Abstract
Epithelially expressed type II collagen is thought to play a prominent role in the embryonic patterning and differentiation of the vertebrate skull, primarily on the basis of data derived from amniotes. We describe the spatiotemporal distribution of type II collagen in the embryonic head of the African clawed frog, Xenopus laevis, using whole-mount and serial-section immunohistochemical analysis. We studied embryos spanning Nieuwkoop and Faber (1967) stages 21–39, a period including cranial neural crest cell migration and ending immediately before the onset of neurocranial chondrogenesis. Xenopus displays a transient expression of type II collagen beginning at least as early as stage 21; staining is most intense and widespread at stages 33/34 and 35/36 and subsequently diminishes. Collagen-positive areas include the ventrolateral surface of the brain, sensory vesicles, notochord, oropharynx, and integument. This expression pattern is similar, but not identical, to that reported for the mouse and two bird species (Japanese quail, domestic fowl); thus epithelially expressed type II collagen appears to be a phylogenetically widespread feature of vertebrate cranial development. Consistent with the proposed role of type II collagen in mediating neurocranial differentiation, most collagen-positive areas lie adjacent to subsequent sites of chondrogenesis in the neurocranium but not the visceral skeleton. However, much of the collagen is expressed after the migration of cranial neural crest, including presumptive chondrogenic crest, seemingly too late to pattern the neurocranium by entrapment of these migrating cells.
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References
Bieker JJ, Yazdani-Buicky M (1992) Distribution of type II collagen mRNA in Xenopus embryos visualized by whole-mount in situ hybridization. J Histochem Cytochem 40:1117–1120
Cheah KSE, Lau ET, Au PKC, Tam PPL (1991) Expression of the mouse α1(II) collagen gene is not restricted to cartilage during development. Development 111:945–953
Chu DTW, Klymkowsky MW (1989) The appearance of acetylated α-tubulin during early development and cellular differentiation in Xenopus. Dev Biol 136:104–117
Croucher S, Tickle C (1989) Characterization of epithelial domains in the nasal passages of chick embryos: spatial and temporal mapping of a range of extracellular matrix and cell surface molecules during development of the nasal placode. Development 106:493–509
Dent J A, Polson A G, Klymkowsky MW (1989) A whole-mount immunocytochemical analysis of the expression of the intermediate filament protein vimentin in Xenopus. Development 105:61–74
Fitch JM, Mentzer A, Mayne R, Linsenmayer TF (1989) Independent deposition of collagen types II and IX at epithelial-mesenchymal interfaces. Development 105:85–95
Hall BK (1983) Tissue interactions and chondrogenesis. In: Hall BK (ed) Cartilage, vol 2. Academic Press, New York, pp 187–222
Hall BK, Hanken J (1985) Foreward. In: deBeer GR (ed) The development of the vertebrate skull. University of Chicago Press, Chicago, pp vii-xxviii
Hall BK, Hörstadius S (1988) The neural crest. Oxford University Press, London
Heath L, Thorogood P (1989) Keratan sulfate expression during craniofacial morphogenesis. Roux Arch Dev Biol 198:103–113
Hunt P, Wilkinson D, Krumlauf R (1991a) Patterning the vertebrate head: murine Hox 2 genes mark distinct subpopulations of premigratory and migrating cranial neural crest. Development 112:43–50
Hunt P, Whiting J, Muchamore I, Marshall H, Krumlauf R (1991b) Homeobox genes and models for patterning the hindbrain and branchial arches. Development [Suppl 1]: 187–196
Klymkowsky MW, Hanken J (1991) Whole-mount staining of Xenopus and other vertebrates. In: Kay BK, Peng HB (eds) Xenopus laevis: practical uses in cell and molecular biology. (Methods in cell biology, vol. 36) Academic Press, New York, pp 410–441
Klymkowsky MW, Maynell LA, Polson AG (1987) Polar asymmetry in the organization of the cortical cytokeratin system of Xenopus laevis oocytes and embryos. Development 100:543–557
Kosher RA, Church RL (1975) Stimulation of in vitro somite chondrogenesis by procollagen and collagen. Nature 258:327–330
Kosher RA, Solursh M (1989) Widespread distribution of type II collagen during embryonic chick development. Dev Biol 131:558–566
Lash JW, Vasan NS (1978) Somite chondrogenesis in vitro. Dev Biol 66:151–171
Linsenmayer TF, Hendrix MJC (1980) Monoclonal antibodies to connective tissue macromolecules: type II collagen. Biochem Biophys Res Commun 92:440–446
Maisey JG (1986) Heads and tails: a chordate phylogeny. Cladistics 2:201–236
Mark K von der, Mollenauer J, Pfaffle M, Van Menxel M, Muller PK (1986) Role of Anchorin CII in the interaction of chondrocytes with extracellular collagen. In: Kuettner K (ed) Articular cartilage biochemistry. Raven Press, New York, pp 125–141
Nah H-D, Upholt WB (1991) Type II collagen mRNA containing an alternatively spliced exon predominates in the chick limb prior to chondrogenesis. J Biol Chem 266:23 446–23 452
Nieto MA, Bradley LC, Hunt P, Das Gupta R, Krumlauf R, Wilkinson DG (1992) Molecular mechanisms of pattern formation in the vertebrate hindbrain. Ciba Found Symp 165:92–107
Nieuwkoop PD, Faber J (1967) Normal Table of Xenopus laevis (Daudin). North-Holland, Amsterdam
Noden DM (1983) The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev Biol 96:144–165
Noden DM (1988) Interactions and fates of avian craniofacial mesenchyme. Development [Suppl]: 121–140
Noden DM (1991) Vertebrate craniofacial development: the relation between ontogenetic process and morphological outcome. Brain Behav Evol 38:190–225
Ryan MC, Sandell, LJ (1990) Differential expression of a cysteine-rich domain in the amino-terminal propeptide of type II (cartilage) procollagen by alternative splicing of mRNA. J Biol Chem 265:10334–10339
Sadaghiani B, Thiébaud CH (1987) Neural crest development in the Xenopus laevis embryo, studied by interspecific transplantation and scanning electron microscopy. Dev Biol 124:91–110
Seufert DW, Hall BK (1990) Tissue interactions involving cranial neural crest in cartilage formation in Xenopus laevis (Daudin). Cell Differ Dev 32:153–165
Su MW, Suzuki HR, Bieker JJ, Solursh M, Ramirez F (1991) Expression of two nonallelic type II procollagen genes during Xenopus laevis embryogenesis is characterized by stage-specific production of alternatively spliced transcripts. J Cell Biol 115:565–575
Thorogood P (1987) Mechanisms of morphogenetic specifications in skull development. In: Wolff JR, Sievers J, Berry M (eds) Mesenchymal-epithelial interactions in neural development. Springer, Berlin Heidelberg New York, pp 141–152
Thorogood P (1988) The developmental specification of the vertebrate skull. Development [Suppl] 104:141–153
Thorogood P, Tickle C (eds) (1988) Craniofacial development. Development [Suppl] 104
Thorogood P, Bee J, Mark K von der (1986) Transient expression of collagen type II at epitheliomesenchymal interfaces during morphogenesis of the cartilaginous neurocranium. Dev Biol 116:497–509
Trueb L, Hanken J (1992) Skeletal development in Xenopus laevis (Anura: Pipidae). J Morphol 214:1–41
Vasan NS (1987) Somite chondrogenesis: the role of the microenvironment. Cell Differ 21:147–159
Wood A, Ashhurst DE, Corbett A, Thorogood P (1991) The transient expression of type II collagen at tissue interfaces during mammalian craniofacial development. Development 111:955–968
Xu Z, Parker SB, Minkoff R (1990) Distribution of type IV collagen, laminin, and fibronectin during maxillary process formation in the chick embryo. Am J Anat 187:232–246
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Seufert, D.W., Hanken, J. & Klymkowsky, M.W. Type II collagen distribution during cranial development in Xenopus laevis . Anat Embryol 189, 81–89 (1994). https://doi.org/10.1007/BF00193131
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DOI: https://doi.org/10.1007/BF00193131