An essential role for functional telomeres in mouse germ cells during fertilization and early development

Developmental Biology

Volumn 249, Issue 1, 2002, Pages 74-84

  Liu, Lin ^a,b   Blasco, Maria A ^c   Trimarchi, James R ^a,b   Keefe, David L ^a,b  

^a BROWN UNIVERSITY   (United States)

^b MARINE BIOLOGICAL LABORATORY   (United States)

^c CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

Apoptosis; Embryo; Fertilization; Telomerase null mice; Telomere

Indexed keywords

TELOMERASE;

ANIMAL CELL; ARTICLE; CELL DIVISION; CELL NUCLEUS; CHROMOSOME LOSS; CHROMOSOME SIZE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME DEFICIENCY; FEMALE; FERTILIZATION; MALE; MEIOSIS; METAPHASE CHROMOSOME; MOUSE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; SPERM; SPERMATOCYTE; TELOMERE; WILD TYPE;

EID: 0036385838     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.2002.0735     Document Type: Article

References (56)

1. Abdalla, H. I., Burton, G., Kirkland, A., Johnson, M. R., Leonard, T., Brooks, A. A., and Studd, J. W. (1993). Age, pregnancy and miscarriage: Uterine versus ovarian factors. Hum. Reprod. 8, 1512-1517.
2. Allworth, A. E., and Albertini, D. F. (1993). Meiotic maturation in cultured bovine oocytes is accompanied by remodeling of the cumulus cell cytoskeleton. Dev. Biol. 158, 101-112.
3. Angell, R. (1997). First-meiotic-division nondisjunction in human oocytes. Am. J. Hum. Genet. 61, 23-32.
4. Antczak, M., and Van Blerkom, J. (1999). Temporal and spatial aspects of fragmentation in early human embryos: Possible effects on developmental competence and association with the differential elimination of regulatory proteins from polarized domains. Hum. Reprod. 14, 429-447.
5. Bass, H. W., Riera-Lizarazu, O., Ananiev, E. V., Bordoli, S. J., Rines, H. W., Phillips, R. L., Sedat, J. W., Agard, D. A., and Cande, W. Z. (2000). Evidence for the coincident initiation of homolog pairing and synapsis during the telomere-clustering (bouquet) stage of meiotic prophase. J. Cell Sci. 113, 1033-1042.
6. Betts, D. H., and King, W. A. (1999). Telomerase activity and telomere detection during early bovine development. Dev. Genet. 25, 397-403.
7. Blackburn, E. H. (2000). Telomere states and cell fates. Nature 408, 53-56.
8. Blackburn, E. H. (2001). Switching and signaling at the telomere. Cell 106, 661-673.
9. Blasco, M. A., Lee, H. W., Hande, M. P., Samper, E., Lansdorp, P. M., DePinho, R. A., and Greider, C. W. (1997). Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91, 25-34.
10. Bodnar, A. G., Ouellette, M., Frolkis, M., Holt, S. E., Chiu, C. P., Morin, G. B., Harley, C. B., Shay, J. W., Lichtsteiner, S., and Wright, W. E. (1998). Extension of life-span by introduction of telomerase into normal human cells. Science 279, 349-352.
11. Brison, D. R., and Schultz, R. M. (1997). Apoptosis during mouse blastocyst formation: Evidence for a role for survival factors including transforming growth factor alpha. Biol. Reprod. 56, 1088-1096.
12. De Lange, T. (1998). Ending up with the right partner. Nature 392, 753-754.
13. Eisenhauer, K. M., Gerstein, R. M., Chiu, C. P., Conti, M., and Hsueh, A. J. (1997). Telomerase activity in female and male rat germ cells undergoing meiosis and in early embryos. Biol. Reprod. 56, 1120-1125.
14. Exley, G. E., Tang, C., McElhinny, A. S., and Warner, C. M. (1999). Expression of caspase and BCL-2 apoptotic family members in mouse preimplantation embryos. Biol. Reprod. 61, 231-239.
15. Greider, C. W. (1990). Telomeres, telomerase and senescence. Bioessays 12, 363-369.
16. Greider, C. W., and Blackburn, E. H. (1996). Telomeres, telomerase and cancer. Sci. Am. 274, 92-97.
17. Hawes, S. M., Gie Chung, Y., and Latham, K. E. (2001). Genetic and epigenetic factors affecting blastomere fragmentation in two-cell stage mouse embryos. Biol. Reprod. 65, 1050-1056.
18. Hemann, M. T., Rudolph, K. L., Strong, M. A., DePinho, R. A., Chin, L., and Greider, C. W. (2001a). Telomere dysfunction triggers developmentally regulated germ cell apoptosis. Mol. Biol. Cell 12, 2023-2030.
19. Hemann, M. T., Strong, M. A., Hao, L. Y., and Greider, C. W. (2001b). The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107, 67-77.
20. Herrera, E., Martinez, A. C., and Blasco, M. A. (2000). Impaired germinal center reaction in mice with short telomeres. EMBO J. 19, 472-481.
21. -/- embryos is associated with failure to close the neural tube. EMBO J. 18, 1172-1181.
22. Herrera, E., Samper, E., Martin-Caballero, J., Flores, J. M., Lee, H. W., and Blasco, M. A. (1999b). Disease states associated with telomerase deficiency appear earlier in mice with short telomeres. EMBO J. 18, 2950-2960.
23. Ho, Y., Wigglesworth, K., Eppig, J. J., and Schultz, R. M. (1995). Preimplantation development of mouse embryos in KSOM: Augmentation by amino acids and analysis of gene expression. Mol. Reprod. Dev. 41, 232-238.
24. Janny, L., and Menezo, Y. J. (1996). Maternal age effect on early human embryonic development and blastocyst formation. Mol. Reprod. Dev. 45, 31-37.
25. Jurisicova, A., Latham, K. E., Casper, R. F., and Varmuza, S. L. (1998a). Expression and regulation of genes associated with cell death during murine preimplantation embryo development. Mol. Reprod. Dev. 51, 243-253.
26. Jurisicova, A., Rogers, I., Fasciani, A., Casper, R. F., and Varmuza, S. (1998b). Effect of maternal age and conditions of fertilization on programmed cell death during murine preimplantation embryo development. Mol. Hum. Reprod. 4, 139-145.
27. Jurisicova, A., Varmuza, S., and Casper, R. F. (1996). Programmed cell death and human embryo fragmentation. Mol. Hum. Reprod. 2,93-98.
28. Kornafel, K. L., and Sauer, M. V. (1994). Increased rates of aneu-ploidy in older women. Increased rates of aneuploidy do not occur in gestations of older embryo recipients. Hum. Reprod. 9, 1981-1982.
29. Lawitts, J. A., and Biggers, J. D. (1993). Culture of preimplantation embryos. Methods Enzymol. 225, 153-164.
30. Lee, H. W., Blasco, M. A., Gottlieb, G. J., Horner, J. W., 2nd, Greider, C. W., and DePinho, R. A. (1998). Essential role of mouse telomerase in highly proliferative organs. Nature 392, 569-574.
31. Liu, L., Blasco, M. A., and Keefe, D. L. (2002a). Requirement of functional telomeres for metaphase chromosome alignments and integrity of meiotic spindles. EMBO Rep. 3, 230-234.
32. Liu, L., and Keefe, D. L. (2000). Cytoplasm mediates both development and oxidation-induced apoptotic cell death in mouse zygotes. Biol. Reprod. 62, 1828-1834.
33. Liu, L., Trimarchi, J. R., and Keefe, D. L. (2002b). Haploidy but not parthenogenetic activation leads to increased incidence of apoptosis in mouse embryos. Biol. Reprod. 64, 204-210.
34. Londono-Vallejo, J. A., DerSarkissian, H., Cazes, L., and Thomas, G. (2001). Differences in telomere length between homologous chromosomes in humans. Nucleic Acids Res. 29, 3164-3171.
35. Marciniak, R., and Guarente, L. (2001). Human genetics. Testing telomerase. Nature 413, 370-373.
36. Marciniak, R. A., Johnson, F. B., and Guarente, L. (2000). Dyskera-tosis congenita, telomeres and human ageing. Trends Genet. 16, 193-195.
37. Martens, U. M., Chavez, E. A., Poon, S. S., Schmoor, C., and Lansdorp, P. M. (2000). Accumulation of short telomeres in human fibroblasts prior to replicative senescence. Exp. Cell Res. 256, 291-299.
38. Moley, K. H., Chi, M. M., Knudson, C. M., Korsmeyer, S. J., and Mueckler, M. M. (1998). Hyperglycemia induces apoptosis in pre-implantation embryos through cell death effector pathways. Nat. Med. 4, 1421-1424.
39. Navot, D., Bergh, P. A., Williams, M. A., Garrisi, G. J., Guzman, I., Sandler, B., and Grunfeld, L. (1991). Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet 337, 1375-1377.
40. Navot, D., Drews, M. R., Bergh, P. A., Guzman, I., Karstaedt, A., Scott, R. T., Jr., Garrisi, G. J., and Hofmann, G. E. (1994). Age-related decline in female fertility is not due to diminished capacity of the uterus to sustain embryo implantation. Fertil. Steril. 61, 97-101.
41. Plachot, M., Veiga, A., Montagut, J., de Grouchy, J., Calderon, G., Lepretre, S., Junca, A. M., Santalo, J., Carles, E., Mandelbaum, J., et al. (1988). Are clinical and biological IVF parameters correlated with chromosomal disorders in early life: A multicentric study. Hum. Reprod. 3, 627-635.
42. Prowse, K. R., and Greider, C. W. (1995). Developmental and tissue-specific regulation of mouse telomerase and telomere length. Proc. Natl. Acad. Sci. USA 92, 4818-4822.
43. Romanov, S. R., Kozakiewicz, B. K., Holst, C. R., Stampfer, M. R., Haupt, L. M., and Tisty, T. D. (2001). Normal human mammary epithelial cells spontaneously escape senescence and acquire genomic changes. Nature 409, 633-637.
44. Rudolph, K. L., Chang, S., Lee, H. W., Blasco, M., Gottlieb, G. J., Greider, C., and DePinho, R. A. (1999). Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell 96, 701-712.
45. -/- mice with short telomeres. EMBO Rep. 2, 800-807.
46. Scherthan, H., Jerratsch, M., Li, B., Smith, S., Hulten, M., Lock, T., and de Lange, T. (2000). Mammalian meiotic telomeres: Protein composition and redistribution in relation to nuclear pores. Mol. Biol. Cell 11, 4189-4203.
47. Scherthan, H., Weich, S., Schwegler, H., Heyting, C., Harle, M., and Cremer, T. (1996). Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J. Cell Biol. 134, 1109-1125.
48. Tease, C., and Fisher, G. (1998). Analysis of meiotic chromosome pairing in the female mouse using a novel minichromosome. Chromosome Res. 6, 269-276.
49. Van Blerkom, J., Davis, P., and Alexander, S. (2001). A microscopic and biochemical study of fragmentation phenotypes in stage-appropriate human embryos. Hum. Reprod. 16, 719-729.
50. Vaziri, H., and Benchimol, S. (1998). Reconstitution of telomerase activity in normal human cells leads to elongation of telomeres and extended replicative life span. Curr. Biol. 8, 279-282.
51. Vulliamy, T., Marrone, A., Goldman, F., Dearlove, A., Bessler, M., Mason, P. J., and Dokal, I. (2001). The RNA component of telomerase is mutated in autosomal dominant dyskeratosis con-genita. Nature 413, 432-435.
52. Wakayama, T., and Yanagimachi, R. (1998). Fertilisability and developmental ability of mouse oocytes with reduced amounts of cytoplasm. Zygote 6, 341-346.
53. Wright, D. L., Jones, E. L., Mayer, J. F., Oehninger, S., Gibbons, W. E., and Lanzendorf, S. E. (2001). Characterization of telomer-ase activity in the human oocyte and preimplantation embryo. Mol. Hum. Reprod. 7, 947-955.
54. Wright, W. E., Piatyszek, M. A., Rainey, W. E., Byrd, W., and Shay, J. W. (1996). Telomerase activity in human germline and embryonic tissues and cells. Dev. Genet. 18, 173-179.
55. Xu, J., and Yang, X. (2000). Telomerase activity in bovine embryos during early development. Biol. Reprod. 63, 1124-1128.
56. Zijlmans, J. M., Martens, U. M., Poon, S. S., Raap, A. K., Tanke, H. J., Ward, R. K., and Lansdorp, P. M. (1997). Telomeres in the mouse have large inter-chromosomal variations in the number of T2AG3 repeats. Proc. Natl. Acad. Sci. USA 94, 7423-7428.