Metabolic Respiration Induces AMPK- and Ire1p-Dependent Activation of the p38-Type HOG MAPK Pathway


In fungal species, differentiation to the filamentous/hyphal cell type is critical for entry into host cells and virulence. Comparative RNA sequencing was used to explore the pathways that regulate differentiation to the filamentous cell type in yeast. This approach uncovered a role for the stress-response MAPK pathway, HOG, during the increased metabolic respiration that induces filamentous growth. In this context, the AMPK Snf1p and ER stress kinase Ire1p regulated the HOG pathway. Cross-modulation between the HOG and filamentous growth (ERK-type) MAPK pathways optimized the differentiation response. The regulatory circuit described here may extend to behaviors in metazoans.


Vyšlo v časopise: Metabolic Respiration Induces AMPK- and Ire1p-Dependent Activation of the p38-Type HOG MAPK Pathway. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004734
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pgen.1004734

Souhrn

In fungal species, differentiation to the filamentous/hyphal cell type is critical for entry into host cells and virulence. Comparative RNA sequencing was used to explore the pathways that regulate differentiation to the filamentous cell type in yeast. This approach uncovered a role for the stress-response MAPK pathway, HOG, during the increased metabolic respiration that induces filamentous growth. In this context, the AMPK Snf1p and ER stress kinase Ire1p regulated the HOG pathway. Cross-modulation between the HOG and filamentous growth (ERK-type) MAPK pathways optimized the differentiation response. The regulatory circuit described here may extend to behaviors in metazoans.


Zdroje

1. NobileCJ, MitchellAP (2006) Genetics and genomics of Candida albicans biofilm formation. Cell Microbiol 8: 1382–1391.

2. LengelerKB, DavidsonRC, D'SouzaC, HarashimaT, ShenWC, et al. (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64: 746–785.

3. CullenPJ, SpragueGFJr (2012) The regulation of filamentous growth in yeast. Genetics 190: 23–49.

4. BrucknerS, MoschHU (2012) Choosing the right lifestyle: adhesion and development in Saccharomyces cerevisiae. FEMS Microbiol Rev 36: 25–58.

5. SaitoH, PosasF (2012) Response to hyperosmotic stress. Genetics 192: 289–318.

6. HohmannS (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66: 300–372.

7. SchwartzMA, MadhaniHD (2004) Principles of map kinase signaling specificity in Saccharomyces cerevisiae. Annu Rev Genet 38: 725–748.

8. QiM, ElionEA (2005) MAP kinase pathways. J Cell Sci 118: 3569–3572.

9. MurphyLO, BlenisJ (2006) MAPK signal specificity: the right place at the right time. Trends Biochem Sci 31: 268–275.

10. YangHY, TatebayashiK, YamamotoK, SaitoH (2009) Glycosylation defects activate filamentous growth Kss1 MAPK and inhibit osmoregulatory Hog1 MAPK. Embo J 28: 1380–1391.

11. CullenPJ, SabbaghWJr, GrahamE, IrickMM, van OldenEK, et al. (2004) A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev 18: 1695–1708.

12. O'RourkeSM, HerskowitzI (1998) The Hog1 MAPK prevents cross talk between the HOG and pheromone response MAPK pathways in Saccharomyces cerevisiae. Genes Dev 12: 2874–2886.

13. PosasF, Wurgler-MurphySM, MaedaT, WittenEA, ThaiTC, et al. (1996) Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 “two-component” osmosensor. Cell 86: 865–875.

14. PosasF, SaitoH (1997) Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. Science 276: 1702–1705.

15. WuC, JansenG, ZhangJ, ThomasDY, WhitewayM (2006) Adaptor protein Ste50p links the Ste11p MEKK to the HOG pathway through plasma membrane association. Genes Dev 20: 734–746.

16. PitoniakA, BirkayaB, DionneHM, VadaieN, CullenPJ (2009) The Signaling Mucins Msb2 and Hkr1 Differentially Regulate the Filamentation Mitogen-activated Protein Kinase Pathway and Contribute to a Multimodal Response. Molecular Biology of the Cell 20: 3101–3114.

17. TatebayashiK, TanakaK, YangHY, YamamotoK, MatsushitaY, et al. (2007) Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. Embo J 26: 3521–3533.

18. MaedaT, TakekawaM, SaitoH (1995) Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science 269: 554–558.

19. PosasF, SaitoH (1998) Activation of the yeast SSK2 MAP kinase kinase kinase by the SSK1 two-component response regulator. Embo J 17: 1385–1394.

20. MaedaT, Wurgler-MurphySM, SaitoH (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369: 242–245.

21. OtaIM, VarshavskyA (1993) A yeast protein similar to bacterial two-component regulators. Science 262: 566–569.

22. RobertsCJ, NelsonB, MartonMJ, StoughtonR, MeyerMR, et al. (2000) Signaling and circuitry of multiple MAPK pathways revealed by a matrix of global gene expression profiles. Science 287: 873–880.

23. 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.

24. PosasF, ChambersJR, HeymanJA, HoefflerJP, de NadalE, et al. (2000) The transcriptional response of yeast to saline stress. J Biol Chem 275: 17249–17255.

25. McCleanMN, ModyA, BroachJR, RamanathanS (2007) Cross-talk and decision making in MAP kinase pathways. Nat Genet 39: 409–414.

26. RuaD, TobeBT, KronSJ (2001) Cell cycle control of yeast filamentous growth. Curr Opin Microbiol 4: 720–727.

27. 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.

28. KronSJ, StylesCA, FinkGR (1994) Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae. Mol Biol Cell 5: 1003–1022.

29. 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.

30. 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.

31. 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.

32. CullenPJ, SpragueGFJr (2002) The roles of bud-site-selection proteins during haploid invasive growth in yeast. Mol Biol Cell 13: 2990–3004.

33. TaheriN, KohlerT, BrausGH, MoschHU (2000) Asymmetrically localized Bud8p and Bud9p proteins control yeast cell polarity and development. Embo J 19: 6686–6696.

34. BrewsterJL, GustinMC (1994) Positioning of cell growth and division after osmotic stress requires a MAP kinase pathway. Yeast 10: 425–439.

35. BaltanasR, BushA, CoutoA, DurrieuL, HohmannS, et al. (2013) Pheromone-induced morphogenesis improves osmoadaptation capacity by activating the HOG MAPK pathway. Sci Signal 6: ra26.

36. WarringerJ, HultM, RegotS, PosasF, SunnerhagenP (2010) The HOG pathway dictates the short-term translational response after hyperosmotic shock. Mol Biol Cell 21: 3080–3092.

37. TeigeM, ScheiklE, ReiserV, RuisH, AmmererG (2001) Rck2, a member of the calmodulin-protein kinase family, links protein synthesis to high osmolarity MAP kinase signaling in budding yeast. Proc Natl Acad Sci U S A 98: 5625–5630.

38. Bilsland-MarchesanE, ArinoJ, SaitoH, SunnerhagenP, PosasF (2000) Rck2 kinase is a substrate for the osmotic stress-activated mitogen-activated protein kinase Hog1. Mol Cell Biol 20: 3887–3895.

39. LeeJ, ReiterW, DohnalI, GregoriC, Beese-SimsS, et al. (2013) MAPK Hog1 closes the S. cerevisiae glycerol channel Fps1 by phosphorylating and displacing its positive regulators. Genes Dev 27: 2590–2601.

40. Nadal-RibellesM, CondeN, FloresO, Gonzalez-VallinasJ, EyrasE, et al. (2012) Hog1 bypasses stress-mediated down-regulation of transcription by RNA polymerase II redistribution and chromatin remodeling. Genome Biol 13: R106.

41. De NadalE, ZapaterM, AlepuzPM, SumoyL, MasG, et al. (2004) The MAPK Hog1 recruits Rpd3 histone deacetylase to activate osmoresponsive genes. Nature 427: 370–374.

