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Endogenous hypometabolic-hypothermic factors and their possible application to life in the cold

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Abstract

Mammalian hibernation is a natural model of tolerance of oragnisms, its tissues and cells to hypometabolism, hypothermia, hypoxia, bradycardia, and long-term hypophagia. Here, we review recent advances in the isolation and identification of some natural endogenous regulators from hibernating and cold-adapted animals: proteins, peptides, and nonpeptide substances. We also discuss the employment of molecular, biochemical, and physiological mechanisms of natural hypobiosis in ecology, cryomedicine, and the cryopreservation of genetic material from rare and endangered species. We suppose that our approaches can be extensively used (i) in medicine, when there is a need to slow down or suspend life processes for a short time; (ii) for the adaptation of humans to the cold; and (iii) in long-term space flights.

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Abbreviations

HIT:

hibernation induction trigger

HHFs:

hypometabolic-hypotermic factors

References

  1. Polge, C., Smith, A.U., and Parkes, A., Nature, 1949, vol. 164, pp. 666–667.

    PubMed  CAS  Google Scholar 

  2. Lozina-Lozinskii, L.K., Ocherki po kriobiologii. Adaptatsii i ustoichivost’ organizmov i kletok k nizkim i sverkhnizkim temperaturam (Essays in Cryobiology. Adaptation and Resistance of Organisms and Cells to Low and Ultralow Temperatures), Leningrad: Nauka, 1972.

    Google Scholar 

  3. Pushkar’, N.S., Belous, A.M., Itkin, Yu.A., Vishnevskii, V.I., and Rozanov, L.F., Nizkotemperaturnaya kristallizatsiya v biologicheskikh sistemakh (Low-Temperature Crystallization in Biological Systems), Kiev: Naukova dumka, 1977.

    Google Scholar 

  4. De Vries, A.L., Nimp. Biochem. Physiol. B, 1988, vol. 90, pp. 611–621.

    Google Scholar 

  5. Gakhova, E.N., CryoLetters. Supp. l, 1998, pp. 57–64.

  6. Sumida, S., Cell Tissue Bank, 2006, vol. 7, no. 4, pp. 265–305.

    PubMed  Google Scholar 

  7. Pegg, D.E., Tissue Bank, 2006, vol. 7, no. 4, pp. 349–358.

    Google Scholar 

  8. Yurchenko, T.N., Kozlova, V.F., Skornyakov, B.A., Strona, V.I., and Repin, N.V., Vliyanie krioprotektorov na biologicheskie sistemy (Effect of Cryoprotectors on Biological Systems), Kiev: Naukova dumka, 1989.

    Google Scholar 

  9. Kramarova, L.I., Gakhova, E.N., and Karnaukhov, V.N., Biofiz. Zhiv. Kletki, 1995, vol. 6, pp. 47–55.

    Google Scholar 

  10. Hochachka, P.W., Science, 1986, vol. 231, pp. 234–241.

    PubMed  CAS  Google Scholar 

  11. Freichs, K.U. and Hallenbeck, J.M., J. Cereb. Blood Flow Metab., 1998, vol. 18, pp. 168–175.

    Google Scholar 

  12. Harlow, H.J., Lohuis, T., Beck, T.D., and Iaizzo, P.A., Nature, 2001, vol. 409, p. 997.

    PubMed  CAS  Google Scholar 

  13. Sharapov, V.M., Mycopathologia, 1984, vol. 84, pp. 77–80.

    PubMed  CAS  Google Scholar 

  14. Kemper, G.B. and Ruben, R.L., Comp. Biochem. Physiol. C, 1982, vol. 73, pp. 445–450.

    PubMed  CAS  Google Scholar 

  15. Rouke, B.C, in Hypometabolism in Animals. Hibernation, Torpor and Cryobiology, Lovergrove, B.G. and McKechnie, A.E., Eds., Pietermaritzburg: Interpack Books, 2008, pp. 57–65.

    Google Scholar 

  16. Gracey, A, in Environmental Stress and Gene Regulation, Storey, K.B., Ed., Oxford: BIOS Sci. Publ. Ltd, 1999, pp. 81–94.

    Google Scholar 

  17. Carrey, H.V., Andrews, M.T., and Martin, S., Physiol. Rev., 2003, vol. 83, pp. 1153–1181.

    Google Scholar 

  18. Cannon, B., Jacobsson, A., and Nedergaard, J., in Environmental Stress and Gene Regulation, Storey, K.B., Ed., Oxford: BIOS Sci. Publ. Ltd., 1999, pp. 109–123.

