An Activated 5′ Cryptic Splice Site in the Human ALG3 Gene Generates a Premature Termination Codon Insensitive to Nonsense-Mediated mRNA Decay in a New Case of Congenital Disorder of Glycosylation Type Id (CDG-Id)

Human Mutation

Volumn 23, Issue 5, 2004, Pages 477-486

  Denecke, Jonas ^a   Kranz, Christian ^a   Kemming, Dirk ^b   Koch, Hans Georg ^a   Marquardt, Thorsten ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b Institute of Clinical Chemistry and Laboratory Medicine   (Germany)

Author keywords

Activated cryptic splice site; ALG3; CDG Id, glycosylation defect; Congenital disorder of glycosylation type Id; Nonsense mediated mRNA decay; NOT56L

Indexed keywords

CYCLOHEXIMIDE; DOLICHOL PHOSPHATE MANNOSE; DOLICHYL MANNOSYLTRANSFERASE; GENOMIC DNA; MANNOSYLTRANSFERASE; MESSENGER RNA; UNCLASSIFIED DRUG; VALINE; ALG3 PROTEIN, HUMAN; DOLICHYL PHOSPHATE MANNOSE GLYCOLIPID ALPHA MANNOSYLTRANSFERASE; DOLICHYL-PHOSPHATE-MANNOSE-GLYCOLIPID ALPHA-MANNOSYLTRANSFERASE; RNA PRECURSOR;

ALG3 GENE; AMINO TERMINAL SEQUENCE; ARTICLE; CONGENITAL DISORDER OF GLYCOSYLATION TYPE 1D; CONTROLLED STUDY; EXON; GENE; GENE ACTIVATION; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; HUMAN; HUMAN CELL; MOLECULAR CLONING; MOLECULAR STABILITY; MUTATIONAL ANALYSIS; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA DEGRADATION; RNA SPLICING; SEQUENCE ANALYSIS; STOP CODON; AMINO ACID SEQUENCE; BIOSYNTHESIS; DISORDERS OF CARBOHYDRATE METABOLISM; DRUG EFFECT; GENETICS; GLYCOSYLATION; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; RNA STABILITY;

ALIAS;

AMINO ACID SEQUENCE; BASE SEQUENCE; CARBOHYDRATE METABOLISM, INBORN ERRORS; CODON, NONSENSE; CODON, TERMINATOR; CYCLOHEXIMIDE; DNA MUTATIONAL ANALYSIS; EXONS; GLYCOSYLATION; HUMANS; MANNOSYLTRANSFERASES; MOLECULAR SEQUENCE DATA; RNA PRECURSORS; RNA SPLICE SITES; RNA SPLICING; RNA STABILITY; RNA, MESSENGER; SEQUENCE DELETION;

EID: 2342594629     PISSN: 10597794     EISSN: None     Source Type: Journal    
DOI: 10.1002/humu.20026     Document Type: Article

References (58)

