1,096
Views
6
CrossRef citations to date
0
Altmetric
Report

Expression of cancer related BRCA1 missense variants decreases MMS-induced recombination in Saccharomyces cerevisiae without altering its nuclear localization

, , &
Pages 2723-2731 | Received 18 May 2016, Accepted 15 Jul 2016, Published online: 15 Aug 2016

References

  • Powell SN, Kachnic LA. Roles of BRCA1 and BRCA2 in homologous recombination, DNA replication fidelity and the cellular response to ionizing radiation. Oncogene 2003; 22:5784-91; PMID:12947386; http://dx.doi.org/10.1038/sj.onc.1206678
  • Deng CX. BRCA1: cell cycle checkpoint, genetic instability, DNA damage response and cancer evolution. Nucleic Acids Res 2006; 34:1416-26; PMID:16522651; http://dx.doi.org/10.1093/nar/gkl010
  • Prakash R, Zhang Y, Feng W, Jasin M. Homologous recombination and human health: the roles of BRCA1, BRCA2, and associated proteins. Cold Spring Harb Perspect Biol 2015; 7:a016600; PMID:25833843; http://dx.doi.org/10.1101/cshperspect.a016600
  • King MC, Marks JH, Mandell JB. Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2. Science 2003; 302:643-6; PMID:14576434; http://dx.doi.org/10.1126/science.1088759
  • Metcalfe K, Lubinski J, Lynch HT, Ghadirian P, Foulkes WD, Kim-Sing C, Neuhausen S, Tung N, Rosen B, Gronwald J, et al. Family history of cancer and cancer risks in women with BRCA1 or BRCA2 mutations. J Natl Cancer Inst 2010; 102:1874-8; PMID:21098759; http://dx.doi.org/10.1093/jnci/djq443
  • Clark SL, Rodriguez AM, Snyder RR, Hankins GD, Boehning D. Structure-Function Of The Tumor Suppressor BRCA1. Comput Struct Biotechnol J 2012; 1:1-8; PMID:22737296
  • Wu LC, Wang ZW, Tsan JT, Spillman MA, Phung A, Xu XL, Yang MC, Hwang LY, Bowcock AM, Baer R. Identification of a RING protein that can interact in vivo with the BRCA1 gene product. Nat Genet 1996; 14:430-40; PMID:8944023; http://dx.doi.org/10.1038/ng1296-430
  • Brzovic PS, Meza JE, King MC, Klevit RE. BRCA1 RING domain cancer-predisposing mutations. Structural consequences and effects on protein-protein interactions. J Biol Chem 2001; 276:41399-406; PMID:11526114; http://dx.doi.org/10.1074/jbc.M106551200
  • Yu X, Chini CC, He M, Mer G, Chen J. The BRCT domain is a phospho-protein binding domain. Science 2003; 302:639-42; PMID:14576433; http://dx.doi.org/10.1126/science.1088753
  • Mohammad DH, Yaffe MB. 14-3-3 proteins, FHA domains and BRCT domains in the DNA damage response. DNA Repair (Amst) 2009; 8:1009-17; PMID:19481982; http://dx.doi.org/10.1016/j.dnarep.2009.04.004
  • King MC. “The race” to clone BRCA1. Science 2014; 343:1462-5; PMID:24675952; http://dx.doi.org/10.1126/science.1251900
  • Humphrey JS, Salim A, Erdos MR, Collins FS, Brody LC, Klausner RD. Human BRCA1 inhibits growth in yeast: potential use in diagnostic testing. Proc Natl Acad Sci U S A 1997; 94:5820-5; PMID:9159158; http://dx.doi.org/10.1073/pnas.94.11.5820
  • Monteiro AN, Humphrey JS. Yeast-based assays for detection and characterization of mutations in BRCA1. Breast Dis 1998; 10:61-70; PMID:15687549; http://dx.doi.org/10.3233/BD-1998-101-208
  • Coyne RS, McDonald HB, Edgemon K, Brody LC. Functional characterization of BRCA1 sequence variants using a yeast small colony phenotype assay. Cancer Biol Ther 2004; 3:453-7; PMID:15004537; http://dx.doi.org/10.4161/cbt.3.5.809
  • Millot GA, Carvalho MA, Caputo SM, Vreeswijk MP, Brown MA, Webb M, Rouleau E, Neuhausen SL, Hansen T, Galli A, et al. A guide for functional analysis of BRCA1 variants of uncertain significance. Hum Mutat 2012; 33:1526-37; PMID:22753008; http://dx.doi.org/10.1002/humu.22150
