Genetic analysis of cerebral malaria in the mouse model infected with Plasmodium berghei

Torre, Sabrina; Langlais, David; Gros, Philippe

doi:10.1007/s00335-018-9752-9

Published: 19 June 2018

Genetic analysis of cerebral malaria in the mouse model infected with Plasmodium berghei

Sabrina Torre¹,
David Langlais^1,2 &
Philippe Gros^1,3

Mammalian Genome volume 29, pages 488–506 (2018)Cite this article

1098 Accesses
9 Citations
4 Altmetric
Metrics details

Abstract

Malaria is a common and sometimes fatal disease caused by infection with Plasmodium parasites. Cerebral malaria (CM) is a most severe complication of infection with Plasmodium falciparum parasites which features a complex immunopathology that includes a prominent neuroinflammation. The experimental mouse model of cerebral malaria (ECM) induced by infection with Plasmodium berghei ANKA has been used abundantly to study the role of single genes, proteins and pathways in the pathogenesis of CM, including a possible contribution to neuroinflammation. In this review, we discuss the Plasmodium berghei ANKA infection model to study human CM, and we provide a summary of all host genetic effects (mapped loci, single genes) whose role in CM pathogenesis has been assessed in this model. Taken together, the reviewed studies document the many aspects of the immune system that are required for pathological inflammation in ECM, but also identify novel avenues for potential therapeutic intervention in CM and in diseases which feature neuroinflammation.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

