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. 1985 Dec;5(12):3497–3506. doi: 10.1128/mcb.5.12.3497

Genetic engineering in the Precambrian: structure of the chicken triosephosphate isomerase gene.

D Straus, W Gilbert
PMCID: PMC369180  PMID: 3837846

Abstract

We report the sequence of the single chicken triosephosphate isomerase gene and its flanking regions. The 3-kilobase-long gene is composed of seven similarly sized exons and six introns. By using crystallographic and sequence data, we argue that this ancient gene was originally assembled from the genetic antecedents of exons.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alber T., Kawasaki G. Nucleotide sequence of the triose phosphate isomerase gene of Saccharomyces cerevisiae. J Mol Appl Genet. 1982;1(5):419–434. [PubMed] [Google Scholar]
  2. Ambartsumyan N. S., Mazo A. M. Elimination of the secondary structure effect in gell sequencing of nucleic acids. FEBS Lett. 1980 Jun 2;114(2):265–268. doi: 10.1016/0014-5793(80)81130-6. [DOI] [PubMed] [Google Scholar]
  3. Artavanis-Tsakonas S., Harris J. I. Primary structure of triosephosphate isomerase from Bacillus stearothermophilus. Eur J Biochem. 1980 Jul;108(2):599–611. doi: 10.1111/j.1432-1033.1980.tb04755.x. [DOI] [PubMed] [Google Scholar]
  4. Banner D. W., Bloomer A. C., Petsko G. A., Phillips D. C., Pogson C. I., Wilson I. A., Corran P. H., Furth A. J., Milman J. D., Offord R. E. Structure of chicken muscle triose phosphate isomerase determined crystallographically at 2.5 angstrom resolution using amino acid sequence data. Nature. 1975 Jun 19;255(5510):609–614. doi: 10.1038/255609a0. [DOI] [PubMed] [Google Scholar]
  5. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blake C. Exons--present from the beginning? Nature. 1983 Dec 8;306(5943):535–537. doi: 10.1038/306535a0. [DOI] [PubMed] [Google Scholar]
  7. Boyer H. W., Roulland-Dussoix D. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol. 1969 May 14;41(3):459–472. doi: 10.1016/0022-2836(69)90288-5. [DOI] [PubMed] [Google Scholar]
  8. Brack C., Tonegawa S. Variable and constant parts of the immunoglobulin light chain gene of a mouse myeloma cell are 1250 nontranslated bases apart. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5652–5656. doi: 10.1073/pnas.74.12.5652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Breathnach R., Chambon P. Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem. 1981;50:349–383. doi: 10.1146/annurev.bi.50.070181.002025. [DOI] [PubMed] [Google Scholar]
  10. Chu F. K., Maley G. F., Maley F., Belfort M. Intervening sequence in the thymidylate synthase gene of bacteriophage T4. Proc Natl Acad Sci U S A. 1984 May;81(10):3049–3053. doi: 10.1073/pnas.81.10.3049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Clewell D. B., Helinski D. R. Properties of a supercoiled deoxyribonucleic acid-protein relaxation complex and strand specificity of the relaxation event. Biochemistry. 1970 Oct 27;9(22):4428–4440. doi: 10.1021/bi00824a026. [DOI] [PubMed] [Google Scholar]
  12. Corran P. H., Waley S. G. The amino acid sequence of rabbit muscle triose phosphate isomerase. Biochem J. 1975 Feb;145(2):335–344. doi: 10.1042/bj1450335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Craik C. S., Sprang S., Fletterick R., Rutter W. J. Intron-exon splice junctions map at protein surfaces. Nature. 1982 Sep 9;299(5879):180–182. doi: 10.1038/299180a0. [DOI] [PubMed] [Google Scholar]
  14. Dagert M., Ehrlich S. D. Prolonged incubation in calcium chloride improves the competence of Escherichia coli cells. Gene. 1979 May;6(1):23–28. doi: 10.1016/0378-1119(79)90082-9. [DOI] [PubMed] [Google Scholar]
  15. Early P. W., Davis M. M., Kaback D. B., Davidson N., Hood L. Immunoglobulin heavy chain gene organization in mice: analysis of a myeloma genomic clone containing variable and alpha constant regions. Proc Natl Acad Sci U S A. 1979 Feb;76(2):857–861. doi: 10.1073/pnas.76.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Eiferman F. A., Young P. R., Scott R. W., Tilghman S. M. Intragenic amplification and divergence in the mouse alpha-fetoprotein gene. Nature. 1981 Dec 24;294(5843):713–718. doi: 10.1038/294713a0. [DOI] [PubMed] [Google Scholar]
  17. Frischauf A. M., Garoff H., Lehrach H. A subcloning strategy for DNA sequence analysis. Nucleic Acids Res. 1980 Dec 11;8(23):5541–5549. doi: 10.1093/nar/8.23.5541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Furth A. J., Milman J. D., Priddle J. D., Offord R. E. Studies on the subunit structure and amino acid sequence of trisoe phosphate isomerase from chicken breast muscle. Biochem J. 1974 Apr;139(1):11–22. doi: 10.1042/bj1390011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. doi: 10.1038/271501a0. [DOI] [PubMed] [Google Scholar]
  20. Go M. Correlation of DNA exonic regions with protein structural units in haemoglobin. Nature. 1981 May 7;291(5810):90–92. doi: 10.1038/291090a0. [DOI] [PubMed] [Google Scholar]
