Heme oxygenase isozymes in bone: Induction of HO-1 mRNA following physiological levels of mechanical loading in vivo

Bone

Volumn 23, Issue 5, 1998, Pages 433-436

  Rawlinson, S C F ^a   Zaman, G ^a   Mosley, J R ^a   Pitsillides, A A ^a   Lanyon, L E ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

Heme oxygenase; Mechanical load; Osteoblasts; Osteocytes

Indexed keywords

CARBON MONOXIDE; HEME OXYGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BONE METABOLISM; BONE STRESS; CONTROLLED STUDY; NONHUMAN; NORTHERN BLOTTING; OSTEOBLAST; OSTEOCYTE; RAT; ULNA;

ANIMALS; BLOTTING, NORTHERN; DNA PRIMERS; FEMALE; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; IMMUNOENZYME TECHNIQUES; OSTEOBLASTS; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STRESS, MECHANICAL; ULNA; WEIGHT-BEARING;

EID: 0031682171     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/S8756-3282(98)00125-2     Document Type: Article

References (48)

1. Balla J., Nath K.A., Balla G., Juckett M.B., Jacob H.S., Vercellotti G.M. Endothelial-cell heme oxygenase and ferritin induction in rat lung by hemoglobin in-vivo. Am J Physiol Lung Cell Molec Physiol. 12:1995;L321-L327.
2. Buga G.M., Gold M.E., Fukuto J.M., Ignarro L.J. Shear stress-induced release of nitric oxide from endothelial cells grown on beads. Hypertension. 17:1991;187-193.
3. Busse R., Fleming I. Regulation and functional consequences of endothelial nitric oxide formation. Ann Med. 27:1995;331-340.
4. Choi A.M., Tucker R.W., Carlson S.G., Weigand G., Holbrook N.J. Calcium mediates expression of stress-response genes in prostaglandin A2-induced growth arrest. FASEB J. 8:1994;1048-1054.
5. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 162:1987;156-159.
6. Chow J.W., Chambers T.J. Indomethacin has distinct early and late actions on bone formation induced by mechanical stimulation. Am J Physiol. 267:1994;E287-E292.
7. Cruse I., Maines M.D. Evidence suggesting that the two forms of heme oxygenase are products of different genes. J Biol Chem. 263:1988;3348-3353.
8. Essig D.A., Borger D.R., Jackson D.A. Induction of heme oxygenase-1 (HSP32) mRNA in skeletal muscle following contractions. Am J Physiol. 272:1997;C59-C67.
9. Fox S.W., Chambers T.J., Chow J.W. Nitric oxide is an early mediator of the increase in bone formation by mechanical stimulation. Am J Physiol. 270:1996;E955-E960.
10. Frangos J.A., Huang T.Y., Clark C.B. Steady shear and step changes in shear stimulate endothelium via independent mechanisms - superposition of transient and sustained nitric oxide production. Biochem Biophys Res Commun. 224:1996;660-665.
11. Fukushima O., Gay C.V. Ultrastructural localization of guanylate cyclase in bone cells. J Histochem Cytochem. 39:1991;529-535.
12. Hara S., Miyata A., Yokoyama C., Inoue H., Brugger R., Lottspeich F., Ullrich V., Tanabe T. Isolation and molecular cloning of prostacyclin synthase from bovine endothelial cells. J Biol Chem. 269:1994;19897-19903.
13. Hecker M., Mulsch A., Bassenge E., Busse R. Vasoconstriction and increased flow Two principal mechanisms of shear stress-dependent endothelial autacoid release . Am J Physiol. 265:1993;H828-H833.
14. Hukkanen M., Pitsillides A.A., Rawlinson S.C.F., Suswillo R., Zaman G., Platts L.A.M., Polak J.M., Lanyon L.E. A putative role for osteocyte eNOS-derived NO in adaptive bone remodelling. J Pathol. 181:1997;A42.
15. Ingi T., Cheng J., Ronnett G.V. Carbon monoxide An endogenous modulator of the nitric oxide-cyclic GMP signaling system . Neuron. 16:1996;835-842.
16. Iversen P.O., Nicolaysen G., Benestad H.B. Endogenous nitric oxide causes vasodilation in rat bone marrow, bone, and spleen during accelerated hematopoiesis. Exp Hematol. 22:1994;1297-1302.
17. Johnson D.L., McAllister T.N., Frangos J.A. Fluid flow stimulates rapid and continuous release of nitric oxide in osteoblasts. Am J Physiol. 271:1996;E205-E208.
18. Kleinnulend J., Semeins C.M., Ajubi N.E., Nijweide P.J., Burger E.H. Pulsating fluid-flow increases nitric-oxide (No) synthesis by osteocytes but not periosteal fibroblasts - correlation with prostaglandin up-regulation. Biochem Biophys Res Commun. 217:1995;640-648.
19. Kutty R.K., Kutty G., Rodriguez I.R., Chader G.J., Wiggert B. Chromosomal localization of the human heme oxygenase genes Heme oxygenase-1 (HMOX1) maps to chromosome 22q12 and heme oxygenase-2 (HMOX2) maps to chromosome 16p13.3 . Genomics. 20:1994;513-516.
20. Llesuy S.F., Tomaro M.L. Heme oxygenase and oxidative stress Evidence of involvement of bilirubin as physiological protector against oxidative damage . Biochim Biophys Acta. 1223:1994;9-14.
21. Luscher T.F., Tanner F.C., Noll G. Lipids and endothelial function Effects of lipid-lowering and other therapeutic interventions . Curr Opin Lipidol. 7:1996;234-240.
22. Maines M.D. Heme oxygenase Function, multiplicity, regulatory mechanisms, and clinical applications . FASEB J. 2:1988;2557-2568.
23. McCoubrey W.K., Huang T.J., Maines M.D. Isolation and characterization of a cDNA from the brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem. 247:1997;725-732.
24. McDonagh A.F. Is bilirubin good for you? Clin Perinatol. 17:1990;359-369.
25. Morita T., Perrella M.A., Lee M.E., Kourembanas S. Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc Natl Acad Sci USA. 92:1995;1475-1479.
26. Nose K., Shibanuma M., Kikuchi K., Kageyama H., Sakiyama S., Kuroki T. Transcriptional activation of early-response genes by hydrogen-peroxide in a mouse osteoblastic cell-line. Eur J Biochem. 201:1991;99-106.
27. Okiji T., Morita I., Kawashima N., Kosaka T., Suda H., Murota S. Immunohistochemical detection of prostaglandin I2 synthase in various calcified tissue-forming cells in rat. Arch Oral Biol. 38:1993;31-36.
28. Pead M.J., Lanyon L.E. Indomethacin modulation of load-related stimulation of new bone formation in vivo. Calcif Tissue Int. 45:1989;34-40.
29. Pereira B., Wu K.K., Wang L.H. Molecular cloning and characterization of bovine prostacyclin synthase. Biochem Biophys Res Commun. 203:1994;59-66.
30. Pineda J., Kogan J.H., Aghajanian G.K. Nitric oxide and carbon monoxide activate locus coeruleus neurons through a cGMP-dependent protein kinase Involvement of a nonselective cationic channel . J Neurosci. 16:1996;1389-1399.
31. Pitsillides A.A., Rawlinson S.C.F., Suswillo R.F., Bourrin S., Zaman G., Lanyon L.E. Mechanical strain-induced NO production by bone cells A possible role in adaptive bone (re)modeling? FASEB J. 9:1995;1614-1622.
32. Poss K.D., Tonegawa S. Reduced stress defence in heme oxygenase 1-deficient cells. Proc Natl Acad Sci USA. 94:1997;10925-10930.
33. Raju V.S., McCoubrey W.K. Jr, Maines M.D. Regulation of heme oxygenase-2 by glucocorticoids in neonatal rat brain Characterization of a functional glucocorticoid response element . Biochim Biophys Acta. 1351:1997;89-104.
34. Rawlinson S.C.F., El Haj A.J., Minter S.L., Tavares I.A., Bennett A., Lanyon L.E. Loading-related increases in prostaglandin production in cores of adult canine cancellous bone in vitro A role for prostacyclin in adaptive bone remodeling? J Bone Miner Res. 6:1991;1345-1351.
35. Rawlinson S.C.F., Pitsillides A.A., Lanyon L.E. Involvement of different ion channels in osteoblasts' and osteocytes' early response to mechanical strain. Bone. 19:1996;609-614.
36. Rawlinson S.C.F., Pitsillides A.A., Zaman G., Lanyon L.E. Effect of exogenous carbon monoxide on loading-related pre-osteogenic responses. J Bone Miner Res. 12:1997;P13-P13.
37. Rotenberg M.O., Maines M.D. Isolation, characterization, and expression in Escherichia coli of a cDNA encoding rat heme oxygenase-2. J Biol Chem. 265:1990;7501-7506.
38. Rotenberg M.O., Maines M.D. Characterization of a cDNA-encoding rabbit brain heme oxygenase-2 and identification of a conserved domain among mammalian heme oxygenase isozymes Possible heme-binding site? Arch Biochem Biophys. 290:1991;336-344.
39. Rubin C.T., Lanyon L.E. Regulation of bone formation by applied dynamic loads. J Bone J Surg [Am]. 66:1984;397-402.
40. Rubin C.T., Lanyon L.E. Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int. 37:1985;411-417.
41. Tetsuka T., Daphnaiken D., Srivastava S.K., Morrison A.R. Regulation of heme oxygenase messenger-RNA in mesangial cells - prostaglandin E(2), negatively modulates interleukin-1-induced heme oxygenase-1 messenger RNA. Biochem Biophys Res Commun. 212:1995;617-623.
42. Turner C.H., Takano Y., Owan I., Murrell G.A.C. Nitric-oxide inhibitor L-NAME suppresses mechanically induced bone - formation in rats. Am J Phys Endocrinol Metab. 33:1996;E634-E639.
43. VanUffelen B.E., de Koster B.M., VanSteveninck J., Elferink J.G. Carbon monoxide enhances human neutrophil migration in a cyclic GMP-dependent way. Biochem Biophys Res Commun. 226:1996;21-26.
44. Verma A., Hirsch D.J., Glatt C.E., Ronnett G.V., Snyder S.H. Carbon monoxide A putative neural messenger . Science. 259:1993;381-384.
45. Wagner C.T., Durante W., Christodoulides N., Hellums J.D., Schafer A.I. Hemodynamic forces induce the expression of heme oxygenase in cultured vascular smooth muscle cells. J Clin Invest. 100:1997;589-596.
46. Yamaguchi T., Terakado M., Horio F., Aoki K., Tanaka M., Nakajima H. Role of bilirubin as an antioxidant in an ischemia-reperfusion of rat liver and induction of heme oxygenase. Biochem Biophys Res Commun. 223:1996;129-135.
47. Yoshida T., Biro P., Cohen T., Muller R.M., Shibahara S. Human heme oxygenase cDNA and induction of its mRNA by hemin. Eur J Biochem. 171:1988;457-461.
48. Zakhary R., Gaine S.P., Dinerman J.L., Ruat M., Flavahan N.A., Snyder S.H. Heme oxygenase 2 Endothelial and neuronal localization and role in endothelium-dependent relaxation . Proc Natl Acad Sci USA. 93:1996;795-798.