An intact unfolded protein response in Trpt1 knockout mice reveals phylogenic divergence in pathways for RNA ligation

RNA

Volumn 14, Issue 2, 2008, Pages 225-232

  Harding, Heather P ^a   Lackey, Jeremy G ^b   Hsu, Hao Chi ^a   Zhang, Yuhong ^a   Deng, Jing ^a,c   Xu, Rui Ming ^a   Damha, Masad J ^b   Ron, David ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

Mouse genetics; Protein folding; RNA ligase, 2 phosphotransferase; Translation; tRNA splicing

Indexed keywords

PHOSPHOTRANSFERASE; RNA LIGASE; TRANSFER RNA; TYROSINE; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE; GENE FUNCTION; GENE INACTIVATION; GENETIC VARIABILITY; MOUSE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FOLDING; RNA SPLICING; RNA TRANSLATION; TRPT1 GENE;

ANIMALS; DNA-BINDING PROTEINS; EXORIBONUCLEASES; MICE; MICE, KNOCKOUT; NUCLEAR PROTEINS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PHYLOGENY; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; RNA SPLICE SITES; RNA SPLICING; RNA, MESSENGER; RNA, TRANSFER, TYR; TYROSINE; VARIATION (GENETICS);

ANIMALIA; EUKARYOTA; MAMMALIA; MUS;

EID: 38649087626     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.859908     Document Type: Article

References (42)

1. Abelson, J., Trotta, C.R., and Li, H. 1998. tRNA splicing. J. Biol. Chem. 273: 12685-12688.
2. Calfon, M., Zeng, H., Urano, F., Till, J.H., Hubbard, S.R., Harding, H.P., Clark, S.G., and Ron, D. 2002. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415: 92-96.
3. Cox, J.S. and Walter, P. 1996. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87: 391-404.
4. Culver, G.M., McCraith, S.M., Zillmann, M., Kierzek, R., Michaud, N., LaReau, R.D., Turner, D.H., and Phizicky, E.M. 1993. An NAD derivative produced during transfer RNA splicing: ADP-ribose 1″-2″ cyclic phosphate. Science 261: 206-208.
5. Culver, G.M., McCraith, S.M., Consaul, S.A., Stanford, D.R., and Phizicky, E.M. 1997. A 2′-phosphotransferase implicated in tRNA splicing is essential in Saccharomyces cerevisiae. J. Biol. Chem. 272: 13203-13210.
6. Damha, M.J. and Ogilvie, K.K. 1993. Oligoribonucleotide synthesis. The silyl-phosphoramidite method. Methods Mol. Biol. 20: 81-114.
7. Echols, N., Harrison, P., Balasubramanian, S., Luscombe, N.M., Bertone, P., Zhang, Z., and Gerstein, M. 2002. Comprehensive analysis of amino acid and nucleotide composition in eukaryotic genomes, comparing genes and pseudogenes. Nucleic Acids Res. 30: 2515-2523. doi: 10.1093/nar/30.11.2515.
8. Filipowicz, W. and Shatkin, A.J. 1983. Origin of splice junction phosphate in tRNAs processed by HeLa cell extract. Cell 32: 547-557.
9. Gonzalez, T.N., Sidrauski, C., Dorfler, S., and Walter, P. 1999. Mechanism of non-spliceosomal mRNA splicing in the unfolded protein response pathway. EMBO J. 18: 3119-3132.
10. Harding, H., Zeng, H., Zhang, Y., Jungreis, R., Chung, P., Plesken, H., Sabatini, D., and Ron, D. 2001a. Diabetes mellitus and exocrine pancreatic dysfunction in Perk-/- mice reveals a role for translational control in survival of secretory cells. Mol. Cell 7: 1153-1163.
11. Harding, H.P., Novoa, I., Bertolotti, A., Zeng, H., Zhang, A., Urano, F., Jousse, C., and Ron, D. 2001b. Translational regulation in the cellular response to biosynthetic load on the endoplasmic reticulum. Cold Spring Harb. Symp. Quant. Biol. 66: 499-508.
12. Hopper, A.K. and Phizicky, E.M. 2003. tRNA transfers to the limelight. Genes & Dev. 17: 162-180.
13. Hu, Q.D., Lu, H., Huo, K., Ying, K., Li, J., Xie, Y., Mao, Y., and Li, Y.Y. 2003. A human homolog of the yeast gene encoding tRNA 2′- phosphotransferase: Cloning, characterization and complementation analysis. Cell. Mol. Life Sci. 60: 1725-1732.
14. Lackey, J.G., Sabatino, D., and Damha, M.J. 2007. Solid-phase synthesis and on-column deprotection of RNA from 2′- (and 3′-) O-levulinated (Lv) ribonucleoside monomers. Org. Lett. 9: 789-792.
15. Lappe-Siefke, C., Goebbels, S., Gravel, M., Nicksch, E., Lee, J., Braun, P.E., Griffiths, I.R., and Nave, K.A. 2003. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat. Genet. 33: 366-374.
16. Laski, F.A., Fire, A.Z., Rajbhandary, U.L., and Sharp, P.A. 1983. Characterization of tRNA precursor splicing in mammalian extracts. J. Biol. Chem. 258: 11974-11980.
17. Lee, A.H., Chu, G.C., Iwakoshi, N.N., and Glimcher, L.H. 2005. XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J. 24: 4368-4380.
18. Lowe, T.M. and Eddy, S.R. 1997. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964. doi: 10.1093/nar/25.5.955.
19. Mori, K., Kawahara, T., Yoshida, H., Yanagi, H., and Yura, T. 1996. Signalling from endoplasmic reticulum to nucleus: Transcription factor with a basic-leucine zipper motif is required for the unfolded protein-response pathway. Genes Cells 1: 803-817.
20. Novoa, I., Zeng, H., Harding, H., and Ron, D. 2001. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J. Cell Biol. 153: 1011-1022.
21. Ogle, J.M., Brodersen, D.E., Clemons Jr., W.M., Tarry, M.J., Carter, A.P., and Ramakrishnan, V. 2001. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292: 897-902.
22. Ozcan, U., Cao, Q., Yilmaz, E., Lee, A.H., Iwakoshi, N.N., Ozdelen, E., Tuncman, G., Gorgun, C., Glimcher, L.H., and Hotamisligil, G.S. 2004. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306: 457-461.
23. Paushkin, S.V., Patel, M., Furia, B.S., Peltz, S.W., and Trotta, C.R. 2004. Identification of a human endonuclease complex reveals a link between tRNA splicing and pre-mRNA 3′ end formation. Cell 117: 311-321.
24. Ron, D. and Walter, P. 2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8: 519-529.
25. Ruegsegger, U., Leber, J.H., and Walter, P. 2001. Block of HAC1 mRNA translation by long-range base-pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 107: 103-114.
26. Salgia, S.R., Singh, S.K., Gurha, P., and Gupta, R. 2003. Two reactions of Haloferax volcanii RNA splicing enzymes: Joining of exons and circularization of introns. RNA 9: 319-330.
27. +-dependent tRNA 2′-phosphotransferase Tpt1. RNA 11: 107-113.
28. Schwer, B., Aronova, A., Ramirez, A., Braun, P., and Shuman, S. 2007. Mammalian 2′, 3′ cyclic nucleotide phosphodiesterase (CNP) can function as a tRNA splicing enzyme in vivo. RNA (this issue). doi: 10.1261/rna.858108.
29. Schwer, B., Sawaya, R., Ho, C.K., and Shuman, S. 2004. Portability and fidelity of RNA-repair systems. Proc. Natl. Acad. Sci. 101: 2788-2793.
30. Sidrauski, C., Cox, J.S., and Walter, P. 1996. tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell 87: 405-413.
31. Spinelli, S.L., Consaul, S.A., and Phizicky, E.M. 1997. A conditional lethal yeast phosphotransferase (tpt1) mutant accumulates tRNAs with a 2′-phosphate and an undermodified base at the splice junction. RNA 3: 1388-1400.
32. Spinelli, S.L., Malik, H.S., Consaul, S.A., and Phizicky, E.M. 1998. A functional homolog of a yeast tRNA splicing enzyme is conserved in higher eukaryotes and in Escherichia coli. Proc. Natl. Acad. Sci. 95: 14136-14141.
33. Standring, D.N., Venegas, A., and Rutter, W.J. 1981. Yeast tRNA3Leu gene transcribed and spliced in a HeLa cell extract. Proc. Natl. Acad. Sci. 78: 5963-5967.
34. Steiger, M.A., Jackman, J.E., and Phizicky, E.M. 2005. Analysis of 2′-phosphotransferase (Tpt1p) from Saccharomyces cerevisiae: Evidence for a conserved two-step reaction mechanism. RNA 11: 99-106.
35. Tirasophon, W., Welihinda, A.A., and Kaufman, R.J. 1998. A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes & Dev. 12: 1812-1824.
36. Usman, N., Ogilvie, K.K., Jiang, M.Y., and Cedergren, R.J. 1987. The automated chemical synthesis of long oligoribuncleotides using 2′-O-silylated ribonucleoside 3′-O-phosphoramidites on a controlled-pore glass support: Synthesis of a 43-nucleotide sequence similar to the 3′-half molecule of an Escherichia coli formylmethionine tRNA. J. Am. Chem. Soc. 109: 7845-7854.
37. Wang, X.Z., Harding, H.P., Zhang, Y., Jolicoeur, E.M., Kuroda, M., and Ron, D. 1998. Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J. 17: 5708-5717.
38. Weitzer, S. and Martinez, J. 2007. The human RNA kinase hClp1 is active on 3′ transfer RNA exons and short interfering RNAs. Nature 447: 222-226.
39. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T., and Mori, K. 2001. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107: 881-891.
40. Zillmann, M., Gorovsky, M.A., and Phizicky, E.M. 1991. Conserved mechanism of tRNA splicing in eukaryotes. Mol. Cell. Biol. 11: 5410-5416.
41. Zillmann, M., Gorovsky, M.A., and Phizicky, E.M. 1992. HeLa cells contain a 2′-phosphate-specific phosphotransferase similar to a yeast enzyme implicated in tRNA splicing. J. Biol. Chem. 267: 10289-10294.
42. Zofallova, L., Guo, Y., and Gupta, R. 2000. Junction phosphate is derived from the precursor in the tRNA spliced by the archaeon Haloferax volcanii cell extract. RNA 6: 1019-1030.