    Google Scholar 

  19. Cannon, B. and Nedergaard, J., Physiol. Rev., 2004, vol. 84, pp. 277–359.

    PubMed  CAS  Google Scholar 

  20. Costanzo, J.P., Grenot, C., and Lee, R.E., J. Comp. Physiol. B, 1995, vol. 165, pp. 238–244.

    PubMed  CAS  Google Scholar 

  21. Yeh, Y. and Feeney, R.E., Chem. Rev., 1996, vol. 96, pp. 601–618.

    PubMed  CAS  Google Scholar 

  22. Amir, G., Horowitz, L., Rubinsky, B., Yousif, B.S., Lavee, J., and Smolinsky, A.K., Cryobiology, 2004, vol. 48, pp. 273–282.

    PubMed  CAS  Google Scholar 

  23. Amir, G., Rubinsky, B., Horowitz, L., Miller, L., Leor, J., Kassif, Y., Mishaly, D., Smolinsky, A.K., and Lavee, J., Ann. Thorac. Surg., 2004, vol. 77, pp. 1648–1655.

    PubMed  Google Scholar 

  24. Storey, K., Hypometabolism in Animals. Hibernation, Torpor and Cryobiology, Lovergrove, B.G. and McKechnie, A.E., Eds., Pietermaritzburg: Interpack Books, 2008, pp. 101–109.

    Google Scholar 

  25. Kalabukhov, N.I., Spyachka mlekopitayushchikh (Hybernation of Mammals), Moscow: Nauka, 1985.

    Google Scholar 

  26. Kayser, C., in The Physiology of Natural Hibernation, Knight, C.A., Ed., New York: Pergamon Press, 1961.

    Google Scholar 

  27. Lyman, C.P., Willis, J.C., Malan, A., and Wang, L.C.H., Hibernation and Torpor in Mammals and Birds, New York: Academic Press, 1982.

    Google Scholar 

  28. Wang, L.C.H., Advances in Comparative and Environmental Physiology, Berlin: Springer, 1988, vol. 2, pp. 1–45.

    Google Scholar 

  29. Kramarova, L.I, Ziganshin, R.Y, Kokoz, Y.M, and Bronnikov, G.E, in Recent Research Developments in Endocrinology, Pandalai, S.G., Ed., Kerala: Research Signpost, 2004, vol. 4,Part 2, pp. 227–263.

    Google Scholar 

  30. Barnes, A.I., Science, 1989, vol. 244, pp. 93–95.

    Google Scholar 

  31. Anufriev, A.I and Akhremenko, A.K, in Mechanisms of Natural Hypometabolic States, Kolaeva, S., Popova, N., Solomonov, N., and Wang, L.C.H., Eds., Pushchino: Pushchino Research Centre, 1992, pp. 31–35.

    Google Scholar 

  32. Frerichs, K.U., Dienel, G.A., Cruz, N.F., Sokoloff, L., and Hallenbeck, J.M., Am. J. Physiol., 1995, vol. 268, pp. R445–453.

