Skip to main content

Mechanical Load ± Growth Factors Induce [Ca2+]i Release, Cyclin D1 Expression and DNA Synthesis in Avian Tendon Cells

  • Chapter
Cell Mechanics and Cellular Engineering

Abstract

Tendons are fibrous connective tissues designed to transmit the force of muscle contraction to bone to effect limb movement. To accomplish the latter task, tendons mandate a more complex architecture than is generally appreciated: the origin is spread over muscle in a trellis-like epimycium to permit maximum surface area for contractile input. The principle bulk of tendon is comprised of highly aligned matrix containing 70–80% type I collagen to provide tensile strength, 10–40% elastin, yielding compliance and elasticity, proteoglycans as pulse dampeners, as well as lipids, whose presence in the tendon epitenon may reduce shear stress-induced friction (Oakes and Bialkower 1977; Vogel and Evanko 1988; Banes et al. 1988; Tsuzaki et al. 1993; Brigman et al. In press). There are at least two cell populations represented in the major anatomical compartments of tendon (Riederer-Henderson et al. 1983; Banes et al. 1988; Tsuzaki et al. 1993). The epitenon contains a large, polygonal to round cell (tendon epitenon synovial cell, TSC) embedded in a lipid and proteoglycan-rich matrix containing only 25% collagen, while the internal portion of tendon contains fibroblasts (tendon internal fibroblasts, TIF) in tightly packed rows amidst linear and branching collagen fascicles and bundles (Riederer-Henderson et al. 1983; Banes et al. 1988). TSC occupy the surface of tendon in a 2–8 cell-thick border contiguous with cells in the endotenon that partition collagen fascicles from one another (Greenlee and Ross 1967; Rowe 1985a, b).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  • Abrahams, M. Mechanical behavior of tendon in vitro. Med. Biol. Engin. 5:433; 1967.

    Article  CAS  Google Scholar 

  • Allbritton, N. L.; Meyer, T.; Stryer, L. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258:1812–1815; 1992.

    Article  PubMed  CAS  Google Scholar 

  • Baird, C. W.; Boitano, S.; Brigman, B.; Sanderson, M.; Keagy, B. A.; Banes, A. J. Heparin inhibits mechanically induced calcium wave propagation in smooth muscle cells. Submitted.

    Google Scholar 

  • Banes, A. J.; et al. Cell cycle kinetics and stimulation of DNA synthesis in tendon synovial and internal fibroblasts released from quiescence by serum or growth factors. J. Orthop. Res. Submitted.

    Google Scholar 

  • Banes, A. J.; Brigman, B. E.; Baird, C.; Yin, H.; Tsuzaki, M.; Almekinders, L.; Lawrence, W. T. Stimulation of DNA synthesis in tendon synovial and internal fibroblasts released from quiescence by serum, growth factors or mechanical loading. Orthop. Trans. In Press.

    Google Scholar 

  • Banes, A. J. Mechanical strain and the mammalian cell. In: Frangos, J., ed. Physical forces and the mammalian cell. Orlando: Academic Press; 1993.

    Google Scholar 

  • Banes, A. J.; Baird, C.; Tsuzaki, M.; Brigman, B.; Lawrence, W. T.; Keagy, B.; Sanderson, M.; Boitano, S. Tendon synovial and internal fibroblasts respond rapidly to mechanical load with IP and Ca2+ bursts communicated to adjacent cells, followed by DNA synthesis. Abstracts of the 38th Plastic Surgery Research Council Meeting: 25–29; 1993.

    Google Scholar 

  • Banes, A. J.; Link, G. W.; Gilbert, J. W.; Monbureau, O. Culturing cells in a mechanically active environment: I. The Flexercell Strain Unit can apply cyclic or static tension or compression to cells in culture. Am. Biotech. Lab. 8:12–22; 1990.

    CAS  Google Scholar 

  • Banes, A. J.; Donlon, K.; Link, G. W.; Gillespie, G. Y.; Bevin, A. G.; Peterson, H. D.; Bynum, D.; Watts, S.; Dahners, L. A simplified method for isolation of tendon synovial cells and internal fibroblasts: Conformation of origin and biological properties. J. Orthop. Res. 6:83–94; 1988a.

    Article  CAS  Google Scholar 

  • Banes, A. J.; Link, G. W.; Bevin, A. G.; Peterson, H. D.; Gillespie, G. Y.; Bynum, D.; Watts, S.; Dahners, L. Tendon synovial cells secrete fibronectin in vivo and in vitro. J. Orthop. Res. 6:73–82; 1988b.

    Article  CAS  Google Scholar 

  • Banes, A. J.; Gilbert, J.; Taylor, D.; Monbureau, O. A new vacuum-operated stress-providing instrument that applies static or variable duration cyclic tension or compression to cells in vitro. J. Cell Sci. 75:35–42; 1985.

    PubMed  CAS  Google Scholar 

  • Bennett, M. V. L.; Barrio, L. C.; Bargiello, T. A.; Spray, D. C.; Hertzberg, E.; Saez, J. C. Gap junctions: New tools, new answers, new questions. Neuron 6:305–320; 1991.

    Article  PubMed  CAS  Google Scholar 

  • Berk, A. J.; Sharp, P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of SI endonuclease-digested hybrids. Cell 12:721–732; 1977.

    Article  PubMed  CAS  Google Scholar 

  • Beyer, E. C.; Paul, D. L.; Goodenough, D. A. Connexin family of gap junction proteins. J. Mem. Biol. 116:187–194; 1990.

    Article  CAS  Google Scholar 

  • Boitano, S.; Dirksen, E. R.; Sanderson, M. Intercellular propagation of calcium waves mediated by inositol trisphosphate. Science 258:292–295; 1992.

    Article  PubMed  CAS  Google Scholar 

  • Brighton, C. T.; Strafford, B.; Gross, S. B.; Leatherwood, D. F.; Williams, U. L.; Pollack, S. R. The proliferative and synthetic response of isolated calvarial bone cells of rats to cyclic biaxial mechanical strain. J. Bone Joint Surg. Am 73:320–331; 1991.

    PubMed  CAS  Google Scholar 

  • Brigman, B. E.; Yin, H.; Tsuzaki, M.; Lawrence, W. T.; Banes, A. J. Fibronectin in the tendon-synovial complex: Quantitation in vivo and in vitro by ELISA and relative mRNA levels by quantitative PCR and Northern analysis. J. Orthop. Res. In Press.

    Google Scholar 

  • Chaplin, D. M.; Greenlee, T. K. The development of human digital tendons. J. Anat. 120:253–274; 1975.

    PubMed  CAS  Google Scholar 

  • Charles, A. C.; Merrill, J. E.; Dirksen, E. R.; Sanderson, M. J. Intercellular calcium signaling via gap junctions in glioma cells. J. Cell. Bio. 118:195–201; 1992.

    Article  CAS  Google Scholar 

  • Christ, G. J.; Moreno, A. P.; Melman, A.; Spray, D. C. Gap junction-mediated intercellular diffusion of Ca2+ in cultured human corporal smooth muscle cells. Am. J.Phys.C373–C383;1992.

    Google Scholar 

  • Clemmons, D. R. Insulin-like growth factor binding protein control secretion and mechanisms of action. Adv Exp Med Biol 293:113–123; 1991.

    PubMed  CAS  Google Scholar 

  • Crow, D. S.; Beyer, E. C.; Paul, D. L.; Kobe, S. S.; Lau, A. F. Phosphorylation of connexin43 gap junction protein in uninfected and Rous sarcoma virus-transformed mammalian fibroblasts. Mol. Cell Biol. 10:1754–1763; 1990.

    PubMed  CAS  Google Scholar 

  • Demer, L. L.; Wortham, C. M.; Dirksen, E. R.; Sanderson, M. J. Mechanical stimulation induces intercellular calcium signaling in bovine aortic endothelial cells. Am. J. Physiol. 264:H2094–H2102; 1993.

    PubMed  CAS  Google Scholar 

  • Eberhard, D.A. and Holz, R.W. Intracellular Ca2+ activates phospholipase C. Trends Neurosci. 11:517–520.

    Google Scholar 

  • Ehrlich, H. P.; Buttle, D. J.; Bernanke, D. H. Physiological variables affecting collagen lattice contraction by human dermal fibroblasts. Exp. Mol. Pathol. 50:220–229; 1989.

    Article  PubMed  CAS  Google Scholar 

  • Ehrlich, H.P. The modulation of contraction of fibroblast populated collagen lattices by types I, II, and III collagen. Tissue-Cell. 20:47–50; 1988.

    Article  PubMed  CAS  Google Scholar 

  • Greco, R.M., Ehrlich, H.P. Differences in cell division and thymidine incorporation with rat and primate fibroblasts in collagen lattices. Tissue-Cell. 24: 843–851; 1992.

    Article  PubMed  CAS  Google Scholar 

  • Favoloro, J.; Treisman, R.; Kannen, R. Transcription maps of polyoma virus-specific RNA: Analysis by two-dimensional nuclease S1 gel mapping. Meth. Enzymol. 65:718–749; 1980.

    Article  Google Scholar 

  • Geist, S. T.; Civitelli, R.; Beyer, E. C.; Steinberg. Calcium waves in osteoblastic cells. Mol. Biol. Cell 4:218a; 1993.

    Google Scholar 

  • Gilbert, J. A.; Weinhold, P. S.; Banes, A. J.; Link, G. W.; Jones, G. L. Strain profiles for circular cell culture plates containing flexible surfaces employed to mechanically deform cells in vitro. J. Biomech. In Press.

    Google Scholar 

  • Gilman, M. Preparation of cytoplasmic RNA from tissue culture cells. In: Ausubel, F. M.; et al. eds. Current protocols in molecular biology. New York: Greene.; 1989: pp 4.1.2–4.1.6.

    Google Scholar 

  • Greco, R. M.; Ehrlich, H. P. Differences in cell division and thymidine incorporation with rat and primate fibroblasts in collagen lattices. Tiss. Cell. 24:843–851; 1992.

    Article  CAS  Google Scholar 

  • Greenlee, T. K.; Ross, R. The development of rat flexor digital tendon, a fine structure study. J. Ultrastr. Res. 18:354–376; 1967.

    Article  Google Scholar 

  • Hasson, H. A.; Engstrom, A. M. C.; Holm, S.; Rosenqvist, A. L. Somatomedin C immunoreactivity in the Achilles tendon varies in a dynamic manner with the mechanical load. Acta Physiol. Scand. 134: 199–208; 1988.

    Article  Google Scholar 

  • Hassouna, N; Michot, B.; Bachellerie, J.-P. The complete nucleotide sequence of mouse 28 S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucl. Acids Res. 12:3563; 1984.

    Article  PubMed  CAS  Google Scholar 

  • Herrick, W. C.; Kingsbury, H. B.; Lou, D. Y. S. A study of the normal range of strain, strain rate and stiffness of tendon. J. Biomed. Matls. Res. 12:877–894; 1978.

    Article  CAS  Google Scholar 

  • Hu, P.; Xiao, H.; Brigman, B.; Lawrence, W. T.; Banes, A. J. G1 D cyclins are differentially regulated in tendon epitenon and internal fibroblasts. Trans. Orthop Res. Soc. In Press.

    Google Scholar 

  • Hu, P.; Xiao, H.; Brigman, B.; Lawrence, W. T.; Banes, A. J. Serum, growth factors, and mechanical load stimulate cyclin D1 mRNA and protein in quiescent tendon cells. Molec. Bio. Cell 4:239a; 1993.

    Google Scholar 

  • Ingber, D. E. Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J. Cell Sci. 104:613–627; 1993.

    PubMed  Google Scholar 

  • Ingber, D. E. Control of capillary growth and differentiation by extracellular matrix. Use of a tensegrity (tensional integrity) mechanism for signal processing. Chest 99:34s–40s; 1991.

    PubMed  CAS  Google Scholar 

  • Laird, D. W.; Puranam, K. L.; Revel, J. P. Turnover and phosphorylation dynamics of connexin 43 gap junction protein in cultured cardiac myocytes. Biochem. J. 273:67–72; 1991.

    PubMed  CAS  Google Scholar 

  • Lehrach, H.; Diamond, D.; Wozney, J. M.; Boedtker, H. RNA molecular weight determinations by gel electrophoresis under denaturing conditions: a critical reexamination. Biochem. 16:4743; 1977.

    Article  CAS  Google Scholar 

  • Mitsumata, M.; Fishel, R. S.; Nerem, R. M.; Alexander, R. W.; Berk, B. C. Fluid shear stress stimulates platelet-derived growth factor expression in endothelial cells. Am. J. Physiol. 265:H3–H8; 1993.

    PubMed  CAS  Google Scholar 

  • Mullis, K. B.; Faloona, F. A. Specific synthesis of DNA in vitro via a polymerasecatalyzed chain reaction. In Wu, R., ed. Methods in Enzymology 155:335–350; 1987.

    Google Scholar 

  • Oakes, B. W.; Bialkower, B. Biomechanical and ultrastructural studies on the elastic wing tendon from the domestic fowl. J. Anat. 123:369–387; 1977.

    PubMed  CAS  Google Scholar 

  • Okamoto, T.; Dorofi, D.; Hu, P.; Tsuzaki, M.; Keagy, B. A.; Banes, A. J. Mechanical load stimulates αvβ3 mRNA and protein in human umbilical endothelial cells. Mol. Bio. Cell 4:406a; 1993.

    Google Scholar 

  • Pedersen, D. R.; Bottlang, M.; Brown, T. D.; Banes, A. J. Hyperelastic constitutive properties of polydimethyl siloxane cell cuture membranes. Meeting of the American Society of Mechanical Engineering (ASME); 1993.

    Google Scholar 

  • Pedersen, D. R.; Brown, T. D.; Banes, A. J. Mechanical behavior of a new substratum for strain-mediated cell culture experiments. NACOB II:The Second North American Congress on Biomechanics. Chicago, IL, Aug 24–28, 1992.

    Google Scholar 

  • Peracchia, C. Effects of the anesthetics heptanol, halothane and isoflurane on gap junction conductance in crayfish septate axons: a calcium-and hydrogen-independent phenomenon potentiated by caffeine and theophylline, and inhibited by 4-aminopyridine. J. Mem. Bio. 121:67–78; 1991.

    Article  CAS  Google Scholar 

  • Pledger, W. J.; Stiles, C. D.; Antoniades, H. N; Scher, C. D. An ordered sequence of events is required before BALB/c-3T3 cells become committed to DNA synthesis. Proc. Natl. Acad. Sci. U. S. A. 75:2839–2843; 1978.

    Article  PubMed  CAS  Google Scholar 

  • Raynal, F.; Michot, B.; Bachellerie, J. P. Complete nucleotide sequence of mouse 18S rRNA gene: Comparisons with other available homologs. FEBS Lett. 167:263; 1984.

    Article  PubMed  CAS  Google Scholar 

  • Revel, J. P.; Karnovsky, J. J. Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol. 33:C7–C12; 1967.

    Article  PubMed  CAS  Google Scholar 

  • Riederer-Henderson, M. A.; Gauger, A.; Olson, L.; Robertson, C.; Greenlee, T.K. Jr. Attachment and extracellular matrix differences between tendon and synovial fibroblastic cells. In Vitro 19:127–133; 1983.

    Article  PubMed  CAS  Google Scholar 

  • Robertson, J. D. The occurrence of a subunit pattern in the unit membrane of club ending in Mauthner cell synapses in goldfish brains. J. Cell Biol. 19:201–221; 1963.

    Article  PubMed  CAS  Google Scholar 

  • Robotewskyj, A.; Griem, M. L.; Davies, P. F. Remodeling of endothelial focal adhesion sites in response to flow: quantitative studies by confocal image analysis. Faseb J. 7(3):A54; 1993.

    Google Scholar 

  • Rodbard, S. Negative feedback mechanisms in the architecture and function of the connective and cardiovascular tissues. Perspect. on Med. Biol. 13: 507–727; 1970.

    CAS  Google Scholar 

  • Rowe, R. W. D. The structure of the rat tail tendon. Conn. Tiss. Res. 14:9–20; 1985a.

    Article  CAS  Google Scholar 

  • Rowe, R. W. D. The structure of rat tail tendon fasicles. Conn. Tiss. Res. 14:21–30; 1985b.

    Article  CAS  Google Scholar 

  • Saez, J. C.; Connor, J. A.; Spray, D. C.; Bennett, M. V. Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-trisphosphate, and to calcium ions. Proc. Natl. Acad. Sci. U. S. A. 86:2708–2712; 1989.

    Article  PubMed  CAS  Google Scholar 

  • Sanderson, M. J.; Charles, A. C.; Dirksen, E. R. Mechanical stimulation and intracellular communication increases intracellular Ca2+ in epithelial cells. Cell Regulation 1:585–596; 1990.

    PubMed  CAS  Google Scholar 

  • Sanderson, M. J.; Dirksen, E. R. Inositol trisphosphate mediates intercellular communication between ciliated epithelial cells. J. Cell Biol. 109:304a; 1989.

    Google Scholar 

  • Sanderson, M. J.; Chow, I.; Dirksen, E. R. Intercellular communictaion between ciliated cells in culture. Am. J. Physiol. 254:C63–C74; 1988.

    PubMed  CAS  Google Scholar 

  • Sanderson, M. J.; Dirksen, E. R. Mechanosensitivity of cultured ciliated cells from the mammalian respiratory tract: implications for the regulationof mucociliary transport. Proc. Natl. Acad. Sci. U. S. A. 83:7302–7306; 1986.

    Article  PubMed  CAS  Google Scholar 

  • Stopak, D.; Harris, A. Connective tissue morphogenesis by fibroblast traction. Devel. Biol. 90: 383–398; 1982.

    Article  CAS  Google Scholar 

  • Thomas, P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc. Natl. Acad. Sci. U. S. A 77:5201; 1980.

    Article  PubMed  CAS  Google Scholar 

  • Tsuzaki, M.; Xiao, H.; Brigman, B.; Lawrence, W. T.; Van Wyk, J.; Banes, A. J. Growth stimulatory and inhibitory factors in tendon: autocrine/paracrine functions of IGF-1 and TGF-b in maintenance and repair. J. Orthop. Res. Submitted.

    Google Scholar 

  • Tsuzaki, M.; Yamauchi, M.; Banes, A. J. Tendon Collagens: Extracellular matrix composition in shear stress and tensile components of flexor tendon. Conn. Tiss. Res. 29:141–152; 1993.

    Article  CAS  Google Scholar 

  • Vogel, K.; Evanko, S. P. Proteoglycans of fetal bovine tendon. Trans. Orthop. Res. Soc. 13:182; 1988.

    Google Scholar 

  • Walker, L. B.; Harris, E. H.; Benedict, J. V. Stress-strain relationship in human cadaveric plantaris tendon: A preliminary study. Med. Elect. Bio. Engin. 2:31; 1964.

    Article  CAS  Google Scholar 

  • Walker, P.; Amstutz, H. C.; Rubinfeld, M. J. Canine tendon studies. II. Biomechanical evaluation of normal and regrown canine tendons. Biomed. Matls. Res. 10:61; 1976.

    Article  CAS  Google Scholar 

  • Wang, N.; Butler, J. P.; Ingber, D. E. Mechanotransduction across the cell surface and through the cytoskeleton. Science 260:1124–1127; 1993.

    Article  PubMed  CAS  Google Scholar 

  • Whitaker, M. Phosphoinositide second mesengers in eggs and oocytes. In: Inositol lipids in cell signalling, ed. R.H. Michell, A.H. Drummond and C.P. Downes. London: Academic Press, 459–483.

    Google Scholar 

  • Winston, J. T.; Pledger, W. J. Growth factor regulation of cyclin D1 mRNA expression through protein synthesis dependent and independent mechanisms. Mol. Bio. Cell 4:1133–1144; 1993.

    CAS  Google Scholar 

  • Xiao, H.; Hu, P.; Banes, A. J.; Lawrence, W. T. Cyclin D1 mRNA is serum inducible in both normal human dermal and keloid fibroblasts but temporally later in keloid cells. Mol. Cell. Bio. 4:240a; 1993.

    Google Scholar 

  • Xiong, Y.; Menninger, J.; Beach, D.; Ward, D. C. Molecular cloning and chromosomal mapping of CCND genes encoding human D-type cyclins. Genomics 13:575–584; 1992.

    Article  PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1994 Springer-Verlag New York, Inc.

About this chapter

Cite this chapter

Banes, A.J. et al. (1994). Mechanical Load ± Growth Factors Induce [Ca2+]i Release, Cyclin D1 Expression and DNA Synthesis in Avian Tendon Cells. In: Mow, V.C., Tran-Son-Tay, R., Guilak, F., Hochmuth, R.M. (eds) Cell Mechanics and Cellular Engineering. Springer, New York, NY. https://doi.org/10.1007/978-1-4613-8425-0_13

Download citation

  • DOI: https://doi.org/10.1007/978-1-4613-8425-0_13

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4613-8427-4

  • Online ISBN: 978-1-4613-8425-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics