Bone Biology

You have full text access to this OnlineOpen article

Tumor necrosis factor α and interleukin-1β modulate calcium and nitric oxide signaling in mechanically stimulated osteocytes

  1. A. D. Bakker1,†,
  2. V. C. da Silva2,†,
  3. R. Krishnan3,
  4. R. G. Bacabac1,
  5. M. E. Blaauboer1,
  6. Y.-C. Lin3,
  7. R. A. C. Marcantonio4,
  8. J. A. Cirelli4,
  9. J. Klein-Nulend1,*

Article first published online: 29 OCT 2009

DOI: 10.1002/art.24920

Issue

Arthritis & Rheumatism

Arthritis & Rheumatism

Volume 60, Issue 11, pages 3336–3345, November 2009

Additional Information

How to Cite

Bakker, A. D., da Silva, V. C., Krishnan, R., Bacabac, R. G., Blaauboer, M. E., Lin, Y.-C., Marcantonio, R. A. C., Cirelli, J. A. and Klein-Nulend, J. (2009), Tumor necrosis factor α and interleukin-1β modulate calcium and nitric oxide signaling in mechanically stimulated osteocytes. Arthritis & Rheumatism, 60: 3336–3345. doi: 10.1002/art.24920

Author Information

  1. 1

    ACTA–Universiteit van Amsterdam and Vrije Universiteit, Research Institute MOVE, Amsterdam, The Netherlands

  2. 2

    ACTA–Universiteit van Amsterdam and Vrije Universiteit, Research Institute MOVE, Amsterdam, The Netherlands, and UNESP-São Paulo State University, School of Dentistry at Araraquara, São Paulo, Brazil

  3. 3

    Harvard School of Public Health, Boston, Massachusetts

  4. 4

    UNESP–São Paulo State University, School of Dentistry at Araraquara, São Paulo, Brazil

  1. †

    Drs. Bakker and da Silva contributed equally to this work.

*Department of Oral Cell Biology, ACTA–Vrije Universiteit, Van der Boechorststraat 7, 1081 BT Amsterdam, The Netherlands

Publication History

  1. Issue published online: 29 OCT 2009
  2. Article first published online: 29 OCT 2009
  3. Manuscript Accepted: 27 JUL 2009
  4. Manuscript Received: 1 AUG 2008

Funded by

  • Research Institute MOVE of the Vrije Universiteit Amsterdam
  • Foundation for the Coordination of Higher Education and Graduate Training, Brazil. Grant Number: MEC/CAPES BEX0481/06-8
  • Space Research Organization of The Netherlands. Grant Number: MG-055
  • Netherlands Organization For International Cooperation In Higher Education. Grant Number: Physics Development Project grant PHL-146

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (437K)

REFERENCES

  • 1
    Haugeberg G, Uhlig T, Falch JA, Halse JI, Kvien TK. Bone mineral density and frequency of osteoporosis in female patients with rheumatoid arthritis: results from 394 patients in the Oslo County rheumatoid arthritis register. Arthritis Rheum 2000; 43: 522–30.
    Direct Link:
  • 2
    Lane NE, Pressman AR, Star VL, Cummings SR, Nevitt MC. Rheumatoid arthritis and bone mineral density in elderly women: The Study of Osteoporotic Fractures Research Group. J Bone Miner Res 1995; 10: 257–63.
    Direct Link:
  • 3
    Bettica P, Cline G, Hart DJ, Meyer J, Spector TD. Evidence for increased bone resorption in patients with progressive knee osteoarthritis: longitudinal results from the Chingford study. Arthritis Rheum 2002; 46: 3178–84.
    Direct Link:
  • 4
    Lodder MC, Haugeberg G, Lems WF, Uhlig T, Orstavik RE, Kostense PJ, et al. Radiographic damage associated with low bone mineral density and vertebral deformities in rheumatoid arthritis: the Oslo-Truro-Amsterdam (OSTRA) collaborative study. Arthritis Rheum 2003; 49: 209–15.
    Direct Link:
  • 5
    Bingham CO 3rd. The pathogenesis of rheumatoid arthritis: pivotal cytokines involved in bone degradation and inflammation. J Rheumatol Suppl 2002; 65: 3–9.
  • 6
    Vis M, Havaardsholm EA, Haugeberg G, Uhlig T, Voskuyl AE, van de Stadt RJ, et al. Evaluation of bone mineral density, bone metabolism, osteoprotegerin and receptor activator of the NFκB ligand serum levels during treatment with infliximab in patients with rheumatoid arthritis. Ann Rheum Dis 2006; 65: 1495–9.
  • 7
    Bertolini DR, Nedwin GE, Bringman TS, Smith DD, Mundy GR. Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature 1986; 319: 516–8.
  • 8
    Canalis E. Effects of tumor necrosis factor on bone formation in vitro. Endocrinology 1987; 121: 1596–604.
  • 9
    Li YP, Stashenko P. Proinflammatory cytokines tumor necrosis factor-α and IL-6, but not IL-1, down-regulate the osteocalcin gene promoter. J Immunol 1992; 148: 788–94.
  • 10
    Gowen M, Wood DD, Ihrie EJ, McGuire MK, Russell RG. An interleukin 1 like factor stimulates bone resorption in vitro. Nature 1983; 306: 378–80.
  • 11
    Heath JK, Saklatvala J, Meikle MC, Atkinson SJ, Reynolds JJ. Pig interleukin 1 (catabolin) is a potent stimulator of bone resorption in vitro. Calcif Tissue Int 1985; 37: 95–7.
  • 12
    Stashenko P, Obernesser MS, Dewhirst FE. Effect of immune cytokines on bone. Immunol Invest 1989; 18: 239–49.
  • 13
    Parfitt AM. The cellular basis of bone turnover and bone loss: a rebuttal of the osteocytic resorption–bone flow theory. Clin Orthop Relat Res 1977; 127: 236–47.
  • 14
    Westerlind KC, Turner RT. The skeletal effects of spaceflight in growing rats: tissue-specific alterations in mRNA levels for TGF. J Bone Miner Res 1995; 10: 844–8.
    Direct Link:
  • 15
    Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am 1984; 66: 397–402.
  • 16
    Tatsumi S, Ishii K, Amizuka N, Li M, Kobayashi T, Kohno K, et al. Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab 2007; 5: 464–75.
  • 17
    Burger EH, Klein-Nulend J. Mechanotransduction in bone: role of the lacuno-canalicular network. FASEB J 1999; 13 Suppl: S101–12.
  • 18
    Vezeridis PS, Semeins CM, Chen Q, Klein-Nulend J. Osteocytes subjected to pulsating fluid flow regulate osteoblast proliferation and differentiation. Biochem Biophys Res Commun 2006; 29: 1082–8.
  • 19
    Vatsa A, Mizuno D, Smit TH, Schmidt CF, MacKintosh FC, Klein-Nulend J. Bio imaging of intracellular NO production in single bone cells after mechanical stimulation. J Bone Miner Res 2006; 21: 1722–8.
    Direct Link:
  • 20
    Tan SD, de Vries TJ, Kuijpers-Jagtman AM, Semeins CM, Everts V, Klein-Nulend J. Osteocytes subjected to fluid flow inhibit osteoclast formation and bone resorption. Bone 2007; 41: 745–51.
  • 21
    Kato Y, Windle JJ, Koop BA, Mundy GR, Bonewald LF. Establishment of an osteocyte-like cell line, MLO-Y4. J Bone Miner Res 1997; 12: 2014–23.
  • 22
    Bakker AD, Soejima K, Klein-Nulend J, Burger EH. The production of nitric oxide and prostaglandin E(2) by primary bone cells is shear stress dependent. J Biomech 2001; 34: 671–7.
  • 23
    Bacabac RG, Smit TH, Cowin SC, van Loon JJ, Nieuwstadt FT, Heethaar R, et al. Dynamic shear stress in parallel-plate flow chambers. J Biomech 2005; 38: 159–67.
  • 24
    Eastgate JA, Symons JA, Wood NC, Grinlinton FM, di Giovine FS, Duff GW. Correlation of plasma interleukin 1 levels with disease activity in rheumatoid arthritis. Lancet 1988; 2: 706–9.
  • 25
    Vignon E, Balblanc JC, Mathieu P, Louisot P, Richard M. Metalloprotease activity, phospholipase A2 activity and cytokine concentration in osteoarthritis synovial fluids. Osteoarthritis Cartilage 1993; 2: 115–20.
  • 26
    Westacott CI, Whicher JT, Barnes IC, Thompson D, Swan AJ, Dieppe PA. Synovial fluid concentration of five different cytokines in rheumatic diseases. Ann Rheum Dis 1990; 49: 676–81.
  • 27
    Chow JW, Fox SW, Lean JM, Chambers TJ. Role of nitric oxide and prostaglandins in mechanically induced bone formation. J Bone Miner Res 1998; 13: 1039–44.
    Direct Link:
  • 28
    Turner CH, Takano Y, Owan I, Murrell GA. Nitric oxide inhibitor L-NAME suppresses mechanically induced bone formation in rats. Am J Physiol 1996; 270: E634–9.
  • 29
    Ajubi NE, Klein-Nulend J, Alblas MJ, Burger EH, Nijweide PJ. Signal transduction pathways involved in fluid flow-induced PGE2 production by cultured osteocytes. Am J Physiol 1999; 276: E171–8.
  • 30
    Pritchard S, Guilak F. Effects of interleukin-1 on calcium signaling and the increase of filamentous actin in isolated and in situ articular chondrocytes. Arthritis Rheum 2006; 54: 2164–74.
    Direct Link:
  • 31
    Butler JP, Tolic-Norrelykke IM, Fabry B, Fredberg JJ. Traction fields, moments, and strain energy that cells exert on their surroundings. Am J Physiol Cell Physiol 2002; 282: C595–605.
  • 32
    Wang N, Tolic-Norrelykke IM, Chen J, Mijailovich SM, Butler JP, Fredberg JJ, et al. Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am J Physiol Cell Physiol 2002; 282: C606–16.
  • 33
    Fabry B, Maksym GN, Butler JP, Glogauer M, Navajas D, Fredberg JJ. Scaling the microrheology of living cells. Phys Rev Lett 2001; 87: 148102.
  • 34
    Trepat X, Deng L, An SS, Navajas D, Tschumperlin DJ, Gerthoffer WT, et al. Universal physical responses to stretch in the living cell. Nature 2007; 447: 592–5.
  • 35
    Godin LM, Suzuki S, Jacobs CR, Donahue HJ, Donahue SW. Mechanically induced intracellular calcium waves in osteoblasts demonstrate calcium fingerprints in bone cell mechanotransduction. Biomechan Model Mechanobiol 2007; 6: 391–8.
  • 36
    Bacabac RG, Mizuno D, Schmidt CF, MacKintosh FC, van Loon JJ, Klein-Nulend J, et al. Round versus flat: bone cell morphology, elasticity, and mechanosensing. J Biomech 2008; 41: 1590–8.
  • 37
    Zaman G, Pitsillides AA, Rawlinson SC, Suswillo RF, Mosley JR, Cheng MZ, et al. Mechanical strain stimulates nitric oxide production by rapid activation of endothelial nitric oxide synthase in osteocytes. J Bone Miner Res 1999; 14: 1123–31.
    Direct Link:
  • 38
    Klein-Nulend J, Helfrich MH, Sterck JG, MacPherson H, Joldersma M, Ralston SH. Nitric oxide response to shear stress by human bone cell cultures is endothelial nitric oxide synthase dependent. Biochem Biophys Res Commun 1998; 250: 108–14.
  • 39
    Presta A, Liu J, Sessa WC, Stuehr DJ. Substrate binding and calmodulin binding to endothelial nitric oxide synthase coregulate its enzymatic activity. Nitric Oxide 1997; 1: 74–87.
  • 40
    Chowdhury TT, Bader DL, Lee DA. Dynamic compression inhibits the synthesis of nitric oxide and PGE2 by IL-1β-stimulated chondrocytes cultured in agarose constructs. Biochem Biophys Res Commun 2001; 285: 1168–74.
  • 41
    Yokoyama T, Vaca L, Rossen RD, Durante W, Hazarika P, Mann DL. Cellular basis for the negative inotropic effects of tumor necrosis factor-α in the adult mammalian heart. J Clin Invest 1993; 92: 2303–12.
  • 42
    Vandamme W, Braet K, Cabooter L, Leybaert L. Tumour necrosis factor α inhibits purinergic calcium signalling in blood-brain barrier endothelial cells. J Neurochem 2004; 88: 411–21.
  • 43
    Bacabac RG, Smit TH, Mullender MG, Dijcks SJ, van Loon JJ, Klein-Nulend J. Nitric oxide production by bone cells is fluid shear stress rate dependent. Biochem Biophys Res Commun 2004; 315: 823–9.
  • 44
    Weinbaum S, Cowin SC, Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech 1994; 27: 339–60.
  • 45
    Ahuja SS, Zhao S, Bellido T, Plotkin LI, Jimenez F, Bonewald LF. CD40 ligand blocks apoptosis induced by tumor necrosis factor α, glucocorticoids, and etoposide in osteoblasts and the osteocyte-like cell line murine long bone osteocyte-Y4. Endocrinology 2003; 144: 1761–9.
  • 46
    Tan SD, Kuijpers-Jagtman AM, Semeins CM, Bronckers AL, Maltha JC, von den Hoff J, et al. Fluid shear stress inhibits TNFα-induced osteocyte apoptosis. J Dent Res 2006; 85: 905–9.
  • 47
    Bidwell JP, Yang J, Robling AG. Is HMGB1 an osteocyte alarmin? Cell Biochem 2008; 103: 1671–80.
    Direct Link:
  • 48
    Kogianni G, Mann V, Noble BS. Apoptotic bodies convey activity capable of initiating osteoclastogenesis and localized bone destruction. J Bone Miner Res 2008; 23: 915–27.
    Direct Link:
  • 49
    Rawlinson SC, Pitsillides AA, Lanyon LE. Involvement of different ion channels in osteoblasts' and osteocytes' early responses to mechanical strain. Bone 1996; 19: 609–14.
  • 50
    McAllister TN, Frangos JA. Steady and transient fluid shear stress stimulate NO release in osteoblasts through distinct biochemical pathways. J Bone Miner Res 1999; 14: 930–6.
    Direct Link:
View Full Article (HTML) Get PDF (437K)