Angiogenesis in peripheral artery disease: An emerging therapy targeting skeletal muscle

Angiogenesis: Insights from a Systematic Overview

Volumn , Issue , 2013, Pages 99-134

  Duscha, Brian D ^a   Robbins, Jennifer L ^a   Kontos, Christopher D ^a   Kraus, William E ^a   Annex, Brian H ^b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84887848754     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (196)

1. Hirsch AT, Criqui MH, Treat-Jacobson D. Peripheral arterial disease detection, awareness, and treatment in primary care. JAMA. Sep 19 2001;286(11):1317-1324.
2. Hirsch AT, Haskal ZJ, Hertzer NR. ACC/AHA 2005 Practice Guidelines for the management of patients with peripheral arterial disease (lower extremity, renal, mesenteric, and abdominal aortic): a collaborative report from the American Association for Vascular Surgery/Society for Vascular Surgery, Society for Cardiovascular Angiography and Interventions, Society for Vascular Medicine and Biology, Society of Interventional Radiology, and the ACC/AHA Task Force on Practice Guidelines (Writing Committee to Develop Guidelines for the Management of Patients With Peripheral Arterial Disease): endorsed by the American Association of Cardiovascular and Pulmonary Rehabilitation; National Heart, Lung, and Blood Institute; Society for Vascular Nursing; Trans Atlantic Inter-Society Consensus; and Vascular Disease Foundation. Circulation. Mar 21 2006;113(11):e463-654.
3. McDermott MM, Liu K, Greenland P. Functional decline in peripheral arterial disease: associations with the ankle brachial index and leg symptoms. JAMA. Jul 28 2004;292(4):453-461.
4. Olsen PS, Gustafsen J, Rasmussen L, Lorentzen JE. Long-term results after arterial surgery for arteriosclerosis of the lower limbs in young adults. Eur J Vasc Surg. Feb 1988;2(1):15-18.
5. Hiatt WR, Regensteiner JG, Hargarten ME, Wolfel EE, Brass EP. Benefit of exercise conditioning for patients with peripheral arterial disease. Circulation. Feb 1990;81(2):602-609.
6. Goodney PP, Beck AW, Nagle J, Welch HG, Zwolak RM. National trends in lower extremity bypass surgery, endovascular interventions, and major amputations. J Vasc Surg. Jul 2009;50(1):54-60.
7. Stewart KJ, Hiatt WR, Regensteiner JG, Hirsch AT. Exercise training for claudication. NEngl J Med. Dec 12 2002;347(24):1941-1951.
8. Caro J, Migliaccio-Walle K, Ishak KJ, Proskorovsky I. The morbidity and mortality following a diagnosis of peripheral arterial disease: long-term follow-up of a large database. BMC Cardiovasc Disord. 2005;5:14.
9. Gillum RF. Peripheral arterial occlusive disease of the extremities in the United States: hospitalization and mortality. Am Heart J. Dec 1990;120(6 Pt 1):1414-1418.
10. Landry GJ. Functional outcome of critical limb ischemia. J Vasc Surg. Jun 2007;45 Suppl A:A141-148.
11. Hiatt WR. Medical treatment of peripheral arterial disease and claudication. N Engl J Med. May 24 2001;344(21):1608-1621.
12. Mohler ER, 3rd, Hiatt WR, Creager MA. Cholesterol reduction with atorvastatin improves walking distance in patients with peripheral arterial disease. Circulation. Sep 23 2003;108(12):1481-1486.
13. Hiatt WR. Pharmacologic therapy for peripheral arterial disease and claudication. J Vasc Surg. Dec 2002;36(6):1283-1291.
14. Regensteiner JG, Hiatt WR. Current medical therapies for patients with peripheral arterial disease: a critical review. Am J Med. Jan 2002;112(1):49-57.
15. Beebe HG, Dawson DL, Cutler BS. A new pharmacological treatment for intermittent claudication: results of a randomized, multicenter trial. Arch Intern Med. Sep 27 1999;159(17):2041-2050.
16. Money SR, Herd JA, Isaacsohn JL. Effect of cilostazol on walking distances in patients with intermittent claudication caused by peripheral vascular disease. J Vasc Surg. Feb 1998;27(2):267-274; discussion 274-265.
17. Bhatt DL, Steg PG, Ohman EM. International prevalence, recognition, and treatment of cardiovascular risk factors in outpatients with atherothrombosis. JAMA. Jan 11 2006;295(2):180-189.
18. Valentine RJ, Myers SI, Inman MH, Roberts JR, Clagett GP. Late outcome of amputees with premature atherosclerosis. Surgery. May 1996;119(5):487-493.
19. Ouriel K. Peripheral arterial disease. Lancet. Oct 13 2001;358(9289):1257-1264.
20. Albers M, Romiti M, Brochado-Neto FC, De Luccia N, Pereira CA. Meta-analysis of popliteal-to-distal vein bypass grafts for critical ischemia. J Vasc Surg. Mar 2006;43(3):498-503.
