A genomewide oscillation in transcription gates DNA replication and cell cycle.

Microarray analysis from a yeast continuous synchrony culture system shows a genomewide oscillation in transcription. Maximums in transcript levels occur at three nearly equally spaced intervals in this approximately 40-min cycle of respiration and reduction. Two temporal clusters (4,679 of 5,329) are maximally expressed during the reductive phase of the cycle, whereas a third cluster (650) is maximally expressed during the respiratory phase. Transcription is organized functionally into redox-state superclusters with genes known to be important in respiration or reduction being synthesized in opposite phases of the cycle. The transcriptional cycle gates synchronous bursts in DNA replication in a constant fraction of the population at 40-min intervals. Restriction of DNA synthesis to the reductive phase of the cycle may be an evolutionarily important mechanism for reducing oxidative damage to DNA during replication.

[1]  C. Waddington.  The strategy of the genes , 1957 .

[2]  F. Ruddle,et al.  Cyclic Changes in Enzyme Activity in Synchronized Mammalian Cell Cultures , 1968, Science.

[3]  D. Lloyd,et al.  Respiratory Oscillations and Heat Evolution in Synchronously Dividing Cultures of the Fission Yeast Schizosaccharomyces pombe 972h , 1973 .

[4]  N. Shackleton,et al.  Non-equilibrium Isotopic Fractionation between Seawater and Planktonic Foraminiferal Tests , 1973, Nature.

[5]  E Mochan,et al.  Respiratory oscillations in adapting yeast cultures. , 1973, Nature: New biology.

[6]  S. Kauffman,et al.  The mitotic oscillator in Physarum polycephalum. , 1975, Journal of theoretical biology.

[7]  R. Klevecz,et al.  Quantized generation time in mammalian cells as an expression of the cellular clock. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[8]  L. Glass,et al.  Oscillation and chaos in physiological control systems. , 1977, Science.

[9]  M. Eigen,et al.  The hypercycle. A principle of natural self-organization. Part A: Emergence of the hypercycle. , 1977, Die Naturwissenschaften.

[10]  P. Lord,et al.  Dependency of size of Saccharomyces cerevisiae cells on growth rate , 1979, Journal of bacteriology.

[11]  S. Chisholm,et al.  INFLUENCE OF ENVIRONMENTAL FACTORS AND POPULATION COMPOSITION ON THE TIMING OF CELL DIVISION IN THALASSIOSIRA FLUVIATILIS (BACILLARIOPHYCEAE) GROWN ON LIGHT/DARK CYCLES 1 , 1980 .

[12]  S. Kauffman,et al.  Cellular clocks and oscillators. , 1984, International review of cytology.

[13]  J. W. Hastings,et al.  Cell Cycle Synchronization of Gonyaulax polyedra by Filtration: Quantized Generation Times , 1988, Journal of biological rhythms.

[14]  Robert R. Klevecz,et al.  SELF-ORGANIZATION IN BIOLOGICAL TISSUES: ANALYSIS OF ASYNCHRONOUS AND SYNCHRONOUS PERIODICITY, TURBULENCE AND SYNCHRONOUS CHAOS EMERGENT IN COUPLED CHAOTIC ARRAYS , 1992 .

[15]  H. Kuriyama,et al.  Oscillatory metabolism of Saccharomyces cerevisiae in continuous culture. , 1992, FEMS microbiology letters.

[16]  P. Ueland,et al.  DNA cell cycle distribution and glutathione (GSH) content according to circadian stage in bone marrow of cancer patients. , 1992, British Journal of Cancer.

[17]  R. Klevecz,et al.  Amplification and damping of deterministic noise in coupled cellular arrays , 1993 .

[18]  W. V. Burnett.  Northern blotting of RNA denatured in glyoxal without buffer recirculation. , 1997, BioTechniques.

[19]  L. Wodicka,et al.  Genome-wide expression monitoring in Saccharomyces cerevisiae , 1997, Nature Biotechnology.

[20]  Ronald W. Davis,et al.  A genome-wide transcriptional analysis of the mitotic cell cycle. , 1998, Molecular cell.

[21]  Michael Ruogu Zhang,et al.  Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. , 1998, Molecular biology of the cell.

[22]  Phenotypic heterogeneity and genotypic instability in coupled cellular arrays , 1998 .

[23]  Steven B. Haase,et al.  Evidence that a free-running oscillator drives G1 events in the budding yeast cell cycle , 1999, Nature.

[24]  D. Botstein,et al.  Singular value decomposition for genome-wide expression data processing and modeling. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J. Tyson,et al.  Modeling the fission yeast cell cycle: quantized cycle times in wee1- cdc25Delta mutant cells. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[26]  H. Sohn,et al.  Ultradian oscillation of Saccharomyces cerevisiae during aerobic continuous culture: hydrogen sulphide mediates population synchrony , 2000, Yeast.

[27]  J. Warrington,et al.  Comparison of human adult and fetal expression and identification of 535 housekeeping/maintenance genes. , 2000, Physiological genomics.

[28]  Robert R. Klevecz,et al.  Dynamic architecture of the yeast cell cycle uncovered by wavelet decomposition of expression microarray data , 2000, Functional & Integrative Genomics.

[29]  A Orimo,et al.  Molecular cloning of ring finger protein 21 (RNF21)/interferon-responsive finger protein (ifp1), which possesses two RING-B box-coiled coil domains in tandem. , 2000, Genomics.

[30]  R. Nuttall,et al.  An evaluation of the performance of cDNA microarrays for detecting changes in global mRNA expression. , 2001, Nucleic acids research.

[31]  M. G. Koerkamp,et al.  Dissection of transient oxidative stress response in Saccharomyces cerevisiae by using DNA microarrays. , 2002, Molecular biology of the cell.

[32]  J. Kim,et al.  Geometry of gene expression dynamics , 2002, Bioinform..

[33]  D. Lloyd,et al.  Cycles of mitochondrial energization driven by the ultradian clock in a continuous culture of Saccharomyces cerevisiae. , 2002, Microbiology.

[34]  G. Georgiou.  How to Flip the (Redox) Switch , 2002, Cell.

[35]  D. Botstein,et al.  Generalized singular value decomposition for comparative analysis of genome-scale expression data sets of two different organisms , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[36]  D. Lloyd,et al.  The Gts1 protein stabilizes the autonomous oscillator in yeast , 2003, Yeast.

[37]  B. Birren,et al.  Sequencing and comparison of yeast species to identify genes and regulatory elements , 2003, Nature.

[38]  David Lloyd,et al.  Generation and maintenance of synchrony in Saccharomyces cerevisiae continuous culture. , 2003, Experimental cell research.

[39]  D. Murray,et al.  Genome wide oscillations in expression – Wavelet analysis of time series data from yeast expression arrays uncovers the dynamic architecture of phenotype , 2004, Molecular Biology Reports.

[40]  Peter Schuster,et al.  A principle of natural self-organization , 1977, Naturwissenschaften.

[41]  Stuart A. Kauffman,et al.  ORIGINS OF ORDER , 2019, Origins of Order.