GABAergic Mechanisms of the Brain Tolerance to Hypoxia in Lower Vertebrates

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Hypoxic/ischemic brain injuries a major medical challenge. One of the approaches to the development of therapeutic interventions is to establish the pathways of survival for neurons in tolerant to O2 deficiency vertebrates, which could suggest the ways to mitigate hypoxic catastrophe for separate cells under oxygen starvation. Metabolic depression is considered to be a universal strategy for the survival of hypoxia tolerant animals; however, the details of the mechanism of brain metabolism limitation with a decrease in PO2 have not hitherto been established. Under oxygen starvation, an increase in the extracellular concentration of inhibitory neurotransmitters can be one of the significant links in the apparatus for suppression of electrical activity, which makes it possible to reduce energy demand. GABA (γ-aminobutyric acid) serves as a universal inhibitory neurotransmitter in the CNS of higher and lower vertebrates, the functioning of which is associated with the metabolism suppression and leveling the consequences of an energy failure. GABA is found in various taxonomic groups of vertebrates. This review considers strategies for GABA involvement in the mechanisms of ensuring a brain tolerance to oxygen starvation in representatives of various taxonomic groups of lower vertebrates (cyclostomes, cartilaginous and bony fish, amphibians, reptiles), which are distinguished by a most pronounced ability to survive under acute and chronic hypoxia/anoxia.

Sobre autores

E. Kolesnikova

Kovalevsky Institute of Biology of the Southern Seas of RAS

Autor responsável pela correspondência
Email: dr-kolesnikova@mail.ru
Russia, Sevastopol

Bibliografia

  1. Mulvey JM, Renshaw GM (2009) GABA is not elevated during neuroprotective neuronal depression in the hypoxic epaulette shark (Hemiscyllium ocellatum). Comp Biochem Physiol A Mol Integr Physiol 152: 273–277. https://doi.org/10.1016/j.cbpa.2008.10.017
  2. Geßner C, Krüger A, Folkow LP, Fehrle W, Mikkelsen B, Burmester T (2022) Transcriptomes Suggest That Pinniped and Cetacean Brains Have a High Capacity for Aerobic Metabolism While Reducing Energy-Intensive Processes Such as Synaptic Transmission. Front Mol Neurosci 15. https://doi.org/10.3389/fnmol.2022.877349
  3. Bickler PE (2004) Clinical perspectives: neuroprotection lessons from hypoxia-tolerant organisms. J Exp Biol 207: 3243–3249. https://doi.org/10.1242/jeb.00977
  4. Nilsson GE (2001) Surviving anoxia with the brain turned on. Physiology 16: 217–221. https://doi.org/10.1152/physiologyonline.2001.16.5.217
  5. Larson J, Park TJ (2009) Extreme hypoxia tolerance of naked mole-rat brain. Neuroreport 20:1634–1637. https://doi.org/10.1097/WNR.0b013e32833370cf
  6. Hochachka PW, Lutz PL (2001) Mechanism, origin, and evolution of anoxia tolerance in animals. Comp Biochem Physiol B Biochem Mol Biol 130: 435–459. https://doi.org/10.1016/s1096-4959(01)00408-0
  7. McDougal DB, Holowach J, Howe MC, Jones EM, Thomas CA (1968) The effects of anoxia upon energy sources and selected metabolic intermediates in the brain of fish, frog and turtle. J Neurochem 15: 577–588. https://doi.org/10.1111/j.1471-4159.1968.tb08956.x
  8. Schmidt H, Wegener G (1988) Glycogen phosphorylase in fish brain (Carassius carassius) during hypoxia. Biochem Soc Trans 16 (4): 621–622.https://doi.org/10.1042/bst0160621
