The fanconi anemia proteins FANCD2 and FANCJ interact and regulate each other's chromatin localization

Journal of Biological Chemistry

Volumn 289, Issue 37, 2014, Pages 25774-25782

  Chen, Xiaoyong ^a   Wilson, James B ^b   McChesney, Patricia ^a   Williams, Stacy A ^a   Kwon, Youngho ^a   Longerich, Simonne ^a   Marriott, Andrew S ^b   Sung, Patrick ^a   Jones, Nigel J ^b   Kupfer, Gary M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN LOCALIZATION; FANCONI ANEMIAS;

FANCONI ANEMIA GROUP D2 PROTEIN; FANCONI ANEMIA PROTEIN; PROTEIN FANCJ; UNCLASSIFIED DRUG; BACH1 PROTEIN, HUMAN; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CHROMATIN; DNA BINDING PROTEIN; FANCD2 PROTEIN, HUMAN; PROTEIN BINDING;

ARTICLE; BINDING SITE; CELL LYSATE; CELLULAR DISTRIBUTION; CHROMATIN; CHROMATOGRAPHY; COMPLEX FORMATION; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; GEL FILTRATION; GENE MUTATION; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; DNA REPAIR; FANCONI ANEMIA; GENETICS; GENOMIC INSTABILITY; HUMAN; METABOLISM; MUTATION; PATHOLOGY;

BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CHROMATIN; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP D2 PROTEIN; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; GENOMIC INSTABILITY; HUMANS; MUTATION; PROTEIN BINDING;

EID: 84907164604     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.552570     Document Type: Article

References (51)

1. Alter, B. P. (2003) Cancer in Fanconi anemia, 1927-2001. Cancer 97, 425-440
2. Green, A. M., and Kupfer, G. M. (2009) Fanconi anemia. Hematol. Oncol. Clin. North Am. 23, 193-214
3. Collins, N., and Kupfer, G. M. (2005) Molecular pathogenesis of Fanconi anemia. Int. J. Hematol. 82, 176-183
4. Moldovan, G. L., and D'Andrea, A. D. (2009) How the fanconi anemia pathway guards the genome. Annu. Rev. Genet. 43, 223-249
5. Wang, W. (2007) Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat. Rev. Genet. 8, 735-748
6. Constantinou, A. (2012) Rescue of replication failure by Fanconi anaemia proteins. Chromosoma 121, 21-36
7. Kee, Y., and D'Andrea, A. D. (2012) Molecular pathogenesis and clinical management of Fanconi anemia. J. Clin. Invest. 122, 3799-3806
8. Garaycoechea, J. I., and Patel, K. J. (2014) Why does the bone marrow fail in Fanconi anemia? Blood 123, 26-34
9. Kee, Y., and D'Andrea, A. D. (2010) Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev. 24, 1680-1694
10. Kupfer, G. M., Yamashita, T., Naf, D., Suliman, A., Asano, S., and D'Andrea, A. D. (1997) The Fanconi anemia polypeptide, FAC, binds to the cyclin-dependent kinase, cdc2. Blood 90, 1047-1054
11. Thomashevski, A., High, A. A., Drozd, M., Shabanowitz, J., Hunt, D. F., Grant, P. A., and Kupfer, G. M. (2004) The Fanconi anemia core complex forms four complexes of different sizes in different subcellular compartments. J. Biol. Chem. 279, 26201-26209
12. Waisfisz, Q., de Winter, J. P., Kruyt, F. A., de Groot, J., van der Weel, L., Dijkmans, L. M., Zhi, Y., Arwert, F., Scheper, R. J., Youssoufian, H., Hoatlin, M. E., and Joenje, H. (1999) A physical complex of the Fanconi anemia proteins FANCG/XRCC9 and FANCA. Proc. Natl. Acad. Sci. U.S.A. 96, 10320-10325
13. Yamashita, T., Kupfer, G. M., Naf, D., Suliman, A., Joenje, H., Asano, S., and D'Andrea, A. D. (1998) The fanconi anemia pathway requires FAA phosphorylation and FAA/FAC nuclear accumulation. Proc. Natl. Acad. Sci. U.S.A. 95, 13085-13090
14. Meetei, A. R., Yan, Z., and Wang, W. (2004) FANCL replaces BRCA1 as the likely ubiquitin ligase responsible for FANCD2 monoubiquitination. Cell Cycle 3, 179-181
15. Wang, X., Andreassen, P. R., and D'Andrea, A. D. (2004) Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol. Cell Biol. 24, 5850-5862
16. Andreassen, P. R., D'Andrea, A. D., and Taniguchi, T. (2004) ATR couples FANCD2 monoubiquitination to the DNA-damage response. Genes Dev. 18, 1958-1963
17. Hussain, S., Wilson, J. B., Medhurst, A. L., Hejna, J., Witt, E., Ananth, S., Davies, A., Masson, J. Y., Moses, R., West, S. C., de Winter, J. P., Ashworth, A., Jones, N. J., and Mathew, C. G. (2004) Direct interaction of FANCD2 with BRCA2 in DNA damage response pathways. Hum. Mol. Genet. 13, 1241-1248
18. Kitao, H., Yamamoto, K., Matsushita, N., Ohzeki, M., Ishiai, M., and Takata, M. (2006) Functional interplay between BRCA2/FancD1 and FancC in DNA repair. J. Biol. Chem. 281, 21312-21320
19. Wang, X., and D'Andrea, A. D. (2004) The interplay of Fanconi anemia proteins in the DNA damage response. DNA Repair 3, 1063-1069
20. Garcia-Higuera, I., Taniguchi, T., Ganesan, S., Meyn, M. S., Timmers, C., Hejna, J., Grompe, M., and D'Andrea, A. D. (2001) Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell 7, 249-262
21. Howlett, N. G., Taniguchi, T., Olson, S., Cox, B., Waisfisz, Q., De Die-Smulders, C., Persky, N., Grompe, M., Joenje, H., Pals, G., Ikeda, H., Fox, E. A., and D'Andrea, A. D. (2002) Biallelic inactivation of BRCA2 in Fanconi anemia. Science 297, 606-609
22. Reid, S., Schindler, D., Hanenberg, H., Barker, K., Hanks, S., Kalb, R., Neveling, K., Kelly, P., Seal, S., Freund, M., Wurm, M., Batish, S. D., Lach, F. P., Yetgin, S., Neitzel, H., Ariffin, H., Tischkowitz, M., Mathew, C. G., Auerbach, A. D., and Rahman, N. (2007) Biallelic mutations in PALB2 cause Fanconi anemia subtype FA-N and predispose to childhood cancer. Nat. Genet. 39, 162-164
23. Xia, B., Dorsman, J. C., Ameziane, N., de Vries, Y., Rooimans, M. A., Sheng, Q., Pals, G., Errami, A., Gluckman, E., Llera, J., Wang, W., Livingston, D. M., Joenje, H., and de Winter, J. P. (2007) Fanconi anemia is associated with a defect in the BRCA2 partner PALB2. Nat. Genet. 39, 159-161
24. 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
25. Cantor, S., Drapkin, R., Zhang, F., Lin, Y., Han, J., Pamidi, S., and Livingston, D. M. (2004) The BRCA1-associated protein BACH1 is a DNA helicase targeted by clinically relevant inactivating mutations. Proc. Natl. Acad. Sci. U.S.A. 101, 2357-2362
26. Levitus, M., Waisfisz, Q., Godthelp, B. C., de Vries, Y., Hussain, S., Wiegant, W. W., Elghalbzouri-Maghrani, E., Steltenpool, J., Rooimans, M. A., Pals, G., Arwert, F., Mathew, C. G., Zdzienicka, M. Z., Hiom, K., De Winter, J. P., and Joenje, H. (2005) The DNA helicase BRIP1 is defective in Fanconi anemia complementation group J. Nat. Genet. 37, 934-935
27. Litman, R., Peng, M., Jin, Z., Zhang, F., Zhang, J., Powell, S., Andreassen, P. R., and Cantor, S. B. (2005) BACH1 is critical for homologous recombination and appears to be the Fanconi anemia gene product FANCJ. Cancer Cell 8, 255-265
28. Seal, S., Thompson, D., Renwick, A., Elliott, A., Kelly, P., Barfoot, R., Chagtai, T., Jayatilake, H., Ahmed, M., Spanova, K., North, B., McGuffog, L., Evans, D. G., Eccles, D., Easton, D. F., Stratton, M. R., and Rahman, N. (2006) Truncating mutations in the Fanconi anemia J gene BRIP1 are low-penetrance breast cancer susceptibility alleles. Nat. Genet. 38, 1239-1241
29. Zhang, F., Fan, Q., Ren, K., Auerbach, A. D., and Andreassen, P. R. (2010) FANCJ/BRIP1 recruitment and regulation of FANCD2 in DNA damage responses. Chromosoma 119, 637-649
30. Collins, N. B., Wilson, J. B., Bush, T., Thomashevski, A., Roberts, K. J., Jones, N. J., and Kupfer, G. M. (2009) ATR-dependent phosphorylation of FANCA on serine 1449 after DNA damage is important for FA pathway function. Blood 113, 2181-2190
31. Wilson, J. B., Yamamoto, K., Marriott, A. S., Hussain, S., Sung, P., Hoatlin, M. E., Mathew, C. G., Takata, M., Thompson, L. H., Kupfer, G. M., and Jones, N. J. (2008) FANCG promotes formation of a newly identified protein complex containing BRCA2, FANCD2 and XRCC3. Oncogene 27, 3641-3652
32. Park, W. H., Margossian, S., Horwitz, A. A., Simons, A. M., D'Andrea, A. D., and Parvin, J. D. (2005) Direct DNA binding activity of the Fanconi anemia D2 protein. J. Biol. Chem. 280, 23593-23598
33. Montes de Oca, R., Andreassen, P. R., Margossian, S. P., Gregory, R. C., Taniguchi, T., Wang, X., Houghtaling, S., Grompe, M., and D'Andrea, A. D. (2005) Regulated interaction of the Fanconi anemia protein, FANCD2, with chromatin. Blood 105, 1003-1009
34. Thompson, L. H., and Hinz, J. M. (2009) Cellular and molecular consequences of defective Fanconi anemia proteins in replication-coupled DNA repair: mechanistic insights. Mutat. Res. 668, 54-72
35. Xie, J., Guillemette, S., Peng, M., Gilbert, C., Buermeyer, A., and Cantor, S. B. (2010) An MLH1 mutation links BACH1/FANCJ to colon cancer, signaling, and insight toward directed therapy. Cancer Prev. Res. (Phila.) 3, 1409-1416
36. Garcia-Higuera, I., Kuang, Y., Näf, D., Wasik, J., and D'Andrea, A. D. (1999) Fanconi anemia proteins FANCA, FANCC, and FANCG/XRCC9 interact in a functional nuclear complex. Mol. Cell Biol. 19, 4866-4873
37. Peng, M., Litman, R., Jin, Z., Fong, G., and Cantor, S. B. (2006) BACH1 is a DNA repair protein supporting BRCA1 damage response. Oncogene 25, 2245-2253
38. Levran, O., Attwooll, C., Henry, R. T., Milton, K. L., Neveling, K., Rio, P., Batish, S. D., Kalb, R., Velleuer, E., Barral, S., Ott, J., Petrini, J., Schindler, D., Hanenberg, H., and Auerbach, A. D. (2005) The BRCA1-interacting helicase BRIP1 is deficient in Fanconi anemia. Nat. Genet. 37, 931-933
39. Matsushita, N., Kitao, H., Ishiai, M., Nagashima, N., Hirano, S., Okawa, K., Ohta, T., Yu, D. S., McHugh, P. J., Hickson, I. D., Venkitaraman, A. R., Kurumizaka, H., and Takata, M. (2005) A FancD2-monoubiquitin fusion reveals hidden functions of Fanconi anemia core complex in DNA repair. Mol. Cell 19, 841-847
40. Vandenberg, C. J., Gergely, F., Ong, C. Y., Pace, P., Mallery, D. L., Hiom, K., and Patel, K. J. (2003) BRCA1-independent ubiquitination of FANCD2. Mol. Cell 12, 247-254
41. Bogliolo, M., Lyakhovich, A., Callén, E., Castellà, M., Cappelli, E., Ramírez, M. J., Creus, A., Marcos, R., Kalb, R., Neveling, K., Schindler, D., and Surrallés, J. (2007) Histone H2AX and Fanconi anemia FANCD2 function in the same pathway to maintain chromosome stability. EMBO J. 26, 1340-1351
42. Cantor, S. B., Bell, D. W., Ganesan, S., Kass, E. M., Drapkin, R., Grossman, S., Wahrer, D. C., Sgroi, D. C., Lane, W. S., Haber, D. A., and Livingston, D. M. (2001) BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function. Cell 105, 149-160
43. Sobhian, B., Shao, G., Lilli, D. R., Culhane, A. C., Moreau, L. A., Xia, B., Livingston, D. M., and Greenberg, R. A. (2007) RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316, 1198-1202
44. Wang, B., Matsuoka, S., Ballif, B. A., Zhang, D., Smogorzewska, A., Gygi, S. P., and Elledge, S. J. (2007) Abraxas and RAP80 form a BRCA1 protein complex required for theDNAdamage response. Science 316, 1194-1198
45. Gupta, R., Sharma, S., Sommers, J. A., Kenny, M. K., Cantor, S. B., and Brosh, R. M., Jr. (2007) FANCJ (BACH1) helicase forms DNA damage inducible foci with replication proteinAand interacts physically and functionally with the single-stranded DNA-binding protein. Blood 110, 2390-2398
46. Krejci, L., Van Komen, S., Li, Y., Villemain, J., Reddy, M. S., Klein, H., Ellenberger, T., and Sung, P. (2003) DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423, 305-309
47. Sommers, J. A., Rawtani, N., Gupta, R., Bugreev, D. V., Mazin, A. V., Cantor, S. B., and Brosh, R. M., Jr. (2009) FANCJ uses its motor ATPase to destabilize protein-DNA complexes, unwind triplexes, and inhibit RAD51 strand exchange. J. Biol. Chem. 284, 7505-7517
48. London, T. B., Barber, L. J., Mosedale, G., Kelly, G. P., Balasubramanian, S., Hickson, I. D., Boulton, S. J., and Hiom, K. (2008) FANCJ is a structurespecific DNA helicase associated with the maintenance of genomic G/C tracts. J. Biol. Chem. 283, 36132-36139
49. Wu, Y., Shin-ya, K., and Brosh, R. M., Jr. (2008) FANCJ helicase defective in Fanconia anemia and breast cancer unwinds G-quadruplex DNA to defend genomic stability. Mol. Cell Biol. 28, 4116-4128
50. Gong, Z., Kim, J. E., Leung, C. C., Glover, J. N., and Chen, J. (2010) BACH1/ FANCJ acts with TopBP1 and participates early in DNA replication checkpoint control. Mol. Cell 37, 438-446
51. Wu, Y., and Brosh, R. M., Jr. (2009) FANCJ helicase operates in the Fanconi AnemiaDNArepair pathway and the response to replicational stress. Curr. Mol. Med. 9, 470-482