SLX4 contributes to telomere preservation and regulated processing of telomeric joint molecule intermediates

Nucleic Acids Research

Volumn 43, Issue 12, 2015, Pages 5912-5923

  Sarkar, Jaya ^a   Wan, Bingbing ^b,c   Yin, Jinhu ^a   Vallabhaneni, Haritha ^a   Horvath, Kent ^a   Kulikowicz, Tomasz ^a   Bohr, Vilhelm A ^a   Zhang, Yanbin ^d   Lei, Ming ^a,b   Liu, Yie ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE; PROTEIN SLX1; PROTEIN SLX2; PROTEIN SLX3; PROTEIN SLX4; TELOMERIC REPEAT BINDING FACTOR 1; TELOMERIC REPEAT BINDING FACTOR 2; UNCLASSIFIED DRUG; BLOOM SYNDROME HELICASE; DNA; RECOMBINASE; RECQ HELICASE; SLX1 PROTEIN, HUMAN; SLX4 PROTEIN, HUMAN; TELOMERE BINDING PROTEIN;

ARTICLE; BINDING AFFINITY; CELL CYCLE S PHASE; CELL DIVISION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; GENETIC STABILITY; GENOTOXICITY; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; TELOMERE; CELL CYCLE; HELA CELL LINE; HOMOLOGOUS RECOMBINATION; METABOLISM; SISTER CHROMATID EXCHANGE;

CELL CYCLE; DNA; ENDONUCLEASES; HELA CELLS; HOMOLOGOUS RECOMBINATION; HUMANS; RECOMBINASES; RECQ HELICASES; SISTER CHROMATID EXCHANGE; TELOMERE; TELOMERE-BINDING PROTEINS;

EID: 84942156300     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv522     Document Type: Article

References (98)

