Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1996 Oct;16(10):5375–5385. doi: 10.1128/mcb.16.10.5375

Prenylated isoforms of yeast casein kinase I, including the novel Yck3p, suppress the gcs1 blockage of cell proliferation from stationary phase.

X Wang 1, M F Hoekstra 1, A J DeMaggio 1, N Dhillon 1, A Vancura 1, J Kuret 1, G C Johnston 1, R A Singer 1
PMCID: PMC231536  PMID: 8816449

Abstract

The GCS1 gene of the budding yeast Saccharomyces cerevisiae mediate the resumption of cell proliferation from the starved, stationary-phase state. Here we identify yeast genes that, in increased dosages, overcome the growth defect of gcs1 delta mutant cells. Among these are YCK1 (CK12) and YCK2 (CKI1), encoding membrane-associated casein kinase I, and YCK3, encoding a novel casein kinase I isoform. Some Yck3p gene product was found associated with the plasma membrane, like Yck1p and Yck2p, but most confractionated with the nucleus, like another yeast casein kinase I isoform, Hrr25p. Genetic studies showed that YCK3 and HRR25 constitute an essential gene family and that Yck3p can weakly substitute for Yck1p-Yck2p. For gcs1 delta suppression, both a protein kinase domain and a C-terminal prenylation motif were shown to be necessary. An impairment in endocytosis was found for gcs1 delta mutant cells, which was alleviated by an increased YCK2 gene dosage. The ability of an increased casein kinase I gene dosage to suppress the effects caused by the absence of Gcs1p suggests that Gcs1p and Yck1p-Yck2p affect parallel pathways.

Full Text

The Full Text of this article is available as a PDF (511.6 KB).

Selected References

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

  1. Ballou C. E., Maitra S. K., Walker J. W., Whelan W. L. Developmental defects associated with glucosamine auxotrophy in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4351–4355. doi: 10.1073/pnas.74.10.4351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brewster J. L., de Valoir T., Dwyer N. D., Winter E., Gustin M. C. An osmosensing signal transduction pathway in yeast. Science. 1993 Mar 19;259(5102):1760–1763. doi: 10.1126/science.7681220. [DOI] [PubMed] [Google Scholar]
  3. Briza P., Breitenbach M., Ellinger A., Segall J. Isolation of two developmentally regulated genes involved in spore wall maturation in Saccharomyces cerevisiae. Genes Dev. 1990 Oct;4(10):1775–1789. doi: 10.1101/gad.4.10.1775. [DOI] [PubMed] [Google Scholar]
  4. Brockman J. L., Gross S. D., Sussman M. R., Anderson R. A. Cell cycle-dependent localization of casein kinase I to mitotic spindles. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9454–9458. doi: 10.1073/pnas.89.20.9454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Celenza J. L., Carlson M. A yeast gene that is essential for release from glucose repression encodes a protein kinase. Science. 1986 Sep 12;233(4769):1175–1180. doi: 10.1126/science.3526554. [DOI] [PubMed] [Google Scholar]
  6. Celenza J. L., Carlson M. Mutational analysis of the Saccharomyces cerevisiae SNF1 protein kinase and evidence for functional interaction with the SNF4 protein. Mol Cell Biol. 1989 Nov;9(11):5034–5044. doi: 10.1128/mcb.9.11.5034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Celenza J. L., Eng F. J., Carlson M. Molecular analysis of the SNF4 gene of Saccharomyces cerevisiae: evidence for physical association of the SNF4 protein with the SNF1 protein kinase. Mol Cell Biol. 1989 Nov;9(11):5045–5054. doi: 10.1128/mcb.9.11.5045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cesarone C. F., Bolognesi C., Santi L. Improved microfluorometric DNA determination in biological material using 33258 Hoechst. Anal Biochem. 1979 Nov 15;100(1):188–197. doi: 10.1016/0003-2697(79)90131-3. [DOI] [PubMed] [Google Scholar]
  9. Cukierman E., Huber I., Rotman M., Cassel D. The ARF1 GTPase-activating protein: zinc finger motif and Golgi complex localization. Science. 1995 Dec 22;270(5244):1999–2002. doi: 10.1126/science.270.5244.1999. [DOI] [PubMed] [Google Scholar]
  10. DeMaggio A. J., Lindberg R. A., Hunter T., Hoekstra M. F. The budding yeast HRR25 gene product is a casein kinase I isoform. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7008–7012. doi: 10.1073/pnas.89.15.7008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Depaoli-Roach A. A., Park I. K., Cerovsky V., Csortos C., Durbin S. D., Kuntz M. J., Sitikov A., Tang P. M., Verin A., Zolnierowicz S. Serine/threonine protein phosphatases in the control of cell function. Adv Enzyme Regul. 1994;34:199–224. doi: 10.1016/0065-2571(94)90017-5. [DOI] [PubMed] [Google Scholar]
  12. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dhillon N., Hoekstra M. F. Characterization of two protein kinases from Schizosaccharomyces pombe involved in the regulation of DNA repair. EMBO J. 1994 Jun 15;13(12):2777–2788. doi: 10.1002/j.1460-2075.1994.tb06571.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Drebot M. A., Barnes C. A., Singer R. A., Johnston G. C. Genetic assessment of stationary phase for cells of the yeast Saccharomyces cerevisiae. J Bacteriol. 1990 Jul;172(7):3584–3589. doi: 10.1128/jb.172.7.3584-3589.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Drebot M. A., Johnston G. C., Singer R. A. A yeast mutant conditionally defective only for reentry into the mitotic cell cycle from stationary phase. Proc Natl Acad Sci U S A. 1987 Nov;84(22):7948–7952. doi: 10.1073/pnas.84.22.7948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Drebot M. A., Veinot-Drebot L. M., Singer R. A., Johnston G. C. Induction of yeast histone genes by stimulation of stationary-phase cells. Mol Cell Biol. 1990 Dec;10(12):6356–6361. doi: 10.1128/mcb.10.12.6356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Field J., Nikawa J., Broek D., MacDonald B., Rodgers L., Wilson I. A., Lerner R. A., Wigler M. Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol Cell Biol. 1988 May;8(5):2159–2165. doi: 10.1128/mcb.8.5.2159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gietz R. D., Sugino A. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene. 1988 Dec 30;74(2):527–534. doi: 10.1016/0378-1119(88)90185-0. [DOI] [PubMed] [Google Scholar]
  19. Gross S. D., Hoffman D. P., Fisette P. L., Baas P., Anderson R. A. A phosphatidylinositol 4,5-bisphosphate-sensitive casein kinase I alpha associates with synaptic vesicles and phosphorylates a subset of vesicle proteins. J Cell Biol. 1995 Aug;130(3):711–724. doi: 10.1083/jcb.130.3.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Healy A. M., Zolnierowicz S., Stapleton A. E., Goebl M., DePaoli-Roach A. A., Pringle J. R. CDC55, a Saccharomyces cerevisiae gene involved in cellular morphogenesis: identification, characterization, and homology to the B subunit of mammalian type 2A protein phosphatase. Mol Cell Biol. 1991 Nov;11(11):5767–5780. doi: 10.1128/mcb.11.11.5767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Herskowitz I., Jensen R. E. Putting the HO gene to work: practical uses for mating-type switching. Methods Enzymol. 1991;194:132–146. doi: 10.1016/0076-6879(91)94011-z. [DOI] [PubMed] [Google Scholar]
  22. Hill J. E., Myers A. M., Koerner T. J., Tzagoloff A. Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast. 1986 Sep;2(3):163–167. doi: 10.1002/yea.320020304. [DOI] [PubMed] [Google Scholar]
  23. Hoekstra M. F., Liskay R. M., Ou A. C., DeMaggio A. J., Burbee D. G., Heffron F. HRR25, a putative protein kinase from budding yeast: association with repair of damaged DNA. Science. 1991 Aug 30;253(5023):1031–1034. doi: 10.1126/science.1887218. [DOI] [PubMed] [Google Scholar]
  24. Hoekstra M. F., Seifert H. S., Nickoloff J., Heffron F. Shuttle mutagenesis: bacterial transposons for genetic manipulations in yeast. Methods Enzymol. 1991;194:329–342. doi: 10.1016/0076-6879(91)94025-8. [DOI] [PubMed] [Google Scholar]
  25. Ireland L. S., Johnston G. C., Drebot M. A., Dhillon N., DeMaggio A. J., Hoekstra M. F., Singer R. A. A member of a novel family of yeast 'zn-finger' proteins mediates the transition from stationary phase to cell proliferation. EMBO J. 1994 Aug 15;13(16):3812–3821. doi: 10.1002/j.1460-2075.1994.tb06692.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Johnston S. A., Hopper J. E. Isolation of the yeast regulatory gene GAL4 and analysis of its dosage effects on the galactose/melibiose regulon. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6971–6975. doi: 10.1073/pnas.79.22.6971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lew D. J., Reed S. I. Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins. J Cell Biol. 1993 Mar;120(6):1305–1320. doi: 10.1083/jcb.120.6.1305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Maeda T., Takekawa M., Saito H. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science. 1995 Jul 28;269(5223):554–558. doi: 10.1126/science.7624781. [DOI] [PubMed] [Google Scholar]
  29. Maeda T., Wurgler-Murphy S. M., Saito H. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature. 1994 May 19;369(6477):242–245. doi: 10.1038/369242a0. [DOI] [PubMed] [Google Scholar]
  30. Morishima N., Nakagawa K., Yamamoto E., Shibata T. A subunit of yeast site-specific endonuclease SceI is a mitochondrial version of the 70-kDa heat shock protein. J Biol Chem. 1990 Sep 5;265(25):15189–15197. [PubMed] [Google Scholar]
  31. Nelson M., Silver P. Context affects nuclear protein localization in Saccharomyces cerevisiae. Mol Cell Biol. 1989 Feb;9(2):384–389. doi: 10.1128/mcb.9.2.384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pausch M. H., Kaim D., Kunisawa R., Admon A., Thorner J. Multiple Ca2+/calmodulin-dependent protein kinase genes in a unicellular eukaryote. EMBO J. 1991 Jun;10(6):1511–1522. doi: 10.1002/j.1460-2075.1991.tb07671.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Riles L., Dutchik J. E., Baktha A., McCauley B. K., Thayer E. C., Leckie M. P., Braden V. V., Depke J. E., Olson M. V. Physical maps of the six smallest chromosomes of Saccharomyces cerevisiae at a resolution of 2.6 kilobase pairs. Genetics. 1993 May;134(1):81–150. doi: 10.1093/genetics/134.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Robinson L. C., Hubbard E. J., Graves P. R., DePaoli-Roach A. A., Roach P. J., Kung C., Haas D. W., Hagedorn C. H., Goebl M., Culbertson M. R. Yeast casein kinase I homologues: an essential gene pair. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):28–32. doi: 10.1073/pnas.89.1.28. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Robinson L. C., Menold M. M., Garrett S., Culbertson M. R. Casein kinase I-like protein kinases encoded by YCK1 and YCK2 are required for yeast morphogenesis. Mol Cell Biol. 1993 May;13(5):2870–2881. doi: 10.1128/mcb.13.5.2870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ronne H., Carlberg M., Hu G. Z., Nehlin J. O. Protein phosphatase 2A in Saccharomyces cerevisiae: effects on cell growth and bud morphogenesis. Mol Cell Biol. 1991 Oct;11(10):4876–4884. doi: 10.1128/mcb.11.10.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rothman J. E. Mechanisms of intracellular protein transport. Nature. 1994 Nov 3;372(6501):55–63. doi: 10.1038/372055a0. [DOI] [PubMed] [Google Scholar]
  38. Rowles J., Slaughter C., Moomaw C., Hsu J., Cobb M. H. Purification of casein kinase I and isolation of cDNAs encoding multiple casein kinase I-like enzymes. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9548–9552. doi: 10.1073/pnas.88.21.9548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Schiestl R. H., Gietz R. D. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet. 1989 Dec;16(5-6):339–346. doi: 10.1007/BF00340712. [DOI] [PubMed] [Google Scholar]
  40. Seufert W., McGrath J. P., Jentsch S. UBC1 encodes a novel member of an essential subfamily of yeast ubiquitin-conjugating enzymes involved in protein degradation. EMBO J. 1990 Dec;9(13):4535–4541. doi: 10.1002/j.1460-2075.1990.tb07905.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. Sneddon A. A., Cohen P. T., Stark M. J. Saccharomyces cerevisiae protein phosphatase 2A performs an essential cellular function and is encoded by two genes. EMBO J. 1990 Dec;9(13):4339–4346. doi: 10.1002/j.1460-2075.1990.tb07883.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Vancura A., Sessler A., Leichus B., Kuret J. A prenylation motif is required for plasma membrane localization and biochemical function of casein kinase I in budding yeast. J Biol Chem. 1994 Jul 29;269(30):19271–19278. [PubMed] [Google Scholar]
  44. Vida T. A., Emr S. D. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol. 1995 Mar;128(5):779–792. doi: 10.1083/jcb.128.5.779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wang P. C., Vancura A., Desai A., Carmel G., Kuret J. Cytoplasmic forms of fission yeast casein kinase-1 associate primarily with the particulate fraction of the cell. J Biol Chem. 1994 Apr 22;269(16):12014–12023. [PubMed] [Google Scholar]
  46. Wang P. C., Vancura A., Mitcheson T. G., Kuret J. Two genes in Saccharomyces cerevisiae encode a membrane-bound form of casein kinase-1. Mol Biol Cell. 1992 Mar;3(3):275–286. doi: 10.1091/mbc.3.3.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. 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]
  48. Whelan W. L., Ballou C. E. Sporulation in D-glucosamine auxotrophs of Saccharomyces cerevisiae: meiosis with defective ascospore wall formation. J Bacteriol. 1975 Dec;124(3):1545–1557. doi: 10.1128/jb.124.3.1545-1557.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Xu R. M., Carmel G., Sweet R. M., Kuret J., Cheng X. Crystal structure of casein kinase-1, a phosphate-directed protein kinase. EMBO J. 1995 Mar 1;14(5):1015–1023. doi: 10.1002/j.1460-2075.1995.tb07082.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. van Zyl W., Huang W., Sneddon A. A., Stark M., Camier S., Werner M., Marck C., Sentenac A., Broach J. R. Inactivation of the protein phosphatase 2A regulatory subunit A results in morphological and transcriptional defects in Saccharomyces cerevisiae. Mol Cell Biol. 1992 Nov;12(11):4946–4959. doi: 10.1128/mcb.12.11.4946. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES