Gene therapy in peripheral artery disease

Expert Opinion on Biological Therapy

Volumn 15, Issue 3, 2015, Pages 381-390

  Sanada, Fumihiro ^a   Taniyama, Yoshiaki ^a   Kanbara, Yasuhiro ^a   Otsu, Rei ^a   Ikeda Iwabu, Yuka ^a   Carracedo, Miguel ^a   Rakugi, Hiromi ^a   Morishita, Ryuichi ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Angiogenesis; Fibroblast growth factor; Gene therapy; Hepatocyte growth factor; Peripheral artery disease; VEGF

Indexed keywords

FIBROBLAST GROWTH FACTOR; SCATTER FACTOR; VASCULOTROPIN;

CRITICAL LIMB ISCHEMIA; ENDOVASCULAR SURGERY; GENE THERAPY; HUMAN; LEG AMPUTATION; LEG PAIN; LEG REVASCULARIZATION; LEG ULCER; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); QUALITY OF LIFE; REVIEW; TREATMENT OUTCOME; ANIMAL; CLINICAL TRIAL (TOPIC); GENETICS; ISCHEMIA; PERIPHERAL ARTERIAL DISEASE; PROCEDURES;

ANIMALS; CLINICAL TRIALS AS TOPIC; FIBROBLAST GROWTH FACTORS; GENETIC THERAPY; HEPATOCYTE GROWTH FACTOR; HUMANS; ISCHEMIA; PERIPHERAL ARTERIAL DISEASE; QUALITY OF LIFE;

EID: 84923112762     PISSN: 14712598     EISSN: 17447682     Source Type: Journal    
DOI: 10.1517/14712598.2015.1007039     Document Type: Review

References (93)

