Atm Inactivation Results in Aberrant Telomere Clustering during Meiotic Prophase

REFERENCES

• Ashley, T. 1994. Mammalian meiotic recombination: a reexamination. Hum. Genet. 94:587–593.
   PubMedGoogle Scholar
• Bailis, J. M., and J. Roeder 1998. Synaptonemal complex morphogenesis and sister-chromatid cohesion require MEK1-dependent phosphorylation of a meiotic chromosomal protein. Genes Dev. 12:3551–3563.
   PubMedGoogle Scholar
• Barlow, C., S. Hirotsune, R. Paylor, M. Liyanage, M. Eckhaus, F. Collins, Y. Shiloh, J. N. Crawley, T. Ried, D. Tagel, and J. Wynshaw-Boris 1996. Atm-deficient mice: a paradigm of ataxia-telangiectasia. Cell 86:159–171.
   PubMed Web of Science ®Google Scholar
• Barlow, C., M. Liyanage, P. B. Moens, C.-X. Deng, T. Ried, and J. Wynshaw-Boris 1997. Partial rescue of the prophase 1 defects of Atm-deficient mice by p53 and p21 null alleles. Nat. Genet. 17:462–466.
   PubMed Web of Science ®Google Scholar
• Barlow, C., M. Liyanage, P. B. Moens, M. Tarsounas, K. Nagashima, K. Brown, S. P. Rottinghaus, S. P. Jackson, D. Tagle, T. Ried, and J. Wynshaw-Boris 1998. Atm deficiency results in severe meiotic disruption as early as leptonema of prophase. Development 125:4007–4017.
   PubMed Web of Science ®Google Scholar
• Baskaran, R., L. D. Wood, L. L. Whitaker, C. E. Canman, S. E. Morgan, Y. Xu, D. Baltimore, M. B. Kastan, and J. Wang 1997. Ataxia telangiectasia mutant protein activates c-Abl tyrosine kinase in response to ionizing radiation. Nature 387:516–519.
   PubMed Web of Science ®Google Scholar
• Bilaud, T., C. Brun, K. Ancelin, C. E. Koering, T. Laroche, and J. Gilson 1997. Telomeric localization of TRF2, a novel human telobox protein. Nat. Genet. 17:236–239.
   PubMed Web of Science ®Google Scholar
• Blackburn, E. H. 1991. Structure and function of telomeres. Nature 350:569–573.
   PubMed Web of Science ®Google Scholar
• Bridges, B. A., D. G. Harnden 1982. Ataxia telangiectasia: a cellular and molecular link between cancer, neuropathology, and immune deficiency. John Wiley, Chichester, England.
   Google Scholar
• Brinkley, B. R., S. L. Brenner, J. M. Hall, A. Tousson, R. D. Balczon, and J. Valdivia 1986. Arrangement of kinetochores in mouse cells during meiosis and spermiogenesis. Chromosoma 94:309–317.
   PubMedGoogle Scholar
• Broccoli, D., L. Chong, S. Oelmann, A. A. Fernald, N. Marziliano, B. van Steensel, D. Kipling, M. M. Le Beau, and J. de Lange 1997. Comparison of the human and mouse genes encoding the telomeric protein, TRF1: chromosomal localization, expression and conserved protein domains. Hum. Mol. Genet. 6:69–76.
   PubMedGoogle Scholar
• Broccoli, D., A. Smogorzewska, L. Chong, and J. de Lange 1997. Human telomeres contain two distinct Myb-related proteins TRF1 and TRF2. Nat. Genet. 17:231–235.
   PubMed Web of Science ®Google Scholar
• Cao, L., E. Alani, and J. Kleckner 1990. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61:1089–1101.
   PubMedGoogle Scholar
• Chong, L., B. van Steensel, D. Broccoli, H. Erdjument-Bromage, J. Hanish, O. Tempst, and J. de Lange 1995. A human telomeric protein. Science 270:1663–1667.
   PubMed Web of Science ®Google Scholar
• Chua, P. R., and J. Roeder 1997. Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev. 11:1786–1800.
