Nuclear history of a pre-mRNA determines the translational activity of cytoplasmic mRNA

EMBO Journal

Volumn 17, Issue 7, 1998, Pages 2107-2121

  Matsumoto, Ken ^a,b   Wassarman, Karen Montzka ^a   Wolffe, Alan P ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

Author keywords

Nuclear compartments; Ribonuclear protein; Splicing control; Transcriptional control; Translational control

Indexed keywords

MESSENGER RNA; MESSENGER RNA PRECURSOR; PLASMID DNA; RIBONUCLEOPROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENE MUTATION; INTRON; NONHUMAN; OOCYTE; PRIORITY JOURNAL; RNA TRANSCRIPTION; RNA TRANSLATION; SILENCER GENE; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; XENOPUS;

ANIMALS; CELL NUCLEUS; CHLORAMPHENICOL O-ACETYLTRANSFERASE; CYTOPLASM; HISTONES; INTRONS; NUCLEAR PROTEINS; OOCYTES; PROTEIN BIOSYNTHESIS; RNA; RNA PRECURSORS; RNA SPLICING; RNA, MESSENGER; TRANSCRIPTION FACTOR TFIIA; TRANSCRIPTION FACTORS; XENOPUS;

ANIMALIA;

EID: 0032055114     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.7.2107     Document Type: Article

References (95)

1. Almouzni,G. and Wolffe,A.P. (1993) Replication coupled chromatin assembly is required for the repression of basal transcription in vivo. Genes Dev., 7, 2033-2047.
2. Alzhanova-Ericsson,A.T., Sun,X., Visa,N., Kiseleva,E., Wurtz,T. and Daneholt,B. (1996) A protein of the SR family of splicing factors binds extensively to Balbiani ring pre-mRNA and accompanies the RNA from the gene to the nuclear pore. Genes Dev., 10, 2881-2893.
3. Baurén,G. and Wieslander,L. (1994) Splicing of Balbiani ring 1 genepre-mRNA occurs simultaneously with transcription. Cell, 76, 183-192.
4. Baurén,G., Jiang,W.-O., Bernholm,K., Gu,F. and Wieslander,L. (1996) Demonstration of a dynamic, transcription-dependent organization of pre-mRNA splicing factors in polytene nuclei. J. Cell Biol., 133, 929-941.
5. Bienz,M. (1984) Xenopus hsp70 genes are constitutively expressed in injected oocytes. EMBO J., 3, 2477-2483.
6. Boshart,M., Weber,F., Gerhard,J., Dorsch-Hasler,K., Fleckenstern,B. and Schaffner,W. (1985) A very strong enhancer is located upstream of an immediate early gene of human cytomegalovirus. Cell, 41, 521-530.
7. Bouvet,P. and Wolffe,A.P. (1994) A role for transcription and FRGY2 in masking maternal mRNA in Xenopus oocytes. Cell, 77, 931-941.
8. Braddock,M., Muckenthaler,M., White,M.R.H., Thorburn,A.M., Sommerville,J., Kingsman,A.J. and Kingsman,S.M. (1994) Intron-less RNA injected into the nucleus of Xenopus oocytes accesses a regulated translation control pathway. Nucleic Acids Res., 22, 5255-5264.
9. Buchman,A.R. and Berg,P. (1988) Comparison of intron-dependent and intron-independent gene expression. Mol. Cell. Biol., 8, 4395-4405.
10. Cáceres,J.F., Stamm,S., Helfman,D.M. and Krainer,A.R. (1994) Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science, 265, 1706-1709.
11. Carter,M.S., Li,S. and Wilkinson,M.F. (1996) A splicing-dependent regulatory mechanism that detects translation signals. EMBO J., 15, 5965-5975.
12. Champlin,D.T. and Lis,J.T. (1994) Distribution of B52 within a chromosomal locus depends on the level of transcription. Mol. Biol. Cell, 5, 71-79.
13. Champlin,D.T., Frasch,M., Sammweber,H. and Lis,J.T. (1991) Characterization of a Drosophila protein associated with boundaries of transcriptionally active chromatin. Genes Dev., 5, 1611-1621.
14. Chang,D.D. and Sharp,P.A. (1989) Regulation by HIV rev depends upon recognition of splice sites. Cell, 59, 789-795.
15. Cheng,J., Fogel-Petrovic,M. and Maquat,L.E. (1990) Translation to near the distal end of the penultimate exon is required for normal levels of spliced triosephosphate isomerase mRNA. Mol. Cell. Biol., 10, 5215-5225.
16. Cho,H. and Wolffe,A.P. (1994) Characterization of the Xenopus laevis B4 gene: an oocyte specific vertebrate linker histone gene containing introns. Gene, 143, 233-238.
17. Cullen,B.R. (1992) Mechanism of action of regulatory proteins encoded by complex retroviruses. Microbiol. Rev., 56, 375-394.
18. Dantonel,J.C., Murthy,K.G.K., Manley,J.L. and Tora,L. (1997) Transcription factor TFIID recruits factor CPSF for formation of 3′ end of mRNA. Nature, 389, 389-402.
19. Davidson,E.H. (1986) Gene Activity in Early Development. 3rd edn. Academic Press Orlando, USA.
20. Davydova,E.K., Evdokimora,V.M., Ovchinikov,L.P. and Hershey,J.W.B. (1997) Overexpression in COS cells of p50, the major core protein associated with mRNA results in translation inhibition. Nucleic Acids Res., 25, 2911-2916.
21. Dimitrov,S., Almouzni,G., Dasso,M. and Wolffe,A.P., (1993) Chromatin transitions during early Xenopus embryogenesis: changes in histone H4 acetylation and in linker histone type. Dev. Biol.,160, 214-227.
22. Dimitrov,S., Dasso,M.C. and Wolffe,A.P. (1994) Remodeling sperm chromatin in Xenopus laevis egg extracts: the role of core histone phosphorylation and linker histone B4 in chromatin assembly. J. Cell Biol., 126, 591-601.
23. Dreyfuss,G., Matunis,M.J., Pinol-Roma,S. and Burd,C.G. (1993) hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem., 62, 289-321.
24. Du,L. and Warren,S. (1997) A functional interaction between the carboxy-terminal domain of RNA polymerase II and pre-mRNA splicing. J. Cell Biol., 136, 5-18.