21. Connelly J, Airey M, Chell S. Variation in clinical decision making is a partial explanation for geographical variation in lower extremity amputation rates. Br J Surg. Apr 2001;88(4):529-535.
22. McDermott MM, Hahn EA, Greenland P. Atherosclerotic risk factor reduction in peripheral arterial diseasea: results of a national physician survey. J Gen Intern Med. Dec 2002;17(12):895-904.
23. Regensteiner JG. Exercise in the treatment of claudication: assessment and treatment of functional impairment. Vasc Med. 1997;2(3):238-242.
24. Gardner AW, Poehlman ET. Exercise rehabilitation programs for the treatment of claudication pain. A meta-analysis. JAMA. Sep 27 1995;274(12):975-980.
25. Thom T, Haase N, Rosamond W. Heart disease and stroke statistics--2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. Feb 14 2006;113(6):e85-151.
26. Ostchega Y, Paulose-Ram R, Dillon CF, Gu Q, Hughes JP. Prevalence of peripheral arterial disease and risk factors in persons aged 60 and older: data from the National Health and Nutrition Examination Survey 1999-2004. J Am Geriatr Soc. Apr 2007;55(4):583-589.
27. Hirsch AT, Hartman L, Town RJ, Virnig BA. National health care costs of peripheral arterial disease in the Medicare population. Vasc Med. Aug 2008;13(3):209-215.
28. Krogh A. The number and distribution of capillaries in muscles with calculations of the oxygen pressure head necessary for supplying the tissue. J Physiol. May 20 1919;52(6):409-415.
29. Krogh A. The supply of oxygen to the tissues and the regulation of the capillary circulation. J Physiol. May 20 1919;52(6):457-474.
30. Bergstrom J. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest. Nov 1975;35(7):609-616.
31. Egginton S. Invited review: activity-induced angiogenesis. Pflugers Arch. Mar 2009;457(5):963-977.
32. Milkiewicz M, Ispanovic E, Doyle JL, Haas TL. Regulators of angiogenesis and strategies for their therapeutic manipulation. Int J Biochem Cell Biol. Mar 2006;38(3):333-357.
33. Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med. Jun 2003;9(6):677-684.
34. Saltin B, Kiens B, Savard G, Pedersen PK. Role of hemoglobin and capillarization for oxygen delivery and extraction in muscular exercise. Acta Physiol Scand Suppl. 1986;556:21-32.
35. Adair TH, Gay WJ, Montani JP. Growth regulation of the vascular system: evidence for a metabolic hypothesis. Am J Physiol. Sep 1990;259(3 Pt 2):R393-404.
36. Hepple RT. Skeletal muscle: microcirculatory adaptation to metabolic demand. Med Sci Sports Exerc. Jan 2000;32(1):117-123.
37. Hoppeler H, Kayar SR. Capillarity and oxidative capacity of muscles. News Physiol Sci. 1988;3:113-116.
38. Mathieu-Costello O, Hepple RT. Muscle structural capacity for oxygen flux from capillary to fiber mitochondria. Exerc Sport Sci Rev. Apr 2002;30(2):80-84.
39. Brodal P, Ingjer F, Hermansen L. Capillary supply of skeletal muscle fibers in untrained and endurance-trained men. Am J Physiol. Jun 1977;232(6):H705-712.
40. Andersen P, Henriksson J. Capillary supply of the quadriceps femoris muscle of man: adaptive response to exercise. J Physiol. Sep 1977;270(3):677-690.
41. Hoppeler H, Howald H, Conley K. Endurance training in humans: aerobic capacity and structure of skeletal muscle. JAppl Physiol. Aug 1985;59(2):320-327.
42. Rosler K, Hoppeler H, Conley KE, Claassen H, Gehr P, Howald H. Transfer effects in endurance exercise. Adaptations in trained and untrained muscles. Eur J Appl Physiol Occup Physiol. 1985;54(4):355-362.
43. Carpenter S, Karpati G. Necrosis of capillaries in denervation atrophy of human skeletal muscle. Muscle Nerve. Mar 1982;5(3):250-254.
44. Jozsa L, Balint J, Reffy A, Jarvinen M, Kvist M. Capillary density of tenotomized skeletal muscles. II. Observations on human muscles after spontaneous rupture of tendon. Eur J Appl Physiol Occup Physiol. 1980;44(2): 183-188.
45. Ingjer F. Maximal aerobic power related to the capillary supply of the quadriceps femoris muscle in man. Acta Physiol Scand. Oct 1978;104(2):238-240.
46. Ingjer F. Effects of endurance training on muscle fibre ATP-ase activity, capillary supply and mitochondrial content in man. J Physiol. Sep 1979;294:419-432.
47. Ingjer F, Brodal P. Capillary supply of skeletal muscle fibers in untrained and endurance-trained women. Eur J Appl Physiol Occup Physiol. May 30 1978;38(4):291-299.
48. Duscha BD, Annex BH, Johnson JL, Huffman K, Houmard J, Kraus WE. Exercise Dose Response in Muscle. Int J Sports Med. Jan 19 2012.