  9. Lutz P, Nilsson G (1997) Contrasting strategies for anoxic brain survival—glycolysis up or down. J Exp Biol 200: 411–419. https://doi.org/10.1242/jeb.200.2.411
  10. van Ginneken V, Nieveen M, Van Eersel R, Van den Thillart G, Addink A (1996) Neurotransmitter levels and energy status in brain of fish species with and without the survival strategy of metabolic depression. Comp Biochem Physiol A: Physiol 114: 189–196. https://doi.org/10.1016/0300-9629(95)02127-2
  11. Lutz PL, Nilsson GE, Peréz-Pinzón MA (1996) Anoxia tolerant animals from a neurobiological perspective. Comp Biochem Physiol B Biochem Mol Biol 113: 3–13. https://doi.org/10.1016/0305-0491(95)02046-2
  12. Nilsson GE, Renshaw GM (2004) Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark. J Exp Biol 207: 3131–3139. https://doi.org/10.1242/jeb.00979
  13. Nilsson GE, Lutz PL (1993) Role of GABA in hypoxia tolerance, metabolic depression and hibernation—possible links to neurotransmitter evolution. Comp Biochem Physiol C Comp Pharmacol 105: 329–336. https://doi.org/10.1016/0742-8413(93)90069-w
  14. Folkow LP, Ramirez JM, Ludvigsen S, Ramirez N, Blix AS (2008) Remarkable neuronal hypoxia tolerance in the deep-diving adult hooded seal (Cystophora cristata). Neurosci Lett 46: 147–150. https://doi.org/10.1016/j.neulet.2008.09.040
  15. Larson J, Drew KL, Folkow LP, Milton SL, Park TJ (2014) No oxygen? No problem! Intrinsic brain tolerance to hypoxia in vertebrates. J Exp Biol 217: 1024–1039. https://doi.org/10.1242/jeb.085381
  16. Hossein-Javaheri N, Buck LT (2021) GABA receptor inhibition and severe hypoxia induce a paroxysmal depolarization shift in goldfish neurons. J Neurophysiol 125: 321–330. https://doi.org/10.1152/jn.00149.2020
  17. Nilsson GE, Lutz PL (1991) Release of inhibitory neurotransmitters in response to anoxia in turtle brain. Am J Physiol Regul Integr Comp Physiol 261: R32–R37. https://doi.org/10.1152/ajpregu.1991.261.1.R32
  18. Nilsson GE, Lutz PL, Jackson T L (1991) Neurotransmitters and anoxic survival of the brain: a comparison of anoxia-tolerant and anoxia-intolerant vertebrates. Physiol Zool 64: 638–652. https://doi.org/10.1086/physzool.64.3.30158198
  19. Zajic DE, Podrabsky JE (2020) GABA metabolism is crucial for long-term survival of anoxia in annual killifish embryos. J Exp Zool 223:jeb229716. https://doi.org/10.1242/jeb.229716
  20. Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3: 728–739. https://doi.org/10.1038/nrn920
  21. Schousboe A, Bak LK, Waagepetersen HS (2013) Astrocytic control of biosynthesis and turnover of the neurotransmitters glutamate and GABA. Front Endocrinol 4: 102. https://doi.org/10.3389/fendo.2013.00102
  22. Cocco A, Rönnberg AC, Jin Z, André GI, Vossen LE, Bhandage AK, Thörnqvist PO, Birnir B, Winberg S (2017) Characterization of the γ-aminobutyric acid signaling system in the zebrafish (Danio rerio Hamilton) central nervous system by reverse transcription-quantitative polymerase chain reaction. Neuroscience 343: 300–321. https://doi.org/10.1016/j.neuroscience.2016.07.018
  23. Nilsson GE, Lutz PL (2004) Anoxia tolerant brains. J Cereb Blood Flow Metab 24: 475–486. https://doi.org/10.1097/00004647-200405000-00001
  24. Nilsson GE (1992) Evidence for a role of GABA in metabolic depression during anoxia in crucian carp (Carassius carassius). J Exp Biol 164: 243–259. https://doi.org/10.1242/jeb.164.1.243
  25. Podrabsky JE, Lopez JP, Fan TW, Higashi R, Somero GN (2007) Extreme anoxia tolerance in embryos of the annual killifish Austrofundulus limnaeus: insights from a metabolomics analysis. J Exp Biol 210: 2253–2266. https://doi.org/10.1242/jeb.005116
