Functional and mutational landscapes of BRCA1 for homology-directed repair and therapy resistance

eLife

Volumn 6, Issue , 2017, Pages

  Anantha, Rachel W ^a,b   Simhadri, Srilatha ^a,b,c   Foo, Tzeh Keong ^a,b   Miao, Susanna ^b   Liu, Jingmei ^a,b   Shen, Zhiyuan ^a,b   Ganesan, Shridar ^a,b,c   Xia, Bing ^a  

^a RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; CISPLATIN; COMPLEMENTARY DNA; OLAPARIB; RAD52 PROTEIN; UBIQUITIN PROTEIN LIGASE E3; ANTINEOPLASTIC AGENT; BRCA1 PROTEIN, HUMAN; MUTANT PROTEIN; PHTHALAZINE DERIVATIVE; PIPERAZINE DERIVATIVE;

ARTICLE; BREAST CANCER; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA TRANSFECTION; GENETIC VARIABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MISSENSE MUTATION; MUTAGENESIS; MUTANT; OVARY CANCER; PLASMID; RECEIVER OPERATING CHARACTERISTIC; RECOMBINATION REPAIR; SENSITIVITY AND SPECIFICITY; SEQUENCE HOMOLOGY; SUMOYLATION; THERAPY RESISTANCE; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING; BASE PAIRING; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DRUG RESISTANCE; GENETICS; METABOLISM; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; BASE PAIRING; BRCA1 PROTEIN; CELL LINE, TUMOR; CISPLATIN; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DRUG RESISTANCE, NEOPLASM; HOMOLOGOUS RECOMBINATION; HUMANS; MUTANT PROTEINS; PHTHALAZINES; PIPERAZINES;

EID: 85019854232     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.21350     Document Type: Article

References (58)

1. Bouwman P, van der Gulden H, van der Heijden I, Drost R, Klijn CN, Prasetyanti P, Pieterse M, Wientjens E, Seibler J, Hogervorst FB, Jonkers J. 2013. A high-throughput functional complementation assay for classification of BRCA1 missense variants. Cancer Discovery 3: 1142-1155. doi: 10.1158/2159-8290.CD-13-0094, PMID: 23867111
2. Brzovic PS, Keeffe JR, Nishikawa H, Miyamoto K, Fox D, Fukuda M, Ohta T, Klevit R. 2003. Binding and recognition in the assembly of an active BRCA1/BARD1 ubiquitin-ligase complex. PNAS 100: 5646-5651. doi: 10.1073/pnas.0836054100, PMID: 12732733
3. Bunting SF, Callén E, Wong N, Chen HT, Polato F, Gunn A, Bothmer A, Feldhahn N, Fernandez-Capetillo O, Cao L, Xu X, Deng CX, Finkel T, Nussenzweig M, Stark JM, Nussenzweig A. 2010. 53bp1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141: 243-254. doi: 10.1016/j.cell.2010.03.012, PMID: 20362325
4. Cantor SB, Bell DW, Ganesan S, Kass EM, Drapkin R, Grossman S, Wahrer DC, Sgroi DC, Lane WS, Haber DA, Livingston DM. 2001. BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function. Cell 105: 149-160. doi: 10.1016/S0092-8674(01)00304-X, PMID: 11301010
5. Chang S, Biswas K, Martin BK, Stauffer S, Sharan SK. 2009. Expression of human BRCA1 variants in mouse ES cells allows functional analysis of BRCA1 mutations. Journal of Clinical Investigation 119: 3160-3171. doi: 10.1172/JCI39836, PMID: 19770520
6. Chen CF, Li S, Chen Y, Chen PL, Sharp ZD, Lee WH. 1996. The nuclear localization sequences of the BRCA1 protein interact with the importin-alpha subunit of the nuclear transport signal receptor. Journal of Biological Chemistry 271: 32863-32868. doi: 10.1074/jbc.271.51.32863, PMID: 8955125
7. Chen J, Silver DP, Walpita D, Cantor SB, Gazdar AF, Tomlinson G, Couch FJ, Weber BL, Ashley T, Livingston DM, Scully R. 1998. Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells. Molecular Cell 2: 317-328. doi: 10.1016/S1097-2765(00)80276-2, PMID: 9774 970
8. Couch FJ, Nathanson KL, Offit K. 2014. Two decades after BRCA: setting paradigms in personalized Cancer care and prevention. Science 343: 1466-1470. doi: 10.1126/science.1251827, PMID: 24675953
9. Deng CX. 2006. BRCA1: cell cycle checkpoint, genetic instability, DNA damage response and Cancer evolution. Nucleic Acids Research 34: 1416-1426. doi: 10.1093/nar/gkl010, PMID: 16522651
10. Densham RM, Garvin AJ, Stone HR, Strachan J, Baldock RA, Daza-Martin M, Fletcher A, Blair-Reid S, Beesley J, Johal B, Pearl LH, Neely R, Keep NH, Watts FZ, Morris JR. 2016. Human BRCA1-BARD1 ubiquitin ligase activity counteracts chromatin barriers to DNA resection. Nature Structural & Molecular Biology 23: 647-655. doi: 10.1038/nsmb.3236, PMID: 27239795
11. Drost R, Bouwman P, Rottenberg S, Boon U, Schut E, Klarenbeek S, Klijn C, van der Heijden I, van der Gulden H, Wientjens E, Pieterse M, Catteau A, Green P, Solomon E, Morris JR, Jonkers J. 2011. BRCA1 RING function is essential for tumor suppression but dispensable for therapy resistance. Cancer Cell 20: 797-809. doi: 10.1016/j.ccr.2011.11.014, PMID: 22172724
12. Elstrodt F, Hollestelle A, Nagel JH, Gorin M, Wasielewski M, van den Ouweland A, Merajver SD, Ethier SP, Schutte M. 2006. BRCA1 mutation analysis of 41 human breast Cancer cell lines reveals three new deleterious mutants. Cancer Research 66: 41-45. doi: 10.1158/0008-5472.CAN-05-2853, PMID: 16397213
13. Fabbro M, Rodriguez JA, Baer R, Henderson BR. 2002. BARD1 induces BRCA1 intranuclear foci formation by increasing RING-dependent BRCA1 nuclear import and inhibiting BRCA1 nuclear export. Journal of Biological Chemistry 277: 21315-21324. doi: 10.1074/jbc.M200769200, PMID: 11925436
14. Fackenthal JD, Olopade OI. 2007. Breast Cancer risk associated with BRCA1 and BRCA2 in diverse populations. Nature Reviews Cancer 7: 937-948. doi: 10.1038/nrc2054, PMID: 18034184
15. Foo TK, Tischkowitz M, Simhadri S, Boshari T, Zayed N, Burke KA, Berman SH, Blecua P, Riaz N, Huo Y, Ding YC, Neuhausen SL, Weigelt B, Reis-Filho JS, Foulkes WD, Xia B. 2017. Compromised BRCA1-PALB2 interaction is associated with breast Cancer risk. Oncogene. doi: 10.1038/onc.2017.46, PMID: 28319063
16. Greenberg RA, Sobhian B, Pathania S, Cantor SB, Nakatani Y, Livingston DM. 2006. Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. Genes & Development 20: 34-46. doi: 10.1101/gad.1381306, PMID: 16391231
17. Guidugli L, Pankratz VS, Singh N, Thompson J, Erding CA, Engel C, Schmutzler R, Domchek S, Nathanson K, Radice P, Singer C, Tonin PN, Lindor NM, Goldgar DE, Couch FJ. 2013. A classification model for BRCA2 DNA binding domain missense variants based on homology-directed repair activity. Cancer Research 73: 265-275. doi: 10.1158/0008-5472.CAN-12-2081, PMID: 23108138
18. Gunn A, Stark JM. 2012. I-SceI-based assays to examine distinct repair outcomes of mammalian chromosomal double strand breaks. Methods in Molecular Biology 920: 379-391. doi: 10.1007/978-1-61779-998-3_27, PMID: 22941618
19. Hashizume R, Fukuda M, Maeda I, Nishikawa H, Oyake D, Yabuki Y, Ogata H, Ohta T. 2001. The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. Journal of Biological Chemistry 276: 14537-14540. doi: 10.1074/jbc.C000881200, PMID: 11278247
20. Huen MS, Sy SM, Chen J. 2010. BRCA1 and its toolbox for the maintenance of genome integrity. Nature Reviews Molecular Cell Biology 11: 138-148. doi: 10.1038/nrm2831, PMID: 20029420
21. Jensen RB, Carreira A, Kowalczykowski SC. 2010. Purified human BRCA2 stimulates RAD51-mediated recombination. Nature 467: 678-683. doi: 10.1038/nature09399, PMID: 20729832
22. Jiang Q, Greenberg RA. 2015. Deciphering the BRCA1 tumor Suppressor Network. Journal of Biological Chemistry 290: 17724-17732. doi: 10.1074/jbc.R115.667931, PMID: 26048987
23. Li ML, Greenberg RA. 2012. Links between genome integrity and BRCA1 tumor suppression. Trends in Biochemical Sciences 37: 418-424. doi: 10.1016/j.tibs.2012.06.007, PMID: 22836122
24. Liu J, Doty T, Gibson B, Heyer WD. 2010. Human BRCA2 protein promotes RAD51 filament formation on RPA- covered single-stranded DNA. Nature Structural & Molecular Biology 17: 1260-1262. doi: 10.1038/nsmb.1904, PMID: 20729859
25. Lord CJ, Ashworth A. 2013. Mechanisms of resistance to therapies targeting BRCA-mutant cancers. Nature Medicine 19: 1381-1388. doi: 10.1038/nm.3369, PMID: 24202391
26. Lord CJ, Ashworth A. 2016. BRCAness revisited. Nature Reviews Cancer 16: 110-120. doi: 10.1038/nrc.2015.21, PMID: 26775620
27. Lu C, Xie M, Wendl MC, Wang J, McLellan MD, Leiserson MD, Huang KL, Wyczalkowski MA, Jayasinghe R, Banerjee T, Ning J, Tripathi P, Zhang Q, Niu B, Ye K, Schmidt HK, Fulton RS, McMichael JF, Batra P, Kandoth C, et al. 2015. Patterns and functional implications of rare germline variants across 12 cancer types. Nature Communications 6: 10086. doi: 10.1038/ncomms10086, PMID: 26689913
28. Ma J, Cai H, Wu T, Sobhian B, Huo Y, Alcivar A, Mehta M, Cheung KL, Ganesan S, Kong AN, Zhang DD, Xia B. 2012. PALB2 interacts with KEAP1 to promote NRF2 nuclear accumulation and function. Molecular and Cellular Biology 32: 1506-1517. doi: 10.1128/MCB.06271-11, PMID: 22331464
29. Millot GA, Carvalho MA, Caputo SM, Vreeswijk MP, Brown MA, Webb M, Rouleau E, Neuhausen SL, Hansen T, Galli A, Brandão RD, Blok MJ, Velkova A, Couch FJ, Monteiro AN, ENIGMA Consortium Functional Assay Working Group. 2012. A guide for functional analysis of BRCA1 variants of uncertain significance. Human Mutation 33: 1526-1537. doi: 10.1002/humu.22150, PMID: 22753008
30. Morris JR, Boutell C, Keppler M, Densham R, Weekes D, Alamshah A, Butler L, Galanty Y, Pangon L, Kiuchi T, Ng T, Solomon E. 2009. The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462: 886-890. doi: 10.1038/nature08593, PMID: 20016594
31. Mortensen UH, Bendixen C, Sunjevaric I, Rothstein R. 1996. DNA strand annealing is promoted by the yeast Rad52 protein. PNAS 93: 10729-10734. doi: 10.1073/pnas.93.20.10729, PMID: 8855248
32. Moynahan ME, Jasin M. 2010. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nature Reviews Molecular Cell Biology 11: 196-207. doi: 10.1038/nrm2851, PMID: 20177395
33. Mullan PB, Quinn JE, Harkin DP. 2006. The role of BRCA1 in transcriptional regulation and cell cycle control. Oncogene 25: 5854-5863. doi: 10.1038/sj.onc.1209872, PMID: 16998500
34. Nakanishi K, Yang YG, Pierce AJ, Taniguchi T, Digweed M, D’Andrea AD, Wang ZQ, Jasin M. 2005. Human fanconi Anemia monoubiquitination pathway promotes homologous DNA repair. PNAS 102: 1110-1115. doi: 10.1073/pnas.0407796102, PMID: 15650050
35. Obermeier K, Sachsenweger J, Friedl TW, Pospiech H, Winqvist R, Wiesmüller L. 2016. Heterozygous PALB2 c. 1592delt mutation channels DNA double-strand break repair into error-prone pathways in breast Cancer patients. Oncogene 35: 3796-3806. doi: 10.1038/onc.2015.448, PMID: 26640152
36. Oliver AW, Swift S, Lord CJ, Ashworth A, Pearl LH. 2009. Structural basis for recruitment of BRCA2 by PALB2. EMBO Reports 10: 990-996. doi: 10.1038/embor.2009.126, PMID: 19609323
37. Polato F, Callen E, Wong N, Faryabi R, Bunting S, Chen HT, Kozak M, Kruhlak MJ, Reczek CR, Lee WH, Ludwig T, Baer R, Feigenbaum L, Jackson S, Nussenzweig A. 2014. CtIP-mediated resection is essential for viability and can operate independently of BRCA1. The Journal of Experimental Medicine 211: 1027-1036. doi: 10.1084/jem.20131939, PMID: 24842372
38. Ransburgh DJ, Chiba N, Ishioka C, Toland AE, Parvin JD. 2010. Identification of breast tumor mutations in BRCA1 that abolish its function in homologous DNA recombination. Cancer Research 70: 988-995. doi: 10.1158/0008-5472.CAN-09-2850, PMID: 20103620
39. Reczek CR, Szabolcs M, Stark JM, Ludwig T, Baer R. 2013. The interaction between CtIP and BRCA1 is not essential for resection-mediated DNA repair or tumor suppression. The Journal of Cell Biology 201: 693-707. doi: 10.1083/jcb.201302145, PMID: 23712259
40. Reid LJ, Shakya R, Modi AP, Lokshin M, Cheng JT, Jasin M, Baer R, Ludwig T. 2008. E3 ligase activity of BRCA1 is not essential for mammalian cell viability or homology-directed repair of double-strand DNA breaks. PNAS 105: 20876-20881. doi: 10.1073/pnas.0811203106, PMID: 19088202
41. Rodriguez JA, Au WW, Henderson BR. 2004. Cytoplasmic mislocalization of BRCA1 caused by cancer-associated mutations in the BRCT domain. Experimental Cell Research 293: 14-21. doi: 10.1016/j.yexcr.2003.09.027, PMID: 14729053
42. Rodríguez JA, Henderson BR. 2000. Identification of a functional nuclear export sequence in BRCA1. Journal of Biological Chemistry 275: 38589-38596. doi: 10.1074/jbc.M003851200, PMID: 10991937
43. Roy R, Chun J, Powell SN. 2012. BRCA1 and BRCA2: different roles in a common pathway of genome protection. Nature Reviews Cancer 12: 68-78. doi: 10.1038/nrc3181
44. Ruffner H, Joazeiro CA, Hemmati D, Hunter T, Verma IM. 2001. Cancer-predisposing mutations within the RING domain of BRCA1: loss of ubiquitin protein ligase activity and protection from radiation hypersensitivity. PNAS 98: 5134-5139. doi: 10.1073/pnas.081068398, PMID: 11320250
45. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, Baer R, Lukas J, Jackson SP. 2007. Human CtIP promotes DNA end resection. Nature 450: 509-514. doi: 10.1038/nature06337, PMID: 17965729
46. Scully R, Chen J, Plug A, Xiao Y, Weaver D, Feunteun J, Ashley T, Livingston DM. 1997. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell 88: 265-275. doi: 10.1016/S0092-8674(00)81847-4, PMID: 9008167
47. Shakya R, Reid LJ, Reczek CR, Cole F, Egli D, Lin CS, deRooij DG, Hirsch S, Ravi K, Hicks JB, Szabolcs M, Jasin M, Baer R, Ludwig T. 2011. BRCA1 tumor suppression depends on BRCT phosphoprotein binding, but not its E3 ligase activity. Science 334: 525-528. doi: 10.1126/science.1209909, PMID: 22034435
48. Shakya R, Szabolcs M, McCarthy E, Ospina E, Basso K, Nandula S, Murty V, Baer R, Ludwig T. 2008. The basal- like mammary carcinomas induced by Brca1 or Bard1 inactivation implicate the BRCA1/BARD1 heterodimer in tumor suppression. PNAS 105: 7040-7045. doi: 10.1073/pnas.0711032105, PMID: 18443292
49. Stark JM, Pierce AJ, Oh J, Pastink A, Jasin M. 2004. Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Molecular and Cellular Biology 24: 9305-9316. doi: 10.1128/MCB.24.21.9305-9316.2004, PMID: 15485900
50. Sy SM, Huen MS, Chen J. 2009. PALB2 is an integral component of the BRCA complex required for homologous recombination repair. PNAS 106: 7155-7160. doi: 10.1073/pnas.0811159106, PMID: 19369211
51. Towler WI, Zhang J, Ransburgh DJ, Toland AE, Ishioka C, Chiba N, Parvin JD. 2013. Analysis of BRCA1 variants in double-strand break repair by homologous recombination and single-strand annealing. Human Mutation 34: 439-445. doi: 10.1002/humu.22251, PMID: 23161852
52. Tutt A, Bertwistle D, Valentine J, Gabriel A, Swift S, Ross G, Griffin C, Thacker J, Ashworth A. 2001. Mutation in Brca2 stimulates error-prone homology-directed repair of DNA double-strand breaks occurring between repeated sequences. The EMBO Journal 20: 4704-4716. doi: 10.1093/emboj/20.17.4704, PMID: 11532935
53. Venkitaraman AR. 2014. Cancer suppression by the chromosome custodians, BRCA1 and BRCA2. Science 343: 1470-1475. doi: 10.1126/science.1252230, PMID: 24675954
54. Wang B, Matsuoka S, Ballif BA, Zhang D, Smogorzewska A, Gygi SP, Elledge SJ. 2007. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316: 1194-1198. doi: 10.1126/science.1139476, PMID: 17525340
55. Wu LC, Wang ZW, Tsan JT, Spillman MA, Phung A, Xu XL, Yang MC, Hwang LY, Bowcock AM, Baer R. 1996. Identification of a RING protein that can interact in vivo with the BRCA1 gene product. Nature Genetics 14: 430-440. doi: 10.1038/ng1296-430, PMID: 8944023
56. Xia B, Sheng Q, Nakanishi K, Ohashi A, Wu J, Christ N, Liu X, Jasin M, Couch FJ, Livingston DM. 2006. Control of BRCA2 cellular and clinical functions by a nuclear partner, PALB2. Molecular Cell 22: 719-729. doi: 10.1016/j.molcel.2006.05.022, PMID: 16793542
57. Zhang F, Fan Q, Ren K, Andreassen PR. 2009a. PALB2 functionally connects the breast Cancer susceptibility proteins BRCA1 and BRCA2. Molecular Cancer Research 7: 1110-1118. doi: 10.1158/1541-7786.MCR-09-0123, PMID: 19584259
58. Zhang F, Ma J, Wu J, Ye L, Cai H, Xia B, Yu X. 2009b. PALB2 links BRCA1 and BRCA2 in the DNA-damage response. Current Biology 19: 524-529. doi: 10.1016/j.cub.2009.02.018, PMID: 19268590