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. 1980 Oct;77(10):5759–5763. doi: 10.1073/pnas.77.10.5759

Exons encode functional and structural units of chicken lysozyme.

A Jung, A E Sippel, M Grez, G Schütz
PMCID: PMC350150  PMID: 6934509

Abstract

The nucleotide sequence was determined for the chicken egg white lysozyme mRNA and for the exons of the gene together with their flanking intron regions. The exon pattern is to some degree related to the structural subdivision of the final protein product. However, the relationship of exons to functional units of the enzyme is better established. Exon 2 codes for amino acids 28-82, which include the catalytically active residues and a cluster of amino acids which bind rings C, D, E, and F of the oligosaccharide substrate. Exon 3 codes for amino acids 82-108, which give additional substrate specificity, determine the cleavage frame for the alternating N-acetylglucosamine/N-acetylmuramic acid chain, and increase the catalytic efficiency of the active center. Exons 1 and 4, respectively, code for translational signal sequences on the mRNA, for the signal peptide of prelysozyme, and for the amino- and carboxy-terminal regions of the enzyme. These regions increase the stability of the molecule but are not directly involved in the catalytic function.

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Selected References

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

  1. Aleström P., Akusjärvi G., Perricaudet M., Mathews M. B., Klessig D. F., Pettersson U. The gene for polypeptide IX of adenovirus type 2 and its unspliced messenger RNA. Cell. 1980 Mar;19(3):671–681. doi: 10.1016/s0092-8674(80)80044-4. [DOI] [PubMed] [Google Scholar]
  2. Baldacci P., Royal A., Cami B., Perrin F., Krust A., Garapin A., Kourilsky P. Isolation of the lysozyme gene of chicken. Nucleic Acids Res. 1979 Jun 25;6(8):2667–2681. doi: 10.1093/nar/6.8.2667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berget S. M., Moore C., Sharp P. A. Spliced segments at the 5' terminus of adenovirus 2 late mRNA. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3171–3175. doi: 10.1073/pnas.74.8.3171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blake C. C. Exons encode protein functional units. Nature. 1979 Feb 22;277(5698):598–598. doi: 10.1038/277598a0. [DOI] [PubMed] [Google Scholar]
  5. Blake C. C., Koenig D. F., Mair G. A., North A. C., Phillips D. C., Sarma V. R. Structure of hen egg-white lysozyme. A three-dimensional Fourier synthesis at 2 Angstrom resolution. Nature. 1965 May 22;206(4986):757–761. doi: 10.1038/206757a0. [DOI] [PubMed] [Google Scholar]
  6. Breathnach R., Benoist C., O'Hare K., Gannon F., Chambon P. Ovalbumin gene: evidence for a leader sequence in mRNA and DNA sequences at the exon-intron boundaries. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4853–4857. doi: 10.1073/pnas.75.10.4853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. CANFIELD R. E. THE AMINO ACID SEQUENCE OF EGG WHITE LYSOZYME. J Biol Chem. 1963 Aug;238:2698–2707. [PubMed] [Google Scholar]
  8. Chow L. T., Gelinas R. E., Broker T. R., Roberts R. J. An amazing sequence arrangement at the 5' ends of adenovirus 2 messenger RNA. Cell. 1977 Sep;12(1):1–8. doi: 10.1016/0092-8674(77)90180-5. [DOI] [PubMed] [Google Scholar]
