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. 1998 Sep 1;17(17):5026–5036. doi: 10.1093/emboj/17.17.5026

Cell-cycle arrest and inhibition of G1 cyclin translation by iron in AFT1-1(up) yeast.

C C Philpott 1, J Rashford 1, Y Yamaguchi-Iwai 1, T A Rouault 1, A Dancis 1, R D Klausner 1
PMCID: PMC1170830  PMID: 9724638

Abstract

Although iron is an essential nutrient, it is also a potent cellular toxin, and the acquisition of iron is a highly regulated process in eukaryotes. In yeast, iron uptake is homeostatically regulated by the transcription factor encoded by AFT1. Expression of AFT1-1(up), a dominant mutant allele, results in inappropriately high rates of iron uptake, and AFT1-1(up) mutants grow slowly in the presence of high concentrations of iron. We present evidence that when Aft1-1(up) mutants are exposed to iron, they arrest the cell division cycle at the G1 regulatory point Start. This arrest is dependent on high-affinity iron uptake and does not require the activation of the DNA damage checkpoint governed by RAD9. The iron-induced arrest is bypassed by overexpression of a mutant G1 cyclin, cln3-2, and expression of the G1-specific cyclins Cln1 and Cln2 is reduced when yeast are exposed to increasing amounts of iron, which may account for the arrest. This reduction is not due to changes in transcription of CLN1 or CLN2, nor is it due to accelerated degradation of the protein. Instead, this reduction occurs at the level of Cln2 translation, a recently recognized locus of cell-cycle control in yeast.

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Selected References

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  1. Askwith C., Eide D., Van Ho A., Bernard P. S., Li L., Davis-Kaplan S., Sipe D. M., Kaplan J. The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell. 1994 Jan 28;76(2):403–410. doi: 10.1016/0092-8674(94)90346-8. [DOI] [PubMed] [Google Scholar]
  2. Bai C., Sen P., Hofmann K., Ma L., Goebl M., Harper J. W., Elledge S. J. SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell. 1996 Jul 26;86(2):263–274. doi: 10.1016/s0092-8674(00)80098-7. [DOI] [PubMed] [Google Scholar]
  3. Bailey R. B., Woodword A. Isolation and characterization of a pleiotropic glucose repression resistant mutant of Saccharomyces cerevisiae. Mol Gen Genet. 1984;193(3):507–512. doi: 10.1007/BF00382091. [DOI] [PubMed] [Google Scholar]
  4. Barbet N. C., Schneider U., Helliwell S. B., Stansfield I., Tuite M. F., Hall M. N. TOR controls translation initiation and early G1 progression in yeast. Mol Biol Cell. 1996 Jan;7(1):25–42. doi: 10.1091/mbc.7.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baroni M. D., Monti P., Alberghina L. Repression of growth-regulated G1 cyclin expression by cyclic AMP in budding yeast. Nature. 1994 Sep 22;371(6495):339–342. doi: 10.1038/371339a0. [DOI] [PubMed] [Google Scholar]
  6. Barral Y., Jentsch S., Mann C. G1 cyclin turnover and nutrient uptake are controlled by a common pathway in yeast. Genes Dev. 1995 Feb 15;9(4):399–409. doi: 10.1101/gad.9.4.399. [DOI] [PubMed] [Google Scholar]
  7. Berlett B. S., Stadtman E. R. Protein oxidation in aging, disease, and oxidative stress. J Biol Chem. 1997 Aug 15;272(33):20313–20316. doi: 10.1074/jbc.272.33.20313. [DOI] [PubMed] [Google Scholar]
  8. Blondel M., Mann C. G2 cyclins are required for the degradation of G1 cyclins in yeast. Nature. 1996 Nov 21;384(6606):279–282. doi: 10.1038/384279a0. [DOI] [PubMed] [Google Scholar]
