Activated Brain Endothelial Cells Cross-Present Malaria Antigen

PLoS Pathogens

Volumn 11, Issue 6, 2015, Pages

  Howland, Shanshan W ^a   Poh, Chek Meng ^a,b   Rénia, Laurent ^a,b  

^a AGENCY FOR SCIENCE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD31 ANTIGEN; CD45 ANTIGEN; GAMMA INTERFERON; LACTACYSTIN; LYMPHOTOXIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MALARIA ANTIGEN; POLYCLONAL ANTIBODY; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; PARASITE ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; BRAIN CAPILLARY ENDOTHELIAL CELL; BRAIN MALARIA; CD8+ T LYMPHOCYTE; CELL INTERACTION; CELL KILLING; CELL MATURATION; CONTROLLED STUDY; CROSS PRESENTATION; FLOW CYTOMETRY; FLUORESCENCE IMAGING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MEROZOITE; MOUSE; NONHUMAN; OLFACTORY BULB; PHAGOCYTOSIS; PLASMODIUM BERGHEI; ANIMAL; BRAIN; C57BL MOUSE; CELL LINE; CEREBRAL MALARIA; DISEASE MODEL; ENDOTHELIUM CELL; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; PARASITOLOGY;

MURINAE; MUS; PLASMODIUM FALCIPARUM;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, PROTOZOAN; BRAIN; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CROSS-PRIMING; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MALARIA, CEREBRAL; MICE; MICE, INBRED C57BL;

EID: 84936743898     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004963     Document Type: Article

References (60)