1. Ohnishi H, Sawayama Y, Furusyo N, et al. Risk factors for and the prevalence of peripheral arterial disease and its relationship to carotid atherosclerosis: the Kyushu and Okinawa Population Study (KOPS). J Atheroscler Thromb 2010;17:751-8
2. Go AS, Mozaffarian D, Roger VL, et al. Executive summary: heart disease and stroke statistics-2014 update: a report from the American Heart Association. Circulation 2014;129(3):399-410
3. The PARTNERS program: a national survey of peripheral arterial disease detection, awareness, and treatment. JAMA 2001;286:1317-24
4. Fowkes FG, Rudan D, Rudan I, et al. Comparison of global estimates of prevalence and risk factors for peripheral artery disease in 2000 and 2010: a systematic review and analysis. Lancet 2013;382(9901):1329-40
5. Belch JJ, Topol EJ, Agnelli G, et al. Critical issues in peripheral arterial disease detection and management: a call to action. Arch Intern Med 2003;163(8):884-92
6. Norgren L, Hiatt WR, Dormandy JA, et al. Inter-society consensus for the management of peripheral arterial disease (TASC II). J Vasc Surg 2007;45(Suppl S):S5-67
7. Nehler MR, Duval S, Diao L, et al. Epidemiology of peripheral arterial disease and critical limb ischemia in an insured national population. J Vasc Surg 2014;60(3):686-95
8. Lau JF, Weinberg MD, Olin JW. Peripheral artery disease. Part 1: clinical evaluation and noninvasive diagnosis. Nat Rev Cardiol 2011;8(7):405-18
9. Hiatt WR. Medical treatment of peripheral arterial disease and claudication. N Engl J Med 2001;344(21):1608-21
10. Annex BH. Therapeutic angiogenesis for critical limb ischaemia. Nat Rev Cardiol 2013;10(7):387-96
11. Hirsch AT, Haskal ZJ, Hertzer NR, et al. Acc/aha 2005 guidelines for the management of patients with peripheral arterial disease. J Am Coll Cardiol 2006;47(6):1239-312
12. Rastan A, Tepe G, Krankenberg H, et al. Sirolimus-eluting stents vs. bare-metal stents for treatment of focal lesions in infrapopliteal arteries: a double-blind, multi-centre, randomized clinical trial. Eur Heart J 2011;32(18):2274-81
13. Shimamura M, Nakagami H, Koriyama H, Morishita R. Gene therapy and cell-based therapies for therapeutic angiogenesis in peripheral artery disease. Biomed Res Int 2013;2013:186215
14. Blum A, Balkan W, Hare JM. Advances in cell-based therapy for peripheral vascular disease. Atherosclerosis 2012;223(2):269-77
15. Baumgartner I, Pieczek A, Manor O, et al. Constitutive expression of phVEGF165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation 1998;97(12):1114-23
16. Comerota AJ, Throm RC, Miller KA, et al. 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 2002;35(5):930-6
17. Kusumanto YH, van Weel V, Mulder NH, et al. 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 2006;17(6):683-91
18. Belch J, Hiatt WR, Baumgartner I, et al. Effect of fibroblast growth factor NV1 FGF on amputation and death: a randomised placebo-controlled trial of gene therapy in critical limb ischaemia. Lancet 2011;377(9781):1929-37
19. Powell RJ, Simons M, Mendelsohn FO, et al. 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 2008;118(1):58-65
20. Shigematsu H, Yasuda K, Iwai T, et al. Randomized, double-blind, placebo-controlled clinical trial of hepatocyte growth factor plasmid for critical limb ischemia. Gene Ther 2010;17(9):1152-61
21. Laughlin MH, Roseguini B. Mechanisms for exercise training-induced increases in skeletal muscle blood flow capacity: differences with interval sprint training versus aerobic endurance training. J Physiol Pharmacol 2008;59(Suppl 7):71-88
22. Groen BB, Hamer HM, Snijders T, et al. Skeletal muscle capillary density and microvascular function are compromised with aging and type 2 diabetes. J Appl Physiol (1985) 2014;116(8):998-1005
23. Selvin E, Erlinger TP. Prevalence of and risk factors for peripheral arterial disease in the United States: results from the national health and nutrition examination survey, 1999-2000. Circulation 2004;110(6):738-43
24. Gardner AW, Parker DE, Montgomery PS, et al. Greater endothelial apoptosis and oxidative stress in patients with peripheral artery disease. Int J Vasc Med 2014;2014:160534
