Experimental analysis of Msx‐1 and Msx‐2 gene expression during chick mandibular morphogenesis

Homeobox‐containing genes are thought to be involved in regulating pattern formation in a variety of tissues during embryogenesis. We have examined the expression of the homeobox‐related genes Msx‐1 and Msx‐2 during the development of the chick mandibular arch. Northern blot hybridization indicates that transcripts for both Msx‐1 (1.6 Kb) and Msx‐2 (3 Kb) are present in the mandibular arch as early as stage 18. The levels of both transcripts in the whole mandible decrease as cartilage is formed in vivo and in vitro. Using in situ hybridization, transcripts of Msx‐1 were localized in high amounts to the mesenchyme of the mesial tips of the arches. Msx‐2 transcripts were localized in high amounts to medial regions of the arches. Little or no hybridization of either probe was detected in the chondrogenic and myogenic regions of the arches. Transcripts of both genes were also excluded from calcified bone and cartilage. Our results further demonstrate that the mesial tip mesenchyme expressing Msx‐1 includes areas of highly proliferative cells and has in vitro chondrogenic potential. The region of mesenchymal cells expressing the Msx‐2 gene overlap with areas of developmentally programmed cell death which also contain very few proliferative cells and lack chondrogenic potential in vitro. These results are consistent with the possibility that Msx‐1 may be involved in the outgrowth of the mandibular arch and Msx‐2 may be involved in both developmentally programmed cell death and delineating the non‐chondrogenic region of the medial part of the mandibular arch. © 1995 Wiley‐Liss, Inc.

[1]  E. Kollar,et al.  Enhancement of avian mandibular chondrogenesis in vitro in the absence of epithelium. , 1994, Archives of oral biology.

[2]  R. Maas,et al.  Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development , 1994, Nature Genetics.

[3]  S A Newman,et al.  Morphogenetic differences between fore and hind limb precartilage mesenchyme: relation to mechanisms of skeletal pattern formation. , 1994, Developmental biology.

[4]  D. Sassoon,et al.  Msx1 (Hox-7.1) in the adult mouse uterus: cellular interactions underlying regulation of expression. , 1994, Development.

[5]  A. Graham,et al.  Even-numbered rhombomeres control the apoptotic elimination of neural crest cells from odd-numbered rhombomeres in the chick hindbrain. , 1993, Development.

[6]  C. Tickle,et al.  Experimental analysis of the control of expression of the homeobox-gene Msx-1 in the developing limb and face. , 1993, Development.

[7]  R. P. Thompson,et al.  Expression of homeobox genes Msx‐1 (Hox‐7) and Msx‐2 (Hox‐8) during cardiac development in the chick , 1993, Developmental dynamics : an official publication of the American Association of Anatomists.

[8]  R. Kosher,et al.  Ectoderm from various regions of the developing chick limb bud differentially regulates the expression of the chicken homeobox-containing genes GHox-7 and GHox-8 by limb mesenchymal cells. , 1993, Developmental biology.

[9]  M. Ferguson,et al.  Epithelial-mesenchymal interactions are required for msx 1 and msx 2 gene expression in the developing murine molar tooth. , 1993, Development.

[10]  N M Le Douarin,et al.  The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. , 1993, Development.

[11]  K. Song,et al.  Expression of Hox-7.1 in myoblasts inhibits terminal differentiation and induces cell transformation , 1992, Nature.

[12]  C. Tickle,et al.  Epithelial-mesenchymal interactions in the outgrowth of limb buds and facial primordia in chick embryos. , 1992, Developmental biology.

[13]  G. Lyons,et al.  Apical ridge dependent and independent mesodermal domains of GHox-7 and GHox-8 expression in chick limb buds. , 1992, Development.

[14]  G. Lyons,et al.  Multiple sites of HOX‐7 expression during mouse embryogenesis: Comparison with retinoic acid receptor mRNA localization , 1992, Molecular reproduction and development.

[15]  M. Ferguson,et al.  Expression patterns of the homeobox gene, Hox-8, in the mouse embryo suggest a role in specifying tooth initiation and shape. , 1992, Development.

[16]  J. Fallon,et al.  Talpid2 limb bud mesoderm does not express GHox‐8 and has an altered expression pattern of GHox‐7 , 1992, Developmental dynamics : an official publication of the American Association of Anatomists.

[17]  L. Sumoy,et al.  GHox-7: a chicken homeobox-containing gene expressed in a fashion consistent with a role in patterning events during embryonic chick limb development. , 1992, Differentiation; research in biological diversity.

[18]  T. Saito,et al.  Differential expression of two msh-related homeobox genes Chox-7 and Chox-8 during chick limb development. , 1992, Biochemical and biophysical research communications.

[19]  J. Fallon,et al.  Altered expression of the chicken homeobox-containing genes GHox-7 and GHox-8 in the limb buds of limbless mutant chick embryos. , 1991, Development.

[20]  A. Graham,et al.  Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. , 1991, Development.

[21]  G. Lyons,et al.  The apical ectodermal ridge regulates Hox-7 and Hox-8 gene expression in developing chick limb buds. , 1991, Genes & development.

[22]  E. Vitale,et al.  Repeating developmental expression of G-Hox 7, a novel homeobox-containing gene in the chicken. , 1991, Developmental biology.

[23]  A. Kuroiwa,et al.  Chicken homeobox gene Msx-1: structure, expression in limb buds and effect of retinoic acid. , 1991, Development.

