Circadian variation of cell proliferation and cell cycle protein expression in man: clinical implications.

Most physiological, biochemical and behavioural processes have been shown to vary in a regular and predictable periodic manner with respect to time. This review focuses on the circadian rhythm in cell proliferation in bone marrow and gut and how this is associated with a circadian expression of cell cycle proteins in human oral mucosa. The control of circadian rhythms by the suprachiasmatic nuclei and the evolving understanding of the genetic and molecular biology of the circadian clock is outlined. Finally, the potential clinical impact of chronobiology in cancer medicine is discussed.

[1]  T. Hunter,et al.  Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport , 1991, The Journal of cell biology.

[2]  J. Kornhauser,et al.  Light, immediate-early genes, and circadian rhythms , 1996, Behavior genetics.

[3]  R. Moore,et al.  Retinohypothalamic projection in mammals: a comparative study. , 1973, Brain research.

[4]  F. Lévi,et al.  Randomised multicentre trial of chronotherapy with oxaliplatin, fluorouracil, and folinic acid in metastatic colorectal cancer , 1997, The Lancet.

[5]  A. Reinberg,et al.  Circadian Changes of Drug Disposition in Man , 1982, Clinical pharmacokinetics.

[6]  J. D. Miller,et al.  New insights into the mammalian circadian clock. , 1996, Sleep.

[7]  Steven M Reppert,et al.  Three period Homologs in Mammals: Differential Light Responses in the Suprachiasmatic Circadian Clock and Oscillating Transcripts Outside of Brain , 1998, Neuron.

[8]  I. Carré,et al.  Oscillator control of cell division in Euglena: cyclic AMP oscillations mediate the phasing of the cell division cycle by the circadian clock. , 1993, Journal of cell science.

[9]  G. Ogden,et al.  The use of antigen retrieval for immunohistochemical detection of p53 over-expression in malignant and benign oral mucosa: a cautionary note. , 1996, Journal of oral pathology & medicine : official publication of the International Association of Oral Pathologists and the American Academy of Oral Pathology.

[10]  V. Rotter,et al.  Subcellular distribution of the p53 protein during the cell cycle of Balb/c 3T3 cells. , 1990, Oncogene.

[11]  Anne-Marie Chang,et al.  Functional Identification of the Mouse Circadian Clock Gene by Transgenic BAC Rescue , 1997, Cell.

[12]  A. Norton,et al.  Brief, high‐temperature heat denaturation (pressure cooking): A simple and effective method of antigen retrieval for routinely processed tissues , 1994, The Journal of pathology.

[13]  R. Drucker-Colín,et al.  Fetal suprachiasmatic nucleus transplants: diurnal rhythm recovery of lesioned rats , 1984, Brain Research.

[14]  C A Czeisler,et al.  Circadian timekeeping in health and disease. Part 2. Clinical implications of circadian rhythmicity. , 1983, The New England journal of medicine.

[15]  J. Concannon,et al.  Radiation and actinomycin D mortality studies: circadian variations in lethality due to independent effects of either agent. , 1973, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[16]  R. Schimke,et al.  Dissociation of nuclear and cytoplasmic cell cycle progression by drugs employed in cell synchronization. , 1995, Experimental cell research.

[17]  O. Laerum,et al.  Alterations of cell cycle distribution in the bone marrow of aging mice measured by flow cytometry , 1988, Experimental Gerontology.

[18]  Jeffrey C. Hall,et al.  The cryb Mutation Identifies Cryptochrome as a Circadian Photoreceptor in Drosophila , 1998, Cell.

[19]  M. Schroll,et al.  RECOMMENDED DIETARY ALLOWANCES FOR EUROPE , 1989, The Lancet.

[20]  A. Reinberg,et al.  A chronopharmacologic phase II clinical trial with 5‐fluorouracil, folinic acid, and oxaliplatin using an ambulatory multichannel programmable pump. High antitumor effectiveness against metastatic colorectal cancer , 1992, Cancer.

[21]  M. Anti,et al.  Rectal epithelial cell proliferation patterns as predictors of adenomatous colorectal polyp recurrence. , 1993, Gut.

[22]  I. Zucker,et al.  Neural regulation of circadian rhythms. , 1979, Physiological reviews.

[23]  J. Newport,et al.  Evidence that the G1-S and G2-M transitions are controlled by different cdc2 proteins in higher eukaryotes , 1991, Cell.

[24]  M. Solomon,et al.  Activation of the various cyclin/cdc2 protein kinases. , 1993, Current opinion in cell biology.

[25]  W. Hrushesky,et al.  Circadian-shaped infusions of floxuridine for progressive metastatic renal cell carcinoma. , 1990, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[26]  V. Devita,et al.  Cancer : Principles and Practice of Oncology , 1982 .

[27]  O D Laerum,et al.  DNA synthesis in human bone marrow is circadian stage dependent. , 1991, Blood.

[28]  T. Hunter,et al.  The differential localization of human cyclins A and B is due to a cytoplasmic retention signal in cyclin B. , 1994, The EMBO journal.

[29]  C. Potten,et al.  Circadian rhythms in the incidence of apoptotic cells and number of clonogenic cells in intestinal crypts after radiation using normal and reversed light conditions. , 1988, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[30]  J. Tong,et al.  Role of cyclic GMP in the mediation of circadian rhythmicity of the adenylate cyclase-cyclic AMP-phosphodiesterase system in Euglena. , 1993, Biochemical pharmacology.

[31]  E. Cronkite,et al.  Mitotic indices of human bone marrow cells. I. Number and cytologic distribution of mitoses. , 1962, Blood.

[32]  J. Dunlap Closely watched clocks: molecular analysis of circadian rhythms in Neurospora and Drosophila. , 1990, Trends in genetics : TIG.

[33]  R. Sothern,et al.  DNA synthesis and ploidy in non-Hodgkin's lymphomas demonstrate intrapatient variation depending on circadian stage of cell sampling. , 1993, Cancer research.

[34]  D. P. King,et al.  Mammalian Circadian Autoregulatory Loop A Timeless Ortholog and mPer1 Interact and Negatively Regulate CLOCK-BMAL1-Induced Transcription , 1998, Neuron.

[35]  J. Pauly,et al.  CIRCADIAN PHASE RELATIONSHIPS OF THYMIDINE-3H UPTAKE, LABELED NUCLEI, GRAIN COUNTS, AND CELL DIVISION RATE IN RAT CORNEAL EPITHELIUM , 1967, The Journal of cell biology.

[36]  James M. Roberts,et al.  Expression of cell-cycle regulators p27Kip1 and cyclin E, alone and in combination, correlate with survival in young breast cancer patients , 1997, Nature Medicine.

[37]  W. K. Sinclair,et al.  X-ray sensitivity during the cell generation cycle of cultured Chinese hamster cells. , 1966, Radiation research.

[38]  R. Silver,et al.  Dispersed cell suspensions of fetal SCN restore circadian rhythmicity in SCN-lesioned adult hamsters , 1990, Brain Research.

[39]  S. Benchimol,et al.  Growth suppression of Friend virus-transformed erythroleukemia cells by p53 protein is accompanied by hemoglobin production and is sensitive to erythropoietin , 1993, Molecular and cellular biology.

[40]  G. Bjarnason Chronobiology. Implications for cancer chemotherapy. , 1995, Acta oncologica.

[41]  M. Kubbutat,et al.  Assessment of cell proliferation by means of an enzyme-linked immunosorbent assay based on the detection of the Ki-67 protein. , 1994, Journal of immunological methods.

