Yeast Terminator Function Can Be Modulated and Designed on the Basis of Predictions of Nucleosome Occupancy

ACS Synthetic Biology

Volumn 6, Issue 11, 2017, Pages 2086-2095

  Morse, Nicholas J ^a   Gopal, Madan R ^a   Wagner, James M ^a   Alper, Hal S ^a,b  

^a The University of Texas at Austin   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

3 UTR; nucleosome; Saccharomyces cerevisiae; terminator; yeast

Indexed keywords

ITACONIC ACID; MESSENGER RNA; FUNGAL DNA;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; FLOW CYTOMETRY; GENE LOCUS; NONHUMAN; NUCLEOSOME; OPEN READING FRAME; POLYADENYLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS; REGULATOR GENE; RNA DEGRADATION; SACCHAROMYCES CEREVISIAE; SYNTHETIC BIOLOGY; TRANSCRIPTION TERMINATION; GENETICS; HOMOLOGOUS RECOMBINATION; METABOLISM;

DNA, FUNGAL; HOMOLOGOUS RECOMBINATION; NUCLEOSOMES; SACCHAROMYCES CEREVISIAE; TERMINATOR REGIONS, GENETIC;

EID: 85034609659     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/acssynbio.7b00138     Document Type: Article

References (47)

1. Blazeck, J. and Alper, H. S. (2013) Promoter engineering: recent advances in controlling transcription at the most fundamental level Biotechnol. J. 8, 46-58 10.1002/biot.201200120
2. Redden, H., Morse, N., and Alper, H. S. (2015) The synthetic biology toolbox for tuning gene expression in yeast FEMS Yeast Res. 15, 1-10 10.1111/1567-1364.12188
3. Blazeck, J., Liu, L., Redden, H., and Alper, H. (2011) Tuning gene expression in Yarrowia lipolytica by a hybrid promoter approach Appl. Environ. Microbiol. 77, 7905-7914 10.1128/AEM.05763-11
4. Blazeck, J., Garg, R., Reed, B., and Alper, H. S. (2012) Controlling promoter strength and regulation in Saccharomyces cerevisiae using synthetic hybrid promoters Biotechnol. Bioeng. 109, 2884-2895 10.1002/bit.24552
5. Curran, K. A., Crook, N. C., Karim, A. S., Gupta, A., Wagman, A. M., and Alper, H. S. (2014) Design of synthetic yeast promoters via tuning of nucleosome architecture Nat. Commun. 5, 4002 10.1038/ncomms5002
6. Ito, Y., Yamanishi, M., Ikeuchi, A., Imamura, C., Tokuhiro, K., Kitagawa, T., and Matsuyama, T. (2013) Characterization of five terminator regions that increase the protein yield of a transgene in Saccharomyces cerevisiae J. Biotechnol. 168, 486-492 10.1016/j.jbiotec.2013.09.024
7. Yamanishi, M., Ito, Y., Kintaka, R., Imamura, C., Katahira, S., Ikeuchi, A., Moriya, H., and Matsuyama, T. (2013) A genome-wide activity assessment of terminator regions in Saccharomyces cerevisiae provides a ''terminatome'' toolbox ACS Synth. Biol. 2, 337-347 10.1021/sb300116y
8. Curran, K. A., Karim, A. S., Gupta, A., and Alper, H. S. (2013) Use of expression-enhancing terminators in Saccharomyces cerevisiae to increase mRNA half-life and improve gene expression control for metabolic engineering applications Metab. Eng. 19, 88-97 10.1016/j.ymben.2013.07.001
9. Zhao, J., Hyman, L., and Moore, C. (1999) Formation of mRNA 3′ ends in eukaryotes: mechanism, regulation, and interrelationships with other steps in mRNA synthesis Microbiol. Mol. Biol. Rev. 63, 405-445
10. Guo, Z. and Sherman, F. (1996) 3′-end-forming signals of yeast mRNA Trends Biochem. Sci. 21, 477-481 10.1016/S0968-0004(96)10057-8
11. Guo, Z., Russo, P., Yun, D. F., Butler, J. S., and Sherman, F. (1995) Redundant 3′ end-forming signals for the yeast CYC1 mRNA Proc. Natl. Acad. Sci. U. S. A. 92, 4211-4214 10.1073/pnas.92.10.4211
12. Mischo, H. E. and Proudfoot, N. J. (2013) Disengaging polymerase: terminating RNA polymerase II transcription in budding yeast Biochim. Biophys. Acta, Gene Regul. Mech. 1829, 174-185 10.1016/j.bbagrm.2012.10.003
13. Gross, S. and Moore, C. L. (2001) Rna15 interaction with the A-rich yeast polyadenylation signal is an essential step in mRNA 3′-end formation Mol. Cell. Biol. 21, 8045-8055 10.1128/MCB.21.23.8045-8055.2001
14. Minvielle-Sebastia, L., Beyer, K., Krecic, A. M., Hector, R. E., Swanson, M. S., and Keller, W. (1998) Control of cleavage site selection during mRNA 3′ end formation by a yeast hnRNP EMBO J. 17, 7454-7468 10.1093/emboj/17.24.7454
15. Dichtl, B. and Keller, W. (2001) Recognition of polyadenylation sites in yeast pre-mRNAs by cleavage and polyadenylation factor EMBO J. 20, 3197-3209 10.1093/emboj/20.12.3197
16. Valentini, S. R., Weiss, V. H., and Silver, P. A. (1999) Arginine methylation and binding of Hrp1p to the efficiency element for mRNA 3′-end formation RNA 5, 272-280 10.1017/S1355838299981633
17. Perez-Canadillas, J. M. (2006) Grabbing the message: structural basis of mRNA 3′UTR recognition by Hrp1 EMBO J. 25, 3167-3178 10.1038/sj.emboj.7601190
18. Kessler, M. M., Henry, M. F., Shen, E., Zhao, J., Gross, S., Silver, P. A., and Moore, C. L. (1997) Hrp1, a sequence-specific RNA-binding protein that shuttles between the nucleus and the cytoplasm, is required for mRNA 3′-end formation in yeast Genes Dev. 11, 2545-2556 10.1101/gad.11.19.2545
19. Ezeokonkwo, C., Ghazy, M. A., Zhelkovsky, A., Yeh, P. C., and Moore, C. (2012) Novel interactions at the essential N-terminus of poly(A) polymerase that could regulate poly(A) addition in Saccharomyces cerevisiae FEBS Lett. 586, 1173-1178 10.1016/j.febslet.2012.03.036
20. Curran, K. A., Morse, N. J., Markham, K. A., Wagman, A. M., Gupta, A., and Alper, H. S. (2015) Short Synthetic Terminators for Improved Heterologous Gene Expression in Yeast ACS Synth. Biol. 4, 824-832 10.1021/sb5003357
21. Gupta, I., Clauder-Munster, S., Klaus, B., Jarvelin, A. I., Aiyar, R. S., Benes, V., Wilkening, S., Huber, W., Pelechano, V., and Steinmetz, L. M. (2014) Alternative polyadenylation diversifies post-transcriptional regulation by selective RNA-protein interactions Mol. Syst. Biol. 10, 719 10.1002/msb.135068
22. Geisberg, J. V., Moqtaderi, Z., Fan, X., Ozsolak, F., and Struhl, K. (2014) Global analysis of mRNA isoform half-lives reveals stabilizing and destabilizing elements in yeast Cell 156, 812-824 10.1016/j.cell.2013.12.026
23. Shalem, O., Carey, L., Zeevi, D., Sharon, E., Keren, L., Weinberger, A., Dahan, O., Pilpel, Y., and Segal, E. (2013) Measurements of the impact of 3′ end sequences on gene expression reveal wide range and sequence dependent effects PLoS Comput. Biol. 9, e1002934 10.1371/journal.pcbi.1002934
24. Spies, N., Nielsen, C. B., Padgett, R. A., and Burge, C. B. (2009) Biased chromatin signatures around polyadenylation sites and exons Mol. Cell 36, 245-254 10.1016/j.molcel.2009.10.008
25. Huang, H., Chen, J., Liu, H., and Sun, X. (2013) The nucleosome regulates the usage of polyadenylation sites in the human genome BMC Genomics 14, 912 10.1186/1471-2164-14-912
26. Huang, H., Liu, H., and Sun, X. (2013) Nucleosome distribution near the 3′ ends of genes in the human genome Biosci., Biotechnol., Biochem. 77, 2051-2055 10.1271/bbb.130399
27. Mavrich, T. N., Ioshikhes, I. P., Venters, B. J., Jiang, C., Tomsho, L. P., Qi, J., Schuster, S. C., Albert, I., and Pugh, B. F. (2008) A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome Genome Res. 18, 1073-1083 10.1101/gr.078261.108
28. Ji, Z., Luo, W., Li, W., Hoque, M., Pan, Z., Zhao, Y., and Tian, B. (2011) Transcriptional activity regulates alternative cleavage and polyadenylation Mol. Syst. Biol. 7, 534 10.1038/msb.2011.69
29. Grosso, A. R., de Almeida, S. F., Braga, J., and Carmo-Fonseca, M. (2012) Dynamic transitions in RNA polymerase II density profiles during transcription termination Genome Res. 22, 1447-1456 10.1101/gr.138057.112
30. Xi, L., Fondufe-Mittendorf, Y., Xia, L., Flatow, J., Widom, J., and Wang, J. P. (2010) Predicting nucleosome positioning using a duration Hidden Markov Model BMC Bioinf. 11, 346 10.1186/1471-2105-11-346
31. Mumberg, D., Muller, R., and Funk, M. (1995) Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds Gene 156, 119-122 10.1016/0378-1119(95)00037-7
32. Alper, H., Fischer, C., Nevoigt, E., and Stephanopoulos, G. (2005) Tuning genetic control through promoter engineering Proc. Natl. Acad. Sci. U. S. A. 102, 12678-12683 10.1073/pnas.0504604102
33. Nevoigt, E., Kohnke, J., Fischer, C. R., Alper, H., Stahl, U., and Stephanopoulos, G. (2006) Engineering of promoter replacement cassettes for fine-tuning of gene expression in Saccharomyces cerevisiae Appl. Environ. Microbiol. 72, 5266-5273 10.1128/AEM.00530-06
34. Blazeck, J., Miller, J., Pan, A., Gengler, J., Holden, C., Jamoussi, M., and Alper, H. S. (2014) Metabolic engineering of Saccharomyces cerevisiae for itaconic acid production Appl. Microbiol. Biotechnol. 98, 8155-8164 10.1007/s00253-014-5895-0
35. Shivaswamy, S., Bhinge, A., Zhao, Y., Jones, S., Hirst, M., and Iyer, V. R. (2008) Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation PLoS Biol. 6, e65 10.1371/journal.pbio.0060065
36. Swaminathan, A. and Beilharz, T. H. (2016) Epitope-tagged yeast strains reveal promoter driven changes to 3′-end formation and convergent antisense-transcription from common 3′ UTRs Nucleic Acids Res. 44, 377-386 10.1093/nar/gkv1022
37. Xu, Z., Wei, W., Gagneur, J., Perocchi, F., Clauder-Munster, S., Camblong, J., Guffanti, E., Stutz, F., Huber, W., and Steinmetz, L. M. (2009) Bidirectional promoters generate pervasive transcription in yeast Nature 457, 1033-1037 10.1038/nature07728
38. Martens, J. A., Wu, P. Y., and Winston, F. (2005) Regulation of an intergenic transcript controls adjacent gene transcription in Saccharomyces cerevisiae Genes Dev. 19, 2695-2704 10.1101/gad.1367605
39. Palmer, A. C., Egan, J. B., and Shearwin, K. E. (2011) Transcriptional interference by RNA polymerase pausing and dislodgement of transcription factors Transcription 2, 9-14 10.4161/trns.2.1.13511
40. Shearwin, K. E., Callen, B. P., and Egan, J. B. (2005) Transcriptional interference - a crash course Trends Genet. 21, 339-345 10.1016/j.tig.2005.04.009
41. Fan, X., Moqtaderi, Z., Jin, Y., Zhang, Y., Liu, X. S., and Struhl, K. (2010) Nucleosome depletion at yeast terminators is not intrinsic and can occur by a transcriptional mechanism linked to 3′-end formation Proc. Natl. Acad. Sci. U. S. A. 107, 17945-17950 10.1073/pnas.1012674107
42. Pancevac, C., Goldstone, D. C., Ramos, A., and Taylor, I. A. (2010) Structure of the Rna15 RRM-RNA complex reveals the molecular basis of GU specificity in transcriptional 3′-end processing factors Nucleic Acids Res. 38, 3119-3132 10.1093/nar/gkq002
43. Menconi, G., Bedini, A., Barale, R., and Sbrana, I. (2015) Global mapping of DNA conformational flexibility on Saccharomyces cerevisiae PLoS Comput. Biol. 11, e1004136 10.1371/journal.pcbi.1004136
44. Sheff, M. A. and Thorn, K. S. (2004) Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae Yeast 21, 661-670 10.1002/yea.1130
45. Montgomery, D. L., Hall, B. D., Gillam, S., and Smith, M. (1978) Identification and isolation of the yeast cytochrome c gene Cell 14, 673-680 10.1016/0092-8674(78)90250-7
46. Gibson, D. G., Smith, H. O., Hutchison, C. A., 3rd, Venter, J. C., and Merryman, C. (2010) Chemical synthesis of the mouse mitochondrial genome Nat. Methods 7, 901-903 10.1038/nmeth.1515
47. Gibson, D. G., Young, L., Chuang, R. Y., Venter, J. C., Hutchison, C. A., 3rd, and Smith, H. O. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases Nat. Methods 6, 343-345 10.1038/nmeth.1318