The Fission Yeast Stress-Responsive MAPK Pathway Promotes Meiosis via the Phosphorylation of Pol II CTD in Response to Environmental and Feedback Cues
The RRM-type RNA-binding protein Mei2 is a master regulator of meiosis in fission yeast, in which it stabilizes meiosis-specific mRNAs by blocking their destruction. Artificial activation of Mei2 can provoke the entire meiotic process, and it is suspected that Mei2 may do more than the stabilization of meiosis-specific mRNAs. In our current study using a new screening system, we show that Mei2 genetically interacts with subunits of CTDK-I, which phosphorylates serine-2 residues on the C-terminal domain of RNA polymerase II (Pol II CTD). Phosphorylation of CTD Ser-2 is essential to enable the robust transcription of ste11, which encodes an HMG-type transcription factor that regulates the expression of mei2 and other genes necessary for sexual development. CTD Ser-2 phosphorylation increases under nitrogen starvation, and the stress-responsive MAP kinase pathway, mediated by Wis1 MAPKK and Sty1 MAPK, is critical for this stress response. Sty1 phosphorylates Lsk1, the catalytic subunit of CTDK-I. Furthermore, a feedback loop stemming from activated Mei2 to Win1 and Wis4 MAPKKKs operates in this pathway and eventually enhances CTD Ser-2 phosphorylation and ste11 transcription. Hence, in addition to starting meiosis, Mei2 functions to reinforce the commitment to it, once cells have entered this process. This study also demonstrates clearly that the stress-responsive MAP kinase pathway can modulates gene expression through phosphorylation of Pol II CTD.
Vyšlo v časopise:
The Fission Yeast Stress-Responsive MAPK Pathway Promotes Meiosis via the Phosphorylation of Pol II CTD in Response to Environmental and Feedback Cues. PLoS Genet 7(12): e32767. doi:10.1371/journal.pgen.1002387
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002387
Souhrn
The RRM-type RNA-binding protein Mei2 is a master regulator of meiosis in fission yeast, in which it stabilizes meiosis-specific mRNAs by blocking their destruction. Artificial activation of Mei2 can provoke the entire meiotic process, and it is suspected that Mei2 may do more than the stabilization of meiosis-specific mRNAs. In our current study using a new screening system, we show that Mei2 genetically interacts with subunits of CTDK-I, which phosphorylates serine-2 residues on the C-terminal domain of RNA polymerase II (Pol II CTD). Phosphorylation of CTD Ser-2 is essential to enable the robust transcription of ste11, which encodes an HMG-type transcription factor that regulates the expression of mei2 and other genes necessary for sexual development. CTD Ser-2 phosphorylation increases under nitrogen starvation, and the stress-responsive MAP kinase pathway, mediated by Wis1 MAPKK and Sty1 MAPK, is critical for this stress response. Sty1 phosphorylates Lsk1, the catalytic subunit of CTDK-I. Furthermore, a feedback loop stemming from activated Mei2 to Win1 and Wis4 MAPKKKs operates in this pathway and eventually enhances CTD Ser-2 phosphorylation and ste11 transcription. Hence, in addition to starting meiosis, Mei2 functions to reinforce the commitment to it, once cells have entered this process. This study also demonstrates clearly that the stress-responsive MAP kinase pathway can modulates gene expression through phosphorylation of Pol II CTD.
Zdroje
1. MataJLyneRBurnsGBahlerJ 2002 The transcriptional program of meiosis and sporulation in fission yeast. Nat Genet 32 143 147
2. KassirYAdirNBoger-NadjarERavivNGRubin-BejeranoI 2003 Transcriptional regulation of meiosis in budding yeast. Int Rev Cytol 224 111 171
3. HarigayaYTanakaHYamanakaSTanakaKWatanabeY 2006 Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442 45 50
4. YamanakaSYamashitaAHarigayaYIwataRYamamotoM 2010 Importance of polyadenylation in the selective elimination of meiotic mRNAs in growing S. pombe cells. EMBO J 29 2173 2181
5. WatanabeYYamamotoM 1994 S.pombe mei2+ encodes an RNA-binding protein essential for premeiotic DNA synthesis and meiosis I, which cooperates with a novel RNA species meiRNA. Cell 78 487 498
6. WatanabeYYabanaSChikashigeYHiraokaYYamamotoM 1997 Phosphorylation of RNA-binding protein controls cell cycle switch from mitotic to meiotic in fission yeast. Nature 386 187 190