[42]  R. Silver,et al.  Circadian rhythmicity restored by neural transplant. Immunocytochemical characterization of the graft and its integration with the host brain , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  J. Hogenesch,et al.  The basic-helix-loop-helix-PAS orphan MOP3 forms transcriptionally active complexes with circadian and hypoxia factors. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[44]  O. Laerum,et al.  Cytometry and time-dependent variations in peripheral blood and bone marrow cells: a literature review and relevance to the chronotherapy of cancer. , 1991, Chronobiology international.

[45]  S. T. Inouye,et al.  Persistence of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[46]  O. Laerum,et al.  Circadian variations in mouse bone marrow. , 1983, Experimental hematology.

[47]  C S Pittendrigh,et al.  Temporal organization: reflections of a Darwinian clock-watcher. , 1993, Annual review of physiology.

[48]  H. Maurer Potential Pitfalls of [3H]Thymidine Techniques to Measure Cell Proliferation , 1981, Cell and tissue kinetics.

[49]  D. Lane,et al.  A comparison of immunohistochemical markers of cell proliferation with experimentally determined growth fraction , 1991, The Journal of pathology.

[50]  R. Sothern,et al.  Colony-forming unit-granulocyte-macrophage and DNA synthesis of human bone marrow are circadian stage-dependent and show covariation. , 1992, Blood.

[51]  P. Lange,et al.  High-dose intensity systemic therapy of metastatic bladder cancer. , 1987, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[52]  J. Haley,et al.  Transforming growth factor-β3 mediated modulation of cell cycling and attenuation of 5-fluorouracil induced oral mucositis , 1997 .

[53]  M. Anti,et al.  Circadian variations of epithelial cell proliferation in human rectal crypts. , 1994, Gastroenterology.

[54]  W. Hrushesky,et al.  Circadian cancer therapy. , 1994, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[55]  D. P. King,et al.  Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. , 1994, Science.

[56]  A. Reinberg,et al.  Chemotherapy of advanced ovarian cancer with 4'-O-tetrahydropyranyl doxorubicin and cisplatin: a randomized phase II trial with an evaluation of circadian timing and dose-intensity. , 1990, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[57]  U. Schibler,et al.  A Serum Shock Induces Circadian Gene Expression in Mammalian Tissue Culture Cells , 1998, Cell.

[58]  F. Davis,et al.  Transplanted suprachiasmatic nucleus determines circadian period. , 1990, Science.

[59]  R. Fox,et al.  Dirunal variations in rabbits: hematological parameters. , 1970, The American journal of physiology.

[60]  W. Hrushesky,et al.  Circadian patterning of continuous floxuridine infusion reduces toxicity and allows higher dose intensity in patients with widespread cancer. , 1989, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[61]  C. Potten,et al.  The circadian rhythm for the number and sensitivity of radiation-induced apoptosis in the crypts of mouse small intestine. , 1990, International journal of radiation biology.

[62]  Jeffrey C. Hall,et al.  CRY, a Drosophila Clock and Light-Regulated Cryptochrome, Is a Major Contributor to Circadian Rhythm Resetting and Photosensitivity , 1998, Cell.

[63]  E. R. Burns,et al.  Circadian rhythms in mitotic activity and 3 H-thymidine uptake in the duodenum: effect of isoproterenol on the mitotic rhythm. , 1972, The American journal of anatomy.

[64]  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.

[65]  B. Lemmer Chronopharmacology : cellular and biochemical interactions , 1989 .

[66]  L. Tolmach,et al.  Variations in several responses of HeLa cells to x-irradiation during the division cycle. , 1963, Biophysical journal.

[67]  C A Czeisler,et al.  Circadian timekeeping in health and disease. Part 1. Basic properties of circadian pacemakers. , 1983, The New England journal of medicine.

[68]  F. Lévi,et al.  Chronomodulated versus fixed-infusion-rate delivery of ambulatory chemotherapy with oxaliplatin, fluorouracil, and folinic acid (leucovorin) in patients with colorectal cancer metastases: a randomized multi-institutional trial. , 1994, Journal of the National Cancer Institute.

[69]  L. Hengst,et al.  A cell cycle-regulated inhibitor of cyclin-dependent kinases. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[70]  Lange Rd,et al.  Circadian variation in reticulocyte counts and immuno-detectable erythropoietin titers. , 1974 .

[71]  V. Rotter,et al.  Involvement of wild-type p53 in pre-B-cell differentiation in vitro. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[72]  H Stein,et al.  Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. , 1984, Journal of immunology.

[73]  M. S. Johnson,et al.  Activity and Distribution of Certain Wild Mice in Relation to Biotic Communities , 1926 .

[74]  Z. Boulos,et al.  PATHWAYS FOR PHOTIC ENTRAINMENT OF MAMMALIAN CIRCADIAN RHYTHMS * , 1981, Photochemistry and photobiology.

[75]  R. Jordan,et al.  Circadian variation in the expression of cell-cycle proteins in human oral epithelium. , 1999, The American journal of pathology.

[76]  R. Moore,et al.  A retinohypothalamic projection in the rat , 1972, The Journal of comparative neurology.

[77]  W. Hrushesky Circadian timing of cancer chemotherapy. , 1985, Science.

[78]  Minoru Tanaka,et al.  Positional Cloning of the Mouse Circadian Clock Gene , 1997, Cell.

[79]  Anne Fernandez,et al.  Cyclin a is required for the onset of DNA replication in mammalian fibroblasts , 1991, Cell.

[80]  A. Murray,et al.  Creative blocks: cell-cycle checkpoints and feedback controls , 1992, Nature.

[81]  S. Reed,et al.  The role of p34 kinases in the G1 to S-phase transition. , 1992, Annual review of cell biology.

[82]  W. R. Fleischmann,et al.  Optimal circadian timing reduces the myelosuppressive activity of recombinant murine interferon-gamma administered to mice. , 1993, Journal of interferon research.

[83]  J. Meijer,et al.  Neurophysiology of the suprachiasmatic circadian pacemaker in rodents. , 1989, Physiological reviews.

[84]  F. Lévi,et al.  Circadian rhythm-varying plasma concentration of 5-fluorouracil during a five-day continuous venous infusion at a constant rate in cancer patients. , 1988, Cancer research.

[85]  N. H. Rubin Influence of the circadian rhythm in cell division on radiation-induced mitotic delay in vivo. , 1982, Radiation Research.

[86]  Z. Darżynkiewicz,et al.  Growth imbalance and altered expression of cyclins B1, A, E, and D3 in MOLT-4 cells synchronized in the cell cycle by inhibitors of DNA replication. , 1995, Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research.

[87]  L. N. Edmunds Cell cycle clocks , 1984 .

[88]  H. Kawamura,et al.  Transplantation of the neonatal suprachiasmatic nuclei into rats with complete bilateral suprachiasmatic lesions , 1984, Neuroscience Research.

[89]  Lily Yan,et al.  Light-Induced Resetting of a Mammalian Circadian Clock Is Associated with Rapid Induction of the mPer1 Transcript , 1997, Cell.

[90]  P. Rushton,et al.  Daily variation in radiosensitivity of circulating blood cells and bone marrow cellularity of mice. , 1984, Comparative biochemistry and physiology. A, Comparative physiology.

[91]  F. Halberg,et al.  Circadian rhythmometry of mammalian radiosensitivity , 1974 .

[92]  P. Tresco,et al.  A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms , 1996, Nature.

[93]  D. S. Hsu,et al.  Role of mouse cryptochrome blue-light photoreceptor in circadian photoresponses. , 1998, Science.

[94]  A. Mauer,et al.  DIURNAL VARIATION OF PROLIFERATIVE ACTIVITY IN THE HUMAN BONE MARROW. , 1965, Blood.

[95]  David O. Morgan,et al.  Principles of CDK regulation , 1995, Nature.

[96]  Joel D Levine,et al.  Molecular Analysis of Mammalian Timeless , 1998, Neuron.

