MOLECULAR MECHANISMS OF DEVELOPMENT OF CEREBRAL TOLERANCE TO ISCHEMIA (REVIEW. PART 2)

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Abstract

In the 2nd part the authors describe in details the main aspects of protective effect of preconditioning of the brain: inhibition of programmed cell death, weakening of phenomenon of excitotoxicity, activation of endogenous antioxidant systems, anti-inflammatory effects, modulation of glial cell function, changes in regional blood flow and vascular reactivity. In addition, data analysis on the impact of preconditioning on brain neurogenesis, the state of the blood-brain barrier, ion homeostasis and metabolism of neurons is presented. Review emphasizes the role of microRNAs in mechanisms of ischemic tolerance of brain. Profound understanding of molecular mechanisms of increased tolerance of brain to ischemic and reperfusion injury requires the implementation of this phenomenon in clinical practice.

 

About the authors

E. V. Shlyakhto

Saint-Petersburg State Medical Pavlov’s University, Saint-Petersburg
Saint-Petersburg, Almazov Federal Heart, Blood and Endocrinology Centre

Author for correspondence.
Email: Shlyakhto@inbox.ru
доктор медицинских наук, профессор, академик РАМН, директор ФГБУ «Федеральный центр сердца, крови и эндокринологии им. В.А. Алмазова» Минздравсоцразвития России, заведу- ющий кафедрой факультетской терапии СПбГМУ им. акад. И.П. Павлова Адрес: 197341, Санкт-Петербург, ул. Аккуратова, д. 2 Тел.: (812) 702-37-00 Russian Federation

E. R. Barantsevich

Saint-Petersburg State Medical Pavlov’s University, Saint-Petersburg
Saint-Petersburg, Almazov Federal Heart, Blood and Endocrinology Centre

Email: profossrerb@yandex.ru
доктор медицинских наук, профессор, заведующий кафедрой неврологии и ману- альной медицины ФПО СПбГМУ им. акад. И.П. Павлова, заведующий НИО ангионеврологии ФГБУ «Федеральный центр сердца, крови и эндокринологии им. В.А. Алмазова» Минздравсоцразвития России Адрес: 197022, Санкт-Петербург, ул. Л. Толстого, д. 6/8 Тел/факс: (812) 233-45-26 Russian Federation

N. S. Shcherbak

Saint-Petersburg State Medical Pavlov’s University, Saint-Petersburg
Saint-Petersburg, Almazov Federal Heart, Blood and Endocrinology Centre

Email: shcherbakns@yandex.ru
кандидат биологических наук, старший научный сотрудник лаборатории неот- ложной кардиологии Института сердечно-сосудистых заболеваний СПбГМУ им. акад. И.П. Павлова, ведущий научный сотрудник лаборатории нанотехнологий ФГБУ «Федеральный центр сердца, крови и эндокринологии им. В.А. Алмазова» Минздравсоцразвития России Адрес: 197341, Санкт-Петербург, ул. Аккуратова, д. 2 Тел.: (812) 702-37-00 Russian Federation

M. M. Galagudza

Saint-Petersburg State Medical Pavlov’s University, Saint-Petersburg
Saint-Petersburg, Almazov Federal Heart, Blood and Endocrinology Centre

Email: galagoudza@mail.ru
доктор медицинских наук, руководитель Института экспериментальной медицины ФГБУ «Федеральный центр сердца, крови и эндокринологии им. В.А. Алмазова» Минздравсоцразвития России, профессор кафедры патофизиологии СПбГМУ им. акад. И.П. Павлова Адрес: 197022, Санкт-Петербург, ул. Л. Толстого, д. 6/8 Russian Federation

References

  1. Gidday J.M. Cerebral preconditioning and ischaemic tolerance. Nat. Rev. Neurosci. 2006; 7: 437–448.
  2. Miyawaki T., Mashiko T., Ofengeim D. et al. Ischemic preconditioning blocks BAD translocation, Bcl-xL cleavage, and large channel activity in mitochondria of postischemic hippocampal neurons. Proc. Natl. Acad. Sci. USA. 2008; 105 (12): 4892–4897.
  3. Xu Z., Ford G.D., Croslan D.R. et al. Neuroprotection by neuregulin-1 following focal stroke is associated with the attenuation of ischemia-induced pro-inflammatory and stress gene expression. Neurobiol. Dis. 2005; 19 (3): 461–470.
  4. Yanamoto H., Xue J.H., Miyamoto S. et al. Spreading depression induces long-lasting brain protection against infarcted lesion development via BDNF gene-dependent mechanism. Brain Res. 2004; 1019 (1–2): 178–188.
  5. Hazell A.S. Excitotoxic mechanisms in stroke: an update of concepts and treatment strategies. Neurochem. Int. 2007; 50 (7–8): 941–953.
  6. Aarts M.M., Arundine M., Tymianski M. Novel concepts in excitotoxic neurodegeneration after stroke. Expert Rev. Mol. Med. 2003; 5 (30): 1–22.
  7. Shpargel K.B., Jalabi W., Jin Y. et al., Preconditioning paradigms and pathways in the brain. Cleve. Clin. J. Med. 2008; 75 (2): 77–82.
  8. Grabb M.C., Choi D.W. Ischemic tolerance in murine cortical cell culture: critical role for NMDA receptors. J. Neurosci. 1999; 19: 1657–1662.
  9. Ridder D.A., Schwaninger M. NF-kappaB signaling in cerebral ischemia. Neuroscience. 2009; 158 (3): 995–1006.
  10. Dave K.R., Lange-Asschenfeldt C., Raval A.P. et al. Ischemic preconditioning ameliorates excitotoxicity by shifting glutamate/gamma-aminobutyric acid release and biosynthesis. J. Neurosci. Res. 2005; 82 (5): 665–673.
  11. Omata N., Murata T., Takamatsu S. et al. Region-specific induction of hypoxic tolerance by expression of stress proteins and antioxidant enzymes. Neurol. Sci. 2006; 27: 74–77.
  12. Bordet R., Deplanque D., Maboudou P. et al. Increase in endogenous brain superoxide dismutase as a potential mechanism of lipopolysaccharide-induced brain ischemic tolerance. J. Cereb. Blood Flow Metab. 2000; 20: 1190–1196.
  13. Ohtsuki T., Matsumoto M., Kuwabara K. et al. Influence of oxidative stress on induced tolerance to ischemia in gerbil hippocampal neurons. Brain Res. 1992; 599: 246–252.
  14. Puisieux F., Deplanque D., Bulckaen H. et al. Brain ischemic preconditioning is abolished by antioxidant drugs but does not up-regulate superoxide dismutase and glutathione peroxidase. Brain Res. 2004; 1027: 30–37.
  15. Wiggins A.K., Shen P.J., Gundlach A.L. Neuronal-NOS adaptor protein expression after spreading depression: implications for NO production and ischemic tolerance. J. Neurochem. 2003; 87: 1368–1380.
  16. Mori T., Muramatsu H., Matsui T. et al. Possible role of the superoxide anion in the development of neuronal tolerance following ischaemic preconditioning in rats. Neuropathol. Appl. Neurobiol. 2000; 26: 31–40.
  17. Rosenzweig H.L., Lessov N.S., Henshall D.C. et al. Endotoxin preconditioning prevents cellular inflammatory response during ischemic neuroprotection in mice. Stroke. 2004; 35 (11): 2576–2581.
  18. Pera J., Zawadzka M., Kaminska B., Szczudlik A. Influence of chemical and ischemic preconditioning on cytokine expression after focal brain ischemia. J. Neurosci. Res. 2004; 78: 132–140.
  19. Bowen K.K., Naylor M., Vemuganti R. Prevention of inflammation is a mechanism of preconditioning-induced neuroprotection against focal cerebral ischemia. Neurochem. Int. 2006; 49: 127–135.
  20. Zubakov D., Hoheisel J.D., Kluxen F.W. et al. Late ischemic preconditioning of the myocardium alters the expression of genes involved in inflammatory response. FEBS Lett. 2003; 547: 51–55.
  21. Becker K., Kindrick D., McCarron R. et al. Adoptive transfer of myelin basic protein-tolerized splenocytes to naive animals reduces infarct size: a role for lymphocytes in ischemic brain injury? Stroke. 2003; 34: 1809–1815.
  22. Lagos-Quintana M., Rauhut R., Lendeckel W., Tuschl T. Identification of novel genes coding for small expressed RNAs. Science. 2001; 294: 853–858.
  23. Lau N.C., Lim L.P., Weinstein E.G., Bartel D.P. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science. 2001; 294: 858–862.
  24. Lee R.C., Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science. 2001; 294: 862–864.
  25. Sempere L.F., Freemantle S., Pitha-Rowe I. et al. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 2004; 5: 13.
  26. He X., Zhang Q., Liu Y., Pan X. Cloning and identification of novel microRNAs from rat hippocampus. Acta Biochim. Biophys. Sin. (Shanghai). 2007; 39: 708–714.
  27. Mishima T., Mizuguchi Y., Kawahigashi Y. et al. RT-PCR-based analysis of microRNA (miR-1 and -124) expression in mouse CNS. Brain Res. 2007; 1131: 37–43.
  28. Dharap A., Bowen K., Place R., Li L.C., Vemuganti R. Transient focal ischemia induces extensive temporal changes in rat cerebral MicroRNAome. J. Cereb. Blood Flow Metab. 2009; 29: 675–687.
  29. Barone F.C., White R.F., Spera P.A. et al. Ischemic preconditioning and brain tolerance: temporal histological and functional outcomes, protein synthesis requirement, and interleukin-1 receptor antagonist and early gene expression. Stroke. 1998; 29 (9): 1937–1950.
  30. Stenzel-Poore M.P., Stevens S.L., Xiong Z. et al. Effect of ischaemic preconditioning on genomic response to cerebral ischaemia: similarity to neuroprotective strategies in hibernation and hypoxia-tolerant states. Lancet. 2003; 362: 1028–1037.
  31. Lusardi T.A., Farr C.D., Faulkner C.L. et al. Ischemic preconditioning regulates expression of microRNAs and a predicted target, MeCP2, in mouse cortex. J. Cereb. Blood Flow Metab. 2010; 30 (4): 744–756.
  32. Saugstad J.A. MicroRNAs as effectors of brain function with roles in ischemia and injury, neuroprotection, and neurodegeneration. J. Cereb. Blood Flow Metab. 2010; 30 (9): 1564–1576.
  33. Takano T., Oberheim N., Cotrina M.L., Nedergaard M. Astrocytes and ischemic injury. Stroke. 2009; 40: 8–12.
  34. 62. Trendelenburg G., Dirnagl U. Neuroprotective role of astrocytes in cerebral ischemia: focus on ischemic preconditioning. Glia. 2005; 50 (4): 307–320.
  35. Mabuchi T., Kitagawa K., Ohtsuki T. et al. Contribution of microglia/macrophages to expansion of infarction and response of oligodendrocytes after focal cerebral ischemia in rats. Stroke. 2000; 31: 1735–1743.
  36. Lai A.Y., Todd K.G. Microglia in cerebral ischemia: molecular actions and interactions. Can. J. Physiol. Pharmacol. 2006; 84: 49–59.
  37. Lalancette-Hebert M., Gowing G., Simard A. et al. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 2007; 27: 2596–2605.
  38. De Souza Wyse A.T., Streck E.L., Worm P. et al. Preconditioning prevents the inhibition of Na, K-ATPase activity after brain ischemia. Neurochem. Res. 2000; 25: 971–975.
  39. Ohta S., Furuta S., Matsubara I. et al. Calcium movement in ischemia-tolerant hippocampal CA1 neurons after transient forebrain ischemia in gerbils. J. Cereb. Blood Flow Metab. 1996; 16: 915–922.
  40. Shimazaki K., Nakamura T., Nakamura K. et al. Reduced calcium elevation in hippocampal CA1 neurons of ischemia-tolerant gerbils. Neuroreport. 1998; 9: 1875–1878.
  41. Bojarski C., Meloni B.P., Moore S.R., et al. Na+/Ca2+ exchanger subtype (NCX1, NCX2, NCX3) protein expression in the rat hippocampus following 3 min and 8 min durations of global cerebral ischemia. Brain Res. 2008; 1189: 198–202.
  42. Yu S., Zhao T., Guo M. et al. Hypoxic preconditioning up-regulates glucose transport activity and glucose transporter (GLUT1 and GLUT3) gene expression after acute anoxic exposure in the cultured rat hippocampal neurons and astrocytes. Brain Res. 2008; 1211: 22–29.
  43. Li G.C., Vasquez J.A., Gallagher K.P., Lucchesi B.R. Myocardial protection with preconditioning. Circulation. 1990; 82 (2): 609–619.
  44. Schott R. J., Rohmann S., Braun E. R. et al. Ischemic preconditioning reduces infarct size in swine myocardium. Circulat. Res. 1990; 66: 1133–1144.
  45. Matsushima K., Hakim A.M. Transient forebrain ischemia protects against subsequent focal cerebral ischemia without changing cerebral perfusion. Stroke. 1995; 26 (6): 1047–1052.
  46. Chen J., Graham S.H., Zhu R.L., Simon R.P. Stress proteins and tolerance to focal cerebral ischemia. J. Cereb. Blood Flow Metab.1996; 16: 566–577.
  47. Nakamura H., Katsumata T., Nishiyama Y. et al. Effect of ischemic preconditioning on cerebral blood flow after subsequent lethal ischemia in gerbils. Life Sci. 2006; 78: 1713–1719.
  48. Otori T., Greenberg J.H., Welsh F.A. Cortical spreading depression causes a long-lasting decrease in cerebral blood flow and induces tolerance to permanent focal ischemia in rat brain. J. Cereb. Blood Flow Metab. 2003; 23: 43–50.
  49. Hoyte L.C., Papadakis M., Barber P.A., Buchan A.M. Improved regional cerebral blood flow is important for the protection seen in a mouse model of late phase ischemic preconditioning. Brain Res. 2006; 1121: 231–237.
  50. Ara J., Fekete S., Frank M. et al. Hypoxic-preconditioning induces neuroprotection against hypoxia-ischemia in newborn piglet brain. Neurobiol. Dis. 2011; 43 (2): 473–485.
  51. Obrenovitch T.P. Molecular physiology of preconditioning-induced brain tolerance to ischemia. Physiol. Rev. 2008; 88 (1): 211–247.
  52. Atochin D.N., Clark J., Demchenko I.T. et al. Rapid cerebral ischemic preconditioning in mice deficient in endothelial and neuronal nitric oxide synthases. Stroke. 2003; 34 (5): 1299–1303.
  53. Li Y., Lu Z., Keogh C.L. et al. Erythropoietin-induced neurovascular protection, angiogenesis, and cerebral blood flow restoration after focal ischemia in mice. J. Cereb. Blood Flow Metab. 2007; 27: 1043–1054.
  54. Andjelkovic A.V., Stamatovic S.M., Keep R.F. The protective effects of preconditioning on cerebral endothelial cells in vitro. J. Cereb. Blood Flow Metab.2003; 23: 1348–1355.
  55. Vlasov T.D., Korzhevskii D.E., Polyakova E.A. Ischemic preconditioning of the rat brain as a method of endothelial protection from ischemic/repercussion injury. Neurosci. Behav. Physiol. 2005; 35: 567–572.
  56. Sutherland B.A., Papadakis M., Chen R.L., Buchan A.M. Cerebral blood flow alteration in neuroprotection following cerebral ischemia. J. Physiol. 2011 (in press).
  57. Masada T., Hua Y., Xi G. et al. Attenuation of ischemic brain edema and cerebrovascular injury after ischemic preconditioning in the rat. J. Cereb. Blood Flow Metab. 2001; 21: 22–33.
  58. Ikeda T., Xia X.Y., Xia Y.X., Ikenoue T. Hyperthermic preconditioning prevents blood-brain barrier disruption produced by hypoxia-ischemia in newborn rat. Brain Res. 1999; 117: 53–58.
  59. Gesuete R., Orsini F., Zanier E.R. et al. Glial cells drive preconditioning-induced blood-brain barrier protection. Stroke. 2011; 42 (5): 1445–1453.
  60. Naylor M., Bowen K.K., Sailor K.A. et al. Preconditioning-induced ischemic tolerance stimulates growth factor expression and neurogenesis in adult rat hippocampus. Neurochem. Int. 2005; 47: 565–572.
  61. Pourie G., Blaise S., Trabalon M. et al. Mild, non-lesioning transient hypoxia in the newborn rat induces delayed brain neurogenesis associated with improved memory scores. Neuroscience. 2006; 140: 1369–1379.
  62. Li Y., Yu S.P., Mohamad O. et al. Sublethal transient global ischemia stimulates migration of neuroblasts and neurogenesis in mice. Transl. Stroke Res. 2010; 1 (3): 184–196.
  63. Corbett D., Giles T., Evans S. et al. Dynamic changes in CA1 dendritic spines associated with ischemic tolerance. Exp. Neurol. 2006; 202: 133–138.
  64. Blokhin I.O., Galagudza M.M., Vlasov T.D. et al. The dependence of the infarct-limiting effect of ischemic preconditioning local myocardium from ischemia duration of the test. Ross. fiziol. zhurn. im. I.M. Sechenova – Sechenov Russian physiological journal. 2008; 94 (7): 785–789.
  65. Murry C.E., Jennings R.B., Reimer K.A. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986; 74 (5): 1124–1136.
  66. Furuya K., Zhu L., Kawahara N. et al. Differences in infarct evolution between lipopolysaccharide-induced tolerant and nontolerant conditions to focal cerebral ischemia. J. Neurosurg. 2005; 103: 715–723.
  67. Gustavsson M., Anderson M.F., Mallard C., Hagberg H. Hypoxic preconditioning confers long-term reduction of brain injury and improvement of neurological ability in immature rats. Pediatr. Res. 2005; 57(2): 305–309.
  68. Dooley P., Corbett D. Competing processes of cell death and recovery of function following ischemic preconditioning. Brain Res. 1998; 794 (1): 119–126.

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