Expression of an inducible nitric oxide synthase gene in rainbow trout Oncorhynchus mykiss

Developmental and Comparative Immunology

Volumn 23, Issue 1, 1999, Pages 71-85

  Laing, Kerry J ^c   Hardie, Laura J ^a,c   Aartsen, Wendy ^c   Grabowski, Peter S ^b,c   Secombes, Christopher J ^c  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Expression; Fish; INOS; Macrophages; RT CR; Sequence

Indexed keywords

GAMMA INTERFERON; IMMUNOMODULATING AGENT; INTERLEUKIN 1; LIPOPOLYSACCHARIDE; NITRIC OXIDE SYNTHASE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; ENZYME INDUCTION; EVOLUTION; FISH; GENE EXPRESSION; GENE SEQUENCE; GENETIC DISTANCE; MACROPHAGE; MOLECULAR CLONING; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; RAINBOW TROUT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY;

AVES; CARASSIUS AURATUS; EUKARYOTA; GALLUS GALLUS; MAMMALIA; MYKISS; ONCORHYNCHUS MYKISS; SALMONIDAE;

EID: 0033031623     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0145-305X(98)00036-6     Document Type: Article

References (65)

1. Knowles RG, Moncada S. Nitric oxide synthases in mammals. Biochem. J. 1994;298:249-258.
2. Bredt DS, Hwang PM, Snyder SH. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 1990;347:768-770.
3. Bredt DS, Hwang PM, Glatt CE, Lowenstein C, Reed RR, Snyder SH. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 1991;351:714-718.
4. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J. 1992;6:3051-3064.
5. Bredt DS, Snyder SH. Isolation of nitric oxide synthase, a calmodulin-requiring enzyme. In: Proceedings of Natl. Acad. Sci. USA, Vol. 87, 1990. pp. 682-685.
6. Janssens SP, Shimouchi A, Quertermous T, Bloch DB, Bloch KD. Cloning and expression of a cDNA encoding human endothelium-derived relaxing factor/nitric oxide synthase. J. Biol. Chem. 1992;267:14519-14522.
7. Nishida K, Harrison DG, Navas JP, Fisher AA, Dockery SP, Uematsu M, Nerem RM, Alexander RW, Murphy TJ. Molecular cloning and characterization of the constitutive bovine aortic endothelial cell nitric oxide synthase. J. Clin. Invest. 1992;90:2092-2096.
8. Steuhr D, Marletta MA. Mammalian nitrate biosynthesis: mouse macrophages produce nitrite and nitrate in response to Escherichia coli lipopolysaccharide. In: Proceedings of Natl. Acad. Sci. USA, Vol. 82, 1985. pp. 7738-7742.
9. Nussler AK, Billiar TR. Inflammation, immunoregulation, and inducible nitric oxide synthase. J. Leukocyte Biol. 1993;54:171-178.
10. Kunz D, Muhl H, Walker G, Pfeilschifter J. Two distinct signaling pathways trigger the expression of inducible nitric oxide synthase in rat renal mesangial cells. In: Proceedings of Natl. Acad. Sci. USA, Vol. 91, 1994. pp. 5387-5391.
11. Yui Y, Hatori R, Kosuga K, Eizawa H, Hiki K, Kawai C. Purification of nitric oxide synthase from rat macrophages. J. Biol. Chem. 1991;266:12544-12547.
12. Gross SS, Jaffe EA, Levi R, Kilbourn RG. Cytokine-activated endothelial cells express an isotype of nitric oxide synthase which is tetrahydrobiopterin-dependent, calmodulin-independent and inhibited by arginine analogs with a rank-order of potency characteristic of activated macrophages. Biochem. Biophys. Res. Comm. 1991;178: 823-829.
13. Steuhr DJ, Cho HJ, Kwon SS, Weise MF, Nathan CF. Purification and characterization of the cytokine-induced macrophage nitric oxide synthase: an FAD- and FMN-containing flavoprotein. In: Proceedings of Natl. Acad. Sci. USA, Vol. 88, 1991. pp. 7773-7777.
14. Lyons CR, Orloff GJ, Cunningham JM. Molecular cloning and functional expression of an inducible nitric oxide synthase from a murine macrophage cell line. J. Biol. Chem. 1992;267:6370-6374.
15. Delpozo V, Dearrudachaves E, Deandres B, Cardaba B, Lopezfarre A, Gallardo S, Cortegano I, Vidarte L, Jurado A, Sastre J, Palomino P, Lahoz C. Eosinophils transcribe and translate messenger RNA for inducible nitric oxide synthase. J. Immunol. 1997;158:859-864.
16. Qureshi AA, Hosoi J, Xu S, Takashima A, Granstein RD, Lerner EA. Langerhans cells express inducible nitric oxide synthase and produce nitric oxide. J. Investigative Dermatol. 1996;107:815-821.
17. Wood ER, Berger Jr. H, Sherman PA, Lapetina EG. Hepatocytes and macrophages express an identical cytokine inducible nitric oxide synthase gene. Biochem. Biophys. Res. Comm. 1993;191:767-774.
18. Chartrain NA, Geller DA, Koty PP, Sitrin NF, Nussler AK, Hoffman EP, Billiar TR, Hutchinson NI, Mudgett JS. Molecular cloning, structure, and chromosomal localization of the human inducible nitric oxide synthase gene. J. Biol Chem. 1994;269:765-6772.
19. Maier R, Bilbe G, Rediske J, Lotz M. Inducible nitric oxide synthase from human articular chondrocytes: cDNA cloning and analysis of mRNA expression. Biochim. Biophys. Acta 1994;1208:145-150.
20. Moncada S. The L-arginine: nitric oxide pathway. Acta Physiol. Scand. 1992;145:201-227.
21. Moncada S, Higgs A. The L-arginine-nitric oxide pathway. New Eng. J. Med. 1993;329:2002-2012.
22. Liew FY, Milliott S, Parkinson C, Palmer RMJ, Moncada S. Macrophage killing of Leishmania parasite in vivo is mediated by nitric oxide from L-arginine. J. Immunol. 1990;144:4794-4797.
23. Green SJ, Meltzer MS, Hibbs Jr. JB, Nacy CA. Activated macrophages destroy intracellular leishmania major amastigotes by an L-arginine-dependent killing mechanism. J. Immunol. 1990;144:278-283.
24. Werner-Felmeyer G, Golderer G, Werner ER, Gröbner P, Wachter H. Pteridine biosynthesis and nitric oxide synthase in Physarum polycephalum. Biochem J. 1994;304:105-111.
25. Elphick MR, Green IC, O'Shea M. Nitric oxide synthesis and action in an invertebrate brain. Brain Research 1993;619:344-346.
26. Ribeiro JMC, Nussenveig RH. Nitric oxide synthase activity from a haematophagus insect salivary gland. FEBS 1993;330:165-168.
27. Gelperin A. Nitric oxide mediates network oscillations of olfactory interneurones in a terrestrial mollusc. Nature 1994;369:61-63.
28. Ottaviani E, Paemen LR, Cadet P, Stefano GB. Evidence for nitric oxide production and utilization as a bacteriocidal agent by invertebrate immunocytes. Eur. J. Pharm. 1993;248:319-324.
29. Martinez A, Riveros-Moreno V, Polak JM, Moncada S, Sesma P. Nitric oxide (NO) synthase immunoreactivity in the starfish Marhasterias glacialis. Cell Tissue Res. 1994;275:599-603.
30. Huque T, Brand JG. Nitric oxide synthase activity of the taste organ of the channel catfish, Ictalurus punctatus. Comp. Biochem. Physiol. 1994;108B:481-486.
31. Östholm T, Holmqvist BI, Aim P, Ekstrom P. Nitric oxide in the CNS of the atlantic salmon. Neuroscience Letters 1994;168:233-237.
32. Schoor WP, Plumb JA. Induction of nitric oxide synthase in channel catfish Ictalurus punctatus by Edwardsiella ictaluri. Dis. Aquat. Organisms 1994;19:153-155.
33. Neumann NF, Fagan D, Belosevic M. Macrophage activating factor(s)secreted by mitogen stimulated goldfish kidney leukocytes synergize with bacterial lipopolysaccharide to induce nitric oxide production in teleost macrophages. Dev. Comp. Immunol. 1995;19:473-482.
34. Nöll GN, Billek M, Pietruck C, Schmidt K-F. Inhibition of nitric oxide synthase alters light responses and dark voltage of amphibian photoreceptors. Neuropharmacology 1994;33:1407-1412.
35. Leipe BA, Stone C, Koistinaho J, Copenhagen DR. Nitric oxide synthase in Muller cells and neurons of salamander and fish retina. J. Neuroscience 1994;14:7641-7654.
36. Knight GE, Burnstock G. Acetylcholine induces relaxation via the release of nitric oxide from endotheilial cells of the garter snake (Thamnophis sirtalis parietalis) aorta. Comp. Biochem. Physiol. 1993;106:383-388.
37. Brüning G, Wiese S, Mayer B. Nitric oxide synthase in the brain of the turtle Pseudemys scripta elegans. J. Comp. Neurol. 1994;348:183-206.
38. Brüning G, Funk U, Mayer B. Immunocytochemical localization of nitric oxide synthase in the brain of the chicken. NeuroReport 1994;5:2425-2428.
39. Lin AW, Chang CC, McCormick CC. Molecular cloning and expression of an avian macrophage nitric-oxide synthase cDNA and the analysis of the genomic 5′-flanking region. J. Biol. Chem. 1996;271:11911-11919.
40. 2+/calmodulin-dependent nitric oxide synthase. In: Proceedings of Natl. Acad. Sci. USA, Vol. 92, 1995. pp. 9027-9076.
41. Yuda M, Hirai M, Miura K, Matsumura H, Ando K, Chinzei Y. cDNA cloning, expression and characterization of nitric-oxide synthase from the salivary glands of the blood-sucking insect Rhodnius prolixus. Eur. J. Biochem. 1996;242:807-812.
