Incomplete nonsense-mediated mRNA decay in Giardia lamblia

International Journal for Parasitology

Volumn 38, Issue 11, 2008, Pages 1305-1317

  Chen, Yi Hsiu ^a   Su, Li Hsin ^a   Sun, Chin Hung ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Cyst wall protein; Encystation; G418; Giardia; NMD; UPF1

Indexed keywords

ANTIBIOTIC G 418; LUCIFERASE; MESSENGER RNA; PROTOZOAL RNA; TRANSCRIPTION FACTOR; UP FRAMESHIFT 1;

CYST; ENCYSTMENT; ENZYME ACTIVITY; FLAGELLATE; MUTATION; PROTEIN; RNA;

ARTICLE; CONTROLLED STUDY; CYST WALL PROTEIN 3; CYTOPLASM; EUKARYOTIC CELL; GENE; GIARDIA LAMBLIA; IMMUNOFLUORESCENCE TEST; NONHUMAN; NONSENSE MEDIATED MESSENGER RNA DECAY; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; NUCLEUS ACCUMBENS; PROTEIN EXPRESSION; STOP CODON; TRANSLATION REGULATION;

ANIMALS; CODON, NONSENSE; EUKARYOTIC INITIATION FACTOR-4A; FLUORESCENT ANTIBODY TECHNIQUE; GIARDIA LAMBLIA; PLASMIDS; RNA STABILITY; RNA, MESSENGER; RNA, PROTOZOAN; RNA-BINDING PROTEINS; TRANSFECTION; TROPHOZOITES;

EUKARYOTA; GIARDIA; GIARDIA INTESTINALIS; MAMMALIA; PROTOZOA;

EID: 48349096149     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2008.02.006     Document Type: Article

References (62)