25. Dworkin,M.B., Shrutkowski,A. and Dworkin-Rastl,E. (1985) Mobilization of specific maternal RNA species into polysomes after fertilization in Xenopus laevis. Proc. Natl Acad. Sci. USA, 82, 7636-7640.
26. Dworkin-Rastl,E., Kandolf,H. and Smith,R.C. (1994) The maternal histone H1 variant HIM (B4 protein) is the predominant HI histone in Xenopus pregastrula embryos. Dev. Biol., 161, 425-439.
27. Enssle,J., Kugler,W., Hentze,M.W. and Kulozik,A.E. (1993) Determination of mRNA fate by different RNA polymerase II promoters. Proc. Natl Acad. Sci. USA. 90, 10091-10095.
28. Fischer,U., Meyer,S., Teufel,M., Heckel,G. Lührmann,R. and Rautmann,G. (1994) Evidence that HIV-1 Rev directly promotes the nuclear export of unspliced RNA. EMBO J., 13, 4105-4112.
29. Fischer,U., Huber J.,Boelens,W.C., Mattaj,I.W. and Lührmann,R. (1995) The HIV-1 rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell, 82, 475-483.
30. Fu,X.-D. (1993) Specific commitment of different pre-mRNAs to splicing by single SR proteins. Nature, 365, 82-85.
31. Gurikel,N., Braddock,M., Thorburn,A.M., Muckenthaler,M., Kingsman,A.J. and Kingsman,S.M. (1995) Promoter control of translation in Xenopus oocytes. Nucleic Acids Res., 23, 405-412.
32. Hamer,D., Smith,K., Boyer,S. and Leder,P. (1979) SV40 recombinants carrying rabbit β-globin coding sequences. Cell, 17, 725-735.
33. Hawkins,J.D. (1988) A survey of intron and exon lengths. Nucleic Acids Res., 16, 9893-9908.
34. Horell,A., Shuttlewonh,J. and Colman,A. (1987) Transcript level and translational control of hsp 70 synthesis in Xenopus oocytes. Genes Dev., 1, 433-444.
35. Huang,J. and Liang,T.J. (1993) A novel hepatitis B virus (HBV) genetic element with Rev response element-like properties that is essential for expression of HBV gene products. Mol. Cell. Biol., 13, 7476-7486.
36. Huang,M.T.F. and Gorman,C.M. (1990) The simian virus 40 small t intron, present in many common expression vectors, leads to aberrant splicing. Mol. Cell. Biol., 10, 1805-1810.
37. Huang,S. and Spector,D.L. (1996) Intron-dependent recruitment of pre-mRNA splicing factors to sites of transcription. J. Cell Biol., 133, 719-732.
38. Huang,Y. and Carmichael,G.G. (1996) A suboptimal 5′ splice site is a cis-acting determinant of nuclear export of polyoma late mRNAs. Mol. Cell. Biol., 16, 6046-6054.
39. Jarmolowski,A., Boelens,W.C., Izaurralde,E. and Mattaj,J.W. (1994) Nuclear export of different classes of RNA is mediated by specific factors. J. Cell Biol., 124, 627-635.
40. Jiang,W., Hou,Y. and Inouye,M. (1997) CspA, the major cold shock protein of Escherichia coli is an RNA chaperone. J. Biol. Chem., 272, 196-202.
41. Jiménez-Garcia,L.F. and Spector,D.L. (1993) In vivo evidence that transcription and splicing are coordinated by a recruiting mechanism. Cell, 73, 47-59.
42. Kim,E., Du,L., Bregman,D.B. and Warren,S.L. (1997) Splicing factors associate with hyperphosphorylated RNA polymerase II in the absence of pre-mRNA. J. Cell Biol., 136, 19-28.
43. Kim,Y.-J., Zuo,P., Manley,J.L. and Baker,B.S. (1992) The Drosophila RNA-binding protein RBP1 is localized to transcriptionally active sites of chromsomes and shows a functional similarity to human splicing factor ASF/SF2. Genes Dev., 6, 2569-2579.
44. Kiseleva,E., Wurtz,T., Visa,N. and Daneholt,B. (1994) Assembly and disassembly of spliceosomes along a specific pre-messenger RNP fiber. EMBO J., 13, 6052-6061.
45. Kjems,J. and Sharp,P.A. (1993) The basic domain of rev from human immunodeficiency virus type-1 specifically blocks the entry of U4/U6 u5 small nuclear ribonucleoprotein in spliceosome assembly. J. Virol., 67, 4769-4776.
46. Kozak,M. (1992) Regulation of translation in eukaryotic systems. Annu. Rev. Cell Biol. 8, 197-225.
47. Kuge,H. and Richter,J.D. (1995)Cytoplasmic 3′ poly(A) addition induces 5′ cap ribose methylation: implications for translational control of maternal mRNA. EMBO J., 14, 6301-6310.
48. Legrain,P. and Rosbash,M. (1989) Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm. Cell, 57, 573-583.
49. Lonnroth,A., Alexciev,K., Mehlin,H., Wurtz,T., Skoglund,U. and Daneholt,B. (1992) Demonstration of a 7 nm RNP fiber as the basic structural element in a premessenger RNP particle. Exp. Cell Res., 199, 292-296.
50. McGrew,L.L., Dworkin-Rastl,E., Dworkin,M.B. and Richter,J.D. (1989) Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes Dev. , 3, 803-815.
51. Maquat,L.E. (1991) Nuclear mRNA export. Curr. Opin. Cell Biol., 3, 1004-1012.
52. Matsumoto,K., Okuwaki,M., Kawase,H., Handa,H., Hanaoka,F. and Nagata,K. (1995) Stimulation of DNA transcription by the replication factor from the adenovirus genome in a chromatin-like structure. J. Biol. Chem., 270, 9645-9650.
53. Matsumoto,K., Meric,F. and Wolffe,A.P. (1996) Translational repression dependent on the interaction of the Xenopus Y-box protein FRGY2 with mRNA. J. Biol. Chem., 271, 22706-22712.
54. Mayeda,A. and Krainer,A.R. (1992) Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell, 68, 365-375.
55. Mehlin,H., Daneholt,B. and Skoglund,U. (1992) Translocation of a specific premessenger ribonucleoprotein particle through the nuclear pore studied with electron microscope tomography. Cell, 69, 605-613.
56. Mehlin,H., Daneholt,B. and Skoglund,U. (1995) Structural interaction between the nuclear pore complex and a specific translocating RNP particle. J. Cell Biol., 129, 1205-1216.
57. Meric,F., Matsumoto,K. and Wolffe,A.P. (1997) Regulated unmasking of in vivo synthesized maternal mRNA at oocyte maturation: a role for the chaperone nucleoplasmin. J. Biol. Chem., 272, 12840-12846.
58. Meric,F., Searfoss,A.M., Wormington,M. and Wolffe,A.P. (1996) Masking and unmasking maternal mRNA: the role of polyadenylation, transcriptions splicing and nuclear history. J. Biol. Chem., 271, 30804-30810.
59. Murray,M.T., Schiller,D.L. and Franke,W.W. (1992) Sequence analysis of cytoplasmic mRNA-binding proteins of Xenopus oocytes identifies a family of RNA-binding proteins. Proc. Natl Acad. Sci. USA, 89, 11-15.
60. Osheim,Y.N., Miller,O.L., Jr, and Beyer,A.L. (1985) RNP particles at splice junction sequences on Drosophila chorion transcripts. Cell, 43, 143-151.
61. Perry,M., Thomson,G.H. and Roeder,R.G. (1985) Genomic organization and nucleotide sequence of two distinct histone gene clusters from Xenopus laevis: identification of novel conserved upstream sequence elements. J. Mol. Biol., 185, 479-499.
62. Pinol-Roma,S. and Dreyfuss,G. (1992) Shutting of pre-mRNA binding proteins between nucleus and cytoplasm. Nature, 355, 730-732.
63. Ramamurthy,L., Ingledue,T.C, Pilch,D.R., Kay,B.K. and MarzInff,W.F. (1996) Increasing the distance between the snRNA promoter and the 3′ box decreases the efficiency of snRNA 3′-end formation. Nucleic Acids Res., 24, 4524-4534.
64. Ranjan,M., Tafuri,S.R. and Wolffe,A.P. (1993) Masking mRNA from translation in somatic cells. Genes Dev., 7, 1725-1736.
65. Richter,J.D. (1988) Information relay from gene to protein: the mRNP connection. Trends Biochem. Sci., 13, 483-486.
66. Richter,J.D. and Smith,L.D. (1984) Reversible inhibition of translation by Xenopus oocyte specific proteins. Nature, 309, 378-380.
67. Roth,M.B., Murphy,C. and Gall,J.G. (1990) A monoclonal antibody that recognizes a phosphorylated epitope stains lampbrush chromosome loops and small granules in the amphibian germinal vesicle. J. Cell Biol., 111, 2217-2223.
68. Ruderman,J.V., Woodland,H.R. and Sturgess,E.A. (1979) Modulations of histone mRNA during the early development of Xenopus laevis. Dev. Biol., 71, 71-82.
69. Ryu,W.S. and Mertz,J.E. (1989) Simian virus 40 late transcripts lacking excisable intervening sequences are defective in both stability in the nucleus and transport to the cytoplasm. J. Virol., 63, 4386-4394.
70. Senapathy,P., Shapiro,M.B. and Harris,N.L. (1990) Splice junctions, branch point sites, and exons: sequence statistics, identification and applications to the genome project. Methods Enzymol. 183, 252-278.
71. Sheets,M.D., Fox,C.A., Hunt,T., Vande Wonde,G. and Wickens,M. (1994) The 3′-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev., 8, 926-938.
72. Sheets,M.D., Wu,M. and Wickens,M. (1995) Polyadenylation of c-mos mRNA as a control point in Xenopus meiotic maturation. Nature. 374, 511-516.
73. Smith,R.C., Dworkin-Rastl,E. and Dworkin,M.D. (1988) Expression of a histone H1-like protein is restricted to early Xenopus development. Genes Dev., 2, 1284-1295.
74. Sommerville,J. (1990) RNA binding phosphoproteins and the regulation of maternal mRNA in Xenopus. J. Reprod. Fertil. Suppl., 42, 225-233.
75. Sommerville,J., Baird,J. and Turner,B.M. (1993) Histone H4 acetylation and transcription in amphibian chromatin. J. Cell Biol., 120, 277-290.
76. Spirin,A.S. (1966) On 'masked' forms of messenger RNA in early embrogenesis and in other differentiating systems. Curr. Top. Dev. Biol., 1, 1-63.
77. Standart,N. (1992) Masking and unmasking of maternal mRNA. Semin. Dev. Biol., 3, 367-379.
78. Steinmetz,E.J. and Brow,D.A. (1996) Repression of gene expression by an exogenous sequence element acting in concert with a heterogenous nuclear ribonucleoprotein-like protein, Nrd1, and the putative helicase Sen1. Mol. Cell. Biol., 16, 6993-7003.
79. Stutz,F., Neville,M. and Rosbash,M. (1995) Identification of a novel nuclear pore associated protein as a functional target of the HIV-1 rev protein in yeast. Cell, 82, 495-506.
80. Tafuri,S.R. and Wolffe,A.P. (1990) Xenopus Y-box transcription factors: molecular cloning, functional analysis and developmental regulation. Proc. Natl Acad. Sci. USA, 87, 9028-9032.
81. Tafuri,S.R. and Wolffe,A.P. (1993) Selective recruitment of masked maternal mRNA from messenger ribonucleoprotein particles containing FRGY2 (mRNP4). J. Biol. Chem., 257, 24255-24261.
82. Tarun,S.Z., Jr, and Sachs,A.B. (1995) A common function for mRNA 5′ and 3′ ends in translation initiation in yeast. Genes Dev., 9, 2997-3007.
83. Tarun,S.Z., Jr, and Sachs,A.B. (1996) Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J., 15, 7168-7177.
84. Tso,J.Y., Van Den Berg,D.J. and Korn,L.J. (1986) Structure of the gene for Xenopus transcription factor TFIIIA. Nucleic Acids Res., 14, 2187-2200.
85. Visa,N., Alzhanova-Ericsson,A.T., Sun,X., Kiseleva,E., Bjorkroth,B., Wurtz,T. and Daneholt,B. (1996) A pre-mRNA-binding protein accompanies the RNA from the gene through the nuclear pores and into polysomes. Cell, 84, 253-264.
86. Wang,J. and Manley,J.L. (1995) Overexpression of the SR proteins ASF/SF2 and SC35 influences alternative splicing in vivo in diverse ways. RNA, 1, 335-346.
87. Watanabe,N., van de Woude,G.F., Ikawa,Y. and Sagata,N. (1989) Specific proteolysis of the c-mos proto-oncogene product by calpain on fertilization of Xenopus eggs. Nature, 342, 505-511.
88. Wickens,M. (1992) Forward, backward, how much, when: mechanisms of poly(A) addition and removal and their role in early development. Semin. Dev. Biol., 3, 399-412.
89. Wolffe,A.P. (1995) Chromatin: Structure and Function. 2nd edn. Academic Press, London, UK.
90. Wolffe,A.P. and Meric,F. (1996) Coupling transcription to translation: a novel site for the regulation of eukaryotic gene expression. Int. J. Biochem. Cell Biol., 28, 247-257.
91. Wolffe,A.P., Tafuri,S., Ranjan,M. and Familari,M. (1992) The Y-box factors: a family of nucleic acid binding proteins conserved from Escherichia coli to man. New Biol., 4, 290-298.
92. Wormington,M.W. (1993) Poly(A) and translation: developmental control. Curr. Opin. Cell Biol., 5, 950-954.
93. Wurtz,T.A., Lönnroth,L., Ovchinnikov,L., Skoglund,U. and Daneholt,B. (1990) Isolation and initial characterization of a specific premessenger ribonucleoprotein particle. Proc. Natl Acad. Sci. USA, 87, 831-835.
94. Wurtz,T., Kiseleva,E., Nacheva,G., Alzhanova-Ericsson,A., Rosén,A. and Daneholt,B. (1996) Identification of two RNA-binding proteins in Balbiani ring premessenger ribonucleoprotein granules and presence of these proteins in specific subsets of heterogenous nuclear ribonucleoprotein panicles. Mol. Cell. Biol., 16, 1425-1435.
95. Yuryev,A., Patturajan,M., Litingtung,Y., Joshi,R.V., Gentile,C., Gebara,M. and Corden,J.L. (1996) The C-terminal domain of the largest subunit of RNA polymerase II interacts with a novel set of serine/arginine-rich proteins. Proc. Natl Acad. Sci. USA, 93, 6975-6980.