Age-related changes in ADMA-DDAH-NO pathway in rat liver subjected to partial ischemia followed by global reperfusion

Experimental Gerontology

Volumn 50, Issue 1, 2013, Pages 45-51

  Trocha, Małgorzata ^a   Merwid Lad, Anna ^a   Chlebda Sieragowska, Ewa ^a   Szuba, Andrzej ^a,b   Pieśniewska, Małgorzata ^a   Fereniec Gołebiewska, Lidia ^a   Kwiatkowska, Joanna ^a   Szelag, Adam ^a   Sozański, Tomasz ^a  

^a WROCLAW MEDICAL UNIVERSITY   (Poland)

^b 4TH MILITARY HOSPITAL   (Poland)

Author keywords

ADMA; Age; INOS; Ischemia reperfusion; Liver; Rat

Indexed keywords

6 N,N' DIMETHYLARGININE; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; DIMETHYLARGININASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; N(G),N(G) DIMETHYLARGININE;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME SYNTHESIS; LIVER BLOOD FLOW; LIVER FUNCTION; LIVER INJURY; LIVER ISCHEMIA; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION; TRANSCRIPTION REGULATION; VASODILATATION;

70KDA HEAT SHOCK PROTEIN; A/A RATIO; ADMA; AGE; ALANINE AMINOTRANSFERASE; ALT; ARG; ARGININE; ARGININE/ADMA RATIO; ASPARAGINE AMINOTRANSFERASE; AST; ASYMMETRIC DIMETHYLARGININE; DDAH; DIMETHYLARGININE DIMETHYLAMINOHYDROLASE; ELISA; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENOS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HIGH-PERFORMANCE LIQUID CHROMATOGRAPHY; HPLC; HSP70; INDUCIBLE NITRIC OXIDE SYNTHASE; INOS; IR; ISCHEMIA/REPERFUSION; L-NMMA; LIVER; MACROPHAGE INFLAMMATORY PROTEIN 2; MIP-2; N(G)-MONOMETHYL-L-ARGININE; NADPH; NF-KAPPA B; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NITRIC OXIDE; NO; NUCLEAR FACTOR KAPPA B; PRMTS; PROTEIN ARGININE METHYLTRANSFERASES; RAT; REACTIVE OXYGEN SPECIES; ROS; SDMA; SYMMETRIC DIMETHYLARGININE; TNFΑ; TUMOR NECROSIS FACTOR Α;

AGING; AMIDOHYDROLASES; ANIMALS; ARGININE; LIVER; MALE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, WISTAR; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TRANSAMINASES;

EID: 84890218225     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2013.11.004     Document Type: Article

References (53)

1. Abe Y., Hines I.N., Zibari G., Pavlick K., Gray L., Kitagawa Y., Grisham M.B. Mouse model of liver ischemia and reperfusion injury: method to study reactive oxygen and nitrogen metabolites in vivo. Free Radic. Biol. Med. 2009, 46:1-7.
2. Alkofer B., Samstein B., Guarrera J.V., Kin C., Jan D., Bellemare S., Kinkhabwala M., Brown R., Emond J.C., Renz J.F. Extended-donor criteria liver allografts. Semin. Liver Dis. 2006, 26:221-233.
3. Anantharaju A., Feler A., Chedid A. Aging liver. Gerontology 2002, 48:343-353.
4. Boger R.H., Bode-Boger S.M., Szuba A., Tsao P.S., Chan J.R., Tangphao O., Blaschke T.F., Cooke J.P. Asymmetric dimethylarginine (ADMA): a novel risk factor for endothelial dysfunction: its role in hypercholesterolemia. Circulation 1998, 98:1842-1847.
5. Buttery L.D., Springall D.R., Chester A.H., Evans T.J., Stanfield E.N., Parums D.V., Yacoub M.H., Polak J.M. Inducible nitric oxide synthase is present within human atherosclerotic lesions and promotes the formation and activity of peroxynitrite. Lab. Invest. 1996, 1996(75):77-85.
6. Chobanyan K., Thum T., Suchy M.T., Zhu B., Mitschke A., Gutzki F.M., Beckmann B., Stichtenoth D.O., Tsikas D. GC-MS assay for hepatic DDAH activity in diabetic and non-diabetic rats by measuring dimethylamine (DMA) formed from asymmetric dimethylarginine (ADMA): evaluation of the importance of S-nitrosothiols as inhibitors of DDAH activity in vitro and in vivo in humans. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2007, 858:32-41.
7. Clavien P.A., Selzner M., Rudiger H.A., Graf R., Kadry Z., Rousson V., Jochum W. A prospective randomized study in 100 consecutive patients undergoing major liver resection with versus without ischemic preconditioning. Ann. Surg. 2003, 238:843-850.
8. Collins B.H., Pirsch J.D., Becker Y.T., Hanaway M.J., Van der Werf W.J., D'Alessandro A.M., Knechtle S.J., Odorico J.S., Leverson G., Musat A., Armbrust M., Becker B.N., Sollinger H.W., Kalayoglu M. Long-term results of liver transplantation in patients 60years of age and older. Transplantation 2000, 70:780-783.
9. Dimitrow P.P., Undas A., Bober M., Tracz W., Dubiel J.S. Plasma biomarkers of endothelial dysfunction in patients with hypertrophic cardiomyopathy. Pharmacol. Rep. 2007, 59:715-720.
10. Fan C., Zwacka R.M., Engelhardt J.F. Therapeutic approaches for ischemia/reperfusion injury in the liver. J. Mol. Med. 1999, 77:577-596.
11. Feng S., Goodrich N.P., Bragg-Gresham J.L., Dykstra D.M., Punch J.D., DebRoy M.A., Greenstein S.M., Merion R.M. Characteristics associated with liver graft failure: the concept of a donor risk index. Am. J. Transplant. 2006, 6:783-790.
12. Foster R., Zimmermann M., Trotter J.F. Expanding donor options: marginal, living and split donors. Clin. Liver Dis. 2007, 11:417-429.
13. Fu A., Nair K.S. Age effect on fibrinogen and albumin synthesis in humans. Am. J. Physiol. 1998, 275:E1023-E1030.
14. Furchgott R.F. The 1996 Albert Lasker Medical Research Awards. The discovery of endothelium-derived relaxing factor and its importance in the identification of nitric oxide. JAMA 1996, 276:1186-1188.
15. Gasbarrini A., Pasini P., Nardo B., De Notariis S., Simoncini M., Cavallari A., Roda E., Bernardi M., Roda A. Chemiluminescent real time imaging of post-ischemic oxygen free radicals formation in livers isolated from young and older rats. Free Radic. Biol. Med. 1998, 24:211-216.
16. Habior A., Rawa T., Krawczyk M., Zych W., Nyckowski P., Zieniewicz K., Butruk E. Transplantacja watroby - ocena zapotrzebowania, wskazania i zasady kwalifikacji. Med. Sci. Rev. - Hepatologia 2002, 2:85-90.
17. Hierholzer C., Harbrecht B., Menezes J.M., Kane J., Mac-Micking J., Nathan C.F., Peitzman A.B., Billiar T.R., Tweardy D.J. Essential role of induced nitric oxide in the initiation of the inflammatory response after hemorrhagic shock. J. Exp. Med. 1998, 187:917-928.
18. Hines I.N., Harada H., Flores S., Gao B., McCord J.M., Grisham M.B. Endothelial nitric oxide synthase protects the post-ischemic liver: potential interactions with superoxide. Biomed. Pharmacother. 2005, 59:183-189.
19. Hornig B., Arakawa N., Böger R.H., Bode-Böger S.M., Frölich J.C., Drexler H. Plasma levels of ADMA are increased and inversely related to endothelium-mediated vasodilation in patients with chronic heart failure: a new predictor of endothelial dysfunction?. Circulation 1998, 98. (Suppl. I-318).
20. Ignarro L.J. Endothelium derived nitric oxide: actions and properties. FASEB J. 1989, 3:31-36.
21. Kang E.S., Tevlin M.T., Wang Y.B., Chiang T.M., Cardenas R., Myers L.K., Acchiardo S.R. Hemodialysis hypotension: interaction of inhibitors, iNOS, and the interdialytic period. Am. J. Med. Sci. 1999, 317:9-21.
22. Kelly D.M., Shiba H., Nakagawa S., Irefin S., Eghtesad B., Quintini C., Aucejo F., Hashimoto K., Fung J.J., Miller C. Hepatic blood flow plays an important role in ischemia-reperfusion injury. Liver Transpl. 2011, 17:1448-1456.
23. Kireev R.A., Cuesta S., Ibarrola C., Bela T., Moreno G.E., Vara E., Tresguerres J.A. Age-related differences in hepatic ischemia/reperfusion: gene activation, liver injury, and protective effect of melatonin. Surg. Res. 2012, 178:922-934.
24. Kobayashi H., Nonami T., Kurokawa T., Takeuchi Y., Harada A., Nakao A., Takagi H. Role of endogenous nitric oxide in ischemia reperfusion injury in the rat liver. J. Surg. Res. 1995, 59:772-779.
25. Laleman W., Omasta A., Van de Casteele M., Zeegers M., Vander E.I., Van Landeghem L., Severi T., van Pelt J., Roskams T., Fevery J., Nevens F. A role for asymmetric dimethylarginine in the pathophysiology of portal hypertension in rats with biliary cirrhosis. Hepatology 2005, 42:1382-1390.
26. Le Couteur D.G., Rivory L.P., Pond S.M. The effects of aging and nutritional state on hypoxia-reoxygenation injury in the perfused rat liver. Transplantation 1994, 58:531-536.
27. Leiper J., Vallance P. Biological significance of endogenous methylarginines that inhibit nitric oxide synthases. Cardiovasc. Res. 1999, 43:542-548.
28. Leiper J., Murray-Rust J., McDonald N., Vallance P. S-nitrosylation of dimethylarginine dimethylaminohydrolase regulates enzyme activity: further interactions between nitric oxide synthase and dimethylarginine dimethylaminohydrolase. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:13527-13532.
29. Lhuillier F., Parmantier P., Goudable J., Crova P., Delafosse B., Annat G., Cespuglio R., Viale J.P. Hepatic ischemia is associated with an increase in liver parenchyma nitric oxide that is in part enzyme-independent. Anesthesiology 2003, 98:373-378.
30. Lin K.Y., Ito A., Asagami T., Tsao P.S., Adimoolam S., Kimoto M., Tsuji H., Reaven G.M., Cooke J.P. Impaired nitric oxide synthase pathway in diabetes mellitus: role of asymmetric dimethylarginine and dimethylarginine dimethylaminohydrolase. Circulation 2002, 106:987-992.
31. Martin-Sanz P., Olmedilla L., Dulin E., Casado M., Callejas N.A., Pérez-Peña J., Garutti I., Sanz J., Calleja J., Barrigón S., Boscá L. Presence of methylated arginine derivatives in orthotopic human liver transplantation: relevance for liver function. Liver Transpl. 2003, 9:40-48.
32. Massip-Salcedo M., Roselló-Catafau J., Prieto J., Avíla M.A., Peralta C. The response of the hepatocyte to ischemia. Liver Int. 2007, 27:6-16.
33. Mishima T., Hamada T., Ui-Tei K., Takahashi F., Miyata Y., Imaki J., Suzuki H., Yamashita K. Expression of DDAH1 in chick and rat embryos. Brain Res. Dev. Brain Res. 2004, 148:223-232.
34. Mookerjee R.P., Dalton R.N., Davies N.A., Hodges S.J., Turner C., Williams R., Jalan R. Inflammation is an important determinant of levels of the endogenous nitric oxide synthase inhibitor asymmetric dimethylarginine (ADMA) in acute liver failure. Liver Transpl. 2007, 13:400-405.
35. Nijveldt R.J., Teerlink T., Siroen M.P., van Lambalgen A.A., Rauwerda J.A., van Leeuwen P.A. The liver is an important organ in the metabolism of asymmetrical dimethylarginine (ADMA). Clin. Nutr. 2003, 22:17-22.
36. Okaya T., Blanchard J., Schuster R., Kuboki S., Husted T., Cadwell C.C., Zingarelli B., Wong H., Solomkin J.S., Lentsch A.B. Age-dependent responses to hepatic ischemia/reperfusion injury. Shock 2005, 24:421-427.
37. Parker R.A., Huang Q., Tesfamariam B. Influence of 3-hydroxy-3-methylglutaryl-CoA (HMG-CoA) reductase inhibitors on endothelial nitric oxide synthase and the formation of oxidants in the vasculature. Atherosclerosis 2003, 169:19-29.
38. Peralta C., Rull R., Rimola A., Deulofeu R., Roselló-Catafau J., Gelpí E., Rodés J. Endogenous nitric oxide and exogenous nitric oxide supplementation in hepatic ischemia-reperfusion injury in the rat. Transplantation 2001, 71:529-536.
39. Rivera-Chavez F.A., Toledo-Pereyra L.H., Dean R.E., Crouch L., Ward P.A. Exogenous and endogenous nitric oxide but not iNOS inhibition improves function and survival of ischemically injured livers. J. Invest. Surg. 2001, 14:267-273.
40. Scalera F., Borlak J., Beckmann B., Martens-Lobenhoffer J., Thum T., Tager M., Bode-Boger S.M. Endogenous nitric oxide synthesis inhibitor asymmetric dimethyl l-arginine accelerates endothelial cell senescence. Arterioscler. Thromb. Vasc. Biol. 2004, 24:1816-1822.
41. Schemmer P., Connor H.D., Arteel G.E., Raleigh J.A., Bunzendahl H., Mason R.P., Thurman R.G. Reperfusion injury in livers due to gentle in situ organ manipulation during harvest involves hypoxia and free radicals. J. Pharmacol. Exp. Ther. 1999, 290:235-240.
42. Schmucker D.L. Aging and the liver: an update. J. Gerontol. 1998, 53A:B315-B320.
43. Shah V., Haddad F.G., Garcia-Cardena G., Frangos J.A., Mennone A., Groszmann R.J., Sessa W.C. Liver sinusoidal endothelial cells are responsible for nitric oxide modulation of resistance in the hepatic sinusoids. J. Clin. Invest. 1997, 100:2923-2930.
44. Sohal R.S., Mockett R.J., Orr W.C. Mechanisms of aging: an appraisal of the oxidative stress hypothesis. Free Radic. Biol. Med. 2002, 33:575-586.
45. Tran C.T., Leiper J.M., Vallance P. The DDAH/ADMA/NOS pathway. Atherosclerosis 2003, (4 Suppl.):33-40.
46. Trocha M., Szelag A., Pieśniewska M., Fereniec - Goebiewska L., Grotthus B., Merwid - Lad A. Effect of aging process on liver function in extracorporeal rat liver perfusion. Hepato-Gastroenterology 2007, 54:1207-1211.
47. Trocha M., Merwid-Lad A., Szuba A., Chlebda E., Pieśniewska M., Sozański T., Szelag A. Effect of simvastatin on nitric oxide synthases (eNOS, iNOS) and arginine and its derivatives (ADMA, SDMA) in ischemia/reperfusion injury in rat liver. Pharmacol. Rep. 2010, 62:343-351.
48. Trocha M., Merwid-Lad A., Szuba A., Sozański T., Magdalan J., Szelag A. Asymmetric dimethylarginine synthesis and degradation under physiological and pathological conditions. Adv. Clin. Exp. Med. 2010, 19:223-243.
49. Trocha M., Merwid-Lad A., Sozański T., Chlebda E., Szuba A., Dziegiel P., Pieśniewska M., Fereniec-Gołebiewska L., Kwiatkowska J., Gomułkiewicz A., Cwynar-Zajac Ł., Brykner R., Szelag A. Influence of ezetimibe on ADMA-DDAH-NO pathway in rat liver subjected to partial ischemia followed by global reperfusion. Pharm. Rep. 2013, 65:122-133.
50. Ueda S., Kato S., Matsuoka H., Kimoto M., Okuda S., Morimatsu M., Imaizumi T. Regulation of cytokine-induced nitric oxide synthesis by asymmetric dimethylarginine: role of dimethylarginine dimethylaminohydrolase. Circ. Res. 2003, 92:226-233.
51. Vallance P., Leiper J. Cardiovascular biology of the asymmetric dimethylarginine: dimethylarginine dimethylaminohydrolase pathway. Arterioscler. Thromb. Vasc. Biol. 2004, 24:1023-1030.
52. Wnuk Z., Kokot F., Kunsdorf-Wnuk A. Diagnostic value of plasma asymmetric and symmetric dimethylarginine levels in liver transplant recipients. Pol. Arch. Int. Med. 2012, 122:367-373.
53. Xiong Y., Fu Y.F., Fu S.H., Zhou H.H. Elevated levels of the serum endogenous inhibitor of nitric oxide synthase and metabolic control in rats with streptozotocin-induced diabetes. J. Cardiovasc. Pharmacol. 2003, 42:191-196.