Xanthine oxidoreductase function contributes to normal wound healing

Molecular Medicine

Volumn 21, Issue , 2015, Pages 313-322

  Madigan, Michael C ^a,b   McEnaney, Ryan M ^a,b   Shukla, Ankur J ^a,b   Hong, Guiying ^a,b   Kelley, Eric E ^c   Tarpey, Margaret M ^a,c   Gladwin, Mark ^d   Zuckerbraun, Brian S ^a,b   Tzeng, Edith ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPURINOL; ARGINASE 1; HYDROGEN PEROXIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRITE; REACTIVE OXYGEN METABOLITE; SULFITE OXIDASE; TUNGSTEN; XANTHINE OXIDASE; ALDEHYDE OXIDASE; ARG1 PROTEIN, MOUSE; ARGINASE; REACTIVE NITROGEN SPECIES; XANTHINE DEHYDROGENASE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIETARY INTAKE; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME INHIBITION; GRANULATION TISSUE; HISTOPATHOLOGY; KERATINOCYTE; MALE; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SKIN INJURY; TISSUE DISTRIBUTION; WOUND HEALING; WOUND HEALING IMPAIRMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; DIETARY SUPPLEMENT; DISEASE MODEL; GENE EXPRESSION; GENETICS; METABOLISM; PHYSIOLOGY;

ALDEHYDE OXIDASE; ANIMALS; ARGINASE; CELL PROLIFERATION; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; GENE EXPRESSION; GRANULATION TISSUE; HYDROGEN PEROXIDE; KERATINOCYTES; MALE; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; TUNGSTEN; WOUND HEALING; XANTHINE DEHYDROGENASE;

EID: 84937570589     PISSN: 10761551     EISSN: None     Source Type: Journal    
DOI: 10.2119/molmed.2014.00191     Document Type: Article

References (52)