  26. Yoon BE, Lee CJ (2014) GABA as a rising gliotransmitter. Front Neural Circuits 8: 141. https://doi.org/10.3389/fncir.2014.00141
  27. Rossi DJ, Hamann M, Attwell D (2003) Multiple modes of GABAergic inhibition of rat cerebellar granule cells. J Physiol 548: 97–110. https://doi.org/10.1111/j.1469-7793.2003.00097.x
  28. Lee S, Yoon BE, Berglund K, Oh SJ, Park H, Shin HS, Augustine GJ, Lee CJ (2010) Channel-mediated tonic GABA release from glia. Science 330: 790–796. https://doi.org/10.1126/science.1184334
  29. Wójtowicz AM, Dvorzhak A, Semtner M, Grantyn R (2013) Reduced tonic inhibition in striatal output neurons from Huntington mice due to loss of astrocytic GABA release through GAT-3. Front Neural Circuits 7: 88. https://doi.org/10.3389/fncir.2013.00188
  30. Bickler PE, Buck LT (2007) Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69: 145–170. https://doi.org/10.1146/annurev.physiol.69.031905.162529
  31. Ramirez J-M, Folkow LP, Blix AS (2007) Hypoxia tolerance in mammals and birds: from the wilderness to the clinic. Annu Rev Physiol 69: 113–143. https://doi.org/10.1146/annurev.physiol.69.031905.163111
  32. Miyashita T, Coates MI, Farrar R, Larson P, Manning PL, Wogelius RA, Currie PJ (2019) Hagfish from the Cretaceous Tethys Sea and a reconciliation of the morphological–molecular conflict in early vertebrate phylogeny. Proc Natl Acad Sci USA 116: 2146–2151. https://doi.org/10.1073/pnas.1814794116
  33. Cox GK, Sandblom E, Richards JG, Farrell AP (2011) Anoxic survival of the Pacific hagfish (E-ptatretus stoutii). J Comp Physiol 181: 361–371. https://doi.org/10.1007/s00360-010-0532-4
  34. Cox GK, Sandblom E, Farrell AP (2010) Cardiac responses to anoxia in the Pacific hagfish, E-ptatretus stoutii. J Exp Biol 213: 3692–3698. https://doi.org/10.1242/jeb.046425
  35. Malte H, Lomholt JP (1998) Ventilation and gas exchange. The biology of hagfishes. Dordrecht: Springer Netherlands. 223–234.
  36. Johansen K, Lenfant C, Hanson D (1973) Gas exchange in the lamprey, Entosphenus tridentatus. Comp Biochem Physiol A Physiol 44: 107–119. https://doi.org/10.1016/0300-9629(73)90374-5
  37. Rovainen CM (1970) Glucose production by lamprey meninges. Science 167: 889–890. https://doi.org/10.1126/science.167.3919.889
  38. Rovainen CM, Lowry OH, Passonneau JV (1969) level of metabolites and production of glucose in the lamprey brain. J Neurochem 16: 1451–1458. https://doi.org/10.1111/j.1471-4159.1969.tb09897.x
  39. Osório J, Rétaux S (2008) The lamprey in evolutionary studies. Dev Genes Evol 218:221–235. https://doi.org/10.1007/s00427-008-0208-1
  40. Pombal MA, Álvarez-Otero R, Pérez-Fernández J, Solveira C, Megías M (2011) Development and organization of the lamprey telencephalon with special reference to the GABAergic system. Front Neuroanat 5: 20. https://doi.org/10.3389/fnana.2011.00020
  41. Robertson B, Auclair F, Ménard A, Grillner S, Dubuc R (2007) GABA distribution in lamprey is phylogenetically conserved. J Comp Neurol 503: 47–63. https://doi.org/10.1002/cne.21348
  42. Barreiro-Iglesias A, Cornide-Petronio ME, Anadón R., Rodicio MC (2009a) Serotonin and GABA are colocalized in restricted groups of neurons in the larval sea lamprey brain: insights into the early evolution of neurotransmitter colocalization in vertebrates. J Anat 215: 435–443. https://doi.org/10.1111/j.1469-7580.2009.01119.x
