Olfactory plays a key role in spatiotemporal pathogenesis of cerebral malaria

Cell Host and Microbe

Volumn 15, Issue 5, 2014, Pages 551-563

  Zhao, Hong ^a   Aoshi, Taiki ^a,b   Kawai, Satoru ^c   Mori, Yuki ^a   Konishi, Aki ^a   Ozkan, Muge ^a   Fujita, Yukiko ^a   Haseda, Yasunari ^b   Shimizu, Mikiko ^a   Kohyama, Masako ^a   Kobiyama, Kouji ^a,b   Eto, Kei ^d   Nabekura, Junichi ^d   Horii, Toshihiro ^e   Ishino, Tomoko ^f   Yuda, Masao ^f   Hemmi, Hiroaki ^a   Kaisho, Tsuneyasu ^a   Akira, Shizuo ^a   Kinoshita, Manabu ^g   Tohyama, Koujiro ^h   Yoshioka, Yoshichika ^a   Ishii, Ken J ^a,b   Coban, Cevayir ^a   more..

^a OSAKA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^c DOKKYO MEDICAL UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^e OSAKA UNIVERSITY   (Japan)

^f MIE UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^g OSAKA MEDICAL CENTER FOR CANCER AND CARDIOVASCULAR DISEASES   (Japan)

^h IWATE MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR3; SECONDARY LYMPHOID TISSUE CHEMOKINE; CCR7 PROTEIN, MOUSE; CXCR3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY; BRAIN HEMORRHAGE; BRAIN MALARIA; CD8+ T LYMPHOCYTE; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE STORM; DIFFUSION WEIGHTED IMAGING; ERYTHROCYTE; FEVER; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOGENESIS; MOUSE; MULTIPHOTON MICROSCOPY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OLFACTORY BULB; PARASITE SURVIVAL; PARASITE VIRULENCE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; SMELLING; ANIMAL; C57BL MOUSE; FEMALE; GENETICS; HUMAN; IMMUNOLOGY; MALARIA; MALE; PARASITOLOGY; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; VIRULENCE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CHEMOKINE CCL21; FEMALE; HUMANS; MALARIA, CEREBRAL; MALE; MICE; MICE, INBRED C57BL; OLFACTORY BULB; PLASMODIUM FALCIPARUM; RECEPTORS, CCR7; RECEPTORS, CXCR3; VIRULENCE;

EID: 84900988314     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2014.04.008     Document Type: Article

References (55)

1. F.G. Baptista, A. Pamplona, A.C. Pena, M.M. Mota, S. Pied, and A.M. Vigário 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
2. M. Barresi, R. Ciurleo, S. Giacoppo, V. Foti Cuzzola, D. Celi, P. Bramanti, and S. Marino Evaluation of olfactory dysfunction in neurodegenerative diseases J. Neurol. Sci. 323 2012 16 24
3. E. Belnoue, F.T. Costa, A.M. Vigário, T. Voza, F. Gonnet, I. Landau, N. Van Rooijen, M. Mack, W.A. Kuziel, and L. Rénia Chemokine receptor CCR2 is not essential for the development of experimental cerebral malaria Infect. Immun. 71 2003 3648 3651
4. E. Belnoue, M. Kayibanda, J.C. Deschemin, M. Viguier, M. Mack, W.A. Kuziel, and L. Rénia CCR5 deficiency decreases susceptibility to experimental cerebral malaria Blood 101 2003 4253 4259
5. S. Bovetti, Y.C. Hsieh, P. Bovolin, I. Perroteau, T. Kazunori, and A.C. Puche Blood vessels form a scaffold for neuroblast migration in the adult olfactory bulb J. Neurosci. 27 2007 5976 5980
6. 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
7. G.S. Campanella, A.M. Tager, J.K. El Khoury, S.Y. Thomas, T.A. Abrazinski, L.A. Manice, R.A. Colvin, and A.D. Luster Chemokine receptor CXCR3 and its ligands CXCL9 and CXCL10 are required for the development of murine cerebral malaria Proc. Natl. Acad. Sci. USA 105 2008 4814 4819
8. E. Chaigneau, M. Oheim, E. Audinat, and S. Charpak Two-photon imaging of capillary blood flow in olfactory bulb glomeruli Proc. Natl. Acad. Sci. USA 100 2003 13081 13086
9. Y. Chen, J. Mancuso, Z. Zhao, X. Li, J. Cheng, G. Roman, and S.T. Wong Vasodilation by in vivo activation of astrocyte endfeet via two-photon calcium uncaging as a strategy to prevent brain ischemia J. Biomed. Opt. 18 2013 126012
10. C. Coban, K.J. Ishii, S. Uematsu, N. Arisue, S. Sato, M. Yamamoto, T. Kawai, O. Takeuchi, H. Hisaeda, T. Horii, and S. Akira Pathological role of Toll-like receptor signaling in cerebral malaria Int. Immunol. 19 2007 67 79
11. L. Danielyan, R. Schäfer, A. von Ameln-Mayerhofer, M. Buadze, J. Geisler, T. Klopfer, U. Burkhardt, B. Proksch, S. Verleysdonk, and M. Ayturan et al. Intranasal delivery of cells to the brain Eur. J. Cell Biol. 88 2009 315 324
12. A.H. de Haas, H.R. van Weering, E.K. de Jong, H.W. Boddeke, and K.P. Biber Neuronal chemokines: versatile messengers in central nervous system cell interaction Mol. Neurobiol. 36 2007 137 151
13. D. De Saint Jan, and G.L. Westbrook Detecting activity in olfactory bulb glomeruli with astrocyte recording J. Neurosci. 25 2005 2917 2924
14. R. Förster, A. Schubel, D. Breitfeld, E. Kremmer, I. Renner-Müller, E. Wolf, and M. Lipp CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs Cell 99 1999 23 33
15. D.S. Hansen, N.J. Bernard, C.Q. Nie, and L. Schofield NK cells stimulate recruitment of CXCR3+ T cells to the brain during Plasmodium berghei-mediated cerebral malaria J. Immunol. 178 2007 5779 5788
16. A. Haque, S.E. Best, K. Unosson, F.H. Amante, F. de Labastida, N.M. Anstey, G. Karupiah, M.J. Smyth, W.R. Heath, and C.R. Engwerda Granzyme B expression by CD8+ T cells is required for the development of experimental cerebral malaria J. Immunol. 186 2011 6148 6156
17. S.W. Howland, C.M. Poh, S.Y. Gun, C. Claser, B. Malleret, N. Shastri, F. Ginhoux, G.M. Grotenbreg, and L. Renia Brain microvessel cross-presentation is a hallmark of experimental cerebral malaria EMBO Mol. Med. 5 2013 916 931
18. 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
19. T. Ishino, Y. Orito, Y. Chinzei, and M. Yuda A calcium-dependent protein kinase regulates Plasmodium ookinete access to the midgut epithelial cell Mol. Microbiol. 59 2006 1175 1184