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31. Stavropoulos, D.J., Bradshaw, P.S., Li, X., Pasic, I., Truong, K., Ikura, M., Ungrin, M. and Meyn, M.S. (2002) The Bloom syndrome helicase BLM interacts with TRF2 in ALT cells and promotes telomeric DNA synthesis. Hum. Mol. Genet., 11, 3135-3144.
32. Barefield, C. and Karlseder, J. (2012) The BLM helicase contributes to telomere maintenance through processing of late-replicating intermediate structures. Nucleic Acids Res., 40, 7358-7367.
33. Mohaghegh, P., Karow, J.K., Brosh, R.M. Jr, Bohr, V.A. and Hickson, I.D. (2001) The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res., 29, 2843-2849.
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45. Galati, A., Magdinier, F., Colasanti, V., Bauwens, S., Pinte, S., Ricordy, R., Giraud-Panis, M.J., Pusch, M.C., Savino, M., Cacchione, S. et al. (2012) TRF2 controls telomeric nucleosome organization in a cell cycle phase-dependent manner. PLoS One, 7, e34386.
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50. Palm, W. and de Lange, T. (2008) How shelterin protects mammalian telomeres. Annu. Rev. Genet., 42, 301-334.
51. Griffith, J.D., Comeau, L., Rosenfield, S., Stansel, R.M., Bianchi, A., Moss, H. and de Lange, T. (1999) Mammalian telomeres end in a large duplex loop. Cell, 97, 503-514.
52. Doksani, Y, Wu, J.Y, de Lange, T. and Zhuang, X. (2013) Super-resolution fluorescence imaging of telomeres reveals TRF2-dependent T-loop formation. Cell, 155, 345-356.
53. Cesare, A.J. and Reddel, R.R. (2010) Alternative lengthening of telomeres: models, mechanisms and implications. Nat. Rev. Genet., 11, 319-330.
54. Pickett, H.A. and Reddel, R.R. (2012) The role of telomere trimming in normal telomere length dynamics. Cell Cycle, 11, 1309-1315.
55. Croteau, D.L., Popuri, V, Opresko, P.L. and Bohr, V.A. (2014) Human RecQ helicases in DNA repair, recombination, and replication. Annu. Rev. Biochem., 83, 519-552.
56. Vannier, J.B., Sarek, G. and Boulton, S.J. (2014) RTEL1: functions of a disease-associated helicase. Trends Cell Biol, 24, 416-425.
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59. Lenain, C, Bauwens, S., Amiard, S., Brunori, M., Giraud-Panis, M.J. and Gilson, E. (2006) The Apollo 5' exonuclease functions together with TRF2 to protect telomeres from DNA repair. Curr. Biol., 16, 1303-1310.
60. Leon-Ortiz, A.M, Svendsen, J. and Boulton, S.J. (2014) Metabolism of DNA secondary structures at the eukaryotic replication fork. DNA Repair (Amst), 19, 152-162.
61. Wan, B., Yin, J., Horvath, K., Sarkar, J., Chen, Y, Wu, J., Wan, K., Lu, J., Gu, P, Yu, EY. et al. (2013) SLX4 assembles a telomere maintenance toolkit by bridging multiple endonucleases with telomeres. Cell Rep., 4, 861-869.
62. Wilson, J.S., Tejera, A.M., Castor, D., Toth, R., Blasco, M.A. and Rouse, J. (2013) Localization-dependent and -independent roles of SLX4 in regulating telomeres. Cell Rep., 4, 853-860.
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64. Zellinger, B., Akimcheva, S., Puizina, J., Schirato, M. and Riha, K. (2007) Ku suppresses formation of telomeric circles and alternative telomere lengthening in Arabidopsis. Mol. Cell, 27, 163-169.
65. Durkin, S.G. and Glover, TW. (2007) Chromosome fragile sites. Annu. Rev. Genet., 41, 169-192.
66. Sfeir, A., Kosiyatrakul, S.T, Hockemeyer, D, MacRae, S.L., Karlseder, J., Schildkraut, C.L. and de Lange, T (2009) Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell, 138, 90-103.
67. Saint-Leger, A., Koelblen, M., Civitelli, L., Bah, A., Djerbi, N, Giraud-Panis, M.J., Londono-Vallejo, A., Ascenzioni, F and Gilson, E. (2014) The basic N-terminal domain of TRF2 limits recombination endonuclease action at human telomeres. Cell Cycle, 13, 2469-2474.
68. Opresko, PL, Otterlei, M., Graakjaer, J., Bruheim, P, Dawut, L., Kolvraa, S., May, A., Seidman, M.M. and Bohr, VA. (2004) The Werner syndrome helicase and exonuclease cooperate to resolve telomeric D loops in a manner regulated by TRF1 and TRF2. Mol Cell, 14, 763-774.
69. Wang, R.C., Smogorzewska, A. and de Lange, T (2004) Homologous recombination generates T-loop-sized deletions at human telomeres. Cell, 119, 355-368.
70. Bucholc, M., Park, Y and Lustig, A.J. (2001) Intrachromatid excision of telomeric DNA as a mechanism for telomere size control in Saccharomyces cerevisiae. Mol. Cell. Biol, 21, 6559-6573.
71. Webb, C.J., Wu, Y and Zakian, VA. (2013) DNA repair at telomeres: keeping the ends intact. Cold Spring Harb. Perspect. Biol, 5, a012666.
72. Opresko, PL, von Kobbe, C, Laine, J.P, Harrigan, J., Hickson, I.D and Bohr, VA. (2002) Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J. Biol. Chem., 277, 41110-41119.
73. Machwe, A., Xiao, L. and Orren, DK. (2004) TRF2 recruits the Werner syndrome (WRN) exonuclease for processing of telomeric DNA. Oncogene, 23, 149-156.
74. Popuri, V., Hsu, J., Khadka, P., Horvath, K., Liu, Y., Croteau, D.L. and Bohr, V.A. (2014) Human RECQL1 participates in telomere maintenance. Nucleic Acids Res., 42, 5671-5688.
75. Fairall, L., Chapman, L., Moss, H., de Lange, T. and Rhodes, D. (2001) Structure of the TRFH dimerization domain of the human telomeric proteins TRF1 and TRF2. Mol. Cell, 8, 351-361.
76. Court, R., Chapman, L., Fairall, L. and Rhodes, D. (2005) How the human telomeric proteins TRF1 and TRF2 recognize telomeric DNA: a view from high-resolution crystal structures. EMBO Rep., 6, 39-45.
77. Fouche, N., Cesare, A.J., Willcox, S., Ozgur, S., Compton, S.A. and Griffith, J.D. (2006) The basic domain of TRF2 directs binding to DNA junctions irrespective of the presence of TTAGGG repeats. J. Biol. Chem., 281, 37486-37495.
78. Poulet, A., Buisson, R., Faivre-Moskalenko, C., Koelblen, M., Amiard, S., Montel, F., Cuesta-Lopez, S., Bornet, O., Guerlesquin, F., Godet, T. et al. (2009) TRF2 promotes, remodels and protects telomeric Holliday junctions. EMBO J., 28, 641-651.
79. Lillard-Wetherell, K., Machwe, A., Langland, G.T., Combs, K.A., Behbehani, G.K., Schonberg, S.A., German, J., Turchi, J.J., Orren, D.K. and Groden, J. (2004) Association and regulation of the BLM helicase by the telomere proteins TRF1 and TRF2. Hum. Mol. Genet., 13, 1919-1932.
80. Stavropoulos, D.J., Bradshaw, P.S., Li, X., Pasic, I., Truong, K., Ikura, M., Ungrin, M. and Meyn, M.S. (2002) The Bloom syndrome helicase BLM interacts with TRF2 in ALT cells and promotes telomeric DNA synthesis. Hum. Mol. Genet., 11, 3135-3144.
81. Barefield, C. and Karlseder, J. (2012) The BLM helicase contributes to telomere maintenance through processing of late-replicating intermediate structures. Nucleic Acids Res., 40, 7358-7367.
82. Mohaghegh, P., Karow, J.K., Brosh, R.M. Jr, Bohr, V.A. and Hickson, I.D. (2001) The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res., 29, 2843-2849.
83. Zeng, S., Xiang, T., Pandita, T.K., Gonzalez-Suarez, I., Gonzalo, S., Harris, C.C. and Yang, Q. (2009) Telomere recombination requires the MUS81 endonuclease. Nat. Cell Biol., 11, 616-623.
84. Calado, R.T. and Young, N.S. (2009) Telomere diseases. N. Engl. J. Med., 361, 2353-2365.
85. Taboski, M.A., Sealey, D.C., Dorrens, J., Tayade, C., Betts, D.H. and Harrington, L. (2012) Long telomeres bypass the requirement for telomere maintenance in human tumorigenesis. Cell Rep., 1, 91-98.
86. Zheng, Y.L., Zhang, F., Sun, B., Du, J., Sun, C., Yuan, J., Wang, Y., Tao, L., Kota, K., Liu, X. et al. (2014) Telomerase enzymatic component hTERT shortens long telomeres in human cells. Cell Cycle, 13, 1765-1776.
87. Verdun, R.E. and Karlseder, J. (2006) The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell, 127, 709-720.
88. Gilson, E. and Geli, V. (2007) How telomeres are replicated. Nat. Rev. Mol. Cell Biol., 8, 825-838.
89. Chow, T.T., Zhao, Y., Mak, S.S., Shay, J.W. and Wright, W.E. (2012) Early and late steps in telomere overhang processing in normal human cells: the position of the final RNA primer drives telomere shortening. Genes Dev., 26, 1167-1178.
90. Rossiello, F., Herbig, U., Longhese, M.P., Fumagalli, M. and d'Adda di Fagagna, F. (2014) Irreparable telomeric DNA damage and persistent DDR signalling as a shared causative mechanism of cellular senescence and ageing. Curr. Opin. Genet. Dev., 26, 89-95.
91. Chen, Y., Yang, Y., van Overbeek, M., Donigian, J.R., Baciu, P., de Lange, T. and Lei, M. (2008) A shared docking motif in TRF1 and TRF2 used for differential recruitment of telomeric proteins. Science, 319, 1092-1096.
92. Mattern, K.A., Swiggers, S.J., Nigg, A.L., Lowenberg, B., Houtsmuller, A.B. and Zijlmans, J.M. (2004) Dynamics of protein binding to telomeres in living cells: implications for telomere structure and function. Mol. Cell. Biol., 24, 5587-5594.
93. Wyatt, H.D., Sarbajna, S., Matos, J. and West, S.C. (2013) Coordinated actions of SLX1-SLX4 and MUS81-EME1 for Holliday junction resolution in human cells. Mol. Cell, 52, 234-247.
94. Galati, A., Magdinier, F., Colasanti, V., Bauwens, S., Pinte, S., Ricordy, R., Giraud-Panis, M.J., Pusch, M.C., Savino, M., Cacchione, S. et al. (2012) TRF2 controls telomeric nucleosome organization in a cell cycle phase-dependent manner. PLoS One, 7, e34386.
95. Vannier, J.B., Pavicic-Kaltenbrunner, V., Petalcorin, M.I., Ding, H. and Boulton, S.J. (2012) RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell, 149, 795-806.
96. Deng, Z., Glousker, G., Molczan, A., Fox, A.J., Lamm, N., Dheekollu, J., Weizman, O.E., Schertzer, M., Wang, Z., Vladimirova, O. et al. (2013) Inherited mutations in the helicase RTEL1 cause telomere dysfunction and Hoyeraal-Hreidarsson syndrome. Proc. Natl. Acad. Sci. U.S.A., 110, E3408-E3416.
97. Ballew, B.J., Yeager, M., Jacobs, K., Giri, N., Boland, J., Burdett, L., Alter, B.P. and Savage, S.A. (2013) Germline mutations of regulator of telomere elongation helicase 1, RTEL1, in Dyskeratosis congenita. Hum. Genet., 132, 473-480.
98. Schertzer, M., Jouravleva, K., Perderiset, M., Dingli, F., Loew, D., Le Guen, T., Bardoni, B., de Villartay, J., Revy, P. and Londono-Vallejo, A. (2015) Human regulator of telomere elongation helicase 1 (RTEL1) is required for nuclear and cytoplasmic trafficking of pre-U2 RNA. Nucleic Acids Res., 18, 1834-1847.