Preferencje help
Widoczny [Schowaj] Abstrakt
Liczba wyników
2011 | 71 | 2 |
Tytuł artykułu

One- and three-time mild hypoxia modifies expression of mitochondrial thioredoxin-2 in hippocampus of rat

Treść / Zawartość
Warianty tytułu
Języki publikacji
Our previous study demonstrated that preconditioning by 3-times repetitive mild hypoxia significantly augmented expression of mitochondrial thioredoxin-2 (Trx-2) at 3 h after subsequent acute severe hypoxia in rat hippocampus. However, it was unclear whether this augmentation was due to build up of Trx-2 by mild hypoxia before severe hypoxia or by modification of reaction to severe hypoxia itself. To answer on this question we study the expression level during and after preconditioning without subsequent severe hypoxia. Trx-2 expression was studied by immunocytochemistry 3 h and 24 h after first session and 3 h and 24 h after last session of 3-times (spaced at 24 h) mild hypobaric hypoxia (360 Torr, 2h). At 3 h after 1-time hypoxia (first session of 3-time hypoxia) the total number of Trx-2-immunoreactive cells (Nt) was significantly decreased in contrast with control in CA2, CA3 and DG. The number of cells with intensive expression of Trx-2 (Ni) was reduced in CA1 and CA3. At 24 h after the same 1-time hypoxia Nt was lower than in control and at 3 h time-point in all hippocampal areas studied (CA1, CA2, CA3 and DG); Ni was decreased only compared to control in CA1 and CA3. At 3 h after last session of 3-times hypoxia Nt and Ni were significantly down regulated in comparison with control only in CA1. At 24 h after it Nt was significantly decreased compared to control in CA1, CA2 and CA3 (in DG the decrease was not statistically significant) but in all areas was higher than at 24 h after 1-time hypoxia. Dynamics of Nt changes from 3-hours after single to 24-hours after triple moderate hypoxia had the wave phase character. These findings indicate that Trx-2 expression in most areas of hippocampus was decreased to 24 h after 3-time mild hypoxia. Thus the augmentation of Trx-2 expression in hippocampal neurons of preconditioned animals in response to subsequent severe hypoxia is caused obviously not by Trx-2 accumulation during preconditioning sessions but by modification of reaction to severe impact.
Słowa kluczowe
Opis fizyczny
  • Department of Anatomy II, Tampere University Medical School and Department of Pathology, Tampere University Hospital, 33014 Tampere, Finland
  • Laboratory of Regulation of Brain Neuron Functions, Pavlov Institute of Physiology RAS, 199034 St.Petersburg, Russia
  • Laboratory of Regulation of Brain Neuron Functions, Pavlov Institute of Physiology RAS, 199034 St.Petersburg, Russia
  • Laboratory of Regulation of Brain Neuron Functions, Pavlov Institute of Physiology RAS, 199034 St.Petersburg, Russia
  • Department of Anatomy II, Tampere University Medical School and Department of Pathology, Tampere University Hospital, 33014 Tampere, Finland
  • Akamatsu Y, Ohno T, Hirota K, Kagoshima H, Yodoi J, Shigesada K (1997) Redox regulation of the DNA bind­ing activity in transcription factor PEBP2. The roles of two conserved cysteine residues. J Biol Chem 272: 14497-14500.
  • Alanen HI, Williamson RA, Howard MJ, Lappi AK, Jantti HP, Rautio SM, Kellokumpu S, Ruddock LW (2003) Functional characterisation of ERp18, a new endoplasmic reticulum located thioredoxin superfamily member. J Biol Chem 278: 28912-28920. Andoh T, Chock PB, Chiueh CC (2002) The roles of thiore­doxin in protection against oxidative stress-induced apoptosis in SH-SY5Y cells. J Biol Chem 277: 9655-9660.
  • Baines CP, Goto M, Downey JM (1997) Oxygen radicals released during ischemic preconditioning contribute to cardioprotection in the rabbit myocardium. J Mol Cell Cardiol 29: 207-216.
