Common variation at BARD1 results in the expression of an oncogenic isoform that influences neuroblastoma susceptibility and oncogenicity

Cancer Research

Volumn 72, Issue 8, 2012, Pages 2068-2078

  Bosse, Kristopher R ^a   Diskin, Sharon J ^a   Cole, Kristina A ^a   Wood, Andrew C ^a   Schnepp, Robert W ^a   Norris, Geoffrey ^a   Nguyen, Le B ^a   Jagannathan, Jayanti ^a   Laquaglia, Michael ^a   Winter, Cynthia ^a   Diamond, Maura ^a   Hou, Cuiping ^a   Attiyeh, Edward F ^a   Mosse, Yael P ^a   Pineros, Vanessa ^a   Dizin, Eva ^c   Zhang, Yongqiang ^c   Asgharzadeh, Shahab ^d   Seeger, Robert C ^d   Capasso, Mario ^e   Pawel, Bruce R ^a   Devoto, Marcella ^a,f   Hakonarson, Hakon ^a   Rappaport, Eric F ^a   Irminger Finger, Irmgard ^c   Maris, John M ^a,b   more..

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^f SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1BETA; CARRIER PROTEINS AND BINDING PROTEINS; UNCLASSIFIED DRUG;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ARTICLE; BARD1 GENE; CANCER GROWTH; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CARCINOGENICITY; CELL ADHESION; CONTROLLED STUDY; FETUS; FIBROBLAST; GENE; GENE EXPRESSION; GENE SILENCING; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOTYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; MALIGNANT TRANSFORMATION; MOUSE; NEUROBLASTOMA; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

ANIMALS; APOPTOSIS; BASE SEQUENCE; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICE; MOLECULAR SEQUENCE DATA; NEUROBLASTOMA; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN ISOFORMS; REAL-TIME POLYMERASE CHAIN REACTION; TISSUE ARRAY ANALYSIS; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84860207105     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-3703     Document Type: Article

References (38)