49. Hepple RT, Mackinnon SL, Goodman JM, Thomas SG, Plyley MJ. Resistance and aerobic training in older men: effects on VO2peak and the capillary supply to skeletal muscle. J Appl Physiol. Apr 1997;82(4):1305-1310.
50. Klausen K, Andersen LB, Pelle I. Adaptive changes in work capacity, skeletal muscle capillarization and enzyme levels during training and detraining. Acta Physiol Scand. Sep 1981;113(1):9-16.
51. Murias JM, Kowalchuk JM, Ritchie D, Hepple RT, Doherty TJ, Paterson DH. Adaptations in capillarization and citrate synthase activity in response to endurance training in older and young men. J Gerontol A Biol Sci Med Sci. Sep 2011;66(9):957-964.
52. Hermansen L, Wachtlova M. Capillary density of skeletal muscle in well-trained and untrained men. J Appl Physiol. Jun 1971;30(6):860-863.
53. Kayar SR, Hoppeler H, Howald H, Claassen H, Oberholzer F. Acute effects of endurance exercise on mitochondrial distribution and skeletal muscle morphology. Eur J Appl Physiol Occup Physiol. 1986;54(6):578-584.
54. Oelz O, Howald H, Di Prampero PE. Physiological profile of world-class high-altitude climbers. J Appl Physiol. May 1986;60(5):1734-1742.
55. Coggan AR, Spina RJ, King DS. Skeletal muscle adaptations to endurance training in 60-to 70-yr-old men and women. J Appl Physiol. May 1992;72(5):1780-1786.
56. Coggan AR, Spina RJ, Rogers MA. Histochemical and enzymatic characteristics of skeletal muscle in master athletes. J Appl Physiol. May 1990;68(5):1896-1901.
57. Gavin TP, Ruster RS, Carrithers JA. No difference in the skeletal muscle angiogenic response to aerobic exercise training between young and aged men. J Physiol. Nov 15 2007;585(Pt 1):231-239.
58. Duscha BD, Kraus WE, Keteyian SJ. Capillary density of skeletal muscle: a contributing mechanism for exercise intolerance in class II-III chronic heart failure independent of other peripheral alterations. J Am Coll Cardiol. Jun 1999;33(7):1956-1963.
59. Jobin J, Maltais F, Doyon JF. Chronic obstructive pulmonary disease: capillarity and fiber-type characteristics of skeletal muscle. J Cardiopulm Rehabil. Nov-Dec 1998;18(6):432-437.
60. Bassett DR, Jr. Skeletal muscle characteristics: relationships to cardiovascular risk factors. Med Sci Sports Exerc. Aug 1994;26(8):957-966.
61. Makitie J. Skeletal muscle capillaries in intermittent claudication. Arch Pathol Lab Med. Sep 1977;101(9):500-503.
62. Askew CD, Green S, Walker PJ. Skeletal muscle phenotype is associated with exercise tolerance in patients with peripheral arterial disease. J Vasc Surg. May 2005;41(5):802-807.
63. Clyne CA, Weller RO, Bradley WG, Silber DI, O'Donnell TF, Jr., Callow AD. Ultrastructural and capillary adaptation of gastrocnemius muscle to occlusive peripheral vascular disease. Surgery. Aug 1982;92(2):434-440.
64. Hedberg B, Angquist KA, Henriksson-Larsen K, Sjostrom M. Fibre loss and distribution in skeletal muscle from patients with severe peripheral arterial insufficiency. Eur J Vasc Surg. Aug 1989;3(4):315-322.
65. McGuigan MR, Bronks R, Newton RU. Muscle fiber characteristics in patients with peripheral arterial disease. Med Sci Sports Exerc. Dec 2001;33(12):2016-2021.
66. Regensteiner JG, Wolfel EE, Brass EP. Chronic changes in skeletal muscle histology and function in peripheral arterial disease. Circulation. Feb 1993;87(2):413-421.
67. Jansson E, Johansson J, Sylven C, Kaijser L. Calf muscle adaptation in intermittent claudication. Side-differences in muscle metabolic characteristics in patients with unilateral arterial disease. Clin Physiol. Feb 1988;8(1):17-29.
68. Lexell J, Taylor C, Sjostrom M. Analysis of sampling errors in biopsy techniques using data from whole muscle cross sections. J Appl Physiol. Oct 1985;59(4): 1228-1235.
69. McCall GE, Byrnes WC, Dickinson AL, Fleck SJ. Sample size required for the accurate determination of fiber area and capillarity of human skeletal muscle. Can J Appl Physiol. Dec 1998;23(6):594-599.
70. Steinacker JM, Opitz-Gress A, Baur S. Expression of myosin heavy chain isoforms in skeletal muscle of patients with peripheral arterial occlusive disease. J Vasc Surg. Mar 2000;31(3):443-449.
71. Robbins JL, Jones WS, Duscha BD. Relationship between leg muscle capillary density and peak hyperemic blood flow with endurance capacity in peripheral artery disease. J Appl Physiol. Jul 2011;111(1):81-86.
