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Expression of the HB9 Homeobox Gene Concomitant with Proliferation Accompanying Epidermal Stratification During Development of Chick Embryonic Tarsometatarsal Skin

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Abstract

A homeobox gene, HB9, has been isolated from the tarsometatarsal skin of 13-day-old chick embryos using a degenerate RT-PCR-based screening method. In situ hybridization analysis revealed that, during development of chick embryonic skin, the HB9 gene was expressed in epidermal basal cells of the placodes, but not in those of interplacodes, and in the dermal cells under the placodes at 9 days before addition of an intermediate layer by proliferation of the basal cells in the placodes. With the onset of epidermal stratification, the direction of the basal cell mitosis changed, with the axis becoming vertical to the epidermal surface. Placodes and interplacodes form outer and inner scales, respectively, after they have elongated distally (Tanaka S, Kato Y (1983b) J Exp Zool 225: 271–283). During scale ridge elongation at 12–15 days, HB9 was strongly expressed in the epidermis of the outer scale face, where the cell proliferation is more active than in the epidermis of the inner scale face; hence, stratification of the outer scale face is more prominent than that of the inner scale face. After 16 days, when mitotic activity in the epidermal basal cells decreases and the thickness of the epidermis is maintained at a constant level, the HB9 expression decreases with the onset of epidermal keratinization. These results suggest that HB9 may be involved in the proliferation of the epidermal basal cells that accompanies epidermal stratification.

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References cited

  • Altaba AR (1997) Catching a glimpse of hedgehog. Cell 90: 193–196.

    Google Scholar 

  • Amo FFD, Smith DE, Swiatek PJ, Gendron-Maguire M, Greenspan RJ, McMahon AP, Gridley T (1992) Expression pattern of Motch, a mouse homolog of Drosophila Notch, suggests an important role in early postimplantation mouse development. Development 115: 737–744.

    Google Scholar 

  • Beckingham-Smith KB (1973) The proteins of the embryonic chick epidermis. I. During the normal development in ovo. Dev Biol 30: 249–262.

    Google Scholar 

  • Brown WM, Stenn KS (1993) Homeobox genes and the patterning of skin diseases. J Cutan Pathol 20: 289–293.

    Google Scholar 

  • Chuong CM (1993) The making of a feather: homeoproteins, retinoids and adhesion molecules. Bioessays 15: 513–521.

    Google Scholar 

  • Crowe R, Niswander L (1998) Disruption of scale development by Delta-1 misexpression. Dev Biol 195: 70–74.

    Google Scholar 

  • Davidson D (1995) The function and evolution of Msx genes: pointers and paradoxes. Trends Genet 11: 405–411.

    Google Scholar 

  • Detmer K, Lawrence HJ, Largman C (1993) Expression of class I homeobox genes in fetal and adult murine skin. J Invest Dermatol 101: 517–522.

    Google Scholar 

  • Faus I, Hsu HJ, Fuchs E (1994) Oct-6: a regulator of keratinocyte gene expression in stratified squamous epithelia. Mol Cell Biol 14: 3263–3275.

    Google Scholar 

  • Gehring WJ, Qian YQ, Billeter M, Furukubo-Tokunaga K, Schier AF, Resendez-Perez D, Affolter M, Otting G, Wüthrich K (1994) Homeodomain-DNA recognition. Cell 78: 211–223.

    Google Scholar 

  • Hamburger V, Hamilton H (1951) A series of normal stages in the development of the chick embryo. J Morphol 88: 49–92.

    Google Scholar 

  • Harrison KA, Druey KM, Deguchi Y, Tuscano JM, Kehrl JH (1994) A novel human homeobox gene distantly related to proboscipedia is expressed in lymphoid and pancreatic tissues. J Biol Chem 269: 19968–19975.

    Google Scholar 

  • Kanzler B, Prin F, Thelu J, Dhouailly D (1997) CHOXC-8 and CHOXD-13 expression in embryonic chick skin and cutaneous appendage specification. Dev Dyn 210: 274–287.

    Google Scholar 

  • Kawabata M, Imamura T, Miyazono K (1998) Signal transduction by bone morphogenetic proteins. Cyto Growth Fact Rev 9: 49–61.

    Google Scholar 

  • Krumlauf R (1994) Hox genes in vertebrate development. Cell 78: 191–201.

    Google Scholar 

  • Mathews CE, Detmer K, Lawrence HJ, Largman C (1993) Expression of the hox2.2 homeobox gene in murine embryonic epidermis. Differentiation 52: 177–184.

    Google Scholar 

  • McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68: 283–302.

    Google Scholar 

  • Najfeld V, Menninger J, Ballard SG, Deguchi Y, Ward DC, Kehrl JH (1992) Two diverged human homeobox genes involved in the differentiation of human hematopoietic progenitors map to chromosome I, band q41–42.1. Genes Chrom Cancer 5: 343–347.

    Google Scholar 

  • Noveen A, Jiang TX, Ting-Berreth SA, Choung CM (1995) Homeobox genes Msx-1 and Msx-2 are associated with induction and growth of skin appendages. J Invest Dermatol 104: 711–719.

    Google Scholar 

  • Rothberg S, Ekel TM (1967) Mitotic activity in the chick embryo epidermis. Nature 216: 1352.

    Google Scholar 

  • Saha MS, Miles RR, Grainger RM (1997) Dorsal-ventral patterning during neural induction in Xenopus: assessment of spinal cord regionalization with xHB9, a marker for the motor neuron region. Dev Biol 187: 209–223.

    Google Scholar 

  • Sawyer RH (1972a) Avian scale development. I. Histogenesis and morphogenesis of the epidermis and dermis during formation of the scale ridge. J Exp Zool 181: 365–384.

    Google Scholar 

  • Sawyer RH (1972b) Avian scale development. II. A study of cell proliferation. J Exp Zool 181: 385–408.

    Google Scholar 

  • Scott GA, Goldsmith LA (1993) Homeobox genes and skin development: a review. J Invest Dermatol 101: 3–8.

    Google Scholar 

  • Smart IHM (1970) Variation in the plane of cell cleavage during the process of stratification in the mouse epidermis. Br J Derm 82: 276–282.

    Google Scholar 

  • Stelnicki EJ, Kömüves LG, Kwong AO, Holmes D, Klein P, Rozenfeld S, Lawrence HJ, Adzick NS, Harrison M, Largman C (1998) Hox homeobox genes exhibit spatial and temporal changes in expression during human skin development. J Invest Dermatol 110: 110–115.

    Google Scholar 

  • Tanabe Y, William C, Jessell TM (1998) Specification of motor neuron identity by the MNR2 homeodomain protein. Cell 95: 67–80.

    Google Scholar 

  • Tanaka S, Kato Y (1983a) Epigenesis in developing avian scales. I. Qualitative and quantitative characterization of finite cell populations. J Exp Zool 225: 257–269.

    Google Scholar 

  • Tanaka S, Kato Y (1983b) Epigenesis in developing avian scales. II. Cell proliferation in relation to morphogenesis and differentiation in the epidermis. J Exp Zool 225: 271–283.

    Google Scholar 

  • Thélu J, Viallet JP, Dhouailly D (1998) Differential expression pattern of the three Fringe genes is associated with epidermal differentiation. J Invest Dermatol 111: 903–906.

    Google Scholar 

  • Vollmer JY, Clerc RG (1998) Homeobox genes in the developing mouse brain. J Neurochem 71: 1–19.

    Google Scholar 

  • Wessells NK (1961) An analysis of chick epidermis differentiation in situ and in vitro in chemically defined media. Dev Biol 3: 355–389.

    Google Scholar 

  • Zeltinger J, Sawyer RH (1991) Avian scale development. XIII. Epidermal germinative cells are committed to appendage-specific differentiation and respond to patterned cues in the dermis. Dev Biol 144: 335–352.

    Google Scholar 

  • Zeltinger J, Sawyer RH (1992) Avian scale development. XVI. Epidermal commitment to terminal differentiation is prior to definitive scale ridge formation. Dev Biol 149: 55–65.

    Google Scholar 

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Kosaka, Y., Akimoto, Y., Omoto, Y. et al. Expression of the HB9 Homeobox Gene Concomitant with Proliferation Accompanying Epidermal Stratification During Development of Chick Embryonic Tarsometatarsal Skin. Histochem J 32, 275–280 (2000). https://doi.org/10.1023/A:1004032828098

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