Alferink J, Specht S, Arends H et al (2016) Cannabinoid receptor 2 modulates susceptibility to experimental cerebral malaria through a CCL17-dependent Mechanism. J Biol Chem 291:19517–19531. https://doi.org/10.1074/jbc.M116.746594
PubMed PubMed Central CAS Article Google Scholar
Amani V, Vigário AM, Belnoue E, et al (2000) Involvement of IFN-γ receptor-mediated signaling in pathology and anti-malarial immunity induced by Plasmodium berghei infection. Eur J Immunol 30:1646–1655
PubMed CAS Article Google Scholar
Amante FH, Haque A, Stanley AC et al (2010) Immune-mediated mechanisms of parasite tissue sequestration during experimental cerebral malaria. J Immunol 185:3632–3642. https://doi.org/10.4049/jimmunol.1000944
PubMed CAS Article Google Scholar
Baccarella A, Huang BW, Fontana MF, Kim CC (2014) Loss of Toll-like receptor 7 alters cytokine production and protects against experimental cerebral malaria. Malar J 13:1–8. https://doi.org/10.1186/1475-2875-13-354
CAS Article Google Scholar
Bagot S, Campino S, Penha-Gonçalves C et al (2002) Identification of two cerebral malaria resistance loci using an inbred wild-derived mouse strain. Proc Natl Acad Sci U S A 99:9919–9923. https://doi.org/10.1073/pnas.152215199
PubMed PubMed Central CAS Article Google Scholar
Bagot S, Nogueira F, Collette A et al (2004) Comparative study of brain CD8 + T cells induced by sporozoites and those induced by blood-stage Plasmodium berghei ANKA involved in the development of cerebral malaria. Infect Immun 72:2817–2826. https://doi.org/10.1128/IAI.72.5.2817
PubMed PubMed Central CAS Article Google Scholar
Ball EA, Sambo MR, Martins M et al (2013) IFNAR1 controls progression to cerebral malaria in children and CD8+ T Cell brain pathology in Plasmodium berghei-infected mice. J Immunol 190:5118–5127. https://doi.org/10.4049/jimmunol.1300114
PubMed CAS Article Google Scholar
Band G, Le QS, Jostins L et al (2013) Imputation-based meta-analysis of severe malaria in three african populations. PLoS Genet 9:e1003509. https://doi.org/10.1371/journal.pgen.1003509
PubMed PubMed Central CAS Article Google Scholar
Band G, Rockett KA, Spencer CCA et al (2015) A novel locus of resistance to severe malaria in a region of ancient balancing selection. Nature 526:253–257. https://doi.org/10.1038/nature15390
PubMed CAS Article Google Scholar
Barbosa MDFS., Nguyen QA, Tchernev VT et al (1996) Identification of the homologous beige and Chediak-Higashi syndrome genes. Nature 382:262–265. https://doi.org/10.1038/382262a0
PubMed PubMed Central CAS Article Google Scholar
Beghdadi W, Porcherie A, Schneider BS et al (2008) Inhibition of histamine-mediated signaling confers significant protection against severe malaria in mouse models of disease. J Exp Med 205:395–408. https://doi.org/10.1084/jem.20071548
PubMed PubMed Central CAS Article Google Scholar
Beghdadi W, Porcherie A, Schneider BS et al (2009) Histamine H3 receptor-mediated signaling protects mice from cerebral malaria. PLoS ONE 4:. https://doi.org/10.1371/journal.pone.0006004
Belnoue E, Kayibanda M, Vigario AM et al (2002) On the pathogenic role of brain-sequestered CD8+ T cells in experimental cerebral malaria. J Immunol 169:6369–6375. https://doi.org/10.4049/jimmunol.169.11.6369
PubMed CAS Article Google Scholar
Belnoue E, Costa F, Vigário A et al (2003a) Chemokine receptor CCR2 is not essential for the development of experimental cerebral malaria. Infect Immun 71:3648. https://doi.org/10.1128/IAI.71.6.3648
PubMed PubMed Central CAS Article Google Scholar
Belnoue E, Kayibanda M, Deschemin JC et al (2003b) CCR5 deficiency decreases susceptibility to experimental cerebral malaria. Blood 101:4253–4259. https://doi.org/10.1182/blood-2002-05-1493
PubMed CAS Article Google Scholar
Belnoue E, Potter SM, Rosa DS et al (2008) Control of pathogenic CD8 + T cell migration to the brain by IFN-γ during experimental cerebral malaria. Parasite Immunol 30:544–553. https://doi.org/10.1111/j.1365-3024.2008.01053.x
PubMed CAS Article Google Scholar
Berghout J, Min-Oo G, Tam M et al (2010) Identification of a novel cerebral malaria susceptibility locus (Berr5) on mouse chromosome 19. Genes Immun 11:310–318. https://doi.org/10.1038/gene.2009.79
PubMed CAS Article Google Scholar
Berghout J, Langlais D, Radovanovic I et al (2013) Irf8-regulated genomic responses drive pathological inflammation during cerebral malaria. PLoS Pathog 9:e1003491. https://doi.org/10.1371/journal.ppat.1003491
PubMed PubMed Central CAS Article Google Scholar
Betz RC, Petukhova L, Ripke S et al (2015) Genome-wide meta-analysis in alopecia areata resolves HLA associations and reveals two new susceptibility loci. Nat Commun 6:1–8. https://doi.org/10.1038/ncomms6966
CAS Article Google Scholar
Bongfen SE, Laroque A, Berghout J, Gros P (2009) Genetic and genomic analyses of host-pathogen interactions in malaria. Trends Parasitol 25:417–422
PubMed CAS Article Google Scholar
Bongfen SE, Rodrigue-Gervais IG, Berghout J et al (2012) An N-ethyl-N-nitrosourea (ENU)-induced dominant negative mutation in the JAK3 kinase protects against cerebral malaria. PLoS ONE 7:e31012. https://doi.org/10.1371/journal.pone.0031012
PubMed PubMed Central CAS Article Google Scholar
Bopp SER, Ramachandran V, Henson K et al (2010) Genome wide analysis of inbred mouse lines identifies a locus containing ppar-γ as contributing to enhanced malaria survival. PLoS ONE 5:e10903. https://doi.org/10.1371/journal.pone.0010903
PubMed PubMed Central CAS Article Google Scholar
Bopp SE, Rodrigo E, González-Páez GE et al (2013) Identification of the Plasmodium berghei resistance locus 9 linked to survival on chromosome 9. Malar J 12:316. https://doi.org/10.1186/1475-2875-12-316
PubMed PubMed Central CAS Article Google Scholar
Boubou MI, Collette A, Voegtlé D et al (1999) T cell response in malaria pathogenesis: Selective increase in T cells carrying the TCR V(β)8 during experimental cerebral malaria. Int Immunol 11:1553–1562. https://doi.org/10.1093/intimm/11.9.1553
PubMed CAS Article Google Scholar
Brant F, Miranda AS, Esper L et al (2014) Role of the aryl hydrocarbon receptor in the immune response profile and development of pathology during Plasmodium berghei Anka infection. Infect Immun 82:3127–3140. https://doi.org/10.1128/IAI.01733-14
PubMed PubMed Central CAS Article Google Scholar
Brant F, Miranda AS, Esper L et al (2016) Suppressor of cytokine signaling 2 modulates the immune response profile and development of experimental cerebral malaria. Brain Behav Immun 54:73–85. https://doi.org/10.1016/j.bbi.2016.01.002
PubMed CAS Article Google Scholar
Brockmeyer C, Paster W, Pepper D et al (2011) T cell receptor (TCR)-induced tyrosine phosphorylation dynamics identifies THEMIS as a new TCR signalosome component. J Biol Chem 286:7535–7547. https://doi.org/10.1074/jbc.M110.201236
PubMed CAS Article Google Scholar
Bullen DVR, Hansen DS, Siomos MAV et al (2003) The lack of suppressor of cytokine signalling-1 (SOCS1) protects mice from the development of cerebral malaria caused by Plasmodium berghei ANKA. Parasite Immunol 25:113–118. https://doi.org/10.1046/j.1365-3024.2003.00616.x
PubMed CAS Article Google Scholar
Caignard G, Eva MM, Van Bruggen R et al (2014) Mouse ENU mutagenesis to understand immunity to infection: methods, selected examples, and perspectives. Genes (Basel) 5:887–925
PubMed Central Article Google Scholar
Campanella GSV, Tager AM, El Khoury JK et al (2008) Chemokine receptor CXCR3 and its ligands CXCL9 and CXCL10 are required for the development of murine cerebral malaria. Proc Natl Acad Sci U S A 105:4814–4819. https://doi.org/10.1073/pnas.0801544105
PubMed PubMed Central Article Google Scholar
Campino S, Bagot S, Bergman ML et al (2005) Genetic control of parasite clearance leads to resistance to Plasmodium berghei ANKA infection and confers immunity. Genes Immun 6:416–421. https://doi.org/10.1038/sj.gene.6364219
PubMed CAS Article Google Scholar
Candotti BF, Oakes SA, Johnston JA et al (1997) Structural and functional basis for JAK3-deficient severe combined immunodeficiency. Blood 90:3996–4003
PubMed CAS Google Scholar
