Peroxynitrite is Involved in the Apoptotic Death of Cultured Cerebellar Granule Neurons Induced by Staurosporine, but not by Potassium Deprivation

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• 作者：Mauricio Olguín-Albuerne ; José Miguel Ramos-Pittol…
• 关键词：Reactive nitrogen species ; Peroxynitrite ; Nitric oxide ; Apoptosis ; Cerebellar granule neurons ; Potassium deprivation ; Staurosporine
• 刊名：Neurochemical Research
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：41
• 期：1-2
• 页码：316-327
• 全文大小：6,759 KB
• 参考文献：1.Moran J, Itoh T, Reddy UR, Chen M, Alnemri ES, Pleasure D (1999) Caspase-3 expression by cerebellar granule neurons is regulated by calcium and cyclic AMP. J Neurochem 73:568–577CrossRef PubMed
  2.Nardi N, Avidan G, Daily D, Zilkha-Falb R, Barzilai A (1997) Biochemical and temporal analysis of events associated with apoptosis induced by lowering the extracellular potassium concentration in mouse cerebellar granule neurons. J Neurochem 68:750–759CrossRef PubMed
  3.D’Mello SR, Galli C, Ciotti T, Calissano P (1993) Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc Natl Acad Sci USA 90:10989–10993CrossRef PubMed PubMedCentral
  4.D’Mello SR, Borodezt K, Soltoff SP (1997) Insulin-like growth factor and potassium depolarization maintain neuronal survival by distinct pathways: possible involvement of PI 3-kinase in IGF-1 signaling. J Neurosci 17:1548–1560PubMed
  5.Nicholls DG, Budd SL (2000) Mitochondria and neuronal survival. Physiol Rev 80:315–360PubMed
  6.Cohen GM (1997) Caspases: the executioners of apoptosis. Biochem J 326(Pt 1):1–16CrossRef PubMed PubMedCentral
  7.Ramiro-Cortes Y, Moran J (2009) Role of oxidative stress and JNK pathway in apoptotic death induced by potassium deprivation and staurosporine in cerebellar granule neurons. Neurochem Int 55:581–592CrossRef PubMed
  8.Ramiro-Cortes Y, Guemez-Gamboa A, Moran J (2011) Reactive oxygen species participate in the p38-mediated apoptosis induced by potassium deprivation and staurosporine in cerebellar granule neurons. Int J Biochem Cell Biol 43:1373–1382CrossRef PubMed
  9.Valencia A, Moran J (2001) Role of oxidative stress in the apoptotic cell death of cultured cerebellar granule neurons. J Neurosci Res 64:284–297CrossRef PubMed
  10.Valencia A, Moran J (2004) Reactive oxygen species induce different cell death mechanisms in cultured neurons. Free Radic Biol Med 36:1112–1125CrossRef PubMed
  11.Olguin-Albuerne M, Dominguez G, Moran J (2014) Effect of staurosporine in the morphology and viability of cerebellar astrocytes: role of reactive oxygen species and NADPH oxidase. Oxid Med Cell Longev 2014:678371CrossRef PubMed PubMedCentral
  12.Zhang Y, Wang H, Li J, Jimenez DA, Levitan ES, Aizenman E, Rosenberg PA (2004) Peroxynitrite-induced neuronal apoptosis is mediated by intracellular zinc release and 12-lipoxygenase activation. J Neurosci 24:10616–10627CrossRef PubMed PubMedCentral
  13.Shacka JJ, Sahawneh MA, Gonzalez JD, Ye YZ, D’Alessandro TL, Estevez AG (2006) Two distinct signaling pathways regulate peroxynitrite-induced apoptosis in PC12 cells. Cell Death Differ 13:1506–1514CrossRef PubMed
  14.Martinez MC, Andriantsitohaina R (2009) Reactive nitrogen species: molecular mechanisms and potential significance in health and disease. Antioxid Redox Signal 11:669–702CrossRef PubMed
  15.Szabo C (1996) Physiological and pathophysiological roles of nitric oxide in the central nervous system. Brain Res Bull 41:131–141CrossRef PubMed
  16.Szabo C (2006) Poly(ADP-ribose) polymerase activation by reactive nitrogen species–relevance for the pathogenesis of inflammation. Nitric Oxide 14:169–179CrossRef PubMed
  17.Beckman JS (1996) Oxidative damage and tyrosine nitration from peroxynitrite. Chem Res Toxicol 9:836–844CrossRef PubMed
  18.Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA (1995) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-d -aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA 92:7162–7166CrossRef PubMed PubMedCentral
  19.Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87:1620–1624CrossRef PubMed PubMedCentral
  20.Chabrier PE, Demerle-Pallardy C, Auguet M (1999) Nitric oxide synthases: targets for therapeutic strategies in neurological diseases. Cell Mol Life Sci 55:1029–1035CrossRef PubMed
  21.Klotz LO, Schieke SM, Sies H, Holbrook NJ (2000) Peroxynitrite activates the phosphoinositide 3-kinase/Akt pathway in human skin primary fibroblasts. Biochem J 352(Pt 1):219–225CrossRef PubMed PubMedCentral
  22.Wang L, Zhu ZA (2014) Nitric oxide show its survival role by NO-PKC pathway through cGMP-dependent or independent on the culture of cerebella granular neurons. Neurosci Lett 583:165–169CrossRef PubMed
  23.Duport S, Garthwaite J (2005) Pathological consequences of inducible nitric oxide synthase expression in hippocampal slice cultures. Neuroscience 135:1155–1166CrossRef PubMed
  24.Erusalimsky JD, Moncada S (2007) Nitric oxide and mitochondrial signaling: from physiology to pathophysiology. Arterioscler Thromb Vasc Biol 27:2524–2531CrossRef PubMed
  25.Li J, Loukili N, Rosenblatt-Velin N, Pacher P, Feihl F, Waeber B, Liaudet L (2013) Peroxynitrite is a key mediator of the cardioprotection afforded by ischemic postconditioning in vivo. PLoS ONE 8:e70331CrossRef PubMed PubMedCentral
  26.Gallo V, Kingsbury A, Balazs R, Jorgensen OS (1987) The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J Neurosci 7:2203–2213PubMed
  27.Caballero-Benitez A, Moran J (2003) Caspase activation pathways induced by staurosporine and low potassium: role of caspase-2. J Neurosci Res 71:383–396CrossRef PubMed
  28.Schulz JB, Weller M, Klockgether T (1996) Potassium deprivation-induced apoptosis of cerebellar granule neurons: a sequential requirement for new mRNA and protein synthesis, ICE-like protease activity, and reactive oxygen species. J Neurosci 16:4696–4706PubMed
  29.Atlante A, Calissano P, Bobba A, Azzariti A, Marra E, Passarella S (2000) Cytochrome c is released from mitochondria in a reactive oxygen species (ROS)-dependent fashion and can operate as a ROS scavenger and as a respiratory substrate in cerebellar neurons undergoing excitotoxic death. J Biol Chem 275:37159–37166CrossRef PubMed
  30.Sanchez-Carbente MR, Castro-Obregon S, Covarrubias L, Narvaez V (2005) Motoneuronal death during spinal cord development is mediated by oxidative stress. Cell Death Differ 12:279–291CrossRef PubMed
  31.Moran J, Patel AJ (1989) Effect of potassium depolarization on phosphate-activated glutaminase activity in primary cultures of cerebellar granule neurons and astroglial cells during development. Brain Res Dev Brain Res 46:97–105CrossRef PubMed
  32.Guemez-Gamboa A, Moran J (2009) NOX2 mediates apoptotic death induced by staurosporine but not by potassium deprivation in cerebellar granule neurons. J Neurosci Res 87:2531–2540CrossRef PubMed
  33.Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84CrossRef PubMed
  34.Jensen MP, Riley DP (2002) Peroxynitrite decomposition activity of iron porphyrin complexes. Inorg Chem 41:4788–4797CrossRef PubMed
  35.Brown GC (2010) Nitric oxide and neuronal death. Nitric Oxide 23:153–165CrossRef PubMed
  36.Fatokun AA, Stone TW, Smith RA (2008) Prolonged exposures of cerebellar granule neurons to S-nitroso-N-acetylpenicillamine (SNAP) induce neuronal damage independently of peroxynitrite. Brain Res 1230:265–272CrossRef PubMed
  37.Estevez AG, Spear N, Thompson JA, Cornwell TL, Radi R, Barbeito L, Beckman JS (1998) Nitric oxide-dependent production of cGMP supports the survival of rat embryonic motor neurons cultured with brain-derived neurotrophic factor. J Neurosci 18:3708–3714PubMed
  38.Bonthius DJ, Bonthius NE, Li S, Karacay B (2008) The protective effect of neuronal nitric oxide synthase (nNOS) against alcohol toxicity depends upon the NO-cGMP-PKG pathway and NF-kappaB. Neurotoxicology 29:1080–1091CrossRef PubMed
  39.Vitecek J, Lojek A, Valacchi G, Kubala L (2012) Arginine-based inhibitors of nitric oxide synthase: therapeutic potential and challenges. Mediators Inflamm 2012:318087CrossRef PubMed PubMedCentral
  40.Coyoy A, Olguin-Albuerne M, Martinez-Briseno P, Moran J (2013) Role of reactive oxygen species and NADPH-oxidase in the development of rat cerebellum. Neurochem Int 62:998–1011CrossRef PubMed
  41.Kawano T, Kunz A, Abe T, Girouard H, Anrather J, Zhou P, Iadecola C (2007) iNOS-derived NO and nox2-derived superoxide confer tolerance to excitotoxic brain injury through peroxynitrite. J Cereb Blood Flow Metab 27:1453–1462CrossRef PubMed
  42.Li CY, Chin TY, Chueh SH (2004) Rat cerebellar granule cells are protected from glutamate-induced excitotoxicity by S-nitrosoglutathione but not glutathione. Am J Physiol Cell Physiol 286:C893–C904CrossRef PubMed
  43.Thiyagarajan M, Kaul CL, Sharma SS (2004) Neuroprotective efficacy and therapeutic time window of peroxynitrite decomposition catalysts in focal cerebral ischemia in rats. Br J Pharmacol 142:899–911CrossRef PubMed PubMedCentral
  44.Lane P, Hao G, Gross SS (2001) S-nitrosylation is emerging as a specific and fundamental posttranslational protein modification: head-to-head comparison with O-phosphorylation. Sci STKE 2001:re1
  45.Patel RP, McAndrew J, Sellak H, White CR, Jo H, Freeman BA, Darley-Usmar VM (1999) Biological aspects of reactive nitrogen species. Biochim Biophys Acta 1411:385–400CrossRef PubMed
  46.Mannick JB (2007) Regulation of apoptosis by protein S-nitrosylation. Amino Acids 32:523–526CrossRef PubMed
  47.Huang Z, Pinto JT, Deng H, Richie JP Jr (2008) Inhibition of caspase-3 activity and activation by protein glutathionylation. Biochem Pharmacol 75:2234–2244CrossRef PubMed PubMedCentral
  48.Mitchell DA, Marletta MA (2005) Thioredoxin catalyzes the S-nitrosation of the caspase-3 active site cysteine. Nat Chem Biol 1:154–158CrossRef PubMed
  49.Bao F, Liu D (2003) Peroxynitrite generated in the rat spinal cord induces apoptotic cell death and activates caspase-3. Neuroscience 116:59–70CrossRef PubMed
  50.Dohi K, Ohtaki H, Inn R, Ikeda Y, Shioda HS, Aruga T (2003) Peroxynitrite and caspase-3 expression after ischemia/reperfusion in mouse cardiac arrest model. Acta Neurochir Suppl 86:87–91PubMed
  51.Lau A, Arundine M, Sun HS, Jones M, Tymianski M (2006) Inhibition of caspase-mediated apoptosis by peroxynitrite in traumatic brain injury. J Neurosci 26:11540–11553CrossRef PubMed
  52.Viner RI, Williams TD, Schoneich C (1999) Peroxynitrite modification of protein thiols: oxidation, nitrosylation, and S-glutathiolation of functionally important cysteine residue(s) in the sarcoplasmic reticulum Ca-ATPase. Biochemistry 38:12408–12415CrossRef PubMed
  53.Adachi T, Weisbrod RM, Pimentel DR, Ying J, Sharov VS, Schoneich C, Cohen RA (2004) S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat Med 10:1200–1207CrossRef PubMed
  54.Ghafourifar P, Schenk U, Klein SD, Richter C (1999) Mitochondrial nitric-oxide synthase stimulation causes cytochrome c release from isolated mitochondria. Evidence for intramitochondrial peroxynitrite formation. J Biol Chem 274:31185–31188CrossRef PubMed
  55.Borutaite V, Morkuniene R, Brown GC (1999) Release of cytochrome c from heart mitochondria is induced by high Ca2+ and peroxynitrite and is responsible for Ca(2+)-induced inhibition of substrate oxidation. Biochim Biophys Acta 1453:41–48CrossRef PubMed
  56.Al-Ani B, Hewett PW, Ahmed S, Cudmore M, Fujisawa T, Ahmad S, Ahmed A (2006) The release of nitric oxide from S-nitrosothiols promotes angiogenesis. PLoS ONE 1:e25CrossRef PubMed PubMedCentral
  57.Virgili M, Monti B, LoRusso A, Bentivogli M, Contestabile A (1999) Developmental effects of in vivo and in vitro inhibition of nitric oxide synthase in neurons. Brain Res 839:164–172CrossRef PubMed
  58.Salykina MA, Sorokina EG, Krasilnikova IA, Reutov VP, Pinelis VG (2013) Effects of selective inhibitors of neuronal and inducible NO-synthase on ATP content and survival of cultured rat cerebellar neurons during hyperstimulation of glutamate receptors. Bull Exp Biol Med 155:40–43CrossRef PubMed
  59.Ciani E, Virgili M, Contestabile A (2002) Akt pathway mediates a cGMP-dependent survival role of nitric oxide in cerebellar granule neurones. J Neurochem 81:218–228CrossRef PubMed
  60.Pantazis NJ, West JR, Dai D (1998) The nitric oxide-cyclic GMP pathway plays an essential role in both promoting cell survival of cerebellar granule cells in culture and protecting the cells against ethanol neurotoxicity. J Neurochem 70:1826–1838CrossRef PubMed
  61.Karacay B, Li G, Pantazis NJ, Bonthius DJ (2007) Stimulation of the cAMP pathway protects cultured cerebellar granule neurons against alcohol-induced cell death by activating the neuronal nitric oxide synthase (nNOS) gene. Brain Res 1143:34–45CrossRef PubMed PubMedCentral
  62.Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH (2001) Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 3:193–197CrossRef PubMed
  63.Riccio A, Alvania RS, Lonze BE, Ramanan N, Kim T, Huang Y, Dawson TM, Snyder SH, Ginty DD (2006) A nitric oxide signaling pathway controls CREB-mediated gene expression in neurons. Mol Cell 21:283–294CrossRef PubMed
  
• 作者单位：Mauricio Olguín-Albuerne (1)
  José Miguel Ramos-Pittol (1)
  Angélica Coyoy (1)
  Carlos Patricio Martínez-Briseño (1)
  Guadalupe Domínguez (1)
  Julio Morán (1)
  
  1. Departamento de Neurociencias, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Apartado Postal 70-253, 04510, Mexico, DF, Mexico
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Biomedicine
  Neurosciences
  Biochemistry
  Neurology
  
• 出版者：Springer Netherlands
• ISSN：1573-6903

文摘

Nitric oxide (NO) regulates numerous physiological process and is the main source of reactive nitrogen species (RNS). NO promotes cell survival, but it also induces apoptotic death having been involved in the pathogenesis of several neurodegenerative diseases. NO and superoxide anion react to form peroxynitrite, which accounts for most of the deleterious effects of NO. The mechanisms by which these molecules regulate the apoptotic process are not well understood. In this study, we evaluated the role of NO and peroxynitrite in the apoptotic death of cultured cerebellar granule neurons (CGN), which are known to experience apoptosis by staurosporine (St) or potassium deprivation (K5). We found that CGN treated with the peroxynitrite catalyst, FeTTPs were completely rescued from St-induced death, but not from K5-induced death. On the other hand, the inhibition of the inducible nitric oxide synthase partially protected cell viability in CGN treated with K5, but not with St, while the inhibitor L-NAME further reduced the cell viability in St, but it did not affect K5. Finally, an inhibitor of the soluble guanylate cyclase (sGC) diminished the cell viability in K5, but not in St. Altogether, these results shows that NO promotes cell survival in K5 through sGC-cGMP and promotes cell death by other mechanisms, while in St NO promotes cell survival independently of cGMP and peroxynitrite results critical for St-induced death. Our results suggest that RNS are differentially handled by CGN during cell death depending on the death-inducing conditions.