Circadian rhythm of cell division

  • Rune Smaaland
Part of the Progress in Cell Cycle Research book series (PCCR)

Abstract

The existence of circadian oscillations in the level of hormones, in numerous physiological parameters, in toxicity and in behavior is now fully recognized in all living organisms. In contrast, the synchronisation and regulation of cell proliferation by circadian rhythms in vivo is only starting to be appreciated. This article reviews the experimental evidence for circadian synchronisation of cell division in different mammalian tissues (mainly the gastro-intestinal tract and hemapoietic system), including tumoral tissues. The possible causes of this coupling of the cell cycle phases to the circadian rhythm are discussed. Testing of novel antitumour agents using murine models should take into consideration the temporal difference between murine and human circadian control of proliferation (the peak of DNA synthesis occurs during the activity period, i.e. during daytime in man, and at night-time in mice and rats). Experimental and clinical data clearly support the important implications of the circadian control of the cell cycle in the optimisation of cancer chemotherapy, both for reducing toxicity and increasing the antitumour effects.

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References

  1. 1.
    Edmunds, Jr. L.N. and Laval-Martin, D.L. (1982) in Cell cycle clocks (Edmunds Jr., L. N. ed.), pp. 295–324, New York, Marcel Dekker.Google Scholar
  2. 2.
    Touitou, Y. and Haus, E. (1992) Biologic rhythms in clinical and laboratory medicine Berlin, Springer-Verlag.Google Scholar
  3. 3.
    Smaaland, R. and Sothern, R.B. (1994) in Circadian cancer therapy (Hrushesky, W.J.M. ed.) Boca Raton, CRC Press.Google Scholar
  4. 4.
    Hastings, M. (1995) Nature 376, 296–297PubMedGoogle Scholar
  5. 5.
    Cross. F., Roberts, J. and Weintraub, H. (1989) Annu Rev Cell. Biol. 5, 341–395.PubMedGoogle Scholar
  6. 6.
    Murray, A.W. and Kirschner. M.W. (1989) Science 246, 614–621.PubMedGoogle Scholar
  7. 7.
    Lewin, B. (1990) Cell. 61, 743–752.PubMedGoogle Scholar
  8. 8.
    King, R.W. Jackson, P.K. and Kirschner, M.W. (1993) Cell. 79, 563–571.Google Scholar
  9. 9.
    Sherr, C.J. (1994) Cell. 79, 551–555.PubMedGoogle Scholar
  10. 10.
    Coleman, T.R. and Dumphy, W.G. (1994) Curr. Opin. Cell. Biol. 6, 877–882.PubMedGoogle Scholar
  11. 11.
    Sherr, C.J. and Roberts, J.M. (1995) Genes Dev. 9, 1149–1163.PubMedGoogle Scholar
  12. 12.
    Peters, G. (1994) Nature 371, 204–205.PubMedGoogle Scholar
  13. 13.
    Polyak, K., Lee, M.H., Erdjument-Bromage, H., Tempst, P. and Massague, J. (1994) Cell. 78, 59–66.PubMedGoogle Scholar
  14. 14.
    Kato, J., Matsuoka, M., Polyak, K., Massague, J. and Sherr, C.J. (1994) Cell. 79, 487–496.PubMedGoogle Scholar
  15. 15.
    Hengst, L. and Reed, S.I. (1996) Science 271, 1861–1864.PubMedGoogle Scholar
  16. 16.
    Wood, P.A. and Hrushesky, W.J.M. (1994) in Circadian cancer therapy (Hrushesky, W. J. M. ed.) Boca Raton, CRC Press.Google Scholar
  17. 17.
    Young, M.R.I., Matthewa, J.P., Kanabrocki, E.L., Sothern, R.B., Roitman-Johnson, B. and Scheving, L.E. (1995) Int. J. Chronobiol. 12, 19–27.Google Scholar
  18. 18.
    Sothern, R.B., Roitman-Johnson, B., Kanabrocki, E.L., Yager, J.G., Roodell, M.M., Weatherbee, J.A., Young, M.R.I., Nemchausky, B.M. and Scheving, L.E. (1995) J. Allergy Clin. Immunol 95, 1029–1035.PubMedGoogle Scholar
  19. 19.
    Perpoint, B., Le Bousse-Kerdiles, C., Clay, D., Smadja-Joffe, F., Depres-Brummer, P., Laporte-Simitsidis, S., Jasmin, C. and Lévi, F. (1995) Exp. Hematol. 23, 362–368.PubMedGoogle Scholar
  20. 20.
    Cos, S. and Sanches-Barcelo, E.J. (1994) Cancer lett. 85, 105–109.PubMedGoogle Scholar
  21. 21.
    Creanor, J. and Mitchison, J.M. (1986) J. Cell. Sci. 86, 207–215.PubMedGoogle Scholar
  22. 22.
    Novak, B. and Mitchison, J.M. (1986) J. Cell. Sci. 86, 191–206.PubMedGoogle Scholar
  23. 23.
