The metabolic coupling of arginine metabolism to nitric oxide generation by astrocytes

Antioxidants and Redox Signaling

Volumn 8, Issue 5-6, 2006, Pages 919-928

  Gensert, Joann M ^a   Ratan, Rajiv R ^b  

^a Burke Cornell Medical Research Institute   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSPORTER; ARGININE; GLUTAMIC ACID; NITRIC OXIDE;

AMINO ACID METABOLISM; ASTROCYTE; BIOLOGY; BLOOD; BRAIN CELL; CELL FUNCTION; CELL INTERACTION; CEREBROSPINAL FLUID; ENDOTHELIUM; ENDOTHELIUM CELL; EPENDYMA CELL; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PARENCHYMA; PRECURSOR; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN SECRETION; PROTEIN TRANSPORT; REVIEW; SYNAPSE;

ANIMALS; ARGININE; ASTROCYTES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTAMIC ACID; HUMANS; ISOENZYMES; NEURONS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

EID: 33745825574     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2006.8.919     Document Type: Review

References (91)

1. Aarts M, Liu Y, Liu L, Besshoh S, Arundine M, Gurd JW, Wang YT, Salter MW, and Tymianski M. Treatment of ischemic brain damage by perturbing NMDA receptor-PSD-95 protein interactions. Science 298: 846-850, 2002.
2. Aoki E, Semba R, and Kashiwamata S. Evidence for the presence of L-arginine in the glial components of the peripheral nervous system. Brain Res 559: 159-162, 1991.
3. Aoki E, Semba R, Mikoshiba K, and Kashiwamata S. Pre-dominant localization in glial cells of free L-arginine. Immunocytochemical evidence. Brain Res 547: 190-192, 1991.
4. Bal-Price A, Moneer Z, and Brown GC. Nitric oxide induces rapid, calcium-dependent release of vesicular glutamate and ATP from cultured rat astrocytes. Glia 40: 312-223, 2002.
5. Bauer PM, Fukuto JM, Buga GM, Pegg AE, and Ignarro LJ. Nitric oxide inhibits ornithine decarboxylase by S-nitrosylation. Biochem Biophys Res Commun 262: 355-358, 1999.
6. Bernstein HG and Muller M. The cellular localization of the L-ornithine decarboxylase/polyamine system in normal and diseased central nervous systems. Prog Neurobiol 57: 485-505, 1999.
7. Blantz RC, Satriano J, Gabbai F, and Kelly C. Biological effects of arginine metabolites. Acta Physiol Scand 168: 21-25, 2000.
8. Braissant O, Honegger P, Loup M, Iwase K, Takiguchi M, and Bachmann C. Hyperammonemia: regulation of argininosuccinate synthetase and argininosuccinate lyase genes in aggregating cell cultures of fetal rat brain. Neurosci Lett 266: 89-92, 1999.
9. Brown GC, Bolanos JP, Heales SJ, and Clark JB. Nitric oxide produced by activated astrocytes rapidly and reversibly inhibits cellular respiration. Neurosci Lett 193: 201-204, 1995.
10. G-hydroxy-L-arginine during high-output NO production. Am J Physiol 271: H1988-1998, 1996.
11. Burnett AL, Lowenstein CJ, Bredt DS, Chang TS, and Snyder SH. Nitric oxide: a physiologic mediator of penile erection. Science 257: 401-403, 1992.
12. Buskila Y, Farkash S, Hershfinkel M, and Amitai Y. Rapid and reactive nitric oxide production by astrocytes in mouse neocortical slices. Glia 52: 169-176, 2005.
13. Cai D, Deng K, Mellado W, Lee J, Ratan RR, and Filbin MT. Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron 35: 711-719, 2002.
14. Chartrain NA, Geller DA, Koty PP, Sitrin NF, Nussler AK, Hoffman EP, Billiar TR, Hutchinson NI, and Mudgett JS. Molecular cloning, structure, and chromosomal localization of the human inducible nitric oxide synthase gene. J Biol Chem 269: 6765-6772, 1994.
