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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1993 Aug 1;90(15):7205–7209. doi: 10.1073/pnas.90.15.7205

Sequential insertion of Alu family repeats into specific genomic sites of higher primates.

A D Bailey 1, C K Shen 1
PMCID: PMC47105  PMID: 8394013

Abstract

The presence of Alu family repeats is closely associated with interspecies length polymorphisms of certain genomic regions among different higher primates. By sequence analysis of cloned DNA, we show that one major cause for the length difference between the gibbon adult alpha-globin locus and those of human, orangutan, and Old World monkeys is the existence of multimeric Alu family repeats. Triplet Alu family repeats exist at two genomic sites of gibbon. Instead, singleton or doublet Alu family repeats are present at the orthologous positions in other higher primates. Sequence comparisons suggest that these doublet and triplet Alu repeats have been created by successive insertion of different singleton Alu repeat sequences, of approximately 300 bp, into the same genomic spot(s) during primate evolution. The approximate dates of insertion of these singleton Alu repeats support the concept of overlapping periods of active transposition or retroposition of Alu repeat subfamilies. This dynamic flow of Alu repeat sequences during primate evolution into the adult alpha-globin loci, but not beta-globin-like loci, is consistent with the previous finding that R-banding regions of the primate chromosomes are enriched in Alu repeats.

