Conservation of RNA chaperone activity of the human La-related proteins 4, 6 and 7

Nucleic Acids Research

Volumn 41, Issue 18, 2013, Pages 8715-8725

  Hussain, Rawaa H ^a   Zawawi, Mariam ^a   Bayfield, Mark A ^a  

^a YORK UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; LA RELATED PROTEIN 4; LA RELATED PROTEIN 6; LA RELATED PROTEIN 7; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN RNA BINDING;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AUTOANTIGENS; HUMANS; MOLECULAR SEQUENCE DATA; RIBONUCLEOPROTEINS; RNA PRECURSORS; RNA, TRANSFER; SCHIZOSACCHAROMYCES; SEQUENCE ALIGNMENT;

EID: 84885896091     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt649     Document Type: Article

References (49)

1. Bousquet-Antonelli, C. and Deragon, J. (2009) A comprehensive analysis of the La-motif protein superfamily. RNA, 15, 750-764.
2. Bayfield, M.A., Yang, R. and Maraia, R.J. (2010) Conserved and divergent features of the structure and function of La and Larelated proteins (LARPs). Biochim. Biophys. Acta, 1799, 365-378.
3. Dong, G., Chakshusmathi, G., Wolin, S.L. and Reinisch, K.M. (2004) Structure of the La motif: A winged helix domain mediates RNA binding via a conserved aromatic patch. EMBO J., 23, 1000-1007.
4. Alfano, C., Sanfelice, D., Babon, J., Kelly, G., Jacks, A., Curry, S. and Conte, M.R. (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, 7-12.
5. Wolin, S.L. and Cedervall, T. (2002) The La protein. Annu. Rev. Biochem., 71, 375-403.
6. Meerovitch K. Svitkin Y.V. Lee H.S. Lejbkowicz F. Kenan D.J. Chan ,E.K. Agol V.I. Keene J.D. and Sonenberg N. (1993) La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. J. Virol.,67 3798-3807.
7. Costa-Mattioli M.Svitkin Y. and SonenbergN. (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 6861-6870.
8. Trotta, R., Vignudelli, T., Pecorari, L., Intine, R.V., Guerzoni, C., Santilli, G., Candini, O., Byrom, M.W., Goldoni, S., Ford, L.P. et al. (2003) BCR/ABL activates mdm2 mRNA translation via the La antigen. Cancer Cell, I3, 145-160.
9. Intine, R.V., Tenenbaum, S.A., Sakulich, A.S., Keene, J.D. and Maraia, R.J. (2003) Differential phosphorylation and subcellular localization of La RNPs associated with precursor tRNAs and translation-related mRNAs. Mol. Cell, 12, 1301-1307.
10. Sommer, G., Dittmann, J., Kuehnert, J., Reumann, K., Schwartz, P.E., Will, H., Coulter, B.L., Smith, M.T. and Heise, T. (2011) The RNA-binding protein La contributes to cell proliferation and CCND1 expression. Oncogene, 30, 434-444.
11. Schwartz, E., Intine, R.V. and Maraia, R.J. (2004) CK2 is responsible for phosphorylation of human La protein serine-366 and can modulate 50TOP mRNA metabolism. Mol. Cell. Biol., 24, 9580-9591.
12. Ali, N., Pruijn, G.J., Kenan, D.J., Keene, J.D. and Siddiqui, A. (2000) Human La antigen is required for the hepatitis C virus internal ribosome entry site (IRES)-mediated translation. J. Biol. Chem., 275, 27531-27540.
13. Pudi, R., Srinivasan, P. and Das, S. (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, 29879-29888.
14. Bayfield, M.A. and Maraia, R.J. (2009) Precursor-product discrimination by La protein during tRNA metabolism. Nat Struct. Mol. Biol., 16, 430-437.
15. Teplova, M., Yuan, Y.R., Phan, A.T., Malinina, L., Ilin, S., Teplov, A. and Patel, D.J. (2006) Structural basis for recognition and sequestration of UUU(OH) 30 temini of nascent RNA polymerase III transcripts by La, a rheumatic disease autoantigen. Mol. Cell, 21, 75-85.
16. Kucera, N.J., Hodsdon, M.E. and Wolin, S.L. (2011) An intrinsically disordered C terminus allows the La protein to assist the biogenesis of diverse noncoding RNA precursors. Proc. Natl Acad. Sci. USA, 108, 1308-1313.
17. Kotik-Kogan, O., Valentine, E.R., Sanfelice, D., Conte, M.R. and Curry, S. (2008) Structural analysis reveals conformational plasticity in the recognition of RNA 30 ends by the human La protein. Structure, 16, 852-862.
18. Maraia, R.J. and Bayfield, M.A. (2006) The La protein-RNA complex surfaces. Mol. Cell, 21, 149-152.
19. Naeeni, A.R., Conte, M.R. and Bayfield, M.A. (2012) RNA chaperone activity of the human La protein is mediated by a variant RNA recognition motif. J. Biol. Chem., 287, 5472-5482.
20. Van Horn, D.J., Yoo, C.J., Xue, D., Shi, H. and Wolin, S.L. (1997) The La protein in Schizosaccharomyces pombe: A conserved yet dispensable phosphoprotein that functions in tRNA maturation. RNA, 3, 1434-1443.
21. Intine, R.V.A., Sakulich, A.L., Koduru, S.B., Huang, Y., Pierstorrf, E., Goodier, J.L., Phan, L. and Maraia, R.J. (2000) Transfer RNA maturation is controlled by phosphorylation of the human La antigen on serine Mol. Cell, 6, 339-348.
22. Maraia, R.J. and Lamichhane, T.N. (2011) 30 processing of eukaryotic precursor tRNAs. Wiley Interdiscip. Rev. RNA, 2, 362-375.
23. Chakshusmathi, G., Kim, S.D., Rubinson, D.A. and Wolin, S.L. (2003) A La protein requirement for efficient pre-tRNA folding. EMBO J., 22, 6562-6572.
24. Copela, L.A., Chakshusmathi, G., Sherrer, R.L. and Wolin, S.L. (2006) The La protein functions redundantly with tRNA modification enzymes to ensure tRNA structural stability. RNA, 12, 644-654.
25. Huang, Y., Bayfield, M.A., Intine, R.V. and Maraia, R.J. (2006) Separate RNA-binding surfaces on the multifunctional La protein mediate distinguishable activities in tRNA maturation. Nat. Struct. Mol. Biol., 13, 611-618.
26. Belisova, A., Semrad, K., Mayer, O., Kocian, G., Waigmann, E., Schroeder, R. and Steiner, G. (2005) RNA chaperone activity of protein components of human Ro RNPs. RNA, 11, 1084-1094.
27. Liu, Y., Tan, H., Tian, H., Liang, C., Chen, S. and Liu, Q. (2011) Autoantigen La promotes efficient RNAi, antiviral response, and transposon silencing by facilitating multiple-turnover RISC catalysis. Mol. Cell, 44, 502-508.
28. He, N., Jahchan, N.S., Hong, E., Li, Q., Bayfield, M.A., Maraia, R.J., Luo, K. and Zhou, Q. (2008) A La-related protein modulates 7SK snRNP integrity to suppress P-TEFb-dependent transcriptional elongation and tumorigenesis. Mol. Cell, 29, 588-599.
29. Krueger, B.J., Jeronimo, C., Roy, B.B., Bouchard, A., Barrandon, C., Byers, S.A., Searcey, C.E., Cooper, J.J., Bensaude, O., Cohen, E.A. et al. (2008) LARP7 is a stable component of the 7SK snRNP while P-TEFb, HEXIM1 and hnRNP A1 are reversibly associated. Nucleic Acids Res., 36, 2219-2229.
30. Markert, A., Grimm, M., Martinez, J., Wiesner, J., Meyerhans, A., Meyuhas, O., Sickmann, A. and Fischer, U. (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, 569-575.
31. Remillieux-Leschelle, N., Santamaria, P. and Randsholt, N.B. (2002) Regulation of larval hematopoiesis in Drosophila melanogaster: A role for the multi sex combs gene. Genetics, 162, 1259-1274.
32. Mori, Y., Sato, F., Selaru, F.M., Olaru, A., Perry, K., Kimos, M.C., Tamura, G., Matsubara, N., Wang, S., Xu, Y. et al. (2002) Instabilotyping reveals unique mutational spectra in microsatelliteunstable gastric cancers. Cancer Res., 62, 3641-3645.
33. Merret, R., Martino, L., Bousquet-Antonelli, C., Fneich, S., Descombin, J., Billey, E., Conte, M.R. and Deragon, J.M. (2013) The association of a La module with the PABP-interacting motif PAM2 is a recurrent evolutionary process that led to the neofunctionalization of La-related proteins. RNA, 19, 36-50.
34. Cai, L., Fritz, D., Stefanovic, L. and Stefanovic, B. (2010) Binding of LARP6 to the conserved 50 stem-loop regulates translation of mRNAs encoding type I collagen. J. Mol. Biol., 395, 309-326.
35. Schaffler, K., Schulz, K., Hirmer, A., Wiesner, J., Grimm, M., Sickmann, A. and Fischer, U. (2010) A stimulatory role for the Larelated protein 4B in translation. RNA, 16, 1488-1499.
36. Yang, R., Gaidamakov, S.A., Xie, J., Lee, J., Martino, L., Kozlov, G., Crawford, A.K., Russo, A.N., Conte, M.R., Gehring, K. et al. (2010) LARP4 binds poly(A), interacts with poly(A)-binding protein MLLE domain via a variant PAM2w motif and can promote mRNA stability. Mol. Cell. Biol., 31, 542-556.
37. Chambers, J.C., Kurilla, M.G. and Keene, J.D. (1983) Association between the 7 S RNA and the lupus La protein varies among cell types. J. Biol. Chem., 258, 11438-11441.
38. Yoo, C.J. and Wolin, S.L. (1997) The yeast La protein is required for the 30 endonucleolytic cleavage that matures tRNA precursors. Cell, 89, 393-402.
39. Park, J.M., Intine, R.V. and Maraia, R.J. (2007) Mouse and human La proteins differ in kinase substrate activity and activation mechanism for tRNA processing. Gene Expr., 14, 71-81.
40. Katzman, S., Barrett, C., Thiltgen, G., Karchin, R. and Karplus, K. (2008) PREDICT-2ND: A tool for generalized protein local structure prediction. Bioinformatics, 24, 2453-2459.
41. Rajkowitsch, L., Chen, D., Stampfl, S., Semrad, K., Waldsich, C., Mayer, O., Jantsch, M.F., Konrat, R., Blasi, U. and Schroeder, R. (2007) RNA chaperones, RNA annealers and RNA helicases. RNA Biol., 4, 118-130.
42. Rajkowitsch, L. and Schroeder, R. (2007) Dissecting RNA chaperone activity. RNA, 13, 2053-2060.
43. Gottlieb, E. and Steitz, J.A. (1989) The RNA binding protein La influences both the accuracy and the efficiency of RNA polymerase III transcription in vitro. EMBO J., 8, 841-850.
44. Inada, M. and Guthrie, C. (2004) Identification of Lhp1passociated RNAs by microarray analysis in Saccharomyces cerevisiae reveals association with coding and noncoding RNAs. Proc. Natl Acad. Sci. USA, 101, 434-439.
45. Karlas, A., Machuy, N., Shin, Y., Pleissner, K.P., Artarini, A., Heuer, D., Becker, D., Khalil, H., Ogilvie, L.A., Hess, S. et al. (2010) Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature, 463, 818-822.
46. Burrows, C., Abd Latip, N., Lam, S.J., Carpenter, L., Sawicka, K., Tzolovsky, G., Gabra, H., Bushell, M., Glover, D.M., Willis, A.E. et al. (2010) The RNA binding protein Larp1 regulates cell division, apoptosis and cell migration. Nucleic Acids Res., 38, 5542-5553.
47. Martino, L., Pennell, S., Kelly, G., Bui, T.T., Kotik-Kogan, O., Smerdon, S.J., Drake, A.F., Curry, S. and Conte, M.R. (2012) Analysis of the interaction with the hepatitis C virus mRNA reveals an alternative mode of RNA recognition by the human La protein. Nucleic Acids Res., 40, 1381-1394.
48. Liang, C., Xiong, K., Szulwach, K.E., Zhang, Y., Wang, Z., Peng, J., Fu, M., Jin, P., Suzuki, H.I. and Liu, Q. (2013) Sjogren syndrome antigen B (SSB)/La promotes global microRNA expression by binding microRNA precursors through stem-loop recognition. J. Biol. Chem., 288, 723-736.
49. Stone, M.D., Mihalusova, M., O?Connor, C.M., Prathapam, R., Collins, K. and Zhuang, X. (2007) Stepwise protein-mediated RNA folding directs assembly of telomerase ribonucleoprotein. Nature, 446, 458-461.