Summary
The goal of this chapter is to examine some of the best-known examples of ultradian biochemical oscillations and to draw a comparison between these periodic phenomena and circadian rhythms. Successively considered in the first part of the chapter are (i) glycolytic oscillations observed in yeast and muscle, (ii) the periodic synthesis of cyclic AMP (cAMP) signals which govern aggregation and differentiation in the cellular slime mold Dictyostelium discoideum, and (iii) the mitotic oscillator that controls the early cell division cycles in amphibian embryos. For each of these biochemical rhythms, the salient experimental aspects and the insights provided by theoretical models are summarized in turn. The second part of the chapter is devoted to the mechanism of circadian rhythms in Drosophila. A theoretical model for circadian oscillations in the period protein (PER) is presented. This minimal model is based on multiple phosphorylation of PER and on the negative feedback exerted by PER on the transcription of the period gene. Parallels are drawn between the mechanisms underlying ultradian biochemical oscillations and the mechanism that governs the circadian, periodic variation of PER in Drosophila.
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References
Abbott L, Zeng H, Rosbash M (1995) A model of circadian rhythm generation in Drosophila. Submitted for publication.
Alcantara F, Monk M (1974) Signal propagation during aggregation in the slime mould Dictyostelium discoideum. J Gen Microbiol 85: 321–334.
Aronson BD, Johnson KA, Loros JL, Dunlap JC (1994) Negative feedback defining a circadian clock: autoregulation of the clock gene frequency. Science 263: 1578–1584.
Baylies MK, Bargiello TA, Jackson FR, Young MW (1987) Changes in abundance or structure of the per gene product can alter periodicity of the Drosophila clock. Nature 326: 390–392.
Baylies MK, Weiner L, Vosshall LB, Saez L, Young MW (1993) Genetic, molecular, and cellular studies of the per locus and its products in Drosophila melanogaster. In: Young MW (ed) Molecular genetics of biological rhythms. Marcel Dekker, New York, pp 123–153.
Berridge MJ, Rapp PE (1979) A comparative survey of the function, mechanism and control of cellular oscillations. J Exp Biol 81: 217–279.
Bliss RD, Painter PR, Marr AG (1982) Role of feedback inhibition in stabilizing the classical operon. J Theor Biol 97: 177–193.
Boiteux A, Goldbeter A, Hess B (1975) Control of oscillating glycolysis of yeast by stochastic, periodic, and steady source of substrate: a model and experimental study. Proc Natl Acad Sci USA 72: 3829–3833.
Bonner JT (1967) The cellular slime molds. Princeton University Press, Princeton, NJ.
Chance B, Schoener B, Elsaesser S (1964) Control of the waveform of oscillations of the reduced pyridine nucleotide level in a cell-free extract. Proc Natl Acad Sci USA 52: 337–341.
Chance B, Pye K, Higgins J (1967) Waveform generation by enzymatic oscillators. IEEE Spectrum 4: 79–86.
Chou HF, Berman N, Ipp E (1992) Oscillations of lactate released from islets of Langerhans: evidence for oscillatory glycolysis in b-cells. Am J Physiol 262: E800–E805.
Coté GG, Brody S (1986) Circadian rhythms in Drosophila melanogaster. analysis of period as a function of gene dosage at the per (period) locus. J Theor Biol 121: 487–503.
Cross F, Roberts J, Weintraub H (1989) Simple and complex cell cycles. Annu Rev Cell Biol 5: 341–395.
Curtin KD, Huang ZJ, Rosbash M (1995) Temporally regulated nuclear entry of the Drosophila period protein contributes to the circadian clock. Neuron 14: 365–372.
Devreotes PN (1989) Dictyostelium discoideum: A model system for cell-cell interactions in development. Science 245: 1054–1058.
Devreotes PN, Sherring JA (1985) Kinetics and concentration dependence of reversible cAMP-induced modification of the surface cAMP receptor in Dictyostelium. J Biol Chem 260: 6378–6384.
Dowse HB, Ringo JM (1993) Is the circadian clock a “meta-oscillator”? Evidence from studies of ultradian rhythms in Drosophila. In: Young MW (ed) Molecular genetics of biological rhythms. Marcel Dekker, New York, pp 195–220.
Draetta G (1990) Cell cycle control in eukaryotes: Molecular mechanism of cdc2 activation. Trends Biochem Sci 15: 378–383.
Drescher K, Cornelius G, Rensing L (1982) Phase response curves obtained by perturbing different variables of a 24 hr model oscillator based on translational control. J Theor Biol 94: 345–353.
Dulie V, Lees E, Reed SI (1992) Association of human cyclin E with a periodic G1 -S phase protein kinase. Science 257: 1958–1961.
Dunlap JC (1993) Genetic analysis of circadian clocks. Annu Rev Physiol 55: 683–728.
Durston AJ (1974) Pacemaker activity during aggregation in Dictyostelium discoideum. Dev Biol 37: 225–235.
Edery I, Zwiebel LJ, Dembinska ME, Rosbash M (1994) Temporal phosphorylation of the Drosophila period protein. Proc Natl Acad Sci USA 91: 2260–2264.
Edmunds LN Jr (1988) Cellular and molecular bases of biological clocks. Models and mechanisms for circadian timekeeping. Springer, New York.
Félix MA, Labbé JC, Dorée M, Hunt T, Karsenti E (1990) Triggering of cyclin degradation in interphase extracts of amphibian eggs by cdc2 kinase. Nature 346: 379–382.
Frenkel R (1968) Control of reduced diphosphopyridine nucleotide oscillations in beef heart extracts. I. Effect of modifiers of phosphofructokinase activity. Arch Biochem Biophys 125: 151–156.
Gerisch G (1987) Cyclic AMP and other signals controlling cell development and differentiation in Dictyostelium. Annu Rev Biochem 56: 853–879.
Gerisch G, Hess B (1974) Cyclic-AMP controlled oscillations in suspended Dictyostelium cells: their relation to morphogenetic cell interactions. Proc Natl Acad Sci USA 71: 2118–2122.
Gerisch G, Malchow D, Roos W, Wick U (1979) Oscillations of cyclic nucleotide concentrations in relation to the excitability of Dictyostelium cells. J Exp Biol 81: 33–47.
Gerisch G, Wick U (1975) Intracellular oscillations and release of cyclic AMP from Dictyostelium cells. Biochem Biophys Res Commun 65: 364–370.
Ghosh AK, Chance B (1964) Oscillations of glycolytic intermediates in yeast cells. Biochem Biophys Res Commun 16: 174–181.
Goldbeter A (1991) A minimal cascade model for the mitotic oscillator involving cyclin and cdc2 kinase. Proc Natl Acad Sci USA 88: 9107–9111.
Goldbeter A (1993) Modeling the mitotic oscillator driving the cell division cycle. Comments Theor Biol 3: 75–107.
Goldbeter A (1995a) Biochemical oscillations and cellular rhythms: the molecular bases of periodic and chaotic behaviour. Cambridge University Press, Cambridge, UK (in press).
Goldbeter A (1995b) A model for circadian oscillations in the Drosophila period protein (PER). Proc R Soc Lond B (in press).
Goldbeter A, Caplan SR (1976) Oscillatory enzymes. Annu Rev Biophys Bioeng 5: 449–476.
Goldbeter A, Lefever R (1972) Dissipative structures for an allosterie model. Application to glycolytic oscillations. Biophys J 12: 1302–1315.
Goldbeter A, Martiel JL (1988) Developmental control of a biological rhythm: the onset of cAMP oscillations in Dictyostelium cells. In: Markus M, Millier S, Nicolis G (eds) From chemical to biological organization. Springer, Berlin, pp 248–254.
Goldbeter A, Nicolis G (1976) An allosterie enzyme model with positive feedback applied to glycolytic oscillations. In: Snell F, Rosen R (eds) Progress in theoretical biology, vol 4. Academic Press, New York, pp 65–160.
Goldbeter A, Segel LA (1980) Control of developmental transitions in the cyclic AMP signaling system of Dictyostelium discoideum. Differentiation 17: 127–135.
Goodwin BC (1965) Oscillatory behavior in enzymatic control processes. Adv Enzyme Regul 3: 425–438.
Griffith JS (1968) Mathematics of cellular control processes. I. Negative feedback to one gene. J Theor Biol 20: 202–208.
Gundersen RE, Johnson R, Lilly P, Pitt G, Pupillo M, Sun T, Vaughan R, Devreotes PN (1989) Reversible phosphorylation of G-protein-coupled receptors controls cAMP oscillations in Dictyostelium. In: Goldbeter A (ed) Cell to cell signalling: from experiments to theoretical models. Academic Press, London, pp 477–488.
Hall JC, Rosbash M (1988) Mutations and molecules influencing biological rhythms. Annu Rev Neurosci 11: 373–393.
