Home LiteratureArticle Details
PMID: 9584086 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Regulation of yeast glycogen metabolism and sporulation by Glc7p protein phosphatase.

Genetics ·Vol. 149 ·No. 1 ·1998-05-00 ·Pages 57-72

Ramaswamy NT, Li L, Khalil M, Cannon JF

Abstract

Glc7p is an essential serine/threonine type 1 protein phosphatase (PP1) from the yeast Saccharomyces cerevisiae, which has a role in many processes including cell cycle progression, sporulation, glycogen accumulation, translation initiation, and glucose repression. Two hallmarks of PP1 enzymes are very high amino acid sequence conservation and association of the catalytic subunit with a variety of noncatalytic, regulatory subunits. We tested the hypothesis that PP1 sequence conservation was the result of each PP1 residue playing a role in multiple intermolecular interactions. Analysis of 24 glc7 mutants, isolated primarily by their glycogen accumulation traits, revealed that every mutated Glc7p residue altered many noncatalytic subunit affinities and conferred unselected sporulation traits to various degrees. Furthermore, quantitative analysis showed that Glc7p affinity for the glycogen-binding noncatalytic subunit Gac1p was not the only parameter that determines the glycogen accumulation by a glc7 mutant. Sds22p is one Glc7p noncatalytic subunit that is essential for mitotic growth. Surprisingly, several mutant Glc7p proteins had undetectable affinity for Sds22p, yet grew apparently normally. The characterization of glc7 diploid sporulation revealed that Glc7p has at least two meiotic roles. Premeiotic DNA synthesis was undetectable in glc7 mutants with the poorest sporulation. In the glc7 diploids examined, expression of the meiotic inducer IME1 was proportional to the glc7 diploid sporulation frequency. Moreover, IME1 hyperexpression could not suppress glc7 sporulation traits. The Glc7p/Gip1p holoenzyme may participate in completion of meiotic divisions or spore packaging because meiotic dyads predominate when some glc7 diploids sporulate.

MeSH Terms
Alleles Cell Cycle Proteins DNA, Fungal/metabolism Fungal Proteins/biosynthesis,genetics,physiology Gene Expression Regulation Glycogen/metabolism Intracellular Signaling Peptides and Proteins Meiosis Mutation Nuclear Proteins/biosynthesis,genetics Phosphoprotein Phosphatases/genetics,physiology Protein Kinases/biosynthesis,genetics Protein Serine-Threonine Kinases Saccharomyces cerevisiae/enzymology,physiology Saccharomyces cerevisiae Proteins Spores, Fungal/enzymology Transcription Factors
Chemicals
Cell Cycle Proteins DNA, Fungal Fungal Proteins IME1 protein, S cerevisiae Intracellular Signaling Peptides and Proteins Nuclear Proteins Saccharomyces cerevisiae Proteins Transcription Factors Glycogen Protein Kinases IME2 protein, S cerevisiae Protein Serine-Threonine Kinases Phosphoprotein Phosphatases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Ramaswamy N T
Department of Molecular Microbiology and Immunology, University of Missouri, Columbia, Missouri 65212, USA.
Li L
Khalil M
Cannon J F
References (46)
46 references, click to expand
  1. Conservation analysis and structure prediction of the protein serine/threonine phosphatases. Sequence similarity with diadenosine tetraphosphatase from Escherichia coli suggests homology to the protein phosphatases.
    Eur J Biochem. 1994 Feb 15;220(1):225-37 PMID: 8119291
  2. The mutant type 1 protein phosphatase encoded by glc7-1 from Saccharomyces cerevisiae fails to interact productively with the GAC1-encoded regulatory subunit.
    Mol Cell Biol. 1994 Feb;14(2):896-905 PMID: 8289829
  3. The Glc7 type 1 protein phosphatase of Saccharomyces cerevisiae is required for cell cycle progression in G2/M.
    Mol Cell Biol. 1994 May;14(5):3158-65 PMID: 8164671
  4. Control of meiotic gene expression in Saccharomyces cerevisiae.
    Microbiol Rev. 1994 Mar;58(1):56-70 PMID: 8177171
  5. IME1 gene encodes a transcription factor which is required to induce meiosis in Saccharomyces cerevisiae.
    Dev Genet. 1994;15(2):139-47 PMID: 8205723
  6. Suppressors of thermosensitive mutations in the DNA polymerase delta gene of Saccharomyces cerevisiae.
    Mol Gen Genet. 1995 Jan 20;246(2):212-22 PMID: 7862092
  7. The Saccharomyces SHP1 gene, which encodes a regulator of phosphoprotein phosphatase 1 with differential effects on glycogen metabolism, meiotic differentiation, and mitotic cell cycle progression.
    Mol Cell Biol. 1995 Apr;15(4):2037-50 PMID: 7891699
  8. Positive control of yeast meiotic genes by the negative regulator UME6.
    Mol Cell Biol. 1995 Jun;15(6):2955-61 PMID: 7760793
  9. Heat-shock proteins Hsp104 and Hsp70 reactivate mRNA splicing after heat inactivation.
    Curr Biol. 1995 Mar 1;5(3):306-17 PMID: 7780741
  10. Three-dimensional structure of the catalytic subunit of protein serine/threonine phosphatase-1.
    Nature. 1995 Aug 31;376(6543):745-53 PMID: 7651533
  11. A regulated MET3-GLC7 gene fusion provides evidence of a mitotic role for Saccharomyces cerevisiae protein phosphatase 1.
    Yeast. 1995 Jun 30;11(8):747-59 PMID: 7668044
  12. Regulation of chromosome segregation by Glc8p, a structural homolog of mammalian inhibitor 2 that functions as both an activator and an inhibitor of yeast protein phosphatase 1.
    Mol Cell Biol. 1995 Nov;15(11):6064-74 PMID: 7565759
  13. Crystal structure of the catalytic subunit of human protein phosphatase 1 and its complex with tungstate.
    J Mol Biol. 1995 Dec 15;254(5):942-59 PMID: 7500362
  14. 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):12490-4 PMID: 8618927
  15. Genetic interactions between REG1/HEX2 and GLC7, the gene encoding the protein phosphatase type 1 catalytic subunit in Saccharomyces cerevisiae.
    Genetics. 1996 May;143(1):119-27 PMID: 8722767
  16. Protein phosphatase type 1 interacts with proteins required for meiosis and other cellular processes in Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Aug;16(8):4199-206 PMID: 8754819
  17. Novel, activated RAS mutations alter protein-protein interactions.
    Oncogene. 1996 Sep 19;13(6):1209-20 PMID: 8808695
  18. Yeast protein serine/threonine phosphatases: multiple roles and diverse regulation.
    Yeast. 1996 Dec;12(16):1647-75 PMID: 9123967
  19. Alanine-scanning mutagenesis of protein phosphatase type 1 in the yeast Saccharomyces cerevisiae.
    Genetics. 1997 Mar;145(3):615-26 PMID: 9055072
  20. The yeast Red1 protein localizes to the cores of meiotic chromosomes.
    J Cell Biol. 1997 Mar 10;136(5):957-67 PMID: 9060462
  21. Structural basis for the recognition of regulatory subunits by the catalytic subunit of protein phosphatase 1.
    EMBO J. 1997 Apr 15;16(8):1876-87 PMID: 9155014
  22. Isolation and sequence of the gene for actin in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1980 Jul;77(7):3912-6 PMID: 7001447
  23. Transformation of intact yeast cells treated with alkali cations.
    J Bacteriol. 1983 Jan;153(1):163-8 PMID: 6336730
  24. Expression and DNA sequence of RED1, a gene required for meiosis I chromosome segregation in yeast.
    Mol Gen Genet. 1989 Aug;218(2):293-301 PMID: 2550770
  25. Positive control of sporulation-specific genes by the IME1 and IME2 products in Saccharomyces cerevisiae.
    Mol Cell Biol. 1990 May;10(5):2104-10 PMID: 2183020
  26. Yeast cAMP-dependent protein kinase regulatory subunit mutations display a variety of phenotypes.
    J Biol Chem. 1990 Jul 15;265(20):11897-904 PMID: 2164021
  27. Distinct, essential roles of type 1 and 2A protein phosphatases in the control of the fission yeast cell division cycle.
    Cell. 1990 Oct 19;63(2):405-15 PMID: 2170029
  28. The adenylate cyclase/protein kinase cascade regulates entry into meiosis in Saccharomyces cerevisiae through the gene IME1.
    EMBO J. 1990 Oct;9(10):3225-32 PMID: 2209544
  29. S. pombe gene sds22+ essential for a midmitotic transition encodes a leucine-rich repeat protein that positively modulates protein phosphatase-1.
    Cell. 1991 Jan 11;64(1):149-57 PMID: 1846086
  30. Protein phosphatases: recent progress.
    Adv Second Messenger Phosphoprotein Res. 1991;23:1-121 PMID: 1847640
  31. Use of lacZ fusions to delimit regulatory elements of the inducible divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae.
    Mol Cell Biol. 1984 Oct;4(10):1985-98 PMID: 6390181
  32. KAR1, a gene required for function of both intranuclear and extranuclear microtubules in yeast.
    Cell. 1987 Mar 27;48(6):1047-60 PMID: 3030557
  33. The fission yeast dis2+ gene required for chromosome disjoining encodes one of two putative type 1 protein phosphatases.
    Cell. 1989 Jun 16;57(6):997-1007 PMID: 2544298
  34. A novel genetic system to detect protein-protein interactions.
    Nature. 1989 Jul 20;340(6230):245-6 PMID: 2547163
  35. The control of acute postoperative pain.
    Br J Anaesth. 1989 Aug;63(2):147-58 PMID: 2491735
  36. The EGP1 gene may be a positive regulator of protein phosphatase type 1 in the growth control of Saccharomyces cerevisiae.
    Mol Cell Biol. 1995 Jul;15(7):3767-76 PMID: 7791784
  37. Putting the HO gene to work: practical uses for mating-type switching.
    Methods Enzymol. 1991;194:132-46 PMID: 2005783
  38. In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast.
    Methods Enzymol. 1991;194:302-18 PMID: 2005795
  39. The yeast GLC7 gene required for glycogen accumulation encodes a type 1 protein phosphatase.
    J Biol Chem. 1991 Dec 15;266(35):23796-801 PMID: 1660885
  40. GAC1 may encode a regulatory subunit for protein phosphatase type 1 in Saccharomyces cerevisiae.
    EMBO J. 1992 Jan;11(1):87-96 PMID: 1310938
  41. Multifunctional yeast high-copy-number shuttle vectors.
    Gene. 1992 Jan 2;110(1):119-22 PMID: 1544568
  42. Bipartite structure of an early meiotic upstream activation sequence from Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Apr;13(4):2172-81 PMID: 8455605
  43. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit.
    Genes Dev. 1993 Apr;7(4):555-69 PMID: 8384581
  44. On target with a new mechanism for the regulation of protein phosphorylation.
    Trends Biochem Sci. 1993 May;18(5):172-7 PMID: 8392229
  45. Molecular characterization of the yeast meiotic regulatory gene RIM1.
    Nucleic Acids Res. 1993 Aug 11;21(16):3789-97 PMID: 8367297
  46. Characterization of glycogen-deficient glc mutants of Saccharomyces cerevisiae.
    Genetics. 1994 Feb;136(2):485-503 PMID: 8150278
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
1998-05-00
Pages
57-72
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1460142
Subset
IM
Grants
NIGMS NIH HHS · GM-40326 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com