Mapping of transcription start sites in Saccharomyces cerevisiae using 5′ SAGE
10.1093/nar/gki583
Crossref journal-article
Oxford University Press (OUP)
Nucleic Acids Research (286)
Abstract

Abstract A minimally addressed area in Saccharomyces cerevisiae research is the mapping of transcription start sites (TSS). Mapping of TSS in S.cerevisiae has the potential to contribute to our understanding of gene regulation, transcription, mRNA stability and aspects of RNA biology. Here, we use 5′ SAGE to map 5′ TSS in S.cerevisiae . Tags identifying the first 15–17 bases of the transcripts are created, ligated to form ditags, amplified, concatemerized and ligated into a vector to create a library. Each clone sequenced from this library identifies 10–20 TSS. We have identified 13 746 unique, unambiguous sequence tags from 2231 S.cerevisiae genes. TSS identified in this study are consistent with published results, with primer extension results described here, and are consistent with expectations based on previous work on transcription initiation. We have aligned the sequence flanking 4637 TSS to identify the consensus sequence A(A rich ) 5 NPy A (A/T)NN(A rich ) 6 , which confirms and expands the previous reported Py A (A/T)Pu consensus pattern. The TSS data allowed the identification of a previously unrecognized gene, uncovered errors in previous annotation, and identified potential regulatory RNAs and upstream open reading frames in 5′-untranslated region.

Bibliography

Zhang, Z., & Dietrich, F. S. (2005). Mapping of transcription start sites in Saccharomyces cerevisiae using 5′ SAGE. Nucleic Acids Research, 33(9), 2838–2851.

Authors 2
  1. Zhihong Zhang (first)
  2. Fred S. Dietrich (additional)
References 88 Referenced 174
  1. Dietrich, F.S., Voegeli, S., Brachat, S., Lerch, A., Gates, K., Steiner, S., Mohr, C., Pohlmann, R., Luedi, P., Choi, S., et al. 2004 The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome Science304304 –307
  2. Kellis, M., Birren, B.W., Lander, E.S. 2004 Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiaeNature428617 –624 (10.1038/nature02424)
  3. Cliften, P., Sudarsanam, P., Desikan, A., Fulton, L., Fulton, B., Majors, J., Waterston, R., Cohen, B.A., Johnston, M. 2003 Finding functional features in Saccharomyces genomes by phylogenetic footprinting Science30171 –76 (10.1126/science.1084337)
  4. Sherman, D., Durrens, P., Beyne, E., Nikolski, M., Souciet, J.L. 2004 Genolevures: comparative genomics and molecular evolution of hemiascomycetous yeasts Nucleic Acids Res.32D315 –D318 (10.1093/nar/gkh091)
  5. Zhang, Z. and Dietrich, F.S. 2003 Verification of a new gene on Saccharomyces cerevisiae chromosome III Yeast20731 –738 (10.1002/yea.996)
  6. Brachat, S., Dietrich, F.S., Voegeli, S., Zhang, Z., Stuart, L., Lerch, A., Gates, K., Gaffney, T., Philippsen, P. 2003 Reinvestigation of the Saccharomyces cerevisiae genome annotation by comparison to the genome of a related fungus: Ashbya gossypiiGenome Biol.4R45 (10.1186/gb-2003-4-7-r45)
  7. Hannenhalli, S. and Levy, S. 2001 Promoter prediction in the human genome Bioinformatics17 Suppl. 1, S90 –S96 (10.1093/bioinformatics/17.suppl_1.S90)
  8. Shiraki, T., Kondo, S., Katayama, S., Waki, K., Kasukawa, T., Kawaji, H., Kodzius, R., Watahiki, A., Nakamura, M., Arakawa, T., et al. 2003 Cap analysis gene expression for high-throughput analysis of transcriptional starting point and identification of promoter usage Proc. Natl Acad. Sci. USA10015776 –15781 (10.1073/pnas.2136655100)
