The Importance of Nitric Oxide and Arginase in the Pathogenesis of Acute Neuroinflammation: Are Those Contra Players with the Same Direction?

Neurotoxicity Research

Volumn 26, Issue 4, 2014, Pages 392-399

  Ljubisavljevic, Srdjan ^a,b   Stojanovic, Ivana ^b   Pavlovic, Radmila ^b   Pavlovic, Dusica ^b  

^a CLINICAL CENTER NIS   (Serbia)

^b UNIVERSITY OF NI   (Serbia)

Author keywords

Arginase; Neuroinflammation; Nitric oxide

Indexed keywords

ARGINASE; GADOBUTROL; NITRATE; NITRIC OXIDE; NITRITE;

ADOLESCENT; ADULT; ARTICLE; BLOOD ANALYSIS; CEREBROSPINAL FLUID ANALYSIS; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DEMYELINATING DISEASE; DISEASE ACTIVITY; ENZYME ACTIVITY; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PATHOGENESIS; CROSS-SECTIONAL STUDY; METABOLISM; MIDDLE AGED; PATHOLOGY; SEVERITY OF ILLNESS INDEX; YOUNG ADULT;

ADOLESCENT; ADULT; ARGINASE; CROSS-SECTIONAL STUDIES; DEMYELINATING DISEASES; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; NITRIC OXIDE; SEVERITY OF ILLNESS INDEX; YOUNG ADULT;

EID: 84919386605     PISSN: 10298428     EISSN: 14763524     Source Type: Journal    
DOI: 10.1007/s12640-014-9470-3     Document Type: Article

References (45)

