Skip to main content
PMC home page
Journal of Anatomy logoLink to Journal of Anatomy
. 1997 Feb;190(Pt 2):239–260. doi: 10.1046/j.1469-7580.1997.19020239.x

Stage-specific expression patterns of alkaline phosphatase during development of the first arch skeleton in inbred C57BL/6 mouse embryos

T MIYAKE 1, A M CAMERON 1, B K HALL 1
PMCID: PMC1467603  PMID: 9061447

Abstract

Timing and pattern of expression of alkaline phosphatase was examined during early differentiation of the 1st arch skeleton in inbred C57BL/6 mice. Embryos were recovered between 10 and 18 d of gestation and staged using a detailed staging table of craniofacial development prior to histochemical examination. Expression of alkaline phosphatase is initiated at stage 20.2 in the plasma membrane of mesenchymal cells in the distal region of the first arch. Expression is strongest in osteoid (unmineralised bone matrix) and presumptive periosteum at stage 21.32. Mineralisation begins at stage E23. Expression is present in the mineralised bone matrix. Secondary cartilages form in the condylar and angular processes by stage M24. The cartilaginous cells and surrounding cells in the processes are all alkaline phosphatase-positive and surrounded by the common periosteum, suggesting that progenitor cells of the processes, dentary ramus and secondary cartilages all originate from a common pool. Nonhypertrophied chondrocytes of Meckel's cartilage express alkaline phosphatase at stage M23. Expression in these chondrocytes is preceded by the expression in their adjacent perichondrium. This is true of chondrocytes in all other cranial cartilages examined. 3-D reconstruction of expression in Meckel's cartilage also revealed that the chondrocytes of Meckel's cartilage which express alkaline phosphatase and the matrix of which undergoes mineralisation are those surrounded by the alkaline phosphatase-positive dentary ramus. By stage 25, coincident with mineralisation in the distal section of Meckel's cartilage, most chondrocytes are strongly positive. The perichondria of malleus and incus cartilages express alkaline phosphatase at stage M24. Nonhypertrophied chondrocytes along these perichondria also express alkaline phosphatase. Superficial and deep cells in the dental laminae of incisor and 1st molar teeth become alkaline phosphatase-positive at the bud stage, stages 21.16 and 21.32, respectively. Dental papillae are negative until stage M24 when alkaline phosphatase expression begins in the dental papillae and follicles of the incisor teeth and the dental follicles of the 1st molar teeth. The dental papillae of the 1st molar teeth express alkaline phosphatase at stage 25. Expression in the dental papillae and follicles appears to coincide with cellular differentiation of follicle from papilla. The presumptive squamosal, ectotympanic and gonial membrane bones, lingual oral epithelial cells connected to the dental laminae of the incisor teeth, hair follicle papillae and sheath and surrounding dermis all express alkaline phosphatase in a stage-specific manner.

Keywords: Dentary ramus, articulating processes, Meckel's cartilage, secondary cartilages, hypertrophy, incisor and molar teeth, mineralisation, hair follicles

