medigraphic.com
Órgano Oficial del Instituto de Ciencias de la Salud, Hospital Escuela y Facultad de Medicina-Xalapa

2012, Number 1

<< Back Next >>

Rev Med UV 2012; 12 (1)

Importance of nitric oxide synthases in bone metabolism

Valdez-Mijares R, Franco-Bourland RE, Quintana-Armenta A, Ruiz-Rosano L

Language: Spanish
References: 89
Page: 37-44
PDF size: 580.92 Kb.


ABSTRACT

In the last 20 years, nitric oxide NO has proven to be a universal molecular messenger essential in multiple physiological functions of diversely tissues, including bone. In bone, NO is produced by nitric oxide synthase (NOS) which exists in three isomorphs: endothelial, neuronal and inducible nitric oxide synthase NOSe, NOSn, and NOSi, respectively, each one with specific functions. This review describes the importance of each NOS isomorph for bone tissue, as well as the controversy surrounding the action of NO in bone produced endogenously by these isomorphs and organic NO donors.


REFERENCES

  1. Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med. 1993; 329 (27): 2002-12.

  2. Bredt DS, Snyder SH. Isolation of nitric oxide synthetase, a calmodulin requiring enzyme. Proc Natl Acad Sci USA. 1990; 87 (2): 682 - 685.

  3. Pollock JS, Förstermann U, Mitchell JA, Warner TD, Schmidt HH, Nakane M, y col. Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc Natl Acad Sci USA.1991; 88 (23): 10480-10484.

  4. Xie QW, Cho HJ, Calaycay J, Mumford RA, Swiderek KM, Lee TD y col. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science. 1992; 256 (5054): 225-228.

  5. Feelisch M, Stamler JS. Methods in nitric oxide research. J Wiley y Sons, New York.1996; 712 pp.

  6. Gross S, Wolin M. Nitric oxide: Pathophysiological mechanisms. Annu Rev Physiol. 1995; 57: 737-769.

  7. Cuzzocrea S, Mazzon E, Dugo L, Genovese T, Di Paola R, Ruggeri Z y col. Inducible nitric oxide synthase mediates bone loss in ovariectomized mice. Endocrinology. 2003; 144 (3): 1098 -1107.

  8. Flavahan NA. Atherosclerosis or lipoprotein-induced endothelial dysfunction. Potential mechanisms underlying reduction in EDRF/ nitric oxide activity. Circulation.1992; 85 (5): 1927-1938.

  9. Armour KE, Ralston SH. Estrogen upregulates endothelial constitutive nitric oxide synthase expression in human osteoblast-like cells. Endocrinology.1998; 139 (2):799 -802.

  10. Armour KE, Armour KJ, Gallagher ME, Gödecke A, Helfrich MH, Reid DM, y col. Defective bone formation and anabolic responses to exogenous estrogen in mice with targeted disruption of endothelial nitric oxide synthase. Endocrinology. 2001; 142 (2): 760 - 766.

  11. Berka V, Chen PF, Tsai AL. Spatial relationship between L-arginine and heme binding sites of endothelial nitric-oxide synthase. J Biol Chem. 1996; 271 (52): 33293-33300.

  12. Marcelín JG, Ceja OI, Hernández PA, Escalante AB. El 17-β estradiol induce la expresión de la sintasa de óxido nítrico tipo III en células endoteliales en culvito. Arch Cardiol Mex. 2001; 71 (2): 114-120.

  13. Chambliss KL, Shaul WP. Estrogen modulation of endothelial nitric oxide synthase. Endocr Rev. 2002; 23 (5): 665 - 686.

  14. Simoncini T, Genazzani AR, Liao JK. Nongenomic mechanisms of endothelial nitric oxide synthase activation by the selective estrogen receptor modulator raloxifene. Circulation. 2002; 105: 1368-1373.

  15. De Nigris F, Lerman LO, Ignarro SW, Sica G, Lerman A, Palinski W, y col. Benefical effects of antioxidants and L-arginine on oxidationsensitive gene expression and endothelial NO synthase activity at sites of disturbed shear stress. Proc Natl Acad Sci U S A. 2003; 100 (3): 1420 - 1425.

  16. Rubin J, Murphy TC, Zhu L, Roy E, Nanes MS, Fan X. Mechanical strain differentially regulates endothelial nitric-oxide synthase and receptor activator of nuclear kappa B ligand expression via ERK1/2MAPK. J Biol Chem. 2003; 278 (36): 34018-34025.

  17. Govers R, Rabelink TJ. Cellular regulation of endothelial nitric oxide synthase. Am J Physiol Renal Physiol. 2001; 280 (2): F193-F206.

  18. Solomon KR , Adolphson LD, Wank DA, McHugh KP, Hauschka PV. Caveolae in human and murine osteoblasts. J Bone Miner Res. 2000;

  19. 15 (12): 2391- 2401.

  20. Solomon KR, Danciu TE, Adolphson LD, Hecht LE, Hauschka PV. Caveolin-enriched membrane signaling complexes in human and murine osteoblasts. J Bone Miner Res. 2000; 15 (12): 2380-2390.

  21. Van´t Hof RJ, Macphee J, Libouban H, Helfrich MH, Ralston SH. Regulation of bone mass and bone turnover by neuronal nitric oxide synthase. Endocrinology. 2004; 145 (11): 5068-5074.

  22. Mori M, Gotoh T. Arginine metabolic Enzymes, Nitric oxide and infection. J Nutr. 2004; 134 (10 Suppl): 2820S-2825S.

  23. Stuehr DJ. Mammalian nitric oxide synthases. Biochim Biophys Acta. 1999; 1411 (2-3): 217-230.

  24. Rodrigo J, Alonso D, Fernández A, Serrano J, López J. El óxido nítrico: síntesis, neuroprotección, y neurotoxicidad. An Sist Sanit Navar. 2000; 23 (2): 195-235.

  25. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases, structure, funtion and inhibition. Biochem J. 2001; 357: 593 – 615.

  26. Hibbs JB Jr, Taintor RR, Vavrin Z. Macrophage cytotoxicity: role for L-arginine deiminase and imino nitrogen oxidation to nitrite. Science. 1987; 235 (4787): 473-476.

  27. Vallance P, Leone A, Calver A, Collier J, Moncada S. Accumulation of an endogenous inhibitor of nitric oxide synthesis in chronic renal failure. Lancet. 1992; 339 (8793): 572-575.

  28. McCall TB, Feelisch M, Palmer RMJ, Moncada S. Indentification of N-iminoethyl-L-ornithine as an irreversible inhibitor of nitric oxide synthase in phagocytic cells. Br J Pharmacol. 1992; 102 (1): 234-238.

  29. Lambert LE, French JF, Whitten JP, Baron BM, McDonald IA. Characterization of cell selectivity of two novel inhibitors of nitric oxide synthesis. Eur J Pharmacol. 1992; 216 (1): 131-134.

  30. Knowles RG, Palacios M, Palmer RMJ, Moncada S. Formation of nitric oxide from L-arginine in the central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase. Proc Natl Acad Sci USA. 1989; 89 (13): 5159-5162.

  31. Shaul PW. Regulation of endothelial nitric oxide synthase: location, location, location. Annu Rev Physiol. 2002; 64: 749-774.

  32. Kone BC, Kuncewicz T, Zhang W, Yu Z-Y. Protein interactions with nitric oxide synthases: controlling the right time, the right place, and the right amount of nitric oxide. Am J Physiol Renal Physiol. 2003; 285(2): F178-F190.

  33. Brandi ML, Hukkanen M, Umeda T, Moradi-Bidhendi N, Bianchi S, Gross SS y col. Bidirectional regulation of osteoclast function by nitric oxide synthase isoforms. Proc Natl Acad Sci USA. 1995; 92 (7): 2954-2958.

  34. Helfrich MH, Evans DE, Grabowski PS, Pollock JS, Ohshima H y col. Expression of nitric oxide synthase isoforms in bone and bone cell cultures. J Bone Miner Res. 1997; 12 (7): 1108-1115.

  35. Fox SW, Chow JW. Nitric oxide synthase expression in bone cells. Bone. 1998; 23 (1): 1-6.

  36. Aguirre J, Buttery L, O’Shaughnessy M, Afzal F, Fernandez de Marticorena I, Hukkanen M, y col. Endotelial nitric oxide synthase gene-deficient mice demonstrate marked retardation in postnatal bone formation, reduced bone volume, and defects in osteoblast maturation and activity. Am J Pathol. 2001; 158 (1): 247 – 257.

  37. Ralston SH, Ho LP, Helfrich MH, Grabowski PS, Johnston PW, Benjamin N. Nitric oxide: a cytokine-induced regulator of bone resorption. J Bone Miner Res. 1995; 10 (7):1040-1049.

  38. van´t Hof R, Ralston S H. Cytokine-induced nitric oxide inhibits bone resorption by inducing apoptosis of osteoclast progenitors and suppressing osteoclast activity. J Bone Miner Res. 1997; 12 (11): 1797-1804.

  39. Van´t Hof RJ, Ralston HS. Nitric oxide is essential for IL-1 stimulated osteoclast formation in mouse co-cultures. J Bone Miner Res. 1997; 12:1531.

  40. Van´t Hof RJ, Armour KJ, Smith LM, Armour KE, Wei XQ, Liew FY y col. Requirement of the inducible nitric oxide synthase pathway for IL-1 induced osteoclastic bone resorption. Proc Natl Acad Sci USA. 2000; 97 (14): 7993-7998.

  41. Armour KJ, Armour KE, van’t Hof RJ, Reid DM, Wei XQ, Liew FY, y col. Activation of the inducible nitric oxide synthase pathway contributes to inflammation-induced osteoporosis by suppressing bone formation and causing osteoblast apoptosis. Arthritis Rheum. 2001; 44 (12): 2790 - 2796.

  42. Pitsillides AA, Rawlinson SC, Suswillo RF, Bourrin S, Zaman G, Lanyon LE.. Mechanical strain-induced NO production by bone cells: a possible role in adaptive bone (re) modeling? FASEB J. 1995; 9 (15):1614-1622.

  43. Klein-Nulend J, Helfrich MH, Sterck JG, MacPherson H, Joldersma M, Ralston SH y col. Nitric oxide response to shear stress by human bone cell cultures is endothelial nitric oxide synthase dependent. Biochem Biophys Res Commun.1998; 250 (1): 108-114.

  44. Fleming I, Busse R. Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. Am J Physiol Regul Integr Comp Physiol. 2003; 284 (1): R1-R12.

  45. Chae HJ, Park RK, Chung HT, Kang JS, Kim MS, Choi DY y col. Nitric oxide is a regulator of bone remodelling. J Pharm Pharmacol. 1997; 49 (9): 897-902.

  46. Evans DM, Ralston SH. Nitric oxide and bone. J Bone Miner Res.1996; 11 (3): 300 -305.

  47. Ralston SH. The Michael Mason Prize Essay 1997. Nitric oxide and bone: What a gast!. Br J Rheumatol.1997; 36: 831-838.

  48. Hayashi T, Yamada K, Esaki T, Kuzuya M, Satake S, Ishikawa T y col. Estrogen increases endothelial nitric oxide by a receptor-mediated system. Biochem Biophys Res Commun. 1995; 214 (3): 847-855.

  49. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, y col. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature.1999; 399(6736): 597-601.

  50. Dedio J, König P, Wohlfart P, Schroeder C, Kummer W, Müller-Esterl W. NOSIP, a novel modulator of endothelial nitric oxide synthase activity. FASEB J. 2001; 15 (1): 79-89.

  51. Huesa CH, Helfrich MH, Aspden RM. Role of caveolin-1 in regulation of eNOS activation in osteoblastic cells. Seventh International Bone Fluid Flow Workshop, Septermber. 2005. New york city.

  52. Fulton D, Gratton JP, Sessa WC. Post-translational control of endothelial nitric oxide synthase: Why Isn´t Calcium/Calmodulin Enough?. J Pharmacol Exp Ther. 2001; 299 (3): 818-824.

  53. Förstermann U, Pollock JS, Schmidt HH, Heller M, Murad F. Calmodulin dependent entothelium-derived relaxing factor/nitric oxide synthase activity is present in the particulate and cytosolic fractions of bovine aortic endothelial cells. Proc Natl Acad Sci U S A. 1991; 88 (5): 1788-1792.

  54. Chen Z, Yuhanna IS, Galcheva-Gargova Z, Karas RH, Mendelsohn ME, Shaul PW. Estrogen receptor α mediates the nongenomic activation of endothelial nitric oxide synthase by estrogen. J Clin Invest. 1999; 103(3): 401 – 406

  55. Haynes MP, Sinha D, Russell KS, Collinge M, Fulton D, Morales- Ruiz M y col. Membrane estrogen receptor engagement activates endothelial nitric oxide synthase via the PI3- kinase-Akt pathway in human endothelial cells. Circ Res. 2000; 87(8): 677-82.

  56. Bennell KL, Malcolm SA, Khan KM, Thomas SA, Reid SJ, Brukner PD y col. Bone mass and bone turnover in power athletes, endurance athletes and controls: a 12 month longitudinal study. Bone. 1997; 20 (5): 477-484.

  57. Judex S, Gross TS, Zernicke RF. Strain gradients correlate with sites of exercise-induced bone forming surfaces in the adult skeleton. J Bone Miner Res. 1997; 12 (10): 1737-1745.

  58. Rubin C, Xu G, Judex S. The anabolic activity of bone tissue, suppressed by disuse, is normalized by brief exposure to extremely low-magnitude mechanical stimuli. FASEB J. 2001; 15(12): 2225-29.

  59. Watanuki M, Sakai A, Sakata T, Tsurukami H, Miwa M, Uchida Y y col. Role of inducible nitric oxide synthase in skeletal adaptation to acute increases in mechanical loading. J Bone Miner Res. 2002; 17(6):1015-1025.

  60. Haapasalo H, Sievanen H, Kannus P, Heinonen A, Oja P, Vuori I. Dimensions and estimated mechanical characteristics of the humerus after long-term tennis loading. J Bone Miner Res. 1996; 11 (6): 864-872.

  61. Haapasalo H, Kontulainen S, Sievänen H, Kannus P, Järvinen M, Vuori I. Exercise- Induced bone gain is due to enlargement in bone size without a change in volumetric bone density: a peripheral quantitative computed tomography study of the upper arms of male tennis players. Bone.2000; 27(3): 351-357.

  62. Uebelhart D, Demiaux- Domenech B, Roth M, Chantraine A. Bone metabolism in spinal cord injured individuals and in others who have prolonged immobilisation. A review. Paraplegia. 1995; 33 (11): 669-673.

  63. Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am. 1984; 66 (3): 397-402.

  64. Rubin J, Murphy TC, Fan X, Goldschmidt M, Taylor WR. Activation of extracellular signal-regulated kinase is involved in mechanical strain inhibition of RANKL expression in bone stromal cells. J Bone Miner Res. 2002; 17 (8): 1452-1460.

  65. Van´t Hof RJ, Ralston HS. Nitric oxide and bone. Immunology. 2001; 103 (3): 255-261.

  66. Armour KE, Van’T Hof RJ, Grabowski PS, Reid DM, Ralston SH. Evidence for a pathogenic role of nitric oxide in inflammation-induced osteoporosis. J Bone Miner Res. 1999; 14 (12): 2137-2142.

  67. Pacifici R, Brown C, Puscheck E, Friedrich E, Slatopolsky E, Maggio D, y col. Effect of surgical menopause and estrogen replacement on cytokine release from human blood mononuclear cells. Proc Natl Acad Sci USA. 1991; 88(12): 5134-5138.

  68. Shen F, Ruddy MJ, Plamondon P, Gaffen SL. Cytokines link osteoblasts and inflammation: microarray analysis of interleukin-17-and TNF alpha-induced genes in bone cells. J Leukoc Biol. 2005; 77 (3): 388-399.

  69. Zancan V, Santagati S, Bolego C, Vegeto E, Maggi A, Puglisi L. 17 β-Estradiol decreases nitric oxide synthase II síntesis in vascular smooth muscle cells. Endocrinology. 1999; 140 (5): 2004-2009.

  70. Pacifici R. Estrogen, cytokines and pathogenesis of postmenopausal osteoporosis. J Bone Miner Res. 1996; 11 (8): 1043-1051.

