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Telomerase gene expression in the chicken: Telomerase RNA (TR) and reverse transcriptase (TERT) transcript profiles are tissue-specific and correlate with telomerase activity

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Abstract

Telomerase is the specialized enzyme which replicates the telomeres, thus maintaining the integrity of the chromosome ends; in absence of enzyme activity telomere lengths decrease, ultimately impacting genome stability. In this study, we examined the mRNA expression of both enzyme components, the RNA template (TR) and catalytic subunit (TERT) during growth and development of the chicken to better understand mechanisms which regulate telomerase activity in vertebrates. Quantitative real-time PCR was used to establish transcript profiles for six ages ranging from pre-blastula to two-year old adults. Organ-specific profiles were established for brain, heart, liver, intestine, spleen and gonad. The pre-blastula and gastrula stages exhibited very high transcript levels of both telomerase components; organs from the embryos and adult showed transcript levels either similar or down-regulated relative to the early differentiation embryo stages. Organs which are known to become negative for telomerase activity between the embryo and adult stages (brain, heart, liver) exhibited down-regulation of TR and either no change or an increase in TERT transcripts. Whereas, organs which maintain high telomerase activity even in adults (intestine, spleen, gonad), generally exhibited up-regulation of transcripts for both components. However, there were some tissue-specific differences between telomerase-positive tissues. These results show that TERT and TR transcript levels correlate with telomerase activity profiles and suggest that TR is the rate-limiting component in telomerase-negative tissues.

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References

  • Abplanalp H (1992) Inbred lines as genetic resources of chickens. Poult Sci Rev 4: 29–39

    Google Scholar 

  • Allsopp RC, Vaziri H, Patterson C, Goldstein S, Younglai EV and Futcher AB et al. (1992) Telomere length predicts replicative capacity of human fibroblasts. Proc Natl Acad Sci USA 89: 10114–10118

    CAS  PubMed  Google Scholar 

  • Allsopp RC, Chang E, Kashefi-Aazam M, Rogaev EI, Piatyszek MA and Shay JW et al (1995) Telomere shortening is associated with cell division in vitro and in vivo. Exp Cell Res 220: 194–200

    Article  CAS  PubMed  Google Scholar 

  • Arai K, Masutomi K, Khurts S, Kaneko S, Kobayashi K and Murakami S (2002) Two independent regions of human telomerase reverse transcriptase are important for its oligomerization and telomerase activity. J Biol Chem 277: 8538– 8544

    CAS  PubMed  Google Scholar 

  • Avilion AA, Piatyszek MA, Gupta J, Shay JW, Bacchetti S and Greider CW (1996) Human telomerase RNA and telomerase activity in immortal cell lines and tumor tissues. Cancer Res 56: 645–650

    CAS  PubMed  Google Scholar 

  • Beattie TL, Zhou W, Robinson MO and Harrington L (2001) Functional multimerization of the human telomerase reverse transcriptase. Mol Cell Biol 21: 6151–6160

    Article  CAS  PubMed  Google Scholar 

  • Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP and Morin GB et al (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279: 349–352

    Article  CAS  PubMed  Google Scholar 

  • Chan SR and Blackburn EH (2004) Telomeres and telomerase. Philos Trans R Soc Lond, B Biol Sci 359: 109–121

    CAS  Google Scholar 

  • Chang H and Delany ME (2005) Alternative splice variants of the chicken telomerase reverse transcriptase (chTERT) catalytic subunit in vivo and in vitro. International Plant and Animal Genome XIII, San Diego, California. (poster 545)

  • Chang H and Delany ME (in prep) Chicken telomerase reverse transcriptase (cTERT) exhibited complicated alternative splicing variation

  • Colgin LM, Wilkinson C, Englezou A, Kilian A, Robinson MO and Reddel RR (2000) The hTERTalpha splice variant is a dominant negative inhibitor of telomerase activity. Neoplasia 2: 426–432

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Counter CM, Avilion AA, Lefeuvre CE, Stewart NG, Greider CWand Harley CB et al. (1992) Telomere shortening associatedwith chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J 11: 1921– 1929

    CAS  PubMed  Google Scholar 

  • Crittenden LB, Provencher L, Santangelo L, Levin I, Abplanalp H and Briles RW et al. (1993) Characterization of a red jungle fowlby White Leghorn backcross reference population for molecular mapping of the chicken genome. Poult Sci 72: 334– 348

    Google Scholar 

  • Delany ME (2004) Genetic variants for chick biology research: From breeds to mutants. Mech Dev 121: 1169–1177

    Article  CAS  PubMed  Google Scholar 

  • Delany ME and Daniels LM (2003) The chicken telomerase RNA gene: conservation of sequence, regulatory elements and synteny among viral, avian and mammalian genomes. Cytogenet Genome Res 102: 309–317

    Article  CAS  PubMed  Google Scholar 

  • Delany ME and Daniels LM (2004) The chicken telomerase reverse transcriptase (chTERT): Molecular and cytogenetic characterization with a comparative analysis. Gene 339: 61–69

    Article  CAS  PubMed  Google Scholar 

  • Delany ME, Krupkin AB and Miller MM (2000) Organization of telomere sequences in birds: Evidence for arrays of extreme length and for in vivo shortening. Cytogenet Cell Genet 90: 139–145

    Article  CAS  PubMed  Google Scholar 

  • Delany ME, Daniels LM, Swanberg SE and Taylor HA (2003) Telomeres in the chicken: Genome stability and chromosome ends. Poult Sci 82: 917–926

    CAS  PubMed  Google Scholar 

  • Ducrest AL, Szutorisz H, Lingner J and Nabholz M (2002) Regulation of the human telomerase reverse transcriptase gene. Oncogene 21: 541–552

    Article  CAS  PubMed  Google Scholar 

  • Eyal-Giladi H and Kochav S (1976) From cleavage to primitive streak formation: a complementary normal table and a new look at the first stages of the development of the chick. Dev Biol 49: 321–337

    CAS  PubMed  Google Scholar 

  • Feng J, Funk WD, Wang SS, Weinrich SL, Avilion AA and Chiu CP et al. (1995) The RNA component of human telomerase. Science 269: 1236–1241

    CAS  PubMed  Google Scholar 

  • Forsyth NR, Wright WE and Shay JW (2002) Telomerase and differentiation in multicellular organisms: Turn it off, turn it on, and turn it off again. Differentiation 69: 188–197

    Article  CAS  PubMed  Google Scholar 

  • Greider CW and Blackburn EH (1989) A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337: 331–337

    Article  CAS  PubMed  Google Scholar 

  • Groenen MA, Cheng HH, Bumstead N, Benkel BF, Briles WE and Burke T et al. (2000) A consensus linkage map of the chicken genome. Genome Res 10: 137–147

    CAS  PubMed  Google Scholar 

  • Hamburger V and Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88: 49–92

    Article  Google Scholar 

  • Harley CB, Futcher AB and Greider CW (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345: 458– 460

    Article  CAS  PubMed  Google Scholar 

  • Holt SE, Aisner DL, Shay JW and Wright WE (1997) Lack of cell cycle regulation of telomerase activity in human cells. Proc Natl Acad Sci USA 94: 10687–10692

    Article  CAS  PubMed  Google Scholar 

  • Hubbard SJ, Grafham DV, Beattie KJ, Overton IM, McLaren SR and Croning MD et al. (2005) Transcriptome analysis for the chicken based on 19,626 finished cDNA sequences and 485,337 expressed sequence tags. Genome Res 15: 174–183

    Article  PubMed  Google Scholar 

  • International Chicken Genome Sequencing Consortium (ICGSC) (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695–716

    Google Scholar 

  • Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD andHo PL et al. (1994) Specific association of human telomerase activity with immortal cells and cancer. Science 266: 2011–2015

    CAS  PubMed  Google Scholar 

  • Krams M, Claviez A, Heidorn K, Krupp G, Parwaresch R and Harms D et al. (2001) Regulation of telomerase activity by alternate splicing of human telomerase reverse transcriptase mRNA in a subset of neuroblastomas. Am J Pathol 159: 1925– 1932

    CAS  PubMed  Google Scholar 

  • Lee MK, Ren CW, Yan B, Cox B, Zhang HB and Romanov MN et al. (2003) Construction and characterization of three BAC libraries for analysis of the chicken genome. Anim Genet 34: 151–152

    CAS  PubMed  Google Scholar 

  • Leutenegger CM, Alluwaimi AM, Smith WL, Perani L and Cullor JS (2000) Quantitation of bovine cytokine mRNA in milk cells of healthy cattle by real-time TaqMan polymerase chain reaction. Vet Immunol Immunopathol 77: 275–287

    CAS  PubMed  Google Scholar 

  • Levy MZ, Allsopp RC, Futcher AB, Greider CW and Harley CB (1992) Telomere end replication problem and cell aging. J Mol Biol 225: 951–960

    Article  CAS  PubMed  Google Scholar 

  • Lindsey J, McGill NI, Lindsey LA, Green DK and Cooke HJ (1991) In vivo loss of telomeric repeats with age in humans. Mutat Res 256: 45–48

    CAS  PubMed  Google Scholar 

  • Lingner J, Hughes TR, Shevchenko A, Mann M, Lundblad V and Cech TR (1997) Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276: 561–567

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Lai S, Andrews LG and Tollefsbol TO (2004) Genetic and epigenetic modulation of telomerase activity in development and disease. Gene 340: 1–10

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ and Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25: 402–408

    Article  CAS  PubMed  Google Scholar 

  • Mergny JL, Riou JF, Mailliet P, Teulade-Fichou MP and Gilson E (2002) Natural and pharmacological regulation of telomerase. Nucleic Acids Res 30: 839–865

    Article  CAS  PubMed  Google Scholar 

  • Michailidis G, Saretzki G and Hall J (2005) Endogenous and ectopic expression of telomere regulating genes in chicken embryonic fibroblasts. Biochem Biophys Res Commun 335: 240– 246

    Article  CAS  PubMed  Google Scholar 

  • Mozdziak PE, McFarland DC and Schultz E (2000) Telomeric profiles and telomerase activity in turkey satellite cell clones with different in vitro growth characteristics. Biochim Biophys Acta 1492: 362–368

    CAS  PubMed  Google Scholar 

  • Pisenti JM, Delany ME, Taylor RL, Abbott UK, Abplanalp H andArthur JA et al. (1999) Avian genetic resources at risk: an assessment and proposal for conservation of genetic stocks in the USA and Canada. University of California Division of Agriculture and Natural Resources, Genetic Resources Conservation Program, Davis, CA Report No. 20 http://grcp.ucdavis. edu/publications/index.htm

  • Poole JC, Andrews LG and Tollefsbol TO (2001) Activity, function, and gene regulation of the catalytic subunit of telomerase (hTERT). Gene 269: 1–12

    Article  CAS  PubMed  Google Scholar 

  • Ramakers C, Ruijter JM, Deprez RH and Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerasechain reaction (PCR) data. Neurosci Lett 339: 62–66

    Article  CAS  PubMed  Google Scholar 

  • Sharma HW, Sokoloski JA, Perez JR, Maltese JY, Sartorelli AC and Stein CA et al. (1995) Differentiation of immortal cells inhibits telomerase activity. Proc Natl Acad Sci USA 92: 12343– 12346

    CAS  PubMed  Google Scholar 

  • Stern CD (2005) The chick; a great model system becomes even greater. Dev Cell 8: 9–17

    CAS  PubMed  Google Scholar 

  • Swanberg SE and Delany ME (2003) Dynamics of telomere erosion in transformed and non-transformed avian cells in vitro. Cytogenet Genome Res 102: 318–325

    Article  CAS  PubMed  Google Scholar 

  • Swanberg SE and Delany ME (2005) Differential expression of genes associated with telomere length homeostasis and oncogenesis in an avian model. Mech Ageing Dev 126: 1060–1070

    Article  CAS  PubMed  Google Scholar 

  • Swanberg SE and Delany ME (2006) Telomeres in aging: Birds. In: Handbook of Models for Human Aging, Chapter 29, pp 339–349. Academic Press Burlington MA, USA

  • Swanberg SE, Payne WS, Hunt HD, Dodgson JB and Delany ME (2004) Telomerase activity and differential expression of telomerase genes and c-myc in chicken cells in vitro. Dev Dyn 231: 14–21

    Article  CAS  PubMed  Google Scholar 

  • Szenberg A (1976) Ontogenesis of the immune system in birds. In: Marchalonis JJ (ed) Comparative Immunology, pp 419–431. Wiley, New York

    Google Scholar 

  • Taylor HA and Delany ME (2000) Ontogeny of telomerase in chicken: Impact of downregulation on pre- and postnatal telomere length in vivo. Dev Growth Differ 42: 613–621

    Article  CAS  PubMed  Google Scholar 

  • Ulaner GA and Giudice LC (1997) Developmental regulation of telomerase activity in human fetal tissues during gestation. Mol Hum Reprod 3: 769–773

    Article  CAS  PubMed  Google Scholar 

  • Ulaner GA, Hu JF, Vu TH, Giudice LC and Hoffman AR (1998) Telomerase activity in human development is regulated by human telomerase reverse transcriptase (hTERT) transcription and by alternate splicing of hTERT transcripts. Cancer Res 58: 4168–4172

    CAS  PubMed  Google Scholar 

  • Ulaner GA, Hu JF, Vu TH, Giudice LC and Hoffman AR (2001) Tissue-specific alternate splicing of human telomerase reverse transcriptase (hTERT) influences telomere lengths during human development. Int J Cancer 91: 644–649

    Article  CAS  PubMed  Google Scholar 

  • Urquidi V, Tarin D and Goodison S (2000) Role of telomeraseincell senescence and oncogenesis. Annu Rev Med 51: 65–79

    Article  CAS  PubMed  Google Scholar 

  • Villa R, Porta CD, Folini M, Daidone MG and Zaffaroni N (2001) Possible regulation of telomerase activity by transcription and alternative splicing of telomerase reverse transcriptase in human melanoma. J Invest Dermatol 116: 867–873

    Article  CAS  PubMed  Google Scholar 

  • Wenz C, Enenkel B, Amacker M, Kelleher C, Damm K and Lingner J (2001) Human telomerase contains two cooperating telomerase RNA molecules. EMBO J 20: 3526–3534

    Article  CAS  PubMed  Google Scholar 

  • Wright WE, Piatyszek MA, Rainey WE, Byrd W and Shay JW (1996) Telomerase activity in human germline and embryonic tissues and cells. Dev Genet 18: 173–179

    Article  CAS  PubMed  Google Scholar 

  • Yi X, Tesmer VM, Savre-Train I, Shay JW and Wright WE (1999) Both transcriptional and posttranscriptional mechanisms regulate human telomerase template RNA levels. Mol Cell Biol 19: 3989–3997

    CAS  PubMed  Google Scholar 

  • Yi X, White DM, Aisner DL, Baur JA, Wright WE and Shay JW (2000) An alternate splicing variant of the human telomerase catalytic subunit inhibits telomerase activity. Neoplasia 2: 433– 440

    CAS  PubMed  Google Scholar 

  • Yi X, Shay JW and Wright WE (2001) Quantitation of telomerase components and hTERT mRNA splicing patterns in immortal human cells. Nucleic Acids Res 29: 4818–4825

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Mary E. Delany.

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O'Hare, T.H., Delany, M.E. Telomerase gene expression in the chicken: Telomerase RNA (TR) and reverse transcriptase (TERT) transcript profiles are tissue-specific and correlate with telomerase activity. AGE 27, 257–266 (2005). https://doi.org/10.1007/s11357-005-4558-6

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  • DOI: https://doi.org/10.1007/s11357-005-4558-6

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