Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1996 Aug;16(8):4199–4206. doi: 10.1128/mcb.16.8.4199

Protein phosphatase type 1 interacts with proteins required for meiosis and other cellular processes in Saccharomyces cerevisiae.

J Tu 1, W Song 1, M Carlson 1
PMCID: PMC231417  PMID: 8754819

Abstract

Protein phosphatase type I (PP1) is involved in diverse cellular processes, and its activity toward specific substrates is thought to be controlled by different regulatory or targeting subunits. To identify regulatory subunits and substrates of the Saccharomyces cerevisiae PP1, encoded by GLC7, we used the two-hybrid system to detect interacting proteins. Among the many proteins identified were Gac1, a known glycogen regulatory subunit, and a protein with homology to Gac1. We also characterized a new gene designated GIP1, for Glc7-interacting protein. We show that a Gip1 fusion protein coimmunoprecipitates with PP1 from cell extracts. Molecular and genetic analyses indicate that GIP1 is expressed specifically during meiosis, affects transcription of late meiotic genes, and is essential for sporulation. Thus, the Gip1 protein is a candidate for a meiosis-specific substrate or regulator of PP1. Finally, we recovered two genes, RED1 and SCD5, with roles in meiosis and the vesicular secretory pathway, respectively. These results provide strong evidence implicating PP1 function in meiosis. In addition, this study indicates that the two-hybrid system offers a promising approach to understanding the multiple roles and interactions of PP1 in cellular regulation.

Full Text

The Full Text of this article is available as a PDF (346.2 KB).

