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Self-Organized Intracellular Ultradian Rhythms Provide Direct Cell-Cell Communication

  • Chapter
Ultradian Rhythms from Molecules to Mind

Abstract

The ultradian rhythm of protein synthesis in hepatocytes in vitro was used as a marker for direct cell-cell communication. Self-organization of the rhythms leads to cell co-operation and synchronization throughout the population. Gangliosides and/or catecholamines and Ca2+ dependent protein kinase mediated protein phosphorylation gives phase modulation for cell-cell interaction during the establishment of synchrony. Thus the pathway involves signalling of gangliosides or other calcium agonists, Ca2+ release from intracellular stores, elevation of Ca2+ cytosol protein kinase activation steps, protein phosphorylation, synchronisation of protein synthesis rates and results in common rhythm induction throughout the population.

Analogous processes in yeast, as yet not mechanistically investigated, leads to spontaneous self-synchrony in continuously-stirred aerobic cultures.

Messengers responsible for cell-cell interactions in the expression of this 40 min ultradian clock include H2S and acetaldehyde, as shown by phase-resetting experiments. Cell division cycle synchrony is spontaneously achieved for about 8% of the total population of approximately 5 × 10e8 organisms/ml for each ultradian clock cycle. A faster respiratory oscillation (period 4min) also occurs concomitantly in these cultures.

This shorter-period oscillation is also evident in monolayers of organisms perfused with glucose and O2, as revealed by 2-photon excitation. Several mitochondrial activities: (NAD(P)H redox state, inner membrane electrochemical potential and levels of reactive O2 species) were simultaneously observed. This intracellular rhythm is synchronous amongst the mitochondria within a single yeast as well as across the population of organisms.

We conclude that the development of cellular co-operation leading to the multicellular organization of tissues and the harmonious functioning of the whole organism is based on ancient mechanisms, and that hepatocytes and yeast provide highly convenient systems for study.

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References

  • Aldridge J (1976) Short-range intercellular communication, biochemical oscillations and circadian rhythms. In: Handbook of Engineering in Medicine and Biology (Fleming DG, Ternberg BN, eds) CRC, Cleveland OH, pp 55–147.

    Google Scholar 

  • Aon MA, Cortassa S (2006) Metabolic dynamics in cells viewed as multilayered, distributed, mass-energy-information networks. In: Encyclopedia of Genetics, Genomics, Protemics and Bioinformatics, Systems Biology, Vol. 6 (Dunn MY et al., eds) Wiley Interscience, New York.

    Google Scholar 

  • Aon MA, Cortassa S, Westerhoff HV, Van Dam K (1992) Synchrony and mutual stimulation of yeast cells during fast glycolytic oscillations. J Gen Microbiol 138:2219–2227.

    Google Scholar 

  • Aon MA, Cortassa S, Lloyd D (2000) Chaotic dynamics and fractal space in biochemistry: simplicity underlies complexity. Cell Biol Int 24:581–587.

    PubMed  Google Scholar 

  • Aon MA, Cortassa S, Marbán E, O’Rourke B (2003) Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J Biol Chem 278:44735–44744.

    PubMed  Google Scholar 

  • Aon MA, Cortassa SC, O’Rourke B (2006) The fundamental organization of cardiac mitochondria as a network of coupled oscillators. Biophys J 91:4317–4327.

    PubMed  Google Scholar 

  • Aon MA, Cortassa S, Lemar KM, Hayes AJ, Lloyd D (2007) Single and cell population respiratory oscillations in yeast: a 2-photon scanning laser microscopy study. FEBS Lett 581:8–14.

    PubMed  Google Scholar 

  • Barford D (1999) Structural studies of reversible protein phosphorylation and protein phosphatases. Biochem Soc Trans 27:751–766.

    PubMed  Google Scholar 

  • Barnsley MF, Massopust P, Strickland H, Sloan AD (1987) Fractal modelling of biological structures. Ann NY Acad Sci 504:179–194.

    PubMed  Google Scholar 

  • Bashford CL, Chance B, Lloyd D, Poole RK (1980) Oscillations of redox states in synchronous cultures of Acanthamoeba castellanii and Schizosaccharomynces pombe. J Biophys 29:1–11.

    Google Scholar 

  • Bektas M, Spiegel S (2004) Glycosphingolipids and cell death. Glycoconj J 20:39–47.

    PubMed  Google Scholar 

  • Bennett M, Schatz MF, Rockwood H, Wisenfeld K (2002) Huygens’s clocks. Proc Roy Soc A 458:563–579.

