Cellular and Molecular Aspects of Circadian Oscillators: Models and Mechanisms for Biological Timekeeping
Abstract
Several approaches to elucidate the nature of biological clocks, particularly circadian oscillators, have emerged over the years (Hastings and Schweiger 1976; Edmunds 1988). These include the attempt to locate the anatomical loci responsible for generating these periodicities, efforts to trace the entrainment pathway for light signals (and other zeitgebers) from the photoreceptor(s) to the clock itself, the experimental dissection of the clock using chemicals and metabolic inhibitors and employing the exciting new techniques of molecular genetics, and the characterization of the coupling pathways and the transducing mechanisms between the clock(s) and the overt rhythmicities (hands) it drives. The results obtained by these experimental lines of attack, in turn, have provided the grist for several classes of biochemical and molecular model for autonomous circadian oscillators (COs).
Keywords
Circadian Rhythm Circadian Clock Clock Gene Compound Action Potential Circadian OscillatorPreview
Unable to display preview. Download preview PDF.
References
- Bargiello TA, Saez L, Baylies MK, Gasic G, Young MW, Spray DC (1987) The Drosophila clock gene per affects intercellular junctional communication. Nature 328: 686–691PubMedCrossRefGoogle Scholar
- 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: 390–392PubMedCrossRefGoogle Scholar
- Block GD, McMahon DG (1984) Cellular analysis of the Bulla ocular circadian pacemaker system. III. Localization of the circadian pacemaker. J Comp Physiol [A] 155: 387–395CrossRefGoogle Scholar
- Broda H, Brugge D, Homma K, Hastings JW (1986) Circadian communication between unicells? Effects on period by cell-conditioning of medium. Cell Biophys 8: 47–67PubMedGoogle Scholar
- Carré IA, Laval-Martin DL, Edmunds LN Jr (1989) Circadian changes in cyclic AMP levels in synchronously dividing and stationary-phase cultures of the achlorophyllous ZC mutant fo Euglena gracilis. J Cell Sci 94: 267–272Google Scholar
- Citri Y, Colot HV, Jacquier AC, Yu Q, Hall JC, Baltimore D, Rosbash M (1987) A family of unusually spliced biologically active transcripts encoded by a Drosophila clock gene. Nature 326:42–47PubMedCrossRefGoogle Scholar
- DeCoursey PJ, Buggy J (1988) Restoration of circadian locomotor activity in arrhythmic hamsters by fetal SCN transplants. Comp Endocrinol 7: 49–64Google Scholar
- DeCoursey PJ, Buggy J (1989) Circadian rhythmicity after neural transplant to hamster third ventricle: specificity of supra-chiasmatic nuclei. Brain Res 500: 263–275PubMedCrossRefGoogle Scholar
- Deng MD, Moureaux T, Ley decker MT, Caboche M (1990) Nitrate-reductase expression is under the control of a circadian rhythm and is light inducible in Nicotiana tabacum leaves. Planta 180: 257–261CrossRefGoogle Scholar
- Dowse HB, Ringo JM (1987) Further evidence that the circadian clock in Drosophila is a population of coupled ultradian oscillators. J Biol Rhythms 2: 65–76PubMedCrossRefGoogle Scholar
- Dowse HB, Ringo JM (1989) Rearing Drosophila in constant darkness produces phenocopies of period circadian clock mutants. Physiol Zool 62: 785–803Google Scholar