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Selected References

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

  1. Bailey A. D., Stanhope M., Slightom J. L., Goodman M., Shen C. C., Shen C. K. Tandemly duplicated alpha globin genes of gibbon. J Biol Chem. 1992 Sep 15;267(26):18398–18406. [PubMed] [Google Scholar]
  2. Bailey W. J., Fitch D. H., Tagle D. A., Czelusniak J., Slightom J. L., Goodman M. Molecular evolution of the psi eta-globin gene locus: gibbon phylogeny and the hominoid slowdown. Mol Biol Evol. 1991 Mar;8(2):155–184. doi: 10.1093/oxfordjournals.molbev.a040641. [DOI] [PubMed] [Google Scholar]
  3. Britten R. J., Baron W. F., Stout D. B., Davidson E. H. Sources and evolution of human Alu repeated sequences. Proc Natl Acad Sci U S A. 1988 Jul;85(13):4770–4774. doi: 10.1073/pnas.85.13.4770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Ellis N., Yen P., Neiswanger K., Shapiro L. J., Goodfellow P. N. Evolution of the pseudoautosomal boundary in Old World monkeys and great apes. Cell. 1990 Nov 30;63(5):977–986. doi: 10.1016/0092-8674(90)90501-5. [DOI] [PubMed] [Google Scholar]
  6. Hardison R. C., Sawada I., Cheng J. F., Shen C. K., Schmid C. W. A previously undetected pseudogene in the human alpha globin gene cluster. Nucleic Acids Res. 1986 Feb 25;14(4):1903–1911. doi: 10.1093/nar/14.4.1903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Hess J., Perez-Stable C., Wu G. J., Weir B., Tinoco I., Jr, Shen C. K. End-to-end transcription of an Alu family repeat. A new type of polymerase-III-dependent terminator and its evolutionary implication. J Mol Biol. 1985 Jul 5;184(1):7–21. doi: 10.1016/0022-2836(85)90039-7. [DOI] [PubMed] [Google Scholar]
  9. Holmquist G. P. Chromosome bands, their chromatin flavors, and their functional features. Am J Hum Genet. 1992 Jul;51(1):17–37. [PMC free article] [PubMed] [Google Scholar]
  10. Hsu S. L., Marks J., Shaw J. P., Tam M., Higgs D. R., Shen C. C., Shen C. K. Structure and expression of the human theta 1 globin gene. Nature. 1988 Jan 7;331(6151):94–96. doi: 10.1038/331094a0. [DOI] [PubMed] [Google Scholar]
  11. Jagadeeswaran P., Forget B. G., Weissman S. M. Short interspersed repetitive DNA elements in eucaryotes: transposable DNA elements generated by reverse transcription of RNA pol III transcripts? Cell. 1981 Oct;26(2 Pt 2):141–142. doi: 10.1016/0092-8674(81)90296-8. [DOI] [PubMed] [Google Scholar]
  12. Jurka J., Smith T. F., Labuda D. Small cytoplasmic Ro RNA pseudogene and an Alu repeat in the human alpha-1 globin gene. Nucleic Acids Res. 1988 Jan 25;16(2):766–766. doi: 10.1093/nar/16.2.766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jurka J., Smith T. A fundamental division in the Alu family of repeated sequences. Proc Natl Acad Sci U S A. 1988 Jul;85(13):4775–4778. doi: 10.1073/pnas.85.13.4775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Koop B. F., Miyamoto M. M., Embury J. E., Goodman M., Czelusniak J., Slightom J. L. Nucleotide sequence and evolution of the orangutan epsilon globin gene region and surrounding Alu repeats. J Mol Evol. 1986;24(1-2):94–102. doi: 10.1007/BF02099956. [DOI] [PubMed] [Google Scholar]
  15. Korenberg J. R., Rykowski M. C. Human genome organization: Alu, lines, and the molecular structure of metaphase chromosome bands. Cell. 1988 May 6;53(3):391–400. doi: 10.1016/0092-8674(88)90159-6. [DOI] [PubMed] [Google Scholar]
  16. Leung S., Proudfoot N. J., Whitelaw E. The gene for theta-globin is transcribed in human fetal erythroid tissues. Nature. 1987 Oct 8;329(6139):551–554. doi: 10.1038/329551a0. [DOI] [PubMed] [Google Scholar]
  17. Liebhaber S. A., Goossens M., Kan Y. W. Homology and concerted evolution at the alpha 1 and alpha 2 loci of human alpha-globin. Nature. 1981 Mar 5;290(5801):26–29. doi: 10.1038/290026a0. [DOI] [PubMed] [Google Scholar]
  18. Manuelidis L., Ward D. C. Chromosomal and nuclear distribution of the HindIII 1.9-kb human DNA repeat segment. Chromosoma. 1984;91(1):28–38. doi: 10.1007/BF00286482. [DOI] [PubMed] [Google Scholar]
  19. Marks J., Shaw J. P., Shen C. K. Sequence organization and genomic complexity of primate theta 1 globin gene, a novel alpha-globin-like gene. Nature. 1986 Jun 19;321(6072):785–788. doi: 10.1038/321785a0. [DOI] [PubMed] [Google Scholar]
  20. Marks J., Shaw J. P., Shen C. K. The orangutan adult alpha-globin gene locus: duplicated functional genes and a newly detected member of the primate alpha-globin gene family. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1413–1417. doi: 10.1073/pnas.83.5.1413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Matera A. G., Hellmann U., Schmid C. W. A transpositionally and transcriptionally competent Alu subfamily. Mol Cell Biol. 1990 Oct;10(10):5424–5432. doi: 10.1128/mcb.10.10.5424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Michelson A. M., Orkin S. H. Boundaries of gene conversion within the duplicated human alpha-globin genes. Concerted evolution by segmental recombination. J Biol Chem. 1983 Dec 25;258(24):15245–15254. [PubMed] [Google Scholar]
  24. Perez-Stable C., Shen C. C., Shen C. K. Enrichment and depletion of Hela topoisomerase I recognition sites among specific types of DNA elements. Nucleic Acids Res. 1988 Aug 25;16(16):7975–7993. doi: 10.1093/nar/16.16.7975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rogers J. H. The origin and evolution of retroposons. Int Rev Cytol. 1985;93:187–279. doi: 10.1016/s0074-7696(08)61375-3. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Sawada I., Willard C., Shen C. K., Chapman B., Wilson A. C., Schmid C. W. Evolution of Alu family repeats since the divergence of human and chimpanzee. J Mol Evol. 1985;22(4):316–322. doi: 10.1007/BF02115687. [DOI] [PubMed] [Google Scholar]
  28. Shaw J. P., Marks J., Shen C. K. Evidence that the recently discovered theta 1-globin gene is functional in higher primates. Nature. 1987 Apr 16;326(6114):717–720. doi: 10.1038/326717a0. [DOI] [PubMed] [Google Scholar]
  29. Shaw J. P., Marks J., Shen C. K. The adult alpha-globin locus of Old World monkeys: an abrupt breakdown of sequence similarity to human is defined by an Alu family repeat insertion site. J Mol Evol. 1991 Dec;33(6):506–513. doi: 10.1007/BF02102803. [DOI] [PubMed] [Google Scholar]
  30. Shen M. R., Batzer M. A., Deininger P. L. Evolution of the master Alu gene(s). J Mol Evol. 1991 Oct;33(4):311–320. doi: 10.1007/BF02102862. [DOI] [PubMed] [Google Scholar]
  31. Singer M. F. SINEs and LINEs: highly repeated short and long interspersed sequences in mammalian genomes. Cell. 1982 Mar;28(3):433–434. doi: 10.1016/0092-8674(82)90194-5. [DOI] [PubMed] [Google Scholar]
  32. Trabuchet G., Chebloune Y., Savatier P., Lachuer J., Faure C., Verdier G., Nigon V. M. Recent insertion of an Alu sequence in the beta-globin gene cluster of the gorilla. J Mol Evol. 1987;25(4):288–291. doi: 10.1007/BF02603112. [DOI] [PubMed] [Google Scholar]
  33. Van Arsdell S. W., Denison R. A., Bernstein L. B., Weiner A. M., Manser T., Gesteland R. F. Direct repeats flank three small nuclear RNA pseudogenes in the human genome. Cell. 1981 Oct;26(1 Pt 1):11–17. doi: 10.1016/0092-8674(81)90028-3. [DOI] [PubMed] [Google Scholar]
  34. Wallace M. R., Andersen L. B., Saulino A. M., Gregory P. E., Glover T. W., Collins F. S. A de novo Alu insertion results in neurofibromatosis type 1. Nature. 1991 Oct 31;353(6347):864–866. doi: 10.1038/353864a0. [DOI] [PubMed] [Google Scholar]
  35. Weiner A. M., Deininger P. L., Efstratiadis A. Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu Rev Biochem. 1986;55:631–661. doi: 10.1146/annurev.bi.55.070186.003215. [DOI] [PubMed] [Google Scholar]
  36. Willard C., Nguyen H. T., Schmid C. W. Existence of at least three distinct Alu subfamilies. J Mol Evol. 1987;26(3):180–186. doi: 10.1007/BF02099850. [DOI] [PubMed] [Google Scholar]
  37. Zimmer E. A., Martin S. L., Beverley S. M., Kan Y. W., Wilson A. C. Rapid duplication and loss of genes coding for the alpha chains of hemoglobin. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2158–2162. doi: 10.1073/pnas.77.4.2158. [DOI] [PMC free article] [PubMed] [Google Scholar]

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