Negative feedback that improves information transmission in yeast signalling

Nature

Volumn 456, Issue 7223, 2008, Pages 755-761

  Yu, Richard C ^a   Pesce, C Gustavo ^a   Colman Lerner, Alejandro ^a,c   Lok, Larry ^a,d   Pincus, David ^a,e   Serra, Eduard ^a,f   Holl, Mark ^b,g   Benjamin, Kirsten ^a,h   Gordon, Andrew ^a,i   Brent, Roger ^a  

^a The Molecular Sciences Institute   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^d SYNOPSYS INC   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^g Arizona State University   (United States)

^h Amyris Biotechnologies   (United States)

ⁱ BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN SIGNALLING PROTEIN SST2; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE FUS3; SEX PHEROMONE; UNCLASSIFIED DRUG;

CONCENTRATION (COMPOSITION); DOSE-RESPONSE RELATIONSHIP; ENZYME ACTIVITY; FEEDBACK MECHANISM; MATING BEHAVIOR; PROTEIN; SEX PHEROMONE; SIGNALING; YEAST;

ARTICLE; CELL COMMUNICATION; CELL FUNCTION; DOSE RESPONSE; DOWNSTREAM PROCESSING; HORMONE RELEASE; INFORMATION DISSEMINATION; LIGAND BINDING; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; YEAST CELL;

SACCHAROMYCES CEREVISIAE;

EID: 57649130757     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature07513     Document Type: Article

References (47)

