Combination of hyperhomocysteinemia and ischemic tolerance in experimental model of global ischemia in rats

Journal of Physiology and Pharmacology

Volumn 66, Issue 6, 2015, Pages 887-897

  Kovalska, M ^a   Kovalska, L ^a   Tothova, B ^a   Mahmood, Silvia ^a   Adamkov, M ^a   Lehotsky, Jan ^a  

^a Physics and Informatics   (Slovakia)

Author keywords

Brain; Hippocampus; Homocysteine; Ischemia; Ischemic preconditioning; Mitogen activated protein kinases

Indexed keywords

HOMOCYSTEINE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38;

ADULT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL OCCLUSION; BRAIN CORTEX; BRAIN ISCHEMIA; CONTROLLED STUDY; DEGENERATIVE DISEASE; HIPPOCAMPUS; HYPERHOMOCYSTEINEMIA; IMMUNOASSAY; IMMUNOHISTOCHEMISTRY; ISCHEMIC PRECONDITIONING; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; RISK FACTOR; SIGNAL TRANSDUCTION; TUNEL ASSAY; WESTERN BLOTTING; ANIMAL; BLOOD; BRAIN; DISEASE MODEL; METABOLISM; VASCULARIZATION; WISTAR RAT;

ANIMALS; BRAIN; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; HOMOCYSTEINE; HYPERHOMOCYSTEINEMIA; ISCHEMIC PRECONDITIONING; MALE; MITOGEN-ACTIVATED PROTEIN KINASES; RATS, WISTAR;

