Telomere regulation and function during meiosis

Chromosome Research

Volumn 15, Issue 5, 2007, Pages 667-679

  Siderakis, Manos ^a   Tarsounas, Madalena ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Homologous recombination; Meiosis; t loop; Telomerase; Telomeres

Indexed keywords

ALANINE AMINOTRANSFERASE; DNA; TELOMERASE;

CELL FUNCTION; CELL NUCLEUS MEMBRANE; CELL PROTECTION; CHROMOSOME MAP; CHROMOSOME SIZE; GENE FUNCTION; GENETIC REGULATION; HOMOLOGOUS RECOMBINATION; HUMAN; MEIOSIS; NONHUMAN; OVARY; PRIORITY JOURNAL; REVIEW; T WAVE; TELOMERE; TESTIS;

ANIMALS; FEMALE; HUMANS; MALE; MEIOSIS; MICE; MODELS, GENETIC; OOGENESIS; SPERMATOGENESIS; TELOMERASE; TELOMERE;

EID: 34547697566     PISSN: 09673849     EISSN: 15736849     Source Type: Journal    
DOI: 10.1007/s10577-007-1149-7     Document Type: Review

References (92)

1. Amiard S, Doudeau M, Pinte S et al. (2007) A topological mechanism for TRF2-enhanced strand invasion. Nat Struct Mol Biol 14: 147-154.
2. Baumann P, Cech TR (2001) Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292: 1171-1175.
3. Bekaert S, Derradji H, Baatout S (2004) Telomere biology in mammalian germ cells and during development. Dev Biol 274: 15-30.
4. Betts DH, King WA (1999) Telomerase activity and telomere detection during early bovine development. Dev Genet 25: 397-403.
5. Blackburn EH (2001) Switching and signaling at the telomere. Cell 106: 661-673.
6. Blanco R, Munoz P, Flores JM, Klatt P, Blasco MA (2007) Telomerase abrogation dramatically accelerates TRF2-induced epithelial carcinogenesis. Genes Dev 21: 206-220.
7. Blasco MA (2005) Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet 6: 611-622.
8. Blasco MA, Funk W, Villeponteau B, Greider CW (1995) Functional characterization and developmental regulation of mouse telomerase RNA. Science 269: 1267-1270.
9. Blasco MA, Lee H-W, Hande MP et al. (1997) Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91: 25-34.
10. Bodnar AG, Ouellette M, Frolkis M et al. (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279: 349-352.
11. Bucholc M, Park Y, Lustig AJ (2001) Intrachromatid excision of telomeric DNA as a mechanism for telomere size control in Saccharomyces cerevisiae. Mol Cell Biol 21: 6559-6573.
12. Carlton PM, Cande WZ (2002) Telomeres act autonomously in maize to organize the meiotic bouquet from a semipolarized chromosome orientation. J Cell Biol 157: 231-242.
13. Celli GB, de Lange T (2005) DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat Cell Biol 7: 712-718.
14. Chikashige Y, Tsutsumi C, Yamane M, Okamasa K, Haraguchi T, Hiraoka Y (2006) Meiotic proteins Bqt1 and Bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125: 59-69.
15. Chin L, Artandi SE, Shen Q et al. (1999) p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell 97: 527-538.
16. Chong L, van Steensel B, Broccoli D, Erdjument-Bromage H, Hanish J, Tempst P, de Lange T (1995) A human telomeric protein. Science 270: 1663-1667.
17. Cooper JP, Watanabe Y, Nurse P (1998) Fission yeast Taz1 protein is required for meiotic telomere clustering and recombination. Nature 392: 828-831.
18. de Lange T (2002) Protection of mammalian telomeres. Oncogene 21: 532-540.
19. de Lange T (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19: 2100-2110.
20. de Lange T, Shiue L, Myers RM et al. (1990) Structure and variability of human chromosome ends. Mol Cell Biol 10: 518-527.
21. de Lange T, Lundblad V, Blackburn E (2006) Telomeres, 2nd edn. New York: CSH Laboratory Press.