   PubMed Web of Science ®Google Scholar
• Conrad, M. N., A. M. Dominguez, and J. Dresser 1997. Ndj1p, a meiotic telomere protein required for normal chromosome synapsis and segregation in yeast. Science 276:1252–1255.
   PubMed Web of Science ®Google Scholar
• Cooper, J. P., Y. Watanabe, and J. Nurse 1998. Fission yeast Taz1 protein is required for meiotic telomere clustering and recombination. Nature 392:828–831.
   PubMed Web of Science ®Google Scholar
• Counter, C. M., A. A. Avilion, C. E. LeFeuvre, N. G. Stewart, C. W. Greider, C. B. Harley, and J. Bacchetti 1992. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J. 11:1921–1929.
   PubMed Web of Science ®Google Scholar
• de Lange, T. 1992. Human telomeres are attached to the nuclear matrix. EMBO J. 11:717–724.
   PubMed Web of Science ®Google Scholar
• de Lange, T. 1998. Ending up with the right partner. Nature 392:753–754.
   PubMedGoogle Scholar
• Dernburg, A. F., J. W. Sedat, W. Z. Cande, H. W. Bass 1995. The cytology of telomeres, p. 295–338. In E. H. Blackburn, C. W. Greider (ed.), Telomeres. Cold Spring Harbor monograph series. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Dijkwel, P. A., and J. Hamlin 1988. Matrix attachment regions are positioned near replication initiation sites, genes, and an interamplicon junction in the amplified dihydrofolate reductase domain of Chinese hamster ovary cells. Mol. Cell. Biol. 8:5398–5409.
   PubMedGoogle Scholar
• Elson, A., Y. Wang, C. J. Daugherty, C. C. Morton, F. Zhou, J. Campos-Torres, and J. Leder 1996. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. USA 93:13084–13089.
   PubMed Web of Science ®Google Scholar
• Gately, D. P., J. C. Hittle, G. K. T. Chan, and J. Yen 1998. Characterization of ATM expression, localization, and associated DNA-dependent protein kinase activity. Mol. Biol. Cell. 9:2361–2374.
   PubMedGoogle Scholar
• Glamann, J. 1986. Crossing over in the male mouse as analyzed by recombination nodules and bars. Carlsberg Res. Commun. 51:143–162.
   Google Scholar
• Goetz, P., A. C. Chandley, and J. Speed 1984. Morphological and temporal sequence of meiotic prophase development at puberty in the male mouse. J. Cell Sci. 65:249–263.
   PubMedGoogle Scholar
• Greenwell, P. W., S. L. Kronmal, S. E. Porter, J. Gassenhuber, B. Obermaier, and J. Petes 1995. TEL1, a gene involved in controlling telomere length in S. cerevisiae, is homologous to the human ataxia telangiectasia gene. Cell 82:823–829.
   PubMed Web of Science ®Google Scholar
• Griffith, J., A. Bianchi, and J. de Lange 1998. TRF1 promotes parallel pairing of telomeric tracts in vitro. J. Mol. Biol. 278:79–88.
   PubMed Web of Science ®Google Scholar
• Guitart, M., M. D. Coll, M. Ponsa, and J. Egozcue 1985. Sequential study of synaptonemal complexes in mouse spermatocytes by light and electron microscopy. Genetica 67:21–30.
   Google Scholar
• Haaf, T., and J. Ward 1995. Higher order nuclear structure in mammalian sperm revealed by in situ hybridization and extended chromatin fibers. Exp. Cell Res. 219:604–611.
   PubMed Web of Science ®Google Scholar
• Harnden, D. G. 1994. The nature of ataxia-telangiectasia: problems and perspectives. Int. J. Radiat. Biol. 66:S13–S19.
   PubMed Web of Science ®Google Scholar
• Hoekstra, M. F. 1997. Responses to DNA damage and regulation of cell cycle checkpoints by the ATM protein kinase family. Curr. Opin. Genet. Dev. 7:170–175.