1. Adam R.D. Biology of Giardia lamblia. Clin. Microbiol. Rev. 14 (2001) 447-475
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
3. Andreutti-Zaugg C., Scott R.J., and Iggo R. 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 (1997) 3288-3293
4. Applequist S.E., Selg M., Raman C., and Jack H.M. Cloning and characterization of HUPF1, a human homolog of the Saccharomyces cerevisiae nonsense mRNA-reducing UPF1 protein. Nucleic Acids Res. 25 (1997) 814-821
5. Baumann B., Potash M.J., and Kohler G. Consequences of frameshift mutations at the immunoglobulin heavy chain locus of the mouse. EMBO J. 4 (1985) 351-359
6. Bedwell D.M., Kaenjak A., Benos D.J., Bebok Z., Bubien J.K., Hong J., Tousson A., Clancy J.P., and Sorscher E.J. Suppression of a CFTR premature stop mutation in a bronchial epithelial cell line. Nat. Med. 3 (1997) 1280-1284
7. Bhattacharya A., Czaplinski K., Trifillis P., He F., Jacobson A., and Peltz S.W. Characterization of the biochemical properties of the human Upf1 gene product that is involved in nonsense-mediated mRNA decay. RNA 6 (2000) 1226-1235
8. Burke J.F., and Mogg A.E. Suppression of a nonsense mutation in mammalian cells in vivo by the aminoglycoside antibiotics G-418 and paromomycin. Nucleic Acids Res. 13 (1985) 6265-6272
9. Chenna R., Sugawara H., Koike T., Lopez R., Gibson T.J., Higgins D.G., and Thompson J.D. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31 (2003) 3497-3500
10. Chiu S.Y., Serin G., Ohara O., and Maquat L. Characterization of human Smg5/7a: a protein with similarities to Caenorhabditis elegans SMG5 and SMG7 that functions in the dephosphorylation of Upf1. RNA 9 (2003) 77-87
11. Conti E., Franks N.P., and Brick P. Crystal structure of firefly luciferase throws light on a superfamily of adenylate-forming enzymes. Structure 4 (1996) 287-298
12. Culbertson M., and Neeno-Eckwall E. Transcript selection and the recruitment of mRNA decay factors for NMD in Saccharomyces cerevisiae. RNA 11 (2005) 1333-1339
13. Czaplinski K., Ruiz-Echevarria M.J., Paushkin S.V., Han X., Weng Y., Perlick H.A., Dietz H.C., Ter-Avanesyan M.D., and Peltz S.W. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev. 12 (1998) 1665-1677
14. Czaplinski K., Weng Y., Hagan K.W., and Peltz S.W. Purification and characterization of the Upf1 protein: a factor involved in translation and mRNA degradation. RNA 1 (1995) 610-623
15. Eichinger D. Encystation in parasitic protozoa. Curr. Opin. Microbiol. 4 (2001) 421-426
16. Eustice D.C., and Wilhelm J.M. Fidelity of the eukaryotic codon-anticodon interaction: interference by aminoglycoside antibiotics. Biochemistry 23 (1984) 1462-1467
17. Finn R.D., Mistry J., Schuster-Bockler B., Griffiths-Jones S., Hollich V., Lassmann T., Moxon S., Marshall M., Khanna A., Durbin R., Eddy S.R., Sonnhammer E.L., and Bateman A. Pfam: clans, web tools and services. Nucleic Acids Res. 34 (2006) D247-D251
18. Geiger, S.K., Bär, H., Ehlermann, P., Wälde, S., Rutschow, D., Zeller, R., Ivandic, B.T., Zentgraf, H., Katus, H.A., Herrmann, H., Weichenhan, D., 2007. Incomplete nonsense-mediated decay of mutant lamin A/C mRNA provokes dilated cardiomyopathy and ventricular tachycardia. J. Mol. Med. (Epub ahead of print).
19. Gillin F.D., Reiner D.S., and McCaffery J.M. Cell biology of the primitive eukaryote Giardia lamblia. Annu. Rev. Microbiol. 50 (1996) 679-705
20. Gonzalez C.I., Bhattacharya A., Wang W., and Peltz S.W. Nonsense-mediated mRNA decay in Saccharomyces cerevisiae. Gene 274 (2001) 15-25
21. Hashimoto T., Nakamura Y., Kamaishi T., Nakamura F., Adachi J., Okamoto K., and Hasegawa M. Phylogenetic place of mitochondrion-lacking protozoan, Giardia lamblia, inferred from amino acid sequences of elongation factor 2. Mol. Biol. Evol. 12 (1995) 782-793
22. Hashimoto T., Nakamura Y., Nakamura F., Shirakura T., Adachi J., Goto N., Okamoto K., and Hasegawa M. Protein phylogeny gives a robust estimation for early divergences of eukaryotes: phylogenetic place of a mitochondria-lacking protozoan, Giardia lamblia. Mol. Biol. Evol. 11 (1994) 65-71