7. YamashitaAWatanabeYNukinaNYamamotoM 1998 RNA-assisted nuclear transport of the meiotic regulator Mei2p in fission yeast. Cell 95 115 123
8. YamamotoM 2010 The selective elimination of messenger RNA underlies the mitosis-meiosis switch in fission yeast. Proc Jpn Acad Ser B Phys Biol Sci 86 788 797
9. HiroseYManleyJL 2000 RNA polymerase II and the integration of nuclear events. Genes Dev 14 1415 1429
10. PhatnaniHPGreenleafAL 2006 Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev 20 2922 2936
11. CoudreuseDvan BakelHDewezMSoutourinaJParnellT 2010 A gene-specific requirement of RNA polymerase II CTD phosphorylation for sexual differentiation in S. pombe. Curr Biol 20 1053 1064
12. LeeJMGreenleafAL 1991 CTD kinase large subunit is encoded by CTK1, a gene required for normal growth of Saccharomyces cerevisiae. Gene Expr 1 149 167
13. SternerDELeeJMHardinSEGreenleafAL 1995 The yeast carboxyl-terminal repeat domain kinase CTDK-I is a divergent cyclin-cyclin-dependent kinase complex. Mol Cell Biol 15 5716 5724
14. KaragiannisJBimboARajagopalanSLiuJBalasubramanianMK 2005 The nuclear kinase Lsk1p positively regulates the septation initiation network and promotes the successful completion of cytokinesis in response to perturbation of the actomyosin ring in Schizosaccharomyces pombe. Mol Biol Cell 16 358 371
15. KaragiannisJBalasubramanianMK 2007 A cyclin-dependent kinase that promotes cytokinesis through modulating phosphorylation of the carboxy terminal domain of the RNA Pol II Rpb1p sub-unit. PLoS ONE 2 e433 doi:10.1371/journal.pone.0000433
16. SugimotoAIinoYMaedaTWatanabeYYamamotoM 1991 Schizosaccharomyces pombe ste11+ encodes a transcription factor with an HMG motif that is a critical regulator of sexual development. Genes Dev 5 1990 1999
17. SipiczkiM 1988 The role of sterility genes (ste and aff) in the initiation of sexual development in Schizosaccharomyces pombe. Mol Gen Genet 213 529 534
18. WatanabeYIinoYFuruhataKShimodaCYamamotoM 1988 The S.pombe mei2 gene encoding a crucial molecule for commitment to meiosis is under the regulation of cAMP. EMBO J 7 761 767
19. MataJBahlerJ 2006 Global roles of Ste11p, cell type, and pheromone in the control of gene expression during early sexual differentiation in fission yeast. Proc Natl Acad Sci U S A 103 15517 15522
20. TakedaTTodaTKominamiKKohnosuAYanagidaM 1995 Schizosaccharomyces pombe atf1+ encodes a transcription factor required for sexual development and entry into stationary phase. EMBO J 14 6193 6208
21. KanohJWatanabeYOhsugiMIinoYYamamotoM 1996 Schizosaccharomyces pombe gad7+ encodes a phosphoprotein with a bZIP domain, which is required for proper G1 arrest and gene expression under nitrogen starvation. Genes Cells 1 391 408
22. ShiozakiKRussellP 1996 Conjugation, meiosis, and the osmotic stress response are regulated by Spc1 kinase through Atf1 transcription factor in fission yeast. Genes Dev 10 2276 2288
23. WatanabeYYamamotoM 1996 Schizosaccharomyces pombe pcr1+ encodes a CREB/ATF protein involved in regulation of gene expression for sexual development. Mol Cell Biol 16 704 711
24. KunitomoHHiguchiTIinoYYamamotoM 2000 A zinc-finger protein, Rst2p, regulates transcription of the fission yeast ste11+ gene, which encodes a pivotal transcription factor for sexual development. Mol Biol Cell 11 3205 3217
25. HiguchiTWatanabeYYamamotoM 2002 Protein kinase A regulates sexual development and gluconeogenesis through phosphorylation of the Zn finger transcriptional activator Rst2p in fission yeast. Mol Cell Biol 22 1 11
26. SchwerBShumanS 2011 Deciphering the RNA polymerase II CTD code in fission yeast. Mol Cell 43 311 318
27. KimuraMSuzukiHIshihamaA 2002 Formation of a carboxy-terminal domain phosphatase (Fcp1)/TFIIF/RNA polymerase II (pol II) complex in Schizosaccharomyces pombe involves direct interaction between Fcp1 and the Rpb4 subunit of pol II. Mol Cell Biol 22 1577 1588
28. HausmannSShumanS 2002 Characterization of the CTD phosphatase Fcp1 from fission yeast. Preferential dephosphorylation of serine 2 versus serine 5. J Biol Chem 277 21213 21220
29. PatturajanMSchulteRJSeftonBMBerezneyRVincentM 1998 Growth-related changes in phosphorylation of yeast RNA polymerase II. J Biol Chem 273 4689 4694
30. OstapenkoDSolomonMJ 2003 Budding yeast CTDK-I is required for DNA damage-induced transcription. Eukaryot Cell 2 274 283
31. ShiozakiKRussellP 1995 Cell-cycle control linked to extracellular environment by MAP kinase pathway in fission yeast. Nature 378 739 743
32. MillarJBBuckVWilkinsonMG 1995 Pyp1 and Pyp2 PTPases dephosphorylate an osmosensing MAP kinase controlling cell size at division in fission yeast. Genes Dev 9 2117 2130
33. KatoTJrOkazakiKMurakamiHStettlerSFantesPA 1996 Stress signal, mediated by a Hog1-like MAP kinase, controls sexual development in fission yeast. FEBS Lett 378 207 212
34. ReiterWWattSDawsonKLawrenceCLBahlerJ 2008 Fission yeast MAP kinase Sty1 is recruited to stress-induced genes. J Biol Chem 283 9945 9956
35. DegolsGShiozakiKRussellP 1996 Activation and regulation of the Spc1 stress-activated protein kinase in Schizosaccharomyces pombe. Mol Cell Biol 16 2870 2877
36. DegolsGRussellP 1997 Discrete roles of the Spc1 kinase and the Atf1 transcription factor in the UV response of Schizosaccharomyces pombe. Mol Cell Biol 17 3356 3363
37. WilkinsonMGMillarJB 1998 SAPKs and transcription factors do the nucleocytoplasmic tango. Genes Dev 12 1391 1397
38. ShiehJCWilkinsonMGMillarJB 1998 The Win1 mitotic regulator is a component of the fission yeast stress-activated Sty1 MAPK pathway. Mol Biol Cell 9 311 322
39. ShiozakiKShiozakiMRussellP 1998 Heat stress activates fission yeast Spc1/StyI MAPK by a MEKK-independent mechanism. Mol Biol Cell 9 1339 1349
40. BuckVQuinnJSoto PinoTMartinHSaldanhaJ 2001 Peroxide sensors for the fission yeast stress-activated mitogen-activated protein kinase pathway. Mol Biol Cell 12 407 419
41. GaitsFDegolsGShiozakiKRussellP 1998 Phosphorylation and association with the transcription factor Atf1 regulate localization of Spc1/Sty1 stress-activated kinase in fission yeast. Genes Dev 12 1464 1473
42. AlepuzPMJovanovicAReiserVAmmererG 2001 Stress-induced map kinase Hog1 is part of transcription activation complexes. Mol Cell 7 767 777
43. AlepuzPMde NadalEZapaterMAmmererGPosasF 2003 Osmostress-induced transcription by Hot1 depends on a Hog1-mediated recruitment of the RNA Pol II. EMBO J 22 2433 2442
44. OrlandiICavadiniPPopoloLVaiM 1996 Cloning, sequencing and regulation of a cDNA encoding a small heat-shock protein from Schizosaccharomyces pombe. Biochim Biophys Acta 1307 129 131
45. ChenDTooneWMMataJLyneRBurnsG 2003 Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 14 214 229
46. GutzHHeslotHLeupoldULoprienoN 1974 Schizosaccharomyces pombe. KingRD Handbook of Genetics New York Plenum Publishing Corporation 395 446
47. MorenoSKlarANurseP 1991 Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194 795 823
48. EgelREgel-MitaniM 1974 Premeiotic DNA synthesis in fission yeast. Exp Cell Res 88 127 134
49. OkazakiKOkazakiNKumeKJinnoSTanakaK 1990 High-frequency transformation method and library transducing vectors for cloning mammalian cDNAs by trans-complementation of Schizosaccharomyces pombe. Nucleic Acids Res 18 6485 6489
50. ChuaGTaricaniLStangleWYoungPG 2000 Insertional mutagenesis based on illegitimate recombination in Schizosaccharomyces pombe. Nucleic Acids Res 28 E53
51. ImaiYYamamotoM 1994 The fission yeast mating pheromone P-factor: its molecular structure, gene structure, and ability to induce gene expression and G1 arrest in the mating partner. Genes Dev 8 328 338
52. MatsuoTOtsuboYUranoJTamanoiFYamamotoM 2007 Loss of the TOR kinase Tor2 mimics nitrogen starvation and activates the sexual development pathway in fission yeast. Mol Cell Biol 27 3154 3164
53. YamashitaAWatanabeYYamamotoM 1997 Microtubule-associated coiled-coil protein Ssm4 is involved in the meiotic development in fission yeast. Genes Cells 2 155 166
54. KohdaTATanakaKKonomiMSatoMOsumiM 2007 Fission yeast autophagy induced by nitrogen starvation generates a nitrogen source that drives adaptation processes. Genes Cells 12 155 170
55. WoodsASherwinTSasseRMcRaeTHBainesAJ 1989 Definition of individual components within the cytoskelton of Trypanosoma brucei by a library of monoclonal antibodies. J Cell Sci 93 491 500
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 12
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