[97]  P. Decoursey,et al.  Circadian rhythmicity after neural transplant to hamster third ventricle: specificity of suprachiasmatic nuclei , 1989, Brain Research.

[98]  T. Riise,et al.  Age‐related differences and circadian and seasonal variations of myelopoietic progenitor cell (CFU‐GM) numbers in mice , 1988, European journal of haematology.

[99]  A. Svardal,et al.  Glutathione content in human bone marrow and circadian stage relation to DNA synthesis. , 1991, Journal of the National Cancer Institute.

[100]  Gregor Eichele,et al.  RIGUI, a Putative Mammalian Ortholog of the Drosophila period Gene , 1997, Cell.

[101]  R. Swank,et al.  Circadian Periodicity in Some Physicochemical Parameters of Circulating Blood , 1965, Nature.

[102]  E. R. Burns Circadian rhythmicity in DNA synthesis in untreated and saline-treated mice as a basis for improved chronochemotherapy. , 1981, Cancer research.

[103]  Leland Hartwell,et al.  Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells , 1992, Cell.

[104]  Yoshiyuki Sakaki,et al.  Circadian oscillation of a mammalian homologue of the Drosophila period gene , 1997, Nature.

[105]  D. Weaver The Suprachiasmatic Nucleus: A 25-Year Retrospective , 1998, Journal of biological rhythms.

[106]  K. Gatter,et al.  Monoclonal antibody Ki‐67: its use in histopathology , 1990, Histopathology.

[107]  A. Morley A neutrophil cycle in healthy individuals. , 1966, Lancet.

[108]  J. Goodenough,et al.  DAILY VARIATIONS OF MARROW AND SPLENIC ERYTHROPOIESIS, PINNA EPIDERMAL CELL MITOSIS AND PHYSICAL ACTIVITY IN C57Bl/6J MICE , 1974 .

[109]  R C Hermida,et al.  Chronolab: an interactive software package for chronobiologic time series analysis written for the Macintosh computer. , 1992, Chronobiology international.

[110]  R. Reiter,et al.  Pineal melatonin: cell biology of its synthesis and of its physiological interactions. , 1991, Endocrine reviews.

[111]  W R Brown,et al.  A review and mathematical analysis of circadian rhythms in cell proliferation in mouse, rat, and human epidermis. , 1991, The Journal of investigative dermatology.

[112]  D. Macdonald,et al.  Diurnal variation in labelling index in human buccal epithelium. , 1993, Archives of oral biology.

[113]  H. Gainer,et al.  Suprachiasmatic nucleus: use of 14C-labeled deoxyglucose uptake as a functional marker. , 1977, Science.

[114]  R. Moore,et al.  Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. , 1972, Brain research.

[115]  T. Riise,et al.  Circadian and circannual variations of cell cycle distribution in the mouse bone marrow. , 1988, Chronobiology international.

[116]  R. Gillette,et al.  Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice , 1982, Brain Research.

[117]  P. Hall,et al.  Ki67—Structure, function, and new antibodies , 1992, The Journal of pathology.

[118]  W J Hrushesky,et al.  Circadian dynamics of tumor necrosis factor alpha (cachectin) lethality , 1994, The Journal of experimental medicine.

[119]  J. C. Hall,et al.  Mutations and molecules influencing biological rhythms. , 1988, Annual review of neuroscience.

[120]  F. Lévi,et al.  Circadian time dependence of cisplatin urinary kinetics , 1982, Clinical pharmacology and therapeutics.

[121]  A. Reinberg,et al.  Interindividual differences in the circadian hematologic time structure of cancer patients. , 1986, Chronobiology international.

[122]  D. Earnest,et al.  Circadian rhythms of vasopressin release from individual rat suprachiasmatic explants in vitro , 1986, Brain Research.

