A systems biology analysis of long and short-term memories of osmotic stress adaptation in fungi
详细信息    查看全文
  • 作者:Tao You (1) (7)
    Piers Ingram (2)
    Mette D Jacobsen (3)
    Emily Cook (4)
    Andrew McDonagh (5)
    Thomas Thorne (6)
    Megan D Lenardon (3)
    Alessandro PS de Moura (1)
    M Carmen Romano (1)
    Marco Thiel (1)
    Michael Stumpf (6)
    Neil AR Gow (3)
    Ken Haynes (4)
    Celso Grebogi (1)
    Jaroslav Stark (8)
    Alistair JP Brown (3)
  • 刊名:BMC Research Notes
  • 出版年:2012
  • 出版时间:December 2012
  • 年:2012
  • 卷:5
  • 期:1
  • 全文大小:861KB
  • 参考文献:1. Maeda T, Wurgler-Murphy SM, Saito H: A two-component system that regulates an osmosensing MAP kinase cascade in yeast. / Nature 1994, 369:242鈥?45. CrossRef
    2. Posas F, Wurgler-Murphy SM, Maeda T, Witten EA, Thai TC, Saito H: YeastHOG1MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 鈥渢wo-component鈥?osmosensor. / Cell 1996, 86:865鈥?75. CrossRef
    3. Maeda T, Takekawa M, Saito H: Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. / Science 1995, 269:554鈥?58. CrossRef
    4. Posas F, Saito H: Osmotic activation of the HOG MAP kinase pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. / Science 1997, 276:1702鈥?705. CrossRef
    5. Hohmann S: Osmotic stress signaling and osmoadaptation in Yeasts. / Microbiol Mol Biol Rev 2002, 66:300鈥?72. CrossRef
    6. Hao N, Behar M, Parnell SC, Torres MP, Borchers CH, Elston TC, Dohlman HG: A systems-biology analysis of feedback inhibition in the Sho1 osmotic-stress-response pathway. / Curr Biol 2007, 17:659鈥?67. CrossRef
    7. Hao N, Zeng Y, Elston TC, Dohlman HG: Control of MAPK specificity by feedback phosphorylation of shared adaptor protein Ste50. / J Biol Chem 2008, 283:33798鈥?3802. CrossRef
    8. Sturm OE, Orton R, Grindlay J, Birtwistle M, Vyshemirsky V, Gilbert D, Calder M, Pitt A, Kholodenko B, Kolch W: The mammalian MAPK/ERK pathway exhibits properties of a negative feedback amplifier. / Sci Signal 2010,3(153):ra90. CrossRef
    9. Macia J, Regot S, Peeters T, Conde N, Sol茅 R, Posas F: Dynamic signaling in the Hog1 MAPK pathway relies on high basal signal transduction. / Sci Signal 2009, 2:ra13. CrossRef
    10. Sato N, Kawahara H, Toh-e A, Maeda T: Phosphorelay-regulated degradation of the yeast Ssk1p response regulator by the ubiquitin-proteasome system. / Mol Cell Biol 2003,23(18):6662鈥?671. CrossRef
    11. Hohmann S: Control of high osmolarity signaling in the yeast Saccharomyces cerevisiae. / FEBS Lett 2009, 583:4025鈥?029. CrossRef
    12. Tatebayashi K, Tanaka K, Yang HY, Yamamoto K, Matsushita Y, Tomida T, Imai M, Saito H: Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. / EMBO J 2007, 26:3521鈥?533. CrossRef
    13. Takahashi S, Pryciak PM: Identification of novel membrane-binding domains in multiple yeast Cdc42 effectors. / Mol Biol Cell 2007, 18:4945鈥?956. CrossRef
    14. Tatebayashi K, Yamamoto K, Tanaka K, Tomida T, Maruoka T, Kasukawa E, Saito H: Adaptor functions of Cdc42, Ste50, and Sho1 in the yeast osmoregulatory HOG MAPK pathway. / EMBO J 2006, 25:3033鈥?044. CrossRef
    15. Brown AJP, Haynes K, Gow NAR, Quinn J: Stress responses inCandida. In / Candida and Candidiasis. Edited by: Clancy CJ, Calderone RA. ASM Press, Clancy CJ, Calderone RA; 2011. in press
    16. Calderone RA: / Candida and Candidiasis. ASM Press, Washington, D.C; 2002.
    17. Alonso-Monge R, Navarro-Garcia F, Molero G, Diez-Orejas R, Gustin M, Pla J, Sanchez M, Nombela C: Role of the mitogen-activated protein kinase Hog1p in morphogenesis and virulence ofCandida albicans. / J Bacteriol 1999, 181:3058鈥?068.