    Google Scholar 

  • Berridge MJ (1990) Calcium oscillations. J Biol Chem 265:9583–9586.

    PubMed  Google Scholar 

  • Berridge MJ (1993) Inositol triphosphate and calcium signalling. Nature 361:315–325.

    PubMed  Google Scholar 

  • Berridge MJ, Galione A (1988) Cytosolic calcium oscillators. FASEB J 2:3074–3082.

    PubMed  Google Scholar 

  • Bergelson LD (1995) Serum gangliosides as endogenous immunomodulators. Immunol Today 16:483–486.

    PubMed  Google Scholar 

  • Bizik J, Kanhuri E, Ristimaki A, Taieb A, Vaatalo H, Lubitz W, Vaheri A (2004) Cell-cell contacts trigger programmed necrosis and induce cyclooxygenase-2 expression. Cell Death Differ 11(2):183–195.

    PubMed  Google Scholar 

  • Brodsky VY (1960) Quantitative studies of RNA and proteins in ganglion cells of retina. In 1st Conference on Cytochemistry, Moscow, pp 7–9.

    Google Scholar 

  • Brodsky VY (1975) Protein synthesis rhythm. J Theoret Biol 55:397–407.

    Google Scholar 

  • Brodsky VY (1992) Rhythm of protein synthesis and other circahoralian oscillations. The possible involvement of fractals. In: Ultradian rhythms in life processes (Lloyd D, Rossi EL, eds) Springer, London, pp 23–40.

    Google Scholar 

  • Brodsky VY (2006) Direct cell-cellcommunication: a new approach derived from recent data on the nature and self-organisation of ultradian (circahoralian intracellular rhythms. Biol Rev Camb Philos Soc 81:143–162.

    PubMed  Google Scholar 

  • Brodsky VY, Dubovaja TK, Nechaeva NV, Fateeva VI, Novikova TE, Gvasava IG (1995) Protein synthesis rhythm in the denervated rat liver. Izv Akad Nauk Ser Biol 2:133–137.

    Google Scholar 

  • Brodsky VY, Nechaeva NV, Zvezdina ND, Novikova TE, Gvasava IG, Fateeva VI, Prokazova NV, Golovanova NK (2000) Ganglioside mediated metabolic synchronisation of protein synthesis activity in cultured hepatocyces. Cell Biol Int 24:211–222.

    PubMed  Google Scholar 

  • Brodsky VY, Zvezdina ND, Nechaeva NV, Avdonin PV, Novgikova Te, Gvasava IG, Fateeva VI, Malchenko LA (2003a) Calcium ions as a factor of cell-cell cooperation in hepatocyte cultures. Cell Biol Int 27:965–976.

    PubMed  Google Scholar 

  • Brodsky VY, Zvezdina ND, Nechaeva NV, Novikova TE, Gvasava IG, Fateeva VI, Gracheva HV (2003b) Loss of the hepatocyte co-operative activity after inhibition of ganglioside synthesis and shedding. Cell Biol Int 27:935–942.

    PubMed  Google Scholar 

  • Brodsky VY, Nechaeva NV, Zvezdina ND, Novikova TE, Gvasava IG, Fateeva VI, Malchenko LA (2004) Small cooperative activity of old rat hepatocytes may depend on composition of the intercellular medium. Cell Biol Int 28:311–316.

    PubMed  Google Scholar 

  • Brodsky VY, Zvezdina ND, Nechaeva NV, Novikova TE, Gvasava IG, Fateeva VI, Malchenko LA (2005) Single short-term signal that enhances cooperative activity of the old rat hepatocytes acts for several days. Cell Biol Int 29:971–975.

    PubMed  Google Scholar 

  • Brodsky VY, Zvezdina ND, Fateeva VI, Malchenko LA (2007) Involvement of protein kinases in self-organization of the rhythm of protein synthesis by direct cell-cell communication. Cell Biol Int 31:65–73.

    PubMed  Google Scholar 

  • Buck J (1988) Synchronous rhythmic flashing of fireflies. Quart Rev Biol 63:265–289.

    PubMed  Google Scholar 

  • Buznikov GA (1990) Neurotransmitters in Embryogenesis. Harwood, New York/London.

    Google Scholar 

  • Carafoli E (2002) Calcium signalling: a fate for all seasons. Proc Natl Acad Sci USA 99:1169–1179.

