Genetic and pharmacological inhibition of dimethylarginine dimethylaminohydrolase 1 is protective in endotoxic shock

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 11, 2012, Pages 2589-2597

  Nandi, Manasi ^a   Kelly, Peter ^c   Torondel, Belen ^b   Wang, Zhen ^c   Starr, Anna ^a   Ma, Yue ^c   Cunningham, Philip ^a   Stidwill, Raymond ^b   Leiper, James ^c  

^a Centre for Research in Rehabilitation School of Health Science and Social Care   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c MRC CLINICAL SCIENCES CENTRE   (United Kingdom)

Author keywords

NO; Shock; Vascular

Indexed keywords

COMPLEMENTARY DNA; DIMETHYLARGININASE; ENZYME INHIBITOR; LIPOPOLYSACCHARIDE; MESSENGER RNA; NITRIC OXIDE; RECOMBINANT PROTEIN; AMIDASE;

ANESTHESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; ARTICLE; CATHETER; CELL CULTURE; CONTROLLED STUDY; ENDOTOXEMIA; ENZYME INHIBITION; HEMODYNAMICS; HEREDITY; HETEROZYGOTE; HYPOTENSION; MALE; MEDICAL DEVICE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; SEPTIC SHOCK; SHOCK; TELEMETRY; WILD TYPE; ANIMAL; C57BL MOUSE; CELL LINE; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; ENDOTHELIUM CELL; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MACROPHAGE; METABOLISM; MOUSE MUTANT; PATHOPHYSIOLOGY; RAT; SITE DIRECTED MUTAGENESIS; SPRAGUE DAWLEY RAT; TIME; TISSUE CULTURE TECHNIQUE;

AMIDOHYDROLASES; ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEMODYNAMICS; HUMANS; HYPOTENSION; LIPOPOLYSACCHARIDES; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTAGENESIS, SITE-DIRECTED; NITRIC OXIDE; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; RNA, MESSENGER; SHOCK, SEPTIC; TIME FACTORS; TISSUE CULTURE TECHNIQUES;

EID: 84871851533     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.300232     Document Type: Article

References (55)

1. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med. 2001;29:1303-1310.
2. Dellinger RP, Levy MM, Carlet JM, et al; International Surviving Sepsis Campaign Guidelines Committee; American Association of Critical-Care Nurses; American College of Chest Physicians; American College of Emergency Physicians; Canadian Critical Care Society; European Society of Clinical Microbiology and Infectious Diseases; European Society of Intensive Care Medicine; European Respiratory Society; International Sepsis Forum; Japanese Association for Acute Medicine; Japanese Society of Intensive Care Medicine; Society of Critical Care Medicine; Society of Hospital Medicine; Surgical Infection Society; World Federation of Societies of Intensive and Critical Care Medicine. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2008. Crit Care Med. 2008;36:296-327.
3. Rittirsch D, Huber-Lang MS, Flierl MA, Ward PA. Immunodesign of experimental sepsis by cecal ligation and puncture. Nat Protoc. 2009;4:31-36.
4. Link A, Selejan S, Maack C, Lenz M, Böhm M. Phosphodiesterase 4 inhibition but not beta-adrenergic stimulation suppresses tumor necrosis factor-alpha release in peripheral blood mononuclear cells in septic shock. Crit Care. 2008;12:R159.
5. Annane D, Trabold F, Sharshar T, Jarrin I, Blanc AS, Raphael JC, Gajdos P. Inappropriate sympathetic activation at onset of septic shock: a spectral analysis approach. Am J Respir Crit Care Med. 1999;160:458-465.
6. Silverman HJ, Penaranda R, Orens JB, Lee NH. Impaired beta-adrener-gic receptor stimulation of cyclic adenosine monophosphate in human septic shock: association with myocardial hyporesponsiveness to cat-echolamines. Crit Care Med. 1993;21:31-39.
7. Sakr Y, Reinhart K, Vincent JL, Sprung CL, Moreno R, Ranieri VM, De Backer D, Payen D. Does dopamine administration in shock infu-ence outcome? Results of the Sepsis Occurrence in Acutely Ill Patients (SOAP) Study. Crit Care Med. 2006;34:589-597.
8. De Backer D, Creteur J, Silva E, Vincent JL. Effects of dopamine, nor-epinephrine, and epinephrine on the splanchnic circulation in septic shock: which is best? Crit Care Med. 2003;31:1659-1667.
9. Levy B, Collin S, Sennoun N, Ducrocq N, Kimmoun A, Asfar P, Perez P, Meziani F. Vascular hyporesponsiveness to vasopressors in septic shock: from bench to bedside. Intensive Care Med. 2010;36:2019-2029.
10. De Backer D, Aldecoa C, Njimi H, Vincent JL. Dopamine versus nor-epinephrine in the treatment of septic shock: a meta-analysis&z.ast;. Crit Care Med. 2012;40:725-730.
11. Radomski MW, Palmer RM, Moncada S. Glucocorticoids inhibit the expression of an inducible, but not the constitutive, nitric oxide synthase in vascular endothelial cells. Proc Natl Acad Sci USA. 1990;87:10043-10047.
12. Rees DD, Cellek S, Palmer RM, Moncada S. Dexamethasone prevents the induction by endotoxin of a nitric oxide synthase and the associated effects on vascular tone: an insight into endotoxin shock. Biochem Biophys Res Commun. 1990;173:541-547.
13. Schulz R, Nava E, Moncada S. Induction and potential biological relevance of a Ca(2+)-independent nitric oxide synthase in the myocardium. Br J Pharmacol. 1992;105:575-580.
14. Baydoun AR, Bertran J, Thakur S, Dawson J, Palacín M, Knowles RG. y+ LAT-1 mediates transport of the potent and selective iNOS inhibitor, GW274150, in control J774 macrophages. Amino Acids. 2006;31:101-109.
15. Julou-Schaeffer G, Gray GA, Fleming I, Schott C, Parratt JR, Stoclet JC. Loss of vascular responsiveness induced by endotoxin involves L-arginine pathway. Am J Physiol. 1990;259(4 Pt 2):H1038-H1043.
16. Ochoa JB, Udekwu AO, Billiar TR, Curran RD, Cerra FB, Simmons RL, Peitzman AB. Nitrogen oxide levels in patients after trauma and during sepsis. Ann Surg. 1991;214:621-626.
17. Lorente JA, Landín L, Renes E, De Pablo R, Jorge P, Ródena E, Liste D. Role of nitric oxide in the hemodynamic changes of sepsis. Crit Care Med. 1993;21:759-767.
18. Landry DW, Oliver JA. The pathogenesis of vasodilatory shock. N Engl J Med. 2001;345:588-595.
19. Sharshar T, Gray F, Lorin de la Grandmaison G, Hopkinson NS, Ross E, Dorandeu A, Orlikowski D, Raphael JC, Gajdos P, Annane D. Apoptosis of neurons in cardiovascular autonomic centres triggered by inducible nitric oxide synthase after death from septic shock. Lancet. 2003;362:1799-1805.
20. Thiemermann C, Szabó C, Mitchell JA, Vane Jr. Vascular hyporeactiv-ity to vasoconstrictor agents and hemodynamic decompensation in hem-orrhagic shock is mediated by nitric oxide. Proc Natl Acad Sci USA. 1993;90:267-271.
21. Hollenberg SM, Cunnion RE, Zimmerberg J. Nitric oxide synthase inhibition reverses arteriolar hyporesponsiveness to catecholamines in septic rats. Am J Physiol. 1993;264(2 Pt 2):H660-H663.
22. Gunnett CA, Chu Y, Heistad DD, Loihl A, Faraci FM. Vascular effects of LPS in mice defcient in expression of the gene for inducible nitric oxide synthase. Am J Physiol. 1998;275(2 Pt 2):H416-H421.
23. Vouldoukis I, Riveros-Moreno V, Dugas B, Ouaaz F, Bécherel P, Debré P, Moncada S, Mossalayi MD. The killing of Leishmania major by human macrophages is mediated by nitric oxide induced after ligation of the Fc epsilon RII/CD23 surface antigen. Proc Natl Acad Sci USA. 1995;92:7804-7808.
24. Dugas B, Debré P, Moncada S. Nitric oxide, a vital poison inside the immune and infammatory network. Res Immunol. 1995;146:664-670.
25. Szabó C, Ischiropoulos H, Radi R. Peroxynitrite: biochemistry, patho-physiology and development of therapeutics. Nat Rev Drug Discov. 2007;6:662-680.
26. Rees DD, Monkhouse JE, Cambridge D, Moncada S. Nitric oxide and the haemodynamic profle of endotoxin shock in the conscious mouse. Br J Pharmacol. 1998;124:540-546.
27. Petros A, Bennett D, Vallance P. Effect of nitric oxide synthase inhibitors on hypotension in patients with septic shock. Lancet. 1991;338:1557-1558.
28. Petros A, Lamb G, Leone A, Moncada S, Bennett D, Vallance P. Effects of a nitric oxide synthase inhibitor in humans with septic shock. Cardiovasc Res. 1994;28:34-39.
29. López A, Lorente JA, Steingrub J, et al. Multiple-center, randomized, placebo-controlled, double-blind study of the nitric oxide synthase inhibitor 546C88: effect on survival in patients with septic shock. Crit Care Med. 2004;32:21-30.
30. Paik WK, Kim S. Enzymatic methylation of protein fractions from calf thymus nuclei. Biochem Biophys Res Commun. 1967;29:14-20.
31. Gary JD, Clarke S. RNA and protein interactions modulated by protein arginine methylation. Prog Nucleic Acid Res Mol Biol. 1998;61:65-131.
32. Leiper J, Nandi M. The therapeutic potential of targeting endogenous inhibitors of nitric oxide synthesis. Nat Rev Drug Discov. 2011;10:277-291.
33. Kakimoto Y, Akazawa S. Isolation and identifcation of N-G, N-G-and N-G, N'-G-dimethyl-arginine, N-epsilon-mono-, di-, and trimethylly-sine, and glucosylgalactosyl-and galactosyl-delta-hydroxylysine from human urine. J Biol Chem. 1970;245:5751-5758.
34. Vallance P, Leone A, Calver A, Collier J, Moncada S. Accumulation of an endogenous inhibitor of nitric oxide synthesis in chronic renal failure. Lancet. 1992;339:572-575.
35. Ogawa T, Kimoto M, Sasaoka K. Purifcation and properties of a new enzyme, NG, NG-dimethylarginine dimethylaminohydrolase, from rat kidney. J Biol Chem. 1989;264:10205-10209.
36. Ogawa T, Kimoto M, Sasaoka K. Occurrence of a new enzyme catalyzing the direct conversion of NG, NG-dimethyl-L-arginine to L-citrulline in rats. Biochem Biophys Res Commun. 1987;148:671-677.
37. Leiper JM, Santa Maria J, Chubb A, MacAllister RJ, Charles IG, Whitley GS, Vallance P. Identifcation of two human dimethylarginine dimethylami- nohydrolases with distinct tissue distributions and homology with micro-bial arginine deiminases. Biochem J. 1999;343 Pt 1:209-214.
38. Achan V, Broadhead M, Malaki M, Whitley G, Leiper J, MacAllister R, Vallance P. Asymmetric dimethylarginine causes hypertension and cardiac dysfunction in humans and is actively metabolized by dimethylarginine dimethylaminohydrolase. Arterioscler Thromb Vasc Biol. 2003;23:1455-1459.
39. Leiper J, Nandi M, Torondel B, et al. Disruption of methylarginine metabolism impairs vascular homeostasis. Nat Med. 2007;13:198-203.
40. Pullamsetti SS, Maring D, Ghofrani HA, Mayer K, Weissmann N, Rosengarten B, Lehner M, Schudt C, Boer R, Grimminger F, Seeger W, Schermuly RT. Effect of nitric oxide synthase (NOS) inhibition on macro-and microcirculation in a model of rat endotoxic shock. Thromb Haemost. 2006;95:720-727.
41. Chauhan SD, Seggara G, Vo PA, Macallister RJ, Hobbs AJ, Ahluwalia A. Protection against lipopolysaccharide-induced endothelial dysfunction in resistance and conduit vasculature of iNOS knockout mice. FASEB J. 2003;17:773-775.
42. Rossiter S, Smith CL, Malaki M, Nandi M, Gill H, Leiper JM, Vallance P, Selwood DL. Selective substrate-based inhibitors of mammalian dimeth-ylarginine dimethylaminohydrolase. J Med Chem. 2005;48:4670-4678.
43. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 2010;8:e1000412.
44. Leiper J, Murray-Rust J, McDonald N, Vallance P. S-nitrosylation of dimethylarginine dimethylaminohydrolase regulates enzyme activity: further interactions between nitric oxide synthase and dimethyl-arginine dimethylaminohydrolase. Proc Natl Acad Sci USA. 2002;99: 13527-13532.
45. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005;5:953-964.
46. Zhang X, Goncalves R, Mosser DM. The isolation and characterization of murine macrophages. Curr Protoc Immunol. 2008;Chapter 14:Unit 14.1.
47. Nandi M, Kelly P, Vallance P, Leiper J. Over-expression of GTP-cyclohydrolase 1 feedback regulatory protein attenuates LPS and cyto-kine-stimulated nitric oxide production. Vasc Med. 2008;13:29-36.
48. Rosser DM, Stidwill RP, Jacobson D, Singer M. Oxygen tension in the bladder epithelium rises in both high and low cardiac output endotox-emic sepsis. J Appl Physiol. 1995;79:1878-1882.
49. Teerlink T, Nijveldt RJ, de Jong S, van Leeuwen PA. Determination of arginine, asymmetric dimethylarginine, and symmetric dimethylarginine in human plasma and other biological samples by high-performance liquid chromatography. Anal Biochem. 2002;303:131-137.
50. Woods A, Heslegrave AJ, Muckett PJ, Levene A P, Clements M, Mobberley M, Ryder TA, Abu-Hayyeh S, Williamson C, Goldin RD, Ashworth A, Withers DJ, Carling D. LKB1 is required for hepatic bile acid transport and canalicular membrane integrity in mice. Biochem J. 2011;434:49-60.
51. Aisaka K, Mitani A, Kitajima Y, Ohno T, Ishihara T. Difference in pres-sor responses to NG-monomethyl-L-arginine between conscious and anesthetized rats. Jpn J Pharmacol. 1991;56:245-248.
52. Toda N, Toda H, Hatano Y. Nitric oxide: involvement in the effects of anesthetic agents. Anesthesiology. 2007;107:822-842.
53. Grover R, Zaccardelli D, Colice G, Guntupalli K, Watson D, Vincent JL. An open-label dose escalation study of the nitric oxide synthase inhibitor, N(G)-methyl-L-arginine hydrochloride (546C88), in patients with septic shock. Glaxo Wellcome International Septic Shock Study Group. Crit Care Med. 1999;27:913-922.
54. Hom GJ, Grant SK, Wolfe G, Bach TJ, MacIntyre DE, Hutchinson NI. Lipopolysaccharide-induced hypotension and vascular hyporeactivity in the rat: tissue analysis of nitric oxide synthase mRNA and protein expression in the presence and absence of dexamethasone, NG-monomethyl-L-arginine or indomethacin. J Pharmacol Exp Ther. 1995;272:452-459.
55. Hu X, Atzler D, Xu X, Zhang P, Guo H, Lu Z, Fassett J, Schwedhelm E, Böger RH, Bache RJ, Chen Y. Dimethylarginine dimethylaminohy-drolase-1 is the critical enzyme for degrading the cardiovascular risk factor asymmetrical dimethylarginine. Arterioscler Thromb Vasc Biol. 2011;31:1540-1546.