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.
Insects telomere telomerase
Telomerase reverse transcriptase (TERT)
Telomeric repeat amplification protocol
Real-time quantitative TRAP
This is a preview of subscription content, log in to check access.
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.
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.
Biessmann H, Zurovcova M, Yao JG et al. (2000) A telomeric satellite in Drosophila virilis and its sibling species. Chromosoma 109:372–380PubMedCrossRefGoogle Scholar
Capkova Frydrychova R, Mason JM, Biessmann H (2009) Regulation of telomere length in Drosophila. Cytogenet Genome Res 122:356–364CrossRefGoogle 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 100:14091–14096PubMedCentralPubMedCrossRefGoogle Scholar
Chan SW, Blackburn EH (2002) New ways not to make ends meet: telomerase, DNA damage proteins and heterochromatin. Oncogene 21:553–563PubMedCrossRefGoogle 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.Google Scholar
Frydrychova R, Marec F (2002) Repeated losses of TTAGG telomere repeats in evolution of beetles (Coleoptera). Genetica 115:179–187PubMedCrossRefGoogle Scholar
Frydrychova R, Grossmann P, Trubac P et al. (2004) Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47:163–178PubMedCrossRefGoogle 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 13:455–467Google Scholar
Gomes NMV, Shay JW, Wright WE (2011) Telomere biology in Metazoa. Fed Eur Biochem Soc 584:3741–3751CrossRefGoogle 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 85:6622–6626PubMedCentralPubMedCrossRefGoogle Scholar
Mravinac B, Meštrović N, Cavrak VV, Plohl M (2011) TCAGG, an alternative telomeric sequence in insects. Chromosoma 120:367–376PubMedCrossRefGoogle 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 15:4545–4552Google Scholar
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 376:281–289PubMedCrossRefGoogle 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 122:380–387PubMedCrossRefGoogle Scholar
Roth CW, Kobeski F, Walter MF, Biessmann H (1997) Chromosome end elongation by recombination in the mosquito Anopheles gambiae. Mol Cell Biol 17:5176–5183PubMedCentralPubMedGoogle Scholar
Sahara K, Marec F, Traut W (1999) TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res 7:449–460PubMedCrossRefGoogle Scholar
Sasaki T, Fujiwara H (2000) Detection and distribution patterns of telomerase activity in insects. Eur J Biochem 267:3025–3031PubMedCrossRefGoogle Scholar
Sýkorová E, Leitch AR, Fajkus J (2006) Asparagales telomerases which synthesize the human type of telomeres. Plant Mol Biol 60:633–646PubMedCrossRefGoogle Scholar
Traut W, Szczepanowski M, Vítková M et al. (2007) The telomere repeat motif of basal Metazoa. Chromosome Res 15:371–382PubMedGoogle Scholar
Vítková M, Král J, Traut W et al. (2005) The evolutionary origin of insect telomeric repeats, (TTAGG)n. Chromosome Res 13:145–156PubMedCrossRefGoogle Scholar
Wege H, Chui MS, Le HT, et al. (2003) SYBR Green real-time telomeric repeat amplification protocol for the rapid quantification of telomerase activityGoogle Scholar
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 93:8983–8988PubMedCentralPubMedCrossRefGoogle Scholar
Wright WE, Piatyszek MA, Rainey WE et al. (1996) Telomerase activity inhuman germline and embryonic tissues and cells. Dev Genet 18:173–179PubMedCrossRefGoogle Scholar