72. Makitie J, Teravainen H. Histochemical changes in striated muscle in patients with intermittent claudication. Arch Pathol Lab Med. Dec 1977;101(12):658-663.
73. Teravainen H, Makitie J. Striated muscle ultrastructure in intermittent claudication. Arch Pathol Lab Med. May 1977;101(5):230-235.
74. Saltin B, Henriksson J, Nygaard E, Andersen P, Jansson E. Fiber types and metabolic potentials of skeletal muscles in sedentary man and endurance runners. Ann N Y Acad Sci. 1977;301:3-29.
75. Saltin B. The interplay between peripheral and central factors in the adaptive response to exercise and training. Ann N Y Acad Sci. 1977;301:224-231.
76. Saltin B, Strange S. Maximal oxygen uptake: "old" and "new" arguments for a cardiovascular limitation. Med Sci Sports Exerc. Jan 1992;24(1):30-37.
77. Saltin B, Calbet JA. Point: in health and in a normoxic environment, VO2 max is limited primarily by cardiac output and locomotor muscle blood flow. J Appl Physiol. Feb 2006;100(2):744-745.
78. Gonzalez-Alonso J, Calbet JA. Reductions in systemic and skeletal muscle blood flow and oxygen delivery limit maximal aerobic capacity in humans. Circulation. Feb 18 2003;107(6):824-830.
79. Aunola S, Marniemi J, Alanen E, Mantyla M, Saraste M, Rusko H. Muscle metabolic profile and oxygen transport capacity as determinants of aerobic and anaerobic thresholds. Eur J Appl Physiol Occup Physiol. 1988;57(6):726-734.
80. Aunola S, Rusko H. Aerobic and anaerobic thresholds determined from venous lactate or from ventilation and gas exchange in relation to muscle fiber composition. Int J Sports Med. Jun 1986;7(3):161-166.
81. Gollnick PD, Saltin B. Significance of skeletal muscle oxidative enzyme enhancement with endurance training. Clin Physiol. Feb 1982;2(1):1-12.
82. Robbins JL, Duscha BD, Bensimhon DR. A sex-specific relationship between capillary density and anaerobic threshold. J Appl Physiol. Apr 2009;106(4):1181-1186.
83. Saltin B, Rowell LB. Functional adaptations to physical activity and inactivity. Fed Proc. Apr 1980;39(5):1506-1513.
84. Henriksson J, Nygaard E, Andersson J, Eklof B. Enzyme activities, fibre types and capillarization in calf muscles of patients with intermittent claudication. Scand J Clin Lab Invest. Jun 1980;40(4):361-369.
85. Hammarsten J, Bylund-Fellenius AC, Holm J, Schersten T, Krotkiewski M. Capillary supply and muscle fibre types in patients with intermittent claudication: relationships between morphology and metabolism. Eur J Clin Invest. Aug 1980;10(4):301-305.
86. Clyne CA, Mears H, Weller RO, O'Donnell TF. Calf muscle adaptation to peripheral vascular disease. CardiovascRes. Aug 1985;19(8):507-512.
87. Belch JJ, Topol EJ, Agnelli G. Critical issues in peripheral arterial disease detection and management: a call to action. Arch Intern Med. Apr 28 2003;163(8):884-892.
88. Gardner AW, Skinner JS, Cantwell BW, Smith LK. Prediction of claudication pain from clinical measurements obtained at rest. Med Sci Sports Exerc. Feb 1992;24 (2):163-170.
89. Pernow B, Zetterquist S. Metabolic evaluation of the leg blood flow in claudicating patients with arterial obstructions at different levels. Scand J Clin Lab Invest. 1968;21(3):277-287.
90. Szuba A, Oka RK, Harada R, Cooke JP. Limb hemodynamics are not predictive of functional capacity in patients with PAD. Vasc Med. Nov 2006;11(3): 155-163.
91. Bradbury AW. Bypass versus Angioplasty in Severe Ischaemia of the Leg (BASIL) trial in perspective. J Vasc Surg. May 2010;51(5 Suppl):1S-4S.
92. Bosch JL, van der Graaf Y, Hunink MG. Health-related quality of life after angioplasty and stent placement in patients with iliac artery occlusive disease: results of a randomized controlled clinical trial. The Dutch Iliac Stent Trial Study Group. Circulation. Jun 22 1999;99(24):3155-3160.
93. Gardner AW, Killewich LA. Lack of functional benefits following infrainguinal bypass in peripheral arterial occlusive disease patients. Vasc Med. 2001;6(1):9-14.
94. Lundgren F, Dahllof AG, Lundholm K, Schersten T, Volkmann R. Intermittent claudication--surgical reconstruction or physical training? A prospective randomized trial of treatment efficiency. Ann Surg. Mar 1989;209(3):346-355.
95. Whyman MR, Fowkes FG, Kerracher EM. Is intermittent claudication improved by percutaneous transluminal angioplasty? A randomized controlled trial. J Vasc Surg. Oct 1997;26(4):551-557.