    Whitfield. J.F., Durkin, J.P., Franks, D.J., Kleine, L.P., Raptis, L., Rixon, R.H., Sikorska, M. and Walker, P.R. (1987) Cancer Metast. Rev. 5, 205–250.Google Scholar
  24. 24.
    Dumont, J.E., Jauniaux, J.C. and Roger, P.P. (1989) Trends Biochem. Sci. 14, 67–71.PubMedGoogle Scholar
  25. 25.
    Boynton, A.L. and Whitfield, J.F. (1983) Adv. Cyclic Nucleotide Res. 15, 193–294.Google Scholar
  26. 26.
    Matsumoto, K., Uno, I. and Ishiakawa, T. (1985) Yeast 1, 15–24.PubMedGoogle Scholar
  27. 27.
    Carell, E.F. and Deardfield, K.L. (1982) Life Sci. 31, 249–254.PubMedGoogle Scholar
  28. 28.
    Carré, I.A., Laval-Martin, D.L. and Edmunds, Jr. L.N. (1989) J. Cell. Sci. 94, 267–272.Google Scholar
  29. 29.
    Edmunds, Jr. L.N., Carré, I.A., Tamponnet, C. and Tong, J. (1992) Chronobiol. Int. 9, 180–200.PubMedGoogle Scholar
  30. 30.
    Carré, I.A. and Edmunds, Jr. L.N. (1990) Cyclic AMP, cell division cycles, and circadian oscillators in Euglena. Bethesda, MD. ASCB/EMBO Conference on’ The Cell. Cycle”.Google Scholar
  31. 31.
    Edmunds, Jr. L.N. and Carré, I.A. (1990) Cyclic AMP, cell division cycles, and circadian oscillators in Euglena, 37. 2nd. meeting of the Society for Research on Biological Rhythms. Amelia Island, Jacksonville, FL.Google Scholar
  32. 32.
    Draetta, G., Luca, F., Westendorf, J., Brizuela, L., Ruderman, J. and Beach, D. (1989) Cell. 56, 829–838.PubMedGoogle Scholar
  33. 33.
    Edmunds, Jr. L. (1993) Signal transduction between circadian clock and cell division cycle. I-4, 21st. Conference of the International Society for Chronobiology. Quebec City.Google Scholar
  34. 34.
    Fortuyn-Van Leyden, C.E.D. (1917) Proc. kon. nederl. Akad. Wet. (c) 19, 38–44.Google Scholar
  35. 35.
    Pilgrim, C., Erb, W. and Maurer, W. (1963) Nature 199, 863–865.PubMedGoogle Scholar
  36. 36.
    Halberg, F., Halberg, E., Barnum, C.P. and Bittner, J.J. (1959) in Photoperiodism and Related Phenomena in Plants and Animals (Withrow, R. B. ed.) pp. 803–878, Ed. Publ. No 55 of the Amer. Assoc. Adv. Sci. Washington D.C.Google Scholar
  37. 37.
    Thorud, E., Clausen, O.P.F. and Laerum, O.D. (1984) in Cell. cycle clocks (Edmunds, L. N. j. ed.) pp. 113–133, New York, Basel, Marcel Dekker, Inc.Google Scholar
  38. 38.
    Cooper, Z.K. and Schiff, A. (1938) Proc. Soc. exp. Biol. (N.Y.) 39, 323–324.Google Scholar
  39. 39.
    Bullough, W.S. (1948) Proc. roy. Soc. Lond. (Biol.) 135, 212–232.Google Scholar
  40. 40.
    Scheving, L.E. (1959) Anat. Rec. 135, 7–19.PubMedGoogle Scholar
  41. 41.
    Evensen, A. (1963) Bull. WHO 28, 513–515.PubMedGoogle Scholar
  42. 42.
    Rubin, N. and Scheving, L.E. (1983) J. invest. Dermatol. 80, 79–80.PubMedGoogle Scholar
  43. 43.
    Frentz, G., Moller, U., Holmich, P. and Christensen, I.J. (1991) Acta Derm. Venereol. 71, 85–87.PubMedGoogle Scholar
  44. 44.
    Tvermyr, E.M.F. (1972) Virch Arch (Cell. Pathol) 11, 43–54.Google Scholar
  45. 45.
    Clausen, O.P.F., Thorud, E. and Kaufman, S.L. (1982) Int. J. Chronobiol 8, 83–93.PubMedGoogle Scholar
  46. 46.
    Møller, U. and Keiding, N. (1982) Cell. Tiss. Kinet. 15, 341–350.Google Scholar
  47. 47.
    Møller, U., Keiding, N. and Engel, F. (1982) Cell. Tiss. Kinet. 15, 157–168.Google Scholar
  48. 48.
    Brown, W.R. (1991) J. Invest, dermatol 97, 273–280.Google Scholar
  49. 49.
    Halberg, F., Barnum, C.P., Silber, R.H. and Bittner, J.J. (1958) Proc. Soc. Exp. Biol. (N.Y.) 97, 897–900.Google Scholar
  50. 50.
