A complex containing the CPSF73 endonuclease and other polyadenylation factors associates with U7 snrnp and is recruited to histone pre-mRNA for 3'-end processing

Molecular and Cellular Biology

Volumn 33, Issue 1, 2013, Pages 28-37

  Yang, Xiao Cui ^a   Sabath, Ivan ^a   Dȩbski, Jan ^b   Kaus Drobek, Magdalena ^b   Dadlez, Michał ^b,c   Marzluff, William ^a   Dominski, Zbigniew ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^c UNIVERSITY OF WARSAW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CPSF73 ENDONUCLEASE; CSTF64 PROTEIN; ENDONUCLEASE; FLASH PROTEIN; HISTONE; LSM11 PROTEIN COMPLEX; MESSENGER RNA PRECURSOR; PROTEIN; RECOMBINANT PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN; SYMPLEKIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BASE PAIRING; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; POINT MUTATION; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION;

AMINO ACID MOTIFS; ANIMALS; APOPTOSIS REGULATORY PROTEINS; BASE SEQUENCE; CALCIUM-BINDING PROTEINS; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; HELA CELLS; HISTONES; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; MUTATION; NUCLEAR PROTEINS; RECOMBINANT PROTEINS; RIBONUCLEOPROTEIN, U7 SMALL NUCLEAR; RNA 3' END PROCESSING; RNA PRECURSORS; RNA-BINDING PROTEINS;

ANIMALIA;

EID: 84871898346     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00653-12     Document Type: Article

References (54)

