Coordination of tRNA transcription with export at nuclear pore complexes in budding yeast

Genes and Development

Volumn 28, Issue 9, 2014, Pages 959-970

  Chen, Miao ^a   Gartenberg, Marc R ^a,b  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

Author keywords

Cell cycle; Cohesin; Los1 exportin; Nuclear pore complex; RNA polymerase III; tRNA gene

Indexed keywords

DNA DIRECTED RNA POLYMERASE III; TRANSFER RNA;

ARTICLE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; DNA SEQUENCE; FUNGAL STRAIN; GENE EXPRESSION; INTRACELLULAR TRANSPORT; MOLECULAR DOCKING; NONHUMAN; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; YEAST;

CELL CYCLE; COHESIN; LOS1 EXPORTIN; NUCLEAR PORE COMPLEX; RNA POLYMERASE III; TRNA GENE;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL DIVISION; MUTATION; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84899769826     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.236729.113     Document Type: Article

References (61)

1. Aguilera A., Garcia-Muse T. 2012. R loops: from transcription byproducts to threats to genome stability. Mol Cell 46: 115-124.
2. Ausubel F. M, Brent R, Kingston RE, Moore DD, Seidman JG, Smith J. A, Struhl K, ed. 2010. Current protocols in molecular biology. John Wiley & Sons, New York.
3. Bermejo R., Capra T, Jossen R, Colosio A, Frattini C, Carotenuto W, Cocito A, Doksani Y, Klein H, Gomez-Gonzalez B, et al. 2011. The replication checkpoint protects fork stability by releasing transcribed genes from nuclear pores. Cell 146: 233-246.
4. Bertrand E., Houser-Scott F, Kendall A, Singer RH, Engelke DR. 1998. Nucleolar localization of early tRNA processing. Genes Dev 12: 2463-2468.
5. Blobel G. 1985. Gene gating: a hypothesis. Proc Natl Acad Sci 82: 8527-8529.
6. Boguta M. 2013. Maf1, a general negative regulator of RNA polymerase III in yeast. Biochim Biophys Acta 1829: 376-384.
7. Bose T., Lee KK, Lu S, Xu B, Harris B, Slaughter B, Unruh J, Garrett A., McDowell W, Box A, et al. 2012. Cohesin proteins promote ribosomal RNA production and protein translation in yeast and human cells. PLoS Genet 8: e1002749.
8. Brickner D. G, Brickner JH. 2010. Cdk phosphorylation of a nucleoporin controls localization of active genes through the cell cycle. Mol Biol Cell 21: 3421-3432.
9. Cabal G. G, Genovesio A, Rodriguez-Navarro S, Zimmer C, Gadal O., Lesne A, Buc H, Feuerbach-Fournier F, Olivo-Marin JC, Hurt EC, et al. 2006. SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 441: 770-773.
10. Capelson M., Liang Y, Schulte R, MairW, Wagner U, HetzerMW. 2010. Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 140: 372-383.
11. Casolari J. M, Brown CR, Komili S, West J, Hieronymus H, Silver PA. 2004. Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117: 427-439.
12. Chang C. R, Wu CS, Hom Y, Gartenberg MR. 2005. Targeting of cohesin by transcriptionally silent chromatin. Genes Dev 19: 3031-3042.
13. Clelland B. W, Schultz MC. 2010. Genome stability control by checkpoint regulation of tRNA gene transcription. Transcription 1: 115-125.
14. D'Ambrosio C, Schmidt CK, Katou Y, Kelly G, Itoh T, Shirahige K, Uhlmann F. 2008. Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev 22: 2215-2227.
15. Denning D., Mykytka B, Allen NP, Huang L, Al B, Rexach M. 2001. The nucleoporin Nup60p functions as a Gsp1p-GTPsensitive tether for Nup2p at the nuclear pore complex. J Cell Biol 154: 937-950.
16. Deshpande A. M, Newlon CS. 1996. DNA replication fork pause sites dependent on transcription. Science 272: 1030-1033.
17. Dieppois G., Stutz F. 2010. Connecting the transcription site to the nuclear pore: a multi-tether process that regulates gene expression. J Cell Sci 123: 1989-1999.
18. Dilworth D. J, Tackett AJ, Rogers RS, Yi EC, Christmas RH, Smith J. J, Siegel AF, Chait BT, Wozniak RW, Aitchison JD. 2005. The mobile nucleoporin Nup2p and chromatin-bound Prp20p function in endogenous NPC-mediated transcriptional control. J Cell Biol 171: 955-965.
19. Donze D., Kamakaka RT. 2001. RNA polymerase III and RNA polymerase II promoter complexes are heterochromatin barriers in Saccharomyces cerevisiae. EMBO J 20: 520-531.
20. Donze D., Adams CR, Rine J, Kamakaka RT. 1999. The boundaries of the silenced HMR domain in Saccharomyces cerevisiae. Genes Dev 13: 698-708.
21. Doye V., Wepf R, Hurt EC. 1994. A novel nuclear pore protein Nup133p with distinct roles in poly(A)+ RNA transport and nuclear pore distribution. EMBO J 13: 6062-6075.
22. Duan Z., Andronescu M, Schutz K, McIlwain S, Kim YJ, Lee C, Shendure J., Fields S, Blau CA, Noble WS. 2010. A threedimensional model of the yeast genome. Nature 465: 363-367.
23. Dubey R. N, Gartenberg MR. 2007. A tDNA establishes cohesion of a neighboring silent chromatin domain. Genes Dev 21: 2150-2160.
24. Egecioglu D., Brickner JH. 2011. Gene positioning and expression. Curr Opin Cell Biol 23: 338-345.
25. Gard S., LightW, Xiong B, Bose T, McNairn AJ, Harris B, Fleharty B, Seidel C, Brickner JH, Gerton JL. 2009. Cohesinopathy mutations disrupt the subnuclear organization of chromatin. J Cell Biol 187: 455-462.
26. Gartenberg M. R, Neumann FN, Laroche T, Blaszczyk M, Gasser S.M. 2004. Sir-mediated repression can occur independently of chromosomal and subnuclear contexts. Cell 119: 955-967.
27. Gottesfeld J. M, Forbes DJ. 1997. Mitotic repression of the transcriptional machinery. Trends Biochem Sci 22: 197-202.
28. Haeusler R. A, Engelke DR. 2006. Spatial organization of transcription by RNA polymerase III. Nucleic Acids Res 34: 4826-4836.
29. Haeusler R. A, Pratt-Hyatt M, Good PD, Gipson TA, Engelke DR. 2008. Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes. Genes Dev 22: 2204-2214.
30. Hampsey M., Singh BN, Ansari A, Laine JP, Krishnamurthy S. 2011. Control of eukaryotic gene expression: gene loops and transcriptional memory. Adv Enzyme Regul 15: 118-125.
31. Hellmuth K., Lau DM, Bischoff FR, Kunzler M, Hurt E, Simos G. 1998. Yeast Los1p has properties of an exportin-like nucleocytoplasmic transport factor for tRNA. Mol Cell Biol 18: 6374-6386.
32. Hiraga S., Botsios S, Donze D, Donaldson AD. 2012. TFIIIC localizes budding yeast ETC sites to the nuclear periphery. Mol Biol Cell 23: 2741-2754.
33. Hopper A.K. 2013. Transfer RNA post-transcriptional processing, turnover, and subcellular dynamics in the yeast Saccharomyces cerevisiae. Genetics 194: 43-67.
34. Hopper A. K, Schultz LD, Shapiro RA. 1980. Processing of intervening sequences: a new yeast mutant which fails to excise intervening sequences from precursor tRNAs. Cell 19: 741-751.
35. Hurt D. J, Wang SS, Lin YH, Hopper AK. 1987. Cloning and characterization of LOS1, a Saccharomyces cerevisiae gene that affects tRNA splicing. Mol Cell Biol 7: 1208-1216.
36. Ikegami K., Lieb JD. 2013. Integral nuclear pore proteins bind to Pol III-transcribed genes and are required for Pol III transcript processing in C. elegans. Mol Cell 51: 840-849.
37. Ivessa A. S, Lenzmeier BA, Bessler JB, Goudsouzian LK, Schnakenberg SL, Zakian VA. 2003. The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol Cell 12: 1525-1536.
38. Iwasaki O., Tanaka A, Tanizawa H, Grewal SI, Noma K. 2010. Centromeric localization of dispersed Pol III genes in fission yeast. Mol Biol Cell 21: 254-265.
39. Kalverda B., Pickersgill H, Shloma VV, Fornerod M. 2010. Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell 140: 360-371.
40. Karkusiewicz I., Turowski TW, Graczyk D, Towpik J, Dhungel N, Hopper AK, Boguta M. 2011. Maf1 protein, repressor of RNA polymerase III, indirectly affects tRNA processing. J Biol Chem 286: 39478-39488.
41. Kirkland J. G, Raab JR, Kamakaka RT. 2013. TFIIIC bound DNA elements in nuclear organization and insulation. Biochim Biophys Acta 1829: 418-424.
42. Kobayashi T., Horiuchi T, Tongaonkar P, Vu L, Nomura M. 2004. SIR2 regulates recombination between different rDNA repeats, but not recombination within individual rRNA genes in yeast. Cell 117: 441-453.
43. Menon B. B, Sarma NJ, Pasula S, Deminoff SJ, Willis KA, Barbara KE, Andrews B, Santangelo GM. 2005. Reverse recruitment: the Nup84 nuclear pore subcomplex mediates Rap1/Gcr1/ Gcr2 transcriptional activation. Proc Natl Acad Sci 102: 5749-5754.
44. Murthi A., Shaheen HH, Huang HY, Preston MA, Lai TP, Phizicky E. M, Hopper AK. 2010. Regulation of tRNA bidirectional nuclear-cytoplasmic trafficking in Saccharomyces cerevisiae. Mol Biol Cell 21: 639-649.
45. Nguyen V. C, Clelland BW, Hockman DJ, Kujat-Choy SL, Mewhort H. E, Schultz MC. 2010. Replication stress checkpoint signaling controls tRNA gene transcription. Nat Struct Mol Biol 17: 976-981.
46. Noma K., Cam HP, Maraia RJ, Grewal SI. 2006. A role for TFIIIC transcription factor complex in genome organization. Cell 125: 859-872.
47. Oeffinger M., Zenklusen D. 2012. To the pore and through the pore: a story of mRNA export kinetics. Biochim Biophys Acta 1819: 494-506.
48. Roberts D. N, Wilson B, Huff JT, Stewart AJ, Cairns BR. 2006. Dephosphorylation and genome-wide association of Maf1 with Pol III-transcribed genes during repression. Mol Cell 22: 633-644.
49. Ruben G. J, Kirkland JG, Macdonough T, Chen M, Dubey RN, Gartenberg M. R, Kamakaka RT. 2011. Nucleoporin mediated nuclear positioning and silencing of HMR. PLoS ONE 6: e21923.
50. Sarkar S., Hopper AK. 1998. tRNA nuclear export in Saccharomyces cerevisiae: in situ hybridization analysis. Mol Biol Cell 9: 3041-3055.
51. Schmid M., Arib G, Laemmli C, Nishikawa J, Durussel T, Laemmli U.K. 2006. Nup-PI: the nucleopore-promoter interaction of genes in yeast. Mol Cell 21: 379-391.
52. Shaheen H. H, Hopper AK. 2005. Retrograde movement of tRNAs from the cytoplasm to the nucleus in Saccharomyces cerevisiae. Proc Natl Acad Sci 102: 11290-11295.
53. Singh A. 1977. Nonsense suppressors of yeast cause osmoticsensitive growth. Proc Natl Acad Sci 74: 305-309.
54. Szilard R. K, Jacques PE, Laramee L, Cheng B, Galicia S, Bataille AR, Yeung M, Mendez M, Bergeron M, Robert F, et al. 2010. Systematic identification of fragile sites via genome-wide location analysis of γ-H2AX. Nat Struct Mol Biol 17: 299-305.
55. Taddei A., Gasser SM. 2012. Structure and function in the budding yeast nucleus. Genetics 192: 107-129.
56. Takano A., Endo T, Yoshihisa T. 2005. tRNA actively shuttles between the nucleus and cytosol in yeast. Science 309: 140-142.
57. Texari L., Dieppois G, Vinciguerra P, Contreras MP, Groner A, Letourneau A., Stutz F. 2013. The nuclear pore regulates GAL1 gene transcription by controlling the localization of the SUMO protease Ulp1. Mol Cell 51: 807-818.
58. Thompson M., Haeusler RA, Good PD, Engelke DR. 2003. Nucleolar clustering of dispersed tRNA genes. Science 302: 1399-1401.
59. Valenzuela L., Dhillon N, Dubey RN, Gartenberg MR, Kamakaka RT. 2008. Long-range communication between the silencers of HMR. Mol Cell Biol 28: 1924-1935.
60. van Attikum H, Fritsch O, Hohn B, Gasser SM. 2004. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119: 777-788.
61. Yoshihisa T., Yunoki-Esaki K, Ohshima C, Tanaka N, Endo T. 2003. Possibility of cytoplasmic pre-tRNA splicing: the yeast tRNA splicing endonuclease mainly localizes on the mitochondria. Mol Biol Cell 14: 3266-3279.