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. 1990 Apr;9(4):1283–1288. doi: 10.1002/j.1460-2075.1990.tb08237.x

Repetitive sequence involvement in the duplication and divergence of mouse lysozyme genes.

M Cross 1, R Renkawitz 1
PMCID: PMC551806  PMID: 2323338

Abstract

Mouse M and P lysozymes are the products of separate genes, are specifically expressed in separate tissues, and are adapted to different functions. The lysozyme genes have assumed these markedly different characteristics following their generation by gene duplication 30-50 million years ago. The discovery of the lysozyme P gene only 5 kb upstream from the M gene in tandem repeat has enabled an investigation of the molecular basis of their duplication and subsequent divergence. The duplication is shown to have involved recombination between two B2 repeat sequences flanking the original gene. The resulting downstream copy has retained the myeloid specificity of expression along with just 1.7 kb of upstream sequences, while the upstream copy is inactive in macrophages and has become expressed instead in the small intestine. Although multiple gene conversion events have served to maintain a generally high homology between the genes, certain regions have been found to be specific for either one of the gene pair: two repetitive sequences peculiar to the P region may serve to protect the coding regions from gene conversion, while sequences unique to the M gene may be more directly involved in differential regulation.

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Selected References

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

  1. Barsh G. S., Seeburg P. H., Gelinas R. E. The human growth hormone gene family: structure and evolution of the chromosomal locus. Nucleic Acids Res. 1983 Jun 25;11(12):3939–3958. doi: 10.1093/nar/11.12.3939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Carle G. F., Frank M., Olson M. V. Electrophoretic separations of large DNA molecules by periodic inversion of the electric field. Science. 1986 Apr 4;232(4746):65–68. doi: 10.1126/science.3952500. [DOI] [PubMed] [Google Scholar]
  3. Chen E. Y., Seeburg P. H. Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA. 1985 Apr;4(2):165–170. doi: 10.1089/dna.1985.4.165. [DOI] [PubMed] [Google Scholar]
  4. Chung L. P., Keshav S., Gordon S. Cloning the human lysozyme cDNA: inverted Alu repeat in the mRNA and in situ hybridization for macrophages and Paneth cells. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6227–6231. doi: 10.1073/pnas.85.17.6227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cross M., Mangelsdorf I., Wedel A., Renkawitz R. Mouse lysozyme M gene: isolation, characterization, and expression studies. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6232–6236. doi: 10.1073/pnas.85.17.6232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dobson D. E., Prager E. M., Wilson A. C. Stomach lysozymes of ruminants. I. Distribution and catalytic properties. J Biol Chem. 1984 Sep 25;259(18):11607–11616. [PubMed] [Google Scholar]
  8. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  9. Fisher D. A., Pecht M., Hood L. DNA sequence of a class I pseudogene from the Tla region of the murine MHC: recombination at a B2 alu repetitive sequence. J Mol Evol. 1989 Apr;28(4):306–312. doi: 10.1007/BF02103426. [DOI] [PubMed] [Google Scholar]
  10. Hammer M. F., Schilling J. W., Prager E. M., Wilson A. C. Recruitment of lysozyme as a major enzyme in the mouse gut: duplication, divergence, and regulatory evolution. J Mol Evol. 1987;24(3):272–279. doi: 10.1007/BF02111240. [DOI] [PubMed] [Google Scholar]
  11. Hammer M. F., Wilson A. C. Regulatory and structural genes for lysozymes of mice. Genetics. 1987 Mar;115(3):521–533. doi: 10.1093/genetics/115.3.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hess J. F., Fox M., Schmid C., Shen C. K. Molecular evolution of the human adult alpha-globin-like gene region: insertion and deletion of Alu family repeats and non-Alu DNA sequences. Proc Natl Acad Sci U S A. 1983 Oct;80(19):5970–5974. doi: 10.1073/pnas.80.19.5970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Irwin D. M., Wilson A. C. Multiple cDNA sequences and the evolution of bovine stomach lysozyme. J Biol Chem. 1989 Jul 5;264(19):11387–11393. [PubMed] [Google Scholar]
  14. Jeffreys A. J., Harris S. Processes of gene duplication. Nature. 1982 Mar 4;296(5852):9–10. doi: 10.1038/296009a0. [DOI] [PubMed] [Google Scholar]
  15. Jollès P., Jollès J. What's new in lysozyme research? Always a model system, today as yesterday. Mol Cell Biochem. 1984 Sep;63(2):165–189. doi: 10.1007/BF00285225. [DOI] [PubMed] [Google Scholar]
  16. Klockars M., Osserman E. F. Localization of lysozyme in normal rat tissues by an immunoperoxidase method. J Histochem Cytochem. 1974 Mar;22(3):139–146. doi: 10.1177/22.3.139. [DOI] [PubMed] [Google Scholar]
  17. Krayev A. S., Markusheva T. V., Kramerov D. A., Ryskov A. P., Skryabin K. G., Bayev A. A., Georgiev G. P. Ubiquitous transposon-like repeats B1 and B2 of the mouse genome: B2 sequencing. Nucleic Acids Res. 1982 Dec 11;10(23):7461–7475. doi: 10.1093/nar/10.23.7461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Li W. H., Tanimura M., Sharp P. M. An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol. 1987;25(4):330–342. doi: 10.1007/BF02603118. [DOI] [PubMed] [Google Scholar]
  19. Maeda N., Smithies O. The evolution of multigene families: human haptoglobin genes. Annu Rev Genet. 1986;20:81–108. doi: 10.1146/annurev.ge.20.120186.000501. [DOI] [PubMed] [Google Scholar]
  20. Nicholls R. D., Fischel-Ghodsian N., Higgs D. R. Recombination at the human alpha-globin gene cluster: sequence features and topological constraints. Cell. 1987 May 8;49(3):369–378. doi: 10.1016/0092-8674(87)90289-3. [DOI] [PubMed] [Google Scholar]
  21. Prieur D. J. Tissue specific deficiency of lysozyme in ruminants. Comp Biochem Physiol B. 1986;85(2):349–353. doi: 10.1016/0305-0491(86)90011-8. [DOI] [PubMed] [Google Scholar]
  22. Ralph P., Moore M. A., Nilsson K. Lysozyme synthesis by established human and murine histiocytic lymphoma cell lines. J Exp Med. 1976 Jun 1;143(6):1528–1533. doi: 10.1084/jem.143.6.1528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Schimenti J. C., Duncan C. H. Ruminant globin gene structures suggest an evolutionary role for Alu-type repeats. Nucleic Acids Res. 1984 Feb 10;12(3):1641–1655. doi: 10.1093/nar/12.3.1641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Shen S. H., Slightom J. L., Smithies O. A history of the human fetal globin gene duplication. Cell. 1981 Oct;26(2 Pt 2):191–203. doi: 10.1016/0092-8674(81)90302-0. [DOI] [PubMed] [Google Scholar]
  25. Soares M. B., Schon E., Henderson A., Karathanasis S. K., Cate R., Zeitlin S., Chirgwin J., Efstratiadis A. RNA-mediated gene duplication: the rat preproinsulin I gene is a functional retroposon. Mol Cell Biol. 1985 Aug;5(8):2090–2103. doi: 10.1128/mcb.5.8.2090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wu C. I., Li W. H. Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1741–1745. doi: 10.1073/pnas.82.6.1741. [DOI] [PMC free article] [PubMed] [Google Scholar]

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