Decoding the Substrate Supply to Human Neuronal Nitric Oxide Synthase

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Simon, Alexandra ^a   Karbach, Susanne ^a   Habermeier, Alice ^a   Closs, Ellen I ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CITRULLINE; CYCLIC GMP; HISTIDINE; LYSINE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PROTEINASE INHIBITOR;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CELL TYPE; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MOUSE; MULTIPLE SCLEROSIS; NEUROBLASTOMA CELL; NEUROEPITHELIOMA; NONHUMAN; PARKINSON DISEASE; RAT; SECOND MESSENGER;

ARGININE; CELL LINE; CITRULLINE; ENZYME ACTIVATION; EXTRACELLULAR SPACE; HUMANS; LYSOSOMES; NEUROBLASTOMA; NEURONS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; SUBSTRATE SPECIFICITY;

EID: 84879903065     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067707     Document Type: Article

References (51)

1. Förstermann U, Münzel T, (2006) Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 113: 1708-1714.
2. Cross AH, Keeling RM, Goorha S, San M, Rodi C, et al. (1996) Inducible nitric oxide synthase gene expression and enzyme activity correlate with disease activity in murine experimental autoimmune encephalomyelitis. Journal of neuroimmunology 71: 145-153.
3. Xu W, Liu LZ, Loizidou M, Ahmed M, Charles IG, (2002) The role of nitric oxide in cancer. Cell research 12: 311-320.
4. Christopherson KS, Bredt DS, (1997) Nitric oxide in excitable tissues: physiological roles and disease. The Journal of clinical investigation 100: 2424-2429.
5. Orlando GF, Langnaese K, Schulz C, Wolf G, Engelmann M, (2008) Neuronal nitric oxide synthase gene inactivation reduces the expression of vasopressin in the hypothalamic paraventricular nucleus and of catecholamine biosynthetic enzymes in the adrenal gland of the mouse. Stress 11: 42-51.
6. Prast H, Philippu A, (2001) Nitric oxide as modulator of neuronal function. Progress in neurobiology 64: 51-68.
7. Silverman RB, (2009) Design of selective neuronal nitric oxide synthase inhibitors for the prevention and treatment of neurodegenerative diseases. Accounts of chemical research 42: 439-451.
8. Orlando GF, Wolf G, Engelmann M, (2008) Role of neuronal nitric oxide synthase in the regulation of the neuroendocrine stress response in rodents: insights from mutant mice. Amino acids 35: 17-27.
9. Boissel JP, Bros M, Schrock A, Godtel-Armbrust U, Forstermann U, (2004) Cyclic AMP-mediated upregulation of the expression of neuronal NO synthase in human A673 neuroepithelioma cells results in a decrease in the level of bioactive NO production: analysis of the signaling mechanisms that are involved. Biochemistry 43: 7197-7206.
10. Schulz JB, Matthews RT, Klockgether T, Dichgans J, Beal MF, (1997) The role of mitochondrial dysfunction and neuronal nitric oxide in animal models of neurodegenerative diseases. Molecular and cellular biochemistry 174: 193-197.
11. Pou S, Keaton L, Surichamorn W, Rosen GM, (1999) Mechanism of superoxide generation by neuronal nitric-oxide synthase. The Journal of biological chemistry 274: 9573-9580.
12. Li L, Yang R, Sun K, Bai Y, Zhang Z, et al. (2011) Cerebroside-A provides potent neuroprotection after cerebral ischaemia through reducing glutamate release and Ca2+ influx of NMDA receptors. The international journal of neuropsychopharmacology/official scientific journal of the Collegium Internationale Neuropsychopharmacologicum: 1-11.
13. Dawson VL, Dawson TM, (1996) Nitric oxide neurotoxicity. Journal of chemical neuroanatomy 10: 179-190.
14. Malinski T, (2007) Nitric oxide and nitroxidative stress in Alzheimer's disease. Journal of Alzheimer's disease: JAD 11: 207-218.
15. Calabresi P, Di Filippo M, Gallina A, Wang Y, Stankowski JN, et al. (2012) New synaptic and molecular targets for neuroprotection in Parkinson's disease. Movement disorders: official journal of the Movement Disorder Society.
16. Colombo E, Cordiglieri C, Melli G, Newcombe J, Krumbholz M, et al. (2012) Stimulation of the neurotrophin receptor TrkB on astrocytes drives nitric oxide production and neurodegeneration. The Journal of experimental medicine 209: 521-535.
17. Hunot S, Boissiere F, Faucheux B, Brugg B, Mouatt-Prigent A, et al. (1996) Nitric oxide synthase and neuronal vulnerability in Parkinson's disease. Neuroscience 72: 355-363.
18. Haider L, Fischer MT, Frischer JM, Bauer J, Hoftberger R, et al. (2011) Oxidative damage in multiple sclerosis lesions. Brain: a journal of neurology 134: 1914-1924.
19. Verrey F, Closs EI, Wagner CA, Palacin M, Endou H, et al. (2004) CATs and HATs: the SLC7 family of amino acid transporters. Pflugers Archiv: European journal of physiology 447: 532-542.
20. Braissant O, Gotoh T, Loup M, Mori M, Bachmann C, (1999) L-arginine uptake, the citrulline-NO cycle and arginase II in the rat brain: an in situ hybridization study. Brain research Molecular brain research 70: 231-241.
21. Simon A, Plies L, Habermeier A, Martine U, Reining M, et al. (2003) Role of neutral amino acid transport and protein breakdown for substrate supply of nitric oxide synthase in human endothelial cells. Circulation research 93: 813-820.
22. Karbach S, Simon A, Slenzka A, Jaenecke I, Habermeier A, et al. (2011) Relative contribution of different l-arginine sources to the substrate supply of endothelial nitric oxide synthase. Journal of molecular and cellular cardiology 51: 855-861.
23. Bae SY, Xu Q, Hutchinson D, Colton CA, (2005) Y+ and y+ L arginine transporters in neuronal cells expressing tyrosine hydroxylase. Biochimica et biophysica acta 1745: 65-73.
24. Nawrath H, Wegener JW, Rupp J, Habermeier A, Closs EI, (2000) Voltage dependence of L-arginine transport by hCAT-2A and hCAT-2B expressed in oocytes from Xenopus laevis. American journal of physiology Cell physiology 279: C1336-1344.
25. Rotmann A, Closs EI, Liewald JF, Nawrath H, (2004) Intracellular accumulation of L-Arg, kinetics of transport, and potassium leak conductance in oocytes from Xenopus laevis expressing hCAT-1, hCAT-2A, and hCAT-2B. Biochimica et biophysica acta 1660: 138-143.
26. Kavanaugh MP, Wang H, Zhang Z, Zhang W, Wu YN, et al. (1994) Control of cationic amino acid transport and retroviral receptor functions in a membrane protein family. The Journal of biological chemistry 269: 15445-15450.
27. Giard DJ, Aaronson SA, Todaro GJ, Arnstein P, Kersey JH, et al. (1973) In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. Journal of the National Cancer Institute 51: 1417-1423.
28. Fujisawa H, Ogura T, Kurashima Y, Yokoyama T, Yamashita J, et al. (1994) Expression of two types of nitric oxide synthase mRNA in human neuroblastoma cell lines. Journal of neurochemistry 63: 140-145.
29. Ogura T, Nakayama K, Fujisawa H, Esumi H, (1996) Neuronal nitric oxide synthase expression in neuronal cell differentiation. Neuroscience letters 204: 89-92.
30. Edgell CJ, McDonald CC, Graham JB, (1983) Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proceedings of the National Academy of Sciences of the United States of America 80: 3734-3737.
31. Forstermann U, Gorsky LD, Pollock JS, Ishii K, Schmidt HH, et al. (1990) Hormone-induced biosynthesis of endothelium-derived relaxing factor/nitric oxide-like material in N1E-115 neuroblastoma cells requires calcium and calmodulin. Molecular pharmacology 38: 7-13.
32. Berson SA, Yalow RS, (1968) General principles of radioimmunoassay. Clinica chimica acta; international journal of clinical chemistry 22: 51-69.