20. T. Junt, E. Scandella, R. Förster, P. Krebs, S. Krautwald, M. Lipp, H. Hengartner, and B. Ludewig Impact of CCR7 on priming and distribution of antiviral effector and memory CTL J. Immunol. 173 2004 6684 6693
21. E.A. Kiyatkin, and H.S. Sharma Permeability of the blood-brain barrier depends on brain temperature Neuroscience 161 2009 926 939
22. S.J. Lalor, and B.M. Segal Lymphoid chemokines in the CNS J. Neuroimmunol. 224 2010 56 61
23. T.J. Lamb, D.E. Brown, A.J. Potocnik, and J. Langhorne Insights into the immunopathogenesis of malaria using mouse models Expert Rev. Mol. Med. 8 2006 1 22
24. J. Langhorne, P. Buffet, M. Galinski, M. Good, J. Harty, D. Leroy, M.M. Mota, E. Pasini, L. Renia, and E. Riley et al. The relevance of non-human primate and rodent malaria models for humans Malar. J. 10 2011 23
25. R.J. Lundie, T.F. de Koning-Ward, G.M. Davey, C.Q. Nie, D.S. Hansen, L.S. Lau, J.D. Mintern, G.T. Belz, L. Schofield, and F.R. Carbone et al. Blood-stage Plasmodium infection induces CD8+ T lymphocytes to parasite-expressed antigens, largely regulated by CD8alpha+ dendritic cells Proc. Natl. Acad. Sci. USA 105 2008 14509 14514
26. R.R. Machado, D.M. Soares, A.E. Proudfoot, and G.E. Souza CCR1 and CCR5 chemokine receptors are involved in fever induced by LPS (E. coli) and RANTES in rats Brain Res. 1161 2007 21 31
27. A.D. McLellan, M. Kapp, A. Eggert, C. Linden, U. Bommhardt, E.B. Bröcker, U. Kämmerer, and E. Kämpgen Anatomic location and T-cell stimulatory functions of mouse dendritic cell subsets defined by CD4 and CD8 expression Blood 99 2002 2084 2093
28. J.A. McQuillan, A.J. Mitchell, Y.F. Ho, V. Combes, H.J. Ball, J. Golenser, G.E. Grau, and N.H. Hunt Coincident parasite and CD8 T cell sequestration is required for development of experimental cerebral malaria Int. J. Parasitol. 41 2011 155 163
29. I.M. Medana, T. Chan-Ling, and N.H. Hunt Redistribution and degeneration of retinal astrocytes in experimental murine cerebral malaria: relationship to disruption of the blood-retinal barrier Glia 16 1996 51 64
30. R.I. Mesholam, P.J. Moberg, R.N. Mahr, and R.L. Doty Olfaction in neurodegenerative disease: a meta-analysis of olfactory functioning in Alzheimer's and Parkinson's diseases Arch. Neurol. 55 1998 84 90
31. F. Miragall, D. Krause, U. de Vries, and R. Dermietzel Expression of the tight junction protein ZO-1 in the olfactory system: presence of ZO-1 on olfactory sensory neurons and glial cells J. Comp. Neurol. 341 1994 433 448
32. J. Miu, A.J. Mitchell, M. Müller, S.L. Carter, P.M. Manders, J.A. McQuillan, B.M. Saunders, H.J. Ball, B. Lu, I.L. Campbell, and N.H. Hunt Chemokine gene expression during fatal murine cerebral malaria and protection due to CXCR3 deficiency J. Immunol. 180 2008 1217 1230
33. M. Miyakoda, D. Kimura, M. Yuda, Y. Chinzei, Y. Shibata, K. Honma, and K. Yui Malaria-specific and nonspecific activation of CD8+ T cells during blood stage of Plasmodium berghei infection J. Immunol. 181 2008 1420 1428
34. Y. Mori, M. Umeda, M. Fukunaga, K. Ogasawara, and Y. Yoshioka MR contrast in mouse lymph nodes with subcutaneous administration of iron oxide particles: size dependency Magn. Reson. Med. Sci. 10 2011 219 227
35. T.L. Murphy, R. Tussiwand, and K.M. Murphy Specificity through cooperation: BATF-IRF interactions control immune-regulatory networks Nat. Rev. Immunol. 13 2013 499 509
36. A. Nacer, A. Movila, K. Baer, S.A. Mikolajczak, S.H. Kappe, and U. Frevert Neuroimmunological blood brain barrier opening in experimental cerebral malaria PLoS Pathog. 8 2012 e1002982
37. M.G. Netea, B.J. Kullberg, and J.W. Van der Meer Circulating cytokines as mediators of fever Clin. Infect. Dis. 31 Suppl 5 2000 S178 S184
38. S. Noor, and E.H. Wilson Role of C-C chemokine receptor type 7 and its ligands during neuroinflammation J. Neuroinflammation 9 2012 77