23. Hausmann S., Altura M.A., Witmer M., Singer S.M., Elmendorf H.G., and Shuman S. Yeast-like mRNA capping apparatus in Giardia lamblia. J. Biol. Chem. 280 (2005) 12077-12086
24. He F., Brown A.H., and Jacobson A. Upf1p, Nmd2p, and Upf3p are interacting components of the yeast nonsense-mediated mRNA decay pathway. Mol. Cell Biol. 117 (1997) 1580-1594
25. Kadlec J., Guilligay D., Ravelli R.B., and Cusack S. Crystal structure of the UPF2-interacting domain of nonsense-mediated mRNA decay factor UPF1. RNA 12 (2006) 1817-1824
26. Keister D.B. Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans. R. Soc. Trop. Med. Hyg. 77 (1983) 487-488
27. Kirillov S., Porse B.T., Vester B., Woolley P., and Garrett R.A. Movement of the 3′-end of tRNA through the peptidyl transferase centre and its inhibition by antibiotics. FEBS Lett. 406 (1997) 223-233
28. Knodler L.A., Svard S.G., Silberman J.D., Davids B.J., and Gillin F.D. Developmental gene regulation in Giardia lamblia: first evidence for an encystation-specific promoter and differential 5′ mRNA processing. Mol. Microbiol. 34 (1999) 327-340
29. Koeller D.M., Horowitz J.A., Casey J.L., Klausner R.D., and Harford J.B. Translation and the stability of mRNAs encoding the transferrin receptor and c-fos. Proc. Natl. Acad. Sci. USA 88 (1991) 7778-7782
30. Leeds P., Peltz S.W., Jacobson A., and Culbertson M.R. The product of the yeast UPF1 gene is required for rapid turnover of mRNAs containing a premature translational termination codon. Genes Dev. 5 (1991) 2303-2314
31. Leeds P., Wood J.M., Lee B.S., and Culbertson M.R. Gene products that promote mRNA turnover in Saccharomyces cerevisiae. Mol. Cell Biol. 12 (1992) 2165-2177
32. Li L., and Wang C.C. Identification in the ancient protist Giardia lamblia of two eukaryotic translation initiation factor 4E homologues with distinctive functions. Eukaryot. Cell 4 (2005) 948-959
33. Lim S.K., Sigmund C.D., Gross K.W., and Maquat L.E. Nonsense codons in human beta-globin mRNA result in the production of mRNA degradation products. Mol. Cell Biol. 12 (1992) 1149-1161
34. Lykke-Andersen J., Shu M.D., and Steitz J.A. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 103 (2000) 1121-1131
35. Maderazo A.B., He F., Mangus D.A., and Jacobson A. Upf1p control of nonsense mRNA translation is regulated by Nmd2p and Upf3p. Mol. Cell Biol. 20 (2000) 4591-4603
36. McArthur A.G., Morrison H.G., Nixon J.E., Passamaneck N.Q., Kim U., Hinkle G., Crocker M.K., Holder M.E., Farr R., Reich C.I., Olsen G.E., Aley S.B., Adam R.D., Gillin F.D., and Sogin M.L. The Giardia genome project database. FEMS Microbiol. Lett. 189 (2000) 271-273
37. Mendell J.T., Medghalchi S.M., Lake R.G., Noensie E.N., and Dietz H.C. Novel Upf2p orthologues suggest a functional link between translation initiation and nonsense surveillance complexes. Mol. Cell Biol. 20 (2000) 8944-8957
38. Morrison H.G., McArthur A.G., Gillin F.D., Aley S.B., Adam R.D., Olsen G.J., Best A.A., Cande W.Z., Chen F., Cipriano M.J., Davids B.J., Dawson S.C., Elmendorf H.G., Hehl A.B., Holder M.E., Huse S.M., Kim U.U., Lasek-Nesselquist E., Manning G., Nigam A., Nixon J.E., Palm D., Passamaneck N.E., Prabhu A., Reich C.I., Reiner D.S., Samuelson J., Svard S.G., and Sogin M.L. Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317 (2007) 1921-1926
39. Morrison H.G., Zamora G., Campbell R.K., and Sogin M.L. Inferring protein function from genomic sequence: Giardia lamblia expresses a phosphatidylinositol kinase-related kinase similar to yeast and mammalian TOR. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 133 (2002) 477-491
40. Nagy E., and 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
41. Nathans D. Puromycin inhibition of protein synthesis: incorporation of puromycin into peptide chains. Proc. Natl. Acad. Sci. USA 51 (1964) 585-592