  9. Craik C. S., Buchman S. R., Beychok S. Characterization of globin domains: heme binding to the central exon product. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1384–1388. doi: 10.1073/pnas.77.3.1384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Crick F. Split genes and RNA splicing. Science. 1979 Apr 20;204(4390):264–271. doi: 10.1126/science.373120. [DOI] [PubMed] [Google Scholar]
  11. Crippen G. M. The tree structural organization of proteins. J Mol Biol. 1978 Dec 15;126(3):315–332. doi: 10.1016/0022-2836(78)90043-8. [DOI] [PubMed] [Google Scholar]
  12. Darnell J. E., Jr Implications of RNA-RNA splicing in evolution of eukaryotic cells. Science. 1978 Dec 22;202(4374):1257–1260. doi: 10.1126/science.364651. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Eaton W. A. The relationship between coding sequences and function in haemoglobin. Nature. 1980 Mar 13;284(5752):183–185. doi: 10.1038/284183a0. [DOI] [PubMed] [Google Scholar]
  15. Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. doi: 10.1038/271501a0. [DOI] [PubMed] [Google Scholar]
  16. Gronenborn B., Messing J. Methylation of single-stranded DNA in vitro introduces new restriction endonuclease cleavage sites. Nature. 1978 Mar 23;272(5651):375–377. doi: 10.1038/272375a0. [DOI] [PubMed] [Google Scholar]
  17. Hynes N. E., Groner B., Sippel A. E., Jeep S., Wurtz T., Nguyen-Huu M. C., Giesecke K., Schütz G. Control of cellular content of chicken egg white protein specific RNA during estrogen administration and withdrawal. Biochemistry. 1979 Feb 20;18(4):616–624. doi: 10.1021/bi00571a011. [DOI] [PubMed] [Google Scholar]
  18. JOLLES J., JAUREGUI ADELL J., BERNIER I., JOLLES P. LA STRUCTURE CHIMIQUE DU LYSOZYME DE BLANC D'OEUF DE POULE: 'ETUDE D'ETAILL'EE. Biochim Biophys Acta. 1963 Dec 13;78:668–689. doi: 10.1016/0006-3002(63)91033-3. [DOI] [PubMed] [Google Scholar]
  19. Kelly J. A., Sielecki A. R., Sykes B. D., James M. N., Phillips D. C. X-ray crystallography of the binding of the bacterial cell wall trisaccharide NAM-NAG-NAM to lysozyme. Nature. 1979 Dec 20;282(5741):875–878. doi: 10.1038/282875a0. [DOI] [PubMed] [Google Scholar]
  20. Konkel D. A., Tilghman S. M., Leder P. The sequence of the chromosomal mouse beta-globin major gene: homologies in capping, splicing and poly(A) sites. Cell. 1978 Dec;15(4):1125–1132. doi: 10.1016/0092-8674(78)90040-5. [DOI] [PubMed] [Google Scholar]
  21. Lai E. C., Stein J. P., Catterall J. F., Woo S. L., Mace M. L., Means A. R., O'Malley B. W. Molecular structure and flanking nucleotide sequences of the natural chicken ovomucoid gene. Cell. 1979 Nov;18(3):829–842. doi: 10.1016/0092-8674(79)90135-1. [DOI] [PubMed] [Google Scholar]
  22. Lai E. C., Woo S. L., Dugaiczyk A., O'Malley B. W. The ovalbumin gene: alleles created by mutations in the intervening sequences of the natural gene. Cell. 1979 Jan;16(1):201–211. doi: 10.1016/0092-8674(79)90201-0. [DOI] [PubMed] [Google Scholar]
  23. Lerner M. R., Boyle J. A., Mount S. M., Wolin S. L., Steitz J. A. Are snRNPs involved in splicing? Nature. 1980 Jan 10;283(5743):220–224. doi: 10.1038/283220a0. [DOI] [PubMed] [Google Scholar]
  24. Levy S., Sures I., Kedes L. H. Sequence of the 5'-end of Strongylocentrotus purpuratus H2b histone mRNA and its location within histone DNA. Nature. 1979 Jun 21;279(5715):737–739. doi: 10.1038/279737a0. [DOI] [PubMed] [Google Scholar]