1. Aebi M, Gassenhuber J, Domdey H, te Heesen S. 1996. Cloning and characterization of the ALG3 gene of Saccharomyces cerevisiae. Glycobiology 6:439-444.
2. Aebi M, Hennet T 2001. Congenital disorders of glycosylation: genetic model systems lead the way. Trends Cell Biol 11:136-141.
3. Bateman JF, Freddi S, Lamande SR, Byers P, Nasioulas S, Douglas J, Otway R, Kohonen-Corish M, Edkins E, Forrest S. 1999. Reliable and sensitive detection of premature termination mutations using a protein truncation test designed to overcome problems of nonsense-mediated mRNA instability. Hum Mutat 13:311-317.
4. Byers PH. 2002. Killing the messenger: new insights into nonsense-mediated mRNA decay. J Clin Invest 109:3-6.
5. Cartegni L, Chew SL, Krainer AR. 2002. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat Rev Genet 3:285-298.
6. Carter MS, Doskow J, Morris P, Li S, Nhim RP, Sandstedt S, Wilkinson ME 1995. A regulatory mechanism that detects premature nonsense codons in T-cell receptor transcripts in vivo is reversed by protein synthesis inhibitors in vitro. J Biol Chem 270:28995-29003.
7. Chen W, Kubota S, Seyama Y. 1998a. Alternative pre-mRNA splicing of the sterol 27-hydroxylase gene (CYP 27) caused by a G to A mutation at the last nucleotide of exon 6 in a patient with cerebrotendinous xanthomatosis (CTX). J Lipid Res 39:509-517.
8. Chen W, Kubota S, Teramoto T, Nishimura Y, Yonemoto K, Seyama Y. 1998b. Silent nucleotide substitution in the sterol q27-hydroxylase gene (CYP 27) leads to alternative pre-mRNA splicing by activating a cryptic 5′ splice site at the mutant codon in cerebrotendinous xanthomatosis patients. Biochemistry 37:4420-4428.
9. Cheng J, Belgrader P, Zhou X, Maquat LE. 1994. Introns are cis effectors of the nonsense-codon-mediated reduction in nuclear mRNA abundance. Mol Cell Biol 14:6317-6325.
10. Custodio N, Carmo-Fonseca M. 2001. Quality control of gene expression in the nucleus. J Cell Mol Med 5:267-275.
11. Danckwardt S, Neu-Yilik G, Thermann R, Frede U, Hentze MW, Kulozik AE. 2002. Abnormally spliced beta-globin mRNAs: a single point mutation generates transcripts sensitive and insensitive to nonsense-mediated mRNA decay. Blood 99:1811-1816.
12. Dreyfuss G, Kim VN, Kataoka N. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 3:195-205.
13. Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, Scott L, Erdos MR, Robbins CM, Moses TY, Berglund P, Dutra A, Pak E, Durkin S, Csoka AB, Brehnke M, Collins FS. 2003. Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423:293-298.
14. Frischmeyer PA, Dietz HC. 1999. Nonsense-mediated mRNA decay in health and disease. Hum Mol Genet 8:1893-1900.
15. Haberle J, Denecke J, Schmidt E, Koch HG. 2003. Diagnosis of N-acetylglutamate synthase deficiency by use of cultured fibroblasts and avoidance of nonsense-mediated mRNA decay. J Inherit Metab Dis 26:601-605.
16. Harrison PM, Gerstein M. 2002. Studying genomes through the aeons: protein families, pseudogenes and proteome evolution. J Mol Biol 318:1155-1174.
17. Hentze MW, Kulozik AE. 1999. A perfect message: RNA surveillance and nonsense-mediated decay. Cell 96:307-310.
18. Korner C, Knauer R, Stephani U, Marquardt T, Lehle L, von Figura K. 1999. Carbohydrate deficient glycoprotein syndrome type IV: deficiency of dolichyl-P-Man:Man(5)GlcNAc(2)-PP-dolichyl mannosyltransferase. Embo J 18:6816-6822.
19. Kranz C, Denecke J, Lehrman MA, Ray S, Kienz P, Kreissel G, Sagi D, Peter-Katalinic J, Freeze HH, Schmid T and others. 2001. A mutation in the human MPDU1 gene causes congenital disorder of glycosylation type If (CDG-If). J Clin Invest 108:1613-1619.
20. Krawczak M, Reiss J, Cooper DN. 1992. The mutational spectrum of single base-pair substitutions in mRNA splice junctions of human genes: causes and consequences. Hum Genet 90:41-54.
21. Lehrman MA, Schneider WJ, Brown MS, Davis CG, Elhammer A, Russell DW, Goldstein JL. 1987. The Lebanese allele at the low density lipoprotein receptor locus. Nonsense mutation produces truncated receptor that is retained in endoplasmic reticulum. J Biol Chem 262:401-410.
22. Li B, Wachtel C, Miriami E, Yahalom G, Friedlander G, Sharon G, Sperling R, Sperling J. 2002. Stop codons affect 5′ splice site selection by surveillance of splicing. Proc Natl Acad Sci USA 99:5277-5282.
23. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
24. Maquat LE, Carmichael GG. 2001. Quality control of mRNA function. Cell 104:173-176.
25. Marquardt T, Denecke J. 2003. Congenital disorders of glycosylation: review of their molecular bases, clinical presentations and specific therapies. Eur J Pediatr 162:359-379.
26. Maser RS, Zinkel R, Petrini JH. 2001. An alternative mode of translation permits production of a variant NBS1 protein from the common Nijmegen breakage syndrome allele. Nat Genet 27:417-421.
27. Matthijs G, Schollen E, Pardon E, Veiga-Da-Cunha M, Jaeken J, Cassiman JJ, Van Schaftingen E. 1997. Mutations in PMM2, a phosphomannomutase gene on chromosome 16p13, in carbohydrate-deficient glycoprotein type I syndrome (Jaeken syndrome). Nat Genet 16:88-92.
28. Medghalchi SM, Frischmeyer PA, Mendell JT, Kelly AG, Lawler AM, Dietz HC. 2001. Rent1, a trans-effector of nonsense-mediated mRNA decay, is essential for mammalian embryonic viability. Hum Mol Genet 10:99-105.
