BRCA1 haploinsufficiency leads to altered expression of genes involved in cellular proliferation and development

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Feilotter, Harriet E ^a,b   Michel, Claire ^a   Uy, Paolo ^a   Bathurst, Lauren ^a   Davey, Scott ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BCR GENE; BIOASSAY; CD24 GENE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; CSRP2 GENE; CXCR3 GENE; CYP1B1 GENE; DUSP23 GENE; ENPP2 GENE; ETV7 GENE; FAM79B GENE; FCGRT GENE; FOXP1 GENE; FYN GENE; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE IDENTIFICATION; GENE LOSS; GENE MUTATION; GENOME; GLDC GENE; HAPLOINSUFFICIENCY; HLA DMB; IFI44L GENE; IFIT1 GENE; IFIT2 GENE; IFIT3 GENE; IFNA4 GENE; IFNA5 GENE; IFNG GENE; IGHD GENE; IGHG1 GENE; IL18BP GENE; JAKMIP2 GENE; LAG3 GENE; LFNG GENE; LYMPHOBLASTOID CELL LINE; MMP7 GENE; MX1 GENE; MX2 GENE; NUCLEOTIDE SEQUENCE; PLA2G4A GENE; PRLR GENE; PWWP2 GENE; PXDN GENE; SERPINF1 GENE; SLC16A10 GENE; SOX4 GENE; TBX21 GENE; TNS4 GENE; TUMOR SUPPRESSOR GENE; UBD GENE; USP18 GENE; ZBED3 GENE; ZBTB38 GENE; CARCINOGENESIS; EPSTEIN BARR VIRUS; GENETIC TRANSCRIPTION; GENETICS; HETEROZYGOTE; HUMAN; HUMAN GENOME; LYMPHOCYTE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; VIROLOGY; VIRUS CELL TRANSFORMATION;

INTERFERON;

CARCINOGENESIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, VIRAL; GENE EXPRESSION PROFILING; GENES, BRCA1; GENOME, HUMAN; HAPLOINSUFFICIENCY; HERPESVIRUS 4, HUMAN; HETEROZYGOTE; HUMANS; INTERFERONS; LYMPHOCYTES; TRANSCRIPTION, GENETIC;

EID: 84903546359     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100068     Document Type: Article

References (59)

1. Brody LC, Biesecker BB (1998) Breast cancer susceptibility genes. BRCA1 and BRCA2. Medicine (Baltimore) 77: 208-226. (Pubitemid 28290021)
2. Ford D, Easton DF, Stratton M, Narod S, Goldgar D, et al. (1998) Genetic heterogeneity and penetrance analysis of the BRCA1 and BRCA2 genes in breast cancer families. The Breast Cancer Linkage Consortium. Am J Hum Genet 62: 676-689. (Pubitemid 28164626)
3. Miki Y, Swensen J, Shattuck-Eidens D, Futreal PA, Harshman K, et al. (1994) A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 266: 66-71. (Pubitemid 24345325)
4. Lorick KL, Jensen JP, Fang S, Ong AM, Hatakeyama S, et al. (1999) RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc Natl Acad Sci U S A 96: 11364-11369. (Pubitemid 29487386)
5. Bork P, Hofmann K, Bucher P, Neuwald AF, Altschul SF, et al. (1997) A superfamily of conserved domains in DNA damage-responsive cell cycle checkpoint proteins. Faseb J 11: 68-76.
6. Hashizume R, Fukuda M, Maeda I, Nishikawa H, Oyake D, et al. (2001) The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. The Journal of biological chemistry 276: 14537- 14540.
7. Chen A, Kleiman FE, Manley JL, Ouchi T, Pan ZQ (2002) Autoubiquitination of the BRCA1*BARD1 RING ubiquitin ligase. The Journal of biological chemistry 277: 22085-22092. (Pubitemid 34952363)
8. Zhu Q, Pao GM, Huynh AM, Suh H, Tonnu N, et al. (2011) BRCA1 tumour suppression occurs via heterochromatin-mediated silencing. Nature 477: 179- 184.
9. Starita LM, Machida Y, Sankaran S, Elias JE, Griffin K, et al. (2004) BRCA1- dependent ubiquitination of gamma-tubulin regulates centrosome number. Molecular and cellular biology 24: 8457-8466. (Pubitemid 39245068)
10. Fabbro M, Savage K, Hobson K, Deans AJ, Powell SN, et al. (2004) BRCA1- BARD1 complexes are required for p53Ser-15 phosphorylation and a G1/S arrest following ionizing radiation-induced DNA damage. The Journal of biological chemistry 279: 31251-31258. (Pubitemid 39037790)
11. Xu B, O'Donnell AH, Kim ST, Kastan MB (2002) Phosphorylation of serine 1387 in Brca1 is specifically required for the Atm-mediated S-phase checkpoint after ionizing irradiation. Cancer research 62: 4588-4591.
12. Cortez D, Wang Y, Qin J, Elledge SJ (1999) Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks. Science 286: 1162-1166.
13. Xu B, Kim S, Kastan MB (2001) Involvement of Brca1 in S-phase and G(2)- phase checkpoints after ionizing irradiation. Molecular and cellular biology 21: 3445-3450. (Pubitemid 32381780)
14. Yarden RI, Pardo-Reoyo S, Sgagias M, Cowan KH, Brody LC (2002) BRCA1 regulates the G2/M checkpoint by activating Chk1 kinase upon DNA damage. Nat Genet 30: 285-289.
15. Xu X, Weaver Z, Linke SP, Li C, Gotay J, et al. (1999) Centrosome amplification and a defective G2-M cell cycle checkpoint induce genetic instability in BRCA1 exon 11 isoform-deficient cells. Molecular cell 3: 389-395. (Pubitemid 29290679)
16. Scully R, Anderson SF, Chao DM, Wei W, Ye L, et al. (1997) BRCA1 is a component of the RNA polymerase II holoenzyme. Proc Natl Acad Sci U S A 94: 5605-5610. (Pubitemid 27241816)
17. Anderson SF, Schlegel BP, Nakajima T, Wolpin ES, Parvin JD (1998) BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase A. Nat Genet 19: 254-256. (Pubitemid 28309336)
18. Monteiro AN, August A, Hanafusa H (1996) Evidence for a transcriptional activation function of BRCA1 C-terminal region. Proc Natl Acad Sci U S A 93: 13595-13599. (Pubitemid 26424164)
19. Chapman MS, Verma IM (1996) Transcriptional activation by BRCA1. Nature 382: 678-679. (Pubitemid 26282163)
20. Ganesan S, Silver DP, Greenberg RA, Avni D, Drapkin R, et al. (2002) BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell 111: 393-405. (Pubitemid 35341392)
21. Ganesan S, Silver DP, Drapkin R, Greenberg R, Feunteun J, et al. (2004) Association of BRCA1 with the inactive X chromosome and XIST RNA. Philos Trans R Soc Lond B Biol Sci 359: 123-128. (Pubitemid 38106455)
22. Turner JM, Aprelikova O, Xu X, Wang R, Kim S, et al. (2004) BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr Biol 14: 2135-2142. (Pubitemid 39623196)
23. Silver DP, Dimitrov SD, Feunteun J, Gelman R, Drapkin R, et al. (2007) Further evidence for BRCA1 communication with the inactive X chromosome. Cell 128: 991-1002. (Pubitemid 46341424)
24. Moynahan ME, Chiu JW, Koller BH, Jasin M (1999) Brca1 controls homologydirected DNA repair. Molecular cell 4: 511-518. (Pubitemid 29531131)
25. Moynahan ME, Cui TY, Jasin M (2001) Homology-directed dna repair, mitomycin-c resistance, and chromosome stability is restored with correction of a Brca1 mutation. Cancer research 61: 4842-4850. (Pubitemid 32691900)
26. Venkitaraman AR (2002) Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 108: 171-182.
27. 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.
28. Furuta S, Jiang X, Gu B, Cheng E, Chen PL, et al. (2005) Depletion of BRCA1 impairs differentiation but enhances proliferation of mammary epithelial cells. Proc Natl Acad Sci U S A 102: 9176-9181. (Pubitemid 40923537)
29. Liu S, Ginestier C, Charafe-Jauffret E, Foco H, Kleer CG, et al. (2008) BRCA1 regulates human mammary stem/progenitor cell fate. Proc Natl Acad Sci U S A 105: 1680-1685. (Pubitemid 351346574)
30. Burga LN, Tung NM, Troyan SL, Bostina M, Konstantinopoulos PA, et al. (2009) Altered proliferation and differentiation properties of primary mammary epithelial cells from BRCA1 mutation carriers. Cancer research 69: 1273-1278.
31. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, et al. (2009) Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nature medicine 15: 907-913.
32. Frank TS, Deffenbaugh AM, Reid JE, Hulick M, Ward BE, et al. (2002) Clinical characteristics of individuals with germline mutations in BRCA1 and BRCA2: analysis of 10,000 individuals. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 20: 1480-1490.
33. Vallon-Christersson J, Cayanan C, Haraldsson K, Loman N, Bergthorsson JT, et al. (2001) Functional analysis of BRCA1 C-terminal missense mutations identified in breast and ovarian cancer families. Human molecular genetics 10: 353-360. (Pubitemid 32166546)
34. Lee MS, Green R, Marsillac SM, Coquelle N, Williams RS, et al. (2010) Comprehensive analysis of missense variations in the BRCT domain of BRCA1 by structural and functional assays. Cancer research 70: 4880-4890.
35. Morris JR, Pangon L, Boutell C, Katagiri T, Keep NH, et al. (2006) Genetic analysis of BRCA1 ubiquitin ligase activity and its relationship to breast cancer susceptibility. Human molecular genetics 15: 599-606. (Pubitemid 43205424)
36. 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. The Journal of clinical investigation 119: 3160-3171.
37. Proia TA, Keller PJ, Gupta PB, Klebba I, Jones AD, et al. (2011) Genetic predisposition directs breast cancer phenotype by dictating progenitor cell fate. Cell stem cell 8: 149-163.
38. Kote-Jarai Z, Williams RD, Cattini N, Copeland M, Giddings I, et al. (2004) Gene expression profiling after radiation-induced DNA damage is strongly predictive of BRCA1 mutation carrier status. Clin Cancer Res 10: 958-963. (Pubitemid 38198896)
39. Kote-Jarai Z, Matthews L, Osorio A, Shanley S, Giddings I, et al. (2006) Accurate prediction of BRCA1 and BRCA2 heterozygous genotype using expression profiling after induced DNA damage. Clin Cancer Res 12: 3896- 3901.
40. Bellacosa A, Godwin AK, Peri S, Devarajan K, Caretti E, et al. (2010) Altered gene expression in morphologically normal epithelial cells from heterozygous carriers of BRCA1 or BRCA2 mutations. Cancer prevention research 3: 48-61.
41. Salmon AY, Salmon-Divon M, Zahavi T, Barash Y, Levy-Drummer RS, et al. (2013) Determination of molecular markers for BRCA1 and BRCA2 heterozygosity using gene expression profiling. Cancer prevention research 6: 82-90.
42. Andrulis IL, Anton-Culver H, Beck J, Bove B, Boyd J, et al. (2002) Comparison of DNA- and RNA-based methods for detection of truncating BRCA1 mutations. Human mutation 20: 65-73. (Pubitemid 34747718)
43. Tibshirani R, Hastie T, Narasimhan B, Chu G (2002) Diagnosis of multiple cancer types by shrunken centroids of gene expression. Proc Natl Acad Sci U S A 99: 6567-6572. (Pubitemid 34526173)
44. Sturn A, Quackenbush J, Trajanoski Z (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18: 207-208. (Pubitemid 34145055)
45. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116- 5121.
46. Calvano SE, Xiao W, Richards DR, Felciano RM, Baker HV, et al. (2005) A network-based analysis of systemic inflammation in humans. Nature 437: 1032- 1037.
47. Rieger KE, Chu G (2004) Portrait of transcriptional responses to ultraviolet and ionizing radiation in human cells. Nucleic Acids Res 32: 4786-4803. (Pubitemid 39429683)
48. Jen KY, Cheung VG (2003) Transcriptional response of lymphoblastoid cells to ionizing radiation. Genome Res 13: 2092-2100.
49. Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, et al. (2000) A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100: 655-669.
50. Mak TW, Hakem A, McPherson JP, Shehabeldin A, Zablocki E, et al. (2000) Brca1 required for T cell lineage development but not TCR loci rearrangement. Nat Immunol 1: 77-82.
51. Kubista M, Rosner M, Kubista E, Bernaschek G, Hengstschlager M (2002) Brca1 regulates in vitro differentiation of mammary epithelial cells. Oncogene 21: 4747-4756. (Pubitemid 34879450)
52. Wright MH, Calcagno AM, Salcido CD, Carlson MD, Ambudkar SV, et al. (2008) Brca1 breast tumors contain distinct CD44+/CD24- and CD133+ cells with cancer stem cell characteristics. Breast Cancer Res 10: R10.
53. Smith SA, Easton DF, Evans DG, Ponder BA (1992) Allele losses in the region 17q12-21 in familial breast and ovarian cancer involve the wild-type chromosome. Nat Genet 2: 128-131.
54. Cornelis RS, Neuhausen SL, Johansson O, Arason A, Kelsell D, et al. (1995) High allele loss rates at 17q12-q21 in breast and ovarian tumors from BRCAllinked families. The Breast Cancer Linkage Consortium. Genes Chromosomes Cancer 13: 203-210.
55. Merajver SD, Pham TM, Caduff RF, Chen M, Poy EL, et al. (1995) Somatic mutations in the BRCA1 gene in sporadic ovarian tumours. Nat Genet 9: 439- 443.
56. Neuhausen SL, Marshall CJ (1994) Loss of heterozygosity in familial tumors from three BRCA1-linked kindreds. Cancer research 54: 6069-6072. (Pubitemid 24378631)
57. King TA, Li W, Brogi E, Yee CJ, Gemignani ML, et al. (2007) Heterogenic loss of the wild-type BRCA allele in human breast tumorigenesis. Ann Surg Oncol 14: 2510-2518. (Pubitemid 47389559)
58. Futreal PA, Liu Q, Shattuck-Eidens D, Cochran C, Harshman K, et al. (1994) BRCA1 mutations in primary breast and ovarian carcinomas. Science 266: 120- 122.
59. Sorlie T, Andersen TI, Bukholm I, Borresen-Dale AL (1998) Mutation screening of BRCA1 using PTT and LOH analysis at 17q21 in breast carcinomas from familial and non-familial cases. Breast Cancer Res Treat 48: 259-264. (Pubitemid 28159953)