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Atchley W. R., Hall B. K. A model for development and evolution of complex morphological structures. Biol Rev Camb Philos Soc. 1991 May;66(2):101–157. doi: 10.1111/j.1469-185x.1991.tb01138.x. [DOI] [PubMed] [Google Scholar]
  2. Bitgood M. J., McMahon A. P. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev Biol. 1995 Nov;172(1):126–138. doi: 10.1006/dbio.1995.0010. [DOI] [PubMed] [Google Scholar]
  3. Blake M. S., Johnston K. H., Russell-Jones G. J., Gotschlich E. C. A rapid, sensitive method for detection of alkaline phosphatase-conjugated anti-antibody on Western blots. Anal Biochem. 1984 Jan;136(1):175–179. doi: 10.1016/0003-2697(84)90320-8. [DOI] [PubMed] [Google Scholar]
  4. Bossi M., Hoylaerts M. F., Millán J. L. Modifications in a flexible surface loop modulate the isozyme-specific properties of mammalian alkaline phosphatases. J Biol Chem. 1993 Dec 5;268(34):25409–25416. [PubMed] [Google Scholar]
  5. Bourque W. T., Gross M., Hall B. K. A histological processing technique that preserves the integrity of calcified tissues (bone, enamel), yolky amphibian embryos, and growth factor antigens in skeletal tissue. J Histochem Cytochem. 1993 Sep;41(9):1429–1434. doi: 10.1177/41.9.7689084. [DOI] [PubMed] [Google Scholar]
  6. Bronckers A. L., Gay S., Finkelman R. D., Butler W. T. Developmental appearance of Gla proteins (osteocalcin) and alkaline phosphatase in tooth germs and bones of the rat. Bone Miner. 1987 Aug;2(5):361–373. [PubMed] [Google Scholar]
  7. Böhme K., Winterhalter K. H., Bruckner P. Terminal differentiation of chondrocytes in culture is a spontaneous process and is arrested by transforming growth factor-beta 2 and basic fibroblast growth factor in synergy. Exp Cell Res. 1995 Jan;216(1):191–198. doi: 10.1006/excr.1995.1024. [DOI] [PubMed] [Google Scholar]
  8. Chung K. S., Park H. H., Ting K., Takita H., Apte S. S., Kuboki Y., Nishimura I. Modulated expression of type X collagen in Meckel's cartilage with different developmental fates. Dev Biol. 1995 Aug;170(2):387–396. doi: 10.1006/dbio.1995.1224. [DOI] [PubMed] [Google Scholar]
  9. Dunlop L. L., Hall B. K. Relationships between cellular condensation, preosteoblast formation and epithelial-mesenchymal interactions in initiation of osteogenesis. Int J Dev Biol. 1995 Apr;39(2):357–371. [PubMed] [Google Scholar]
  10. Fang J., Hall B. K. Differential expression of neural cell adhesion molecule (NCAM) during osteogenesis and secondary chondrogenesis in the embryonic chick. Int J Dev Biol. 1995 Jun;39(3):519–528. [PubMed] [Google Scholar]
  11. Granström G., Zellin G., Magnusson B. C., Mångs H. Enzyme histochemical analysis of Meckel's cartilage. J Anat. 1988 Oct;160:101–108. [PMC free article] [PubMed] [Google Scholar]
  12. Hahnel A. C., Rappolee D. A., Millan J. L., Manes T., Ziomek C. A., Theodosiou N. G., Werb Z., Pedersen R. A., Schultz G. A. Two alkaline phosphatase genes are expressed during early development in the mouse embryo. Development. 1990 Oct;110(2):555–564. doi: 10.1242/dev.110.2.555. [DOI] [PubMed] [Google Scholar]
  13. Hall B. K. Distribution of osteo- and chondrogenic neural crest-derived cells and of osteogenically inductive epithelia in mandibular arches of embryonic chicks. J Embryol Exp Morphol. 1982 Apr;68:127–136. [PubMed] [Google Scholar]
  14. Hall B. K., Miyake T. Divide, accumulate, differentiate: cell condensation in skeletal development revisited. Int J Dev Biol. 1995 Dec;39(6):881–893. [PubMed] [Google Scholar]
  15. Hall B. K., Miyake T. The membranous skeleton: the role of cell condensations in vertebrate skeletogenesis. Anat Embryol (Berl) 1992 Jul;186(2):107–124. doi: 10.1007/BF00174948. [DOI] [PubMed] [Google Scholar]
  16. Hall B. K. The role of movement and tissue interactions in the development and growth of bone and secondary cartilage in the clavicle of the embryonic chick. J Embryol Exp Morphol. 1986 Apr;93:133–152. [PubMed] [Google Scholar]