42. MasG, de NadalE, DechantR, Rodriguez de la ConcepcionML, LogieC, et al. (2009) Recruitment of a chromatin remodelling complex by the Hog1 MAP kinase to stress genes. EMBO J 28: 326–336.

43. ZapaterM, SohrmannM, PeterM, PosasF, de NadalE (2007) Selective requirement for SAGA in Hog1-mediated gene expression depending on the severity of the external osmostress conditions. Mol Cell Biol 27: 3900–3910.

44. ChowdhuryS, SmithKW, GustinMC (1992) Osmotic stress and the yeast cytoskeleton: phenotype-specific suppression of an actin mutation. J Cell Biol 118: 561–571.

45. YuzyukT, AmbergDC (2003) Actin recovery and bud emergence in osmotically stressed cells requires the conserved actin interacting mitogen-activated protein kinase kinase kinase Ssk2p/MTK1 and the scaffold protein Spa2p. Mol Biol Cell 14: 3013–3026.

46. YuzyukT, FoehrM, AmbergDC (2002) The MEK kinase Ssk2p promotes actin cytoskeleton recovery after osmotic stress. Mol Biol Cell 13: 2869–2880.

47. ShockTR, ThompsonJ, YatesJR3rd, MadhaniHD (2009) Hog1 mitogen-activated protein kinase (MAPK) interrupts signal transduction between the Kss1 MAPK and the Tec1 transcription factor to maintain pathway specificity. Eukaryot Cell 8: 606–616.

48. DavenportKD, WilliamsKE, UllmannBD, GustinMC (1999) Activation of the Saccharomyces cerevisiae filamentation/invasion pathway by osmotic stress in high-osmolarity glycogen pathway mutants. Genetics 153: 1091–1103.

49. WestfallPJ, ThornerJ (2006) Analysis of mitogen-activated protein kinase signaling specificity in response to hyperosmotic stress: use of an analog-sensitive HOG1 allele. Eukaryot Cell 5: 1215–1228.

50. LevinDE (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189: 1145–1175.

51. Rodriguez-PenaJM, GarciaR, NombelaC, ArroyoJ (2010) The high-osmolarity glycerol (HOG) and cell wall integrity (CWI) signalling pathways interplay: a yeast dialogue between MAPK routes. Yeast 27: 495–502.

52. GarciaR, Rodriguez-PenaJM, BermejoC, NombelaC, ArroyoJ (2009) The High Osmotic Response and Cell Wall Integrity Pathways Cooperate to Regulate Transcriptional Responses to Zymolyase-induced Cell Wall Stress in Saccharomyces cerevisiae. J Biol Chem 284: 10901–10911.

53. BermejoC, RodriguezE, GarciaR, Rodriguez-PenaJM, Rodriguez de la ConcepcionML, et al. (2008) The sequential activation of the yeast HOG and SLT2 pathways is required for cell survival to cell wall stress. Mol Biol Cell 19: 1113–1124.

54. DohlmanHG, ThornerJW (2001) Regulation of G protein-initiated signal transduction in yeast: paradigms and principles. Annu Rev Biochem 70: 703–754.

55. ElionEA (2000) Pheromone response, mating and cell biology. Curr Opin Microbiol 3: 573–581.

56. RagniE, PibergerH, NeupertC, Garcia-CantalejoJ, PopoloL, et al. (2011) The genetic interaction network of CCW12, a Saccharomyces cerevisiae gene required for cell wall integrity during budding and formation of mating projections. BMC Genomics 12: 107.

57. YasharB, IrieK, PrintenJA, StevensonBJ, SpragueGFJr, et al. (1995) Yeast MEK-dependent signal transduction: response thresholds and parameters affecting fidelity. Mol Cell Biol 15: 6545–6553.

