The control of the controller: Molecular mechanisms for robust perfect adaptation and temperature compensation

Biophysical Journal

Volumn 97, Issue 5, 2009, Pages 1244-1253

  Xiao, Yu Ni ^a   Drengstig, Tormod ^a   Ruoff, Peter ^a  

^a UNIVERSITY OF STAVANGER   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CALCITONIN; CALCIUM; FERROPORTIN; HEPCIDIN; IRON; METAL ION; MITOGEN ACTIVATED PROTEIN KINASE; PARATHYROID HORMONE; VITAMIN D;

ARTICLE; BACTERIUM; BONE METABOLISM; CALCIUM HOMEOSTASIS; CALCIUM METABOLISM; CELL TRANSPORT; CHEMOTAXIS; EVOLUTIONARY ADAPTATION; HOMEOSTASIS; INTESTINE CELL; KINETICS; LIVER CELL; MACROPHAGE; MOLECULAR MECHANICS; PHOTORECEPTOR; PLASMA; TEMPERATURE ACCLIMATIZATION;

BACTERIA (MICROORGANISMS); MAMMALIA;

ALGORITHMS; BLOOD; BODY TEMPERATURE REGULATION; CALCIUM; COMPUTER SIMULATION; FEEDBACK, PHYSIOLOGICAL; HOMEOSTASIS; HUMANS; IRON; KINETICS; MODELS, BIOLOGICAL; TEMPERATURE;

EID: 70349598539     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.06.030     Document Type: Article

References (51)

