Brain-derived neurotrophic factor and the course of experimental cerebral malaria

Brain Research

Volumn 1490, Issue , 2013, Pages 210-224

  Linares, María ^a,b   Marín García, Patricia ^a,b   Pérez Benavente, Susana ^a   Sánchez Nogueiro, Jesús ^a   Puyet, Antonio ^a,b   Bautista, José M ^a,b   Diez, Amalia ^a,b  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

Author keywords

Adhesion molecule; BDNF; Cerebral malaria; Cytokine; Proteasome

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA; PADGEM PROTEIN; PROTEASOME; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN MALARIA; BRAIN STEM; C57BL 6 MOUSE; CEREBELLUM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISEASE CLASSIFICATION; DISEASE COURSE; DISEASE SEVERITY; ERYTHROCYTE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PLASMODIUM BERGHEI; PLASMODIUM BERGHEI INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; RECEPTOR DOWN REGULATION; THALAMUS; UPREGULATION;

ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; BRAIN CHEMISTRY; BRAIN-DERIVED NEUROTROPHIC FACTOR; CYTOKINES; DISEASE PROGRESSION; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; MALARIA, CEREBRAL; MALE; MICE; MICE, INBRED C57BL; NEURAL CELL ADHESION MOLECULES; PARASITE LOAD; PLASMODIUM BERGHEI; POLYMERASE CHAIN REACTION; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA;

MUS; PLASMODIUM BERGHEI;

EID: 84871293454     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.10.040     Document Type: Article

References (64)