  9. Brennan R. J., Swoboda B. E., Schiestl R. H. Oxidative mutagens induce intrachromosomal recombination in yeast. Mutat Res. 1994 Jul 16;308(2):159–167. doi: 10.1016/0027-5107(94)90151-1. [DOI] [PubMed] [Google Scholar]
  10. Brenner C., Nakayama N., Goebl M., Tanaka K., Toh-e A., Matsumoto K. CDC33 encodes mRNA cap-binding protein eIF-4E of Saccharomyces cerevisiae. Mol Cell Biol. 1988 Aug;8(8):3556–3559. doi: 10.1128/mcb.8.8.3556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cross F. R. Cell cycle arrest caused by CLN gene deficiency in Saccharomyces cerevisiae resembles START-I arrest and is independent of the mating-pheromone signalling pathway. Mol Cell Biol. 1990 Dec;10(12):6482–6490. doi: 10.1128/mcb.10.12.6482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cross F. R. DAF1, a mutant gene affecting size control, pheromone arrest, and cell cycle kinetics of Saccharomyces cerevisiae. Mol Cell Biol. 1988 Nov;8(11):4675–4684. doi: 10.1128/mcb.8.11.4675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cross F. R., Hoek M., McKinney J. D., Tinkelenberg A. H. Role of Swi4 in cell cycle regulation of CLN2 expression. Mol Cell Biol. 1994 Jul;14(7):4779–4787. doi: 10.1128/mcb.14.7.4779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cross F. R. Starting the cell cycle: what's the point? Curr Opin Cell Biol. 1995 Dec;7(6):790–797. doi: 10.1016/0955-0674(95)80062-x. [DOI] [PubMed] [Google Scholar]
  15. Dancis A., Haile D., Yuan D. S., Klausner R. D. The Saccharomyces cerevisiae copper transport protein (Ctr1p). Biochemical characterization, regulation by copper, and physiologic role in copper uptake. J Biol Chem. 1994 Oct 14;269(41):25660–25667. [PubMed] [Google Scholar]
  16. Dancis A., Klausner R. D., Hinnebusch A. G., Barriocanal J. G. Genetic evidence that ferric reductase is required for iron uptake in Saccharomyces cerevisiae. Mol Cell Biol. 1990 May;10(5):2294–2301. doi: 10.1128/mcb.10.5.2294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dancis A., Roman D. G., Anderson G. J., Hinnebusch A. G., Klausner R. D. Ferric reductase of Saccharomyces cerevisiae: molecular characterization, role in iron uptake, and transcriptional control by iron. Proc Natl Acad Sci U S A. 1992 May 1;89(9):3869–3873. doi: 10.1073/pnas.89.9.3869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Deshaies R. J., Chau V., Kirschner M. Ubiquitination of the G1 cyclin Cln2p by a Cdc34p-dependent pathway. EMBO J. 1995 Jan 16;14(2):303–312. doi: 10.1002/j.1460-2075.1995.tb07004.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dirick L., Böhm T., Nasmyth K. Roles and regulation of Cln-Cdc28 kinases at the start of the cell cycle of Saccharomyces cerevisiae. EMBO J. 1995 Oct 2;14(19):4803–4813. doi: 10.1002/j.1460-2075.1995.tb00162.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Dix D. R., Bridgham J. T., Broderius M. A., Byersdorfer C. A., Eide D. J. The FET4 gene encodes the low affinity Fe(II) transport protein of Saccharomyces cerevisiae. J Biol Chem. 1994 Oct 21;269(42):26092–26099. [PubMed] [Google Scholar]
  21. Dix D., Bridgham J., Broderius M., Eide D. Characterization of the FET4 protein of yeast. Evidence for a direct role in the transport of iron. J Biol Chem. 1997 May 2;272(18):11770–11777. doi: 10.1074/jbc.272.18.11770. [DOI] [PubMed] [Google Scholar]
  22. Espinoza F. H., Ogas J., Herskowitz I., Morgan D. O. Cell cycle control by a complex of the cyclin HCS26 (PCL1) and the kinase PHO85. Science. 1994 Nov 25;266(5189):1388–1391. doi: 10.1126/science.7973730. [DOI] [PubMed] [Google Scholar]
  23. Farr S. B., D'Ari R., Touati D. Oxygen-dependent mutagenesis in Escherichia coli lacking superoxide dismutase. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8268–8272. doi: 10.1073/pnas.83.21.8268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Flick J. S., Johnston M. GRR1 of Saccharomyces cerevisiae is required for glucose repression and encodes a protein with leucine-rich repeats. Mol Cell Biol. 1991 Oct;11(10):5101–5112. doi: 10.1128/mcb.11.10.5101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gallego C., Garí E., Colomina N., Herrero E., Aldea M. The Cln3 cyclin is down-regulated by translational repression and degradation during the G1 arrest caused by nitrogen deprivation in budding yeast. EMBO J. 1997 Dec 1;16(23):7196–7206. doi: 10.1093/emboj/16.23.7196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Georgatsou E., Alexandraki D. Two distinctly regulated genes are required for ferric reduction, the first step of iron uptake in Saccharomyces cerevisiae. Mol Cell Biol. 1994 May;14(5):3065–3073. doi: 10.1128/mcb.14.5.3065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Gerlach M., Ben-Shachar D., Riederer P., Youdim M. B. Altered brain metabolism of iron as a cause of neurodegenerative diseases? J Neurochem. 1994 Sep;63(3):793–807. doi: 10.1046/j.1471-4159.1994.63030793.x. [DOI] [PubMed] [Google Scholar]
  28. Gorell J. M., Johnson C. C., Rybicki B. A., Peterson E. L., Kortsha G. X., Brown G. G., Richardson R. J. Occupational exposures to metals as risk factors for Parkinson's disease. Neurology. 1997 Mar;48(3):650–658. doi: 10.1212/wnl.48.3.650. [DOI] [PubMed] [Google Scholar]
  29. Gralla E. B., Valentine J. S. Null mutants of Saccharomyces cerevisiae Cu,Zn superoxide dismutase: characterization and spontaneous mutation rates. J Bacteriol. 1991 Sep;173(18):5918–5920. doi: 10.1128/jb.173.18.5918-5920.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hadwiger J. A., Wittenberg C., Richardson H. E., de Barros Lopes M., Reed S. I. A family of cyclin homologs that control the G1 phase in yeast. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6255–6259. doi: 10.1073/pnas.86.16.6255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hanic-Joyce P. J., Johnston G. C., Singer R. A. Regulated arrest of cell proliferation mediated by yeast prt1 mutations. Exp Cell Res. 1987 Sep;172(1):134–145. doi: 10.1016/0014-4827(87)90100-5. [DOI] [PubMed] [Google Scholar]
  32. Imlay J. A., Chin S. M., Linn S. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science. 1988 Apr 29;240(4852):640–642. doi: 10.1126/science.2834821. [DOI] [PubMed] [Google Scholar]
  33. Iwai K., Drake S. K., Wehr N. B., Weissman A. M., LaVaute T., Minato N., Klausner R. D., Levine R. L., Rouault T. A. Iron-dependent oxidation, ubiquitination, and degradation of iron regulatory protein 2: implications for degradation of oxidized proteins. Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):4924–4928. doi: 10.1073/pnas.95.9.4924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Jenner P. Oxidative stress in Parkinson's disease and other neurodegenerative disorders. Pathol Biol (Paris) 1996 Jan;44(1):57–64. [PubMed] [Google Scholar]
  35. Keyer K., Gort A. S., Imlay J. A. Superoxide and the production of oxidative DNA damage. J Bacteriol. 1995 Dec;177(23):6782–6790. doi: 10.1128/jb.177.23.6782-6790.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Keyer K., Imlay J. A. Superoxide accelerates DNA damage by elevating free-iron levels. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13635–13640. doi: 10.1073/pnas.93.24.13635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kienzl E., Puchinger L., Jellinger K., Linert W., Stachelberger H., Jameson R. F. The role of transition metals in the pathogenesis of Parkinson's disease. J Neurol Sci. 1995 Dec;134 (Suppl):69–78. doi: 10.1016/0022-510x(95)00210-s. [DOI] [PubMed] [Google Scholar]
  38. King R. W., Deshaies R. J., Peters J. M., Kirschner M. W. How proteolysis drives the cell cycle. Science. 1996 Dec 6;274(5293):1652–1659. doi: 10.1126/science.274.5293.1652. [DOI] [PubMed] [Google Scholar]
  39. Lanker S., Valdivieso M. H., Wittenberg C. Rapid degradation of the G1 cyclin Cln2 induced by CDK-dependent phosphorylation. Science. 1996 Mar 15;271(5255):1597–1601. doi: 10.1126/science.271.5255.1597. [DOI] [PubMed] [Google Scholar]
  40. Lee J., Romeo A., Kosman D. J. Transcriptional remodeling and G1 arrest in dioxygen stress in Saccharomyces cerevisiae. J Biol Chem. 1996 Oct 4;271(40):24885–24893. doi: 10.1074/jbc.271.40.24885. [DOI] [PubMed] [Google Scholar]
  41. Li F. N., Johnston M. Grr1 of Saccharomyces cerevisiae is connected to the ubiquitin proteolysis machinery through Skp1: coupling glucose sensing to gene expression and the cell cycle. EMBO J. 1997 Sep 15;16(18):5629–5638. doi: 10.1093/emboj/16.18.5629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Liu H., Krizek J., Bretscher A. Construction of a GAL1-regulated yeast cDNA expression library and its application to the identification of genes whose overexpression causes lethality in yeast. Genetics. 1992 Nov;132(3):665–673. doi: 10.1093/genetics/132.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lydall D., Weinert T. From DNA damage to cell cycle arrest and suicide: a budding yeast perspective. Curr Opin Genet Dev. 1996 Feb;6(1):4–11. doi: 10.1016/s0959-437x(96)90003-9. [DOI] [PubMed] [Google Scholar]
  44. Mathias N., Johnson S. L., Winey M., Adams A. E., Goetsch L., Pringle J. R., Byers B., Goebl M. G. Cdc53p acts in concert with Cdc4p and Cdc34p to control the G1-to-S-phase transition and identifies a conserved family of proteins. Mol Cell Biol. 1996 Dec;16(12):6634–6643. doi: 10.1128/mcb.16.12.6634. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Montgomery E. B., Jr Heavy metals and the etiology of Parkinson's disease and other movement disorders. Toxicology. 1995 Mar 31;97(1-3):3–9. doi: 10.1016/0300-483x(94)02962-t. [DOI] [PubMed] [Google Scholar]
  46. Naranda T., MacMillan S. E., Hershey J. W. Purified yeast translational initiation factor eIF-3 is an RNA-binding protein complex that contains the PRT1 protein. J Biol Chem. 1994 Dec 23;269(51):32286–32292. [PubMed] [Google Scholar]
  47. Nasmyth K. At the heart of the budding yeast cell cycle. Trends Genet. 1996 Oct;12(10):405–412. doi: 10.1016/0168-9525(96)10041-x. [DOI] [PubMed] [Google Scholar]
  48. Nasmyth K. Control of the yeast cell cycle by the Cdc28 protein kinase. Curr Opin Cell Biol. 1993 Apr;5(2):166–179. doi: 10.1016/0955-0674(93)90099-c. [DOI] [PubMed] [Google Scholar]
  49. Nasmyth K., Dirick L. The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast. Cell. 1991 Sep 6;66(5):995–1013. doi: 10.1016/0092-8674(91)90444-4. [DOI] [PubMed] [Google Scholar]
  50. Nunes E., Siede W. Hyperthermia and paraquat-induced G1 arrest in the yeast Saccharomyces cerevisiae is independent of the RAD9 gene. Radiat Environ Biophys. 1996 Feb;35(1):55–57. doi: 10.1007/BF01211243. [DOI] [PubMed] [Google Scholar]
  51. Ogas J., Andrews B. J., Herskowitz I. Transcriptional activation of CLN1, CLN2, and a putative new G1 cyclin (HCS26) by SWI4, a positive regulator of G1-specific transcription. Cell. 1991 Sep 6;66(5):1015–1026. doi: 10.1016/0092-8674(91)90445-5. [DOI] [PubMed] [Google Scholar]
  52. Peter M., Herskowitz I. Joining the complex: cyclin-dependent kinase inhibitory proteins and the cell cycle. Cell. 1994 Oct 21;79(2):181–184. doi: 10.1016/0092-8674(94)90186-4. [DOI] [PubMed] [Google Scholar]
  53. Polymenis M., Schmidt E. V. Coupling of cell division to cell growth by translational control of the G1 cyclin CLN3 in yeast. Genes Dev. 1997 Oct 1;11(19):2522–2531. doi: 10.1101/gad.11.19.2522. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Richardson H. E., Wittenberg C., Cross F., Reed S. I. An essential G1 function for cyclin-like proteins in yeast. Cell. 1989 Dec 22;59(6):1127–1133. doi: 10.1016/0092-8674(89)90768-x. [DOI] [PubMed] [Google Scholar]
  55. Rosenwald I. B., Kaspar R., Rousseau D., Gehrke L., Leboulch P., Chen J. J., Schmidt E. V., Sonenberg N., London I. M. Eukaryotic translation initiation factor 4E regulates expression of cyclin D1 at transcriptional and post-transcriptional levels. J Biol Chem. 1995 Sep 8;270(36):21176–21180. doi: 10.1074/jbc.270.36.21176. [DOI] [PubMed] [Google Scholar]
  56. Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. doi: 10.1016/0076-6879(91)94022-5. [DOI] [PubMed] [Google Scholar]
  57. Rouault T. A., Klausner R. D. The impact of oxidative stress on eukaryotic iron metabolism. EXS. 1996;77:183–197. doi: 10.1007/978-3-0348-9088-5_12. [DOI] [PubMed] [Google Scholar]
  58. Rowley A., Johnston G. C., Butler B., Werner-Washburne M., Singer R. A. Heat shock-mediated cell cycle blockage and G1 cyclin expression in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1993 Feb;13(2):1034–1041. doi: 10.1128/mcb.13.2.1034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Schiestl R. H., Reynolds P., Prakash S., Prakash L. Cloning and sequence analysis of the Saccharomyces cerevisiae RAD9 gene and further evidence that its product is required for cell cycle arrest induced by DNA damage. Mol Cell Biol. 1989 May;9(5):1882–1896. doi: 10.1128/mcb.9.5.1882. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Shen W. C., Green M. R. Yeast TAF(II)145 functions as a core promoter selectivity factor, not a general coactivator. Cell. 1997 Aug 22;90(4):615–624. doi: 10.1016/s0092-8674(00)80523-1. [DOI] [PubMed] [Google Scholar]
  61. Sherr C. J. G1 phase progression: cycling on cue. Cell. 1994 Nov 18;79(4):551–555. doi: 10.1016/0092-8674(94)90540-1. [DOI] [PubMed] [Google Scholar]
  62. Sidorova J. M., Breeden L. L. Rad53-dependent phosphorylation of Swi6 and down-regulation of CLN1 and CLN2 transcription occur in response to DNA damage in Saccharomyces cerevisiae. Genes Dev. 1997 Nov 15;11(22):3032–3045. doi: 10.1101/gad.11.22.3032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Siede W., Friedberg A. S., Friedberg E. C. RAD9-dependent G1 arrest defines a second checkpoint for damaged DNA in the cell cycle of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):7985–7989. doi: 10.1073/pnas.90.17.7985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Sikorski R. S., Boeke J. D. In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast. Methods Enzymol. 1991;194:302–318. doi: 10.1016/0076-6879(91)94023-6. [DOI] [PubMed] [Google Scholar]
  65. 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]
  66. Skowyra D., Craig K. L., Tyers M., Elledge S. J., Harper J. W. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell. 1997 Oct 17;91(2):209–219. doi: 10.1016/s0092-8674(00)80403-1. [DOI] [PubMed] [Google Scholar]
  67. Sofic E., Paulus W., Jellinger K., Riederer P., Youdim M. B. Selective increase of iron in substantia nigra zona compacta of parkinsonian brains. J Neurochem. 1991 Mar;56(3):978–982. doi: 10.1111/j.1471-4159.1991.tb02017.x. [DOI] [PubMed] [Google Scholar]
  68. Sonenberg N. Regulation of translation and cell growth by eIF-4E. Biochimie. 1994;76(9):839–846. doi: 10.1016/0300-9084(94)90185-6. [DOI] [PubMed] [Google Scholar]
  69. Stearman R., Yuan D. S., Yamaguchi-Iwai Y., Klausner R. D., Dancis A. A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science. 1996 Mar 15;271(5255):1552–1557. doi: 10.1126/science.271.5255.1552. [DOI] [PubMed] [Google Scholar]
  70. Stuart D., Wittenberg C. Cell cycle-dependent transcription of CLN2 is conferred by multiple distinct cis-acting regulatory elements. Mol Cell Biol. 1994 Jul;14(7):4788–4801. doi: 10.1128/mcb.14.7.4788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Tokiwa G., Tyers M., Volpe T., Futcher B. Inhibition of G1 cyclin activity by the Ras/cAMP pathway in yeast. Nature. 1994 Sep 22;371(6495):342–345. doi: 10.1038/371342a0. [DOI] [PubMed] [Google Scholar]
  72. Touati D., Jacques M., Tardat B., Bouchard L., Despied S. Lethal oxidative damage and mutagenesis are generated by iron in delta fur mutants of Escherichia coli: protective role of superoxide dismutase. J Bacteriol. 1995 May;177(9):2305–2314. doi: 10.1128/jb.177.9.2305-2314.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Tyers M., Tokiwa G., Futcher B. Comparison of the Saccharomyces cerevisiae G1 cyclins: Cln3 may be an upstream activator of Cln1, Cln2 and other cyclins. EMBO J. 1993 May;12(5):1955–1968. doi: 10.1002/j.1460-2075.1993.tb05845.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Tyers M., Tokiwa G., Nash R., Futcher B. The Cln3-Cdc28 kinase complex of S. cerevisiae is regulated by proteolysis and phosphorylation. EMBO J. 1992 May;11(5):1773–1784. doi: 10.1002/j.1460-2075.1992.tb05229.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Walker S. S., Shen W. C., Reese J. C., Apone L. M., Green M. R. Yeast TAF(II)145 required for transcription of G1/S cyclin genes and regulated by the cellular growth state. Cell. 1997 Aug 22;90(4):607–614. doi: 10.1016/s0092-8674(00)80522-x. [DOI] [PubMed] [Google Scholar]
  76. Watt F. Nuclear microscope analysis in Alzheimer's and Parkinson's disease: A review. Cell Mol Biol (Noisy-le-grand) 1996 Feb;42(1):17–26. [PubMed] [Google Scholar]
  77. Willems A. R., Lanker S., Patton E. E., Craig K. L., Nason T. F., Mathias N., Kobayashi R., Wittenberg C., Tyers M. Cdc53 targets phosphorylated G1 cyclins for degradation by the ubiquitin proteolytic pathway. Cell. 1996 Aug 9;86(3):453–463. doi: 10.1016/s0092-8674(00)80118-x. [DOI] [PubMed] [Google Scholar]
  78. Yamaguchi-Iwai Y., Dancis A., Klausner R. D. AFT1: a mediator of iron regulated transcriptional control in Saccharomyces cerevisiae. EMBO J. 1995 Mar 15;14(6):1231–1239. doi: 10.1002/j.1460-2075.1995.tb07106.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Yamaguchi-Iwai Y., Stearman R., Dancis A., Klausner R. D. Iron-regulated DNA binding by the AFT1 protein controls the iron regulon in yeast. EMBO J. 1996 Jul 1;15(13):3377–3384. [PMC free article] [PubMed] [Google Scholar]
  80. Zhu Z., Thiele D. J. Toxic metal-responsive gene transcription. EXS. 1996;77:307–320. doi: 10.1007/978-3-0348-9088-5_20. [DOI] [PubMed] [Google Scholar]

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