58. Rodriguez-PenaJM, Diez-MunizS, BermejoC, NombelaC, ArroyoJ (2013) Activation of the yeast cell wall integrity MAPK pathway by zymolyase depends on protease and glucanase activities and requires the mucin-like protein Hkr1 but not Msb2. FEBS Lett 587: 3675–3680.

59. AriasP, Diez-MunizS, GarciaR, NombelaC, Rodriguez-PenaJM, et al. (2011) Genome-wide survey of yeast mutations leading to activation of the yeast cell integrity MAPK pathway: novel insights into diverse MAPK outcomes. BMC Genomics 12: 390.

60. CullenPJ, SpragueGFJr (2000) Glucose depletion causes haploid invasive growth in yeast. Proc Natl Acad Sci U S A 97: 13619–13624.

61. CaustonHC, RenB, KohSS, HarbisonCT, KaninE, et al. (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12: 323–337.

62. GaschAP, SpellmanPT, KaoCM, Carmel-HarelO, EisenMB, et al. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241–4257.

63. BicknellAA, TourtellotteJ, NiwaM (2010) Late phase of the endoplasmic reticulum stress response pathway is regulated by Hog1 MAP kinase. J Biol Chem 285: 17545–17555.

64. Torres-QuirozF, Garcia-MarquesS, CoriaR, Randez-GilF, PrietoJA (2010) The activity of yeast Hog1 MAPK is required during endoplasmic reticulum stress induced by tunicamycin exposure. J Biol Chem 285: 20088–20096.

65. NagalakshmiU, WangZ, WaernK, ShouC, RahaD, et al. (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344–1349.

66. Randez-GilF, SanzP, EntianKD, PrietoJA (1998) Carbon source-dependent phosphorylation of hexokinase PII and its role in the glucose-signaling response in yeast. Mol Cell Biol 18: 2940–2948.

67. HeifetzA, KeenanRW, ElbeinAD (1979) Mechanism of action of tunicamycin on the UDP-GlcNAc:dolichyl-phosphate Glc-NAc-1-phosphate transferase. Biochemistry 18: 2186–2192.

68. BroC, KnudsenS, RegenbergB, OlssonL, NielsenJ (2005) Improvement of galactose uptake in Saccharomyces cerevisiae through overexpression of phosphoglucomutase: example of transcript analysis as a tool in inverse metabolic engineering. Appl Environ Microbiol 71: 6465–6472.

69. LashkariDA, DeRisiJL, McCuskerJH, NamathAF, GentileC, et al. (1997) Yeast microarrays for genome wide parallel genetic and gene expression analysis. Proc Natl Acad Sci U S A 94: 13057–13062.

70. TraversKJ, PatilCK, WodickaL, LockhartDJ, WeissmanJS, et al. (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101: 249–258.

71. PatilC, WalterP (2001) Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr Opin Cell Biol 13: 349–355.

72. AlepuzPM, JovanovicA, ReiserV, AmmererG (2001) Stress-induced map kinase Hog1 is part of transcription activation complexes. Mol Cell 7: 767–777.

73. TatebayashiK, YamamotoK, TanakaK, TomidaT, MaruokaT, et al. (2006) Adaptor functions of Cdc42, Ste50, and Sho1 in the yeast osmoregulatory HOG MAPK pathway. Embo J 25: 3033–3044.

74. KarunanithiS, CullenPJ (2012) The filamentous growth MAPK Pathway Responds to Glucose Starvation Through the Mig1/2 transcriptional repressors in Saccharomyces cerevisiae. Genetics 192: 869–887.

75. SuranaU, RobitschH, PriceC, SchusterT, FitchI, et al. (1991) The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell 65: 145–161.

76. BooherRN, DeshaiesRJ, KirschnerMW (1993) Properties of Saccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins. EMBO J 12: 3417–3426.

77. ZahnerJE, HarkinsHA, PringleJR (1996) Genetic analysis of the bipolar pattern of bud site selection in the yeast Saccharomyces cerevisiae. Mol Cell Biol 16: 1857–1870.

