Biochemistry (Moscow)

, Volume 79, Issue 6, pp 483–495 | Cite as

Circahoralian (Ultradian) metabolic rhythms

Review

Abstract

This review presents data concerning metabolic rhythms with periods close to one hour (20 to 120 min): their occurrence, biochemical organization, nature, and significance for adaptations and age-related changes of cells and organs. Circahoralian (ultradian) rhythms have been detected for cell mass and size, protein synthesis, enzyme activities, concentration of ATP and hormones, cell respiration, and cytoplasm pH. Rhythms have been observed in bacteria, yeasts, and protozoa, as well as in many cells of metazoans, including mammals, in vivo and in cell cultures. In cell populations, the rhythms are organized by direct cell-cell communication. The biochemical mechanism involves membrane signal factors and cytoplasmic processes resulting in synchronization of individual oscillations to a common rhythm. Phosphorylation of proteins is the key process of coordination of protein synthesis and enzyme activity kinetics. The fractal nature of circahoralian rhythms is discussed as well as the involvement of these rhythms in adaptations of the cells and organs. Senescent decrease in rhythm amplitudes and correspondingly in cell-cell communication has been observed. The possibility of remodeling these changes through the intercellular medium has been predicted and experimentally shown. Perspectives for studies of the organizers and disorganizers of cell-cell communication in the intercellular medium along with appropriate receptors are discussed with special emphasis on aging and pathology. One perspective can be more precise definition of the range of normal biochemical and physiological state with the goal of correction of cellular functions.

Key words

metabolic rhythms kinetics of protein synthesis kinetics of enzyme activities direct cell-cell communication fractals aging 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Brodsky, V. Y., and Kuznetsova, A. F. (1961) Tsitologiya, 3, 89–92.Google Scholar
  2. 2.
    Brodsky, V. Y. (1970) in Works of 5 Histochem. Conf. [in Russian], Tbilisi, pp. 114–128.Google Scholar
  3. 3.
    Brodsky, V. Y., and Nechaeva, N. V. (1973) Tsitologiya, 15, 52–59.Google Scholar
  4. 4.
    Brodsky, V. Y. (1975) J. Theor. Biol., 55, 157–200.Google Scholar
  5. 5.
    Lloyd, D., and Rossi, E. L. (eds.) (1992) Ultradian Rhythms in Life Processes, Springer-Verlag, London.Google Scholar
  6. 6.
    Lloyd, D., and Rossi, E. L. (eds.) (2008) Ultradian Rhythms from Molecules to Mind, Springer-Verlag, London-NY.Google Scholar
  7. 7.
    Brodsky, V. Y., Zaguskin, S. L., and Lebedev, E. A. (1977) Tsitologiya, 19, 931–934.Google Scholar
  8. 8.
    Litinskaya, L. L., Ogloblina, T. A., Veksler, A. M., Agroskin, L. S., Papayan, G. V., Khrust, Yu. R., and Eydus, L. Kh. (1982) Tsitologiya, 24, 1215–1222.Google Scholar
  9. 9.
    Kosykh, M. I., and Chentsov, Yu. S. (1991) Doklady RAN, 316, 475–478.Google Scholar
  10. 10.
    Skulachev, V. P. (1989) Energetics of Biological Membranes [in Russian], Nauka, Moscow.Google Scholar
  11. 11.
    Edwards, S. W., and Lloyd, D. (1980) FEBS Lett., 109, 21–26.PubMedGoogle Scholar
  12. 12.
    Lloyd, D., Edwards, S. W., and Fry, J. C. (1982) Proc. Natl. Acad. Sci. USA, 79, 3785–3788.PubMedCentralPubMedGoogle Scholar
  13. 13.
    Lloyd, D., Poole, R. K., and Edwards, S. W. (1982) The Cell Division Cycle: Temporal Control of Cellular Growth and Reproduction, Academic Press, London.Google Scholar
  14. 14.