  9. Wei, C.L., Ng, P., Chiu, K.P., Wong, C.H., Ang, C.C., Lipovich, L., Liu, E.T., Ruan, Y. 2004 5′ Long serial analysis of gene expression (LongSAGE) and 3′ LongSAGE for transcriptome characterization and genome annotation Proc. Natl Acad. Sci. USA10111701 –11706 (10.1073/pnas.0403514101)
  10. Hashimoto, S., Suzuki, Y., Kasai, Y., Morohoshi, K., Yamada, T., Sese, J., Morishita, S., Sugano, S., Matsushima, K. 2004 5′-end SAGE for the analysis of transcriptional start sites Nat. Biotechnol.221146 –1149 (10.1038/nbt998)
  11. Hurowitz, E.H. and Brown, P.O. 2003 Genome-wide analysis of mRNA lengths in Saccharomyces cerevisiaeGenome Biol.5R2 (10.1186/gb-2003-5-1-r2)
  12. Pesole, G., Liuni, S., Grillo, G., Licciulli, F., Mignone, F., Gissi, C., Saccone, C. 2002 UTRdb and UTRsite: specialized databases of sequences and functional elements of 5′ and 3′ untranslated regions of eukaryotic mRNAs. Update 2002 Nucleic Acids Res.30335 –340 (10.1093/nar/30.1.335)
  13. Buratowski, S., Hahn, S., Guarente, L., Sharp, P.A. 1989 Five intermediate complexes in transcription initiation by RNA polymerase II Cell56549 –561 (10.1016/0092-8674(89)90578-3)
  14. Hampsey, M. 1998 Molecular genetics of the RNA polymerase II general transcriptional machinery Microbiol. Mol. Biol. Rev.62465 –503 (10.1128/MMBR.62.2.465-503.1998)
  15. Smale, S.T. and Baltimore, D. 1989 The ‘initiator’ as a transcription control element Cell57103 –113 (10.1016/0092-8674(89)90176-1)
  16. Weis, L. and Reinberg, D. 1992 Transcription by RNA polymerase II: initiator-directed formation of transcription-competent complexes FASEB J.63300 –3309 (10.1096/fasebj.6.14.1426767)
  17. Weis, L. and Reinberg, D. 1997 Accurate positioning of RNA polymerase II on a natural TATA-less promoter is independent of TATA-binding-protein-associated factors and initiator-binding proteins Mol. Cell. Biol.172973 –2984 (10.1128/MCB.17.6.2973)
  18. Bucher, P. 1990 Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences J. Mol. Biol.212563 –578 (10.1016/0022-2836(90)90223-9)
  19. Basehoar, A.D., Zanton, S.J., Pugh, B.F. 2004 Identification and distinct regulation of yeast TATA box-containing genes Cell116699 –709 (10.1016/S0092-8674(04)00205-3)
  20. Cherry, J.M., Ball, C., Weng, S., Juvik, G., Schmidt, R., Adler, C., Dunn, B., Dwight, S., Riles, L., Mortimer, R.K., et al. 1997 Genetic and physical maps of Saccharomyces cerevisiaeNature38767 –73 (10.1038/387s067)
  21. Burke, D., Dawson, D., Stearns, T. Methods in Yeast Genetics; A Cold Spring Harbor Laboratory Course manual2000 Cold Spring Harbor, NY CSHL Press
  22. Ewing, B., Hillier, L., Wendl, M.C., Green, P. 1998 Base-calling of automated sequencer traces using phred. I. Accuracy assessment Genome Res.8175 –185 (10.1101/gr.8.3.175)
  23. Ewing, B. and Green, P. 1998 Base-calling of automated sequencer traces using phred. II. Error probabilities Genome Res.8186 –194 (10.1101/gr.8.3.186)
  24. Holstege, F.C., Jennings, E.G., Wyrick, J.J., Lee, T.I., Hengartner, C.J., Green, M.R., Golub, T.R., Lander, E.S., Young, R.A. 1998 Dissecting the regulatory circuitry of a eukaryotic genome Cell95717 –728 (10.1016/S0092-8674(00)81641-4)
  25. Dance, G.S., Beemiller, P., Yang, Y., Mater, D.V., Mian, I.S., Smith, H.C. 2001 Identification of the yeast cytidine deaminase CDD1 as an orphan C → U RNA editase Nucleic Acids Res.291772 –1780 (10.1093/nar/29.8.1772)
  26. Wickens, M.P., Buell, G.N., Schimke, R.T. 1978 Synthesis of double-stranded DNA complementary to lysozyme, ovomucoid, and ovalbumin mRNAs. Optimization for full length second strand synthesis by Escherichia coli DNA polymerase I J Biol. Chem.2532483 –2495 (10.1016/S0021-9258(17)38098-5)
  27. Berk, A.J. and Sharp, P.A. 1977 Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids Cell12721 –732 (10.1016/0092-8674(77)90272-0)
  28. Karin, M., Najarian, R., Haslinger, A., Valenzuela, P., Welch, J., Fogel, S. 1984 Primary structure and transcription of an amplified genetic locus: the CUP1 locus of yeast Proc. Natl Acad. Sci. USA81337 –341 (10.1073/pnas.81.2.337)
  29. Liao, X.B., Clare, J.J., Farabaugh, P.J. 1987 The upstream activation site of a Ty2 element of yeast is necessary but not sufficient to promote maximal transcription of the element Proc. Natl Acad. Sci. USA848520 –8524 (10.1073/pnas.84.23.8520)
  30. Fulton, A.M., Rathjen, P.D., Kingsman, S.M., Kingsman, A.J. 1988 Upstream and downstream transcriptional control signals in the yeast retrotransposon, TY Nucleic Acids Res.165439 –5458 (10.1093/nar/16.12.5439)
  31. Nagashima, K., Kasai, M., Nagata, S., Kaziro, Y. 1986 Structure of the two genes coding for polypeptide chain elongation factor 1 alpha (EF-1 alpha) from Saccharomyces cerevisiaeGene45265 –273
  32. Alber, T. and Kawasaki, G. 1982 Nucleotide sequence of the triose phosphate isomerase gene of Saccharomyces cerevisiaeJ. Mol. Appl. Genet.1419 –434
  33. Strathern, J.N., Jones, E.W., Broach, J.R. 1982 The molecular biology of the yeast Sacchromyces : metabolism and gene expression Cold Spring Harbor Monograph Series; 11B Cold Spring Harbor, NY Cold Spring Harbor Laboratory pp. x, 680 p
  34. Morlando, M., Greco, P., Dichtl, B., Fatica, A., Keller, W., Bozzoni, I. 2002 Functional analysis of yeast snoRNA and snRNA 3′-end formation mediated by uncoupling of cleavage and polyadenylation Mol. Cell. Biol.221379 –1389 (10.1128/MCB.22.5.1379-1389.2002)
  35. Martens, J.A., Laprade, L., Winston, F. 2004 Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene Nature429571 –574 (10.1038/nature02538)
  36. Morey, C. and Avner, P. 2004 Employment opportunities for non-coding RNAs FEBS Lett.56727 –34 (10.1016/j.febslet.2004.03.117)
  37. Hahn, S., Hoar, E.T., Guarente, L. 1985 Each of three ‘TATA elements’ specifies a subset of the transcription initiation sites at the CYC-1 promoter of Saccharomyces cerevisiaeProc. Natl Acad. Sci. USA828562 –8566 (10.1073/pnas.82.24.8562)
  38. Schneider, T.D. and Stephens, R.M. 1990 Sequence logos: a new way to display consensus sequences Nucleic Acids Res.186097 –6100 (10.1093/nar/18.20.6097)
  39. Crooks, G.E., Hon, G., Chandonia, J.M., Brenner, S.E. 2004 WebLogo: a sequence logo generator Genome Res.141188 –1190 (10.1101/gr.849004)
  40. Oshiro, G., Wodicka, L.M., Washburn, M.P., Yates, J.R., III, Lockhart, D.J., Winzeler, E.A. 2002 Parallel identification of new genes in Saccharomyces cerevisiaeGenome Res.121210 –1220 (10.1101/gr.226802)
  41. Wolfe, K.H. and Shields, D.C. 1997 Molecular evidence for an ancient duplication of the entire yeast genome Nature387708 –713 (10.1038/42711)
  42. Kellis, M., Patterson, N., Endrizzi, M., Birren, B., Lander, E.S. 2003 Sequencing and comparison of yeast species to identify genes and regulatory elements Nature423241 –254 (10.1038/nature01644)
  43. Natsoulis, G., Hilger, F., Fink, G.R. 1986 The HTS1 gene encodes both the cytoplasmic and mitochondrial histidine tRNA synthetases of Saccaromyces cerevisiaeCell46235 –243 (10.1016/0092-8674(86)90740-3)
  44. Velculescu, V.E., Zhang, L., Zhou, W., Vogelstein, J., Basrai, M.A., Bassett, D.E., Jr, Hieter, P., Vogelstein, B., Kinzler, K.W. 1997 Characterization of the yeast transcriptome Cell88243 –251 (10.1016/S0092-8674(00)81845-0)
  45. Vilela, C. and McCarthy, J.E. 2003 Regulation of fungal gene expression via short open reading frames in the mRNA 5′ untranslated region Mol. Microbiol.49859 –867 (10.1046/j.1365-2958.2003.03622.x)
  46. Dujon, B., Sherman, D., Fischer, G., Durrens, P., Casaregola, S., Lafontaine, I., De Montigny, J., Marck, C., Neuveglise, C., Talla, E., et al. 2004 Genome evolution in yeasts Nature43035 –44
  47. Chenchik, A., Zhu, Y.Y., Diatchenko, L., Li, R., Jill, J., Siebert, P.D. RT–PCR Methods for Gene Cloning and Analysis1998 MA, USA Eaton, Natick
  48. Zhu, Y.Y., Machleder, E.M., Chenchik, A., Li, R., Siebert, P.D. 2001 Reverse transcriptase template switching: a SMART approach for full-length cDNA library construction Biotechniques30892 –897 (10.2144/01304pf02)
  49. Struhl, K. 1987 Promoters, activator proteins, and the mechanism of transcriptional initiation in yeast Cell49295 –297 (10.1016/0092-8674(87)90277-7)
  50. Russell, P.R. 1983 Evolutionary divergence of the mRNA transcription initiation mechanism in yeast Nature301167 –169 (10.1038/301167a0)
  51. Corden, J., Wasylyk, B., Buchwalder, A., Sassone-Corsi, P., Kedinger, C., Chambon, P. 1980 Promoter sequences of eukaryotic protein-coding genes Science2091406 –1414 (10.1126/science.6251548)
  52. Giardina, C. and Lis, J.T. 1993 DNA melting on yeast RNA polymerase II promoters Science261759 –762 (10.1126/science.8342041)
  53. Choi, W.S., Yan, M., Nusinow, D., Gralla, J.D. 2002In vitro transcription and start site selection in Schizosaccharomyces pombeJ. Mol. Biol.3191005 –1013 (10.1016/S0022-2836(02)00329-7)
  54. Healy, A.M., Helser, T.L., Zitomer, R.S. 1987 Sequences required for transcriptional initiation of the Saccharomyces cerevisiae CYC7 genes Mol. Cell. Biol.73785 –3791 (10.1128/MCB.7.10.3785)
  55. Healy, A.M. and Zitomer, R.S. 1990 A sequence that directs transcriptional initiation in yeast Curr. Genet.18105 –109 (10.1007/BF00312597)
  56. Wood, V., Rutherford, K.M., Ivens, A., Rajandream, M.A., Barrell, B. 2001 A Re-annotation of the Saccharomyces cerevisiae Genome Comp. Funct. Genomics2143 –154 (10.1002/cfg.86)
  57. Magdolen, V., Oechsner, U., Muller, G., Bandlow, W. 1988 The intron-containing gene for yeast profilin (PFY) encodes a vital function Mol. Cell. Biol.85108 –5115 (10.1128/MCB.8.12.5108)
  58. Nagawa, F. and Fink, G.R. 1985 The relationship between the ‘TATA’ sequence and transcription initiation sites at the HIS4 gene of Saccharomyces cerevisiaeProc. Natl Acad. Sci. USA828557 –8561 (10.1073/pnas.82.24.8557)
  59. van den Heuvel, J.J., Bergkamp, R.J., Planta, R.J., Raue, H.A. 1989 Effect of deletions in the 5′-noncoding region on the translational efficiency of phosphoglycerate kinase mRNA in yeast Gene7983 –95 (10.1016/0378-1119(89)90094-2)
  60. Wright, R.M., Dircks, L.K., Poyton, R.O. 1986 Characterization of COX9, the nuclear gene encoding the yeast mitochondrial protein cytochrome c oxidase subunit VIIa. Subunit VIIa lacks a leader peptide and is an essential component of the holoenzyme J. Biol. Chem.26117183 –17191 (10.1016/S0021-9258(19)76017-7)
  61. Newton, C.H., Shimmin, L.C., Yee, J., Dennis, P.P. 1990 A family of genes encode the multiple forms of the Saccharomyces cerevisiae ribosomal proteins equivalent to the Escherichia coli L12 protein and a single form of the L10-equivalent ribosomal protein J. Bacteriol.172579 –588 (10.1128/jb.172.2.579-588.1990)
  62. Paravicini, G., Braus, G., Hutter, R. 1988 Structure of the ARO3 gene of Saccharomyces cerevisiaeMol. Gen. Genet.214165 –169 (10.1007/BF00340197)
  63. Dabeva, M.D. and Warner, J.R. 1987 The yeast ribosomal protein L32 and its gene J. Biol. Chem.26216055 –16059 (10.1016/S0021-9258(18)47695-8)
  64. Escobar-Henriques, M., Daignan-Fornier, B., Collart, M.A. 2003 The critical cis-acting element required for IMD2 feedback regulation by GDP is a TATA box located 202 nucleotides upstream of the transcription start site Mol. Cell. Biol.236267 –6278 (10.1128/MCB.23.17.6267-6278.2003)
  65. Huet, J., Cottrelle, P., Cool, M., Vignais, M.L., Thiele, D., Marck, C., Buhler, J.M., Sentenac, A., Fromageot, P. 1985 A general upstream binding factor for genes of the yeast translational apparatus EMBO J.43539 –3547 (10.1002/j.1460-2075.1985.tb04114.x)
  66. Ogawa, N., Saitoh, H., Miura, K., Magbanua, J.P., Bun-ya, M., Harashima, S., Oshima, Y. 1995 Structure and distribution of specific cis -elements for transcriptional regulation of PHO84 in Saccharomyces cerevisiaeMol. Gen. Genet.249406 –416 (10.1007/BF00287102)
  67. Cumsky, M.G., Trueblood, C.E., Ko, C., Poyton, R.O. 1987 Structural analysis of two genes encoding divergent forms of yeast cytochrome c oxidase subunit V Mol. Cell. Biol.73511 –3519 (10.1128/MCB.7.10.3511)
  68. Crabeel, M., de Rijcke, M., Seneca, S., Heimberg, H., Pfeiffer, I., Matisova, A. 1995 Further definition of the sequence and position requirements of the arginine control element that mediates repression and induction by arginine in Saccharomyces cerevisiaeYeast111367 –1380 (10.1002/yea.320111405)
  69. Faitar, S.L., Brodie, S.A., Ponticelli, A.S. 2001 Promoter-specific shifts in transcription initiation conferred by yeast TFIIB mutations are determined by the sequence in the immediate vicinity of the start sites Mol. Cell. Biol.214427 –4440 (10.1128/MCB.21.14.4427-4440.2001)
  70. Russell, D.W., Smith, M., Williamson, V.M., Young, E.T. 1983 Nucleotide sequence of the yeast alcohol dehydrogenase II gene J. Biol. Chem.2582674 –2682 (10.1016/S0021-9258(18)32979-X)
  71. Schneider, J.C. and Guarente, L. 1991 Regulation of the yeast CYT1 gene encoding cytochrome c1 by HAP1 and HAP2/3/4 Mol. Cell. Biol.114934 –4942 (10.1128/MCB.11.10.4934)
  72. Minehart, P.L. and Magasanik, B. 1992 Sequence of the GLN1 gene of Saccharomyces cerevisiae : role of the upstream region in regulation of glutamine synthetase expression J. Bacteriol.1741828 –1836 (10.1128/jb.174.6.1828-1836.1992)
  73. Freeman, K.B., Karns, L.R., Lutz, K.A., Smith, M.M. 1992 Histone H3 transcription in Saccharomyces cerevisiae is controlled by multiple cell cycle activation sites and a constitutive negative regulatory element Mol. Cell. Biol.125455 –5463 (10.1128/MCB.12.12.5455)
  74. Kunzler, M., Paravicini, G., Egli, C.M., Irniger, S., Braus, G.H. 1992 Cloning, primary structure and regulation of the ARO4 gene, encoding the tyrosine-inhibited 3-deoxy- d -arabino-heptulosonate-7-phosphate synthase from Saccharomyces cerevisiaeGene11367 –74 (10.1016/0378-1119(92)90670-K)
  75. Zagorec, M., Buhler, J.M., Treich, I., Keng, T., Guarente, L., Labbe-Bois, R. 1988 Isolation, sequence, and regulation by oxygen of the yeast HEM13 gene coding for coproporphyrinogen oxidase J. Biol. Chem.2639718 –9724 (10.1016/S0021-9258(19)81577-6)
  76. Schneider, J.C. and Guarente, L. 1987 The untranslated leader of nuclear COX4 gene of Saccharomyces cerevisiae contains an intron Nucleic Acids Res.153515 –3529 (10.1093/nar/15.8.3515)
  77. Pavlovic, B. and Horz, W. 1988 The chromatin structure at the promoter of a glyceraldehyde phosphate dehydrogenase gene from Saccharomyces cerevisiae reflects its functional state Mol. Cell. Biol.85513 –5520 (10.1128/MCB.8.12.5513)
  78. Brindle, P.K., Holland, J.P., Willett, C.E., Innis, M.A., Holland, M.J. 1990 Multiple factors bind the upstream activation sites of the yeast enolase genes ENO1 and ENO2: ABFI protein, like repressor activator protein RAP1, binds cis -acting sequences which modulate repression or activation of transcription Mol. Cell. Biol.104872 –4885 (10.1128/MCB.10.9.4872)
  79. Beacham, I.R., Schweitzer, B.W., Warrick, H.M., Carbon, J. 1984 The nucleotide sequence of the yeast ARG4 gene Gene29271 –279 (10.1016/0378-1119(84)90056-8)
  80. Repetto, B. and Tzagoloff, A. 1989 Structure and regulation of KGD1, the structural gene for yeast alpha-ketoglutarate dehydrogenase Mol. Cell. Biol.92695 –2705 (10.1128/MCB.9.6.2695)
  81. Sarokin, L. and Carlson, M. 1985 Comparison of two yeast invertase genes: conservation of the upstream regulatory region Nucleic Acids Res.136089 –6103 (10.1093/nar/13.17.6089)
  82. Dohrmann, P.R., Voth, W.P., Stillman, D.J. 1996 Role of negative regulation in promoter specificity of the homologous transcriptional activators Ace2p and Swi5p Mol. Cell. Biol.161746 –1758 (10.1128/MCB.16.4.1746)
  83. Nouraini, S., Hu, J., McBroom, L.D., Friesen, J.D. 1996 Mutations in an Abf1p binding site in the promoter of yeast RPO26 shift the transcription start sites and reduce the level of RPO26 mRNA Yeast121339 –1350 (10.1002/(SICI)1097-0061(199610)12:13<1339::AID-YEA31>3.0.CO;2-C)
  84. Hahn, S., Pinkham, J., Wei, R., Miller, R., Guarente, L. 1988 The HAP3 regulatory locus of Saccharomyces cerevisiae encodes divergent overlapping transcripts Mol. Cell. Biol.8655 –663 (10.1128/MCB.8.2.655)
  85. Urban-Grimal, D., Volland, C., Garnier, T., Dehoux, P., Labbe-Bois, R. 1986 The nucleotide sequence of the HEM1 gene and evidence for a precursor form of the mitochondrial 5-aminolevulinate synthase in Saccharomyces cerevisiaeEur. J. Biochem.156511 –519 (10.1111/j.1432-1033.1986.tb09610.x)
  86. Losson, R., Fuchs, R.P., Lacroute, F. 1985 Yeast promoters URA1 and URA3. Examples of positive control J. Mol. Biol.18565 –81 (10.1016/0022-2836(85)90183-4)
  87. Kim, G.J., Park, J.H., Lee, D.C., Ro, H.S., Kim, H.S. 1997 Primary structure, sequence analysis, and expression of the thermostable d -hydantoinase from Bacillus stearothermophilus SD1 Mol. Gen. Genet.255152 –156 (10.1007/PL00008610)
  88. Erkine, A.M., Adams, C.C., Gao, M., Gross, D.S. 1995 Multiple protein–DNA interactions over the yeast HSC82 heat shock gene promoter Nucleic Acids Res.231822 –1829 (10.1093/nar/23.10.1822)
Dates
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Created 20 years, 2 months ago (May 27, 2005, 2:48 p.m.)
Deposited 1 year, 4 months ago (March 28, 2024, 9:46 a.m.)
Indexed 12 hours, 24 minutes ago (Aug. 21, 2025, 1:21 p.m.)
Issued 20 years, 7 months ago (Jan. 1, 2005)
Published 20 years, 7 months ago (Jan. 1, 2005)
Published Online 20 years, 7 months ago (Jan. 1, 2005)
Published Print 20 years, 3 months ago (May 1, 2005)
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@article{Zhang_2005, title={Mapping of transcription start sites in Saccharomyces cerevisiae using 5′ SAGE}, volume={33}, ISSN={0305-1048}, url={http://dx.doi.org/10.1093/nar/gki583}, DOI={10.1093/nar/gki583}, number={9}, journal={Nucleic Acids Research}, publisher={Oxford University Press (OUP)}, author={Zhang, Zhihong and Dietrich, Fred S.}, year={2005}, month=jan, pages={2838–2851} }