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Characterization of TTAGG telomeric repeats, their interstitial occurrence and constitutively active telomerase in the mealybug Planococcus lilacinus (Homoptera; Coccoidea)

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Abstract

We confirmed the occurrence of the insect TTAGG telomeric repeats in the mealybug Planococcus lilacinus, a radiation-resistant coccid, by single primer polymerase chain reaction (PCR) and Southern hybridization. Analysis of Bal31 nuclease-digested DNA by Southern hybridization and chromosomes by FISH suggests that these repeats occur mainly at the ends of the chromosomes. However, sequence analysis of the PCR products of TTAGG-associated sequences from genomic DNA showed their interstitial occurrence and association with certain unrelated low-copy repeats. Because of their shorter length, the interstitial TTAGG sequences were detectable by primed in situ hybridizations but not by FISH. Analysis of chromosomes recovered after irradiation by fluorescent in situ hybridization suggested acquisition of TTAGG repeats at a majority of the healed ends. We also observed mild telomerase activity in unirradiated insects which was further enhanced after irradiation. Taken together, these results suggest that the mealybug has an efficient mechanism of formation of TTAGG repeats at radiation-induced chromosome ends and constitutively active telomerase may be a feature associated with rapid recovery of chromosome ends damaged by ionizing radiation.

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References

  • Ahmed S, Hodgkin J (2000) MTR-2 check point protein is required for germline immortality and telomere replication in C. elegans. Nature 403:159–164

    Article  PubMed  CAS  Google Scholar 

  • Azzalin CM, Nergadze SG, Giulotto E (2001) Human intrachromosomal telomeric-like repeats: sequence organization and mechanisms of origin. Chromosoma 110:75–82

    Article  PubMed  CAS  Google Scholar 

  • Biessmann H, Champion LE, O’Hair M, Ikenaga K, Kasravi B, Mason JM (1992) Frequent transpositions of Drosophila melanogaster HeT-A transposable elements to receding chromosome ends. EMBO J 11:4459–4469

    PubMed  CAS  Google Scholar 

  • Blackburn E (1991) Structure and function of telomeres. Nature 350:569–573

    Article  PubMed  CAS  Google Scholar 

  • Boulton SJ, Jackson SP (1998) Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J 17:1819–1828

    Article  PubMed  CAS  Google Scholar 

  • Bryan TM, Englezou A, Gupta J, Bacchetti S, Reddel RR (1995) Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J 14:4240–4248

    PubMed  CAS  Google Scholar 

  • Cesare AJ, Reddel RR (2010) Alternative lengthening of telomeres: models, mechanisms and implications. Nat Rev Genet 11:319–330

    Article  PubMed  CAS  Google Scholar 

  • Chandra HS (1963a) Cytogenetic analysis following high dosage paternal irradiation in the mealybug Planococcus citri. I. Cytology of X1 embryos. Chromosoma 14:310–329

    Article  Google Scholar 

  • Chandra HS (1963b) Cytogenetic analysis following high dosage paternal irradiation in the mealybug Planococcus citri. II. Cytology of X1 females and the problem of lecanoid sex determination. Chromosoma 14:330–346

    Article  Google Scholar 

  • Chomczynski P (1992) One-hour downward alkaline capillary transfer for blotting of DNA and RNA. Anal Biochem 201:134–139

    Article  PubMed  CAS  Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci U SA 81:1991–1995

    Article  CAS  Google Scholar 

  • Crompton NE (1997) Telomeres, senescence and cellular radiation response. Cell Mol Life Sci 53:568–575

    Article  PubMed  CAS  Google Scholar 

  • D’Aiuto L, de las Heras JI, Ross A, Shen MH, Cooke H (2003) Generation of a telomere-based episomal vector. Biotechnol Prog 2003(19):1775–1780

    Article  Google Scholar 

  • deLange T (1992) Human telomeres are attached to the nuclear matrix. EMBO J 11:717–724

    CAS  Google Scholar 

  • deLange T (2005) Sheltrin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19:2100–2110

    Article  CAS  Google Scholar 

  • Dunham MA, Neumann AA, Fasching CL, Reddel RR (2000) Telomere maintenance by recombination in human cells. Nat Genet 26:447–450

    Article  PubMed  CAS  Google Scholar 

  • Frydrychová R, Grossmann P, Trubac P, Vítková M, Marec F (2004) Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47:163–178

    Article  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. Chromosome Res 13:455–467

    Article  PubMed  CAS  Google Scholar 

  • Genesca A, Martin M, Latre L, Soler D, Pampalona J, Tusell L (2006) Telomere dysfunction: a new player in radiation sensitivity. Bioessays 26:1172–1180

    Article  Google Scholar 

  • Goytisolo F, Samper E, Cabellero J, Finnon P, Herrera E, Flores JM, Bouffler D, Blasco MA (2000) Short telomeres result in organismal hypersensitivity to ionizing radiation in mammals. J Exp Med 11:1625–1636

    Article  Google Scholar 

  • Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, de Lange T (1999) Mammalian telomeres end in a large duplex loop. Cell 97:503–514

    Article  PubMed  CAS  Google Scholar 

  • Haber JE (1998) The many interphases of Mre11. Cell 97:829–832

    Article  Google Scholar 

  • Hande MP, Balajee AS, Tchirkov A, Wynshaw-Boris A, Lansdorp PM (2001) Extra-chromosomal telomeric DNA in cells from Atm(−/−) mice and patients with ataxia-telangiectasia. Hum Mol Genet 10:519–528

    Article  PubMed  CAS  Google Scholar 

  • Hastie ND, Allshire RC (1989) Human telomeres: fusion and interstitial sites. Trends Genet 10:326–331

    Article  Google Scholar 

  • Jiang WQ, Zhong ZH, Henson JD, Neumann AA, Chang AC, Reddel RR (2005) Suppression of alternative lengthening of telomeres by Sp100-mediated sequestration of the MRE11/RAD50/NBS1 complex. Mol Cell Biol 25(7):2708–2721

    Article  PubMed  CAS  Google Scholar 

  • Jönsson F, Postberg J, Schaffitzel C, Lipps HJ (2002) Organization of the macronuclear gene-sized pieces of stichotrichous ciliates into a higher order structure via telomere–matrix interactions. Chromosome Res 10:445–453

    Article  PubMed  Google Scholar 

  • Kojima KK, Kubo Y, Fujiwara H (2002) Complex and tandem repeat structure of subtelomeric regions in the Taiwan cricket, Teleogryllus taiwanemma. J Mol Evol 54:474–485

    Article  PubMed  CAS  Google Scholar 

  • Levis RW, Ganesan R, Houtchens K, Tolar LA, Sheen FM (1993) Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75:1083–1093

    Article  PubMed  CAS  Google Scholar 

  • Lopez CC, Nielsen L, Edstrom JE (1996) Terminal long tandem repeats in chromosomes from Chironomus pallidivittatus. Mol Cell Biol 16:3285–3290

    PubMed  CAS  Google Scholar 

  • Lundblad V, Blackburn EH (1993) An alternative pathway for yeast telomere maintenance rescues est1− senescence. Cell 73:347–360

    Article  PubMed  CAS  Google Scholar 

  • Martin SG, Laroche T, Suka N, Grunstein M, Gasser SM (1999) Relocation of telomeric Ku and SIR proteins in response to DNA double-strand breaks. Cell 97:621–633

    Article  PubMed  CAS  Google Scholar 

  • Mason JM, Beissmann H (1995) The unusual telomeres of Drosophila. Trends Genet 11:58–62

    Article  PubMed  CAS  Google Scholar 

  • McClintock B (1938) The production of homozygous deficient tissues with mutant characteristics by means of the aberrant mitotic behavior of ring-shaped chromosomes. Genetics 23:315–376

    PubMed  CAS  Google Scholar 

  • Mills KD, Sinclair DA, Guarente L (1999) MEC1-dependent redistribution of the Sir3 silencing protein from telomeres to DNA double-strand breaks. Cell 97:608–620

    Article  Google Scholar 

  • Mohan KN, Ray P, Chandra HS (2002) Characterization of the genome of the mealybug Planococcus lilacinus, a model organism for studying whole-chromosome imprinting and inactivation. Genet Res 79:111–118

    Article  PubMed  CAS  Google Scholar 

  • Murnane JP, Sabatier L, Marder BA, Morgan WF (1994) Telomere dynamics in an immortal human cell line. EMBO J 13:4953–4962

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pardue ML, DeBaryshe PG (1999) Telomeres and telomerase: more than the end of the line. Chromosoma 108:73–82

    Article  PubMed  CAS  Google Scholar 

  • Potts PR, Yu H (2007) The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat Struct Mol Biol 14:581–590

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Herrera A, Garcia F, Giulotto E, Attolini C, Egozcue J et al (2005) Evolutionary breakpoints are co-localized with fragile sites and intrachromosomal telomeric sequences in primates. Cytogenet Genome Res 108:234–247

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Slijepcevic P, Al-Wahiby S (2005) Telomere biology: integrating chromosomal end protection with DNA damage response. Chromosoma 114:275–285

    Article  PubMed  CAS  Google Scholar 

  • Vamvakas S, Vock EH, Lutz VK (1997) On the role of double-strand breaks in toxicity and carcinogenesis. Crit Rev Toxicol 27:155–174

    Article  PubMed  CAS  Google Scholar 

  • Villasante A, de Pablos B, Mendez-lago M, Abad JP (2008) Telomere maintenance in Drosophila. Cell Cycle 7:2134–2138

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Wilkie AO, Lamb J, Harris PC, Finney RD, Higgs DR (1990) A truncated human chromosome 16 associated with alpha thalassaemia is stabilized by addition of telomeric repeat (TTAGGG)n. Nature 346:868–871

    Article  PubMed  CAS  Google Scholar 

  • Zhong ZH, Jiang WQ, Cesare AJ, Neumann AA, Wadhwa R, Reddel RR (2007) Disruption of telomere maintenance by depletion of the MRE11/RAD50/NBS1 complex in cells that use alternative lengthening of telomeres. J Biol Chem 282:29314–29322

    Article  PubMed  CAS  Google Scholar 

  • Zhu X, Kuster B, Mann M, Petrini JHJ, Lange T (2000) Cell cycle regulated association of RAD50/MRE11/NBS1 and TRF2 at telomeres. Nat Genet 25:347–351

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank the reviewers for their insightful comments, H. Sharat Chandra and Leonardo D’Aiuto for discussions, and Anuranjan Anand for providing the isotope facility. Irradiation experiments were done at the Indian Institute of Science with the help of Dr. Manjunath, Department of Biochemistry. This work is supported by a grant from the Department of Biotechnology (KNM). KNM thanks the Centre for Human Genetics for supporting the initial phase of the work and the Institute of Biotechnology and Applied Biotechnology for extending their research facilities.

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  1. Centre for Human Genetics, Biotech Park, Next to Aravind Mills, Bangalore, 560100, India

    Kommu Naga Mohan, B. Sandya Rani, Pooja Swaroop Kulashreshta & Jayarama S. Kadandale

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  1. Kommu Naga Mohan
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  2. B. Sandya Rani
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Correspondence to Kommu Naga Mohan.

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Communicated by R. Allshire

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Mohan, K.N., Rani, B.S., Kulashreshta, P.S. et al. Characterization of TTAGG telomeric repeats, their interstitial occurrence and constitutively active telomerase in the mealybug Planococcus lilacinus (Homoptera; Coccoidea). Chromosoma 120, 165–175 (2011). https://doi.org/10.1007/s00412-010-0299-0

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