78. ChenT, HirokoT, ChaudhuriA, InoseF, LordM, et al. (2000) Multigenerational cortical inheritance of the Rax2 protein in orienting polarity and division in yeast. Science 290: 1975–1978.

79. ChantJ, HerskowitzI (1991) Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway. Cell 65: 1203–1212.

80. VernaJ, LodderA, LeeK, VagtsA, BallesterR (1997) A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 94: 13804–13809.

81. GavriasV, AndrianopoulosA, GimenoCJ, TimberlakeWE (1996) Saccharomyces cerevisiae TEC1 is required for pseudohyphal growth. Mol Microbiol 19: 1255–1263.

82. MadhaniHD, FinkGR (1997) Combinatorial control required for the specificity of yeast MAPK signaling. Science 275: 1314–1317.

83. HaoN, BeharM, ParnellSC, TorresMP, BorchersCH, et al. (2007) A systems-biology analysis of feedback inhibition in the Sho1 osmotic-stress-response pathway. Curr Biol 17: 659–667.

84. BrewsterJL, de ValoirT, DwyerND, WinterE, GustinMC (1993) An osmosensing signal transduction pathway in yeast. Science 259: 1760–1763.

85. MurakamiY, TatebayashiK, SaitoH (2008) Two adjacent docking sites in the yeast Hog1 mitogen-activated protein (MAP) kinase differentially interact with the Pbs2 MAP kinase kinase and the Ptp2 protein tyrosine phosphatase. Mol Cell Biol 28: 2481–2494.

86. CarlsonM (1999) Glucose repression in yeast. Curr Opin Microbiol 2: 202–207.

87. SchneperL, DuvelK, BroachJR (2004) Sense and sensibility: nutritional response and signal integration in yeast. Curr Opin Microbiol 7: 624–630.

88. BhatPJ, MurthyTV (2001) Transcriptional control of the GAL/MEL regulon of yeast Saccharomyces cerevisiae: mechanism of galactose-mediated signal transduction. Mol Microbiol 40: 1059–1066.

89. JohnstonM, FlickJS, PextonT (1994) Multiple mechanisms provide rapid and stringent glucose repression of GAL gene expression in Saccharomyces cerevisiae. Mol Cell Biol 14: 3834–3841.

90. LohrD, VenkovP, ZlatanovaJ (1995) Transcriptional regulation in the yeast GAL gene family: a complex genetic network. FASEB J 9: 777–787.

91. JohnstonM (1987) A model fungal gene regulatory mechanism: the GAL genes of Saccharomyces cerevisiae. Microbiol Rev 51: 458–476.

92. HoldenHM, RaymentI, ThodenJB (2003) Structure and function of enzymes of the Leloir pathway for galactose metabolism. J Biol Chem 278: 43885–43888.

93. Melcher K (1997) Galactose metabolism in Saccharomyces cerevisiae: a paradigm for eukaryotic gene regulation. FK Zimmermann, K-D Entian (Eds), Yeast Sugar Metabolism, Technomic Publishing Inc, Lancaster, PA 235–269.

94. GruningNM, RinnerthalerM, BluemleinK, MullederM, WamelinkMM, et al. (2011) Pyruvate kinase triggers a metabolic feedback loop that controls redox metabolism in respiring cells. Cell Metab 14: 415–427.

95. RuckenstuhlC, ButtnerS, Carmona-GutierrezD, EisenbergT, KroemerG, et al. (2009) The Warburg effect suppresses oxidative stress induced apoptosis in a yeast model for cancer. PLoS One 4: e4592.

96. AlexandreA, LehningerAL (1984) Bypasses of the antimycin a block of mitochondrial electron transport in relation to ubisemiquinone function. Biochim Biophys Acta 767: 120–129.

97. PhamNA, RobinsonBH, HedleyDW (2000) Simultaneous detection of mitochondrial respiratory chain activity and reactive oxygen in digitonin-permeabilized cells using flow cytometry. Cytometry 41: 245–251.

