The role of Nox2-derived ROS in the development of cognitive impairment after sepsis

详细信息    查看全文

• 作者：Marina S Hernandes (1) (6)
  Joana C D’Avila (3)
  Silvia C Trevelin (4)
  Patricia A Reis (3)
  Erika R Kinjo (1)
  Lucia R Lopes (2)
  Hugo C Castro-Faria-Neto (3)
  Fernando Q Cunha (4)
  Luiz RG Britto (1)
  Fernando A Bozza (5) (7)
  
• 关键词：Systemic inflammation ; Brain ; NADPH oxidase ; Oxidative stress ; Encephalopathy
• 刊名：Journal of Neuroinflammation
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：11
• 期：1
• 全文大小：1,078 KB
• 参考文献：1. Ebels EJ: plus-plus">Iatrogenic damage to the central nervous system in malignant systemic disease. / Acta Neuropathol Suppl 1981, plus-plus">7:352-55.
  2. Forbes GB: plus-plus">Neurologic complications of systemic disease. / Postgrad Med 1954,plus-plus">15(2):157-62.
  3. Young RS, Yagel SK, Towfighi J: plus-plus">Systemic and neuropathologic effects of E. coli endotoxin in neonatal dogs. / Pediatr Res 1983,plus-plus">17(5):349-53.
  4. Eidelman LA, Putterman D, Putterman C, Sprung CL: plus-plus">The spectrum of septic encephalopathy. Definitions, etiologies, and mortalities. / JAMA 1996,plus-plus">275(6):470-73.
  5. Iwashyna TJ, Ely EW, Smith DM, Langa KM: plus-plus">Long-term cognitive impairment and functional disability among survivors of severe sepsis. / JAMA 2010,plus-plus">304(16):1787-794.
  6. Adam N, Kandelman S, Mantz J, Chretien F, Sharshar T: plus-plus">Sepsis-induced brain dysfunction. / Expert Rev Anti Infect Ther 2013,plus-plus">11(2):211-21.
  7. Comim CM, Cassol-Jr OJ, Constantino LS, Felisberto F, Petronilho F, Rezin GT, Scaini G, Daufenbach JF, Streck EL, Quevedo J, Dal-Pizzol F: plus-plus">Alterations in inflammatory mediators, oxidative stress parameters and energetic metabolism in the brain of sepsis survivor rats. / Neurochem Res 2011,plus-plus">36(2):304-11.
  8. Gomes RN, Teixeira-Cunha MG, Figueiredo RT, Almeida PE, Alves SC, Bozza PT, Bozza FA, Bozza MT, Zimmerman GA, Castro-Faria-Neto HC: plus-plus">Bacterial clearance in septic mice is modulated by MCP-1/CCL2 and nitric oxide. / Shock 2013,plus-plus">39(1):63-9.
  9. Barichello T, Fortunato JJ, Vitali AM, Feier G, Reinke A, Moreira JC, Quevedo J, Dal-Pizzol F: plus-plus">Oxidative variables in the rat brain after sepsis induced by cecal ligation and perforation. / Crit Care Med 2006,plus-plus">34(3):886-89.
  10. Berg RM, Moller K, Bailey DM: plus-plus">Neuro-oxidative-nitrosative stress in sepsis. / J Cereb Blood Flow Metab 2011,plus-plus">31(7):1532-544.
  11. Ritter C, Andrades M, Frota Junior ML, Bonatto F, Pinho RA, Polydoro M, Klamt F, Pinheiro CT, Menna-Barreto SS, Moreira JC, Dal-Pizzol F: plus-plus">Oxidative parameters and mortality in sepsis induced by cecal ligation and perforation. / Intensive Care Med 2003,plus-plus">29(10):1782-789.
  12. Borrelli E, Roux-Lombard P, Grau GE, Girardin E, Ricou B, Dayer J, Suter PM: plus-plus">Plasma concentrations of cytokines, their soluble receptors, and antioxidant vitamins can predict the development of multiple organ failure in patients at risk. / Crit Care Med 1996,plus-plus">24(3):392-97.
  13. Chuang CC, Shiesh SC, Chi CH, Tu YF, Hor LI, Shieh CC, Chen MF: plus-plus">Serum total antioxidant capacity reflects severity of illness in patients with severe sepsis. / Crit Care 2006,plus-plus">10(1):R36.
