Endothelial nitric oxide synthase is not essential for nitric oxide production by osteoblasts subjected to fluid shear stress in vitro

Calcified Tissue International

Volumn 92, Issue 3, 2013, Pages 228-239

  Bakker, Astrid D ^a   Huesa, Carmen ^b   Hughes, Alun ^c   Aspden, Richard M ^c   Van'T Hof, Rob J ^d   Klein Nulend, Jenneke ^a   Helfrich, Miep H ^c  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Endothelial nitric oxide synthase; Inducible nitric oxide synthase; Mechanical stimulation; Neuronal nitric oxide synthase; Osteoblast

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BIOSYNTHESIS; BONE GROWTH; BONE MASS; BONE STRENGTH; BONE STRUCTURE; CALVARIA; CELL STIMULATION; CELL TYPE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; FEMUR; FLUID FLOW; IN VITRO STUDY; LIMIT OF DETECTION; MECHANICAL STIMULATION; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEAR STRESS; TIBIA; UPREGULATION; WILD TYPE;

EID: 84873719784     PISSN: 0171967X     EISSN: 14320827     Source Type: Journal    
DOI: 10.1007/s00223-012-9670-x     Document Type: Article

References (41)

1. Wei XQ, Charles IG, Smith A, Ure J, Feng GJ, Huang FP, Xu D, Muller W, Moncada S, Liew FY (1995) Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 375:408-411
2. van't Hof RJ, Ralston SH (2001) Nitric oxide and bone. Immunology 103:255-261
3. Moncada S, Higgs EA (2006) The discovery of nitric oxide and its role in vascular biology. Br J Pharmacol 147(Suppl 1):S193-S201
4. Zhou L, Zhu DY (2009) Neuronal nitric oxide synthase: structure, subcellular localization, regulation, and clinical implications. Nitric Oxide 20:223-230
5. Zaman G, Pitsillides AA, Rawlinson SC, Suswillo RF, Mosley JR, Cheng MZ, Platts LA, Hukkanen M, Polak JM, Lanyon LE (1999) Mechanical strain stimulates nitric oxide production by rapid activation of endothelial nitric oxide synthase in osteocytes. J Bone Miner Res 14:1123-1131
6. Hukkanen MV, Platts LA, Fernandez DM, O'Shaughnessy M, MacIntyre I, Polak JM (1999) Developmental regulation of nitric oxide synthase expression in rat skeletal bone. J Bone Miner Res 14:868-877
7. Helfrich MH, Evans DE, Grabowski PS, Pollock JS, Ohshima H, Ralston SH (1997) Expression of nitric oxide synthase isoforms in bone and bone cell cultures. J Bone Miner Res 12:1108-1115
8. Loveridge N, Fletcher S, Power J, Caballero-Alias AM, Das-Gupta V, Rushton N, Parker M, Reeve J, Pitsillides AA (2002) Patterns of osteocytic endothelial nitric oxide synthase expression in the femoral neck cortex: differences between cases of intracapsular hip fracture and controls. Bone 30:866-871
9. van't Hof RJ, Armour KJ, Smith LM, Armour KE, Wei XQ, Liew FY, Ralston SH (2000) Requirement of the inducible nitric oxide synthase pathway for IL-1-induced osteoclastic bone resorption. Proc Natl Acad Sci USA 97:7993-7998
10. Armour KE, Armour KJ, Gallagher ME, Gödecke A, Helfrich MH, Reid DM, Ralston SH (2001) Defective bone formation and anabolic response to exogenous estrogen in mice with targeted disruption of endothelial nitric oxide synthase. Endocrinology 142:760-766
11. Aguirre J, Buttery L, O'Shaughnessy M, Afzal F, Fernandez DM, Hukkanen M, Huang P, MacIntyre I, Polak J (2001) Endothelial 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 158:247-257
12. van't Hof RJ, MacPhee J, Libouban H, Helfrich MH, Ralston SH (2004) Regulation of bone mass and bone turnover by neuronal nitric oxide synthase. Endocrinology 145:5068-5074
13. Grassi F, Fan X, Rahnert J, Weitzmann MN, Pacifici R, Nanes MS, Rubin J (2006) Bone re/modeling is more dynamic in the endothelial nitric oxide synthase(-/-) mouse. Endocrinology 147:4392-4399
14. Cuzzocrea S, Mazzon E, Dugo L, Genovese T, Di PR, Ruggeri Z, Vegeto E, Caputi AP, Van De Loo FA, Puzzolo D, Maggi A (2003) Inducible nitric oxide synthase mediates bone loss in ovariectomized mice. Endocrinology 144:1098-1107
15. Baldik Y, Diwan AD, Appleyard RC, Fang ZM, Wang Y, Murrell GA (2005) Deletion of iNOS gene impairs mouse fracture healing. Bone 37:32-36
16. Watanuki M, Sakai A, Sakata T, Tsurukami H, Miwa M, Uchida Y, Watanabe K, Ikeda K, Nakamura T (2002) Role of inducible nitric oxide synthase in skeletal adaptation to acute increases in mechanical loading. J Bone Miner Res 17:1015-1025
17. Sabanai K, Tsutsui M, Sakai A, Hirasawa H, Tanaka S, Nakamura E, Tanimoto A, Sasaguri Y, Ito M, Shimokawa H, Nakamura T, Yanagihara N (2008) Genetic disruption of all NO synthase isoforms enhances BMD and bone turnover in mice in vivo: involvement of the renin-angiotensin system. J Bone Miner Res 23:633-643
18. Skerry TM (2008) The response of bone to mechanical loading and disuse: fundamental principles and influences on osteoblast/osteocyte homeostasis. Arch Biochem Biophys 473:117-123
19. Turner CH, Owan I, Jacob DS, McClintock R, Peacock M (1997) Effects of nitric oxide synthase inhibitors on bone formation in rats. Bone 21:487-490
20. Chow JW, Fox SW, Lean JM, Chambers TJ (1998) Role of nitric oxide and prostaglandins in mechanically induced bone formation. J Bone Miner Res 13:1039-1044
21. Burger EH, Klein-Nulend J (1999) Mechanotransduction in bone - role of the lacuno-canalicular network. FASEB J 13:S101-S112
22. Klein-Nulend J, van der Plas A, Semeins CM, Ajubi NE, Frangos JA, Nijweide PJ, Burger EH (1995) Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J 9:441-445
23. Johnson DL, McAllister TN, Frangos JA (1996) Fluid flow stimulates rapid and continuous release of nitric oxide in osteoblasts. Am J Physiol Endocrinol Metab 271:E205-E208
24. Klein-Nulend J, Helfrich MH, Sterck JG, MacPherson H, Joldersma M, Ralston SH, Semeins CM, Burger EH (1998) Nitric oxide response to shear stress by human bone cell cultures is endothelial nitric oxide synthase dependent. Biochem Biophys Res Commun 250:108-114
25. Das-Gupta V, Williamson RA, Pitsillides AA (2012) Expression of endothelial nitric oxide synthase protein is not necessary for mechanical strain-induced nitric oxide production by cultured osteoblasts. Osteoporos Int 23:2635-2647
26. Gödecke A, Decking UK, Ding Z, Hirchenhain J, Bidmon HJ, Godecke S, Schrader J (1998) Coronary hemodynamics in endothelial NO synthase knockout mice. Circ Res 82:186-194
27. Goodyear SR, Aspden RM (2012) Mechanical properties of bone ex vivo. Methods Mol Biol 816:555-571
28. Orriss IR, Taylor SE, Arnett TR (2012) Rat osteoblast cultures. Methods Mol Biol 816:31-41
29. Huesa C, Helfrich MH, Aspden RM (2010) Parallel-plate fluid flow systems for bone cell stimulation. J Biomech 43:1182-1189
30. Bakker AD, Silva VC, Krishnan R, Bacabac RG, Blaauboer ME, Lin YC, Marcantonio RA, Cirelli JA, Klein-Nulend J (2009) Tumor necrosis factor alpha and interleukin-1beta modulate calcium and nitric oxide signaling in mechanically stimulated osteocytes. Arthr Rheum 60:3336-3345
31. Vatsa A, Mizuno D, Smit TH, Schmidt CF, MacKintosh FC, Klein-Nulend J (2006) Bio imaging of intracellular NO production in single bone cells after mechanical stimulation. J Bone Miner Res 21:1722-1728
32. Jamal SA, Hamilton CJ (2012) Nitric oxide donors for the treatment of osteoporosis. Curr Osteoporos Rep 10:86-92
33. Yan Q, Feng Q, Beier F (2010) Endothelial nitric oxide synthase deficiency in mice results in reduced chondrocyte proliferation and endochondral bone growth. Arthr Rheum 62:2013-2022
34. Yan Q, Feng Q, Beier F (2012) Reduced chondrocyte proliferation, earlier cell cycle exit and increased apoptosis in neuronal nitric oxide synthase-deficient mice. Osteoarthr Cartil 20:144-151
35. Fox SW, Chow JW (1998) Nitric oxide synthase expression in bone cells. Bone 23:1-6
36. Coers W, Timens W, Kempinga C, Klok PA, Moshage H (1998) Specificity of antibodies to nitric oxide synthase isoforms in human, guinea pig, rat, and mouse tissues. J Histochem Cytochem 46:1385-1392
37. Rahnert J, Fan X, Case N, Murphy TC, Grassi F, Sen B, Rubin J (2008) The role of nitric oxide in the mechanical repression of RANKL in bone stromal cells. Bone 43:48-54
38. Zweier JL, Wang P, Samouilov A, Kuppusamy P (1995) Enzyme-independent formation of nitric oxide in biological tissues. Nat Med 1:804-809
39. Godber BL, Doel JJ, Sapkota GP, Blake DR, Stevens CR, Eisenthal R, Harrison R (2000) Reduction of nitrite to nitric oxide catalyzed by xanthine oxidoreductase. J Biol Chem 275:7757-7763
40. Foster MW, Hess DT, Stamler JS (2009) Protein S-nitrosylation in health and disease: a current perspective. Trends Mol Med 15:391-404
41. Huang B, Chen SC, Wang DL (2009) Shear flow increases S-nitrosylation of proteins in endothelial cells. Cardiovasc Res 83:536-546