Hardin PE, Hall JC, Rosbash M (1990) Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343: 536–540.
Hardin PE, Hall JC, Rosbash M (1992) Circadian oscillations in period gene mRNA levels are transcriptionally regulated. Proc Natl Acad Sci USA 89: 11711–11715.
Hartwell LH, Weinert TA (1989) Checkpoints: Controls that ensure the order of cell cycle events. Science 246: 629–634.
Hess B, Boiteux A (1968) Control of glycolysis. In: Järnefelt J (ed) Regulatory functions of biological membranes. Elsevier, Amsterdam, pp 148–162.
Hess, B, Boiteux A (1971) Oscillatory phenomena in biochemistry. Annu Rev Biochem 40: 237–258.
Hess B, Boiteux A, Krüger J (1969) Cooperation of glycolytic enzymes. Adv Enzyme Regul 7: 149–167.
Higgins J (1964) A chemical mechanism for oscillation of glycolytic intermediates in yeast cells. Proc Natl Acad Sci USA 51: 989–994.
Hoffmann I, Clarke PR, Marcote MJ, Karsenti E, Draetta G (1993) Phosphorylation and activation of human cdc25-C by cdc2-cyclin B and its involvement in the self- amplification of MPF at mitosis. EMBO J 12: 53–63.
Huang ZJ, Edery I, Rosbash M (1993) PAS is a dimerization domain common to Drosophila Period and several transcription factors. Nature 364: 259–262.
Huang ZJ, Curtin KD, Rosbash M (1995) PER protein interactions and temperature compensation of a circadian clock in Drosophila. Science 267: 1169–1172.
Hunding A (1974) Limit cycles in enzyme systems with nonlinear negative feedback. Biophys Struct Mechan 1: 47–54.
Kauffman S, Wille JJ (1975) The mitotic oscillator in Physarum polycephalum. J Theor Biol 55: 47–93.
Konopka RJ (1979) Genetic dissection of the Drosophila circadian system. Fed Proc 38: 2602–2605.
Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci USA 68: 2112–2116.
Konopka RJ, Hamblen-Coyle MJ, Jamison CF, Hall JC (1994) An ultrashort clock mutation at the period locus of Drosophila melanogaster that reveals some new features of the fly’s circadian system. J Biol Rhythms 9: 189–216.
Konopka RJ, Pittendrigh CS, Orr D (1989) Reciprocal behaviour associated with altered homeostasis and photosensitivity of Drosophila clock mutants. J Neurogenet 6: 1–10.
Kronauer RE, Czeisler CA, Pilato S, Moore-Ede MC, Weitzman ED (1982) Mathematical model of the human circadian system with two interacting oscillators. Am J Physiol 242: R3–R17.
Kyriacou CP, Hall JC (1980) Circadian rhythm mutations in Drosophila melanogaster affect the short-term fluctuations in the male’s courtship song. Proc. Natl Acad Sci USA 77: 6729–6733.
Lakin-Thomas PL, Brody S, Coté GG (1991) Amplitude model for the effects of mutations and temperature on period and phase resetting of the Neurospora circadian oscillator. J Biol Rhythms 6: 281–297.
Landahl HD (1969) Some conditions for sustained oscillations in biochemical chains with feedback inhibition. Bull Math Biophys 31: 775–787.
Liu X, Zwiebel LJ, Hinton D, Benzer S, Hall JC, Rosbash M (1992) The period gene encodes a predominantly nuclear protein in adult Drosophila. J Neurosci 12: 2735–2744.
Lloyd D, Stupfel M (1991) The occurrence and functions of ultradian rhythms. Biol Rev 66: 275–299.
Martiel JL, Goldbeter A (1987) A model based on receptor desensitization for cyclic AMP signaling in Dictyostelium cells. Biophys J 52: 807–828.
Morales M, McKay D (1967) Biochemical oscillations in “controlled” systems. Biophys J 7: 621–625.
Murray AW, Hunt T (1993) The cell cycle: an introduction. Oxford University Press, Oxford.
Murray AW, Kirschner MW (1989a) Cyclin synthesis drives the early embryonic cell cycle. Nature 339: 275–280.
Murray AW, Kirschner MW (1989b) Dominoes and clocks: The union of two views of the cell cycle. Science 246: 614–621.
Novak B, Tyson JJ (1993a) Modeling the cell division cycle: M-phase trigger, oscillations, and size control. J Theor Biol 165: 101–134.
Novak B, Tyson JJ (1993b) Numerical analysis of a comprehensive model of M-phase control in Xenopus oocytes extracts and intact embryos. J Cell Science 106: 1153–1168.
Nurse P (1990) Universal control mechanism regulating onset of M-phase. Nature 344: 503–508.
O’Rourke B, Ramza BM, Marban E (1994) Oscillations of membrane current and excitability driven by metabolic oscillations in heart cells. Science 265: 962–966.
Pavlidis T (1973) Biological oscillators: their mathematical analysis. Academic Press, New York.
Pavlidis T, Kauzmann W (1969) Toward a quantitative biochemical model for circadian oscillators. Arch Biochem Biophys 132: 338–348.
Pittendrigh C (1960) Circadian rhythms and the circadian organization of living systems. Cold Spring Harbor Symp Quant Biol XXV: 159–184.
Pye EK (1969) Biochemical mechanisms underlying the metabolic oscillations in yeast. Can J Bot 47: 271–285.
Pye EK, Chance B (1966) Sustained sinusoidal oscillations of reduced pyridine nucleotide in a cell-free extract of S. carlsbergensis. Proc Natl Acad Sci USA 55: 888–894.
Rapp PE (1975) A theoretical investigation of a large class of biochemical oscillators. Math Biosci 25: 165–188.
Romond PC, Guilmot JM, Goldbeter A (1994) The mitotic oscillator: Temporal self- organization in a phosphorylation-dephosphorylation enzymatic cascade. Ber Bunsenges Phys Chem 98: 1152–1159.
Sassone-Corsi P (1994) Rhythmic transcription and autoregulatory loops: winding up the biological clock. Cell 78: 361–364.
Sehgal A, Price JL, Man B, Young MW (1994) Loss of circadian behavioral rhythms and per RNA oscillations in the Drosophila mutant timeless. Science 263: 1603–1606.
Seltcov EE (1968) Self-oscillations in glycolysis. 1. A simple kinetic model. Eur. J. Biochem. 4: 79–86.
Takahashi JS (1992) Circadian clock genes are ticking. Science 258: 238–240.
Takahashi JS (1993) Circadian-clock regulation of gene expression. Curr Opin Genet Dev 3: 301–309.
Takahashi JS, Kornhauser JM, Koumenis C, Eskin A (1993) Molecular approaches to understanding circadian oscillations. Annu Rev Physiol 55: 729–753.
Tornheim K, Andrés V, Schulz V (1991) Modulation by citrate of glycolytic oscillations in skeletal muscle extracts. J Biol Chem 266: 15675–15678.
Tyson JJ, Othmer HG (1978) The dynamics of feedback control circuits in biochemical pathways. In: Snell F, Rosen R (eds) Progress in Theoretical Biology, vol. 5. Academic Press, New York, pp 2–62.
Von Klitzing L, Betz A (1970) Metabolic control in flow systems. I. Sustained glycolytic oscillations in yeast suspensions under continuous substrate infusion. Arch Mikrobiol 71: 220–225.
Vosshall LB, Price JL, Sehgal A, Saez L, Young MW (1994) Block in nuclear localization of period protein by a second clock mutation, timeless. Science 263: 1606–1609.
Walter C (1970) The occurrence and the significance of limit cycle behavior in controlled biochemical systems. J Theor Biol 27: 259–272.
Wever RA (1972) Virtual synchronization towards the limits of the range of entrainment. J Theor Biol 36: 119–132.
Winfree AT (1972) Spiral waves of chemical activity. Science 175: 634–636.
Winfree AT (1980) The geometry of biological time. Springer, New York (reprinted as Springer Study Edition, 1990, Springer, Berlin ).
Yu Q, Jacquier AC, Citri Y, Hamblen M, Hall JC, Rosbash M (1987) Molecular mapping of point mutations in the period gene that stop or speed up biological clocks in Drosophila melanogaster. Proc Natl Acad Sci USA 84: 784–788.
Zeng H, Hardin PE, Rosbash M (1994) Constitutive overexpression of the Drosophila period protein inhibits period mRNA cycling. EMBO J 13: 3590–3598.
Zerr DM, Rosbash M, Hall JC, Siwicki KK (1990) Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J Neurosci 10: 2749–2762.
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Goldbeter, A. (1996). From Ultradian Biochemical Oscillations to Circadian Rhythms. In: Vanden Driessche, T., Guisset, JL., Petiau-de Vries, G.M. (eds) Membranes and Circadian Rythms. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-79903-7_4
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