Oral tetrahydrobiopterin improves the beneficial effect of adenoviral-mediated eNOS gene transfer after induction of hindlimb ischemia

Molecular Therapy

Volumn 18, Issue 8, 2010, Pages 1482-1489

  Yan, Jinglian ^a   Tie, Guodong ^a   Hoffman, Ari ^b   Yang, Yagai ^b   Nowicki, Philip T ^a   Messina, Louis M ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; ADENOVIRUS VECTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; NITRATE; NITRIC OXIDE; NITRITE; PHOSPHATE BUFFERED SALINE; SERINE; TETRAHYDROBIOPTERIN;

ADJUVANT THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG EFFICACY; DRUG POTENTIATION; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; HUMAN; HUMAN CELL; LIMB ISCHEMIA; MALE; MONOTHERAPY; MUSCLE NECROSIS; NONHUMAN; OXIDATIVE STRESS; RAT; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS RECOMBINANT;

ADENOVIRIDAE; BOVINAE; RATTUS;

EID: 77955176647     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2010.109     Document Type: Article

References (32)

1. Shammas, NW (2007). Epidemiology, classifcation, and modifable risk factors of peripheral arterial disease. Vasc Health Risk Manag 3: 229-234.
2. Brevetti, LS, Chang, DS, Tang, GL, Sarkar, R and Messina, LM (2003). Overexpression of endothelial nitric oxide synthase increases skeletal muscle blood fow and oxygenation in severe rat hind limb ischemia. J Vasc Surg 38: 820-826.
3. Yan, J, Tang, GL, Wang, R and Messina, LM (2005). Optimization of adenovirus-mediated endothelial nitric oxide synthase delivery in rat hindlimb ischemia. Gene Ther 12: 1640-1650.
4. Smith, RS Jr, Lin, KF, Agata, J, Chao, L and Chao, J (2002). Human endothelial nitric oxide synthase gene delivery promotes angiogenesis in a rat model of hindlimb ischemia. Arterioscler Thromb Vasc Biol 22: 1279-1285.
5. Tsutsui, M, Chen, AF, O'Brien, T, Crotty, TB and Katusic, ZS (1998). Adventitial expression of recombinant eNOS gene restores NO production in arteries without endothelium. Arterioscler Thromb Vasc Biol 18: 1231-1241.
6. Katusic, ZS (2002). Therapeutic angiogenesis: new indication for endothelial NO synthase gene transfer. Arterioscler Thromb Vasc Biol 22: 1254-1255.
7. Murohara, T, Asahara, T, Silver, M, Bauters, C, Masuda, H, Kalka, C et al. (1998). Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 101: 2567-2578.
8. Buckwalter, JB, Curtis, VC, Valic, Z, Ruble, SB and Clifford, PS (2003). Endogenous vascular remodeling in ischemic skeletal muscle: a role for nitric oxide. J Appl Physiol 94: 935-940.
9. Lloyd, PG, Yang, HT and Terjung, RL (2001). Arteriogenesis and angiogenesis in rat ischemic hindlimb: role of nitric oxide. Am J Physiol Heart Circ Physiol 281: H2528-H2538.
10. Mees, B, Wagner, S, Ninci, E, Tribulova, S, Martin, S, van Haperen, R et al. (2007). Endothelial nitric oxide synthase activity is essential for vasodilation during blood fow recovery but not for arteriogenesis. Arterioscler Thromb Vasc Biol 27: 1926-1933.
11. Aicher, A, Heeschen, C, Mildner-Rihm, C, Urbich, C, Ihling, C, Technau-Ihling, K et al. (2003). Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 9: 1370-1376.
12. Marletta, MA (1993). Nitric oxide synthase structure and mechanism. J Biol Chem 268: 12231-12234.
13. Schmidt, TS and Alp, NJ (2007). Mechanisms for the role of tetrahydrobiopterin in endothelial function and vascular disease. Clin Sci (Lond) 113: 47-63.
14. Vásquez-Vivar, J, Kalyanaraman, B, Martásek, P, Hogg, N, Masters, BS, Karoui, H et al. (1998). Superoxide generation by endothelial nitric oxide synthase: the infuence of cofactors. Proc Natl Acad Sci USA 95: 9220-9225. (Pubitemid 28506212)
15. Kuzkaya, N, Weissmann, N, Harrison, DG and Dikalov, S (2003). Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: implications for uncoupling endothelial nitric-oxide synthase. J Biol Chem 278: 22546-22554.