15. Cirino G. Multiple controls in inflammation. Extracellular and intracellular phospholipase A2, inducible and constitutive cyclooxygenase, and inducible nitric oxide synthase. Biochem Pharmacol 55: 105-111, 1998.
16. 2+ homeostasis. Biochem Pharmacol 55: 713-718, 1998.
17. Corraliza IM, Modolell M, Ferber E, and Soler G. Involvement of protein kinase A in the induction of arginase in murine bone marrow-derived macrophages. Biochim Biophys Acta 1334: 123-128, 1997.
18. Cross AH, Keeling RM, Goorha S, San M, Rodi C, Wyatt PS, Manning PT, and Misko TP. Inducible nitric oxide synthase gene expression and enzyme activity correlate with disease activity in murine experimental autoimmune encephalomyelitis. J Neuroimmunol 71: 145-153, 1996.
19. Cross AH, Manning PT, Stern MK, and Misko TP. Evidence for the production of peroxynitrite in inflammatory CNS demyelination. J Neuroimmunol 80: 121-130, 1997.
20. Cross AH, Misko TP, Lin RF, Hickey WF, Trotter JL, and Tilton RG. Aminoguanidine, an inhibitor of inducible nitric oxide synthase, ameliorates experimental autoimmune encephalomyelitis in SJL mice. J Clin Invest 93: 2684-2690, 1994.
21. Davis KL, Martin E, Turko IV, and Murad F. Novel effects of nitric oxide. Annu Rev Pharmacol Toxicol 41: 203-236, 2001.
22. de Vera ME, Shapiro RA, Nussler AK, Mudgett JS, Simmons RL, Morris SM, Jr, Billiar TR, and Geller DA. Transcriptional regulation of human inducible nitric oxide synthase (NOS2) gene by cytokines: initial analysis of the human NOS2 promoter. Proc Natl Acad Sci USA 93: 1054-1059, 1996.
23. Do KQ, Binns KE, and Salt TE. Release of the nitric oxide precursor, arginine, from the thalamus upon sensory afferent stimulation, and its effect on thalamic neurons in vivo. Neuroscience 60: 581-586, 1994.
24. Do KQ, Grima G, Benz B, and Salt TE. Glial-neuronal transfer of arginine and S-nitrosothiols in nitric oxide transmission. Ann NY Acad Sci 962: 81-92, 2002.
25. Estall LB, Grant SJ, and Cicala GA. Inhibition of nitric oxide (NO) production selectively impairs learning and memory in the rat. Pharmacol Biochem Behav 46: 959-962, 1993.
26. Galea E, Feinstein DL, and Reis DJ. Induction of calcium-independent nitric oxide synthase activity in primary rat glial cultures. Proc Natl Acad Sci USA 89: 10945-10949, 1992.
27. Gao J, Morrison DC, Parmely TJ, Russell SW, and Murphy WJ. An interferon-gamma-activated site (GAS) is necessary for full expression of the mouse iNOS gene in response to interferon-gamma and lipopolysaccharide. J Biol Chem 272: 1226-1230, 1997.
28. Gao Y, Deng K, Hou J, Bryson JB, Barco A, Nikulina E, Spencer T, Mellado W, Kandel ER, and Filbin MT. Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo. Neuron 44: 609-621, 2004.
29. Griffin WS, Sheng JG, Royston MC, Gentleman SM, McKenzi JE, Graham DI, Roberts GW, and Mrak RE. Glial-neuronal interactions in Alzheimer's disease: the potential role of a 'cytokine cycle' in disease progression. Brain Pathol 8: 65-72, 1998.
30. Grima G, Benz B, and Do KQ. Glutamate-induced release of the nitric oxide precursor, arginine, from glial cells. Eur J Neurosci 9: 2248-2258, 1997.
31. Grima G, Cuenod M, Pfeiffer S, Mayer B, and Do KQ. Arginine availability controls the N-methyl-D-aspartate-induced nitric oxide synthesis: involvement of a glial-neuronal arginine transfer. J Neurochem 71: 2139-2144, 1998.
32. Hansel C, Batchelor A, Cuenod M, Garthwaite J, Knopfel T, and Do KQ. Delayed increase of extracellular arginine, the nitric oxide precursor, following electrical white matter stimulation in rat cerebellar slices. Neurosci Lett 142: 211-214, 1992.