25. Norgren L, Hiatt WR, Dormandy JA, et al. on behalf of the TASC II Working Group. Inter-society consensus for the management of peripheral arterial disease (TASC II). Eur J Vasc Endovasc Surg 2007;33(Suppl 1):S1-75
26. Pipinos I, Judge A, Selsby J, et al. The myopathy of peripheral arterial occlusive disease: part 1. Functional and histomorphological changes and evidence for mitochondrial dysfunction. Vasc Endovascular Surg 2008;41(6):481-9
27. Pipinos I, Judge A, Selsby J, et al. The myopathy of peripheral arterial occlusive disease: part 2.oxidative stress, neuropathy, and shift in muscle fiber type. Vasc Endovascular Surg 2008;42(2):101-12
28. Sanada F, Taniyama Y, Iekushi K, et al. Negative action of hepatocyte growth factor/c-met system on angiotensin II signaling via ligand-dependent epithelial growth factor receptor degradation mechanism in vascular smooth muscle cells. Circ Res 2009;105(7):667-75
29. Minamino T, Komuro I. Vascular cell senescence: contribution to atherosclerosis. Circ Res 2007;100(1):15-26
30. Sanada F, Taniyama Y, Azuma J, et al. Hepatocyte growth factor, but not vascular endothelial growth factor, attenuates angiotensin II-induced endothelial progenitor cell senescence. Hypertension 2009;53(1):77-82
31. Yokoi T, Fukuo K, Yasuda O, et al. Apoptosis signal-regulating kinase 1 mediates cellular senescence induced by high glucose in endothelial cells. Diabetes 2006;55(6):1660-5
32. Sasaki M, Ikeda H, Sato Y, Nakanuma Y. Proinflammatory cytokine-induced cellular senescence of biliary epithelial cells is mediated via oxidative stress and activation of atm pathway: a culture study. Free Radic Res 2008;42(7):625-32
33. Sanada F, Kim J, Czarna A, et al. c-Kit-positive cardiac stem cells nested in hypoxic niches are activated by stem cell factor reversing the aging myopathy. Circ Res 2014;114(1):41-55
34. Robbins JL, Jones WS, Duscha BD, et al. Relationship between leg muscle capillary density and peak hyperemic blood flow with endurance capacity in peripheral artery disease. J Appl Physiol 2011;111(1):81-6
35. Muhlhauser J, Merrill MJ, Pili R, et al. VEGF165 expressed by a replication-deficient recombinant adenovirus vector induces angiogenesis in vivo. Circ Res 1995;77(6):1077-86
36. Gowdak LH, Poliakova L, Wang X, et al. Adenovirus-mediated VEGF (121) gene transfer stimulates angiogenesis in normoperfused skeletal muscle and preserves tissue perfusion after induction of ischemia. Circulation 2000;102(5):565-71
37. Kerbel RS. Tumor angiogenesis. N Engl J Med 2008;358(19):2039-49
38. Isner JM. Therapeutic angiogenesis: a new frontier for vascular therapy. Vasc Med 1996;1(1):79-87
39. Takahashi H, Shibuya M. The vascular endothelial growth factor (VEGF)/VEGF receptor system and its role under physiological and pathological conditions. Clin Sci (Lond) 2005;109(3):227-41
40. Takeshita S, Zheng LP, Brogi E, et al. 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(2):662-70
41. Walder CE, Errett CJ, Bunting S, et al. Vascular endothelial growth factor augments muscle blood flow and function in a rabbit model of chronic hindlimb ischemia. J Cardiovasc Pharmacol 1996;27(1):91-8
42. Kalka C, Tehrani H, Laudenberg B, et al. VEGF gene transfer mobilizes endothelial progenitor cells in patients with inoperable coronary disease. Ann Thorac Surg 2000;70(3):829-34
43. Asahara T, Takahashi T, Masuda H, et al. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J 1999;18(14):3964-72
44. Makinen K, Manninen H, Hedman M, et al. 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 2002;6(1):127-33
45. Rajagopalan S, Mohler E III, Lederman RJ, et al. Regional angiogenesis with vascular endothelial growth factor (VEGF) in peripheral arterial disease: design of the rave trial. Am Heart J 2003;145(6):1114-18
46. Baumgartner I, Rauh G, Pieczek A, et al. Lower-extremity edema associated with gene transfer of naked DNA encoding vascular endothelial growth factor. Ann Intern Med 2000;132:880-4
47. Detmar M, Brown LF, Schon MP, et al. Increased microvascular density and enhanced leukocyte rolling and adhesion in the skin of VEGF transgenic mice. J Invest Dermatol 1998;111:1-6