- Dowse HB, Hall JC, Ringo JM (1987) Circadian and ultradian rhythms in period mutants of Drosophila melanogaster. Behav Genet 17:19–35PubMedCrossRefGoogle Scholar
- Dunlap JC, Feldman JF (1988) On the role of protein synthesis in the circadian clock of Neurospora crassa. Proc Natl Acad Sci USA 85:1096–1100PubMedCrossRefGoogle Scholar
- Earnest DJ, Sladek CD (1987) Circadian vasopressin release from perifused rat suprachiasmatic explants in vitro: effects of acute stimulation. Brain Res 422: 398–402PubMedCrossRefGoogle Scholar
- Earnest DJ, Sladek CD, Gash DM, Wiegand SJ (1989) Specificity of circadian function in transplants of the fetal suprachiasmatic nucleus. J Neurosci 9: 2671–2677PubMedGoogle Scholar
- Editorial (1971) Is it time to wind up the biological clock? Nature [New Biol] 231: 97–98Google Scholar
- Edmunds LN Jr (1984) Physiology of circadian rhythms in microorganisms. Adv Microb Physiol 25: 61–148PubMedCrossRefGoogle Scholar
- Edmunds LN Jr (1988) Cellular and molecular bases of biological clocks. Springer, Berlin Heidelberg New YorkGoogle Scholar
- Edmunds LN Jr, Tamponnet C (1990) Oscillator control of cell division cycles in Euglena: role of calcium in circadian timekeeping. In: O’Day DH (ed) Calcium as an intracellular messenger in eucaryotic microbes. American Society for Microbiology, Washington, pp 97–123Google Scholar
- Feldman J (1982) Genetic approaches to circadian clocks. Annu Rev Plant Physiol 33: 583–608CrossRefGoogle Scholar
- Feldman JF (1988) Genetics of circadian clocks. Bot Acta 101: 128–132Google Scholar
- Feldman J, Dunlap JC (1983) Neurospora crassa: a unique system for studying circadian rhythms. Photochem Photobiol Rev 7: 319–368Google Scholar
- Fritz BJ, Kasai S, Matsui K (1989) Free cellular riboflavin is involved in phase shifting by light of the circadian clock in Neurospora crassa. Plant Cell Physiol 30: 557–564Google Scholar
- Gamalega NF, Shishko ED, Chyorny AP (1988) Preservation of circadian rhythms by human lymphocytes in vitro (in Russian). Bull Eksp Biol Med 106: 598–600Google Scholar
- Giuliano G, Hoffman NE, Ko K, Scolnik PA, Cashmore AR (1988) A light-entrained circadian clock controls transcription of several plant genes. EMBO J 4: 3635–3642Google Scholar
- Goto K, Laval-Martin D, Edmunds LN Jr (1985) Biochemical modeling of an autonomously oscillatory circadian clock in Euglena. Science 228:1284–1288PubMedCrossRefGoogle Scholar
- Grobbelaar N, Huang TC, Lin HY, Chow TJ (1986) Dinitrogen-fixing endogenous rhythm in Synechococcus RF-1. FEMS Microbiol Lett 37:173–178CrossRefGoogle Scholar
- Hall JC, Rosbash M (1987) Genetic and molecular analysis of biological rhythms. J Biol Rhythms 2:152–178CrossRefGoogle Scholar
- Hall JC, Rosbash M (1988) Mutations and molecules influencing biological rhythms. Annu Rev Neurosci 11: 373–393PubMedCrossRefGoogle Scholar
- Hamblen M, Zehring WA, Kyriacou CP, Reddy P, Yu Q, Wheeler DA, Zwiebel LJ, Konopka RJ, Robash M, Hall JC (1986) Germ-line transformation involving DNA from the period locus in Drosophila melanogaster: overlapping genomic fragments that restore circadian and ultradian rhythmicity to per 0 and per ~ mutants. J Neurogenet 3: 249–291PubMedCrossRefGoogle Scholar
- Hardin PE, Hall JC, Rosbash M (1990) Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343: 536–540PubMedCrossRefGoogle Scholar