    PubMed  CAS  Google Scholar 

  33. Yasuma, Y., McCarron, R.M., Spatz, M., and Hallenbeck, J.M., Am. J. Physiol., 1997, vol. 273, pp. R1861–1869.

    PubMed  CAS  Google Scholar 

  34. Green, C., Cryo Letters, 2000, vol. 21, pp. 91–98.

    PubMed  Google Scholar 

  35. Carey, H.V., Lindell, S., Fleck, C.C., and Southard, J.H., Gastroenterology, 2002, vol. 122, p. A354.

    Google Scholar 

  36. Gavrilyuk, B.K., Kriobiologiya, 1985, no. 3, pp. 28–30.

  37. Pakhotin, P.I., Belousov, A.B., and Otmakhov, N.A., Neuroscience, 1990, vol. 38, pp. 591–598.

    PubMed  CAS  Google Scholar 

  38. Kroll, F.W., Dtsch. Med. Wochenschr., 1952, vol. 77, pp. 879–880.

    PubMed  CAS  Google Scholar 

  39. Dawe, A. and Spurrier, W., Science, 1969, vol. 163, pp. 298–300.

    PubMed  CAS  Google Scholar 

  40. Dawe, A., Spurrier, W., and Armour, J., Science, 1970, vol. 168, no. 930, pp. 497–498.

    PubMed  CAS  Google Scholar 

  41. Dawe, A. and Spurrier, W., Cryobiology, 1971, vol. 302, p. 302.

    Google Scholar 

  42. Dawe, A. and Spurrier, W., Cryobiology, 1972, vol. 9, pp. 163–172.

    PubMed  CAS  Google Scholar 

  43. Dawe, A., Spurrier, V.., and Circannual, Clock., Annual Biological Rhythms, New York: Academic, 1974.

    Google Scholar 

  44. Swan, H., Jenkins, D., and Knox, K., Nature, 1968, vol. 217, p. 671.

    PubMed  CAS  Google Scholar 

  45. Swan, H., Jenkins, D., and Knox, K., The American Naturalist, 1969, vol. 103, pp. 247–257.

    CAS  Google Scholar 

  46. Swan, H. and Schatte, C., Science, 1977, vol. 195, pp. 84–85.

    PubMed  CAS  Google Scholar 

  47. Swan, H., Reinhard, F.G., Caprio, D.L., and Schatte, C.L., Cryobiology, 1981, vol. 18, pp. 598–602.

    PubMed  CAS  Google Scholar 

  48. Amorese, D., Swan, H., and Bamburg, J., Proc. Natl. Acad. Sci. USA, 1982, vol. 79, pp. 6375–6379.

    PubMed  CAS  Google Scholar 

  49. Oeltgen, P.R., Walsh, J.W., Hamman, S.R., Randall, D.C., Spurrier, W.A., and Myers, R.D., Pharm. Biochem. Behav, 1982, vol. 17, pp. 1271–1274.

    CAS  Google Scholar 

  50. Bruce, D.S., Tuggy, M.L., and Pearson, P.J., Cryobiology, 1984, vol. 21, pp. 371–374.

    Google Scholar 

  51. Bruce, D.S., Cope, G.W., Elam, T.R., Ruit, K.A., Oeltgen, P.R., and Su, T.P., Life Sci., 1987, vol. 41, no. 18, pp. 2107–2113.

    PubMed  CAS  Google Scholar 

  52. Bruce, D., Cox, D., Crane, S., Denholm, M., Dhyanchand, R., Hampl, M., Kary, J., Krober, A., Oeltgen, P., Horton, N., and Harlow, H., Pharmacol. Biochem. Behav., 1997, vol. 58, pp. 627–630.

    PubMed  CAS  Google Scholar 

  53. Horton, N.D., Kaftani, D.J., Bruce, D.S., Bailey, E.C., Krober, A.S., Jones, J.R., Turker, M., Khattar, N., Su, T.P., Bolling, S.F., and Oeltgen, P.R., Comp. Biochem. Phys. (B), 1998, vol. 119, pp. 787–805.

    CAS  Google Scholar 

  54. Sieckmann, D.G, Cai, D, Jaffe, H, Hallenbeck, J, and McCarron, R.M, in Life in the Cold, Barnes, B.M. and Carey, H.V., Eds., Fairbanks: Univ. Alaska Fairbanks Press, 2004, pp. 519–527.

    Google Scholar 

  55. Kondo, N. and Kondo, J., J. Biol. Chem, 1992, vol. 267, pp. 473–478.

    PubMed  CAS  Google Scholar 

  56. Kondo, N and Kondo, J, in Life in the Cold, Carey, C., FIorant, G.., Wunder, B.., and Horwitz, B., Eds., Westiver Press, 1993, pp. 297–303.

  57. Takamatsu, N., Ohba, K., Kondo, J., Kondo, N., and Shiba, T., Mol. Cell. Biol., 1993, vol. 13, pp. 1516–1521.

    PubMed  CAS  Google Scholar 

  58. Kondo, N and Joh, T, in Adaptation to the Cold, Geiser, F., Hulbert, A.J., and Nicols, S.C., Eds., Armidale, NSW, Australia: Univ. New England Press, 1996, pp. 341–345.

    Google Scholar 

  59. Kondo, N., Sekijima, T., Kondo, J., Takamatsu, N., Tohya, K., and Ohtsu, T., Cell, 2006, vol. 125, no. 1, pp. 161–172.

    PubMed  CAS  Google Scholar 

  60. Kondo, N., Cold Spring Harb. Symp. Quant. Biol., 2007, vol. 72, pp. 607–613.

    PubMed  CAS  Google Scholar 

  61. Takamatsu, N., Ohba, K., Kondo, J., Kondo, N., and Shiba, T., Mol. Cell. Biol., 1993, vol. 13, pp. 1516–1521.

    PubMed  CAS  Google Scholar 

  62. Takamatsu, N., Kojima, M., Taniyama, M., Ohba, K., Uematsu, T., Segawa, C., Tsutou, S., Watanabe, M., Kondo, J., Kondo, N., and Shiba, T., Gene, 1997, vol. 204, pp. 127–132.

    PubMed  CAS  Google Scholar 

  63. Sekijuma, T., Kondo, J., Ohtsu, T., and Kondo, N., in Life in the Cold, Heldmaier, G. and Klingenspor, M., Eds., Berlin: Springer, 2000, pp. 367–376.

    Google Scholar 

  64. Reinhard, F.G., Acta Universitatis Carolinae. Biologica, 1979, nos. 3–4, pp. 275–276.

  65. Reinhard, F.G., Hormone-Like Peptides and Use Thereof, US Patent 4 332 920, 1983.

  66. Kolaeva, S.G., Kramarova, L.I., Iljasova, E.N., and Iliasov, F.E., Int. Rev. Cytol., 1980, vol. 66, pp. 147–169.

    PubMed  CAS  Google Scholar 

  67. Svieryev, V.I., Vakovsky, B.I., Ziganshin, R.H., Mikhaleva, I.I., Ivanov, V.T., Kokoz, Y.M., Povzun, A.A., Aleksev, A.E., Sukhova G.S., in Proceeding of the 21 European Symp. Peptides, Giraltand, E. and Andreu, D., Eds., Leiden: Escom, 1990, pp. 751–752.

    Google Scholar 

  68. Mikhaleva, I.I. and Svieryev, V.I., Vaskovsky A.I., Ziganshin R.H., Kokoz Y.M., Povzun A.A., Alekseev A.E., Ignatiev D.A., Sukhova G.S., Emelyanova T.G., Ivanov V.T, Abstracts of the 8th FRG-USSR Symp. on Chemistry of Peptides and Proteins. Aahen, 1991, p. 27.

  69. Mikhaleva, I.I., Svieryev, V.I., Vaskovsky, B.I., Ziganshin, R.H., Ivanov, V.T., Kokoz, Y.M., Povzun, A.A., Alekseev, A.E., Ignatiev, D.A., and Sukhova, G.S., in Chemistry of Peptides and Proteins, Voelter, W., Bayer, E., Ivanov, V.T., and De Gruyter, W., Eds., Berlin, 1993, vol. 5/6,part A, pp. 286–297.

  70. Mikhaleva, I.I., Svieryev, V.I., Vaskovsky, B.I., Ziganshin, R.H., Ivanov, V.T., Kokoz, Y.M., Povzun, A.A., Alekseev, A.E., Ignatiev, D.A., Kruman, I.M., and Sukhova, G.S., in Chemistry of Peptides and Proteins, Voelter, W., Bayer, E., Ivanov, V.T., and De Gruyter, W., Eds., Berlin, 1993, vol. 5/6,part A, pp. 298–308.

  71. Kokoz, Yu.M., Nakipova, O.V., Sviryaev, V.I., Kramarova, L.I., Povzun, A.A., Mikhaleva, I.I., Freidin, A.A., Malygin, A.M., Kolaeva, S.G., and Il’yasov, F.E., in Mekhanizmy zimnei spyachki (Mechanisms of Hibernation), Pushchino: Pushch. Nauch. Tsentr Akad. Nauk SSSR, 1987, pp. 146–159.

    Google Scholar 

  72. Kondo, N., Circ. Res., 1986, vol. 59, pp. 221–228.

    PubMed  CAS  Google Scholar 

  73. Sukhova, G.S., Levashova, V.G., Kramarova, L.I., Sviryaev, V.I., Ziganshin, R.Kh., Kolaeva, S.G., Mikhaleva, I.I., and Povzun, A.A., Dokl. Akad. Nauk SSSR, 1989, vol. 307, pp. 1512–1514.

    PubMed  CAS  Google Scholar 

  74. Sukhova, G.S., Ignat’ev, D.A., Akhremenko, A.K., Levashova, V.G., Mikhaleva, I.I., Sviryaev, V.I., Anufriev, A.I., Ziganshin, R.Kh., Kramarova, L.I., and Gnutov, D.A., Zh. Evol. Biokhim. Fiziol., 1990, vol. 26, pp. 623–629.

    PubMed  CAS  Google Scholar 

  75. Sukhova, G.S, Ignatiev, D.A, Levashova, V.G, Sukhov, V.P, Mikhaleva, I.I., Kramarova L.I., Svieryev, V.I., Ziganshin, R.C., Kolaeva, S.G., and Ashmarin, I.P., in Mechanisms of Natural Hypometabolic States, Kolaeva, S., Popova, N., Solomonov, N., and Wang, L.C.H., Eds., Pushchino: Pushchino Research Centre, 1992, pp. 190–202.

    Google Scholar 

  76. Pokrovskii, V.M. and Osadchii, O.E., Sheikhzade Yu.R., Sviryaev V.I., Vas’kovskii B.V., Ziganshin R.Kh., Mikhaleva I.I, Fiziol. Zh. SSSR im. I.M. Sechenova, 1992, vol. 78, pp. 26–31.

    PubMed  CAS  Google Scholar 

  77. Kokoz, Y.M., Zenchenko, K.I., Alekseev, A.E., Korystova, A.F., Lankina, D.A., Ziganshin, R.H., Mikhaleva, I.I., and Ivanov, V.T., FEBS Lett., 1997, vol. 411, pp. 71–76.

    PubMed  CAS  Google Scholar 

  78. Blishenko, E.Yu., Mernenko, O.A., Yatskin, O.N., Ziganshin, R.H., Philippova, M.M., Karelin, A.A., and Ivanov, V.T., FEBS Lett., 1997, vol. 414, pp. 125–128.

    Google Scholar 

  79. Bronnikov, G., Dolgacheva, L.P., Zhang, S.J., Galitovskaya, E., Kramarova, L., and Zinchenko, V.P., FEBS Lett., 1997, vol. 407, pp. 73–77.

    PubMed  CAS  Google Scholar 

  80. Kharchenko, I.B., Nazarenko, I.V., Ziganshin, R.Kh., Koshelev, V.B., Kamenskii, A.A., and Volkov, A.V., Eksperimental’nye, klinicheskie i organizatsionnye problemy obshchei reanimatologii: Sbornik trudov k 60-letiyu NII obshchei reanimatologii RAMN, (Experimental, Clinical, and Organizational Problems of Gen eral Resuscitation Science: Collected Works on the 60th Anniversary of the Research Institute of General Resuscitation Studies), Negovskii, V.A., Ed., Moscow, 1996, pp. 101–118.

  81. Zenchenko, K.I., Kokoz, Yu.M., Ivanov, V.T., Ziganshin, R.Kh., and Vinogradova, O.S., Zh. Vyssh. Nerv. Deyat. Im. I.P. Pavlova, 2000, vol. 50, pp. 647–657.

    CAS  Google Scholar 

  82. Zenchenko, K.I., Kokoz, Y.M., Ivanov, V.T., Ziganshin, R.H., and Vinogradova, O.S., Neuroscience, 2000, vol. 96, pp. 791–805.

    PubMed  CAS  Google Scholar 

  83. Popova, I.Yu., Vinogradova, O.S., Kokoz, Yu.M., Ziganshin, R.Kh., and Ivanov, V.T., Zh. Vyssh. Nerv. Deyat. Im. I.P. Pavlova, 2002, vol. 52, pp. 218–227.

    CAS  Google Scholar 

  84. Popova, I.Yu., Vinogradova, O.S., Kokoz, Yu.M., Ziganshin, R.Kh., and Ivanov, V.T., Zh. Vyssh. Nerv. Deyat. Im. I.P. Pavlova, 2006, vol. 52, pp. 347–355.

    Google Scholar 

  85. Ziganshin, R.H, Mikhaleva, I.I, Ivanov, V.T, Kokoz, Yu.M, Korystova, A.F, Mavlyutova, D.A, and Emelyanova, T.G, in Adaptation to the Cold, Geiser, F., Hulbert, A.J., and Nicols, S.C., Eds., Armidale, NSW, Australia: Univ. New England Press, 1996, pp. 373–378.

    Google Scholar 

  86. Ignat’ev, D.A., Mikhaleva, I.I., Sosulina, L.Yu., Zakaryan, A.A., Sukhova, G.S., and Ziganshin, R.Kh., Zh. Evol. Biokhim. Fiziol, 2001, vol. 37, pp. 201–205.

    PubMed  Google Scholar 

  87. Kramarova, L, Ziganshin, R, Timoshenko, M, Mikhaleva, I, and Karnaukhov, V, in Adaptation to the Cold, Geiser, F., Hulbert, A.J., and Nicols, S.C., Eds., Armidale, NSW, Australia: Univ. New England Press, 1996, pp. 379–384.

    Google Scholar 

  88. Ivanitskii, G.R., Kolaeva, S.G., Pastukhov, Yu.F., Kramarova, L.I., Sapozhkova, G.G., Chepkasov, I.E., Il’yasov, F.E., and Il’yasova, E.N., Dokl. Akad. Nauk SSSR, 1982, vol. 267, pp. 978–980.

    Google Scholar 

  89. Kramarova, L.I., Kolaeva, S.G., Bronnikov, T.E., and Krasts, I.V., in Mekhanizmy zimnei spyachki (Mechanisms of Hibernation), Pushchino: Pushch. Nauch. Tsentr Akad. Nauk SSSR, 1987, pp. 138–145.

    Google Scholar 

  90. Kramarova, L.I., Kolaeva, S.G., Bronnikov, G.E., Ignatiev, A.D., and Krasts, I.V., Can. J. Physiol. Pharmacol., 1993, vol. 71, pp. 293–296.

    PubMed  CAS  Google Scholar 

  91. Ignat’ev, D.A., Zh. Obshch. Biol., 1995, vol. 56, pp. 450–469.

    PubMed  Google Scholar 

  92. Belyavskii, M.A., Matveeva, N.B., and Beilina, S.I., Mekhanizmy zimnei spyachki (Mechanisms of Hibernation), Pushchino: Pushch. Nauch. Tsentr Akad. Nauk SSSR, 1987, pp. 133–136.

    Google Scholar 

  93. Karmanova, I.G., Kolaeva, S.G., Kramarova, L.I., Aristakesyan, E.A., Shilling, N.V., Khomutetskaya, O.E., and Sapozhkova, G.G., Kriobiol. Kriomed., 1984, vol. 15, pp. 36–40.

    Google Scholar 

  94. Wang, L.C.H, in Life in the Cold, Carey, C., FIorant, G.L., Wunder, B., and Horwitz, B., Eds., Westviev Press, 1993, pp. 297–303.

  95. Kramarova, L.I., Kolaeva, S.G., Yukhananov, R.Y., and Rozhanets, V.V., Comp. Biochem. Physiol. C, 1983, vol. 74, pp. 31–33.

    PubMed  CAS  Google Scholar 

  96. Kramarova, L.I., Lee, T.F., and Wang, L.C.H., Life Sci., 1991, vol. 48, pp. 175–181.

    PubMed  CAS  Google Scholar 

  97. Stanton, T.L., Beckman, A.L., and Winikur, A.N., Reg. Pept., 1982, vol. 3, pp. 135–144.

    CAS  Google Scholar 

  98. Ziganshin, R.Kh., Sviryaev, V.I., Vas’kovskii, B.V., Mikhaleva, I.I., Ivanov, V.T., Kokoz, Yu.M., Alekseev, A.E., Kor’gstova, A.F., Sukhova, G.S., Emel’-yanova, T.G., and Usenko, A.B., Bioorg. Khim., 1994, vol. 20, pp. 899–918.

    PubMed  CAS  Google Scholar 

  99. Cui, Y., Lee, T.F., Kramarova, L.I., and Wang, L.C.H., Life Sci., 1993, vol. 50, pp. 215–223.

    Google Scholar 

  100. Walker, J., Haakel, E., and Berger, I., Heller N, Experientia, 1981, vol. 37, pp. 726–728.

    PubMed  CAS  Google Scholar 

  101. Lynch, G., White, S., Grundel, R., and Berger, M., J. Comp. Physiol., 1978, vol. 125, pp. 157–163.

    CAS  Google Scholar 

  102. Hishikawa, Y., Gramer, H., and Kulio, W., Exp. Brain Res., 1969, vol. 7, pp. 84–94.

    PubMed  CAS  Google Scholar 

  103. Inoue, S., Honda E., Komoda Y., Uchizono E., Ueno R, Proc. Natl. Acad. Sci. USA, 1984, vol. 81, pp. 6240–6244.

    PubMed  CAS  Google Scholar 

  104. Young, A. and Key, B., Neuropharm., 1984, vol. 23, pp. 1347–1350.

    CAS  Google Scholar 

  105. Graf, M. and Kastin, A., Neurosci. Biobehav. Rev., 1984, vol. 8, pp. 83–93.

    PubMed  CAS  Google Scholar 

  106. Dick, P., Costa, G., and Fayolle, K., Eur. Neurol., 1984, vol. 23, pp. 364–371.

    PubMed  CAS  Google Scholar 

  107. Dick, P., Grandjean, M., and Tissot, R., Neuropsychobiology, 1983, vol. 10, pp. 205–208.

    PubMed  CAS  Google Scholar 

  108. Koplik, E.V., Vedyaev, D.F., and Mikhaleva, I.I., Dokl. Akad. Nauk SSSR, 1982, vol. 267, pp. 230–233.

    PubMed  CAS  Google Scholar 

  109. Sudakov, K.V., Ivanov, V.T., Koplik, E.V., Vedjaev, D.F., Michaleva, I.I., and Sargsjan, A.S., Pavlov J. Biol. Sci., 1983, vol. 18, pp. 1–5.

    PubMed  CAS  Google Scholar 

  110. Krueger, J.M., Pappenheimer, J.R., and Karnovsky, M.L., J. Biol. Chem., 1982, vol. 257, pp. 1664–1669.

    PubMed  CAS  Google Scholar 

  111. Martin, S.A., Karnovsky, M.L., Krueger, J.M., Pappenheimer, J.R., and Biemann, K., J. Biol. Chem., 1984, vol. 259, pp. 12652–12658.

    PubMed  CAS  Google Scholar 

  112. Krueger, J.M., Karnovsky, M.L., Martin, S.A., Pappenheimer, J.R., Walter, J., and Biemann, K., J. Biol. Chem., 1984, vol. 259, pp. 12659–12662.

    PubMed  CAS  Google Scholar 

  113. Krueger, J.M., Pappenheimer, J.R., and Karnovsky, M.L., Proc. Natl. Acad. Sci. USA, 1982, vol. 79, pp. 6102–6106.

    PubMed  CAS  Google Scholar 

  114. Wang, L.C.H and Lee, T.F, in Torpor and Hibernation in Mammals: Metabolic, Physiological and Biochemical Adaptations, Fregley, M.J. and Blatteis, C.M., Eds., Handbook of Physiology, Environmental Physiology, Section 4, New York: Oxford Univ. Press, 1996, vol. 1, pp. 507–532.

    Google Scholar 

  115. Popova, N.K., Fiziol. Zh. SSSR im. I.M. Sechenova, 1975, vol. 61, pp. 153–156.

    PubMed  CAS  Google Scholar 

  116. Popova, N.K., Naumenko, E.V., and Kolpakov, V.G., Serotonin i povedenie (Serotonin and Behavior), Novosibirsk: Nauka, 1978.

    Google Scholar 

  117. Ates, B., Yilmaz, I., Geckil, H., Iraz, M., Birincioglu, M., and Fiskin, K., J. Pineal Res., 2004, vol. 37, pp. 149–152.

    PubMed  CAS  Google Scholar 

  118. Tamura, Y., Monden, M., Shintani, M., Kawai, A., and Shiomi, H., Brain Res., 2006, vol. 1108, pp. 107–116.

    PubMed  CAS  Google Scholar 

  119. Atanassov, C.L., Naegelit, H.-U., Zenket, G., Schneider, C., Kramarova, L.I., Bronnikov, G.E., and van Regenmortel, M.H.V., Comp. Biochem. Physiol. (C), 1995, vol. 112, pp. 93–100.

    CAS  Google Scholar 

  120. Sukhova, G.S., Sosulina, L.Yu., Negulyaev, O.V., Ziganshin, R.Kh., and Mikhaleva, I.I., Zh. Evol. Biokhim. Fiziol., 1998, vol. 34, pp. 43–47.

    PubMed  CAS  Google Scholar 

  121. Nystul, T.G. and Roth, M.B., Proc. Natl. Acad. Sci. USA, 2004, vol. 15, pp. 9133–9136.

    Google Scholar 

  122. Blackstone, E. and Roth, M.B., Shock, 2007, vol. 27, pp. 370–372.

    PubMed  CAS  Google Scholar 

  123. Rubinsky, B., Arav, A., and DeVries, A.L., Cryobiology, 1992, vol. 29, pp. 69–79.

    PubMed  CAS  Google Scholar 

  124. Rubinsky, A., Arav, A., Hong, J.-S., Lee, C.Y., Biochem. Biophys. Res. Commun., 1994, vol. 200, pp. 732–741.

    PubMed  CAS  Google Scholar 

  125. Soltys, K.A., Batta, A.K., and Konery, B., J. Surg. Res., 2001, vol. 96, pp. 30–34.

    PubMed  CAS  Google Scholar 

  126. Wang, T., Connery, C., Batty, P., Hicks, G., and DeWeese, J., Layne JR, Cryobiology, 1991, vol. 28, pp. 171–176.

    PubMed  CAS  Google Scholar 

  127. Wang, T., Banker, M.C., Claydon, M., Hicks, G.L., and Layne, J.R., Cryobiology, 1992, vol. 29, pp. 470–477.

    PubMed  CAS  Google Scholar 

  128. Banker, M., Layne, J.R., Hicks, G.L., and Wang, T., Cryobiology, 1992, vol. 29, pp. 87–94.

    PubMed  CAS  Google Scholar 

  129. Zhu, Q., Layne, J.R., Claydon, M., Hicks, G.L., and Wang, T., Cryobiology, 1992, vol. 29, pp. 478–484.

    PubMed  CAS  Google Scholar 

  130. Storey, K.B., Biochem. Cell Biol., 1990, vol. 68, pp. 687–698.

    PubMed  CAS  Google Scholar 

  131. Chien, S., Oeltgen, P., Diana, J., Shi, X., Nilekani, S., and Salley, R., J. Thorac. Cardiovasc. Surg., 1991, vol. 102, pp. 224–234.

    PubMed  CAS  Google Scholar 

  132. Hittel, D. and Storey, K., Biochim. Biophys. Acta, 2001, vol. 1522, pp. 238–243.

    PubMed  CAS  Google Scholar 

  133. Cochrane, J., Williams, B., Banerjee, A., Harkenm, A.H., Burke, T.J., Cairns, C.B., and Shapiro, J.I., Ren. Fail., 1999, vol. 21, pp. 135–145.

    PubMed  CAS  Google Scholar 

  134. Hittel, D.S. and Storey, K.B., J. Exp. Biol., 2002, vol. 205, pp. 1625–1631.

    PubMed  CAS  Google Scholar 

  135. Drew, K.L., Rice, M., Kuhn, T.B., and Smith, M., Free Radic. Biol. Med., 2001, vol. 31, pp. 563–573.

    PubMed  CAS  Google Scholar 

  136. May, T., Drug Discovery Today, 2003, vol. 8, pp. 51–52.

    PubMed  Google Scholar 

  137. Zhou, F., Zhu, X., Castellani, R.J., Simmelmayr, R., Perry, G., Smith, M.A., and Drew, K.L., Am. J. Pathol., 2001, vol. 158, pp. 2145–2151.

    PubMed  CAS  Google Scholar 

  138. Brown, S.A, Givindaswami, M, Bishop, P.D, Kindy, M.S, and Oeltgen, P.R, in Hypometabolism in Animals. Hibernation, Torpor and Cryobiology, Lovergrove, B.G. and McKechnie, A.E., Eds., Pietermaritzburg: Interpack Books, 2008, pp. 37–49.

    Google Scholar 

  139. Oeltgen, P.R., Horton, N.D., Bolling, S.F., and Su, T.P., Ann. Thorac. Surg., 1996, vol. 61, pp. 1488–1493.

    PubMed  CAS  Google Scholar 

  140. Govindaswami, M, Sanchez, J.A, Wedge, J, Langstone, M.D, Bishop, P.D, Bruce, D.S, and Oeltgen, P.R, in Life in the Cold, Heldmaier, G. and Klingenspor, M., Eds., Berlin: Springer, 2000, pp. 377–386.

    Google Scholar 

  141. Yamanouchi, K., Yanaga, K., Okudaira, S., Eguchi, S., Furui, J., and Kanematsu, T., J. Surg. Res., 2003, vol. 114, pp. 72–77.

    PubMed  CAS  Google Scholar 

  142. Cui, J., Chen, Q., Yu, L.C., and Zhang, Y., Neuroreport, 2008, vol. 19, pp. 1745–1749.

    PubMed  CAS  Google Scholar 

  143. Goncharevskaya, O.A., Monin, Y.G., Kramarova, L.I., and Kolaeva, S.G., Physiologia Bohemoslovaca, 1990, vol. 39, pp. 425–431.

    PubMed  CAS  Google Scholar 

  144. Ignat’ev, D.A., Ekologofiziologicheskie kharakteristiki prirodnykh gipometabolicheskikh sostoyanii (Ecological-Physiological Characteristics of Natural Hypometabolic States), Pushchino, 1992, pp. 101–116.

  145. Timofeev, N.N., Iskusstvennyi gipobioz (Artificial Hypobiosis), Moscow: Meditsina, 1983.

    Google Scholar 

  146. Geiser, F., Hibernation and Daily Torpor in Marsupials, Aust. J. Zool., 1994, vol. 42, pp. 1–16.

    Google Scholar 

  147. Geiser, F., in Adaptation to the Cold, Geiser, F., Hulbert, A.J., and Nicols, S.C., Eds., Armidale, NSW, Australia: Univ. New England Press, 1996, pp. 81–86.

    Google Scholar 

  148. Geiser, F., in Hypometabolism in Animals. Hibernation, Torpor and Cryobiology, Lovergrove, B.G. and McKechnie, A.E., Eds., Pietermaritzburg: Interpack Books, 2008, pp. 297–306.

    Google Scholar 

  149. Nicol, S.C, Morrow, G., and Andersen, N.A, in Hypometabolism in Animals. Hibernation, Torpor and Cryobiology, Lovergrove, B.G. and McKechnie, A.E., Eds., Pietermaritzburg: Interpack Books, 2008, pp. 251–263.

    Google Scholar 

  150. Dausmann, K.H., Glos, J., Ganzhorn, J.U., and Heldmaier, G., Nature, 2004, vol. 429, pp. 825–826.

    PubMed  CAS  Google Scholar 

  151. Dausmann, K.H., Glos, J., Ganzhorn, J.U., and Heldmaier, G., J. Comp. Physiol. (B), 2005, vol. 175, pp. 147–155.

    Google Scholar 

  152. Hammel, H.T, in Adaptation to the Environment. Handbook of Physiology, Section 4, Dill, D.B., Adolph, E.F., and Wilber, C.G., Eds., Washington, DC: Amer. Physiol. Soc., 1964, pp. 413–434.

    Google Scholar 

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Original Russian Text © L.I. Kramarova, R.Kh. Ziganshin, E.N. Gakhova, 2009, published in Bioorganicheskaya Khimiya, 2009, Vol. 35, No. 5, pp. 597–609.

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Kramarova, L.I., Ziganshin, R.K. & Gakhova, E.N. Endogenous hypometabolic-hypothermic factors and their possible application to life in the cold. Russ J Bioorg Chem 35, 538–548 (2009). https://doi.org/10.1134/S1068162009050021

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