Multiple Signals Converge on a Differentiation MAPK Pathway
An important emerging question in the area of signal transduction is how information from different pathways becomes integrated into a highly coordinated response. In budding yeast, multiple pathways regulate filamentous growth, a complex differentiation response that occurs under specific environmental conditions. To identify new aspects of filamentous growth regulation, we used a novel screening approach (called secretion profiling) that measures release of the extracellular domain of Msb2p, the signaling mucin which functions at the head of the filamentous growth (FG) MAPK pathway. Secretion profiling of complementary genomic collections showed that many of the pathways that regulate filamentous growth (RAS, RIM101, OPI1, and RTG) were also required for FG pathway activation. This regulation sensitized the FG pathway to multiple stimuli and synchronized it to the global signaling network. Several of the regulators were required for MSB2 expression, which identifies the MSB2 promoter as a target “hub” where multiple signals converge. Accessibility to the MSB2 promoter was further regulated by the histone deacetylase (HDAC) Rpd3p(L), which positively regulated FG pathway activity and filamentous growth. Our findings provide the first glimpse of a global regulatory hierarchy among the pathways that control filamentous growth. Systems-level integration of signaling circuitry is likely to coordinate other regulatory networks that control complex behaviors.
Vyšlo v časopise:
Multiple Signals Converge on a Differentiation MAPK Pathway. PLoS Genet 6(3): e32767. doi:10.1371/journal.pgen.1000883
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1000883
Souhrn
An important emerging question in the area of signal transduction is how information from different pathways becomes integrated into a highly coordinated response. In budding yeast, multiple pathways regulate filamentous growth, a complex differentiation response that occurs under specific environmental conditions. To identify new aspects of filamentous growth regulation, we used a novel screening approach (called secretion profiling) that measures release of the extracellular domain of Msb2p, the signaling mucin which functions at the head of the filamentous growth (FG) MAPK pathway. Secretion profiling of complementary genomic collections showed that many of the pathways that regulate filamentous growth (RAS, RIM101, OPI1, and RTG) were also required for FG pathway activation. This regulation sensitized the FG pathway to multiple stimuli and synchronized it to the global signaling network. Several of the regulators were required for MSB2 expression, which identifies the MSB2 promoter as a target “hub” where multiple signals converge. Accessibility to the MSB2 promoter was further regulated by the histone deacetylase (HDAC) Rpd3p(L), which positively regulated FG pathway activity and filamentous growth. Our findings provide the first glimpse of a global regulatory hierarchy among the pathways that control filamentous growth. Systems-level integration of signaling circuitry is likely to coordinate other regulatory networks that control complex behaviors.
Zdroje
1. DoroquezDB
RebayI
2006 Signal integration during development: mechanisms of EGFR and Notch pathway function and cross-talk. Crit Rev Biochem Mol Biol 41 339 385
2. HurlbutGD
KankelMW
LakeRJ
Artavanis-TsakonasS
2007 Crossing paths with Notch in the hyper-network. Curr Opin Cell Biol 19 166 175
3. WagnerEF
NebredaAR