EID: 84954517025     PISSN: 08675910     EISSN: 18991505     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. Rabaneda LG, Carrasco M, Lopez-Toledano MA, et al. Homocysteine inhibits proliferation of neuronal precursors in the mouse adult brain by impairing the bFGF signaling cascade and reducing Erk1/2-dependent cyclin E expression. FASEB J 2008; 22: 3823-3835.
2. Pavlikova M, Kovalska M, Tatarkova Z, Sivonova-Kmetova M, Kaplan P, Lehotsky J. Response of secretory pathways Ca2+ ATPase gene expression to hyperhomocysteinemia and/or ischemic preconditioning in rat cerebral cortex and hippocampus. Gen Physiol Biophys 2011; 30 (Spec.): S61-S69.
3. Lominadze D, Roberts AM, Tyagi N, Moshal KS, Tyagi SC. Homocysteine causes cerebrovascular leakage in mice Am J Physiol Heart Circ Physiol 2006; 290: H1206-H1213.
4. Sachdev PS. Homocysteine and brain atrophy. Prog Neuropsychopharmacol Biol Psychiatry 2005; 29: 1152-1161.
5. Sharma VK. Homocysteine induced dementia: collecting evideneces for Alzheimer's disease. Int J Pharma Biol Sci 2010; 1: 1-14.
6. Zhuo JM, Wang H, Pratico D. Is hyperhomocysteinemia an Alzheimer's disease (AD) risk factor, an AD marker, or neither? Trends Pharmacol Sci 2011; 32: 562-571.
7. Dorszewska J, Florczak-Wyspianska J, Oczkowska A, Dezor M, Prendecki M, Kozubski W. Homocysteine and asymmetric dimethylarginine concentrations in the plasma of Alzheimer's disease patients with varying degrees of dementia. Adv Alzheimer Dis 2013; 2: 1-6.
8. Streck EL, Matte C, Vieira PS, et al. Reduction of Na+,K+- ATPase activity in hippocampus of rats subjected to chemically-induced hyperhomocysteinemia. Neurochem Res 2002; 27: 1585-1590.
9. Wyse AT, Zugno AI, Streck EL, et al. Inhibition of Na(+), K(+)-ATPase activity in hippocampus of rats subjected to acute administration of homocysteine is prevented by vitamins E and C treatment. Neurochem Res 2002; 27: 1685-1689.
10. Matte C, Mussulini BH, dos Santos TM, et al. Hyperhomocysteinemia reduces glutamate uptake in parietal cortex of rats. Int J Dev Neurosci 2010; 28: 183-187.
11. Poddar R, Paul S. Novel crosstalk between ERK MAPK and p38 MAPK leads to homocysteine-NMDA receptor-mediated neuronal cell death. J Neurochem 2013; 124: 558-570.
12. Lehotsky J, Petras M, Kovalska M, Tothova B, Drgova H, Kaplan P. Mechanisms involved in the ischemic tolerance in brain: effect of the homocysteine. Cell Mol Neurobiol 2015; 35: 7-15.
13. Petras M, Tatarkova Z, Kovalska M, et al. Hyperhomocysteinemia as a risk factor for the neuronal system disorders. J Physiol Pharmacol 2014; 65: 15-23.
14. Hrncic D, Rasic-Markovic A, Macut D, Susic V, Djuric D, Stanojlovic O. Homocysteine thiolactone-induced seizures in adult rats are aggravated by inhibition of inducible nitric oxide synthase. Hum Exp Toxicol 2014; 33: 496-503.
15. Serdarevic N, Begic L, Mulaomerovic-Softic A. The concentration of homocysteine in patients after ischemic brain stroke and vascular dementia. J Health Sci 2011; 1: 4-9.
16. Abushik PA, Niittykoski M, Giniatullina R, et al. The role of NMDA and mGluR5 receptors in calcium mobilization and neurotoxicity of homocysteine in trigeminal and cortical neurons and glial cells. J Neurochem 2014; 129: 264-274.
17. Sakata H, Niizuma K, Yoshioka H, et al. Minocycline-preconditioned neural stem cells enhance neuroprotection after ischemic stroke in rats. J Neurosci 2012; 32: 3462-3473.
18. Liu XQ, Sheng R, Qin ZH. The neuroprotective mechanism of brain ischemic preconditioning. Acta Pharmacol Sin 2009; 30: 1071-1080.
19. Pavlikova M, Tatarkova Z, Sivonova M, Kaplan P, Krizanova O, Lehotsky J. Alterations induced by ischemic preconditioning on secretory pathways Ca2+-ATPase (SPCA) gene expression and oxidative damage after global cerebral ischemia/reperfusion in rats. Cell Mol Neurobiol 2009; 29: 909-916.
20. Paul S, Nairn AC, Wang P, Lombroso PJ. NMDA-mediated activation of the tyrosine phosphatase STEP regulates the duration of ERK signaling. Nature Neurosci 2003; 6: 34-42.
21. Zhao H, Joo S, Xie W, Ji X. Using hormetic strategies to improve ischemic preconditioning and postconditioning against stroke. Int J Physiol Pathophysiol Pharmacol 2013; 5: 61-72.
22. Ataie A, Sabetkasaei M, Haghparast A, Hajizadeh Moghaddam A, Ataie R, Nasiraei Moghaddam Sh. An investigation of the neuroprotective effects of curcumin in a model of homocysteine - induced oxidative stress in the rat's brain. Daru 2010; 18: 128-136.
23. Lehotsky J, Burda J, Danielisova V, Gottlieb M, Kaplan P, Saniova B. Ischemic tolerance: the mechanisms of neuroprotective strategy. Anat Rec (Hoboken) 2009; 292: 2002-2012.
24. Kovalska M, Kovalska L, Pavlikova M, et al. Intracellular signaling MAPK pathway after cerebral ischemia-reperfusion injury. Neurochem Res 2012; 37: 1568-1577.
25. Kovalska M, Kovalska L, Mikuskova K, Adamkov M, Tatarkova Z, Lehotsky J. p-ERK involvement in the neuroprotection exerted by ischemic preconditioning in rat hippocampus subjected to four vessel occlusion. J Physiol Pharmacol 2014; 65: 767-776.
26. Lehotsky J, Racay P, Pavlikova M, et al. Cross-talk of intracellular calcium stores in the response to neuronal ischemia and ischemic tolerance. Gen Physiol Biophys 2009; 28: 104-113.
27. Pignataro G, Scorziello A, Di Renzo G, Annunziato L. Post- ischemic brain damage: effect of ischemic preconditioning and postconditioning and identification of potential candidates for stroke therapy. FEBS J 2009; 276: 46-57.
28. Zhao L, Liu X, Liang J, et al. Phosphorylation of p38 MAPK mediates hypoxic preconditioning-induced neuroprotection against cerebral ischemic injury via mitochondria translocation of Bcl-xL in mice. Brain Res 2013; 1503: 78-88.
29. Ding ZM, Wu B, Zhang WQ, et al. Neuroprotective effects of ischemic preconditioning and postconditioning on global brain ischemia in rats through the same effect on inhibition of apoptosis. Int J Mol Sci 2012; 13: 6089-6101.
30. Iadecola C, Anrather J. Stroke research at a crossroad: asking the brain for directions. Nature Neurosci 2011; 14: 1363-1368.
31. Gidday JM. Cerebral preconditioning and ischaemic tolerance. Nat Rev Neurosci 2006; 7: 437-448.
32. Danielisova V, Burda J, Nemethova M, Gottlieb M, Burda R. An effective combination of two different method of postconditioning. Neurochem Res 2012; 37: 2085-2091.
33. Poddar R, Paul S. Homocysteine-NMDA receptor-mediated activation of extracellular signal-regulated kinase leads to neuronal cell death. J Neurochem 2009; 110: 1095-1106.
34. Zhang QG, Wang RM, Han D, Yang LC, Li J, Brann DW. Preconditioning neuroprotection in global cerebral ischemia involves NMDA receptor-mediated ERK-JNK3 crosstalk. Neurosci Res 2009; 63: 205-212.
35. Cargnello M, Roux PP. Activation and function of MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev 2011; 75: 50-83.
36. Lee CH, Yoo KY, Park OK, et al. Phosphorylated extracellular signal-regulated kinase 1/2 immunoreactivity and its protein levels in the gerbil hippocampus during normal aging. Mol Cells 2010; 29: 373-378.
37. Carletti R, Tacconi S, Bettini E, Ferraguiti F. Stress activated protein kinases, a novel family of mitogen-activated protein kinases are heterogeneously expressed in the adult rat brain and differentially disturbed extracellular-signal-regulated protein kinases. Neuroscience 1995; 69: 1103-1110.
38. Vizzardi E, Bonadei I, Zanini G, et al. Homocysteine and heart failure: an overview. Recent Pat Cardiovasc Drug Discov 2009; 4: 15-21.
39. Menon V, Wang X, Greene T, et al. Homocysteine in chronic kidney disease: effect of low protein diet and repletion with B vitamins. Kidney Int 2005; 67: 1539-1546.
40. Mudd SH, Levy HL, Skovby F. Disorders of transsulfuration. In: The Metabolic and Molecular Basis of Inherited Disease. CR Scriver, AL Beaudet, WS Sly, D Valle (eds). New York, McGraw-Hill, 2001, pp. 1279-1327.
41. Tatarkova Z, Engler I, Calkovska A, et al. Effect of long-term normobaric hypoxia on oxidative stress in mitochondria of the guinea pig brain. Neurochem Res 2011; 36: 1475-1481.
42. Martins PJ, Galdieri LC, Souza FG, et al. Physiological variation in plasma total homocysteineconcentrations in rats. Life Sci 2005; 76: 2621-2629.
43. Colombo JA, Puissant VI. Fluoro Jade Stains early and reactive astroglia in the primate cerebral cortex. J Histochem Cytochem 2002; 50: 1135-1137.
44. Anderson KJ, Fugaccia I, Scheff SW. Fluoro-jade B stains quiescent and reactive astrocytes in the rodent spinal cord. J Neurotrauma 2003; 20: 1223-1231.
45. Kruman II, Culmsee C, Chan SL, et al. Homocysteine elicits a DNA damage response in neurons that promotes apoptosis and hypersensitivity to excitotoxicity. J Neurosci 2000; 20: 6920-6926.
46. Kim SJ, Lee BH, Kim YM, Kim GH, Yoo HW. Congenital MTHFR deficiency causing early-onset cerebral stroke in a case homozygous for MTHFR thermolabile variant. Metab Brain Dis 2013; 28: 519-522.
47. Loureiro SO, Romao L, Alves T, et al. Homocysteine induces cytoskeletal remodeling and production of reactive oxygen species in cultured cortical astrocytes. Brain Res 2010; 1355: 151-164.
48. Volterra A, Meldolesi J. Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 2005; 6: 626-640.
49. Maler JM, Seifert W, Huther G, et al. Homocysteine induces cell death of rat astrocytes in vitro. Neurosci Lett 2003; 347: 85-88.
50. Buffo A, Rolando C, Ceruti S. Astrocytes in the damaged brain: molecular and cellular insights into their reactive response and healing potential. Biochem Pharmacol 2010; 79: 77-89.
51. Lehotsky J, Urban P, Pavlikova M, Tatarkova Z, Kaminska B, Kaplan P. Molecular mechanisms leading to neuroprotection/ischemic tolerance. Effect of preconditioning on the stress reaction of endoplasmic reticulum. Cell Mol Neurobiol 2009; 29: 917-925.
52. Lu Q, Rau TF, Harris V, Johnson M, Poulsen DJ, Black SM. Increased p38 mitogen-activated protein kinase signaling is involved in the oxidative stress associated with oxygen and glucose deprivation in neonatal hippocampal slice cultures. Eur J Neurosci 2011; 34: 1093-1101.
53. Cao Q, Qian M, Wang XF, et al. Negative feedback regulation of Raf/MEK/ERK cascade after sublethal cerebra ischemia in the rat hippocampus. Neurochem Res 2011; 36: 153-162.
54. Liu AJ, Hu YY, Li WB, Xu J, Zhang M. Cerebral ischemic pre-conditioning enhances the binding characteristics and glutamate uptake of glial glutamate transporter-1 in hippocampal CA1 subfield of rats. J Neurochem 2011; 119: 202-209.
55. Lennmyr F, Karlsson S, Gerwins P, Ata KA, Terent A. Activation of mitogen-activated protein kinases in experimental cerebral ischemia. Acta Neurol Scand 2002; 106: 333-340.
56. Zhuang S, Schnellmann RG. A death-promoting role for extracellular signal-regulated kinase. J Pharmacol Exp Ther 2006; 319: 991-997.
57. Alonso M, Medina JH, Pozzo-Miller L. ERK1/2 activation is necessary for BDNF to increase dendritic spine density in hippocampal CA1 pyramidal neurons. Learn Mem 2004; 11: 172-178.
58. Gu Z, Jiang Q, Zhang G. Extracellular signal-regulated kinase 1/2 activation in hippocampus after cerebral ischemia may not interfere with postischemic cell death. Brain Res 2001; 901: 79-84.
59. Yamashita S, Hirata T, Mizukami Y, et al. Repeated preconditioning with hyperbaric oxygen induces neuroprotection against forebrain ischemia via suppression of p38 mitogen activated protein kinase. Brain Res 2009; 1301: 171-179.
60. Thompson JW, Dave KR, Young JI, Perez-Pinzon MA. Ischemic preconditioning alters the epigenetic profile of the brain from ischemic intolerance to ischemic tolerance. Neurotherapeutics 2013; 10: 789-797.
61. Dirnagl U, Becker K, Meisel A. Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol 2009; 8: 398-412.
62. Danielisova V, Gottlieb M, Bonova P, Nemethova M, Burda J. Bradykinin postconditioning ameliorates focal cerebral ischemia in the rat. Neurochem Int 2014; 72: 22-29.
63. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. London, Academic Press, 2006. http://www.scribd.com/doc/22822097/Rat-Brain-Atlas. Acessed 26 June 2012