33. Heneka MT and Feinstein DL. Expression and function of inducible nitric oxide synthase in neurons. J Neuroimmunol 114: 8-18, 2001.
34. Heneka MT, Schmidlin A, and Wiesinger H. Induction of argininosuccinate synthetase in rat brain glial cells after striatal microinjection of immunostimulants. J Cereb Blood Flow Metab 19: 898-907, 1999.
35. Hesse M, Modolell M, La Flamme AC, Schito M, Fuentes JM, Cheever AW, Pearce EJ, and Wynn TA. Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. J Immunol 167: 6533-6544, 2001.
36. Hewett SJ, Corbett JA, McDaniel ML, and Choi DW. Interferon-gamma and interleukin-1 beta induce nitric oxide formation from primary mouse astrocytes. Neurosci Lett 164: 229-232, 1993.
37. Ishide T, Hara Y, Maher TJ, and Ally A. Glutamate neurotransmission and nitric oxide interaction within the ventrolateral medulla during cardiovascular responses to muscle contraction. Brain Res 874: 107-115, 2000.
38. Jana M, Anderson JA, Saha RN, Liu X, and Pahan K. Regulation of inducible nitric oxide synthase in proinflammatory cytokine-stimulated human primary astrocytes. Free Radic Biol Med 38: 655-664, 2005.
39. Kara P and Friedlander MJ. Arginine analogs modify signal detection by neurons in the visual cortex. J Neurosci 19: 5528-5548, 1999.
40. Karin M and Delhase M. The I kappa B kinase (IKK) and NF-kappa B: key elements of proinflammatory signaling. Semin Immunol 12: 85-98, 2000.
41. Kendrick KM, Guevara-Guzman R, de la Riva C, Christensen J, Ostergaard K, and Emson PC. NMDA and kainate-evoked release of nitric oxide and classical transmitters in the rat striatum: in vivo evidence that nitric oxide may play a neuroprotective role. Eur J Neurosci 8: 2619-2634, 1996.
42. Khan NA, Quemener V, Seiler N, and Moulinoux JP. Mechanism of spermidine uptake in cultured mammalian cells and its inhibition by some polyamine analogues. Pathobiology 58: 172-178, 1990.
43. Kim N, Vardi Y, Padma-Nathan H, Daley J, Goldstein I, and Saenz de Tejada I. Oxygen tension regulates the nitric oxide pathway. Physiological role in penile erection. J Clin Invest 91: 431-442, 1993.
44. Lee J, Ryu H , Ferrante RJ, Morris SM, Jr, and Ratan RR. Translational control of inducible nitric oxide synthase expression by arginine can explain the arginine paradox. Proc Natl Acad Sci USA 100: 4843-4848, 2003.
45. Loih AK and Murphy S. Expression of nitric oxide synthase-2 in glia associated with CNS pathology. Prog Brain Res 118: 253-267, 1998.
46. Lowenstein CJ, Alley EW, Raval P, Snowma AM, Snyder SH, Russell SW, and Murphy WJ. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by Interferon gamma and lipopolysaccharide. Proc Natl Acad Sci USA 90: 9730-9734, 1993.
47. Manner CK, Nicholson B, and MacLeod CL. CAT2 arginine transporter deficiency significantly reduces iNOS-mediated NO production in astrocytes. J Neurochem 85: 476-482, 2003.
48. Marletta M.A. Nitric oxide synthase: aspects concerning structure and catalysis. Cell 78: 927-930, 1994.
49. Mazzanti M, Sul JY, and Haydon PG. Glutamate on demand: astrocytes as a ready source. Neuroscientist 7: 396-405, 2001.
50. Modolell M, Corraliza IM, Link F, Soler G, and Eichmann K. Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH1 and TH2 cytokines. Eur J Immunol 25: 1101-1104, 1995.
51. Mori M and Gotoh T. Regulation of nitric oxide production by arginine metabolic enzymes. Biochem Biophys Res Commun 275: 715-719, 2000.
