Conserved and divergent features of the structure and function of La and La-related proteins (LARPs)

Mark A. Bayfield1, Ruiqing Yang2, Richard J. Maraia2,3
1Department of Biology, York University, Toronto, ON, Canada
2Intramural Research Program, NICHD, NIH, Bethesda, MD USA
3Commissioned Corps, U.S. Public Health Service, USA

Tài liệu tham khảo

Bousquet-Antonelli, 2009, A comprehensive analysis of the La-motif protein superfamily, RNA, 15, 750, 10.1261/rna.1478709 Mattioli, 1974, Heterogeneity of RNA protein antigens reactive with sera of patients with systemic lupus erythematosus. Description of a cytoplasmic nonribosomal antigen, Arthritis Rheum., 17, 421, 10.1002/art.1780170413 Reichlin, 1981, Current perspectives on serological reactions in SLE patients, Clin. Exp. Immunol., 44, 1 Casciola-Rosen, 1999, Cleavage by granzyme B is strongly predictive of autoantigen status: implications for initiation of autoimmunity, J. Exp. Med., 190, 815, 10.1084/jem.190.6.815 Romero, 2009, Cleavage of La protein by granzyme H induces cytoplasmic translocation and interferes with La-mediated HCV-IRES translational activity, Cell Death Differ., 16, 340, 10.1038/cdd.2008.165 Rosen, 2001, Clearing the way to mechanisms of autoimmunity, Nat. Med., 7, 664, 10.1038/89034 Terzoglou, 2006, Preferential recognition of the phosphorylated major linear B-cell epitope of La/SSB 349-368 aa by anti-La/SSB autoantibodies from patients with systemic autoimmune diseases, Clin. Exp. Immunol., 144, 432, 10.1111/j.1365-2249.2006.03088.x Park, 2006, The multifunctional RNA-binding protein La is required for mouse development and for the establishment of embryonic stem cells, Mol. Cell. Biol., 26, 1445, 10.1128/MCB.26.4.1445-1451.2006 Bai, 2000, Genetic analysis of a La homolog in Drosophila melanogaster, Nucleic Acids Res., 28, 1078, 10.1093/nar/28.5.1078 Arhin, 2005, Downregulation of the essential Trypanosoma brucei La protein affects accumulation of elongator methionyl-tRNA, Mol. Biochem. Parasitol., 144, 104, 10.1016/j.molbiopara.2005.06.006 Fleurdepine, 2007, A bona fide La protein is required for embryogenesis in Arabidopsis thaliana, Nucleic Acids Res., 35, 3306, 10.1093/nar/gkm200 Yoo, 1994, La proteins from Drosophila melanogaster and Saccharomyces cerevisiae: a yeast homolog of the La autoantigen is dispensable for growth, Mol. Cell. Biol., 14, 5412, 10.1128/MCB.14.8.5412 Van Horn, 1997, The La protein in Schizosaccharomyces pombe: a conserved yet dispensable phosphoprotein that functions in tRNA maturation, RNA, 3, 1434 Stefano, 1984, Purified lupus antigen La recognizes an oligouridylate stretch common to the 3′ termini of RNA polymerase III transcripts, Cell, 36, 145, 10.1016/0092-8674(84)90083-7 Mathews, 1984, La antigen recognizes and binds to the 3′-oligouridylate tail of a small RNA, Mol. Cell. Biol., 4, 1134, 10.1128/MCB.4.6.1134 Reddy, 1983, Identification of a La protein binding site in a RNA polymerase III transcript (4.5 I RNA), J. Biol. Chem., 258, 8352, 10.1016/S0021-9258(20)82072-9 Hendrick, 1981, Ro small cytoplasmic ribonucleoproteins are a subclass of La ribonucleoproteins: further characterization of the Ro and La small ribonucleoproteins from uninfected mammalian cells, Mol. Cell. Biol., 1, 1138, 10.1128/MCB.1.12.1138 Yoo, 1997, The yeast La protein is required for the 3′ endonucleolytic cleavage that matures tRNA