Export and stability of naturally intronless mRNAs require specific coding region sequences and the TREX mRNA export complex

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 44, 2011, Pages 17985-17990

  Lei, Haixin ^a   Dias, Anusha P ^a   Reed, Robin ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA1 INTERFERON; BETA1 INTERFERON; COMPLEMENTARY DNA; HEAT SHOCK PROTEIN; INTRONLESS MESSENGER RNA; MESSENGER RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; INTRON; PRIORITY JOURNAL; REGULATORY RNA SEQUENCE; RNA STABILITY; RNA TRANSPORT;

BIOLOGICAL TRANSPORT; CELL NUCLEUS; CYTOPLASM; DNA, COMPLEMENTARY; INTRONS; RNA, MESSENGER;

EID: 81055126291     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1113076108     Document Type: Article

References (51)

1. Shabalina SA, et al. (2010) Distinct patterns of expression and evolution of intronless and intron-containing mammalian genes. Mol Biol Evol 27:1745-1749.
2. Cramer P, et al. (2001) Coordination between transcription and pre-mRNA processing. FEBS Lett 498:179-182. (Pubitemid 32539198)
3. Maniatis T, Reed R (2002) An extensive network of coupling among gene expression machines. Nature 416:499-506. (Pubitemid 34288845)
4. Perales R, Bentley D (2009) "Cotranscriptionality": The transcription elongation complex as a nexus for nuclear transactions. Mol Cell 36:178-191.
5. Moore MJ, Proudfoot NJ (2009) Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136:688-700.
6. Reed R, Hurt E (2002) A conserved mRNA export machinery coupled to pre-mRNA splicing. Cell 108:523-531. (Pubitemid 34260877)
7. Köhler A, Hurt E (2007) Exporting RNA from the nucleus to the cytoplasm. Nat Rev Mol Cell Biol 8:761-773. (Pubitemid 47462133)
8. Dufu K, et al. (2010) ATP is required for interactions between UAP56 and two conserved mRNA export proteins, Aly and CIP29, to assemble the TREX complex. Genes Dev 24:2043-2053.
9. Masuda S, et al. (2005) Recruitment of the human TREX complex to mRNA during splicing. Genes Dev 19:1512-1517. (Pubitemid 41002995)
10. Cheng H, et al. (2006) Human mRNA export machinery recruited to the 5′ end of mRNA. Cell 127:1389-1400. (Pubitemid 44960410)
11. Zenklusen D, Vinciguerra P, Wyss JC, Stutz F (2002) Stable mRNP formation and export require cotranscriptional recruitment of the mRNA export factors Yra1p and Sub2p by Hpr1p. Mol Cell Biol 22:8241-8253. (Pubitemid 35304057)
12. Abruzzi KC, Lacadie S, Rosbash M (2004) Biochemical analysis of TREX complex recruitment to intronless and intron-containing yeast genes. EMBO J 23:2620-2631. (Pubitemid 38988233)
13. Johnson SA, Cubberley G, Bentley DL (2009) Cotranscriptional recruitment of the mRNA export factor Yra1 by direct interaction with the 3′ end processing factor Pcf11. Mol Cell 33:215-226.
14. Zhao R, Bodnar MS, Spector DL (2009) Nuclear neighborhoods and gene expression. Curr Opin Genet Dev 19:172-179.
15. Molenaar C, Abdulle A, Gena A, Tanke HJ, Dirks RW (2004) Poly(A)+ RNAs roam the cell nucleus and pass through speckle domains in transcriptionally active and inactive cells. J Cell Biol 165:191-202. (Pubitemid 38544522)
16. Hall LL, Smith KP, Byron M, Lawrence JB (2006) Molecular anatomy of a speckle. Anat Rec A Discov Mol Cell Evol Biol 288:664-675. (Pubitemid 44015467)
17. Dias AP, Dufu K, Lei H, Reed R (2010) A role for TREX components in the release of spliced mRNA from nuclear speckle domains. Nat Commun, 10.1038/ncomms1103.
18. Moore MJ (2005) From birth to death: The complex lives of eukaryotic mRNAs. Science 309:1514-1518.
19. Boyne JR, Colgan KJ, Whitehouse A (2008) Herpesvirus saimiri ORF57: A post-transcriptional regulatory protein. Front Biosci 13:2928-2938. (Pubitemid 351606108)
20. Chen IH, Sciabica KS, Sandri-Goldin RM (2002) ICP27 interacts with the RNA export factor Aly/REF to direct herpes simplex virus type 1 intronless mRNAs to the TAP export pathway. J Virol 76:12877-12889. (Pubitemid 35386971)
21. Guang S, Felthauser AM, Mertz JE (2005) Binding of hnRNP L to the pre-mRNA processing enhancer of the herpes simplex virus thymidine kinase gene enhances both polyadenylation and nucleocytoplasmic export of intronless mRNAs. Mol Cell Biol 25:6303-6313. (Pubitemid 41023208)
22. Toth Z, Stamminger T (2008) The human cytomegalovirus regulatory protein UL69 and its effect on mRNA export. Front Biosci 13:2939-2949. (Pubitemid 351589210)
23. Wang W, et al. (2008) Imaging and characterizing influenza A virus mRNA transport in living cells. Nucleic Acids Res 36:4913-4928.
24. Huang Y, Carmichael GG (1997) The mouse histone H2a gene contains a small element that facilitates cytoplasmic accumulation of intronless gene transcripts and of unspliced HIV-1-related mRNAs. Proc Natl Acad Sci USA 94:10104-10109.
25. Huang Y, Wimler KM, Carmichael GG (1999) Intronless mRNA transport elements may affect multiple steps of pre-mRNA processing. EMBO J 18:1642-1652.
26. Erkmann JA, Sànchez R, Treichel N, Marzluff WF, Kutay U (2005) Nuclear export of metazoan replication-dependent histone mRNAs is dependent on RNA length and is mediated by TAP. RNA 11:45-58. (Pubitemid 40041572)
27. Huang Y, Gattoni R, Stévenin J, Steitz JA (2003) SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol Cell 11:837-843. (Pubitemid 36385134)
28. Gilbert W, Guthrie C (2004) The Glc7p nuclear phosphatase promotes mRNA export by facilitating association of Mex67p with mRNA. Mol Cell 13:201-212. (Pubitemid 38183267)
29. Kimura T, Hashimoto I, Nagase T, Fujisawa J (2004) CRM1-dependent, but not ARE-mediated, nuclear export of IFN-alpha1 mRNA. J Cell Sci 117:2259-2270. (Pubitemid 38807494)
30. Masuyama K, Taniguchi I, Kataoka N, Ohno M (2004) RNA length defines RNA export pathway. Genes Dev 18:2074-2085. (Pubitemid 39166625)
31. Nojima T, Hirose T, Kimura H, Hagiwara M (2007) The interaction between cap-binding complex and RNA export factor is required for intronless mRNA export. J Biol Chem 282:15645-15651. (Pubitemid 47093268)
32. Ullman KS (2002) RNA export: Searching for mRNA identity. Curr Biol 12:R461-R463.
33. Conrad NK, Steitz JA (2005) A Kaposi's sarcoma virus RNA element that increases the nuclear abundance of intronless transcripts. EMBO J 24:1831-1841. (Pubitemid 40769502)
34. Nott A, Meislin SH, Moore MJ (2003) A quantitative analysis of intron effects on mammalian gene expression. RNA 9:607-617. (Pubitemid 36505458)
35. Lu S, Cullen BR (2003) Analysis of the stimulatory effect of splicing on mRNA production and utilization in mammalian cells. RNA 9:618-630. (Pubitemid 36505459)
36. Taniguchi I, Ohno M (2008) ATP-dependent recruitment of export factor Aly/REF onto intronless mRNAs by RNA helicase UAP56. Mol Cell Biol 28:601-608.
37. Conrad NK, Mili S, Marshall EL, Shu MD, Steitz JA (2006) Identification of a rapid mammalian deadenylation-dependent decay pathway and its inhibition by a viral RNA element. Mol Cell 24:943-953. (Pubitemid 44960087)
38. Wyers F, et al. (2005) Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121:725-737. (Pubitemid 40797595)
39. Lei EP, Silver PA (2002) Intron status and 3′-end formation control cotranscriptional export of mRNA. Genes Dev 16:2761-2766. (Pubitemid 35253143)
40. Libri D, et al. (2002) Interactions between mRNA export commitment, 3′-end quality control, and nuclear degradation. Mol Cell Biol 22:8254-8266. (Pubitemid 35304058)
41. Hilleren P, McCarthy T, Rosbash M, Parker R, Jensen TH (2001) Quality control of mRNA 3′-end processing is linked to the nuclear exosome. Nature 413:538-542. (Pubitemid 32938754)
42. Huang Y, Carmichael GG (1996) Role of polyadenylation in nucleocytoplasmic transport of mRNA. Mol Cell Biol 16:1534-1542. (Pubitemid 26095624)
43. Fuke H, Ohno M (2008) Role of poly (A) tail as an identity element for mRNA nuclear export. Nucleic Acids Res 36:1037-1049. (Pubitemid 351267257)
44. Valencia P, Dias AP, Reed R (2008) Splicing promotes rapid and efficient mRNA export in mammalian cells. Proc Natl Acad Sci USA 105:3386-3391. (Pubitemid 351723562)
45. Hautbergue GM, et al. (2009) UIF, a new mRNA export adaptor that works together with REF/ALY, requires FACT for recruitment to mRNA. Curr Biol 19:1918-1924.
46. Rougemaille M, Villa T, Gudipati RK, Libri D (2008) mRNA journey to the cytoplasm: Attire required. Biol Cell 100:327-342. (Pubitemid 351803963)
47. Saguez C, Olesen JR, Jensen TH (2005) Formation of export-competent mRNP: Escaping nuclear destruction. Curr Opin Cell Biol 17:287-293. (Pubitemid 40719919)
48. Guang S, Mertz JE (2005) Pre-mRNA processing enhancer (PPE) elements from intronless genes play additional roles in mRNA biogenesis than do ones from intron-containing genes. Nucleic Acids Res 33:2215-2226. (Pubitemid 41439890)
49. Conrad NK, Shu MD, Uyhazi KE, Steitz JA (2007) Mutational analysis of a viral RNA element that counteracts rapid RNA decay by interaction with the polyadenylate tail. Proc Natl Acad Sci USA 104:10412-10417. (Pubitemid 47185679)
50. Mitton-Fry RM, DeGregorio SJ, Wang J, Steitz TA, Steitz JA (2010) Poly(A) tail recognition by a viral RNA element through assembly of a triple helix. Science 330:1244-1247.
51. Lei H, Vorechovsky I (2005) Identification of splicing silencers and enhancers in sense Alus: A role for pseudoacceptors in splice site repression. Mol Cell Biol 25:6912-6920. (Pubitemid 41105892)