Abstract
The 25-kDa heat-shock protein (Hsp25) is expressed in the cartilage of the growth plate and suggested to function in chondrocyte differentiation and degeneration. Using immunohistochemistry, we examined the temporal and spatial occurrence of Hsp25 in Meckel's cartilage in embryonic mice mandibles, and in other types of cartilage in both embryonic and adult mice. In adults, Hsp25 immunoreactivity was detected in the hypertrophic chondrocytes located in growth plates of long bones and in non-osteogenic laryngeal and tracheal cartilages. No chondrocytes in the resting or proliferating phase exhibited Hsp25 immunoreactivity. In the embryonic mandibles, resting and proliferating chondrocytes in the anterior and intermediate portions of Meckel's cartilage showed Hsp25 immunoreactivity from the 12th day of gestation (E12) through E15, whereas those in the posterior portion showed little or no immunoreactivity. After E16, the overall Hsp25 immunoreactivity in Meckel's cartilage substantially reduced in intensity, and little or no immunoreactivity was detected in the hypertrophic chondrocytes located in the degenerating portions of Meckel's cartilage. The antisense oligonucleotide for Hsp25 mRNA applied to the culture media of the mandibular explants from E10 embryos caused significant inhibition of the development of the anterior and middle portions of Meckel's cartilage. These results suggested that Hsp25 is essential for the development of Meckel's cartilage and plays different roles in Meckel's cartilage from those in the permanent cartilages and the cartilages undergoing endochondral ossification.
Similar content being viewed by others
Reference
Akisaka T, Suemune S, Nishimori T, Shiba T, Hosoi M, Imanishi I (1980) Distribution pattern of alkaline phosphatase activity in Meckel's cartilage of the mouse embryos. J Hiroshima Univ Dent Soc 12:182–189
Akisaka T (1982) The localization of thiamine pyrophosphatase activity in Meckel's cartilage cells during endochondral ossification. Histochemistry 76:539–546
Amano O, Koshimizu U, Nakamura T, Iseki S (1999) Enhancement by hepatocyte growth factor of bone and cartilage formation during the embryonic mouse mandibular development in vitro. Arch Oral Biol 44:946–953
Amano O, Kudo Y, Shimada M, Wakayama T, Yamamoto M, Iseki S (2001) Transient occurrence of 27 kDa heat-shock protein in the terminal tubule cells during postnatal development of the rat submandibular gland. Anat Rec 264:358–366
Amano O, Yamane A, Shimada M, Koshimizu U, Nakamura T, Iseki S (2002) Hepatocyte growth factor is essential for migration of myogenic cells and promotes their proliferation during the early periods of tongue myogenesis in mouse embryos. Dev Dyn 223:169–179
Arrigo A-P, Preville X (1999) Role oh Hsp27 and related proteins. Handb Exp Pharmacol 136:101–132
Bernick S, Patek PQ (1969) Postnatal development of the rat mandible. J Dent Res 48:1258–1263
Bhaskar SN, Weinmann JP, Schour I (1953) Roles of Meckel's cartilage in the development and growth of the rat mandible. J Dent Res 32:398–410
Bruey JM, Ducasse C, Bonniaud P, Ravagnan L, Susin SA, Diaz-Latoud C, Gurbuxani S, Arrigo AP, Kroemer G, Solary E, Garrido C (2000) Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat Cell Biol 2:645–652
Chai Y, Mah A, Crohin C, Groff S, Bringas P Jr, Le T, Santos V, Slavkin HC (1994) Specific transforming growth factor-β subtypes regulate embryonic mouse Meckel's cartilage and tooth development. Dev Biol 162: 85–103
Crombrugghe BD, Lefebvre V, Nakashima K (2001) Regulatory mechanisms in the pathways of cartilage and bone formation. Cell Biol 13:721–727
Fawcett DW (1986) A Textbook of Histology, 11th edn. Saunders, Philadelphia
Frommer J, Michael R, Margolies MR (1971) Contribution of Meckel's cartilage to ossification of the mandible in mice. J Dent Res 50:1261–l267
Gaestel M, Gross B, Benndorf R, Strauss M, Schunk WH, Kraft R, Otto A, Bohm H, Stahl J, Drabsch H (1989) Molecular cloning, sequencing and expression in Escherichia coli of the 25-kDa growth-related protein of Ehrlich ascites tumor and its homology to mammalian stress proteins. Eur J Biochem 179:209–213
Granstöm G, Zellin G, Magnusson B, Mangs H (1988) Enzyme histochemical analysis of Meckel's cartilage. J Anat 160:101–l08
Haudenschild DR, McPherson JM, Tubo R, Binette F (2001) Differential expression of multiple genes during articular chondrocyte redifferentiation. Anat Rec 263:91–98
Ishizeki K, Takigawa M, Harada Y, Suzuki F, Nawa T (1996a) Meckel's cartilage chondrocytes in organ culture synthesize bone-type proteins accompanying osteocytic phenotype expression. Anat Embryol 193:61–71
Ishizeki K, Takigawa M, Nawa T, Suzuki F (1996b) Mouse Meckel's cartilage chondrocytes evoke bone-like matrix and further transform into osteocyte-like cells in culture. Anat Rec 245:25–35
Ishizeki K, Hiraki Y, Kim H, Suzuki F, Nawa T (1996c) High-density culture of mouse Meckel's cartilage cells stimulates phenotypic conversion to osteocyte-like cells. J Bone Mineral Metab 14:202–213
Ishizeki K, Hiraki Y, Kuno M, Nawa T (1997) Sequential synthesis of cartilage and bone marker proteins during trans-differentiation of mouse Meckel's cartilage chondrocytes in vitro. Int J Dev Biol 41:83–89
Ishizeki K, Nomura S, Takigawa M, Shioji H, Nawa T (1998) Expression of osteopontin in Meckel's cartilage cells during phenotypic transdifferentiation in vitro, as detected by in situ hybridization and immunocytochemical analysis. Histochem Cell Biol 110:457–466
Ishizeki K, Saito H, Shinagawa T, Fujiwara N, Nawa T (1999) Histochemical and immunohistochemical analysis of the mechanism of calcification of Meckel's cartilage during mandible development in rodents. J Anat 194:265–277
Iwamoto M, Shimizu A, Nakashima K, Suzuki F, Kato Y (1991) Reduction in basic fibroblast growth factor receptor is coupled with terminal differentiation of chondrocytes. J Biol Chem 266:461–467
Lavoie JN, Hickey E, Weber LA, Landry J (1993) Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27. J Biol Chem 268:24210–24214
Luo W, Guo C, Zheng J, Chen TL, Wang PY, Vertel BM, Tanzer ML (2000) Aggrecan from start to finish. J Bone Miner Metab 18:5156
Meckel JF (1820) Handbuch der menschlichen Anatomie, Bd. IV. Halle
Mehlen P, Schulze-Osthoff K, Arrigo AP (1996) Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/APO-1- and staurosporine-induced cell death. J Biol Chem 271:16510–16514
Mehlen P, Mehlen A, Godet J, Arrigo AP (1997) Hsp27 as a switch between differentiation and apoptosis in murine embryonic stem cells. J Biol Chem 272:31657–31665.
Melcher AH (1972) Role of chondrocytes and hydrocortisone in resorption of proximal fragment of Meckel's cartilage: an in vitro and in vivo study. Anat Rec 172:21–36
Minina E, Wenzel HM, Kreschel C, Karp S, Gaffield W, McMahon AP, Vortkamp A (2001) BMP and Ihh/PTHrP signaling interact to coordinate chondrocyte proliferation and differentiation. Development 128:4523–4534
Morange M (1999) Heat shock proteins in embryonic development. Handb Exp Pharmacol 136:305–327
Nozawa-Inoue K, Ohshima H, Kawano Y, Yamamoto H, Takagi R, Maeda T (1999) Immunocytochemical demonstration of heat shock protein 25 in the rat temporomandibular joint. Arch Histol Cytol 62:483–491
Otsuka G, Kubo T, Imanishi J, Hirasawa Y (1996) Expression of heat-shock-proteins in the differentiation process of chondrocytes. Arch Jpn Chir 65:39–48
Pacifici M (1994) Tenascin-C and the development of articular cartilage. Matrix Biol 14:689–698
Rugh R (1990) The mouse. Oxford University Press, Oxford
Savostin-Asling I, Asling CW (1973) Resorption of calcified cartilage as seen in Meckel's cartilage of rats. Anat Rec 176:345–359
Shum L, Sakakura Y, Bringas P Jr, Luo W, Snead ML, Mayo ML, Crohin C, Millar S, Werb Z, Buckly S, Hall FL, Warburton D, Slavkin HC (1993) EGF abrogation induced fusilli-form dysmorphogenesis of Meckel's cartilage during embryonic mouse mandibular morphogenesis in vitro. Development 118:903–917
Sohal GS, Ali MM, Dai D (1999) Ventrally emigrating neural tube cells contribute to the formation of Meckel's cartilage and quadrate cartilage. Dev Dyn 216:37–44
Theiler K (1972) The house mouse. Springer, New York
Tiffee JC, Griffin JP, Cooper LF (2000) Immunolocalization of stress proteins and extracellular matrix proteins in the rat tibia. Tissue Cell 32:141–147
Trichilis A, Wroblewski J (1997) Expression of p53 and hsp70 in relation to apoptosis during Meckel's cartilage development in the mouse. Anat Embryol (Berl) 196:107–113
Vanmuylder N, Evrard L, Dourov N (1997) Strong expression of heat shock proteins in growth plate cartilage, an immunohistochemical study of HSP28, HSP70 and HSP110. Anat Embryol (Berl) 195:359–362
Wakayama T, Iseki S (1998) Expression and cellular localization of the mRNA for the 25-kDa heat-shock protein in the mouse. Cell Biol Int 22:295–304
Wakayama T, Iseki S (1999) Specific expression of the mRNA for 25 kDA heat-shock protein in the spermatocytes of mouse seminiferous tubules. Anat Embryol (Berl) 199:419–425
Yamamoto M, Fan L, Wakayama T, Amano O, Iseki S (2001) Constitutive expression of the 27-kDa heat-shock protein in neurons and satellite cells in the peripheral nervous system of the rat. Anat Rec 262:213–220
Zschäbitz A, Weiser H, Stofft E, Krahn V, Gabius HJ, Khaw A, Biesalski HK (1995) Characterization of glycoconjugate expression during development of Meckel's cartilage in the rat. Anat Embryol (Berl) 191:47–59
Zheug J, Luo W, Tanzer ML (1998) Aggrecan synthesis and secretion. J Biol Chem 273:12999–13006
Acknowledgements
We thank Prof. Etsuhide Yamamoto (Department of Oral and Maxillofacial Surgery, Kanazawa University Graduate School of Medical Science) for his helpful suggestions and support of this study. We also acknowledge the assistance of the staff of the Department of Histology and Embryology, Kanazawa University Graduate School of Medical Science. The Ministry of Education, Science, Sports and Culture of Japan awarded a Grant-in-Aid for Scientific Research C (14571745) to O.A.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Shimada, M., Yamamoto, M., Wakayama, T. et al. Different expression of 25-kDa heat-shock protein (Hsp25) in Meckel's cartilage compared with other cartilages in the mouse. Anat Embryol 206, 163–173 (2003). https://doi.org/10.1007/s00429-002-0297-y
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-002-0297-y