1. Colgan DF, Manley JL. 1997. Mechanism and regulation of mRNA polyadenylation. Genes Dev. 11:2755-2766.
2. Mandel CR, Bai Y, Tong L. 2008. Protein factors in pre-mRNA 3=-end processing. Cell Mol. Life Sci. 65:1099-1122.
3. Proudfoot NJ. 2011. Ending the message: poly(A) signals then and now. Genes Dev. 25:1770-1782.
4. Zhao J, Hyman L, Moore C. 1999. Formation of mRNA 3= ends in eukaryotes: mechanism, regulation, and interrelationships with other steps in mRNA synthesis. Microbiol. Mol. Biol. Rev. 63:405-445.
5. Kaufmann I, Martin G, Friedlein A, Langen H, Keller W. 2004. Human Fip1 is a subunit of CPSF that binds to U-rich RNA elements and stimulates poly(A) polymerase. EMBO J. 23:616-626.
6. Shi Y, Di Giammartino DC, Taylor D, Sarkeshik A, Rice WJ, Yates JR III, Frank J, Manley JL. 2009. Molecular architecture of the human pre-mRNA 3= processing complex. Mol. Cell 33:365-376.
7. Mandel CR, Kaneko S, Zhang H, Gebauer D, Vethantham V, Manley JL, Tong L. 2006. Polyadenylation factor CPSF-73 is the pre-mRNA 3=- end-processing endonuclease. Nature 444:953-956.
8. Takagaki Y, Manley JL. 2000. Complex protein interactions within the human polyadenylation machinery identify a novel component. Mol. Cell. Biol. 20:1515-1525.
9. Ruegsegger U, Blank D, Keller W. 1998. Human pre-mRNA cleavage factor Im is related to spliceosomal SR proteins and can be reconstituted in vitro from recombinant subunits. Mol. Cell 1:243-253.
10. De Vries H, Rüegsegger U, Hübner W, Friedlein A, Langen H, Keller W. 2000. Human pre-mRNA cleavage factor IIm contains homologs of yeast proteins and bridges two other cleavage factors. EMBO J. 19:5895-5904.
11. Ghazy MA, He X, Singh BN, Hampsey M, Moore C. 2009. The essential N terminus of the Pta1 scaffold protein is required for snoRNA transcrip tion termination and Ssu72 function but is dispensable for pre-mRNA 3=-end processing. Mol. Cell. Biol. 29:2296-2307.
12. Kyburz A, Sadowski M, Dichtl B, Keller W. 2003. The role of the yeast cleavage and polyadenylation factor subunit Ydh1p/Cft2p in pre-mRNA 3=-end formation. Nucleic Acids Res. 31:3936-3945.
13. Barnard DC, Ryan K, Manley JL, Richter JD. 2004. Symplekin and xGLD-2 are required for CPEB-mediated cytoplasmic polyadenylation. Cell 119:641-651.
14. Dominski Z, Marzluff WF. 2007. Formation of the 3= end of histone mRNA: getting closer to the end. Gene 396:373-390.
15. Muller B, Schumperli D. 1997. The U7 snRNP and the hairpin binding protein: key players in histone mRNA metabolism. Semin. Cell Dev. Biol. 8:567-576.
16. Galli G, Hofstetter H, Stunnenberg HG, Birnstiel ML. 1983. Biochemical complementation with RNA in the Xenopus oocyte: a small RNA is required for the generation of 3= histonemRNAtermini. Cell 34:823-828.
17. Mowry KL, Steitz JA. 1987. Identification of the human U7 snRNP as one of several factors involved in the 3= end maturation of histone premessenger RNA's. Science 238:1682-1687.
18. Scharl EC, Steitz JA. 1994. The site of 3= end formation of histone messenger RNA is a fixed distance from the downstream element recognized by the U7 snRNP. EMBO J. 13:2432-2440.
19. Schumperli D, Pillai RS. 2004. The special Sm core structure of the U7 snRNP: far-reaching significance of a small nuclear ribonucleoprotein. Cell. Mol. Life Sci. 61:2560-2570.
20. Cotten M, Gick O, Vasserot A, Schaffner G, Birnstiel ML. 1988. Specific contacts between mammalian U7 snRNA and histone precursor RNA are indispensable for the in vitro RNA processing reaction. EMBO J. 7:801-808.
21. Martin F, Schaller A, Eglite S, Schümperli D, Müller B. 1997. The gene for histone RNA hairpin binding protein is located on human chromosome 4 and encodes a novel type of RNA binding protein. EMBO J. 16: 769-778.
22. Wang Z-F, Whitfield ML, Ingledue TI, Dominski Z, Marzluff WF. 1996. The protein which binds the 3= end of histone mRNA: a novel RNAbinding protein required for histone pre-mRNA processing. Genes Dev. 10:3028-3040.
23. Dominski Z, Zheng LX, Sanchez R, Marzluff WF. 1999. Stem-loop binding protein facilitates 3=-end formation by stabilizing U7 snRNP binding to histone pre-mRNA. Mol. Cell. Biol. 19:3561-3570.
24. Streit A, Koning TW, Soldati D, Melin L, Schümperli D. 1993. Variable effects of the conserved RNA hairpin element upon 3= end processing of histone pre-mRNA in vitro. Nucleic Acids Res. 21:1569-1575.
25. Azzouz TN, Gruber A, Schumperli D. 2005. U7 snRNP-specific Lsm11 protein: dual binding contacts with the 100 kDa zinc finger processing factor (ZFP100) and a ZFP100-independent function in histone RNA 3= end processing. Nucleic Acids Res. 33:2106-2117.
26. Yang XC, Burch BD, Yan Y, Marzluff WF, Dominski Z. 2009. FLASH, a proapoptotic protein involved in activation of caspase-8, is essential for 3= end processing of histone pre-mRNAs. Mol. Cell 36:267-278.
27. Barcaroli D, Bongiorno-Borbone L, Terrinoni A, Hofmann TG, Rossi M, Knight RA, Matera AG, Melino G, De Laurenzi V. 2006. FLASH is required for histone transcription and S-phase progression. Proc. Natl. Acad. Sci. U. S. A. 103:14808-14812.
28. De Cola A, Bongiorno-Borbone L, Bianchi E, Barcaroli D, Carletti E, Knight RA, Di Ilio C, Melino G, Sette C, De Laurenzi V. 2012. FLASH is essential during early embryogenesis and cooperates with p73 to regulate histone gene transcription. Oncogene 31:573-582.
29. Alm-Kristiansen AH, Saether T, Matre V, Gilfillan S, Dahle O, Gabrielsen OS. 2008. FLASH acts as a co-activator of the transcription factor c-Myb and localizes to activeRNApolymerase II foci. Oncogene 27:4644-4656.
30. Imai Y, Kimura T, Murakami A, Yajima N, Sakamaki K, Yonehara S. 1999. The CED-4-homologous protein FLASH is involved in Fasmediated activation of caspase-8 during apoptosis. Nature 398:777-785.
31. Dominski Z, Yang XC, Marzluff WF. 2005. The polyadenylation factor CPSF-73 is involved in histone-pre-mRNA processing. Cell 123:37-48.
32. Kolev NG, Steitz JA. 2005. Symplekin and multiple other polyadenylation factors participate in 3=-end maturation of histone mRNAs. Genes Dev. 19:2583-2592.
33. Kolev NG, Yario TA, Benson E, Steitz JA. 2008. Conserved motifs in both CPSF73 and CPSF100 are required to assemble the active endonuclease for histone mRNA 3=-end maturation. EMBO Rep. 9:1013-1018.
34. Wagner EJ, Burch BD, Godfrey AC, Salzler HR, Duronio RJ, Marzluff WF. 2007. A genome-wide RNA interference screen reveals that variant histones are necessary for replication-dependent histone pre-mRNA processing. Mol. Cell 28:692-699.
35. Dominski Z, Sumerel J, Hanson RJ, Marzluff WF. 1995. The polyribosomal protein bound to the 3= end of histone mRNA can function in histone pre-mRNA processing. RNA 1:915-923.
36. Yang XC, Torres MP, Marzluff WF, Dominski Z. 2009. Three proteins of the U7-specificSmring function as the molecular ruler to determine the site of 3=-end processing in mammalian histone pre-mRNA. Mol. Cell. Biol. 29:4045-4056.
37. Yang XC, Xu B, Sabath I, Kunduru L, Burch BD, Marzluff WF, Dominski Z. 2011. FLASH is required for the endonucleolytic cleavage of histone pre-mRNAs but is dispensable for the 5= exonucleolytic degradation of the downstream cleavage product. Mol. Cell. Biol. 31:1492-1502.
38. Burch BD, Godfrey AC, Gasdaska PY, Salzler HR, Duronio RJ, Marzluff WF, Dominski Z. 2011. Interaction between FLASH and Lsm11 is essential for histone pre-mRNA processing in vivo in Drosophila. RNA 17: 1132-1147.
39. Wei N, Serino G, Deng XW. 2008. The COP9 signalosome: more than a protease. Trends Biochem. Sci. 33:592-600.
40. Ruepp MD, Schweingruber C, Kleinschmidt N, Schumperli D. 2011. Interactions of CstF-64, CstF-77, and symplekin: implications on localisation and function. Mol. Biol. Cell 22:91-104.
41. McCall CM, Miliani de Marval PL, Chastain PD, Jackson SC, He YJ, Kotake Y, Cook JG, Xiong Y. 2008. Human immunodeficiency virus type 1 Vpr-binding protein VprBP, aWD40protein associated with the DDB1- CUL4 E3 ubiquitin ligase, is essential for DNA replication and embryonic development. Mol. Cell. Biol. 28:5621-5633.
42. Yang XC, Sullivan KD, Marzluff WF, Dominski Z. 2009. Studies of the 5= exonuclease and endonuclease activities of CPSF-73 in histone premRNA processing. Mol. Cell. Biol. 29:31-42.
43. Kiriyama M, Kobayashi Y, Saito M, Ishikawa F, Yonehara S. 2009. Interaction of FLASH with arsenite resistance protein 2 is involved in cell cycle progression at S phase. Mol. Cell. Biol. 29:4729-4741.
44. Gilmartin GM. 2005. Eukaryotic mRNA 3= processing: a common means to different ends. Genes Dev. 19:2517-2521.
45. Pillai RS, Will CL, Lührmann R, Schümperli D, Müller B. 2001. Purified U7 snRNPs lack the Sm proteins D1 and D2 but contain Lsm10, a new 14 kDa Sm D1-like protein. EMBO J. 20:5470-5479.
46. Smith HO, Tabiti K, Schaffner G, Soldati D, Albrecht U, Birnstiel ML. 1991. Two-step affinity purification of U7 small nuclear ribonucleoprotein particles using complementary biotinylated 2=-O-methyl oligoribonucleotides. Proc. Natl. Acad. Sci. U. S. A. 88:9784-9788.
47. Ruepp MD, Vivarelli S, Pillai RS, Kleinschmidt N, Azzouz TN, Barabino SM, Schumperli D. 2010. The 68 kDa subunit of mammalian cleavage factor I interacts with the U7 small nuclear ribonucleoprotein and participates in 3=-end processing of animal histone mRNAs. Nucleic Acids Res. 38:7637-7650.
48. Zhao J, Kessler M, Helmling S, O'Connor JP, Moore C. 1999. Pta1, a component of yeast CFII, is required for both cleavage and poly(A) addition of mRNA precursor. Mol. Cell. Biol. 19:7733-7740.
49. Keon BH, Schafer S, Kuhn C, Grund C, Franke WW. 1996. Symplekin, a novel type of tight junction plaque protein. J. Cell Biol. 134:1003-1018.
50. Bai Y, Auperin TC, Chou CY, Chang CG, Manley JL, Tong L. 2007. Crystal structure of murine CstF-77: dimeric association and implications for polyadenylation of mRNA precursors. Mol. Cell 25:863-875.
51. Martincic K, Campbell R, Edwalds-Gilbert G, Souan L, Lotze MT, Milcarek C. 1998. Increase in the 64-kDa subunit of the polyadenylation/ cleavage stimulatory factor during the G0 to S phase transition. Proc. Natl. Acad. Sci. U. S. A. 95:11095-11100.
52. Takagaki Y, Manley JL. 1998. Levels of polyadenylation factor CstF-64 control IgM heavy chainmRNAaccumulation and other events associated with B cell differentiation. Mol. Cell 2:761-771.
53. Dominski Z. 2010. The hunt for the 3= endonuclease. Wiley Interdiscip. Rev. RNA 1:325-340.
54. Dominski Z. 2007. Nucleases of the metallo-beta-lactamase family and their role in DNA and RNA metabolism. Crit. Rev. Biochem. Mol. Biol. 42:67-93.