Abstract
The rat tracheal cartilage was shown to calcify during development. The process of calcification was characterized in terms of distribution of alkaline phosphatase (ALP) activity and alterations to immunolocalization of types I and II collagens and glycosaminoglycans of proteoglycans during the development of the tracheal cartilage, in comparison with calcification of the epiphyseal growth plate cartilage. ALP activity was not identified in the tracheal cartilage in the course of calcification, which therefore differed from that in the growth plate. The tracheal cartilage matrix was not resorbed or invaded by type I collagen during calcification. This suggests that no osteogenesis is involved in calcification of the cartilage. Immunoreactivity for type II collagen became weaker in the central region of the tracheal cartilage during development. No net loss of proteoglycans was identified with Alcian blue staining after calcification of the tracheal cartilage. Immunoreactivity for chondroitin 4-sulphate increased in the calcified tracheal cartilage, while reactivity for chondroitin 6-sulphate was weaker in the calcified area than in the surrounding uncalcified region of the tracheal cartilage. The alteration of the extracellular matrices during development may be involved in the calcification of the rat tracheal cartilage.
Similar content being viewed by others
References
Akita H, Kobayashi Y, Kagayama M (1988) A histochemical study on lectin binding in the immature enamel and secretory ameloblasts of rat incisors. Tohoku J Exp Med 155:139–149
Alini M, Matsui Y, Dodge GR, Poole AR (1992) The extracellular matrix of cartilage in the growth plate before and during calcification: Changes in composition and degradation of type II collagen. Calcif Tissue Int 50:327–335
de Bernard B, Bianco P, Bonucci E, Costantini M, Lunazzi GC, Martinuzzi P, Modricky C, Moro L, Panfili E, Pollesello P, Stagni N, Vittur F (1986) Biochemical and immunohistochemical evidence that in cartilage an alkaline phosphatase is a Ca2+-binding glycoprotein. J Cell Biol 103:1615–1623
Blumenthal NC, Posner AS, Silverman LD, Rosenberg LC (1979) Effect of proteoglycans on in vitro hydroxyapatite formation. Calcif Tissue Int 27:75–82
Bonucci E, Cuicchio M, Dearden LC (1974) Investigations of ageing in costal and tracheal cartilage of rats. Z Zellforsch Mikrosk Anat 147:505–527
Buckwalter JA (1983) Proteoglycan structure in calcifying cartilage. Clin Orthop 172:207–232
Caplan AI, Pechak DG (1987) The cellular and molecular embryology of bone formation. Bone and Mineral Res 5:117–183
Carrino DA, Caplan AI (1985) Isolation and characterization of proteoglycans synthesized in ovo by embryonic chick cartilage and new bone. J Biol Chem 260:122–127
Caterson B, Christner JE, Baker JR (1983) Identification of a monoclonal antibody that specifically recognizes corneal and skeletal keratan sulfate. J Biol Chem 258:8848–8854
Chen C, Bosky AL, Rosenberg LC (1984) The inhibitory effect of cartilage proteoglycans on hydroxyapatite growth. Calcif Tissue Int 36:285–290
Couchman JR, Caterson B, Christner JE, Baker JR (1984) Mapping by monoclonal antibody detection of glycosaminoglycans in connective tissues. Nature 307:650–652
Cuervo LA, Pita JC, Howell DS (1973) Inhibition of calcium phosphate mineral growth by proteoglycan aggregate fractions in a synthetic lymph. Calcif Tissue Res 13:1–10
Daugaard S, Strange L, Schiødt T (1991) Immunohistochemical staining for chondroitin sulfate and keratan sulfate. An evaluation of two monoclonal antibodies. Histochemistry 95:585–589
Dziewiatkowski DD, Majznerski LL (1985) Role of proteoglycans in endochondral ossification: inhibition of calcification. Calcif Tissue Int 37:560–564
Harab RC, Mourão PAS (1989) Increase of chondroitin 4-sulfate concentration in the endochondral ossification cartilage of normal dogs. Biochim Biophys Acta 992:237–240
Hargest TE, Gay CV, Schraer H, Wasserman AJ (1985) Vertical distribution of elements in cells and matrix of epiphyseal growth plate cartilage determined by quantitative electron probe analysis. J Histochem Cytochem 33:275–286
Horton WA, Dwyer C, Goering R, Dean DC (1983) Immunohistochemistry of types I and II collagen in undecalcified skeletal tissues. J Histochem Cytochem 31:417–425
Lennette DA (1978) An improved mounting medium for immunofluorescence microscopy. Am J Clin Pathol 69:647–648
Liu C, Sanghvi R, Burnell JM, Howard GA (1987) Simultaneous demonstration of bone alkaline and acid phosphatase activities in plastic-embedded sections and differential inhibition of the activities. Histochemistry 86:559–565
von der Mark K, von der Mark H, Gay S (1976) Study of differential collagen synthesis during development of the chick embryo by immunofluorescence. II. Localization of type I and type II collagen during long bone development. Dev Biol 53:153–170
Matsuzawa T, Anderson HC (1971) Phosphatases of epiphyseal cartilage studied by electron microscopic cytochemical methods. J Histochem Cytochem 19:801–808
Mizoguchi I, Nakamura M, Takahashi I, Kagayama M, Mitani H (1990) An immunohistochemical study of localization of type I and type II collagens in mandibular condylar cartilage compared with tibial growth plate. Histochemistry 93:593–599
Murata H, Yamada K (1985) Effects of contaminating proteinase activities in chondroitinase and keratanase preparations upon the histochemical results obtained by their digestion procedures. Acta Histochem Cytochem 18:59–67
Oike Y, Kimata K, Shinomura T, Suzuki S (1980) Protease activity in chondroitin lyase (chondroitinase) and endo-β-d-galactosidase (keratanase) preparations and a method to abolish their proteolytic effect on proteoglycan. Biochem J 191:203–207
Poole AR, Matsui Y, Hinek A, Lee ER (1989) Cartilage macromolecules and the calcification of cartilage matrix. Anat Rec 224:167–179
Poole AR, Pidoux I, Rosenberg L (1982a) Role of proteoglycans in endochondral ossification: immunofluorescent localization of link protein and proteoglycan monomer in bovine fetal epiphyseal growth plate. J Cell Biol 92:249–260
Poole AR, Reddi AH, Rosenberg LC (1982b) Persistence of cartilage proteoglycan and link protein during matrix-induced endochondral bone development: an immunofluorescent study. Dev Biol 89:532–539
Prince CW, Rahemtulla F, Butler WT (1983) Metabolism in rat bone proteoglycans in vivo. Biochem J 216:589–596
Sasano Y, Mizoguchi I, Kagayama M, Shum L, Bringas P, Slavkin HC (1992) Distribution of type I collagen, type II collagen and PNA binding glycoconjugates during chondrogenesis of three distinct embryonic cartilages. Anat Embryol 186:205–213
Scott JE, Dorling J (1965) Differential staining of acid glycosaminoglycans (mucopolysaccharides) by alcian blue in salt solutions. Histochemie 5:221–233
Scott JH (1953) The cartilage of the nasal septum (a contribution of the study of facial growth). Br Dent J 95:37–43
Scherft JP, Moskalewski S (1984) The amount of proteoglycans in cartilage matrix and the onset of mineralization. Metab Bone Dis Rel Res 5:195–203
Sobue M, Nakashima N, Fukatsu T, Nagasaka T, Katoh T, Ogura T, Takeuchi J (1988) Production and characterization of monoclonal antibody to dermatan sulfate proteoglycan. J Histochem Cytochem 36:479–485
Sobue M, Takeuchi J, Fukatsu T, Nagasaka T, Nakashima N, Ogura T, Katoh T, Yoshida K (1989) Immunohistochemical techniques for detection of dermatan sulfate proteoglycan in tissue sections. Stain Technol 64:43–47
Sorrell JM, Lintala AM, Nahmoodian F, Caterson B (1988) Epitope-specific changes in chondroitin sulfate/dermatan sulfate proteoglycans as markers in the lymphopoietic and granulopoietic compartments of developing bursae of fabricius. J Immunol 140:4263–4270
Takagi M, Maeno M, Kagami A, Takahashi Y, Otsuka K (1991) Biochemical and immunocytochemical characterization of mineral binding proteoglycans in rat bone. J Histochem Cytochem 39:41–50
Thompson SW, Hunt RD (1966) Histochemical procedures: Von Kossa staining for calcium. In: Selected histochemical and histopathological methods. Thomas, Springfield, Ill, pp 581–584
Upholt WB, Olsen BR (1991) The active genes of cartilage. In: Hall B, Newman S (eds) Cartilage: molecular aspects. CRC Press, Boca Raton Ann Arbor Boston London, pp 1–57
Väänänen HK (1980) Immunohistochemical localization of alkaline phosphatase in the chicken epiphyseal growth cartilage. Histochemistry 65:143–148
Väänänen HK, Korhonen LK (1978) Histochemistry of epiphyseal plate. J Cell Mol Biol 23:105–111
Weiss A, Livne E, Bernheim J, Silbermann M (1986) Structural and metabolic changes characterizing the aging of various cartilages in mice. Mech Ageing Dev 35:145–160
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Sasano, Y., Mizoguchi, I., Furusawa, M. et al. The process of calcification during development of the rat tracheal cartilage characterized by distribution of alkaline phosphatase activity and immunolocalization of types I and II collagens and glycosaminoglycans of proteoglycans. Anat Embryol 188, 31–39 (1993). https://doi.org/10.1007/BF00191449
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00191449