   PubMedGoogle Scholar
• Kastan, M. B., Q. Zhan, W. S. El Deiry, F. Carrier, T. Jacks, W. V. Walsh, B. S. Plunkett, B. Vogelstein, A. J. Fornace Jr.. 1992. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell 71:587–597.
   PubMed Web of Science ®Google Scholar
• Keegan, K. S., D. A. Holtzman, A. W. Plug, E. R. Christenson, E. E. Brainerd, G. Flaggs, N. J. Bentley, E. M. Taylor, M. S. Meyn, S. B. Moss, A. M. Carr, T. Ashley, and J. Hoekstra 1996. The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes Dev. 10:2423–2437.
   PubMed Web of Science ®Google Scholar
• Keith, C. T., and J. Schreiber 1995. PIK-related kinases: DNA repair, recombination, and cell cycle checkpoint. Science 270:50–51.
   PubMed Web of Science ®Google Scholar
• Klapholz, S., C. S. Waddell, and J. Esposito 1985. The role of the SPO11 gene in meiotic recombination in yeast. Genetics 110:187–216.
   PubMed Web of Science ®Google Scholar
• Ko, L. J., and J. Prives 1996. p53: puzzle and paradigm. Genes Dev. 10:1054–1072.
   PubMed Web of Science ®Google Scholar
• Kojis, T. L., R. A. Gatti, and J. Sparkes 1991. The cytogenetics of ataxia telangiectasia. Cancer Genet. Cytogenet. 56:143–156.
   PubMedGoogle Scholar
• Kyrion, G., K. A. Boakye, and J. Lustig 1992. C-terminal truncation of RAP1 results in the deregulation of telomere size, stability, and function in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:5159–5173.
   PubMedGoogle Scholar
• Lammers, J. H. M., H. H. Offenberg, M. van Aalderen, A. C. Vink, A. J. Dietrich, and J. Heyting 1994. The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol. Cell. Biol. 14:1137–1146.
   PubMedGoogle Scholar
• Loidl, J. 1990. The initiation of meiotic chromosome pairing: the cytological view. Genome 33:759–778.
   PubMed Web of Science ®Google Scholar
• Loidl, J., F. Klein, and J. Scherthan 1994. Homologous pairing is reduced but not abolished in asynaptic mutants in yeast. J. Cell Biol. 125:1191–1200.
   PubMedGoogle Scholar
• Lu, X., and J. Lane 1993. Differential induction of transcriptionally active p53 following UV or ionizing radiation: defects in chromosome instability syndromes? Cell 75:765–778.
   PubMed Web of Science ®Google Scholar
• Luderus, M. E. E., B. van Steensel, L. Chong, O. C. M. Sibon, F. F. M. Cremers, and J. de Lange 1996. Structure, subnuclear distribution, and nuclear matrix association of the mammalian telomeric complex. J. Cell Biol. 135:867–881.
   PubMed Web of Science ®Google Scholar
• Lustig, A. J., S. Kurtz, and J. Shore 1990. Involvement of the silencer and UAS binding protein RAP1 in regulation of telomere length. Science 250:549–553.
   PubMedGoogle Scholar
• Lydall, D., Y. Nikolsky, D. K. Bishop, and J. Weinert 1996. A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature 383:840–843.
   PubMedGoogle Scholar
• Ma, C., S. Martin, B. Trask, and J. Hamlin 1993. Sister chromatid fusion initiates amplification of the dihydrofolate reductase gene in Chinese hamster cells. Genes Dev. 7:605–620.
   PubMed Web of Science ®Google Scholar
• McClintock, B. 1941. The stability of broken ends of chromosomes of Zea mays. Genetics 26:234–282.
   PubMedGoogle Scholar
• McEachern, M. J., and J. Blackburn 1995. Runaway telomere elongation caused by telomerase RNA gene mutations. Nature 376:403–409.
   PubMed Web of Science ®Google Scholar
• Metcalf, J. A., J. Parkhill, L. Cambell, M. Stacey, P. Biggs, P. J. Byrd, and J. Taylor 1996. Accelerated telomere shortening in ataxia telangiectasia. Nat. Genet. 13:350–353.
   PubMedGoogle Scholar
• Meyn, M. S. 1995. Ataxia-telangiectasia and cellular responses to DNA damage. Cancer Res. 55:5991–6001.
   PubMed Web of Science ®Google Scholar
• Mirkovitch, J., M.-E. Mirault, and J. Laemmli 1984. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell 39:223–232.
   PubMed Web of Science ®Google Scholar
• Moens, P. B., and J. Pearlman 1990. Telomere and centromere DNA are associated with the cores of meiotic prophase chromosomes. Chromosoma 100:8–14.
   PubMedGoogle Scholar
• Moses, M. J. 1968. Synaptonemal complex. Annu. Rev. Genet. 2:363–412.
   Google Scholar
• Muller, H. J. 1938. The remaking of chromosomes. Collecting Net (Woods Hole, Mass.) 13:181–195.
   Google Scholar
• Nag, D., H. Scherthan, B. Rockmill, J. Bhargava, and J. Roeder 1995. Heteroduplex DNA formation and homolog pairing in yeast meiotic mutants. Genetics 141:75–86.
   PubMedGoogle Scholar
• Naito, T., A. Matsuura, and J. Ishikawa 1998. Circular chromosome formation in a fission yeast mutant defective in two ATM homologues. Nat. Genet. 20:203–206.
   PubMed Web of Science ®Google Scholar
• Nimmo, E. R., A. L. Pidoux, P. E. Perry, and J. Allshire 1998. Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe. Nature 392:825–828.
   PubMed Web of Science ®Google Scholar
• Odorisio, T., T. A. Rodriguez, E. P. Evans, A. R. Clarke, and J. Burgoyne 1998. The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis. Nat. Genet. 18:257–261.
   PubMed Web of Science ®Google Scholar
• Pandita, T. K., and J. DeRubeis 1995. Spontaneous amplification of interstitial telomeric bands in Chinese hamster ovary cells. Cytogenet. Cell Genet. 68:95–101.
   PubMedGoogle Scholar
• Pandita, T. K., E. J. Hall, T. K. Hei, M. A. Piatyszek, W. E. Wright, C. Q. Piao, R. K. Pandita, J. V. Willey, C. R. Geard, M. B. Kastan, and J. Shay 1996. Chromosome end-to-end associations and telomerase activity during cancer progression in human cells after treatment with α-particles simulating radon progeny. Oncogene 13:1423–1430.
   PubMedGoogle Scholar
• Pandita, T. K., and J. Hittelman 1992. Initial chromosome damage but not DNA damage is greater in ataxia telangiectasia cells. Radiat. Res. 130:94–103.
   PubMed Web of Science ®Google Scholar
• Pandita, T. K., S. Pathak, and J. Geard 1995. Chromosome end association, telomeres and telomerase activity in ataxia telangiectasia cells. Cytogenet. Cell Genet. 71:86–93.
   PubMedGoogle Scholar
• Pittman, D. L., J. Cobb, K. J. Schimenti, L. A. Wilson, D. M. Cooper, E. Brignull, M. A. Handel, and J. Schimenti 1998. Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol. Cell 1:697–705.
   PubMed Web of Science ®Google Scholar
• Plug, A. W., A. H. Peters, Y. Xu, K. S. Keegan, M. F. Hoekstra, D. Baltimore, P. de Boer, and J. Ashley 1997. ATM and RPA in meiotic chromosome synapsis and recombination. Nat. Genet. 17:457–461.
   PubMedGoogle Scholar
• Plug, A. W., A. H. Peters, K. S. Keegan, M. F. Hoekstra, P. de Boer, and J. Ashley 1998. Changes in protein composition of meiotic nodules during mammalian meiosis. J. Cell Sci. 111:413–423.
   PubMedGoogle Scholar
• Rockmill, B., and J. Roeder 1998. Telomere-mediated chromosome pairing during meiosis in budding yeast. Genes Dev. 12:2574–2586.