  • Jhuraney A, Velkova A, Johnson RC, Kessing B, Carvalho RS, Whiley P, Spurdle AB, Vreeswijk MP, Caputo SM, Millot GA, et al. BRCA1 Circos: a visualisation resource for functional analysis of missense variants. J Med Genet 2015; 52:224-30; PMID:25643705; http://dx.doi.org/10.1136/jmedgenet-2014-102766
  • Hashizume R, Fukuda M, Maeda I, Nishikawa H, Oyake D, Yabuki Y, Ogata H, Ohta T. The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J Biol Chem 2001; 276:14537-40; PMID:11278247; http://dx.doi.org/10.1074/jbc.C000881200
  • Mallery DL, Vandenberg CJ, Hiom K. Activation of the E3 ligase function of the BRCA1/BARD1 complex by polyubiquitin chains. Embo J 2002; 21:6755-62; PMID:12485996; http://dx.doi.org/10.1093/emboj/cdf691
  • Caligo MA, Bonatti F, Guidugli L, Aretini P, Galli A. A yeast recombination assay to characterize human BRCA1 missense variants of unknown pathological significance. Hum Mutat 2009; 30:123-33; PMID:18680205; http://dx.doi.org/10.1002/humu.20817
  • Dever SM, Golding SE, Rosenberg E, Adams BR, Idowu MO, Quillin JM, Valerie N, Xu B, Povirk LF, Valerie K. Mutations in the BRCT binding site of BRCA1 result in hyper-recombination. Aging (Albany NY) 2011; 3:515-32; PMID:21666281; http://dx.doi.org/10.18632/aging.100325
  • Woods NT, Baskin R, Golubeva V, Jhuraney A, De-Gregoriis G, Vaclova T, Goldgar DE, Couch FJ, Carvalho MA, Iversen ES, et al. Functional assays provide a robust tool for the clinical annotation of genetic variants of uncertain significance. Npj Genomic Medicine 2016; 1:16001; http://dx.doi.org/10.1038/npjgenmed.2016.1
  • Konishi H, Mohseni M, Tamaki A, Garay JP, Croessmann S, Karnan S, Ota A, Wong HY, Konishi Y, Karakas B, et al. Mutation of a single allele of the cancer susceptibility gene BRCA1 leads to genomic instability in human breast epithelial cells. Proc Natl Acad Sci U S A 2011; 108:17773-8; PMID:21987798; http://dx.doi.org/10.1073/pnas.1110969108
  • Lindor NM, Guidugli L, Wang X, Vallee MP, Monteiro AN, Tavtigian S, Goldgar DE, Couch FJ. A review of a multifactorial probability-based model for classification of BRCA1 and BRCA2 variants of uncertain significance (VUS). Hum Mutat 2012; 33:8-21; PMID:21990134; http://dx.doi.org/10.1002/humu.21627
  • Tavtigian SV, Greenblatt MS, Goldgar DE, Boffetta P. Assessing pathogenicity: overview of results from the IARC Unclassified Genetic Variants Working Group. Hum Mutat 2008; 29:1261-4; PMID:18951436; http://dx.doi.org/10.1002/humu.20903
  • Henderson BR. Regulation of BRCA1, BRCA2 and BARD1 intracellular trafficking. Bioessays 2005; 27:884-93; PMID:16108063; http://dx.doi.org/10.1002/bies.20277
  • Au WW, Henderson BR. The BRCA1 RING and BRCT domains cooperate in targeting BRCA1 to ionizing radiation-induced nuclear foci. J Biol Chem 2005; 280:6993-7001; PMID:15569676; http://dx.doi.org/10.1074/jbc.M408879200
  • Au WW, Henderson BR. Identification of sequences that target BRCA1 to nuclear foci following alkylative DNA damage. Cell Signal 2007; 19:1879-92; PMID:17531442; http://dx.doi.org/10.1016/j.cellsig.2007.04.010
  • Millot GA, Berger A, Lejour V, Boule JB, Bobo C, Cullin C, Lopes J, Stoppa-Lyonnet D, Nicolas A. Assessment of human Nter and Cter BRCA1 mutations using growth and localization assays in yeast. Hum Mutat 2011; 32:1470-80; PMID:21922593; http://dx.doi.org/10.1002/humu.21608
  • Loeb LA. Human cancers express mutator phenotypes: origin, consequences and targeting. Nat Rev Cancer 2011; 11:450-7; PMID:21593786; http://dx.doi.org/10.1038/nrc3063
  • Goode EL, Dunning AM, Kuschel B, Healey CS, Day NE, Ponder BA, Easton DF, Pharoah PP. Effect of germ-line genetic variation on breast cancer survival in a population-based study. Cancer Res 2002; 62:3052-7; PMID:12036913