42. Ong S.J., Huang L.C., Liu H.W., Chang S.C., Yang Y.C., Bessarab I., and Tai J.H. Characterization of a bi-directional promoter for divergent transcription of a PHD-zinc finger protein gene and a ran gene in the protozoan pathogen Giardia lamblia. Mol. Microbiol. 43 (2002) 665-676
43. Page M.F., Carr B., Anders K.R., Grimson A., and Anderson P. SMG-2 is a phosphorylated protein required for mRNA surveillance in Caenorhabditis elegans and related to Upf1p of yeast. Mol. Cell Biol. 19 (1999) 5943-5951
44. Perlick H.A., Medghalchi S.M., Spencer F.A., Kendzior Jr. R.J., and Dietz H.C. Mammalian orthologues of a yeast regulator of nonsense transcript stability. Proc. Natl. Acad. Sci. USA 93 (1996) 10928-10932
45. Schroeder R., Waldsich C., and Wank H. Modulation of RNA function by aminoglycoside antibiotics. EMBO J. 19 (2000) 1-9
46. Serin G., Gersappe A., Black J.D., Aronoff R., and Maquat L.E. Identification and characterization of human orthologues to Saccharomyces cerevisiae Upf2 protein and Upf3 protein (Caenorhabditis elegans SMG-4). Mol. Cell Biol. 21 (2001) 209-223
47. Singer S.M., Yee J., and Nash T.E. Episomal and integrated maintenance of foreign DNA in Giardia lamblia. Mol. Biochem. Parasitol. 92 (1998) 59-69
48. Sogin M.L., Gunderson J.H., Elwood H.J., Alonso R.A., and Peattie D.A. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243 (1989) 75-77
49. Su L.H., Lee G.A., Huang Y.C., Chen Y.H., and Sun C.H. Neomycin and puromycin affect gene expression in Giardia lamblia stable transfection. Mol. Biochem. Parasitol. 156 (2007) 124-135
50. Sun C.H., Chou C.F., and Tai J.H. Stable DNA transfection of the primitive protozoan pathogen Giardia lamblia. Mol. Biochem. Parasitol. 92 (1998) 123-132
51. Sun C.H., McCaffery J.M., Reiner D.S., and Gillin F.D. Mining the Giardia lamblia genome for new cyst wall proteins. J. Biol. Chem. 278 (2003) 21701-21708
52. Sun C.H., Palm D., McArthur A.G., Svard S.G., and Gillin F.D. A novel Myb-related protein involved in transcriptional activation of encystation genes in Giardia lamblia. Mol. Microbiol. 46 (2002) 971-984
53. Sun C.H., Su L.H., and Gillin F.D. Influence of 5′ sequences on expression of the Tet repressor in Giardia lamblia. Mol. Biochem. Parasitol. 142 (2005) 1-11
54. Sun C.H., Su L.H., and Gillin F.D. Novel plant-GARP-like transcription factors in Giardia lamblia. Mol. Biochem. Parasitol. 146 (2006) 45-57
55. Sun C.H., and Tai J.H. Identification and characterization of a ran gene promoter in the primitive protozoan pathogen Giardia lamblia. J. Biol. Chem. 274 (1999) 19699-19706
56. Takahashi S., Araki Y., Sakuno T., and Katada T. Interaction between Ski7p and Upf1p is required for nonsense-mediated 3′-to-5′ mRNA decay in yeast. EMBO J. 22 (2003) 3951-3959
57. Teodorovic S., Walls C.D., and Elmendorf H.G. Bidirectional transcription is an inherent feature of Giardia lamblia promoters and contributes to an abundance of sterile antisense transcripts throughout the genome. Nucleic Acids Res. 35 (2007) 2544-2553
58. Urlaub G., Mitchell P.J., Ciudad C.J., and Chasin L.A. Nonsense mutations in the dihydrofolate reductase gene affect RNA processing. Mol. Cell Biol. 9 (1989) 2868-2880
59. von Allmen N., Bienz M., Hemphill A., and Muller N. Quantitative assessment of sense and antisense transcripts from genes involved in antigenic variation (vsp genes) and encystation (cwp1 gene) of Giardia lamblia clone GS/M-83-H7. Parasitology 130 (2005) 389-396
60. Weng Y., Czaplinski K., and Peltz S.W. Genetic and biochemical characterization of mutations in the ATPase and helicase regions of the Upf1 protein. Mol. Cell Biol. 16 (1996) 5477-5490
61. Wilkinson M.F. A new function for nonsense-mediated mRNA-decay factors. Trends Genet. 21 (2005) 143-148
62. Yamashita A., Ohnishi T., Kashima I., Taya Y., and Ohno S. Human SMG-1, a novel phosphatidylinositol 3-kinase-related protein kinase, associates with components of the mRNA surveillance complex and is involved in the regulation of nonsense-mediated mRNA decay. Genes Dev. 15 (2001) 2215-2228