   PubMedGoogle Scholar
• Roeder, G. S. 1997. Meiotic chromosomes: it takes two to tango. Genes Dev. 11:2600–2621.
   PubMedGoogle 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
• Savitsky, K., A. Bar-Shira, S. Gilad, G. Rotman, Y. Ziv, L. Vanagaite, D. A. Tagle, S. Smith, T. Uziel, S. Sfez, M. Ashkenazi, I. Pecker, M. Frydman, R. Harnik, S. R. Patanjali, A. Simmons, G. A. Clines, A. Sartiel, R. A. Gatti, L. Chessa, O. Sanyal, M. F. Lavin, N. G. J. Jaspers, A. M. R. Taylor, C. F. Arlett, T. Miki, S. M. Weissman, M. Lovett, F. S. Collins, and J. Shiloh 1995. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268:1749–1753.
   PubMed Web of Science ®Google Scholar
• Savitsky, K., S. Sfez, D. A. Tagel, Y. Ziv, A. Sartiel, F. S. Collins, Y. Shiloh, and J. Rotman 1995. The complete sequence of the coding region of the ATM gene reveals similarity to cell cycle regulators in different species. Hum. Mol. Genet. 4:2025–2032.
   PubMed Web of Science ®Google Scholar
• Sawant, S. G., V. Gregoire, C. B. Umbricht, S. Cvilic, S. Sukumar, and J. Pandita 1999. Telomerase activity as a measure for monitoring radiocurability of tumor cells. FASEB J. 13:1047–1054.
   PubMed Web of Science ®Google Scholar
• Scherthan, H. 1997. Chromosome behavior in earliest meiotic prophase. Chromosomes Today 12:217–248.
   Google Scholar
• Scherthan, H., J. Bahler, and J. Kohli 1994. Dynamic chromosome organization and pairing during meiotic prophase of fission yeast. J. Cell Biol. 127:273–285.
   PubMed Web of Science ®Google Scholar
• Scherthan, H., and T. K. Pandita. Unpublished data.
   Google Scholar
• Scherthan, H., S. Weich, H. Schwegler, C. Heyting, M. Harle, and J. Cremer 1996. Centromere and telomere movement during early prophase of mouse and man are associated with the onset of chromosome pairing. J. Cell Sci. 134:1109–1125.
   Google Scholar
• Shafman, T., K. K. Khanna, P. Kedar, K. Spring, S. Kozlov, T. Yen, K. Hobson, M. Gatei, N. Zhang, D. Watters, M. Egerton, Y. Shiloh, S. Kharbanda, D. Kufe, and J. Lavin 1997. Interactions between ATM protein and c-Abl in response to DNA damage. Nature 387:520–523.
   PubMed Web of Science ®Google Scholar
• Shen, M., C. Haggblom, M. Vogt, T. Hunter, and J. Lu 1997. Characterization and cell cycle regulation of the related human telomeric proteins Pin2 and TRF1 suggest a role in mitosis. Proc. Natl. Acad. Sci. USA 94:13618–13623.
   PubMed Web of Science ®Google Scholar
• Shiloh, Y. 1995. Ataxia-telangiectasia: closer to unraveling the mystery. Eur. J. Hum. Genet. 3:116–138.
   PubMed Web of Science ®Google Scholar
• Smilenov, L. B., W. Mellado, P. H. Rao, S. G. Sawant, C. B. Umbricht, S. Sukumar, and J. Pandita 1998. Molecular cloning and chromosomal localization of Chinese hamster telomeric protein chTRF1: its potential role in chromosomal instability. Oncogene 17:2137–2142.
   PubMedGoogle Scholar
• Smilenov, L. B., S. E. Morgan, W. Mellado, S. G. Sawant, M. B. Kastan, and J. Pandita 1997. Influence of ATM function on telomere metabolism. Oncogene 15:2659–2665.