  17. Hall B. K. Tissue interactions and the initiation of osteogenesis and chondrogenesis in the neural crest-derived mandibular skeleton of the embryonic mouse as seen in isolated murine tissues and in recombinations of murine and avian tissues. J Embryol Exp Morphol. 1980 Aug;58:251–264. [PubMed] [Google Scholar]
  18. Hardy M. H. The secret life of the hair follicle. Trends Genet. 1992 Feb;8(2):55–61. doi: 10.1016/0168-9525(92)90350-d. [DOI] [PubMed] [Google Scholar]
  19. Kwong W. H., Tam P. P. The pattern of alkaline phosphatase activity in the developing mouse spinal cord. J Embryol Exp Morphol. 1984 Aug;82:241–251. [PubMed] [Google Scholar]
  20. Livne E., Silbermann M. The mouse mandibular condyle: an investigative model in developmental biology. J Craniofac Genet Dev Biol. 1990;10(1):95–98. [PubMed] [Google Scholar]
  21. MacGregor G. R., Zambrowicz B. P., Soriano P. Tissue non-specific alkaline phosphatase is expressed in both embryonic and extraembryonic lineages during mouse embryogenesis but is not required for migration of primordial germ cells. Development. 1995 May;121(5):1487–1496. doi: 10.1242/dev.121.5.1487. [DOI] [PubMed] [Google Scholar]
  22. MacKenzie A., Ferguson M. W., Sharpe P. T. Expression patterns of the homeobox gene, Hox-8, in the mouse embryo suggest a role in specifying tooth initiation and shape. Development. 1992 Jun;115(2):403–420. doi: 10.1242/dev.115.2.403. [DOI] [PubMed] [Google Scholar]
  23. MacKenzie A., Ferguson M. W., Sharpe P. T. Hox-7 expression during murine craniofacial development. Development. 1991 Oct;113(2):601–611. doi: 10.1242/dev.113.2.601. [DOI] [PubMed] [Google Scholar]
  24. Mackenzie A., Leeming G. L., Jowett A. K., Ferguson M. W., Sharpe P. T. The homeobox gene Hox 7.1 has specific regional and temporal expression patterns during early murine craniofacial embryogenesis, especially tooth development in vivo and in vitro. Development. 1991 Feb;111(2):269–285. doi: 10.1242/dev.111.2.269. [DOI] [PubMed] [Google Scholar]
  25. Manes T., Glade K., Ziomek C. A., Millán J. L. Genomic structure and comparison of mouse tissue-specific alkaline phosphatase genes. Genomics. 1990 Nov;8(3):541–554. doi: 10.1016/0888-7543(90)90042-s. [DOI] [PubMed] [Google Scholar]
  26. Martin K. J., McConkey C. L., Baldassare J. J., Jacob A. K. Effect of triamcinolone on parathyroid hormone-stimulated second messenger systems and phosphate transport in opossum kidney cells. Endocrinology. 1994 Jan;134(1):331–336. doi: 10.1210/endo.134.1.7506208. [DOI] [PubMed] [Google Scholar]
  27. Miyake T., Cameron A. M., Hall B. K. Detailed staging of inbred C57BL/6 mice between Theiler's [1972] stages 18 and 21 (11-13 days of gestation) based on craniofacial development. J Craniofac Genet Dev Biol. 1996 Jan-Mar;16(1):1–31. [PubMed] [Google Scholar]
  28. Miyake T., Cameron A. M., Hall B. K. Stage-specific onset of condensation and matrix deposition for Meckel's and other first arch cartilages in inbred C57BL/6 mice. J Craniofac Genet Dev Biol. 1996 Jan-Mar;16(1):32–47. [PubMed] [Google Scholar]
  29. Morris D. C., Masuhara K., Takaoka K., Ono K., Anderson H. C. Immunolocalization of alkaline phosphatase in osteoblasts and matrix vesicles of human fetal bone. Bone Miner. 1992 Dec;19(3):287–298. doi: 10.1016/0169-6009(92)90877-g. [DOI] [PubMed] [Google Scholar]
  30. Narisawa S., Hasegawa H., Watanabe K., Millán J. L. Stage-specific expression of alkaline phosphatase during neural development in the mouse. Dev Dyn. 1994 Nov;201(3):227–235. doi: 10.1002/aja.1002010306. [DOI] [PubMed] [Google Scholar]
  31. POURTOIS M. [Contribution to the study of tooth buds in the mouse. I. Periods of induction and morphodifferentiation]. Arch Biol (Liege) 1961;72:17–95. [PubMed] [Google Scholar]
  32. RICHANY S. F., BAST T. H., ANSON B. J. The development of the first branchial arch in man and the fate of Meckel's cartilage. Q Bull Northwest Univ Med Sch. 1956;30(4):331–355. [PMC free article] [PubMed] [Google Scholar]
  33. Rockwell J. C., Sorensen A. M., Baran D. T. Na+/H+ exchange and PLA2 activity act interdependently to mediate the rapid effects of 1 alpha, 25-dihydroxyvitamin D3. Steroids. 1993 Oct;58(10):491–494. doi: 10.1016/0039-128x(93)90008-b. [DOI] [PubMed] [Google Scholar]
  34. Rodríguez Vázquez J. F., Mérida Velasco J. R., Jiménez Collado J. A study of the os goniale in man. Acta Anat (Basel) 1991;142(2):188–192. doi: 10.1159/000147188. [DOI] [PubMed] [Google Scholar]
  35. Schmid T. M., Linsenmayer T. F. Developmental acquisition of type X collagen in the embryonic chick tibiotarsus. Dev Biol. 1985 Feb;107(2):373–381. doi: 10.1016/0012-1606(85)90319-7. [DOI] [PubMed] [Google Scholar]
  36. Schmid T. M., Linsenmayer T. F. Immunohistochemical localization of short chain cartilage collagen (type X) in avian tissues. J Cell Biol. 1985 Feb;100(2):598–605. doi: 10.1083/jcb.100.2.598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Studer M., Terao M., Gianni M., Garattini E. Characterization of a second promoter for the mouse liver/bone/kidney-type alkaline phosphatase gene: cell and tissue specific expression. Biochem Biophys Res Commun. 1991 Sep 30;179(3):1352–1360. doi: 10.1016/0006-291x(91)91722-o. [DOI] [PubMed] [Google Scholar]
  38. Tenenbaum H. C., McCulloch C. A., Fair C., Birek C. The regulatory effect of phosphates on bone metabolism in vitro. Cell Tissue Res. 1989 Sep;257(3):555–563. doi: 10.1007/BF00221466. [DOI] [PubMed] [Google Scholar]
  39. Terao M., Studer M., Gianní M., Garattini E. Isolation and characterization of the mouse liver/bone/kidney-type alkaline phosphatase gene. Biochem J. 1990 Jun 15;268(3):641–648. doi: 10.1042/bj2680641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Thesleff I., Jalkanen M., Vainio S., Bernfield M. Cell surface proteoglycan expression correlates with epithelial-mesenchymal interaction during tooth morphogenesis. Dev Biol. 1988 Oct;129(2):565–572. doi: 10.1016/0012-1606(88)90401-0. [DOI] [PubMed] [Google Scholar]
  41. Thesleff I., Partanen A. M., Vainio S. Epithelial-mesenchymal interactions in tooth morphogenesis: the roles of extracellular matrix, growth factors, and cell surface receptors. J Craniofac Genet Dev Biol. 1991 Oct-Dec;11(4):229–237. [PubMed] [Google Scholar]
  42. Vainio S., Jalkanen M., Vaahtokari A., Sahlberg C., Mali M., Bernfield M., Thesleff I. Expression of syndecan gene is induced early, is transient, and correlates with changes in mesenchymal cell proliferation during tooth organogenesis. Dev Biol. 1991 Oct;147(2):322–333. doi: 10.1016/0012-1606(91)90290-j. [DOI] [PubMed] [Google Scholar]
  43. Väkevä L., Mackie E., Kantomaa T., Thesleff I. Comparison of the distribution patterns of tenascin and alkaline phosphatase in developing teeth, cartilage, and bone of rats and mice. Anat Rec. 1990 Sep;228(1):69–76. doi: 10.1002/ar.1092280111. [DOI] [PubMed] [Google Scholar]
  44. Watson L. P., Kang Y. H., Falk M. C. Cytochemical properties of osteoblast cell membrane domains. J Histochem Cytochem. 1989 Aug;37(8):1235–1246. doi: 10.1177/37.8.2526836. [DOI] [PubMed] [Google Scholar]
  45. Yoshiki S., Umeda T., Kurahashi Y. An effective reactivation of alkaline phosphatase in hard tissues completely decalcified for light and electron microscopy. Histochemie. 1972;29(4):296–304. doi: 10.1007/BF00279812. [DOI] [PubMed] [Google Scholar]
  46. Zernik J., Twarog K., Upholt W. B. Regulation of alkaline phosphatase and alpha 2(I) procollagen synthesis during early intramembranous bone formation in the rat mandible. Differentiation. 1990 Sep;44(3):207–215. doi: 10.1111/j.1432-0436.1990.tb00619.x. [DOI] [PubMed] [Google Scholar]
  47. de Bernard B., Bianco P., Bonucci E., Costantini M., Lunazzi G. C., Martinuzzi P., Modricky C., Moro L., Panfili E., Pollesello P. Biochemical and immunohistochemical evidence that in cartilage an alkaline phosphatase is a Ca2+-binding glycoprotein. J Cell Biol. 1986 Oct;103(4):1615–1623. doi: 10.1083/jcb.103.4.1615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. van Genderen C., Okamura R. M., Fariñas I., Quo R. G., Parslow T. G., Bruhn L., Grosschedl R. Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev. 1994 Nov 15;8(22):2691–2703. doi: 10.1101/gad.8.22.2691. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

RESOURCES