39. S. Noor, A.S. Habashy, J.P. Nance, R.T. Clark, K. Nemati, M.J. Carson, and E.H. Wilson CCR7-dependent immunity during acute Toxoplasma gondii infection Infect. Immun. 78 2010 2257 2263
40. T.L. Perry, P. Pandey, J.M. Grant, and K.C. Kain Severe atovaquone-resistant Plasmodium falciparum malaria in a Canadian traveller returned from the Indian subcontinent Open Med. 3 2009 e10 e16
41. G.C. Petzold, D.F. Albeanu, T.F. Sato, and V.N. Murthy Coupling of neural activity to blood flow in olfactory glomeruli is mediated by astrocytic pathways Neuron 58 2008 897 910
42. L. Piva, P. Tetlak, C. Claser, K. Karjalainen, L. Renia, and C. Ruedl Cutting edge: Clec9A+ dendritic cells mediate the development of experimental cerebral malaria J. Immunol. 189 2012 1128 1132
43. A. Rappert, K. Biber, C. Nolte, M. Lipp, A. Schubel, B. Lu, N.P. Gerard, C. Gerard, H.W. Boddeke, and H. Kettenmann Secondary lymphoid tissue chemokine (CCL21) activates CXCR3 to trigger a Cl- current and chemotaxis in murine microglia J. Immunol. 168 2002 3221 3226
44. M. Sawada, N. Kaneko, H. Inada, H. Wake, Y. Kato, Y. Yanagawa, K. Kobayashi, T. Nemoto, J. Nabekura, and K. Sawamoto Sensory input regulates spatial and subtype-specific patterns of neuronal turnover in the adult olfactory bulb J. Neurosci. 31 2011 11587 11596
45. R.D. Strous, and Y. Shoenfeld To smell the immune system: olfaction, autoimmunity and brain involvement Autoimmun. Rev. 6 2006 54 60
46. T. Tamura, K. Kimura, M. Yuda, and K. Yui Prevention of experimental cerebral malaria by Flt3 ligand during infection with Plasmodium berghei ANKA Infect. Immun. 79 2011 3947 3956
47. T.E. Taylor, W.J. Fu, R.A. Carr, R.O. Whitten, J.S. Mueller, N.G. Fosiko, S. Lewallen, N.G. Liomba, and M.E. Molyneux Differentiating the pathologies of cerebral malaria by postmortem parasite counts Nat. Med. 10 2004 143 145
48. P.E. Van den Steen, K. Deroost, I. Van Aelst, N. Geurts, E. Martens, S. Struyf, C.Q. Nie, D.S. Hansen, P. Matthys, J. Van Damme, and G. Opdenakker CXCR3 determines strain susceptibility to murine cerebral malaria by mediating T lymphocyte migration toward IFN-gamma-induced chemokines Eur. J. Immunol. 38 2008 1082 1095
49. H.R. van Weering, A.P. de Jong, A.H. de Haas, K.P. Biber, and H.W. Boddeke CCL21-induced calcium transients and proliferation in primary mouse astrocytes: CXCR3-dependent and independent responses Brain Behav. Immun. 24 2010 768 775
50. H. Wake, A.J. Moorhouse, S. Jinno, S. Kohsaka, and J. Nabekura Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals J. Neurosci. 29 2009 3974 3980
51. J. Wang, H. You, J.F. Liu, D.F. Ni, Z.X. Zhang, and J. Guan Association of olfactory bulb volume and olfactory sulcus depth with olfactory function in patients with Parkinson disease AJNR Am. J. Neuroradiol. 32 2011 677 681
52. M.C. Whitman, W. Fan, L. Rela, D.J. Rodriguez-Gil, and C.A. Greer Blood vessels form a migratory scaffold in the rostral migratory stream J. Comp. Neurol. 516 2009 94 104
53. E.H. Wilson, T.H. Harris, P. Mrass, B. John, E.D. Tait, G.F. Wu, M. Pepper, E.J. Wherry, F. Dzierzinski, and D. Roos et al. Behavior of parasite-specific effector CD8+ T cells in the brain and visualization of a kinesis-associated system of reticular fibers Immunity 30 2009 300 311
54. M. Yang, and J.N. Crawley Simple behavioral assessment of mouse olfaction Curr. Protoc. Neurosci. Chapter 8 2009 Unit 8 24
55. H. Zhao, A. Konishi, Y. Fujita, M. Yagi, K. Ohata, T. Aoshi, S. Itagaki, S. Sato, H. Narita, and N.H. Abdelgelil et al. Lipocalin 2 bolsters innate and adaptive immune responses to blood-stage malaria infection by reinforcing host iron metabolism Cell Host Microbe 12 2012 705 716