Nonsense mutations in the COL1A1 gene preferentially reduce nuclear levels of mRNA but not hnRNA in osteogenesis imperfecta type I cell strains

Matrix Biology

Volumn 19, Issue 1, 2000, Pages 1-9

  Slayton, Rebecca L ^a   Deschenes, Sachi P ^b   Willing, Marcia C ^b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

COL1A1; mRNA decay; Nonsense codon; Osteogenesis imperfecta; Premature termination

Indexed keywords

ARTICLE; CELL CULTURE; DISEASE CLASSIFICATION; DISEASE SEVERITY; HUMAN; HUMAN CELL; NONSENSE MUTATION; OSTEOGENESIS IMPERFECTA; PATHOGENESIS; PRIORITY JOURNAL; RNA ANALYSIS;

CELL NUCLEUS; CELLS, CULTURED; CODON, NONSENSE; CODON, TERMINATOR; EXONS; HUMANS; MUTATION; OSTEOGENESIS IMPERFECTA; PROCOLLAGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, HETEROGENEOUS NUCLEAR; RNA, MESSENGER;

MAMMALIA;

EID: 0033968084     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0945-053X(99)00056-6     Document Type: Article

References (53)

1. Alzhanova-Ericsson A.T., Sun X., Visa N., Kiseleva E., Wurtz T., Daneholt B. A protein of the SR family of splicing factors binds extensively to exonic Balbiani ring pre-mRNA and accompanies the RNA from the gene to the nuclear pore. Genes Dev. 10:1996;2881-2893.
2. Atkin A.L., Altamura N., Leeds P., Culbertson M.R. The majority of yeast UPF1 co-localizes with polyribosomes in the cytoplasm. Mol Biol Cell. 6:1995;611-625.
3. Ausubel, F.M., Brent, R., Kingston, R.E. et al., 1992. Preparation and analysis of RNA. In: Current Protocols in Molecular Biology, John Wiley & Sons, New York, p. 4-3-4-4.
4. Baserga S.J., Benz E.J. Jr. Beta-globin nonsense mutation: deficient accumulation of mRNA occurs despite normal cytoplasmic stability. Proc. Natl. Acad. Sci. USA. 89:1992;2935-2939.
5. Belgrader P., Maquat L.E. 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. 14:1994;6326-6336.
6. Belgrader P., Cheng J., Maquat L.E. Evidence to implicate translation by ribosomes in the mechanism by which nonsense codons reduce the nuclear level of human triosephosphate isomerase mRNA. Proc. Natl. Acad. Sci. USA. 90:1993;482-486.
7. Belgrader P., Cheng J., Zhou X., Stephenson L.S., Maquat L.E. Mammalian nonsense codons can be cis effectors of nuclear mRNA half-life. Mol. Cell. Biol. 14:1994;8219-8228.
8. Caceres J.F., Screaton G.R., Krainer A.R. A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev. 12:1998;55-66.
9. Cheng J., Maquat L.E. Nonsense codons can reduce the abundance of nuclear mRNA without affecting the abundance of pre-mRNA or the half-life of cytoplasmic mRNA. Mol. Cell Biol. 13:1892;1993.
10. Cheng J., Fogel-Petrovic M., Maquat L.E. Translation to near the distal end of the penultimate exon is required for normal levels of spliced triosephosphate isomerase mRNA. Mol. Cell. Biol. 10:1990;5215-5225.
11. Cheng J., Belgrader P., Zhou X., Maquat L.E. Introns are cis effectors of the nonsense-codon-mediated reduction in nuclear mRNA abundance. Mol. Cell. Biol. 14:1994;6317-6325.
12. Cui Y., Hagan K.W., Zhang S., Peltz S.W. Identification and characterization of genes that are required for the accelerated degradation of mRNAs containing a premature translational termination codon. Genes Dev. 9:1995;423-436.
13. Culbertson M.R. RNA surveillance. Unforeseen consequences for gene expression, inherited genetic disorders and cancer. Trends Genet. 15:1999;74-80.