1. Singh N, Armstrong DG, Lipsky BA. (2005) Preventing foot ulcers in patients with diabetes. JAMA. 293:217-28.
2. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M. (2008) Growth factors and cytokines in wound healing. Wound Repair Regen. 16:585-601.
3. Smiell JM, et al. (1999) Efficacy and safety of becaplermin (recombinant human platelet-derived growth factor-BB) in patients with non-healing, lower extremity diabetic ulcers: a combined analysis of four randomized studies. Wound Repair Regen. 7:335-46.
4. Soneja A, Drews M, Malinski T. (2005) Role of nitric oxide, nitroxidative and oxidative stress in wound healing. Pharmacol. Rep. 57(Suppl):108-19.
5. Schafer M, Werner S. (2008) Oxidative stress in normal and impaired wound repair. Pharmacol. Res. 58:165-71.
6. Roy S, Khanna S, Nallu K, Hunt TK, Sen CK. (2006) Dermal wound healing is subject to redox control. Mol. Ther. 13:211-20.
7. Sen CK, Roy S. (2008) Redox signals in wound healing. Biochim. Biophys. Acta. 1780:1348-61.
8. Niethammer P, Grabher C, Look AT, Mitchison TJ. (2009) A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature. 459:996-9.
9. Senel O, Cetinkale O, Ozbay G, Ahcioglu F, Bulan R. (1997) Oxygen free radicals impair wound healing in ischemic rat skin. Ann. Plast. Surg. 39:516-23.
10. Loo AE, et al. (2012) Effects of hydrogen peroxide on wound healing in mice in relation to oxidative damage. PLoS One. 7:e49215.
11. Lee RH, Efron D, Tantry U, Barbul A. (2001) Nitric oxide in the healing wound: a time-course study. J. Surg. Res. 1001:104-8.
12. Fukumura D, et al. (2001) Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc. Natl. Acad. Sci. U. S. A. 98:2604-9.
13. Schäffer MR, et al. (1997) Nitric oxide, and autocrine regulator of wound fibroblast synthetic function. J. Immunol. 158:2375-81.
14. Ziche M, et al. (1994) Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by Substance P. J. Clin. Invest. 94:2036-44.
15. Schäffer MR, et al. (1997) Diabetes-impaired healing and reduced wound nitric oxide synthesis: a possible pathophysiologic correlation. Surgery. 121:513-9.
16. Kampfer H, Pfeilschifter J, Frank S. (2003) Expression and activity of arginase isoenzymes during normal and diabetes-impaired skin repair. J. Invest. Dermatol. 121:1544-51.
17. Albina JE, Mills CD, Henry WL, Caldwell MD. (1990) Temporal expression of different pathways of L-arginine metabolism in healing wounds. J. Immunol. 144:3877-80.
18. Stallmeyer B, et al. (2002) Regulation of eNOS in normal and diabetes-impaired skin repair: implications for tissue regeneration. Nitric Oxide. 6:168-77.
19. Yamasaki K, et al. (1998) Reversal of impaired wound repair in iNOS-deficient mice by topical adenoviral-mediated iNOS gene transfer. J. Clin. Invest. 101:967-71.
20. Lee PC, et al. (1999) Impaired wound healing and angiogenesis in eNOS-deficient mice. Am. J. Physiol. 277:H1600-8.
21. Brondino CD, Romao MJ, Moura I, Moura JJ. (2006) Molybdenum and tungsten enzymes: the xanthine oxidase family. Curr. Opin. Chem. Biol. 10:109-14.
22. Li H, Cui H, Kundu TK, Alzawahra W, Zweier JL. (2008) Nitric oxide production from nitrite occurs primarily in tissues not in the blood. J. Biol. Chem. 283:17855-63.
23. Alef MJ, et al. (2011) Nitrite-generated NO circumvents dysregulated arginine/NOS signaling to protect against intimal hyperplasia in Sprague-Dawley rats. J. Clin. Invest. 121:1646-56.
24. Zuckerbraun BS, et al. (2010) Nitrite potently inhibits hypoxic and inflammatory artery hypertension and smooth muscle proliferation via xanthine oxidoreductase-dependent nitric oxide generation. Circulation. 121:98-109.
25. Nakai K, Kadiiska MB, Jiang JJ, Stadler K, Mason RP. (2006) Free radical production requires both inducible nitric oxide synthase and xanthine oxidase in LPS-treated skin. Proc. Natl. Acad. Sci. U. S. A. 103:4616-21.
26. Portugal-Cohen M, et al. (2011) Skin organ culture as a model to study oxidative stress, inflammation and structural alterations associated with UVB-induced photodamage. Exp. Dermatol. 20:749-55.
27. Johnson JL, Rajagopalan KV, Cohen HJ. (1974) Molecular basis of the biological function of molybdenum. J. Biol. Chem. 249:859-66.
28. Pacher P, Nivorozhkin A, Szabo A. (2006) Therapeutic effects of xanthine oxidase inhibitors: renaissance half a century after the discovery of allopurinol. Pharmacol. Rev. 58:87-114.
29. Committee for the Update of the Guide for the Care and Use of Laboratory Animals, Institute for Laboratory Animal Research, Division on Earth and Life Studies, National Research Council of the National Academies. (2011) Guide for the Care and Use of Laboratory Animals. 8th edition. Washington (DC): National Academies Press.
30. Sachdev U, et al. (2012) High mobility group box 1 promotes endothelial cell angiogenic behavior in vitro and improves muscle perfusion in vivo in response to ischemic injury. J. Vasc. Surg. 55:180-91.
31. Kibbe MR, et al. (2000) Inducible nitric oxide synthase (iNOS) expression upregulates p21 and inhibits vascular smooth muscle cell proliferation through p42/44 mitogen-activated protein kinase activation and independent of p53 and cyclic guanosine monophosphate. J. Vasc. Surg. 31:1214-28.
32. Liang CC, Park AY, Guan JL. (2007) In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat. Protoc. 2:329-33.
33. Adkins WK, Taylor AE. (1990) Role of xanthine oxidase and neutrophils in ischemia-reperfusion injury in rabbit lung. J. Appl. Physiol. 69:2012-8.
34. White CR, et al. (1996) Circulating plasma xanthine oxidase contributes to vascular dysfunction in hypercholesterolemic rabbits. Proc. Natl. Acad. Sci. U. S. A. 93:8745-9.
35. Linas SL, Whittenburg D, Repine JE. (1990) Role of xanthine oxidase is ischemia/reprofusion injury. Am. J. Physiol. 258:F711-6.
36. Sen CK. (2003) The general case for redox control and wound repair. Wound Repair Regen. 11:431-8.
37. Baliga RS, et al. (2012) Dietary nitrate ameliorates pulmonary hypertension: cytoprotective role for endothelial nitric oxide synthase and xanthine oxidoreductase. Circulation. 125:2922-32.
38. Malik UZ, et al. (2011) Febuxostat inhibition of endothelial-bound XO: implications for targeting vascular ROS production. Free Radic. Biol. Med. 51:179-84.
39. Kelley EE, et al. (2004) Binding of xanthine oxidase to glycosaminoglycans limits inhibition by oxypurinol. J. Biol. Chem. 279:37231-4.
40. Pence BC, Reiners JJ Jr. (1987) Murine epidermal xanthine oxidase activity: correlation with degree of hyperplasia induced by tumor promoters. Cancer Res. 47:6388-92.
41. Vermeij WP, Backendorf C. (2010) Skin cornification proteins provide global link between ROS detoxification and cell migration during wound healing. PLoS One. 5:e11957.
42. Roy S, Khanna S, Sen CK. (2008) Redox regulation of the VEGF signaling path and tissue vascularization: hydrogen peroxide, the common link between physical exercise and cutaneous wound healing. Free Radic. Biol. Med. 44:180-92.
43. Kelley EE, et al. (2010) Hydrogen peroxide is the major oxidant product of xanthine oxidase. Free Radic. Biol. Med. 48:493-8.
44. Nam HJ, Park YY, Yoon G, Cho H, Lee JH. (2010) Co-treatment with hepatocyte growth factor and TGF-β1 enhance migration of HaCaT cells through NADPH oxidase-dependent ROS generation. Exp. Mol. Med. 42:270-9.
45. Fernandez ML, Upton Z, Shooter GK. (2014) Uric acid and xanthine oxidoreductase in wound healing. Curr. Rheumatol. Rep. 16:396.
46. Goldkorn T, et al. (1998) EGF-receptor phosphorylation and signaling are targeted by H2O2 redox stress. Am. J. Respir. Cell Mol. Biol. 19:786-98.
47. Peus D, et al. (1998) H2O2 is an important mediator of UVB-induced EGF-receptor phosphorylation in cultured keratinocytes. J. Invest. Dermatol. 110:966-71.
48. Kou B, Ni J, Vatish M, Singer DR. (2008) Xanthine oxidase interaction with vascular endothelial growth factor in human endothelial cell angiogenesis. Microcirculation. 15:251-67.
49. Bir SC, et al. (2012) Hydrogen sulfide stimulates ischemic vascular remodeling through nitric oxide synthase and nitrite reduction activity regulating hypoxia-inducible factor-1a and vascular endothelial growth factor-dependent angiogenesis. J. Am. Heart Assoc. 1:e004093.
50. Ichida, K, et al. (1997) Identification of two mutations in human xanthine dehydrogenase gene responsible for classical type I xanthinuria. J. Clin. Invest. 99:2391-7.
51. Mateos FA, Puig JG, Jimenez ML, Fox IH. (1987) Hereditary xanthinuria: evidence for enhanced hypozanthine salvage. J. Clin. Invest. 79:847-52.
52. Reiss J, Johnson JL. (2003) Mutations in the molybdenum cofactor biosynthetic genes MOCS1, MOCS2, and GEPH. Hum. Mutat. 21:569-76.