Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1997 Nov;17(11):6223–6235. doi: 10.1128/mcb.17.11.6223

Role of UME6 in transcriptional regulation of a DNA repair gene in Saccharomyces cerevisiae.

D H Sweet 1, Y K Jang 1, G B Sancar 1
PMCID: PMC232473  PMID: 9343383

Abstract

In Saccharomyces cerevisiae UV radiation and a variety of chemical DNA-damaging agents induce the transcription of specific genes, including several involved in DNA repair. One of the best characterized of these genes is PHR1, which encodes the apoenzyme for DNA photolyase. Basal-level and damage-induced expression of PHR1 require an upstream activation sequence, UAS(PHR1), which has homology with DRC elements found upstream of at least 19 other DNA repair and DNA metabolism genes in yeast. Here we report the identification of the UME6 gene of S. cerevisiae as a regulator of UAS(PHR1) activity. Multiple copies of UME6 stimulate expression from UAS(PHR1) and the intact PHR1 gene. Surprisingly, the effect of deletion of UME6 is growth phase dependent. In wild-type cells PHR1 is induced in late exponential phase, concomitant with the initiation of glycogen accumulation that precedes the diauxic shift. Deletion of UME6 abolishes this induction, decreases the steady-state concentration of photolyase molecules and PHR1 mRNA, and increases the UV sensitivity of a rad2 mutant. Despite the fact that UAS(PHR1) does not contain the URS1 sequence, which has been previously implicated in UME6-mediated transcriptional regulation, we find that Ume6p binds to UAS(PHR1) with an affinity and a specificity similar to those seen for a URS1 site. Similar binding is also seen for DRC elements from RAD2, RAD7, and RAD53, suggesting that UME6 contributes to the regulated expression of a subset of damage-responsive genes in yeast.

Full Text

The Full Text of this article is available as a PDF (1.7 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson S. F., Steber C. M., Esposito R. E., Coleman J. E. UME6, a negative regulator of meiosis in Saccharomyces cerevisiae, contains a C-terminal Zn2Cys6 binuclear cluster that binds the URS1 DNA sequence in a zinc-dependent manner. Protein Sci. 1995 Sep;4(9):1832–1843. doi: 10.1002/pro.5560040918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Belazzi T., Wagner A., Wieser R., Schanz M., Adam G., Hartig A., Ruis H. Negative regulation of transcription of the Saccharomyces cerevisiae catalase T (CTT1) gene by cAMP is mediated by a positive control element. EMBO J. 1991 Mar;10(3):585–592. doi: 10.1002/j.1460-2075.1991.tb07985.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bowdish K. S., Yuan H. E., Mitchell A. P. Positive control of yeast meiotic genes by the negative regulator UME6. Mol Cell Biol. 1995 Jun;15(6):2955–2961. doi: 10.1128/mcb.15.6.2955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Buckingham L. E., Wang H. T., Elder R. T., McCarroll R. M., Slater M. R., Esposito R. E. Nucleotide sequence and promoter analysis of SPO13, a meiosis-specific gene of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9406–9410. doi: 10.1073/pnas.87.23.9406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cameron S., Levin L., Zoller M., Wigler M. cAMP-independent control of sporulation, glycogen metabolism, and heat shock resistance in S. cerevisiae. Cell. 1988 May 20;53(4):555–566. doi: 10.1016/0092-8674(88)90572-7. [DOI] [PubMed] [Google Scholar]
  6. Carlson M., Botstein D. Two differentially regulated mRNAs with different 5' ends encode secreted with intracellular forms of yeast invertase. Cell. 1982 Jan;28(1):145–154. doi: 10.1016/0092-8674(82)90384-1. [DOI] [PubMed] [Google Scholar]
