Developmentally Regulated Telomerase Activity Is Correlated with Chromosomal Healing during Chromatin Diminution in Ascaris suum

REFERENCES

• Avilion, A. A., L. A. Harrington, and J. Greider 1992. Tetrahymena telomerase RNA levels increase during macronuclear development. Dev. Genet. 13:80–86.
   PubMedGoogle Scholar
• Barnett, M. A., V. J. Buckle, E. P. Evans, A. C. Porter, D. Rout, A. G. Smith, and J. Brown 1993. Telomere directed fragmentation of mammalian chromosomes. Nucleic Acids Res. 21:27–36.
   PubMedGoogle Scholar
• Bednenko, J., M. Melek, E. C. Greene, and J. Shippen 1997. Developmentally regulated initiation of DNA synthesis by telomerase: evidence for factor-assisted de novo telomere formation. EMBO J. 16:2507–2518.
   PubMedGoogle Scholar
• Bennett, K. L., and J. Ward 1986. Neither a germ line-specific nor several somatically expressed genes are lost or rearranged during embryonic chromatin diminution in the nematode Ascaris lumbricoides var. suum. Dev. Biol. 118:141–147.
   PubMedGoogle Scholar
• Biessmann, H., and J. Mason 1997. Telomere maintenance without telomerase. Chromosoma 106:63–69.
   PubMedGoogle Scholar
• Blackburn, E. H. 1995. Developmentally programmed healing of chromosomes, p. 193–218. In E. H. Blackburn, C. W. Greider (ed.), Telomeres. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
   Google Scholar
• Bodnar, A. G., M. Ouellette, M. Frolkis, S. E. Holt, C. P. Chiu, G. B. Morin, C. B. Harley, J. W. Shay, S. Lichtsteiner, and J. Wright 1998. Extension of life-span by introduction of telomerase into normal human cells. Science 279:349–352.
   PubMed Web of Science ®Google Scholar
• Bottius, E., N. Bakhsis, and J. Scherf 1998. Plasmodium falciparum telomerase: de novo telomere addition to telomeric and nontelomeric sequences and role in chromosome healing. Mol. Cell. Biol. 18:919–925.
   PubMed Web of Science ®Google Scholar
• Broccoli, D., J. W. Young, and J. de Lange 1995. Telomerase activity in normal and malignant hematopoietic cells. Proc. Natl. Acad. Sci. USA 92:9082–9086.
   PubMed Web of Science ®Google Scholar
• Bryan, T. M., J. M. Sperger, K. B. Chapman, and J. Cech 1998. Telomerase reverse transcriptase genes identified in Tetrahymena thermophila and Oxytricha trifallax. Proc. Natl. Acad. Sci. USA 95:8479–8484.
   PubMed Web of Science ®Google Scholar
• Cohn, M., and J. Blackburn 1995. Telomerase in yeast. Science 269:396–400.
   PubMed Web of Science ®Google Scholar
• Collins, K., and J. Greider 1993. Tetrahymena telomerase catalyzes nucleolytic cleavage and nonprocessive elongation. Genes Dev. 7:1364–1376.
   PubMed Web of Science ®Google Scholar
• Counter, C. M., J. Gupta, C. B. Harley, B. Leber, and J. Bacchetti 1995. Telomerase activity in normal leukocytes and in hematologic malignancies. Blood 85:2315–2320.
   PubMed Web of Science ®Google Scholar
• Davis, A. H., G. H. Kidd, and J. Carter 1979. Chromosome diminution in Ascaris suum: two fold increase of nucleosomal histone to DNA ratios during development. Biochim. Biophys. Acta 565:315–325.
   PubMedGoogle Scholar
• Fairbairn, D. 1957. The biochemistry of Ascaris. Exp. Parasitol. 6:491–554.
   PubMedGoogle Scholar
• Fajkus, J., A. Kovarik, and J. Kralovics 1996. Telomerase activity in plant cells. FEBS Lett. 391:307–309.
   PubMed Web of Science ®Google Scholar
• Fan, Q., and J. Yao 1996. New telomere formation coupled with site-specific chromosome breakage in Tetrahymena thermophila. Mol. Cell. Biol. 16:1267–1274.
   PubMedGoogle Scholar
• Fitzgerald, M. S., T. D. McKnight, and J. Shippen 1996. Characterization and developmental patterns of telomerase expression in plants. Proc. Natl. Acad. Sci. USA 93:14422–14427.
   PubMed Web of Science ®Google Scholar
• Flint, J., C. F. Craddock, A. Villegas, D. P. Bentley, H. J. Williams, R. Galanello, A. Cao, W. G. Wood, H. Ayyub, and J. Higgs 1994. Healing of broken human chromosomes by the addition of telomeric repeats. Am. J. Hum. Genet. 55:505–512.
   PubMed Web of Science ®Google Scholar
• Goldstein, P. 1977. Chromatin diminution in early embryogenesis of Ascaris umbricoides L. var. suum. J. Morphol. 152:141–152.
   PubMedGoogle Scholar
• Greene, E. C., J. Bednenko, and J. Shippen 1998. Flexible positioning of the telomerase-associated nuclease leads to preferential elimination of nontelomeric DNA. Mol. Cell. Biol. 18:1544–1552.
   PubMed Web of Science ®Google Scholar
• Greider, C. W. 1996. Telomere length regulation. Annu. Rev. Biochem. 65:337–365.
   PubMed Web of Science ®Google Scholar
• Greider, C. W., and J. Blackburn 1985. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43:405–413.
   PubMed Web of Science ®Google Scholar
• Greider, C. W., and J. Blackburn 1987. The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell 51:887–898.
   PubMed Web of Science ®Google Scholar
• Greider, C. W., and J. Blackburn 1989. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337:331–337.
   PubMed Web of Science ®Google Scholar
• Hanish, J. P., J. L. Yanowitz, and J. de Lange 1994. Stringent sequence requirements for the formation of human telomeres. Proc. Natl. Acad. Sci. USA 91:8861–8865.
   PubMed Web of Science ®Google Scholar
• Hannon, G. J., P. A. Maroney, J. A. Denker, and J. Nilsen 1990. Trans-splicing of nematode pre-messenger RNA in vitro. Cell 61:1247–1255.
   PubMedGoogle Scholar
• Heller, K., A. Kilian, M. A. Piatyszek, and J. Kleinhofs 1996. Telomerase activity in plant extracts. Mol. Gen. Genet. 252:342–345.
   PubMedGoogle Scholar
• Hiyama, K., Y. Hirai, S. Kyoizumi, M. Akiyama, E. Hiyama, M. A. Piatyszek, J. W. Shay, S. Ishioka, and J. Yamakido 1995. Activation of telomerase in human lymphocytes and hematopoietic progenitor cells. J. Immunol. 155:3711–3715.
   PubMed Web of Science ®Google Scholar
• Jentsch, S., G. Khoudoli, C. Zenhäusern, H. Tobler, and F. Müller. Unpublished data.
   Google Scholar
• Kim, N. W., M. A. Piatyszek, K. R. Prowse, C. B. Harley, M. D. West, P. L. Ho, G. M. Coviello, W. E. Wright, S. L. Weinrich, and J. Shay 1994. Specific association of human telomerase activity with immortal cells and cancer. Science 266:2011–2015.
   PubMed Web of Science ®Google Scholar
• Koziol, C., R. Borojevic, R. Steffen, and J. Muller 1998. Sponges (Porifera) model systems to study the shift from immortal to senescent somatic cells: the telomerase activity in somatic cells. Mech. Ageing Dev. 100:107–120.
   PubMed Web of Science ®Google Scholar
• Kramer, K. M., and J. Haber 1993. New telomeres in yeast are initiated with a highly selected subset of TG1-3 repeats. Genes Dev. 7:2345–2356.
   PubMed Web of Science ®Google Scholar
• Krupp, G., K. Kuhne, S. Tamm, W. Klapper, K. Heidorn, A. Rott, and J. Parwaresch 1997. Molecular basis of artifacts in the detection of telomerase activity and a modified primer for a more robust ‘TRAP’ assay. Nucleic Acids Res. 25:919–921.
   PubMedGoogle Scholar
• Lamb, J., P. C. Harris, A. O. Wilkie, W. G. Wood, J. G. Dauwerse, and J. Higgs 1993. De novo truncation of chromosome 16p and healing with (TTAGGG)n in the alpha-thalassemia/mental retardation syndrome (ATR-16). Am. J. Hum. Genet. 52:668–676.
   PubMedGoogle Scholar
• Lin, J. J., and J. Zakian 1995. An in vitro assay for Saccharomyces telomerase requires EST1. Cell 81:1127–1135.
   PubMedGoogle Scholar
• Lue, N. F., and J. Peng 1997. Identification and characterization of a telomerase activity from Schizosaccharomyces pombe. Nucleic Acids Res. 25:4331–4337.
   PubMedGoogle Scholar
• Mantell, L. L., and J. Greider 1994. Telomerase activity in germline and embryonic cells of Xenopus. EMBO J. 13:3211–3217.
   PubMed Web of Science ®Google Scholar
• Maroney, P. A., G. J. Hannon, and J. Nilsen 1990. Transcription and cap trimethylation of a nematode spliced leader RNA in a cell-free system. Proc. Natl. Acad. Sci. USA 87:709–713.
   PubMedGoogle Scholar
• Mattei, D., and J. Scherf 1994. Subtelomeric chromosome instability in Plasmodium falciparum: short telomere-like sequence motifs found frequently at healed chromosome breakpoints. Mutat. Res. 324:115–120.
   PubMedGoogle Scholar
• McClintock, B. 1941. The stability of broken ends of chromosomes of Zea mays. Genetics 26:234–282.
   PubMedGoogle Scholar
• Melek, M., E. C. Greene, and J. Shippen 1996. Processing of nontelomeric 3′ ends by telomerase: default template alignment and endonucleolytic cleavage. Mol. Cell. Biol. 16:3437–3445.
   PubMedGoogle Scholar
• Melek, M., and J. Shippen 1996. Chromosome healing: spontaneous and programmed de novo telomere formation by telomerase. Bioessays 18:301–308.
   PubMedGoogle Scholar
• Meyer, O. 1895. Celluläre Untersuchungen an Nematoden-Eiern. Jena. Z. Naturwiss. 29:391–410.
   Google Scholar
• Morin, G. B. 1989. The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats. Cell 59:521–529.
   PubMed Web of Science ®Google Scholar
• Morin, G. B. 1991. Recognition of a chromosome truncation site associated with alpha-thalassaemia by human telomerase. Nature 353:454–456.
   PubMedGoogle Scholar
• Müller, F., V. Bernard, and J. Tobler 1996. Chromatin diminution in nematodes. Bioessays 18:133–138.
   PubMedGoogle Scholar
• Müller, F., C. Wicky, A. Spicher, and J. Tobler 1991. New telomere formation after developmentally regulated chromosomal breakage during the process of chromatin diminution in Ascaris lumbricoides. Cell 67:815–822.
   PubMedGoogle Scholar
• Müller, H. J. 1938. The remaking of chromosomes. Collecting Net 8:181–195.
   Google Scholar
• Murray, A. W., T. E. Claus, and J. Szostak 1988. Characterization of two telomeric DNA processing reactions in Saccharomyces cerevisiae. Mol. Cell. Biol. 8:4642–4650.
   PubMed Web of Science ®Google Scholar
• Nakayama, J., H. Tahara, E. Tahara, M. Saito, K. Ito, H. Nakamura, T. Nakanishi, E. Tahara, T. Ide, and J. Ishikawa 1998. Telomerase activation by hTRT in human normal fibroblasts and hepatocellular carcinomas. Nat. Genet. 18:65–68.
   PubMed Web of Science ®Google Scholar
• Noll, F., and J. Bielka 1968. Zur Biochemie der Embryogenese von Ascaris. Acta Biol. Med. Germ. 20:565–575.
   PubMedGoogle Scholar
• Nugent, C. I., and J. Lundblad 1998. The telomerase reverse transcriptase: components and regulation. Genes Dev. 12:1073–1085.
   PubMed Web of Science ®Google Scholar
• Oliver, B. C., and J. Shen 1986. Cytoplasmic control of chromosome diminution in Ascaris suum. J. Exp. Zool. 239:41–55.
   Google Scholar
• Olovnikov, A. 1971. Principles of marginotomy in template synthesis of polynucleotides. Dokl. Akad. Nauk SSSR 201:1496–1499.
   PubMedGoogle Scholar
• Piatyszek, M. A., N. W. Kim, S. L. Weinrich, K. Hiyama, E. Hiyama, W. E. Wright, and J. Shay 1995. Detection of telomerase activity in human cells and tumors by a telomeric repeat amplification protocol (TRAP). Methods Cell Sci. 17:1–15.
   Google Scholar
• Pologe, L. G., and J. Ravetch 1988. Large deletions result from breakage and healing of P. falciparum chromosomes. Cell 55:869–874.
   PubMedGoogle Scholar
• Prescott, D. M. 1994. The DNA of ciliated protozoa. Microbiol. Rev. 58:233–267.
   PubMedGoogle Scholar
• Price, C. M., A. K. Adams, and J. Vermeesch 1994. Accumulation of telomerase RNA and telomere protein transcripts during telomere synthesis in Euplotes. J. Eukaryot. Microbiol. 41:267–275.
   PubMedGoogle Scholar
• Prowse, K. R., A. A. Avilion, and J. Greider 1993. Identification of a nonprocessive telomerase activity from mouse cells. Proc. Natl. Acad. Sci. USA 90:1493–1497.
   PubMedGoogle Scholar
• Ray, A., and J. Runge 1998. The C terminus of the major yeast telomere binding protein Rap1p enhances telomere formation. Mol. Cell. Biol. 18:1284–1295.
   PubMed Web of Science ®Google Scholar
• Sandell, L. L., and J. Zakian 1993. Loss of a yeast telomere: arrest, recovery and chromosome loss. Cell 75:729–739.
   PubMed Web of Science ®Google Scholar
• Scherf, A., and J. Mattei 1992. Cloning and characterization of chromosome breakpoints of Plasmodium falciparum: breakage and new telomere formation occurs frequently and randomly in subtelomeric genes. Nucleic Acids Res. 20:1491–1496.
   PubMedGoogle Scholar
• Shippen, L. D., and J. Blackburn 1989. Telomere terminal transferase activity from Euplotes crassus adds large numbers of TTTTGGGG repeats onto telomeric primers. Mol. Cell. Biol. 9:2761–2764.
   PubMedGoogle Scholar
• Spicher, A., A. Etter, V. Bernard, H. Tobler, and J. Müller 1994. Extremely stable transcripts may compensate for the elimination of the gene fert-1 from all Ascaris lumbricoides somatic cells. Dev. Biol. 164:72–86.
   PubMedGoogle Scholar
• Tobler, H., K. D. Smith, and J. Ursprung 1972. Molecular aspects of chromatin elimination in Ascaris lumbricoides. Dev. Biol. 27:190–203.
   PubMedGoogle Scholar
• von Ehrenstein, G., and J. Schierenberg 1980. Cell lineages and development of Caenorhabditis elegans and other nematodes Nematodes as biological models In B. M. Zuckerman (ed.), 1:1–71 Academic Press, New York, N.Y.
   Google Scholar
• Wang, H., and J. Blackburn 1997. De novo telomere addition by Tetrahymena telomerase in vitro. EMBO J. 16:866–879.
   PubMedGoogle Scholar
• Wang, S., N. L. V. Lapitan, M. Roder, and J. Tsuchyia 1992. Characterization of telomeres in Hordeum vulgare chromosomes by in situ hybridization. II. Healed broken chromosomes in telotrisomic 4L and acrotrisomic 4L4s lines. Genome 35:975–980.
   Google Scholar
• Watson, J. D. 1972. Origin of concatameric T4 DNA. Nat. New Biol. 239:197–201.
   PubMedGoogle Scholar
• Werner, J. E., R. S. Kota, and J. Gill 1992. Distribution of telomeric repeats and their role in the healing of broken chromosome ends in wheat. Genome 35:844–848.
   Google Scholar
• Wicky, C., A. M. Villeneuve, N. Lauper, L. Codourey, H. Tobler, and F. Müller. 1996. Telomeric repeats (TTAGGC)n are sufficient for chromosome capping function in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 93:8983–8988.
   PubMed Web of Science ®Google Scholar
• Wilkie, A. O., J. Lamb, P. C. Harris, R. D. Finney, and J. Higgs 1990. A truncated human chromosome 16 associated with alpha-thalassaemia is stabilized by addition of telomeric repeat (TTAGGG)n. Nature 346:868–871.
   PubMedGoogle Scholar
• Wright, W. E., M. A. Piatyszek, W. E. Rainey, W. Byrd, and J. Shay 1996. Telomerase activity in human germline and embryonic tissues and cells. Dev. Genet. 18:173–179.
   PubMedGoogle Scholar
• Yu, G. L., and J. Blackburn 1991. Developmentally programmed healing of chromosomes by telomerase in Tetrahymena. Cell 67:823–832.
   PubMedGoogle Scholar
• Zahler, A. M., and J. Prescott 1988. Telomere terminal transferase activity in the hypotrichous ciliate Oxytricha nova and a model for replication of the ends of linear DNA molecules. Nucleic Acids Res. 16:6953–6972.
   PubMed Web of Science ®Google Scholar