22. diFagagna FD, Teo SH, Jackson SP (2004) Functional links between telomeres and proteins of the DNA-damage response. Genes Dev 18: 1781-1799.
23. Di Giacomo M, Barchi M, Baudat F, Edelmann W, Keeney S, Jasin M (2005) Distinct DNA-damage-dependent and -independent responses drive the loss of oocytes in recombination-defective mouse mutants. Proc Natl Acad Sci USA 102: 737-742.
24. Eisenhauer KM, Gerstein RM, Chiu C-P, Conti M, Hsueh AJW (1997) Telomerase activity in female and male rat germ cells undergoing meiosis and in early embryos. Biol Reprod 56: 1120-1125.
25. Flores JM, Cayuela ML, Blasco MA (2005) Effects of telomerase and telomere length on epidermal stem cell behavior. Science 309: 1253-1256.
26. Franco S, Alsheimer M, Herrera E, Benavente R, Blasco MA (2002) Mammalian meiotic telomeres: composition and ultrastructure in telomerase-deficient mice. Eur J Cell Biol 81: 335-340.
27. Garcia-Higuera I, Taniguchi T, Ganesan S et al. (2001) Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 7: 249-262.
28. Goedecke W, Eijpe M, Offenberg HH, van Aalderen M, Heyting C (1999) Mre11 and Ku70 interact in somatic cells, but are differentially expressed in early meiosis. Nat Genet 23: 194-198.
29. Golubovskaya IN, Harper LC, Pawlowski WP, Schichnes D, Cande WZ (2002) The pam1 gene is required for meiotic bouquet formation and efficient homologous synapsis in maize (Zea mays L.). Genetics 162: 1979-1993.
30. Golubovskaya IN, Hamant, O, Timofejeva L et al. (2006) Alleles of afd1 dissect REC8 functions during meiotic prophase I. J Cell Sci 119: 3306-3315.
31. Grabske RJ, Lake S, Gledhill BL, Meistrich ML (1975) Centrifugal elutriation: separation of spermatogenic cells on the basis of sedimentation velocity. J Cell Physiol 86: 177-189.
32. Greider CW, Blackburn EH (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43: 405-413.
33. Griffith JD, Comeau L, Rosenfield S et al. (1999) Mammalian telomeres end in a large duplex loop. Cell 97: 503-514.
34. Harley CB, Futcher AB, Greider CW (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345: 458-460.
35. Harper L, Golubovskaya I, Zacheus Cande W (2004) A bouquet of chromosomes. J Cell Sci 117: 4025-4032.
36. Hassold T, Hunt P (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2: 280-291.
37. Hemann MT, Strong MA, Hao LY, Greider CW (2001) The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107: 67-77.
38. Henson JD, Neumann AA, Yeager TR, Reddel RR (2002) Alternative lengthening of telomeres in mammalian cells. Oncogene 21: 598-610.
39. Herrera E, Samper E, MartIn-Caballero J, Flores JM, Lee H-W, Blasco MA (1999) Disease states associated with telomerase deficiency appear earlier in mice with short telomeres. EMBO J 18: 2950-2960.
40. Herrera E, Carlos Martinez A, Blasco, MA (2000) Impaired germinal center reaction in mice with short telomeres. EMBO J 19: 472-481.
41. Hiyama E, Hiyama K (2002) Clinical utility of telomerase in cancer. Oncogene 21: 643-649.
42. Hunt PA, Hassold TJ (2002) Sex matters in meiosis. Science 296: 2181-2183.
43. Jaco I, Munoz P, Goytisolo F et al. (2003) Role of mammalian Rad54 in telomere length maintenance. Mol Cell Biol 16: 5572-5580.
44. Jeggo PA, Lobrich M (2006) Contribution of DNA repair and cell cycle checkpoint arrest to the maintenance of genomic stability. DNA Repair (Amst) 5: 1192-1198.
45. Joseph I, Jia D, Lustig AJ (2005) Ndj1p-dependent epigenetic resetting of telomere size in yeast meiosis. Curr Biol 15: 231-237.
46. Kim NW, Piatyszek MA, Prowse KR et al. (1994) Specific association of human telomerase activity with immortal cells and cancer. Science 266: 2011-2015.
47. Leblond CP, Clermont Y (1952) Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann NY Acad Sci 55: 548-573.
48. Lee HW, Blasco MA, Gottlieb GJ, Horner JWn, Greider CW, DePinho RA (1998) Essential role of mouse telomerase in highly proliferative organs. Nature 392: 569-574.
49. Liebe B, Alsheimer M, Hoog C, Benavente R, Scherthan H (2004) Telomere attachment, meiotic chromosome condensation, pairing, and bouquet stage duration are modified in spermatocytes lacking axial elements. Mol Biol Cell 15(2): 827-837.
50. Liebe B, Petukhova G, Barchi M et al. (2006) Mutations that affect meiosis in male mice influence the dynamics of the mid-preleptotene and bouquet stages. Exp Cell Res 312: 3768-3781.
51. Liu L, Blasco MA, Keefe DL (2002a) Requirement of functional telomeres for metaphase chromosome alignments and integrity of meiotic spindles. EMBO Rep 3: 230-234.
52. Liu L, Blasco MA, Trimarchi JR, Keefe DL (2002b) An essential role for functional telomeres in mouse germ cells during fertilization and early development. Dev Biol 249: 74-84.
53. Liu Y, West SC (2004) Happy Hollidays: 40th anniversary of the Holliday junction. Nat Rev Mol Cell Biol 5: 937-944.
54. Liu L, Franco S, Spyropoulos B, Moens PB, Blasco MA, Keefe DL (2004a) Irregular telomeres impair meiotic synapsis and recombination in mice. Proc Natl Acad Sci USA 101: 6496-6501.
55. Liu Y, Masson JY, Shah R, O'Regan P, West SC (2004b) RAD51C is required for Holliday junction processing in mammalian cells. Science 303: 243-246.
56. Lustig AJ (2003) Clues to catastrophic telomere loss in mammals from yeast telomere rapid deletion. Nat Rev Genet 4: 916-923.
57. Maddar H, Ratzkovsky N, Krauskopf A (2001) Role for telomere cap structure in meiosis. Mol Biol Cell 12: 3191-3203.
58. Marcand S, Gilson E, Shore D (1997) A protein-counting mechanism for telomere length regulation in yeast. Science 275: 986-990.
59. Marcand S, Brevet V, Mann C, Gilson E (2000) Cell cycle restriction of telomere elongation. Curr Biol 10: 487-490.
60. Maser RS, DePinho RA (2002) Connecting chromosomes, crisis, and cancer. Science 297: 565-569.
61. McEachern MJ, Krauskopf A, Blackburn EH (2000) Telomeres and their control. Annu Rev Genet 34: 331-358.
62. Meistrich ML, Grdina DJ, Meyn RE, Barlogie B (1977) Separation of cells from mouse solid tumors by centrifugal elutriation. Cancer Res 37: 4291-4296.
63. Nimmo ER, Pidoux AL, Perry PE, Allshire RC (1998) Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe. Nature 392: 825-828.
64. Revenkova E, Eijpe M, Heyting C et al. (2004) Cohesin SMC1β is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat Cell Biol 6: 555-562.
65. Sadaie M, Naito T, Ishikawa F (2003) Stable inheritance of telomere chromatin structure and function in the absence of telomeric repeats. Genes Dev 17: 2271-2282.
66. Samper E, Goytisolo FA, Menissier-de Murcia J, Gonzales-Suarez E, Cigudosa JC, de Murcia G, Blasco MA (2001) Normal telomere length and chromosomal end capping in poly(ADP-ribose) polymerase-deficient mice and primary cells despite increased chromosomal instability. J Cell Biol 154: 49-60.
67. Scherthan H (2001) A bouquet makes ends meet. Nat Rev Mol Cell Biol 2: 621-627.
68. Scherthan H, Jerratsch M, Li B et al. (2000) Mammalian meiotic telomeres: protein composition and redistribution in relation to nuclear pores. Mol Biol Cell 11: 4189-4203.
69. Schmitt J, Benavente R, Hodzic D, Hoog C, Stewart CL, Alsheimer M (2007) Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope. Proc Natl Acad Sci USA 104: 7426-7431.
70. Shiloh Y (2003) ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3: 155-168.
71. Takai H, Smogorzewska A, de Lange T (2003) DNA damage foci at dysfunctional telomeres. Curr Biol 13: 1549-1556.
72. Tanemura K, Ogura A, Cheong C et al. (2005) Dynamic rearrangement of telomeres during spermatogenesis in mice. Dev Biol 281: 196-207.
73. Tarsounas M, West SC (2005) Recombination at mammalian telomeres: an alternative mechanism for telomere protection and elongation. Cell Cycle 4: 672-674.
74. Tarsounas M, Pearlman RE, Moens PB (1999) Meiotic activation of rat pachytene spermatocytes with okadaic acid: the behaviour of synaptonemal complex components SYN1/SCP1 and COR1/SCP3. J Cell Sci 112: 423-434.
75. Tarsounas M, Munoz P, Claas A et al. (2004) Telomere maintenance requires the RAD51D recombination/repair protein. Cell 117: 337-347.
76. Trelles-Sticken E, Dresser ME, Scherthan H (2000) Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J Cell Biol 151: 95-106.
77. Trelles-Sticken E, Bonfils S, Sollier J, Géli V, Scherthan H, de La Roche Saint-André C (2005) Set1- and Clb5-deficiencies disclose the differential regulation of centromere and telomere dynamics in Saccharomyces cerevisiae meiosis. J Cell Sci 118: 4985-4994.
78. van Steensel B, de Lange T (1997) Control of telomere length by the human telomeric protein TRF1. Nature 385: 740-743.
79. van Steensel B, Smogorzewska A, de Lange T (1998) TRF2 protects human telomeres from end-to-end fusions. Cell 92: 401-413.
80. Verdun RE, Karlseder J (2006) The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell 127: 709-720.
81. Voet T, Liebe B, Labaere C, Marynen P, Scherthan H (2003) Telomere-independent homologue pairing and checkpoint escape of accessory ring chromosomes in male mouse meiosis. J Cell Biol 162: 795-807.
82. Wahl GM, Carr AM (2001) The evolution of diverse biological responses to DNA damage: insights from yeast and p53. Nat Cell Biol 12: 277-286.
83. Wang RC, Smogorzewska A, de Lange T (2004) Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119: 355-368.
84. Watson JD (1972) Origin of concatemeric T7 DNA. Nat New Biol 239: 197-201.
85. Wright DL, Jones EL, Mayer JF, Oehninger S, Gibbons WE, Lanzendorf SE (2001) Characterization of telomerase activity in the human oocyte and preimplantation embryo. Mol Hum Reprod 7: 947-955.
86. Wright WE, Piatyszek MA, Rainey WE, Byrd W, Shay JW (1996) Telomerase activity in human germline and embryonic tissues and cells. Dev Genet 18: 173-179.
87. Wu H-Y, Burgess SM (2006) Ndj1, a telomere-associated protein, promotes meiotic recombination in budding yeast. Mol Cell Biol 26: 3683-3694.
88. Xu J, Yang X (2000) Telomerase activity in bovine embryos during early development. Biol Reprod 63: 1124-1128.
89. Yashima K, Maitra A, Barton Rogers B et al. (1998) Expression of the RNA component of telomerase during human development and differentiation. Cell Growth Differ 9: 805-813.
90. Yokoyama H, Sarai N, Kagawa W et al. (2004) Preferential binding to branched DNA strands and strand-annealing activity of the human Rad51B, Rad51C, Rad51D and Xrcc2 protein complex. Nucleic Acids Res 32: 2556-2565.
91. Zickler D, Kleckner N (1998) The leptotene-zygotene transition of meiosis. Annu Rev Genet 32: 619-697.
92. Zijlmans JM, Martens UM, Poon SS et al. (1997) Telomeres in the mouse have large inter-chromosomal variations in the number of T2AG3 repeats. Proc Natl Acad Sci USA 94: 7423-7428.