  25. Lindenmaier W., Nguyen-Huu M. C., Lurz R., Stratmann M., Blin N., Wurtz T., Hauser H. J., Sippel A. E., Schütz G. Arrangement of coding and intervening sequences of chicken lysozyme gene. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6196–6200. doi: 10.1073/pnas.76.12.6196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lindenmaier W., Nguyen-Huu M. C., Stratmann L. M., Blin N., Wurtz T., Hauser H. J., Giesecke K., Land H., Jeep S., Grez M. The isolation and characterization of the chicken lysozyme and ovomucoid gene. J Steroid Biochem. 1980 Jan;12:211–218. doi: 10.1016/0022-4731(80)90270-8. [DOI] [PubMed] [Google Scholar]
  27. Lomedico P., Rosenthal N., Efstratidadis A., Gilbert W., Kolodner R., Tizard R. The structure and evolution of the two nonallelic rat preproinsulin genes. Cell. 1979 Oct;18(2):545–558. doi: 10.1016/0092-8674(79)90071-0. [DOI] [PubMed] [Google Scholar]
  28. Mantei N., Boll W., Weissmann C. Rabbit beta-globin mRNA production in mouse L cells transformed with cloned rabbit beta-globin chromosomal DNA. Nature. 1979 Sep 6;281(5726):40–46. doi: 10.1038/281040a0. [DOI] [PubMed] [Google Scholar]
  29. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nguyen-Huu M. C., Stratmann M., Groner B., Wurtz T., Land H., Giesecke K., Sippel A. E., Schütz G. Chicken lysozyme gene contains several intervening sequences. Proc Natl Acad Sci U S A. 1979 Jan;76(1):76–80. doi: 10.1073/pnas.76.1.76. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Palmiter R. D., Gagnon J., Ericsson L. H., Walsh K. A. Precursor of egg white lysozyme. Amino acid sequence of an NH2-terminal extension. J Biol Chem. 1977 Sep 25;252(18):6386–6393. [PubMed] [Google Scholar]
  32. Proudfoot N. J., Brownlee G. G. 3' non-coding region sequences in eukaryotic messenger RNA. Nature. 1976 Sep 16;263(5574):211–214. doi: 10.1038/263211a0. [DOI] [PubMed] [Google Scholar]
  33. Rose G. D. Hierarchic organization of domains in globular proteins. J Mol Biol. 1979 Nov 5;134(3):447–470. doi: 10.1016/0022-2836(79)90363-2. [DOI] [PubMed] [Google Scholar]
  34. Rüther U. Construction and properties of a new cloning vehicle, allowing direct screening for recombinant plasmids. Mol Gen Genet. 1980;178(2):475–477. doi: 10.1007/BF00270503. [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. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schreier P. H., Cortese R. A fast and simple method for sequencing DNA cloned in the single-stranded bacteriophage M13. J Mol Biol. 1979 Mar 25;129(1):169–172. doi: 10.1016/0022-2836(79)90068-8. [DOI] [PubMed] [Google Scholar]
  38. Schütz G., Nguyen-Huu M. C., Giesecke K., Hynes N. E., Groner B., Wurtz T., Sippel A. E. Hormonal control of egg white protein messenger RNA synthesis in the chicken oviduct. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):617–624. doi: 10.1101/sqb.1978.042.01.064. [DOI] [PubMed] [Google Scholar]
  39. Seif I., Khoury G., Dhar R. A rapid enzymatic DNA sequencing technique: determination of sequence alterations in early simian virus 40 temperature sensitive and deletion mutants. Nucleic Acids Res. 1980 May 24;8(10):2225–2240. doi: 10.1093/nar/8.10.2225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sippel A. E., Land H., Lindenmaier W., Nguyen-Huu M. C., Wurtz T., Timmis K. N., Giesecke K., Schütz G. Cloning of chicken lysozyme structural gene sequences synthesized in vitro. Nucleic Acids Res. 1978 Sep;5(9):3275–3294. doi: 10.1093/nar/5.9.3275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. Wetlaufer D. B. Nucleation, rapid folding, and globular intrachain regions in proteins. Proc Natl Acad Sci U S A. 1973 Mar;70(3):697–701. doi: 10.1073/pnas.70.3.697. [DOI] [PMC free article] [PubMed] [Google Scholar]

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