Selected References

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

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Axton J. M., Dombrádi V., Cohen P. T., Glover D. M. One of the protein phosphatase 1 isoenzymes in Drosophila is essential for mitosis. Cell. 1990 Oct 5;63(1):33–46. doi: 10.1016/0092-8674(90)90286-n. [DOI] [PubMed] [Google Scholar]
  3. Bartel P., Chien C. T., Sternglanz R., Fields S. Elimination of false positives that arise in using the two-hybrid system. Biotechniques. 1993 Jun;14(6):920–924. [PubMed] [Google Scholar]
  4. Booher R., Beach D. Involvement of a type 1 protein phosphatase encoded by bws1+ in fission yeast mitotic control. Cell. 1989 Jun 16;57(6):1009–1016. doi: 10.1016/0092-8674(89)90339-5. [DOI] [PubMed] [Google Scholar]
  5. Bossier P., Fernandes L., Rocha D., Rodrigues-Pousada C. Overexpression of YAP2, coding for a new yAP protein, and YAP1 in Saccharomyces cerevisiae alleviates growth inhibition caused by 1,10-phenanthroline. J Biol Chem. 1993 Nov 5;268(31):23640–23645. [PubMed] [Google Scholar]
  6. Bowdish K. S., Yuan H. E., Mitchell A. P. Analysis of RIM11, a yeast protein kinase that phosphorylates the meiotic activator IME1. Mol Cell Biol. 1994 Dec;14(12):7909–7919. doi: 10.1128/mcb.14.12.7909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Breeden L., Nasmyth K. Regulation of the yeast HO gene. Cold Spring Harb Symp Quant Biol. 1985;50:643–650. doi: 10.1101/sqb.1985.050.01.078. [DOI] [PubMed] [Google Scholar]
  8. Cannon J. F., Pringle J. R., Fiechter A., Khalil M. Characterization of glycogen-deficient glc mutants of Saccharomyces cerevisiae. Genetics. 1994 Feb;136(2):485–503. doi: 10.1093/genetics/136.2.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Chen Y. H., Hansen L., Chen M. X., Bjørbaek C., Vestergaard H., Hansen T., Cohen P. T., Pedersen O. Sequence of the human glycogen-associated regulatory subunit of type 1 protein phosphatase and analysis of its coding region and mRNA level in muscle from patients with NIDDM. Diabetes. 1994 Oct;43(10):1234–1241. doi: 10.2337/diabetes.43.10.1234. [DOI] [PubMed] [Google Scholar]
  11. Chien C. T., Bartel P. L., Sternglanz R., Fields S. The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9578–9582. doi: 10.1073/pnas.88.21.9578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chun Y. S., Shima H., Nagasaki K., Sugimura T., Nagao M. PP1 gamma 2, a testis-specific protein-serine/threonine-phosphatase type 1 catalytic subunit, is associated with a protein having high sequence homology with the 78-kDa glucose-regulated protein, a member of the 70-kDa heat shock protein family. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3319–3323. doi: 10.1073/pnas.91.8.3319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Clark-Maguire S., Mains P. E. mei-1, a gene required for meiotic spindle formation in Caenorhabditis elegans, is a member of a family of ATPases. Genetics. 1994 Feb;136(2):533–546. doi: 10.1093/genetics/136.2.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cohen P. Signal integration at the level of protein kinases, protein phosphatases and their substrates. Trends Biochem Sci. 1992 Oct;17(10):408–413. doi: 10.1016/0968-0004(92)90010-7. [DOI] [PubMed] [Google Scholar]
  15. Cohen P. The structure and regulation of protein phosphatases. Annu Rev Biochem. 1989;58:453–508. doi: 10.1146/annurev.bi.58.070189.002321. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Dohadwala M., da Cruz e Silva E. F., Hall F. L., Williams R. T., Carbonaro-Hall D. A., Nairn A. C., Greengard P., Berndt N. Phosphorylation and inactivation of protein phosphatase 1 by cyclin-dependent kinases. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6408–6412. doi: 10.1073/pnas.91.14.6408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Doonan J. H., Morris N. R. The bimG gene of Aspergillus nidulans, required for completion of anaphase, encodes a homolog of mammalian phosphoprotein phosphatase 1. Cell. 1989 Jun 16;57(6):987–996. doi: 10.1016/0092-8674(89)90337-1. [DOI] [PubMed] [Google Scholar]
  19. Durfee T., Becherer K., Chen P. L., Yeh S. H., Yang Y., Kilburn A. E., Lee W. H., Elledge S. J. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 1993 Apr;7(4):555–569. doi: 10.1101/gad.7.4.555. [DOI] [PubMed] [Google Scholar]
  20. Entian K. D., Zimmermann F. K. Glycolytic enzymes and intermediates in carbon catabolite repression mutants of Saccharomyces cerevisiae. Mol Gen Genet. 1980 Jan;177(2):345–350. doi: 10.1007/BF00267449. [DOI] [PubMed] [Google Scholar]
  21. Feldmann H., Aigle M., Aljinovic G., André B., Baclet M. C., Barthe C., Baur A., Bécam A. M., Biteau N., Boles E. Complete DNA sequence of yeast chromosome II. EMBO J. 1994 Dec 15;13(24):5795–5809. doi: 10.1002/j.1460-2075.1994.tb06923.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Feng Z. H., Wilson S. E., Peng Z. Y., Schlender K. K., Reimann E. M., Trumbly R. J. The yeast GLC7 gene required for glycogen accumulation encodes a type 1 protein phosphatase. J Biol Chem. 1991 Dec 15;266(35):23796–23801. [PubMed] [Google Scholar]
  23. Fields S., Song O. A novel genetic system to detect protein-protein interactions. Nature. 1989 Jul 20;340(6230):245–246. doi: 10.1038/340245a0. [DOI] [PubMed] [Google Scholar]
  24. Francisco L., Wang W., Chan C. S. Type 1 protein phosphatase acts in opposition to IpL1 protein kinase in regulating yeast chromosome segregation. Mol Cell Biol. 1994 Jul;14(7):4731–4740. doi: 10.1128/mcb.14.7.4731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. François J. M., Thompson-Jaeger S., Skroch J., Zellenka U., Spevak W., Tatchell K. GAC1 may encode a regulatory subunit for protein phosphatase type 1 in Saccharomyces cerevisiae. EMBO J. 1992 Jan;11(1):87–96. doi: 10.1002/j.1460-2075.1992.tb05031.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Friedman D. B., Hollingsworth N. M., Byers B. Insertional mutations in the yeast HOP1 gene: evidence for multimeric assembly in meiosis. Genetics. 1994 Feb;136(2):449–464. doi: 10.1093/genetics/136.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Friesen H., Lunz R., Doyle S., Segall J. Mutation of the SPS1-encoded protein kinase of Saccharomyces cerevisiae leads to defects in transcription and morphology during spore formation. Genes Dev. 1994 Sep 15;8(18):2162–2175. doi: 10.1101/gad.8.18.2162. [DOI] [PubMed] [Google Scholar]
  28. Goldberg J., Huang H. B., Kwon Y. G., Greengard P., Nairn A. C., Kuriyan J. Three-dimensional structure of the catalytic subunit of protein serine/threonine phosphatase-1. Nature. 1995 Aug 31;376(6543):745–753. doi: 10.1038/376745a0. [DOI] [PubMed] [Google Scholar]
  29. Hisamoto N., Frederick D. L., Sugimoto K., Tatchell K., Matsumoto K. 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):3767–3776. doi: 10.1128/mcb.15.7.3767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hisamoto N., Sugimoto K., Matsumoto K. 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):3158–3165. doi: 10.1128/mcb.14.5.3158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hollingsworth N. M., Goetsch L., Byers B. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell. 1990 Apr 6;61(1):73–84. doi: 10.1016/0092-8674(90)90216-2. [DOI] [PubMed] [Google Scholar]
  32. Hollingsworth N. M., Johnson A. D. A conditional allele of the Saccharomyces cerevisiae HOP1 gene is suppressed by overexpression of two other meiosis-specific genes: RED1 and REC104. Genetics. 1993 Apr;133(4):785–797. doi: 10.1093/genetics/133.4.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Holtzman D. A., Yang S., Drubin D. G. Synthetic-lethal interactions identify two novel genes, SLA1 and SLA2, that control membrane cytoskeleton assembly in Saccharomyces cerevisiae. J Cell Biol. 1993 Aug;122(3):635–644. doi: 10.1083/jcb.122.3.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hubbard M. J., Cohen P. On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem Sci. 1993 May;18(5):172–177. doi: 10.1016/0968-0004(93)90109-z. [DOI] [PubMed] [Google Scholar]
  35. Hunter T. A thousand and one protein kinases. Cell. 1987 Sep 11;50(6):823–829. doi: 10.1016/0092-8674(87)90509-5. [DOI] [PubMed] [Google Scholar]
  36. Kane S. M., Roth R. Carbohydrate metabolism during ascospore development in yeast. J Bacteriol. 1974 Apr;118(1):8–14. doi: 10.1128/jb.118.1.8-14.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Kinoshita N., Ohkura H., Yanagida M. 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):405–415. doi: 10.1016/0092-8674(90)90173-c. [DOI] [PubMed] [Google Scholar]
  39. Krisak L., Strich R., Winters R. S., Hall J. P., Mallory M. J., Kreitzer D., Tuan R. S., Winter E. SMK1, a developmentally regulated MAP kinase, is required for spore wall assembly in Saccharomyces cerevisiae. Genes Dev. 1994 Sep 15;8(18):2151–2161. doi: 10.1101/gad.8.18.2151. [DOI] [PubMed] [Google Scholar]
  40. Kunz J., Henriquez R., Schneider U., Deuter-Reinhard M., Movva N. R., Hall M. N. Target of rapamycin in yeast, TOR2, is an essential phosphatidylinositol kinase homolog required for G1 progression. Cell. 1993 May 7;73(3):585–596. doi: 10.1016/0092-8674(93)90144-f. [DOI] [PubMed] [Google Scholar]
  41. Lai M. H., Bard M., Kirsch D. R. Identification of a gene encoding a new Ypt/Rab-like monomeric G-protein in Saccharomyces cerevisiae. Yeast. 1994 Mar;10(3):399–402. doi: 10.1002/yea.320100313. [DOI] [PubMed] [Google Scholar]
  42. Law D. T., Segall J. The SPS100 gene of Saccharomyces cerevisiae is activated late in the sporulation process and contributes to spore wall maturation. Mol Cell Biol. 1988 Feb;8(2):912–922. doi: 10.1128/mcb.8.2.912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lesage P., Yang X., Carlson M. Analysis of the SIP3 protein identified in a two-hybrid screen for interaction with the SNF1 protein kinase. Nucleic Acids Res. 1994 Feb 25;22(4):597–603. doi: 10.1093/nar/22.4.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Lesage P., Yang X., Carlson M. Yeast SNF1 protein kinase interacts with SIP4, a C6 zinc cluster transcriptional activator: a new role for SNF1 in the glucose response. Mol Cell Biol. 1996 May;16(5):1921–1928. doi: 10.1128/mcb.16.5.1921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. MacKelvie S. H., Andrews P. D., Stark M. J. The Saccharomyces cerevisiae gene SDS22 encodes a potential regulator of the mitotic function of yeast type 1 protein phosphatase. Mol Cell Biol. 1995 Jul;15(7):3777–3785. doi: 10.1128/mcb.15.7.3777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Matsumoto K., Yoshimatsu T., Oshima Y. Recessive mutations conferring resistance to carbon catabolite repression of galactokinase synthesis in Saccharomyces cerevisiae. J Bacteriol. 1983 Mar;153(3):1405–1414. doi: 10.1128/jb.153.3.1405-1414.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. 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]
  48. Murakami Y., Naitou M., Hagiwara H., Shibata T., Ozawa M., Sasanuma S., Sasanuma M., Tsuchiya Y., Soeda E., Yokoyama K. Analysis of the nucleotide sequence of chromosome VI from Saccharomyces cerevisiae. Nat Genet. 1995 Jul;10(3):261–268. doi: 10.1038/ng0795-261. [DOI] [PubMed] [Google Scholar]
  49. Neigeborn L., Carlson M. Mutations causing constitutive invertase synthesis in yeast: genetic interactions with snf mutations. Genetics. 1987 Feb;115(2):247–253. doi: 10.1093/genetics/115.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Nelson K. K., Holmer M., Lemmon S. K. SCD5, a suppressor of clathrin deficiency, encodes a novel protein with a late secretory function in yeast. Mol Biol Cell. 1996 Feb;7(2):245–260. doi: 10.1091/mbc.7.2.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Ohkura H., Kinoshita N., Miyatani S., Toda T., Yanagida M. 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. doi: 10.1016/0092-8674(89)90338-3. [DOI] [PubMed] [Google Scholar]
  52. Ohkura H., Yanagida M. 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):149–157. doi: 10.1016/0092-8674(91)90216-l. [DOI] [PubMed] [Google Scholar]
  53. Percival-Smith A., Segall J. Isolation of DNA sequences preferentially expressed during sporulation in Saccharomyces cerevisiae. Mol Cell Biol. 1984 Jan;4(1):142–150. doi: 10.1128/mcb.4.1.142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Périer F., Coulter K. L., Liang H., Radeke C. M., Gaber R. F., Vandenberg C. A. Identification of a novel mammalian member of the NSF/CDC48p/Pas1p/TBP-1 family through heterologous expression in yeast. FEBS Lett. 1994 Sep 5;351(2):286–290. doi: 10.1016/0014-5793(94)00879-5. [DOI] [PubMed] [Google Scholar]
  55. Rockmill B., Roeder G. S. Meiosis in asynaptic yeast. Genetics. 1990 Nov;126(3):563–574. doi: 10.1093/genetics/126.3.563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Rockmill B., Roeder G. S. RED1: a yeast gene required for the segregation of chromosomes during the reductional division of meiosis. Proc Natl Acad Sci U S A. 1988 Aug;85(16):6057–6061. doi: 10.1073/pnas.85.16.6057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Rothstein R. J. One-step gene disruption in yeast. Methods Enzymol. 1983;101:202–211. doi: 10.1016/0076-6879(83)01015-0. [DOI] [PubMed] [Google Scholar]