Chang WL, Li J, Sun G et al (2003) P-selectin contributes to severe experimental malaria but is not required for leukocyte adhesion to brain microvasculature. Infect Immun 71:1911–1918. https://doi.org/10.1128/IAI.71.4.1911-1918.2003
PubMed PubMed Central CAS Article Google Scholar
Clark IA, Budd AC, Alleva LM, Cowden WB (2006) Human malarial disease: a consequence of inflammatory cytokine release. Malar J 5:85. https://doi.org/10.1186/1475-2875-5-85
PubMed PubMed Central CAS Article Google Scholar
Claser C, Malleret B, Gun SY et al (2011) CD8 + T cells and IFN-γ mediate the time-dependent accumulation of infected red blood cells in deep organs during experimental cerebral malaria. PLoS ONE 6:e18720. https://doi.org/10.1371/journal.pone.0018720
PubMed PubMed Central CAS Article Google Scholar
Coban C, Ishii KJ, Uematsu S et al (2007) Pathological role of Toll-like receptor signaling in cerebral malaria. Int Immunol 19:67–79. https://doi.org/10.1093/intimm/dxl123
PubMed CAS Article Google Scholar
Combes V, Rosenkranz AR, Redard M et al (2004) Pathogenic role of P-selectin in experimental cerebral malaria: importance of the endothelial compartment. Am J Pathol 164:781–786. https://doi.org/10.1016/S0002-9440(10)63166-5
PubMed PubMed Central CAS Article Google Scholar
Combes V, Coltel N, Alibert M et al (2005) ABCA1 Gene Deletion Protects against Cerebral Malaria. Am J Pathol 166:295–302. https://doi.org/10.1016/S0002-9440(10)62253-5
PubMed PubMed Central CAS Article Google Scholar
Cowman AF, Crabb BS (2006) Invasion of red blood cells by malaria parasites. Cell 124:755–766
PubMed CAS Article Google Scholar
Cox FE (2010) History of the discovery of the malaria parasites and their vectors. Parasites Vectors 3:5
PubMed PubMed Central Article Google Scholar
Craig AG, Grau GE, Janse C et al (2012) The role of animal models for research on severe malaria. PLoS Pathog 8:e1002401. https://doi.org/10.1371/journal.ppat.1002401
PubMed PubMed Central CAS Article Google Scholar
Cunha-Rodrigues M, Portugal S, Febbraio M, Mota MM (2006) Infection by and protective immune responses against Plasmodium berghei ANKA are not affected in macrophage scavenger receptors A deficient mice. BMC Microbiol 6:1–5. https://doi.org/10.1186/1471-2180-6-73
CAS Article Google Scholar
Darley MM, Ramos TN, Wetsel RA, Barnum SR (2012) Deletion of carboxypeptidase N delays onset of experimental cerebral malaria. Parasite Immunol 34:444–447. https://doi.org/10.1111/j.1365-3024.2012.01376.x
PubMed PubMed Central CAS Article Google Scholar
De Souza J, Riley E (2002) Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis. Microbes Infect 4:291–300
PubMed Article Google Scholar
De Souza J, Hafalla J, Riley E, Couper K (2010) Cerebral malaria: Why experimental murine models are required to understand the pathogenesis of disease. Parasitology 137:755–772
PubMed Article Google Scholar
Dondorp AM, Kager PA, Vreeken J, White NJ (2000) Abnormal blood flow and red blood cell deformability in severe malaria. Parasitol Today 16:228–232. https://doi.org/10.1016/S0169-4758(00)01666-5
PubMed CAS Article Google Scholar
Dostert C, Guarda G, Romero JF et al (2009) Malarial hemozoin is a Nalp3 inflammasome activating danger signal. PLoS One 4:1–10. https://doi.org/10.1371/journal.pone.0006510
CAS Article Google Scholar
Driss A, Hibbert JM, Wilson NO et al (2011) Genetic polymorphisms linked to susceptibility to malaria. Malar J 10:271. https://doi.org/10.1186/1475-2875-10-271
PubMed PubMed Central Article Google Scholar
Dubois PCA, Trynka G, Franke L et al (2010) Multiple common variants for celiac disease influencing immune gene expression. Nat Genet 42:295–302. https://doi.org/10.1038/ng.543
PubMed PubMed Central CAS Article Google Scholar
Dunst J, Kamena F, Matuschewski K (2017) Cytokines and Chemokines in Cerebral Malaria Pathogenesis. Front Cell Infect Microbiol 7:. https://doi.org/10.3389/fcimb.2017.00324
Edwards CL, Best SE, Gun SY et al (2015) Spatiotemporal requirements for IRF7 in mediating type I IFN-dependent susceptibility to blood-stage Plasmodium infection. Eur J Immunol 45:130–141. https://doi.org/10.1002/eji.201444824
PubMed CAS Article Google Scholar
El-Assaad F, Wheway J, Mitchell AJ 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. https://doi.org/10.1128/IAI.00428-13
PubMed PubMed Central CAS Article Google Scholar
El-Assaad F, Combes V, Grau GE (2014) Experimental models of microvascular immunopathology: the example of cerebral malaria. J Neuroinfect Dis 2:92–94. https://doi.org/10.14440/jbm.2015.54.A
Article Google Scholar
Ellinghaus D, Ellinghaus E, Nair RP et al (2012) Combined analysis of genome-wide association studies for Crohn disease and psoriasis identifies seven shared susceptibility loci. Am J Hum Genet 90:636–647. https://doi.org/10.1016/j.ajhg.2012.02.020
PubMed PubMed Central CAS Article Google Scholar
Elphinstone RE, Besla R, Shikatani EA et al (2017) S-Nitrosoglutathione reductase deficiency confers improved survival and neurological outcome in experimental cerebral malaria. Infect Immun 85:1–12. https://doi.org/10.1128/IAI.00371-17
Article Google Scholar
Engelhardt KR, McGhee S, Winkler S et al (2009) Large deletions and point mutations involving the dedicator of cytokinesis 8 (DOCK8) in the autosomal-recessive form of hyper-IgE syndrome. J Allergy Clin Immunol 124:. https://doi.org/10.1016/j.jaci.2009.10.038
Engwerda CR, Mynott TL, Sawhney S et al (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. https://doi.org/10.1084/jem.20020128
PubMed PubMed Central CAS Article Google Scholar
Engwerda C, Belnoue E, Gruner AC, Renia L (2005) Experimental models of cerebral malaria. Curr Top Microbiol Immunol 297:103–143
PubMed CAS Google Scholar
Everitt AR, Clare S, McDonald JU et al (2013) Defining the range of pathogens susceptible to ifitm3 restriction using a knockout mouse model. PLoS One 8:1–12. https://doi.org/10.1371/journal.pone.0080723
Article Google Scholar
Fauconnier M, Bourigault M-L, Meme S et al (2011) Protein kinase C-Theta is required for development of experimental cerebral malaria. Am J Pathol 178:212–221. https://doi.org/10.1016/j.ajpath.2010.11.008
PubMed PubMed Central CAS Article Google Scholar
Fauconnier M, Palomo J, Bourigault M-L et al (2012) IL-12R 2 Is essential for the development of experimental cerebral malaria. J Immunol 188:1905–1914. https://doi.org/10.4049/jimmunol.1101978
PubMed CAS Article Google Scholar
Favre N, Da Laperousaz C, Ryffel B et al (1999a) Role of ICAM-1 (CD54) in the development of murine cerebral malaria. Microbes Infect 1:961–968. https://doi.org/10.1016/S1286-4579(99)80513-9
PubMed CAS Article Google Scholar
Favre N, Ryffel B, Rudin W (1999b) The development of murine cerebral malaria does not require nitric oxide production. Parasitology 118:135–138. https://doi.org/10.1017/S0031182098003606
PubMed CAS Article Google Scholar
Fodil N, Moradin N, Leung V et al (2017) CCDC88B is required for pathogenesis of inflammatory bowel disease. Nat Commun 8:1–12. https://doi.org/10.1038/s41467-017-01381-y
CAS Article Google Scholar
Frank J, Pignata C, Panteleyev AA et al (1999) Exposing the human nude phenotype. Nature 398:473–474. https://doi.org/10.1038/18997
PubMed CAS Article Google Scholar
Franke-Fayard B, Janse CJ, Cunha-Rodrigues M et al (2005) From the cover: murine malaria parasite sequestration: CD36 is the major receptor, but cerebral pathology is unlinked to sequestration. Proc Natl Acad Sci 102:11468–11473. https://doi.org/10.1073/pnas.0503386102
PubMed CAS Article Google Scholar
Gazzinelli RT, Kalantari P, Fitzgerald KA, Golenbock DT (2014) Innate sensing of malaria parasites. Nat Rev Immunol 14:744–757
PubMed CAS Article Google Scholar
Goldman FD, Ballas ZK, Schutte BC et al (1998) Defective p56lck expression in an Infant with SCID defective expression of p56lck in an infant with severe combined immunodeficiency. J Clin Invest 102:421–429. https://doi.org/10.1172/JCI3205
PubMed PubMed Central CAS Article Google Scholar
Gramaglia I, Sobolewski P, Meays D et al (2006) Low nitric oxide bioavailability contributes to the genesis of experimental cerebral malaria. Nat Med 12:1417–1422. https://doi.org/10.1038/nm1499
PubMed CAS Article Google Scholar
Griffith JW, O’Connor C, Bernard K et al (2007) Toll-like receptor modulation of murine cerebral malaria is dependent on the genetic background of the host. J Infect Dis 196:1553–1564. https://doi.org/10.1086/522865
PubMed CAS Article Google Scholar
Guo J, McQuillan JA, Yau B et al (2015) IRGM3 contributes to immunopathology and is required for differentiation of antigen-specific effector CD8+ T cells in experimental cerebral malaria. Infect Immun 83:1406–1417. https://doi.org/10.1128/IAI.02701-14
PubMed PubMed Central CAS Article Google Scholar
Ham H, Huynh W, Schoon R et al (2015) HkRP3 Is a microtubule-binding protein regulating lytic granule clustering and NK cell killing. J Immunol 194:3984–3996. https://doi.org/10.4049/jimmunol.1402897
PubMed PubMed Central CAS Article Google Scholar
Hansen DS (2012) Inflammatory responses associated with the induction of cerebral malaria: lessons from experimental murine models. PLoS Pathog 8:e1003045. https://doi.org/10.1371/journal.ppat.1003045
PubMed PubMed Central CAS Article Google Scholar
Hansen DS, Siomos MA, Buckingham L et al (2003) Regulation of murine cerebral malaria pathogenesis by CD1d-restricted NKT cells and the natural killer complex. Immunity 18:391–402. https://doi.org/10.1016/S1074-7613(03)00052-9
PubMed CAS Article Google Scholar
Haque A, Best SE, Unosson K et al (2011) Granzyme B Expression by CD8 + T Cells Is Required for the Development of Experimental Cerebral Malaria. J Immunol 186:6148–6156. https://doi.org/10.4049/jimmunol.1003955
PubMed CAS Article Google Scholar
Hearn J, Rayment N, Landon DN et al (2000) Immunopathology of cerebral malaria: Morphological evidence of parasite sequestration in murine brain microvasculature. Infect Immun 68:5364–5376. https://doi.org/10.1128/IAI.68.9.5364-5376.2000
PubMed PubMed Central CAS Article Google Scholar
Hempel C, Combes V, Hunt NH et al (2011) CNS hypoxia is more pronounced in murine cerebral than noncerebral malaria and is reversed by erythropoietin. Am J Pathol 179:1939–1950. https://doi.org/10.1016/j.ajpath.2011.06.027
PubMed PubMed Central CAS Article Google Scholar
Herbas MS, Okazaki M, Terao E et al (2010) a-Tocopherol transfer protein inhibition is effective in the prevention of cerebral malaria in mice 1–3. 200–207. https://doi.org/10.3945/ajcn.2009.28260.200
Hernandez-Valladares M, Rihet P, Iraqi FA (2014) Host susceptibility to malaria in human and mice: compatible approaches to identify potential resistant genes. Physiol Genomics 46:1–16. https://doi.org/10.1152/physiolgenomics.00044.2013
PubMed CAS Article Google Scholar
Hiller NL, Bhattacharjee S, Van Ooij C et al (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306:1934–1937. https://doi.org/10.1126/science.1102737
PubMed CAS Article Google Scholar
Hora R, Kapoor P, Thind KK, Mishra PC (2016) Cerebral malaria – clinical manifestations and pathogenesis. Metab Brain Dis 31:225–237. https://doi.org/10.1007/s11011-015-9787-5
PubMed CAS Article Google Scholar
Howland SW, Claser C, Poh CM et al (2015) Pathogenic CD8 + T cells in experimental cerebral malaria. Semin Immunopathol 37:221–231. https://doi.org/10.1007/s00281-015-0476-6
PubMed CAS Article Google Scholar
Hulden L, Hulden L, Hay S et al (2011) Activation of the hypnozoite: a part of Plasmodium vivax life cycle and survival. Malar J 10:90. https://doi.org/10.1186/1475-2875-10-90
PubMed PubMed Central Article Google Scholar
Hunt NH, Grau GE (2003a) Cytokines: Accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol 24:491–499. https://doi.org/10.1016/S1471-4906(03)00229-1
PubMed CAS Article Google Scholar
Hunt NH, Grau GE (2003b) Cytokines: Accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol 24:491–499
PubMed CAS Article Google Scholar
Hunt NH, Driussi C, Sai-Kiang L (2001) Haptoglobin and malaria. Redox Rep 6:389–392. https://doi.org/10.1179/135100001101536508
PubMed CAS Article Google Scholar
Hunt NH, Golenser J, Chan-Ling T et al (2006) Immunopathogenesis of cerebral malaria. Int J Parasitol 36:569–582
PubMed CAS Article Google Scholar
Ioannidis LJ, Nie CQ, Ly A et al (2016) Monocyte- and neutrophil-derived CXCL10 Impairs efficient control of blood-stage malaria infection and promotes severe disease. J Immunol 196:1227–1238. https://doi.org/10.4049/jimmunol.1501562
PubMed CAS Article Google Scholar
Ishida H, Matsuzaki-Moriya C, Imai T et al (2010) Development of experimental cerebral malaria is independent of IL-23 and IL-17. Biochem Biophys Res Commun 402:790–795. https://doi.org/10.1016/j.bbrc.2010.10.114
PubMed CAS Article Google Scholar
Ishikawa S, Uozumi N, Shiibashi T et al (2004) Short report: Lethal malaria in cytosolic phospholipase A2- and phospholipase A2IIA-deficient mice. Am J Trop Med Hyg 70:645–650
PubMed CAS Article Google Scholar
Jallow M, Teo YY, Small KS et al (2009) Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat Genet 41:657–665. https://doi.org/10.1038/ng.388
PubMed PubMed Central CAS Article Google Scholar
Jamison DT, Feachem RG, Makgoba MW et al (2006) Disease and Mortality in Sub-Saharan Africa. The International Bank for Reconstruction and Development/The World Bank, Washington (DC)
Google Scholar
Jostins L, Ripke S, Weersma RK et al (2012) Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491:119–124. https://doi.org/10.1038/nature11582
PubMed PubMed Central CAS Article Google Scholar
Kain KC, Yeh W-C, Liles WC et al (2010) Divergent Roles of IRAK4-Mediated Innate Immune Responses in Two Experimental Models of Severe Malaria. Am J Trop Med Hyg 83:69–74. https://doi.org/10.4269/ajtmh.2010.09-0753
PubMed PubMed Central CAS Article Google Scholar
Kassa FA, Van Den Ham K, Rainone A et al (2016) Absence of apolipoprotein e protects mice from cerebral malaria. Sci Rep 6:1–13. https://doi.org/10.1038/srep33615
CAS Article Google Scholar
Kennedy JM, Fodil N, Torre S et al (2014) CCDC88B is a novel regulator of maturation and effector functions of T cells during pathological inflammation. J Exp Med 211:2519–2535. https://doi.org/10.1084/jem.20140455
PubMed PubMed Central CAS Article Google Scholar
Kim H, Erdman LK, Lu Z et al (2014) Functional roles for C5a and C5aR but not C5L2 in the pathogenesis of human and experimental cerebral malaria. Infect Immun 82:371–379. https://doi.org/10.1128/IAI.01246-13
PubMed PubMed Central CAS Article Google Scholar
Kordes M, Matuschewski K, Hafalla JCR (2011) Caspase-1 activation of interleukin-1β (IL-1β) And IL-18 Is Dispensable for Induction of Experimental Cerebral Malaria. Infect Immun 79:3633–3641. https://doi.org/10.1128/IAI.05459-11
PubMed PubMed Central CAS Article Google Scholar
Kwiatkowski DP (2005) How malaria has affected the human genome and what human genetics can teach us about malaria. Am J Hum Genet 77:171–192. https://doi.org/10.1086/432519
PubMed PubMed Central CAS Article Google Scholar
Labbe K, Miu J, Yeretssian G et al (2010) Caspase-12 dampens the immune response to malaria independently of the inflammasome by targeting NF- B signaling. J Immunol 185:5495–5502. https://doi.org/10.4049/jimmunol.1002517
PubMed CAS Article Google Scholar
Lacerda-Queiroz N, Rodrigues DH, Vilela MC et al (2012) Platelet-activating factor receptor is essential for the development of experimental cerebral malaria. Ajpa 180:246–255. https://doi.org/10.1016/j.ajpath.2011.09.038
CAS Article Google Scholar
Lacerda-Queiroz N, Brant F, Rodrigues DH et al (2015) Phosphatidylinositol 3-kinase ? is required for the development of experimental cerebral malaria. PLoS ONE 10:1–13. https://doi.org/10.1371/journal.pone.0119633
CAS Article Google Scholar
Lambert JC, Ibrahim-Verbaas C, Harold D et al (2013) Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer’s disease. Nat Genet 45:1452–1458. https://doi.org/10.1038/ng.2802
PubMed PubMed Central CAS Article Google Scholar
Langhorne J, Buffet P, Galinski M et al (2011) The relevance of non-human primate and rodent malaria models for humans. Malar J 10:23
PubMed PubMed Central Article Google Scholar