  7. Cleary M. A., Herr W. Mechanisms for flexibility in DNA sequence recognition and VP16-induced complex formation by the Oct-1 POU domain. Mol Cell Biol. 1995 Apr;15(4):2090–2100. doi: 10.1128/mcb.15.4.2090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. De Rijcke M., Seneca S., Punyammalee B., Glansdorff N., Crabeel M. Characterization of the DNA target site for the yeast ARGR regulatory complex, a sequence able to mediate repression or induction by arginine. Mol Cell Biol. 1992 Jan;12(1):68–81. doi: 10.1128/mcb.12.1.68. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Einerhand A. W., Kos W., Smart W. C., Kal A. J., Tabak H. F., Cooper T. G. The upstream region of the FOX3 gene encoding peroxisomal 3-oxoacyl-coenzyme A thiolase in Saccharomyces cerevisiae contains ABF1- and replication protein A-binding sites that participate in its regulation by glucose repression. Mol Cell Biol. 1995 Jun;15(6):3405–3414. doi: 10.1128/mcb.15.6.3405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Flick J. S., Johnston M. Two systems of glucose repression of the GAL1 promoter in Saccharomyces cerevisiae. Mol Cell Biol. 1990 Sep;10(9):4757–4769. doi: 10.1128/mcb.10.9.4757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. François J., Eraso P., Gancedo C. Changes in the concentration of cAMP, fructose 2,6-bisphosphate and related metabolites and enzymes in Saccharomyces cerevisiae during growth on glucose. Eur J Biochem. 1987 Apr 15;164(2):369–373. doi: 10.1111/j.1432-1033.1987.tb11067.x. [DOI] [PubMed] [Google Scholar]
  12. Gardner K. H., Anderson S. F., Coleman J. E. Solution structure of the Kluyveromyces lactis LAC9 Cd2 Cys6 DNA-binding domain. Nat Struct Biol. 1995 Oct;2(10):898–905. doi: 10.1038/nsb1095-898. [DOI] [PubMed] [Google Scholar]
  13. Hamil K. G., Nam H. G., Fried H. M. Constitutive transcription of yeast ribosomal protein gene TCM1 is promoted by uncommon cis- and trans-acting elements. Mol Cell Biol. 1988 Oct;8(10):4328–4341. doi: 10.1128/mcb.8.10.4328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hardy T. A., Huang D., Roach P. J. Interactions between cAMP-dependent and SNF1 protein kinases in the control of glycogen accumulation in Saccharomyces cerevisiae. J Biol Chem. 1994 Nov 11;269(45):27907–27913. [PubMed] [Google Scholar]
  15. Harm W., Harm H., Rupert C. S. Analysis of photoenzymatic repair of UV lesions in DNA by single light flashes. II. In vivo studies with Escherichia coli cells and bacteriophage. Mutat Res. 1968 Nov-Dec;6(3):371–385. doi: 10.1016/0027-5107(68)90054-7. [DOI] [PubMed] [Google Scholar]
  16. Ho Y., Mason S., Kobayashi R., Hoekstra M., Andrews B. Role of the casein kinase I isoform, Hrr25, and the cell cycle-regulatory transcription factor, SBF, in the transcriptional response to DNA damage in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):581–586. doi: 10.1073/pnas.94.2.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jackson J. C., Lopes J. M. The yeast UME6 gene is required for both negative and positive transcriptional regulation of phospholipid biosynthetic gene expression. Nucleic Acids Res. 1996 Apr 1;24(7):1322–1329. doi: 10.1093/nar/24.7.1322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jang Y. K., Jin Y. H., Kim M. J., Seong R. H., Hong S. H., Park S. D. A simple and efficient method for the isolation of total RNA from the fission yeast Schizosaccharomyces pombe. Biochem Mol Biol Int. 1995 Oct;37(2):339–344. [PubMed] [Google Scholar]
  19. Kadosh D., Struhl K. Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell. 1997 May 2;89(3):365–371. doi: 10.1016/s0092-8674(00)80217-2. [DOI] [PubMed] [Google Scholar]
  20. Kassir Y., Granot D., Simchen G. IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell. 1988 Mar 25;52(6):853–862. doi: 10.1016/0092-8674(88)90427-8. [DOI] [PubMed] [Google Scholar]