96. Creasy TS, McMillan PJ, Fletcher EW, Collin J, Morris PJ. Is percutaneous transluminal angioplasty better than exercise for claudication? Preliminary results from a prospective randomised trial. Eur J Vasc Surg. Apr 1990;4(2):135-140.
97. Isbell DC, Epstein FH, Zhong X. Calf muscle perfusion at peak exercise in peripheral arterial disease: measurement by first-pass contrast-enhanced magnetic resonance imaging. J Magn Reson Imaging. May 2007;25(5):1013-1020.
98. West AM, Anderson JD, Epstein FH. Improvement in calf muscle energetics after percutaneous intervention in patients with symptomatic peripheral arterial disease as measured with MRI. J Vasc Surg. 2012;in press.
99. Leng GC, Fowler B, Ernst E. Exercise for intermittent claudication. Cochrane Database Syst Rev. 2000(2):CD000990.
100. Larsen OA, Lassen NA. Effect of daily muscular exercise in patients with intermittent claudication. Lancet. Nov 19 1966;2(7473):1093-1096.
101. Skinner JS, Strandness DE, Jr. Exercise and intermittent claudication.II. Effect of physical training. Circulation. Jul 1967;36(1):23-29.
102. Parmenter BJ, Raymond J, Fiatarone Singh MA. The effect of exercise on haemodynamics in intermittent claudication: a systematic review of randomized controlled trials. Sports Med. May 1 2010;40(5):433-447.
103. Wang J, Zhou S, Bronks R, Graham J, Myers S. Effects of supervised treadmill walking training on calf muscle capillarization in patients with intermittent claudication. Angiology. Feb-Mar 2009;60(1):36-41.
104. Duscha BD, Robbins JL, Jones WS. Angiogenesis in skeletal muscle precede improvements in peak oxygen uptake in peripheral artery disease patients. Arterioscler Thromb Vasc Biol. Nov 2011;31(11):2742-2748.
105. Augustin HG, Koh GY, Thurston G, Alitalo K. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol. Mar 2009;10(3):165-177.
106. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. May 19 2011;473(7347):298-307.
107. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev. Aug 2004;25(4):581-611.
108. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling-in control of vascular function. Nat Rev Mol Cell Biol. May 2006;7(5):359-371.
109. Harris AL. Hypoxia--a key regulatory factor in tumour growth. Nat Rev Cancer. Jan 2002;2(1):38-47.
110. Jaakkola P, Mole DR, Tian YM. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science. Apr 20 2001;292(5516):468-472.
111. Lando D, Peet DJ, Whelan DA, Gorman JJ, Whitelaw ML. Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science. Feb 1 2002; 295(5556):858-861.
112. Schofield CJ, Ratcliffe PJ. Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol. May 2004;5(5):343-354.
113. Yu F, White SB, Zhao Q, Lee FS. HIF-1alpha binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proceedings of the National Academy of Sciences of the United States of America. Aug 14 2001;98(17):9630-9635.
114. Detmar M, Brown LF, Berse B. Hypoxia regulates the expression of vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) and its receptors in human skin. J Invest Dermatol. 1997;108:263-268.
115. Tang N, Wang L, Esko J. Loss of HIF-1alpha in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis. Cancer Cell. Nov 2004;6(5):485-495.
116. Oh H, Takagi H, Suzuma K, Otani A, Matsumura M, Honda Y. Hypoxia and vascular endothelial growth factor selectively up-regulate angiopoietin-2 in bovine microvascular endothelial cells. J Biol Chem. 1999;274(22):15732-15739.
117. Arany Z, Foo SY, Ma Y. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature. Feb 21 2008;451(7181):1008-1012.
118. Annex BH, Torgan CE, Lin P. Induction and maintenance of increased VEGF protein by chronic motor nerve stimulation in skeletal muscle. Am J Physiol. 1998;274(3 Pt 2):H860-867.
119. Richardson RS, Wagner H, Mudaliar SR, Saucedo E, Henry R, Wagner PD. Exercise adaptation attenuates VEGF gene expression in human skeletal muscle. Am J Physiol Heart Circ Physiol. Aug 2000;279(2):H772-778.
120. Tuomisto TT, Rissanen TT, Vajanto I, Korkeela A, Rutanen J, Yla-Herttuala S. HIF-VEGF-VEGFR-2, TNF-alpha and IGF pathways are upregulated in critical human skeletal muscle ischemia as studied with DNA array. Atherosclerosis. May 2004;174(1): 111-120.
121. Senger DR, Galli SJ, Dvorak AM, Pernuzzi CA, Harvey VS, Dvorak HF. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science. 1983;219:983-985.
122. Gale NW, Thurston G, Hackett SF. Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Developmental cell. Sep 2002;3(3):411-423.
123. Maisonpierre PC, Suri C, Jones PF. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science. 1997;277:55-60.
124. Davis S, Aldrich TH, Jones PF. Isolation of angiopoietin-1, a ligand for the Tie-2 receptor, by secretion-trap expression cloning. Cell. 1996;87:1161-1169.
125. Suri C, Jones PF, Patan S. Requisite role of angiopoietin-1, a ligand for the Tie-2 receptor, during embryonic angiogenesis. Cell. 1996;87:1171-1180.
126. Dumont DJ, Gradwohl G, Fong G-H. Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes & Development. 1994;8:1897-1909.
127. Dumont DJ, Gradwohl GJ, Puri M. The TEK endothelial receptor tyrosine kinase is required for mouse development. Developmental Dynamics. 1995;203:80-92.
128. Dumont DJ, Yamaguchi TP, Conlon RA, Rossant J, Breitman ML. tek, a novel tyrosine kinase gene located on mouse chromosome 4, is expressed in endothelial cells and their presumptive precursors. Oncogene. 1992;7(8):1471-1480.
129. Lin P, Buxton JA, Acheson A. Anti-angiogenic gene therapy targeting the endothelium-specific receptor tyrosine kinase, Tie2. Proc. Natl. Acad. Sci. USA. 1998;95:8829-8834.
130. Lin P, Polverini P, Dewhirst M, Shan S, Rao PS, Peters KG. Inhibition of tumor angiogenesis using a soluble receptor establishes a role for Tie-2 in pathologic vascular growth. J. Clin. Invest. 1997;100:2072-2078.
131. Davis S, Papadopoulos N, Aldrich TH. Angiopoietins have distinct modular domains essential for receptor binding, dimerization and superclustering. Nat Struct Biol. Dec 9 2003;10(1):38-44.
132. Baffert F, Le T, Thurston G, McDonald DM. Angiopoietin-1 decreases plasma leakage by reducing number and size of endothelial gaps in venules. Am J Physiol Heart Circ Physiol. August 26, 2005 2005:00542.02005.
133. Thurston G, Rudge JS, Ioffe E. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med. 2000;6(4):460-463.
134. Wong AL, Haroon ZA, Werner S, Dewhirst MW, Greenberg CS, Peters KG. Tie-2 expression and phosphorylation in angiogenic and quiescent adult tissues. Circ Res. 1997;81:567-574.
135. Oliner J, Min H, Leal J. Suppression of angiogenesis and tumor growth by selective inhibition of angiopoietin-2. Cancer Cell. Nov 2004;6(5):507-516.
136. Reiss Y, Droste J, Heil M. Angiopoietin-2 impairs revascularization after limb ischemia. Circulation research. Jul 6 2007;101(1):88-96.
137. Tressel SL, Kim H, Ni CW. Angiopoietin-2 stimulates blood flow recovery after femoral artery occlusion by inducing inflammation and arteriogenesis. Arteriosclerosis, thrombosis, and vascular biology. Nov 2008;28(11):1989-1995.
138. Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nature reviews. Cancer. Jan 2010;10(1):9-22.
139. Tzima E, Irani-Tehrani M, Kiosses WB. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature. Sep 15 2005;437(7057):426-431.
140. Fiedler U, Augustin HG. Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol. Dec 2006;27(12):552-558.
141. Fiedler U, Reiss Y, Scharpfenecker M. Angiopoietin-2 sensitizes endothelial cells to TNF-alpha and has a crucial role in the induction of inflammation. Nat Med. Feb 2006;12(2):235-239.
142. Kim I, Moon SO, Kim SH, Kim HJ, Koh YS, Koh GY. Vascular endothelial growth factor expression of intercellular adhesion molecule 1 (ICAM-1), vascular cell adhesion molecule 1 (VCAM-1), and E-selectin through nuclear factor-kappa B activation in endothelial cells. J Biol Chem. 2001;276(10):7614-7620.
143. Ferrara N, Carver-Moore K, Chen H. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 1996;380:439-442.
144. Shalaby F, Ho J, Stanford WL. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell. 1997;89(6):981-990.
145. Shalaby F, Rossant J, Yamaguchi TP. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 1995;376:62-66.
146. Grunewald M, Avraham I, Dor Y. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell. Jan 13 2006;124(1):175-189.
147. Barleon B, Sozzani S, Zhou D, Weich HA, Mantovani A, Marme D. Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood. 1996;87:3336-3343.
148. Schaper W. Collateral circulation: past and present. Basic research in cardiology. Jan 2009;104(1):5-21.
149. Kim I, Moon SO, Park SK, Chae SW, Koh GY. Angiopoietin-1 reduces VEGF-stimulated leukocyte adhesion to endothelial cells by reducing ICAM-1, VCAM-1, and E-selectin expression. Circ Res. 2001;89(6):477-479.
150. Potente M, Gerhardt H, Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell. Sep 16 2011;146(6):873-887.
151. Iruela-Arispe ML, Davis GE. Cellular and molecular mechanisms of vascular lumen formation. Developmental cell. Feb 2009;16(2):222-231.