1. World Health Organization (2013) World Malaria Report: 2013. France: WHO Press.
2. Milner DA, Jr.Whitten RO, Kamiza S, Carr R, Liomba G, et al. (2014) The systemic pathology of cerebral malaria in African children. Front Cell Infect Microbiol 4: 104. doi: 10.3389/fcimb.2014.00104 25191643
3. Craig AG, Grau GE, Janse C, Kazura JW, Milner D, et al. (2012) The role of animal models for research on severe malaria. PLoS Pathog 8: e1002401. doi: 10.1371/journal.ppat.1002401 22319438
4. Yanez DM, Manning DD, Cooley AJ, Weidanz WP, van der Heyde HC, (1996) Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria. J Immunol 157: 1620–1624. 8759747
5. 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. 12444144
6. Nitcheu J, Bonduelle O, Combadiere C, Tefit M, Seilhean D, et al. (2003) Perforin-dependent brain-infiltrating cytotoxic CD8+ T lymphocytes mediate experimental cerebral malaria pathogenesis. J Immunol 170: 2221–2228. 12574396
7. Yanez DM, Batchelder J, van der Heyde HC, Manning DD, Weidanz WP, (1999) Gamma delta T-cell function in pathogenesis of cerebral malaria in mice infected with Plasmodium berghei ANKA. Infect Immun 67: 446–448. 9864254
8. Hansen DS, Bernard NJ, Nie CQ, Schofield L, (2007) NK cells stimulate recruitment of CXCR3+ T cells to the brain during Plasmodium berghei-mediated cerebral malaria. J Immunol 178: 5779–5788. 17442962
9. Hansen DS, Siomos MA, Buckingham L, Scalzo AA, Schofield L, (2003) Regulation of murine cerebral malaria pathogenesis by CD1d-restricted NKT cells and the natural killer complex. Immunity 18: 391–402. 12648456
10. Chen L, Zhang Z, Sendo F, (2000) Neutrophils play a critical role in the pathogenesis of experimental cerebral malaria. Clin Exp Immunol 120: 125–133. 10759773
11. Pai S, Qin J, Cavanagh L, Mitchell A, El-Assaad F, et al. (2014) Real-time imaging reveals the dynamics of leukocyte behaviour during experimental cerebral malaria pathogenesis. PLoS Pathog 10: e1004236. doi: 10.1371/journal.ppat.1004236 25033406
12. Medana IM, Hunt NH, Chan-Ling T, (1997) Early activation of microglia in the pathogenesis of fatal murine cerebral malaria. Glia 19: 91–103. 9034826
13. Lundie RJ, de Koning-Ward TF, Davey GM, Nie CQ, Hansen DS, et al. (2008) Blood-stage Plasmodium infection induces CD8+ T lymphocytes to parasite-expressed antigens, largely regulated by CD8alpha+ dendritic cells. Proc Natl Acad Sci USA 105: 14509–14514. doi: 10.1073/pnas.0806727105 18799734
14. Piva L, Tetlak P, Claser C, Karjalainen K, Renia L, et al. (2012) Cutting edge: Clec9A+ dendritic cells mediate the development of experimental cerebral malaria. J Immunol 189: 1128–1132. doi: 10.4049/jimmunol.1201171 22732587
15. Belnoue E, Potter SM, Rosa DS, Mauduit M, Gruner AC, et al. (2008) Control of pathogenic CD8+ T cell migration to the brain by IFN-gamma during experimental cerebral malaria. Parasite Immunol 30: 544–553. doi: 10.1111/j.1365-3024.2008.01053.x 18665903
16. Villegas-Mendez A, Greig R, Shaw TN, de Souza JB, Gwyer Findlay E, et al. (2012) IFN-gamma-producing CD4+ T cells promote experimental cerebral malaria by modulating CD8+ T cell accumulation within the brain. J Immunol 189: 968–979. doi: 10.4049/jimmunol.1200688 22723523
17. Haque A, Best SE, Unosson K, Amante FH, de LF, et al. (2011) Granzyme B expression by CD8+ T cells is required for the development of experimental cerebral malaria. J Immunol 186: 6148–6156. doi: 10.4049/jimmunol.1003955 21525386
18. Lau LS, Fernandez Ruiz D, Davey GM, de Koning-Ward TF, Papenfuss AT, et al. (2011) Blood-stage Plasmodium berghei infection generates a potent, specific CD8+ T-cell response despite residence largely in cells lacking MHC I processing machinery. J Infect Dis 204: 1989–1996. doi: 10.1093/infdis/jir656 21998471
19. Howland SW, Poh CM, Gun SY, Claser C, Malleret B, et al. (2013) Brain microvessel cross-presentation is a hallmark of experimental cerebral malaria. EMBO Mol Med 5: 916–931. doi: 10.1002/emmm.201202273 23681698
20. Lau LS, Fernandez-Ruiz D, Mollard V, Sturm A, Neller MA, et al. (2014) CD8+ T cells from a novel T cell receptor transgenic mouse induce liver-stage immunity that can be boosted by blood-stage infection in rodent malaria. PLoS Pathog 10: e1004135. doi: 10.1371/journal.ppat.1004135 24854165
21. Poh CM, Howland SW, Grotenbreg GM, Renia L, (2014) Damage to the blood-brain barrier during experimental cerebral malaria results from synergistic effects of CD8+ T cells with different specificities. Infect Immun 82: 4854–4864. doi: 10.1128/IAI.02180-14 25156726
