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Evolution of chick type I procollagen genes

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Summary

Although the major types of vertebrate collagen have a number of structural properties in common, significant DNA sequence homologies have not been detected between different portions of the helical coding domains within the same gene or between different genes. However, under non-stringent hybridization conditions we found considerable cross-homology within and between α1(I) and α2(I) chick cDNAs in the coding regions for helical sequences. Detailed analyses at the DNA sequence level have led us to propose that the gene for chick pro α2(I) collagen arose from a 9-bp primordial sequence. A consensus sequence for the 9-bp repeat was derived: GGTCCTCCT, which codes for a Gly-Pro-Pro triplet. The primordial ancestor of this 9-bp unit, GGTCCTXCT, apparently underwent duplication and divergence. Each resulting 9-bp sequence was triplicated to form a 27-bp domain, and a condensation event produced a 54-bp domain. This genetic unit then underwent multiple rounds of amplification to form the ancestral gene for the full-length helical section of α2(I). A different 9-bp consensus sequence (GGTCCCCCC) seems to have been the basis of the chick pro α1(I) gene.

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References

  • Alexander F, Young PR, Tilghman SJ (1984) Evolution of the albumin: α-fetoprotein ancestral gene from the amplification of a 27 nucleotide sequence. J Mol Biol 173:159–176

    Article  PubMed  Google Scholar 

  • Baltimore D (1981) Gene conversion: some implication for immunoglobin genes. Cell 24:592–594

    Article  PubMed  Google Scholar 

  • Bentz H, Morris NP, Murray LW, Sakai LY, Hollister D, Burgeson RE (1983) Isolation and partial characterization of a new human collagen with an extended triple-helical structural domain. Proc Natl Acad Sci USA 80:3168–3172

    PubMed  Google Scholar 

  • Bernard MP, Chu M-L, Myers JC, Ramirez F, Eikenberry EF, Prockop D (1983) Nucleotide sequences of cDNAs for the pro α1 chain of human type 1 procollagen. Statistical evaluation of structures which are conserved during evolution. Biochemistry 22:5213–5223

    Article  PubMed  Google Scholar 

  • Bornstein P, Sage H (1980) Structurally distinct collagen types. Annu Rev Biochem 49:957–1003

    Article  PubMed  Google Scholar 

  • Case ST, Summers RL, Jones AG (1983) A variant tandemly repeated nucleotide sequence in Balbiani ring 2 ofChironomus tentans. Cell 33:555–562

    Article  PubMed  Google Scholar 

  • Chu M-L, Williams CJ, Pepe G, Hirsch JL, Prockop DJ, Ramirez F (1983) Internal deletion in a collagen gene in a perinatal lethal form of osteogenesis imperfecta. Nature 304:78–80

    Article  PubMed  Google Scholar 

  • Chu M-L, de Wet W, Bernard M, Ding J-F, Morabito M, Myers J, Williams C, Ramirez F (1984) Human pro α1(I) collagen gene structure reveals evolutionary conservation of a pattern of introns and exons. Nature 310:337–340

    PubMed  Google Scholar 

  • Doering JL, Jelachich ML, Hanlon KM (1982) Identification and genomic organization of human tRNALys genes. FEBS Lett 146:47–51

    Article  PubMed  Google Scholar 

  • Eyre DR (1980) Collagen molecular diversity in the body's protein scaffold. Science 207:1315–1322

    PubMed  Google Scholar 

  • Fienberg SE (1977) The analysis of cross-classified categorial data. MIT Press, Cambridge

    Google Scholar 

  • Fuller F, Boedtker H (1981) Sequence determination and analysis of the 3′ region of chick pro-α1(I) and pro-α2(I) collagen messenger ribonucleic acids including the carboxy-terminal propeptide sequences. Biochemistry 20:996–1006

    Article  PubMed  Google Scholar 

  • Hofmann H, Fietzek PP, Kuhn K (1978) The role of polar and hydrophobic interactions for the molecular packing of type I collagen: a three-dimensional evaluation of the amino acid sequence. J Mol Biol 125:137–165

    Article  PubMed  Google Scholar 

  • Hofmann H, Fietzek PP, Kuhn K (1980) Comparative analysis of the sequences of the three collagen chains α1(I), α2(I), and α1(III). Functional and genetic aspects. J Mol Biol 141:293–314

    Article  PubMed  Google Scholar 

  • Kramer JM, Cox GN, Hirsh D (1982) Comparisons of the complete sequences of two collagen genes inCaenorhabditis elegans. Cell 30:599–606