Langlais D, Fodil N, Gros P (2017) Genetics of infectious and inflammatory diseases: overlapping discoveries from association and exome-sequencing studies. Annu Rev Immunol 35:1–30. https://doi.org/10.1146/annurev-immunol-051116-052442
PubMed CAS Article Google Scholar
Leitner WW, Bergmann-Leitner ES, Angov E (2010) Comparison of Plasmodium berghei challenge models for the evaluation of pre-erythrocytic malaria vaccines and their effect on perceived vaccine efficacy. Malar J 9:145. https://doi.org/10.1186/1475-2875-9-145
PubMed PubMed Central CAS Article Google Scholar
Lelliott PM, McMorran BJ, Foote SJ, Burgio G (2015) The influence of host genetics on erythrocytes and malaria infection: Is there therapeutic potential? Malar J 14:289
PubMed PubMed Central Article Google Scholar
Li J, Chang W-L, Sun G et al (2003) Intercellular adhesion molecule 1 is important for the development of severe experimental malaria but is not required for leukocyte adhesion in the brain. J Investig Med 51:128–140. https://doi.org/10.1136/jim-51-03-15
PubMed CAS Article Google Scholar
Liehl P, Zuzarte-Luís V, Chan J et al (2014) Host-cell sensors for Plasmodium activate innate immunity against liver-stage infection. Nat Med 20:47–53. https://doi.org/10.1038/nm.3424
PubMed CAS Article Google Scholar
Lindblade KA, Steinhardt L, Samuels A et al (2013) The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti Infect Ther 11:623–639. https://doi.org/10.1586/eri.13.45
PubMed CAS Article Google Scholar
Longley R, Smith C, Fortin A et al (2011) Host resistance to malaria: using mouse models to explore the host response. Mamm Genome 22:32–42. https://doi.org/10.1007/s00335-010-9302-6
PubMed CAS Article Google Scholar
Lou J, Lucas R, Grau GE (2001) Pathogenesis of cerebral malaria: Recent experimental data and possible applications for humans. Clin Microbiol Rev 14:810–820
PubMed PubMed Central CAS Article Google Scholar
Lu Z, Serghides L, Patel SN et al (2006) Disruption of JNK2 decreases the cytokine response to Plasmodium falciparum glycosylphosphatidylinositol in vitro and confers protection in a cerebral malaria model. J Immunol 177:6344–6352. https://doi.org/10.4049/jimmunol.177.9.6344
PubMed CAS Article Google Scholar
Lucas R, Juillard P, Decoster E et al (1997) Crucial role of tumor necrosis factor (TNF) receptor 2 and membrane-bound TNF in experimental cerebral malaria. Eur J Immunol 27:1719–1725. https://doi.org/10.1002/eji.1830270719
PubMed CAS Article Google Scholar
MacKintosh CL, Beeson JG, Marsh K (2004) Clinical features and pathogenesis of severe malaria. Trends Parasitol 20:597–603
PubMed CAS Article Google Scholar
Maglinao M, Klopfleisch R, Seeberger PH, Lepenies B (2013) The C-type lectin receptor DCIR is crucial for the development of experimental cerebral malaria. J Immunol 191:2551–2559. https://doi.org/10.4049/jimmunol.1203451
PubMed CAS Article Google Scholar
Maitland K (2006) Severe malaria: lessons learned from the management of critical illness in children. Trends Parasitol 22:457–462. https://doi.org/10.1016/j.pt.2006.07.006
PubMed CAS Article Google Scholar
Maitland K, Newton CRJC. (2005) Acidosis of severe falciparum malaria: Heading for a shock? Trends Parasitol 21:11–16
PubMed Article Google Scholar
Malaria Genomic Epidemiology Network (2014) Reappraisal of known malaria resistance loci in a large multicenter study. Nat Genet 46:1197–1204. https://doi.org/10.1038/ng.3107
PubMed Central CAS Article Google Scholar
Porcherie A, Mathieu C, Peronet R, et al (1894) Two monographs on malaria and the parasites of malarial fevers (translated from the first Italian edition by JH Thompson). New Sydenham Soc, London
Google Scholar
Mcmorran BJ, Marshall VM, Graaf C, De et al (2009) Platelets Kill Intraerythrocytic malarial parasites and mediate survival to infection. Science 323:797–800. https://doi.org/10.1126/science.1166296
PubMed CAS Article Google Scholar
Medana IM, Chaudhri G, Chan-Ling T, Hunt NH (2001) Central nervous system in cerebral malaria: “Innocent bystander” or active participant in the induction of immunopathology? Immunol. Cell Biol 79:101–120
CAS Google Scholar
Mells GF, Floyd JAB, Morley KI et al (2011) Genome-wide association study identifies 12 new susceptibility loci for primary biliary cirrhosis. Nat Genet 43:1164–1164. https://doi.org/10.1038/ng1111-1164b
CAS Article Google Scholar
Mestas J, Hughes CCW (2004) Of Mice and Not Men: Differences between Mouse and Human Immunology. J Immunol 172:2731–2738. https://doi.org/10.4049/jimmunol.172.5.2731
PubMed CAS Article Google Scholar
Miller LH, Baruch DI, Marsh K, Doumbo OK (2002) The pathogenic basis of malaria. Nature 415:673–679
PubMed CAS Article Google Scholar
Miller LH, Ackerman HC, Su XZ, Wellems TE (2013) Malaria biology and disease pathogenesis: insights for new treatments. Nat Med 19:156–167. https://doi.org/10.1038/nm.3073
PubMed PubMed Central CAS Article Google Scholar
Miller JL, Sack BK, Baldwin M et al (2014) Interferon-mediated innate immune responses against malaria parasite liver stages. Cell Rep 7:436–447. https://doi.org/10.1016/j.celrep.2014.03.018
PubMed CAS Article Google Scholar
Mishra SK, Newton CRJC. (2009) Diagnosis and management of the neurological complications of falciparum malaria. Nat Rev Neurol 5:189–198. https://doi.org/10.1038/nrneurol.2009.23
PubMed PubMed Central Article Google Scholar
Miu J, Muller MaJ M, et al (2008) Chemokine gene expression during fatal murine cerebral Malaria and protection due to CXCR3 deficiency. J Immunol 180:1217–1230. https://doi.org/10.4049/jimmunol.180.2.1217
PubMed CAS Article Google Scholar
Miu J, Ball HJ, Mellor AL, Hunt NH (2009) Effect of indoleamine dioxygenase-1 deficiency and kynurenine pathway inhibition on murine cerebral malaria. Int J Parasitol 39:363–370. https://doi.org/10.1016/j.ijpara.2008.10.005
PubMed CAS Article Google Scholar
Miyakoda M, Kimura D, Yuda M et al (2008) Malaria-specific and nonspecific activation of CD8 + T cells during blood stage of Plasmodium berghei infection. J Immunol 181:1420–1428. doi: 181/2/1420 [pii]
PubMed CAS Article Google Scholar
Moya-Alvarez V, Abellana R, Cot M (2014) Pregnancy-associated malaria and malaria in infants: An old problem with present consequences. Malar J 13:271
PubMed PubMed Central Article Google Scholar
Nagayasu E, Nagakura K, Akaki M et al (2002) Association of a determinant on mouse chromosome 18 with experimental severe Plasmodium berghei malaria. Infect Immun 70:512–516. https://doi.org/10.1128/IAI.70.2.512-516.2002
PubMed PubMed Central CAS Article Google Scholar
Nagle DL, Karim MA, Woolf EA et al (1996) Identification and mutation analysis of the complete gene for Chediak-Higashi syndrome. Nat Genet 14:307–311. https://doi.org/10.1038/ng1196-307
PubMed CAS Article Google Scholar
Nehls M, Pfeifer D, Schorpp M et al (1994) New member of the winged-helix protein family disrupted in mouse and rat nude mutations. Nature 372:103–107. https://doi.org/10.1038/372103a0
PubMed CAS Article Google Scholar
Newbold C, Warn P, Black G et al (1997) Receptor-specific adhesion and clinical disease in Plasmodium falciparum. Am J Trop Med Hyg 57:389–398. https://doi.org/10.1038/nm1297-1315
PubMed CAS Article Google Scholar
Nie CQ, Bernard NJ, Norman MU et al (2009) IP-10-mediated T cell homing promotes cerebral inflammation over splenic immunity to malaria infection. PLoS Pathog 5:e1000369. https://doi.org/10.1371/journal.ppat.1000369
PubMed PubMed Central CAS Article Google Scholar
Nitcheu J, Bonduelle O, Combadiere C et al (2003) Perforin-dependent brain-infiltrating cytotoxic CD8+ T lymphocytes mediate experimental cerebral malaria pathogenesis. J Immunol 170:2221–2228. https://doi.org/10.4049/jimmunol.170.4.2221
PubMed CAS Article Google Scholar
O’regan NO, Gegenbauer K, Sullivan JMO et al (2016) A novel role for von Willebrand factor in the pathogenesis of experimental cerebral malaria. Blood 127:1192–1202. https://doi.org/10.1182/blood-2015-07-654921
PubMed PubMed Central CAS Article Google Scholar
Oakley MS, McCutchan TF, Anantharaman V et al (2008) Host biomarkers and biological pathways that are associated with the expression of experimental cerebral malaria in mice. Infect Immun 76:4518–4529. https://doi.org/10.1128/IAI.00525-08
PubMed PubMed Central CAS Article Google Scholar
Oakley MS, Majam V, Mahajan B et al (2009) Pathogenic roles of CD14, galectin-3, and OX40 during experimental cerebral malaria in mice. PLoS One 4:. https://doi.org/10.1371/journal.pone.0006793
Oakley MS, Sahu BR, Lotspeich-Cole L et al (2013) The transcription factor T-bet regulates parasitemia and promotes pathogenesis during Plasmodium berghei ANKA murine malaria. J Immunol 191:4699–4708. https://doi.org/10.4049/jimmunol.1300396
PubMed CAS Article Google Scholar
Ohayon A, Golenser J, Sinay R et al (2010) Protein kinase C θ deficiency increases resistance of C57BL/6J mice to Plasmodium berghei infection-induced cerebral malaria. Infect Immun 78:4195–4205. https://doi.org/10.1128/IAI.00465-10
PubMed PubMed Central CAS Article Google Scholar
Ohno T, Nishimura M (2004) Detection of a new cerebral malaria susceptibility locus, using CBA mice. Immunogenetics 56:675–678. https://doi.org/10.1007/s00251-004-0739-1
PubMed CAS Article Google Scholar
Ohno T, Kobayashi F, Nishimura M (2005) Fas has a role in cerebral malaria, but not in proliferation or exclusion of the murine parasite in mice. Immunogenetics 57:293–296. https://doi.org/10.1007/s00251-005-0791-5
PubMed Article Google Scholar
Palomo J, Fauconnier M, Coquard L et al (2013) Type I interferons contribute to experimental cerebral malaria development in response to sporozoite or blood-stage Plasmodium berghei ANKA. Eur J Immunol 43:2683–2695. https://doi.org/10.1002/eji.201343327
PubMed CAS Article Google Scholar
Palomo J, Reverchon F, Piotet J et al (2015) Critical role of IL-33 receptor ST2 in experimental cerebral malaria development. Eur J Immunol 45:1354–1365. https://doi.org/10.1002/eji.201445206
PubMed CAS Article Google Scholar
Pamplona A, Ferreira A, Balla J et al (2007) Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med 13:703–710. https://doi.org/10.1038/nm1586
PubMed CAS Article Google Scholar
Patel SN, Berghout J, Lovegrove FE et al (2008) C5 deficiency and C5a or C5aR blockade protects against cerebral malaria. J Exp Med 205:1133–1143. https://doi.org/10.1084/jem.20072248
PubMed PubMed Central CAS Article Google Scholar
Pauli EK, Chan YK, Davis ME et al (2014) The ubiquitin-specific protease USP15 promotes RIG-I-mediated antiviral signaling by deubiquitylating TRIM25. Sci Signal 7:ra3. https://doi.org/10.1126/scisignal.2004577
PubMed PubMed Central CAS Article Google Scholar
Pignata C, Fiore M, Guzzetta V, et al (1996) Congenital alopecia and nail dystrophy associated with severe functional T-cell immunodeficiency in two sibs. Am J Med Genet 65:167–170
PubMed CAS Article Google Scholar
Piguet PF, Laperrousaz CDA, Tacchini-cottier F et al (2000) Delayed mortality and attenuated thrombocytopenia associated with severe malaria in Urokinase- and Urokinase receptor-deficient mice delayed mortality and attenuated thrombocytopenia associated with severe malaria in Urokinase- and Urokinase receptor-defi. Infect Immun 68:3822–3829. https://doi.org/10.1128/IAI.68.7.3822-3829.2000.Updated
PubMed PubMed Central CAS Article Google Scholar
Piguet PF, Kan CD, Vesin C et al (2001) Role of CD40-CVD40L in mouse severe malaria. Am J Pathol 159:733–742. https://doi.org/10.1016/S0002-9440(10)61744-0
PubMed PubMed Central CAS Article Google Scholar
Piguet PF, Da Kan C, Vesin C (2002) Role of the tumor necrosis factor receptor 2 (TNFR2) in cerebral malaria in mice. Lab Investig 82:1155–1166. https://doi.org/10.1097/01.LAB.0000028822.94883.8A
PubMed CAS Article Google Scholar
Porcherie A, Mathieu C, Peronet R, et al (2011) Critical role of the neutrophil-associated high-affinity receptor for IgE in the pathogenesis of experimental cerebral malaria. J Exp Med 208:2225–2236. https://doi.org/10.1084/jem.20110845
PubMed PubMed Central CAS Article Google Scholar
Potter S, Chaudhri G, Hansen A, Hunt NH (1999) Fas and perforin contribute to the pathogenesis of murine cerebral malaria. Redox Rep 4:333–335. https://doi.org/10.1179/135100099101535070
PubMed CAS Article Google Scholar
Potter SM, Mitchell AJ, Cowden WB et al (2005) Phagocyte-derived reactive oxygen species do not influence the progression of murine blood-stage malaria infections. Infect Immun 73:4941–4947. https://doi.org/10.1128/IAI.73.8.4941
PubMed PubMed Central CAS Article Google Scholar
Potter SM, Chan-Ling T, Rosinova E et al (2006a) A role for Fas-Fas ligand interactions during the late-stage neuropathological processes of experimental cerebral malaria. J Neuroimmunol 173:96–107. https://doi.org/10.1016/j.jneuroim.2005.12.004
PubMed CAS Article Google Scholar
Potter S, Chan-Ling T, Ball HJ et al (2006b) Perforin mediated apoptosis of cerebral microvascular endothelial cells during experimental cerebral malaria. Int J Parasitol 36:485–496. https://doi.org/10.1016/j.ijpara.2005.12.005
PubMed CAS Article Google Scholar
Power HJ (2001) History of Malaria. In: Encyclopedia of Life Sciences. Wiley, Chichester
Google Scholar
Price RN, Simpson JA, Nosten F et al (2001) Factors contributing to anemia after uncomplicated falciparum malaria. Am J Trop Med Hyg 65:614–622
PubMed PubMed Central CAS Article Google Scholar
Ramos TN, Darley MM, Hu X et al (2011) Cutting edge: the membrane attack complex of complement is required for the development of murine experimental cerebral malaria. J Immunol 186:6657–6660. https://doi.org/10.4049/jimmunol.1100603
PubMed PubMed Central CAS Article Google Scholar
Ramos TN, Bullard DC, Barnum SR (2012a) Deletion of the complement phagocytic receptors CR3 and CR4 does not alter susceptibility to experimental cerebral malaria. Parasite Immunol 34:547–550. https://doi.org/10.1111/pim.12002
PubMed PubMed Central CAS Article Google Scholar
Ramos TN, Darley MM, Weckbach S et al (2012b) The C5 convertase is not required for activation of the terminal complement pathway in murine experimental cerebral malaria. J Biol Chem 287:24734–24738. https://doi.org/10.1074/jbc.C112.378364
PubMed PubMed Central CAS Article Google Scholar
Ramos TN, Bullard DC, Darley MM et al (2013) Experimental cerebral malaria develops independently of endothelial expression of intercellular adhesion molecule-1 (ICAM-1). J Biol Chem 288:10962–10966. https://doi.org/10.1074/jbc.C113.457028
PubMed PubMed Central CAS Article Google Scholar
Reimer T, Shaw MH, Franchi L et al (2010) Experimental cerebral malaria progresses independently of the Nlrp3 inflammasome. Eur J Immunol 40:764–769. https://doi.org/10.1002/eji.200939996
PubMed PubMed Central CAS Article Google Scholar
Rest JR (1982) Cerebral malaria in inbred mice. I. A new model and its pathology. Trans R Soc Trop Med Hyg 76:410–415
PubMed CAS Article Google Scholar
Reverchon F, Mortaud S, Sivoyon M et al (2017) IL-33 receptor ST2 regulates the cognitive impairments associated with experimental cerebral malaria. PLoS Pathog 13:1–25. https://doi.org/10.1371/journal.ppat.1006322
CAS Article Google Scholar
Riley EM, Couper KN, Helmby H et al (2010) Neuropathogenesis of human and murine malaria. Trends Parasitol 26:277–278
PubMed Article Google Scholar
Russell SM, Tayebi N, Nakajima H et al (1995) Mutation of Jak3 in a patient with SCID: essential role of Jak3 in lymphoid development. Science 270:797–800. https://doi.org/10.1126/science.270.5237.797
PubMed CAS Article Google Scholar
Saeftel M, Krueger A, Arriens S et al (2004) Mice Deficient in Interleukin-4 (IL-4) or IL-4 Receptor α Have Higher Resistance to Sporozoite Infection with Plasmodium berghei (ANKA) than Do Naive Wild-Type Mice. Infect Immun 72:322–331. https://doi.org/10.1128/IAI.72.1.322-331.2004
PubMed PubMed Central CAS Article Google Scholar
Sanni LA, Thomas SR, Tattam BN et al (1998) Dramatic changes in oxidative tryptophan metabolism along the kynurenine pathway in experimental cerebral and noncerebral malaria. Am J Pathol 152:611–619
PubMed PubMed Central CAS Google Scholar
Sanni LA, Fu S, Dean RT et al (1999) Are reactive oxygen species involved in the pathogenesis of murine cerebral malaria? J Infect Dis 179:217–222. https://doi.org/10.1086/314552
PubMed CAS Article Google Scholar
Sawcer S, Hellenthal G, Pirinen M et al (2011) Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 476:214–219. https://doi.org/10.1038/nature10251
PubMed PubMed Central CAS Article Google Scholar
Schmid U, Stenzel W, Koschel J et al (2017) The deubiquitinating enzyme cylindromatosis dampens CD8 + T cell responses and is a critical factor for experimental cerebral malaria and blood-brain barrier damage. Front Immunol 8:1–17. https://doi.org/10.3389/fimmu.2017.00027
CAS Article Google Scholar
Schofield L, Grau GE (2005) Immunological processes in malaria pathogenesis. Nat Rev Immunol 5:722–735. https://doi.org/10.1038/nri1686
PubMed CAS Article Google Scholar
Sellau J, Alvarado CF, Hoenow S et al (2016) IL-22 dampens the T cell response in experimental malaria. Sci Rep 6:1–11. https://doi.org/10.1038/srep28058
CAS Article Google Scholar
Senaldi G, Shaklee CL, Guo J et al (1999) Protection against the mortality associated with disease models mediated by TNF and IFN-γ in mice lacking IFN regulatory factor-1. J Immunol 163:6820–6826
PubMed CAS Google Scholar
Sharma S, DeOliveira RB, Kalantari P et al (2011) Innate immune recognition of an AT-rich stem-loop DNA motif in the Plasmodium falciparum genome. Immunity 35:194–207. https://doi.org/10.1016/j.immuni.2011.05.016
PubMed PubMed Central CAS Article Google Scholar
Shibui A, Takamori A, Tolba MEM et al (2016) IL-25, IL-33 and TSLP receptor are not critical for development of experimental murine malaria. Biochem Biophys Reports 5:191–195. https://doi.org/10.1016/j.bbrep.2015.12.007
Article Google Scholar
Shryock N, McBerry C, Salazar Gonzalez RM et al (2013) Lipoxin A4 and 15-Epi-Lipoxin A4 protect against experimental cerebral malaria by inhibiting IL-12/IFN-γ in the brain. PLoS ONE 8:2–10. https://doi.org/10.1371/journal.pone.0061882
CAS Article Google Scholar
Srivastava K, Cockburn IA, Swaim A et al (2008) Platelet factor 4 mediates inflammation in experimental cerebral malaria. Cell Host Microbe 4:179–187. https://doi.org/10.1016/j.chom.2008.07.003
PubMed PubMed Central CAS Article Google Scholar
Stevenson MM, Gros P, Olivier M et al (2010) Cerebral malaria: human versus mouse studies. Trends Parasitol 26:274–275
PubMed Article Google Scholar
Su X, Hayton K, Wellems TE (2007) Genetic linkage and association analyses for trait mapping in Plasmodium falciparum. Nat Rev Genet 8:497–506
PubMed CAS Article Google Scholar
Szalai AJ, Barnum SR, Ramos TN (2014) Deletion of C-reactive protein ameliorates experimental cerebral malaria? Trans R Soc Trop Med Hyg 108:591–593. https://doi.org/10.1093/trstmh/tru098
PubMed PubMed Central CAS Article Google Scholar
Taylor TE, Borgstein A, Molyneux ME (1993) Acid-base status in paediatric Plasmodium falciparum malaria. Q J Med 86:99–109
PubMed CAS Google Scholar
Taylor-Robinson AW (2010) Validity of modelling cerebral malaria in mice: argument and counter argument. J Neuroparasitol 1:45–49. https://doi.org/10.4303/jnp/N100601
Article Google Scholar
Timmann C, Thye T, Vens M et al (2012) Genome-wide association study indicates two novel resistance loci for severe malaria. Nature 489:443–446. https://doi.org/10.1038/nature11334
PubMed CAS Article Google Scholar
Togbe D, Schofield L, Grau GE et al (2007) Murine cerebral malaria development is independent of toll-like receptor signaling. Am J Pathol 170:1640–1648. https://doi.org/10.2353/ajpath.2007.060889
PubMed PubMed Central CAS Article Google Scholar
Togbe D, de Sousa PL, Fauconnier M et al (2008) Both functional LTβ receptor and TNF receptor 2 are required for the development of experimental cerebral malaria. PLoS ONE 3:. https://doi.org/10.1371/journal.pone.0002608
Torre S, Van Bruggen R, Kennedy JM et al (2013) Susceptibility to lethal cerebral malaria is regulated by epistatic interaction between chromosome 4 (Berr6) and chromosome 1 (Berr7) loci in mice. Genes Immun 14:249–257. https://doi.org/10.1038/gene.2013.16
PubMed CAS Article Google Scholar
Torre S, Faucher SP, Fodil N et al (2015) THEMIS Is required for pathogenesis of cerebral malaria and protection against pulmonary tuberculosis. Infect Immun 83:759–768. https://doi.org/10.1128/IAI.02586-14
PubMed PubMed Central CAS Article Google Scholar
Torre S, Polyak MJ, Langlais D et al (2017) USP15 regulates type I interferon response and is required for pathogenesis of neuroinflammation. Nat Immunol 18:54–63. https://doi.org/10.1038/ni.3581
PubMed CAS Article Google Scholar
Trampuz A, Jereb M, Muzlovic I, Prabhu RM (2003) Clinical review: Severe malaria. Crit Care 7:315–323
PubMed PubMed Central Article Google Scholar
Van Bruggen R, Gualtieri C, Iliescu A et al (2015) Modulation of malaria phenotypes by pyruvate kinase (pklr) variants in a Thai population. PLoS ONE 10:e0144555. https://doi.org/10.1371/journal.pone.0144555
PubMed PubMed Central CAS Article Google Scholar
Van Den Steen PE, Van Aelst I, Starckx S et al (2006) Matrix metalloproteinases, tissue inhibitors of MMPs and TACE in experimental cerebral malaria. Lab Investig 86:873–888. https://doi.org/10.1038/labinvest.3700454
PubMed CAS Article Google Scholar
Van Der Heyde HC, Bauer P, Sun G et al (2001) Assessing vascular permeability during experimental cerebral malaria by a radiolabeled monoclonal antibody technique. Infect Immun 69:3460–3465. https://doi.org/10.1128/IAI.69.5.3460-3465.2001
PubMed PubMed Central CAS Article Google Scholar
van der Heyde HC, Nolan J, Combes V et al (2006) A unified hypothesis for the genesis of cerebral malaria: sequestration, inflammation and hemostasis leading to microcirculatory dysfunction. Trends Parasitol 22:503–508. https://doi.org/10.1016/j.pt.2006.09.002
PubMed CAS Article Google Scholar
Verra F, Mangano VD, Modiano D (2009) Genetics of susceptibility to Plasmodium falciparum: from classical malaria resistance genes towards genome-wide association studies. Parasite Immunol 31:234–253
PubMed CAS Article Google Scholar
Villegas-Mendez A, Greig R, Shaw TN et al (2012) IFN-γ-producing CD4+ T Cells promote experimental cerebral malaria by modulating CD8+ T cell accumulation within the brain. J Immunol 189:968–979. https://doi.org/10.4049/jimmunol.1200688
PubMed PubMed Central CAS Article Google Scholar
Wah ST, Hananantachai H, Kerdpin U et al (2016) Molecular basis of human cerebral malaria development. Trop Med Health 44:2401–2407
Article Google Scholar
Waisberg M, Tarasenko T, Vickers BK et al (2011) Genetic susceptibility to systemic lupus erythematosus protects against cerebral malaria in mice. Proc Natl Acad Sci 108:1122–1127. https://doi.org/10.1073/pnas.1017996108
PubMed Article Google Scholar
Wassmer SC, Grau GER (2016) Platelets as pathogenetic effectors and killer cells in cerebral malaria. Expert Rev Hematol 9:515–517. https://doi.org/10.1080/17474086.2016.1179571
PubMed CAS Article Google Scholar
White NJ, Turner GDH, Medana IM et al (2010) The murine cerebral malaria phenomenon. Trends Parasitol 26:11–15. https://doi.org/10.1016/j.pt.2009.10.007
PubMed PubMed Central Article Google Scholar
White NJ, Turner GDH, Day NPJ, Dondorp AM (2013) Lethal malaria: marchiafava and bignami were right. J Infect Dis 208:192–198
PubMed PubMed Central CAS Article Google Scholar
White NJ, Pukrittayakamee S, Hien TT et al (2014) Malaria Lancet 383:723–735. https://doi.org/10.1016/S0140-6736(13)60024-0
PubMed Article Google Scholar
World Health Organization (2016) World Malaria Report 2016. World Health Organization, Geneva
Book Google Scholar
World Health Organization (2017) World Malaria Report 2017. World Health Organization, Geneva
Book Google Scholar
Yanez DM, Manning DD, Cooley AJ et al (1996) Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria. J Immunol 157:1620–1624
PubMed CAS Google Scholar
Zhang Q, Davis JC, Lamborn IT et al (2009) Combined immunodeficiency associated with DOCK8 Mutations. N Engl J Med 361:2046–2055. https://doi.org/10.1056/NEJMoa0905506
PubMed PubMed Central CAS Article Google Scholar