  21. Go M. Modular structural units, exons, and function in chicken lysozyme. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1964–1968. doi: 10.1073/pnas.80.7.1964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ish-Horowicz D., Burke J. F. Rapid and efficient cosmid cloning. Nucleic Acids Res. 1981 Jul 10;9(13):2989–2998. doi: 10.1093/nar/9.13.2989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kaine B. P., Gupta R., Woese C. R. Putative introns in tRNA genes of prokaryotes. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3309–3312. doi: 10.1073/pnas.80.11.3309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kolb E., Harris J. I., Bridgen J. Triose phosphate isomerase from the coelacanth. An approach to the rapid determination of an amino acid sequence with small amounts of material. Biochem J. 1974 Feb;137(2):185–197. doi: 10.1042/bj1370185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lee B., Richards F. M. The interpretation of protein structures: estimation of static accessibility. J Mol Biol. 1971 Feb 14;55(3):379–400. doi: 10.1016/0022-2836(71)90324-x. [DOI] [PubMed] [Google Scholar]
  26. Levine M., Muirhead H., Stammers D. K., Stuart D. I. Structure of pyruvate kinase and similarities with other enzymes: possible implications for protein taxonomy and evolution. Nature. 1978 Feb 16;271(5646):626–630. doi: 10.1038/271626a0. [DOI] [PubMed] [Google Scholar]
  27. Little P. F. Globin pseudogenes. Cell. 1982 Apr;28(4):683–684. doi: 10.1016/0092-8674(82)90045-9. [DOI] [PubMed] [Google Scholar]
  28. Lonberg N., Gilbert W. Intron/exon structure of the chicken pyruvate kinase gene. Cell. 1985 Jan;40(1):81–90. doi: 10.1016/0092-8674(85)90311-3. [DOI] [PubMed] [Google Scholar]
  29. Lu H. S., Yuan P. M., Gracy R. W. Primary structure of human triosephosphate isomerase. J Biol Chem. 1984 Oct 10;259(19):11958–11968. [PubMed] [Google Scholar]
  30. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  31. Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Perler F., Efstratiadis A., Lomedico P., Gilbert W., Kolodner R., Dodgson J. The evolution of genes: the chicken preproinsulin gene. Cell. 1980 Jun;20(2):555–566. doi: 10.1016/0092-8674(80)90641-8. [DOI] [PubMed] [Google Scholar]
  33. Pichersky E., Gottlieb L. D., Hess J. F. Nucleotide sequence of the triose phosphate isomerase gene of Escherichia coli. Mol Gen Genet. 1984;195(1-2):314–320. doi: 10.1007/BF00332765. [DOI] [PubMed] [Google Scholar]
  34. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  35. Sakano H., Rogers J. H., Hüppi K., Brack C., Traunecker A., Maki R., Wall R., Tonegawa S. Domains and the hinge region of an immunoglobulin heavy chain are encoded in separate DNA segments. Nature. 1979 Feb 22;277(5698):627–633. doi: 10.1038/277627a0. [DOI] [PubMed] [Google Scholar]
  36. Shah D. M., Hightower R. C., Meagher R. B. Genes encoding actin in higher plants: intron positions are highly conserved but the coding sequences are not. J Mol Appl Genet. 1983;2(1):111–126. [PubMed] [Google Scholar]
  37. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  38. Stammers D. K., Muirhead H. Three-dimensional structure of cat muscle pyruvate kinase at 3-1 A resolution. J Mol Biol. 1977 May 15;112(2):309–316. doi: 10.1016/s0022-2836(77)80146-0. [DOI] [PubMed] [Google Scholar]
  39. Stein J. P., Catterall J. F., Kristo P., Means A. R., O'Malley B. W. Ovomucoid intervening sequences specify functional domains and generate protein polymorphism. Cell. 1980 Oct;21(3):681–687. doi: 10.1016/0092-8674(80)90431-6. [DOI] [PubMed] [Google Scholar]
  40. Stone E. M., Rothblum K. N., Alevy M. C., Kuo T. M., Schwartz R. J. Complete sequence of the chicken glyceraldehyde-3-phosphate dehydrogenase gene. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1628–1632. doi: 10.1073/pnas.82.6.1628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Straus D., Gilbert W. Chicken triosephosphate isomerase complements an Escherichia coli deficiency. Proc Natl Acad Sci U S A. 1985 Apr;82(7):2014–2018. doi: 10.1073/pnas.82.7.2014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Tonegawa S., Maxam A. M., Tizard R., Bernard O., Gilbert W. Sequence of a mouse germ-line gene for a variable region of an immunoglobulin light chain. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1485–1489. doi: 10.1073/pnas.75.3.1485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wozney J., Hanahan D., Tate V., Boedtker H., Doty P. Structure of the pro alpha 2 (I) collagen gene. Nature. 1981 Nov 12;294(5837):129–135. doi: 10.1038/294129a0. [DOI] [PubMed] [Google Scholar]
  44. Wu C. The 5' ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature. 1980 Aug 28;286(5776):854–860. doi: 10.1038/286854a0. [DOI] [PubMed] [Google Scholar]
  45. Yamada Y., Avvedimento V. E., Mudryj M., Ohkubo H., Vogeli G., Irani M., Pastan I., de Crombrugghe B. The collagen gene: evidence for its evolutinary assembly by amplification of a DNA segment containing an exon of 54 bp. Cell. 1980 Dec;22(3):887–892. doi: 10.1016/0092-8674(80)90565-6. [DOI] [PubMed] [Google Scholar]
  46. Zakut R., Shani M., Givol D., Neuman S., Yaffe D., Nudel U. Nucleotide sequence of the rat skeletal muscle actin gene. Nature. 1982 Aug 26;298(5877):857–859. doi: 10.1038/298857a0. [DOI] [PubMed] [Google Scholar]

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