1. Acar G, Idiman F, Idiman E, Kırkalı G, Çakmakçı H, Özakbas S (2003) Nitric oxide as an activity marker in multiple sclerosis. J Neurol 250:588–592
2. Ahn M, Lee C, Jung K, Kim H, Moon C, Sim KB, Shin T (2012a) Immunohistochemical study of arginase-1 in the spinal cords of rats with clip compression injury. Brain Res 1445:11–19
3. Ahn M, Yang W, Kim H, Jin JK, Moon C, Shin T (2012b) Immunohistochemical study of arginase-1 in the spinal cords of Lewis rats with experimental autoimmune encephalomyelitis. Brain Res 1453:77–86
4. Bansal V, Ochoa B (2003) Arginine availability, arginase, and the immune response. Curr Opin Clin Nutrit Met Care 6:223–228
5. Brettschneider J, Petzold A, Junker A, Tumani H (2006) Axonal damage markers in the cerebrospinal fluid of patients with clinically isolated syndrome improve predicting conversion to definite multiple sclerosis. Mult Scler 12:143–148
6. Broholm H, Andersen B, Wanscher B, Frederiksen JL, Rubin I, Pakkenberg B, Larsson HBW, Lauritzen M (2004) Nitric oxide synthase expression and enzymatic activity in multiple sclerosis. Acta Neurol Scand 109:261–269
7. Bronte V, Zanovello P (2005) Regulation of immune responses by l-arginine metabolism. Nat Rev Immunol 5:641–654
8. Danilov AI, Andersson M, Bavand N, Wiklund NP, Olsson T, Brundin L (2003) Nitric oxide metabolite determinations reveal continuous inflammation in multiple sclerosis. J Neuroimmunol 136:112–118
9. Durante W, Fruzsina K, Johnson FJ, Johnson RA (2007) Arginase: a critical regulator of nitric oxide synthesis and vascular function. Clin Exp Pharmacol Physiol 34:906–911
10. El-Gayar S, Thuring-Nahler H, Pfeilschifter J, Rollinghoff M, Bogdan C (2003) Translational control of inducible nitric oxide synthase by IL-13 and arginine availability in inflammatory macrophages. J Immunol 171:4561–4568
11. Hill KE, Zollinger LV, Watt HE, Carlson NG, Rose JW (2004) Inducible nitric oxide synthase in chronic active multiple sclerosis plaques: distribution, cellular expression and association with myelin damage. J Neuroimmunol 151:171–179
12. Ibragic S, Sofic E, Suljic E, Avdagic N, Bajraktarevic A, Tahirovic I (2012) Serum nitric oxide concentrations in patients with multiple sclerosis and patients with epilepsy. J Neural Transm 119:7–11
13. Jolivalt CG, Howard RB, Chen LS, Mizisin AP, Lai CS (2003) A novel nitric oxide scavenger in combination with cyclosporine A ameliorates experimental autoimmune encephalomyelitis progression in mice. J Neuroimmunol 138(1–2):56–64
14. Kahl KG, Zielasek J, Uttenthal LO, Rodrigo J, Toyka KV, Schmidt HH (2003) Protective role of the cytokine-inducible isoform of nitric oxide synthase induction and nitrosative stress in experimental autoimmune encephalomyelitis of the DA rat. J Neurosci Res 73:198–205
15. Kahl KG, Schmidt HHW, Jung S, Sherman P, Toyka KV, Zielasek J (2004) Experimental autoimmune encephalomyelitis in mice with a targeted deletion of the inducible nitric oxide synthase gene: increased T-helper 1 response. Neurosci Lett 358(1):58–62
16. Kapoor R, Davies M, Blaker PA, Hall SM, Smith KJ (2003) Blockers of sodium and calcium entry protect axons from nitric oxide-mediated degeneration. Ann Neurol 53(2):174–180
17. Kepka-Lenhart D, Mistry SK, Wu G, Morris SM (2000) Arginase I: a limiting factor for nitric oxide and polyamine synthesis by activated macrophages? Am J Physiol Regul Integr Comp Physiol 279:R2237–R2242
18. Kim H, Ahn M, Choi S, Kim M, Sim KB, Kim J, Moon C, Shin T (2013) Potential role of fibronectin in microglia/macrophage activation following cryoinjury in the rat brain: an immunohistochemical study. Brain Res 1502:11–19
19. King NE, Rothenberg ME, Zimmermann N (2004) Arginine in asthma and lung inflammation. J Nutr 134:2830S–2836S
20. Kuhlmann T, Lingfeld G, Bitsch A, Schuchardt J, Bruck W (2002) Acute axonal damage in multiple sclerosis is most extensive in early disease stages and decreases over time. Brain 125:2202–2212
21. Kurtzke JF (1983) Rating neurologic impairment in multiple sclero-sis: an expanded disability status scale (EDSS). Neurology 33:1444–1452
22. Lassmann H (2003) Axonal injury in multiple sclerosis. J Neurol Neurosurg Psychiatry 74:695–697
23. Lee J, Ryu H, Ferrante RJ, Morris SM Jr, Ratan RR (2003) Translational control of inducible nitric oxide synthase expression by arginine can explain the arginase paradox. Proc Natl Acad Sci USA 100:4843–4848