Download references

Acknowledgements

The work in PG lab was supported by grants to PG from the Canadian Institutes of Health Research, and the Canadian Institute for Advanced Research. PG is endebted to the many trainees in his lab that have contributed to the genetic analysis of susceptibility to malaria in mouse models of infection.

Author information

Sabrina Torre and David Langlais have contributed equally to this work.

Affiliations

Department of Biochemistry, Department of Human Genetics, McGill University Research Centre on Complex Traits, McGill University, Montreal, QC, Canada
Sabrina Torre, David Langlais & Philippe Gros
McGill University and Genome Quebec Innovation Centre, Montreal, QC, Canada
David Langlais
Department of Biochemistry, McGill University, 3649 Sir William Osler Promenade, room 366, Montreal, QC, H3G-0B1, Canada
Philippe Gros

Authors

Sabrina Torre
View author publications
You can also search for this author in PubMed Google Scholar
David Langlais
View author publications
You can also search for this author in PubMed Google Scholar
Philippe Gros
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philippe Gros.

Ethics declarations

Confilct of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Torre, S., Langlais, D. & Gros, P. Genetic analysis of cerebral malaria in the mouse model infected with Plasmodium berghei. Mamm Genome 29, 488–506 (2018). https://doi.org/10.1007/s00335-018-9752-9

Download citation

Received: 28 January 2018
Accepted: 05 June 2018
Published: 19 June 2018
Issue Date: August 2018
DOI: https://doi.org/10.1007/s00335-018-9752-9

Keywords

Cerebral Malaria (CM)
Plasmodium Berghei ANKA (PbA)
Blood Parasitaemia
P. Falciparum Erythrocyte Membrane Protein 1 (PfEMP1)
Lysosomal Trafficking Regulator (LYST)