Expression of endothelial nitric oxide synthase protein is not necessary for mechanical strain-induced nitric oxide production by cultured osteoblasts

Osteoporosis International

Volumn 23, Issue 11, 2012, Pages 2635-2647

  Das Gupta, V ^a   Williamson, R A ^b   Pitsillides, A A ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Endothelial nitric oxide synthase; Mechanical strain; Nitric oxide; Osteoblast

Indexed keywords

ARGININE; CITRULLINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEAT SHOCK PROTEIN 90; NITRIC OXIDE;

AMINO ACID METABOLISM; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; IMMUNOBLOTTING; MECHANICAL STRESS; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; BENZOQUINONES; CELLS, CULTURED; FEMALE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; OSTEOBLASTS; RATS; RATS, SPRAGUE-DAWLEY; STRESS, MECHANICAL;

EID: 84868208113     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-012-1957-2     Document Type: Article

References (61)

1. Rubin CT, Lanyon LE (1984) Dynamic strain similarity in vertebrates; an alternative to allometric limb bone scaling. J Theor Biol 107:321-327
2. Turner CH, Takano Y, Owan I, Murrell GA (1996) Nitric oxide inhibitor L-NAME suppresses mechanically induced bone formation in rats. Am J Physiol 270:E634-E639
3. Fox SW, Chambers TJ, Chow JW (1996) Nitric oxide is an early mediator of the increase in bone formation by mechanical stimulation. Am J Physiol 270:E955-E960
4. 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
5. Pitsillides AA, Rawlinson SC, Suswillo RF, Bourrin S, Zaman G, Lanyon LE (1995) Mechanical strain-induced NO production by bone cells: a possible role in adaptive bone (re)modeling? FASEB J 9:1614-1622
6. van't Hof RJ, Ralston SH (2001) Nitric oxide and bone. Immunology 103:255-261
7. 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
8. Sessa WC, Harrison JK, Barber CM, Zeng D, Durieux ME, D'Angelo DD, Lynch KR, Peach MJ (1992) Molecular cloning and expression of a cDNA encoding endothelial cell nitric oxide synthase. J Biol Chem 267:15274-15276
9. Michell BJ, Chen Z, Tiganis T, Stapleton D, Katsis F, Power DA, Sim AT, Kemp BE (2001) Coordinated control of endothelial nitric-oxide synthase phosphorylation by protein kinase C and the cAMP-dependent protein kinase. J Biol Chem 276:17625-17628
10. Chen ZP, Mitchelhill KI, Michell BJ, Stapleton D, Rodriguez-Crespo I, Witters LA, Power DA, Ortiz de Montellano P, Kemp BE (1999) AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett 443:285-289
11. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC (1999) Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399:597-601
12. Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357: 593-615
13. Garcia-Cardena G, Fan R, Shah V, Sorrentino R, Cirino G, Papapetropoulos A, Sessa WC (1998) Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature 392:821-824
14. Tang Y, Scheef EA, Gurel Z, Sorenson CM, Jefcoate CR, Sheibani N (2010) CYP1B1 and endothelial nitric oxide synthase combine to sustain proangiogenic functions of endothelial cells under hyperoxic stress. Am J Physiol Cell Physiol 298:C665-C678
15. Quintero M, Colombo SL, Godfrey A, Moncada S (2006) Mitochondria as signaling organelles in the vascular endothelium. Proc Natl Acad Sci U S A 103:5379-5384
16. Cao S, Yao J, McCabe TJ, Yao Q, Katusic ZS, Sessa WC, Shah V (2001) Direct interaction between endothelial nitric-oxide synthase and dynamin-2. Implications for nitric-oxide synthase function. J Biol Chem 276:14249-14256
17. Huang PL, Huang Z, Mashimo H, Bloch KD, Moskowitz MA, Bevan JA, Fishman MC (1995) Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 377:239-242
18. MacIntyre I, Zaidi M, Alam AS, Datta HK, Moonga BS, Lidbury PS, Hecker M, Vane JR (1991) Osteoclastic inhibition: an action of nitric oxide not mediated by cyclic GMP. Proc Natl Acad Sci U S A 88:2936-2940
19. Pitsillides AA, Das-Gupta V, Simon D, Rawlinson SC (2003) Methods: for analyzing bone cell responses to mechanical loading using in vitro monolayer and organ culture models. Methods: Mol Med 80:399-422
20. Piper PW (2001) The Hsp90 chaperone as a promising drug target. Curr Opin Investig Drugs 2:1606-1610
21. Dodds RA, Ali N, Pead MJ, Lanyon LE (1993) Early loading-related changes in the activity of glucose 6-phosphate dehydrogenase and alkaline phosphatase in osteocytes and periosteal osteoblasts in rat fibulae in vivo. J Bone Miner Res 8:261-267
22. Fairchild TA, Fulton D, Fontana JT, Gratton JP, McCabe TJ, Sessa WC (2001) Acidic hydrolysis as a mechanism for the cleavage of the Glu(298)-Asp variant of human endothelial nitric-oxide synthase. J Biol Chem 276:26674-26679
23. Solomon KR, Danciu TE, Adolphson LD, Hecht LE, Hauschka PV (2000) Caveolin-enriched membrane signaling complexes in human and murine osteoblasts. J Bone Miner Res 15:2380-2390
24. Knowles RG, Salter M (1998) Measurement of NOS activity by conversion of radiolabeled arginine to citrulline using ionexchange separation. Methods: Mol Biol 100:67-73
25. Mancini L, Moradi-Bidhendi N, Becherini L, Martineti V, MacIntyre I (2000) The biphasic effects of nitric oxide in primary rat osteoblasts are cGMP dependent. Biochem Biophys Res Commun 274:477-481
26. Gratton JP, Fontana J, O'Connor DS, Garcia-Cardena G, McCabe TJ, Sessa WC (2000) Reconstitution of an endothelial nitric-oxide synthase (eNOS), hsp90, and caveolin-1 complex in vitro. Evidence that hsp90 facilitates calmodulin stimulated displacement of eNOS from caveolin-1. J Biol Chem 275:22268-22272
27. Garcia-Cardena G, Martasek P, Masters BS, Skidd PM, Couet J, Li S, Lisanti MP, Sessa WC (1997) Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo. J Biol Chem 272:25437-25440
28. Michel JB, Feron O, Sase K, Prabhakar P, Michel T (1997) Caveolin versus calmodulin. Counterbalancing allosteric modulators of endothelial nitric oxide synthase. J Biol Chem 272:25907-25912
29. Hukkanen MV, Platts LA, Fernandez De Marticorena I, 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
30. Corbett SA, Hukkanen M, Batten J, McCarthy ID, Polak JM, Hughes SP (1999) Nitric oxide in fracture repair. Differential localisation, expression and activity of nitric oxide synthases. J Bone Joint Surg Br 81:531-537
31. MacPherson H, Noble BS, Ralston SH (1999) Expression and functional role of nitric oxide synthase isoforms in human osteoblast-like cells. Bone 24:179-185
32. Grabowski PS, Macpherson H, Ralston SH (1996) Nitric oxide production in cells derived from the human joint. Br J Rheumatol 35:207-212
33. Kanazawa I, Yamaguchi T, Yano S, Yamauchi M, Sugimoto T (2009) Activation of AMP kinase and inhibition of Rho kinase induce the mineralization of osteoblastic MC3T3-E1 cells through endothelial NOS and BMP-2 expression. Am J Physiol Endocrinol Metab 296:E139-E146
34. Hukkanen M, Hughes FJ, Buttery LD, Gross SS, Evans TJ, Seddon S, Riveros-Moreno V, Macintyre I, Polak JM (1995) 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 136:5445-5453
35. O'Shaughnessy MC, Polak JM, Afzal F, Hukkanen MV, Huang P, MacIntyre I, Buttery LD (2000) Nitric oxide mediates 17beta-estradiol-stimulated human and rodent osteoblast proliferation and differentiation. Biochem Biophys Res Commun 277:604-610
36. 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
37. Kanazawa I, Yamaguchi T, Yano S, Yamauchi M, Sugimoto T (2008) Metformin enhances the differentiation and mineralization of osteoblastic MC3T3-E1 cells via AMP kinase activation as well as eNOS and BMP-2 expression. Biochem Biophys Res Commun 375:414-419
38. Rawlinson SC, McKay IJ, Ghuman M, Wellmann C, Ryan P, Prajaneh S, Zaman G, Hughes FJ, Kingsmill VJ (2009) Adult rat bones maintain distinct regionalized expression of markers associated with their development. PLoS One 4:e8358