  • Berggren M, Gallegos A, Gasdaska JR, Gasdaska PY, Warneke J, Powis G (1996) Thioredoxin and thioredoxin reductase gene expression in human tumors and cell lines, and the effects of serum stimulation and hypoxia. Anticancer Res 16: 3459-3466. Biaglow JE, Miller RA (2005) The thioredoxin reductase/ thioredoxin system: novel redox targets for cancer thera­py. Cancer Biol Ther 4: 6-13.
  • Cai XH, Zhou YH, Zhang CX, Hu LG, Fan XF, Li CC, Zheng GQ, Gong YS (2010) Chronic intermittent hypoxia exposure induces memory impairment in growing rats. Acta Neurobiol Exp (Wars) 70: 279-287.
  • Chen Y, Cai J, Murphy TJ, Jones DP (2002) Overexpressed human mitochondrial thioredoxin confers resistance to oxidant-induced apoptosis in human osteosarcoma cells. J Biol Chem 277: 33242-33248.
  • Chiueh CC, Andoh T, Chock PB (2005) Induction of thiore­doxin and mitochondrial survival proteins mediates pre- conditioning-induced cardioprotection and neuroprotec­tion. Ann NY Acad Sci 1042: 403-418.
  • Corbett D, Crooks P (1997) Ischemic preconditioning: a long term survival study using behavioural and histological endpoints. Brain Res 760: 129-136.
  • Csiki I, Yanagisawa K, Haruki N, Nadaf S, Morrow JD, Johnson DH, Carbone DP (2006) Thioredoxin-1 modu­lates transcription of cyclooxygenase-2 via hypoxia-in­ducible factor-1alpha in non-small cell lung cancer. Cancer Res 66: 143-150.
  • Cunnea PM, Miranda-Vizuete A, Bertoli G, Simmen T, Damdimopoulos AE, Hermann S, Leinonen S, Huikko MP, Gustafsson JA, Sitia R, Spyrou G (2003) ERdj5, an endoplasmic reticulum (ER)-resident protein containing DnaJ and thioredoxin domains, is expressed in secretory cells or following ER stress. J Biol Chem 278: 1059­1066.
  • Damdimopoulos AE, Miranda-Vizuete A, Pelto-Huikko M, Gustafsson JA, Spyrou G (2002) Human mitochondrial thioredoxin. Involvement in mitochondrial membrane potential and cell death. J Biol Chem 277: 33249-33257.
  • Das DK, Maulik N, Sato M, Ray PS (1999) Reactive oxygen species function as second messenger during ischemic preconditioning of heart. Mol Cell Biochem 196: 59-67.
  • Das KC, Lewis-Molock Y, White CW (1997) Elevation of manganese superoxide dismutase gene expression by thioredoxin. Am J Respir Cell Mol Biol 17: 713-726.
  • Das KC (2001) c-Jun NH2-terminal kinase-mediated redox- dependent degradation of IkappaB: role of thioredoxin in NF-kappaB activation. J Biol Chem 276: 4662-4670.
  • Duszczyk M, Ziembowicz A, Gadamski R, Lazarewicz JW (2006) Behavioral evaluation of ischemic damage to CA1 hippocampal neurons: effects of preconditioning. Acta Neurobiol Exp (Wars) 66: 311-319.
  • Hashimoto S, Matsumoto K, Gon Y, Furuichi S, Maruoka S, Takeshita I, Hirota K, Yodoi J, Horie T (1999) Thioredoxin negatively regulates p38 MAP kinase activation and IL-6 production by tumor necrosis factor-alpha. Biochem Biophys Res Commun 258: 443-447.
  • Hattori I, Takagi Y, Nozaki K, Kondo N, Bai J, Nakamura H, Hashimoto N, Yodoi J (2002) Hypoxia-ischemia induces thioredoxin expression and nitrotyrosine formation in new-born rat brain. Redox Rep 7: 256-259.
  • Hayashi T, Ueno Y, Okamoto T (1993) Oxidoreductive regu­lation of nuclear factor kappa B. Involvement of a cellular reducing catalyst thioredoxin. J Biol Chem 268: 11380­11388.
  • Hirano N, Shibasaki F, Kato H, Sakai R, Tanaka T, Nishida J, Yazaki Y, Takenawa T, Hirai H (1994) Molecular clon­ing and characterization of a cDNA for bovine phospholipase C-alpha: proposal of redesignation of phospholipase C-alpha. Biochem Biophys Res Commun 204: 375-382.
  • Hirota K, Matsui M, Iwata S, Nishiyama A, Mori K, Yodoi J (1997) AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1. Proc Natl Acad Sci USA 94: 3633-3638.
  • Hirota K, Murata M, Sachi Y, Nakamura H, Takeuchi J, Mori K, Yodoi J (1999) Distinct roles of thioredoxin in the cytoplasm and in the nucleus. A two-step mechanism of redox regulation of transcription factor NF-kappaB. J Biol Chem 274: 27891-27897.
  • Hirota K, Matsui M, Murata M, Takashima Y, Cheng FS, Itoh T, Fukuda K, Yodoi J (2000) Nucleoredoxin, glutaredoxin, and thioredoxin differentially regulate NF-kappaB, AP-1, and CREB activation in HEK293 cells. Biochem Biophys Res Commun 274: 177-182.
  • Hirota K, Nakamura H, Masutani H, Yodoi J (2002) Thioredoxin superfamily and thioredoxin-inducing agents. Ann N Y Acad Sci 957: 189-199.
  • Holmgren A (1985) Thioredoxin. Annu Rev Biochem 54: 237-271.
  • Holmgren A (1989) Thioredoxin and glutaredoxin systems. J Biol Chem 264: 13963-13966.
  • Hori K, Katayama M, Sato N, Ishii K, Waga S, Yodoi J (1994) Neuroprotection by glial cells through adult T cell leukemia-derived factor/human thioredoxin (ADF/TRX). Brain Res 652: 304-310.
  • Isowa N, Yoshimura T, Kosaka S, Liu M, Hitomi S, Yodoi J, Wada H (2000) Human thioredoxin attenuates hypoxia- reoxygenation injury of murine endothelial cells in a thi- ol-free condition. J Cell Physiol 182: 33-40.
  • Jiménez A, Oko R, Gustafsson JA, Spyrou G, Pelto-Huikko M, Miranda-Vizuete A (2002a) Cloning, expression and characterization of mouse spermatid specific thioredox- in-1 gene and protein. Mol Hum Reprod 8: 710-718.
  • Jiménez A, Johansson C, Ljung J, Sagemark J, Berndt KD, Ren B, Tibbelin G, Ladenstein R, Kieselbach T, Holmgren A, Gustafsson JA, Miranda-Vizuete A (2002b) Human spermatid-specific thioredoxin-1 (Sptrx-1) is a two-do­main protein with oxidizing activity. FEBS Lett 530: 79-84.
  • Jiménez A, Zu W, Rawe VY, Pelto-Huikko M, Flickinger CJ, Sutovsky P, Gustafsson JA, Oko R, Miranda-Vizuete A (2004) Spermatocyte/spermatid-specific thioredoxin-3, a novel Golgi apparatus-associated thioredoxin, is a spe­cific marker of aberrant spermatogenesis. J Biol Chem 279: 34971-34982.
  • Jiménez A, Pelto-Huikko M, Gustafsson JA, Miranda- Vizuete A (2006) Characterization of human thioredoxin- like-1: potential involvement in the cellular response against glucose deprivation. FEBS Lett 580: 960-967.
  • Kaeffer N, Richard V, Thuillez C (1997) Delayed coronary endothelial protection 24 hours after preconditioning: role of free radicals. Circulation 96: 2311-2316.
  • Kirino T, Tsujita Y, Tamura A (1991) Induced tolerance to ischemia in gerbil hippocampal neurons. J Cereb Blood Flow Metab 11: 299-307.
  • Kitagawa K, Matsumoto M, Tagaya M, Hata R, Ueda H, Niinobe M, Handa N, Fukunaga R, Kimura K, Mikoshiba K, Kamada T (1990) 'Ischemic tolerance' phenomenon found in the brain. Brain Res 528: 21-24.
  • Kondo N, Nakamura H, Masutani H, Yodoi J (2006) Redox regulation of human thioredoxin network. Antioxid Redox Signal 8: 1881-1890.
  • Kreps EM, Verzhbinskaja NA, Chenykaeva EJu, Chirkovskaja EV, Govurina TK (1956) About adaptation of animals to chronic hypoxia (in Russian). Physiol J USSR 42: 149-158.
  • Leak RK, Liou AK, Zigmond MJ (2006) Effect of sublethal 6-hydroxydopamine on the response to subsequent oxidative stress in dopaminergic cells: evidence for precondi­tioning. J Neurochem 99: 1151-1163.
  • Marini M, Frabetti F, Musiani D, Franceschi C (1996) Oxygen radicals induce stress proteins and tolerance to oxidative stress in human lymphocytes. Int J Radiat Biol 70: 337-350.
  • Miranda-Vizuete A, Gustafsson JA, Spyrou G (1998) Molecular cloning and expression of a cDNA encoding a human thioredoxin-like protein. Biochem Biophys Res Commun 243: 284-288.
  • Miranda-Vizuete A, Ljung J, Damdimopoulos AE, Gustafsson JA, Oko R, Pelto-Huikko M, Spyrou G (2001) Characterization of Sptrx, a novel member of the thiore- doxin family specifically expressed in human spermato­zoa. J Biol Chem 276: 31567-31574.
  • Miranda-Vizuete A, Tsang K, Yu Y, Jiménez A, Pelto- Huikko M, Flickinger CJ, Sutovsky P, Oko R (2003) Cloning and developmental analysis of murid spermatid- specific thioredoxin-2 (SPTRX-2), a novel sperm fibrous sheath protein and autoantigen. J Biol Chem 278: 44874­44885.
  • Moon S, Fernando MR, Lou MF (2005) Induction of thiol- transferase and thioredoxin/thioredoxin reductase sys­tems in cultured porcine lenses under oxidative stress. Invest Ophthalmol Vis Sci 46: 3783-3789.
  • Nakamura H, Matsuda M, Furuke K, Kitaoka Y, Iwata S, Toda K, Inamoto T, Yamaoka Y, Ozawa K, Yodoi J (1994) Adult T cell leukemia-derived factor/human thioredoxin protects endothelial F-2 cell injury caused by activated neutrophils or hydrogen peroxide. Immunol Lett 42: 75-80.
  • Nakamura H (2005) Thioredoxin and its related molecules: update 2005. Antioxid Redox Signal 7: 823-828.
  • Nonn L, Williams RR, Erickson RP, Powis G (2003) The absence of mitochondrial thioredoxin 2 causes massive apoptosis, exencephaly, and early embryonic lethality in homozygous mice. Mol Cell Biol 23: 916-922.
  • Patenaude A, Murthy MR, Mirault ME (2005) Emerging roles of thioredoxin cycle enzymes in the central nervous system. Cell Mol Life Sci 62: 1063-1080.
  • Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Second edition Academic Press. Philadelphia.
  • Rauca C, Zerbe R, Jantze H, Krug M (2000) The importance of free hydroxyl radicals to hypoxia preconditioning. Brain Res 868: 147-149.
  • Ravati A, Ahlemeyer B, Becker A, Krieglstein J (2000) Preconditioning-induced neuroprotection is mediated by reactive oxygen species. Brain Res 866: 23-32.
  • Ravati A, Ahlemeyer B, Becker A, Klumpp S, Krieglstein J (2001) Preconditioning-induced neuroprotection is medi­ated by reactive oxygen species and activation of the transcription factor nuclear factor-KB. J Neurochem 78: 909-919.
  • Rudiger HA, Graf R, Clavien PA (2003) Sub-lethal oxida- tive stress triggers the protective effects of ischemic pre­conditioning in the mouse liver. J Hepatol 39: 972-977.
  • Rupp K, Birnbach U, Lundstrom J, Van PN, Soling HD (1994) Effects of CabP2, the rat analog of ERp72, and of CabP1 on the refolding of denatured reduced proteins. Comparison with protein disulfide isomerase. J Biol Chem 269: 2501-2507.
  • Rybnikova EA, Khozhai LI, Tyul'kova EI, Glushchenko TS, Sitnik NA, Pelto-Huikko M, Otellin VA, Samoilov MO (2005a) Expression of early gene proteins, structural changes in brain neurons in hypobaric hypoxia, and the correcting effects of preconditioning. Neurosci Behav Physiol 35: 383-388.
  • Rybnikova E, Vataeva L, Tyulkova E, Gluschenko T, Otellin V, Pelto-Huikko M, Samoilov MO (2005b) Mild hypoxia preconditioning prevents impairment of passive avoid­ance learning and suppression of brain NGFI-A expres­sion induced by severe hypoxia. Behav Brain Res 160: 107-114.
  • Rybnikova E, Sitnik N, Gluschenko T, Tjulkova E, Samoilov MO (2006a) The preconditioning modified neuronal expression of apoptosis-related proteins of Bcl-2 super- family following severe hypobaric hypoxia in rats. Brain Res 1089: 195-202.
  • Rybnikova EA, Mironova VI, Pivina SG, Ordyan NE, Tyulkova EI, Samoilov MO (2006b) Hypoxic precondi­tioning prevents development of post-stress depressions in rats. Dokl Biol Sci 411: 431-433.
  • Rybnikova E, Mironova V, Pivina S, Tulkova E, Ordyan N, Vataeva L, Vershinina E, Abritalin E, Kolchev A, Nalivaeva N, Turner AJ, Samoilov M (2007a) Antidepressant-like effects of mild hypoxia precondition­ing in the learned helplessness model in rats. Neurosci Lett 417: 234-239.
  • Rybnikova E, Mironova V, Pivina S, Tulkova E, Ordyan N, Nalivaeva N, Turner A, Samoilov M (2007b) Involvement of the hypothalamic-pituitary-adrenal axis in the antide- pressant-like effects of mild hypoxic preconditioning in rats. Psychoneuroendocrinology 32: 813-823.
  • Sadek CM, Damdimopoulos AE, Pelto-Huikko M, Gustafsson JA, Spyrou G, Miranda-Vizuete A (2001) Sptrx-2, a fusion protein composed of one thioredoxin and three tandemly repeated NDP-kinase domains is expressed in human testis germ cells. Genes Cells 6: 1077-1090.
  • Sadek CM, Jimenez A, Damdimopoulos AE, Kieselbach T, Nord M, Gustafsson JA, Spyrou G, Davis EC, Oko R, van der Hoorn FA, Miranda-Vizuete A (2003) Characterization of human thioredoxin-like 2. A novel microtubule-bind- ing thioredoxin expressed predominantly in the cilia of lung airway epithelium and spermatid manchette and axoneme. J Biol Chem 278: 13133-13142.
  • Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazono K, Ichijo H (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulat­ing kinase (ASK) 1. EMBO J 17: 2596-2606.
  • Samoilov MO, Rybnikova EA, Tjulkova EI, Spyrou G, Pelto-Huikko M (2002) The mitochondrial antioxidants thioredoxin-2 and Mn-superoxide dismutase are involved in the mechanisms of brain hypoxic tolerance. Dokl Biol Sci 387: 498-500.
  • Samoilov MO, Lazarevich EV, Semenov DG, Mokrushin AA, Tyul'kova EI, Romanovskii DY, Milyakova EA, Dudkin KN (2003) The adaptive effects of hypoxic pre­conditioning of brain neurons. Neurosci Behav Physiol 33: 1-11.
  • Samoilov MO, Sitnik NA, Rybnikova EA, Gluschenko TS, Tjulkova EI (2005) The expression pattern of pro- and antiapoptotic proteins bax and Bcl-2 in rat brain neurons in response to severe hypobaric hypoxia: the correcting effect of hypoxic preconditioning. Dokl Biol Sci 402: 176-178.
  • Sasada T, Iwata S, Sato N, Kitaoka Y, Hirota K, Nakamura K, Nishiyama A, Taniguchi Y, Takabayashi A, Yodoi J (1996) Redox control of resistance to cis-diamminedi- chloroplatinum (II) (CDDP): protective effect of human thioredoxin against CDDP-induced cytotoxicity. J Clin Invest 97: 2268-2276.
  • Semenov DG, Samoilov MO, Lazarewicz JW (2008) Preconditioning reduces hypoxia-evoked alterations in glutamatergic Ca2+ signaling in rat cortex. Acta Neurobiol Exp (Wars) 68: 169-179.
  • Simonova Z, Sterbova K, Brozek G, Komarek V, Sykova E (2003) Postnatal hypobaric hypoxia in rats impairs water maze learning and the morphology of neurones and mac- roglia in cortex and hippocampus. Behav Brain Res 141: 195-205.
  • Sirotinin NN (1939) Life on the highlands and the altitude sickness (in Ukrainian). Kiev.
  • Spyrou G, Enmark E, Miranda-Vizuete A, Gustafsson J (1997) Cloning and expression of a novel mammalian thioredoxin. J Biol Chem 272: 2936-2941.
  • Stroev SA, Tjulkova EI, Gluschenko TS, Rybnikova EA, Samoilov MO, Pelto-Huikko M (2004a) The augmenta­tion of brain thioredoxin-1 expression after severe hypo- baric hypoxia by the preconditioning in rats. Neurosci Lett 370: 224-229.
  • Stroev SA, Gluschenko TS, Tjulkova EI, Spyrou G, Rybnikova EA, Samoilov MO, Pelto-Huikko M (2004b) Preconditioning enhances the expression of mitochon- drial antioxidant thioredoxin-2 in the forebrain of rats exposed to severe hypobaric hypoxia. Journal of Neuroscience Research 78: 563-569.
  • Stroev SA, Gluschenko TS, Tjulkova EI, Rybnikova EA, Samoilov MO, Pelto-Huikko M (2005a) The effect of preconditioning on the Cu, Zn superoxide dismutase expression and enzyme activity in rat brain at the early period after severe hypobaric hypoxia. Neuroscience Research 53: 39-47.
  • Stroev SA, Gluschenko TS, Tjulkova EI, Rybnikova EA, Samoilov MO, Pelto-Huikko M (2005b) Induction of the manganese superoxide dismutase expression after severe hypobaric hypoxia in the hippocampus of preconditioned and non-preconditioned rats (in Russian). Nejrokhimia 22: 292-298.
  • Stroev SA, Tjulkova EI, Tugoy IA, Gluschenko TS, Samoilov MO, Pelto-Huikko M (2007) Effects of preconditioning by mild hypobaric hypoxia on the expression of manga­nese superoxide dismutase in the rat hippocampus. Neurochemical Journal 1: 312-317.
  • Stroev SA, Tyul'kova EI, Glushchenko TS, Tugoi IA, Samoilov MO, Pelto-Huikko M (2009) Thioredoxin-1 expression levels in rat hippocampal neurons in moderate hypobaric hypoxia. Neurosci Behav Physiol 39: 1-5.
  • Stroev SA, Tjulkova EI, Pelto-Huikko MT, Samoilov MO (2011) Three-time mild hypobaric hypoxia decreases the Cu, Zn superoxide dismutase expression in some areas of rat hippocampus (in Russian). Bull Exp Biol Med 151: 273-277.
  • Takagi Y, Horikawa F, Nozaki K, Sugino T, Hashimoto N, Yodoi J (1998a) Expression and distribution of redox regulatory protein, thioredoxin during transient focal brain ischemia in the rat. Neurosci Lett 251: 25-28.
  • Takagi Y, Tokime T, Nozaki K, Gon Y, Kikuchi H, Yodoi J (1998b) Redox control of neuronal damage during brain ischemia after middle cerebral artery occlusion in the rat: immunohistochemical and hybridization studies of thi­oredoxin. J Cereb Blood Flow Metab 18: 206-214.
  • Takagi Y, Mitsui A, Nishiyama A, Nozaki K, Sono H, Gon Y, Hashimoto N, Yodoi J (1999) Overexpression of thi­oredoxin in transgenic mice attenuates focal ischemic brain damage. Proc Natl Acad Sci USA 96: 4131-4136.
  • Tanaka T, Hosoi F, Yamaguchi-Iwai Y, Nakamura H, Masutani H, Ueda S, Nishiyama A, Takeda S, Wada H, Spyrou G, Yodoi J (2002) Thioredoxin-2 (TRX-2) is an essential gene regulating mitochondria-dependent apop- tosis. EMBO J 21: 1695-1703.
  • Taniguchi Y, Taniguchi-Ueda Y, Mori K, Yodoi J (1996) A novel promoter sequence is involved in the oxidative stress-induced expression of the adult T-cell leukemia- derived factor (ADF)/human thioredoxin (Trx) gene. Nucleic Acids Res 24: 2746-2752.
  • Tomimoto H, Akiguchi I, Wakita H, Kimura J, Hori K, Yodoi J (1993) Astroglial expression of ATL-derived fac­tor, a human thioredoxin homologue, in the gerbil brain after transient global ischemia. Brain Res 625: 1-8.
  • Tugoy IA, Stroev SA (2006) Morphix - the program for morphological and densitometrical analysis of digital images (in Russian). Morfologiia 129: 96.
  • Ueda S, Masutani H, Nakamura H, Tanaka T, Ueno M, Yodoi J (2002) Redox control of cell death. Antioxid Redox Signal 4: 405-414.
  • Ueno M, Masutani H, Arai RJ, Yamauchi A, Hirota K, Sakai T, Inamoto T, Yamaoka Y, Yodoi J, Nikaido T (1999) Thioredoxin-dependent redox regulation of p53-mediated p21 activation. J Biol Chem 274: 35809-35815.
  • Vanden Hoek TL, Becker LB, Shao Z, Li C, Schumacker PT (1998) Reactive oxygen species released from mitochon­dria during brief hypoxia induce preconditioning in car- diomyocytes. J Biol Chem 273: 18092-18098.
  • Vataeva LA, Tyul'kova EI, Samoilov MO (2004a) Influence of severe hypoxia on rat emotional behavior: the modify­ing effect of preconditioning. Dokl Biol Sci 395: 109­111.
  • Vataeva LA, Tulkova EI, Samoilov MO (2004b) The effect of preceding mild hypoxia on the alteration of the acqui­sition and retention of passive avoidance behaviour caused by the severe hypobaric hypoxia in rats (in Russian). Zh Vyssh Nervn Dejat 54: 795-801.
  • Vladimirov GE, Galvjalo MJa, Gorjuhina TA, Dmitriev GA, Oppel VV, Raiko ZA (1939) Using the stay at high- mountainous climate for aims of high-altitude pilot train­ing (in Russian). In: Oxygen starvation and struggle against it (Questions of training and diet). Leningrad, p. 43-104.
  • Welsh SJ, Bellamy WT, Briehl MM, Powis G (2002) The redox protein thioredoxin-1 (Trx-1) increases hypoxia- inducible factor 1alpha protein expression: Trx-1 overex­pression results in increased vascular endothelial growth factor production and enhanced tumor angiogenesis. Cancer Res 62: 5089-5095.
  • Welsh SJ, Williams RR, Birmingham A, Newman DJ, Kirkpatrick DL, Powis G (2003) The thioredoxin redox inhibitors 1-methylpropyl 2-imidazolyl disulfide and pleurotin inhibit hypoxia-induced factor 1alpha and vascular endothelial growth factor formation. Mol Cancer Ther 2: 235-243.
  • Wojcik L, Sawicka A, Rivera S, Zalewska T (2009) Neurogenesis in gerbil hippocampus following brain ischemia: focus on the involvement of metalloproteinas- es. Acta Neurobiol Exp (Wars) 69: 52-61.
  • Yamamoto M, Yang G, Hong C, Liu J, Holle E, Yu X, Wagner T, Vatner SF, Sadoshima J (2003) Inhibition of endogenous thioredoxin in the heart increases oxidative stress and car­diac hypertrophy. J Clin Invest 112: 1395-1406.
  • Yang R, Weber DJ, Carrier F (2006) Post-transcriptional regulation of thioredoxin by the stress inducible heterog­enous ribonucleoprotein A18. Nucleic Acids Res 34: 1224-1236.
  • Zhang R, Al-Lamki R, Bai L, Streb JW, Miano JM, Bradley J, Min W (2004) Thioredoxin-2 inhibits mitochondria- located ASK1-mediated apoptosis in a JNK-independent manner. Circ Res 94: 1483-1491.
Rekord w opracowaniu
Typ dokumentu
Identyfikator YADDA
JavaScript jest wyłączony w Twojej przeglądarce internetowej. Włącz go, a następnie odśwież stronę, aby móc w pełni z niej korzystać.