16. Crabtree, MJ, Tatham, AL, Al-Wakeel, Y, Warrick, N, Hale, AB, Cai, S et al. (2009). Quantitative regulation of intracellular endothelial nitric-oxide synthase (eNOS) coupling by both tetrahydrobiopterin-eNOS stoichiometry and biopterin redox status: insights from cells with tet-regulated GTP cyclohydrolase I expression. J Biol Chem 284: 1136-1144.
17. Bendall, JK, Alp, NJ, Warrick, N, Cai, S, Adlam, D, Rockett, K et al. (2005). Stoichiometric relationships between endothelial tetrahydrobiopterin, endothelial NO synthase (eNOS) activity, and eNOS coupling in vivo: insights from transgenic mice with endothelial-targeted GTP cyclohydrolase 1 and eNOS overexpression. Circ Res 97: 864-871.
18. Stoffels, F, Lohöfener, F, Beisenhirtz, M, Lisdat, F and Büttemeyer, R (2007). Concentration decrease of nitric oxide in the postischemic muscle is not only caused by the generation of O2-. Microsurgery 27: 565-568.
19. Misko, TP, Schilling, RJ, Salvemini, D, Moore, WM and Currie, MG (1993). A fuorometric assay for the measurement of nitrite in biological samples. Anal Biochem 214: 11-16.
20. Inoue, M, Saito, Y, Hirata, E, Morino, Y and Nagase, S (1987). Regulation of redox states of plasma proteins by metabolism and transport of glutathione and related compounds. J Protein Chem 6: 207-225.
21. Dumitrescu, C, Biondi, R, Xia, Y, Cardounel, AJ, Druhan, LJ, Ambrosio, G et al. (2007). Myocardial ischemia results in tetrahydrobiopterin (BH4) oxidation with impaired endothelial function ameliorated by BH4. Proc Natl Acad Sci USA 104: 15081-15086.
22. Elrod, JW, Duranski, MR, Langston, W, Greer, JJ, Tao, L, Dugas, TR et al. (2006). eNOS gene therapy exacerbates hepatic ischemia-reperfusion injury in diabetes: a role for eNOS uncoupling. Circ Res 99: 78-85.
23. Fiege, B, Ballhausen, D, Kierat, L, Leimbacher, W, Goriounov, D, Schircks, B et al. (2004). Plasma tetrahydrobiopterin and its pharmacokinetic following oral administration. Mol Genet Metab 81: 45-51.
24. Sawabe, K, Wakasugi, KO and Hasegawa, H (2004). Tetrahydrobiopterin uptake in supplemental administration: elevation of tissue tetrahydrobiopterin in mice following uptake of the exogenously oxidized product 7,8-dihydrobiopterin and subsequent reduction by an anti-folate-sensitive process. J Pharmacol Sci 96: 124-133.
25. Sawabe, K, Suetake, Y, Nakanishi, N, Wakasugi, KO and Hasegawa, H (2005). Cellular accumulation of tetrahydrobiopterin following its administration is mediated by two different processes; direct uptake and indirect uptake mediated by a methotrexate-sensitive process. Mol Genet Metab 86 (suppl. 1): S133-S138.
26. Scholz, D, Cai, WJ and Schaper, W (2001). Arteriogenesis, a new concept of vascular adaptation in occlusive disease. Angiogenesis 4: 247-257.
27. Jain, RK (2003). Molecular regulation of vessel maturation. Nat Med 9: 685-693.
28. Brevetti, LS, Paek, R, Brady, SE, Hoffman, JI, Sarkar, R and Messina, LM (2001). Exercise-induced hyperemia unmasks regional blood fow defcit in experimental hindlimb ischemia. J Surg Res 98: 21-26.
29. Hoefer, IE, van Royen, N, Buschmann, IR, Piek, JJ and Schaper, W (2001). Time course of arteriogenesis following femoral artery occlusion in the rabbit. Cardiovasc Res 49: 609-617.
30. Regensteiner, JG and Hiatt, WR (2002). Current medical therapies for patients with peripheral arterial disease: a critical review. Am J Med 112: 49-57.
31. Waters, R, Terjung, R, Peters, K and Annex, B (2004). Preclinical models of human peripheral arterial occlusive disease: implications for investigating therapeutic agents. Am J Physiol 97: 773-780.
32. Henry, TD, Annex, BH, McKendall, GR, Azrin, MA, Lopez, JJ, Giordano, FJ et al.; VIVA Investigators. (2003). The VIVA trial: Vascular endothelial growth factor in Ischemia for Vascular Angiogenesis. Circulation 107: 1359-1365.