- Hartwig R, Schweiger M, Schweiger R, Schweiger HG (1985) Identification of a high molecular weight polypeptide that may be part of the circadian clockwork in Acetabularia. Proc Natl Acad Sci 82: 6899–6902PubMedCrossRefGoogle Scholar
- Hartwig R, Schweiger R, Schweiger HG (1986) Circadian rhythm of the synthesis of a high molecular weight protein in anucleate cells of the green alga Acetabularia. Eur J Cell Biol 41:139–141Google Scholar
- Hastings JW, Schweiger HG (eds) (1976) The molecular basis of circadian rhythms. Abakon, Berlin (Dahlem Konferenzen)Google Scholar
- Hastings JW, Johnson C, Kondo T (1987) Action spectrum for phase shifting of the circadian rhythm of phototaxis in Chlamydomonas. Photochem Photobiol [Suppl] 45: 86SGoogle Scholar
- Inouye ST, Takahashi JS, Wollnik F, Turek FW (1988) Inhibitor of protein synthesis phase shifts a circadian pacemaker in mammalian SCN. Am J Physiol 255: R1055-R1058PubMedGoogle Scholar
- Jacklet JW (1984) Neural organization and cellular mechanisms of circadian pacemakers. Int Rev Cytol 89: 252–294Google Scholar
- Jacklet JW (ed) (1989 a) Neuronal and cellular oscillators. Dekker, New YorkGoogle Scholar
- Jacklet JW (1989 b) Circadian neuronal oscillators. In: Jacklet JW (ed) Neuronal and cellular oscillators. Dekker, New York, pp 483–527Google Scholar
- Jackson FR, Bargiello TA, Yun SH, Young MW (1986) Product of per locus of Drosophila shares homology with proteoglycans. Nature 320:185–187PubMedCrossRefGoogle Scholar
- James AA, Ewer J, Reddy P, Hakk JC, Rosbash M (1986) Embryonic expression of the period clock gene in the central nervous system of Drosophila melanogaster. EMBO J 5: 2313–2320PubMedGoogle Scholar
- Jenkins HA, Griffiths AJ, Lloyd D (1989) Simultaneous operation of ultradian and circadian rhythms in Chlamydomonas reinhardii. J Interdiscip Cycle Res 20: 257–264CrossRefGoogle Scholar
- Johnson CH, Hastings JW (1986) The elusive mechanism of the circadian clock. Am Sci 74: 29–36Google Scholar
- Khalsa SBS, Block GD (1986) The Bulla ocular circadian pacemaker is phase shifted by pentylenetetrazole independently of extracellular calcium concentration. Soc Neurosci Abstr 12: 596Google Scholar
- Khalsa SBS, Block GD (1988 a) Calcium channels mediate phase shifts of the Bulla circadian pacemaker. J Comp Physiol [A] 164:195–206CrossRefGoogle Scholar
- Khalsa SBS, Block GD (1988b) Phase-shifts of the Bulla ocular circadian pacemaker in the presence of calmodulin antagonists. Life Sci 43:1551–1556PubMedCrossRefGoogle Scholar
- Khalsa SBS, Block GD (1990) Calcium in phase control of the Bulla circadian pacemaker. Brain Res 506: 40–15PubMedCrossRefGoogle Scholar
- Kippert F (1987) Endocytobiotic coordination: intracellular calcium signalling and the origin of endogenous rhythms. Ann NY Acad Sci 503:476–495PubMedCrossRefGoogle Scholar
- Lakin-Thomas PL (1985) Biochemical genetics of the circadian rhythm in Neurospora crassa: studies on the eel strain. Thesis, University of California, San DiegoGoogle Scholar
- Lehman MN, Silver R, Gladstone WR, Kahn RM, Gibson M, Bittman EL (1987) Circadian rhythmicity restored by neural transplant. Immunocytochemical characterization of the graft and its integration with the host brain. J Neurosci 7: 1626–1638PubMedGoogle Scholar
- Lillo C (1989) An unusually rapid light-induced nitrate reductase mRNA pulse and circadian oscillations. Naturwissen-schaften 76: 526–528CrossRefGoogle Scholar
- Liu X, Lorenz L, Yu Q, Hall JC, Rosbash M (1988) Spatial and temporal expression of the period gene in Drosophila melanogaster. Genes Dev 2: 228–238PubMedCrossRefGoogle Scholar
- Li-Weber M, de Groot EJ, Schweiger HG (1987) Sequence homology to the Drosophila per locus in higher plant nuclear DNA and in Acetabularia chloroplast DNA. Mol Gen Genet 209:1–7PubMedCrossRefGoogle Scholar
- Lorenz LJ, Hall JC, Rosbash M (1989) Expression of a Drosophila mRNA is under circadian clock control during pupation. Development 107: 869–880PubMedGoogle Scholar
- Loros JJ, Denome SA, Dunlap JC (1989) Molecular cloning of genes under control of the circadian clock in Neurospora. Science 243: 385–388PubMedCrossRefGoogle Scholar
- Lotshaw DP, Jacklet JW (1987) Serotonin induced protein phosphorylation in the Aplysia eye. Comp Biochem Physiol 86C: 27–32Google Scholar
- McClung CR, Fox BA, Dunlap JC (1989) The Neurospora clock gene frequency shares a sequence element with the Drosophila clock gene period. Nature 339: 558–562PubMedCrossRefGoogle Scholar
- McMahon DG, Block GD (1987a) The Bulla ocular circadian pacemaker. I. Pacemaker neuron membrane potential controls phase through a calcium-dependent mechanism. J Comp Physiol [A] 161: 335–346CrossRefGoogle Scholar
- McMahon DG, Block GD (1987 b) The Bulla ocular circadian pacemaker. II. Chronic changes in membrane potential lengthen free running period. J Comp Physiol [A] 161: 347–354Google Scholar
- Milos P, Morse D, Hastings JW (1990) Circadian control over synthesis of many Gonyaulax proteins is at a translational level. Naturwissenschaften 77: 87–89PubMedCrossRefGoogle Scholar
- Mitsui A, Kumazawa S, Takahashi A, Ikemoto H, Cao S, Arai T (1986) Strategy by which nitrogen-fixing unicellular cyano-bacteria grow photoautotrophically. Nature 323: 720–722CrossRefGoogle Scholar
- Miwa I, Nagatoshi H, Horie T (1987) Circadian rhythmicity within single cells of Paramecium bursaria. J Biol Rhythms 2: 57–64PubMedCrossRefGoogle Scholar
- Moore RY (1983) Organization and function of a central nervous system circadian oscillator: the suprachiasmatic hypothalamic nucleus. Fed Proc 42: 2783–2789PubMedGoogle Scholar
- Moore RY, Card JP (1986) Visual pathways and the en-trainment of circadian rhythms. Ann NY Acad Sci 453:123–133CrossRefGoogle Scholar
- Morse D, Milos PM, Roux E, Hastings JW (1989) Circadian regulation of bioluminescence in Gonyaulax involves translational control. Proc Natl Acad Sci USA 86:172–176PubMedCrossRefGoogle Scholar
- Morse MJ, Crain RC, Satter RL (1987) Phosphatidylinositol cycle metabolites in Samanea saman pulvini. Plant Physiol 83: 640–644PubMedCrossRefGoogle Scholar
- Nagy F, Kay SA, Chua NH (1988 a) A circadian clock regulates transcription of the wheat Cab-1 gene. Genes Dev 2: 376–382CrossRefGoogle Scholar
- Nagy F, Kay SA, Chua NH (1988 b) Gene regulation by photochrome. Trends Genet 4: 37–42PubMedCrossRefGoogle Scholar
- Nakashima H (1986) Phase shifting of the circadian conidiation rhythm in Neurospora crassa by calmodulin antagonists. J Biol Rhythms 1:163–169PubMedCrossRefGoogle Scholar
- Nikaido SS, Takahashi JS (1989) Twenty-four hour oscillation of cAMP in chick pineal cells: role of cAMP in the acute and circadian regulation of melatonin production. Neuron 3:609–619PubMedCrossRefGoogle Scholar
- Ninnemann H (1979) Photoreceptors for circadian rhythms. Photochem Photobiol Rev 4: 207–265Google Scholar
- Olesiak W, Ungar A, Johnson CH, Hastings JW (1987) Are protein synthesis inhibition and phase shifting of the circadian clock in Gonyaulax correlated? J Biol Rhythms 2:121–138PubMedCrossRefGoogle Scholar
- Otto B, Grimm B, Ottersbach P, Kloppstech K (1988) Circadian control of the accumulation of mRNAs for light- and heat-in-ducible chloroplast proteins in pea (Pisum sativum L.). Plant Physiol 88: 21–25PubMedCrossRefGoogle Scholar
- Paulsen H, Bogorad L (1988) Diurnal and circadian rhythms in the accumulation and synthesis of mRNA for the light-harvesting chlorophyll a/b-binding protein in tobacco. Plant Physiol 88:1104–1109PubMedCrossRefGoogle Scholar
- Peleg L, Dotan A, Luzato P, Ashkenazi IE (1990) “Long ultra-dian” rhythms in red blood cells and ghost suspensions: possible involvement of cell membrane. In Vitro Cell Dev Biol 26: 978–982CrossRefGoogle Scholar
- Piechulla B (1988) Plastid and nuclear mRNA fluctuations in tomato leaves - diurnal and circadian rhythms during extended dark and light periods. Plant Mol Biol 11: 345–353CrossRefGoogle Scholar
- Piechulla B (1989) Changes of the diurnal and circadian (endogenous) mRNA oscillations of the chlorophyll a/b binding protein in tomato leaves during altered day/night (light/dark) regimes. Plant Mol Biol 12: 317–327CrossRefGoogle Scholar
- Pittendrigh CS (1960) In “Discussion” following his article “Circadian rhythms and the Circadian Organization of Living Systems.” Cold Spring Harbor Symp Quant Biol 25: 183Google Scholar
- Prosser RA, Gillette MU (1989) The mammalian circadian clock in the suprachiasmatic nuclei is reset in vitro by cAMP. J Neurosci 9:1073–1081PubMedGoogle Scholar
- Prosser RA, McArthur AJ, Gillette MU (1989) cGMP induces phase shifts of a mammalian circadian pacemaker at night, in antiphase to cAMP effects. Proc Natl Acad Sci USA 86: 6812–6815CrossRefGoogle Scholar
- Radha E, Hill TD, Rao GHR, White JG (1985) Glutathione levels in human platelets display a circadian rhythm in vitro. Thromb Res 40: 823–831PubMedCrossRefGoogle Scholar
- Raju U, Yeung SJ, Eskin A (1990) Involvement of proteins in light resetting ocular circadian oscillators in Aplysia. Am J Physiol 258: R256-R262PubMedGoogle Scholar
- Ralph MR, Foster RG, Davis FC, Menaker M (1990) Transplanted suprachiasmatic nucleus determines circadian period. Science 247: 975–978PubMedCrossRefGoogle Scholar
- Reddy P, Jacquier AC, Abovich N, Petersen G, Rosbash G (1986) The period clock locus of D. melanogaster codes for a proteoglycan. Cell 46: 53–61PubMedCrossRefGoogle Scholar
- Reppert SM, Uhl GR (1987) Vasopressin messenger ribonucleic acid in supraoptic and suprachiasmatic nuclei: appearance and circadian regulation during development. J Endocrinol 120: 2483–2487CrossRefGoogle Scholar
- Roberts MH, Bedian V, Chen Y (1989) Kinase inhibition lengthens the period of the circadian pacemaker in the eye of Bulla gouldiana. Brain Res 504: 211–215PubMedCrossRefGoogle Scholar
- Robertson LM, Takahashi JS (1988a) Circadian clock in cell culture. I. Oscillation of melatonin release from dissociated chick pineal cells in flow-through microcarrier culture. J Neurosci 8:12–21PubMedGoogle Scholar
- Robertson LM, Takahashi JS (1988b) Circadian clock in cell culture. II. In vitro photic entrainment of melatonin oscillation from dissociated chick pineal cells. J Neurosci 8: 22–30PubMedGoogle Scholar
- Roenneberg T, Hastings JW (1988) Two photoreceptors control the circadian clock of a unicellular alga. Naturwissenschaften 75: 206–207PubMedCrossRefGoogle Scholar
- Roenneberg T, Nakamura H, Cranmer LD III, Ryan K, Kishi Y, Hastings JW (1991) Gonyauline: a novel endogenous substance shortening the period of the circadian clock of a unicellular alga. Experientia 47:103–106PubMedCrossRefGoogle Scholar
- Rosbash M, Hall JC (1989) The molecular biology of circadian rhythms. Neuron 3: 387–398PubMedCrossRefGoogle Scholar
- Saez L, Young M (1988) In situ localization of the per clock protein during development of Drosophila melanogaster. Mol Cell Biol 8: 5378–5385PubMedGoogle Scholar
- Satter RL, Morse MJ, Lee Y, Crain RC, Coté GG, Moran N (1988) Light- and clock-controlled leaflet movements in Sa-manea saman: a physiological, biophysical and biochemical analysis. Bot Acta 101: 205–213Google Scholar
- Saunders DS, Henrich VC, Gilbert LI (1989) Induction of diapause in Drosophila melanogaster: photoperiodic regulation and the impact of arrhythmic clock mutations on time measurement. Proc Natl Acad Sci USA 86: 3748–3752PubMedCrossRefGoogle Scholar
- Sawaki Y, Nihonmatsu I, Kawamura H (1984) Transplantation of the neonatal suprachiasmatic nuclei into rats with complete bilateral suprachiasmatic lesions. Neurosci Res 1:67–72PubMedCrossRefGoogle Scholar
- Scammell TE, Schwartz WJ, Smith CB (1989) No evidence for a circadian rhythm of protein synthesis in the rat suprachiasmatic nuclei. Brain Res 494:155–158PubMedCrossRefGoogle Scholar
- Schweiger HG, Hartwig R, Schweiger M (1986) Cellular aspects of circadian rhythms. J Cell Sci [Suppl] 4:181–200Google Scholar
- Shibata S, Newman GC, Moore RY (1987) Effects of calcium ions on 2-deoxyglucose uptake in the suprachiasmatic nucleus in vitro. Brain Res 426: 332–338PubMedCrossRefGoogle Scholar
- Shin HS, Bargiello TA, Clark BT, Jackson RJ, Young MW (1985) An unusual coding sequence from Drosophila clock gene is conserved in vertebrates. Nature 317: 445–148PubMedCrossRefGoogle Scholar
- Siwicki KK, Strack S, Rosbash M, Hall JC, Jacklet JW (1989) An antibody to the Drosophila period protein recognizes circadian pacemaker neurons in Aplysia and Bulla. Neuron 3: 51–58PubMedCrossRefGoogle Scholar
- Stal LJ, Krumbein WE (1987) Temporal separation of nitrogen fixation and photosynthesis in the filamentous, non-hetero-cystous cyanobacterium Oscillatoria sp. Arch Microbiol 149: 76–80CrossRefGoogle Scholar
- Sweeney BM, Borgese MB (1989) A circadian rhythm in cell division in a prokaryote, the cyanobacterium Synechococcus WH7803. J Phycol 25:183–186CrossRefGoogle Scholar
- Takahashi JS, Turek FW (1987) Anisomycin, an inhibitor of protein synthesis, perturbs the phase of a mammalian circadian pacemaker. Brain Res 405:199–203PubMedCrossRefGoogle Scholar
- Takahashi JS, Murakami N, Nikaido SS, Pratt BL, Robertson LM (1989) The avian pineal, a vertebrate model system of the circadian oscillator: cellular regulation of circadian rhythms by light, second messengers, and macromolecular synthesis. Recent Prog Horm Res 45: 279–352PubMedGoogle Scholar