    Ferreira, G. M. N., Hammond, K. D., and Gilbert, D. A. (1994) Biosystems, 32, 183–190.PubMedGoogle Scholar
  15. 15.
    Novikova, T. Ye., and Borovkov, A. Yu. (1987) Tsitologiya, 29, 236–239.Google Scholar
  16. 16.
    Bodalina, U. M., Hammond, K. D., and Gilbert, D. A. (2007) Mol. Cell Biochem., 294, 155–162.PubMedGoogle Scholar
  17. 17.
    Geva-Zatorsky, N., Rosenfeld, N., Itzkovitz, S., Milo, R., Sigal, A., Dekel, E., Liron, Y., Polak, P., Lahav, G., and Alon, U. (2006) Mol. Syst. Biol., 2, 13550–13555.Google Scholar
  18. 18.
    Hat, B., Puszynski, K., and Lipniacki, T. (2009) IET Syst. Biol., 3, 342–355.PubMedGoogle Scholar
  19. 19.
    Costero, J., Chevez, A., Peralta, L., Monroy, E., and Ramon, F. (1965) Texas Rep. Biol. Med., 23, 213–220.Google Scholar
  20. 20.
    Mityushin, V. M., Litinskaya, L. L., and Kaminir, L. B. (1967) Biofizika, 12, 89–96.Google Scholar
  21. 21.
    Veksler, A. M., Kostenko, G. A., Eydus, L. Kh., and Litinskaya, L. L. (1973) in Scanning Technique in the Study of Cell Populations (Ivanitsky, ed.) [in Russian], Pushchino-on-Oka, pp. 101–112.Google Scholar
  22. 22.
    Svanidze, I. K., and Didimova, Ye. V. (1974) Tsitologiya, 16, 187–192.Google Scholar
  23. 23.
    Kostenko, G. A., Litinskaya, L. L., Veksler, A. M., and Eydus, L. Kh. (1975) Doklady AN SSSR, 211, 714–717.Google Scholar
  24. 24.
    Brodsky, V. Y. (2006) Biol. Rev. Cambridge Phylosoph. Soc., 82, 143–162.Google Scholar
  25. 25.
    Brodsky, V. Y., Terskikh, V. V., Vasiliev, A. V., Zvezdina, N. D., Vorotelyak, Ye. A., Fateeva, V. I., and Malchenko, L. A. (2011) Ontogenez, 4, 312–319.Google Scholar
  26. 26.
    Boykov, P. Ya. (1987) Mechanisms of Cell Cycle Initiation: Doctoral dissertation [in Russian], ICP AS, Moscow.Google Scholar
  27. 27.
    Brodsky, V. Y., Boikov, P. Y., Nechaeva, N. V., Yurovitsky, Y. G., Novikova, T. E., Fateeva, V. I., and Shevchenko, N. A. (1992) J. Cell Sci., 103, 363–370.PubMedGoogle Scholar
  28. 28.
    Kuempel, P. L., Masters, M., and Pardee, A. B. (1965) Biochem. Biophys. Res. Commun., 18, 858–867.Google Scholar
  29. 29.
    Knorre, W. A. (1968) in Biological and Biochemical Oscillators (Chance, B., Pye, E. K., and Ghosh, A. K., eds.) Academic Press, NY, pp. 449–455.Google Scholar
  30. 30.
    Masters, M., and Donachie, W. D. (1966) Nature, 209, 476–479.PubMedGoogle Scholar
  31. 31.
    Boddy, A., Clark, P. H., Houldsworth, M. A., and Lilly, M. D. (1967) J. Gen. Microbiol., 48, 137–145.Google Scholar
  32. 32.
    Lloyd, D., Salgado, L. E., Turner, M. P., Suller, M. T. E., and Murray, D. (2002) Microbiology, 148, 3715–3724.PubMedGoogle Scholar
  33. 33.
    Michel, U., and Hardeland, R. (1985) J. Interdiscipl. Cycle Res., 16, 17–23.Google Scholar
  34. 34.
    Lloyd, D. (1992) in Ultradian Rhythms in Life Processes (Lloyd, D., and Rossi, E. L., eds.) Springer, London, pp. 5–22.Google Scholar
  35. 35.
    Holvorson, H. O., Bock, R. M., Tauro, P., Epstein, R., and Laberge, M. (1966) in Cell Synchrony (Cameron, I. L., and Padilla, G. M., eds.) Academic Press, NY-London, pp. 102–116.Google Scholar
  36. 36.
    Mano, Y. (1970) Devel. Biol., 22, 433–460.Google Scholar
  37. 37.
    Petzelt, C. (1972) Exp. Cell Res., 70, 333–339.PubMedGoogle Scholar
  38. 38.
    Yarygin, K. N., Nechaeva, N. V., Fateeva, V. I., Novikova, T. Ye., and Brodsky, V. Y. (1978) Byul. Eksp. Biol. Med., 86, 726–728.Google Scholar
  39. 39.
    Hammond, K. D., Wollbrandt, R. K., and Gilbert, D. A. (1985) Int. J. Biochem., 17, 259–264.PubMedGoogle Scholar
  40. 40.
    Hammond, K. D., Cloutman, L., Mindel, B., and Gilbert, D. A. (1989) Int. J. Biochem., 21, 197–201.PubMedGoogle Scholar
  41. 41.
    Hammond, K. D., Bhoola, R., Bodalina, U., and Gilbert, D. A. (1998) Trends Comp. Biochem. Physiol., 4, 75–88.Google Scholar
  42. 42.
    Hammond, K. D., Savage, N., and Littlewood, M. (2000) Cell Biol. Int., 24, 549–557.PubMedGoogle Scholar
  43. 43.
    Calvert-Evers, J. L., and Hammond, K. D. (2002) Cell Biol. Int., 26, 1035–1042.PubMedGoogle Scholar
  44. 44.
    Bodalina, U. M., Hammond, K. D., and Gilbert, D. A. (2005) Cell Biol. Int., 29, 287–299.PubMedGoogle Scholar
  45. 45.
    Kippert, F. (1996) Chronobiol. Int., 13, 1–13.PubMedGoogle Scholar
  46. 46.
    Murray, D., Klevecz, R. R., and Lloyd, D. (2003) Exp. Cell Res., 287, 10–15.PubMedGoogle Scholar
  47. 47.
    Murray, D. B., Roller, S., Kuriyama, H., and Lloyd, D. (2001) J. Bacteriol., 183, 7253–7259.PubMedCentralPubMedGoogle Scholar
  48. 48.
    Litinskaya, L. L., Ogloblina, T. A., Veksler, A. M., Agroskin, L. S., Papayan, G. V., Khrust, Yu. R., and Eydus, L. Kh. (1982) Tsitologiya, 24, 1215–1222.Google Scholar
  49. 49.
    Litinskaya, L. L., Veksler, A. M., Nechaeva, N. V., Novikova, T. Ye., Fateeva, V. I., and Brodsky, V. Y. (1987) Tsitologiya, 29, 917–921.Google Scholar
  50. 50.
    Droste, K., De Groote, L., Lightman, S. L., Reul, J. M., and Linthorst, A. C. (2009) J. Endocrinol., 21, 132–140.Google Scholar
  51. 51.
    Lightman, S. L., Wiles, C. C., Atkinson, H. C., Henley, D. E., Russell, G. M., Leendertz, J. A., McKenna, M. A., Spiga, F., Wood, S. A., and Conway-Campbell, B. L. (2008) Eur. J. Pharmacol., 583, 255–262.PubMedGoogle Scholar
  52. 52.
    Lefcourt, A. M., Bitman, J., Kahl, S., and Wood, D. L. (1993) J. Dairy Sci., 76, 2607–2612.PubMedGoogle Scholar
  53. 53.
    Bergendahl, M., Evans, W. S., and Veldhuis, J. D. (1996) Human Reprod. Update, 2, 507–518.Google Scholar
  54. 54.
    Backstrom, C. T., McNeilly, A. S., Leask, R. M., and Baird, D. T. (1982) Clin. Endocrinol., 16, 29–42.Google Scholar
  55. 55.
    Dunkel, L., Alfthan, H., and Stenman, U. H. (1990) Pediatr. Res., 27, 215–219.PubMedGoogle Scholar
  56. 56.
    Schlatt, S., Pohl, C. R., Ehmcke, J., and Ramaswamy, S. (2008) Biol. Reprod., 79, 93–99.PubMedGoogle Scholar
  57. 57.
    Geoffriau, M., Claustrat, B., and Veldhuis, J. (1999) J. Pineal Res., 27, 139–144.PubMedGoogle Scholar
  58. 58.
    Oz-Hoyos, A., Jaldo, R., Molina-Carballo, A., Escames, G., Fernandez-Garcia, J. M., and Reiter, J. (2001) J. Clin. Endocrinol. Metab., 86, 1181–1187.Google Scholar
  59. 59.
    Matthews, D. R., Naylor, B. A., and Jones, R. G. (1983) Diabetes, 37, 617–621.Google Scholar
  60. 60.
    Schaefer, A., Simon, C., Frank, A. V., Piquard, O., Geny, B., and Brandenberger, G. (2003) Diabetes Care, 26, 168–171.PubMedGoogle Scholar
  61. 61.
    Otukonyong, E. E., Dube, M. G., Torto, R., Kalra, P. S., and Kalra, S. P. (2005) Peptides, 26, 2559–2566.PubMedGoogle Scholar
  62. 62.
    Rossmanith, W. G., Laughlin, G. A., and Mortola, J. F. (1990) J. Clin. Endocrinol. Metab., 70, 990–995.PubMedGoogle Scholar
  63. 63.
    Gronfier, C., and Brandenberger, G. (1998) Sleep Med. Rev., 2, 17–29.PubMedGoogle Scholar
  64. 64.
    Tannenbaum, G., and Martin, J. (2011) Endocrinology, 98, 562–570.Google Scholar
  65. 65.
    Togo, F., Natelson, B. H., Adler, G. K., Ottenweller, J. E., Goldenberg, D., Struzik, Z., and Yamamoto, Y. (2009) Exp. Biol. Med., 234, 232–240.Google Scholar
  66. 66.
    Ichikawa, T. (2001) Zool. Sci., 18, 151–158.Google Scholar
  67. 67.
    Rott, N. N. (1984) Ontogenez, 15, 5–19.PubMedGoogle Scholar
  68. 68.
    Mano, Y. (1975) Biosystems, 7, 51–65.PubMedGoogle Scholar
  69. 69.
    Mano, Y., Suzuki, N., and Shimatake, H. (1977) Growth Differentiation, 19, 31–39.Google Scholar
  70. 70.
    Yasumasu, I., Fujiwara, A., and Ishida, K. (1973) Biochem. Biophys. Res. Commun., 54, 628–632.PubMedGoogle Scholar
  71. 71.
    Gelfand, I. M., and Tsetlin, M. L. (1960) Doklady AN SSSR, 131, 1242–1245.Google Scholar
  72. 72.
    Brodsky, V. Y., Nechaeva, N. V., Novikova, T. E., and Gvazava, I. G. (1994) Izvest. AN, Ser. Biol., 6, 853–858.Google Scholar
  73. 73.
    Brodsky, V. Y., Nechaeva, N. V., Zvezdina, N. D., Prokazova, N. V., Golovanova, N. K., Novikova, T. E., Gvasava, I. G., and Fateeva, V. I. (2000) Cell Biol. Int., 24, 211–222.PubMedGoogle Scholar
  74. 74.
    Brodsky, V. Y., Zvezdina, N. D., Nechaeva, N. V., Novikova, T. E., Gvasava, I. G., Fateeva, V. I., and Gracheva, H. (2003) Cell Biol. Int., 27, 935–942.PubMedGoogle Scholar
  75. 75.
    Brodsky, V. Y., Zvezdina, N. D., Nechaeva, N. V., Avdonin, P. V., Novikova, T. E., Gvasava, I. G., Fateeva, V. I., and Malchenko, L. A. (2003) Cell Biol. Int., 27, 965–976.PubMedGoogle Scholar
  76. 76.
    Brodsky, V. Y., Nechaeva, N. V., Zvezdina, N. D., Novikova, T. E., Gvasava, I. G., Fateeva, V. I., and Malchenko, L. A. (2004) Cell Biol. Int., 28, 311–316.PubMedGoogle Scholar
  77. 77.
    Brodsky, V. Y., Zvezdina, N. D., Nechaeva, N. V., Novikova, T. E., Gvasava, I. G., Fateeva, V. I., and Malchenko, L. A. (2005) Cell Biol. Int., 29, 971–975.PubMedGoogle Scholar
  78. 78.
    Brodsky, V. Y., Zvezdina, N. D., Fateeva, V. I., and Malchenko, L. A. (2007) Cell Biol. Int., 31, 65–73.PubMedGoogle Scholar
  79. 79.
    Zvezdina, N. D., Malchenko, L. A., Fateeva, V. I., and Brodsky, V. Y. (2008) Ontogenez, 39, 198–207.PubMedGoogle Scholar
  80. 80.
    Brodsky, V. Y., and Zvezdina, N. D. (2010) Cell Biol. Int., 34, 1199–1204.PubMedGoogle Scholar
  81. 81.
    Dyatlovitskaya, E. V. (1992) Biokhimiya, 57, 1004–1010.Google Scholar
  82. 82.
    Brodsky, V. Y., Vasiliev, A. V., Terskikh, V. V., Zvezdina, N. D., Fateeva, V. I., Malchenko, L. A., Kiseleva, E. V., and Bueverova, E. I. (2012) J. Cell Tissue Res., 12, 3157–3162.Google Scholar
  83. 83.
    Jin, J., and Pawson, T. (2012) Philos. Trans R Soc. Lond. B Biol. Sci., 367, 2540–2555.PubMedCentralPubMedGoogle Scholar
  84. 84.
    Gilbert, D. A., and Hammond, K. D. (2008) in Ultradian Rhythms from Molecules to Mind (Lloyd, D., and Rossi, E. L., eds.) Springer-Verlag, London-NY, pp. 105–128.Google Scholar
  85. 85.
    Brodsky, V. Y., Konchenko, D. S., Zvezdina, N. D., Malchenko, L. A., and Dubovaja, T. K. (2012) J. Cell Tissue Res., 12, 3265–3271.Google Scholar
  86. 86.
    Brodsky, V. Y., Dubovaya, T. K., Nechaeva, N. V., Fateeva, V. I., Novikova, T. E., and Gvazava, I. G. (1995) Izvest. AN, Ser. Biol., 2, 133–136.Google Scholar
  87. 87.
    Brodsky, V. Y., Nechaeva, N. V., Novikova, T. E., Gvazava, I. G., and Fateeva, V. I. (1995) Izvest. AN, Ser. Biol., 5, 517–520.Google Scholar
  88. 88.
    Nakamura, Y., Hishimoto, Y., Yamakawa, T., and Suzuki, A. (1988) J. Biochem., 103, 396–398.PubMedGoogle Scholar
  89. 89.
    Ozkok, E., Cendiz, S., and Guevener, B. (1999) J. Basic Clin. Physiol. Pharmacol., 10, 337–344.PubMedGoogle Scholar
  90. 90.
    Prozorovskaya, M. P. (1983) Fiziol. Zh. SSSR, 69, 1244–1246.Google Scholar
  91. 91.
    Brodsky, V. Y., Nechaeva, N. V., Zvezdina, N. D., Novikova, T. Ye., Gvazava, I. G., Fateeva, V. I., and Malchenko, L. A. (2003) Izvest. AN, Ser. Biol., 6, 650–657.Google Scholar
  92. 92.
    Mandelbrot, B. B. (1980) The Fractal Geometry of Nature, Freeman, NY.Google Scholar
  93. 93.
    Feder, Ye. (1991) Fractals [Russian translation], Mir, Moscow.Google Scholar
  94. 94.
    Lloyd, A. L., and Lloyd, D. (1993) Biosystem, 29, 77–85.Google Scholar
  95. 95.
    Bunde, A., and Havlin, S. (1994) Fractals in Science, Springer, New York-London.Google Scholar
  96. 96.
    Goldbeter, A. (1996) Biochemical Oscillations and Cellular Rhythms: the Molecular Basis of Periodic and Chaotic Behaviour, Cambridge University Press, Cambridge.Google Scholar
  97. 97.
    Lloyd, D., and Kippert, F. (1987) in Temperature and Animal Cells (Bowler, K., and Fuller, B. J., eds.) Cambridge University Press, Cambridge.Google Scholar
  98. 98.
    Lloyd, D., and Kippert, F. (1993) Cell Biol. Int., 17, 1047–1052.PubMedGoogle Scholar
  99. 99.
    Mano, Y. (1968) Biochem. Biophys. Res. Commun., 33, 877–882.PubMedGoogle Scholar
  100. 100.
    Kharazova, A. D. (1999) Cytological Basis of Marine Molluscs Adaptation to Salinity Changes: Doctoral dissertation [in Russian], St. Petersburg University, St. Petersburg.Google Scholar
  101. 101.
    Brodsky, V. Y., Nechaeva, N. V., and Prilutsky, V. I. (1973) Tsitologiya, 15, 177–182.Google Scholar
  102. 102.
    Ferreira, G. M., Hammond, K. D., and Gilbert, D. A. (1996) Cell Biol. Int., 20, 625–633.PubMedGoogle Scholar
  103. 103.
    Goldberger, A. L., and West, B. J. (1987) Ann. NY Acad. Sci., 504, 195–213.PubMedGoogle Scholar
  104. 104.
    Garfinkel, A., Spano, M. L., Ditto, W. L., and Weiss, J. N. (1992) Science, 257, 1230–1235.PubMedGoogle Scholar
  105. 105.
    Skinner, J. E., Goldberger, A. L., Mayer-Kress, G., and Ideker, R. F. (1990) Biotechnology, 8, 1018–1024.Google Scholar
  106. 106.
    Szeto, H., Dwyer, G., Cheng, P., and Decena, J. (1990) Proc. Conf. IEEE Medicine and Biology, 12, 1390–1391.Google Scholar
  107. 107.
    Pool, R. (1989) Science, 243, 604–607.PubMedGoogle Scholar
  108. 108.
    Elbert, T., Ray, W. J., Kovalic, Z. J., Skinner, J. E., Graf, K. E., and Birbaumer, N. (1994) Physiol. Rev., 74, 1–47.PubMedGoogle Scholar
  109. 109.
    Kleitman, N. (1963) Sleep and Wakefulness, University of Chicago Press, Chicago.Google Scholar
  110. 110.
    Kobayashi, T. Y. (1988) EEG Clin. Neurophysiol., 70, 110–117.Google Scholar
  111. 111.
    Daan, S., and Slopsema, S. (1978) J. Comp. Physiol., 127, 215–227.Google Scholar
  112. 112.
    Delgado-Garcia, I. M., Gran, C., and De Feudis, P. (1976) Exp. Brain Res., 25, 79–91.PubMedGoogle Scholar
  113. 113.
    Murell, K. F. (1971) in Biological Rhythms and Human Performance (Colquhoun, W. P., ed.) Academic Press, London-NY, pp. 241–272.Google Scholar
  114. 114.
    Brodsky, V. Y., Rapoport, S. I., Fateeva, V. I., Nechaeva, N. V., Kharayan, L. V., and Rasulov, M. I. (1984) BEBM, 5, 612–614.Google Scholar
  115. 115.
    Brodsky, V. Y., Komarov, F. I., and Rapoport, S. I. (2007) Klin. Med., 5, 4–10.Google Scholar
  116. 116.
    Zaguskin, S. L., Grinchenko, S. N., and Brodsky, V. Y. (1991) Izvest. AN, Ser. Biol., 6, 950–954.Google Scholar
  117. 117.
    Brodsky, V. Y. (1992) in Ultradian Rhythms in Life Processes (Lloyd, D., and Rossi, E., eds.) Springer, London, pp. 23–40.Google Scholar
  118. 118.
    Anisimov, V. N., Popovich, I. G., Zaberzhinski, M. A., Anisimov, S. V., Vesnushkin, G. M., and Vinogradova, I. A. (2006) Biochim. Biophys. Acta, 1757, 573–589.PubMedGoogle Scholar
  119. 119.
    Shnol, S. E. (1979) Physicochemical Factors of Biological Evolution [in Russian], Nauka, Moscow.Google Scholar
  120. 120.
    Buznikov, G. A. (1967) Low Molecular Regulators of Development [in Russian], Nauka, Moscow.Google Scholar
  121. 121.
    Buznikov, G. A. (1987) Neurotransmitters in Embryogenesis [in Russian], Nauka, Moscow.Google Scholar
  122. 122.
    Sakharov, D. A. (1991) in Early Brain (Gustavson, M., and Reuter, M., eds.) Abo Academic Press, Abo, pp. 73–88.Google Scholar
  123. 123.
    Ugrumov, M. V. (2002) Microsc. Res. Tech., 56, 164–171.PubMedGoogle Scholar
  124. 124.
    Pronina, T., Adamskaya, E., Ugrumov, M., Kuznetsova, T., Shishkina, I., Babichev, V., Calas, A., Tramu, G., Mailly, P., and Makarenko, I. (2003) J. Neuroendocrinol., 15, 549–558.PubMedGoogle Scholar
  125. 125.
    Voronezhskaya, E. E., Khabarova, M. Yu., and Nezlin, L. P. (2004) Development, 131, 3671–3680.PubMedGoogle Scholar
  126. 126.
    Oleskin, A. V. (2001) Biopolitics [in Russian], MSU, Moscow.Google Scholar
  127. 127.
    Oleskin, A. V., and Kirovskaya, T. A. (2007) Vestnik RAN, 77, 139–148.Google Scholar
  128. 128.
    Brodsky, V. Y., and Lloyd, D. (2008) in Ultadian Rhythms from Molecules to Mind (Lloyd D., and Rossi, E., eds.) Springer, London, pp. 85–104.Google Scholar
  129. 129.
    Harper, N., Hughes, M. A., Farrow, S. N., Cohen, G. M., and MacFarlane, M. (2003) J. Biol. Chem., 278, 44338–44347.PubMedGoogle Scholar
  130. 130.
    Sanchez, V., Lucas, M., Sanz, A., and Goberna, R. (1992) Biosci. Rep., 12, 199–206.PubMedGoogle Scholar
  131. 131.
    Bektas, M., and Spiegel, S. (2004) Glycoconj. J., 20, 39–47.PubMedGoogle Scholar
  132. 132.
    Segui, B., Andrieu-Abadie, N., Jaffrezou, J. P., Benoist, H., and Levade, T. (2006) Biochim. Biophys. Acta, 1758, 2104–2120.PubMedGoogle Scholar
  133. 133.
    Fouquet, S., Lugo-Martinez, V. N., Faussat, A. M., Renaud, F., and Cardot, P. (2004) J. Biol. Chem., 279, 43061–43069.PubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  1. 1.Koltsov Institute of Developmental BiologyRussian Academy of SciencesMoscowRussia

Personalised recommendations