1. R. Aharoni, R. Eilam, H. Domev, G. Labunskay, M. Sela, and R. Arnon The immunomodulator glatiramer acetate augments the expression of neurotrophic factors in brains of experimental autoimmune encephalomyelitis mice Proc. Natl. Acad. Sci. U.S.A. 102 2005 19045 19050
2. F.H. Amante, A.C. Stanley, L.M. Randall, Y. Zhou, A. Haque, K. McSweeney, A.P. Waters, C.J. Janse, M.F. Good, G.R. Hill, and C.R. Engwerda A role for natural regulatory T cells in the pathogenesis of experimental cerebral malaria Am. J. Pathol. 171 2007 548 559
3. Anand, S.S.; Babu, P.P. Endoplasmic reticulum stress and neurodegeneration in experimental cerebral malaria. Neurosignals, 10.1159/000336970, in press.
4. H. Armah, E.K. Wired, A.K. Dodoo, A.A. Adjei, Y. Tettey, and R. Gyasi Cytokines and adhesion molecules expression in the brain in human cerebral malaria Int. J. Environ. Res. Public Health 2 2005 123 131
5. F.G. Baptista, A. Pamplona, A.C. Pena, M.M. Mota, S. Pied, and A.M. Vigario Accumulation of Plasmodium berghei-infected red blood cells in the brain is crucial for the development of cerebral malaria in mice Infect. Immun. 78 2010 4033 4039
6. M. Bentivoglio, R. Mariotti, and G. Bertini Neuroinflammation and brain infections: historical context and current perspectives Brain Res. Rev. 66 2011 152 173
7. B. Bingol, and M. Sheng Deconstruction for reconstruction: the role of proteolysis in neural plasticity and disease Neuron 69 2011 22 32
8. R. Bisaz, L. Conboy, and C. Sandi Learning under stress: a role for the neural cell adhesion molecule NCAM Neurobiol. Learn. Mem. 91 2009 333 342
9. M.J. Boivin, P. Bangirana, J. Byarugaba, R.O. Opoka, R. Idro, A.M. Jurek, and C.C. John Cognitive impairment after cerebral malaria in children: a prospective study Pediatrics 119 2007 e360 e366
10. P. Cabrales, G.M. Zanini, D. Meays, J.A. Frangos, and L.J. Carvalho Murine cerebral malaria is associated with a vasospasm-like microcirculatory dysfunction, and survival upon rescue treatment is markedly increased by nimodipine Am. J. Pathol. 176 2010 1306 1315
11. V. Combes, F. El-Assaad, D. Faille, R. Jambou, N.H. Hunt, and G.E. Grau Microvesiculation and cell interactions at the brain-endothelial interface in cerebral malaria pathogenesis Prog. Neurobiol. 91 2010 140 151
12. C. Cunha, R. Brambilla, and K.L. Thomas A simple role for BDNF in learning and memory? Front Mol. Neurosci. 3 2010 1
13. Q. Chen, M. Schlichtherle, and M. Wahlgren Molecular aspects of severe malaria Clin. Microbiol. Rev. 13 2000 439 450
14. B.J. de Souza, J.C. Hafalla, E.M. Riley, and K.N. Couper Cerebral malaria: why experimental murine models are required to understand the pathogenesis of disease Parasitology 137 2010 755 772
15. J.B. de Souza, and E.M. Riley Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis Microbes Infect. 4 2002 291 300
16. N.F. Delahaye, N. Coltel, D. Puthier, M. Barbier, P. Benech, F. Joly, F.A. Iraqi, G.E. Grau, C. Nguyen, and P. Rihet Gene expression analysis reveals early changes in several molecular pathways in cerebral malaria-susceptible mice versus cerebral malaria-resistant mice BMC Genom. 8 2007 452
17. M.S. Desruisseaux, D.A. Iacobas, S. Iacobas, S. Mukherjee, L.M. Weiss, H.B. Tanowitz, and D.C. Spray Alterations in the brain transcriptome in Plasmodium berghei ANKA infected mice J. Neuroparasitol. 1 2010 1 8
18. M. Di Filippo, P. Sarchielli, B. Picconi, and P. Calabresi Neuroinflammation and synaptic plasticity: theoretical basis for a novel, immune-centred, therapeutic approach to neurological disorders Trends Pharmacol. Sci. 29 2008 402 412
19. C. Dong, S.C. Upadhya, L. Ding, T.K. Smith, and A.N. Hegde Proteasome inhibition enhances the induction and impairs the maintenance of late-phase long-term potentiation Learn. Mem. 15 2008 335 347
20. M. Ebadi, R.M. Bashir, M.L. Heidrick, F.M. Hamada, H.E. Refaey, A. Hamed, G. Helal, M.D. Baxi, D.R. Cerutis, and N.K. Lassi Neurotrophins and their receptors in nerve injury and repair Neurochem. Int. 30 1997 347 374
21. P. Eeka, G.V. Chaitanya, and P.P. Babu Proteolytic breakdown of cytoskeleton induces neurodegeneration during pathology of murine cerebral malaria Brain Res. 1417 2011 103 114
