Pre-emptive hypoxia-regulated HO-1 gene therapy improves post-ischaemic limb perfusion and tissue regeneration in mice

Cardiovascular Research

Volumn 97, Issue 1, 2013, Pages 115-124

  Jazwa, Agnieszka ^a   Stepniewski, Jacek ^a   Zamykal, Martin ^a   Jagodzinska, Jolanta ^a   Meloni, Marco ^b   Emanueli, Costanza ^b   Jozkowicz, Alicja ^a   Dulak, Jozef ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Angiogenesis; Gene therapy; HO 1; MicroRNA; Satellite cells

Indexed keywords

CXCL1 CHEMOKINE; HEME OXYGENASE 1; INTERLEUKIN 6; MICRORNA; MICRORNA 146A; MICRORNA 206; MYOD PROTEIN; MYOGENIN; TRANSCRIPTION FACTOR PAX7; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CELL MIGRATION; CONTROLLED STUDY; CRITICAL LIMB ISCHEMIA; FEMALE; GASTROCNEMIUS MUSCLE; GENE THERAPY; GENE TRANSFER; HUMAN; HUMAN CELL; IN VITRO STUDY; LIMB PERFUSION; MALE; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; MUSCLE BLOOD FLOW; MUSCLE CELL; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; TISSUE REGENERATION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CELL HYPOXIA; CELLS, CULTURED; CHEMOKINE CXCL1; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; GENETIC THERAPY; HEME OXYGENASE-1; HINDLIMB; HUMANS; HYDROGEN PEROXIDE; INFLAMMATION MEDIATORS; INTERLEUKIN-6; ISCHEMIA; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MYOD PROTEIN; MYOGENIN; NECROSIS; NEOVASCULARIZATION, PHYSIOLOGIC; OXIDANTS; PAX7 TRANSCRIPTION FACTOR; RECOVERY OF FUNCTION; REGENERATION; REGIONAL BLOOD FLOW; RESPONSE ELEMENTS; TIME FACTORS;

EID: 84871759354     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvs284     Document Type: Article

References (36)

1. Feiring AJ, Krahn M, Nelson L, Wesolowski A, Eastwood D, Szabo A. Preventing leg amputations in critical limb ischemia with below-the-knee drug-eluting stents: the PaRADISE (PReventing Amputations using Drug eluting StEnts) trial. J Am Coll Cardiol 2010;55:1580-1589.
2. Maines MD. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 1988;2:2557-2568.
3. Jozkowicz A, Huk I, Nigisch A, Weigel G, Dietrich W, Motterlini R et al. Heme oxy-genase and angiogenic activity of endothelial cells: stimulation by carbon monoxide and inhibition by tin protoporphyrin-IX. Antioxid Redox Signal 2003;5:155-162. (Pubitemid 36457591)
4. Kozakowska M, Ciesla M, Stefanska A, Skrzypek K, Was H, Jazwa A et al. Heme oxygenase-1 inhibits myoblast differentiation by targeting myomirs. Antioxid Redox Signal 2012;16:113-127.
5. Suttner DM, Dennery PA. Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J 1999;13:1800-1809. (Pubitemid 29473342)
6. Semenza GL. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology (Bethesda) 2004;19:176-182. (Pubitemid 39481932)
7. Pachori AS, Melo LG, Zhang L, Solomon SD, Dzau VJ. Chronic recurrent myocardial ischemic injury is significantly attenuated by pre-emptive adeno-associated virus heme oxygenase-1 gene delivery. J Am Coll Cardiol 2006;47:635-643. (Pubitemid 43170857)
8. Tang YL, Qian K, Zhang YC, Shen L, Phillips MI. A vigilant, hypoxia-regulated heme oxygenase-1 gene vector in the heart limits cardiac injury after ischemia-reperfusion in vivo. J Cardiovasc Pharmacol Ther 2005;10:251-263. (Pubitemid 43003335)
9. Tongers J, Knapp JM, Korf M, Kempf T, Limbourg A, Limbourg FP et al. Haeme oxygenase promotes progenitor cell mobilization, neovascularization, and functional recovery after critical hindlimb ischaemia in mice. Cardiovasc Res 2008;78:294-300. (Pubitemid 351556094)
10. Grochot-Przeczek A, Lach R, Mis J, Skrzypek K, Gozdecka M, Sroczynska P et al. Heme oxygenase-1 accelerates cutaneous wound healing in mice. PLoS ONE 2009;4:e5803.
11. Jazwa A, Kucharzewska P, Leja J, Zagorska A, Sierpniowska A, Stepniewski J et al. Combined vascular endothelial growth factor-A and fibroblast growth factor 4 gene transfer improves wound healing in diabetic mice. Genet Vaccines Ther 2010;8:6.
12. Kitamuro T, Takahashi K, Ogawa K, Udono-Fujimori R, Takeda K, Furuyama K et al. Bach1 functions as a hypoxia-inducible repressor for the heme oxygenase-1 gene in human cells. J Biol Chem 2003;278:9125-9133. (Pubitemid 36800393)
13. Loboda A, Stachurska A, Florczyk U, Rudnicka D, Jazwa A, Wegrzyn J et al. HIF-1 induction attenuates Nrf2-dependent IL-8 expression in human endothelial cells. Antioxid Redox Signal 2009;11:1501-1517.
14. Rao PK, Kumar RM, Farkhondeh M, Baskerville S, Lodish HF. Myogenic factors that regulate expression of muscle-specific microRNAs. Proc Natl Acad Sci USA 2006; 103:8721-8726. (Pubitemid 43878086)
15. Williams AH, Liu N, van Rooij E, Olson EN. MicroRNA control of muscle development and disease. Curr Opin Cell Biol 2009;21:461-469.
16. Kuang W, Tan J, Duan Y, Duan J, Wang W, Jin F et al. Cyclic stretch induced miR-146a upregulation delays C2C12 myogenic differentiation through inhibition of Numb. Biochem Biophys Res Commun 2009;378:259-263.
17. Bhang SH, Kim JH, Yang HS, La WG, Lee TJ, Sun AY et al. Combined delivery of heme oxygenase-1 gene and fibroblast growth factor-2 protein for therapeutic angiogenesis. Biomaterials 2009;30:6247-6256.
18. Suzuki M, Iso-o N, Takeshita S, Tsukamoto K, Mori I, Sato T et al. Facilitated angio-genesis induced by heme oxygenase-1 gene transfer in a rat model of hindlimb ischemia. Biochem Biophys Res Commun 2003;302:138-143. (Pubitemid 36268931)
19. Gozzelino R, Jeney V, Soares MP. Mechanisms of cell protection by heme oxygenase-1. Annu Rev Pharmacol Toxicol 2010;50:323-354.
20. Pachori AS, Melo LG, Hart ML, Noiseux N, Zhang L, Morello F et al. Hypoxia-regulated therapeutic gene as a preemptive treatment strategy against ische-mia/reperfusion tissue injury. Proc Natl Acad Sci USA 2004;101:12282- 12287. (Pubitemid 39145435)
21. Becker LB. New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovasc Res 2004;61:461-470. (Pubitemid 38210152)
22. Wang G, Hamid T, Keith RJ, Zhou G, Partridge CR, Xiang X et al. Cardioprotective and antiapoptotic effects of heme oxygenase-1 in the failing heart. Circulation 2010; 121:1912-1925.
23. Li P, Elrayess MA, Gomma AH, Palmen J, Hawe E, Fox KM et al. The microsatellite polymorphism of heme oxygenase-1 is associated with baseline plasma IL-6 level but not with restenosis after coronary in-stenting. Chin Med J (Engl) 2005;118:1525-1532. (Pubitemid 41404202)
24. Pae HO, Oh GS, Choi BM, Kim YM, Chung HT. A molecular cascade showing nitric oxide-heme oxygenase-1-vascular endothelial growth factor-interleukin-8 sequence in human endothelial cells. Endocrinology 2005;146:2229-2238.
25. Loboda A, Jazwa A, Wegiel B, Jozkowicz A, Dulak J. Heme oxygenase-1-dependent and-independent regulation of angiogenic genes expression: effect of cobalt proto-porphyrin and cobalt chloride on VEGF and IL-8 synthesis in human microvascular endothelial cells. Cell Mol Biol (Noisy-le-grand) 2005;51:347-355. (Pubitemid 41596311)
26. Engstrom G, Site-Flondell D, Lindblad B, Janzon L, Lindgarde F. Risk of treatment of peripheral arterial disease is related to inflammation-sensitive plasma proteins: a prospective cohort study. J Vasc Surg 2004;40:1101-1105. (Pubitemid 40037277)
27. Soares MP, Seldon MP, Gregoire IP, Vassilevskaia T, Berberat PO, Yu J et al. Heme oxygenase-1 modulates the expression of adhesion molecules associated with endo-thelial cell activation. J Immunol 2004;172:3553-3563. (Pubitemid 38337936)
28. Bussolati B, Ahmed A, Pemberton H, Landis RC, Di Carlo F, Haskard DO et al. Bifunc-tional role for VEGF-induced heme oxygenase-1 in vivo: induction of angiogenesis and inhibition of leukocytic infiltration. Blood 2004;103:761-766. (Pubitemid 38129530)
29. Barbagallo I, Vanella A, Peterson SJ, Kim DH, Tibullo D, Giallongo C et al. Overex-pression of heme oxygenase-1 increases human osteoblast stem cell differentiation. J Bone Miner Metab 2010;28:276-288.
30. Vanella L, Kim DH, Asprinio D, Peterson SJ, Barbagallo I, Vanella A et al. HO-1 expression increases mesenchymal stem cell-derived osteoblasts but decreases adipo-cyte lineage. Bone 2010;46:236-243.
31. Lang D, Reuter S, Buzescu T, August C, Heidenreich S. Heme-induced heme oxygenase-1 (HO-1) in human monocytes inhibits apoptosis despite caspase-3 up-regulation. Int Immunol 2005;17:155-165. (Pubitemid 40246580)
32. Cao YA, Kusy S, Luong R, Wong RJ, Stevenson DK, Contag CH. Heme oxygenase-1 deletion affects stress erythropoiesis. PLoS ONE 2011;6:e20634.
33. Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 2001;91:534-551. (Pubitemid 32681081)
34. Paoni NF, Peale F, Wang F, Errett-Baroncini C, Steinmetz H, Toy K et al. Time course of skeletal muscle repair and gene expression following acute hind limb ischemia in mice. Physiol Genomics 2002;11:263-272. (Pubitemid 37128743)
35. Liu N, Williams AH, Kim Y, McAnally J, Bezprozvannaya S, Sutherland LB et al. An intragenic MEF2-dependent enhancer directs muscle-specific expression of micro-RNAs 1 and 133. Proc Natl Acad Sci USA 2007;104:20844-20849.
36. Greco S, De Simone M, Colussi C, Zaccagnini G, Fasanaro P, Pescatori M et al. Common micro-RNA signature in skeletal muscle damage and regeneration induced by Duchenne muscular dystrophy and acute ischemia. FASEB J 2009;23:3335-3346.