1. Freedman ML, Monteiro AN, Gayther SA, Coetzee GA, Risch A, Plass C, et al. Principles for the post-GWAS functional characterization of cancer risk loci. Nat Genet 2011;43:513-8.
2. Maris JM. Recent advances in neuroblastoma. N Engl J Med 2010;362:2202-11.
3. Smith MA, Seibel NL, Altekruse SF, Ries LA, Melbert DL, O'Leary M, et al. Outcomes for children and adolescents with cancer: challenges for the twenty-first century. J Clin Oncol 2010;28:2625-34.
4. Matthay KK, Reynolds CP, Seeger RC, Shimada H, Adkins ES, Haas-Kogan D, et al. Long-term results for children with high-risk neuroblastoma treated on a randomized trial of myeloablative therapy followed by 13-cis-retinoic acid: a children's oncology group study. J Clin Oncol 2009;27:1007-13.
5. Nguyen le B, Diskin SJ, Capasso M, Wang K, Diamond MA, Glessner J, et al. Phenotype restricted genome-wide association study using a gene-centric approach identifies three low-risk neuroblastoma susceptibility loci. PLoS Genet 2011;7:e1002026.
6. Capasso M, Devoto M, Hou C, Asgharzadeh S, Glessner JT, Attiyeh EF, et al.Common variations in BARD1 influence susceptibility to highrisk neuroblastoma. Nat Genet 2009;41:718-23.
7. Diskin SJ, Hou C, Glessner JT, Attiyeh EF, Laudenslager M, Bosse K, et al. Copy number variation at 1q21.1 associated with neuroblastoma. Nature 2009;459:987-91.
8. Maris JM, Mosse YP, Bradfield JP, Hou C, Monni S, Scott RH, et al. Chromosome 6p22 locus associated with clinically aggressive neuroblastoma. N Engl J Med 2008;358:2585-93. (Pubitemid 351831359)
9. Mosse YP, Laudenslager M, Longo L, Cole KA, Wood A, Attiyeh EF, et al. Identification of ALK as a major familial neuroblastoma predisposition gene. Nature 2008;455:930-5.
10. Wang K, Diskin SJ, Zhang H, Attiyeh EF, Winter C, Hou C, et al. Integrative genomics identifies LMO1 as a neuroblastoma oncogene. Nature 2011;469:216-20.
11. Irminger-Finger I, Jefford CE. Is there more to BARD1 than BRCA1? Nat Rev Cancer 2006;6:382-91.
12. Wu LC, Wang ZW, Tsan JT, Spillman MA, Phung A, Xu XL, et al. Identification of a RING protein that can interact in vivo with the BRCA1 gene product. Nat Genet 1996;14:430-40. (Pubitemid 26414587)
13. Li L, Ryser S, Dizin E, Pils D, Krainer M, Jefford CE, et al. Oncogenic BARD1 isoforms expressed in gynecological cancers. Cancer Res 2007;67:11876-85.
14. Ryser S, Dizin E, Jefford CE, Delaval B, Gagos S, Christodoulidou A, et al. Distinct roles of BARD1 isoforms in mitosis: full-length BARD1 mediates Aurora B degradation, cancer-associated BARD1beta scaffolds Aurora B and BRCA2. Cancer Res 2009;69:1125-34.
15. Dizin E, Irminger-Finger I. Negative feedback loop of BRCA1-BARD1 ubiquitin ligase on estrogen receptor alpha stability and activity antagonized by cancer-associated isoform of BARD1. Int J Biochem Cell Biol 2010;42:693-700.
16. Sporn JC, Hothorn T, Jung B. BARD1 expression predicts outcome in colon cancer. Clin Cancer Res 2011;17:5451-62.
17. National Cancer Institute. NCI TARGET data matrix [cited January 3, 2012] Available from: http://target.nci.nih.gov/dataMatrix/TARGET-DataMatrix.html.
18. Winter C, Pawel B, Seiser E, Zhao H, Raabe E, WangQ, et al. Neural cell adhesion molecule (NCAM) isoform expression is associated with neuroblastoma differentiation status. Pediatr Blood Cancer 2008;51:10-6. (Pubitemid 351717383)
19. Peddinti R, Zeine R, Luca D, Seshadri R, Chlenski A, Cole K, et al. Prominent microvascular proliferation in clinically aggressive neuroblastoma. Clin Cancer Res 2007;13:3499-506. (Pubitemid 46955109)
20. Cole KA, Huggins J, Laquaglia M, Hulderman CE, Russell MR, Bosse K, et al. RNAi screen of the protein kinome identifies checkpoint kinase 1 (CHK1) as a therapeutic target in neuroblastoma. Proc Natl Acad Sci U S A 2011;108:3336-41.
21. Cole KA, Attiyeh EF, Mosse YP, Laquaglia MJ, Diskin SJ, Brodeur GM, et al. A functional screen identifies miR-34a as a candidate neuroblastoma tumor suppressor gene. Mol Cancer Res 2008;6:735-42.
22. Conrad DF, Pinto D, Redon R, Feuk L, Gokcumen O, Zhang Y, et al. Origins and functional impact of copy number variation in the human genome. Nature 2010;464:704-12.
23. Stranger BE, Forrest MS, Dunning M, Ingle CE, Beazley C, Thorne N, et al. Relative impact of nucleotide and copy number variation on gene expression phenotypes. Science 2007;315:848-53.
24. Heinzen EL, Ge D, Cronin KD, Maia JM, Shianna KV, Gabriel WN, et al. Tissue specific genetic control of splicing: implications for the study of complex traits. PLoS Biol 2008;6:e1.
25. Feki A, Jefford CE, Berardi P,WuJY, Cartier L, Krause KH, et al. BARD1 induces apoptosis by catalysing phosphorylation of p53 by DNAdamage response kinase. Oncogene 2005;24:3726-36. (Pubitemid 40826872)
26. Irminger-Finger I, Leung WC, Li J, Dubois-Dauphin M, Harb J, Feki A, et al. Identification of BARD1 as mediator between proapoptotic stress and p53-dependent apoptosis. Mol Cell 2001;8:1255-66. (Pubitemid 34084997)
27. Fabbro M, Savage K, Hobson K, Deans AJ, Powell SN, McArthur GA, et al. BRCA1-BARD1 complexes are required for p53Ser-15 phosphorylation and a G1/S arrest following ionizing radiation-induced DNA damage. J Biol Chem 2004;279:31251-8. (Pubitemid 39037790)
28. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly (ADP-ribose) polymerase. Nature 2005;434:913-7. (Pubitemid 40559005)
29. Otto T, Horn S, Brockmann M, Eilers U, Schuttrumpf L, Popov N, et al. Stabilization of N-Myc is a critical function of Aurora A in human neuroblastoma. Cancer Cell 2009;15:67-78.
30. Venables JP, Klinck R, Koh C, Gervais-Bird J, Bramard A, Inkel L, et al. Cancer-associated regulation of alternative splicing. Nat Struct Mol Biol 2009;16:670-6.
31. Maris JM. Unholy matrimony: Aurora A and N-Myc as malignant partners in neuroblastoma. Cancer Cell 2009;15:5-6.
32. Maris JM, Morton CL, Gorlick R, Kolb EA, Lock R, Carol H, et al. Initial testing of the aurora kinase A inhibitor MLN8237 by the Pediatric Preclinical Testing Program (PPTP). Pediatr Blood Cancer 2010;55:26-34.
33. Loven J, Zinin N, Wahlstrom T, Muller I, Brodin P, Fredlund E, et al. MYCN-regulated microRNAs repress estrogen receptor-alpha (ESR1) expression and neuronal differentiation in human neuroblastoma. Proc Natl Acad Sci U S A 2010;107:1553-8.
34. Tsuzuki M, Wu W, Nishikawa H, Hayami R, Oyake D, Yabuki Y, et al. A truncated splice variant of human BARD1 that lacks the RING finger and ankyrin repeats. Cancer Lett 2006;233:108-16. (Pubitemid 43214568)
35. Minovitsky S, Gee SL, Schokrpur S, Dubchak I, Conboy JG. The splicing regulatory element, UGCAUG, is phylogenetically and spatially conserved in introns that flank tissue-specific alternative exons. Nucleic Acids Res 2005;33:714-24. (Pubitemid 40361001)
36. Yeo GW, Coufal NG, Liang TY, Peng GE, Fu XD, Gage FH. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat Struct Mol Biol 2009;16:130-7.
37. Kitajima S, Kudo Y, Ogawa I, Tatsuka M, Kawai H, Pagano M, et al. Constitutive phosphorylation of aurora-a on ser51 induces its stabilization and consequent overexpression in cancer. PLoS One 2007;2:e944.
38. Giubettini M, Asteriti IA, Scrofani J, De Luca M, Lindon C, Lavia P, et al. Control of Aurora-A stability through interaction with TPX2. J Cell Sci 2011;124:113-22.