    Souto, M. and Echavellanos, J.M. (1985) Chronobiol. Int. 2, 169–175.PubMedGoogle Scholar
  51. 51.
    Scheving, L.E. and Pauly, J.E. (1973) Int. J. Chronobiol. 1, 269–286.PubMedGoogle Scholar
  52. 52.
    Scheving, L.E., Pauly, J.E., Von Mayersbach, H. and Dunn, J.D. (1974) Acta Pathol 88, 411–423.Google Scholar
  53. 53.
    Refsum, S.B., Haskjold, E., Bjerknes, R. and Iversen, O.H. (1991) Virchows Arch. B. Cell. Pathol Incl Mol Pathol. 60, 225–230.PubMedGoogle Scholar
  54. 54.
    Benestad, H.B. and Laerum, O.D. (1989) in Current Topics In Pathology (Iversen, O.H. ed.) 79, 7–36, Berlin, Springer-Verlag.PubMedGoogle Scholar
  55. 55.
    Canon, C., Lévi, F., Reinberg, A. and Mathé, G. (1985) Leukemia Res. 9, 1539–1546.Google Scholar
  56. 56.
    Lévi, F., Canon, C., Blum, J.P., Mechkouri, M., Reinberg, A. and Mathé, G. (1985) J. Immunol 134, 217–222.PubMedGoogle Scholar
  57. 57.
    Bartlett, P., Haus, E., Tuason, T., Sackett-Lundeen, L. and Lakatua, D. (1982)in Proc. 15th international Conference on Chronobiology (Haus, E. and Kabat, H. F. eds) Basel, Karger, S.Google Scholar
  58. 58.
    Laerum, O.D. and Aardal, N.P. (1985) in Clinical Aspects of Chronobiology (Rietveld, W. J. eds.) pp. 85–97, Leiden, Meducation Service Hoechst.Google Scholar
  59. 59.
    Lévi, F., Blazcek, I. and Ferlé-Vidovic, A. (1988) Exp. Hematol 16, 696–701.PubMedGoogle Scholar
  60. 60.
    Laerum, O.D; and Paukovits, W.R. (1984) Exp. Hematol. 12, 7–17.PubMedGoogle Scholar
  61. 61.
    Sletvold, O., Laerum, O.D. and Riise, T. (1988) Eur. J. Haematol. 40, 42–49.PubMedGoogle Scholar
  62. 62.
    Sletvold, O., Laerum, O.D. and Riise, T. (1988) Mech. Aging Dev. 42, 91–104.PubMedGoogle Scholar
  63. 63.
    Klein, C.S. and Geisel, H. (1947) Klin. Wochenschr. 25, 662-.Google Scholar
  64. 64.
    Raitsina, S.S. (1961) Bull. Exp. Biol. Med. 51, 494–497.Google Scholar
  65. 65.
    Gololobova, M.T. (1958) Bull Exp. Biol. Med. 40, 1143-.Google Scholar
  66. 66.
    Loisner, L.D., Artemiva, N.S. and Babaeva, A.G. (1962) Bull Exp. Biol. Med. 54, 77-.Google Scholar
  67. 67.
    Sinha, H.P. (1960) Patna. J. Med. 34, 301-.Google Scholar
  68. 68.
    Clark, R.H. and Baker, B.L. (1963) Am. J. Physiol. 204, 1018–1022.PubMedGoogle Scholar
  69. 69.
    Sigdestad, CT., Bauman, J. and Lesher, S. (1969) Exp. Cell. Res. 538, 159–162.Google Scholar
  70. 70.
    Sigdestad, C.T. and Lesher, S. (1970) Experientia (Experimenta) 26, 1321–1322.Google Scholar
  71. 71.
    Leblond, C.P. and Stevens, CE. (1948) Anat. Rec. 100, 357–377.PubMedGoogle Scholar
  72. 72.
    Bertalanfy, F.D. (1960) Acta Anat. 40, 130-.Google Scholar
  73. 73.
    Hunt, T.E. (1952) Anat. Rec. (Abstr.) 112, 346.Google Scholar
  74. 74.
    von Muhlemann, H.R., Marthaler, T.M. and Rateitschak, K.H. (1956) Acta Anat. 28, 331.PubMedGoogle Scholar
  75. 75.
    Scheving, L.E., Burns, E.R. and Pauly, J.E. (1972) Am. J. Anat. 135, 311–317.PubMedGoogle Scholar
  76. 76.
    Appleton, D.R., Sunter, J.P. and Watson, A.J. (1981) Cell. proliferartion in the gastrointestinal tract.London, Pitman Medical Ltd.Google Scholar
  77. 77.
    Scheving, L.E., Tsai, T.H. and Scheving, L.A. (1983) Amer. J. Anat. 168, 433–465.PubMedGoogle Scholar
  78. 78.
    Kennedy, M.F.G., Tutton, P.J.M. and Barkla, D.H. (1985) Cancer Letters 28, 169–175.PubMedGoogle Scholar
  79. 79.
