Effects on human transcriptome of mutated BRCA1 BRCT domain: A microarray study

BMC Cancer

Volumn 12, Issue , 2012, Pages

  Iofrida, Caterina ^a   Melissari, Erika ^a   Mariotti, Veronica ^a   Guglielmi, Chiara ^a   Guidugli, Lucia ^b   Caligo, Maria A ^a   Pellegrini, Silvia ^a  

^a UNIVERSITY OF PISA   (Italy)

^b MAYO CLINIC   (United States)

Author keywords

Apoptosis; BRCA1 gene; Breast neoplasms; Cell proliferation; DNA damage; DNA repair; Gene expression; Genomic instability; Microarray analysis; Missense mutations

Indexed keywords

TRANSCRIPTOME;

ARTICLE; BREAST CANCER; CARBOXY TERMINAL SEQUENCE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCATION; GENETIC VARIABILITY; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; MISSENSE MUTATION; OUTCOME ASSESSMENT; PATHOGENESIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; TUMOR SUPPRESSOR GENE; WILD TYPE; YEAST CELL;

APOPTOSIS; BRCA1 PROTEIN; BREAST NEOPLASMS; CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; DNA REPAIR; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOMIC INSTABILITY; HELA CELLS; HUMANS; MUTATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84861548126     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-12-207     Document Type: Article

References (75)

1. Fabbro M, Savage K, Hobson K, Deans AJ, Powell SN, McArthur GA, Khanna KK. BRCA1-BARD1 complexes are required for p53Ser-15 phosphorylation and a G1/S arrest following ionizing radiation-induced DNA damage. J Biol Chem 2004, 279:31251-31258. 10.1074/jbc.M405372200, 15159397.
2. Chai YL, Cui J, Shao N, Shyam E, Reddy P, Rao VN. The second BRCT domain of BRCA1 proteins interacts with p53 and stimulates transcription from the p21WAF1/CIP1 promoter. Oncogene 1999, 18:263-268. 10.1038/sj.onc.1202323, 9926942.
3. Ouchi T. BRCA1 phosphorylation: biological consequences. Cancer Biol Ther 2006, 5:470-475. 10.4161/cbt.5.5.2845, 16721040.
4. Chen L, Nievera CJ, Lee AY, Wu X. Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J Biol Chem 2008, 283:7713-7720. 10.1074/jbc.M710245200, 18171670.
5. Baer R, Ludwig T. The BRCA1/BARD1 heterodimer, a tumor suppressor complex with ubiquitin E3 ligase activity. Curr Opin Genet Dev 2002, 12:86-91. 10.1016/S0959-437X(01)00269-6, 11790560.
6. Zhu Q, Pao GM, Huynh AM, Suh H, Tonnu N, Nederlof PM, Gage FH, Verma IM. BRCA1 tumour suppression occurs via heterochromatin-mediated silencing. Nature 2011, 477:179-184. 10.1038/nature10371, 3240576, 21901007.
7. Linger RJ, Kruk PA. BRCA1 16 years later: risk-associated BRCA1 mutations and their functional implications. FEBS J 2010, 277:3086-3096. 10.1111/j.1742-4658.2010.07735.x, 20608970.
8. Callebaut I, Mornon JP. From BRCA1 to RAP1: a widespread BRCT module closely associated with DNA repair. FEBS Lett 1997, 400:25-30. 10.1016/S0014-5793(96)01312-9, 9000507.
9. Rodriguez M, Yu X, Chen J, Songyang Z. Phosphopeptide binding specificities of BRCA1 COOH-terminal (BRCT) domains. J Biol Chem 2003, 278:52914-52918. 10.1074/jbc.C300407200, 14578343.
10. 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. BRCA1 tumor suppression depends on BRCT phosphoprotein binding, but not its E3 ligase activity. Science 2011, 334:525-528. 10.1126/science.1209909, 22034435.
11. Di Cecco L, Melissari E, Mariotti V, Iofrida C, Galli A, Guidugli L, Lombardi G, Caligo MA, Iacopetti P, Pellegrini S. Characterisation of gene expression profiles of yeast cells expressing BRCA1 missense variants. Eur J Cancer 2009, 45:2187-2196. 10.1016/j.ejca.2009.04.025, 19493677.
12. Guidugli L, Rugani C, Lombardi G, Aretini P, Galli A, Caligo MA. A recombination-based method to characterize human BRCA1 missense variants. Breast Cancer Res Treat 2011, 125:265-272. 10.1007/s10549-010-1112-8, 20737206.
13. Olopade OI, Fackenthal JD, Dunston G, Tainsky MA, Collins F, Whitfield-Broome C. Breast cancer genetics in African Americans. Cancer 2003, 97(Suppl 1):236-245.
14. 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, 30:123-133. 10.1002/humu.20817, 18680205.
15. Smyth G. Linear models for microarray data. Bioinformatics and computational biology solutions using R and Bioconductor 2005, 397-420. New York: Springer, Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W.
16. Lonnstedt I, Speed T. Replicated microarray data. Stat Sinica 2002, 12:31-46.
17. Draghici S, Khatri P, Tarca AL, Amin K, Done A, Voichita C, Georgescu C, Romero R. A systems biology approach for pathway level analysis. Genome Res 2007, 17:1537-1545. 10.1101/gr.6202607, 1987343, 17785539.
18. Pathway-Express http://vortex.cs.wayne.edu/projects.htm.
19. Khatri P, Draghici S, Ostermeier GC, Krawetz SA. Profiling gene expression using onto-express. Genomics 2002, 79:266-270. 10.1006/geno.2002.6698, 11829497.
20. Onto-Express [http://vortex.cs.wayne.edu/projects.htm].
21. Coremine [http://www.coremine.com/medical].
22. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009, 55:611-622. 10.1373/clinchem.2008.112797, 19246619.
23. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3:research0034.1-research0034.11.
24. ArrayExpress [http://www.ebi.ac.uk/arrayexpress/].
25. Strobl J, Wonderlin W, Flynn D. Mitogenic signal transduction in human breast cancer cells. Gen Pharmacol 1995, 26:1643-1649. 10.1016/0306-3623(95)00062-3, 8745151.
26. Vermeulen K, Van Bockstaele DR, Berneman ZN. The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif 2003, 36:131-149. 10.1046/j.1365-2184.2003.00266.x, 12814430.
27. Zafonte BT, Hulit J, Amanatullah DF, Albanese C, Wang C, Rosen E, Reutens A, Sparano JA, Lisanti MP, Pestell RG. Cell-cycle dysregulation in breast cancer: breast cancer therapies targeting the cell cycle. Front Biosci 2000, 5:D938-961. 10.2741/zafonte, 11102317.
28. Cazzalini O, Scovassi AI, Savio M, Stivala LA, Prosperi E. Multiple roles of the cell cycle inhibitor p21(CDKN1A) in the DNA damage response. Mutat Res 2010, 704:12-20. 10.1016/j.mrrev.2010.01.009, 20096807.
29. Harris TE, Albrecht JH, Nakanishi M, Darlington GJ. CCAAT/enhancer-binding protein-alpha cooperates with p21 to inhibit cyclin-dependent kinase-2 activity and induces growth arrest independent of DNA binding. J Biol Chem 2001, 276:29200-29209. 10.1074/jbc.M011587200, 11369759.
30. Pardali K, Kowanetz M, Heldin CH, Moustakas A. Smad pathway-specific transcriptional regulation of the cell cycle inhibitor p21(WAF1/Cip1). J Cell Physiol 2005, 204:260-272. 10.1002/jcp.20304, 15690394.
31. Tian F, DaCosta Byfield S, Parks WT, Yoo S, Felici A, Tang B, Piek E, Wakefield LM, Roberts AB. Reduction in Smad2/3 signaling enhances tumorigenesis but suppresses metastasis of breast cancer cell lines. Cancer Res 2003, 63:8284-8292.
32. Kohn EA, Du Z, Sato M, Van Schyndle CM, Welsh MA, Yang YA, Stuelten CH, Tang B, Ju W, Bottinger EP, Wakefield LM. A novel approach for the generation of genetically modified mammary epithelial cell cultures yields new insights into TGFβ signaling in the mammary gland. Breast Cancer Res 2010, 12:R83. 10.1186/bcr2728, 3096976, 20942910.
33. Huang SM, Lu KT, Wang YC. ATM/ATR and SMAD3 pathways contribute to 3-indole-induced G1 arrest in cancer cells and xenograft models. Anticancer Res 2011, 31:203-208.
34. Zelivianski S, Cooley A, Kall R, Jeruss JS. Cyclin-dependent kinase 4-mediated phosphorylation inhibits Smad3 activity in cyclin d-overexpressing breast cancer cells. Mol Cancer Res 2010, 8:1375-1387. 10.1158/1541-7786.MCR-09-0537, 3253857, 20736297.
35. Li H, Sekine M, Seng S, Avraham S, Avraham HK. BRCA1 interacts with Smad3 and regulates Smad3-mediated TGF-beta signaling during oxidative stress responses. PLoS One 2009, 4:e7091. 10.1371/journal.pone.0007091, 2740868, 19768112.
36. Carbone R, Pearson M, Minucci S, Pelicci PG. PML NBs associate with the hMre11 complex and p53 at sites of irradiation induced DNA damage. Oncogene 2002, 21:1633-1640. 10.1038/sj.onc.1205227, 11896594.
37. Ikura T, Ogryzko VV, Grigoriev M, Groisman R, Wang J, Horikoshi M, Scully R, Qin J, Nakatani Y. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 2000, 102:463-473. 10.1016/S0092-8674(00)00051-9, 10966108.
38. Han SH, Jeon JH, Ju HR, Jung U, Kim KY, Yoo HS, Lee YH, Song KS, Hwang HM, Na YS, Yang Y, Lee KN, Choi I. VDUP1 upregulated by TGF-beta1 and 1,25-dihydorxyvitamin D3 inhibits tumor cell growth by blocking cell-cycle progression. Oncogene 2003, 22:4035-4046. 10.1038/sj.onc.1206610, 12821938.
39. Burbee D, Forgacs E, Zöchbauer-Müller S, Shivakumar L, Fong K, Gao B, Randle D, Kondo M, Virmani A, Bader S, Sekido Y, Latif F, Milchgrub S, Toyooka S, Gazdar AF, Lerman MI, Zabarovsky E, White M, Minna JD. Epigenetic inactivation of RASSF1A in lung and breast cancers and malignant phenotype suppression. J Natl Cancer Inst 2001, 93:691-699. 10.1093/jnci/93.9.691, 11333291.