precursors, Cell, 89, 393, 10.1016/S0092-8674(00)80220-2 Rinke, 1982, Precursor molecules of both human 5S ribosomal RNA and transfer RNAs are bound by a cellular protein reactive with anti-La lupus antibodies, Cell, 29, 149, 10.1016/0092-8674(82)90099-X Chambers, 1983, Association between the 7S RNA and the lupus La protein varies among cell types, J. Biol. Chem., 258, 11438, 10.1016/S0021-9258(17)44244-X He, 2008, A La-related protein modulates 7SK snRNP integrity to suppress P-TEFb-dependent transcriptional elongation and tumorigenesis, Mol. Cell, 29, 588, 10.1016/j.molcel.2008.01.003 Boire, 1990, Human Ro ribonucleoprotein particles: characterization of native structure and stable association with the La polypeptide, J. Clin. Invest., 85, 1182, 10.1172/JCI114551 Shen, 1982, The organization, structure, and in vitro transcription of Alu family RNA polymerase III transcription units in the human α-like globin gene cluster: precipitation of in vitro transcripts by lupus anti-La antibodies, J. Mol. Appl. Genet., 1, 343 Chang, 1996, Monomeric and dimeric Alu RNAs induced by adenovirus assemble into SRP9/14-containing RNPs in HeLa cells, Nucl. Acids Res., 24, 4165, 10.1093/nar/24.21.4165 Maraia, 1988, Pathway of B1-Alu expression in microinjected oocytes: Xenopus laevis proteins associated with nuclear precursor and processed cytoplasmic RNAs, Mol. Cell. Biol., 8, 4433, 10.1128/MCB.8.10.4433 Maraia, 1994, Eukaryotic transcription termination factor La mediates transcript release and facilitates reinitiation by RNA polymerase III, Mol. Cell. Biol., 14, 2147, 10.1128/MCB.14.3.2147 Rosa, 1981, Striking similarities are exhibited by two small Epstein–Barr virus-encoded ribonucleic acids and the adenovirus-associated ribonucleic acids VAI and VAII, Mol. Cell. Biol., 1, 785, 10.1128/MCB.1.9.785 Weinmann, 1976, Low molecular weight viral RNAs transcribed by RNA polymerase III during adenovirus 2 infection, Cell, 7, 557, 10.1016/0092-8674(76)90206-3 Lerner, 1981, Two small RNAs encoded by Epstein–Barr virus and complexed with protein are precipitated by antibodies from patients with systemic lupus erythematosus, Proc. Natl. Acad. Sci. U. S. A., 78, 805, 10.1073/pnas.78.2.805 Fairley, 2005, Human La is found at RNA polymerase III-transcribed genes in vivo, Proc. Natl. Acad. Sci. U. S. A., 102, 18350, 10.1073/pnas.0506415102 French, 2008, Visual analysis of the yeast 5S rRNA gene transcriptome: regulation and role of La protein, Mol. Cell. Biol., 28, 4576, 10.1128/MCB.00127-08 Wang, 1997, Identification of an autonomously initiating RNA polymerase III holoenzyme containing a novel factor that is selectively inactivated during protein synthesis inhibition, Genes Dev., 11, 2371, 10.1101/gad.11.18.2371 Xue, 2000, U snRNP assembly in yeast involves the La protein, EMBO J., 19, 1650, 10.1093/emboj/19.7.1650 Kufel, 2000, Precursors to the U3 small nucleolar RNA lack small nucleolar RNP proteins but are stabilized by La binding, Mol. Cell. Biol., 20, 5415, 10.1128/MCB.20.15.5415-5424.2000 Kufel, 2003, A complex pathway for 3′ processing of the yeast U3 snoRNA, Nucleic Acids Res., 31, 6788, 10.1093/nar/gkg904 Madore, 1984, Eukaryotic small ribonucleoproteins. Anti-La human autoantibodies react with U1 RNA–protein complexes, J. Biol. Chem., 259, 1929, 10.1016/S0021-9258(17)43496-X Chanfreau, 1997, Alternative 3′-end processing of U5 snRNA by RNase III, Genes Dev., 11, 2741, 10.1101/gad.11.20.2741 Seipelt, 1999, U1 snRNA is cleaved by RNase III and processed through an Sm site-dependent pathway, Nucleic Acids Res., 27, 587, 10.1093/nar/27.2.587 Allmang, 1999, Functions of the exosome in rRNA, snoRNA and snRNA synthesis, EMBO J., 18, 5399, 10.1093/emboj/18.19.5399 Meerovitch, 1993, La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate, J. Virol., 67, 3798, 10.1128/JVI.67.7.3798-3807.1993 Svitkin, 1994, La autoantigen alleviates translational repression by the 5′ leader sequence of the human immunodeficiency virus type 1 mRNA, J. Virol., 68, 7001, 10.1128/JVI.68.11.7001-7007.1994 Pellizzoni, 1996, A Xenopus laevis homologue of the La autoantigen binds the pyrimidine tract of the 5′ UTR of ribosomal protein mRNAs in vitro: implication of a protein factor in complex formation, J. Mol. Biol., 259, 904, 10.1006/jmbi.1996.0368 McLaren, 1997, Human La protein: a stabilizer of histone mRNA, Mol. Cell. Biol., 17, 3028, 10.1128/MCB.17.6.3028 Ali, 2000, Human La antigen is required for the hepatitis C virus internal ribosome entry site (IRES)-mediated translation, J. Biol. Chem., 275, 27531, 10.1074/jbc.M001487200 Kim, 2001, La autoantigen enhances translation of BiP mRNA, Nucleic Acids Res., 29, 5009, 10.1093/nar/29.24.5009 Pudi, 2003, Hepatitis C virus internal ribosome entry site-mediated translation is stimulated by specific interaction of independent regions of human La autoantigen, J. Biol. Chem., 278, 12231, 10.1074/jbc.M210287200 Pudi, 2004, La protein binding at the GCAC site near the initiator AUG facilitates the ribosomal assembly on the hepatitis C virus RNA to influence internal ribosome entry site-mediated translation, J. Biol. Chem., 279, 29879, 10.1074/jbc.M403417200 Costa-Mattioli, 2004, La autoantigen is necessary for optimal function of the poliovirus and hepatitis C virus internal ribosome entry site in vivo and in vitro, Mol. Cell. Biol., 24, 6861, 10.1128/MCB.24.15.6861-6870.2004 Heise, 2001, Characterization of nuclear RNases that cleave hepatitis B virus RNA near the La protein binding site, J. Virol., 75, 6874, 10.1128/JVI.75.15.6874-6883.2001 Trotta, 2003, BCR/ABL activates mdm2 mRNA translation via the La antigen, Cancer Cell, I3, 145, 10.1016/S1535-6108(03)00020-5 Schwartz, 2004, CK2 is responsible for phosphorylation of human La protein serine-366 and can modulate 5′TOP mRNA metabolism, Mol. Cell. Biol., 24, 9580, 10.1128/MCB.24.21.9580-9591.2004 Inada, 2004, Identification of Lhp1p-associated RNAs by microarray analysis in Saccharomyces cerevisiae reveals association with coding and noncoding RNAs, Proc. Natl. Acad. Sci. U. S. A., 101, 434, 10.1073/pnas.0307425100 Ni, 2004, Inhibition of human La protein by RNA interference downregulates hepatitis B virus mRNA in 2.2.15 cells, World J. Gastroenterol., 10, 2050, 10.3748/wjg.v10.i14.2050 Brenet, 2009, Akt phosphorylation of La regulates specific mRNA translation in glial progenitors, Oncogene, 28, 128, 10.1038/onc.2008.376 Bitko, 2008, Cellular La protein shields nonsegmented negative-strand RNA viral leader RNA from RIG-I and enhances virus growth by diverse mechanisms, J. Virol., 82, 7977, 10.1128/JVI.02762-07 Weng, 2009, Acheron, an novel LA antigen family member, binds to CASK and forms a complex with Id transcription factors, Cell Mol. Biol. Lett., 14, 273, 