152. Kamei M, Saunders WB, Bayless KJ, Dye L, Davis GE, Weinstein BM. Endothelial tubes assemble from intracellular vacuoles in vivo. Nature. Jul 27 2006;442 (7101):453-456.
153. Takeshita S, Zheng LP, Brogi E. Therapeutic angiogenesis: A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model. J. Clin. Invest. 1994;93:662-670.
154. Walder CE, Errett CJ, Bunting S. Vascular endothelial growth factor augments muscle blood flow and function in a rabbit model of chronic hindlimb ischemia. Journal of cardiovascular pharmacology. Jan 1996;27(1):91-98.
155. Rajagopalan S, Mohler ER, 3rd, Lederman RJ. Regional angiogenesis with vascular endothelial growth factor in peripheral arterial disease: a phase II randomized, doubleblind, controlled study of adenoviral delivery of vascular endothelial growth factor 121 in patients with disabling intermittent claudication. Circulation. Oct 21 2003;108(16): 1933-1938.
156. Jain RK. Molecular regulation of vessel maturation. Nat Med. Jun 2003;9(6):685-693.
157. Ramsauer M, D'Amore PA. Getting Tie(2)d up in angiogenesis. J Clin Invest. Dec 2002;110(11):1615-1617.
158. Uemura A, Ogawa M, Hirashima M. Recombinant angiopoietin-1 restores higherorder architecture of growing blood vessels in mice in the absence of mural cells. J Clin Invest. Dec 2002;110(11):1619-1628.
159. Wang HU, Chen Z-F, Anderson DJ. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell. 1998;93:741-753.
160. Carmeliet P, Jain RK. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nature reviews. Drug discovery. Jun 2011;10(6):417-427.
161. Goel S, Duda DG, Xu L. Normalization of the vasculature for treatment of cancer and other diseases. Physiological reviews. Jul 2011;91(3):1071-1121.
162. Lederman RJ, Mendelsohn FO, Anderson RD. Therapeutic angiogenesis with recombinant fibroblast growth factor-2 for intermittent claudication (the TRAFFIC study): a randomised trial. Lancet. Jun 15 2002;359(9323):2053-2058.
163. Yla-Herttuala S, Rissanen TT, Vajanto I, Hartikainen J. Vascular endothelial growth factors: biology and current status of clinical applications in cardiovascular medicine. J Am Coll Cardiol. Mar 13 2007;49(10):1015-1026.
164. Opie SR, Dib N. Local endovascular delivery, gene therapy, and cell transplantation for peripheral arterial disease. JEndovasc Ther. Dec 2004;11 Suppl 2:I1151-162.
165. Freedman SB, Isner JM. Therapeutic angiogenesis for coronary artery disease. Ann Intern Med. Jan 1 2002;136(1):54-71.
166. Papetti M, Herman IM. Mechanisms of normal and tumor-derived angiogenesis. Am J Physiol Cell Physiol. May 2002;282(5):C947-970.
167. Witzenbichler B, Mahfoudi A, Soubrier F. Intramuscular gene transfer of fibroblast growth factor-1 using improved pCOR plasmid design stimulates collateral formation in a rabbit ischemic hindlimb model. J Mol Med (Berl). Jun 2006;84(6):491-502.
168. Nakamura Y, Morishita R, Higaki J. Expression of local hepatocyte growth factor system in vascular tissues. Biochem Biophys Res Commun. Oct 13 1995;215(2):483-488.
169. Morishita R, Aoki M, Yo Y, Ogihara T. Hepatocyte growth factor as cardiovascular hormone: role of HGF in the pathogenesis of cardiovascular disease. Endocr J. Jun 2002;49(3):273-284.
170. Taniyama Y, Morishita R, Aoki M. Therapeutic angiogenesis induced by human hepatocyte growth factor gene in rat and rabbit hindlimb ischemia models: preclinical study for treatment of peripheral arterial disease. Gene Ther. Feb 2001;8(3):181-189.
171. Kola I, Brookes S, Green AR. The Ets1 transcription factor is widely expressed during murine embryo development and is associated with mesodermal cells involved in morphogenetic processes such as organ formation. Proc Natl Acad Sci U S A. Aug 15 1993;90(16):7588-7592.
172. Hirota K, Semenza GL. Regulation of angiogenesis by hypoxia-inducible factor 1. Crit Rev Oncol Hematol. Jul 2006;59(1):15-26.
173. Vincent KA, Shyu KG, Luo Y. Angiogenesis is induced in a rabbit model of hindlimb ischemia by naked DNA encoding an HIF-1alpha/VP16 hybrid transcription factor. Circulation. Oct 31 2000;102(18):2255-2261.
174. Baumgartner I, Pieczek A, Manor O. Constitutive expression of phVEGF165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation. Mar 31 1998;97(12): 1114-1123.
175. Shyu KG, Chang H, Wang BW, Kuan P. Intramuscular vascular endothelial growth factor gene therapy in patients with chronic critical leg ischemia. Am J Med. Feb 1 2003;114(2):85-92.
176. Rajagopalan S, Trachtenberg J, Mohler E. Phase I study of direct administration of a replication deficient adenovirus vector containing the vascular endothelial growth factor cDNA (CI-1023) to patients with claudication. Am J Cardiol. Sep 1 2002;90(5):512-516.
177. Mohler ER, 3rd, Rajagopalan S, Olin JW. Adenoviral-mediated gene transfer of vascular endothelial growth factor in critical limb ischemia: safety results from a phase I trial. Vasc Med. 2003;8(1):9-13.
178. Comerota AJ, Throm RC, Miller KA. Naked plasmid DNA encoding fibroblast growth factor type 1 for the treatment of end-stage unreconstructible lower extremity ischemia: preliminary results of a phase I trial. J Vasc Surg. May 2002;35(5):930-936.
179. Lazarous DF, Unger EF, Epstein SE. Basic fibroblast growth factor in patients with intermittent claudication: results of a phase I trial. J Am Coll Cardiol. Oct 2000;36(4):1239-1244.
180. Makinen K, Manninen H, Hedman M. 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. Jul 2002;6(1):127-133.
181. Powell RJ, Simons M, Mendelsohn FO. Results of a double-blind, placebo-controlled study to assess the safety of intramuscular injection of hepatocyte growth factor plasmid to improve limb perfusion in patients with critical limb ischemia. Circulation. Jul 1 2008;118(1):58-65.
182. Shigematsu H, Yasuda K, Iwai T. Randomized, double-blind, placebo-controlled clinical trial of hepatocyte growth factor plasmid for critical limb ischemia. Gene Ther. Sep 2010;17(9):1152-1161.
183. Morishita R, Makino H, Aoki M. Phase I/IIa clinical trial of therapeutic angiogenesis using hepatocyte growth factor gene transfer to treat critical limb ischemia. Arterioscler Thromb Vasc Biol. Mar 2011;31(3):713-720.
184. Nikol S, Baumgartner I, Van Belle E. Therapeutic angiogenesis with intramuscular NV1FGF improves amputation-free survival in patients with critical limb ischemia. Mol Ther. May 2008;16(5):972-978.
185. Creager MA, Olin JW, Belch JJ. Effect of hypoxia-inducible factor-1alpha gene therapy on walking performance in patients with intermittent claudication. Circulation. Oct 18 2011;124(16):1765-1773.
186. Belch J, Hiatt WR, Baumgartner I. Effect of fibroblast growth factor NV1FGF on amputation and death: a randomised placebo-controlled trial of gene therapy in critical limb ischaemia. Lancet. Jun 4 2011;377(9781):1929-1937.
187. Tateishi-Yuyama E, Matsubara H, Murohara T. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Lancet. Aug 10 2002;360(9331):427-435.
188. Burt RK, Testori A, Oyama Y. Autologous peripheral blood CD133+ cell implantation for limb salvage in patients with critical limb ischemia. Bone Marrow Transplant. Jan 2010;45(1):111-116.
189. Higashi Y, Kimura M, Hara K. Autologous bone-marrow mononuclear cell implantation improves endothelium-dependent vasodilation in patients with limb ischemia. Circulation. Mar 16 2004;109(10):1215-1218.
190. Bartsch T, Brehm M, Zeus T, Kogler G, Wernet P, Strauer BE. Transplantation of autologous mononuclear bone marrow stem cells in patients with peripheral arterial disease (the TAM-PAD study). Clin Res Cardiol. Dec 2007;96(12):891-899.
191. Van Tongeren RB, Hamming JF, Fibbe WE. Intramuscular or combined intra-muscular/intra-arterial administration of bone marrow mononuclear cells: a clinical trial in patients with advanced limb ischemia. J Cardiovasc Surg (Torino). Feb 2008;49(1):51-58.
192. Lasala GP, Silva JA, Minguell JJ. Therapeutic angiogenesis in patients with severe limb ischemia by transplantation of a combination stem cell product. J Thorac Cardiovasc Surg. Nov 12 2011.
193. Cobellis G, Silvestroni A, Lillo S. Long-term effects of repeated autologous transplantation of bone marrow cells in patients affected by peripheral arterial disease. Bone Marrow Transplant. Nov 2008;42(10):667-672.
194. Duong Van Huyen JP, Smadja DM, Bruneval P. Bone marrow-derived mononuclear cell therapy induces distal angiogenesis after local injection in critical leg ischemia. Mod Pathol. Jul 2008;21(7):837-846.
195. Rajagopalan S, Olin J, Deitcher S. Use of a constitutively active hypoxia-inducible factor-1alpha transgene as a therapeutic strategy in no-option critical limb ischemia patients: phase I dose-escalation experience. Circulation. Mar 13 2007;115(10):1234-1243.
196. Kusumanto YH, van Weel V, Mulder NH. Treatment with intramuscular vascular endothelial growth factor gene compared with placebo for patients with diabetes mellitus and critical limb ischemia: a double-blind randomized trial. Hum Gene Ther. Jun 2006;17(6):683-691.