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Journal of Anatomy logoLink to Journal of Anatomy
. 1998 Aug;193(Pt 2):215–222. doi: 10.1046/j.1469-7580.1998.19320215.x

Regional differences in cell shape and gap junction expression in rat Achilles tendon: relation to fibrocartilage differentiation

J R RALPHS 1 ,, M BENJAMIN 1 , A D WAGGETT 1 , D C RUSSELL 1 , K MESSNER 2 , J GAO 2
PMCID: PMC1467841  PMID: 9827637

Abstract

Tendon cells have complex shapes, with many cell processes and an intimate association with collagen fibre bundles in their extracellular matrix. Where cells and their processes contact one another, they form gap junctions. In the present study, we have examined the distribution of gap junction components in phenotypically different regions of rat Achilles tendon. This tendon contains a prominent enthesial fibrocartilage at its calcaneal attachment and a sesamoid fibrocartilage where it is pressed against the calcaneus just proximal to the attachment. Studies using DiI staining demonstrated typical stellate cell shape in transverse sections of pure tendon, with cells withdrawing their cell processes and rounding up in the fibrocartilaginous zones. Coincident with change in shape, cells stopped expressing the gap junction proteins connexins 32 and 43, with connexin 43 disappearing earlier in the transition than connexin 32. Thus, there are major differences in the ability of cells to communicate with one another in the phenotypically distinct regions of tendon. Individual fibrocartilage cells must sense alterations in the extracellular matrix by cell/matrix interactions, but can only coordinate their behaviour via indirect cytokine and growth factor signalling. The tendon cells have additional possibilities — in addition to the above, they have the potential to communicate direct cytoplasmic signals via gap junctions. The formation of fibrocartilage in tendons occurs because of the presence of compressive as well as tensile forces. It may be that different systems are used to sense and respond to such forces in fibrous and cartilaginous tissues.

Keywords: Connexins, fibrocartilage, tendon, gap junctions

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Selected References

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  1. Benjamin M., Qin S., Ralphs J. R. Fibrocartilage associated with human tendons and their pulleys. J Anat. 1995 Dec;187(Pt 3):625–633. [PMC free article] [PubMed] [Google Scholar]
  2. Birk D. E., Zycband E. Assembly of the tendon extracellular matrix during development. J Anat. 1994 Jun;184(Pt 3):457–463. [PMC free article] [PubMed] [Google Scholar]
  3. D'Andrea P., Vittur F. Gap junctions mediate intercellular calcium signalling in cultured articular chondrocytes. Cell Calcium. 1996 Nov;20(5):389–397. doi: 10.1016/s0143-4160(96)90001-9. [DOI] [PubMed] [Google Scholar]
  4. Dealy C. N., Beyer E. C., Kosher R. A. Expression patterns of mRNAs for the gap junction proteins connexin43 and connexin42 suggest their involvement in chick limb morphogenesis and specification of the arterial vasculature. Dev Dyn. 1994 Feb;199(2):156–167. doi: 10.1002/aja.1001990208. [DOI] [PubMed] [Google Scholar]
  5. Donahue H. J., Guilak F., Vander Molen M. A., McLeod K. J., Rubin C. T., Grande D. A., Brink P. R. Chondrocytes isolated from mature articular cartilage retain the capacity to form functional gap junctions. J Bone Miner Res. 1995 Sep;10(9):1359–1364. doi: 10.1002/jbmr.5650100913. [DOI] [PubMed] [Google Scholar]
  6. Elfgang C., Eckert R., Lichtenberg-Fraté H., Butterweck A., Traub O., Klein R. A., Hülser D. F., Willecke K. Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J Cell Biol. 1995 May;129(3):805–817. doi: 10.1083/jcb.129.3.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gao J., Messner K., Ralphs J. R., Benjamin M. An immunohistochemical study of enthesis development in the medial collateral ligament of the rat knee joint. Anat Embryol (Berl) 1996 Oct;194(4):399–406. doi: 10.1007/BF00198542. [DOI] [PubMed] [Google Scholar]
  8. Goodenough D. A., Paul D. L., Jesaitis L. Topological distribution of two connexin32 antigenic sites in intact and split rodent hepatocyte gap junctions. J Cell Biol. 1988 Nov;107(5):1817–1824. doi: 10.1083/jcb.107.5.1817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Johnson G. D., Davidson R. S., McNamee K. C., Russell G., Goodwin D., Holborow E. J. Fading of immunofluorescence during microscopy: a study of the phenomenon and its remedy. J Immunol Methods. 1982 Dec 17;55(2):231–242. doi: 10.1016/0022-1759(82)90035-7. [DOI] [PubMed] [Google Scholar]
  10. Jones S. J., Gray C., Sakamaki H., Arora M., Boyde A., Gourdie R., Green C. The incidence and size of gap junctions between the bone cells in rat calvaria. Anat Embryol (Berl) 1993 Apr;187(4):343–352. doi: 10.1007/BF00185892. [DOI] [PubMed] [Google Scholar]
  11. Makarenkova H., Becker D. L., Tickle C., Warner A. E. Fibroblast growth factor 4 directs gap junction expression in the mesenchyme of the vertebrate limb Bud. J Cell Biol. 1997 Sep 8;138(5):1125–1137. doi: 10.1083/jcb.138.5.1125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Matyas J. R., Anton M. G., Shrive N. G., Frank C. B. Stress governs tissue phenotype at the femoral insertion of the rabbit MCL. J Biomech. 1995 Feb;28(2):147–157. doi: 10.1016/0021-9290(94)00058-c. [DOI] [PubMed] [Google Scholar]
  13. McNeilly C. M., Banes A. J., Benjamin M., Ralphs J. R. Tendon cells in vivo form a three dimensional network of cell processes linked by gap junctions. J Anat. 1996 Dec;189(Pt 3):593–600. [PMC free article] [PubMed] [Google Scholar]
  14. Meyer R. A., Cohen M. F., Recalde S., Zakany J., Bell S. M., Scott W. J., Jr, Lo C. W. Developmental regulation and asymmetric expression of the gene encoding Cx43 gap junctions in the mouse limb bud. Dev Genet. 1997;21(4):290–300. doi: 10.1002/(SICI)1520-6408(1997)21:4<290::AID-DVG6>3.0.CO;2-2. [DOI] [PubMed] [Google Scholar]
  15. Rufai A., Benjamin M., Ralphs J. R. Development and ageing of phenotypically distinct fibrocartilages associated with the rat Achilles tendon. Anat Embryol (Berl) 1992 Dec;186(6):611–618. doi: 10.1007/BF00186984. [DOI] [PubMed] [Google Scholar]
  16. Rufai A., Ralphs J. R., Benjamin M. Structure and histopathology of the insertional region of the human Achilles tendon. J Orthop Res. 1995 Jul;13(4):585–593. doi: 10.1002/jor.1100130414. [DOI] [PubMed] [Google Scholar]
  17. Veenstra R. D., Wang H. Z., Westphale E. M., Beyer E. C. Multiple connexins confer distinct regulatory and conductance properties of gap junctions in developing heart. Circ Res. 1992 Nov;71(5):1277–1283. doi: 10.1161/01.res.71.5.1277. [DOI] [PubMed] [Google Scholar]
  18. Vogel K. G., Koob T. J. Structural specialization in tendons under compression. Int Rev Cytol. 1989;115:267–293. doi: 10.1016/s0074-7696(08)60632-4. [DOI] [PubMed] [Google Scholar]

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