42. Secombes CJ, Hardie LJ, Daniels G. Cytokines in fish: an update. Fish Shellfish Immunol. 1996;6:291-304.
43. Laing KJ, Grabowski PS, Belosevic M, Secombes CJ. A partial sequence for nitric oxide synthase from a goldfish (Carassius auratus) macrophage cell line. Immunol Cell Biol. 1996;74:374-379.
44. Marsden MJ, Vaughan LM, Foster TJ, Secombes CJ. A live (ΔaroA) Aeromonas salmonicida vaccine for furunculosis preferentially stimulates T-cell responses relative to B-cell responses in rainbow trout (Oncorhynchus mykiss). Infect. Immun. 1996;64:3863-3869.
45. Secombes CJ. Isolation of salmonid macrophages and analysis of their killing activity. In: Stolen JS, Fletcher TC, Anderson DP, Roberson S, van Muiswinkel WB, editors. Techniques in fish immunology. Fair Haven, New Jersey: SOS Publications, 1990. pp. 137-154.
46. Ralston SH, Todd D, Helfrich M, Benjamin N, Grabowski PS. Human osteoblast-like cells produce nitric oxide and express inducible nitric oxide synthase. Endocrinology 1994;135:330-336.
47. Benson D, Boguski M, Lipman DJ, Ostell J. Genbank, Nucleic Acids Res. 1994;22:3441-3444.
48. Higgins DG, Sharp PM. CLUSTAL: a package for performing multiple alignment on a microcomputer. Gene 1988;73:237-244.
49. Hardie LJ, Laing KJ, Daniels GD, Grabowski PS, Cunningham C, Secombes CJ. Isolation of the first piscine transforming growth factor β gene: analysis reveals tissue specific expression and a potential regulatory sequence in rainbow trout (Oncorhynchus mykiss). Cytokine (in press).
50. Rysavy FR, Bishop MJ, Gibbs GP, Williams GW. The UK Human Genome Mapping Project online computing service. Computer Applications in the Biosciences 1992;8:149-154.
51. Altschul SF, Gish W, Miller W, Myers E, Lipman DJ. Basic local alignment search tool. J. Mol. Biol. 1990;215:403-410.
52. Needleman SB, Wunsch CD. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 1970;48:443-453.
53. Saitou N, Nei M. The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987;4:406-425.
54. Xie QW, Cho HJ, Calaycay J, Mumford R, Swiderek KM, Lee TB, Ding A, Troso T, Nathan C. Cloning and characterization of inducible nitric oxide synthase from mouse macrophage. Science 1992;256:225-228.
55. Knowles R. Nitric oxide synthases. The Biochemist 1994;16:3-6.
56. Bredt DS, Ferris CD, Snyder SH. Nitric oxide synthase regulatory sites: phosphorylation by cyclic AMP-dependent protein kinase, protein kinase C, and calcium/calmodulin protein kinase, identification of flavin and calmodulin binding sites. J. Biol. Chem. 1992;267:10976-10981.
57. Busse R, Mülsch A. Calcium-dependent nitric oxide synthesis in endothelial cytosol is mediated by calmodulin. FEBS Lett. 1990;265:133-136.
58. O'Neill KT, Degrado WF. How calmodulin binds its targets: sequence independent recognition of amphiphilic α-helices. Trends Biochem. Sci. 1990;15:59-64.
59. Baek KJ, Thiel BA, Lucas S, Steuhr DJ. Macrophage nitric oxide synthase subunits: purification, characterization, and role of prosthetic groups and substrate in regulating their association into dimeric enzyme. J. Biol. Chem. 1993;268:21120-21129.
60. Ogden JE, Moore PK. Inhibition of nitric oxide synthase -potential for a novel class of therapeutic agent? Trends in Biotech. 1995;13:70-78.
61. Schober A, Malz CR, Meyer DL. Enzymehistochemical demonstration of nitric oxide synthase in the diencephalon of the rainbow trout (Oncorhynchus mykiss). Neurosci. Lett. 1993;151:67-70.
62. Schober A, Malz CR, Schober W, Meyer DL. NADPH-diaphorase in the central nervous system of the larval lamprey (Lampetra planeri). J. Comp. Neurol. 1994;345:94-104.
63. Adler H, Frech B, Thöny M, Pfister H, Peterhans E, Jungi TW. Inducible nitric oxide synthase in cattle: differential cytokine regulation of nitric oxide synthase in bovine and murine macrophages. J. Immunol. 1995;154:4710-4718.
64. Wang R, Neumann NF, Shen Q, Belosevic M. Establishment and characterization of a macrophage cell line from the goldfish. Fish & Shellfish Immunology. 1995;5: 329-346.
65. Anderson DP. Environmental factors in fish health: immunological aspects. In: Iwama G, Nakanishi T, editors. The fish immune system. Organism, pathogen, and environment. San Diego: Academic Press, 1996. pp. 63-103.