  • Adem C, Soderberg CL, Hafner K, Reynolds C, Slezak JM, Sinclair CS, Sellers TA, Schaid DJ, Couch F, Hartmann LC, et al. ERBB2, TBX2, RPS6KB1, and MYC alterations in breast tissues of BRCA1 and BRCA2 mutation carriers. Genes Chromosomes Cancer 2004; 41:1-11; PMID:15236312; http://dx.doi.org/10.1002/gcc.20057
  • Wang Y, Cortez D, Yazdi P, Neff N, Elledge SJ, Qin J. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev 2000; 14:927-39; PMID:10783165
  • Li GM. Mechanisms and functions of DNA mismatch repair. Cell Res 2008; 18:85-98; PMID:18157157; http://dx.doi.org/10.1038/cr.2007.115
  • Peltomaki P. DNA mismatch repair and cancer. Mutat Res 2001; 488:77-85; PMID:11223406; http://dx.doi.org/10.1016/S1383-5742(00)00058-2
  • Peltomaki P. Role of DNA mismatch repair defects in the pathogenesis of human cancer. J Clin Oncol 2003; 21:1174-9; PMID:12637487; http://dx.doi.org/10.1200/JCO.2003.04.060
  • Kunkel TA, Erie DA. DNA mismatch repair. Annu Rev Biochem 2005; 74:681-710; PMID:15952900; http://dx.doi.org/10.1146/annurev.biochem.74.082803.133243
  • Muller A, Fishel R. Mismatch repair and the hereditary non-polyposis colorectal cancer syndrome (HNPCC). Cancer Invest 2002; 20:102-9; PMID:11852992; http://dx.doi.org/10.1081/CNV-120000371
  • Scott RJ, McPhillips M, Meldrum CJ, Fitzgerald PE, Adams K, Spigelman AD, du Sart D, Tucker K, Kirk J. Hereditary nonpolyposis colorectal cancer in 95 families: differences and similarities between mutation-positive and mutation-negative kindreds. Am J Hum Genet 2001; 68:118-27; PMID:11112663; http://dx.doi.org/10.1086/316942
  • Barrow E, Robinson L, Alduaij W, Shenton A, Clancy T, Lalloo F, Hill J, Evans DG. Cumulative lifetime incidence of extracolonic cancers in Lynch syndrome: a report of 121 families with proven mutations. Clin Genet 2009; 75:141-9; PMID:19215248; http://dx.doi.org/10.1111/j.1399-0004.2008.01125.x
  • Engel C, Loeffler M, Steinke V, Rahner N, Holinski-Feder E, Dietmaier W, Schackert HK, Goergens H, von Knebel Doeberitz M, Goecke TO, et al. Risks of less common cancers in proven mutation carriers with lynch syndrome. J Clin Oncol 2012; 30:4409-15; PMID:23091106; http://dx.doi.org/10.1200/JCO.2012.43.2278
  • Malander S, Rambech E, Kristoffersson U, Halvarsson B, Ridderheim M, Borg A, Nilbert M. The contribution of the hereditary nonpolyposis colorectal cancer syndrome to the development of ovarian cancer. Gynecol Oncol 2006; 101:238-43; PMID:16360201; http://dx.doi.org/10.1016/j.ygyno.2005.10.029
  • Watson P, Lynch HT. Cancer risk in mismatch repair gene mutation carriers. Fam Cancer 2001; 1:57-60; PMID:14574017; http://dx.doi.org/10.1023/A:1011590617833
  • Polaczek P, Putzke AP, Leong K, Bitter GA. Functional genetic tests of DNA mismatch repair protein activity in Saccharomyces cerevisiae. Gene 1998; 213:159-67; PMID:9630599; http://dx.doi.org/10.1016/S0378-1119(98)00150-4
  • Ellison AR, Lofing J, Bitter GA. Functional analysis of human MLH1 and MSH2 missense variants and hybrid human-yeast MLH1 proteins in Saccharomyces cerevisiae. Hum Mol Genet 2001; 10:1889-900; PMID:11555625; http://dx.doi.org/10.1093/hmg/10.18.1889
  • Aldred PM, Borts RH. Humanizing mismatch repair in yeast: towards effective identification of hereditary non-polyposis colorectal cancer alleles. Biochem Soc Trans 2007; 35:1525-8; PMID:18031259; http://dx.doi.org/10.1042/BST0351525
  • Gammie AE, Erdeniz N, Beaver J, Devlin B, Nanji A, Rose MD. Functional characterization of pathogenic human MSH2 missense mutations in Saccharomyces cerevisiae. Genetics 2007; 177:707-21; PMID:17720936
  • Maresca L, Spugnesi L, Lodovichi S, Cozzani C, Naccarato AG, Tancredi M, Collavoli A, Falaschi E, Rossetti E, Aretini P, et al. MSH2 role in BRCA1-driven tumorigenesis: A preliminary study in yeast and in human tumors from BRCA1-VUS carriers. Eur J Med Genet 2015; 58:531-9; PMID:26381082; http://dx.doi.org/10.1016/j.ejmg.2015.09.005
