The Michael Mason prize essay 1997. Nitric oxide and bone: What a gas!

British Journal of Rheumatology

Volumn 36, Issue 8, 1997, Pages 831-838

  Ralston, S H ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Bone; Nitric oxide; Nitric oxide synthase; Rheumatoid arthritis

Indexed keywords

CYTOKINE; ESTROGEN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

BONE; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; TISSUE INJURY;

EID: 0030850373     PISSN: 02637103     EISSN: None     Source Type: Journal    
DOI: 10.1093/rheumatology/36.8.831     Document Type: Review

References (87)

1. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987;327:524-6.
2. Moncada S, Higgs A. The L-arginine nitric oxide pathway. N Engl J Med 1993;329:2002-12.
3. Palmer RMJ. The L-arginine nitric oxide pathway. Curr Opin Nephrol Hypertension 1993;2:122-8.
4. Benjamin N, O'Driscoll F, Dougall H et al. Stomach NO synthesis. Nature 1994;368-502.
5. Moncada S, Palmer RMJ, Higgs EA. Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol Rev 1991;43:109-42.
6. 2 system. Anal Chem 1993;65:1794-9.
7. Bredt DS, Snyder SH. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci USA 1990;87:682-5.
8. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnock JS, Tannenbaum SR. Analysis of nitrate, nitrite and and (15N) nitrate in biological fluids. Anal Biochem 1982;126:131-8.
9. 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;351:714-8.
10. Robinson LJ, Weremowicz S, Morton CC, Michel T. Isolation and chromosomal localization of the human endothelial nitric oxide synthase (nos3) gene. Genomics 1994;19:350-7.
11. Lowenstein CJ, Glatt CS, Bredt DS, Snyder SH. Cloned and expressed macrophage nitric oxide synthase contrasts with the brain enzyme. Proc Natl Acad Sci USA 1992;89:6711-5.
12. Marietta M. Nitric oxide synthase structure and mechanism. J Biol Chem 1993;268:12231-234.
13. Jenkins DC, Charles IG, Baylis SA, Lelchuk R, Radomski MW, Moncada S. Human colon cancer cell lines show a diverse pattern of nitric oxide synthase gene expression and nitric oxide generation. Br J Cancer 1994;70:847-9.
14. Salter M, Knowles RG, Moncada S. Widespread tissue distribution, species distribution and changes in activity of Ca(2+)-dependent and Ca(2+)-independent nitric oxide synthases. FEBS Lett 1991;291:145-9.
15. Brandi ML, Hukkanen M, Umeda T et al. Bidirectional regulation of osteoclast function by nitric oxide synthase isoforms. Proc Natl Acad Sci USA 1995;92:2954-8.
16. Evans DE, Helfrich MH, Grabowski PS, Pollock JS, Ohshima H, Ralston SH. Expression of Nitric Oxide synthase isoforms in bone and bone cell cultures. J Bone Miner Res 1997;12: in press.
17. Venema RC, Nishida K, Alexander RW, Harrison DG, Murphy TJ. Organisation of the bovine gene encoding the endothelial nitric oxide synthase. Biochim Biophys Acta 1993;1218:413-20.
18. Weiner CP, Lizasoain I, Baylis SA, Knowles RG, Charles IG, Moncada S. Induction of calcium-dependent nitric oxide synthases by sex hormones. Proc Natl Acad Sci USA 1994;91:5212-6.
19. Hayashi T, Yamada K, Esaki T et al. Estrogen increases endothelial nitric oxide by a receptor-mediated system. Biochem Biophys Res Commun 1995;214:847-55.
20. Uematsu M, Ohara Y, Navas JP et al. Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress. Am J Physiol 1995;269:C1371-8.
21. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J 1992;6:3051-64.
22. Nunokawa Y, Ishida N, Tanaka S. Promoter analysis of human inducible nitric oxide synthase gene associated with cardiovascular homeostasis. Biochem Biophys Res Commun 1994;200:802-7.
23. Xie QW, Kashiwabara Y, Nathan C. Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J Biol Chem 1994;269:4705-8.
24. Xie Q, Whisnant R, Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J Exp Med 1993;177:1779-84.
25. Lowenstein CJ, Alley EW, Raval P et al. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc Natl Acad Sci USA 1993;90:9730-4.
26. de Vera ME, Shapiro RA, Nussler AK et al. Transcriptional regulation of human inducible nitric oxide synthase (NOS2) gene by cytokines: initial analysis of the human NOS2 promoter. Proc Natl Acad Sci USA 1996;93:1054-9.
27. Albina JE. On the expression of nitric oxide synthase by human macrophages. Why no NO? J Leukocyte Biol 1995;58:643-9.
28. Ralston SH, Todd D, Helfrich MH, Benjamin N, Grabowski P. Human osteoblast-like cells produce nitric oxide and express inducible nitric oxide synthase. Endocrinology 1994;135:330-6.
29. Hickery MS, Palmer RMJ, Charles IG, Moncada S, Bayliss MT. The role of nitric oxide in IL-1 induced inhibition of proteoglycan synthesis in human articular cartilage. Br J Rheumatol 1994;33(suppl. 1):92 (Abstract).
30. Grabowski PS, MacPherson HM, Ralston SH. Nitric oxide production in cells derived from the human joint. Br J Rheumatol 1995;35:207-13.
31. Ralston SH, Grabowski PS. Mechanisms of cytokine induced bone resorption: Role of nitric oxide, cyclic guanosine monophosphate and prostaglandins. Bone 1996;19:29-33.
32. Nussler AK, DiSilvio M, Billiar TR et al. Stimulation of the nitric oxide synthase pathway in human hepatocytes by cytokines and endotoxin. J Exp Med 1992;176:261-4.
33. Ignarro LJ, Adams JB, Horwitz PM, Wood KS. Activation of soluble guanylate cyclase by NO-hemoproteins involves NO-heme exchange. J Biol Chem 1986;261:4997-5002.
34. Ignarro LJ, Buga GM, Woods KS, Bryns RE, Chauduri G. Endothelium derived relaxation factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 1987;84:9265-8.
35. Rogers NE, Ignarro LJ. Constitutive nitric oxide synthase from cerebellum is reversibly inhibited by nitric oxide formed from arginine. Biochem Biophys Res Commun 1992;189:242-9.
36. Garthwaite J, Charles SL, Chess-Williams R. Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intracellular messenger in the brain. Nature 1988;336:385-8.
37. Blake DR, Blades S, Coumbe A, Mapp PI. Nitration of tyrosine in the inflamed human synovium: evidence for the generation of peroxynitrite in vivo. Br J Rheumatol 1996;35(suppl. 1):70.
38. Lepoivre M, Flaman J, Henry Y. Early loss of the tyrosyl radical in ribonucleotide reductase of adenocarcinoma cells producing nitric oxide. J Biol Chem 1992;267:22994-3000.
39. Stamler JS, Singel DJ, Loscalzo J. Biochemistry of nitric oxide and its redox activated forms. Science 1992;258:1898-902.
40. Halliwell B, Gutteridge JM. Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol 1990;186:1-85.
41. Lipton SA, Choi Y, Pan Z et al. A redox based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso compounds. Nature 1993;364:626-32.
42. Hall TJ, Schaeublin M, Fuller K, Chambers TJ. The role of reactive oxygen intermediates in osteoclastic bone resorption. Biochem Biophys Res Commun 1995;207:280-7.
43. Fraser JE, Helfrich MH, Wallace HM, Ralston SH. Hydrogen peroxide, but not superoxide, stimulates bone resorption in mouse calvariae by increasing osteoclast numbers. Bone 1996;18:223-6.
44. Garrett IR, Boyce BF, Oreffo ROC, Bonewald L, Poser J, Mundy GR. Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J Clin Invest 1990;85:632-9.
45. Steinbeck MJ, Appel WH, Verhoeven AJ, Karnovsky MJ. NADPH-oxidase expression and in situ production of superoxide by osteoclasts actively resorbing bone. J Cell Biol 1994;126:765-72.
46. Evans DE, Grabowski PS, Helfrich M, Ralston SH. Localisation of nitric oxide synthesis in bone derived cells. J Bone Miner Res 1996;11:1816 (abstract).
47. Chow JWM, Chambers TJ, Fox SW. Immunolocalisation of nitric oxide synthase in bone cells. J Bone Miner Res 1996;11:s270.
48. Pitsillides AA, Rawlinson SC, Suswillo RF et al. Mechanical strain-induced NO production by bone cells: a possible role in adaptive bone (re)modelling? FASEB J 1995;9:1614-22.
49. Schmidt HHW, Gagne GD, Nakane M, Pollock JS, Miller MF, Murad F. Mapping of neural nitric oxide synthase in the rat suggests frequent co-localisation with NADPH diphorase but not with soluble guanylate cyclase and novel paraneural functions for signal transduction. J Histochem Cytochem 1992;40:1439-56.
50. Ralston SH, Ho LP, Helfrich MH et al. Nitric oxide: a cytokine-induced regulator of bone resorption. J Bone Miner Res 1995;10:1040-9.
51. Van't Hof RJ, Ralston SH. Cytokine induced nitric oxide inhibits bone resorption by inducing apoptosis of osteoclast progenitors and suppressing osteoclast activity. J Bone Miner Res 1997;12: in press.
52. Lowik CWGM, Nibbering PH, Van der Ruit M, Papapoulos SE. Inducible production of nitric oxide in osteoblast like cells and in fetal bone explants is associated with supression of osteoclastic bone resorption. J Clin Invest 1994;93:1465-72.
53. MacPherson H, Noble BS, Ralston SH. Nitric oxide production by human osteoblast-like cells and osteosarcoma cell lines. Calcified Tissue Int 1995;56:431 (Abstract).
54. Damoulis PD, Hauschka PV. Cytokines induce nitric oxide production in mouse osteoblasts. Biochem Biophys Res Commun 1994;201:924-31.
55. Van't Hof RJ. Cytokine induced bone resorption in mouse osteoclast cultures: differences between IL-1 and TNF. Bone 1996;17:815 (Abstract).
56. Riancho JA, Salas E, Zarrabeitia MT et al. Expression and functional role of nitric oxide synthase in osteoblast-like cells. J Bone Miner Res 1995;10:439-46.
57. Wimalawansa SJ, DeMarco G, Gangula P, Yallampalli C. Nitric oxide donor alleviates ovariectomy induced bone loss. Bone 1996; 18:301-4.
58. Klein-Nulend J, Semeins CM, Ajubi NE, Nijweide PJ, Burger EH. Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts - correlation with prostaglandin up-regulation. Biochem Biophys Res Commun 1995;217:640-8.
59. Rawlinson SC et al. Calvarial and limb bone cells in organ and monolayer culture do not show the same early responses to dynamic mechanical strain. J Bone Miner Res 1995;10:1225-32.
60. Maclntyre I, Zaidi M, Towhidul Alam ASM et al. Osteoclast inhibition: An action of nitric oxide not mediated by cyclic GMP. Proc Natl Acad Sci USA 1991;88:2936-40.
61. Punjabi CJ, Laskin DL, Heck DE, Laskin JD. Production of nitric oxide by murine bone marrow cells. J Immunol 1992;149:2179-84.
62. Armour KA, Ralston SH. Oestrogen stimulates endothelial nitric oxide synthase activity in human osteoblast-like cells. Bone 1997;20:67s (abstract).
63. Hukkanen M, Hughes FJ, Lee D et al. Cytokine stimulated expression of inducible nitric oxide synthase by mouse, rat and human osteoblast-like cells and its functional role in osteoblast metabolic activity. Endocrinology 1995;136:5445-53.
64. Pitsillides A et al. Mechanical strain-induced nitric oxide production by osteoblasts and osteocytes. J Bone Miner Res 1995;10(suppl. 1):s217.
65. Evans DM, Ralston SH. Nitric oxide and bone. J Bone Miner Res 1996;11:300-5.
66. Kasten TP, Collin-Osdoby P, Patel N et al. Potentiation of osteoclast bone resorbing activity by inhibition of nitric oxide synthase. Proc Natl Acad Sci USA 1994;91:3569-73.
67. Maciejewski JP, Selleri C, Sato T et al. Nitric oxide suppression of human hematopoiesis in vitro. Contribution to inhibitory action of interferon-gamma and tumor necrosis factor-alpha. J Clin Invest 1995;96:1085-92.
68. Bourke P, van't Hof R, Ralston SH. Nitric oxide inhibits IL-1 induced c-fos expression in MC3T3 osteoblast-like cells. J Bone Miner Res 1996;11:1820 (abstract).
69. Grigoriadis A, Wang ZQ, Cecchini MG et al. c-FOS: A key regulator of osteoclast-macrophage lineage determination and bone remodelling. Science 1994; 266:443-8.
70. Gowen M. Cytokines and bone metabolism, Vol. 1. Boca Raton, FL: CRC Press, 1992:1-407.
71. Croucher PI, Vedi S, Motley RJ, Garrahan NJ, Stanton MR, Compston JE. Reduced bone formation in patients with osteoporosis associated with inflammatory bowel disease. Osteoporosis Int 1993;3:236-41.
72. Compston JE, Vedi S, Croucher PI, Garrahan NJ, O'Sullivan MM. Bone turnover in non-steroid treated rheumatoid arthritis. Ann Rheum Dis 1994;53:163-6.
73. Minne HW, Pfeilschifter J, Scharla S et al. Inflammation mediated osteopenia in the rat: A new animal model for pathological loss of bone mass. Endocrinology 1984;115:50-4.
74. Peterson DA, Peterson DC, Archer S, Weir EK. The non-specificity of specific nitric oxide synthase inhibitors. Biochem Biophys Res Commun 1992;187:797-801.
75. Wei X, Charles IG, Smith A et al. Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 1995;375:408-11.
76. Huang PL, Huang Z, Mashimo H et al. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 1995;377:239-42.
77. Nelson RJ, Demas GE, Huang PL et al. Behavioural abnormalities in male mice lacking neuronal nitric oxide synthase. Nature 1995;378:383-6.
78. Stefanovic-Racic M, Morales TI, Taskiran D, McIntyre LA, Evans CH. The role of nitric oxide in proteoglycan turnover by bovine articular cartilage organ cultures. J Immunol 1996;156:1213-20.
79. Murrell GA, Jang D, Williams RJ. Nitric oxide activates metalloprotease enzymes in articular cartilage. Biochem Biophys Res Commun 1995;206:15-21.
80. Taskiran D et al. Nitric oxide mediates suppression of cartilage proteoglycan synthesis by interleukin-1. Biochem Biophys Res Commun 1994;200:142-8.
81. Grabowski PS, England AJ, Dykhuizen R et al. Detection of increased nitric oxide production in rheumatoid arthritis using the urinary nitrate/creatinine ratio. Arthritis Rheum 1996;39:643-7.
82. Gough AK, Lilley J, Eyre S, Holder RL, Emery P. Generalised bone loss in patients with early rheumatoid arthritis. Lancet 1994;344:23-7.
83. Leibovich SJ, Polverini PJ, Fong TW, Harlow LA, Koch AE. Production of angiogenic activity by human monocytes requires an L-arginine/nitric oxide-synthase-dependent effector mechanism. Proc Natl Acad Sci USA 1994;91:4190-4.
84. Grabowski PS, Wright P, Ralston SH. Immunolocalisation of inducible nitric oxide synthase (iNOS) in rheumatoid synovium. Br J Rheumatol 1996;35(suppl. 1):177.
85. Sakurai H, Koshaka H, Lui M et al. Nitric oxide production and inducible nitric oxide synthase expression in inflammatory arthritides. J Clin Invest 1995;96:2357-63.
86. McCartney-Francis N, Allen JB, Mizel DE et al. Supression of arthritis by an inhibitor of nitric oxide synthase. J Exp Med 1993;178:749-54.
87. Ialenti A, Moncada S, Di Rosa M. Modulation of adjuvant arthritis by endogenous nitric oxide. Br J Pharmacol 1993;110:701-6.