1. Dohlman, H. G. & Thorner, J. W. Regulation of G protein-initiated signal transduction in yeast: Paradigms and principles. Annu. Rev. Biochem. 70, 703-754 (2001).
2. Jackson, C. L. & Hartwell, L. H. Courtship in S. cerevisiae: Both cell types choose mating partners by responding to the strongest pheromone signal. Cell 63, 1039-1051 (1990).
3. Segall, J. E. Polarization of yeast cells in spatial gradients of alpha mating factor. Proc. Natl Acad. Sci. USA 90, 8332-8336 (1993).
4. Schrick, K., Garvik, B. & Hartwell, L. H. Mating in Saccharomyces cerevisiae: The role of the pheromone signal transduction pathway in the chemotropic response to pheromone. Genetics 147, 19-32 (1997).
5. Colman-Lerner, A. et al. Regulated cell-to-cell variation in a cell-fate decision system. Nature 437, 699-706 (2005).
6. Yi, T. M., Kitano, H. & Simon, M. I. A quantitative characterization of the yeast heterotrimeric G protein cycle. Proc. Natl Acad. Sci. USA 100, 10764-10769 (2003).
7. Cuatrecasas, P. Insulin-receptor interactions in adipose tissue cells: Direct measurement and properties. Proc. Natl Acad. Sci. USA 68, 1264-1268 (1971).
8. Kasai, M. & Changeux, J. P. In vitro excitation of purified membrane by cholinergic agonists. J. Membr. Biol. 6, 58-80 (1971).
9. Amir, S. M., Carraway, T. F. Jr, Kohn, L. D. & Winand, R. J. The binding of thyrotropin to isolated bovine thyroid plasma membranes. J. Biol. Chem. 248, 4092-4100 (1973).
10. Lin, S. Y. & Goodfriend, T. L. Angiotensin receptors. Am. J. Physiol. 218, 1319-1328 (1970).
11. Knauer, D. J., Wiley, H. S. & Cunningham, D. D. Relationship between epidermal growth factor receptor occupancy and mitogenic response. Quantitative analysis using a steady state model system. J. Biol. Chem. 259, 5623-5631 (1984).
12. Nagashima, T. et al. Quantitative transcriptional control of Erbb receptor signaling undergoes graded to biphasic response for cell differentiation. J. Biol. Chem. 282, 4045-4056 (2007).
13. Simons, S. S. Jr, Oshima, H. & Szapary, D. Higher levels of control: Modulation of steroid hormone-regulated gene transcription. Mol. Endocrinol. 6, 995-1002 (1992).
14. Rousseau, G. G. & Baxter, J. D. Glucocorticoid receptors. Monogr. Endocrinol. 12, 49-77 (1979).
15. Bloom, E. et al. Nuclear binding of glucocorticoid receptors: Relations between cytosol binding, activation and the biological response. J. Steroid Biochem. 12, 175-184 (1980).
16. Pedraza, J. M. & van Oudenaarden, A. Noise propagation in gene networks. Science 307, 1965-1969 (2005).
17. Black, H. S. Stabilized feed-back amplifiers. Electr. Eng. 53, 114-120 (1934).
18. Bhalla, U. S., Ram, P. T. & Iyengar, R. MAP kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network. Science 297, 1018-1023 (2002).
19. Black, J. W. & Leff, P. Operational models of pharmacological agonism. Proc. R. Soc. Lond. B 220, 141-162 (1983).
20. Savageau, M. A. Comparison of classical and autogenous systems of regulation in inducible operons. Nature 252, 546-549 (1974).
21. Becskei, A. & Serrano, L. Engineering stability in gene networks by autoregulation. Nature 405, 590-593 (2000).
22. Barkai, N. & Leibler, S. Robustness in simple biochemical networks. Nature 387, 913-917 (1997).
23. Gordon, A. et al. Single-cell quantification of molecules and rates using open-source microscope-based cytometry. Nature Methods 4, 175-181 (2007).
24. Gartner, A., Nasmyth, K. & Ammerer, G. Signal transduction in Saccharomyces cerevisiae requires tyrosine and threonine phosphorylation of Fus3 and Kss1. Genes Dev. 6, 1280-1292 (1992).
25. Tedford, K., Kim, S., Sa, D., Stevens, K. & Tyers, M. Regulation of the mating pheromone and invasive growth responses in yeast by two map kinase substrates. Curr. Biol. 7, 228-238 (1997).
26. Miyawaki, A. & Tsien, R. Y. Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Methods Enzymol. 327, 472-500 (2000).
27. van Drogen, F., Stucke, V. M., Jorritsma, G. & Peter, M. Map kinase dynamics in response to pheromones in budding yeast. Nature Cell Biol. 3, 1051-1059 (2001).
28. Bhattacharyya, R. P. et al. The ste5 scaffold allosterically modulates signaling output of the yeast mating pathway. Science 311, 822-826 (2006).
29. Maleri, S. et al. Persistent activation by constitutive Ste7 promotes Kss1-mediated invasive growth but fails to support Fus3-dependent mating in yeast. Mol. Cell. Biol. 24, 9221-9238 (2004).
30. Gruhler, A. et al. Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Mol. Cell. Proteomics 4, 310-327 (2005).
31. Shao, D., Zheng, W., Qiu, W., Ouyang, Q. & Tang, C. Dynamic studies of scaffold-dependent mating pathway in yeast. Biophys. J. 91, 3986-4001 (2006).
32. Bishop, A. C. et al. A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407, 395-401 (2000).
33. Ballon, D. R. et al. DEP-domain-mediated regulation of GPCR signaling responses. Cell 126, 1079-1093 (2006).
34. Heximer, S. P. & Blumer, K. J. RGS proteins: Swiss army knives in seven-transmembrane domain receptor signaling networks. Sci. STKE 2007, pe2 (2007).
35. May, L. T., Leach, K., Sexton, P. M. & Christopoulos, A. Allosteric modulation of G protein-coupled receptors. Annu. Rev. Pharmacol. Toxicol. 47, 1-51 (2007).
36. Budas, G. R., Churchill, E. N. & Mochly-Rosen, D. Cardioprotective mechanisms of PKC isozyme-selective activators and inhibitors in the treatment of ischemia-reperfusion injury. Pharmacol. Res. 55, 523-536 (2007).
37. Lindsley, C. W., Barnett, S. F., Layton, M. E. & Bilodeau, M. T. The PI3K/Akt pathway: Recent progress in the development of ATP-competitive and allosteric Akt kinase inhibitors. Curr. Cancer Drug Targets 8, 7-18 (2008).
38. Shannon, C. A mathematical theory of communication. Bell Syst. Tech. J. 27, 379-423 (1948).
39. Bialek, W., Rieke, F., de Ruyter van Steveninck, R. R. & Warland, D. Reading a neural code. Science 252, 1854-1857 (1991).
40. Tkacik, G., Callan, C. & Bialek, W. Information flow and optimization in transcriptional regulation. Proc. Natl. Acad. Sci. U.S.A. 26, 12265-12270 (2008).
41. Gregor, T., Tank, D. W., Wieschaus, E. F. & Bialek, W. Probing the limits to positional information. Cell 130, 153-164 (2007).
42. Ausubel, F. M. et al. Current Protocols in Molecular Biology (John Wiley & Sons, Inc., 1987-2008).
43. Guthrie, C. & Fink, G. R. Methods in Enzymology, Guide to Yeast Genetics and Molecular Biology (Academic, 1991).
44. Brun, R., Couet, O., Vandroni, C. & Zanarini, O. PAW Physics Analysis Workstation CERN program library entry q121 (CERN, Geneva, 1989).
45. Jenness, D. D., Burkholder, A. C. & Hartwell, L. H. Binding of alpha-factor pheromone to Saccharomyces cerevisiae a cells: Dissociation constant and number of binding sites. Mol. Cell. Biol. 6, 318-320 (1986).
46. Bajaj, A. et al.Afluorescent α-factor analogue exhibits multiple steps on binding to its g protein coupled receptor in yeast. Biochemistry 43, 13564-13578 (2004).
47. Andersson, J., Simpson, D. M., Qi, M., Wang, Y. & Elion, E. A. Differential input by Ste5 scaffold and Msg5 phosphatase route a MAPK cascade to multiple outcomes. EMBO J. 23, 2564-2576 (2004).