2009 Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 9 537 549
4. GimenoCJ
LjungdahlPO
StylesCA
FinkGR
1992 Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68 1077 1090
5. SchwartzMA
MadhaniHD
2004 Principles of map kinase signaling specificity in Saccharomyces cerevisiae. Annu Rev Genet 38 725 748
6. VerstrepenKJ
KlisFM
2006 Flocculation, adhesion and biofilm formation in yeasts. Mol Microbiol 60 5 15
7. JinR
DobryCJ
McCownPJ
KumarA
2008 Large-scale analysis of yeast filamentous growth by systematic gene disruption and overexpression. Mol Biol Cell 19 284 296
8. BornemanAR
Leigh-BellJA
YuH
BertoneP
GersteinM
2006 Target hub proteins serve as master regulators of development in yeast. Genes Dev 20 435 448
9. PrinzS
Avila-CampilloI
AldridgeC
SrinivasanA
DimitrovK
2004 Control of yeast filamentous-form growth by modules in an integrated molecular network. Genome Res 14 380 390
10. MadhaniHD
GalitskiT
LanderES
FinkGR
1999 Effectors of a developmental mitogen-activated protein kinase cascade revealed by expression signatures of signaling mutants. Proc Natl Acad Sci U S A 96 12530 12535
11. LoHJ
KohlerJR
DiDomenicoB
LoebenbergD
CacciapuotiA
1997 Nonfilamentous C. albicans mutants are avirulent. Cell 90 939 949
12. WhitewayM
BachewichC
2007 Morphogenesis in Candida albicans. Annu Rev Microbiol 61 529 553
13. NobileCJ
MitchellAP
2006 Genetics and genomics of Candida albicans biofilm formation. Cell Microbiol 8 1382 1391
14. RobertsRL
FinkGR
1994 Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth. Genes Dev 8 2974 2985
15. MadhaniHD
FinkGR
1997 Combinatorial control required for the specificity of yeast MAPK signaling. Science 275 1314 1317
16. MadhaniHD
StylesCA
FinkGR
1997 MAP kinases with distinct inhibitory functions impart signaling specificity during yeast differentiation. Cell 91 673 684
17. MoschHU
KublerE
KrappmannS
FinkGR
BrausGH
1999 Crosstalk between the Ras2p-controlled mitogen-activated protein kinase and cAMP pathways during invasive growth of Saccharomyces cerevisiae. Mol Biol Cell 10 1325 1335
18. VinodPK
SenguptaN
BhatPJ
VenkateshKV
2008 Integration of global signaling pathways, cAMP-PKA, MAPK and TOR in the regulation of FLO11. PLoS ONE 3 e1663 doi:10.1371/journal.pone.0001663
19. LambTM
MitchellAP
2003 The transcription factor Rim101p governs ion tolerance and cell differentiation by direct repression of the regulatory genes NRG1 and SMP1 in Saccharomyces cerevisiae. Mol Cell Biol 23 677 686
20. BarwellKJ
BoysenJH
XuW
MitchellAP
2005 Relationship of DFG16 to the Rim101p pH response pathway in Saccharomyces cerevisiae and Candida albicans. Eukaryot Cell 4 890 899
21. RothfelsK
TannyJC
MolnarE
FriesenH
CommissoC
2005 Components of the ESCRT pathway, DFG16, and YGR122w are required for Rim101 to act as a corepressor with Nrg1 at the negative regulatory element of the DIT1 gene of Saccharomyces cerevisiae. Mol Cell Biol 25 6772 6788
22. ReynoldsTB
2006 The Opi1p transcription factor affects expression of FLO11, mat formation, and invasive growth in Saccharomyces cerevisiae. Eukaryot Cell 5 1266 1275
23. KuchinS
VyasVK
CarlsonM
2002 Snf1 protein kinase and the repressors Nrg1 and Nrg2 regulate FLO11, haploid invasive growth, and diploid pseudohyphal differentiation. Mol Cell Biol 22 3994 4000
24. KuchinS
VyasVK
CarlsonM
2003 Role of the yeast Snf1 protein kinase in invasive growth. Biochem Soc Trans 31 175 177
25. CullenPJ
SpragueGFJr
2000 Glucose depletion causes haploid invasive growth in yeast. Proc Natl Acad Sci U S A 97 13619 13624
26. PalecekSP
ParikhAS
KronSJ
2000 Genetic analysis reveals that FLO11 upregulation and cell polarization independently regulate invasive growth in Saccharomyces cerevisiae. Genetics 156 1005 1023
27. MoschHU
FinkGR
1997 Dissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae. Genetics 145 671 684
28. CullenPJ
SabbaghWJr
GrahamE
IrickMM
van OldenEK
2004 A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev 18 1695 1708
29. SinghPK
HollingsworthMA
2006 Cell surface-associated mucins in signal transduction. Trends Cell Biol 16 467 476
30. ParkHO
BiE
2007 Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol Mol Biol Rev 71 48 96
31. VadaieN
DionneH
AkajagborDS
NickersonSR
KrysanDJ
2008 Cleavage of the signaling mucin Msb2 by the aspartyl protease Yps1 is required for MAPK activation in yeast. J Cell Biol 181 1073 1081
32. RobertsCJ
RaymondCK
YamashiroCT
StevensTH
1991 Methods for studying the yeast vacuole. Methods Enzymol 194 644 661
33. SchluterC
LamKK
BrummJ
WuBW
SaundersM
2008 Global Analysis of Yeast Endosomal Transport Identifies the Vps55/68 Sorting Complex. Mol Biol Cell 19 1282 1294
34. BonangelinoCJ
ChavezEM
BonifacinoJS
2002 Genomic screen for vacuolar protein sorting genes in Saccharomyces cerevisiae. Mol Biol Cell 13 2486 2501
35. WinzelerEA
ShoemakerDD
AstromoffA
LiangH
AndersonK
1999 Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285 901 906
36. GelperinDM
WhiteMA
WilkinsonML
KonY
KungLA
2005 Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes Dev 19 2816 2826
37. LiuH
StylesCA
FinkGR
1996 Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. Genetics 144 967 978
38. NiuW
LiZ
ZhanW
IyerVR
MarcotteEM
2008 Mechanisms of cell cycle control revealed by a systematic and quantitative overexpression screen in S. cerevisiae. PLoS Genet 4 e1000120 doi:10.1371/journal.pgen.1000120
39. PitoniakA
BirkayaB
DionneHS
VadiaeN
CullenPJ
2009 The Signaling Mucins Msb2 and Hkr1 Differentially Regulate the Filamentation MAPK Pathway and Contribute to a Multimodal Response. Mol Biol Cell
40. TatebayashiK
TanakaK
YangHY
YamamotoK
MatsushitaY
2007 Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. Embo J 26 3521 3533
41. KarunanithiSR
VadaieN
BirkayaB
DionneHM
JoshiJ
(SUBMITTED) Regulation and Functional Basis of Mucin Shedding in a Unicellular Eukaryote.
42. GuoB
StylesCA
FengQ
FinkGR
2000 A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. Proc Natl Acad Sci U S A 97 12158 12163
43. KrysanDJ
TingEL
AbeijonC
KroosL
FullerRS
2005 Yapsins are a family of aspartyl proteases required for cell wall integrity in Saccharomyces cerevisiae. Eukaryot Cell 4 1364 1374
44. AndrewsBJ
HerskowitzI
1989 The yeast SWI4 protein contains a motif present in developmental regulators and is part of a complex involved in cell-cycle-dependent transcription. Nature 342 830 833
45. BreedenL
MikesellGE
1991 Cell cycle-specific expression of the SWI4 transcription factor is required for the cell cycle regulation of HO transcription. Genes Dev 5 1183 1190
46. NasmythK
DirickL
1991 The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast. Cell 66 995 1013
47. OgasJ
AndrewsBJ
HerskowitzI
1991 Transcriptional activation of CLN1, CLN2, and a putative new G1 cyclin (HCS26) by SWI4, a positive regulator of G1-specific transcription. Cell 66 1015 1026
48. BaetzK
AndrewsB
1999 Regulation of cell cycle transcription factor Swi4 through auto-inhibition of DNA binding. Mol Cell Biol 19 6729 6741
49. BeanJM
SiggiaED
CrossFR
2005 High functional overlap between MluI cell-cycle box binding factor and Swi4/6 cell-cycle box binding factor in the G1/S transcriptional program in Saccharomyces cerevisiae. Genetics 171 49 61