  43. Barreiro-Iglesias A, Villar-Cerviño V, Anadón, R, Rodicio MC (2009b) Dopamine and γ-aminobutyric acid are colocalized in restricted groups of neurons in the sea lamprey brain: insights into the early evolution of neurotransmitter colocalization in vertebrates. J Anat 215: 601–610. https://doi.org/10.1111/j.1469-7580.2009.01159.x
  44. Mann E, Enna SJ (1980) Phylogenetic distribution of bicuculline-sensitiveγ-amino-butyric acid (GABA) receptor binding. Brain Res 184: 367–373. https://doi.org/10.1016/0006-8993(80)90805-7
  45. Wise G, Mulvey JM, Renshaw GM (1998) Hypoxia tolerance in the epaulette shark (Hemiscyllium ocellatum). J Exp Zool 281: 1–5. https://doi.org/10.1002/(SICI)1097-010X(19980501)281:1<1::AID-JEZ1>3.0.CO;2-S
  46. Routley MH, Nilsson GE, Renshaw GM (2002) Exposure to hypoxia primes the respiratory and metabolic responses of the epaulette shark to progressive hypoxia. Comp Biochem Physiol A Mol Integr Physiol 131: 313–321. https://doi.org/10.1016/s1095-6433(01)00484-6
  47. Renshaw GM, Kerrisk CB, Nilsson GE (2002) The role of adenosine in the anoxic survival of the epaulette shark, Hemiscyllium ocellatum. Comp Biochem Physiol B Biochem Mol Biol 131: 133–141. https://doi.org/10.1016/s1096-4959(01)00484-5
  48. Mulvey JM, Renshaw GMC (2000) Neuronal oxidative hypometabolism in the brainstem of the epaulette shark (Hemiscyllium ocellatum) in response to hypoxic pre-conditioning. Neurosci Lett 290: 1–4. https://doi.org/10.1016/s0304-3940(00)01321-5
  49. Renshaw GM, Dyson SE (1999) Increased nitric oxide synthase in the vasculature of the epaulette shark brain following hypoxia. Neuroreport 10: 1707–1712. https://doi.org/10.1097/00001756-199906030-00015
  50. Söderström V, Renshaw GM, Nilsson GE (1999) Brain blood flow and blood pressure during hypoxia in the epaulette shark Hemiscyllium ocellatum, a hypoxia-tolerant elasmobranch. J Exp Biol 202: 829–835. https://doi.org/10.1242/jeb.202.7.829
  51. Newby AC (1984) Adenosine and the concept of ‘retaliatory metabolites’. Trends Biochem Sci 9: 42–44. https://doi.org/10.1016/0968-0004(84)90176-2
  52. Nilsson GE, Lutz PL (1992) Adenosine release in the anoxic turtle brain: a possible mechanism for anoxic survival. J Exp Biol 162: 345–351. https://doi.org/10.1242/jeb.162.1.345
  53. Pérez-Pinzón MA, Nilsson GE, Lutz PL (1993) Relationship between ion gradients and neurotransmitter release in the newborn rat striatum during anoxia. Brain Res 602: 228–233. https://doi.org/10.1016/0006-8993(93)90687-i
  54. Smeets W, Nieuwenhuys R, Roberts BL (1983) The Central Nervous System of Cartilaginous Fishes. Structure and functional correlations. Berlin-Heidelberg-New York· Springer. https://doi.org/10.1007/978-3-642-68923-9
  55. Renshaw GM, Wise G, Dodd PR (2010) Ecophysiology of neuronal metabolism in transiently oxygen-depleted environments: evidence that GABA is accumulated pre-synaptically in the cerebellum. Comp Biochem Physiol A Mol Intergr Physiol 155: 486–492. https://doi.org/10.1016/j.cbpa.2009.10.039
  56. Hebebrand J, Friedl W, Breidenbach B, Propping P (1987) Phylogenetic comparison of the photoaffinity-labeled benzodiazepine receptor subunits. J Neurochem 48: 1103–1108. https://doi.org/10.1111/j.1471-4159.1987.tb05633.x
  57. Nilsson GE (1996) Brain and body oxygen requirements of Gnathonemus petersii, a fish with an exceptionally large brain. J Exp Biol 199: 603–607. https://doi.org/10.1242/jeb.199.3.603
  58. Hylland P, Nilsson GE, Johansson D (1995) Anoxic brain failure in an ectothermic vertebrate: release of amino acids and K+ in rainbow trout thalamus. Am J Physiol 269: R1077–R1084. https://doi.org/10.1152/ajpregu.1995.269.5.R1077
  59. Shoubridge EA, Hochachka PW (1980) Ethanol: novel end product of vertebrate anaerobic metabolism. Science 209: 308–309. https://doi.org/10.1126/science.7384807
  60. Nilsson GE (1988) A comparative study of aldehyde dehydrogenase and alcohol dehydrogenase activities in crucian carp and three other vertebrates: apparent adaptations to ethanol production. J Comp Physiol 158: 479–485. https://doi.org/10.1007/BF00691145
  61. Vornanen, M, Stecyk JA, Nilsson GE (2009) The anoxia-tolerant crucian carp (Carassius carassius L.). Fish Physiol 27: 397–441. https://doi.org/10.1016/S1546-5098(08)00009-5
  62. Morosawa T (2011) Hypoxia tolerance of three native and three alien species of bitterling inhabiting Lake Kasumigaura, Japan. Environ Biol Fishes 91: 145–153. https://doi.org/10.1007/s10641-011-9767-5
  63. van Waarde A, Van den Thillart G, Verhagen M (1993) Ethanol formation and pH regulation in fish. Surviving Hypoxia: Mechanisms of Control and Adaptation. [11] CRC Press. 157–170.
  64. Holmqvist BI, Forsell J, Helvik JV (1996) Patterns of embryonic development of the brain and sensory organs studied in three marine teleost species. Soc Neurosci Abst 22: 991
  65. Kim YJ, Nam RH, Yoo YM, Lee CJ (2004) Identification and functional evidence of GABAergic neurons in parts of the brain of adult zebrafish (Danio rerio). Neurosci Lett 355: 29–32. https://doi.org/10.1016/j.neulet.2003.10.024
  66. Doldan MJ, Prego B, Holmqvist BI, de Miguel E (1999) Distribution of GABA-immunolabeling in the early zebrafish (Danio rerio) brain. Eur J Morphol 37: 126–129. https://doi.org/10.1076/ejom.37.2.126.4748
  67. Lauder JM (1993) Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci 16: 233–240. https://doi.org/10.1016/0166-2236(93)90162-f
  68. Meier E, Hertz L, Shousboe A (1991) Neurotransmitters as developmental signals. Neurochem Int 19: 1–15. https://doi.org/10.1016/0197-0186(91)90113-R
  69. Martinoli MG, Dubourg P, Geffard M, Calas A, Kah O (1990) Distribution of GABA-immunoreactive neurons in the forebrain of the goldfish, Carassius auratus. Cell Tissue Res 260: 77–84. https://doi.org https://doi.org/10.1007/BF00297492
  70. Hylland P, Nilsson GE (1999) Extracellular levels of amino acid neurotransmitters during anoxia and forced energy deficiency in crucian carp brain. Brain Res 823: 49–58. https://doi.org/10.1016/s0006-8993(99)01096-3
  71. Nilsson GE (1990) Long-term anoxia in crucian carp: changes in the levels of amino acid and monoamine neurotransmitters in the brain, catecholamines in chromaffin tissue, and liver glycogen. J Exp Biol 150: 295–320. https://doi.org/10.1242/jeb.150.1.295
  72. Buck LT, Pamenter ME (2018) The hypoxia-tolerant vertebrate brain: arresting synaptic activity. Comp Biochem Physiol B Biochem Mol Biol 224: 61–70. https://doi.org/10.1016/j.cbpb.2017.11.015
  73. Lutz PL, Nilsson GE (2004) Vertebrate brains at the pilot light. Resp Physiol Neurobiol 141: 285–296. https://doi.org/10.1016/j.resp.2004.03.013
  74. Lutz PL, Reiners R (1997) Survival of energy failure in the anoxic frog brain: delayed release of glutamate. J Exp Biol 200: 2913–2917. https://doi.org/10.1242/jeb.200.22.2913
  75. Wegener G, Krause U (1993). Environmental and exercise anaerobiosis in frogs. In Surviving Hypoxia: Mechanisms of Control and Adaptation. Boca Raton, FL: CRC Press. 217–236.
