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The multiple origins of human Alu sequences

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Summary

I have analyzed a collection of published human Alu sequences. The compiled sequences show several unexpected features, including a uniform pattern of divergence from their consensus sequence, a mutual divergence that is not correlated with their age, and common features in the genomic DNA flanking the 5′ ends of the elements. I suggest that the Alu family of sequences derives from a large pool of precursors and not from a single precursor similar to the family consensus sequence, and that new elements integrate into the genome selectively at oligo-A-rich sites.

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References

  • Abarbanel RM, Wieneke PR, Mansfield E, Jaffe DA, Brutlag DL (1984) Rapid searches for complex patterns in biological molecules. Nucleic Acids Res 12:263–280

    PubMed  Google Scholar 

  • Bains W (1986) MULTAN: a program to align multiple DNA sequences. Nucleic Acids Res 14:159–177

    PubMed  Google Scholar 

  • Barrie PA, Jeffreys AJ, Scott AF (1981) Evolution of the β-globin genes cluster in man and primates. J Mol Biol 149:319–336

    Article  PubMed  Google Scholar 

  • Bell B, Pictet R, Rutter WJ (1980) Analysis of the regions flanking the human insulin gene and sequence of an Alu family member. Nucleic Acids Res 8:4091–4109

    PubMed  Google Scholar 

  • Bennet K, Hill RE, Pietras DF, Woodsworth-Gutai M, Kane-Haas C, Houston JM, Health JK, Hastie, ND (1984) Most highly repeated dispersed DNA families in the mouse genome. Mol Cell Biol 4:1561–1571

    PubMed  Google Scholar 

  • Bird AP (1980) DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res 8:1499–1504

    PubMed  Google Scholar 

  • Brown AL (1984) On the origin of the Alu family of repeated sequences. Nature 312:106

    Article  PubMed  Google Scholar 

  • Brownell E, Krystal M, Arnheim N (1983) Structure and evolution of human and African ape rDNA pseudogenes. Mol Biol Evol 1:29–37

    PubMed  Google Scholar 

  • Chang L-YE, Slightom JL (1984) Isolation and nucleotide sequence of the beta-type globin pseudogene from human, gorilla and chimpanzee. J Mol Biol 180:767–784

    Article  PubMed  Google Scholar 

  • Chung DW, Que BG, Rixon MW, Mace M Jr, Davie EW (1983) Characterisation of complementary deoxyribonucleic acid and genomic DNA for the beta chain of human fibrinogen. Biochemistry 22:3244–3250

    Article  PubMed  Google Scholar 

  • Clayton J, Kedes L (1982) GEL, a DNA sequencing project management system. Nucleic Acids Res 10:305–321

    PubMed  Google Scholar 

  • Colby WW, Chen EY, Smith DH, Levinson AD (1983) Identification and nucleotide sequence of a human locus homologous to the v-myc oncogene of avian myelocytomatosis virus MC29. Nature 301:722–725

    Article  PubMed  Google Scholar 

  • Comb M, Rosen H, Seeburg P, Adelman J, Herbert E (1983) Primary structure of the human proenkephalin gene. DNA 2:213–229

    PubMed  Google Scholar 

  • Daniels GR, Deininger PL (1985) Integration site preferences of the Alu family and similar repetitive DNA sequences. Nucleic Acids Res 13:8939–8954

    PubMed  Google Scholar 

  • Daniels GR, Fox GM, Loewensteiner D, Schmid CW, Deininger PL (1983) Species-specific homogeneity of the primate Alu family of repeated DNA sequences. Nucleic Acids Res 11:7579–7593

    PubMed  Google Scholar 

  • Das HK, Lawrance SK, Weissman SM (1983) Structure and nucleotide sequence of the heavy chain gene of HLA-DR. Proc Natl Acad Sci USA 80:3543–3547

    PubMed  Google Scholar 

  • Davidson EH, Graham DE, Neufeld BR, Chamberlin ME, Amenson CS, Hough BR, Britten RJ (1973) Arrangement and characterisation of repetitive sequence elements in animal DNAs. Cold Spring Harbor Symp Quant Biol 38:295–301