50. BardwellL
2006 Mechanisms of MAPK signalling specificity. Biochem Soc Trans 34 837 841
51. AbdullahU
CullenPJ
2009 The tRNA modification complex elongator regulates the Cdc42-dependent mitogen-activated protein kinase pathway that controls filamentous growth in yeast. Eukaryot Cell 8 1362 1372
52. JiaY
RothermelB
ThorntonJ
ButowRA
1997 A basic helix-loop-helix-leucine zipper transcription complex in yeast functions in a signaling pathway from mitochondria to the nucleus. Mol Cell Biol 17 1110 1117
53. DilovaI
AronovaS
ChenJC
PowersT
2004 Tor signaling and nutrient-based signals converge on Mks1p phosphorylation to regulate expression of Rtg1.Rtg3p-dependent target genes. J Biol Chem 279 46527 46535
54. Ferreira JuniorJR
SpirekM
LiuZ
ButowRA
2005 Interaction between Rtg2p and Mks1p in the regulation of the RTG pathway of Saccharomyces cerevisiae. Gene 354 2 8
55. LiuZ
SekitoT
EpsteinCB
ButowRA
2001 RTG-dependent mitochondria to nucleus signaling is negatively regulated by the seven WD-repeat protein Lst8p. Embo J 20 7209 7219
56. GiannattasioS
LiuZ
ThorntonJ
ButowRA
2005 Retrograde response to mitochondrial dysfunction is separable from TOR1/2 regulation of retrograde gene expression. J Biol Chem 280 42528 42535
57. KligLS
HomannMJ
CarmanGM
HenrySA
1985 Coordinate regulation of phospholipid biosynthesis in Saccharomyces cerevisiae: pleiotropically constitutive opi1 mutant. J Bacteriol 162 1135 1141
58. WhiteMJ
HirschJP
HenrySA
1991 The OPI1 gene of Saccharomyces cerevisiae, a negative regulator of phospholipid biosynthesis, encodes a protein containing polyglutamine tracts and a leucine zipper. J Biol Chem 266 863 872
59. VothWP
YuY
TakahataS
KretschmannKL
LiebJD
2007 Forkhead proteins control the outcome of transcription factor binding by antiactivation. Embo J 26 4324 4334
60. KimTS
LeeSB
KangHS
2004 Glucose repression of STA1 expression is mediated by the Nrg1 and Sfl1 repressors and the Srb8-11 complex. Mol Cell Biol 24 7695 7706
61. MoschHU
RobertsRL
FinkGR
1996 Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 93 5352 5356
62. CarterGW
RuppS
FinkGR
GalitskiT
2006 Disentangling information flow in the Ras-cAMP signaling network. Genome Res 16 520 526
63. RobertsonLS
CaustonHC
YoungRA
FinkGR
2000 The yeast A kinases differentially regulate iron uptake and respiratory function. Proc Natl Acad Sci U S A 97 5984 5988
64. ZamanS
LippmanSI
SchneperL
SlonimN
BroachJR
2009 Glucose regulates transcription in yeast through a network of signaling pathways. Mol Syst Biol 5 245
65. RobertsCJ
NelsonB
MartonMJ
StoughtonR
MeyerMR
2000 Signaling and circuitry of multiple MAPK pathways revealed by a matrix of global gene expression profiles. Science 287 873 880
66. RuppS
SummersE
LoHJ
MadhaniH
FinkG
1999 MAP kinase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene. Embo J 18 1257 1269
67. ZamanS
LippmanSI
ZhaoX
BroachJR
2008 How Saccharomyces Responds to Nutrients. Annu Rev Genet
68. SantangeloGM
2006 Glucose signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70 253 282
69. Boy-MarcotteE
IkonomiP
JacquetM
1996 SDC25, a dispensable Ras guanine nucleotide exchange factor of Saccharomyces cerevisiae differs from CDC25 by its regulation. Mol Biol Cell 7 529 539
70. PoulletP
CrechetJB
BernardiA
ParmeggianiA
1995 Properties of the catalytic domain of sdc25p, a yeast GDP/GTP exchange factor of Ras proteins. Complexation with wild-type Ras2p, [S24N]Ras2p and [R80D, N81D]Ras2p. Eur J Biochem 227 537 544
71. TodaT
UnoI
IshikawaT
PowersS
KataokaT