40. Shivakumar L, Minna J, Sakamaki T, Pestell R, White M. The RASSF1A tumor suppressor blocks cell cycle progression and inhibits cyclin D1 accumulation. Mol Cell Biol 2002, 22:4309-4318. 10.1128/MCB.22.12.4309-4318.2002, 133879, 12024041.
41. Shaulian E, Karin M. AP-1 in cell proliferation and survival. Oncogene 2001, 20:2390-2400. 10.1038/sj.onc.1204383, 11402335.
42. Nunes-Xavier C, Romá-Mateo C, Ríos P, Tárrega C, Cejudo-Marín R, Tabernero L, Pulido R. Dual-Specificity MAP Kinase Phosphatases as Targets of Cancer Treatment. Anticancer Agents Med Chem 2011, 11:109-132.
43. Small GW, Shi YY, Edmund NA, Somasundaram S, Moore DT, Orlowski RZ. Evidence that mitogen-activated protein kinase phosphatase-1 induction by proteasome inhibitors plays an antiapoptotic role. Mol Pharmacol 2004, 66:1478-1490. 10.1124/mol.104.003400, 15448190.
44. Wang HY, Cheng Z, Malbon CC. Overexpression of mitogen-activated protein kinase phosphatases MKP1, MKP2 in human breast cancer. Cancer Lett 2003, 191:229-237. 10.1016/S0304-3835(02)00612-2, 12618338.
45. Givant-Horwitz V, Davidson B, Goderstad JM, Nesland JM, Tropé CG, Reich R. The PAC-1 dual specificity phosphatase predicts poor outcome in serous ovarian carcinoma. Gynecol Oncol 2004, 93:517-523. 10.1016/j.ygyno.2004.03.009, 15099972.
46. Bagnato A, Rosanò L. The endothelin axis in cancer. Int J Biochem Cell Biol 2008, 40:1443-1451. 10.1016/j.biocel.2008.01.022, 18325824.
47. Bassermann F, Pagano M. Dissecting the role of ubiquitylation in the DNA damage response checkpoint in G2. Cell Death Differ 2010, 17:78-85. 10.1038/cdd.2009.104, 19680264.
48. Kops GJ, Kim Y, Weaver BA, Mao Y, McLeod I, Yates JR, Tagaya M, Cleveland DW. ZW10 links mitotic checkpoint signaling to the structural kinetochore. J Cell Biol 2005, 169:49-60. 10.1083/jcb.200411118, 1351127,1351127, 15824131.
49. Xu L, Begum S, Hearn JD, Hynes RO. GPR56, an atypical G protein-coupled receptor, binds tissue transglutaminase, TG2, and inhibits melanoma tumor growth and metastasis. Proc Natl Acad Sci U S A 2006, 103:9023-9028. 10.1073/pnas.0602681103, 1474142, 16757564.
50. Shishodia S, Aggarwal BB. Nuclear factor-kappaB: a friend or a foe in cancer?. Biochem Pharmacol 2004, 68:1071-1080. 10.1016/j.bcp.2004.04.026, 15313403.
51. Rayet B, Gélinas C. Aberrant rel/nfkb genes and activity in human cancer. Oncogene 1999, 18(49):6938-6947. 10.1038/sj.onc.1203221, 10602468.
52. Kühnel F, Zender L, Paul Y, Tietze MK, Trautwein C, Manns M, Kubicka S. NFkappaB mediates apoptosis through transcriptional activation of Fas (CD95) in adenoviral hepatitis. J Biol Chem 2000, 275:6421-6427. 10.1074/jbc.275.9.6421, 10692445.
53. Shetty S, Graham BA, Brown JG, Hu X, Vegh-Yarema N, Harding G, Paul JT, Gibson SB. Transcription factor NF-kappaB differentially regulates death receptor 5 expression involving histone deacetylase 1. Mol Cell Biol 2005, 25:5404-5416. 10.1128/MCB.25.13.5404-5416.2005, 1156987, 15964798.
54. Sheridan JP, Marsters SA, Pitti RM, Gurney A, Skubatch M, Baldwin D, Ramakrishnan L, Gray CL, Baker K, Wood WI, Goddard AD, Godowski P, Ashkenazi A. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 1997, 277:818-821. 10.1126/science.277.5327.818, 9242611.
55. Suliman A, Lam A, Datta R, Srivastava RK. Intracellular mechanisms of TRAIL: apoptosis through mitochondrial-dependent and -independent pathways. Oncogene 2001, 20:2122-2133. 10.1038/sj.onc.1204282, 11360196.
56. Taira N, Nihira K, Yamaguchi T, Miki Y, Yoshida K. DYRK2 is targeted to the nucleus and controls p53 via Ser46 phosphorylation in the apoptotic response to DNA damage. Mol Cell 2007, 25:725-738. 10.1016/j.molcel.2007.02.007, 17349958.
57. Chen W, Li N, Chen T, Han Y, Li C, Wang Y, He W, Zhang L, Wan T, Cao X. The lysosome-associated apoptosis-inducing protein containing the pleckstrin homology (PH) and FYVE domains (LAPF), representative of a novel family of PH and FYVE domain-containing proteins, induces caspase-independent apoptosis via the lysosomal-mitochondrial pathway. J Biol Chem 2005, 280:40985-40995. 10.1074/jbc.M502190200, 16188880.
58. Li N, Zheng Y, Chen W, Wang C, Liu X, He W, Xu H, Cao X. Adaptor protein LAPF recruits phosphorylated p53 to lysosomes and triggers lysosomal destabilization in apoptosis. Cancer Res 2007, 67:11176-11185. 10.1158/0008-5472.CAN-07-2333, 18056442.
59. Khanna KK, Jackson SP. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet 2001, 27:247-254. 10.1038/85798, 11242102.
60. Martin RW, Orelli BJ, Yamazoe M, Minn AJ, Takeda S, Bishop DK. RAD51 up-regulation bypasses BRCA1 function and is a common feature of BRCA1-deficient breast tumors. Cancer Res 2007, 67:9658-9665. 10.1158/0008-5472.CAN-07-0290, 17942895.
61. Saviozzi S, Ceppi P, Novello S, Ghio P, Lo Iacono M, Borasio P, Cambieri A, Volante M, Papotti M, Calogero RA, Scagliotti GV. Non-small cell lung cancer exhibits transcript overexpression of genes associated with homologous recombination and DNA replication pathways. Cancer Res 2009, 69:3390-3396. 10.1158/0008-5472.CAN-08-2981, 19351853.
62. 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, 3:515-532.
63. Park BJ, Kang JW, Lee SW, Choi SJ, Shin YK, Ahn YH, Choi YH, Choi D, Lee KS, Kim S. The haploinsufficient tumor suppressor p18 upregulates p53 via interactions with ATM/ATR. Cell 2005, 120:209-221. 10.1016/j.cell.2004.11.054, 15680327.
64. Sumara I, Vorlaufer E, Gieffers C, Peters BH, Peters JM. Characterization of vertebrate cohesin complexes and their regulation in prophase. J Cell Biol 2000, 151:749-762. 10.1083/jcb.151.4.749, 2169443, 11076961.
65. Yazdi P, Wang Y, Zhao S, Patel N, Lee E, Qin J. SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev 2002, 16:571-582. 10.1101/gad.970702, 155356, 11877377.
66. Connor J, Weiser D, Li S, Hallenbeck J, Shenolikar S. Growth arrest and DNA damage-inducible protein GADD34 assembles a novel signaling complex containing protein phosphatase 1 and inhibitor 1. Mol Cell Biol 2001, 21:6841-6850. 10.1128/MCB.21.20.6841-6850.2001, 99861, 11564868.
67. Shtivelman E, Cohen FE, Bishop JM. A human gene (AHNAK) encoding an unusually large protein with a 1.2-microns polyionic rod structure. Proc Natl Acad Sci U S A 1992, 89:5472-5476. 10.1073/pnas.89.12.5472, 49314, 1608957.
68. Stiff T, Shtivelman E, Jeggo P, Kysela B. AHNAK interacts with the DNA ligase IV-XRCC4 complex and stimulates DNA ligase IV-mediated double-stranded ligation. DNA Repair (Amst) 2004, 3:245-256.
69. Oberley TD, Oberley LW. Antioxidant enzyme levels in cancer. Histol Histopathol 1997, 12:525-535.
70. Bravard A, Hoffschir F, Sabatier L, Ricoul M, Pinton A, Cassingena R, Estrade S, Luccioni C, Dutrillaux B. Early superoxide dismutase alterations during SV40-transformation of human fibroblasts. Int J Cancer 1992, 52:797-801. 10.1002/ijc.2910520521, 1330936.
71. Li JJ, Oberley LW, St Clair DK, Ridnour LA, Oberley TD. Phenotypic changes induced in human breast cancer cells by overexpression of manganese-containing superoxide dismutase. Oncogene 1995, 10:1989-2000.
72. 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, 14:927-939. 316544, 10783165.
73. Zhang J, Powell S. The role of the BRCA1 tumor suppressor in DNA double-strand break repair. Mol Cancer Res 2005, 3:531-539. 10.1158/1541-7786.MCR-05-0192, 16254187.
74. Kuimov AN. Polypeptide components of telomere nucleoprotein complex. Biochemistry (Mosc) 2004, 69:117-129.
75. Richard DJ, Bolderson E, Cubeddu L, Wadsworth RI, Savage K, Sharma GG, Nicolette ML, Tsvetanov S, McIlwraith MJ, Pandita RK, White MF, Khanna KK. Single-stranded DNA-binding protein hSSB1 is critical for genomic stability. Nature 2008, 453:677-681. 10.1038/nature06883, 18449195.