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Distribution of TTAGG-specific telomerase activity in insects

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Abstract

In most eukaryotes, telomeres consist of tandem arrays of a short repetitive DNA sequence. Insect telomeres are generally constituted by a (TTAGG)n repeat motif. Usually, telomeres are maintained by telomerase, a specialized reverse transcriptase that adds this sequence to chromosome ends. We examined telomerase activity in 15 species across Insecta. Telomerase activity was revealed in Isoptera, Blattaria, Lepidoptera, Hymenoptera, Trichoptera, Coleoptera, and Sternorrhyncha. In contrast, we were not able to detect telomerase activity in Orthoptera, Zygentoma, and Phasmida. Because we found telomerase activity in phylogenetically distant species, we conclude that a distribution pattern of (TTAGG)n sequence in Insecta is generally consistent with that of telomerase activity. Thus, the TTAGG-telomerase system is functional across the Insecta. Using real-time quantitative telomeric repeat amplification protocol (RTQ-TRAP) system, we quantified telomerase activity in different developmental stages and different tissues of a cockroach, Periplaneta americana. We show that telomerase is upregulated in young instars and gradually declines during development. In adults, it is most active in testes and ovaries. Thus, the telomerase activity of hemimetabolous insects seems to be associated with cell proliferation and organismal development.

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Abbreviations

TERT:

Telomerase reverse transcriptase (TERT)

TRAP:

Telomeric repeat amplification protocol

RTQ-TRAP:

Real-time quantitative TRAP

References

  • Biessmann H, Zurovcova M, Yao JG et al. (2000) A telomeric satellite in Drosophila virilis and its sibling species. Chromosoma 109:372–380

    Article  CAS  PubMed  Google Scholar 

  • Capkova Frydrychova R, Mason JM, Biessmann H (2009) Regulation of telomere length in Drosophila. Cytogenet Genome Res 122:356–364

    Article  Google Scholar 

  • Casacuberta E, Pardue M-L (2003) HeT-A elements in Drosophila virilis: retrotransposon telomeres are conserved across the Drosophila genus. Proc Natl Acad Sci U S A 100:14091–14096

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chan SW, Blackburn EH (2002) New ways not to make ends meet: telomerase, DNA damage proteins and heterochromatin. Oncogene 21:553–563

    Article  CAS  PubMed  Google Scholar 

  • Cong Y, Wright WE, Shay JW (2002) Human telomerase and its regulation. Microbiol Mol Biol Rev 66:407–425

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Coviello-McLaughlin GM, Prowse KR (1997) Telomere length regulation during postnatal development and ageing in Mus spretus. Nucleic Acids Res 25:3051–3058

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Delany ME, Krupkin AB, Miller MM (2000) Organization of telomere sequences in birds: evidence for arrays of extreme length and for in vivo shortening. Cytogenet Genome Res 90(1-2):139-45.

  • Frydrychova R, Marec F (2002) Repeated losses of TTAGG telomere repeats in evolution of beetles (Coleoptera). Genetica 115:179–187

    Article  CAS  PubMed  Google Scholar 

  • Frydrychova R, Grossmann P, Trubac P et al. (2004) Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47:163–178

    Article  CAS  PubMed  Google Scholar 

  • Fujiwara H, Osanai M, Matsumoto T, Kojima KK (2005) Telomere-specific non-LTR retrotransposons and telomere maintenance in the silkworm, Bombyx mori. Chromosom Res 13:455–467

  • Gomes NMV, Shay JW, Wright WE (2011) Telomere biology in Metazoa. Fed Eur Biochem Soc 584:3741–3751

    Article  Google Scholar 

  • Greider CW (1996) Telomere length regulation. Annu Rev Biochem 65:337–365

    Article  CAS  PubMed  Google Scholar 

  • Klapper W, Kühne K, Singh KK et al. (1998) Longevity of lobsters is linked to ubiquitous telomerase expression. FEBS Lett 439:143–146

    Article  CAS  PubMed  Google Scholar 

  • 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

  • Mason JM, Frydrychova RC, Biessmann H (2008) Drosophila telomeres: an exception providing new insights. Bioessays 30:25–37

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Meyne J, Ratliff RL, Moyzis RK (1989) Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc Natl Acad Sci U S A 86:7049–7053

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Moyzis RK, Buckingham JM, Cram LS et al. (1988) A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc Natl Acad Sci U S A 85:6622–6626

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mravinac B, Meštrović N, Cavrak VV, Plohl M (2011) TCAGG, an alternative telomeric sequence in insects. Chromosoma 120:367–376

    Article  CAS  PubMed  Google Scholar 

  • 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

  • Osanai M, Kojima KK, Futahashi R et al (2006) Identification and characterization of the telomerase reverse transcriptase of Bombyx mori (silkworm) and Tribolium castaneum (flour beetle). Gene 376:281–289

    Article  CAS  PubMed  Google Scholar 

  • Peška V, Sykorova E, Fajkus J (2008) Two faces of Solanaceae telomeres: a comparison between Nicotiana and Cestrum telomeres and telomere-binding proteins. Cytogenet Genome Res 122:380–387

    Article  PubMed  Google Scholar 

  • Prowse KR, Greider CW (1995) Developmental and tissue-specific regulation of mouse telomerase and telomere length. Proc Natl Acad Sci U S A 92:4818–4822

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Riha K, Fajkus J, Siroky J, Vyskot B (1998) Developmental control of telomere lengths and telomerase activity in plants. Plant Cell 10:1691–1698

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sahara K, Marec F, Traut W (1999) TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res 7:449–460

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Fujiwara H (2000) Detection and distribution patterns of telomerase activity in insects. Eur J Biochem 267:3025–3031

    Article  CAS  PubMed  Google Scholar 

  • Sýkorová E, Leitch AR, Fajkus J (2006) Asparagales telomerases which synthesize the human type of telomeres. Plant Mol Biol 60:633–646

    Article  PubMed  Google Scholar 

  • Traut W, Szczepanowski M, Vítková M et al. (2007) The telomere repeat motif of basal Metazoa. Chromosome Res 15:371–382

    CAS  PubMed  Google Scholar 

  • Vítková M, Král J, Traut W et al. (2005) The evolutionary origin of insect telomeric repeats, (TTAGG)n. Chromosome Res 13:145–156

    Article  PubMed  Google Scholar 

  • Wege H, Chui MS, Le HT, et al. (2003) SYBR Green real-time telomeric repeat amplification protocol for the rapid quantification of telomerase activity

  • Wicky C, Villeneuve AM, Lauper N et al. (1996) Telomeric repeats (TTAGGC)n are sufficient for chromosome capping function in Caenorhabditis elegans. Proc Natl Acad Sci U S A 93:8983–8988

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wright WE, Piatyszek MA, Rainey WE et al. (1996) Telomerase activity inhuman germline and embryonic tissues and cells. Dev Genet 18:173–179

    Article  CAS  PubMed  Google Scholar 

  • Wyatt HDM, West SC, Beattie TL (2010) InTERTpreting telomerase structure and function. Nucleic Acids Res 38:5609–5622

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhou J, Ding D, Wang M, Cong Y-S (2014) Telomerase reverse transcriptase in the regulation of gene expression. BMB Rep 47:8–14

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We are grateful to James Mason for critical review of the manuscript, Aleš Bezděk, Jan Šobotník, Petr Doležal, and David Boukal, who provided us with live materials. This work was supported by the Grant No. 14-07172S from the Grant Agency of the Czech Republic. We acknowledge the use of research infrastructure that has received funding from the European Union Seventh Framework Programme (FP7/2007-2013) under grant agreement No. 316304. Additional support was provided from Grant 052/2013/P of the Grant Agency of the University of South Bohemia.

Ethical standards

The authors declare that all experiments performed in this study comply with the current laws of the Czech Republic. All institutional and national guidelines for the care and use of laboratory animals were followed.

Conflict of interest

Michala Korandová, Tomáš Krůček, Kristýna Vrbová, and Radmila Čapková Frydrychová declare that they have no conflict of interest.

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Correspondence to Radmila Čapková Frydrychová.

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Korandová, M., Krůček, T., Vrbová, K. et al. Distribution of TTAGG-specific telomerase activity in insects. Chromosome Res 22, 495–503 (2014). https://doi.org/10.1007/s10577-014-9436-6

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  • DOI: https://doi.org/10.1007/s10577-014-9436-6

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