Evidence for the contribution of adult neurogenesis and hippocampal cell death in experimental cerebral malaria cognitive outcome

Neuroscience

Volumn 284, Issue , 2015, Pages 920-933

  De Miranda, A S ^a,b   Brant, F ^a   Campos, A C ^a   Vieira, L B ^a   Rocha, N P ^a   Cisalpino, D ^a   Binda, N S ^a   Rodrigues, D H ^a   Ransohoff, R M ^b   Machado, F S ^a   Rachid, M A ^a   Teixeira, A L ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

CCL11; Cerebral malaria; Cognitive dysfunction; Cytokines; Neuroinflammation; Neurotrophin

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; EOTAXIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; MESSENGER RNA; NERVE GROWTH FACTOR; NEUROTROPHIN; TUMOR NECROSIS FACTOR ALPHA; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CYTOKINE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BDNF GENE; BRAIN MALARIA; CELL DEATH; CELL VIABILITY; COGNITIVE DEFECT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMETRY; DENTATE GYRUS; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FRONTAL CORTEX; GENE; GENE EXPRESSION REGULATION; HIPPOCAMPUS; IMMUNOREGULATION; LOCOMOTION; LONG TERM MEMORY; MEMORY DISORDER; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INFLAMMATION; NGF GENE; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; PLASMODIUM BERGHEI; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TRK B GENE; UPREGULATION; WEIGHT REDUCTION; WORKING MEMORY; ANIMAL; C57BL MOUSE; DISEASE MODEL; FRONTAL LOBE; MALARIA; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DEATH; COGNITION DISORDERS; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; FRONTAL LOBE; HIPPOCAMPUS; MALARIA, CEREBRAL; MEMORY DISORDERS; MICE, INBRED C57BL; NEUROGENESIS; PLASMODIUM BERGHEI; RECEPTOR, TRKB; RNA, MESSENGER;

EID: 84913558157     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.10.062     Document Type: Article

References (80)

1. Agostini R.M., do Nascimento Pinheiro A.C., Binda N.S., Romano Silva M.A., do Nascimento Cordeiro M., Richardson M., Sena Guimaraes A.L., Gomez M.V. Phoneutria spider toxins block ischemia-induced glutamate release and neuronal death of cell layers of the retina. Retina 2011, 31:1392-1399.
2. Aloe L., Properzi F., Probert L., Akassoglou K., Kassiotis G., Micera A., Fiore M. Learning abilities, NGF and BDNF brain levels in two lines of TNF-alpha transgenic mice, one characterized by neurological disorders, the other phenotypically normal. Brain Res 1999, 840:125-137.
3. Angelucci F., Brene S., Mathe A.A. BDNF in schizophrenia, depression and corresponding animal models. Mol Psychiatry 2005, 10:345-352.
4. Arslan S.C., Scheidereit C. The prevalence of TNFalpha-induced necrosis over apoptosis is determined by TAK1-RIP1 interplay. PLoS One 2011, 6:e26069.
5. Barichello T., dos Santos I., Savi G.D., Florentino A.F., Silvestre C., Comim C.M., Feier G., Sachs D., Teixeira M.M., Teixeira A.L., Quevedo J. Tumor necrosis factor alpha (TNF-alpha) levels in the brain and cerebrospinal fluid after meningitis induced by Streptococcus pneumoniae. Neurosci Lett 2009, 467:217-219.
6. Barichello T., Belarmino E., Comim C.M., Cipriano A.L., Generoso J.S., Savi G.D., Stertz L., Kapczinski F., Quevedo J. Correlation between behavioral deficits and decreased brain-derived neurotrophic [correction of neurotrophic] factor in neonatal meningitis. J Neuroimmunol 2010, 223:73-76.
7. Barichello T., Simoes L.R., Valvassori S.S., Generoso J.S., Aveline P.E., Dominguini D., Elias S.G., Vilela M.C., Quevedo J., Teixeira A.L. Klebsiella pneumoniae meningitis induces memory impairment and increases pro-inflammatory host response in the central nervous system of Wistar rats. J Med Microbiol 2014, 63:111-117.
8. Barnes P., Thomas K.L. Proteolysis of proBDNF is a key regulator in the formation of memory. PLoS One 2008, 3:e3248.
9. Bastos G.N., Moriya T., Inui F., Katura T., Nakahata N. Involvement of cyclooxygenase-2 in lipopolysaccharide-induced impairment of the newborn cell survival in the adult mouse dentate gyrus. Neuroscience 2008, 155:454-462.
10. Baune B.T., Wiede F., Braun A., Golledge J., Arolt V., Koerner H. Cognitive dysfunction in mice deficient for TNF- and its receptors. Am J Med Genet B 2008, 147B:1056-1064.
11. Belarbi K., Arellano C., Ferguson R., Jopson T., Rosi S. Chronic neuroinflammation impacts the recruitment of adult-born neurons into behaviorally relevant hippocampal networks. Brain Behav Immun 2012, 26:18-23.
12. Bilbo S.D., Barrientos R.M., Eads A.S., Northcutt A., Watkins L.R., Rudy J.W., Maier S.F. Early-life infection leads to altered BDNF and IL-1beta mRNA expression in rat hippocampus following learning in adulthood. Brain Behav Immun 2008, 22:451-455.
13. Boivin M.J., Bangirana P., Byarugaba J., Opoka R.O., Idro R., Jurek A.M., John C.C. Cognitive impairment after cerebral malaria in children: a prospective study. Pediatrics 2007, 119:e360-e366.
14. Butovsky O., Ziv Y., Schwartz A., Landa G., Talpalar A.E., Pluchino S., Martino G., Schwartz M. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 2006, 31:149-160.
15. Cacci E., Ajmone-Cat M.A., Anelli T., Biagioni S., Minghetti L. In vitro neuronal and glial differentiation from embryonic or adult neural precursor cells are differently affected by chronic or acute activation of microglia. Glia 2008, 56:412-425.
16. Campos A.C., Ortega Z., Palazuelos J., Fogaca M.V., Aguiar D.C., Diaz-Alonso J., Ortega-Gutierrez S., Vazquez-Villa H., Moreira F.A., Guzman M., Galve-Roperh I., Guimaraes F.S. The anxiolytic effect of cannabidiol on chronically stressed mice depends on hippocampal neurogenesis: involvement of the endocannabinoid system. Int J Neuropsychopharmacol 2013, 16:1407-1419.
17. Carroll R.W., Wainwright M.S., Kim K.Y., Kidambi T., Gomez N.D., Taylor T., Haldar K. A rapid murine coma and behavior scale for quantitative assessment of murine cerebral malaria. PLoS One 2010, 5.
18. Choy K.H., de Visser Y., Nichols N.R., Van den Buuse M. Combined neonatal stress and young-adult glucocorticoid stimulation in rats reduce BDNF expression in hippocampus: effects on learning and memory. Hippocampus 2008, 18:655-667.
19. Clark I.A., Alleva L.M., Vissel B. The roles of TNF in brain dysfunction and disease. Pharmacol Ther 2010, 128:519-548.
20. Clarke J.R., Cammarota M., Gruart A., Izquierdo I., Delgado-Garcia J.M. Plastic modifications induced by object recognition memory processing. Proc Natl Acad Sci U S A 2010, 107:2652-2657.
21. Clelland C.D., Choi M., Romberg C., Clemenson G.D., Fragniere A., Tyers P., Jessberger S., Saksida L.M., Barker R.A., Gage F.H., Bussey T.J. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009, 325:210-213.
22. Clemmer L., Martins Y.C., Zanini G.M., Frangos J.A., Carvalho L.J. Artemether and artesunate show the highest efficacies in rescuing mice with late-stage cerebral malaria and rapidly decrease leukocyte accumulation in the brain. Antimicrob Agents Chemother 2011, 55:1383-1390.
23. Comim C.M., Reis P.A., Frutuoso V.S., Fries G.R., Fraga D.B., Kapczinski F., Zugno A.I., Barichello T., Quevedo J., Castro-Faria-Neto H.C. Effects of experimental cerebral malaria in memory, brain-derived neurotrophic factor and acetylcholinesterase activity [correction for activity] in the hippocampus of survivor mice. Neurosci Lett 2012, 523:104-107.
24. Conner J.M., Franks K.M., Titterness A.K., Russell K., Merrill D.A., Christie B.R., Sejnowski T.J., Tuszynski M.H. NGF is essential for hippocampal plasticity and learning. J Neurosci 2009, 29:10883-10889.
25. Dambly-Chaudiere C., Cubedo N., Ghysen A. Control of cell migration in the development of the posterior lateral line: antagonistic interactions between the chemokine receptors CXCR4 and CXCR7/RDC1. BMC Dev Biol 2007, 7:23.
26. Das S., Dutta K., Kumawat K.L., Ghoshal A., Adhya D., Basu A. Abrogated inflammatory response promotes neurogenesis in a murine model of Japanese encephalitis. PLoS One 2011, 6:e17225.
27. Daval J.L., Vert P. Apoptosis and neurogenesis after transient hypoxia in the developing rat brain. Semin Perinatol 2004, 28:257-263.
28. de Miranda A.S., Brant F., Machado F.S., Rachid M.A., Teixeira A.L. Improving cognitive outcome in cerebral malaria: insights from clinical and experimental research. Cent Nerv Syst Agents Med Chem 2011, 11:285-295.
29. de Miranda A.S., Lacerda-Queiroz N., de Carvalho Vilela M., Rodrigues D.H., Rachid M.A., Quevedo J., Teixeira A.L. Anxiety-like behavior and proinflammatory cytokine levels in the brain of C57BL/6 mice infected with Plasmodium berghei (strain ANKA). Neurosci Lett 2011, 491:202-206.
30. de Souza J.B., Hafalla J.C., Riley E.M., Couper K.N. Cerebral malaria: why experimental murine models are required to understand the pathogenesis of disease. Parasitology 2010, 137:755-772.
31. Del Bo R., Angeretti N., Lucca E., De Simoni M.G., Forloni G. Reciprocal control of inflammatory cytokines, IL-1 and IL-6, and beta-amyloid production in cultures. Neurosci Lett 1995, 188:70-74.
32. Deng W., Saxe M.D., Gallina I.S., Gage F.H. Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci 2009, 29:13532-13542.
33. Deng W., Aimone J.B., Gage F.H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat Rev Neurosci 2010, 11:339-350.
34. Derecki N.C., Cardani A.N., Yang C.H., Quinnies K.M., Crihfield A., Lynch K.R., Kipnis J. Regulation of learning and memory by meningeal immunity: a key role for IL-4. J Exp Med 2010, 207:1067-1080.
35. Desruisseaux M.S., Gulinello M., Smith D.N., Lee S.C., Tsuji M., Weiss L.M., Spray D.C., Tanowitz H.B. Cognitive dysfunction in mice infected with Plasmodium berghei strain ANKA. J Infect Dis 2008, 197:1621-1627.
36. Ehninger D., Kempermann G. Neurogenesis in the adult hippocampus. Cell Tissue Res 2008, 331:243-250.
37. Ekdahl C.T., Claasen J.H., Bonde S., Kokaia Z., Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci U S A 2003, 100:13632-13637.
38. Evuarherhe O., Barker G.R., Savalli G., Warburton E.C., Brown M.W. Early memory formation disrupted by atypical PKC inhibitor ZIP in the medial prefrontal cortex but not hippocampus. Hippocampus 2014, 24:934-942.
39. Fernando S.D., Rodrigo C., Rajapakse S. The 'hidden' burden of malaria: cognitive impairment following infection. Malaria J 2010, 9:366.
40. Fiore M., Angelucci F., Alleva E., Branchi I., Probert L., Aloe L. Learning performances, brain NGF distribution and NPY levels in transgenic mice expressing TNF-alpha. Behav Brain Res 2000, 112:165-175.
41. Fujioka H., Akema T. Lipopolysaccharide acutely inhibits proliferation of neural precursor cells in the dentate gyrus in adult rats. Brain Res 2010, 1352:35-42.
42. Groettrup M., Kirk C.J., Basler M. Proteasomes in immune cells: more than peptide producers?. Nat Rev Immunol 2010, 10:73-78.
43. Guha S.K., Tillu R., Sood A., Patgaonkar M., Nanavaty I.N., Sengupta A., Sharma S., Vaidya V.A., Pathak S. Single episode of mild murine malaria induces neuroinflammation, alters microglial profile, impairs adult neurogenesis, and causes deficits in social and anxiety-like behavior. Brain Behav Immun 2014.
44. Heldt S.A., Stanek L., Chhatwal J.P., Ressler K.J. Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol Psychiatry 2007, 12:656-670.
45. Hryniewicz A., Bialuk I., Kaminski K.A., Winnicka M.M. Impairment of recognition memory in interleukin-6 knock-out mice. Eur J Pharmacol 2007, 577:219-220.
46. Hunt N.H., Golenser J., Chan-Ling T., Parekh S., Rae C., Potter S., Medana I.M., Miu J., Ball H.J. Immunopathogenesis of cerebral malaria. Int J Parasitol 2006, 36:569-582.
47. Idro R., Jenkins N.E., Newton C.R. Pathogenesis, clinical features, and neurological outcome of cerebral malaria. Lancet Neurol 2005, 4:827-840.
48. Jakubs K., Bonde S., Iosif R.E., Ekdahl C.T., Kokaia Z., Kokaia M., Lindvall O. Inflammation regulates functional integration of neurons born in adult brain. J Neurosci 2008, 28:12477-12488.
49. Jessberger S., Clark R.E., Broadbent N.J., Clemenson G.D., Consiglio A., Lie D.C., Squire L.R., Gage F.H. Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Memory 2009, 16:147-154.
50. John C.C., Panoskaltsis-Mortari A., Opoka R.O., Park G.S., Orchard P.J., Jurek A.M., Idro R., Byarugaba J., Boivin M.J. Cerebrospinal fluid cytokine levels and cognitive impairment in cerebral malaria. Am J Trop Med Hyg 2008, 78:198-205.
51. Jurgens H.A., Amancherla K., Johnson R.W. Influenza infection induces neuroinflammation, alters hippocampal neuron morphology, and impairs cognition in adult mice. J Neurosci 2012, 32:3958-3968.
52. Kiyota T., Ingraham K.L., Swan R.J., Jacobsen M.T., Andrews S.J., Ikezu T. AAV serotype 2/1-mediated gene delivery of anti-inflammatory interleukin-10 enhances neurogenesis and cognitive function in APP+PS1 mice. Gene Ther 2012, 19:724-733.
53. Koo J.W., Duman R.S. IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci U S A 2008, 105:751-756.
54. Krathwohl M.D., Kaiser J.L. Chemokines promote quiescence and survival of human neural progenitor cells. Stem Cells 2004, 22:109-118.
55. Lacerda-Queiroz N., Rodrigues D.H., Vilela M.C., Miranda A.S., Amaral D.C., Camargos E.R., Carvalho L.J., Howe C.L., Teixeira M.M., Teixeira A.L. Inflammatory changes in the central nervous system are associated with behavioral impairment in Plasmodium berghei (strain ANKA)-infected mice. Exp Parasitol 2010, 125:271-278.
56. Li S., Wang C., Wang W., Dong H., Hou P., Tang Y. Chronic mild stress impairs cognition in mice: from brain homeostasis to behavior. Life Sci 2008, 82:934-942.
57. Li L., Shui Q.X., Zhao Z.Y., Zhu X.D., Bao W.D. Dynamic changes of TrkB gene expression in Streptococcus pneumoniae meningitis after treatment with antibiotics and dexamethasone. World J Pediatrics 2011, 7:250-256.
58. Linares M., Marin-Garcia P., Perez-Benavente S., Sanchez-Nogueiro J., Puyet A., Bautista J.M., Diez A. Brain-derived neurotrophic factor and the course of experimental cerebral malaria. Brain Res 2013, 1490:210-224.
59. Lu Y., Christian K., Lu B. BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory?. Neurobiol Learn Mem 2008, 89:312-323.
60. Lyke K.E., Burges R., Cissoko Y., Sangare L., Dao M., Diarra I., Kone A., Harley R., Plowe C.V., Doumbo O.K., Sztein M.B. Serum levels of the proinflammatory cytokines interleukin-1 beta (IL-1beta), IL-6, IL-8, IL-10, tumor necrosis factor alpha, and IL-12(p70) in Malian children with severe Plasmodium falciparum malaria and matched uncomplicated malaria or healthy controls. Infect Immun 2004, 72:5630-5637.
61. Mina F., Comim C.M., Dominguini D., Cassol O.J., Dall Igna D.M., Ferreira G.K., Silva M.C., Galant L.S., Streck E.L., Quevedo J., Dal-Pizzol F. Il1-beta involvement in cognitive impairment after sepsis. Mol Neurobiol 2014, 49:1069-1076.
62. Mineur Y.S., Belzung C., Crusio W.E. Functional implications of decreases in neurogenesis following chronic mild stress in mice. Neuroscience 2007, 150:251-259.
63. Miranda A.S., Brant F., Rocha N.P., Cisalpino D., Rodrigues D.H., Souza D.G., Machado F.S., Rachid M.A., Teixeira A.L., Campos A.C. Further evidence for an anti-inflammatory role of artesunate in experimental cerebral malaria. Malaria J 2013, 12:388.
64. Monje M.L., Toda H., Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003, 302:1760-1765.
65. Parkhurst C.N., Yang G., Ninan I., Savas J.N., Yates J.R., Lafaille J.J., Hempstead B.L., Littman D.R., Gan W.B. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 2013, 155:1596-1609.
66. Peng S., Garzon D.J., Marchese M., Klein W., Ginsberg S.D., Francis B.M., Mount H.T., Mufson E.J., Salehi A., Fahnestock M. Fahnestock decreased brain-derived neurotrophic factor depends on amyloid aggregation state in transgenic mouse models of Alzheimer's disease. J Neurosci 2009, 29:9321-9329.
67. Ransohoff R.M. Chemokines and chemokine receptors: standing at the crossroads of immunobiology and neurobiology. Immunity 2009, 31:711-721.
68. Reis P.A., Comim C.M., Hermani F., Silva B., Barichello T., Portella A.C., Gomes F.C., Sab I.M., Frutuoso V.S., Oliveira M.F., Bozza P.T., Bozza F.A., Dal-Pizzol F., Zimmerman G.A., Quevedo J., Castro-Faria-Neto H.C. Cognitive dysfunction is sustained after rescue therapy in experimental cerebral malaria, and is reduced by additive antioxidant therapy. PLoS Pathog 2010, 6:e1000963.
69. Ringheim G.E., Szczepanik A.M., Petko W., Burgher K.L., Zhu S.Z., Chao C.C. Enhancement of beta-amyloid precursor protein transcription and expression by the soluble interleukin-6 receptor/interleukin-6 complex. Brain Res Mol Brain Res 1998, 55:35-44.
70. Rogers D.C., Fisher E.M., Brown S.D., Peters J., Hunter A.J., Martin J.E. Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm Genome 1997, 8:711-713.
71. Schroder N., O'Dell S.J., Marshall J.F. Neurotoxic methamphetamine regimen severely impairs recognition memory in rats. Synapse 2003, 49:89-96.
72. Sommerfeld M.T., Schweigreiter R., Barde Y.A., Hoppe E. (Down-regulation of the neurotrophin receptor TrkB following ligand binding. Evidence for an involvement of the proteasome and differential regulation of TrkA and TrkB. J Biol Chem 2000, 275:8982-8990.
73. Spooren A., Kolmus K., Laureys G., Clinckers R., De Keyser J., Haegeman G., Gerlo S. Interleukin-6, a mental cytokine. Brain Res Rev 2011, 67:157-183.
74. Taepavarapruk P., Song C. Reductions of acetylcholine release and nerve growth factor expression are correlated with memory impairment induced by interleukin-1beta administrations: effects of omega-3 fatty acid EPA treatment. J Neurochem 2010, 112:1054-1064.
75. Tanaka S., Ide M., Shibutani T., Ohtaki H., Numazawa S., Shioda S., Yoshida T. Lipopolysaccharide-induced microglial activation induces learning and memory deficits without neuronal cell death in rats. J Neurosci Res 2006, 83:557-566.
76. Villeda S.A., Luo J., Mosher K.I., Zou B., Britschgi M., Bieri G., Stan T.M., Fainberg N., Ding Z., Eggel A., Lucin K.M., Czirr E., Park J.S., Couillard-Despres S., Aigner L., Li G., Peskind E.R., Kaye J.A., Quinn J.F., Galasko D.R., Xie X.S., Rando T.A., Wyss-Coray T. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 2011, 477:90-94.
77. Wang Y., Li G., Stanco A., Long J.E., Crawford D., Potter G.B., Pleasure S.J., Behrens T., Rubenstein J.T. CXCR4 and CXCR7 have distinct functions in regulating interneuron migration. Neuron 2011, 69:61-76.
78. Xu H., Chen Z., He J., Haimanot S., Li X., Dyck L., Li X.M. Synergetic effects of quetiapine and venlafaxine in preventing the chronic restraint stress-induced decrease in cell proliferation and BDNF expression in rat hippocampus. Hippocampus 2006, 16:551-559.
79. York J.M., Blevins N.A., Baynard T., Freund G.G. Mouse testing methods in psychoneuroimmunology: an overview of how to measure sickness, depressive/anxietal, cognitive, and physical activity behaviors. Methods Mol Biol 2012, 934:243-276.
80. Zhang C.L., Zou Y., He W., Gage F.H., Evans R.M. A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 2008, 451:1004-1007.