[123]  F. Lévi,et al.  Circadian and seasonal rhythms in murine bone marrow colony-forming cells affect tolerance for the anticancer agent 4'-O-tetrahydropyranyladriamycin (THP). , 1988, Experimental hematology.

[124]  D. E. Somers,et al.  Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. , 1998, Science.

[125]  G. Groos,et al.  Circadian rhythms in electrical discharge of rat suprachiasmatic neurones recorded in vitro , 1982, Neuroscience Letters.

[126]  I. Zucker,et al.  Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[127]  A. Levine p53, the Cellular Gatekeeper for Growth and Division , 1997, Cell.

[128]  D. Korst,et al.  Circadian Periodicity of Bone Marrow Mitotic Activity and Reticulocyte Counts in Rats and Mice , 1969, Science.

[129]  Paolo Sassone-Corsi,et al.  Molecular clocks: mastering time by gene regulation , 1998, Nature.

[130]  E. Hall,et al.  Radiobiology for the radiologist , 1973 .

[131]  R J Konopka,et al.  Clock mutants of Drosophila melanogaster. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[132]  Ludger Hengst,et al.  G1 control in mammalian cells , 1994, Journal of Cell Science.

[133]  F. Lévi,et al.  Phase I trial of 5-day continuous venous infusion of oxaliplatin at circadian rhythm-modulated rate compared with constant rate. , 1990, Journal of the National Cancer Institute.

[134]  J. Pauly,et al.  Circadian variation in cell division of the mouse alimentary tract, bone marrow and corneal epithelium , 1978, The Anatomical record.

[135]  R. Warnke,et al.  Detection of T and B cell antigens hybridoma monoclonal antibodies: a biotin-avidin-horseradish peroxidase method. , 1980, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[136]  C. Sherr G1 phase progression: Cycling on cue , 1994, Cell.

[137]  A. Reinberg Clinical chronopharmacology, an experimental basis for chronotherapy. , 1978, Arzneimittel-Forschung.

[138]  Markus Meister,et al.  Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms , 1995, Neuron.

[139]  R. Sothern,et al.  Circadian rhythm of cellular proliferation in the human rectal mucosa. , 1991, Gastroenterology.

[140]  V. Rotter,et al.  Nuclear localization is essential for the activity of p53 protein. , 1991, Oncogene.

[141]  R. Klevecz,et al.  Circadian gating of S phase in human ovarian cancer. , 1987, Cancer research.

[142]  J. Bartek,et al.  Cyclin D1 oncoprotein aberrantly accumulates in malignancies of diverse histogenesis. , 1995, Oncogene.

[143]  T. Tada,et al.  Circadian rhythm of leucocytes and lymphocyte subsets and its possible correlation with the function of the autonomic nervous system , 1997, Clinical and experimental immunology.

[144]  D. P. King,et al.  Role of the CLOCK protein in the mammalian circadian mechanism. , 1998, Science.

[145]  R. B. Withrow Photoperiodism and related phenomena in plants and animals , 1959 .

[146]  James M. Roberts,et al.  Human cyclin E, a nuclear protein essential for the G1-to-S phase transition , 1995, Molecular and cellular biology.

[147]  J. Dunlap,et al.  An End in the Beginning , 1998, Science.

[148]  Mark J. Zylka,et al.  Two period Homologs: Circadian Expression and Photic Regulation in the Suprachiasmatic Nuclei , 1997, Neuron.

[149]  Charles J. Sherr,et al.  Mammalian G1 cyclins , 1993, Cell.

[150]  E. Zanjani,et al.  Steroid modulation of naturally occurring diurnal variation in circulating pluripotential haematopoietic cells (CFU‐GEMM) , 1983, British journal of haematology.

[151]  R. Camplejohn,et al.  A study of diurnal proliferative activity in tumour and small intestine of C3H mice bearing a transplanted mammary carcinoma , 1983, Virchows Archiv. B, Cell pathology including molecular pathology.

[152]  C. B. Green Time marches on. , 1998, Trends in cell biology.