10.2478/s11658-008-0046-1 Bhattacharyya, 2006, An apical GAGA loop within 5′ UTR of the coxsackievirus B3 RNA maintains structural organization of the IRES element required for efficient ribosome entry, RNA Biol., 3, 60, 10.4161/rna.3.2.2990 Mondal, 2008, Structural determinant of human La protein critical for internal initiation of translation of hepatitis C virus RNA, J. Virol., 82, 11927, 10.1128/JVI.00924-08 Holcik, 2005, Translational control in stress and apoptosis, Nat. Rev. Mol. Cell Biol., 6, 318, 10.1038/nrm1618 Intine, 2003, Differential phosphorylation and subcellular localization of La RNPs associated with precursor tRNAs and translation-related mRNAs, Mol. Cell, 12, 1301, 10.1016/S1097-2765(03)00429-5 Cardinali, 2003, La protein is associated with terminal oligopyrimidine mRNAs in actively translating polysomes, J. Biol. Chem., 278, 35145, 10.1074/jbc.M300722200 Svitkin, 2009, General RNA-binding proteins have a function in poly(A)-binding protein-dependent translation, EMBO J., 28, 58, 10.1038/emboj.2008.259 Svitkin, 1996, General RNA binding proteins render translation cap dependent, EMBO J., 15, 7147, 10.1002/j.1460-2075.1996.tb01106.x Zhu, 2001, Binding of the La autoantigen to the 5′ untranslated region of a chimeric human translation elongation factor 1A reporter mRNA inhibits translation in vitro, Biochim. Biophys. Acta, 1521, 19, 10.1016/S0167-4781(01)00277-9 Bhattacharya, 2002, Methyl-phosphate cap structure in small RNAs reduces the affinity of RNAs to La protein, Gene Exp., 10, 243, 10.3727/000000002783992398 Alfano, 2004, Structural analysis of cooperative RNA binding by the La motif and central RRM domain of human La protein, Nat. Struct. Mol. Biol., 7–14, 7 Kenan, 2004, La gets its wings (news and views), Nat. Struct. Mol. Biol., 11, 303, 10.1038/nsmb0404-303 Dong, 2004, Structure of the La motif: a winged helix domain mediates RNA binding via a conserved aromatic patch, EMBO J., 23, 1000, 10.1038/sj.emboj.7600115 Clark, 1993, Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5, Nature, 364, 412, 10.1038/364412a0 Gajiwala, 2000, Winged helix proteins, Curr. Opin. Struct. Biol., 10, 110, 10.1016/S0959-440X(99)00057-3 Yoshizawa, 2005, Structural basis for mRNA recognition by elongation factor SelB, Nat. Struct. Mol. Biol., 12, 198, 10.1038/nsmb890 Maris, 2005, The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression, FEBS J., 272, 2118, 10.1111/j.1742-4658.2005.04653.x Goodier, 1997, A carboxy-terminal basic region controls RNA polymerase III transcription factor activity of human La protein, Mol. Cell. Biol., 17, 5823, 10.1128/MCB.17.10.5823 Horke, 2004, The La motif and the RNA recognition motifs of human La autoantigen contribute individually to RNA recognition and subcellular localization, J. Biol. Chem., 279, 50302, 10.1074/jbc.M407504200 Maraia, 2006, The La protein–RNA complex surfaces, Mol. Cell, 21, 149, 10.1016/j.molcel.2006.01.004 Teplova, 2006, Structural basis for recognition and sequestration of UUU(OH) 3′ temini of nascent RNA polymerase III transcripts by La, a rheumatic disease autoantigen, Mol. Cell, 21, 75, 10.1016/j.molcel.2005.10.027 Kotik-Kogan, 2008, Structural analysis reveals conformational plasticity in the recognition of RNA 3′ ends by the human La protein, Structure, 16, 852, 10.1016/j.str.2008.02.021 Huang, 2005, Mutations in the RNA polymerase III subunit Rpc11p that decrease RNA 3′ cleavage activity increase 3′-terminal oligo(U) length and La-dependent tRNA processing, Mol. Cell. Biol., 25, 621, 10.1128/MCB.25.2.621-636.2005 Hamada, 2000, Transcription termination by RNA polymerase III in fission yeast: a genetic and biochemical model system, J. Biol. Chem., 275, 29076, 10.1074/jbc.M003980200 Huang, 2006, Separate RNA-binding surfaces on the multifunctional La protein mediate distinguishable activities in tRNA maturation, Nat. Struct. Mol. Biol., 13, 611, 10.1038/nsmb1110 Copela, 2008, Competition between the Rex1 exonuclease and the La protein affects both Trf4p-mediated RNA quality control and pre-tRNA maturation, Rna, 14, 1214, 10.1261/rna.1050408 Hagenbuchle, 1979, The primary transcription product of a silkworm alanine tRNA gene: identification of in vitro sites of initiation, termination and processing, Cell, 18, 1217, 10.1016/0092-8674(79)90234-4 Schiffer, 2002, Assigning a function to a conserved group of proteins: the tRNA 3′-processing enzymes, EMBO J., 21, 2769, 10.1093/emboj/21.11.2769 Nashimoto, 2001, The inhibitory effect of the autoantigen La on in vitro 3′ processing of mammalian precursor tRNAs, J. Mol. Biol., 312, 975, 10.1006/jmbi.2001.5026 Dubrovsky, 2004, Drosophila RNase Z processes mitochondrial and nuclear pre-tRNA 3′ ends in vivo, Nucleic Acids Res., 32, 255, 10.1093/nar/gkh182 de la Sierra-Gallay, 2005, Structural basis for substrate binding, cleavage and allostery in the tRNA maturase RNase Z, Nature, 433, 657, 10.1038/nature03284 Bayfield, 2009, Precursor-product discrimination by La protein during tRNA metabolism, Nat. Struct. Mol. Biol., 16, 430, 10.1038/nsmb.1573 Kufel, 2003, 3′-processing of yeast tRNATrp precedes 5′-processing, RNA, 9, 202, 10.1261/rna.2145103 Intine, 2000, Transfer RNA maturation is controlled by phosphorylation of the human La antigen on serine 366, Mol. Cell, 6, 339, 10.1016/S1097-2765(00)00034-4 Ozanick, 2009, Rex1p deficiency leads to accumulation of precursor initiator tRNAMet and polyadenylation of substrate RNAs in Saccharomyces cerevisiae, Nucleic Acids Res., 37, 298, 10.1093/nar/gkn925 Zhao, 2009, Functional conservation of tRNase ZL among Saccharomyces cerevisiae, Schizosaccharomyces pombe and humans, Biochem. J., 422, 483, 10.1042/BJ20090743 Chakshusmathi, 2003, A La protein requirement for efficient pre-tRNA folding, EMBO J., 22, 6562, 10.1093/emboj/cdg625 Anderson, 1998, The essential Gcd10p–Gcd14p nuclear complex is required for 1-methyladenosine modification and maturation of initiator methionyl-tRNA, Genes Dev., 12, 3650, 10.1101/gad.12.23.3650 Anderson, 2009, Nuclear RNA surveillance: no sign of substrates tailing off, Crit. Rev. Biochem. Mol. Biol., 44, 16, 10.1080/10409230802640218 Copela, 2006, The La protein functions redundantly with tRNA modification enzymes to ensure tRNA structural stability, Rna, 12, 644, 10.1261/rna.2307206 Johansson, 2002, Dual function of the tRNA(m(5)U54)methyltransferase in tRNA maturation, RNA, 8, 324, 10.1017/S1355838202027851 Yu, 1996, Identification of SLF1 as a new copper homeostasis gene involved in copper sulfide mineralization in Saccharomyces cerevisiae, Mol. Cell. Biol., 16, 2464, 10.1128/MCB.16.5.2464 Tsukada, 1996, Isolation and characterization of SYS genes from yeast, multicopy suppressors of the functional loss of the transport GTPase Ypt6p, J. Cell Sci., 109, 2471, 10.1242/jcs.109.10.2471 Kagami, 1997, SRO9, a multicopy suppressor of the bud growth defect in the Saccharomyces cerevisiae rho3-deficient cells, shows strong genetic interactions with tropomyosin genes, suggesting its role in organization of the actin cytoskeleton, Genetics, 147, 1003, 10.1093/genetics/147.3.1003 Sobel, 1999, Two yeast La motif-containing proteins are RNA-binding proteins that associate with polyribosomes, Mol. Biol. Cell, 10, 3849, 10.1091/mbc.10.11.3849 Lan, 2004, A novel mode of chaperone action: heme activation of Hap1 by enhanced association of Hsp90 with the repressed Hsp70–Hap1 complex, J. Biol. Chem., 279, 27607, 10.1074/jbc.M402777200 Valavanis, 2007, Acheron, a novel member of the Lupus Antigen family, is induced during the programmed cell death of skeletal muscles in the moth Manduca sexta, Gene, 393, 101, 10.1016/j.gene.2007.01.033 Krueger, 2008, LARP7 is a stable component of the 7SK snRNP while P-TEFb, HEXIM1 and hnRNP A1 are reversibly associated, Nucleic Acids Res., 36, 2219, 10.1093/nar/gkn061 Markert, 2008, The La-related protein LARP7 is a component of the 7SK ribonucleoprotein and affects transcription of cellular and viral polymerase II genes, EMBO Rep., 9, 569, 10.1038/embor.2008.72 Nykamp, 2008, C. elegans La-related protein, LARP-1, localizes to germline P bodies and attenuates Ras-MAPK signaling during oogenesis, RNA, 14, 1378, 10.1261/rna.1066008 Jacks, 2003, Structure of the C-terminal domain of human La protein reveals a novel RNA recognition motif coupled to a helical nuclear retention element, Structure (Camb), 11, 833, 10.1016/S0969-2126(03)00121-7 Fok, 2006, Epstein–Barr virus noncoding RNAs are confined to the nucleus, whereas their partner, the human La protein, undergoes nucleocytoplasmic shuttling, J. Cell. Biol., 173, 319, 10.1083/jcb.200601026 Simons, 1996, Characterization of cis-acting signals for nuclear import and retention of the La (SS-B) autoantigen, Exp. Cell Res., 224, 224, 10.1006/excr.1996.0132 Rosenblum, 1998, Nuclear import and the evolution of a multifunctional RNA-binding protein, J. Cell Biol., 143, 887, 10.1083/jcb.143.4.887 Intine, 2002, Aberrant nuclear trafficking of La protein leads to disordered processing of associated precursor tRNAs, Mol. Cell, 9, 1113, 10.1016/S1097-2765(02)00533-6 Brenet, 2005, Mammalian peptidylglycine alpha-amidating monooxygenase mRNA expression can be modulated by the La autoantigen, Mol. Cell. Biol., 25, 7505, 10.1128/MCB.25.17.7505-7521.2005 Bayfield, 2007, Conservation of a masked nuclear export activity of La proteins and its effects on tRNA maturation, Mol. Cell. Biol., 27, 3303, 10.1128/MCB.00026-07 Maraia, 2002, La protein and its associated small nuclear and nucleolar precursor RNAs [review], Gene Exp., 10, 41 Fan, 1998, 5′ processing of tRNA precursors can be modulated by the human La antigen phosphoprotein, Mol. Cell. Biol., 18, 3201, 10.1128/MCB.18.6.3201 Intine, 2004, Nonphosphorylated human La antigen interacts with nucleolin at nucleolar sites involved in rRNA biogenesis, Mol. Cell. Biol., 24, 10894, 10.1128/MCB.24.24.10894-10904.2004 Park, 2007, Mouse and human La proteins differ in kinase substrate activity and activation mechanism for tRNA processing, Gene Exp., 14, 71, 10.3727/105221607783417619 Broekhuis, 2000, Detailed analysis of the phosphorylation of human La (SS-B) autoantigen. (De)phosphorylation does not affect subcellular distribution, Biochemistry, 39, 3023, 10.1021/bi992308c van Niekerk, 2007, Sumoylation in axons triggers retrograde transport of the RNA-binding protein La, Proc. Natl. Acad. Sci. U. S. A., 104, 12913, 10.1073/pnas.0611562104 Long, 2001, Phosphorylation of the Saccharomyces cerevisiae La protein does not appear to be required for its functions in tRNA maturation and nascent RNA stabilization, RNA, 7, 1589 Huber, 2009, Characterization of the rapamycin-sensitive phosphoproteome reveals that Sch9 is a central coordinator of protein synthesis, Genes Dev., 23, 1929, 10.1101/gad.532109 Oubridge, 1994, Crystal structure at 1.92 A resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin, Nature, 372, 432, 10.1038/372432a0 Dominguez, 2006, NMR structure of the three quasi RNA recognition motifs (qRRMs) of human hnRNP F and interaction studies with Bcl-x G-tract RNA: a novel mode of RNA recognition, Nucleic Acids Res., 34, 3634, 10.1093/nar/gkl488 Belisova, 2005, RNA chaperone activity of protein components of human Ro RNPs, RNA, 11, 1084, 10.1261/rna.7263905 O′Connor, 2006, A novel RNA binding domain in Tetrahymena telomerase p65 initiates hierarchical assembly of telomerase holoenzyme, Mol. Cell. Biol., 26, 2029, 10.1128/MCB.26.6.2029-2036.2006 Marz, 2009, Evolution of 7SK RNA and its protein partners in metazoa, Mol. Biol. Evol., 10.1093/molbev/msp198 Mori, 2002, Instabilotyping reveals unique mutational spectra in microsatellite-unstable gastric cancers, Cancer Res., 62, 3641 Jeronimo, 2007, Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme, Mol. Cell, 27, 262, 10.1016/j.molcel.2007.06.027 Peterlin, 2006, Controlling the elongation phase of transcription with P-TEFb, Mol. Cell, 23, 297, 10.1016/j.molcel.2006.06.014 Nguyen, 2001, 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes, Nature, 414, 322, 10.1038/35104581 Yang, 2001, The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription, Nature, 414, 317, 10.1038/35104575 Yik, 2003, Inhibition of P-TEFb (CDK9/Cyclin T) kinase and RNA polymerase II transcription by the coordinated actions of HEXIM1 and 7SK snRNA, Mol. Cell, 12, 971, 10.1016/S1097-2765(03)00388-5 Y. Xue, Z. Yang, R. Chen, Q. Zhou, A capping-independent function of MePCE in stabilizing 7SK snRNA and facilitating the assembly of 7SK snRNP, Nucleic Acids Res. (NAR) 38 (2) (2010) 360–369. Remillieux-Leschelle, 2002, Regulation of larval hematopoiesis in Drosophila melanogaster: a role for the multi sex combs gene, Genetics, 162, 1259, 10.1093/genetics/162.3.1259 Gruber, 2008, Arthropod 7SK RNA, Mol. Biol. Evol., 25, 1923, 10.1093/molbev/msn140 Barboric, 2009, 7SK snRNP/P-TEFb couples transcription elongation with alternative splicing and is essential for vertebrate development, Proc. Natl. Acad. Sci. U. S. A., 106, 7798, 10.1073/pnas.0903188106 Wassarman, 1991, Structural analyses of the 7SK ribonucleoprotein (RNP), the most abundant human small RNP of unknown function, Mol. Cell. Biol., 11, 3432, 10.1128/MCB.11.7.3432 Singh, 1990, Capping of mammalian U6 small nuclear RNA in vitro is directed by a conserved stem–loop and AUAUAC sequence: conversion of a noncapped RNA into a capped RNA, Mol. Cell. Biol., 10, 939, 10.1128/MCB.10.3.939 Shumyatsky, 1993, Methylphosphate cap structure increases the stability of 7SK, B2 and U6 small RNAs in Xenopus oocytes, Nucleic Acids Res., 21, 4756, 10.1093/nar/21.20.4756 Stone, 2007, Stepwise protein-mediated RNA folding directs assembly of telomerase ribonucleoprotein, Nature, 446, 458, 10.1038/nature05600 Aigner, 2003, The Euplotes La motif protein p43 has properties of a telomerase-specific subunit, Biochemistry, 42, 5736, 10.1021/bi034121y Aigner, 2004, The Euplotes telomerase subunit p43 stimulates enzymatic activity and processivity in vitro, RNA, 10, 1108, 10.1261/rna.7400704 Witkin, 2004, Holoenzyme proteins required for the physiological assembly and activity of telomerase, Genes Dev., 18, 1107, 10.1101/gad.1201704 Teixeira, 2007, La sets the tone for telomerase assembly, Nat. Struct. Mol. Biol., 14, 261, 10.1038/nsmb0407-261 Greider, 1989, A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis, Nature, 337, 331, 10.1038/337331a0 Shippen-Lentz, 1990, Functional evidence for an RNA template in telomerase, Science, 247, 546, 10.1126/science.1689074 Lingner, 1994, Telomerase RNAs of different ciliates have a common secondary structure and a permuted template, Genes Dev., 8, 1984, 10.1101/gad.8.16.1984 McCormick-Graham, 1995, Ciliate telomerase RNA structural features, Nucleic Acids Res., 23, 1091, 10.1093/nar/23.7.1091 Pannone, 1998, A role for the yeast La protein in U6 snRNP assembly: evidence that the La protein is a molecular chaperone for RNA polymerase III transcripts, EMBO J., 17, 7442, 10.1093/emboj/17.24.7442 Aigner, 2000, Euplotes telomerase contains an La motif protein produced by apparent translational frameshifting, EMBO J., 19, 6230, 10.1093/emboj/19.22.6230 Prathapam, 2005, A telomerase holoenzyme protein enhances telomerase RNA assembly with telomerase reverse transcriptase, Nat. Struct. Mol. Biol., 12, 252, 10.1038/nsmb900 Ohndorf, 2001, Contributions of the individual domains in human La protein to its RNA 3′-end binding activity, J. Biol. Chem., 276, 27188, 10.1074/jbc.M102891200 Wang, 2009, Regulation of muscle differentiation and survival by Acheron, Mech. Dev., 126, 700, 10.1016/j.mod.2009.05.003 Cai, 2009, Binding of LARP6 to the conserved 5′ stem–loop regulates translation of mRNAs encoding type I collagen, J. Mol. Biol. Chauvet, 2000, dlarp, a new candidate Hox target in Drosophila whose orthologue in mouse is expressed at sites of epithelium/mesenchymal interactions, Dev. Dyn., 218, 401, 10.1002/1097-0177(200007)218:3<401::AID-DVDY1009>3.0.CO;2-6 Ichihara, 2007, A Drosophila orthologue of larp protein family is required for multiple processes in male meiosis, Cell Struct. Funct., 32, 89, 10.1247/csf.07027 Blagden, 2009, Drosophila Larp associates with poly(A)-binding protein and is required for male fertility and syncytial embryo development, Dev. Biol., 334, 186, 10.1016/j.ydbio.2009.07.016 Tan, 2000, Multiple mechanisms of suppression circumvent transcription defects in an RNA polymerase mutant, Mol. Cell. Biol., 20, 8124, 10.1128/MCB.20.21.8124-8133.2000 Albrecht, 2004, Survey on the PABC recognition motif PAM2, Biochem. Biophys. Res. Commun., 316, 129, 10.1016/j.bbrc.2004.02.024 Fan, 1997, Phosphorylation of the human La antigen on serine 366 can regulate recycling of RNA polymerase III transcription complexes, Cell, 88, 707, 10.1016/S0092-8674(00)81913-3 Karlas, 2010, Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication, Naturel, 463, 818, 10.1038/nature08760