  21. Kiser G. L., Weinert T. A. Distinct roles of yeast MEC and RAD checkpoint genes in transcriptional induction after DNA damage and implications for function. Mol Biol Cell. 1996 May;7(5):703–718. doi: 10.1091/mbc.7.5.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kriwacki R. W., Hengst L., Tennant L., Reed S. I., Wright P. E. Structural studies of p21Waf1/Cip1/Sdi1 in the free and Cdk2-bound state: conformational disorder mediates binding diversity. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11504–11509. doi: 10.1073/pnas.93.21.11504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lillie S. H., Pringle J. R. Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J Bacteriol. 1980 Sep;143(3):1384–1394. doi: 10.1128/jb.143.3.1384-1394.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Luche R. M., Smart W. C., Cooper T. G. Purification of the heteromeric protein binding to the URS1 transcriptional repression site in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7412–7416. doi: 10.1073/pnas.89.16.7412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Luche R. M., Smart W. C., Marion T., Tillman M., Sumrada R. A., Cooper T. G. Saccharomyces cerevisiae BUF protein binds to sequences participating in DNA replication in addition to those mediating transcriptional repression (URS1) and activation. Mol Cell Biol. 1993 Sep;13(9):5749–5761. doi: 10.1128/mcb.13.9.5749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Luche R. M., Sumrada R., Cooper T. G. A cis-acting element present in multiple genes serves as a repressor protein binding site for the yeast CAR1 gene. Mol Cell Biol. 1990 Aug;10(8):3884–3895. doi: 10.1128/mcb.10.8.3884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Madura K., Prakash S. Nucleotide sequence, transcript mapping, and regulation of the RAD2 gene of Saccharomyces cerevisiae. J Bacteriol. 1986 Jun;166(3):914–923. doi: 10.1128/jb.166.3.914-923.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Marchler G., Schüller C., Adam G., Ruis H. A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions. EMBO J. 1993 May;12(5):1997–2003. doi: 10.1002/j.1460-2075.1993.tb05849.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Marmorstein R., Carey M., Ptashne M., Harrison S. C. DNA recognition by GAL4: structure of a protein-DNA complex. Nature. 1992 Apr 2;356(6368):408–414. doi: 10.1038/356408a0. [DOI] [PubMed] [Google Scholar]
  30. Marmorstein R., Harrison S. C. Crystal structure of a PPR1-DNA complex: DNA recognition by proteins containing a Zn2Cys6 binuclear cluster. Genes Dev. 1994 Oct 15;8(20):2504–2512. doi: 10.1101/gad.8.20.2504. [DOI] [PubMed] [Google Scholar]
  31. Martínez-Pastor M. T., Marchler G., Schüller C., Marchler-Bauer A., Ruis H., Estruch F. The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J. 1996 May 1;15(9):2227–2235. [PMC free article] [PubMed] [Google Scholar]
  32. Matsuura A., Treinin M., Mitsuzawa H., Kassir Y., Uno I., Simchen G. The adenylate cyclase/protein kinase cascade regulates entry into meiosis in Saccharomyces cerevisiae through the gene IME1. EMBO J. 1990 Oct;9(10):3225–3232. doi: 10.1002/j.1460-2075.1990.tb07521.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Misra V., Walter S., Yang P., Hayes S., O'Hare P. Conformational alteration of Oct-1 upon DNA binding dictates selectivity in differential interactions with related transcriptional coactivators. Mol Cell Biol. 1996 Aug;16(8):4404–4413. doi: 10.1128/mcb.16.8.4404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Mitchell A. P. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev. 1994 Mar;58(1):56–70. doi: 10.1128/mr.58.1.56-70.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Mitchell A. P., Driscoll S. E., Smith H. E. Positive control of sporulation-specific genes by the IME1 and IME2 products in Saccharomyces cerevisiae. Mol Cell Biol. 1990 May;10(5):2104–2110. doi: 10.1128/mcb.10.5.2104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Navas T. A., Sanchez Y., Elledge S. J. RAD9 and DNA polymerase epsilon form parallel sensory branches for transducing the DNA damage checkpoint signal in Saccharomyces cerevisiae. Genes Dev. 1996 Oct 15;10(20):2632–2643. doi: 10.1101/gad.10.20.2632. [DOI] [PubMed] [Google Scholar]
  37. Park H. D., Luche R. M., Cooper T. G. The yeast UME6 gene product is required for transcriptional repression mediated by the CAR1 URS1 repressor binding site. Nucleic Acids Res. 1992 Apr 25;20(8):1909–1915. doi: 10.1093/nar/20.8.1909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Perozzi G., Prakash S. RAD7 gene of Saccharomyces cerevisiae: transcripts, nucleotide sequence analysis, and functional relationship between the RAD7 and RAD23 gene products. Mol Cell Biol. 1986 May;6(5):1497–1507. doi: 10.1128/mcb.6.5.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Pfeifer K., Kim K. S., Kogan S., Guarente L. Functional dissection and sequence of yeast HAP1 activator. Cell. 1989 Jan 27;56(2):291–301. doi: 10.1016/0092-8674(89)90903-3. [DOI] [PubMed] [Google Scholar]
  40. Rubin-Bejerano I., Mandel S., Robzyk K., Kassir Y. Induction of meiosis in Saccharomyces cerevisiae depends on conversion of the transcriptional represssor Ume6 to a positive regulator by its regulated association with the transcriptional activator Ime1. Mol Cell Biol. 1996 May;16(5):2518–2526. doi: 10.1128/mcb.16.5.2518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sancar G. B., Ferris R., Smith F. W., Vandeberg B. Promoter elements of the PHR1 gene of Saccharomyces cerevisiae and their roles in the response to DNA damage. Nucleic Acids Res. 1995 Nov 11;23(21):4320–4328. doi: 10.1093/nar/23.21.4320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sancar G. B. Sequence of the Saccharomyces cerevisiae PHR1 gene and homology of the PHR1 photolyase to E. coli photolyase. Nucleic Acids Res. 1985 Nov 25;13(22):8231–8246. doi: 10.1093/nar/13.22.8231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sancar G. B., Smith F. W. Interactions between yeast photolyase and nucleotide excision repair proteins in Saccharomyces cerevisiae and Escherichia coli. Mol Cell Biol. 1989 Nov;9(11):4767–4776. doi: 10.1128/mcb.9.11.4767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Schmitt A. P., McEntee K. Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):5777–5782. doi: 10.1073/pnas.93.12.5777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Sebastian J., Kraus B., Sancar G. B. Expression of the yeast PHR1 gene is induced by DNA-damaging agents. Mol Cell Biol. 1990 Sep;10(9):4630–4637. doi: 10.1128/mcb.10.9.4630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sebastian J., Sancar G. B. A damage-responsive DNA binding protein regulates transcription of the yeast DNA repair gene PHR1. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11251–11255. doi: 10.1073/pnas.88.24.11251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Shiozaki K., Russell P. Conjugation, meiosis, and the osmotic stress response are regulated by Spc1 kinase through Atf1 transcription factor in fission yeast. Genes Dev. 1996 Sep 15;10(18):2276–2288. doi: 10.1101/gad.10.18.2276. [DOI] [PubMed] [Google Scholar]
  48. Siede W., Robinson G. W., Kalainov D., Malley T., Friedberg E. C. Regulation of the RAD2 gene of Saccharomyces cerevisiae. Mol Microbiol. 1989 Dec;3(12):1697–1707. doi: 10.1111/j.1365-2958.1989.tb00155.x. [DOI] [PubMed] [Google Scholar]
  49. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Singh K. K., Samson L. Replication protein A binds to regulatory elements in yeast DNA repair and DNA metabolism genes. Proc Natl Acad Sci U S A. 1995 May 23;92(11):4907–4911. doi: 10.1073/pnas.92.11.4907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Steber C. M., Esposito R. E. UME6 is a central component of a developmental regulatory switch controlling meiosis-specific gene expression. Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):12490–12494. doi: 10.1073/pnas.92.26.12490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Strich R., Slater M. R., Esposito R. E. Identification of negative regulatory genes that govern the expression of early meiotic genes in yeast. Proc Natl Acad Sci U S A. 1989 Dec;86(24):10018–10022. doi: 10.1073/pnas.86.24.10018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Strich R., Surosky R. T., Steber C., Dubois E., Messenguy F., Esposito R. E. UME6 is a key regulator of nitrogen repression and meiotic development. Genes Dev. 1994 Apr 1;8(7):796–810. doi: 10.1101/gad.8.7.796. [DOI] [PubMed] [Google Scholar]
  54. Sun Z., Fay D. S., Marini F., Foiani M., Stern D. F. Spk1/Rad53 is regulated by Mec1-dependent protein phosphorylation in DNA replication and damage checkpoint pathways. Genes Dev. 1996 Feb 15;10(4):395–406. doi: 10.1101/gad.10.4.395. [DOI] [PubMed] [Google Scholar]
  55. Szent-Gyorgyi C. A bipartite operator interacts with a heat shock element to mediate early meiotic induction of Saccharomyces cerevisiae HSP82. Mol Cell Biol. 1995 Dec;15(12):6754–6769. doi: 10.1128/mcb.15.12.6754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Takeda T., Toda T., Kominami K., Kohnosu A., Yanagida M., Jones N. Schizosaccharomyces pombe atf1+ encodes a transcription factor required for sexual development and entry into stationary phase. EMBO J. 1995 Dec 15;14(24):6193–6208. doi: 10.1002/j.1460-2075.1995.tb00310.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Tan S., Richmond T. J. DNA binding-induced conformational change of the yeast transcriptional activator PRTF. Cell. 1990 Jul 27;62(2):367–377. doi: 10.1016/0092-8674(90)90373-m. [DOI] [PubMed] [Google Scholar]
  58. Thompson-Jaeger S., François J., Gaughran J. P., Tatchell K. Deletion of SNF1 affects the nutrient response of yeast and resembles mutations which activate the adenylate cyclase pathway. Genetics. 1991 Nov;129(3):697–706. doi: 10.1093/genetics/129.3.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Unrau P., Wheatcroft R., Cox B., Olive T. The formation of pyrimidine dimers in the DNA of fungi and bacteria. Biochim Biophys Acta. 1973 Jul 27;312(4):626–632. doi: 10.1016/0005-2787(73)90065-8. [DOI] [PubMed] [Google Scholar]
  60. Vidal M., Buckley A. M., Yohn C., Hoeppner D. J., Gaber R. F. Identification of essential nucleotides in an upstream repressing sequence of Saccharomyces cerevisiae by selection for increased expression of TRK2. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2370–2374. doi: 10.1073/pnas.92.6.2370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Werner-Washburne M., Braun E., Johnston G. C., Singer R. A. Stationary phase in the yeast Saccharomyces cerevisiae. Microbiol Rev. 1993 Jun;57(2):383–401. doi: 10.1128/mr.57.2.383-401.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Xiao W., Singh K. K., Chen B., Samson L. A common element involved in transcriptional regulation of two DNA alkylation repair genes (MAG and MGT1) of Saccharomyces cerevisiae. Mol Cell Biol. 1993 Dec;13(12):7213–7221. doi: 10.1128/mcb.13.12.7213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Yasui A., Laskowski W. Determination of the number of photoreactivating enzyme molecules per haploid Saccharomyces cells. Int J Radiat Biol Relat Stud Phys Chem Med. 1975 Dec;28(6):511–518. doi: 10.1080/09553007514551371. [DOI] [PubMed] [Google Scholar]
  64. Zhang L., Guarente L. The yeast activator HAP1--a GAL4 family member--binds DNA in a directly repeated orientation. Genes Dev. 1994 Sep 1;8(17):2110–2119. doi: 10.1101/gad.8.17.2110. [DOI] [PubMed] [Google Scholar]
  65. Zheng P., Fay D. S., Burton J., Xiao H., Pinkham J. L., Stern D. F. SPK1 is an essential S-phase-specific gene of Saccharomyces cerevisiae that encodes a nuclear serine/threonine/tyrosine kinase. Mol Cell Biol. 1993 Sep;13(9):5829–5842. doi: 10.1128/mcb.13.9.5829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Zhou Z., Elledge S. J. DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell. 1993 Dec 17;75(6):1119–1127. doi: 10.1016/0092-8674(93)90321-g. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES