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Neuroprotective Mechanism of Hypoxic Post-conditioning Involves HIF1-Associated Regulation of the Pentose Phosphate Pathway in Rat Brain

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Abstract

Post-conditioning is exposure of an injured organism to the same harmful factors but of milder intensity which mobilizes endogenous protective mechanisms. Recently, we have developed a novel noninvasive post-conditioning (PostC) protocol involving three sequential episodes of mild hypobaric hypoxia which exerts pronounced neuroprotective action. In particular, it prevents development of pathological cascades caused by severe hypobaric hypoxia (SH) such as cellular loss, lipid peroxidation, abnormal neuroendocrine responses and behavioural deficit in experimental animals. Development of these post-hypoxic pathological effects has been associated with the delayed reduction of hypoxia-inducible factor 1 (HIF1) regulatory α-subunit levels in rat hippocampus, whereas PostC up-regulated it. The present study has been aimed at experimental examination of the hypothesis that intrinsic mechanisms underlying the neuroprotective and antioxidant effects of PostC involves HIF1-dependent stimulation of the pentose phosphate pathway (PPP). We have observed that SH leads to a decrease of glucose-6-phosphate dehydrogenase (G6PD) activity in the hippocampus and neocortex of rats as well as to a reduction in NADPH and total glutathione levels. This depletion of the antioxidant defense system together with excessive lipid peroxidation during the reoxygenation phase resulted in increased oxidative stress and massive cellular death observed after SH. In contrast, PostC led to normalization of G6PD activity, stabilization of the NADPH and total glutathione levels and thereby resulted in recovery of the cellular redox state and prevention of neuronal death. Our data suggest that stabilization of the antioxidant system via HIF1-associated PPP regulation represents an important neuroprotective mechanism enabled by PostC.

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Abbreviations

G6PD:

Glucose-6-phosphate dehydrogenase

HIF1:

Hypoxia-inducible factor 1

IPostC:

Ischemic post-conditioning

PostC:

Post-conditioning by mild hypobaric hypoxia

NADPH:

Reduced nicotinamide adenine dinucleotide phosphate

PPP:

Pentose phosphate pathway

ROS:

Reactive oxygen species

SH:

Severe hypobaric hypoxia

TUNEL:

Terminal deoxynucleotidyl transferase (TdT) deoxyuridine triphosphate (dUTP) nick end labeling

References

  1. Van Liere E, Stickney J (1963) Hypoxia. The University of Chicago Press, Chicago

    Google Scholar 

  2. Rybnikova E, Samoilov M (2015) Current insights into the molecular mechanisms of hypoxic pre- and postconditioning using hypobaric hypoxia. Front Neurosci. https://doi.org/10.3389/fnins.2015.00388

    Article  PubMed  PubMed Central  Google Scholar 

  3. Zhao ZQ, Corvera J, Halkos M, Kerendi F, Wang NP, Guyton R, Vinten-Johansen J (2003) Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 285:579–588

    Article  Google Scholar 

  4. Zhao H, Sapolsky R, Steinberg G (2006) Interrupting reperfusion as a stroke therapy: ischemic postconditioning reduces infarct size after focal ischemia in rats. J Cereb Blood Flow Metab 26:1114–1121

    Article  CAS  PubMed  Google Scholar 

  5. Zhao HX, Wang XL, Wang YH, Wu Y, Li XY, Ly XP, Zhao ZQ, Zhao RR, Liu HR (2010) Attenuation of myocardial injury by postconditioning: role of hypoxia inducible factor-1a. Basic Res Cardiol 105:109–118

    Article  CAS  PubMed  Google Scholar 

  6. Danielisova V, Nemethova M, Gottlieb M, Burda J (2006) The changes in endogenous antioxidant enzyme activity after postconditioning. Cell Mol Neurobiol 26:1181–1191

    Article  CAS  PubMed  Google Scholar 

  7. Gao X, Ren C, Zhao H (2008) Protective effects of ischemic postconditioning compared with gradual reperfusion or preconditioning. J Neurosci Res 86:2505–2511

    Article  CAS  PubMed  Google Scholar 

  8. Ren C, Gao X, Niu G, Yan Z, Chen X, Zhao H (2008) Delayed postconditioning protects against focal ischemic brain injury in rats. PLoS ONE 3:e3851. https://doi.org/10.1371/journal.pone.0003851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Song W, Dong H, Cheng O, Lu Z, Wang H, Meng J, Xiong L (2008) Ischemic postconditioning induced neuroprotection via up-regulation of endogenus antioxidant enzyme activities: experiment with rabbits. Zhonghua Yi Xue Za Zhi 88:2355–2359

    CAS  PubMed  Google Scholar 

  10. Scartabelli T, Gerace E, Landucci E, Moroni F, Pellegrini-Giampietro D (2008) Neuroprotection by group I mGlu receptors in a rat hippocampal slice model of cerebral ischemia is associated with the PI3K-Akt signaling pathway: a novel postconditioning strategy? Neuropharmacology 55:509–516

    Article  CAS  PubMed  Google Scholar 

  11. Leconte C, Tixier E, Freret T, Toutain J, Saulnier R, Boulouard M, Roussel S, Schumann-Bard P, Bernaudin M (2009) Delayed hypoxic postconditioning protects against cerebral ischemia in the mouse. Stroke 40:3349–3355

    Article  PubMed  Google Scholar 

  12. Li Z-Y, Liu B, Yu J, Yang FW, Luo YN, Ge PF (2012) Ischaemic postconditioning rescues brain injury caused by focal ischaemia/reperfusion via attenuation of protein oxidization. J Int Med Res 40:954–966

    Article  CAS  PubMed  Google Scholar 

  13. Xing B, Chen H, Zhang M, Zhao D, Jiang R, Liu X, Zhang S (2008) Ischemic postconditioning inhibits apoptosis after focal cerebral ischemia/reperfusion injury in the rat. Stroke 39:2362–2369

    Article  CAS  PubMed  Google Scholar 

  14. Gao X, Zhang H, Takahashi T, Hsieh J, Liao J, Steinberg GK, Zhao H (2008) The Akt signaling pathway contributes to postconditioning’s protection against stroke; the protection is associated with the MAPK and PKC pathways. J Neurochem 105:943–955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Yuan Y, Guo Q, Ye Z, Pingping X, Wang N, Song Z (2011) Ischemic postconditioning protects brain from ischemia/reperfusion injury by attenuating endoplasmic reticulum stress-induced apoptosis through PI3K-Akt pathway. Brain Res 1367:85–93

    Article  CAS  PubMed  Google Scholar 

  16. Wang H, Wang G, Yu Y, Wang Y (2009) The role of phosphoinositide-3-kinase/Akt pathway in propofol-induced postconditioning against focal cerebral ischemia-reperfusion injury in rats. Brain Res 1297:177–184

    Article  CAS  PubMed  Google Scholar 

  17. Grewal S, York R, Stork P (1999) Extracellular-signal-regulated kinase signaling in neurons. Curr Opin Neurobiol 9:544–553

    Article  CAS  PubMed  Google Scholar 

  18. Xing B, Chen H, Zhang M, Zhao D, Jiang R, Liu X, Zhang S (2008) Ischemic post-conditioning protects brain and reduces inflammation in a rat model of focal cerebral ischemia/reperfusion. J Neurochem 105:1737–1745

    Article  CAS  PubMed  Google Scholar 

  19. Gao L, Jiang T, Guo J, Liu Y, Cui G, Gu L, Su L, Zhang Y (2012) Inhibition of autophagy contributes to ischemic postconditioning-induced neuroprotection against focal cerebral ischemia in rats. PLoS ONE 7:e46092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Zhang W, Miao Y, Zhou S, Wang B, Luo Q, Qiu Y (2010) Involvement of glutamate transporter-1 in neuroprotection against global brain ischemia-reperfusion injury induced by postconditioning in rats. Int J Mol Sci 11:4407–4416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zhang W, Mia Y, Zhou S, Jiang J, Luo Q, Qiu Y (2011) Neuroprotective effects of ischemic postconditioning on global brain ischemia in rats through upregulation of hippocampal glutamine synthetase. J Clin Neurosci 18:685–689

    Article  CAS  PubMed  Google Scholar 

  22. Esposito E, Hayakawa K, Maki T, Arai K, Eng H (2015) Effects of postconditioning on neurogenesis and angiogenesis during the recovery phase after focal cerebral ischemia. Stroke 46:2691–2694

    Article  PubMed  PubMed Central  Google Scholar 

  23. Nemethova M, Danielisova V, Gottlieb M, Kravcukova P, Burda J (2010) Ischemic postconditioning in the rat hippocampus: mapping of proteins involved in reversal of delayed neuronal death. Arch Ital Biol 148:23–32

    CAS  PubMed  Google Scholar 

  24. Peng B, Guo Q, He Z, Ye Z, Yuan Y, Wang N, Zhou J (2012) Remote ischemic postconditioning protects the brain from global cerebral ischemia/reperfusion injury by up-regulating endothelial nitric oxide synthase through the PI3K/Akt pathway. Brain Res 1445:92–102

    Article  CAS  PubMed  Google Scholar 

  25. Ma XD, Song JN, Zhang M, An JY, Zhao YL, Zhang B (2014) Advances in research of the neuroprotective mechanisms of cerebral ischemic postconditioning. Int J Neurosci 125:161–169

    Article  CAS  PubMed  Google Scholar 

  26. Zhao H (2009) Ischemic postconditioning as a novel avenue to protect against brain injury after stroke. J Cereb Blood Flow Metab 29:873–885

    Article  CAS  PubMed  Google Scholar 

  27. Rybnikova E, Vorobyev M, Pivina S, Samoilov M (2012) Postconditioning by mild hypoxic exposures reduces rat brain injury caused by severe hypoxia. Neurosci Lett 513:100–105

    Article  CAS  PubMed  Google Scholar 

  28. Vetrovoy O, Tulkova E, Sarieva K, Kotryahova E, Zenko M, Rybnikova E (2017) Neuroprotective effect of hypobaric hypoxic postconditioning is accompanied by dna protection and lipid peroxidation changes in rat hippocampus. Neurosci Lett 639:49–52

    Article  CAS  PubMed  Google Scholar 

  29. Vetrovoy O, Rybnikova E, Glushchenko T, Samoilov M (2015) Effects of hypoxic postconditioning on the expression of antiapoptotic protein Bcl-2 and neurotrophin BDNF in hippocampal field CA1 in rats subjected to severe hypoxia. Neurosci Behav Physiol 45:367–370

    Article  CAS  Google Scholar 

  30. Vetrovoy O, Rybnikova E, Glushchenko T, Baranova K, Samoilov M (2014) Mild Hypobaric Hypoxic postconditioning increases the expression of hif1α and erythropoietin in the ca1 field of the hippocampus of rats that survive after severe hypoxia. Neurochem J 8:103–108

    Article  CAS  Google Scholar 

  31. Rybnikova E, Baranova K, Gluschenko T, Vetrovoy O, Sidorova M, Portnichenko V (2015) Role of HIF-1 in neuronal mechanisms of adaptation to psychoemotional and hypoxic stress. Int J Physiol Pathophysiol 6:1–11

    Article  Google Scholar 

  32. Dengler V, Galbraith M, Espinosa J (2014) Transcriptional regulation by hypoxia inducible factors. Crit Rev Biochem Mol Biol 49:1–15

    Article  CAS  PubMed  Google Scholar 

  33. Semenza G (2001) Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol Med 7:345–350

    Article  CAS  PubMed  Google Scholar 

  34. Kim J, Tchernyshyov I, Semenza G, Dang C (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 3:177–185

    Article  CAS  PubMed  Google Scholar 

  35. Chavez J, Agani F, Pichiule P, LaManna J (2000) Expression of hypoxia-inducible factor-1alpha in the brain of rats during chronic hypoxia. J Appl Physiol 89:1937–1942

    Article  CAS  PubMed  Google Scholar 

  36. Guo S, Bragina O, Xu Y, Cao Z, Chen H, Zhou B, Morgan M, Lin Y, Jiang B, Liu K, Shi H (2008) Glucose up-regulates HIF-1 alpha expression in primary cortical neurons in response to hypoxia through maintaining cellular redox status. J Neurochem 105:1849–1860

    Article  CAS  PubMed  Google Scholar 

  37. Lukyanova L, Kirova Y (2015) Mitochondria-controlled signaling mechanisms of brain protection in hypoxia. Front Neurosci. https://doi.org/10.3389/fnins.2015.00320

    Article  PubMed  PubMed Central  Google Scholar 

  38. Sheldon R, Lee C, Jiang X, Knox R, Ferriero D (2014) Hypoxic preconditioning protection is eliminated in HIF-1α knockout mice subjected to neonatal hypoxia-ischemia. Pediatr Res 76:46–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Giaccia A, Siim B, Johnson R (2003) HIF-1 as a target for drug development. Nat Rev Drug Discov 10:803–811

    Article  CAS  Google Scholar 

  40. Kilkenny C, Browne W, Cuthill I, Emerson M, Altman D (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8:e1000412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Rybnikova E, Sitnik N, Gluschenko T, Tjulkova E, Samoilov M (2006) The preconditioning modified neuronal expression of apoptosis-related proteins of Bcl-2 superfamily following severe hypobaric hypoxia in rats. Brain Res 1089:195–202

    Article  CAS  PubMed  Google Scholar 

  42. Van Essen H, Verdaasdonk M, Elshof S, de Weger R, van Diest P (2010) Alcohol based tissue fixation as an alternative for formaldehyde: influence on immunohistochemistry. J Clin Pathol 63:1090–1094

    Article  PubMed  Google Scholar 

  43. Boulton A, Baker G (1986) General neurochemical techniques. In: Boulton AA, Baker GB (eds) Neuromethods. Humana Press, Clifton, pp 19–67

    Google Scholar 

  44. Akerboom T, Sies H (1981) Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Methods Enzymol 77:373–381

    Article  CAS  PubMed  Google Scholar 

  45. Kumar R, Bukowski M, Wider J, Reynolds C, Calo L, Lepore B, Tousignant R, Jones M, Przyklenk K, Sanderson T (2016) Mitochondrial dynamics following global cerebral ischemia. Mol Cell Neurosci 76:68–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Mozaffarian D, Benjamin E, Go A, Arnett D, Blaha M, Cushman M, Das S, de Ferranti S, Després J, Fullerton H, Howard V, Huffman M, Isasi C, Jiménez M, Judd S, Kissela B, Lichtman J, Lisabeth L, Liu S, Mackey R, Magid D, McGuire D, Mohler E, Moy C, Muntner P, Mussolino M, Nasir K, Neumar R, Nichol G, Palaniappan L, Pandey D, Reeves M, Rodriguez C, Rosamond W, Sorlie P, Stein J, Towfighi A, Turan T, Virani S, Woo D, Yeh R, Turner M (2016) Heart disease and stroke statistics-2016 update: a report from the American heart association. American heart association statistics committee. Stroke statistics subcommittee. Circulation 133:e38–e360

    PubMed  Google Scholar 

  47. Zhao H, Ren C, Chen X, Shen J (2012) From rapid to delayed and remote postconditioning: the evolving concept of ischemic postconditioning in brain ischemia. Curr Drug Tarets 13:173–187

    Article  CAS  Google Scholar 

  48. Zhou C, Tu J, Zhang Q, Lua D, Zhua Y, Zhanga W, Yanga F, Brannb DW, Wang R (2011) Delayed ischemic postconditioning protects hippocampal CA1 neurons by preserving mitochondrial integrity via Akt/GSK3beta signaling. Neurochem Int 59:749–758

    Article  CAS  PubMed  Google Scholar 

  49. Ren C, Yan Z, Wei D, Gao X, Chen X, Zhao H (2009) Limb remote ischemic postconditioning protects against focal ischemia in rats. Brain Res 1288:88–94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zhan L, Li D, Liang D, Wu B, Zhu P, Wang Y, Sun W, Xu E (2012) Activation of Akt/FoxO and inactivation of MEK/ERK pathways contribute to induction of neuroprotection against transient global cerebral ischemia by delayed hypoxic postconditioning in adult rats. Neuropharmacology 63:873e88

    Article  CAS  Google Scholar 

  51. Zhu P, Zhan L, Zhu T, Liang D, Hu J, Sun W, Hou Q, Zhou H, Wu B, Wang Y, Xu E (2013) The roles of p38 MAPK/MSK1 signaling pathway in the neuroprotection of hypoxic postconditioning against transient global cerebral ischemia in adult rats. Mol Neurobiol 49:1338–1349

    Article  CAS  PubMed  Google Scholar 

  52. Zhu T, Zhan L, Liang D, Hu J, Lu Z, Zhu X, Sun W, Liu L, Xu E (2014) Hypoxia-inducible factor 1a mediates neuroprotection of hypoxic postconditioning against global cerebral ischemia. J Neuropathol Exp Neurol 73:975–986

    Article  CAS  PubMed  Google Scholar 

  53. Vetrovoy O, Rybnikova E, Samoilov M (2017) Cerebral mechanisms of hypoxic/ischemic postconditioning. Biochemistry (Mosc) 82:392–400

    Article  CAS  Google Scholar 

  54. Rybnikova E, Gluschenko T, Galeeva A, Tulkova E, Nalivaeva N, Makova N, Turner A, Samoilov M (2012) Differential expression of ADAM15 and ADAM17 metalloproteases in the rat brain after severe hypobaric hypoxia and hypoxic preconditioning. Neurosci Res 72:364–373

    Article  CAS  PubMed  Google Scholar 

  55. Semenza G (2000) HIF-1 and human disease: one highly involved factor. Genes Dev 14:1983–1991

    CAS  PubMed  Google Scholar 

  56. Jones N, Bergeron M (2001) Hypoxic preconditioning induces changes in HIF-1 target genes in neonatal rat brain. J Cereb Blood Flow Metab 21:1105–1114

    Article  CAS  PubMed  Google Scholar 

  57. Meijer T, Kaanders J, Span P, Bussink J (2012) Targeting hypoxia, HIF-1, and tumor glucose metabolism to improve radiotherapy efficacy. Clin Cancer Res 18:5585–5594

    Article  CAS  PubMed  Google Scholar 

  58. Ulusu N, Sahilli M, Avci A, Canbolat O, Ozansoy G, Ari N, Bali M, Stefek M, Stolc S, Gajdosik A, Karasu C (2003) Pentose phosphate pathway, glutathione-dependent enzymes and antioxidant defense during oxidative stress in diabetic rodent brain and peripheral organs: effects of stobadine and vitamin E. Neurochem Res 28:815–823

    Article  CAS  PubMed  Google Scholar 

  59. Fernandez-Fernandez S, Almeida A, Bolaños J (2012) Antioxidant and bioenergetic coupling between neurons and astrocytes. Biochem J 443:3–11

    Article  CAS  PubMed  Google Scholar 

  60. Ben-Yoseph O, Boxer P, Ross B (1996) Assessment of the role of the glutathione and pentose phosphate pathways in the protection of primary cerebrocortical cultures from oxidative stress. J Neurochem 66:2329–2337

    Article  CAS  PubMed  Google Scholar 

  61. Cheng Q, Sandalova T, Lindqvist Y, Arnér E (2009) Crystal structure and catalysis of the selenoprotein thioredoxin reductase 1. J Biol Chem 284:3998–4008

    Article  CAS  PubMed  Google Scholar 

  62. Deponte M (2013) Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim Biophys Acta 1830:3217–3266

    Article  CAS  PubMed  Google Scholar 

  63. Dringen R (2000) Metabolism and functions of glutathione in brain. Prog Neurobiol 62:649–671

    Article  CAS  PubMed  Google Scholar 

  64. Nalivaeva N, Turner A (2017) Role of ageing and oxidative stress in regulation of amyloid-degrading enzymes and development of neurodegeneration. Curr Aging Sci 10:32–40

    Article  CAS  PubMed  Google Scholar 

  65. Sun S, Hu F, Wu J, Zhang S (2017) Cannabidiol attenuates OGD/R-induced damage by enhancing mitochondrial bioenergetics and modulating glucose metabolism via pentose-phosphate pathway in hippocampal neurons. Redox Biol 11:577–585

    Article  CAS  PubMed  Google Scholar 

  66. Li M, Zhou Z, Sun M, Cao L, Chen J, Qin Y, Gu J, Han F, Sheng R, Wu J, Ding Y, Qin Z (2017) Reduced nicotinamide adenine dinucleotide phosphate, a pentose phosphate pathway product, might be a novel drug candidate for ischemic stroke. Stroke 47:187–195

    Article  CAS  Google Scholar 

  67. Maiti P, Singh S, Sharma A, Muthuraju S, Banerjee P, Ilavazhagan G (2006) Hypobaric hypoxia induces oxidative stress in rat brain. Neurochem Int 49:709–716

    Article  CAS  PubMed  Google Scholar 

  68. Nita D, Nita V, Spulber S, Moldovan M, Popa D, Zagrean A, Zagrean L (2001) Oxidative damage following cerebral ischemia depends on reperfusion—a biochemical study in rat. J Cell Mol Med 5:163–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Sanderson T, Reynolds C, Kumar R, Przyklenk K, Hüttemann M (2013) Molecular mechanisms of ischemia-reperfusion injury in brain: pivotal role of the mitochondrial membrane potential in reactive oxygen species generation. Mol Neurobiol 47:9–23

    Article  CAS  PubMed  Google Scholar 

  70. Sugawara T, Chan P (2003) Reactive oxygen radicals and pathogenesis of neuronal death after cerebral ischemia. Antioxid Redox Signal 5:597–607

    Article  CAS  PubMed  Google Scholar 

  71. Fisk L, Nalivaeva N, Boyle J, Peers S, Turner A (2007) Effects of hypoxia and oxidative stress on expression of neprilysin in human neuroblastoma cells and rat cortical neurons and astrocytes. Neurochem Res 32:1741–1748

    Article  CAS  PubMed  Google Scholar 

  72. Turner A, Nalivaeva N (2007) New insights into the roles of metalloproteinases in neurodegeneration and neuroprotection. Int Rev Neurobiol 82:113–135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Kang H, Jo A, Kim H, Khang R, Lee J, Kim H, Park C, Choi J, Lee Y, Shin J (2018) PARIS reprograms glucose metabolism by HIF-1α induction in dopaminergic neurodegeneration. Biochem Biophys Res Commun 495:2498–2504

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Scientific research was performed at the Research park of Saint Petersburg State University, Resource Center for Ecological Safety Observatory and Resource Centre for Molecular and Cell Technologies. The work has been supported by Russian Foundation for Basic Research (RFBR) Grants Nos. 16-34-00027 and 16-04-00987 and Russian Program of State Academies GP-14 (Section 65).

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Authors and Affiliations

  1. Laboratory of Regulation of Brain Neuron Functions, Pavlov Institute of Physiology RAS, Russian Academy of Sciences, Makarova emb. 6, Saint-Petersburg, Russian Federation, 199034

    Oleg Vetrovoy, Kseniia Sarieva, Tatjana Gluschenko, Ekaterina Tyulkova & Elena Rybnikova

  2. Department of Biochemistry, Faculty of Biology, Saint-Petersburg State University, Universitetskaya emb. 7-9, Saint-Petersburg, Russian Federation, 199034

    Oleg Vetrovoy, Kseniia Sarieva, Olga Galkina, Natalia Eschenko & Andrey Lyanguzov

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  1. Oleg Vetrovoy
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  2. Kseniia Sarieva
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Contributions

OV was responsible for conducting the study and experimental design, performed experiments and wrote the paper. KS performed the experiments, contributed to experimental design and data analysis. ET and TG contributed to the experiments. AL analyzed the data statistically. OG, NE, and ER contributed to implementation of the study, data analysis and preparation of the paper. All authors read and approved the final manuscript.

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Correspondence to Oleg Vetrovoy.

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The authors declare no conflict of interest.

Ethical Approval

Animal experiments were carried out according to domestic regulations and the European Community Council Directive of 24 November 1986 (86/609/EEC) [40]. Experimental protocols were approved by the local ethical committee.

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Special Issue: In honor of Prof. Anthony J. Turner.

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Vetrovoy, O., Sarieva, K., Galkina, O. et al. Neuroprotective Mechanism of Hypoxic Post-conditioning Involves HIF1-Associated Regulation of the Pentose Phosphate Pathway in Rat Brain. Neurochem Res 44, 1425–1436 (2019). https://doi.org/10.1007/s11064-018-2681-x

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