    Google Scholar 

  • Chance B, Williamson G, Lee IY, Mela L, DeVault D, Ghoash A, Pye EK (1973) Synelvonization Pnenomena in Oscillations of Yeast Cells and Isolated Mitochondria. Academic, New York.

    Google Scholar 

  • Cortassa A, Aon MA, Winslow RL, O’Rourke B (2004) A mitochondrial oscillator dependent on reactive oxygen species. Biophys J 87:2060–2073.

    PubMed  Google Scholar 

  • Dickinson JR (2005) Are yeasts free-living unicellular eukaryotes? Lett Appl Microbiol 41:445–447.

    PubMed  Google Scholar 

  • Evans WH, DeVuyst E, Leybaert L (2006) The gap junction cellular intern: Connexin nemichannels enter the signalling limelight. Biochem J 397:1–14.

    PubMed  Google Scholar 

  • Foquet S, Lugo-Martinez VN, Faussat AM, Renaud F, Cardot P (2004) Early loss of E-cadherin from cell-cell contacts is involved in the onset of Anoikis in enterocytes. J Biol Chem 279:43061–43069.

    Google Scholar 

  • Frame MK, DeFreijter AW (1997) Propagation mechanically induced intercellular calcium waves via gap junction and ATP receptors in rat liver cells. Exp Cell Res 230:197–207.

    PubMed  Google Scholar 

  • Freestone PPE, Haigh RD, Lyte M (2007) Specificity of catecholamine-induced growth in Escherichia coli, Salmonella enterica and Versinia enterocolitica. Microbiol Lett 269:221–228.

    Google Scholar 

  • Gelfand IM, Tsetlin ML (1960) Continual models controlling systems. Dok Akad Nauk 131:1242 (in Russian).

    Google Scholar 

  • Ghosh A, Chance B (1964) Oscillations of glycolytic intermediates in yeast cells. Biochem Biophys Res Commun 16:174–181.

    PubMed  Google Scholar 

  • Ghosh AK, Chance B, Pye EK (1971) Metabolic coupling and synchronization of NADH oscillations in yeast cell populations. Arch Biochem Biophys 145:319–331.

    PubMed  Google Scholar 

  • Gilbert DA, Visser G, Ferreira GMN, Hammond KD (2000) Transient chaos in intracellular dynamics. Biol Int 24:589–591.

    Google Scholar 

  • Glass L, Mackey MC (1988) From Clocks to Chaos: The Rhythms of Life. Princeton University Press, Princeton NJ.

    Google Scholar 

  • Goldberger AL, West B (1987) Chaos in Pathology. In: Chaos in Biological Systems (Degn H, Holden AV, Olsen LF, eds) Plenum, New York, pp 1–5.

    Google Scholar 

  • Gooch VD, Packer L (1971) Adenine nucleotide control of heart mitochondrial oscillations. Biochim Biophys Acta 245:17–20.

    PubMed  Google Scholar 

  • Gooch VD, Packer L (1974) Oscillation systems in mitochondria. Biochim Biophys Acta 346:245–260.

    PubMed  Google Scholar 

  • Gueron S, Levit-Gurevich K (1998) Computation of the internal forces in cilia: application to ciliary motion, the effects of viscosity and cilia interactions. Biophys J 74:1658–1676.

    PubMed  Google Scholar 

  • Harper N, Hughes MA, Farrow SN, Cohen GM, MacFarlane M (2003) Protein kinase C modulates tumor-necrosis factor-related apoptosis-inducing ligand-induced apoptosis by targeting the apical events of death receptor signalling. J Biol Chem 278:4438–4497.

    Google Scholar 

  • Hastings JW, Greenberg EP (1999) Quorum sensing: the explanation of a curious phenomenon reveals a common characteristic of bacteria. J Bacteriol 181:2667–2668.

    PubMed  Google Scholar 

  • Isakson BE, Seedort GJ, Libman RL, Evans WH, Boitano S (2003) Cell-cell communication in heterocellular cultures of alveolar epithelial cells. Am J Respir Cell Mol Biol 29:552–561.

    PubMed  Google Scholar 

  • Jensen EW, Eldrup E, Kelbaek H, Nielsen SL, Christensen NJ (1993) Venous plasma noradrenaline increases with age: correlation with total blood volume and longterm smoking habits. Clin Phys 13:99–109.

    Google Scholar 

  • Josephson BD (1962) Possible new effects in superconductive tunnelling. Phys Lett 1:251–253.

    Google Scholar 

  • Josephson BD (1974) The discovery of tunnelling supercurrents. Science 184:527–530.

    PubMed  Google Scholar 

  • Keulers M, Kuriyama H (1998) Acetaldehyde influence on metabolic oscillation of Saccharomyces cerevisiae. In: Information Processing in Cells and Tissues. Plenum, New York.

    Google Scholar 

  • Keulers M, Satroutdinov AD, Suzuki T, Kuriyama H (1996) Synchronization affector of autonomous short-period-sustained oscillation of Saccharomyces cerevisiae. Yeast 12:673–682.

    PubMed  Google Scholar 

  • Klarreich E (2002) Huygens’s clocks revisited. Am Sci 90:322–323.

    Google Scholar 

  • Klevecz RR, Bolen J, Forrest G, Murray DB (2004) A genomewide oscillation in transcription gates DNA replication and cell cycle. Proc Natl Acad Sci USA 101:1200–1205.

    PubMed  Google Scholar 

  • Kwak W-J, Kwon G-S, Jin I, Kuriyama H, Sohn H-Y (2003) Involvement of oxidative stress in the regulation of H2S production during ultradian metabolic oscillation of Saccharomyces cerevisiae. FEBS Microbiol Lett 219:99–104.

    Google Scholar 

  • Lee MW, Rees P, Shore KA, Ortin S, Pesquera L, Valle A (2005) Dynamic characterisation of a laser diode subject to double optical feedback for chaotic communications. IEEC Proc Optoelect 152:97–102.

    Google Scholar 

  • Lemar KM, Passa O, Aon MA, Cortassa S, Müller CT, Plummer S, O’Rourke B, Lloyd D (2005) Allyl alcohol and garlic (Alium sativum) extract produce oxidative stress in Candida albicans. Microbiology 151:3257–3265.

    PubMed  Google Scholar 

  • Lemar KM, Aon MA, Cortassa S, O’Rourke B, Plummer S, Müller CT, Lloyd D (2007) Diallyldisulphide depleted glutathione in Candida albicans: oxidative stress mediated cell death studied by two-photon microscopy Yeast 24:698–706.

    Google Scholar 

  • Lloyd D (1992) Intracellular time-keeping: epigenetic oscillations reveal the functions of an ultradian clock. In: Ultradian rhythms in life processes (Lloyd D, Rossi EL, eds) Springer, London, pp 5–22.

    Google Scholar 

  • Lloyd D (2005) Systems dynamics of biology. J Appl Biomed 3:1–12.

    Google Scholar 

  • Lloyd AL, Lloyd D (1993) Hypothesis: the central oscillator of the circadian clock is a controlled chaotic attractor. BioSystems 29:77–85.

    PubMed  Google Scholar 

  • Lloyd AL, Lloyd D (1995) Chaos: its significance and detection in biology. Biol Rhythm Res 26:233–252.

    Google Scholar 

  • Lloyd AL, May RM (1999) Synchronicity, chaos and population cycles: spatial coherence in an uncertain world. Trends Ecol Evol 14:417–418.

    PubMed  Google Scholar 

  • Lloyd D, Murray DB (2005) Ultradian metronome: timekeeper for orchestration of cellular coherence. Trends Biochem Sci 30:373–377.

    PubMed  Google Scholar 

  • Lloyd D, Murray DB (2006) The temporal architecture of eukaryotic growth. FEBS Lett 580:2830–2835.

    PubMed  Google Scholar 

  • Lloyd D, Murray DB (2007) Redox rhythmicity: clocks at the core of temporal coherence. BioEssays 29:1–9.

    Google Scholar 

  • Lloyd D, Salgado LE, Turner MP, Suller MT, Murray D (2002a) Cycles of mitochondrial energization driven by the ultradian clock in a continuous culture of Saccharomyces cerevisiae. Microbiology 148:3715–3724.

    PubMed  Google Scholar 

  • Lloyd D, Lemar KM, Salgado LEJ, Gould TM, Murray DB (2003) Respiratory oscillations in yeast: mitochondrial reactive oxygen species, apoptosis and time: a hypothesis. FEMS Yeast Res 3:333–339.

    PubMed  Google Scholar 

  • Lloyd D, Salgado LEJ, Turner MP, Suller MT, Murray D (2002) Respiratory oscillations in yeast: clock driven mitochondrial cycles of energization. FEBS Lett 519:41–44.

    PubMed  Google Scholar 

  • Lyte M, Ernst S (1992) Catecholamine induced growth of gram negative bacteria. Life Sci 50:203–212.