    Kaur, P. and Porten, C.S. (1986) Cell. Tiss. Kinet. 19, 591–599.Google Scholar
  80. 80.
    Scheving, L.E., Feuers, R.J., Tsai, T.H. and Scheving, L.A. (1994) in Circadian cancer therapy (Hrushesky, W.J.M. ed.) pp. 19–40, Boca Raton.Google Scholar
  81. 81.
    Scheving, L.E., Burns, E.R., Pauli, J.E. and Tsai, T.H. (1978) Anat. Rec. 191, 479–486.PubMedGoogle Scholar
  82. 82.
    Scheving, L.E., Tsai, T.H. and Scheving, L.A. (1983) Am. J. Anat. 168, 433–465.PubMedGoogle Scholar
  83. 83.
    Thorud, E., Clausen, O.P.F. and Bjerknes, R. (1978) in Pulse Cytometry (Lutz, D. ed.) 3, 359, Ghent, European Press.Google Scholar
  84. 84.
    Møller, U. and Larsen, J.K. (1978) Cell. Tissue Kinet. 12, 405–413.Google Scholar
  85. 85.
    Clausen, O.P.F., Thorud, E., Bjerknes, R. and Elgjo, K. (1979) Cell. Tissue Kinet. 12, 319–337.PubMedGoogle Scholar
  86. 86.
    Laerum, O.D. and Aardal, N.P. (1981) in 11th International Congress of Anatomy, part C., Biol.ogical rhythms in structure and function (von Mayersbach, H., Scheving, L.E.and Pauli, J.E. eds.) pp. 87–97, New York, Alan R. Liss.Google Scholar
  87. 87.
    Rubin, N.H. (1981) in Biological Rhythms in Structure and Function (von Mayersbach, H., Scheving, L.E. and Pauly, J.E. eds.) pp. 82, New York, Alan R. Liss.Google Scholar
  88. 88.
    Rubin, N.H. (1982) Radiat. Res. 89, 65–76.PubMedGoogle Scholar
  89. 89.
    Rubin, N.H., Hokanson, J.A. and Mayshak, J.W. (1983) Am. J. Anat. 168, 15–26.PubMedGoogle Scholar
  90. 90.
    Scheving, L.E., Scheving, L.A., Tsai, T.H. and Pauly, J.E. (1984) J. Nutr. 114, 2160–2166.PubMedGoogle Scholar
  91. 91.
    Quastler, H. and Sherman, F.G. (1959) Exp. Cell. Res. 17, 420-.Google Scholar
  92. 92.
    Burns, E.R. and Scheving, L.E. (1975) Cell. Tissue Kinet. 8, 61–66.PubMedGoogle Scholar
  93. 93.
    Burns, E.R., Scheving, L.E., Fawcett, D.F., Gibbs, W.M. and Galatzan, R.E. (1976) Anat. Rec. 184, 265–273.PubMedGoogle Scholar
  94. 94.
    Scheving, L.E., Tsai, T.H., Scheving, L.A., Feuers, R.J. and Kanabrocki, E.L. (1992) in Biol.ogic Rhythms in Clinical and Laboratory Medicine (Touitou, Y. and Haus, E. eds.) 566, Berlin, Springer-Verlag.Google Scholar
  95. 95.
    Warnakulasuriya, K.A. and MacDonald, D.G. (1993) Arch. Oral Biol. 12, 1107–1111.Google Scholar
  96. 96.
    Warnakulasuriya, K.A. and MacDonald, D.G. (1995) Arch. Oral Biol. 40, 107–110.PubMedGoogle Scholar
  97. 97.
    Khan, S., Raza, A., Petrelli, N. and Mittleman, A. (1988) J. Surg. Oncol. 39, 114–118.PubMedGoogle Scholar
  98. 98.
    Buchi, K.N., Moore, J.G., Hrushesky, W.J.M., Sothern, R.B. and Rubin, N.H. (1991) Gastroenterology 101, 410–415.PubMedGoogle Scholar
  99. 99.
    Potten, C.S., Chwalinski, S., Swindell, R. and Palmer, M. (1982) Cell. Tiss. Kinet. 15, 351–370.Google Scholar
  100. 100.
    Marra, G., Anti, M., Percesepe, A., Armelao, F., Ficarelli, R., Coco, C., Rinelli, A., Vecchio, F.M. and D’Arcangelo, E. (1994) Gastroenterology 106, 982–987.PubMedGoogle Scholar
  101. 101.
    Beck, L., Reick, D.V. and Damann, B. (1959) Proc. Soc. Exp. Biol. Med. 97, 229–231.Google Scholar
  102. 102.
    Lohrman, H-P. and Schreml, W. (1982) in Cytotoxic drugs and the granulopoietic system 81, 155–182, Berlin, Heidelberg, New York., Springer-Verlag.Google Scholar
  103. 103.
