Home LiteratureArticle Details
PMID: 8643651 Published · ppublish English Comparative Study Journal Article

Tiggers and DNA transposon fossils in the human genome.

Smit AF, Riggs AD

Abstract

We report several classes of human interspersed repeats that resemble fossils of DNA transposons, elements that move by excision and reintegration in the genome, whereas previously characterized mammalian repeats all appear to have accumulated by retrotransposition, which involves an RNA intermediate. The human genome contains at least 14 families and > 100,000 degenerate copies of short (180-1200 bp) elements that have 14- to 25-bp terminal inverted repeats and are flanked by either 8 bp or TA target site duplications. We describe two ancient 2.5-kb elements with coding capacity, Tigger1 and -2, that closely resemble pogo, a DNA transposon in Drosophila, and probably were responsible for the distribution of some of the short elements. The deduced pogo and Tigger proteins are related to products of five DNA transposons found in fungi and nematodes, and more distantly, to the Tc1 and mariner transposases. They also are very similar to the major mammalian centromere protein CENP-B, suggesting that this may have a transposase origin. We further identified relatively low-copy-number mariner elements in both human and sheep DNA. These belong to two subfamilies previously identified in insect genomes, suggesting lateral transfer between diverse species.

MeSH Terms
Amino Acid Sequence Animals Autoantigens Base Sequence Caenorhabditis elegans/genetics Centromere Protein B Chromosomal Proteins, Non-Histone/genetics DNA/genetics DNA Nucleotidyltransferases/genetics DNA-Binding Proteins Drosophila melanogaster/genetics Evolution, Molecular Genome, Human Humans Molecular Sequence Data Repetitive Sequences, Nucleic Acid Retroelements/genetics Sequence Alignment Sequence Homology Sheep/genetics Species Specificity Transposases Xenopus/genetics
Chemicals
Autoantigens CENPB protein, human Centromere Protein B Chromosomal Proteins, Non-Histone DNA-Binding Proteins Retroelements DNA DNA Nucleotidyltransferases Transposases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Smit A F
Department of Biology, Beckman Research Institute of the City of Hope, Duarte, CA 91010, USA.
Riggs A D
References (50)
50 references, click to expand
  1. Bacterial transposases and retroviral integrases.
    Mol Microbiol. 1995 Jan;15(1):13-23 PMID: 7752887
  2. Evidence for a common evolutionary origin of inverted repeat transposons in Drosophila and plants: hobo, Activator, and Tam3.
    Cell. 1991 Aug 9;66(3):465-71 PMID: 1651170
  3. Pot2, an inverted repeat transposon from the rice blast fungus Magnaporthe grisea.
    Mol Gen Genet. 1994 Nov 1;245(3):339-48 PMID: 7816044
  4. Profile analysis: detection of distantly related proteins.
    Proc Natl Acad Sci U S A. 1987 Jul;84(13):4355-8 PMID: 3474607
  5. A transposon-like element in human DNA.
    Nature. 1985 Jul 25-31;316(6026):359-61 PMID: 2862587
  6. Identification of a new, abundant superfamily of mammalian LTR-transposons.
    Nucleic Acids Res. 1993 Apr 25;21(8):1863-72 PMID: 8388099
  7. Characterisation of PDC2, a gene necessary for high level expression of pyruvate decarboxylase structural genes in Saccharomyces cerevisiae.
    Mol Gen Genet. 1993 Dec;241(5-6):657-66 PMID: 8264540
  8. Master genes in mammalian repetitive DNA amplification.
    Trends Genet. 1992 Sep;8(9):307-11 PMID: 1365396
  9. A novel group of families of short interspersed repetitive elements (SINEs) in Xenopus: evidence of a specific target site for DNA-mediated transposition of inverted-repeat SINEs.
    J Mol Biol. 1995 May 12;248(4):812-23 PMID: 7752242
  10. The mariner transposable element is widespread in insects.
    Nature. 1993 Mar 18;362(6417):241-5 PMID: 8384700
  11. Structural analysis of the entire proopiomelanocortin gene of Xenopus laevis.
    Eur J Biochem. 1991 Oct 1;201(1):129-37 PMID: 1915355
  12. Dense Alu clustering and a potential new member of the NF kappa B family within a 90 kilobase HLA class III segment.
    Nat Genet. 1993 Feb;3(2):137-45 PMID: 8499947
  13. Tc1 transposase of Caenorhabditis elegans is an endonuclease with a bipartite DNA binding domain.
    EMBO J. 1994 Dec 15;13(24):6125-32 PMID: 7813449
  14. Rapid similarity searches of nucleic acid and protein data banks.
    Proc Natl Acad Sci U S A. 1983 Feb;80(3):726-30 PMID: 6572363
  15. Novel families of interspersed repetitive elements from the human genome.
    Nucleic Acids Res. 1990 Jan 11;18(1):137-41 PMID: 2106661
  16. Identification of a subdomain of CENP-B that is necessary and sufficient for localization to the human centromere.
    J Cell Biol. 1992 Mar;116(5):1081-93 PMID: 1740467
  17. Tourist: a large family of small inverted repeat elements frequently associated with maize genes.
    Plant Cell. 1992 Oct;4(10):1283-94 PMID: 1332797
  18. The pogo transposable element family of Drosophila melanogaster.
    Mol Gen Genet. 1992 Mar;232(1):126-34 PMID: 1313144
  19. DNA binding activities of the Caenorhabditis elegans Tc3 transposase.
    Nucleic Acids Res. 1994 Dec 25;22(25):5548-54 PMID: 7838706
  20. Structure of the human CRFB4 gene: comparison with its IFNAR neighbor.
    J Mol Evol. 1995 Sep;41(3):338-44 PMID: 7563119
  21. Medium reiteration frequency repetitive sequences in the human genome.
    Nucleic Acids Res. 1991 Sep 11;19(17):4731-8 PMID: 1891362
  22. The Tc5 family of transposable elements in Caenorhabditis elegans.
    Genetics. 1994 Jul;137(3):771-81 PMID: 8088523
  23. The Tc2 transposon of Caenorhabditis elegans has the structure of a self-regulated element.
    DNA Cell Biol. 1992 Mar;11(2):111-22 PMID: 1312336
  24. Transpositional recombination: mechanistic insights from studies of mu and other elements.
    Annu Rev Biochem. 1992;61:1011-51 PMID: 1323232
  25. Analysis of protein-DNA and protein-protein interactions of centromere protein B (CENP-B) and properties of the DNA-CENP-B complex in the cell cycle.
    Mol Cell Biol. 1995 Mar;15(3):1602-12 PMID: 7862152
  26. Tc4, a Caenorhabditis elegans transposable element with an unusual fold-back structure.
    Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3334-8 PMID: 1849651
  27. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  28. Ancestral, mammalian-wide subfamilies of LINE-1 repetitive sequences.
    J Mol Biol. 1995 Feb 24;246(3):401-417 PMID: 7877164
  29. Identification and characterization of new human medium reiteration frequency repeats.
    Nucleic Acids Res. 1993 Mar 11;21(5):1273-9 PMID: 8464711
  30. Functional domain structure of human centromere protein B. Implication of the internal and C-terminal self-association domains in centromeric heterochromatin condensation.
    J Biol Chem. 1994 Sep 30;269(39):24271-6 PMID: 7929083
  31. Stowaway: a new family of inverted repeat elements associated with the genes of both monocotyledonous and dicotyledonous plants.
    Plant Cell. 1994 Jun;6(6):907-16 PMID: 8061524
  32. High-frequency P element loss in Drosophila is homolog dependent.
    Cell. 1990 Aug 10;62(3):515-25 PMID: 2165865
  33. A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common "D35E" motif.
    Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):942-6 PMID: 8302872
  34. Detection of Caenorhabditis transposon homologs in diverse organisms.
    New Biol. 1992 Apr;4(4):382-8 PMID: 1320399
  35. The structure of hobo transposable elements and their insertion sites.
    EMBO J. 1986 Dec 20;5(13):3615-23 PMID: 16453744
  36. Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome.
    Cell. 1983 Aug;34(1):25-35 PMID: 6309410
  37. Fot1, a new family of fungal transposable elements.
    Mol Gen Genet. 1992 Mar;232(1):12-6 PMID: 1313143
  38. A variant Tc4 transposable element in the nematode C. elegans could encode a novel protein.
    Nucleic Acids Res. 1993 Jan 11;21(1):59-67 PMID: 8382791
  39. Mariner transposons in humans.
    Nature. 1995 Dec 14;378(6558):672 PMID: 7501013
  40. CENP-B is a highly conserved mammalian centromere protein with homology to the helix-loop-helix family of proteins.
    Chromosoma. 1991 Jul;100(6):360-70 PMID: 1893793
  41. Molecular cloning of cDNA for CENP-B, the major human centromere autoantigen.
    J Cell Biol. 1987 Apr;104(4):817-29 PMID: 2435739
  42. Molecular analysis of Ac transposition and DNA replication.
    Genetics. 1992 Mar;130(3):665-76 PMID: 1312981
  43. Human and other mammalian genomes contain transposons of the mariner family.
    FEBS Lett. 1995 Jul 24;368(3):541-6 PMID: 7635217
  44. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  45. The Hermes transposable element from the house fly, Musca domestica, is a short inverted repeat-type element of the hobo, Ac, and Tam3 (hAT) element family.
    Genet Res. 1994 Oct;64(2):87-97 PMID: 7813905
  46. Transcription of the MRP RNA gene in frog stage I oocytes requires a novel cis-element.
    Biochem Biophys Res Commun. 1994 Jul 15;202(1):225-33 PMID: 7518675
  47. Widespread occurrence of the Tc1 transposon family: Tc1-like transposons from teleost fish.
    Mol Gen Genet. 1994 Sep 28;244(6):606-12 PMID: 7969029
  48. The mechanism of transposition of Tc3 in C. elegans.
    Cell. 1994 Oct 21;79(2):293-301 PMID: 7954797
  49. MIRs are classic, tRNA-derived SINEs that amplified before the mammalian radiation.
    Nucleic Acids Res. 1995 Jan 11;23(1):98-102 PMID: 7870595
  50. 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans.
    Nature. 1994 Mar 3;368(6466):32-8 PMID: 7906398
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1996-02-20
Pages
1443-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC39958
Subset
IM
Databases
GENBANK
U49973
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]