29. Mohlke KL, Nichols WC, Rehemtulla A, Kaufman RJ, Fagerstrom HM, Ritvanen KL, Kekomaki R, Ginsburg D. 1996. A common frameshift mutation in von Willebrand factor does not alter mRNA stability but interferes with normal propeptide processing. Br J Haematol 95:184-191.
30. Nakai K, Sakamoto H. 1994. Construction of a novel database containing aberrant splicing mutations of mammalian genes. Gene 141:171-177.
31. Nelson KK, Green MR. 1990. Mechanism for cryptic splice site activation during pre-mRNA splicing. Proc Natl Acad Sci USA 87:6253-6257.
32. Niwa M, MacDonald CC, Berget SM. 1992. Are vertebrate exons scanned during splice-site selection? Nature 360:277-280.
33. Orkin SH, Kazazian HH Jr, Antonarakis SE, Ostrer H, Goff SC, Sexton JP. 1982. Abnormal RNA processing due to the exon mutation of beta E-globin gene. Nature 300:768-769.
34. Peltz SW, Brown AH, 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.
35. Pirard M, Matthijs G, Heykants L, Schollen E, Grunewald S, Jaeken J, van Schaftingen E. 1999. Effect of mutations found in carbohydrate-deficient glycoprotein syndrome type IA on the activity of phosphomannomutase 2. FEBS Lett 452:319-322.
36. Rajavel KS, Neufeld EE 2001. Nonsense-mediated decay of human HEXA mRNA. Mol Cell Biol 21:5512-5519.
37. Rearick JI, Chapman A, Komfeld S. 1981. Glucose starvation alters lipid-linked oligosaccharide biosynthesis in Chinese hamster ovary cells. J Biol Chem 256:6255-6261.
38. Robberson BL, Cote GJ, Berget SM. 1990. Exon definition may facilitate splice site selection in RNAs with multiple exons. Mol Cell Biol 10:84-94.
39. Rogan PK, Faux BM, Schneider TD. 1998. Information analysis of human splice site mutations. Hum Mutat 12:153-171.
40. Rolfini R, Cabrini G. 1993. Nonsense mutation R1162X of the cystic fibrosis transmembrane conductance regulator gene does not reduce messenger RNA expression in nasal epithelial tissue. J Clin Invest 92:2683-2687.
41. Romao L, Inacio A, Santos S, Avila M, Faustino P, Pacheco P, Lavinha J. 2000. Nonsense mutations in the human beta-globin gene lead to unexpected levels of cytoplasmic mRNA accumulation. Blood 96:2895-2901.
42. Ruiz-Echevarria MJ, Gonzalez CI, Peltz SW. 1998. Identifying the right stop: determining how the surveillance complex recognizes and degrades an aberrant mRNA. EMBO J 17:575-589.
43. Ruiz-Echevarria MJ, Peltz SW. 2000. The RNA binding protein Publ modulates the stability of transcripts containing upstream open reading frames. Cell 101:741-751.
44. Ruiz-Echevarria MJ, Munshi R, Tomback J, Kinzy TG, Peltz SW. 2001. Characterization of a general stabilizer element that blocks deadenylation-dependent mRNA decay. J Biol Chem 276:30995-31003.
45. Schell T, Kulozik AE, Hentze MW. 2002. Integration of splicing, transport and translation to achieve mRNA quality control by the nonsense-mediated decay pathway [Review]. Genome Biol 3:REVIEWS1006.
46. Shapiro MB, Senapathy P. 1987. RNA splice junctions of different classes of eukaryotes: sequence statistics and functional impliocations in gene expression. Nucleic Acids Res 15:7155-7174.
47. Stibler H, Stephani U, Kutsch U. 1995. Carbohydrate-deficient glycoprotein syndrome-a fourth subtype. Neuropediatrics 26:235-237.
48. Teraoka SN, Telatar M, Becker-Catania S, Liang T, Onengut S, Tolun A, Chessa L, Sanal O, Bematowska E, Gatti RA and others. 1999. Splicing defects in the ataxia-telangiectasia gene, ATM: underlying mutations and consequences. Am J Hum Genet 64:1617-1631.
49. Thermann R, Neu-Yilik G, Deters A, Frede U, Wehr K, Hagemeier C, Hentze MW, Kulozik AE. 1998. Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J 17:3484-3494.
50. Toutenhoofd SL, Strehler EE. 2002. Regulation of calmodulin mRNAs in differentiating human IMR-32 neuroblastoma cells. Biochim Biophys Acta 1600:95-104.
51. Tsurumi C, Shimizu Y, Saeki M, Kato S, Demartino GN, Slaughter CA, Fujimuro M, Yokosawa H, Yamasaki M, Hendil KB and others. 1996. cDNA cloning and functional analysis of the p97 subunit of the 26S proteasome, a polypeptide identical to the type-1 tumor-necrosis-factor-receptor-associated protein-2/55.11. Eur J Biochem 239:912-921.
52. Vilela C, Linz B, Rodrigues-Pousada C, McCarthy JE. 1998. The yeast transcription factor genes YAP1 and YAP2 are subject to differential control at the levels of both translation and mRNA stability. Nucleic Acids Res 26:1150-1159.
53. Weil D, D'Alessio M, Ramirez F, Steinmann B, Wirtz MK, Glanville RW, Hollister DW. 1989. Temperature-dependent expression of a collagen splicing defect in the fibroblasts of a patient with Ehlers-Danlos syndrome type VII. J Biol Chem 264:16804-16809.
54. Weiss IM, Liebhaber SA. 1995. Erythroid cell-specific mRNA stability elements in the alpha 2-globin 3′ nontranslated region. Mol Cell Biol 15:2457-2465.
55. Zhang J, Maquat LE. 1997. Evidence that translation reinitiation abrogates nonsense-mediated mRNA decay in mammalian cells. EMBO J 16:826-833.
56. Zhang J, Sun X, Qian Y, LaDuca JP, Maquat LE. 1998a. 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.
57. Zhang J, Sun X, Qian Y, Maquat LE. 1998b. 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.
58. Zhang MQ. 1998. Statistical features of human exons and their flanking regions. Hum Mol Genet 7:919-932.