  14. Goode HF, Cowley HC, Walker BE, Howdle PD, Webster NR: plus-plus">Decreased antioxidant status and increased lipid peroxidation in patients with septic shock and secondary organ dysfunction. / Crit Care Med 1995,plus-plus">23(4):646-51.
  15. Huet O, Obata R, Aubron C, Spraul-Davit A, Charpentier J, Laplace C, Nguyen-Khoa T, Conti M, Vicaut E, Mira JP, Duranteau J: plus-plus">Plasma-induced endothelial oxidative stress is related to the severity of septic shock. / Crit Care Med 2007,plus-plus">35(3):821-26.
  16. Guerreiro MO, Petronilho F, Andrades M, Constantino L, Mina FG, Moreira JC, Dal-Pizzol F, Ritter C: plus-plus">Plasma superoxide dismutase activity and mortality in septic patients [corrected]. / J Trauma 2010,plus-plus">69(6):E102-E106.
  17. Cowley HC, Bacon PJ, Goode HF, Webster NR, Jones JG, Menon DK: plus-plus">Plasma antioxidant potential in severe sepsis: a comparison of survivors and nonsurvivors. / Crit Care Med 1996,plus-plus">24(7):1179-183.
  18. West AP, Shadel GS, Ghosh S: plus-plus">Mitochondria in innate immune responses. / Nat Rev Immunol 2011,plus-plus">11(6):389-02.
  19. Sena LA, Li S, Jairaman A, Prakriya M, Ezponda T, Hildeman DA, Wang CR, Schumacker PT, Licht JD, Perlman H, Bryce PJ, Chandel NS: plus-plus">Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. / Immunity 2013,plus-plus">38(2):225-36.
  20. Nohl H, Kozlov AV, Gille L, Staniek K: plus-plus">Cell respiration and formation of reactive oxygen species: facts and artefacts. / Biochem Soc Trans 2003,plus-plus">31(Pt 6):1308-311.
  21. Babior BM: plus-plus">NADPH oxidase: an update. / Blood 1999,plus-plus">93(5):1464-476.
  22. Babior BM: plus-plus">The activity of leukocyte NADPH oxidase: regulation by p47PHOX cysteine and serine residues. / Antioxid Redox Signal 2002,plus-plus">4(1):35-8.
  23. Hernandes MSBL: plus-plus">NADPH oxidase and neurodegeneration. / Curr Neuropharmacol 2012,plus-plus">10(4):321-27.
  24. Bedard K, Krause KH: plus-plus">The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. / Physiol Rev 2007,plus-plus">87(1):245-13.
  25. Yoshioka H, Niizuma K, Katsu M, Okami N, Sakata H, Kim GS, Narasimhan P, Chan PH: plus-plus">NADPH oxidase mediates striatal neuronal injury after transient global cerebral ischemia. / J Cereb Blood Flow Metab 2011,plus-plus">31(3):868-80.
  26. Suh SW, Shin BS, Ma H, Van Hoecke M, Brennan AM, Yenari MA, Swanson RA: plus-plus">Glucose and NADPH oxidase drive neuronal superoxide formation in stroke. / Ann Neurol 2008,plus-plus">64(6):654-63.
  27. Sugawara T, Chan PH: plus-plus">Reactive oxygen radicals and pathogenesis of neuronal death after cerebral ischemia. / Antioxid Redox Signal 2003,plus-plus">5(5):597-07.
  28. Brennan AM, Suh SW, Won SJ, Narasimhan P, Kauppinen TM, Lee H, Edling Y, Chan PH, Swanson RA: plus-plus">NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. / Nat Neurosci 2009,plus-plus">12(7):857-63.
  29. Sorce S, Krause KH: plus-plus">NOX enzymes in the central nervous system: from signaling to disease. / Antioxid Redox Signal 2009,plus-plus">11(10):2481-504.
  30. Alves-Filho JC, Freitas A, Souto FO, Spiller F, Paula-Neto H, Silva JS, Gazzinelli RT, Teixeira MM, Ferreira SH, Cunha FQ: plus-plus">Regulation of chemokine receptor by Toll-like receptor 2 is critical to neutrophil migration and resistance to polymicrobial sepsis. / Proc Natl Acad Sci USA 2009,plus-plus">106(10):4018-023.