    PubMed  Google Scholar 

  • May RM, Lloyd AL (2001) Infection dynamics on scale-free networks. Phys Rev E Stat Nonlin Soft Matter Phys 64: 066112.

    PubMed  Google Scholar 

  • Michaels DC, Matyas EP, Jalife J (1987) Mechanisms of sinoatrial pacemaker synchronization: a new hypothesis. Circ Res 61:704–714.

    PubMed  Google Scholar 

  • Morin LP (2007) SCN organization reconsidered. J Biol Rhythms 22:3–13.

    PubMed  Google Scholar 

  • Murray DB (2004) On the temporal organization of Saccharomyces cerevisiae. Curr Genom 5:665–671.

    Google Scholar 

  • Murray DB, Lloyd D (2006) A tuneable attractor underlies yeast respiratory dynamics. Biosyctems, doi: 10.1016/j.biosystems.2006.09.032.

    Google Scholar 

  • Murray DB, Roller S, Kuriyama H, Lloyd D (2001) Clock control of ultradian respiratory oscillations found during yeast continuous culture. J Bacteriol 183:7253–7259.

    PubMed  Google Scholar 

  • Murray DB, Klevecz RR, Lloyd D (2003) Generation and maintenance of synchrony in Saccharomyces cerevisiae continuous culture. Exp Cell Res 287:10–15.

    PubMed  Google Scholar 

  • Mustafa MG, Utsumi K, Packer L (1966) Damped oscillatory control of mitochondrial respiration and volume. Biochem Biophys Res Commun 24:381–385.

    PubMed  Google Scholar 

  • Nealson KH, Hastings JW (2006) Quorum sensing on a global scale massive numbers of bioluminescent bacteria make milky seas. Appl Environ Microbiol 72:2295–2297.

    PubMed  Google Scholar 

  • Oleskin AV, Kirovskaya TA, Botvinko IV, Lysak LV (1998) Serotonin action on growth and differentiation of microorganisms. Rus J Microbiol 67:305–312 (in Russian).

    Google Scholar 

  • Onkuni K, Hayashi M, Yamashita I (1998) Bicarbonate-mediated social communication stimulates meiosis and sporulation of Saccharomyces cerevisiae. Yeast 14:623–631.

    Google Scholar 

  • O’Rourke B, Cortassa S, Aon MA (2005) Mitochondrial ion channels: gatekeepers of life and death. Physiology (Bethesda) 20:303–315.

    Google Scholar 

  • Packer L, Utsumi R, Mustafa MG (1966) Oscillatory states of mitochondria. Damped oscillatory control of mitochondrial respiration and volume. Biochem Biophys Res Commun 24:381–385.

    PubMed  Google Scholar 

  • Parekh AB, Putney JW (2005) Store-operated calcium channels. Physiol Rev 85:757–810.

    PubMed  Google Scholar 

  • Pavlidis T (1973) Biological Oscillators. Their Mathematical Analysis. Academic, New York.

    Google Scholar 

  • Pikovsky A, Rosenblum M, Kurths J (2002) Synchronization: A Universal Concept in Nonlinear Science. Cambridge University Press, Cambridge.

    Google Scholar 

  • Prozorovskaya MP (1983) Age-related changes of adrenaline and noradrenaline in tissues of rats. Physiol J USSR 69:1244–1246 (in Russian).

    Google Scholar 

  • Pye EK (1969) Biochemical mechanisms underlying the metabolic oscillations in yeast. Can J Bot 47:271–276.

    Google Scholar 

  • Pyragas K (2006) Delayed feedback control of chaos. Phil Trans Roy Soc A 364:2309–2334.

    Google Scholar 

  • Reynolds TB, Fink GR (2001) Baker’s yeast, a model for fungal biofilm formation. Science 291:878–881.

    PubMed  Google Scholar 

  • Romanovsky YM, Chernavsky DS (1972) Mutual synchronisation of many auto-oscillating systems contacted through diffusion. Thesis of 1V Biophysical Congress Moscow pp 51 (in Russian).

    Google Scholar 

  • Rose AH, Harrison JS (eds) (1999) The Yeasts, Academic, London.

    Google Scholar 

  • Roussel MR, Lloyd D (2007) Observation of a chaotic multioscillatory metabolic attractor by real-time monitoring of a yeast continuous culture. FEBS J 274:1011–1018.

    PubMed  Google Scholar 

  • Satroutdinov DV, Kuriyama H, Kobayashi H (1992) Oscillatory metabolism of Saccharomyces cerevisiae in continuous culture. FEMS Microbiol Lett 98:261–268.

    Google Scholar 

  • Segnui B, Andrieu-Abadie N, Jaffrezou JP, Benoist H, Levade T (2006) Sphingolipids as modulators of cancer cell death: potential therapeutic targets. Biochem Biophys Acta 1758(12): 2104–2120.

    Google Scholar 

  • Siren V, Salmenpera P, Kanhuri E, Bizik J, Sorsa T, Tervahartiala T, Vaheri A (2006) Direct cell-cell contacts between human dermal fibroblasts induce a novel form of cell activation leading to non-apoptotic programmed cell death. Ann Med 38:212–220.

    PubMed  Google Scholar 

  • Skinner YE, Goldberger AL, Meyer-Kress G, Ideker RF (1990) Chaos in the heart: implications for clinical cardiology. Biotechnol 8:1018–1024.

    Google Scholar 

  • Sohn H, Kuriyama H (2001) Ultradian metabolic oscillation of Saccharomyces cerevisiae during aerobic continuous culture: hydrogen sulphide, a population synchronizer, is produced by sulphite reductase. Yeast 18:125–135.

    PubMed  Google Scholar 

  • Sohn HY, Murray DB, Kuriyama H (2000) Ultradian oscillation of Saccharomyces cerevisiae during aerobic continuous culture: hydrogen sulphide mediates population synchrony. Yeast 16:1185–1190.

    PubMed  Google Scholar 

  • Sohn HY, Kum EJ, Kwon GS, Jin I, Kuriyama H (2005a) Regulation of branched-charm and sulphur-containing amino acid metabolism by glutathione during ultradian metabolic oscillation of Saccharomyces cerevisiae. J Microbiol 43:375–380.

    PubMed  Google Scholar 

  • Sohn HY, Kum EJ, Kwon GS, Jin I, Adams CA, Kuriyama H (2005b) GLR1 plays an essential role in the homeo dynamics of glutathione and the regulation of the H2S production during respiratory oscillation of Saccharomyces cerevisiae. Biosci Biotechnol Biochem 69:2450–2454.

    PubMed  Google Scholar 

  • Strogatz SH (2000) From Kuramoto Crawford: exploring the onset of chaos in populations of coupled oscillators. Physica D 143:1–20.

    Google Scholar 

  • Strogatz S (2003) Sync: The Emerging Science of Spontaneous Order. Hyperion, New York.

    Google Scholar 

  • Walters M, Sperandio V (2006) Autoinducer 3 and epinephrine signalling in the kinetics of locus of enterocyte gene expression in enterohemorragic Escherichia coli. Infect Immun 74:5445–5455.

    PubMed  Google Scholar 

  • Wheatley D (2000) Ultradian rhythms in cells: questions regarding their existence and significance. Cell Biol Int 24:495–498.

    PubMed  Google Scholar 

  • Wiley DA, Strogatz SH, Girvan M (2006) The size of the synch basin. Chaos 16:05103.

    Google Scholar 

  • Winfree AT (2001) The Geometry of Biological Time. Springer, New York.

    Google Scholar 

  • Woods NM, Cuthbertson KSR, Cobbold PH (1986) Repetitive rises in cytoplasmic free calcium in hormone-stimulated hepatocytes. Nature 319:600–602.

    PubMed  Google Scholar 

  • Wuhl E, Hadstein C, Mehls O, Schaefer F (2005) Ultradian but not circadian blood pressure rhythms correlate with renal disfunction in children with chronic renal failure. J Am Soc Nephrol 16:746–754.

    PubMed  Google Scholar 

  • Wurster B (1976) Oscillations in Dictystelian discoideum. Nature 260:703–704.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Institute of Developmental Biology, Russian Academy of Sciences, 26 Vavilov Street, 119334, GSP-1, Moscow, Russia

    V. Y. Brodsky

  2. Microbiology (BIOSI 1), Cardiff School of Biosciences, Main Building, PO Box 915, Cardiff, CF10 3TL, Wales, UK

    D. Lloyd

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  1. Microbiology (BIOSI 1), Cardiff University, Main Building, Cardiff, CF10 3TL, Wales, UK

    David Lloyd

  2. 125 Howard Ave., Los Osos, CA, 93402, USA

    Ernest L. Rossi

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Brodsky, V.Y., Lloyd, D. (2008). Self-Organized Intracellular Ultradian Rhythms Provide Direct Cell-Cell Communication. In: Lloyd, D., Rossi, E.L. (eds) Ultradian Rhythms from Molecules to Mind. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-8352-5_3

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