14. Czaplinski K., Weng Y., Hagan K.W., Peltz S.W. Purification and characterization of the Upf1 protein: a factor involved in translation and mRNA degradation. RNA. 1:1995;610-623.
15. Czaplinski K., Ruiz-Echevarria M.J., Paushkin S.V. et al. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev. 12:1998;1665-1677.
16. Czaplinski K., Ruiz-Echevarria M.J., lez C.I., Peltz S.W. Should we kill the messenger? The role of the surveillance complex in translation termination and mRNA turnover. Bioessays. 21:1999;685-696.
17. Daar I.O., Maquat L.E. Premature translation termination mediates triosephosphate isomerase mRNA degradation. Mol. Cell. Biol. 8:1988;802-813.
18. D'Alessio M., Bernard M., Pretorious P.J., de Wet W., Ramirez F. Complete nucleotide sequence of the region encompassing the first twenty-five exons of the human pro a1(I) collagen gene (COL1A1). Gene. 67:1988;105-115.
19. Dalgleish R. The human type I collagen mutation database. Nucleic Acids Res. 25:1997;181-187.
20. Das S., Levinson B., Whitney S., Vulpe C., Packman S., Getschier J. Diverse mutations in patients with Menkes disease often lead to exon skipping. Am. J. Hum. Genet. 55:1994;883-889.
21. Dietz H.C., Kendzior R.J.J. Maintenance of an open reading frame as an additional level of scrutiny during splice site selection. Nat. Genet. 8:1994;183-188.
22. Dietz H.C., McIntosh I., Sakai L.Y. Four novel FBN1 mutations: significance for mutant transcript level and EGF-like domain calcium binding in the pathogenesis of Marfan syndrome. Genomics. 17:1993;468-475.
23. Fisher C.W., Fisher C.R., Chuang J.L., Lau K.S., Chuang D.T., Cox R.P. Occurrence of a 2-bp (AT) deletion allele and a nonsense (G-to-T) mutant allele at the E2 (DBT) locus of six patients with maple syrup urine disease: multiple-exon skipping as a secondary effect of the mutations. Am. J. Hum. Genet. 52:1993;414-424.
24. Gibson R.A., Hajianpour A., Murer-Orlando M., Buchwald M., Mathew C.G. A nonsense mutation and exon skipping in the Fanconi anaemia group C gene. Hum. Mol. Genet. 2:1993;797-799.
25. - mutant. Proc. Natl. Acad. Sci. 90:1993;7034-7038.
26. Hentze M.W., Kulozik A.E. A perfect message: RNA surveillance and nonsense-mediated decay. Cell. 96:1999;307-310.
27. Hilleren P., Parker R. mRNA surveillance in eukaryotes: kinetic proofreading of proper translation termination as assessed by mRNP domain organization? RNA. 5:1999;711-719.
28. Kessler O., Chasin L.A. Effects of nonsense mutations on nuclear and cytoplasmic adenine phosphoribosyltransferase RNA. Mol. Cell. Biol. 16:1996;4426-4435.
29. Kugler W., Enssle J., Hentze M.W., Kulozik A.E. Nuclear degradation of nonsense mutated b-globin mRNA: a post-transcriptional mechanism to protect heterozygotes from severe clinical manifestations of b-thalassemia? Nucleic Acids Res. 23:1995;413-418.
30. Losson R., Lacroute F. Interference of nonsense mutations with eukaryotic messenger RNA stability. Proc. Natl. Acad. Sci. 76:1979;5134-5137.
31. Maquat L.E. When cells stop making sense: Effects of nonsense codons on RNA metabolism in vertebrate cells. RNA. 1:1995;453-465.
32. Mashima Y., Murakami A., Weleber R.G. et al. Nonsense-codon mutations of the ornithine aminotransferase gene with decreased levels of mutant mRNA in gyrate atrophy. Am. J. Hum. Genet. 51:1992;81-91.
33. Mehlin H., Daneholt B., Skoglund U. Translocation of a specific pre-messenger ribonucleoprotein particle through the nuclear pore studied with electron microscope tomography. Cell. 69:1992;605-613.
34. Messiaen L., Callens T., De Paepe A., Craen M., Mortier G. Characterisation of two different nonsense mutations, C6792A and C6792G, causing skipping of exon 37 in the NF1 gene. Hum. Genet. 101:1997;75-80.
35. Nagy E., Maquat L.E. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem. Sci. 23:1998;198-199.
36. Peltz S.W., Brown A.H., Jacobson A. mRNA destabilization triggered by premature translational termination depends on at least three cis-acting sequence elements and one trans-acting factor. Genes Dev. 7:1993;1737-1754.
37. Pulak R., Anderson P. mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev. 7:1993;1885-1897.
38. Redford-Badwal D.A., Stover M.L., Valli M., McKinstry M.B., Rowe D.W. Nuclear retention of COL1A1 messenger RNA identifies null alleles causing mild osteogenesis imperfecta. J. Clin. Invest. 97:1996;1035-1040.
39. Slayton R.L., Deschenes S.P., Willing M.C. Premature termination mutations in the COL1A1 gene interfere with mRNA stability during RNA processing in osteogenesis imperfecta type I cell strains. Am. J. Hum. Genet. 57:1995;A34.
40. Thermann R., Neu-Yilik G., Deters A. Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J. 17:1998;3484-3494.
41. Urlaub G., Mitchell P.J., Ciudad C.J., Chasin L.A. Nonsense mutations in the dihydrofolate reductase gene affect RNA processing. Mol. Cell. Biol. 9:1989;2868-2880.
42. Visa M., Alzhanova-Ericsson A.T., Sun X. et al. A pre-mRNA-binding protein accompanies the RNA from the gene through the nuclear pores into polysomes. Cell. 84:1996;253-264.
43. Westerhausen A., Constantinou C.D., Pack M. et al. Completion of the last half of the structure of the human gene for the Pro alpha 1 (I) chain of type I procollagen (COL1A1). Matrix. 11:1991;375-379.
44. Whitfield T.T., Sharpe C.R., Wylie C.C. Nonsense-mediated mRNA decay in Xenopus oocytes and embryos. Dev. Biol. 165:1994;731-734.
45. Willing M.C., Cohn D.H., Byers P.H. Frameshift mutation near the 3′ end of the COL1A1 gene of type I collagen predicts an elongated pro a1(I) chain and results in osteogenesis imperfecta type I. J. Clin. Invest. 85:1990;282-290.
46. Willing M.C., Pruchno C.J., Atkinson M., Byers P.H. Osteogenesis imperfecta type I is commonly due to a COL1A1 null allele of type I collagen. Am. J. Hum. Genet. 51:1992;508-515.
47. Willing M.C., Deschenes S.P., Scott D.A. et al. Osteogenesis Imperfecta Type I: molecular heterogeneity for COL1A1 null alleles of type I collagen. Am. J. Hum. Genet. 55:1994;638-647.
48. Willing M.C., Deschenes S.P., Slayton R.L., Roberts E.J. Premature termination is a unifying mechanism for COL1A1 null alleles in osteogenesis imperfecta type I cell strains. Am. J. Hum. Genet. 59:1996;799-809.
49. Zhang J., Maquat L.E. Evidence that the decay of nucleus-associated nonsense mRNA for human triosephosphate isomerase involves nonsense codon recognition after splicing. RNA. 2:1996;235-243.
50. Zhang J., Maquat L.E. Evidence that translation reinitiation abrogates nonsense-mediated mRNA decay in mammalian cells. EMBO J. 16:1997;826-833.
51. Zhang J., Sun X., Qian Y., LaDuca J.P., Maquat L.E. 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. 18:1998;5272-5283.
52. Zhang J., Sun X., Qian Y., Maquat L.E. 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. 4:1998;801-815.
53. Zhang S., Ruiz-Echevarria M.J., Quan Y., Peltz S.W. Identification and characterization of a sequence motif involved in nonsense-mediated mRNA decay. Mol. Cell. Biol. 15:1995;2231-2244.