Chromosome Research

, Volume 13, Issue 5, pp 455–467 | Cite as

Telomere-specific non-LTR retrotransposons and telomere maintenance in the silkworm, Bombyx mori

  • Haruhiko Fujiwara
  • Mizuko Osanai
  • Takumi Matsumoto
  • Kenji K. Kojima
Article

Abstract

Most insects have telomeres that consist of pentanucleotide (TTAGG) telomeric repeats, which are synthesized by telomerase. However, all species in Diptera so far examined and several species in other orders of insect have lost the (TTAGG)n repeats, suggesting that some of them recruit telomerase-independent telomere maintenance. The silkworm, Bombyx mori, retains the TTAGG motifs in the chromosomal ends but expresses quite a low level of telomerase activity in all stages of various tissues. Just proximal to a 6–8-kb stretch of the TTAGG repeats in B. mori, more than 1000 copies of non-LTR retrotransposons, designated TRAS and SART families, occur among the telomeric repeats and accumulate. TRAS and SART are abundantly transcribed and actively retrotransposed into TTAGG telomeric repeats in a highly sequence-specific manner. They have three possible mechanisms to ensure specific integration into the telomeric repeats. This article focuses on the telomere structure and telomere-specific non-LTR retrotransposons in B. mori and discusses the mechanisms for telomere maintenance in this insect.

Key words

Bombyx mori insect telomerase telomere telomere-specific non-LTR retrotransposon 

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References

  1. Abad JP, De Pablos B, Osoegawa K, De Jong PJ, Martin-Gallardo A, Villasante A (2004) TAHRE, a novel telomeric retrotransposon from Drosophila melanogaster, reveals the origin of Drosophila telomeres. Mol Biol Evol 21: 1620–1624.CrossRefPubMedGoogle Scholar
  2. Anzai T, Takahashi H, Fujiwara H (2001) Sequence-specific recognition and cleavage of telomeric repeat (TTAGG)n by endonuclease of non-long terminal repeat retrotransposon TRAS1. Mol Cell Biol 21: 100–108.CrossRefPubMedGoogle Scholar
  3. Anzai T, Osanai M, Hamada M, Fujiwara H (2005) Functional roles of read-through 28S rRNA sequence in in vivo retrotransposition of non-LTR retrotransposon, R1Bm. Nucl Acids Res 33: 1993–2002.Google Scholar
  4. Biessmann H, Mason JM (2003) Telomerase-independent mechanisms of telomere elongation. Cell Mol Life Sci 60: 2325–2333.CrossRefPubMedGoogle Scholar
  5. Blackburn EH (1991) Structure and function of telomeres. Nature 350: 569–573.CrossRefPubMedGoogle Scholar
  6. Casacuberta E, Pardue ML (2003a) Transposon telomeres are widely distributed in the Drosophila genus: TART elements in the virilis group. Proc Natl Acad Sci USA 100: 3363–3368.PubMedGoogle Scholar
  7. Casacuberta E, Pardue ML (2003b) HeT-A elements in Drosophila virilis: Retrotransposon telomeres are conserved across the Drosophila genus. Proc Natl Acad Sci USA 100: 14091–14096.CrossRefPubMedGoogle Scholar
  8. Chambeyron S, Bucheton A, Busseau I (2002) Tandem UAA repeats at the 3′-end of the transcript are essential for the precise initiation of reverse transcription of the I factor in Drosophila melanogaster. J Biol Chem 277: 17877–17882.CrossRefPubMedGoogle Scholar
  9. Christensen S, Pont-Kingdon G, Carroll D (2000) Target specificity of the endonuclease from the Xenopus laevis non-long terminal repeat retrotransposon Tx1L. Mol Cell Biol 20: 1219–1226.CrossRefPubMedGoogle Scholar
  10. Cohn M, Edstrom JE (1992) Telomere-associated repeats in Chironomus form discrete subfamilies generated by gene conversion. J Mol Evol 35: 114–122.CrossRefPubMedGoogle Scholar
  11. Eickbush TH (1997) Telomerase and retrotransposons: which came first? Science 277: 911–912.CrossRefPubMedGoogle Scholar
  12. Feng Q, Schumann G, Boeke JD (1998) Retrotransposon R1Bm endonuclease cleaves the target sequence. Proc Natl Acad Sci USA 95: 2083–2088.CrossRefPubMedGoogle Scholar
  13. Frydrychoba R, Grossman P, Trubac P, Vitkova M, Marec F (2004) Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47: 163–178.CrossRefGoogle Scholar
  14. Fujiwara H, Ninaki O, Kobayashi M, Kusuda J, Maekawa H (1991) Chromosomal fragment responsible for genetic mosaicism in larval body marking of the silkworm, Bombyx mori. Genet Res 57: 11–16.Google Scholar
  15. Fujiwara H, Yanagawa M, Ishikawa H (1994) Mosaic formation by developmental loss of a chromosomal fragment in a “mottled striped” mosaic strain of the silkworm, Bombyx mori. Roux’s Arch Dev Biol 203: 389–396.CrossRefGoogle Scholar
  16. Fujiwara H, Nakazato Y, Okazaki S, Ninaki O (2000) Stability and telomere structure of chromosomal fragments in two different mosaic strains of the silkworm, Bombyx mori. Zool Sci 17: 743–750.CrossRefGoogle Scholar
  17. Frydrychova R, Marec F (2002) Repeated losses of TTAGG telomere repeats in evolution of beetles (Coleoptera). Genetica 115: 179–187.PubMedGoogle Scholar
  18. Kahn T, Savitsky M, Georgiev P (2000) Attachment of HeT-A sequences to chromosomal termini in Drosophila melanogaster may occur by different mechanisms. Mol Cell Biol 20: 7634–7642.CrossRefPubMedGoogle Scholar
  19. Kajikawa M, Okada N (2002) LINEs mobilize SINEs in the eel through a shared 3′ sequence. Cell 111: 433–444.CrossRefPubMedGoogle Scholar
  20. Klapper W, Kuhne K, Singh KK et al. (1998) Longevity of lobsters is linked to ubiquitous telomerase expression. FEBS Lett 439: 143–146.CrossRefPubMedGoogle Scholar
  21. Kojima KK, Fujiwara H (2003) Evolution of target specificity in R1 clade non-LTR retrotransposons. Mol Biol Evol 20: 351–361.CrossRefPubMedGoogle Scholar
  22. Kojima KK, Fujiwara H (2004) Cross-genome screening of novel sequence-specific non-LTR retrotransposons: various multicopy RNA genes and microsatellites are selected as targets. Mol Biol Evol 21: 207–217.CrossRefPubMedGoogle Scholar
  23. Kojima KK, Matsumoto T, Fujiwara H (2005) Eukaryotic translational coupling in UAAUG stop-start codons for the bicistronic RNA translation of non-LTR retrotransposon SART1. Mol Cell Biol (in press).Google Scholar
  24. Kubo Y, Okazaki S, Anzai T, Fujiwara H (2001) Structural and phylogenetic analysis of TRAS, telomeric repeat-specific non-LTR retrotransposon families in Lepidopteran insects. Mol Biol Evol 18: 848–857.PubMedGoogle Scholar
  25. Lamb J, Jarris PC, Wilkie AOM et al. (1993) De novo truncation of chromosome 16p and healing with (TTAGGG)n in the alpha thalassaemia/mental retardation syndorome (ATR-16). Am J Hum Genet 52: 668–676.PubMedGoogle Scholar
  26. Luan DD, Korman MH, Jakubuczak JL, Eickbush TH (1995) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72: 595–605.CrossRefGoogle Scholar
  27. Lundblad V, Wright WE (1996) Telomeres and telomerase: a simple picture becomes complex. Cell 87: 369–375.PubMedGoogle Scholar
  28. Maita N, Anzai T, Aoyagi H, Mizuno H, Fujiwara H (2004) Crystal structure of the endonuclease domain encoded by the telomere-specific long interspersed nuclear element, TRAS1. J Biol Chem 24: 41067–41076.CrossRefGoogle Scholar
  29. Malik HS, Burke WD, Eickbush TH (1999) The age and evolution of non-LTR retrotransposable elements. Mol Biol Evol 16: 793–805.PubMedGoogle Scholar
  30. Malik HS, Burke WD, Eickbush TH (2000) Putative telomerase catalytic subunits from Giardia lamblia and Caenorhabditis elegans. Gene 251: 101–108.CrossRefPubMedGoogle Scholar
  31. Mandrioli M (2002) Cytogenetic characterization of telomeres in the holocentric chromosomes of the lepidopteran Mamestra brassicae. Chromosome Res 10: 279–286.CrossRefGoogle Scholar
  32. Matsumoto T, Takahashi H, Fujiwara H (2004) Targeted nuclear import of open reading frame 1 is required for in vivo retrotransposition of a telomere-specific non-long terminal repeat retrotransposn, SART1. Mol Cell Biol 24: 105–122.CrossRefPubMedGoogle Scholar
  33. Mita K, Kasahara M, Sasaki S et al. (2004) The genome sequence of silkworm, Bombyx mori. DNA Res 11: 27–35.PubMedGoogle Scholar
  34. Moore LL, Stanvitch G, Roth MB, Rosen D (2005) HCP-4/CENP-C promotes the prophase timing of centromere resolution by enabling the centromere association of HCP-6 in Caenorhabditis elegans. Mol Cell Biol 25: 2583–2592.CrossRefPubMedGoogle Scholar
  35. Moran JV, Holmes SE, Naas TP et al. (1996) High frequency retrotransposition in cultured mammalian cells. Cell 87: 917– 927.CrossRefPubMedGoogle Scholar
  36. Muller F, Wicky C, Spicher A, Tobler H (1991) New telomere formation after developmentally regulated chromosomal breakage during the process of chromatin diminution in Ascaris lumbricoides. Cell 67: 815–822.CrossRefPubMedGoogle Scholar
  37. Murakami A, Imai HT (1974) Cytological evidence for holocentric chromosomes of the silkworm, Bombyx mori and B. mandarina, (Bombycidae, Lepidoptera). Chromosoma 80: 167–178.CrossRefGoogle Scholar
  38. Nakamura TM, Morin GB, Chapman KB et al. (1997) Telomerase catalytic subunit homologs from fission yeast and human. Science 277: 955–959.CrossRefPubMedGoogle Scholar
  39. Nielsen L, Schmidt ER, Edstrom JE (1990) Subrepeats result from regional DNA sequence conservation in tandem repeats in Chironomus telomeres. J Mol Biol 216: 577–584.CrossRefPubMedGoogle Scholar
  40. Nokkala S, Kuznetsova VG, Maryanska-Nadachowska A, Nokkala C (2004) Holocentric chromosomes in meiosis. I. Restriction of the number of chiasmata in bivalents. Chromosome Res 12: 733–739.CrossRefGoogle Scholar
  41. Okazaki S, Tsuchida K, Maekawa H, Ishikawa H, Fujiwara H (1993) Identification of a pentanucleotide telomeric sequence, (TTAGG)n, in the silkworm Bombyx mori and in other insects. Mol Cell Biol 13: 1424–1432.Google Scholar
  42. Okazaki S, Ishikawa H, Fujiwara, H (1995) Structural analysis of TRAS1, a novel family of telomeric repeat-associated retrotransposons in the silkworm, Bombyx mori. Mol Cell Biol 15: 4545–4552.PubMedGoogle Scholar
  43. Osanai M, Takahashi H, Kojima KK, Hamada M, Fujiwara H (2004) Essential motifs in the 3′ untranslated region required for retrotransposition and the precise start of the reverse transcription in non-long-terminal-repeat retrotransposon SART1. Mol Cell Biol 24: 7902–7913.CrossRefPubMedGoogle Scholar
  44. Pardue ML, DeBaryshe PG (1999) Telomeres and telomerase: more than the end of the line. Chromosoma 108: 73–82.CrossRefPubMedGoogle Scholar
  45. Pardue M-L, Rashkova S, Casacuberta E, DeBaryshe PG, George JA, Traverse KL (2005) Two retrotransposons maintain telomeres in Drosophila. Chromosome Research 13: 443–453.Google Scholar
  46. Rashkova S, Karam SE, Kellum R, Pardue ML (2002) Gag proteins of the two Drosophila telomeric retrotransposons are targeted to chromosome ends. J Cell Biol 159: 397–402.CrossRefPubMedGoogle Scholar
  47. Rashkova S, Athanasiadis A, Pardue ML (2003) Intracellular targeting of Gag proteins of the Drosophila telomeric retrotransposons. J Virol 77: 6376–6384.CrossRefPubMedGoogle Scholar
  48. Robin S, Chambeyron S, Brun C, Bucheton A, Busseau I (2002) Trans-complementation of an endonuclease-defective tagged I element as a tool for the study of retrotransposition in Drosophila melanogaster. Mol Genet Genomics 267: 829–834.CrossRefPubMedGoogle Scholar
  49. Roth CW, Kobeski F, Walter MF, Biessmann H (1997) Chromosome end elongation by recombination in the mosquito Anopheles gambiae. Mol Cell Biol 17: 5176–5183.PubMedGoogle Scholar
  50. Sahara K, Marec F, Traut W (1999) TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res 7: 449–460.CrossRefGoogle Scholar
  51. Sasaki T, Fujiwara H (2000) Detection and distribution patterns of telomerase activity in insects. Eur J Biochem 267: 3025–3031.PubMedGoogle Scholar
  52. Takahashi H, Fujiwara H (1999) Transcription analysis of the telomeric repeat-specific retrotransposons TRAS1 and SART1 of the silkworm Bombyx mori. Nucleic Acids Res 27: 2015–2021.CrossRefPubMedGoogle Scholar
  53. Takahashi H, Fujiwara H (2002) Transplantation of target site specificity by swapping the endonuclease domains of two LINEs. EMBO J 21: 408–417.CrossRefPubMedGoogle Scholar
  54. Takahashi H, Okazaki S, Fujiwara, H (1997) A new family of site-specific retrotransposons, SART1, is inserted into telomeric repeats of the silkworm, Bombyx mori. Nucleic Acids Res 25: 1578–1584.CrossRefPubMedGoogle Scholar
  55. Xia Q, Zhou Z, Lu C et al. (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306: 1937–1940.CrossRefPubMedGoogle Scholar
  56. Xiong Y, Eickbush TH (1988) The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons. Mol Cell Biol 8: 114–123.PubMedGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Haruhiko Fujiwara
    • 1
  • Mizuko Osanai
    • 1
  • Takumi Matsumoto
    • 1
  • Kenji K. Kojima
    • 1
  1. 1.Department of Integrated Biosciences, Graduate School of Frontier SciencesUniversity of TokyoKashiwaJapan

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