Out-of-frame T cell receptor beta transcripts are eliminated by multiple pathways In Vivo

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Mahowald, Grace K ^a   Mahowald, Michael A ^a   Moon, Clara ^a   Khor, Bernard ^a   Sleckman, Barry P ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR BETA CHAIN; LYMPHOCYTE ANTIGEN RECEPTOR; MESSENGER RNA;

ANIMAL CELL; ARTICLE; CELL MATURATION; CODON; CONTROLLED STUDY; DNA MODIFICATION; DNA TEMPLATE; GENE EXPRESSION; GENE FREQUENCY; GENE LOCUS; GENE REARRANGEMENT; GENE TARGETING; GENETIC STABILITY; IN VIVO STUDY; INTRON; LEUKOCYTE METABOLISM; MOUSE; NONHUMAN; PREMATURE TERMINATION CODON; T LYMPHOCYTE; THYMOCYTE; ALLELE; ANIMAL; CYTOLOGY; GENETICS; IMMUNOLOGY; METABOLISM; NUCLEOTIDE SEQUENCE; RNA STABILITY; STOP CODON;

MAMMALIA; MUS;

ALLELES; ANIMALS; CODON, NONSENSE; MICE; READING FRAMES; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RNA STABILITY; RNA, MESSENGER; T-LYMPHOCYTES;

EID: 79960258589     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021627     Document Type: Article

References (34)

1. Bassing CH, Swat W, Alt FW, (2002) The mechanism and regulation of chromosomal V(D)J recombination. Cell 109 (Suppl): S45-55.
2. Fugmann SD, Lee AI, Shockett PE, Villey IJ, Schatz DG, (2000) The RAG proteins and V(D)J recombination: complexes, ends, and transposition. Annu Rev Immunol 18: 495-527.
3. Weischenfeldt J, Damgaard I, Bryder D, Theilgaard-Monch K, Thoren LA, et al. (2008) NMD is essential for hematopoietic stem and progenitor cells and for eliminating by-products of programmed DNA rearrangements. Genes Dev 22: 1381-1396.
4. Brogna S, Wen J, (2009) Nonsense-mediated mRNA decay (NMD) mechanisms. Nat Struct Mol Biol 16: 107-113.
5. Carter MS, Li S, Wilkinson MF, (1996) A splicing-dependent regulatory mechanism that detects translation signals. EMBO J 15: 5965-5975.
6. Zhang J, Sun X, Qian Y, Maquat LE, (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.
7. Thermann R, Neu-Yilik G, Deters A, Frede U, Wehr K, et al. (1998) Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J 17: 3484-3494.
8. Le Hir H, Gatfield D, Izaurralde E, Moore MJ, (2001) The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J 20: 4987-4997.
9. Tange TO, Nott A, Moore MJ, (2004) The ever-increasing complexities of the exon junction complex. Curr Opin Cell Biol 16: 279-284.
10. Nagy E, Maquat LE, (1998) A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem Sci 23: 198-199.
11. Zhang J, Sun X, Qian Y, LaDuca JP, Maquat LE, (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.
12. Buhler M, Steiner S, Mohn F, Paillusson A, Muhlemann O, (2006) EJC-independent degradation of nonsense immunoglobulin-mu mRNA depends on 3′ UTR length. Nat Struct Mol Biol 13: 462-464.
13. Wang J, Gudikote JP, Olivas OR, Wilkinson MF, (2002) Boundary-independent polar nonsense-mediated decay. EMBO Rep 3: 274-279.
14. 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.
15. Matsuda D, Hosoda N, Kim YK, Maquat LE, (2007) Failsafe nonsense-mediated mRNA decay does not detectably target eIF4E-bound mRNA. Nat Struct Mol Biol 14: 974-979.
16. Neu-Yilik G, Gehring NH, Thermann R, Frede U, Hentze MW, et al. (2001) Splicing and 3′ end formation in the definition of nonsense-mediated decay-competent human beta-globin mRNPs. EMBO J 20: 532-540.
17. Brocke KS, Neu-Yilik G, Gehring NH, Hentze MW, Kulozik AE, (2002) The human intronless melanocortin 4-receptor gene is NMD insensitive. Hum Mol Genet 11: 331-335.
18. Maquat LE, 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.
19. Chemin G, Tinguely A, Sirac C, Lechouane F, Duchez S, et al. (2010) Multiple RNA surveillance mechanisms cooperate to reduce the amount of nonfunctional Ig kappa transcripts. J Immunol 184: 5009-5017.
20. Chang YF, Chan WK, Imam JS, Wilkinson MF, (2007) Alternatively spliced T-cell receptor transcripts are up-regulated in response to disruption of either splicing elements or reading frame. J Biol Chem 282: 29738-29747.
21. Valentine CR, (1998) The association of nonsense codons with exon skipping. Mutat Res 411: 87-117.
22. Maquat LE, (2002) NASty effects on fibrillin pre-mRNA splicing: another case of ESE does it, but proposals for translation-dependent splice site choice live on. Genes Dev 16: 1743-1753.
23. Wang J, Chang YF, Hamilton JI, Wilkinson MF, (2002) Nonsense-associated altered splicing: a frame-dependent response distinct from nonsense-mediated decay. Mol Cell 10: 951-957.
24. Imam JS, Gudikote JP, Chan WK, Wilkinson MF, (2010) Frame-disrupting mutations elicit pre-mRNA accumulation independently of frame disruption. Nucleic Acids Res 38: 1559-1574.
25. Lozano F, Maertzdorf B, Pannell R, Milstein C, (1994) Low cytoplasmic mRNA levels of immunoglobulin kappa light chain genes containing nonsense codons correlate with inefficient splicing. EMBO J 13: 4617-4622.
26. Aoufouchi S, Yelamos J, Milstein C, (1996) Nonsense mutations inhibit RNA splicing in a cell-free system: recognition of mutant codon is independent of protein synthesis. Cell 85: 415-422.
27. Carter MS, Doskow J, Morris P, Li S, Nhim RP, et al. (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.
28. Glusman G, Rowen L, Lee I, Boysen C, Roach JC, et al. (2001) Comparative genomics of the human and mouse t cell receptor loci. Immunity 15: 337-349.
29. Brady BL, Steinel NC, Bassing CH, (2010) Antigen receptor allelic exclusion: an update and reappraisal. J Immunol 185: 3801-3808.
30. Khor B, Sleckman BP, (2005) Intra- and inter-allelic ordering of T cell receptor beta chain gene assembly. Eur J Immunol 35: 964-970.
31. Delpy L, Sirac C, Magnoux E, Duchez S, Cogne M, (2004) RNA surveillance down-regulates expression of nonfunctional kappa alleles and detects premature termination within the last kappa exon. Proc Natl Acad Sci U S A 101: 7375-7380.
32. Bassing CH, Alt FW, Hughes MM, D'Auteuil M, Wehrly TD, et al. (2000) Recombination signal sequences restrict chromosomal V(D)J recombination beyond the 12/23 rule. Nature 405: 583-586.
33. Khor B, Mahowald GK, Khor K, Sleckman BP, (2009) Functional overlap in the cis-acting regulation of the V(D)J recombination at the TCRbeta locus. Mol Immunol 46: 321-326.
34. Mahowald GK, Baron JM, Mahowald MA, Kulkarni S, Bredemeyer AL, et al. (2009) Aberrantly resolved RAG-mediated DNA breaks in Atm-deficient lymphocytes target chromosomal breakpoints in cis. Proc Natl Acad Sci U S A 106: 18339-18344.