    18. Arana DM, Nombela C, Alonso-Monge R, Pla J: The Pbs2 MAP kinase kinase is essential for the oxidative-stress response in the fungal pathogenCandida albicans. / Microbiol. 2005, 151:1033鈥?049. CrossRef
    19. Cheetham J, Smith DA, da Silva DA, Doris KS, Patterson MJ, Bruce CR, Quinn J: A single MAPKKK regulates the Hog1 MAPK pathway in the pathogenic fungusCandida albicans. / Mol Bio Cell 2007, 18:4603鈥?614. CrossRef
    20. Nikolaou E, Agrafioti I, Stumpf M, Quinn J, Stansfield I, Brown AJP: Phylogenetic diversity of stress signalling pathways in fungi. / BMC Evol Biol 2009, 9:44. CrossRef
    21. Alon U, Surette MG, Barkai N, Leibler S: Robustness in bacterial chemotaxis. / Nature 1999, 397:168鈥?71. CrossRef
    22. Leach MD, Tyc KM, Brown AJP, Klipp E: Modelling the regulation of thermal adaptation inCandida albicans, a major fungal pathogen of humans. / PLoS One 2012, 7:e3246.
    23. Ma W, Trusina A, El-Samad H, Lim WA, Tang C: Defining network topologies that can achieve biochemical adaptation. / Cell 2009,138(4):760鈥?3. CrossRef
    24. Yi TM, Huang Y, Simon MI, Doyle J: Robust perfect adaptation in bacterial chemotaxis through integral feedback control. / Proc Natl Acad Sci U S A 2000, 97:4649鈥?653. CrossRef
    25. El-Samad H, Goff JP, Khammash M: Calcium homeostasis and parturient hypocalcemia: an integral feedback perspective. / J Theor Biol 2002, 214:17鈥?9. CrossRef
    26. Cloutier M, Wellstead P: The control systems structures of energy metabolism. / J R Soc Interface 2010, 7:651鈥?65. CrossRef
    27. Muzzey D, G贸mez-Uribe CA, Mettetal JT, van Oudenaarden A: A systems-level analysis of perfect adaptation in yeast osmoregulation. / Cell 2009, 138:160鈥?71. CrossRef
    28. Gomez-Uribe C, Verghese GC, Mirny LA: Operating regimes of signaling cycles: statics, dynamics, and noise filtering. / PLoS Comp Biol 2007, 3:2487鈥?497. CrossRef
    29. Dihazi H, Kessler R, Eschrich K: High osmolarity glycerol (HOG) pathway-induced phosphorylation and activation of 6-phosphofructo-2-kinase are essential for glycerol accumulation and yeast cell proliferation under hyperosmotic stress. / J Biol Chem 2004,279(23):23961鈥?3968. CrossRef
    30. Westfall PJ, Patterson JC, Chen RE, Thorner J: Stress resistance and signal fidelity independent of nuclear MAPK function. / Proc Natl Acad Sci U S A 2008, 105:12212鈥?2217. CrossRef
    31. Klipp E, Nordlander B, Kr眉ger R, Gennemark P, Hohmann S: Integrative model of the response of yeast to osmotic shock. / Nat Biotech 2005, 23:975鈥?82. CrossRef
    32. Mollapour M, Piper PW: Hog1 mitogen-activated protein kinase phosphorylation targets the yeast Fps1 aquaglyceroporin for endocytosis, thereby rendering cells resistant to acetic acid. / Mol Cell Biol 2007, 27:6446鈥?456. CrossRef
    33. Gennemark P, Nordlander B, Hohmann S, Wedelin D: A simple mathematical model of adaptation to high osmolarity in yeast. / In Silico Biol 2006, 6:193鈥?14.
    34. Reed RH, Chudek JA, Foster R, Gadd GM: Osmotic significance of glycerol accumulation in exponentially growing yeasts. / Appl Environ Microbiol 1987, 53:2119鈥?123.
    35. Zi Z, Liebermeister W, Klipp E: A quantitative study of the Hog1 MAPK response to fluctuating osmotic stress in Saccharomyces cerevisiae. / PLoS One 2010, 5:e9522. CrossRef
    36. Enjalbert B, Smith DA, Cornell MJ, Alam I, Nicholls S, Brown AJP, Quinn J: Role of the Hog1 Stress-Activated Protein Kinase in the Global Transcriptional Response to Stress in the Fungal PathogenCandida albicans. / Molec. Biol. Cell 2006, 17:1018鈥?032. CrossRef
    37. Hersen P, McClean MN, Mahadevan L, Ramanathan S: Signal processing by the HOG MAP kinase pathway. / Proc Natl Acad Sci U S A 2008, 105:7165鈥?170. CrossRef
    38. Mettetal JT, Muzzey D, G贸mez-Uribe C, van Oudenaarden A: The frequency dependence of osmo-adaptation inSaccharomyces cerevisiae. / Science 2008, 319:482鈥?84. CrossRef
    39. Fonzi WA, Irwin MY: Isogenic strain construction and gene mapping inCandida albicans. / Genetics 1993, 134:717鈥?28.
    40. Nicholls S, Leach M, Priest C, Brown AJP: Role of the heat shock transcription factor, Hsf1, in a major fungal pathogen that is obligately associated with warm-blooded animals. / Molec. Microbiol. 2009, 74:844鈥?61. CrossRef
    41. Walker LA, MacCallum DM, Bertram G, Gow NAR, Odds FC, Brown AJP: Genome-wide analysis ofCandida albicansgene expression patterns during infection of the mammalian kidney. / Fungal Gen Biol 2009, 46:210鈥?19. CrossRef
    42. Murad AM, Lee PR, Broadbent ID, Barelle CJ, Brown AJ: CIp10, an efficient and convenient integrating vector forCandida albicans. / Yeast 2000, 16:325鈥?27. CrossRef
    43. Kaloriti D, Tillmann A, Cook E, Jacobsen MD, You T, Lenardon MD, Ames L, Barahona M, Chandrasekaran K, Coghill G, Goodman D, Gow NAR, Grebogi C, Ho HL, Ingram P, McDonagh A, de Moura APS, Pang W, Puttnam M, Radmaneshfar E, Romano MC, Silk D, Stark J, Stumpf M, Thiel M, Thorne T, Usher J, Yin Z, Haynes K, Brown AJP: Combinatorial stresses kill pathogenicCandidaspecies. / Medical Mycol 2012.
    44. Bradford MM: A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. / Anal Biochem 1976, 72:248鈥?54. CrossRef
  • 作者单位:Tao You (1) (7)
    Piers Ingram (2)
    Mette D Jacobsen (3)
    Emily Cook (4)
    Andrew McDonagh (5)
    Thomas Thorne (6)
    Megan D Lenardon (3)
    Alessandro PS de Moura (1)
    M Carmen Romano (1)
    Marco Thiel (1)
    Michael Stumpf (6)
    Neil AR Gow (3)
    Ken Haynes (4)
    Celso Grebogi (1)
    Jaroslav Stark (8)
    Alistair JP Brown (3)

    1. Institute for Complex Systems and Mathematical Biology, School of Natural and Computing Sciences, University of Aberdeen, Old Aberdeen, Aberdeen, AB24 3UE, UK
    7. Computational Biology, AstraZeneca, Innovative Medicines, Alderley Park, Macclesfield, Cheshire, SK10 4TG, UK
    2. Department of Mathematics, Imperial College London, London, SW7 2AZ, UK
    3. School of Medical Sciences, University of Aberdeen, Institute of Medical Sciences, Aberdeen, AB25 2ZD, UK
    4. Department of Biosciences, College of Life and Environmental Sciences, University of Exeter, Stocker Road, Exeter, EX4 4QD, UK
    5. Department of Microbiology, Imperial College London, The Flowers Building, London, SW7 2AZ, UK
    6. Centre for Bioinformatics, Division of Molecular Biosciences, Wolfson Building, Imperial College London, South Kensington Campus, London, SW7 2AY, UK
    8. Formally of the Department of Mathematics, Imperial College London, London, SW7 2AZ, UK
文摘
Background Saccharomyces cerevisiae senses hyperosmotic conditions via the HOG signaling network that activates the stress-activated protein kinase, Hog1, and modulates metabolic fluxes and gene expression to generate appropriate adaptive responses. The integral control mechanism by which Hog1 modulates glycerol production remains uncharacterized. An additional Hog1-independent mechanism retains intracellular glycerol for adaptation. Candida albicans also adapts to hyperosmolarity via a HOG signaling network. However, it remains unknown whether Hog1 exerts integral or proportional control over glycerol production in C. albicans. Results We combined modeling and experimental approaches to study osmotic stress responses in S. cerevisiae and C. albicans. We propose a simple ordinary differential equation (ODE) model that highlights the integral control that Hog1 exerts over glycerol biosynthesis in these species. If integral control arises from a separation of time scales (i.e. rapid HOG activation of glycerol production capacity which decays slowly under hyperosmotic conditions), then the model predicts that glycerol production rates elevate upon adaptation to a first stress and this makes the cell adapts faster to a second hyperosmotic stress. It appears as if the cell is able to remember the stress history that is longer than the timescale of signal transduction. This is termed the long-term stress memory. Our experimental data verify this. Like S. cerevisiae, C. albicans mimimizes glycerol efflux during adaptation to hyperosmolarity. Also, transient activation of intermediate kinases in the HOG pathway results in a short-term memory in the signaling pathway. This determines the amplitude of Hog1 phosphorylation under a periodic sequence of stress and non-stressed intervals. Our model suggests that the long-term memory also affects the way a cell responds to periodic stress conditions. Hence, during osmohomeostasis, short-term memory is dependent upon long-term memory. This is relevant in the context of fungal responses to dynamic and changing environments. Conclusions Our experiments and modeling have provided an example of identifying integral control that arises from time-scale separation in different processes, which is an important functional module in various contexts.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700