  71. Cenci S, Weitzmann MN, Roggia C, Namba N, Novack D, Woodring J y col. Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Invest. 2000; 106(10): 1229 - 1237

  72. RL. Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med. 1995; 332 (5): 305-311.

  73. Hukkanen MV, Platts LA, Fernandez De Marticorena I, O’Shaughnessy M, MacIntyre I, Polak JM. Developmental regulation of nitric oxide synthase expressión in rat skeletal bone. J Bone Miner Res. 1999; 14 (6): 868-877.

  74. Zhu W, Diwan AD, Lin JH, Murrel GA. Nitric oxide synthase isoforms during fracture healing. J Bone Miner Res. 2001; 16 (3): 535-540.

  75. Amling M, Pogoda P, Beil FT, Schilling AF, Holzmann T, Priemel M y col. Central control of bone mass: brainstorming of the skeleton. Adv Exp Med Biol. 2001; 496: 85-94.

  76. Maclntyre I, Zaidi M, Alam AS, Datta HK, Moonga BS, Lidbury PS, y col. Osteoclastic inhibiton: an action of nitric oxide not mediated by cyclic GMP. Proc Natl Acad Sci USA. 1991; 88 (7): 2936-2940.

  77. Riancho JA, Salas E, Zarrabeitia MT, Olmos JM, Amado JA, Fernández- Luna JL y col. Expression and functional role of nitric oxide synthase in osteoblast-like cells. J Bone Miner Res.1995; 10 (3): 439-446.

  78. Kanaoka K, Kobayashi Y, Hashimoto F, Nakashima T, Shibata M, Kobayashi K y col. A common downstream signaling activity of osteoclast survival factors that prevent nitric oxide-promoted osteoclast apoptosis. Endocrinology. 2000; 141 (8): 2995-3005.

  79. Wimalawansa. SJ, De Marco G, Gangula P, Yallampalli C. Nitric oxide donor alleviates ovariectomy induced bone loss. Bone. 1996; 18 (4): 301-304.

  80. Wimalawansa SJ. Restoration of ovariectomy-induced osteopenia by nitroglycerin. Calcif Tissue Int. 2000; 66 (1): 56-60.

  81. Hukkanen M, Platts LA, Lawes T, Girgis SI, Konttinen YT, Goodship AE y col. Effect of nitric oxide donor nitroglycerin on bone mineral density in a rat model of estrogen deficiency-induced osteopenia. Bone. 2003; 32 (2): 142-149.

  82. Hao YJ, Tang Y, Chen FB, Pei FX. Different doses of nitric oxide donor prevent osteoporosis in ovariectomized rats. Clin Orthop Relat Res. 2005; 453: 226-31.

  83. Wimalawansa SJ. Nitroglycerin therapy is as efficacious as standard estrogen replacement therapy (Premarin) in prevention of oophorectomy-induced bone loss: a human pilot clinical study. J Bone Miner Res. 2000; 15 (11): 2240-2244.

  84. Wimalawansa SJ, Grimes JP, Wilson AC, Hoover DR. Transdermal nitroglycerin therapy may not prevent early postmenopausal bone loss. J Clin Endocrinol Metab. 2009; 94 (9): 3356-3364.

  85. Wang FS, Wang CJ, Chen YJ, Huang YT, Huang HC, Chang PR y col. Nitric oxide donor increases osteoprotegerin production and osteoclastogenesis inhibitory activity in bone marrow stromal cells from ovariectomized rats. Endocrinology. 2004; 145 (5): 2148-2156.

  86. Jamal SA, Browner WS, Bauer DC, Cumming SR. Intermittent use of nitrates increases bone mineral density: the study of osteoporotic fractures. J Bone Miner Res. 1998; 13 (11):1755-1759.

  87. Jamal SA, Cummings SR, Hawker GA. Isosorbide mononitrate increases bone formation and decreases bone resorption in postmenopausal women: a randomized trial. J. Bone Miner Res. 2004; 19 (9):1512-1517.

  88. Nabhan AF, Rabie NH. Isosorbide mononitrate versus alendronate for postmenopausal osteoporosis. Int J Gynaecol Obstet. 2008; 103 (3): 213-216.

  89. Pouwels S, Lalmohamed A, van Staa T, Cooper C, Souverein P, Leufkens HG y col. Use of organic nitrates and the risk of hip fracture: a population based case-control study. J Clin Endocrinol Metab. 2010; 95 (4): 1924-1931.




2020     |     www.medigraphic.com