    Google Scholar 

  • Deininger PL, Jolly DJ, Rubin CM, Friedman T, Schmid CW (1981) Base sequence studies of 300 nucleotide renatured repeated human DNA clones. J Mol Biol 151:17–33

    Article  PubMed  Google Scholar 

  • Di Segni G, Carrara G, Tocchini-Valentini GR, Shoulders CC, Baralle FE (1981) Selective in vitro transcription of one of the two Alu family repeats present in the 5′ flanking region of the human epsilon-globin gene. Nucleic Acids Res 9:6709–6722

    PubMed  Google Scholar 

  • Dover GA (1982) Molecular drive: a cohesive mode of species evolution. Nature 299:111–117

    Article  PubMed  Google Scholar 

  • Duncan CH, Jagadeeswaran P, Wang RRC, Weissman SM (1981) Structural analysis of templates and RNA polymerase III transcripts of Alu family sequences interspersed among the human beta-like globin genes. Gene 13:185–196

    Article  PubMed  Google Scholar 

  • Economou-Pachis A, Tsichlis PN (1985) Insertation of an Alu SINE in the human homologue of the Mliv-2 locus. Nucleic Acids Res 13:5073–5091

    Google Scholar 

  • Farris (1972) Estimating phylogenetic trees from distance matrices. Am Nat 106:645–668

    Article  Google Scholar 

  • Friezner Degen SJ, MacGillivray RTA, Davie DW (1983) Characterization of the complementary deoxyribonucleic acid and gene coding for human prothrombin. Biochemistry 22:2087–2097

    Article  PubMed  Google Scholar 

  • Frommer M, Prosser J, Vincent PC (1984) Human satellite I sequences include a male-specific 2.47kb tandemly repeated unit containing one Alu family member per repeat. Nucleic Acids Res 12:2887–2900

    PubMed  Google Scholar 

  • Fukuyami Y, Collins F, Kole R, Stoeckert CJ, Jagadeeswaran P, Duncan CH, Weissman SM (1983) Sequences of human repetitive DNA, alpha globin and MHC locus genes. I. Repeated sequence DNA. Cold Spring Harbor Symp Quant Biol 47:1079–1081

    PubMed  Google Scholar 

  • Goodman M, Koop BF, Czelusniak J, Weiss ML, Slightom JL (1984) Theeta-globin gene. Its long evolutionary history in the mammals. J Mol Biol 180:803–824

    Google Scholar 

  • Greenberg BH, Bencen GH, Seilhamer JJ, Lewicki JA, Fiddes JC (1984) Nucleotide sequence of the gene encoding human natriuetic factor precursor. Nature 312:656–658

    Article  PubMed  Google Scholar 

  • Grimaldi G, Singer MF (1983) Members of the KpnI family of long interspersed repeated sequences join and interrupt alphasatellite in the monkey genome. Nucleic Acids Res 11:321–338

    PubMed  Google Scholar 

  • Hammarstrom K, Westin G, Bark C, Zarielski J, Peterson U (1984) Genes and pseudogenes for human U2 RNA. J Mol Biol 179:157–169

    Article  PubMed  Google Scholar 

  • Harris S, Barrie PA, Weiss ML, Jeffreys AJ (1984) The primate pseudo-beta-1 gene. An ancient beta-globin pseudogene. J Mol Biol 180:785–802

    Google Scholar 

  • Hess JF, Fox M, Schmid C, Shen C-KJ (1983) Molecular evolution of the human adult alpha-globin-like region: insertion and deletion of Alu family repeats and non-Alu DNA sequences. Proc Natl Acad Sci USA 80:5970–5975

    PubMed  Google Scholar 

  • Houck CM, Rinehart FP, Schmid CW (1979) Ubiquitous family of repeated DNA sequences in the human genome. J Mol Biol 132:289–306

    Article  PubMed  Google Scholar 

  • Ito R, Sato K, Helmer T, Jay G, Agarwal K (1984) Structural analysis of the gene encoding human gastrin: The large intron contains an Alu sequence. Proc Natl Acad Sci USA 81:4662–4666

    PubMed  Google Scholar 

  • Jagadeeswaran P, Forget BG, Weissman SM (1981) Short interspersed repetitive DNA elements in eukaryotes: transposable DNA elements generated by reverse transcrption of RNA Pol III transcipts? Cell 26:141–142

    Article  PubMed  Google Scholar 

  • Jeffreys AJ, Wilson V, Thein SL (1985) Hypervariable ‘minisatellite’ regions in human DNA. Nature 314:67–73

    Article  PubMed  Google Scholar 

  • Jelinek WR, Toomey TP, Leinward L, Ducan CH, Biro PA, Choudry PV, Weissman SM, Rubin CM, Houck CM, Deininger PL, Schmid CW (1980) Ubiquitous interspersed repeated sequences in mammalian genomes. Proc Natl Acad Sci USA 77:1398–1402

    PubMed  Google Scholar 

  • Jukes TH, Cantor CR (1969) In: Munro HN (ed) Mammalian protein metabolism III. Academic, New York, pp 21–132

    Google Scholar 

  • Kimura M (1981) Estimation of evolutionary distances between homologous nucleotide sequences. Proc Natl Acad Sci USA 78:454–458

    PubMed  Google Scholar 

  • Krayev AS, Markusheva TV, Kramerov DA, Ryskov AP, Skryabin KG, Bayev AA, Georgiev GP (1982) Ubiquitous transposon-like repeats B1 and B2 of the mouse genome: B1 sequencing. Nucleic Acids Res 10:7461–7475

    PubMed  Google Scholar 

  • Lee MG-S, Lewis SA, Wilde CD, Cowan NJ (1983) Evolutionary history of a multigene family: an expressed human beta-tubulin gene and three processed pseudogenes. Cell 33:477–487

    Article  PubMed  Google Scholar 

  • Lee MG-S, Loomis C, Cowan NJ (1984) Sequence of an expressed human beta-tubulin gene containing ten Alu family members. Nucleic Acids Res 12:5823–5836

    PubMed  Google Scholar 

  • Maeda N, Bliska JB, Smithies O (1983) Recombination and balanced chromosome polymorphism suggested by DNA sequences 5′ to the human δ-globin gene. Proc Natl Acad Sci USA 80:5012–5016

    PubMed  Google Scholar 

  • Martin SL, Vincent KA, Wilson AC (1983) Rise and fall of the delta globin gene. J Mol Biol 164:513–528

    Article  PubMed  Google Scholar 

  • Miyada T, Hayashida H (1981) Extraordinarily high evolutionary rate of pseudogenes: evidence of the presence of selective pressure against changes between synonymous codons. Proc Natl Acad Sci 78:5739–5743

    PubMed  Google Scholar 

  • Miyake T, Migita K, Sakaki Y (1983) Some KpnI family members are associated with the Alu family in the human genome. Nucleic Acids Res 11:6837–6846

    PubMed  Google Scholar 

  • Murphy S, Altruda F, Ullu E, Tripodi M, Silengo L, Melli M (1984) DNA sequences complementary to human 7SK RNA show structural similarities to the short mobile elements of the mammalian genome. J Mol Biol 177:575–590

    Article  PubMed  Google Scholar 

  • Myers JC, Dickson LA, de Wet WJ, Bernard MP, Chu M-L, Di Liberto M, Pepe G, Sangiorgi FO, Ramirez F (1983) Analysis of the 3′ end of the human pro-alpha-2(I) collagen gene. J Biol Chem 258:10128–10135

    PubMed  Google Scholar 

  • Nemer M, Chamberland M, Sirois D, Argentin S, Drouin J, Dixon RAF, Zivin RA, Condra JH (1984) Gene structure of human cardiac hormone precursor, pronatriodilatin. Nature 312:654–656

    Article  PubMed  Google Scholar 

  • Ohta T, Dover GA (1984) The cohesive population genetics of molecular drive. Genetics 108:501–521

    PubMed  Google Scholar 

  • Pan J, Elder JT, Duncan CH, Weissman SM (1981) Structural analysis of interspersed repetitive polymerase III transcription units in human DNA. Nucleic Acids Res 9:1151–1170

    PubMed  Google Scholar 

  • Perez-Stable C, Ayres TM, Shen C-KJ (1984) Distinctive sequence organisation and functional programming of an Alu repeat promoter. Proc Natl Acad Sci USA 81:5291–5295

    PubMed  Google Scholar 

  • Rogers J (1985) Retroposons. Int Rev Cytol 93:187–279

    PubMed  Google Scholar 

  • Sawada I, Beal MP, Shen C-KJ, Chapman B, Wilson AC, Schmid C (1983) Intergenic DNA sequences flanking the pseudo alpha globin genes of human and chimpanzee. Nucleic Acids Res 11:8087–8101

    PubMed  Google Scholar 

  • Sawada I, Willard C, Shen C-KJ, Chapman B, Wilson AC, Schmid CW (1985) Evolution of Alu family repeats since the divergence of human and chimpanzee. J Mol Evol 22:316–322

    PubMed  Google Scholar 

  • Schmid CW, Jelinek WR (1982) The Alu family of dispersed repetitive sequences. Science 216:1065–1070

    PubMed  Google Scholar 

  • Seeburg PH (1982) The growth hormone gene family: Nucleotide sequences show recent divergence and predict a new polypeptide hormone. DNA 1:239–249

    PubMed  Google Scholar 

  • Sharp PA (1983) Conversion of RNA to DNA in mammals: Alu-like elements and pseudogenes. Nature 301:471–472

    Article  PubMed  Google Scholar 

  • Shimada T, Chen M-J, Nienhuis AW (1984) A human dihydrofolate reductase intronless pseudogene with an Alu repetitive sequence: multiple insertions at a single chromosomal site. Gene 31:1–8

    Article  PubMed  Google Scholar 

  • Tajima F (1983) Evolutionary relationships of DNA sequences in finite populations. Genetics 105:437–460

    PubMed  Google Scholar 

  • Tautz D, Renz M (1984) Simple sequences are ubiquitous repetitive components of eukaryotic genomes. Nucleic Acids Res 12:4127–4138

    PubMed  Google Scholar 

  • Tsukada T, Watanabe Y, Nakai Y, Imura H, Nakanashi S, Numa S (1983) Repetitive DNA sequences in the human corticotropin-β-lipotropin precursor gene region: Alu family members. Nucleic Acids Res 10:1471–1479

    Google Scholar 

  • Ullu E, Tschudi C (1984) Alu sequences are processed 7SL RNA genes. Nature 312:171–172

    PubMed  Google Scholar 

  • Wilbur WJ, Lipman DJ (1983) Rapid similarity searches of nucleic acid and protein data bases. Proc Natl Acad Sci USA 80:726–730

    Google Scholar 

  • Willard C, Wong E, Hess JF, Shen C-KJ, Chapman B, Wilson AC, Schmid CW (1985) Comparison of human and chimpanzee zeta-1 globin genes. J Mol Evol 22:309–315

    PubMed  Google Scholar 

  • Yamamoto T, Davis CG, Brown MS, Schneider WJ, Casey ML, Goldstein JL, Russell DW (1984) The human LDL receptor: a cysteine-rich protein with multiple Alu sequences in its mRNA. Cell 39:27–38

    Article  PubMed  Google Scholar 

  • Yang R, Fristensky B, Deutch AH, Huang R-CC, Tan YH, Narang SA, Wu R (1983) The nucleotide sequence of a new human repetitive DNA consists of eight tandem repeats of 66 base pairs. Gene 25:59–66

    Article  PubMed  Google Scholar 

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Bains, W. The multiple origins of human Alu sequences. J Mol Evol 23, 189–199 (1986). https://doi.org/10.1007/BF02115575

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  • DOI: https://doi.org/10.1007/BF02115575

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