Mouse and human la proteins differ in kinase substrate activity and activation mechanism for tRNA processing

Gene Expression

Volumn 14, Issue 2, 2007, Pages 71-81

  Park, Jung Min ^a,b   Intine, Robert V ^a,c   Maraia, Richard J ^a  

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

^b Korea Intellectual Property Office   (South Korea)

^c ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

ade6 704; C5 RNA; CK2; La motif; Mdm2; Protein kinase A; tRNA processing; tRNA mediated suppression

Indexed keywords

CASEIN KINASE II; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; LA ANTIGEN; PROTEIN MDM2; SERINE; TRANSFER RNA;

ANALYTIC METHOD; ARTICLE; COMPARATIVE STUDY; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; RNA BINDING; SACCHAROMYCES POMBE; STOP CODON; YEAST;

AMINO ACID SEQUENCE; ANIMALS; AUTOANTIGENS; BASE SEQUENCE; ENZYME ACTIVATION; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-MDM2; RIBONUCLEOPROTEINS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, TRANSFER; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY;

MAMMALIA; MUS; SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 38949132566     PISSN: 10522166     EISSN: None     Source Type: Journal    
DOI: 10.3727/105221607783417619     Document Type: Article

References (57)

1. Alfano, C.; Sanfelice, D.; Babon, J.; Kelly, G.; Jacks, A.; Curry, S.; Conte, M. R. Structural analysis of cooperative RNA binding by the La motif and central RRM domain of human La protein. Nat. Struct. Mol. Biol. 11:323-329; 2004.
2. Ali, N.; Pruijn, G. J.; Kenan, D. J.; Keene, J. D.; Siddiqui, A. Human La antigen is required for the hepatitis C virus internal ribosome entry site (IRES)-mediated translation. J. Biol. Chem. 275:27531-2740; 2000.
3. Bayfield, M. A.; Kaiser, T. E.; Intine, R. V.; Maraia, R. J. Conservation of a masked nuclear export activity of La proteins and its effects on tRNA maturation. Mol. Cell. Biol. 27:3303-3312; 2007.
4. Broekhuis, C. H.; Neubauer, G.; van der Heijden, A.; Mann, M.; Proud, C. G.; van Venrooij, W. J.; Pruijn, G. J. Detailed analysis of the phosphorylation of human La (SS-B) autoantigen. (De)phosphorylation does not affect subcellular distribution. Biochemistry 39: 3023-3033; 2000.
5. Butt, E.; Immler, D.; Meyer, H. E.; Kotlyarov, A.; Laass, K.; Gaestel, M. Heat shock protein 27 is a substrate of cGMP-dependent protein kinase in intact human platelets: Phosphorylation-induced actin polymerization caused by HSP27 mutants. J. Biol. Chem. 276: 7108-7113; 2001.
6. Chambers, J. C.; Keene, J. D. Isolation and analysis of cDNA clones expressing human lupus La antigen. Proc. Natl. Acad. Sci. USA 82:2115-2119; 1985.
7. Costa-Mattioli, M.; Svitkin, Y.; Sonenberg, N. 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; 2004.
8. Fairley, J. A.; Kantidakis, T.; Kenneth, N. S.; Intine, R. V.; Maraia, R. J.; White, R. J. Human La is found at RNA polymerase III-transcribed genes in vivo. Proc. Natl. Acad. Sci. USA 102:18350-18355; 2005.
9. Fan, H.; Goodier, J. L.; Chamberlain, J.; Engelke, D. R.; Maraia, R. J. 5′ Processing of tRNA precursors can be modulated by the human La antigen phosphoprotein. Mol. Cell. Biol. 18:3201-3211; 1998.
10. Fan, H.; Sakulich, A. L.; Goodier, J. L.; Zhang, X.; Qin, J.; Maraia, R. J. Phosphorylation of the human La antigen on serine 366 can regulate recycling of RNA polymerase III transcription complexes. Cell 88:707-715; 1997.
11. Fouraux, M. A.; Kolkman, M. J.; Van der Heijden, A.; De Jong, A. S.; Van Venrooij, W. J.; Pruijn, G. J. The human La (SS-B) autoantigen interacts with DDX15/ hPrp43, a putative DEAH-box RNA helicase. RNA 8: 1428-1443; 2002.
12. Glover, 3rd, C. V. On the physiological role of casein kinase II in Saccharomyces cerevisiae. Prog. Nucleic Acid Res. Mol. Biol. 59:95-133; 1998.
13. Goodier, J. L.; Fan, H.; Maraia, R. J. A carboxy-terminal basic region controls RNA polymerase III transcription factor activity of human La protein. Mol. Cell. Biol. 17:5823-5832; 1997.
14. Goodier, J. L.; Maraia, R. J. Terminator-specific recycling of a B1-Alu transcription complex by RNA polymerase III is mediated by the RNA terminus-binding protein La. J. Biol. Chem. 273:26110-26116; 1998.
15. Hamada, M.; Sakulich, A. L.; Koduru, S. B.; Maraia, R. Transcription termination by RNA polymerase III in fission yeast: A genetic and biochemical model system. J. Biol. Chem. 275:29076-29081; 2000.
16. Harada, F.; Matsubara, M.; Kato, N. Stable tRNA precursors in HeLa cells. Nucleic Acids Res. 12:9263-9269; 1984.
17. Hendrick, J. P.; Wolin, S. L.; Rinke, J.; Lerner, M. R.; Steitz, J. A. 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: 1138-1149; 1981.
18. Holcik, M.; Korneluk, R. G. Functional characterization of the X-linked inhibitor of apoptosis (XIAP) internal ribosome entry site element: Role of La autoantigen in XIAP translation. Mol. Cell. Biol. 20: 4648-4657; 2000.
19. Holcik, M.; Sonenberg, N. Translational control in stress and apoptosis. Nat. Rev. Mol. Cell. Biol. 6:318-327; 2005.
20. Huang, Y.; Bayfield, M. A.; Intine, R. V.; Maraia, R. J. Separate RNA-binding surfaces on the multifunctional La protein mediate distinguishable activities in tRNA maturation. Nat. Struct. Mol. Biol. 13:611-618; 2006.
21. Huang, Y.; Intine, R. V.; Mozlin, A.; Hasson, S.; Maraia, R. J. 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. 25:621-636; 2005.
22. Hulo, N.; Bairoch, A.; Bulliard, V.; Cerutti, L.; De Castro, E.; Langendijk-Genevaux, P. S.; Pagni, M.; Sigrist, C. J. The PROSITE database. Nucleic Acids Res. 34:D227-D230; 2006.
23. Inada, M.; Guthrie, C. Identification of Lhp1p-associated RNAs by microarray analysis in Saccharomyces cerevisiae reveals association with coding and noncoding RNAs. Proc. Natl. Acad. Sci. USA 101:434-439; 2004.
24. Intine, R. V.; Dundr, M.; Misteli, T.; Maraia, R. J. Aberrant nuclear trafficking of La protein leads to disordered processing of associated precursor tRNAs. Mol. Cell 9:1113-1123; 2002.
25. Intine, R. V.; Dundr, M.; Vassilev, A.; Schwartz, E.; Zhao, Y.; Depamphilis, M. L.; Maraia, R. J. Nonphosphorylated human La antigen interacts with nucleolin at nucleolar sites involved in rRNA biogenesis. Mol. Cell. Biol. 24:10894-10904; 2004.
26. Intine, R. V.; Tenenbaum, S. A.; Sakulich, A. S.; Keene, J. D.; Maraia, R. J. Differential phosphorylation and subcellular localization of La RNPs associated with precursor tRNAs and translation-related mRNAs. Mol. Cell 12:1301-1307; 2003.
27. Intine, R. V.; Sakulich, A. L.; Koduru, S. B.; Huang, Y.; Pierstorrf, E.; Goodier, J. L.; Phan, L.; Maraia, R. J. Transfer RNA maturation is controlled by phosphorylation of the human La antigen on serine 366. Mol. Cell 6:339-348; 2000.
28. Jacks, A.; Babon, J.; Kelly, G.; Manolaridis, I.; Cary, P. D.; Curry, S.; Conte, M. R. Structure of the C-terminal domain of human La protein reveals a novel RNA recognition motif coupled to a helical nuclear retention element. Structure 11:833-843; 2003.
29. Kenan, D. J. RNA recognition by the human La protein and its relevance to transcription, translation and viral infectivity. Ph.D. thesis, Duke University; 1995.
30. Kenan, D. J.; Keene, J. D. La gets its wings. Nat. Struct. Mol. Biol. 11:303-305; 2004.
31. Kohli, J.; Kwong, T.; Altruda, F.; Soll, D.; Wahl, G. Characterization of a UGA-suppressing serine tRNA from Schizosaccharomyces pombe with the help of a new in vitro assay system for eukaryotic suppressor tRNAs. J. Biol. Chem. 254:1546-1551; 1979.
32. Lerner, M. R.; Boyle, J. A.; Hardin, J. A.; Steitz, J. A. Two novel classes of small ribonucleoproteins detected by antibodies associated with lupus erythematosus. Science 211:400-402; 1981.
33. Long, K. S.; Cedervall, T.; Walch-Solimena, C.; Noe, D. A.; Huddleston, M. J.; Annan, R. S.; Wolin, S. L. Phosphorylation of the Saccharomyces cerevisiae La protein does not appear to be required for its functions in tRNA maturation and nascent RNA stabilization. RNA 7:1589-1602; 2001.
34. Maraia, R. The human La antigen [SS/B]. In: Creighton, T. E., ed. Wiley encyclopedia of molecular medicine, vol. 5. New York: John Wiley & Sons; 2002:1883-1886.
35. Maraia, R. J.; Bayfield, M. A. The La protein-RNA complex surfaces. Mol. Cell 21:149-152; 2006.
36. Maraia, R. J.; Intine, R. V. La protein and its associated small nuclear and nucleolar precursor RNAs. Gene Expr. 10:41-57; 2002.
37. Maraia, R. J.; Intine, R. V. Recognition of nascent RNA by the human La antigen: Conserved and diverged features of structure and function. Mol. Cell. Biol. 21:367-379; 2001.
38. Maraia, R. J.; Kenan, D. J.; Keene, J. D. Eukaryotic transcription termination factor La mediates transcript release and facilitates reinitiation by RNA polymerase III. Mol. Cell. Biol. 14:2147-2158; 1984.
39. Meggio, F.; Pinna, L. A. One-thousand-and-one substrates of protein kinase CK2? FASEB J. 17:349-368; 2003.
40. Ohndorf, U. M.; Steegborn, C.; Knijff, R.; Sondermann, P. Contributions of the individual domains in human La protein to its RNA 3′-end binding activity. J. Biol. Chem. 276:27188-27196; 2001.
41. Park, J. M.; Kohn, M. J.; Bruinsma, M.; Vech, C.; Intine, R. V.; Fuhrmann, S.; Grinberg, A.; Mukherjee, I.; Love, P.; Ko, M. s.; DePamphilis, M. L.; Maraia, R. J. The multifunctional RNA-binding protein La is required for mouse development and for the establishment of embryonic stem cells. Mol. Cell. Biol. 26: 1445-1451; 2006.
42. Pearson, R. B.; Kemp, B. E. Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol. 200:62-81; 1991.
43. PROSITE. Database of protein domains, families and functional sites. http://ca.expasy.org/prosite/; 2006.
44. Pudi, R.; Ramamurthy, S. S.; Das, S. A peptide derived from RNA recognition motif 2 of human la protein binds to hepatitis C virus internal ribosome entry site, prevents ribosomal assembly, and inhibits internal initiation of translation. J. Virol. 79:9842-9853; 2005.
45. Rafalski, A.; Kohli, J.; Agris, P.; Soll, D. The nucleotide sequence of a UGA suppressor serine tRNA from Schizosaccharomyces pombe. Nucleic Acids Res. 6: 2683-2695; 1979.
46. Rinke, J.; Steitz, J. A. Association of the lupus antigen La with a subset of U6 snRNA molecules. Nucleic Acids Res. 13:2617-2629; 1985.
47. Rinke, J.; Steitz, J. A. Precursor molecules of both human 5S ribosomal RNA and transfer RNAs are bound by a cellular protein reactive with anti-La lupus antibodies. Cell 29:149-159; 1982.
48. Schar, P.; Kohli, J. Marker effects of G to C trans versions on intragenic recombination and mismatch repair in Schizosaccharomyces pombe. Genetics 133:825-835; 1993.
49. Schwartz, E.; Intine, R. V.; Maraia, R. J. CK2 is responsible for phosphorylation of human La protein serine-366 and can modulate 5′TOP mRNA metabolism. Mol. Cell. Biol. 24:9580-9591; 2004.
50. Stefano, J. E. Purified lupus antigen La recognizes an oligouridylate stretch common to the 3′ termini of RNA polymerase III transcripts. Cell 36:145-154; 1984.
51. Svitkin, Y. V.; Meerovitch, K.; Lee, H. S.; Dholakia, J. N.; Kenan, D. J.; Agol, V. I.; Sonenberg, N. Internal translation initiation on poliovirus RNA: further characterization of La function in poliovirus translation in vitro. J. Virol. 68:1544-1550; 1994.
52. Teplova, M.; Yuan, Y.-R.; Hin, S.; Malinina, L.; Phan, A. T.; Teplov, A.; Patel, D. J. Structural basis for recognition and sequestration of UUU-OH 3′-termini of nascent RNA pol III transcripts by La, a rheumatic disease autoantigen. Mol. Cell 21:75-85; 2006.
53. Topfer, F.; Gordon, T.; McCluskey, J. Characterization of the mouse autoantigen La (SS-B). J. Immunol. 150: 3091-3100; 1993.
54. Trotta, R.; Vignudelli, T.; Pecorari, L.; Intine, R. V.; Guerzoni, C.; Santilli, G.; Candini, O.; Byrom, M. W.; Goldoni, S.; Ford, L. P.; Caligiuri, M. A.; Maraia, R.; Perrotti, D.; Calabretta, B. BCR/ABL activates mdm2 mRNA translation via the La antigen. Cancer Cell 13: 145-160; 2003.
55. Van Horn, D. J.; Yoo, C. J.; Xue, D.; Shi, H.; Wolin, S. L. The La protein in Schizosaccharomyces pombe: a conserved yet dispensable phosphoprotein that functions in tRNA maturation. RNA 3:1434-1443; 1997.
56. Wolin, S. L.; Cedervall, T. The La protein. Annu. Rev. Biochem. 71:375-403; 2002.
57. Yoo, C. J.; Wolin, S. L. The yeast La protein is required for the 3′ endonucleolytic cleavage that matures tRNA precursors. Cell 89:393-402; 1997.