33. Kraft PJ, Haynes-Johnson D, Bhattacharjee S, Lundeen SG, Qiu Y, (2004) Altered activities of cyclic nucleotide phosphodiesterases and soluble guanylyl cyclase in cultured RFL-6 cells. Int J Biochem Cell Biol 36: 2086-2095.
34. Closs EI, Scheld JS, Sharafi M, Forstermann U, (2000) Substrate supply for nitric-oxide synthase in macrophages and endothelial cells: role of cationic amino acid transporters. Molecular pharmacology 57: 68-74.
35. Marques C, Pereira P, Taylor A, Liang JN, Reddy VN, et al. (2004) Ubiquitin-dependent lysosomal degradation of the HNE-modified proteins in lens epithelial cells. The FASEB journal: official publication of the Federation of American Societies for Experimental Biology 18: 1424-1426.
36. Hibbs JB Jr, Vavrin Z, Taintor RR, (1987) L-arginine is required for expression of the activated macrophage effector mechanism causing selective metabolic inhibition in target cells. Journal of immunology 138: 550-565.
37. Nicholson B, Manner CK, Kleeman J, MacLeod CL, (2001) Sustained nitric oxide production in macrophages requires the arginine transporter CAT2. The Journal of biological chemistry 276: 15881-15885.
38. Bogle RG, Baydoun AR, Pearson JD, Moncada S, Mann GE, (1992) L-arginine transport is increased in macrophages generating nitric oxide. The Biochemical journal 284 (Pt 1): 15-18.
39. Rotmann A, Simon A, Martine U, Habermeier A, Closs EI, (2007) Activation of classical protein kinase C decreases transport via systems y+ and y+L. American journal of physiology Cell physiology 292: C2259-2268.
40. Baydoun AR, Bertran J, Thakur S, Dawson J, Palacin M, et al. (2006) y+ LAT-1 mediates transport of the potent and selective iNOS inhibitor, GW274150, in control J774 macrophages. Amino acids 31: 101-109.
41. Lerma J, Herranz AS, Herreras O, Abraira V, Martin del Rio R, (1986) In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain research 384: 145-155.
42. Schmidt HH, Pollock JS, Nakane M, Gorsky LD, Forstermann U, et al. (1991) Purification of a soluble isoform of guanylyl cyclase-activating-factor synthase. Proceedings of the National Academy of Sciences of the United States of America 88: 365-369.
43. Closs EI, Boissel JP, Habermeier A, Rotmann A, (2006) Structure and function of cationic amino acid transporters (CATs). The Journal of membrane biology 213: 67-77.
44. Leiper J, Vallance P, (1999) Biological significance of endogenous methylarginines that inhibit nitric oxide synthases. Cardiovascular research 43: 542-548.
45. Liu B, Du H, Rutkowski R, Gartner A, Wang X, (2012) LAAT-1 is the lysosomal lysine/arginine transporter that maintains amino acid homeostasis. Science 337: 351-354.
46. Jezegou A, Llinares E, Anne C, Kieffer-Jaquinod S, O'Regan S, et al. (2012) Heptahelical protein PQLC2 is a lysosomal cationic amino acid exporter underlying the action of cysteamine in cystinosis therapy. Proceedings of the National Academy of Sciences of the United States of America 109: E3434-3443.
47. Sakata K, Yamashita T, Maeda M, Moriyama Y, Shimada S, et al. (2001) Cloning of a lymphatic peptide/histidine transporter. The Biochemical journal 356: 53-60.
48. Yamashita T, Shimada S, Guo W, Sato K, Kohmura E, et al. (1997) Cloning and functional expression of a brain peptide/histidine transporter. The Journal of biological chemistry 272: 10205-10211.
49. Zhao C, Tampe R, Abele R, (2006) TAP and TAP-like-brothers in arms? Naunyn-Schmiedeberg's archives of pharmacology 372: 444-450.
50. Wyatt AW, Steinert JR, Mann GE (2004) Modulation of the L-arginine/nitric oxide signalling pathway in vascular endothelial cells. Biochemical Society symposium: 143-156.
51. Zhou L, Zhu DY, (2009) Neuronal nitric oxide synthase: structure, subcellular localization, regulation, and clinical implications. Nitric oxide: biology and chemistry/official journal of the Nitric Oxide Society 20: 223-230.