98. CampoML, KinnallyKW, TedeschiH (1992) The effect of antimycin A on mouse liver inner mitochondrial membrane channel activity. J Biol Chem 267: 8123–8127.

99. CelenzaJL, CarlsonM (1986) A yeast gene that is essential for release from glucose repression encodes a protein kinase. Science 233: 1175–1180.

100. SchullerHJ, EntianKD (1991) Extragenic suppressors of yeast glucose derepression mutants leading to constitutive synthesis of several glucose-repressible enzymes. J Bacteriol 173: 2045–2052.

101. McCartneyRR, SchmidtMC (2001) Regulation of Snf1 kinase. Activation requires phosphorylation of threonine 210 by an upstream kinase as well as a distinct step mediated by the Snf4 subunit. J Biol Chem 276: 36460–36466.

102. TreitelMA, KuchinS, CarlsonM (1998) Snf1 protein kinase regulates phosphorylation of the Mig1 repressor in Saccharomyces cerevisiae. Mol Cell Biol 18: 6273–6280.

103. OstlingJ, RonneH (1998) Negative control of the Mig1p repressor by Snf1p-dependent phosphorylation in the absence of glucose. Eur J Biochem 252: 162–168.

104. SmithFC, DaviesSP, WilsonWA, CarlingD, HardieDG (1999) The SNF1 kinase complex from Saccharomyces cerevisiae phosphorylates the transcriptional repressor protein Mig1p in vitro at four sites within or near regulatory domain 1. FEBS Lett 453: 219–223.

105. ZhouH, WinstonF (2001) NRG1 is required for glucose repression of the SUC2 and GAL genes of Saccharomyces cerevisiae. Bmc Genetics 2: 5.

106. VallierLG, CarlsonM (1994) Synergistic release from glucose repression by mig1 and ssn mutations in Saccharomyces cerevisiae. Genetics 137: 49–54.

107. OrlovaM, OzcetinH, BarrettL, KuchinS (2010) Roles of the Snf1-activating kinases during nitrogen limitation and pseudohyphal differentiation in Saccharomyces cerevisiae. Eukaryot Cell 9: 208–214.

108. HerscovicsA, OrleanP (1993) Glycoprotein biosynthesis in yeast. FASEB J 7: 540–550.

109. GracyRW, NoltmannEA (1968) Studies on phosphomannose isomerase. II. Characterization as a zinc metalloenzyme. J Biol Chem 243: 4109–4116.

110. SmithDJ, ProudfootA, FriedliL, KligLS, ParaviciniG, et al. (1992) PMI40, an intron-containing gene required for early steps in yeast mannosylation. Mol Cell Biol 12: 2924–2930.

111. CoxJS, ShamuCE (1993) WalterP (1993) Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73: 1197–1206.

112. RonD, WalterP (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519–529.

113. CoxJS, WalterP (1996) A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87: 391–404.

114. TanigawaM, KiharaA, TerashimaM, TakaharaT, MaedaT (2012) Sphingolipids regulate the yeast high-osmolarity glycerol response pathway. Mol Cell Biol 32: 2861–2870.

115. SinghKK (2000) The Saccharomyces cerevisiae Sln1p-Ssk1p two-component system mediates response to oxidative stress and in an oxidant-specific fashion. Free Radic Biol Med 29: 1043–1050.

116. HaghnazariE, HeyerWD (2004) The Hog1 MAP kinase pathway and the Mec1 DNA damage checkpoint pathway independently control the cellular responses to hydrogen peroxide. DNA Repair (Amst) 3: 769–776.

117. Wurgler-MurphySM, MaedaT, WittenEA, SaitoH (1997) Regulation of the Saccharomyces cerevisiae HOG1 mitogen-activated protein kinase by the PTP2 and PTP3 protein tyrosine phosphatases. Mol Cell Biol 17: 1289–1297.

118. LongtineMS, DeMariniDJ, ValencikML, Al-AwarOS, FaresH, et al. (1996) The septins: roles in cytokinesis and other processes. Curr Opin Cell Biol 8: 106–119.

119. GladfelterAS, PringleJR, LewDJ (2001) The septin cortex at the yeast mother-bud neck. Curr Opin Microbiol 4: 681–689.

120. ReynoldsTB, FinkGR (2001) Bakers' yeast, a model for fungal biofilm formation. Science 291: 878–881.

121. KarunanithiS, JoshiJ, ChavelC, BirkayaB, GrellL, et al. (2012) Regulation of mat responses by a differentiation MAPK pathway in Saccharomyces cerevisiae. PLoS ONE 7: e32294.

122. KarunanithiS, VadaieN, ChavelCA, BirkayaB, JoshiJ, et al. (2010) Shedding of the mucin-like flocculin Flo11p reveals a new aspect of fungal adhesion regulation. Curr Biol 20: 1389–1395.

123. ChenJ, ChenJ, LaneS, LiuH (2002) A conserved mitogen-activated protein kinase pathway is required for mating in Candida albicans. Mol Microbiol 46: 1335–1344.

124. CsankC, SchroppelK, LebererE, HarcusD, MohamedO, et al. (1998) Roles of the Candida albicans mitogen-activated protein kinase homolog, Cek1p, in hyphal development and systemic candidiasis. Infect Immun 66: 2713–2721.

125. KohlerJR, FinkGR (1996) Candida albicans strains heterozygous and homozygous for mutations in mitogen-activated protein kinase signaling components have defects in hyphal development. Proc Natl Acad Sci U S A 93: 13223–13228.

126. San JoseC, MongeRA, Perez-DiazR, PlaJ, NombelaC (1996) The mitogen-activated protein kinase homolog HOG1 gene controls glycerol accumulation in the pathogenic fungus Candida albicans. J Bacteriol 178: 5850–5852.

127. SmithDA, NichollsS, MorganBA, BrownAJ, QuinnJ (2004) A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans. Mol Biol Cell 15: 4179–4190.

128. EismanB, Alonso-MongeR, RomanE, AranaD, NombelaC, et al. (2006) The Cek1 and Hog1 mitogen-activated protein kinases play complementary roles in cell wall biogenesis and chlamydospore formation in the fungal pathogen Candida albicans. Eukaryot Cell 5: 347–358.

129. MitchellAP (1998) Dimorphism and virulence in Candida albicans. Curr Opin Microbiol 1: 687–692.

130. BiswasS, RoyM, DattaA (2003) N-acetylglucosamine-inducible CaGAP1 encodes a general amino acid permease which co-ordinates external nitrogen source response and morphogenesis in Candida albicans. Microbiology 149: 2597–2608.

131. LawrenceCL, BottingCH, AntrobusR, CootePJ (2004) Evidence of a new role for the high-osmolarity glycerol mitogen-activated protein kinase pathway in yeast: regulating adaptation to citric acid stress. Mol Cell Biol 24: 3307–3323.

132. HickmanMJ, SpattD, WinstonF (2011) The Hog1 mitogen-activated protein kinase mediates a hypoxic response in Saccharomyces cerevisiae. Genetics 188: 325–338.

133. PanaderoJ, PallottiC, Rodriguez-VargasS, Randez-GilF, PrietoJA (2006) A downshift in temperature activates the high osmolarity glycerol (HOG) pathway, which determines freeze tolerance in Saccharomyces cerevisiae. J Biol Chem 281: 4638–4645.

134. VendrellA, PosasF (2011) Sir2 plays a key role in cell fate determination upon SAPK activation. Aging (Albany NY) 3: 1163–1168.

135. FanM, RheeJ, St-PierreJ, HandschinC, PuigserverP, et al. (2004) Suppression of mitochondrial respiration through recruitment of p160 myb binding protein to PGC-1alpha: modulation by p38 MAPK. Genes Dev 18: 278–289.

136. PuigserverP, RheeJ, LinJ, WuZ, YoonJC, et al. (2001) Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPARgamma coactivator-1. Mol Cell 8: 971–982.

137. XiX, HanJ, ZhangJZ (2001) Stimulation of glucose transport by AMP-activated protein kinase via activation of p38 mitogen-activated protein kinase. J Biol Chem 276: 41029–41034.

138. LinCC, ChengTL, TsaiWH, TsaiHJ, HuKH, et al. (2012) Loss of the respiratory enzyme citrate synthase directly links the Warburg effect to tumor malignancy. Sci Rep 2: 785.

139. CoxJS, ChapmanRE, WalterP (1997) The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol Biol Cell 8: 1805–1814.

140. MearesGP, HughesKJ, NaatzA, PapaFR, UranoF, et al. (2011) IRE1-dependent activation of AMPK in response to nitric oxide. Mol Cell Biol 31: 4286–4297.

141. KomurovK, TsengJT, MullerM, SeviourEG, MossTJ, et al. (2012) The glucose-deprivation network counteracts lapatinib-induced toxicity in resistant ErbB2-positive breast cancer cells. Mol Syst Biol 8: 596.

142. ChenX, IliopoulosD, ZhangQ, TangQ, GreenblattMB, et al. (2014) XBP1 promotes triple-negative breast cancer by controlling the HIF1alpha pathway. Nature 508: 103–107.

143. YoungRM, AckermanD, QuinnZL, MancusoA, GruberM, et al. (2013) Dysregulated mTORC1 renders cells critically dependent on desaturated lipids for survival under tumor-like stress. Genes Dev 27: 1115–1131.

144. GreenblattMB, ShimJH, GlimcherLH (2013) Mitogen-activated protein kinase pathways in osteoblasts. Annu Rev Cell Dev Biol 29: 63–79.

145. TrovatiM, DoronzoG, BaraleC, VaccherisC, RussoI, et al. (2014) Leptin and vascular smooth muscle cells. Curr Pharm Des 20: 625–634.

146. Sambrook J FEF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

147. Rose MD, Winston F., and Hieter P. (1990) Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

148. 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.

149. FaresH, GoetschL, PringleJR (1996) Identification of a developmentally regulated septin and involvement of the septins in spore formation in Saccharomyces cerevisiae. J Cell Biol 132: 399–411.

150. MadhaniHD, StylesCA, FinkGR (1997) MAP kinases with distinct inhibitory functions impart signaling specificity during yeast differentiation. Cell 91: 673–684.

151. EllisCD, WangF, MacDiarmidCW, ClarkS, LyonsT, et al. (2004) Zinc and the Msc2 zinc transporter protein are required for endoplasmic reticulum function. J Cell Biol 166: 325–335.

152. GoldsteinAL, McCuskerJH (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541–1553.

153. 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.

154. TrapnellC, PachterL, SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111.

155. RobinsonMD, McCarthyDJ, SmythGK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140.

156. ReinerA, YekutieliD, BenjaminiY (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19: 368–375.

157. LivakKJ, SchmittgenTD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25: 402–408.

158. LeeMJ, DohlmanHG (2008) Coactivation of G protein signaling by cell-surface receptors and an intracellular exchange factor. Curr Biol 18: 211–215.

159. SchneiderCA, RasbandWS, EliceiriKW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675.

160. RyanO, ShapiroRS, KuratCF, MayhewD, BaryshnikovaA, et al. (2012) Global gene deletion analysis exploring yeast filamentous growth. Science 337: 1353–1356.

161. LiuH, StylesCA, FinkGR (1993) Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science 262: 1741–1744.

162. FonziWA, IrwinMY (1993) Isogenic strain construction and gene mapping in Candida albicans. Genetics 134: 717–728.

163. BlankenshipJR, FanningS, HamakerJJ, MitchellAP (2010) An extensive circuitry for cell wall regulation in Candida albicans. PLoS Pathog 6: e1000752.

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