   PubMed Web of Science ®Google Scholar
• Smilenov, L. B., S. Dhar, and T. K. Pandita. Altered telomere nuclear matrix interactions and nucleosomal periodicity in ataxia telangiectasia cells. Submitted for publication.
   Google Scholar
• Smith, G. R., M. B. Stark, P. A. Gorman, and J. Stark 1992. Fusion near telomeres occur very early in the amplification of CAD genes in Syrian hamster cells. Proc. Natl. Acad. Sci. USA 89:5427–5431.
   PubMedGoogle Scholar
• Smith, S., and J. de Lange 1997. TRF1, a mammalian telomeric protein. Trends Genet. 13:21–26.
   PubMed Web of Science ®Google Scholar
• Smith, S., I. Giriat, A. Schmitt, and J. de Lange 1998. Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science 282:1484–1487.
   PubMed Web of Science ®Google Scholar
• Speed, R. M. 1982. Meiosis in the foetal mouse ovary. I. An analysis at the light microscope level using surface-spreading. Chromosoma 85:427–437.
   PubMed Web of Science ®Google Scholar
• Stack, S. M. 1984. Heterochromatin, the synaptonemal complex and crossing over. J. Cell Sci. 71:159–176.
   PubMedGoogle Scholar
• Sun, H., D. Dawson, and J. Szostak 1991. Genetic and physical analyses of sister chromatid exchange in yeast meiosis. Mol. Cell. Biol. 11:6328–6336.
   PubMedGoogle Scholar
• Svoboda, A., J. Bahler, and J. Kohli 1995. Microtubule-driven nuclear movements and linear elements as meiosis-specific characteristics of the fission yeasts Schizosaccharomyces versatilis and Schizosaccharomyces pombe. Chromosoma 104:203–214.
   PubMedGoogle Scholar
• Taylor, A. M. R. 1982. Cytogenetics of ataxia-telangiectasia, p. 53–81. In B. A. Bridges, D. G. Harden (ed.), Ataxia-telangiectasia. A cellular and molecular link between cancer, neuropathology, and immune deficiency. John Wiley, Chichester, England.
   Google Scholar
• Therman, E., and J. Sarto 1977. Premeiotic and early meiotic stages in the pollen mother cells of Eremurus and in human embryonic oocytes. Hum. Genet. 35:137–151.
   PubMedGoogle Scholar
• Trelles-Sticken, E., J. Loidl, and J. Scherthan 1999. Bouquet formation in budding yeast: initiation of recombination is not required for meiotic telomere clustering. J. Cell Sci. 112:651–658.
   PubMedGoogle Scholar
• van Steensel, B., and J. de Lange 1997. Control of telomere length by the human telomeric protein TRF1. Nature 385:740–743.
   PubMed Web of Science ®Google Scholar
• Vaziri, H., M. D. West, R. C. Allsopp, T. S. Davidson, Y.-S. Wu, C. H. Arrowsmith, G. G. Priorier, and J. Benchimol 1997. ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the post-translational activation of p53 protein involving poly(ADP-ribose) polymerase. EMBO J. 16:6018–6033.
   PubMed Web of Science ®Google Scholar
• von Wettstein, D., S. W. Rasmussen, and J. Holm 1984. The synaptonemal complex in genetic segregation. Annu. Rev. Genet. 18:331–413.
   PubMedGoogle Scholar
• Weiner, B. M., and J. Kleckner 1994. Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77:977–991.
   PubMed Web of Science ®Google Scholar
• Xu, Y., T. Ashley, E. E. Brainerd, R. T. Bronson, M. S. Meyn, and J. Baltimore 1996. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10:2401–2410.
   PubMed Web of Science ®Google Scholar
• Yoshida, K., G. Kondoh, Y. Matsuda, T. Habu, Y. Nishimune, and J. Morita 1998. The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol. Cell 1:707–718.
   PubMed Web of Science ®Google Scholar
• Zakian, V. A. 1995. Saccharomyces telomeres: function, structure and replication, p. 107–138. In E. H. Blackburn, C. W. Greider (ed.), Telomeres. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar