The role of microglia activation in the development of sepsis-induced long-term cognitive impairment

Brain, Behavior, and Immunity

Volumn 43, Issue , 2015, Pages 54-59

  Michels, Monique ^a   Vieira, Andriele S ^a   Vuolo, Francieli ^a   Zapelini, Hugo Galvane ^a   Mendonça, Bruna ^a   Mina, Francielle ^a   Dominguini, Diogo ^a   Steckert, Amanda ^a   Schuck, Patrícia Fernanda ^a   Quevedo, João ^a,b   Petronilho, Fabrícia ^a,b   Dal Pizzol, Felipe ^a  

^a UNIVERSITY OF SOUTHERN SANTA CATARINA   (Brazil)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

Blood brain barrier; Encephalopathy; Microglia; Minocycline; Sepsis

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; MINOCYCLINE; PROTEIN; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN DISEASE; CELL ACTIVATION; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; ENCEPHALITIS; HIPPOCAMPUS; LATENT PERIOD; MALE; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OXIDATIVE STRESS; RAT; SEPSIS; SEPSIS ASSOCIATED ENCEPHALOPATHY; ANIMAL; AVOIDANCE BEHAVIOR; BLOOD; BRAIN; COGNITION DISORDERS; COMPLICATION; INFLAMMATION; METABOLISM; PHYSIOLOGY; WISTAR RAT;

ANIMALS; AVOIDANCE LEARNING; BRAIN; COGNITION DISORDERS; CYTOKINES; HIPPOCAMPUS; INFLAMMATION; MALE; MICROGLIA; OXIDATIVE STRESS; RATS; RATS, WISTAR; SEPSIS; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 84919438800     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.07.002     Document Type: Article

References (51)

1. Arvin K.L., Han B.H., Du Y., Lin S., Paul S.M., Holtzman D.M. Minocycline markedly protects the neonatal brain against hypoxic-ischemic injury. Ann. Neurol. 2002, 52:54-61.
2. Barichello T., Martins M.R., Reinke A., Feier G., Ritter C., Quevedo J., Dal-Pizzol F. Cognitive impairment in sepsis survivors from cecal ligation and perforation. Crit. Care Med. 2005, 33:221-223.
3. Barichello T., Martins M.R., Reinke A., Feier G., Ritter C., Quevedo J., Dal-Pizzol F. Long-term cognitive impairment in sepsis survivors. Crit. Care Med. 2005, 33:1671.
4. Barichello T., Machado R.A., Constantino L., Valvassori S.S., Réus G.Z., Martins M.R., Petronilho F., Ritter C., Quevedo J., Dal-Pizzol F. Antioxidant treatment prevented late memory impairment in an animal model of sepsis. Crit. Care. Med. 2007, 35:2186-2190.
5. Belayev L., Busto R., Zhao W., Ginsberg M.D. Quantitative evaluation of blood-brain barrier permeability following middle cerebral artery occlusion in rats. Brain Res. 1996, 739:88-96.
6. Biff D., Petronilho F., Constantino L., Vuolo F., Zamora-Berridi G.J., Dall'Igna D.M., Comim C.M., Quevedo J., Kapczinski F., Dal-Pizzol F. Correlation of acute phase inflammatory and oxidative markers with long-term cognitive impairment in sepsis survivors rats. Shock 2013, 40(1):45-48.
7. Bozza F.A., D'Avila J.C., Ritter C., Sonneville R., Sharshar T., Dal-Pizzol F. Bioenergetics, mitochondrial dysfunction, and oxidative stress in the pathophysiology of septic encephalopathy. Shock 2013, 39:10-16.
8. Cassol O.J., Comim C.M., Silva B.R., Hermani F.V., Constantino L.S., Felisberto F., Petronilho F., Hallak J.E., De Martinis B.S., Zuardi A.W., Crippa J.A., Quevedo J., Dal-Pizzol F. Treatment with cannabidiol reverses oxidative stress parameters, cognitive impairment and mortality in rats submitted to sepsis by cecal ligation and puncture. Brain Res. 2010, 12:128-138.
9. Cassol O.J., Rezin G.T., Petronilho F.C., Scaini G., Gonçalves C.L., Ferreira G.K., Roesler R., Schwartsmann G., Dal-Pizzol F., Streck E.L. Effects of N-acetylcysteine/deferoxamine, taurine and RC-3095 on respiratory chain complexes and creatine kinase activities in rat brain after sepsis. Neurochem. Res. 2010, 35(4):515-521.
10. Comim C.M., Vilela M.C., Constantino L.S., Petronilho F., Vuolo F., Lacerda-Queiroz N., Rodrigues D.H., da Rocha J.L., Teixeira A.L., Quevedo J., Dal-Pizzol F. Traffic of leukocytes and cytokine up-regulation in the central nervous system in sepsis. Intensive Care Med. 2011, 37:711-718.
11. Cornelius C., Crupi R., Calabrese V., Graziano A., Milone P., Pennisi G., Radak Z., Calabrese E.J., Cuzzocrea S. Traumatic brain injury: oxidative stress and neuroprotection. Antioxid. Redox Signal. 2013, 19:836-853.
12. Dal-Pizzol F., Rojas H.A., dos Santos E.M., Vuolo F., Constantino L., Feier G., Pasquali M., Comim C.M., Petronilho F., Gelain D.P., Quevedo J., Moreira J.C., Ritter C. Matrix metalloproteinase-2 and metalloproteinase-9 activities are associated with blood-brain barrier dysfunction in an animal model of severe sepsis. Mol. Neurobiol. 2013, 48(1):62-70.
13. Dal-Pizzol F., Tomasi C.D., Ritter C. Septic encephalopathy - does inflammation drive the brain crazy?. Rev. Bras. Psiquiatr. 2014, 10.1590/1516-4446-2013-1233.
14. Dehmer T., Lindenau J., Haid S., Dichgans J., Schulz J.B. Deficiency of inducible nitric oxide synthase protects against MPTP toxicity in vivo. J. Neurochem. 2000, 74:2213-2216.
15. Esterbauer H., Cheeseman K.H. Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. Methods Enzymol. 1990, 186:407-421.
16. Fagan S.C., Cronic L.E., Hess D.C. Minocycline development for acute ischemic stroke. Transl. Stroke Res. 2011, 2:202-208.
17. Fink M.P., Heard S.O. Laboratory models of sepsis and septic shock. J. Surg. Res. 1990, 49:186-196.
18. Garrido-Mesa N., Zarzuelo A., Gálvez J. Minocycline: far beyond an antibiotic. Br. J. Pharmacol. 2013, 169:337-352.
19. Gofton T.E., Young G.B. Sepsis-associated encephalopathy. Nat. Rev. Neurosci. 2010, 8:557-566.
20. Gunther M.L., Morandi A., Krauskopf E., Pandharipande P., Girard T.D., Jackson J.C., Thompson J., Shintani A.K., Geevarghese S., Miller R.R., Canonico A., Merkle K., Cannistraci C.J., Rogers B.P., Gatenby J.C., Heckers S., Gore J.C., Hopkins R.O., Ely E.W. The association between brain volumes, delirium duration, and cognitive outcomes in intensive care unit survivors. Crit. Care Med. 2012, 40:2022-2032.
21. Henry C.J., Huang Y., Wynne A.M., Godbout J.P. Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both pro-inflammatory IL-1beta and anti-inflammatory IL-10 cytokines. Brain Behav. Immun. 2009, 23:309-317.
22. Hernandes M.S., D'Avila J.C., Trevelin S.C., Reis P.A., Kinjo E.R., Lopes L.R., Castro-Faria-Neto H.C., Cunha F.Q., Britto L.R., Bozza F.A. The role of Nox2-derived ROS in the development of cognitive impairment after sepsis. J. Neuroinflamm. 2014, 11:36.
23. Jamin N., Junier M.P., Granned T.G., Cadussaeu J. Two temporal stages of oligodendroglial response to excitotoxic lesion in the gray matter of the adult rat brain. Exp. Neurol. 2001, 172:17-28.
24. Jeremias I.C., Scaini G., Constantino L., Vuolo F., Ferreira A.K., Scherer E.B., Kolling J., da Silva Dornelles A., de Souza Wyse A.T., Bogo M.R., Dal-Pizzol F., Streck E.L. The decrease on Na(+), K(+)-ATPase activity in the cortex, but not in hippocampus, is reverted by antioxidants in an animal model of sepsis. Mol Neurobiol. 2012, 46(2):467-474.
25. Kotowicz K., Dixon G.L., Klein N.J., Peters M.J., Callard R.E. Biological function of CD40 on human endothelial cells: costimulation with CD40 ligand and interleukin-4 selectively induces expression of vascular cell adhesion molecule-1 and P-selectin resulting in preferential adhesion of lymphocytes. Immunology 2000, 100(4):441-448.
26. Lam T.I., Bingham D., Chang T.J., Lee C.C., Shi J., Wang D., Massa S., Swanson R.A., Liu J. Beneficial effects of minocycline and botulinum toxin-induced constraint physical therapy following experimental traumatic brain injury. Neurorehabil. Neural Repair 2013, 27(9):889-899.
27. Levine R.L., Garland D., Oliver C.N. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 1990, 186:464-478.
28. Michels M., Danielski L.G., Dal-Pizzol F., Petronilho F. Neuroinflammation: microglial Activation during sepsis. Curr. Neurovasc. Res. 2014, 10.2174/1567202611666140520122744.
29. Mina F., Comim C.M., Dominguini D., Cassol-Jr O.J., Dall'Igna D.M., Ferreira G.K., Silva M.C., Galant L.S., Streck E.L., Quevedo J., Dal-Pizzol F. Il1-β involvement in cognitive impairment after sepsis. Mol. Neurobiol. 2014, 49:1069-1076.
30. Miyaoka T., Yasukawa R., Yasuda H., Hayashida M., Inagaki T., Horiguchi J. Possible antipsychotic effects of minocycline in patients with schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 2007, 31(1):304-307.
31. Petronilho F., Périco S.R., Vuolo F., Mina F., Constantino L., Comim C.M., Quevedo J., Souza D.O., Dal-Pizzol F. Protective effects of guanosine against sepsis-induced damage in rat brain and cognitive impairment. Brain Behav. Immun. 2012, 26(6):904-910.
32. Roesler R., Vianna M.R., de-Paris F., Quevedo J. Memory-enhancing treatments do not reverse the impairment of inhibitory avoidance retention induced by NMDA receptor blockade. Neurobiol. Learn. Mem. 1999, 72:252-258.
33. Sanchez Mejia R.O., Ona V.O., Li M., Friedlander R.M. Minocycline reduces traumatic brain injury mediated caspase-1 activation, tissue damage, and neurological dysfunction. Neurosurgery 2001, 48:1393-1401.
34. Schmitz T., Krabbe G., Weikert G., Scheuer T., Matheus F., Wang Y., Mueller S., Kettenmann H., Matyash V., Bührer C., Endesfelder S. Minocycline protects the immature white matter against hyperoxia. Exp. Neurol. 2014, 254:153-165.
35. Schwalm M.T., Pasquali M., Miguel S.P., Dos Santos J.P., Vuolo F., Comim C.M., Petronilho F., Quevedo J., Gelain D.P., Moreira J.C., Ritter C., Dal-Pizzol F. Acute brain inflammation and oxidative damage are related to long-term cognitive deficits and markers of neurodegeneration in sepsis-survivor rats. Mol. Neurobiol. 2014, 49(1):380-385.
36. Shan S., Qi-Liang M.Y., Hong C., Tingting L., Mei H., Haili P., Yan-Qing W., Zhi-Qi Z., Yu-Qiu Z. Is functional state of spinal microglia involved in the anti-allodynic and anti-hyperalgesic effects of electroacupuncture in rat model of monoarthritis?. Neurobiol. Dis. 2007, 26(3):558-568.
37. Steckert A.V., Comim C.M., Mina F., Mendonça B.P., Dominguini D., Ferreira G.K., Carvalho-Silva M., Vieira J.S., Streck E.L., Quevedo J., Dal-Pizzol F. Late brain alterations in sepsis-survivor rats. Synapse 2013, 67(11):786-793.
38. Tuon L., Comim C.M., Petronilho F., Barichello T., Izquierdo I., Quevedo J., Dal-Pizzol F. Time-dependent behavioral recovery after sepsis in rats. Intensive Care Med. 2008, 34:1724-1731.
39. Vianna M.R., Alonso M., Viola H., Quevedo J., de Paris F., Furman M., de Stein M.L., Medina J.H., Izquierdo I. Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat. Learn. Mem. 2000, 14(5):333-340.
40. Wang A.L., Yu A.C., Lau L.T., Lee C., Wu L.M., Zhu X., Tso M.O. Minocycline inhibits LPS-induced retinal microglia activation. Neurochem. Int. 2005, 47(1-2):152-158.
41. Wang C.X., Yang T., Schuaib A. Effects of minocycline alone and in combination with mild hypothermia in embolic stroke. Brain Res. 2003, 963:327-329.
42. Widmann C.N., Heneka M.T. Long-term cerebral consequences of sepsis. Lancet Neurol. 2014, 13:630-636.
43. Williamson L.L., Sholar P.W., Mistry R.S., Smith S.H., Bilbo S.D. Microglia and memory: modulation by early-life infection. J. Neurosci. 2011, 26:15511-15521.
44. Whiteman M., Halliwell B. Prevention of peroxynitrite dependent tyrosine nitration and inactivation of alpha1-antiproteinase by antibiotics. Free Radic. Res. 1997, 26:49-56.
45. Xu L., Fagan S.C., Waller J.L., Edwards D., Borlongan C.V., Zheng J., Hill W.D., Feuerstein G., Hess D.C. Low dose intravenous minocycline is neuroprotective after middle cerebral artery occlusion-reperfusion in rats. BMC Neurol. 2004, 26:4-7.
46. Yoon S.Y., Patel D., Dougherty P.M. Minocycline blocks lipopolysaccharide induced hyperalgesia by suppression of microglia but not astrocytes. Neuroscience 2012, 221:214-224.
47. Yrjänheikki J., Keinänen R., Pellikka M., Hokfelt T., Koistinaho J. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:15769-15774.
48. Yrjanheikki J., Tikka T., Keinanen R., Goldstein G., Chan P.H., Koistinaho J. A tetracycline derivative, minocycline, reduces inflammation and protects against cerebral ischemia with a wide therapeutic window. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:13496-13500.
49. Ywashyna T.J., Ely E.W., Smith D.M., Langa K.M. Long-term cognitive impairment and functional disability among survivors of severe sepsis. JAMA 2010, 304:1787-1794.
50. Zhang W., Narayanan M., Friedlander R.M. Additive neuroprotective effects of minocycline with creatine in a mouse model of ALS. Ann. Neurol. 2003, 53:267-270.
51. Zhu F., Zhang L., Ding Y.Q., Zhao J., Zheng Y. Neonatal intrahippocampal injection of lipopolysaccharide induces deficits in social behavior and prepulse inhibition and microglial activation in rats: implication for a new schizophrenia animal model. Brain Behav. Immun. 2014, 38:166-174.