52. Muller M, Pajunen AE, Jarvinen M, Poeggel G, and Bernstein HG. Immunohistochemical demonstration of L-ornithine decarboxylase enzyme protein in different areas of the developing human brain. Dev Neurosci 15: 87-93, 1993.
53. Murad F. The 1996 Albert Lasker Medical Research Awards. Signal transduction using nitric oxide and cyclic guanosine monophosphate. JAMA 276: 1189-1192, 1996.
54. Murad F. The nitric oxide-cyclic GMP signal transduction system for intracellular and intercellular communication. Recent Prog Horm Res 49: 239-248, 1994.
55. Murayama T, Oda H, Sasaki Y, Okada T, and Nomura Y. Regulation of inducible NO synthase expression by endothelin in primary cultured glial cells. Life Sci 62: 1491-1495, 1998.
56. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J 6: 3051-3064, 1992.
57. Neufeld AH and Liu B. Comparison of the signal transduction pathways for the induction of gene expression of nitric oxide synthase-2 in response to two different stimuli. Nitric Oxide 8: 95-102, 2003.
58. Nussler AK and Billiar TR. Inflammation, immunoregulation, and inducible nitric oxide synthase. J Leukoc Biol 54: 171-178, 1993.
59. Oh S. The generation of nitric oxide and its roles in neurotransmission and neurotoxicity. Keio J Med 44: 53-61, 1995.
60. Oleszak EL, Katsetos CD, Kuzmak J, and Varadhachary A. Inducible nitric oxide synthase in Theiler's murine encephalomyelitis virus infection. J Virol 71: 3228-3235, 1997.
61. Oleszak EL, Zaczynska E, Bhattacharjee M, Butunoi C, Legido A, and Katsetos CD. Inducible nitric oxide synthase and nitrotyrosine are found in monocytes/macrophages and/or astrocytes in acute, but not in chronic, multiple sclerosis. Clin Diagn Lab Immunol 5: 438-445, 1998.
62. Palomba L, Bianchi M, Persichini T, Magnani M, Colasanti M, and Cantoni O. Downregulation of nitric oxide formation by cytosolic phospholipase A2-released arachidonic acid. Free Radic Biol Med 36: 319-329, 2004.
63. Qiang M, Chen YC, Wang R, Wu FM, and Qiao JT. Nitric oxide is involved in the formation of learning and memory in rats: studies using passive avoidance response and Morris water maze task. Behav Pharmacol 8: 183-187, 1997.
64. Regunathan S and Piletz JE. Regulation of inducible nitric oxide synthase and agmatine synthesis in macrophages and astrocytes. Ann NY Acad Sci 1009: 20-29, 2003.
65. Robb SJ and Connor JR. Nitric oxide protects astrocytes from oxidative stress. Ann NY Acad Sci 962: 93-102, 2002.
66. Robb SJ, Gaspers LD, Wright KJ, Thomas AP, and Connor JR. Influence of nitric oxide on cellular and mitochondrial integrity in oxidatively stressed astrocytes. J Neurosci Res 56: 166-176, 1999.
67. Satriano J, Matsufuji S, Murakami Y, Lortie MJ, Schwartz D, Kelly CJ, Hayashi S, and Blantz RC. Agmatine suppresses proliferation by frameshift induction of antizyme and attenuation of cellular polyamine levels. J Biol Chem 273: 15313-15316, 1998.
68. Schmidlin A, Fischer S, and Wiesinger H. Transport of L-citrulline in neural cell cultures. Dev Neurosci 22: 393-398, 2000.
69. Schmidlin A and Wiesinger H. Argininosuccinate synthetase: localization in astrocytes and role in the production of glial nitric oxide. Glia 24: 428-436, 1998.
70. Schmidlin A and Wiesinger H. Transport of L-arginine in cultured glial cells. Glia 11: 262-268, 1994.
71. Segal MB, Preston JE, Collis CS, and Zlokovic BV. Kinetics and Na independence of amino acid uptake by blood side of perfused sheep choroid plexus. Am J Physiol 258: F1288-1294, 1990.