  76. Hermes-Lima M, Storey KB (1996) Relationship between anoxia exposure and antioxidant status in the frog Rana pipiens. Am J Physiol 271: R918–R925. https://doi.org/10.1152/ajpregu.1996.271.4.R918
  77. Knickerbocker DL, Lutz PL (2001) Slow ATP loss and the defense of ion homeostasis in the anoxic frog brain. J Exp Biol 204: 3547–3551. https://doi.org/10.1242/jeb.204.20.3547
  78. Siesjö BK (1978) Brain energy metabolism and catecholaminergic activity in hypoxia, hypercapnia and ischemia. J Neural Transm Suppl 14: 17–22.
  79. Franzoni MF, Morino P (1989) The distribution of GABA-like-immunoreactive neurons in the brain of the newt, Triturus cristatus carnifex, and the green frog, Rana esculenta. Cell Tissue Res 255: 155–166. https://doi.org/10.1007/BF00229077
  80. Milton SL, Manuel L, Lutz PL (2003) Slow death in the leopard frog Rana pipiens: neurotransmitters and anoxia tolerance. J Exp Biol 206: 4021–4028. https://doi.org/10.1242/jeb.00647
  81. Saransaari P, Oja SS (1998) Release of endogenous glutamate, aspartate, GABA, and taurine from hippocampal slices from adult and developing mice under cell-damaging conditions. Neurochem Res 23: 563–570. https://doi.org/10.1023/a:1022494921018
  82. Tritsch NX, Ding JB, Sabatini BL (2012) Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature 490: 262–266. https://doi.org/10.1038/nature11466
  83. Jackson DC (2002) Hibernating without oxygen: physiological adaptations of the painted turtle. J Physiol 543: 731–737. https://doi.org/10.1113/jphysiol.2002.024729
  84. Jackson DC, Ultsch GR (2010) Physiology of hibernation under the ice by turtles and frogs. J Exp Zool A Ecol Genet Physiol 313: 311–327. https://doi.org/10.1002/jez.603
  85. Hogg DW, Hawrysh PJ, Buck LT (2014) Environmental remodelling of GABAergic and glutamatergic neurotransmission: Rise of the anoxia-tolerant turtle brain. J Therm Biol 44: 85–92. https://doi.org/10.1016/j.jtherbio.2014.01.003
  86. Reese SA, Jackson DC, Ultsch GR (2002) The physiology of overwintering in a turtle that occupies multiple habitats, the common snapping turtle (Chelydra serpentina). Physiol Biochem Zool 75: 432–438. https://doi.org/10.1086/342802
  87. Crocker CE, Ultsch GR, Jackson DC (1999) The physiology of diving in a north-temperate and three tropical turtle species. J Comp Physiol B 169: 249–255. https://doi.org/10.1007/s003600050218
  88. Bennett AF, Ruben JA (1979) Endothermy and activity in vertebrates. Science 206: 649–654. https://doi.org/10.1126/science.493968
  89. Jackson DC (1968) Metabolic depression and oxygen depletion in the diving turtle. J Appl Physiol 24: 503–509. https://doi.org/10.1152/jappl.1968.24.4.503
  90. Buck LT, Land SC, Hochachka PW (1993) Anoxia-tolerant hepatocytes: model system for study of reversible metabolic suppression. Am J Physiol Regul Integr Comp Physiol 265: R49–R56. https://doi.org/10.1152/ajpregu.1993.265.1.R49
  91. Jackson DC (2000) How a turtle’s shell helps it survive prolonged anoxic acidosis. News Physiol Sci 15: 181–185. https://doi.org/10.1152/physiologyonline.2000.15.4.181
  92. Jackson DC, Ramsey AL, Paulson JM, Crocker CE, Ultsch GR (2000) Lactic acid buffering by bone and shell in anoxic softshell and painted turtles. Physiol Biochem Zool 73: 290–297. https://doi.org/10.1086/316754
  93. Buck LT, Bickler PE (1995) Role of adenosine in NMDA receptor modulation in the cerebral cortex of an anoxia-tolerant turtle (Chrysemys picta belli). J Exp Biol 198: 1621–1628. https://doi.org/10.1242/jeb.198.7.1621
  94. Pék M, Lutz PL (1997) Role for adenosine in channel arrest in the anoxic turtle brain. J Exp Biol 200: 1913–1917. https://doi.org/10.1242/jeb.200.13.1913
  95. Chih CP, Rosenthal M, Sick TJ (1989) Ion leakage is reduced during anoxia in turtle brain: a potential survival strategy. Am J Physiol Regul Integr Comp Physiol 257: R1562–R1564. https://doi.org/10.1152/ajpregu.1989.257.6.R1562
  96. Feng ZC, Rosenthal M, Sick TJ (1988) Suppression of evoked potentials with continued ion transport during anoxia in turtle brain. Am J Physiol Regul Integr Comp Physiol 255: R478–R484. https://doi.org/10.1152/ajpregu.1988.255.3.R478
  97. Milton SL, Thompson JW, Lutz PL (2002) Mechanisms for maintaining extracellular glutamate levels in the anoxic turtle striatum. Am J Physiol Regul Integr Com Physiol 282: R1317–R1323. https://doi.org/10.1152/ajpregu.00484.2001
  98. Pamenter ME, Hogg DW, Ormond J, Shin DS, Woodin, MA, Buck LT (2011) Endogenous GABAA and GABAB receptor-mediated electrical suppression is critical to neuronal anoxia tolerance.Proc Natl Acad Sci USA 108: 1274–11279. https://doi.org/10.1073/pnas.1102429108
  99. Lutz PL, Leone-Kabler SA (1995) Upregulation of GABAA receptor during anoxia in the turtle brain. Am J Physiol 37: R1332–R1335. https://doi.org/10.1152/ajpregu.1995.268.5.R1332
  100. Madsen JG, Wang T, Beedholm K, Madsen PT (2013) Detecting spring after a long winter: coma or slow vigilance in cold, hypoxic turtles? Biol Lett 9: 20130602. https://doi.org/10.1098/rsbl.2013.0602
  101. Lutz PL, Nilsson GE, Prentice H (2003) The Brain Without Oxygen, 3rd ed. Dordrecht: Kluwer Acad Publ.
  102. Buck LT, Hogg DWR, Rodgers-Garlick C, Pamenter ME (2012) Oxygen sensitive synaptic neurotransmission in anoxia-tolerant turtle cerebrocortex. Adv Exp Med Biol 758: 71–79. https://doi.org/10.1007/978-94-007-4584-1_10
  103. Blix AS, Berg T (1974) Arterial hypoxia and the diving responses of ducks. Acta Physiol Scand 92: 566–568. https://doi.org/10.1111/j.1748-1716.1974.tb05779.x
  104. Hudson DM, Jones DR (1986) The Influence of Body Mass on the Endurance to Restrained Submergence in the Pekin Duck. J Exp Biol 120: 351–367. https://doi.org/10.1242/jeb.120.1.351
  105. Kooyman GL, Kooyman TG (1995) Diving behavior of emperor penguins nurturing chicks at Coulman Island, Antarctica. The Condor 97: 536–549. https://doi.org/10.2307/1369039
  106. Caputa M, Folkow L, Blix AS (1998) Rapid brain cooling in diving ducks. Am J Physiol 275: R363–R371. https://doi.org/10.1152/ajpregu.1998.275.2.R363
  107. Blix AS, From SH (1971) Lactate dehydrogenase in diving animals—a comparative study with special reference to the eider (Somateria mollissima). Comp Biochem Physiol B Biochem 40: 579–584. https://doi.org/10.1016/0305-0491(71)90132-5
  108. Folkow LP, Blix AS (1999) Diving behaviour of hooded seals (Cystophora cristata) in the Greenland and Norwegian Seas. Polar Biology 22: 61–74.
  109. Kerem D, Elsner R (1973) Cerebral tolerance to asphyxial hypoxia in the harbour seal. Resp Physiol 19: 188–200. https://doi.org/10.1016/0034-5687(73)90077-7
  110. Erecinska E, Silver IA (2001) Tissue oxygen tension and brain sensitivity to hypoxia. Resp Physiol 128: 263–276. https://doi.org/10.1016/s0034-5687(01)00306-1
  111. Оюн НЮ, Коноров ЕА, Артюшин ИВ, Столповский ЮА (2018) Исследование генетических основ адаптации яка Bos grunniens Саяно-Алтайского региона к условиям высокогорья. Генетика 54: 70–73. [Oyun NYu, Konorov ЕА, Artyushin IV, Stolpovsky Yu A (2018) Study of the Genetic Bases of the Yak (Bos grunniens) Adaptation to the Highlands in Sayan-Altai Region. Genetics 54: 70–73. (In Russ)]. https://doi.org/10.1134/S0016675818130167
  112. Banchero N, Grover RF, Will JA (1971) Oxygen transport in the llama (Lama glama). Respir Physiol 13: 102–115. https://doi.org/10.1016/0034-5687(71)90067-3
  113. Peterson BL, Larson J, Buffenstein R, Park TJ, Fall CP (2012) Blunted neuronal calcium response to hypoxia in naked mole-rat hippocampus. PLoS One 7: e31568. https://doi.org/10.1371/journal.pone.0031568
  114. Singer D (1999) Neonatal tolerance to hypoxia: a comparative-physiological approach. Comp Biochem Physiol A Mol Integr Physiol 123: 221–234. https://doi.org/10.1016/s1095-6433(99)00057-4
  115. Duffy TE, Kohle SJ, Vannucci RC (1975) Carbohydrate and energy metabolism in perinatal rat brain: relation to survival in anoxia. J Neurochem 24: 271–276. https://doi.org/10.1111/j.1471-4159.1975.tb11875.x
  116. Friedman JE, Haddad GG (1993) Major differences in Ca2+ i response to anoxia between neonatal and adult rat CA1 neurons: role of Ca2+o and Na+o. J Neurosci 13: 63–72. https://doi.org/10.1523/JNEUROSCI.13-01-00063.1993
  117. Bickler PE, Hansen BM (1998) Hypoxia-tolerant neonatal CA1 neurons: relationship of survival to evoked glutamate release and glutamate receptor-mediated calcium changes in hippocampal slices. Brain Res Dev Brain Res 106: 57–69. https://doi.org/10.1016/s0165-3806(97)00189-2
  118. Bickler PE, Gallego SM (1993) Inhibition of brain calcium channels by plasma proteins from anoxic turtles. Am J Physiol Regul Integr Comp Physiol 265: R277–R281. https://doi.org/10.1152/ajpregu.1993.265.2.R277
  119. Huerta-Sánchez E, Jin X, Bianba Z, Peter BM, Vinckenbosch N, Liang Y, Nielsen R (2014) Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA. Nature 512: 194–197. https://doi.org/10.1038/nature13408
  120. Ge RL, Simonson TS, Gordeuk V, Prchal JT, McClain DA (2015) Metabolic aspects of high-altitude adaptation in Tibetans. Exp Physiol 100: 1247–1255. https://doi.org/10.1113/EP085292
  121. Julian CG (2017) Epigenomics and human adaptation to high altitude. J Appl Physiol 123: 1362–1370. https://doi.org/10.1152/japplphysiol.00351.2017

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