22. Amani V, Vigario AM, Belnoue E, Marussig M, Fonseca L, et al. (2000) Involvement of IFN-gamma receptor-medicated signaling in pathology and anti-malarial immunity induced by Plasmodium berghei infection. Eur J Immunol 30: 1646–1655. 10898501
23. Engwerda CR, (2002) Locally Up-regulated Lymphotoxin alpha, Not Systemic Tumor Necrosis Factor alpha, Is the Principle Mediator of Murine Cerebral Malaria. J Exp Med 195: 1371–1377. 12021316
24. Jarry U, Jeannin P, Pineau L, Donnou S, Delneste Y, et al. (2013) Efficiently stimulated adult microglia cross-prime naive CD8+ T cells injected in the brain. Eur J Immunol 43: 1173–1184. doi: 10.1002/eji.201243040 23529826
25. Perriere N, Demeuse P, Garcia E, Regina A, Debray M, et al. (2005) Puromycin-based purification of rat brain capillary endothelial cell cultures. Effect on the expression of blood-brain barrier-specific properties. J Neurochem 93: 279–289. 15816851
26. Wheway J, Obeid S, Couraud PO, Combes V, Grau GE, (2013) The brain microvascular endothelium supports T cell proliferation and has potential for alloantigen presentation. PLoS One 8: e52586. doi: 10.1371/journal.pone.0052586 23320074
27. Razakandrainibe R, Pelleau S, Grau GE, Jambou R, (2012) Antigen presentation by endothelial cells: what role in the pathophysiology of malaria? Trends Parasitol 28: 151–160. doi: 10.1016/j.pt.2012.01.004 22365903
28. Zhao H, Aoshi T, Kawai S, Mori Y, Konishi A, et al. (2014) Olfactory plays a key role in spatiotemporal pathogenesis of cerebral malaria. Cell Host Microbe 15: 551–563. doi: 10.1016/j.chom.2014.04.008 24832450
29. Van Amersfoort ES, Van Strijp JA, (1994) Evaluation of a flow cytometric fluorescence quenching assay of phagocytosis of sensitized sheep erythrocytes by polymorphonuclear leukocytes. Cytometry 17: 294–301. 7875036
30. Hill DL, Eriksson EM, Carmagnac AB, Wilson DW, Cowman AF, et al. (2012) Efficient measurement of opsonising antibodies to Plasmodium falciparum merozoites. PLoS One 7: e51692. doi: 10.1371/journal.pone.0051692 23300556
31. Mai J, Virtue A, Shen J, Wang H, Yang XF, (2013) An evolving new paradigm: endothelial cells—conditional innate immune cells. J Hematol Oncol 6: 61. doi: 10.1186/1756-8722-6-61 23965413
32. Jambou R, Combes V, Jambou MJ, Weksler BB, Couraud PO, et al. (2010) Plasmodium falciparum adhesion on human brain microvascular endothelial cells involves transmigration-like cup formation and induces opening of intercellular junctions. PLoS Pathog 6: e1001021. doi: 10.1371/journal.ppat.1001021 20686652
33. Balabanov R, Beaumont T, Dore-Duffy P, (1999) Role of central nervous system microvascular pericytes in activation of antigen-primed splenic T-lymphocytes. J Neurosci Res 55: 578–587. 10082080
34. Potter S, Chan-Ling T, Ball HJ, Mansour H, Mitchell A, et al. (2006) Perforin mediated apoptosis of cerebral microvascular endothelial cells during experimental cerebral malaria. Int J Parasitol 36: 485–496. 16500656
35. Hempel C, Hyttel P, Kurtzhals JA, (2014) Endothelial glycocalyx on brain endothelial cells is lost in experimental cerebral malaria. J Cereb Blood Flow Metab 34: 1107–1110. doi: 10.1038/jcbfm.2014.79 24756075
36. Lackner P, Burger C, Pfaller K, Heussler V, Helbok R, et al. (2007) Apoptosis in experimental cerebral malaria: spatial profile of cleaved caspase-3 and ultrastructural alterations in different disease stages. Neuropathol Appl Neurobiol 33: 560–571. 17442059
37. Nacer A, Movila A, Baer K, Mikolajczak SA, Kappe SH, et al. (2012) Neuroimmunological blood brain barrier opening in experimental cerebral malaria. PLoS Pathog 8: e1002982. doi: 10.1371/journal.ppat.1002982 23133375
38. Saric T, Chang SC, Hattori A, York IA, Markant S, et al. (2002) An IFN-gamma-induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides. Nat Immunol 3: 1169–1176. 12436109
39. Nacer A, Movila A, Sohet F, Girgis NM, Gundra UM, et al. (2014) Experimental cerebral malaria pathogenesis—hemodynamics at the blood brain barrier. PLoS Pathog 10: e1004528. doi: 10.1371/journal.ppat.1004528 25474413
40. Prakash MD, Munoz MA, Jain R, Tong PL, Koskinen A, et al. (2014) Granzyme B promotes cytotoxic lymphocyte transmigration via basement membrane remodeling. Immunity 41: 960–972. doi: 10.1016/j.immuni.2014.11.012 25526309
41. Galea I, Bernardes-Silva M, Forse PA, van Rooijen N, Liblau RS, et al. (2007) An antigen-specific pathway for CD8 T cells across the blood-brain barrier. J Exp Med 204: 2023–2030. 17682068
42. Suidan GL, McDole JR, Chen Y, Pirko I, Johnson AJ, (2008) Induction of blood brain barrier tight junction protein alterations by CD8 T cells. PLoS One 3: e3037. doi: 10.1371/journal.pone.0003037 18725947
43. Johnson HL, Willenbring RC, Jin F, Manhart WA, LaFrance SJ, et al. (2014) Perforin competent CD8 T cells are sufficient to cause immune-mediated blood-brain barrier disruption. PLoS One 9: e111401. doi: 10.1371/journal.pone.0111401 25337791
44. Van den Steen PE, Deroost K, Van Aelst I, Geurts N, Martens E, et al. (2008) CXCR3 determines strain susceptibility to murine cerebral malaria by mediating T lymphocyte migration toward IFN-gamma-induced chemokines. Eur J Immunol 38: 1082–1095. doi: 10.1002/eji.200737906 18383042
45. Amante FH, Haque A, Stanley AC, Rivera Fde L, Randall LM, et al. (2010) Immune-mediated mechanisms of parasite tissue sequestration during experimental cerebral malaria. J Immunol 185: 3632–3642. doi: 10.4049/jimmunol.1000944 20720206
46. Claser C, Malleret B, Gun SY, Wong AY, Chang ZW, et al. (2011) CD8+ T cells and IFN-gamma mediate the time-dependent accumulation of infected red blood cells in deep organs during experimental cerebral malaria. PLoS One 6: e18720. doi: 10.1371/journal.pone.0018720 21494565
47. Schroder K, Hertzog PJ, Ravasi T, Hume DA, (2004) Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75: 163–189. 14525967
48. Lovegrove FE, Gharib SA, Patel SN, Hawkes CA, Kain KC, et al. (2007) Expression microarray analysis implicates apoptosis and interferon-responsive mechanisms in susceptibility to experimental cerebral malaria. Am J Pathol 171: 1894–1903. 17991715
49. Smith JD, Craig AG, Kriek N, Hudson-Taylor D, Kyes S, et al. (2000) Identification of a Plasmodium falciparum intercellular adhesion molecule-1 binding domain: a parasite adhesion trait implicated in cerebral malaria. Proc Natl Acad Sci USA 97: 1766–1771. 10677532
50. El-Assaad F, Wheway J, Mitchell AJ, Lou J, Hunt NH, et al. (2013) Cytoadherence of Plasmodium berghei-infected red blood cells to murine brain and lung microvascular endothelial cells in vitro. Infect Immun 81: 3984–3991. doi: 10.1128/IAI.00428-13 23940206
51. De Togni P, Goellner J, Ruddle NH, Streeter PR, Fick A, et al. (1994) Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science 264: 703–707. 8171322
52. Wu Q, Wang Y, Wang J, Hedgeman EO, Browning JL, et al. (1999) The requirement of membrane lymphotoxin for the presence of dendritic cells in lymphoid tissues. J Exp Med 190: 629–638. 10477548
53. Bagai R, Valujskikh A, Canaday DH, Bailey E, Lalli PN, et al. (2005) Mouse endothelial cells cross-present lymphocyte-derived antigen on class I MHC via a TAP1- and proteasome-dependent pathway. J Immunol 174: 7711–7715. 15944272
54. Chapman LM, Aggrey AA, Field DJ, Srivastava K, Ture S, et al. (2012) Platelets present antigen in the context of MHC class I. J Immunol 189: 916–923. doi: 10.4049/jimmunol.1200580 22706078
55. Couper KN, Barnes T, Hafalla JC, Combes V, Ryffel B, et al. (2010) Parasite-derived plasma microparticles contribute significantly to malaria infection-induced inflammation through potent macrophage stimulation. PLoS Pathog 6: e1000744. doi: 10.1371/journal.ppat.1000744 20126448
56. Mantel PY, Hoang AN, Goldowitz I, Potashnikova D, Hamza B, et al. (2013) Malaria-infected erythrocyte-derived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host Microbe 13: 521–534. doi: 10.1016/j.chom.2013.04.009 23684304
57. Lu C, Pelech S, Zhang H, Bond J, Spach K, et al. (2008) Pertussis toxin induces angiogenesis in brain microvascular endothelial cells. J Neurosci Res 86: 2624–2640. doi: 10.1002/jnr.21716 18500752
58. Boyle MJ, Wilson DW, Richards JS, Riglar DT, Tetteh KK, et al. (2010) Isolation of viable Plasmodium falciparum merozoites to define erythrocyte invasion events and advance vaccine and drug development. Proc Natl Acad Sci USA 107: 14378–14383. doi: 10.1073/pnas.1009198107 20660744
59. Weksler BB, Subileau EA, Perriere N, Charneau P, Holloway K, et al. (2005) Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J 19: 1872–1874. 16141364
60. Malleret B, Claser C, Ong AS, Suwanarusk R, Sriprawat K, et al. (2011) A rapid and robust tri-color flow cytometry assay for monitoring malaria parasite development. Scientific reports 1: 118. doi: 10.1038/srep00118 22355635