1. Asthagiri, A. R., and D. A. Lauffenburger. 2000. Bioengineering models of cell signaling. Annu. Rev. Biomed. Eng. 2:31-53.
2. Carlson, J. M., and J. Doyle. 2002. Complexity and robustness. Proc. Natl. Acad. Sci. USA. 99 (Suppl 1):2538-2545.
3. Stelling, J., U. Sauer, Z. Szallasi, F. J. Doyle, III, and J. Doyle. 2004. Robustness of cellular functions. Cell. 118:675-685.
4. Kitano, H. 2007. Towards a theory of biological robustness. Mol. Syst. Biol. 3:1-7.
5. Berg, H. C., and P. M. Tedesco. 1975. Transient response to chemotactic stimuli in Escherichia coli. Proc. Natl. Acad. Sci. USA. 72:3235-3239.
6. Barkai, N., and S. Leibler. 1997. Robustness in simple biochemical networks. Nature. 387:913-917.
7. Alon, U., M. G. Surette, N. Barkai, and S. Leibler. 1999. Robustness in bacterial chemotaxis. Nature. 397:168-171.
8. Hansen, C. H., R. G. Endres, and N. S. Wingreen. 2008. Chemotaxis in Escherichia coli: a molecular model for robust precise adaptation. PLoS Comput. Biol. 4:0014-0027.
9. Ratliff, F., H. K. Hartline, and W. H. Miller. 1963. Spatial and temporal aspects of retinal inhibitory interaction. J. Opt. Soc. Am. 53:110-120.
10. Asthagiri, A. R., C. M. Nelson, A. F. Horwitz, and D. A. Lauffenburger. 1999. Quantitative relationship among integrin-ligand binding, adhesion, and signaling via focal adhesion kinase and extracellular signal-regulated kinase 2. J. Biol. Chem. 274:27119-27127.
11. Hao, N., M. Behar, T. C. Elston, and H. G. Dohlman. 2007. Systems biology analysis of G protein and MAP kinase signaling in yeast. Oncogene. 26:3254-3266. (Pubitemid 46763019)
12. Mettetal, J. T., D. Muzzey, C. Gómez-Uribe, and A. van Oudenaarden. 2008. The frequency dependence of osmo-adaptation in Saccharomyces cerevisiae. Science. 319:482-484.
13. Wilkie, J., M. Johnson, and K. Reza. 2002. Control Engineering. An Introductory Course. Palgrave, New York.
14. Yi, T. M., Y. Huang, M. I. Simon, and J. Doyle. 2000. Robust perfect adaptation in bacterial chemotaxis through integral feedback control. Proc. Natl. Acad. Sci. USA. 97:4649-4653.
15. El-Samad, H., J. P. Goff, and M. Khammash. 2002. Calcium homeostasis and parturient hypocalcemia: an integral feedback perspective. J. Theor. Biol. 214:17-29.
16. Radhakrishnan, K., and A. C. Hindmarsh. 1993. Description and Use of LSODE, the Livermore Solver for Ordinary Differential Equations. NASA Reference Publication 1327, Lawrence Livermore National Laboratory Report UCRL-ID-113855. National Aeronautics and Space Administration, Lewis Research Center, Cleveland, OH.
17. Ruoff, P., M. Vinsjevik, and L. Rensing. 2000. Temperature compensation in biological oscillators: a challenge for joint experimental and theoretical analysis. Comments Theor. Biol. 5:361-382.
18. Ruoff, P. 1992. Introducing temperature-compensation in any reaction kinetic oscillator model. J. Interdiscipl. Cycle Res. 23:92-99.
19. Ruoff, P., M. K. Christensen, J. Wolf, and R. Heinrich. 2003. Temperature dependency and temperature compensation in a model of yeast glycolytic oscillations. Biophys. Chem. 106:179-192.
20. Ruoff, P., J. J. Loros, and J. C. Dunlap. 2005. The relationship between FRQ-protein stability and temperature compensation in the Neurospora circadian clock. Proc. Natl. Acad. Sci. USA. 102:17681-17686.
21. Ruoff, P., M. Zakhartsev, and H. V. Westerhoff. 2007. Temperature compensation through systems biology. FEBS J. 274:940-950. (Pubitemid 46204414)
22. Heinrich, R., and S. Schuster. 1996. The Regulation of Cellular Systems. Chapman and Hall, New York.
23. Fell, D. 1997. Understanding the Control of Metabolism. Portland Press, London and Miami.
24. Aase, S. O., and P. Ruoff. 2008. Semi-algebraic optimization of temperature compensation in a general switch-type negative feedback model of circadian clocks. J. Math. Biol. 56:279-292.
25. Kacser, H., and J. A. Burns. 1979. Molecular democracy: who shares the controls? Biochem. Soc. Trans. 7:1149-1160.
26. Burns, J. A., A. Cornish-Bowden, A. K. Groen, R. Heinrich, H. Kacser, et al. 1985. Control analysis of metabolic systems. Trends Biochem. Sci. 19:16.
27. Levchenko, A., and P. A. Iglesias. 2002. Models of eukaryotic gradient sensing: application to chemotaxis of amoebae and neutrophils. Biophys. J. 82:50-63. (Pubitemid 34289781)
28. Ingalls, B. P., T.-M. Yi, and P. A. Iglesias. 2006. Using control theory to study biology. In System Modeling in Cellular Biology. Z. Szallasi, J. Stelling, and V. Periwal, editors. MIT Press, Cambridge, MA.
29. Alon, U. 2006. An Introduction to Systems Biology: Design Principles of Biological Circuits. Chapman & Hall, New York.
30. Csikasz-Nagy, A., and O. S. Soyer. 2008. Adaptive dynamics with a single two-state protein. J.R. Soc. Interface. 5 (Suppl 1):S41-S47.
31. Drengstig, T., H. R. Ueda, and P. Ruoff. 2008. Predicting perfect adaptation motifs in reaction kinetic networks. J. Phys. Chem. B. 112:16752-16758.
32. Andrews, N. C., and P. J. Schmidt. 2007. Iron homeostasis. Annu. Rev. Physiol. 69:69-85.
33. Donovan, A., C. A. Lima, J. L. Pinkus, G. S. Pinkus, L. I. Zon, et al. 2005. The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis. Cell Metab. 1:191-200. (Pubitemid 43960600)
34. Nemeth, E., M. S. Tuttle, J. Powelson, M. B. Vaughn, A. Donovan, et al. 2004. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science. 306:2090-2093. (Pubitemid 40007660)
35. Delaby, C., N. Pilard, A. S. Goncalves, C. Beaumont, and F. Canonne- Hergaux. 2005. Presence of the iron exporter ferroportin at the plasma membrane of macrophages is enhanced by iron loading and down-regulated by hepcidin. Blood. 106:3979-3984. (Pubitemid 41739041)
36. Molina, P. E. 2006. Endocrine Physiology. McGraw-Hill, Blacklick, OH.
37. Friedman, P. A. 1999. Calcium transport in the kidney. Curr. Opin. Nephrol. Hypertens. 8:589-595.
38. 2+ homeostasis in rat meiotic and postmeiotic spermatogenic cells. Reproduction. 122:545-551.
39. Hong, C. I., E. D. Conrad, and J. J. Tyson. 2007. A proposal for robust temperature compensation of circadian rhythms. Proc. Natl. Acad. Sci. USA. 104:1195-1200.
40. Hastings, J. W., and B. M. Sweeney. 1957. On the mechanism of temperature independence in a biological clock. Proc. Natl. Acad. Sci. USA. 43:804-811.
41. Bünning, E. 1963. The Physiological Clock. Springer-Verlag, Berlin.
42. Zimmerman, W. F., C. S. Pittendrigh, and T. Pavlidis. 1968. Temperature compensation of the circadian oscillation in Drosophila pseudoobscura and its entrainment by temperature cycles. J. Insect Physiol. 14:669-684.
43. Hazel, J. R., and C. L. Prosser. 1974. Molecular mechanisms of temperature compensation in poikilotherms. Physiol. Rev. 54:620-677.
44. Aronson, B. D., K. A. Johnson, and J. C. Dunlap. 1994. Circadian clock locus frequency: protein encoded by a single open reading frame defines period length and temperature compensation. Proc. Natl. Acad. Sci. USA. 91:7683-7687.
45. Rábai, G., and I. Hanazaki. 1999. Temperature compensation in the oscillatory hydrogen peroxide-thiosulfate-sulfite flow system. Chem. Comm. 19:1965-1966.
46. Kóvacs, K. M., and G. Rábai. 2002. Temperature-compensation in pH-oscillators. Phys. Chem. Chem. Phys. 4:5265-5269.
47. Edwards, K. D., J. R. Lynn, P. Gyula, F. Nagy, and A. J. Millar. 2005. Natural allelic variation in the temperature-compensation mechanisms of the Arabidopsis thaliana circadian clock. Genetics. 170:387-400. (Pubitemid 40800000)
48. Gould, P. D., J. C. Locke, C. Larue, M. Southern, S. J. Davis, et al. 2006. The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell. 18:1177-1187. (Pubitemid 43956124)
49. von Bertalanffy, L. 1975. Perspectives on General System Theory. George Braziller, New York.
50. Sontag, E. D. 2004. Some new directions in control theory inspired by systems biology. Syst. Biol. (Stevenage). 1:9-18.
51. Wolkenhauer, O., S. N. Sreenath, P. Wellstead, M. Ullah, and K. H. Cho. 2005. Asystems- and signal-oriented approach to intracellular dynamics. Biochem. Soc. Trans. 33:507-515.