Enzyme-independent NO stores in human skin: Quantification and influence of UV radiation

Journal of Investigative Dermatology

Volumn 129, Issue 4, 2009, Pages 834-842

  Mowbray, Megan ^a   McLintock, Sara ^b   Weerakoon, Rebecca ^b   Lomatschinsky, Natalia ^b   Jones, Sarah ^b   Rossi, Adriano G ^c   Weller, Richard B ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE; NORADRENALIN;

ARTICLE; CONTROLLED STUDY; EPIDERMIS; HUMAN; HUMAN EXPERIMENT; MICRODIALYSIS; NORMAL HUMAN; PRIORITY JOURNAL; SALIVA; SKIN BLOOD VESSEL; SWEAT; ULTRAVIOLET RADIATION; VASOCONSTRICTION;

ADULT; FEMALE; HUMANS; MALE; NITRATES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRITES; S-NITROSOTHIOLS; SALIVA; SKIN; SWEAT; ULTRAVIOLET RAYS; VASOCONSTRICTION;

EID: 63149137743     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2008.296     Document Type: Article

References (67)

1. Adams LB, Franzblau SG, Vavrin Z, Hibbs JB Jr, Krahenbuhl JL (1991) - arginine-dependent macrophage effector functions inhibit metabolic activity of Mycobacterium leprae. J Immunol 147:1642-1646
2. Baudouin JE, Tachon P (1996) Constitutive nitric oxide synthase is present in normal human keratinocytes. J Invest Dermatol 106:428-31
3. Becherel PA, Mossalayi MD, LeGoff L, Frances C, Chosidow O, Debre P et al. (1994) Mechanism of anti-inflammatory action of retinoids on keratinocytes. Lancet 344:1570-1
4. Benjamin N, O'Driscoll F, Dougall H, Duncan C, Smith L, Golden M et al. (1994) Stomach NO synthesis [letter] [see comments]. Nature 368:502
5. Borland C (1991) Endothelium in control. Br Heart J 66:405
6. Boysen TC, Yanagawa S, Sato F, Sato K (1984) A modified anaerobic method of sweat collection. J Appl Physiol 56:1302-7
7. Bruch-Gerharz D, Ruzicka T, Kolb-Bachofen V (1998) Nitric oxide and its implications in skin homeostasis and disease-a review. Arch Dermatol Res 290:643-51
8. Bryan NS, Fernandez BO, Bauer SM, Garcia-Saura MF, Milsom AB, Rassaf T et al. (2005) Nitrite is a signaling molecule and regulator of gene expression in mammalian tissues. Nat Chem Biol 1:290-7
9. Bull HA, Hothersall J, Chowdhury N, Cohen J, Dowd PM (1996) Neuropeptides induce release of nitric oxide from human dermal microvascular endothelial cells. J Invest Dermatol 106:655-60
10. Cenci E, Romani L, Mencacci A, Spaccapelo R, Schiaffella E, Puccetti P et al. (1993) Interleukin-4 and interleukin-10 inhibit nitric oxide-dependent macrophage killing of Candida albicans. Eur J Immunol 23:1034-1038
11. Clough GF, Bennett AR, Church MK (1998) Measurement of nitric oxide concentration in human skin in vivo using dermal microdialysis. Exp Physiol 83:431-4
12. Feelisch M, Rassaf T, Mnaimneh S, Singh N, Bryan NS, Jourd'heuil D et al. (2002) Concomitant S-, N-, and heme-nitros(yl)ation in biological tissues and fluids: implications for the fate of NO in vivo. FASEB J 16:1775-85
13. Fleck A (1989) Latitude and ischaemic heart disease. Lancet 1:613
14. Furchgott RF (1971) Physiology and Pharmacology of Vascular Neuroeffector Systems. Karger: Basel 247:pp 247-82
15. Furchgott RF, Ehrreich SJ, Greenblatt E (1961) The photoactivated relaxation of smooth muscle of rabbit aorta. J Gen Physiol 44:499-519
16. Gladwin MT, Schechter AN, Kim-Shapiro DB, Patel RP, Hogg N, Shiva S et al. (2005) The emerging biology of the nitrite anion. Nat Chem Biol 1:308-14
17. Gorenflo M, Zheng C, Poge A, Bettendorf M, Werle E, Fiehn W et al. (2001) Metabolites of the L-arginine-NO pathway in patients with left-to-right shunt. Clin Lab 47:441-7
18. Hess DT, Matsumoto A, Nudelman R, Stamler JS (2001) S-nitrosylation: spectrum and specificity. Nat Cell Biol 3:E46-9
19. Ignarro LJ, Lippton H, Edwards JC, Baricos WH, Hyman AL, Kadowitz PJ et al. (1981) Mechanism of vascular smooth muscle relaxation by organic nitrates, nitrites, nitroprusside and nitric oxide: evidence for the involvement of S-nitrosothiols as active intermediates. J Pharmacol Exp Ther 218:739-49
20. Jones-Carson J, Vazquez-Torres A, van der Heyde HC, Warner T, Wagner RD, Balish E (1995) Gamma delta T cell-induced nitric oxide production enhances resistance to mucosal candidiasis. Nat Med 1:552-7
21. Klebanoff SJ (1993) Reactive nitrogen intermediates and antimicrobial activity: role of nitrite. Free Radic Biol Med 14:351-60
22. Kleinbongard P, Dejam A, Lauer T, Rassaf T, Schindler A, Picker O et al. (2003) Plasma nitrite reflects constitutive nitric oxide synthase activity in mammals. Free Radic Biol Med 35:790-6
23. Krischel V, Bruch-Gerharz D, Suschek C, Kroncke KD, Ruzicka T, Kolb-Bachofen V (1998) Biphasic effect of exogenous nitric oxide on proliferation and differentiation in skin derived keratinocytes but not fibroblasts. J Invest Dermatol 111:286-91
24. Kuhn A, Fehsel K, Lehmann P, Krutmann J, Ruzicka T, Kolb-Bachofen V (1998) Aberrant timing in epidermal expression of inducible nitric oxide synthase after UV irradiation in cutaneous lupus erythematosus. J Invest Dermatol 111:149-53
25. Lee PC, Salyapongse AN, Bragdon GA, Shears LL, Watkins SC, Edington HD et al. (1999) Impaired wound healing and angiogenesis in eNOS-deficient mice. Am J Physiol 277:H1600-8
26. Liew FY, Li Y, Moss D, Parkinson C, Rogers MV, Moncada S (1991) Resistance to Leishmania major infection correlates with the induction of nitric oxide synthase in murine macrophages. Eur J Immunol 21:3009-14
27. Liu X, Miller MJ, Joshi MS, Sadowska-Krowicka H, Clark DA, Lancaster JR Jr (1998) Diffusion-limited reaction of free nitric oxide with erythrocytes. J Biol Chem 273:18709-13
28. Lundberg JO, Govoni M (2004) Inorganic nitrate is a possible source for systemic generation of nitric oxide. Free Radic Biol Med 37:395-400
29. Lundberg JO, Weitzberg E, Cole JA, Benjamin N (2004) Nitrate, bacteria and human health. Nat Rev Microbiol 2:593-602
30. Mancinelli RL, McKay CP (1983) Effects of nitric oxide and nitrogen dioxide on bacterial growth. Appl Environ Microbiol 46:198-202
31. Marley R, Feelisch M, Holt S, Moore K (2000) A chemiluminescense-based assay for S-nitrosoalbumin and other plasma S-nitrosothiols. Free Radic Res 32:1-9
32. Marley R, Patel RP, Orie N, Ceaser E, Darley-Usmar V, Moore K (2001) Formation of nanomolar concentrations of S-nitroso-albumin in human plasma by nitric oxide. Free Radic Biol Med 31:688-96
33. Mcaninly J, Williams DLH, Askew SC, Butler AR, Russell C (1993) Metal-ion catalysis in nitrosothiol (RSNO) decomposition. Chem Commun, 1758-9
34. Meulemans A, Delsenne F (1994) Measurement of nitrite and nitrate levels in biological samples by capillary electrophoresis. J Chromatogr B Biomed Appl 660:401-4
35. Moncada S, Higgs A (1993) The L-arginine-nitric oxide pathway. N Engl J Med 329:2002-12
36. Moriel P, Pereira IR, Bertolami MC, Abdalla DS (2001) Is ceruloplasmin an important catalyst for S-nitrosothiol generation in hypercholesterolemia? Free Radic Biol Med 30:318-26
37. Mowbray M, Tan X, Wheatley PS, Morris RE, Weller RB (2008) Topically applied nitric oxide induces T-lymphocyte infiltration in human skin, but minimal inflammation. J Invest Dermatol 128:352-60
38. Paunel AN, Dejam A, Thelen S, Kirsch M, Horstjann M, Gharini P et al. (2005) Enzyme-independent nitric oxide formation during UVA challenge of human skin: characterization, molecular sources, and mechanisms. Free Radic Biol Med 38:606-15
39. Pelletier MM, Kleinbongard P, Ringwood L, Hito R, Hunter CJ, Schechter AN et al. (2006) The measurement of blood and plasma nitrite by chemiluminescence: pitfalls and solutions. Free Radic Biol Med 41:541-8
40. Rassaf T, Bryan NS, Kelm M, Feelisch M (2002) Concomitant presence of N-nitroso and S-nitroso proteins in human plasma. Free Radic Biol Med 33:1590-6
41. Rassaf T, Feelisch M, Kelm M (2004) Circulating NO pool: assessment of nitrite and nitroso species in blood and tissues. Free Radic Biol Med 36:413-22
42. Rocks SA, Davies CA, Hicks SL, Webb AJ, Klocke R, Timmins GS et al. (2005) Measurement of S-nitrosothiols in extracellular fluids from healthy human volunteers and rheumatoid arthritis patients, using electron paramagnetic resonance spectrometry. Free Radic Biol Med 39:937-48
43. Rodriguez J, Maloney RE, Rassaf T, Bryan NS, Feelisch M (2003) Chemical nature of nitric oxide storage forms in rat vascular tissue. Proc Natl Acad Sci USA 100:336-41
44. Romero-Graillet C, Aberdam E, Biagoli N, Massabni W, Ortonne JP, Ballotti R (1996) Ultraviolet B radiation acts through the nitric oxide and cGMP signal transduction pathway to stimulate melanogenesis in human melanocytes. J Biol Chem 271:28052-6
45. Romero-Graillet C, Aberdam E, Clement M, Ortonne JP, Ballotti R (1997) Nitric oxide produced by ultraviolet-irradiated keratinocytes stimulates melanogenesis. J Clin Invest 99:635-42
46. Rostand SG (1997) Ultraviolet light may contribute to geographic and racial blood pressure differences. Hypertension 30:150-6
47. Sakai M, Shimizu Y, Nagatsu I, Ueda H (1996) Immunohistochemical localization of NO synthases in normal human skin and psoriatic skin. Arch Dermatol Res 288:625-7
48. Schmidt HHHW, Kelm M (1996) In: Feelisch M, Stamler JS, eds. John Wiley: Chichester, pp 491-7
49. Spiegelhalder B, Eisenbrand G, Preussmann R (1976) Influence of dietary nitrate on nitrite content of human saliva: possible relevance to in vivo formation of N-nitroso compounds. Food Cosmet Toxicol 14:545-8
50. Stamler JS, Simon DI, Osborne JA, Mullins ME, Jaraki O, Michel T et al. (1992) S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proc Natl Acad Sci USA 89:444-8
51. Suschek CV, Krischel V, Bruch-Gerharz D, Berendji D, Krutmann J, Kroncke KD et al. (1999) Nitric oxide fully protects against UVA-induced apoptosis in tight correlation with Bcl-2 up-regulation. J Biol Chem 274:6130-7
52. Suschek CV, Schroeder P, Aust O, Sies H, Mahotka C, Horstjann M et al. (2003) The presence of nitrite during UVA irradiation protects from apoptosis. FASEB J 17:2342-4
53. Teixeira MM, Williams TJ, Hellewell PG (1993) Role of prostaglandins and nitric oxide in acute inflammatory reactions in guinea-pig skin. Br J Pharmacol 110:1515-21
54. Vaughn MW, Huang KT, Kuo L, Liao JC (2000) Erythrocytes possess an intrinsic barrier to nitric oxide consumption. J Biol Chem 275:2342-8
55. Wang R, Ghahary A, Shen YJ, Scott PG, Tredget EE (1996) Human dermal fibroblasts produce nitric oxide and express both constitutive and inducible nitric oxide synthase isoforms. J Invest Dermatol 106:419-27
56. Wang TJ, Pencina MJ, Booth SL, Jacques PF, Ingelsson E, Lanier K et al. (2008) Vitamin D deficiency and risk of cardiovascular disease. Circulation 117:503-11
57. Warren JB (1994) Nitric oxide and human skin blood flow responses to acetylcholine and ultraviolet light. FASEB J 8:247-51
58. Wei XQ, Charles IG, Smith A, Ure J, Feng GJ, Huang FP et al. (1995) Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 375:408-11
59. Weller R, Schwentker A, Billiar TR, Vodovotz Y (2003) Autologous nitric oxide protects mouse and human keratinocytes from ultraviolet B radiation-induced apoptosis. Am J Physiol Cell Physiol 284:C1140-8
60. Weller R, Pattullo S, Smith L, Golden M, Ormerod A, Benjamin N (1996) Nitric oxide is generated on the skin surface by reduction of sweat nitrate. J Invest Dermatol 107:327-31
61. Wink DA, Grisham MB, Mitchell JB, Ford PC (1996) Direct and indirect effects of nitric oxide in chemical reactions relevant to biology. Methods Enzymol 268:12-31
62. Witte MB, Kiyama T, Barbul A (2002a) Nitric oxide enhances experimental wound healing in diabetes. Br J Surg 89:1594-601
63. Witte MB, Thornton FJ, Tantry U, Barbul A (2002b) -arginine supplementation enhances diabetic wound healing: involvement of the nitric oxide synthase and arginase pathways. Metabolism 51:1269-73
64. Wolf R, Schonfelder G, Paul M, Blume-Peytavi U (2003) Nitric oxide in the human hair follicle: constitutive and dihydrotestosterone-induced nitric oxide synthase expression and NO production in dermal papilla cells. J Mol Med 81:110-7
65. Yamasaki K, Edington HD, McClosky C, Tzeng E, Lizonova A, Kovesdi I 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
66. Ysart G, Miller P, Barrett G, Farrington D, Lawrance P, Harrison N (1999) Dietary exposures to nitrate in the UK. Food Addit Contam 16:521-32
67. Zweier JL, Wang P, Samouilov A, Kuppusamy P (1995) Enzyme-independent formation of nitric oxide in biological tissues. Nat Med 1:804-9