24. Li H, Meininger CJ, Hawker JR, Haynes TE, Kepka-Lenhart D, Mistry SK, Morris SM Jr, Wu G (2001) Regulatory role of arginase I and II in nitric oxide, polyamine, and proline synthesis in endothelial cells. Am J Physiol Endocrinol Metab 280:E75–E82
25. Ljubisavljevic S, Stojanovic I, Pavlovic R, Sokolovic D, Pavlovic D, Cvetkovic T, Stevanovic I (2012) Modulation of nitric oxide synthase by arginase and methylated arginines during the acute phase of experimental multiple sclerosis. J Neurol Sci 318(1–2):106–111
26. Ljubisavljevic S, Stojanovic I, Vojinovic S, Stojanov D, Stojanovic S, Cvetkovic T, Savic D, Pavlovic D (2013a) The patients with clinically isolated syndrome and relapsing remitting multiples sclerosis show different levels of advanced protein oxidation products and reduced thiols content in sera and CSF. Neurochem Int 62(7):988–997
27. Ljubisavljevic S, Stojanovic I, Vojinovic S, Stojanov D, Stojanovic S, Kocic G, Savic D, Cvetkovic T, Pavlovic D (2013b) Cerebrospinal fluid and plasma oxidative stress biomarkers in different clinical phenotypes of neuroinflammatory acute attacks. Conceptual accession: from fundamental to clinic. Cell Mol Neurobiol 33:767–777
28. Lublin FD, Reingold SC (1996) Defining the clinical course of multiple sclerosis: results of an international survey— National Multiple Sclerosis Society (USA) Advisory Committee on Clinical Trials of New Agents in Multiple Sclerosis. Neurology 46:907–911
29. Marchetti B, Morale MC, Brouwer J, Tirolo C, Testa N, Caniglia S, Barden N, Amor S, Smith PA, Dijkstra CD (2002) Exposure to a dysfunctional glucocorticoid receptor from early embryonic life programs the resistance to experimental autoimmune encephalomyelitis via nitric oxide-induced immunosuppression. J Immunol 168(11):5848–5859
30. Moncada S, Bolanos JP (2006) Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 97:1676–1689
31. Mori M, Gotoh T (2004) Arginine metabolic enzymes, nitric oxide and infection. J Nutr 134:2820S–2825S
32. Navaro-Gonzalvez JA, Garcia-Benayas C, Arenas J (1998) Semiautomated measurement of nitrate in biological fluids. Clin Chem 44:679–681
33. Nicholson B, Manner CK, Kleeman J, MacLeod CL (2001) Sustained nitric oxide production in macrophages requires the arginine transporter CAT2. J Biol Chem 276:15881–15885
34. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, Lublin FD, Montalban X, O’Connor P, Sandberg-Wollheim M, Thomp-son AJ, Waubant E, Weinshenker B, Wolinsky JS (2011) Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald criteria. Ann Neurol 69(2):292–302
35. Porembska Z, Kedra M (1975) Early diagnosis of myocardial infarction by arginase activity determination. Clin Chim Acta 60:355–361
36. Rejdak K, Eikelenboom MJ, Petzold A, Thompson EJ, Stelmasiak Z, Lazeron RH, Barkhof F, Polman CH, Uitdehaag BM, Giovannoni G (2004) CSF nitric oxide metabolites are associated with activity and progression of multiple sclerosis. Neurology 63:1439–1445
37. Rejdak K, Petzold A, Stelmasiak Z, Giovannoni G (2008) Cerebrospinal fluid brain specific proteins in relation to nitric oxide metabolites during relapse of multiple sclerosis. Mult Scler 14:59–66
38. Rodríguez-Sáinz MC, Sánchez-Ramón S, de Andrés C, Rodríguez-Mahou M, Muñoz-Fernández MA (2002) Th1/Th2 cytokine balance and nitric oxide in cerebrospinal fluid and serum from patients with multiple sclerosis. Eur Cytokine Netw 13(1):110–114
39. Roghani M, Mahboudi F, Saharian MA, Etemadifar M, Esfahani AN, Nahrevanian H, Elahi E (2010) Concentrations of nitric oxide metabolites in the serum of Iranian multiple sclerosis patients. J Neurol Sci 294:92–94
40. Shin T, Ahn M, Matsumoto Y (2012) Mechanism of experimental autoimmune encephalomyelitis in Lewis rats: recent insights from macrophages. Anat Cell Biol 45(3):141–148
41. Shin T, Ahn M, Matsumoto Y, Moon C (2013a) Mechanism of experimental autoimmune neuritis in Lewis rats: the dual role of macrophages. Histol Histopathol 28(6):679–684
42. Shin T, Ahn M, Moon C, Kim S, Sim KB (2013b) Alternatively activated macrophages in spinal cord injury and remission: another mechanism for repair? Mol Neurobiol 47(3):1011–1019
43. Smith KJ, Lassmann H (2002) The role of nitric oxide in multiple sclerosis. Lancet Neurol 1(4):232–241
44. Staykova MA, Paridaen JT, Cowden WB, Willenborg DO (2005) Nitric Oxide Contributes to Resistance of the Brown Norway Rat to Experimental Autoimmune Encephalomyelitis. Am J Pathol 166(1):147–157
45. Xu L, Hilliard B, Carmody RJ, Tsabary G, Shin H, Christianson DW, Chen YH (2003) Arginase and autoimmune inflammation in the central nervous system. Immunol 110:141–148