    Gordon, M.Y., Barrett, A.J. and Gordon-Smith, E.C. (1985) Bone marrow disorders. The biological basis of clinical problems pp. 1–422, Oxford, Blackwell Scientific.Google Scholar
  104. 104.
    Arendt, J., Minors, D.S. and Waterhouse, J.M. (1989) in Biological rhythms in clinical practice.(Arendt, J., Minors, D. S. and Waterhouse, J. M. eds.) pp. 3–7, London, Boston, Singapore, Sydney, Toronto, Wellington, Wright.Google Scholar
  105. 105.
    Butcher, E.C (1990) Am. J. Pathol. 136, 3–11.PubMedGoogle Scholar
  106. 106.
    Laerum, O.D. (1995) Exp. Hematol. 23, 1145–1147.PubMedGoogle Scholar
  107. 107.
    Fisher, L.B. (1968) Br. J. Dermatol. 60, 75.Google Scholar
  108. 108.
    Spivak, J.L. (1984) in The principles and Practice of Medicine (Harvey, A. M., Johns, R. J., McKusick, V. A., Owens, A. H. and Ross, R. S. eds.) 21st ed., 465, Norwalk, Appleton-Century-Crofts.Google Scholar
  109. 109.
    Nathan, D.G. (1987) in Oxford Textbook of Medicine (Weatherall, D.J., Ledingham, J.G.G. and Warrell, D.A. eds) 2nd. ed. 2, Oxford University Press.Google Scholar
  110. 110.
    Laerum, O.D. and Paukovits, W.R. (1989) Pharmac. Ther. 44, 335–349.Google Scholar
  111. 111.
    Gordon, M.Y., Barrett, A.J. and Gordon-Smith, E.C. (1985) Bone marrow disorders. The biological basis of clinical problems 1–422, Oxford, Blackwell Scientific.Google Scholar
  112. 112.
    Pizzarello, D.J. and Witcofski, R.L. (1970) Radiology 97, 165–167.PubMedGoogle Scholar
  113. 113.
    Burns, E.R. (1981) Cancer Res. 41, 2795–2802.PubMedGoogle Scholar
  114. 114.
    Sharkis, S.J., LoBue, J., Alexander, P.J., Rakowitz, F., Weitz-Hamburger, A. and Gordon, A.S. (1971) Proc. Soc. Exp. Biol. Med. 138, 494–496.PubMedGoogle Scholar
  115. 115.
    Sharkis, S.J., Palmer, J.D., Goodenough, J., LoBue, J. and Gordon, A.S. (1974) Cell. Tiss. Kinet. 7, 381–387.Google Scholar
  116. 116.
    Moskalik, K.G. (1976) Bull Exp. Biol. Med. (USSR) 81, 594.Google Scholar
  117. 117.
    Dörmer, P., Schmolke, W., Muschalik, P. and Brinkman, W. (1970) Beitr. Pathol. 141, 174–186.PubMedGoogle Scholar
  118. 118.
    Stoney, P.J., Halberg, F. and Simpson, H. W. (1975) Chronobiologia 2, 319–323.PubMedGoogle Scholar
  119. 119.
    Aardal, N.P., Laerum, O.D. and Paukovits, W.R. (1982) Virch. Arch. B Cell. Pathol. 38, 253–261.Google Scholar
  120. 120.
    Aardal, N.P. (1984) Exp. Hematol. 12, 61–67.PubMedGoogle Scholar
  121. 121.
    Aardal, N.P. and Laerum, O.D. (1983) Exp. Hematol. 11, 792–801.PubMedGoogle Scholar
  122. 122.
    Smaaland, R. and Sothern, R.B. (1994) in Circadian Cancer Therapy (Hrushesky, W.J.M. ed.) pp. 119–163, Boca Raton, CRC Press.Google Scholar
  123. 123.
    Klevecz, R.R., Shymko, R.M., Blumenfeld, D. and Braly, P.S. (1987) Cancer Res. 47, 6267–6271.PubMedGoogle Scholar
  124. 124.
    Hromas, R.A., Hutchins, J.T., Marke, D.E. and Scholes, V.E. (1981) Chronobiologica 8, 369–373.Google Scholar
  125. 125.
    Clark, R.H. and Korst, D.R. (1969) Science 166, 236–237.PubMedGoogle Scholar
  126. 126.
    Scheving, L.E. and Pauly, J.E. (1973) Int. J. Chronobiol. 1, 269–286.PubMedGoogle Scholar
  127. 127.
    Hunt, N.H. and Perris, A.D. (1974) J. Endocrinol. 62, 451–462.PubMedGoogle Scholar
  128. 128.
    Haus, E., Lakatua, D.J., Swoyer, J. and Sackett-Lundeen, L. (1983) Am. J. Anat. 168, 467–517.PubMedGoogle Scholar
  129. 129.
    Scheving, L.A., Tsai, T.H. and Scheving, L.E. (1986) Chronobiol. Intl. 3, 1–15.Google Scholar
  130. 130.
    Vacek, A. and Rotkovska, D. (1970) Strahlentherapie 140, 302–306.PubMedGoogle Scholar
  131. 131.
    Simmons, DJ., Loeffelman, K., Frier, C., McCoy, R., Friedman, B., Melville, S. and Kahn, A.J. (1984) in Chronobiology (Haus, E. and Kabat, H. eds.) pp. 37–42, Basel, S.Karger.Google Scholar
  132. 132.
    Halder, C., Häussier, D. and Gupta, D. (1992) J. Pineal Res. 12, 79–83.Google Scholar
  133. 133.
    Goldeck, H. (1948) Ärztl Forsch 2, 22–27.Google Scholar
  134. 134.
    Goldeck, H. and Siegel, P. (1948) Ärtzl Forsch 2, 245–248.Google Scholar
  135. 135.
    Killmann, S-Å., Cronkite, E.P., Fliedner, T.M. and Bond, V.P. (1962) Blood 19, 743–750.PubMedGoogle Scholar
  136. 136.
    Mauer, A.M. (1965) Blood 26, 1–7.PubMedGoogle Scholar
  137. 137.
    Lasky, L.C., Ascencao, J., McCullough, J. and Zanjian, E.D. (1983) Br. J. Haemotol. 55, 615–622.Google Scholar
  138. 138.
    Smaaland, R., Laerum, O.D., Lote, K., Sletvold, O., Sothern, R.B. and Bjerknes, R. (1991) Blood 77, 2603–2611.PubMedGoogle Scholar
  139. 139.
    Smaaland, R., Lote, K., Sletvold, O., Bjerknes, R., Aakvaag, A., Vollset, S.E. and Laerum, O.D. (1991) Ann. NY Acad. Sci. 618, 605–609.Google Scholar
  140. 140.
    Morra, L., Ponassi, A., Caristo, G., Bruzzi, P., Zunino, R., Parodi, G.B. and Sacchetti, C. (1984) Biomed. Pharmacother. 38, 167–170.PubMedGoogle Scholar
  141. 141.
    Lund-Johansen, F., Bjerknes, R. and Laerum, O.D. (1990) Cytometry 11, 610–616.PubMedGoogle Scholar
  142. 142.
    Abrahamsen, J.F., Smaaland, R. and Laerum, O.D. (1994) Amelia Island, Abstract VIIIa-2.Google Scholar
  143. 143.
    Nelson, W., Tong, Y., Lee, J.K. and Halberg, F. (1979) Chronobiologia 6, 305–323.PubMedGoogle Scholar
  144. 144.
    Smaaland, R., Abrahamsen, J.F., Svardal, A.M., Lote, K. and Ueland, P.M. (1992) Br. J. Cancer 66, 39–45.PubMedGoogle Scholar
  145. 145.
    Wide, L., Bengtsson, C. and Birgegard, G. (1989) Br. J. Haematol. 72, 85–90.PubMedGoogle Scholar
  146. 146.
    Reiter, R.J. (1986) in Endokrinologie der kindheit und Adoleszenz (Gupta, D. ed.) pp. 53–67, Stuttgart, Thieme Verlag.Google Scholar
  147. 147.
    Aschoff, J. (1979) in Endocrine rhythms (Krieger, D. ed.) pp. 1–67, New York, Raven Press.Google Scholar
  148. 148.
    Haldar, C., Häusßler, D. and Gupta, D. (1992) J. Pineal Res. 12, 79–93.PubMedGoogle Scholar
  149. 149.
    Cassone, V.M. (1990) Trends Neurosci. 13, 457–464.PubMedGoogle Scholar
  150. 150.
    Lampkin, B.C., McWilliams, N.B. and Mauer, A.M. (1976) Br. J. Haematol. 32, 29–40.PubMedGoogle Scholar
  151. 151.
    Pallavicini, M.G. and Gray, J.W. (1982) Med. Ped. Oncol. 1 (Suppl.), 109–123.Google Scholar
  152. 152.
    Tannock I. (1978) Cancer Treat. Rep. 62, 1117.Google Scholar
  153. 153.
    Hill, B.T. (1986) Rec. Results Cancer Res. 103, 41–53.Google Scholar
  154. 154.
    Simpson-Herren, L. (1982) Ann. NY Acad. Sci. 397, 88–100.PubMedGoogle Scholar
  155. 155.
    Klevecz, R.R. and Braly, P.S. (1994) in Circadian cancer therapy (Hrushesky, W.J.M. ed.) pp. 165–183, Boca Raton, CRC Press.Google Scholar
  156. 156.
    Badran, A.F. and Echave-Llanos, J.M. (1965) J. Natl. Cancer Inst. 35, 285.Google Scholar
  157. 157.
    Voutilainen, A. (1953) Acta Path. Microb. Scan. 99, 1–104.Google Scholar
  158. 158.
    Tähti, E. (1956) Acta Path. Microbiol. Scand. 117, 1–61.Google Scholar
  159. 159.
    Stoll, B.A. and Burch, W.M. (1968) Cancer 21, 193–196.PubMedGoogle Scholar
  160. 160.
    Wolley-Hart, A., Twentyman, P., Corfeild, I., Joslin, C., Morrison, R. and Fowler, J.F. (1986) Br. J. Radiol. 41, 440.Google Scholar
  161. 161.
    Klevecz, R.R. and Braly, P.B. (1991) Ann. NY Acad. Sci. 618, 257–276.PubMedGoogle Scholar
  162. 162.
    Braly, P.S. and Klevecz, R.R. (1993) Cancer 71, 1621–1628.PubMedGoogle Scholar
  163. 163.
    Skipper, H.E., Schabel, F.M.J. and Walcox, W.S. (1967) Cancer Chemother. Res. 51, 125.Google Scholar
  164. 164.
    Haus, E., Halberg, F., Scheving, L., Cardoso, S., Kuhl, J.F.W., Sothern, R., Shiotsuka, R., Hwang, D. and Pauli, S.E. (1972) Science 177, 80–82.PubMedGoogle Scholar
  165. 165.
    Scheving, L.E., Haus, E., Kühl, J.F.W., Pauly, J.E., Halberg, F. and Cardoso, S.S. (1976) Cancer Res. 36, 1133–1137.PubMedGoogle Scholar
  166. 166.
    Scheving, L.E., Burns, R., Pauly, J.E., Halberg, F. and Haus, E. (1977) Cancer Res. 37, 3648–3655.PubMedGoogle Scholar
  167. 167.
    Sothern, R.B., Nelson, W.L. and Halberg, F.A. (1977) in 12th International Conference of the International Society for Chronobiologypp.433–438, Milano, II Ponte.Google Scholar
  168. 168.
    Kühl, J.F.K., Haus, E., Halberg, F., Scheving, L.E., Pauly, J.E., Cardoso, S.S. and Rosene, G. (1974) Chronobiologia 1, 316–317.Google Scholar
  169. 169.
    Scheving, L.E., Burns, E.R., Halberg, F. and Pauly, J.E. (1980) Chronobiologia 17, 33–40.Google Scholar
  170. 170.
    Scheving, L.E., Burns, E.R., Pauly, J.E. and Halberg, F. (1980) Cancer Res. 40, 1511–1515.PubMedGoogle Scholar
  171. 171.
    Sothern, R.B., Lévi, F., Haus, E., Halberg, F. and Hrushesky, W.J.M. (1989) J. Natl. Cancer Inst. 81, 135–145.PubMedGoogle Scholar
  172. 172.
    von Roemeling, R. and Hrushesky, W. (1989) J. Clin. Oncol. 7, 1710–1719.Google Scholar
  173. 173.
    Hrushesky, W.J.M. (1985) Science 228, 73–75.PubMedGoogle Scholar
  174. 174.
    Kerr, D.J., Lewis, C., O’Neill, B., Lawson, N., Blackie, R.G., Newell, D.R., Boxall, F., Cox, J., Rankin, E.M. and Kaye, S.B. (1990) Hematol. Oncol. 8, 59–63.PubMedGoogle Scholar
  175. 175.
    Hrushesky, W.J.M., Roemeling, R.V. and Sothern, R.B. (1989) in Biological rhythms in clinical practice (Arendt, J., Minors, D.S. and Waterhouse, J.M. eds.) pp. 225–252, London, Boston, Singapore, Sydney, Toronto, Wellington., Wright.Google Scholar
  176. 176.
    Rivard, G.E., Infante-Rivard, C., Hoyoux, C. and Champagne, J. (1985) Lancet 2, 1264–1266.PubMedGoogle Scholar
  177. 177.
    Rivard, G.E., Infante-Rivard, C., Dresse, M-F., Leclerc, J-M. and Champagne, J. (1993) Chronobiol. Int. 10, 201–204.PubMedGoogle Scholar
  178. 178.
    Aarnaes, E., Clausen, O.P., Kirkhus, B. and De Angelis, P. (1993) Cell. Proliferation 26, 205–219.PubMedGoogle Scholar
  179. 179.
    Hrushesky, W.J.M., Langer, R. and Theeuwes, F. (1991) Ann. NY Acad. Sci. 618.Google Scholar
  180. 180.
    von Roemeling, R. and Hrushesky, W.J.M. (1990) J. Natl. Cancer Inst. 82, 386–393.Google Scholar
  181. 181.
    Scheving, L.E., Pauly, J.E., Tsai, T.H. and Scheving, L.A. (1983) in Biological Rhythms and Medicine. Cellular, metabolic, physiopathologic, and pharmacologie aspects (Reinberg, A. and Smolensky, M.H. eds.) pp. 79–130, Berlin, New York, Springer-Verlag.Google Scholar
  182. 182.
    Lévi, F., Halberg, F., Nesbit, M., Haus, E. and Levine, H. (1981) in Neoplasms-Comparative pathology of growth in animals, plants and man (Kaiser, H. ed.) pp. 267–316, Baltimore, Williams & Wilkins.Google Scholar
  183. 183.
    Focan, C. Le rythme nycthémeral de la prolifération tumorale: Aspects expérimentaux et cliniques: Implication pour la chimiothérapie oncolytique. (1985) Thesis. University of Liège, Belgium.Google Scholar
  184. 184.
    Smaaland, R., Lote, K., Sothern, R.B. and Laerum, O.D. (1993) Cancer Res. 53, 3129–3138.PubMedGoogle Scholar
  185. 185.
    Meyn, R.E. and Murray, D. (1986) in Cell. cycle effects of drugs (Dethlefsen, L. A. ed.) 121, pp. 170–188, Oxford, Pergamon Press.Google Scholar
  186. 186.
    Bhuyan, B.K., Schedit, L.G; and Fraser, T.J. (1972) Cancer Res. 32, 398–407.PubMedGoogle Scholar
  187. 187.
    Traganos, F., Darzynkiewicz, Z. and Melamed, M.R. (1981) Cancer Res. 41, 4566–4576.PubMedGoogle Scholar
  188. 188.
    Trasganos, F., Staiano-Coico, L., Darzynkiewicz, Z. and Melamed, M.R. (1981) Cancer Res. 41, 2728-273.Google Scholar
  189. 189.
    Smaaland, R., Svardal, A.M., Lote, K., Ueland, P.M. and Laerum, O.D. (1991) J. Natl. Cancer Inst. 83, 1092–1098.PubMedGoogle Scholar
  190. 190.
    Smaaland, R., Laerum, O.D., Sothern, R.B., Sletvold, O., Bjerknes, R. and Lote, K. (1992) Blood 79, 2281–2287.PubMedGoogle Scholar
  191. 191.
    Brons, P.P.T., Pennings, A.H.M., Haanen, C., Wessels, H.M.C. and Boezeman, J.B.M. (1990) Cytometry 11, 837.Google Scholar
  192. 192.
    Hrushesky, WJ.M. and Bjarnason, G.A. (1993) in Cancer. Principles and. Practice of Oncology (De Vita, J.V.T., Hellman, S. and Rosenberg, S.A. eds.) Philadelphia., J.B.Lippincott Company.Google Scholar
  193. 193.
    Ludlum, D. (1977) in Cancer, a comprehensive treatise (Becker, F.F. ed.) 5, pp. 285–307, New York, Plenum Press.Google Scholar
  194. 194.
    Petit, E., Milano, G., Lévi, F., Thyss, A., Bailleul, F. and Schneider, M. (1988) Cancer Res. 48, 1676–1679.PubMedGoogle Scholar
  195. 195.
    Mormont, M.C., Boughattas, A.N. and Lévi, F. (1989) in Chronopharmacology. Cellular and biochemical interactions (Lemmer, B. ed.) pp. 395–437, New York, Marcel Dekker.Google Scholar
  196. 196.
    Boughattas, A.N., Lévi, F., Fournier, C., Lemaigre, G., Roulon, A., Hecquet, B., Mathé, G. and Reinberg, A. (1989) Cancer Res. 49, 3362–3368.PubMedGoogle Scholar
  197. 197.
    Harris, B., Song, R., Soong, S. and Diasio, R.B. (1989) Cancer Res. 49, 6610–6614.PubMedGoogle Scholar
  198. 198.
    Boughattas, N.A., Lévi, F., Fournier, C., Hecqet, B., Lemaigre, G., Roulon, A., Mathé, G. and Reinberg, A. (1990) J. Pharmacol Exp. Ther. 255, 672–679.PubMedGoogle Scholar
  199. 199.
    Paukovits, W.R., Guigon, M., Binder, K.A., Hergl, A., Laerum, O.D. and Schulte-Hermann, R. (1990) Cancer Res. 50, 328–332.PubMedGoogle Scholar
  200. 200.
    Nienhuis, A.W. (1988) N. Engl. J. Med. 318, 916–918.PubMedGoogle Scholar
  201. 201.
    Hrushesky, W.J.M. (1987) J. Biol. Response Mod. 6, 587–598.PubMedGoogle Scholar
  202. 202.
    Lévi, F., Misset, J-L., Brienza, S., Adam, R., Metzger, G., Itzakhi, M., Caussanel, J-P., Kunstlinger, F., Lecouturier, S., Descorps-Declere, A., Jasmin, C., Bismuth, H. and Reinberg, A. (1992) Cancer 69, 893–900.PubMedGoogle Scholar
  203. 203.
    Lévi, F., Zidani, R., Vannetzel, J-M., Perpoint, B., Focan, C., Faggiuolo, R., Chollet, P., Garufi, C., Itzakhi, M., Dogliotti, L., Iacobelli, S., Adam, R., Kunstlinger, F., Gastiaburu, J., Bismuth, H., Jasmin, C. and Misset, J-L. (1994) J. Natl. Cancer Inst. 86, 1608–1617.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1996

Authors and Affiliations

  • Rune Smaaland
    • 1
  1. 1.Department of Oncology, Haukeland HospitalUniversity of BergenBergenNorway

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