The nonsense-mediated mRNA decay pathway triggers degradation of most BRCA1 mRNAs bearing premature termination codons

Human Molecular Genetics

Volumn 11, Issue 23, 2002, Pages 2805-2814

  Perrin Vidoz, Laure ^a   Sinilnikova, Olga M ^b,c   Stoppa Lyonnet, Dominique ^d   Lenoir, Gilbert M ^a,e   Mazoyer, Sylvie ^a  

^a CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^b INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^c EDOUARD HERRIOT HOSPITAL   (France)

^d INSTITUT CURIE   (France)

^e INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; MESSENGER RNA;

ALLELE; ARTICLE; BREAST CANCER; CANCER FAMILY; CONTROLLED STUDY; EXON; GENE MUTATION; GERM LINE; HETEROZYGOTE; HUMAN; HUMAN CELL; HYPOTHESIS; LYMPHOBLASTOID CELL LINE; MUTANT; OVARY CANCER; PRIORITY JOURNAL; RNA DEGRADATION; START CODON; STEADY STATE; STOP CODON; TRANSLATION INITIATION;

EID: 0036848138     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/11.23.2805     Document Type: Article

References (63)

1. Miki, Y., Swensen, J., Shattuck-Eidens, D., Futreal, P.A., Harshman, K., Tavtigian, S., Liu, Q., Cochran, C., Bennett, L.M., Ding, W. et al. (1994) A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science, 266, 66-71.
2. Ford, D., Easton, D.F, Stratton, M., Narod, S., Goldgar, D., Devilee, P, Bishop, D.T., Weber, B., Lenoir, G., Chang-Claude, J. 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.
3. Antoniou, A.C., Gayther, S.A., Stratton, J.E, Ponder, B.A. and Easton, D.F. (2000) Risk models for familial ovarian and breast cancer. Genet. Epidemiol., 18, 173-190.
4. Ford, D., Easton, D.F. and Peto, J. (1995) Estimates of the gene frequency of BRCA1 and its contribution to breast and ovarian cancer incidence. Am. J. Hum. Genet., 57, 1457-1462.
5. Friedman, L.S., Szabo, C.I., Ostermeyer, E.A., Dowd, R, Butler, L., Park, T, Lee, M.K., Goode, E.L., Rowell, S.E. and King, M.C. (1995) Novel inherited mutations and variable expressivity of BRCA1 alleles, including the founder mutation 185delAG in Ashkenazi Jewish families. Am. J. Hum. Genet., 57, 1284-1297.
6. Montagna, M., Santacatterina, M., Corneo, B., Menin, C., Serova, O., Lenoir, G.M., Chieco-Bianchi, L. and D'Andrea, E. (1996) Identification of seven new BRCA1 germline mutations in Italian breast and breast/ovarian cancer families. Cancer Res., 56, 5466-5469.
7. Montagna, M., Santacatterina, M., Torri, A., Menin, C., Zullato, D., Chieco-Bianchi, L. and D'Andrea, E. (1999) Identification of a 3 kb Alu-mediated BRCA1 gene rearrangement in two breast/ovarian cancer families. Oncogene, 18, 4160-4165.
8. Puget, N., Sinilnikova, O.M., Stoppa-Lyonnet, D., Audoynaud, C., Pages, S., Lynch, H.T., Goldgar, D., Lenoir, G.M. and Mazoyer, S. (1999) An Alu-mediated 6-kb duplication in the BRCA1 gene: a new founder mutation? Am. J. Hum. Genet., 64, 300-302.
9. Puget, N., Stoppa-Lyonnet, D., Sinilnikova, O.M., Pages, S., Lynch, H.T., Lenoir, G.M. and Mazoyer, S. (1999) Screening for germ-line rearrangements and regulatory mutations in BRCA1 led to the identification of four new deletions. Cancer Res., 59, 455-461.
10. Puget, N., Torchard, D., Serova-Sinilnikova, O.M., Lynch, H.T., Feunteun, J., Lenoir, G.M. and Mazoyer, S. (1997) A 1-kb Alu-mediated germ-line deletion removing BRCA1 exon 17. Cancer Res., 57, 828-831.
11. Serova, O., Montagna, M., Torchard, D., Narod, S.A., Tonin, R, Sylla, B., Lynch, H.T., Feunteun, J. and Lenoir, G.M. (1996) A high incidence of BRCA1 mutations in 20 breast-ovarian cancer families. Am. J. Hum. Genet., 58, 42-51.
12. Losson, R. and Lacroute, F. (1979) Interference of nonsense mutations with eukaryotic messenger RNA stability. Proc. Natl Acad. Sci. USA, 76, 5134-5137.
13. Byers, PH. (2002) Killing the messenger: new insights into nonsense-mediated mRNA decay. J. Clin. Invest., 109, 3-6.
14. Gonzalez, C.I., Bhattacharya, A., Wang, W and Peitz, S.W (2001) Nonsense-mediated mRNA decay in Saccharomyces cerevisiae. Gene, 274, 15-25.
15. Lykke-Andersen, J. (2001) mRNA quality control: Marking the message for life or death. Curr. Biol., 11, R88-91.
16. Wilusz, C.J., Wang, W. and Peltz, S.W. (2001) Curbing the nonsense: the activation and regulation of mRNA surveillance. Genes Dev, 15, 2781-2785.
17. Kataoka, N., Diem, M.D., Kim, V.N., Yong, J. and Dreyfuss, G. (2001) Magoh, a human homolog of Drosophila mago nashi protein, is a component of the splicing-dependent exon-exon junction complex. EMBO J., 20, 6424-6433.
18. Kataoka, N., Yong, J., Kim, VN., Velazquez, F, Perkinson, R.A., Wang, F. and Dreyfuss, G. (2000) Pre-mRNA splicing imprints mRNA in the nucleus with a novel RNA-binding protein that persists in the cytoplasm. Mol. Cell, 6, 673-682.
19. Kim, V.N., Yong, J., Kataoka, N., Abel, L., Diem, M.D. and Dreyfuss, G. (2001) The Y14 protein communicates to the cytoplasm the position of exon-exon junctions. EMBO J., 20, 2062-2068.
20. Le Hir, H., Garfield, D., Braun, I.C., Forler, D. and Izaurralde, E. (2001) The protein Mago provides a link between splicing and MRNA localization. EMBO Rep., 2, 1119-1124.
21. Le Hir, H., Izaurralde, E., Maquat, L.E. and Moore, M.J. (2000) The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J., 19, 6860-6869.
22. Le Hir, H., Moore, M.J. and Maquat, L.E. (2000) Pre-mRNA splicing alters mRNP composition: evidence for stable association of proteins at exon-exon junctions. Genes Dev, 14, 1098-1108.
23. Lykke-Andersen, J., Shu, M.D. and Steitz, JA. (2001) Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1 Science, 293, 1836-1839.
24. Ishigaki, Y., Li, X., Serin, G. and Maquat, L.E. (2001) Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell, 106, 607-617.
25. Peltz, S.W., Brown, A.H. and Jacobson, A. (1993) mRNA destabilization triggered by premature translational termination depends on at least three cis-acting sequence elements and one trans- acting factor. Genes Dev, 7, 1737-1754.
26. Zhang, S., Ruiz-Echevarria, M.J., Quan, Y. and Peltz, SW. (1995) Identification and characterization of a sequence motif involved in nonsense-mediated mRNA decay. Mol. Cell Biol., 15, 2231-2244.
27. Gonzalez, C.I., Ruiz-Echevarria, M.J., Vasudevan, S., Henry, M.F. and Peltz, S.W. (2000) The yeast hnRNP-like protein Hrp1/Nab4 marks a transcript for nonsense- mediated mRNA decay. Mol. Cell, 5, 489-499.
28. Thompson, D. and Easton, D. (2002) Variation in BRCA1 cancer risks by mutation position. Cancer Epidemiol. Biomarkers Prev, 11, 329-336.
29. Shattuck-Eidens, D., McClure, M., Simard, J., Labrie, F., Narod, S., Couch, F., Hoskins, K., Weber, B., Castilla, L., Erdos, M. et al. (1995) A collaborative survey of 80 mutations in the BRCA1 breast and ovarian cancer susceptibility gene. Implications for presymptomatic testing and screening. JAMA, 273, 535-541.
30. Gayther, S.A., Warren, W., Mazoyer, S., Russell, P.A., Harrington, P.A., Chiano, M., Seal, S., Hamoudi, R., van Rensburg, E.J., Dunning, A.M. et al. (1995) Germline mutations of the BRCA1 gene in breast and ovarian cancer families provide evidence for a genotype-phenotype correlation. Nat. Genet., 11, 428-433.
31. Mazoyer, S., Puget, N., Perrin-Vidoz, L., Lynch, H.T., Serova-Sinilnikova, O.M. and Lenoir, G.M. (1998) A BRCA1 nonsense mutation causes exon skipping. Am. J. Hum. Genet., 62, 713-715.
32. Liu, H.X., Cartegni, L., Zhang, M.Q. and Kramer, A.R. (2001) A mechanism for exon skipping caused by nonsense or missense mutations in BRCA1 and other genes. Nat. Genet., 27, 55-58.
33. Belgrader, P. and Maquat, L.E. (1994) Nonsense but not missense mutations can decrease the abundance of nuclear mRNA for the mouse major urinary protein, while both types of mutations can facilitate exon skipping. Mol. Cell Biol., 14, 6326-6336.
34. Carter, M.S., Li, S. and Wilkinson, M.F. (1996) A splicing-dependent regulatory mechanism that detects translation signals. EMBO J, 15, 5965-5975.
35. Thermann, R., Neu-Yilik, G., Deters, A., Frede, U., Wehr, K., Hagemeier, C., Hentze, M.W and Kulozik, A.E. (1998) Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J., 17, 3484-3494.
36. Zhang, J., Sun, X., Qian, Y, LaDuca, J.P. and Maquat, L.E. (1998) At least one intron is required for the nonsense-mediated decay of triosephosphate isomerase mRNA: a possible link between nuclear splicing and cytoplasmic translation. Mol. Cell Biol., 18, 5272-5283.
37. Hilleren, P. and Parker, R. (1999) Mechanisms of mRNA surveillance in eukaryotes. Annu. Rev. Genet., 33, 229-260.
38. Zhang, J., Sun, X., Qian, Y. and Maquat, L.E. (1998) Intron function in the nonsense-mediated decay of beta-globin mRNA: indications that pre-mRNA splicing in the nucleus can influence mRNA translation in the cytoplasm. RNA, 4, 801-815.
39. Neu-Yilik, G., Gehring, N.H., Thermann, R., Frede, U, Hentze, M.W. and Kulozik, A.E. (2001) Splicing and 3′ end formation in the definition of nonsense-mediated decay-competent human beta-globin mRNPs. EMBO J., 20, 532-540.
40. Cheng, J., Belgrader, R, Zhou, X. and Maquat, L.E. (1994) Introns are cis effectors of the nonsense-codon-mediated reduction in nuclear mRNA abundance. Mol. Cell Biol., 14, 6317-6325.
41. Zhang, J. and Maquat, L.E. (1996) Evidence that the decay of nucleus-associated nonsense mRNA for human triosephosphate isomerase involves nonsense codon recognition after splicing. RNA, 2, 235-243.
42. Sun, X., Moriarty, P.M. and Maquat, L.E. (2000) Nonsense-mediated decay of glutathione peroxidase 1 mRNA in the cytoplasm depends on intron position. EMBO J., 19, 4734-4744.
43. Gismondi, V, Stagnaro, P, Pedemonte, S., Biticchi, R., Presciuttini, S., Grammatico, P., Sala, P., Bertario, L., Groden, J. and Varesco, L. (1998) Chain-terminating mutations in the APC gene lead to alterations in APC RNA and protein concentration. Genes Chromosomes Cancer, 22, 278-286.
44. Rodningen, O.K., Tonstad, S., Saugstad, O.D., Ose, L. and Leren, T.P. (1999) Mutant transcripts of the LDL receptor gene: mRNA structure and quantity. Hum. Mutat., 13, 186-196.
45. Cheng, J., Fogel-Petrovic, M. and Maquat, L.E. (1990) Translation to near the distal end of the penultimate exon is required for normal levels of spliced triosephosphate isomerase mRNA. Mol. Cell Biol., 10, 5215-5225.
46. Baserga, S.J. and Benz, E.J., Jr. (1988) Nonsense mutations in the human beta-globin gene affect mRNA metabolism. Proc. Natl Acad. Sci. USA, 85, 2056-2060.
47. Gudikote, J.R and Wilkinson, M.F. (2002) T-cell receptor sequences that elicit strong down-regulation of premature termination codon-bearing transcripts. EMBO J., 21, 125-134.
48. Wang, J., Gudikote, J.P., Olivas, O.R. and Wilkinson, M.F. (2002) Boundary-independent polar nonsense-mediated decay. EMBO Rep., 15, 15.
49. Ruiz-Echevarria, M.J., Gonzalez, C.I. and Peltz, S.W. (1998) Identifying the right stop: determining how the surveillance complex recognizes and degrades an aberrant mRNA. EMBO J., 17, 575-589.
50. Maquat, L.E. and Li, X. (2001) Mammalian heat shock p70 and histone H4 transcripts, which derive from naturally intronless genes, are immune to nonsense-mediated decay. RNA, 7, 445-456.
51. Rajavel, K.S. and Neufeld, E.F. (2001) Nonsense-mediated decay of human HEXA mRNA. Mol. Cell Biol., 21, 5512-5519.
52. Brocke, K.S., Neu-Yilik, G., Gehring, N.H., Hentze, M.W. and Kulozik, A.E. (2002) The human intronless melanocortin 4-receptor gene is NMD insensitive. Hum. Mol. Genet., 11, 331-335.
53. Mendell, J.T. and Dietz, H.C. (2001) When the message goes awry: disease-producing mutations that influence mRNA content and performance. Cell, 107, 411-414.
54. Cartegni, L., Chew, S.L. and Krainer, A.R. (2002) Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat. Rev. Genet., 3, 285-298.
55. Kozak, M. (2001) Constraints on reinitiation of translation in mammals. Nucleic Acids Res., 29, 5226-5232.
56. Zhang, J. and Maqual, L.E. (1997) Evidence that translation reinitiation abrogates nonsense-mediated mRNA decay in mammalian cells. EMBO J., 16, 826-833.
57. Hartge, P., Struewing, J.P., Wacholder, S., Brody, L.C. and Tucker, M.A. (1999) The prevalence of common BRCA1 and BRCA2 mutations among Ashkenazi Jews. Am. J. Hum. Genet., 64, 963-970.
58. Fan, S., Yuan, R., Ma, Y.X., Meng, Q., Goldberg, I.D. and Rosen, E.M. (2001) Mutant BRCA1 genes antagonize phenotype of wild-type BRCA1. Oncogene, 20, 8215-8235.
59. Gad, S., Aurias, A., Puget, N., Mairal, A., Schurra, C., Montagna, M., Pages, S., Caux, V, Mazoyer, S., Bensimon, A. et al. (2001) Color bar coding the BRCAl gene on combed DNA: a useful strategy for detecting large gene rearrangements. Genes Chromosomes Cancer, 31, 75-84.
60. Stoppa-Lyonnet, D., Laurent-Puig, R, Essioux, L., Pages, S., Ithier, G., Ligot, L., Fourquet, A., Salmon, R.J., Clough, K.B., Pouillart, P. et al. (1997) BRCA1 sequence variations in 160 individuals referred to a breast/ovarian family cancer clinic. Institut Curie Breast Cancer Group. Am. J. Hum. Genet., 60, 1021-1030.
61. Andreutti-Zaugg, C., Scott, R.J. and Iggo, R. (1997) Inhibition of nonsense-mediated messenger RNA decay in clinical samples facilitates detection of human MSH2 mutations with an in vivo fusion protein assay and conventional techniques. Cancer Res., 57, 3288-3293.
62. Durocher, F., Shattuck-Eidens, D., McClure, M., Labrie, E, Skolnick, M.H., Goldgar, D.E. and Simard, J. (1996) Comparison of BRCA1 polymorphisms, rare sequence variants and/or missense mutations in unaffected and breast/ovarian cancer populations. Hum. Mol. Genet., 5, 835-842.
63. Friedman, L.S., Ostermeyer, E.A., Szabo, C.I., Dowd, R, Lynch, E.D., Rowell, S.E. and King, M.C. (1994) Confirmation of BRCA1 by analysis of germline mutations linked to breast and ovarian cancer in ten families. Nat. Genet., 8, 399-404.