[24]  J. Fallon,et al.  Talpid2 mutant chick limb has anteroposterior polarity and altered patterns of programmed cell death , 1991, The Anatomical record.

[25]  E. Kollar,et al.  Temporal and spatial expression of genes for cartilage extracellular matrix proteins during avian mandibular arch development. , 1991, Differentiation; research in biological diversity.

[26]  E. Kollar,et al.  Stage-related chondrogenic potential of avian mandibular ectomesenchymal cells. , 1991, Differentiation; research in biological diversity.

[27]  N. L. Le Douarin,et al.  Epithelio‐‐mesenchymal interactions are critical for Quox 7 expression and membrane bone differentiation in the neural crest derived mandibular mesenchyme. , 1991, The EMBO journal.

[28]  R. Baldock,et al.  The Msh-like homeobox genes define domains in the developing vertebrate eye. , 1991, Development.

[29]  D. Davidson,et al.  Expression of the chicken homeobox-containing gene GHox-8 during embryonic chick limb development , 1991, Mechanisms of Development.

[30]  P. Holland,et al.  Cloning and evolutionary analysis of msh-like homeobox genes from mouse, zebrafish and ascidian. , 1991, Gene.

[31]  M. Ferguson,et al.  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. , 1991, Development.

[32]  B. Hall,et al.  DEVELOPMENT AND EVOLUTIONARY ORIGINS OF VERTEBRATE SKELETOGENIC AND ODONTOGENIC TISSUES , 1990, Biological reviews of the Cambridge Philosophical Society.

[33]  W. J. Hume,et al.  Immunohistological optimization of detection of bromodeoxyuridine-labeled cells in decalcified tissue. , 1990, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[34]  C. Tickle,et al.  Epithelia are interchangeable between facial primordia of chick embryos and morphogenesis is controlled by the mesenchyme. , 1989, Developmental biology.

[35]  B. Hall,et al.  Chondrogenesis of mandibular mesenchyme from the embryonic chick is inhibited by mandibular epithelium and by epidermal growth factor. , 1989, The International journal of developmental biology.

[36]  B. Jacq,et al.  Hox‐7, a mouse homeobox gene with a novel pattern of expression during embryogenesis. , 1989, The EMBO journal.

[37]  D. Noden.  Interactions and fates of avian craniofacial mesenchyme. , 1988, Development.

[38]  M. Koike,et al.  Effects of fixation time and enzymatic digestion on immunohistochemical demonstration of bromodeoxyuridine in formalin-fixed, paraffin-embedded tissue. , 1988, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[39]  P. Chomczyński,et al.  Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. , 1987, Analytical biochemistry.

[40]  S. Wedden.  Epithelial-mesenchymal interactions in the development of chick facial primordia and the target of retinoid action. , 1987, Development.

[41]  M. Solursh,et al.  Ectoderm as a determinant of early tissue pattern in the limb bud. , 1984, Cell differentiation.

[42]  R. Kosher,et al.  Uniform cartilage differentiation in micromass cultures prepared from a relatively homogeneous population of chondrogenic progenitor cells of the chick limb bud: effect of prostaglandins. , 1984, The Journal of experimental zoology.

[43]  A. Feinberg,et al.  A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. , 1983, Analytical biochemistry.

[44]  R. Kosher,et al.  In vitro studies on the morphogenesis and differentiation of the mesoderm subjacent to the apical ectodermal ridge of the embryonic chick limb-bud. , 1979, Journal of embryology and experimental morphology.

[45]  B. Hall,et al.  Epithelial influences on skeletogenesis in the mandible of the embryonic chick , 1977, The Anatomical record.

[46]  V. Hamburger,et al.  A series of normal stages in the development of the chick embryo , 1951, Journal of morphology.

[47]  W. Jacobson,et al.  Memoirs: The Developmental Mechanics and Potencies of the Undifferentiated Mesenchyme of the Mandible , 1941 .

[48]  R. Kosher,et al.  The expression pattern of the chicken homeobox-containing gene GHox-7 in developing polydactylous limb buds suggests its involvement in apical ectodermal ridge-directed outgrowth of limb mesoderm and in programmed cell death. , 1993, Differentiation; research in biological diversity.

[49]  Hiroaki Suzuki,et al.  Erratum: Repeating Developmental Expression of G-Hox 7, a novel homeobox- containing gene in the chicken (Developmental Biology (1991) 148 (375-388)) , 1992 .

[50]  D. Wilkinson.  Wholemount in situ hybridization of vertebrate embryos , 1992 .

[51]  E. Vitale,et al.  Repeating developmental expression of G-Hox 7, a novel homeobox-containing gene in the chicken. , 1992, Developmental biology.

[52]  B. Hall,et al.  Reciprocal interactions between epithelium, mesenchyme, and epidermal growth factor (EGF) in the regulation of mandibular mitotic activity in the embryonic chick. , 1990, Journal of craniofacial genetics and developmental biology.

[53]  M. Justice,et al.  A new family of mouse homeo box-containing genes: molecular structure, chromosomal location, and developmental expression of Hox-7.1. , 1989, Genes & development.

[54]  C. Tickle,et al.  The patterns on chondrogenesis of cells from facial primordia of chick embryos in micromass culture. , 1986, Developmental biology.

[55]  A GLUCKSMANN,et al.  Cell deaths in normal vertebrate ontogeny. , 1951, Biological reviews of the Cambridge Philosophical Society.

[56]  J. W. Saunders.  The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm. , 1948, The Journal of experimental zoology.