22. C.R. Engwerda, T.L. Mynott, S. Sawhney, J.B. De Souza, Q.D. Bickle, and P.M. Kaye Locally up-regulated lymphotoxin alpha, not systemic tumor necrosis factor alpha, is the principle mediator of murine cerebral malaria J. Exp. Med. 195 2002 1371 1377
23. B. Franke-Fayard, C.J. Janse, M. Cunha-Rodrigues, J. Ramesar, P. Buscher, I. Que, C. Lowik, P.J. Voshol, M.A. den Boer, S.G. van Duinen, M. Febbraio, M.M. Mota, and A.P. Waters Murine malaria parasite sequestration: CD36 is the major receptor, but cerebral pathology is unlinked to sequestration Proc. Natl. Acad. Sci. U.S.A. 102 2005 11468 11473
24. E. Fukami, A. Nakayama, J. Sasaki, S. Mimura, N. Mori, and K. Watanabe Underexpression of neural cell adhesion molecule and neurotrophic factors in rat brain following thromboxane A(2)-induced intrauterine growth retardation Early Hum. Dev. 58 2000 101 110
25. M.P. Gavilan, A. Castano, M. Torres, M. Portavella, C. Caballero, S. Jimenez, A. Garcia-Martinez, J. Parrado, J. Vitorica, and D. Ruano Age-related increase in the immunoproteasome content in rat hippocampus: molecular and functional aspects J. Neurochem. 108 2009 260 272
26. M.E. Greenberg, B. Xu, B. Lu, and B.L. Hempstead New insights in the biology of BDNF synthesis and release: implications in CNS function J. Neurosci. 29 2009 12764 12767
27. M. Groettrup, C.J. Kirk, and M. Basler Proteasomes in immune cells: more than peptide producers? Nat. Rev. Immunol. 10 2010 73 78
28. J. Hearn, N. Rayment, D.N. Landon, D.R. Katz, and J.B. de Souza Immunopathology of cerebral malaria: morphological evidence of parasite sequestration in murine brain microvasculature Infect. Immun. 68 2000 5364 5376
29. M. Ho, and N.J. White Molecular mechanisms of cytoadherence in malaria Am. J. Physiol. 276 1999 C1231 C1242
30. N.H. Hunt, and G.E. Grau Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria Trends Immunol. 24 2003 491 499
31. N.H. Hunt, J. Golenser, T. Chan-Ling, S. Parekh, C. Rae, S. Potter, I.M. Medana, J. Miu, and H.J. Ball Immunopathogenesis of cerebral malaria Int. J. Parasitol. 36 2006 569 582
32. R. Idro, N.E. Jenkins, and C.R. Newton Pathogenesis, clinical features, and neurological outcome of cerebral malaria Lancet Neurol. 4 2005 827 840
33. R. Idro, A. Kakooza-Mwesige, S. Balyejjussa, G. Mirembe, C. Mugasha, J. Tugumisirize, and J. Byarugaba Severe neurological sequelae and behaviour problems after cerebral malaria in Ugandan children BMC Res. Notes 3 2010 104
34. R. Idro, K. Marsh, C.C. John, and C.R. Newton Cerebral malaria: mechanisms of brain injury and strategies for improved neurocognitive outcome Pediatr. Res. 68 2010 267 274
35. J.Z. Kiss, E. Troncoso, Z. Djebbara, L. Vutskits, and D. Muller The role of neural cell adhesion molecules in plasticity and repair Brain Res. Rev. 36 2001 175 184
36. L.B. Kohler, C. Christensen, C. Rossetti, M. Fantin, C. Sandi, E. Bock, and V. Berezin Dennexin peptides modeled after the homophilic binding sites of the neural cell adhesion molecule (NCAM) promote neuronal survival, modify cell adhesion and impair spatial learning Eur. J. Cell. Biol. 89 2010 817 827
37. M.K. Kwak, N. Wakabayashi, J.L. Greenlaw, M. Yamamoto, and T.W. Kensler Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway Mol. Cell. Biol. 23 2003 8786 8794
38. N. Lacerda-Queiroz, D.H. Rodrigues, M.C. Vilela, A.S. Miranda, D.C. Amaral, E.R. Camargos, L.J. Carvalho, C.L. Howe, M.M. Teixeira, and A.L. Teixeira Inflammatory changes in the central nervous system are associated with behavioral impairment in Plasmodium berghei (strain ANKA)-infected mice Exp. Parasitol. 125 2010 271 278
39. P. Lackner, R. Beer, V. Heussler, G. Goebel, D. Rudzki, R. Helbok, E. Tannich, and E. Schmutzhard Behavioural and histopathological alterations in mice with cerebral malaria Neuropathol. Appl. Neurobiol. 32 2006 177 188
40. P. Lackner, A. Part, C. Burger, A. Dietmann, G. Broessner, R. Helbok, M. Reindl, E. Schmutzhard, and R. Beer Glatiramer acetate reduces the risk for experimental cerebral malaria: a pilot study Malar. J. 8 2009 36
41. M. Linares, P. Marin-Garcia, D. Mendez, A. Puyet, A. Diez, and J.M. Bautista Proteomic approaches to identifying carbonylated proteins in brain tissue J. Proteome Res. 10 2011 1719 1727
42. M. Linares, P. Marin-Garcia, S. Perez-Benavente, J. Sanchez-Nogueiro, A. Puyet, J.M. Bautista, and A. Diez Decreased levels of brain-derived neurotrophic factor across the neurological phenotype of cerebral malaria Eur. J. Trop. Med. Int. Health 16 S1 2011 147
43. J. Lou, R. Lucas, and G.E. Grau Pathogenesis of cerebral malaria: recent experimental data and possible applications for humans Clin. Microbiol. Rev. 14 2001 810 820
44. F.E. Lovegrove, S.A. Gharib, S.N. Patel, C.A. Hawkes, K.C. Kain, and W.C. Liles Expression microarray analysis implicates apoptosis and interferon-responsive mechanisms in susceptibility to experimental cerebral malaria Am. J. Pathol. 171 2007 1894 1903
45. B. Lu BDNF and activity-dependent synaptic modulation Learn. Mem. 10 2003 86 98
46. P. Marin-Garcia, J. Sanchez-Nogueiro, A. Diez, M. Leon-Otegui, M. Linares, P. Garcia-Palencia, J.M. Bautista, and M.T. Miras-Portugal Altered nucleotide receptor expression in a murine model of cerebral malaria J. Infect. Dis. 200 2009 1279 1288
47. I.M. Medana, and M.M. Esiri Axonal damage: a key predictor of outcome in human CNS diseases Brain 126 2003 515 530
48. I.M. Medana, R. Idro, and C.R. Newton Axonal and astrocyte injury markers in the cerebrospinal fluid of Kenyan children with severe malaria J. Neurol. Sci. 258 2007 93 98
49. J. Miu, N.H. Hunt, and H.J. Ball Predominance of interferon-related responses in the brain during murine malaria, as identified by microarray analysis Infect. Immun. 76 2008 1812 1824
50. T.P. Nguyen, V.M. Soukup, and B.B. Gelman Persistent hijacking of brain proteasomes in HIV-associated dementia Am. J. Pathol. 176 2010 893 902
51. M.F. Penet, A. Viola, S. Confort-Gouny, Y. Le Fur, G. Duhamel, F. Kober, D. Ibarrola, M. Izquierdo, N. Coltel, B. Gharib, G.E. Grau, and P.J. Cozzone Imaging experimental cerebral malaria in vivo: significant role of ischemic brain edema J. Neurosci. 25 2005 7352 7358
52. C. Pierrot, E. Adam, S. Lafitte, C. Godin, D. Dive, M. Capron, and J. Khalife Age-related susceptibility and resistance to Plasmodium berghei in mice and rats Exp. Parasitol. 104 2003 81 85
53. P. Pino, Z. Taoufiq, J. Nitcheu, I. Vouldoukis, and D. Mazier Blood-brain barrier breakdown during cerebral malaria: suicide or murder? Thromb Haemost. 94 2005 336 340
54. B. Pouvelle, V. Matarazzo, C. Jurzynski, J. Nemeth, M. Ramharter, G. Rougon, and J. Gysin Neural cell adhesion molecule, a new cytoadhesion receptor for Plasmodium falciparum-infected erythrocytes capable of aggregation Infect. Immun. 75 2007 3516 3522
55. D.C. Rubinsztein The roles of intracellular protein-degradation pathways in neurodegeneration Nature 443 2006 780 786
56. L. Schofield, and G.E. Grau Immunological processes in malaria pathogenesis Nat. Rev. Immunol. 5 2005 722 735
57. K.K. Sein, Y. Maeno, H.V. Thuc, T.K. Anh, and M. Aikawa Differential sequestration of parasitized erythrocytes in the cerebrum and cerebellum in human cerebral malaria Am. J. Trop. Med. Hyg. 48 1993 504 511
58. H. Seo, W. Kim, and O. Isacson Compensatory changes in the ubiquitin-proteasome system, brain-derived neurotrophic factor and mitochondrial complex II/III in YAC72 and R6/2 transgenic mice partially model Huntington's disease patients Hum. Mol. Genet. 17 2008 3144 3153
59. M.T. Sommerfeld, R. Schweigreiter, Y.A. Barde, and E. Hoppe 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. 275 2000 8982 8990
60. G.D. Turner, H. Morrison, M. Jones, T.M. Davis, S. Looareesuwan, I.D. Buley, K.C. Gatter, C.I. Newbold, S. Pukritayakamee, and B. Nagachinta An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration Am. J. Pathol. 145 1994 1057 1069
61. H.C. van der Heyde, J. Nolan, V. Combes, I. Gramaglia, and G.E. Grau A unified hypothesis for the genesis of cerebral malaria: sequestration, inflammation and hemostasis leading to microcirculatory dysfunction Trends Parasitol. 22 2006 503 508
62. L. Vutskits, Z. Djebbara-Hannas, H. Zhang, J.P. Paccaud, P. Durbec, G. Rougon, D. Muller, and J.Z. Kiss PSA-NCAM modulates BDNF-dependent survival and differentiation of cortical neurons Eur. J. Neurosci. 13 2001 1391 1402
63. S. Weiser, J. Miu, H.J. Ball, and N.H. Hunt Interferon-gamma synergises with tumour necrosis factor and lymphotoxin-alpha to enhance the mRNA and protein expression of adhesion molecules in mouse brain endothelial cells Cytokine 37 2007 84 91
64. C. Zuccato, and E. Cattaneo Brain-derived neurotrophic factor in neurodegenerative diseases Nat. Rev. Neurol. 5 2009 311 322