  31. Simons JM, Hart BA, Ip Vai Ching TR, Van Dijk H, Labadie RP: plus-plus">Metabolic activation of natural phenols into selective oxidative burst agonists by activated human neutrophils. / Free Radic Biol Med 1990,plus-plus">8(3):251-58.
  32. Ghosh A, Kanthasamy A, Joseph J, Anantharam V, Srivastava P, Dranka BP, Kalyanaraman B, Kanthasamy AG: plus-plus">Anti-inflammatory and neuroprotective effects of an orally active apocynin derivative in pre-clinical models of Parkinson's disease. / J Neuroinflammation 2012, plus-plus">9:241.
  33. Stolk J, Hiltermann TJ, Dijkman JH, Verhoeven AJ: plus-plus">Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substituted catechol. / Am J Respir Cell Mol Biol 1994,plus-plus">11(1):95-02.
  34. Lafeber FP, Beukelman CJ, van den Worm E, van Roy JL, Vianen ME, van Roon JA, van Dijk H, Bijlsma JW: plus-plus">Apocynin, a plant-derived, cartilage-saving drug, might be useful in the treatment of rheumatoid arthritis. / Rheumatology (Oxford) 1999,plus-plus">38(11):1088-093.
  35. Boillee S, Cleveland DW: plus-plus">Revisiting oxidative damage in ALS: microglia, Nox, and mutant SOD1. / J Clin Invest 2008,plus-plus">118(2):474-78.
  36. Chen H, Song YS, Chan PH: plus-plus">Inhibition of NADPH oxidase is neuroprotective after ischemia-reperfusion. / J Cereb Blood Flow Metab 2009,plus-plus">29(7):1262-272.
  37. Dussault AA, Pouliot M: plus-plus">Rapid and simple comparison of messenger RNA levels using real-time PCR. / Biol Proced Online 2006, plus-plus">8:1-0.
  38. Uchida K: plus-plus">4-hydroxy-2-nonenal: a product and mediator of oxidative stress. / Prog Lipid Res 2003,plus-plus">42(4):318-43.
  39. Sebollela A, Freitas-Correa L, Oliveira FF, Paula-Lima AC, Saraiva LM, Martins SM, Mota LD, Torres C, Alves-Leon S, de Souza JM, Carraro DM, Brentani H, De Felice FG, Ferreira ST: plus-plus">Amyloid-beta oligomers induce differential gene expression in adult human brain slices. / J Biol Chem 2012,plus-plus">287(10):7436-445.
  40. Hernandes MS, Britto LR, Real CC, Martins DO, Lopes LR: plus-plus">Reactive oxygen species and the structural remodeling of the visual system after ocular enucleation. / Neuroscience 2010,plus-plus">170(4):1249-260.
  41. Reis PA, Comim CM, Hermani F, Silva B, Barichello T, Portella AC, Gomes FC, Sab IM, Frutuoso VS, Oliveira MF, Bozza PT, Bozza FA, Dal-Pizzol F, Zimmerman GA, Quevedo J, Castro-Faria-Neto HC: plus-plus">Cognitive dysfunction is sustained after rescue therapy in experimental cerebral malaria, and is reduced by additive antioxidant therapy. / PLoS Pathog 2010,plus-plus">6(6):e1000963.
  42. Morris RG, Garrud P, Rawlins JN, O'Keefe J: plus-plus">Place navigation impaired in rats with hippocampal lesions. / Nature 1982,plus-plus">297(5868):681-83.
  43. Brown DI, Griendling KK: plus-plus">Nox proteins in signal transduction. / Free Radic Biol Med 2009,plus-plus">47(9):1239-253.
  44. Ransohoff RM, Brown MA: plus-plus">Innate immunity in the central nervous system. / J Clin Invest 2012,plus-plus">122(4):1164-171.
  45. Sharshar T, Annane D, de la Grandmaison GL, Brouland JP, Hopkinson NS, Francoise G: plus-plus">The neuropathology of septic shock. / Brain Pathol 2004,plus-plus">14(1):21-3.
  46. Crouser ED, Julian MW, Blaho DV, Pfeiffer DR: plus-plus">Endotoxin-induced mitochondrial damage correlates with impaired respiratory activity. / Crit Care Med 2002,plus-plus">30(2):276-84.
  47. D'Avila JC, Santiago AP, Amancio RT, Galina A, Oliveira MF, Bozza FA: plus-plus">Sepsis induces brain mitochondrial dysfunction. / Crit Care Med 2008,plus-plus">36(6):1925-932.
  48. Barja G: plus-plus">Mitochondrial oxygen radical generation and leak: sites of production in states 4 and 3, organ specificity, and relation to aging and longevity. / J Bioenerg Biomembr 1999,plus-plus">31(4):347-66.
  49. Barja G, Herrero A: plus-plus">Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. / FASEB J 2000,plus-plus">14(2):312-18.
  50. Sipos I, Tretter L, Adam-Vizi V: plus-plus">Quantitative relationship between inhibition of respiratory complexes and formation of reactive oxygen species in isolated nerve terminals. / J Neurochem 2003,plus-plus">84(1):112-18.
  51. Zhang QG, Laird MD, Han D, Nguyen K, Scott E, Dong Y, Dhandapani KM, Brann DW: plus-plus">Critical role of NADPH oxidase in neuronal oxidative damage and microglia activation following traumatic brain injury. / PLoS One 2012,plus-plus">7(4):e34504.
  52. Surace MJ, Block ML: plus-plus">Targeting microglia-mediated neurotoxicity: the potential of NOX2 inhibitors. / Cell Mol Life Sci 2012,plus-plus">69(14):2409-427.
  53. Qin L, Liu Y, Wang T, Wei SJ, Block ML, Wilson B, Liu B, Hong JS: plus-plus">NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. / J Biol Chem 2004,plus-plus">279(2):1415-421.
  54. Wang T, Qin L, Liu B, Liu Y, Wilson B, Eling TE, Langenbach R, Taniura S, Hong JS: plus-plus">Role of reactive oxygen species in LPS-induced production of prostaglandin E2 in microglia. / J Neurochem 2004,plus-plus">88(4):939-47.
  55. Rodriguez-Pallares J, Parga JA, Munoz A, Rey P, Guerra MJ, Labandeira-Garcia JL: plus-plus">Mechanism of 6-hydroxydopamine neurotoxicity: the role of NADPH oxidase and microglial activation in 6-hydroxydopamine-induced degeneration of dopaminergic neurons. / J Neurochem 2007,plus-plus">103(1):145-56.
  56. Choi SH, Aid S, Kim HW, Jackson SH, Bosetti F: plus-plus">Inhibition of NADPH oxidase promotes alternative and anti-inflammatory microglial activation during neuroinflammation. / J Neurochem 2012,plus-plus">120(2):292-01.
  57. Wang Q, Tompkins KD, Simonyi A, Korthuis RJ, Sun AY, Sun GY: plus-plus">Apocynin protects against global cerebral ischemia-reperfusion-induced oxidative stress and injury in the gerbil hippocampus. / Brain Res 2006,plus-plus">1090(1):182-89.
  58. Jensen MD, Sheng W, Simonyi A, Johnson GS, Sun AY, Sun GY: plus-plus">Involvement of oxidative pathways in cytokine-induced secretory phospholipase A2-IIA in astrocytes. / Neurochem Int 2009,plus-plus">55(6):362-68.
  59. Hsieh HL, Lin CC, Shih RH, Hsiao LD, Yang CM: plus-plus">NADPH oxidase-mediated redox signal contributes to lipoteichoic acid-induced MMP-9 upregulation in brain astrocytes. / J Neuroinflammation 2012, plus-plus">9:110.
  60. Lekstrom-Himes JA, Kuhns DB, Alvord WG, Gallin JI: plus-plus">Inhibition of human neutrophil IL-8 production by hydrogen peroxide and dysregulation in chronic granulomatous disease. / J Immunol 2005,plus-plus">174(1):411-17.
  61. Brown KL, Bylund J, MacDonald KL, Song-Zhao GX, Elliott MR, Falsafi R, Hancock RE, Speert DP: plus-plus">ROS-deficient monocytes have aberrant gene expression that correlates with inflammatory disorders of chronic granulomatous disease. / Clin Immunol 2008,plus-plus">129(1):90-02.
  62. Segal BH, Davidson BA, Hutson AD, Russo TA, Holm BA, Mullan B, Habitzruther M, Holland SM, Knight PR 3rd: plus-plus">Acid aspiration-induced lung inflammation and injury are exacerbated in NADPH oxidase-deficient mice. / Am J Physiol Lung Cell Mol Physiol 2007,plus-plus">292(3):L760-L768.
  63. Schappi M, Deffert C, Fiette L, Gavazzi G, Herrmann F, Belli D, Krause KH: plus-plus">Branched fungal beta-glucan causes hyperinflammation and necrosis in phagocyte NADPH oxidase-deficient mice. / J Pathol 2008,plus-plus">214(4):434-44.
  64. Han W, Li H, Cai J, Gleaves LA, Polosukhin VV, Segal BH, Yull FE, Blackwell TS: plus-plus">NADPH oxidase limits lipopolysaccharide-induced lung inflammation and injury in mice through reduction-oxidation regulation of NF-kappaB activity. / J Immunol 2013,plus-plus">190(9):4786-794.
  65. Barichello T, Machado RA, Constantino L, Valvassori SS, Reus GZ, Martins MR, Petronilho F, Ritter C, Quevedo J, Dal-Pizzol F: plus-plus">Antioxidant treatment prevented late memory impairment in an animal model of sepsis. / Crit Care Med 2007,plus-plus">35(9):2186-190.
  
• 作者单位：Marina S Hernandes (1) (6)
  Joana C D’Avila (3)
  Silvia C Trevelin (4)
  Patricia A Reis (3)
  Erika R Kinjo (1)
  Lucia R Lopes (2)
  Hugo C Castro-Faria-Neto (3)
  Fernando Q Cunha (4)
  Luiz RG Britto (1)
  Fernando A Bozza (5) (7)
  
  1. Department of Physiology and Biophysics, University of S?o Paulo, S?o Paulo, Brazil
  6. Laboratory of Cellular Neurobiology, Institute of Biomedical Sciences, University of S?o Paulo, Av. Professor Lineu Prestes, 1524, ZIP: 05508-900, S?o Paulo, Brazil
  3. Laboratório de Imunofarmacologia, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil
  4. Department of Pharmacology, Faculty of Medicine of Ribeir?o Preto, University of S?o Paulo, Ribeir?o Preto, S?o Paulo, Brazil
  2. Department of Pharmacology, Institute of Biomedical Sciences, University of S?o Paulo, S?o Paulo, Brazil
  5. Instituto de Pesquisa Clínica Evandro Chagas, FIOCRUZ, e Instituto D’Or de Pesquisa e Ensino (IDOR), Rio de Janeiro, Brazil
  7. Intensive Care Unit, Instituto de Pesquisa Clinica Evandro Chagas, Funda??o Oswaldo Cruz, Av. Brasil, 4365, Rio de Janeiro RJ, ZIP: 21040-900, Brazil
  
• ISSN：1742-2094

文摘

Background Sepsis- associated encephalopathy (SAE) is an early and common feature of severe infections. Oxidative stress is one of the mechanisms associated with the pathophysiology of SAE. The goal of this study was to investigate the involvement of NADPH oxidase in neuroinflammation and in the long-term cognitive impairment of sepsis survivors. Methods Sepsis was induced in WT and gp91phox knockout mice (gp91phox-/-) by cecal ligation and puncture (CLP) to induce fecal peritonitis. We measured oxidative stress, Nox2 and Nox4 gene expression and neuroinflammation in the hippocampus at six hours, twenty-four hours and five days post-sepsis. Mice were also treated with apocynin, a NADPH oxidase inhibitor. Behavioral outcomes were evaluated 15 days after sepsis with the inhibitory avoidance test and the Morris water maze in control and apocynin-treated WT mice. Results Acute oxidative damage to the hippocampus was identified by increased 4-HNE expression in parallel with an increase in Nox2 gene expression after sepsis. Pharmacological inhibition of Nox2 with apocynin completely inhibited hippocampal oxidative stress in septic animals. Pharmacologic inhibition or the absence of Nox2 in gp91phox-/- mice prevented glial cell activation, one of the central mechanisms associated with SAE. Finally, treatment with apocynin and inhibition of hippocampal oxidative stress in the acute phase of sepsis prevented the development of long-term cognitive impairment. Conclusions Our results demonstrate that Nox2 is the main source of reactive oxygen species (ROS) involved in the oxidative damage to the hippocampus in SAE and that Nox2-derived ROS are determining factors for cognitive impairments after sepsis. These findings highlight the importance of Nox2-derived ROS as a central mechanism in the development of neuroinflammation associated with SAE.