72. Segieth J, Fowler L, Whitton PS, and Pearce B. Arginine release from rat cerebellar astrocytes: autocrine roles for glutamate and nitric oxide? Neurosci Lett 372: 262-265, 2004.
73. Shiao YJ, Lin YL, Sun YH, Chi CW, Chen CF, and Wang CN. Falcarindiol impairs the expression of inducible nitric oxide synthase by abrogating the activation of IKK and JAK in rat primary astrocytes. Br J Pharmacol 144: 42-51, 2005.
74. Simmons ML and Murphy S. Cytokines regulate L-arginine-dependent cyclic GMP production in rat glial cells. Eur J Neurosci 5: 825-831, 1993.
75. Simmons ML and Murphy S. Roles for protein kinases in the induction of nitric oxide synthase in astrocytes. Glia 11: 227-234, 1994.
76. Song H, Ming G, He Z, Lehman M, McKerracher L, Tessier-Lavigne M, and Poo M. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281: 1515-1518, 1998.
77. Stevens BR, Kakuda DK, Yu K, Waters M, Vo CB, and Raizada MK. Induced nitric oxide synthesis is dependent on induced alternatively spliced CAT-2 encoding L-arginine transport in brain astrocytes. J Biol Chem 271: 24017-24022, 1996.
78. Stewart VC, Land JM, Clark JB, and Heales SJ. Pretreatment of astrocytes with interferon-alpha/beta prevents neuronal mitochondrial respiratory chain damage. J Neurochem 70: 432-434, 1998.
79. Stewart VC, Sharpe MA, Clark JB, and Heales SJ. Astrocyte-derived nitric oxide causes both reversible and irreversible damage to the neuronal mitochondrial respiratory chain. J Neurochem 75: 694-700, 2000.
80. Stoll J, Wadhwani KC, and Smith QR. Identification of the cationic amino acid transporter (System y+) of the rat blood-brain barrier. J Neurochem 60: 1956-1959, 1993.
81. Stone R, Stewart VC, Hurst RD, Clark JB, and Heales SJ. Astrocyte nitric oxide causes neuronal mitochondrial damage, but antioxidant release limits neuronal cell death. Ann NY Acad Sci 893: 400-403, 1999.
82. Stuhlmiller DF and Boje KM. Characterization of L-arginine and aminoguanidine uptake into isolated rat choroid plexus: differences in uptake mechanisms and inhibition by nitric oxide synthase inhibitors. J Neurochem 65: 68-74, 1995.
83. Tsikas D, Boger RH, and Sandmann J, Bode-Boger SM, and Frolich JC. Endogenous nitric oxide synthase inhibitors are responsible for the L-arginine paradox. FEBS Lett 478: 1-3, 2000.
84. Vega-Agapito V, Almeida A, Hatzoglou M, and Bolanos JP. Peroxynitrite stimulates L-arginine transport system y(+) in glial cells. A potential mechanism for replenishing neuronal L-arginine. J Biol Chem 277: 29753-29759, 2002.
85. Vega-Agapito V, Almeida A, Heales SJ, Medina JM, and Bolanos JP. Peroxynitrite anion stimulates arginine release from cultured rat astrocytes. J Neurochem 73: 1446-1452, 1999.
86. Wiesinger H. Arginine metabolism and the synthesis of nitric oxide in the nervous system. Prog Neurobiol 64: 365-391, 2001.
87. Wu G and Morris SM, Jr. Arginine metabolism: nitric oxide and beyond. Biochem J 336: 1-17, 1998.
88. Xie QW, Whisnant, R, and Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J Exp Med 177: 1779-1784, 1993.
89. Xu L, Hilliard B, Carmody RJ, Tsabary G, Shin H, Christianson DW, and Chen YH. Arginase and autoimmune inflammation in the central nervous system. Immunology 110: 141-148, 2003.
90. Yudkoff M, Nissim I, Nissim I, Stern J, and Pleasure D. Effects of palmitate on astrocyte amino acid contents. Neurochem Res 14: 367-370, 1989.
91. Zhang F and Iadecola C. Temporal characteristics of the protective effect of aminoguanidine on cerebral ischemic damage. Brain Res 802: 104-110, 1998.