1985 In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 40 27 36
72. SassP
FieldJ
NikawaJ
TodaT
WiglerM
1986 Cloning and characterization of the high-affinity cAMP phosphodiesterase of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 83 9303 9307
73. PanX
HeitmanJ
1999 Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol Cell Biol 19 4874 4887
74. van DykD
PretoriusIS
BauerFF
2005 Mss11p is a central element of the regulatory network that controls FLO11 expression and invasive growth in Saccharomyces cerevisiae. Genetics 169 91 106
75. RobertsonLS
FinkGR
1998 The three yeast A kinases have specific signaling functions in pseudohyphal growth. Proc Natl Acad Sci U S A 95 13783 13787
76. LorenzMC
PanX
HarashimaT
CardenasME
XueY
2000 The G protein-coupled receptor gpr1 is a nutrient sensor that regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Genetics 154 609 622
77. LemaireK
Van de VeldeS
Van DijckP
TheveleinJM
2004 Glucose and Sucrose Act as Agonist and Mannose as Antagonist Ligands of the G Protein-Coupled Receptor Gpr1 in the Yeast Saccharomyces cerevisiae. Mol Cell 16 293 299
78. HarashimaT
AndersonS
YatesJR3rd
HeitmanJ
2006 The kelch proteins Gpb1 and Gpb2 inhibit Ras activity via association with the yeast RasGAP neurofibromin homologs Ira1 and Ira2. Mol Cell 22 819 830
79. PeetersT
LouwetW
GeladeR
NauwelaersD
TheveleinJM
2006 Kelch-repeat proteins interacting with the Galpha protein Gpa2 bypass adenylate cyclase for direct regulation of protein kinase A in yeast. Proc Natl Acad Sci U S A 103 13034 13039
80. HarashimaT
HeitmanJ
2002 The Galpha protein Gpa2 controls yeast differentiation by interacting with kelch repeat proteins that mimic Gbeta subunits. Mol Cell 10 163 173
81. BroachJR
1991 RAS genes in Saccharomyces cerevisiae: signal transduction in search of a pathway. Trends Genet 7 28 33
82. CharizanisC
JuhnkeH
KremsB
EntianKD
1999 The oxidative stress response mediated via Pos9/Skn7 is negatively regulated by the Ras/PKA pathway in Saccharomyces cerevisiae. Mol Gen Genet 261 740 752
83. HasanR
LeroyC
IsnardAD
LabarreJ
Boy-MarcotteE
2002 The control of the yeast H2O2 response by the Msn2/4 transcription factors. Mol Microbiol 45 233 241
84. FabrizioP
LiouLL
MoyVN
DiasproA
ValentineJS
2003 SOD2 functions downstream of Sch9 to extend longevity in yeast. Genetics 163 35 46
85. LongoVD
EllerbyLM
BredesenDE
ValentineJS
GrallaEB
1997 Human Bcl-2 reverses survival defects in yeast lacking superoxide dismutase and delays death of wild-type yeast. J Cell Biol 137 1581 1588
86. SinclairD
MillsK
GuarenteL
1998 Aging in Saccharomyces cerevisiae. Annu Rev Microbiol 52 533 560
87. IgualJC
NavarroB
1996 Respiration and low cAMP-dependent protein kinase activity are required for high-level expression of the peroxisomal thiolase gene in Saccharomyces cerevisiae. Mol Gen Genet 252 446 455
88. RundlettSE
CarmenAA
KobayashiR
BavykinS
TurnerBM
1996 HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc Natl Acad Sci U S A 93 14503 14508
89. KadoshD
StruhlK
1997 Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell 89 365 371
90. KastenMM
DorlandS
StillmanDJ
1997 A large protein complex containing the yeast Sin3p and Rpd3p transcriptional regulators. Mol Cell Biol 17 4852 4858
91. LechnerT
CarrozzaMJ
YuY
GrantPA
EberharterA
2000 Sds3 (suppressor of defective silencing 3) is an integral component of the yeast Sin3[middle dot]Rpd3 histone deacetylase complex and is required for histone deacetylase activity. J Biol Chem 275 40961 40966
92. CarrozzaMJ
LiB
FlorensL
SuganumaT
SwansonSK
2005 Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123 581 592
