Cognitive dysfunction is sustained after rescue therapy in experimental cerebral malaria, and is reduced by additive antioxidant therapy

PLoS Pathogens

Volumn 6, Issue 6, 2010, Pages

  Reis, Patricia A ^a   Comim, Clarissa M ^b   Hermani, Fernanda ^b   Silva, Bruno ^b   Barichello, Tatiana ^b   Portella, Aline C ^c   Gomes, Flavia C A ^c   Sab, Ive M ^a   Frutuoso, Valber S ^a   Oliveira, Marcus F ^c   Bozza, Patricia T ^a   Bozza, Fernando A ^d   Dal Pizzol, Felipe ^b   Zimmerman, Guy A ^e   Quevedo, João ^b   Castro Faria Neto, Hugo C ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b UNIVERSIDADE DO EXTREMO SUL CATARINENSE   (Brazil)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d Funda??o Oswaldo Cruz   (Brazil)

^e UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKADIENE; ANTIOXIDANT; CHLOROQUINE; MALONALDEHYDE; REACTIVE OXYGEN METABOLITE; ANTIMALARIAL AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; BRAIN MALARIA; COGNITIVE DEFECT; CONTROLLED STUDY; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; OXIDATIVE STRESS; PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI; ANIMAL; ANIMAL BEHAVIOR; BAGG ALBINO MOUSE; C57BL MOUSE; DRUG COMBINATION; DRUG EFFECT; ERYTHROCYTE; MALARIA; METABOLISM; PARASITEMIA; PARASITOLOGY; PATHOLOGY; PLASMODIUM YOELII; SURVIVAL RATE;

MUS; PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI CHABAUDI; PLASMODIUM FALCIPARUM; PLASMODIUM YOELII;

ANIMALS; ANTIMALARIALS; ANTIOXIDANTS; BEHAVIOR, ANIMAL; COGNITION DISORDERS; DRUG COMBINATIONS; ERYTHROCYTES; MALARIA, CEREBRAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; OXIDATIVE STRESS; PARASITEMIA; PLASMODIUM BERGHEI; PLASMODIUM YOELII; REACTIVE OXYGEN SPECIES; SURVIVAL RATE;

EID: 77954664054     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000963     Document Type: Article

References (69)

1. Hunt NH, Golenser J, Chan-Ling T, Parekh S, Rae C, et al. (2006) Immunopathogenesis of cerebral malaria. Int J Parasitol 36: 569-582.
2. Golenser J, McQuillan J, Hee L, Mitchell AJ, Hunt NH (2006) Conventional and experimental treatment of cerebral malaria. Int J Parasitol 36: 583-593.
3. van Hensbroek MB, Palmer A, Jaffar S, Schneider G, Kwiatkowski D (1997) Residual neurologic sequelae after childhood cerebral malaria. J Pediatr 131: 125-129.
4. Boivin MJ, Bangirana P, Byarugaba J, Opoka RO, Idro R, et al. (2007) Cognitive impairment after cerebral malaria in children: a prospective study. Pediatrics 119: e360-366.
5. Carter JA, Lees JA, Gona JK, Murira G, Rimba K, et al. (2006) Severe falciparum malaria and acquired childhood language disorder. Dev Med Child Neurol 48: 51-57.
6. Carter JA, Mung'ala-Odera V, Neville BG, Murira G, Mturi N, et al. (2005) Persistent neurocognitive impairments associated with severe falciparum malaria in Kenyan children. J Neurol Neurosurg Psychiatry 76: 476-481.
7. Dugbartey AT, Spellacy FJ, Dugbartey MT (1998) Somatosensory discrimina- tion deficits following pediatric cerebral malaria. Am J Trop Med Hyg 59: 393-396.
8. Holding PA, Stevenson J, Peshu N, Marsh K (1999) Cognitive sequelae of severe malaria with impaired consciousness. Trans R Soc Trop Med Hyg 93: 529-534.
9. Desruisseaux MS, Gulinello M, Smith DN, Lee SC, Tsuji M, et al. (2008) Cognitive dysfunction in mice infected with Plasmodium berghei strain ANKA. J Infect Dis 197: 1621-1627.
10. Schofield L, Grau GE (2005) Immunological processes in malaria pathogenesis. Nat Rev Immunol 5: 722-735.
11. Engwerda C, Belnoue E, Gruner AC, Renia L (2005) Experimental models of cerebral malaria. Curr Top Microbiol Immunol 297: 103-143.
12. de Kossodo S, Grau GE (1993) Profiles of cytokine production in relation with susceptibility to cerebral malaria. J Immunol 151: 4811-4820.
13. Li C, Seixas E, Langhorne J (2001) Rodent malarias: the mouse as a model for understanding immune responses and pathology induced by the erythrocytic stages of the parasite. Med Microbiol Immunol 189: 115-126.
14. Becker K, Tilley L, Vennerstrom JL, Roberts D, Rogerson S, et al. (2004) Oxidative stress in malaria parasite-infected erythrocytes: host-parasite interac- tions. Int J Parasitol 34: 163-189.
15. Pino P, Vouldoukis I, Dugas N, Hassani-Loppion G, Dugas B, et al. (2003) Redox-dependent apoptosis in human endothelial cells after adhesion of Plasmodium falciparum-infected erythrocytes. Ann N Y Acad Sci 1010: 582-586.
16. Wiese L, Kurtzhals JA, Penkowa M (2006) Neuronal apoptosis, metallothionein expression and proinflammatory responses during cerebral malaria in mice. Exp Neurol 200: 216-226.
17. Hopkins RO, Jackson JC (2006) Long-term neurocognitive function after critical illness. Chest 130: 869-878.
18. Pamplona A, Ferreira A, Balla J, Jeney V, Balla G, et al. (2007) Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med 13: 703-710.
19. Lackner P, Beer R, Heussler V, Goebel G, Rudzki D, et al. (2006) Behavioural and histopathological alterations in mice with cerebral malaria. Neuropathol Appl Neurobiol 32: 177-188.
20. Barichello T, Martins MR, Reinke A, Feier G, Ritter C, et al. (2005) Cognitive impairment in sepsis survivors from cecal ligation and perforation. Crit Care Med 33: 221-223; discussion 262-223.
21. Shear HL, Marino MW, Wanidworanun C, Berman JW, Nagel RL (1998) Correlation of increased expression of intercellular adhesion molecule-1, but not high levels of tumor necrosis factor-alpha, with lethality of Plasmodium yoelii 17XL, a rodent model of cerebral malaria. Am J Trop Med Hyg 59: 852-858.
22. Belnoue E, Kayibanda M, Vigario AM, Deschemin JC, van Rooijen N, et al. (2002) On the pathogenic role of brain-sequestered alphabeta CD8+ T cells in experimental cerebral malaria. J Immunol 169: 6369-6375.
23. Randall LM, Amante FH, McSweeney KA, Zhou Y, Stanley AC, et al. (2008) Common strategies to prevent and modulate experimental cerebral malaria in mouse strains with different susceptibilities. Infect Immun 76: 3312-3320.
24. Izquierdo I, Barros DM, Mello e Souza T, de Souza MM, Izquierdo LA, et al. (1998) Mechanisms for memory types differ. Nature 393: 635-636.
25. Bermpohl D, Halle A, Freyer D, Dagand E, Braun JS, et al. (2005) Bacterial programmed cell death of cerebral endothelial cells involves dual death pathways. J Clin Invest 115: 1607-1615.
26. Halliwell B (2006) Oxidative stress and neurodegeneration: where are we now? J Neurochem 97: 1634-1658.
27. Taoufiq Z, Pino P, Dugas N, Conti M, Tefit M, et al. (2006) Transient supplementation of superoxide dismutase protects endothelial cells against Plasmodium falciparum-induced oxidative stress. Mol Biochem Parasitol 150: 166-173.
28. Rosenthal PJ (2008) Artesunate for the treatment of severe falciparum malaria. N Engl J Med 358: 1829-1836.
29. Murphy SC, Breman JG (2001) Gaps in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypogly- cemia, and complications of pregnancy. Am J Trop Med Hyg 64: 57-67.
30. Penet MF, Viola A, Confort-Gouny S, Le Fur Y, Duhamel G, et al. (2005) Imaging experimental cerebral malaria in vivo: significant role of ischemic brain edema. J Neurosci 25: 7352-7358.
31. Glickstein M, Berlucchi G (2008) Classical disconnection studies of the corpus callosum. Cortex 44: 914-927.
32. John CC, Bangirana P, Byarugaba J, Opoka RO, Idro R, et al. (2008) Cerebral malaria in children is associated with long-term cognitive impairment. Pediatrics 122: e92-99.
33. Sanni LA, Fu S, Dean RT, Bloomfield G, Stocker R, et al. (1999) Are reactive oxygen species involved in the pathogenesis of murine cerebral malaria? J Infect Dis 179: 217-222.
34. Nahrevanian H, Dascombe MJ (2001) Nitric oxide and reactive nitrogen intermediates during lethal and nonlethal strains of murine malaria. Parasite Immunol 23: 491-501.
35. Cordeiro RS, Assreuy Filho J, Flores CA, Cunha FQ, Martins MA, et al. (1984) Pulmonary edema in mice infected with Plasmodium berghei. Involvement of catecholamines. Experientia 40: 301-302.
36. Sarfo BY, Armah HB, Irune I, Adjei AA, Olver CS, et al. (2005) Plasmodium yoelii 17XL infection up-regulates RANTES, CCR1, CCR3 and CCR5 expression, and induces ultrastructural changes in the cerebellum. Malar J 4: 63.
37. Martins YC, Carvalho LJ, Daniel-Ribeiro CT (2009) Challenges in the determination of early predictors of cerebral malaria: lessons from the human disease and the experimental murine models. Neuroimmunomodulation 16: 134-145.
38. Budson AE, Price BH (2005) Memory dysfunction. N Engl J Med 352: 692-699.
39. Vianna MR, Alonso M, Viola H, Quevedo J, de Paris F, et al. (2000) Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat. Learn Mem 7: 333-340.
40. Jarrard LE (1995) What does the hippocampus really do? Behav Brain Res 71: 1-10.
41. Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253: 1380-1386.
42. Heidbreder CA, Groenewegen HJ (2003) The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci Biobehav Rev 27: 555-579.
43. Mogensen J, Moustgaard A, Khan U, Wortwein G, Nielsen KS (2005) Egocentric spatial orientation in a water maze by rats subjected to transection of the fimbria-fornix and/or ablation of the prefrontal cortex. Brain Res Bull 65: 41-58.
44. Izquierdo I, Medina JH (1995) Correlation between the pharmacology of long- term potentiation and the pharmacology of memory. Neurobiol Learn Mem 63: 19-32.
45. Izquierdo I, Medina JH (1997) Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol Learn Mem 68: 285-316.
46. Ennaceur A, Delacour J (1988) A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav Brain Res 31: 47-59.
47. Rosa RM, Flores DG, Appelt HR, Braga AL, Henriques JA, et al. (2003) Facilitation of long-term object recognition memory by pretraining administra- tion of diphenyl diselenide in mice. Neurosci Lett 341: 217-220.
48. Laatu S, Revonsuo A, Jaykka H, Portin R, Rinne JO (2003) Visual object recognition in early Alzheimer's disease: deficits in semantic processing. Acta Neurol Scand 108: 82-89.
49. Faille D, El-Assaad F, Alessi MC, Fusai T, Combes V, et al. (2009) Platelet- endothelial cell interactions in cerebral malaria: the end of a cordial understanding. Thromb Haemost 102: 1093-1102.
50. Potter SM, Mitchell AJ, Cowden WB, Sanni LA, Dinauer M, et al. (2005) Phagocyte-derived reactive oxygen species do not influence the progression of murine blood-stage malaria infections. Infect Immun 73: 4941-4947.
51. Favre N, Ryffel B, Rudin W (1999) The development of murine cerebral malaria does not require nitric oxide production. Parasitology 118 (Pt 2): 135-138.
52. Mohanty S, Patel DK, Pati SS, Mishra SK (2006) Adjuvant therapy in cerebral malaria. Indian J Med Res 124: 245-260.
53. Halliwell B (2007) Biochemistry of oxidative stress. Biochem Soc Trans 35: 1147-1150.
54. Ritter C, Andrades ME, Reinke A, Menna-Barreto S, Moreira JC, et al. (2004) Treatment with N-acetylcysteine plus deferoxamine protects rats against oxidative stress and improves survival in sepsis. Crit Care Med 32: 342-349.
55. Barichello T, Machado RA, Constantino L, Valvassori SS, Reus GZ, et al. (2007) Antioxidant treatment prevented late memory impairment in an animal model of sepsis. Crit Care Med 35: 2186-2190.
56. De Flora S, Izzotti A, D'Agostini F, Cesarone CF (1991) Antioxidant activity and other mechanisms of thiols involved in chemoprevention of mutation and cancer. Am J Med 91: 122S-130S.
57. Aruoma OI, Halliwell B, Hoey BM, Butler J (1989) The antioxidant action of N- acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Radic Biol Med 6: 593-597.
58. Halliwell B (1987) Oxidants and human disease: some new concepts. FASEB J 1: 358-364.
59. Halliwell B (1989) Protection against tissue damage in vivo by desferrioxamine: what is its mechanism of action? Free Radic Biol Med 7: 645-651.
60. Mu D, Chang YS, Vexler ZS, Ferriero DM (2005) Hypoxia-inducible factor 1alpha and erythropoietin upregulation with deferoxamine salvage after neonatal stroke. Exp Neurol 195: 407-415.
61. Prass K, Ruscher K, Karsch M, Isaev N, Megow D, et al. (2002) Desferrioxamine induces delayed tolerance against cerebral ischemia in vivo and in vitro. J Cereb Blood Flow Metab 22: 520-525.
62. Teixeira LK, Fonseca BP, Vieira-de-Abreu A, Barboza BA, Robbs BK, et al. (2005) IFN-gamma production by CD8+ T cells depends on NFAT1 transcription factor and regulates Th differentiation. J Immunol 175: 5931-5939.
63. Rogers DC, Fisher EM, Brown SD, Peters J, Hunter AJ, et al. (1997) Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm Genome 8: 711-713.
64. Quevedo J, Vianna MR, Roesler R, de-Paris F, Izquierdo I, et al. (1999) Two time windows of anisomycin-induced amnesia for inhibitory avoidance training in rats: protection from amnesia by pretraining but not pre-exposure to the task apparatus. Learn Mem 6: 600-607.
65. Tuon L, Comim CM, Petronilho F, Barichello T, Izquierdo I, et al. (2008) Memory-enhancing treatments reverse the impairment of inhibitory avoidance retention in sepsis-surviving rats. Crit Care 12: R133.
66. Tuon L, Comim CM, Petronilho F, Barichello T, Izquierdo I, et al. (2008) Time-dependent behavioral recovery after sepsis in rats. Intensive Care Med 34: 1724-1731.
67. Schroder N, O'Dell SJ, Marshall JF (2003) Neurotoxic methamphetamine regimen severely impairs recognition memory in rats. Synapse 49: 89-96.
68. Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186: 421-431.
69. Puhl H, Waeg G, Esterbauer H (1994) Methods to determine oxidation of low- density lipoproteins. Methods Enzymol 233: 425-441.