- Tamponnet C, Edmunds LN Jr (1990) Entrainment and phase-shifting of the circadian rhythm of cell division by calcium in synchronous cultures of the wild-type Z strain and of the ZC achlorophyllous mutant of Euglena gracilis. Plant Physiol 93: 425–131PubMedCrossRefGoogle Scholar
- Tavladoraki P, Argyroudi-Akoyunoglou J (1989) Circadian rhythm and phytochrome control of LHC-I gene transcription. FEBS Lett 255: 305–308CrossRefGoogle Scholar
- Tavladoraki P, Kloppstech K, Argyroudi-Akoyunoglou J (1989) Circadian rhythm in the expression of the mRNA coding for the apoprotein of the light-harvesting complex of photosys-tem II. Plant Physiol 90: 665–672PubMedCrossRefGoogle Scholar
- Taylor WC (1989) Transcriptional regulation by a circadian rhythm. Plant Cell 1: 259–264PubMedCrossRefGoogle Scholar
- Techel D, Gebauer G, Kohler W, Braumann T, Jastorff B, Ren-sing L (1990) On the role of Ca2 + -calmodulin-dependent and cAMP-dependent protein phosphorylation in the circadian rhythm of Neurospora crassa. J Comp Physiol [B] 159: 695–706CrossRefGoogle Scholar
- Vanden Driessche T (1989) The molecular mechanism of circadian rhythms. Arch Int Physiol Biochim 97:1–11PubMedCrossRefGoogle Scholar
- Walla OJ, de Groot EJ, Schweiger M (1989) Identification of a polypeptide in Chlorella that apparently is involved in circadian rhythm. Eur J Cell Biol 50:181–186Google Scholar
- Whitfield JF, Durkin JP, Kleine LP, Raptis L, Rixon RH, Sikor-ska M, Roy Walher P (1987) Calcium, cyclic AMP and protein kinase C - partners in mitogenesis. Cancer Metastasis Rev 5: 205–250PubMedCrossRefGoogle Scholar
- Wollnik F, Turek FW, Majewski P, Takahashi JS (1989) Phase shifting the circadian clock with cycloheximide: response of hamsters with an intact or a split rhythm of locomotor activity. Brain Res 496: 82–88PubMedCrossRefGoogle Scholar
- Yada T, Oiki S, Ueda S, Okada Y (1986) Synchronous oscillation of the cytoplasmic Ca2 + concentration and membrane potential in cultured epithelial cells (intestine 407). Biochim Biophys Acta 887:105–112PubMedCrossRefGoogle Scholar
- Yeung SJ, Eskin A (1987) Involvement of a specific protein in the regulation of a circadian rhythm in Aplysia eye. Proc Natl Acad Sci USA 84: 279–283PubMedCrossRefGoogle Scholar
- Yeung SJ, Eskin A (1988) Responses of the circadian system in the Aplysia eye to inhibitors of protein synthesis. J Biol Rhythms 3: 225–236CrossRefGoogle Scholar
- Yu Q, Jacquier AC, Citri Y, Hamblen M, Hall JC, Rosbash M (1987a) 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: 784–788PubMedCrossRefGoogle Scholar
- Yu Q, Colot HV, Kyriacou P, Hall JC, Rosbash M (1987b) Behaviour modification by in vitro mutagenesis of a variable region within the period gene of Drosophila. Nature 326: 765–769PubMedCrossRefGoogle Scholar
- Zatz M, Mullen DA, Moskal JR (1988) Photoendocrine transduction in cultured chick pineal cells: effects of light, dark, and potassium on the melatonin rhythm. Brain Res 450:199–215CrossRefGoogle Scholar
- Zwartjes RE, Eskin A (1990) Changes in protein phosphorylation in the eye of Aplysia associated with circadian rhythm regulation by serotonin. J Neurobiol 21: 376–383PubMedCrossRefGoogle Scholar