    Article  PubMed  Google Scholar 

  • Manning RF, Gage LP (1980) Internal structure of the silk fibroin gene ofBombyx mori. II. Remarkable polymorphism of the organization of crystalline and amorphous coding sequences. J Biol Chem 255:9451–9457

    PubMed  Google Scholar 

  • McLachlan AD (1976) Evidence for gene duplication in collagen. J Mol Biol 107:159–174

    PubMed  Google Scholar 

  • Monson JM, McCarthy BJ (1981) Identification of a Balb/c mouse pro α1(I) procollagen gene: evidence for insertions or deletions in gene coding sequences. DNA 1:59–69

    PubMed  Google Scholar 

  • Monson JM, Natzle JE, Friedman J, McCarthy BJ (1982) Expression and novel structure of a collagen gene inDrosophila. Proc Natl Acad Sci USA 79:1761–1765

    PubMed  Google Scholar 

  • Naora H, Deacon NJ (1982) Relationship between the total size of exons and introns in protein-coding genes of higher eukaryotes. Proc Natl Acad Sci USA 79:6196–6200

    PubMed  Google Scholar 

  • Peterson RC, Doering JL, Brown DD (1980) Characterization of twoXenopus somatic 5S DNAs and one minor oocyte-specific 5S DNA. Cell 20:131–141

    Article  PubMed  Google Scholar 

  • Piez KA, Torchia DA (1975) Possible contribution of ionic clustering to molecular packing of collagen. Nature 258:87

    Article  PubMed  Google Scholar 

  • Schmid TM, Conrad HE (1982) A unique low molecular weight collagen secreted by cultured chick embryo chondrocytes. J Biol Chem 257:12444–12450

    PubMed  Google Scholar 

  • Slightom JL, Blechl AE, Smithies O (1980) Human fetal °γ and ^γ and °γ and ^γ globin genes: complete nucleotide sequences suggest that DNA can be exchanged between these duplicated genes. Cell 21:627–638

    Article  PubMed  Google Scholar 

  • Smith GP (1976) Evolution of repeated DNA sequences by unequal crossover. Science 191:528–535

    PubMed  Google Scholar 

  • Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517

    PubMed  Google Scholar 

  • Tate V, Finer H, Boedtker H, Doty P (1983) Procollagen genes: further sequence studies and interspecies comparisons. Cold Spring Harbor Symp Quant Biol 47:1039–1049

    PubMed  Google Scholar 

  • Trus BL, Piez KA (1976) Molecular packing of collagen: three-dimensional analysis of electrostatic interactions. J Mol Biol 108:705–732

    PubMed  Google Scholar 

  • Wozney J, Hanahan D, Tate V, Boedtker H, Doty P (1981) Structure of the pro α2(I) collagen gene. Nature 294:129–135

    PubMed  Google Scholar 

  • Yamada Y, Avvedimento VE, Mudryj M, Ohkubo H, Vogeli G, Irani M, Pastan I, deCrombrugghe B (1980) The collagen gene: evidence of its evolutionary assembly by amplification of a DNA segment containing an exon of 54 bp. Cell 22:887–892

    PubMed  Google Scholar 

  • Yamada Y, Liau G, Mudryj M, Obici S, deCrombrugghe B (1984) Conservation of the sizes for one but not another class of exons in two chick collagen genes. Nature 310:333–337

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Oral Biology, Cancer Center, Northwestern University, 60611, Chicago, Illinois, USA

    Kathy Benveniste-Schrode

  2. Biometry Section, Cancer Center, Northwestern University, 60611, Chicago, Illinois, USA

    Walter W. Hauck

  3. Department of Biology, Loyola University of Chicago, 6525 North Sheridan Road, 60626, Chicago, Illinois, USA

    Jeffrey L. Doering

  4. Abbott Laboratories, 60064, North Chicago, Illinois, USA

    James Schrode

  5. Department of Biological Sciences, Northwestern University, 60201, Evanston, Illinois, USA

    Kari L. Kendra & Bonnie K. Drexler

Authors
  1. Kathy Benveniste-Schrode
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  2. Jeffrey L. Doering
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  3. Walter W. Hauck
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  4. James Schrode
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  5. Kari L. Kendra
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  6. Bonnie K. Drexler
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Benveniste-Schrode, K., Doering, J.L., Hauck, W.W. et al. Evolution of chick type I procollagen genes. J Mol Evol 22, 209–219 (1985). https://doi.org/10.1007/BF02099750

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  • DOI: https://doi.org/10.1007/BF02099750

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