48. Kim I, Moon SO, Kim SH, et al. 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;276:7614-20
49. Monaghan-Benson E, Burridge K. The regulation of vascular endothelial growth factor-induced microvascular permeability requires Rac and reactive oxygen species. J Biol Chem 2009;284(38):25602-11
50. Ehrbar M, Djonov VG, Schnell C, et al. Cell-demanded liberation of VEGF121 from fibrin implants induces local and controlled blood vessel growth. Circ Res 2004;94(8):1124-1132
51. Makarevich P, Tsokolaeva Z, Shevelev A, et al. Combined transfer of human VEGF165 and HGF genes renders potent angiogenic effect in ischemic skeletal muscle. PLoS One 2012;7(6):e38776
52. Benest AV, Salmon AH, Wang W, et al. VEGF and angiopoietin-1 stimulate different angiogenic phenotypes that combine to enhance functional neovascularization in adult tissue. Microcirculation 2006;13(6):423-37
53. Gupta R, Tongers J, Losordo DW. Human studies of angiogenic gene therapy. Circ Res 2009;105(8):724-36
54. Beenken A, Mohammadi M. The FGF family: biology, pathophysiology and therapy. Nat Rev Drug Discov 2009;8(3):235-53
55. Burger PE, Coetzee S, McKeehan WL, et al. Fibroblast growth factor receptor-1 is expressed by endothelial progenitor cells. Blood 2002;100(10):3527-35
56. Goncalves LM. Fibroblast growth factor-mediated angiogenesis for the treatment of ischemia. Lessons learned from experimental models and early human experience. Rev Port Cardiol 1998;17(Suppl 2):II11-20
57. Nikol S, Baumgartner I, Van Belle E, et al. Therapeutic angiogenesis with intramuscular NV1 FGF improves amputation-free survival in patients with critical limb ischemia. Mol Ther 2008;16(5):972-8
58. Kriz W, Hähnel B, Rösener S, Elger M. Long-term treatment of rats with FGF-2 results in focal segmental glomerulosclerosis. Kidney Int 1995;48(5):1435-50
59. Yonemitsu Y, Matsumoto T, Itoh H, et al. DVC1-0101 to treat peripheral arterial disease: a Phase I/IIa open-label dose-escalation clinical trial. Mol Ther 2013;21(3):707-14
60. Nakamura T, Teramoto H, Ichihara A. Purification and characterization of a growth factor from rat platelets for mature parenchymal hepatocytes in primary cultures. Proc Natl Acad Sci USA 1986;83(17):6489-93
61. Wojakowski W, Tendera M, Michalowska A, et al. Mobilization of CD34/CXCR4+, CD34/CD117+, c-met + stem cells, and mononuclear cells expressing early cardiac, muscle, and endothelial markers into peripheral blood in patients with acute myocardial infarction. Circulation 2004;110(20):3213-20
62. Morishita R, Makino H, Aoki M, et al. Phase I/IIa clinical trial of therapeutic angiogenesis using hepatocyte growth factor gene transfer to treat critical limb ischemia. Arterioscler Thromb Vasc Biol 2011;31(3):713-20
63. Makino H, Aoki M, Hashiya N, et al. Long-term follow-up evaluation of results from clinical trial using hepatocyte growth factor gene to treat severe peripheral arterial disease. Arterioscler Thromb Vasc Biol 2012;32(10):2503-9
64. Iekushi K, Taniyama Y, Kusunoki H, et al. Hepatocyte growth factor attenuates transforming growth factor-beta-angiotensin ii crosstalk through inhibition of the pten/akt pathway. Hypertension 2011;58(2):190-6
65. Koibuchi N, Kaneda Y, Taniyama Y, et al. Essential role of HGF (hepatocyte growth factor) in blood formation in xenopus. Blood 2004;103(9):3320-5
66. Taniyama Y, Morishita R, Nakagami H, et al. Potential contribution of a novel antifibrotic factor, hepatocyte growth factor, to prevention of myocardial fibrosis by angiotensin II blockade in cardiomyopathic hamsters. Circulation 2000;102(2):246-52
67. Taniyama Y, Morishita R, Aoki M, et al. Angiogenesis and antifibrotic action by hepatocyte growth factor in cardiomyopathy. Hypertension 2002;40(1):47-53
68. Ueki T, Kaneda Y, Tsutsui H, et al. Hepatocyte growth factor gene therapy of liver cirrhosis in rats. Nat Med 1999;5(2):226-30
69. Vlassara H, Cai W, Chen X, et al. Managing chronic inflammation in the aging diabetic patient with ckd by diet or sevelamer carbonate: a modern paradigm shift. J Gerontol A Biol Sci Med Sci 2012;67(12):1410-16
70. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005;352(16):1685-95
71. Mantzouranis EC, Rosen FS, Colten HR. Reticuloendothelial clearance in cystic fibrosis and other inflammatory lung diseases. N Engl J Med 1988;319(6):338-43
72. Brevetti G, Giugliano G, Brevetti L, Hiatt WR. Inflammation in peripheral artery disease. Circulation 2010;122(18):1862-75
73. Kuilman T, Michaloglou C, Vredeveld LC, et al. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 2008;133(6):1019-31
74. Chandeck C, Mooi WJ. Oncogene-induced cellular senescence. Adv Anat Pathol 2010;17(1):42-8
75. Mooi WJ. Oncogene-induced cellular senescence: causal factor in the growth arrest of pituitary microadenomas? Horm Res 2009;71(Suppl 2):78-81
76. Imanishi T, Tsujioka H, Akasaka T. Endothelial progenitor cell senescence-is there a role for estrogen? Ther Adv Cardiovasc Dis 2010;4(1):55-69
77. Shimizu K, Taniyama Y, Sanada F, et al. Hepatocyte growth factor inhibits lipopolysaccharide-induced oxidative stress via epithelial growth factor receptor degradation. Arterioscler Thromb Vasc Biol 2012;32(11):2687-93
78. Kaga T, Kawano H, Sakaguchi M, et al. Hepatocyte growth factor stimulated angiogenesis without inflammation: differential actions between hepatocyte growth factor, vascular endothelial growth factor and basic fibroblast growth factor. Vascul Pharmacol 2012;57(1):3-9
79. Ohtani K, Egashira K, Hiasa K, et al. Blockade of vascular endothelial growth factor suppresses experimental restenosis after intraluminal injury by inhibiting recruitment of monocyte lineage cells. Circulation 2004;110(16):2444-52
80. Matsumoto K, Morishita R, Moriguchi A, et al. Inhibition of neointima by angiotensin-converting enzyme inhibitor in porcine coronary artery balloon-injury model. Hypertension 2001;37(2):270-4
81. Van Belle E, Witzenbichler B, Chen D, et al. Potentiated angiogenic effect of scatter factor/hepatocyte growth factor via induction of vascular endothelial growth factor: the case for paracrine amplification of angiogenesis. Circulation 1998;97(4):381-90
82. Xin X, Yang S, Ingle G, et al. Hepatocyte growth factor enhances vascular endothelial growth factor-induced angiogenesis in vitro and in vivo. Am J Pathol 2001;158(3):1111-20
83. Min JK, Lee YM, Kim JH, et al. Hepatocyte growth factor suppresses vascular endothelial growth factor-induced expression of endothelial icam-1 and vcam-1 by inhibiting the nuclear factor-kappa B pathway. Circ Res 2005;96(3):300-7
84. Hamada N, Kuwano K, Yamada M, et al. Anti-vascular endothelial growth factor gene therapy attenuates lung injury and fibrosis in mice. J Immunol 2005;175(2):1224-31
85. Chaudhary NI, Roth GJ, Hilberg F, et al. VEGF and FGF signalling attenuates fibrosis. Eur Respir J 2007;29(5):976-85
86. Okayama K, Azuma J, Dosaka N, et al. Hepatocyte growth factor reduces cardiac fibrosis by inhibiting endothelial-mesenchymal transition. Hypertension 2012;59(5):958-65
87. Nakano N, Morishita R, Moriguchi A, et al. Negative regulation of local hepatocyte growth factor expression by angiotensin ii and transforming growth factor-beta in blood vessels: potential role of hgf in cardiovascular disease. Hypertension 1998;32(3):444-51
88. Urbanek K, Rota M, Cascapera S, et al. Cardiac stem cells possess growth factor-receptor systems that after activation regenerate the infarcted myocardium, improving ventricular function and long-term survival. Circ Res 2005;97(7):663-73
89. Golomb BA, Dang TT, Criqui MH. Peripheral arterial disease: morbidity and mortality implications. Circulation 2006;114(7):688-99
90. Dor Y, Djonov V, Abramovitch R, et al. Conditional switching of VEGF provides new insights into adult neovascularization and pro angiogenic therapy. EMBO J 2002;21(8):1939-47
91. Gounis MJ, Spiga MG, Graham RM, et al. Angiogenesis is confined to the transient period of VEGF expression that follows adenoviral gene delivery to ischemic muscle. Gene Ther 2005;12(9):762-71
92. Taniyama Y, Tachibana K, Hiraoka K, et al. Local delivery of plasmid DNA into rat carotid artery using ultrasound. Circulation 2002;105(10):1233-9
93. Fumoto S, Nishi J, Nakamura J, Nishida K. Gene therapy for gastric diseases. Curr Gene Ther 2008;8(3):187-200; Review