Abstract
The pattern of type II collagen expression during Xenopus laevis embryogenesis has been established after isolating specific cDNA and genomic clones. Evidence is presented suggesting that in X. laevis there are two transcriptionally active copies of the type II procollagen gene. Both genes are activated at the beginning of neurula stage and steady-state mRNA levels progressively increase thereafter. Initially, the transcripts are localized to notochord, somites, and the dorsal region of the lateral plate mesoderm. At later stages of development and parallel to increased mRNA accumulation, collagen expression becomes progressively more confined to chondrogenic regions of the tadpole. During the early period of mRNA accumulation, there is also a transient pattern of expression in localized sites that will later not undergo chondrogenesis, such as the floor plate in the ventral neural tube. At later times and coincident with the appearance of chondrogenic tissues in the developing embryo, expression of the procollagen genes is characterized by the production of an additional, alternatively spliced transcript. The alternatively spliced sequences encode the cysteine-rich globular domain in the NH2-propeptide of the type II procollagen chain. Immunohistochemical analyses with a type II collagen monoclonal antibody documented the deposition of the protein in the extracellular matrix of the developing embryo. Type II collagen expression is therefore temporally regulated by tissue-specific transcription and splicing factors directing the synthesis of distinct molecular forms of the precursor protein in the developing Xenopus embryo.
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- Cheah K. S., Lau E. T., Au P. K., Tam P. P. Expression of the mouse alpha 1(II) collagen gene is not restricted to cartilage during development. Development. 1991 Apr;111(4):945–953. doi: 10.1242/dev.111.4.945. [DOI] [PubMed] [Google Scholar]
- Dent J. A., Polson A. G., Klymkowsky M. W. A whole-mount immunocytochemical analysis of the expression of the intermediate filament protein vimentin in Xenopus. Development. 1989 Jan;105(1):61–74. doi: 10.1242/dev.105.1.61. [DOI] [PubMed] [Google Scholar]
- Fitch J. M., Mentzer A., Mayne R., Linsenmayer T. F. Independent deposition of collagen types II and IX at epithelial-mesenchymal interfaces. Development. 1989 Jan;105(1):85–95. doi: 10.1242/dev.105.1.85. [DOI] [PubMed] [Google Scholar]
- Fleischmajer R., Olsen B. R., Timpl R., Perlish J. S., Lovelace O. Collagen fibril formation during embryogenesis. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3354–3358. doi: 10.1073/pnas.80.11.3354. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fleischmajer R., Timpl R., Tuderman L., Raisher L., Wiestner M., Perlish J. S., Graves P. N. Ultrastructural identification of extension aminopropeptides of type I and III collagens in human skin. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7360–7364. doi: 10.1073/pnas.78.12.7360. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fritz A. F., Cho K. W., Wright C. V., Jegalian B. G., De Robertis E. M. Duplicated homeobox genes in Xenopus. Dev Biol. 1989 Feb;131(2):584–588. doi: 10.1016/s0012-1606(89)80029-6. [DOI] [PubMed] [Google Scholar]
- Green H., Goldberg B., Schwartz M., Brown D. D. The synthesis of collagen during the development of Xenopus laevis. Dev Biol. 1968 Oct;18(4):391–400. doi: 10.1016/0012-1606(68)90048-1. [DOI] [PubMed] [Google Scholar]
- Gurdon J. B. Embryonic induction--molecular prospects. Development. 1987 Mar;99(3):285–306. doi: 10.1242/dev.99.3.285. [DOI] [PubMed] [Google Scholar]
- Hirano S., Fuse S., Sohal G. S. The effect of the floor plate on pattern and polarity in the developing central nervous system. Science. 1991 Jan 18;251(4991):310–313. doi: 10.1126/science.1987648. [DOI] [PubMed] [Google Scholar]
- Jeffreys A. J., Wilson V., Wood D., Simons J. P., Kay R. M., Williams J. G. Linkage of adult alpha- and beta-globin genes in X. laevis and gene duplication by tetraploidization. Cell. 1980 Sep;21(2):555–564. doi: 10.1016/0092-8674(80)90493-6. [DOI] [PubMed] [Google Scholar]
- Kimelman D., Kirschner M. Synergistic induction of mesoderm by FGF and TGF-beta and the identification of an mRNA coding for FGF in the early Xenopus embryo. Cell. 1987 Dec 4;51(5):869–877. doi: 10.1016/0092-8674(87)90110-3. [DOI] [PubMed] [Google Scholar]
- Kintner C. R., Melton D. A. Expression of Xenopus N-CAM RNA in ectoderm is an early response to neural induction. Development. 1987 Mar;99(3):311–325. doi: 10.1242/dev.99.3.311. [DOI] [PubMed] [Google Scholar]
- Kosher R. A., Solursh M. Widespread distribution of type II collagen during embryonic chick development. Dev Biol. 1989 Feb;131(2):558–566. doi: 10.1016/s0012-1606(89)80026-0. [DOI] [PubMed] [Google Scholar]
- LaFlamme S. E., Jamrich M., Richter K., Sargent T. D., Dawid I. B. Xenopus endo B is a keratin preferentially expressed in the embryonic notochord. Genes Dev. 1988 Jul;2(7):853–862. doi: 10.1101/gad.2.7.853. [DOI] [PubMed] [Google Scholar]
- Linsenmayer T. F., Hendrix M. J. Monoclonal antibodies to connective tissue macromolecules: type II collagen. Biochem Biophys Res Commun. 1980 Jan 29;92(2):440–446. doi: 10.1016/0006-291x(80)90352-6. [DOI] [PubMed] [Google Scholar]
- Linsenmayer T. F., Smith G. N., Jr, Hay E. D. Synthesis of two collagen types by embryonic chick corneal epithelium in vitro. Proc Natl Acad Sci U S A. 1977 Jan;74(1):39–43. doi: 10.1073/pnas.74.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Linsenmayer T. F., Trelstad R. L., Gross J. The collagen of chick embryonic notochord. Biochem Biophys Res Commun. 1973 Jul 2;53(1):39–45. doi: 10.1016/0006-291x(73)91397-1. [DOI] [PubMed] [Google Scholar]
- Mohun T. J., Brennan S., Dathan N., Fairman S., Gurdon J. B. Cell type-specific activation of actin genes in the early amphibian embryo. Nature. 1984 Oct 25;311(5988):716–721. doi: 10.1038/311716a0. [DOI] [PubMed] [Google Scholar]
- Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell. 1982 Oct;30(3):675–686. doi: 10.1016/0092-8674(82)90272-0. [DOI] [PubMed] [Google Scholar]
- Newsome D. A., Linsenmayer T. F., Trelstad R. L. Vitreous body collagen. Evidence for a dual origin from the neural retina and hyalocytes. J Cell Biol. 1976 Oct;71(1):59–67. doi: 10.1083/jcb.71.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Otte A. P., Roy D., Siemerink M., Koster C. H., Hochstenbach F., Timmermans A., Durston A. J. Characterization of a maternal type VI collagen in Xenopus embryos suggests a role for collagen in gastrulation. J Cell Biol. 1990 Jul;111(1):271–278. doi: 10.1083/jcb.111.1.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Paglia L. M., Wiestner M., Duchene M., Ouellette L. A., Hörlein D., Martin G. R., Müller P. K. Effects of procollagen peptides on the translation of type II collagen messenger ribonucleic acid and on collagen biosynthesis in chondrocytes. Biochemistry. 1981 Jun 9;20(12):3523–3527. doi: 10.1021/bi00515a034. [DOI] [PubMed] [Google Scholar]
- Ryan M. C., Sandell L. J. 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. 1990 Jun 25;265(18):10334–10339. [PubMed] [Google Scholar]
- Shuldiner A. R., Phillips S., Roberts C. T., Jr, LeRoith D., Roth J. Xenopus laevis contains two nonallelic preproinsulin genes. cDNA cloning and evolutionary perspective. J Biol Chem. 1989 Jun 5;264(16):9428–9432. [PubMed] [Google Scholar]
- Smith J. C. Mesoderm induction and mesoderm-inducing factors in early amphibian development. Development. 1989 Apr;105(4):665–677. doi: 10.1242/dev.105.4.665. [DOI] [PubMed] [Google Scholar]
- Stutz F., Spohr G. Isolation and characterization of sarcomeric actin genes expressed in Xenopus laevis embryos. J Mol Biol. 1986 Feb 5;187(3):349–361. doi: 10.1016/0022-2836(86)90438-9. [DOI] [PubMed] [Google Scholar]
- Su M. W., Lee B., Ramirez F., Machado M., Horton W. Nucleotide sequence of the full length cDNA encoding for human type II procollagen. Nucleic Acids Res. 1989 Nov 25;17(22):9473–9473. doi: 10.1093/nar/17.22.9473. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Su M. W., Suzuki H. R., Solursh M., Ramirez F. Progressively restricted expression of a new homeobox-containing gene during Xenopus laevis embryogenesis. Development. 1991 Apr;111(4):1179–1187. doi: 10.1242/dev.111.4.1179. [DOI] [PubMed] [Google Scholar]
- Swalla B. J., Upholt W. B., Solursh M. Analysis of type II collagen RNA localization in chick wing buds by in situ hybridization. Dev Biol. 1988 Jan;125(1):51–58. doi: 10.1016/0012-1606(88)90057-7. [DOI] [PubMed] [Google Scholar]
- Thorogood P., Bee J., von der Mark K. Transient expression of collagen type II at epitheliomesenchymal interfaces during morphogenesis of the cartilaginous neurocranium. Dev Biol. 1986 Aug;116(2):497–509. doi: 10.1016/0012-1606(86)90150-8. [DOI] [PubMed] [Google Scholar]
- Vuorio E., de Crombrugghe B. The family of collagen genes. Annu Rev Biochem. 1990;59:837–872. doi: 10.1146/annurev.bi.59.070190.004201. [DOI] [PubMed] [Google Scholar]
- Wahli W., Dawid I. B. Isolation of two closely related vitellogenin genes, including their flanking regions, from a Xenopus laevis gene library. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1437–1441. doi: 10.1073/pnas.77.3.1437. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whitman M., Melton D. A. Growth factors in early embryogenesis. Annu Rev Cell Biol. 1989;5:93–117. doi: 10.1146/annurev.cb.05.110189.000521. [DOI] [PubMed] [Google Scholar]
- Wiestner M., Krieg T., Hörlein D., Glanville R. W., Fietzek P., Müller P. K. Inhibiting effect of procollagen peptides on collagen biosynthesis in fibroblast cultures. J Biol Chem. 1979 Aug 10;254(15):7016–7023. [PubMed] [Google Scholar]
- Wu C. H., Donovan C. B., Wu G. Y. Evidence for pretranslational regulation of collagen synthesis by procollagen propeptides. J Biol Chem. 1986 Aug 15;261(23):10482–10484. [PubMed] [Google Scholar]
- Yamada T., Placzek M., Tanaka H., Dodd J., Jessell T. M. Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord. Cell. 1991 Feb 8;64(3):635–647. doi: 10.1016/0092-8674(91)90247-v. [DOI] [PubMed] [Google Scholar]