FANCC suppresses short telomere-initiated telomere sister chromatid exchange

Human Molecular Genetics

Volumn 19, Issue 5, 2010, Pages 879-887

  Rhee, David B ^a   Wang, Yisong ^b   Mizesko, Melissa ^c   Zhou, Fang ^a   Haneline, Laura ^c   Liu, Yie ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FANCONI ANEMIA GROUP C PROTEIN; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CELL METABOLISM; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE DELETION; GENE FUNCTION; GENETIC RECOMBINATION; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; SISTER CHROMATID EXCHANGE; TELOMERE;

ANIMALS; BONE MARROW CELLS; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP C PROTEIN; MICE; MICE, KNOCKOUT; SISTER CHROMATID EXCHANGE; TELOMERASE; TELOMERE;

MURINAE; MUS;

EID: 77950536222     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp556     Document Type: Article

References (54)

1. Blackburn, E.H. (2001) Switching and signaling at the telomere. Cell, 106, 661-673.
2. Greider, C.W. (2006) Telomerase RNA levels limit the telomere length equilibrium. Cold Spring Harb. Symp. Quant. Biol., 71, 225-229.
3. d'Adda di Fagagna, F., Teo, S.H. and Jackson, S.P. (2004) Functional links between telomeres and proteins of the DNA-damage response. Genes Dev., 18, 1781-1799.
4. de Lange, T. (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev., 19, 2100-2110.
5. 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.
6. Yuan, X., Ishibashi, S., Hatakeyama, S., Saito, M., Nakayama, J., Nikaido, R., Haruyama, T., Watanabe, Y., Iwata, H., Iida, M. et al. (1999) Presence of telomeric G-strand tails in the telomerase catalytic subunit TERT knockout mice. Genes Cells, 4, 563-572.
7. Liu, Y., Snow, B.E., Hande, M.P., Yeung, D., Erdmann, N.J., Wakeham, A., Itie, A., Siderovski, D.P., Lansdorp, P.M., Robinson, M.O. et al. (2000) The telomerase reverse transcriptase is limiting and necessary for telomerase function in vivo. Curr. Biol., 10, 1459-1462.
8. Erdmann, N., Liu, Y. and Harrington, L. (2004) Distinct dosage requirements for the maintenance of long and short telomeres in mTert heterozygous mice. Proc. Natl. Acad. Sci. U.S.A., 101, 6080-6085.
9. 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.
10. 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.
11. Herrera, E., Samper, E., Martin-Caballero, J., Flores, J.M., Lee, H.W. and Blasco, M.A. (1999) Disease states associated with telomerase deficiency appear earlier in mice with short telomeres. EMBO J., 18, 2950-2960.
12. Hathcock, K.S., Hemann, M.T., Opperman, K.K., Strong, M.A., Greider, C.W. and Hodes, R.J. (2002) Haploinsufficiency of mTR results in defects in telomere elongation. Proc. Natl. Acad. Sci. U.S.A., 99, 3591-3596.
13. Hao, L.Y., Armanios, M., Strong, M.A., Karim, B., Feldser, D.M., Huso, D. and Greider, C.W. (2005) Short telomeres, even in the presence of telomerase, limit tissue renewal capacity. Cell, 123, 1121-1131.
14. Savage, S.A. and Alter, B.P. (2008) The role of telomere biology in bone marrow failure and other disorders. Mech. Ageing Dev., 129, 35-47.
15. Ball, S.E., Gibson, F.M., Rizzo, S., Tooze, J.A., Marsh, J.C. and Gordon-Smith, E.C. (1998) Progressive telomere shortening in aplastic anemia. Blood, 91, 3582-3592.
16. Leteurtre, F., Li, X., Guardiola, P., Le Roux, G., Sergere, J.C., Richard, P., Carosella, E.D. and Gluckman, E. (1999) Accelerated telomere shortening and telomerase activation in Fanconi's anaemia. Br. J. Haematol., 105, 883-893.
17. Hanson, H., Mathew, C.G., Docherty, Z. and Mackie Ogilvie, C. (2001) Telomere shortening in Fanconi anaemia demonstrated by a direct FISH approach. Cytogenet. Cell Genet., 93, 203-206.
18. Callen, E., Samper, E., Ramirez, M.J., Creus, A., Marcos, R., Ortega, J.J., Olive, T., Badell, I., Blasco, M.A. and Surralles, J. (2002) Breaks at telomeres and TRF2-independent end fusions in Fanconi anemia. Hum. Mol. Genet., 11, 439-444.
19. Alter, B.P., Baerlocher, G.M., Savage, S.A., Chanock, S.J., Weksler, B.B., Willner, J.P., Peters, J.A., Giri, N. and Lansdorp, P.M. (2007) Very short telomere length by flow fluorescence in situ hybridization identifies patients with dyskeratosis congenita. Blood, 110, 1439-1447.
20. Shay, J.W. (1997) Telomerase in human development and cancer. J. Cell. Physiol., 173, 266-270.
21. Cesare, A.J. and Reddel, R.R. (2008) Telomere uncapping and alternative lengthening of telomeres. Mech. Ageing Dev., 129, 99-108.
22. Bailey, S.M., Brenneman, M.A. and Goodwin, E.H. (2004) Frequent recombination in telomeric DNA may extend the proliferative life of telomerase-negative cells. Nucleic Acids Res., 32, 3743-3751.
23. Bechter, O.E., Shay, J.W. and Wright, W.E. (2004) The frequency of homologous recombination in human ALT cells. Cell Cycle, 3, 547-549.
24. Londono-Vallejo, J.A., Der-Sarkissian, H., Cazes, L., Bacchetti, S. and Reddel, R.R. (2004) Alternative lengthening of telomeres is characterized by high rates of telomeric exchange. Cancer Res., 64, 2324-2327.
25. Wang, Y., Giannone, R.J. and Liu, Y. (2005) Telomere sister chromatid exchange in telomerase deficient murine cells. Cell Cycle, 4, 1320-1322.
26. Wang, Y., Erdmann, N., Giannone, R.J., Wu, J., Gomez, M. and Liu, Y. (2005) An increase in telomere sister chromatid exchange in murine embryonic stem cells possessing critically shortened telomeres. Proc. Natl. Acad. Sci. U.S.A., 102, 10256-10260.
27. Morrish, T.A. and Greider, C.W. (2009) Short telomeres initiate telomere recombination in primary and tumor cells. PLoS Genet., 5, e1000357.
28. Laud, P.R., Multani, A.S., Bailey, S.M., Wu, L., Ma, J., Kingsley, C., Lebel, M., Pathak, S., DePinho, R.A. and Chang, S. (2005) Elevated telomere-telomere recombination in WRN-deficient, telomere dysfunctional cells promotes escape from senescence and engagement of the ALT pathway. Genes Dev., 19, 2560-2570.
29. Celli, G.B., Denchi, E.L. and de Lange, T. (2006) Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination. Nat. Cell Biol., 8, 885-890.
30. Wu, L., Multani, A.S., He, H., Cosme-Blanco, W., Deng, Y., Deng, J.M., Bachilo, O., Pathak, S., Tahara, H., Bailey, S.M. et al. (2006) Pot1 deficiency initiates DNA damage checkpoint activation and aberrant homologous recombination at telomeres. Cell, 126, 49-62.
31. He, H., Multani, A.S., Cosme-Blanco, W., Tahara, H., Ma, J., Pathak, S., Deng, Y. and Chang, S. (2006) POT1b protects telomeres from end-to-end chromosomal fusions and aberrant homologous recombination. EMBO J., 25, 5180-5190.
32. Benetti, R., Gonzalo, S., Jaco, I., Schotta, G., Klatt, P., Jenuwein, T. and Blasco, M.A. (2007) Suv4-20h deficiency results in telomere elongation and derepression of telomere recombination. J. Cell Biol., 178, 925-936.
33. Patel, K.J. and Joenje, H. (2007) Fanconi anemia and DNA replication repair. DNA Repair, 6, 885-890.
34. Wang, W. (2007) Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat. Rev. Genet., 8, 735-748.
35. Pang, Q. and Andreassen, P.R. (2009) Fanconi anemia proteins and endogenous stresses. Mutat. Res., 668, 42-53.
36. Ameziane, N., Errami, A., Leveille, F., Fontaine, C., de Vries, Y., van Spaendonk, R.M., de Winter, J.P., Pals, G. and Joenje, H. (2008) Genetic subtyping of Fanconi anemia by comprehensive mutation screening. Hum. Mutat., 29, 159-166.
37. Meetei, A.R., Sechi, S., Wallisch, M., Yang, D., Young, M.K., Joenje, H., Hoatlin, M.E. and Wang, W. (2003) A multiprotein nuclear complex connects Fanconi anemia and Bloom syndrome. Mol. Cell. Biol., 23, 3417-3426.
38. Niedzwiedz, W., Mosedale, G., Johnson, M., Ong, C.Y., Pace, P. and Patel, K.J. (2004) The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol. Cell, 15, 607-620.
39. Bridge, W.L., Vandenberg, C.J., Franklin, R.J. and Hiom, K. (2005) The BRIP1 helicase functions independently of BRCA1 in the Fanconi anemia pathway for DNA crosslink repair. Nat. Genet., 37, 953-957.
40. Hirano, S., Yamamoto, K., Ishiai, M., Yamazoe, M., Seki, M., Matsushita, N., Ohzeki, M., Yamashita, Y.M., Arakawa, H., Buerstedde, J.M. et al. (2005) Functional relationships of FANCC to homologous recombination, translesion synthesis, and BLM. EMBO J., 24, 418-427.
41. Hemann, M.T. and Greider, C.W. (2000) Wild-derived inbred mouse strains have short telomeres. Nucleic Acids Res., 28, 4474-4478.
42. Blasco, M.A. (2007) Telomere length, stem cells and aging. Nat. Chem. Biol., 3, 640-649.
43. Chen, M., Tomkins, D.J., Auerbach, W., McKerlie, C., Youssoufian, H., Liu, L., Gan, O., Carreau, M., Auerbach, A., Groves, T. et al. (1996) Inactivation of Fac in mice produces inducible chromosomal instability and reduced fertility reminiscent of Fanconi anaemia. Nat. Genet., 12, 448-451.
44. Haneline, L.S., Gobbett, T.A., Ramani, R., Carreau, M., Buchwald, M., Yoder, M.C. and Clapp, D.W. (1999) Loss of FancC function results in decreased hematopoietic stem cell repopulating ability. Blood, 94,1-8.
45. Haneline, L.S., Li, X., Ciccone, S.L., Hong, P., Yang, Y., Broxmeyer, H.E., Lee, S.H., Orazi, A., Srour, E.F. and Clapp, D.W. (2003) Retroviral-mediated expression of recombinant Fancc enhances the repopulating ability of Fancc-/- hematopoietic stem cells and decreases the risk of clonal evolution. Blood, 101, 1299-1307.
46. Franco, S., van de Vrugt, H.J., Fernandez, P., Aracil, M., Arwert, F. and Blasco, M.A. (2004) Telomere dynamics in Fancg-deficient mouse and human cells. Blood, 104, 3927-3935.
47. Haneline, L.S., Broxmeyer, H.E., Cooper, S., Hangoc, G., Carreau, M., Buchwald, M. and Clapp, D.W. (1998) Multiple inhibitory cytokines induce deregulated progenitor growth and apoptosis in hematopoietic cells from Fac-/- mice. Blood, 91, 4092-4098.
48. Li, X., Plett, P.A., Yang, Y., Hong, P., Freie, B., Srour, E.F., Orschell, C.M., Clapp, D.W. and Haneline, L.S. (2003) Fanconi anemia type C-deficient hematopoietic stem/progenitor cells exhibit aberrant cell cycle control. Blood, 102, 2081-2084.
49. Kruyt, F.A., Hoshino, T., Liu, J.M., Joseph, P., Jaiswal, A.K. and Youssoufian, H. (1998) Abnormal microsomal detoxification implicated in Fanconi anemia group C by interaction of the FAC protein with NADPH cytochrome P450 reductase. Blood, 92, 3050-3056.
50. Fan, Q., Zhang, F., Barrett, B., Ren, K. and Andreassen, P.R. (2009) A role for monoubiquitinated FANCD2 at telomeres in ALT cells. Nucleic Acids Res., 37, 1740-1754.
51. Rufer, N., Dragowska, W., Thornbury, G., Roosnek, E. and Lansdorp, P.M. (1998) Telomere length dynamics in human lymphocyte subpopulations measured by flow cytometry. Nat. Biotechnol., 16, 743-747.
52. 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. U.S.A., 94, 7423-7428.
53. Gomez, M., Wu, J., Schreiber, V., Dunlap, J., Dantzer, F., Wang, Y. and Liu, Y. (2006) PARP1 is a TRF2-associated poly(ADP-ribose)polymerase and protects eroded telomeres. Mol. Biol. Cell, 17, 1686-1696.
54. Hemann, M.T. and Greider, C.W. (1999) G-strand overhangs on telomeres in telomerase-deficient mouse cells. Nucleic Acids Res., 27, 3964-3969.