39. McAllister TN, Frangos JA (1999) Steady and transient fluid shear stress stimulate NO release in osteoblasts through distinct biochemical pathways. J Bone Miner Res 14:930-936
40. Miyamoto T, Petrus MJ, Dubin AE, Patapoutian A (2011) TRPV3 regulates nitric oxide synthase-independent nitric oxide synthesis in the skin. Nat Commun 2:369
41. 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
42. Meyer DJ (1995) Enzymatic/non-enzymatic formation of nitric oxide. Nat Med 1:1103-1104
43. Benhar M, Forrester MT, Stamler JS (2009) Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat Rev Mol Cell Biol 10:721-732
44. Skerry TM, Bitensky L, Chayen J, Lanyon LE (1989) Early strainrelated changes in enzyme activity in osteocytes following bone loading in vivo. J Bone Miner Res 4:783-788
45. Rawlinson SC, Murray DH, Mosley JR, Wright CD, Bredl JC, Saxon LK, Loveridge N, Leterrier C, Constantin P, Farquharson C, Pitsillides AA (2009) Genetic selection for fast growth generates bone architecture characterised by enhanced periosteal expansion and limited consolidation of the cortices but a diminution in the early responses to mechanical loading. Bone 45:357-366
46. Yoshida A (1966) Glucose 6-phosphate dehydrogenase of human erythrocytes. I. Purification and characterization of normal (B+) enzyme. J Biol Chem 241:4966-4976
47. Kunnel JG, Igarashi K, Gilbert JL, Stern PH (2004) Bone anabolic responses to mechanical load in vitro involve COX-2 and constitutive NOS. Connect Tissue Res 45:40-49
48. Bergula AP, Haidekker MA, Huang W, Stevens HY, Frangos JA (2004) Venous ligation-mediated bone adaptation is NOS 3 dependent. Bone 34:562-569
49. Klein-Nulend J, Helfrich MH, Sterck JG, MacPherson H, Joldersma M, Ralston SH, Semeins CM, Burger EH (1998) Nitric oxide response to shear stress byhuman bone cell cultures is endothelial nitric oxide synthase dependent. Biochem Biophys Res Commun 250:108-114
50. Stravopodis DJ, Margaritis LH, Voutsinas GE (2007) Drugmediated targeted disruption of multiple protein activities through functional inhibition of the Hsp90 chaperone complex. Curr Med Chem 14:3122-3138
51. Compton SA, Elmore LW, Haydu K, Jackson-Cook CK, Holt SE (2006) Induction of nitric oxide synthase-dependent telomere shortening after functional inhibition of Hsp90 in human tumor cells. Mol Cell Biol 26:1452-1462
52. Miao RQ, Fontana J, Fulton D, Lin MI, Harrison KD, Sessa WC (2008) Dominant-negative Hsp90 reduces VEGF-stimulated nitric oxide release and migration in endothelial cells. Arterioscler Thromb Vasc Biol 28:105-111
53. 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
54. 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
55. Aguirre J, Buttery L, O'Shaughnessy M, Afzal F, Fernandez de Marticorena I, 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
56. Cuzzocrea S, Mazzon E, Dugo L, Genovese T, Di Paola R, Ruggeri Z, VegetoE, Caputi AP, VanDeLoo FA, Puzzolo D, Maggi A (2003) Inducible nitric oxide synthase mediates bone loss in ovariectomized mice. Endocrinology 144:1098-1107
57. Caballero-Alias AM, Loveridge N, Lyon A, Das-Gupta V, Pitsillides A, Reeve J (2004) NOS isoforms in adult human osteocytes: multiple pathways of NO regulation? Calcif Tissue Int 75:78-84
58. Cho K, Demissie S, Dupuis J, Cupples LA, Kathiresan S, Beck TJ, Karasik D, Kiel DP (2008) Polymorphisms in the endothelial nitric oxide synthase gene and bone density/ultrasound and geometry in humans. Bone 42:53-60
59. Riancho JA, Zarrabeitia MT, Fernandez-Luna JL, Gonzalez-Macias J (1995) Mechanisms controlling nitric oxide synthesis in osteoblasts. Mol Cell Endocrinol 107:87-92
60. Riancho JA, Salas E, Zarrabeitia MT, Olmos JM, Amado JA, Fernandez-Luna JL, Gonzalez-Macias J (1995) Expression and functional role of nitric oxide synthase in osteoblast-like cells. J Bone Miner Res 10:439-446
61. 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