., Woodman C.R., and Price E.M. (2001) Training induces nonuniform increases in eNOS content along the coronary arterial tree. Journal of Applied Physiology, 90, 501-510.
30. Lerman A., Burnett J.C.J., Higano S.T., McKinley L.J., and Holmes D.R.J. (1998) Long-term L-arginine supplementation improves small-vessel coronary endothelial function in humans. [comment]. Circulation, 97, 2123-2128.
31. Li J., Parovian C., Li J., Hampton T.G., Metais C., Tkachenko E., Sellke F.W., and Simons M. (2002) Modulation of microvascular signaling by heparan sulfate matrix: Studies in syndecan-4 transgenic mice. Microvascular Research, 64, 38-46.
32. Lloyd P.G., Yang H.T., and Terjung R.L. (2001) Arteriogenesis and angiogenesis in rat ischemic hindlimb: Role of nitric oxide. American Journal of Physiology, 281, H2528-H2538.
33. Mackie B.G., and Terjung R.L. (1983) Blood flow to different skeletal muscle fiber types during contraction. American Journal of Physiology, 245, H265-H275.
34. Masaki I., Yonemitsu Y., Yamashita A., Sata S., Tanii M., Komori K., Nakagawa K., Hou X., Nagai Y., Hasegawa M., Sugimachi K., and Sueishi K. (2002) Angiogenic gene therapy for experimental critical limb ischemia: Acceleration of limb loss by overexpression of vascular endothelial growth factor 165 but not of fibroblast growth factor-2. Circulation Research, 90, 966-973.
35. Morbidelli L., Chang C.H., Douglas J.G., Granger H.J., Ledda F., and Ziche M. (1996) Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. American Journal of Physiology, 270, H411-H415.
36. Murohara T., Asahara T., Silver M., Bauters C., Masuda H., Kalka C., Kearney M., Chen D., Symes J.F., Fishman M.C., Huang P.L., and Isner J.M. (1998) Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. Journal of Clinical Investigation, 101, 2567-2578.
37. Napoli C., and Ignarro L.J. (2001) Nitric oxide and atherosclerosis. Nitric Oxide, 5, 88-97.
38. Noiri E., Lee E., Testa J., Quigley J., Colflesh D., Keese C.R., Giaever I., and Goligorsky M.S. (1998) Podokinesis in endothelial cell migration: Role of nitric oxide. American Journal of Physiology, 274, C236-C244.
39. Nugent M.A., and Iozzo R.V. (2000) Fibroblast growth factor-2. International Journal of Biochemistry and Cell Biology, 32, 115-120.
40. Ozek C., Zhang F., Lineaweaver W.C., Chin B.T., Newlin L., Eiman T., and Buncke H.J. (1997) Arterialization of the venous system in a rat lower limb model. British Journal of Plastic Surgery, 50, 402-407.
41. Papapetropoulos A., Garcia-Cardena G., Madri J.A., and Sessa W.C. (1997) Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. Journal of Clinical Investigation, 100, 3131-3139.
42. Prior B.M., Lloyd P.G., Ren J., Li H., Yang H.T., and Terjung R.L. (2003) Exercise-induced collateral vascular remodeling and function in rats with femoral artery occlusion. FASEB Journal, 17, A501.
43. Rowell L.B., Saltin B., Kiens B., and Christensen N.J. (1986) Is peak quadriceps blood flow in humans even higher during exercise with hypoxemia? American Journal of Physiology, 251, H1038-H1044.
44. Schrage W.G., Woodman C.R., and Laughlin M.H. (2000) Hindlimb unweighting alters endothelium-dependent vasodilation and eNOS expression in soleus arterioles. Journal of Applied Physiology, 89, 1483-1490.
45. Sessa W.C., Pritchard K., Seyedi N., Wang J., and Hintze T.H. (1994) Chronic exercise in dogs increases coronary vascular nitric oxide production and endothelial cell nitric oxide synthase gene expression. Circulation Research, 74, 349-353.
46. Shizukuda Y., Tang S., Yokota R., and Ware J.A. (1999) Vascular endothelial growth factor induced endothelial cell migration and proliferation depend on a nitric oxide-mediated decrease in protein kinase Cdelta activity. Circulation Research, 85, 247-256.
47. Siani A., Pagno E., Iacone R., Iacoviello L., Scopacasa F., and Strazzullo P. (2000) Blood pressure and metabolic changes during dietary L-arginine supplementation in humans. American Journal of Hypertension, 13, 547-551.
48. Stavri G.T., Zachary I.C., Baskerville P.A., Martin J.F., and Erusalimsky J.D. (1995) Basic fibroblast growth factor upregulates the expression of vascular endothelial growth factor in vascular smooth muscle cells: Synergistic interaction with hypoxia. Circulation, 92, 11-14.
49. Takeshita S., Pu L.Q., Stein L.A., Sniderman A.D., Bunting S., Ferrara N., Isner J.M., and Symes J.F. (1994) Intramuscular administration of vascular endothelial growth factor induces dose-dependent collateral artery augmentation in a rabbit model of chronic limb ischemia. Circulation, 90, II228-II234.
50. Takeshita S., Weir L., Chen D., Zheng L.P., Riessen R., Bauters C., Symes J.F., Ferrara N., and Isner J.M. (1996) Therapeutic angiogenesis following arterial gene transfer of vascular endothelial growth factor in a rabbit model of hindlimb ischemia. Biochemical and Biophysical Research Communications, 227, 628-635.
51. Tronc F., Wassef M., Esposito B., Henrion D., Glagov S., and Tedgui A. (1996) Role of NO in flow-induced remodeling of the rabbit common carotid artery. Arteriosclerosis, Thrombosis and Vascular Biology, 16, 1256-1262.
52. Unthank J.L., Nixon J.C., and Dalsing M.C. (1994) Acute compensation to abrupt occlusion of rat femoral artery is prevented by NO synthase inhibitors. American Journal of Physiology, 267, H2523-H2530.
53. Unthank J.L., Nixon J.C., and Dalsing M.C. (1996) Nitric oxide maintains dilatation of immature and mature collaterals in rat hindlimb. Journal of Vascular Research, 33, 471-479.
54. Unthank J.L., Nixon J.C., and Lash J.M. (1995) Early adaptations in collateral and microvascular resistances after ligation of the rat femoral artery. Journal of Applied Physiology, 79, 73-82.
55. Van Der Zee R., Murohara T., Luo Z., Zollmann F., Passeri J., Lekutat C., and Isner J.M. (1997) Vascular endothelial growth factor/vascular permeability factor augments nitric oxide release from quiescent rabbit and human vascular endothelium. Circulation, 95, 1030-1037.
56. Wagner P.D. (2001) Skeletal muscle angiogenesis. A possible role for hypoxia. Advances in Experimental Medicine and Biology, 502, 21-38.
57. Walder C.E., Errett C.J., Bunting S., Lindquist P., Ogez J.R., Heinsohn H.G., Ferrara N., and Thomas G.R. (1996) Vascular endothelial growth factor augments muscle blood flow and function in a rabbit model of chronic hindlimb ischemia. Journal of Cardiovascular Pharmacology, 27, 91-98.
58. Williams I.L., Wheatcroft S.B., Shah A.M., and Kearney M.T. (2002) Obesity, atherosclerosis and the vascular endothelium: Mechanisms of reduced nitric oxide bioavailability in obese humans. [Review, 151 refs]. International Journal of Obesity and Related Metabolic Disorders, 26, 754-764.
59. Woodman C.R., Muller J.M., Laughlin M.H., and Price E.M. (1997) Induction of nitric oxide synthase mRNA in coronary resistance arteries isolated from exercise-trained pigs. American Journal of Physiology, 273, 2575-2579.
60. Wu H.M., Huang Q., Yuan Y., and Granger H.J. (1996) VEGF induces NO-dependent hyperpermeability in coronary venules. American Journal of Physiology, 271, H2735-H2739.
61. 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. Circulation Research, 79, 62-69.
62. Yang H.T., Dinn R.F., and Terjung R.L. (1990) Training increases muscle blood flow in rats with peripheral arterial insufficiency. Journal of Applied Physiology, 69, 1353-1359.
63. Yang H.T., and Feng Y. (2000) bFGF increases collateral blood flow in aged rats with femoral artery ligation. American Journal of Physiology, 278, H85-H93.
64. Yang H.T., Feng Y., Allen L.A., Protter A., and Terjung R.L. (2000) Efficacy and specificity of bFGF increased collateral flow in experimental peripheral arterial insufficiency. American Journal of Physiology, 278, H1966-H1973.
65. Yang H.T., Laughlin M.H., and Terjung R.L. (2000) Prior exercise training increases collateral-dependent blood flow in rats after acute femoral artery occlusion. American Journal of Physiology, 279, H1890-H1897.
66. Yang H.T., Ogilvie R.W., and Terjung R.L. (1994) Peripheral adaptations in trained aged rats with femoral artery stenosis. Circulation Research, 74, 235-243.
67. Yang H.T., Ogilvie R.W., and Terjung R.L. (1995) Heparin increases exercise-induced collateral blood flow in rats with femoral artery ligation. Circulation Research, 76, 448-456.
68. Yang H.T., Ogilvie R.W., and Terjung R.L. (1998) Exercise training enhances basic fibroblast growth factor-induced collateral blood flow. American Journal of Physiology, 274, H2053-H2061.
69. Yang H.T., Ren J., Laughlin M.H., and Terjung R.L. (2002) Prior exercise training produces NO-dependent increases in collateral blood flow after acute arterial occlusion. American Journal of Physiology, 282, H301-H310.
70. Yang H.T., and Terjung R.L. (1993) Angiotensin-converting enzyme inhibition increases collateral-dependent muscle blood flow. Journal of Applied Physiology, 75, 452-457.
71. Yang H.T., Yan Z., Abraham J.A., and Terjung R.L. (2001) VEGF(121)- and bFGF-induced increase in collateral blood flow requires normal nitric oxide production. American Journal of Physiology, 280, H1097-H1104.
72. Zhang Y., Li J., Selke F.W., and Simons M. (2003) Syndecan-4 modulates basic fibroblast growth factor 2 signaling in vivo. American Journal of Physiology, 284, H2078-H2082.
73. Ziche M., Morbidelli L., Choudhuri R., Zhang H.T., Donnini S., Granger H.J., and Bicknell R. (1997) Nitric oxide synthase lies downstream from vascular endothelial growth factor induced but not basic fibroblast growth factor-induced angiogenesis. Journal of Clinical Investigation, 99, 2625-2634.