93. ColinaAR
YoungD
2005 Raf60, a novel component of the Rpd3 histone deacetylase complex required for Rpd3 activity in Saccharomyces cerevisiae. J Biol Chem 280 42552 42556
94. QiM
ElionEA
2005 MAP kinase pathways. J Cell Sci 118 3569 3572
95. MurphyLO
BlenisJ
2006 MAPK signal specificity: the right place at the right time. Trends Biochem Sci 31 268 275
96. CookJG
BardwellL
KronSJ
ThornerJ
1996 Two novel targets of the MAP kinase Kss1 are negative regulators of invasive growth in the yeast Saccharomyces cerevisiae. Genes Dev 10 2831 2848
97. OlsonKA
NelsonC
TaiG
HungW
YongC
2000 Two regulators of Ste12p inhibit pheromone-responsive transcription by separate mechanisms. Mol Cell Biol 20 4199 4209
98. ChouS
LaneS
LiuH
2006 Regulation of mating and filamentation genes by two distinct Ste12 complexes in Saccharomyces cerevisiae. Mol Cell Biol 26 4794 4805
99. De NadalE
ZapaterM
AlepuzPM
SumoyL
MasG
2004 The MAPK Hog1 recruits Rpd3 histone deacetylase to activate osmoresponsive genes. Nature 427 370 374
100. VidalM
StrichR
EspositoRE
GaberRF
1991 RPD1 (SIN3/UME4) is required for maximal activation and repression of diverse yeast genes. Mol Cell Biol 11 6306 6316
101. BarralesRR
JimenezJ
IbeasJI
2008 Identification of novel activation mechanisms for FLO11 regulation in Saccharomyces cerevisiae. Genetics 178 145 156
102. LoWS
DranginisAM
1996 FLO11, a yeast gene related to the STA genes, encodes a novel cell surface flocculin. J Bacteriol 178 7144 7151
103. LambrechtsMG
BauerFF
MarmurJ
PretoriusIS
1996 Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. Proc Natl Acad Sci U S A 93 8419 8424
104. LoWS
DranginisAM
1998 The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol Biol Cell 9 161 171
105. ReynoldsTB
FinkGR
2001 Bakers' yeast, a model for fungal biofilm formation. Science 291 878 881
106. BardwellL
2004 A walk-through of the yeast mating pheromone response pathway. Peptides 25 1465 1476
107. ElionEA
2000 Pheromone response, mating and cell biology. Curr Opin Microbiol 3 573 581
108. NakayamaN
MiyajimaA
AraiK
1987 Common signal transduction system shared by STE2 and STE3 in haploid cells of Saccharomyces cerevisiae: autocrine cell-cycle arrest results from forced expression of STE2. Embo J 6 249 254
109. BenderA
SpragueGFJr
1986 Yeast peptide pheromones, a-factor and alpha-factor, activate a common response mechanism in their target cells. Cell 47 929 937
110. McDonaldCM
WagnerM
DunhamMJ
ShinME
AhmedNT
2009 The Ras/cAMP pathway and the CDK-like kinase Ime2 regulate the MAPK Smk1 and spore morphogenesis in Saccharomyces cerevisiae. Genetics 181 511 523
111. MasG
de NadalE
DechantR
de la ConcepcionML
LogieC
2009 Recruitment of a chromatin remodelling complex by the Hog1 MAP kinase to stress genes. Embo J 28 326 336
112. DunnKL
EspinoPS
DrobicB
HeS
DavieJR
2005 The Ras-MAPK signal transduction pathway, cancer and chromatin remodeling. Biochem Cell Biol 83 1 14
113. KurdistaniSK
RobyrD
TavazoieS
GrunsteinM
2002 Genome-wide binding map of the histone deacetylase Rpd3 in yeast. Nat Genet 31 248 254
114. MiottoB
SagnierT
BerengerH
BohmannD
PradelJ
2006 Chameau HAT and DRpd3 HDAC function as antagonistic cofactors of JNK/AP-1-dependent transcription during Drosophila metamorphosis. Genes Dev 20 101 112
115. SambrookJ
FritschEF
ManiatisT
1989 Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
116. RoseMD
WinstonF
HieterP
1990 Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
117. BaudinA
Ozier-KalogeropoulosO
DenouelA
LacrouteF
CullinC
1993 A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res 21 3329 3330
118. LongtineMS
McKenzieA3rd
DemariniDJ
ShahNG
WachA
1998 Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14 953 961
119. SchneiderBL
SeufertW
SteinerB
YangQH
FutcherAB
1995 Use of polymerase chain reaction epitope tagging for protein tagging in Saccharomyces cerevisiae. Yeast 11 1265 1274
120. GoldsteinAL
McCuskerJH
1999 Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15 1541 1553
121. LalouxI
JacobsE
DuboisE
1994 Involvement of SRE element of Ty1 transposon in TEC1-dependent transcriptional activation. Nucleic Acids Res 22 999 1005
122. ChantJ
PringleJR
1995 Patterns of bud-site selection in the yeast Saccharomyces cerevisiae. J Cell Biol 129 751 765
123. JennessDD
GoldmanBS
HartwellLH
1987 Saccharomyces cerevisiae mutants unresponsive to alpha-factor pheromone: alpha-factor binding and extragenic suppression. Mol Cell Biol 7 1311 1319
124. CullenPJ
SchultzJ
HoreckaJ
StevensonBJ
JigamiY
2000 Defects in protein glycosylation cause SHO1-dependent activation of a STE12 signaling pathway in yeast. Genetics 155 1005 1018
125. GietzRD
SchiestlRH
2007 Microtiter plate transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2 5 8
126. GietzRD
WoodsRA
2002 Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350 87 96
127. EisenMB
SpellmanPT
BrownPO
BotsteinD
1998 Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95 14863 14868
128. DeRisiJL
IyerVR
BrownPO
1997 Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278 680 686
129. LashkariDA
DeRisiJL
McCuskerJH
NamathAF
GentileC
1997 Yeast microarrays for genome wide parallel genetic and gene expression analysis. Proc Natl Acad Sci U S A 94 13057 13062
130. FazzioTG
KooperbergC
GoldmarkJP
NealC
BasomR
2001 Widespread collaboration of Isw2 and Sin3-Rpd3 chromatin remodeling complexes in transcriptional repression. Mol Cell Biol 21 6450 6460
131. YuMC
LammingDW
EskinJA
SinclairDA
SilverPA
2006 The role of protein arginine methylation in the formation of silent chromatin. Genes Dev 20 3249 3254
132. PfafflMW
2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29 e45
133. VoynovV
VerstrepenKJ
JansenA
RunnerVM
BuratowskiS
2006 Genes with internal repeats require the THO complex for transcription. Proc Natl Acad Sci U S A 103 14423 14428
134. McCaffreyG
ClayFJ
KelsayK
SpragueGFJr
1987 Identification and regulation of a gene required for cell fusion during mating of the yeast Saccharomyces cerevisiae. Mol Cell Biol 7 2680 2690
135. O'RourkeSM
HerskowitzI
2004 Unique and redundant roles for HOG MAPK pathway components as revealed by whole-genome expression analysis. Mol Biol Cell 15 532 542
136. RiversDM
SpragueGFJr
2003 Autocrine activation of the pheromone response pathway in matalpha2- cells is attenuated by SST2- and ASG7-dependent mechanisms. Mol Genet Genomics 270 225 233
137. HagenDC
McCaffreyG
SpragueGFJr
1991 Pheromone response elements are necessary and sufficient for basal and pheromone-induced transcription of the FUS1 gene of Saccharomyces cerevisiae. Mol Cell Biol 11 2952 2961
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 3
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Papillorenal Syndrome-Causing Missense Mutations in / Result in Hypomorphic Alleles in Mouse and Human
- Fatal Cardiac Arrhythmia and Long-QT Syndrome in a New Form of Congenital Generalized Lipodystrophy with Muscle Rippling (CGL4) Due to Mutations
- Deciphering Normal Blood Gene Expression Variation—The NOWAC Postgenome Study
- HAP2(GCS1)-Dependent Gamete Fusion Requires a Positively Charged Carboxy-Terminal Domain