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Annals of Biomedical Engineering

, Volume 26, Issue 4, pp 644–659 | Cite as

Electrical Signal Transmission in a Bone Cell Network: The Influence of a Discrete Gap Junction

  • Dajun Zhang
  • Sheldon Weinbaum
  • Stephen C. Cowin
Article

Abstract

A refined electrical cable model is formulated to investigate the role of a discrete gap junction in the intracellular transmission of electrical signals in an electrically coupled system of osteocytes and osteoblasts in an osteon. The model also examines the influence of the ratio q between the membrane's electrical time constant and the characteristic time of pore fluid pressure, the circular, cylindrical geometry of the osteon, and key simplifying assumptions in our earlier continuous cable model (see Zhang, D., S. C. Cowin, and S. Weinbaum. Electrical signal transmission and gap junction regulation in a bone cell network: A cable model for an osteon. Ann. Biomed. Eng. 25:379–396, 1997). Using this refined model, it is shown that (1) the intracellular potential amplitude at the osteoblastic end of the osteonal cable retains the character of a combination of a low-pass and a high-pass filter as the corner frequency varies in the physiological range; (2) the presence of a discrete gap junction near a resting osteoblast can lead to significant modulation of the intracellular potential and current in the osteoblast for measured values of the gap junction coupling strength; and (3) the circular, cylindrical geometry of the osteon is well simulated by the beam analogy used in Zhang et al. © 1998 Biomedical Engineering Society.

PAC98: 8722-q, 8710+e

Gap junctions Intercellular communication Osteon Electrokinetics Poroelasticity Cable theory Streaming potential Extracellular matrix Glycosaminoglycan Fixed-charge density Bone cell network: gap junctions 

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REFERENCES

  1. 1.
    Abramson, H. A., L. S. Moyer, and M. H. Gorin. Electrophoresis of Proteins. New York: Reinhold, 1942, p. 315.Google Scholar
  2. 2.
    Adamson, R. H., and G. Clough. Plasma proteins modify the endothelial cell glycocalyx of frog mesenteric microvessels. J. Physiol. (London)445:473-486, 1992.Google Scholar
  3. 3.
    Bennett, M. V. L. Physiology of electrotonic junctions. Ann. (N.Y.) Acad. Sci.137:509-539, 1966.Google Scholar
  4. 4.
    Bingmann, D., K. Schirrmacher, and D. Jones. Signalling in bone: Electrophysiological studies on cultured cells derived from calvarial fragments of rats. Cells Mater.4:275-285, 1994.Google Scholar
  5. 5.
    Burghardt, R. C., R. Barhoumi, T. C. Sewall, and J. A. Bowen. Cyclic AMP induces rapid increases in gap junction permeability and changes in the cellular distribution of connexin 43. J. Membr. Biol.148:243-253, 1995.Google Scholar
  6. 6.
    Chakkalakal, D. A., M. W. Johnson, R. A. Harper, and J. L. Katz. Dielectric properties of fluid-saturated bone. IEEE Trans. Biomed. Eng.27:95-100, 1980.Google Scholar
  7. 7.
    Chammas, P., W. J. Federspiel, and S. R. Eisenberg. A microcontinuum model of electrokinetic coupling in the extracellular matrix: Perturbation formulation and solution. J. Colloid Interface Sci.168:526-538, 1994.Google Scholar
  8. 8.
    Cowin, S. C. The mechanical properties of cortical bone tissue. In: Bone Mechanics, edited by S. C. Cowin. Boca Raton, FL: CRC, 1989, pp. 97-127.Google Scholar
  9. 9.
    Cowin, S. C., S. Weinbaum, and Y. Zeng. A case for the bone canaliculi as the anatomical site of strain generated potentials. J. Biomech.28:1281-1297, 1995.Google Scholar
  10. 10.
    Darrow, B. J., V. G. Fast, A. G. Kleber, E. C. Beyer, and J. E. Saffitz. Functional and structural assessment of intercellular communication. Increased conduction velocity and enhanced connexin expression in dibutyryl cAMP-treated cultured cardiac myocytes. Circ. Res.79:243-253, 1995.Google Scholar
  11. 11.
    Eisenberg, S. R., and A. J. Grodzinsky. Electrokinetic micromodel of extracellular matrix and other polyelectrolyte networks. PCH PhysicoChem. Hydrodynamics10:517-539, 1988.Google Scholar
  12. 12.
    Eriksson, C. Bone morphogenesis and surface charge. Clin. Orthop.121:295-302, 1976.Google Scholar
  13. 13.
    Fritton, S. P., K. J. McLeod, and C. T. Rubin. Cross-species spectral similarity in the strain history of bone. In: Transactions of 42nd Annual Meeting, Orthopaedic Research Society, Feb. 19-22, Atlanta, Georgia, p. 132-22, 1996.Google Scholar
  14. 14.
    Gross, D., and W. S. Williams. Streaming potential and the electromechanical response of physiologically-moist bone. J. Biomech.15:277-295, 1982.Google Scholar
  15. 15.
    Gu, W. Y., W. M. Lai, and V. C. Mow. Transport of fluid and ions through a porous-permeable charged-hydrated tissue, and streaming potential data on normal bovine articular cartilage. J. Biomech.26:709-723, 1993.Google Scholar
  16. 16.
    Happel, J., and H. Brenner. Low Reynolds Number Hydrodynamics. Englewood Cliffs, NJ: Prentice-Hall, 1965, pp. 392-404.Google Scholar
  17. 17.
    Harrigan, T. P., and J. J. Hamilton. Bone strain sensation via transmembrane potential changes in surface osteoblasts: Loading rate and microstructural implications. J. Biomech.26:183-200, 1993.Google Scholar
  18. 18.
    Helfferich, F. Ion Exchange. New York: McGraw-Hill, 1962, pp. 391-394.Google Scholar
  19. 19.
    Jeansonne, B. G., F. F. Feagin, R. W. McMinn, R. L. Shoemaker, and W. S. Rehm. Cell-to-cell communication of osteoblasts. J. Dent. Res.58:1415-1423, 1979.Google Scholar
  20. 20.
    Koch, J. C. The laws of bone architecture. Am. J. Anat.21:177-298, 1917.Google Scholar
  21. 21.
    Levick, J. R. Flow through interstitium and other fibrous matrices. Q. J. Exp. Physiol.72:409-438, 1987.Google Scholar
  22. 22.
    McLeod, K. J., and C. T. Rubin. The effect of low-frequency electrical fields on osteogenesis. J. Bone Jt. Surg. Am.74:920-929, 1992.Google Scholar
  23. 23.
    Mealing, D., G. Long, and R. W. McCarthy. Vibromyographic recording from human muscles with known fibre composition differences. Br. J. Sports Med.30:27-31, 1996.Google Scholar
  24. 24.
    Michel, C. C. Capillary permeability and how it may change. J. Physiol. (London)404:1-29, 1988.Google Scholar
  25. 25.
    Minkoff, R., V. R. Rundus, S. R. Parker, E. L. Hertzberg, J. G. Laing, and E. C. Beyer. Gap junction proteins exhibit early and specific expression during intramembranous bone formation in the developing chick mandible. Anat. Embryol.190:231-241, 1994.Google Scholar
  26. 26.
    Moreno, A. P., J. G. Laing, E. C. Beyer, and D. C. Spray. Properties of gap junction channels formed of connexin 45 endogenously expressed in human hepatoma (SKHep1) cells. Am. J. Physiol.268:C356-C365, 1995.Google Scholar
  27. 27.
    Pollack, S. R., N. Petrov, R. Salzstein, G. Brankov, and R. Blagoeva. An anatomical model for streaming potentials in osteons. J. Biomech.17:627-636, 1984.Google Scholar
  28. 28.
    Reich, K. M., C. V. Gay, and J. A. Frangos. Fluid shear stress as a mediator of osteoblast cyclic adenosine monophosphate production. J. Cell Physiol.143:100-104, 1990.Google Scholar
  29. 29.
    Rice, J. R., and M. P. Cleary. Some basic stress diffusion solutions for fluid-saturated elastic porous media with compressible constituents. Rev. Geophys. Space Phys.14:227- 241, 1976.Google Scholar
  30. 30.
    Rubin, C. T., and K. J. McLeod. Endogenous control of bone morphology via frequency specific, low magnitude functional strain. In: Bone Structure and Remodeling, edited by A. Odgaard and H. Weinans, Recent Advances in Human Biology series, Vol. 2, Singapore: World Scientific, 1995, pp. 79-90.Google Scholar
  31. 31.
    Schirrmacher, K., D. Nonhoff, D. Bingmann, and P. R. Brink. Calcium effects on gap junctions between rat osteoblast-like cells. in vitro. Pflügers Arch. Eur. J. Phys.(Supplement) 431:R92, 1996.Google Scholar
  32. 32.
    Shaw, D. J. Electrophoresis.London: Academic, 1969, p. 8.Google Scholar
  33. 33.
    Spray, D. C. Physiological and pharmacological regulation of gap junction channels. In: Molecular Mechanisms of Epithelial Cell Junctions: From Development to Disease, edited by S. Citi. Austin, TX: R. G. Landes, 1994, pp. 195-215.Google Scholar
  34. 34.
    Starkebaum, W., S. R. Pollack, and E. Korostoff. Microelectrode studies of stress-generated potentials in four-point bending of bone. J. Biomed. Mater. Res.13:729-751, 1979.Google Scholar
  35. 35.
    Vink, H., and B. R. Duling. Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ. Res.79:581-589, 1996.Google Scholar
  36. 36.
    Wassermann, F., and J. A. Yaeger. Fine structure of the osteocytic capsule and of the wall of the lacunae in bone. Z. Zellforsch.67:636-652, 1965.Google Scholar
  37. 37.
    Weinbaum, S., S. C. Cowin, and Y. Zeng. Excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J. Biomech.27:339-360, 1994.Google Scholar
  38. 38.
    Zeng, Y., S. C. Cowin, and S. Weinbaum. A fiber matrix model for fluid flow and streaming potentials in the canaliculi of an osteon. Ann. Biomed. Eng.22:280-292, 1994.Google Scholar
  39. 39.
    Zhang, D., and S. C. Cowin. Oscillatory bending of a poroelastic beam. J. Mech. Phys. Solids42:1575-1599, 1994.Google Scholar
  40. 40.
    Zhang, D., S. C. Cowin, and S. Weinbaum. Electrical signal transmission and gap junction regulation in a bone cell network: A cable model for an osteon. Ann. Biomed. Eng.25:379-396, 1997.Google Scholar

Copyright information

© Biomedical Engineering Society 1998

Authors and Affiliations

  • Dajun Zhang
    • 1
  • Sheldon Weinbaum
    • 1
  • Stephen C. Cowin
    • 1
  1. 1.CUNY Graduate School and Department of Mechanical EngineeringCity College of New YorkNew York

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