  58. Schnall R., Mannhaupt G., Stucka R., Tauer R., Ehnle S., Schwarzlose C., Vetter I., Feldmann H. Identification of a set of yeast genes coding for a novel family of putative ATPases with high similarity to constituents of the 26S protease complex. Yeast. 1994 Sep;10(9):1141–1155. doi: 10.1002/yea.320100903. [DOI] [PubMed] [Google Scholar]
  59. Shah H. C., Carlson G. P. Alteration by phenobarbital and 3-methyl-cholanthrene of functional and structural changes in rat liver due to carbon tetrachloride inhalation. J Pharmacol Exp Ther. 1975 Apr;193(1):281–292. [PubMed] [Google Scholar]
  60. Smith H. E., Mitchell A. P. A transcriptional cascade governs entry into meiosis in Saccharomyces cerevisiae. Mol Cell Biol. 1989 May;9(5):2142–2152. doi: 10.1128/mcb.9.5.2142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Stone E. M., Yamano H., Kinoshita N., Yanagida M. Mitotic regulation of protein phosphatases by the fission yeast sds22 protein. Curr Biol. 1993 Jan;3(1):13–26. doi: 10.1016/0960-9822(93)90140-j. [DOI] [PubMed] [Google Scholar]
  62. Stuart J. S., Frederick D. L., Varner C. M., Tatchell K. 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. doi: 10.1128/mcb.14.2.896. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Sutton A., Lin F., Arndt K. T. The SIT4 protein phosphatase is required in late G1 for progression into S phase. Cold Spring Harb Symp Quant Biol. 1991;56:75–81. doi: 10.1101/sqb.1991.056.01.011. [DOI] [PubMed] [Google Scholar]
  64. Tang P. M., Bondor J. A., Swiderek K. M., DePaoli-Roach A. A. Molecular cloning and expression of the regulatory (RG1) subunit of the glycogen-associated protein phosphatase. J Biol Chem. 1991 Aug 25;266(24):15782–15789. [PubMed] [Google Scholar]
  65. Thompson E. A., Roeder G. S. 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. doi: 10.1007/BF00331281. [DOI] [PubMed] [Google Scholar]
  66. Tu J., Carlson M. REG1 binds to protein phosphatase type 1 and regulates glucose repression in Saccharomyces cerevisiae. EMBO J. 1995 Dec 1;14(23):5939–5946. doi: 10.1002/j.1460-2075.1995.tb00282.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Tu J., Carlson M. The GLC7 type 1 protein phosphatase is required for glucose repression in Saccharomyces cerevisiae. Mol Cell Biol. 1994 Oct;14(10):6789–6796. doi: 10.1128/mcb.14.10.6789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Tu J., Vallier L. G., Carlson M. Molecular and genetic analysis of the SNF7 gene in Saccharomyces cerevisiae. Genetics. 1993 Sep;135(1):17–23. doi: 10.1093/genetics/135.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Tung K. S., Norbeck L. L., Nolan S. L., Atkinson N. S., Hopper A. K. SRN1, a yeast gene involved in RNA processing, is identical to HEX2/REG1, a negative regulator in glucose repression. Mol Cell Biol. 1992 Jun;12(6):2673–2680. doi: 10.1128/mcb.12.6.2673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Wek R. C., Cannon J. F., Dever T. E., Hinnebusch A. G. Truncated protein phosphatase GLC7 restores translational activation of GCN4 expression in yeast mutants defective for the eIF-2 alpha kinase GCN2. Mol Cell Biol. 1992 Dec;12(12):5700–5710. doi: 10.1128/mcb.12.12.5700. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Whyte W., Keopp L. H., Lamb J., Crowley J. C., Kaback D. B. Molecular cloning of chromosome I DNA from Saccharomyces cerevisiae: isolation, characterization and regulation of the SPO7 sporulation gene. Gene. 1990 Oct 30;95(1):65–72. doi: 10.1016/0378-1119(90)90414-m. [DOI] [PubMed] [Google Scholar]
  72. Wiltshire T., Park C., Caldwell K. A., Handel M. A. Induced premature G2/M-phase transition in pachytene spermatocytes includes events unique to meiosis. Dev Biol. 1995 Jun;169(2):557–567. doi: 10.1006/dbio.1995.1169. [DOI] [PubMed] [Google Scholar]
  73. Yang X., Hubbard E. J., Carlson M. A protein kinase substrate identified by the two-hybrid system. Science. 1992 Jul 31;257(5070):680–682. doi: 10.1126/science.1496382. [DOI] [PubMed] [Google Scholar]
  74. Zhang S., Guha S., Volkert F. C. 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):2037–2050. doi: 10.1128/mcb.15.4.2037. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES