The Histochemical Journal

, Volume 31, Issue 12, pp 761–770

Stromelysin-1 (MMP-3) in Forming Enamel and Predentine in Rat Incisor – Coordinated Distribution with Proteoglycans Suggests a Functional Role

  • Rachel Hall
  • Dominique Septier
  • Graham Embery
  • Michel Goldberg
Article

Abstract

Stromelysin-1 (matrix metalloproteinase-3) or proteoglycanase was visualized by light and electron microscopy immunolabelling in the forming zone of rat incisors. In predentine, labelling was more dense at the transition zone between the inner proximal third and the two outer thirds. Odontoblast processes were also positively stained, mostly in predentine and to a lesser degree in dentine. The dentine–enamel junction was intensely labelled, whereas dentine and forming enamel were only faintly stained. Gold–antibodies complexes were seen inside secretory ameloblasts and odontoblasts in cytosolic locations. The distribution of stromelysin-1 was compared with the distribution of 2-B-6 epitope, an antibody recognizing chondroitin-4-sulphate/dermatan sulphate and which showed a decreasing gradient from the proximal zone to the distal part of predentine. In contrast, both 5-D-4, an anti-keratan sulphate antibody and an anti-lumican antibody displayed a reversed distribution, with an increase seen from the proximal and central thirds to the distal part of predentine. This coordinated distribution suggests that stromelysin-1 may have a functional role, being implicated in predentine in the degradation of chondroitin-4-sulphate/dermatan sulphate-containing proteoglycans, and consequently allowing keratan sulphate proteoglycan concentration to increase near the border where mineralization is initiated.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References cited

  1. Ababneh KT, Hall RC, Embery G (1998) Immunolocalization of glycosaminoglycans in ageing, healthy and periodontally diseased human cementum. Arch Oral Biol 43: 235-246.Google Scholar
  2. Baumeister W, Lupas A (1997) The proteasome. Curr Opinion Cell Biol 7: 273-278.Google Scholar
  3. Birkedal-Hansen H (1995) Proteolytic remodeling of extracellular matrix. Curr Opinion Cell Biol 7: 728-735.Google Scholar
  4. Carter J, Smilie AC, Shepherd MG (1989) Purification and properties of a protease from developing procine dental enamel. Arch Oral Biol 34: 195-202.Google Scholar
  5. Chardin H, Londono I, Goldberg M (1990) Visualization of glycosaminoglycans in rat incisor extracellular matrix using a hyaluronidase-gold complex. Histochem J 22: 588-594.Google Scholar
  6. Cheng H, Caterson B, Neame PJ, Lester GE, Yamauchi M (1996) Differential distribution of lumican and fibromodulin in tooth cementum. Connect Tissue Res 34: 87-96.Google Scholar
  7. Chin JR, Murphy G, Werb Z (1985) Stromelysin, a connective tissuedegrading metalloproteinase secreted by stimulated rabbit synovial fibroblasts in parallel with collagenase. Biosynthesis, isolation, characterization, and substrates. J Biol Chem 260: 12367-12376.Google Scholar
  8. Crenshaw MA, Bawden JW (1984) Proteolytic activity in embryonic bovine secretory enamel. In Fearnhead RW, ed. Tooth Enamel IV Amsterdam: Elsevier Sciences Publishers BV, pp. 109-113.Google Scholar
  9. Dean DD, Schwartz Z, Bonewald L, Muniz OE, Morales S, Gomez R, Brooks BP, Qiao M, Howell DS, Boyan BD (1994) Matrix vesicles produced by osteoblast-like cells in culture become significantly enriched in proteoglycan-degrading metalloproteinases after addition of β-glycerophosphate and ascorbic acid. Calcif Tissue Int 54: 399-408.Google Scholar
  10. Denbesten PK, Heffernan LM (1989) Separation by polyacrylamide gel electrophoresis of multiple proteases in rat and bovine enamel. Arch Oral Biol 34: 399-404.Google Scholar
  11. Denbesten PK, Awbrey BJ, Treadwell BV (1989) Similarities between a proteinase in secretory enamel matrix and a neutral proteinase found in cartilage. In Fearnhead RW ed. Tooth Enamel V. Yokohama, Florence publishers, pp. 278-282.Google Scholar
  12. Docherty AJP, Murphy G (1990) The tissue metalloproteinase family and the inhibitor TIMP: a study using cDNAs and recombinant proteins. Ann Rheumat Diseases 49: 469-479.Google Scholar
  13. Fukae M, Kaneko T, Tanabe T, Shimizu M (1991) Metalloproteinases in the mineralized compartments of procine dentine as detected by substrate-gel electrophoresis. Arch Oral Biol 36: 567-573.Google Scholar
  14. Fukae M, Tanabe T, Yamada M (1994) Action of metalloproteinases on procine dentin mineralization. Calcif Tissue Res 55: 426-435.Google Scholar
  15. Goldberg M, Boskey AL (1996) Lipids and biomineralizations. Progr Histochem Cytochem 31/2, pp. 1-189. Stuttgart: Gustav FischerGoogle Scholar
  16. Goldberg M, Escaig F (1985) Incorporation of (35S)sulfate and (3H)glucosamine into glycosaminoglycans in rat incisor predentin and dentin: comparizon by radioautography of fixation by rapid freezing, freeze substitution, and aldehyde fixation. Calcif Tissue Int 37: 511-518.Google Scholar
  17. Goldberg M, Septier D (1985) Improved lipid preservation by malachite green-glutaraldehyde fixation in rat predentine and dentine. Arch Oral Biol 30: 717-726.Google Scholar
  18. Goldberg M, Septier D (1996) A comparative study of the transition between predentin and dentin, using various preparative procedures in the rat. Eur J Oral Sci 104: 269-277.Google Scholar
  19. Goldberg M, Septier D, Escaig-Haye F (1987) Glycoconjugates in dentinogenesis and dentine. Progr Histochem Cytochem 17/2 pp. 1-113 Stuttgart, Fischer Verlag.Google Scholar
  20. Goldberg M, Septier D, Torres-Quintana MA, Lécolle S, Hall R, Gafni G, Menashi S, Embery G (1999) New insights on the dynamics of dentin formation. In Goldberg M, Robinson C, Boskey A eds. Proceedings of the 6th International Conference on the Chemistry and Biology of Mineralized Tissues. Am Acad Orthop Surgeons (in press).Google Scholar
  21. Hall RC, Llyod D, Embery G (1998) The immunolocalisation of lumican in human predentine. Arch Oral Biol 42: 783-786.Google Scholar
  22. Iozzo RV (1998) Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67: 609-652.Google Scholar
  23. Kinne RW, Fisher LW (1987) Keratan sulfate proteoglycan in rabbit compact bone is bone sialoprotein II. J Biol Chem 262: 10206-10211.Google Scholar
  24. Kresse H, Hausser H, Schönherr E, (1993) Small proteoglycans. Experientia 49: 403-416.Google Scholar
  25. Lormée Ph, Septier D, Lécolle S, Baudouin C, Goldberg M (1996) Dual incorporation of (35S) sulfate proteoglycans acting as mineralization promotors in rat molars and predentin proteoglycans. Calcif Tissue Int 58: 368-375.Google Scholar
  26. MacDougall M, Simmons D, Zianghong L, Nydegger J, Feng J Gu, TT (1997). Dentin phosphoprotein and dentin sialoprotein are cleavage products expressed from a single transcript coded by a gene on human chromosome 4. J Biol Chem 272: 835-842.Google Scholar
  27. Maeno M, Taguchi M, Kosuge K, Otsuka K, Takagi M (1992) Nature and distribution of mineral-binding, keratan sulfate-containing glycoconjugatees in rat and rabbit bone. J Histochem Cytochem 40: 1779-1788.Google Scholar
  28. Nagase H (1997) Activation mechanisms of matrix metalloproteinases. Biol Chem 378: 151-160.Google Scholar
  29. Nagase H, Fields CG, Fields GB (1994) Design and characterization of a fluorogenic substrate selectively hydrolyzed by stromelysis 1 (matrix metalloproteinase-3). J Chem Biol 269: 20952-20957.Google Scholar
  30. Okada Y, Nagase H, Harris ED (1986) A metalloproteinase from human rheumatoid synovial fibroblasts that digests connective tissue matrix components. Purification and characterization. J Biol Chem 261: 14245-14255.Google Scholar
  31. Pentik¨ainen MO, ö örni K, Lassila R Kovanan PT (1997) The proteoglycan decorin links low density lipoproteins with collagen type I. J Biol Chem 272: 7633-7638.Google Scholar
  32. Rada JA, Cornuet PK, Hassell JR (1993) Regulation of corneal collagen fibrillogenesis in vitro by corneal proteoglycan (lumican and decorin) core proteins. Exp Eye Res 56: 635-648.Google Scholar
  33. Robinson C, Brookes SJ, Shore RC, Kirkham J (1998) The developing enamel matrix: nature and function. Eur J Oral Sci 106: (Suppl. 1) 282-291.Google Scholar
  34. Scott JE (1994) On the polylactose nature of chondroitin and keratan sulphates. Biochem J 298: 221-222.Google Scholar
  35. Scott JE (1996) Proteodermatan and proteokeratan sulfate (decorin, lumican/ fibromodulin) proteins are horseshoe shaped. Implications for their interactions with collagen. Biochemistry 35: 8795-8799.Google Scholar
  36. Septier D, Hall RC, Lloyd D, Embery G Goldberg M (1998) Quantitative immunohistochemical evidence of a functional gradient of chondroitin 4-sulphate/dermatan sulphate, developmentally regulated in the predentine of rat incisor. Histochemical J 30: 275-284.Google Scholar
  37. Sini P, Denti A, Tira E, Balduini C (1997) Role of decorin on the in vitro fibrillogenesis of type I collagen. Glycoconjugate J 14: 871-874.Google Scholar
  38. Steinfort J, van de Stadt R Beertsen W (1994) Identification of new rat dentin proteoglycans using C18 chromatography. J Biol Chem 269: 22397-22404.Google Scholar
  39. Takagi M, Hishikawa H, Hosokawa Y, Kagami A Rahemtulla F (1990) Immunohistochemical localization of glycosaminoglycans and proteoglycans in predentin and dentin of rat incisors J Histochem Cytochem 38: 319-324.Google Scholar
  40. Torres-Quintana MA, Septier D, Goldberg M (1999) Differences in the pattern of lanthanum diffusion into predentine and dentine in mouse incisors and molars. Arch Oral Biol 44: 351-360.Google Scholar
  41. Werb Z (1992) The role of metalloproteinases and their inhibitors in matrix remodeling in mineralized tissue. In Slavkin H, Price P, eds. Chemistry and Biology of Mineralized Tissues Amsterdam: Elsevier Science Publishers BV, pp. 321-327.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Rachel Hall
    • 1
  • Dominique Septier
    • 2
  • Graham Embery
    • 1
  • Michel Goldberg
    • 2
  1. 1.Basic Dental Science, Dental SchoolUniversity of Wales College of MedicineCardiffUK
  2. 2.Laboratoire de Biologie et Physiopathologie Cranio-faciales – EA 2496, Groupe Matrices Extracellulaires et Biominéralisations, Faculté de Chirurgie DentaireUniversitéMontrougeFrance

Personalised recommendations