  • Sgagias MK, Wagner KU, Hamik B, Stoeger S, Spieker R, Huber LJ, Chodosh LA, Cowan KH. Brca1-deficient murine mammary epithelial cells have increased sensitivity to CDDP and MMS. Cell Cycle 2004; 3:1451-6; PMID:15492509; http://dx.doi.org/10.4161/cc.3.11.1211
  • Scully R, Chen J, Ochs RL, Keegan K, Hoekstra M, Feunteun J, Livingston DM. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 1997; 90:425-35; PMID:9267023; http://dx.doi.org/10.1016/S0092-8674(00)80503-6
  • Brodie KM, Henderson BR. Differential modulation of BRCA1 and BARD1 nuclear localisation and foci assembly by DNA damage. Cell Signal 2010; 22:291-302; PMID:19796682; http://dx.doi.org/10.1016/j.cellsig.2009.09.034
  • Henderson BR. Regulation of BRCA1, BRCA2 and BARD1 intracellular trafficking. Bioessays 2005; 27:884-93; PMID:16108063; http://dx.doi.org/10.1002/bies.20277
  • Huen MS, Sy SM, Chen J. BRCA1 and its toolbox for the maintenance of genome integrity. Nat Rev Mol Cell Biol 2010; 11:138-48; PMID:20029420; http://dx.doi.org/10.1038/nrm2831
  • Venkitaraman AR. Cancer suppression by the chromosome custodians, BRCA1 and BRCA2. Science 2014; 343:1470-5; PMID:24675954; http://dx.doi.org/10.1126/science.1252230
  • Lundin C, North M, Erixon K, Walters K, Jenssen D, Goldman AS, Helleday T. Methyl methanesulfonate (MMS) produces heat-labile DNA damage but no detectable in vivo DNA double-strand breaks. Nucleic Acids Res 2005; 33:3799-811; PMID:16009812; http://dx.doi.org/10.1093/nar/gki681
  • Galli A, Schiestl RH. Cell division transforms mutagenic lesions into deletion-recombinagenic lesions in yeast cells. Mutat Res 1999; 429:13-26; PMID:10434021; http://dx.doi.org/10.1016/S0027-5107(99)00097-4
  • Galli A, Cervelli T, Schiestl RH. Characterization of the hyperrecombination phenotype of the pol3-t mutation of Saccharomyces cerevisiae. Genetics 2003; 164:65-79; PMID:12750321
  • Kass EM, Jasin M. Collaboration and competition between DNA double-strand break repair pathways. FEBS Lett 2010; 584:3703-8; PMID:20691183; http://dx.doi.org/10.1016/j.febslet.2010.07.057
  • Li X, Heyer WD. Homologous recombination in DNA repair and DNA damage tolerance. Cell Res 2008; 18:99-113; PMID:18166982; http://dx.doi.org/10.1038/cr.2008.1
  • Westmoreland TJ, Olson JA, Saito WY, Huper G, Marks JR, Bennett CB. Dhh1 regulates the G1/S-checkpoint following DNA damage or BRCA1 expression in yeast. J Surg Res 2003; 113:62-73; PMID:12943812; http://dx.doi.org/10.1016/S0022-4804(03)00155-0
  • Bennett CB, Westmoreland TJ, Verrier CS, Blanchette CA, Sabin TL, Phatnani HP, Mishina YV, Huper G, Selim AL, Madison ER, et al. Yeast screens identify the RNA polymerase II CTD and SPT5 as relevant targets of BRCA1 interaction. PLoS ONE 2008; 3:e1448; http://dx.doi.org/10.1371/journal.pone.0001448
  • Belgareh N, Doye V. Dynamics of nuclear pore distribution in nucleoporin mutant yeast cells. J Cell Biol 1997; 136:747-59; PMID:9049242; http://dx.doi.org/10.1083/jcb.136.4.747
  • Gietz RD, Schiestl RH. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2007; 2:31-4; PMID:17401334; http://dx.doi.org/10.1038/nprot.2007.13
  • Schiestl RH, Igarashi S, Hastings PJ. Analysis of the mechanism for reversion of a disrupted gene. Genetics 1988; 119:237-47; PMID:2840335
  • Schiestl RH, Gietz RD, Mehta RD, Hastings PJ. Carcinogens induce intrachromosomal recombination in yeast. Carcinogenesis 1989; 10:1445-55; PMID:2665967; http://dx.doi.org/10.1093/carcin/10.8.1445
  • Schiestl RH. Nonmutagenic carcinogens induce intrachromosomal recombination in yeast. Nature 1989; 337:285-8; PMID:2643057; http://dx.doi.org/10.1038/337285a0

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.