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Understanding host–parasite relationship: the immune central nervous system microenvironment and its effect on brain infections

Published online by Cambridge University Press:  12 December 2017

Laura Adalid-Peralta
Affiliation:
Instituto Nacional de Neurología y Neurocirugía, Mexico City, México Unidad Periférica del Instituto de Investigaciones Biomédicas en el Instituto Nacional de Neurología y Neurocirugía, Mexico City, México
Brenda Sáenz
Affiliation:
Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Coyoacan, México
Gladis Fragoso
Affiliation:
Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Coyoacan, México
Graciela Cárdenas*
Affiliation:
Instituto Nacional de Neurología y Neurocirugía, Mexico City, México Unidad Periférica del Instituto de Investigaciones Biomédicas en el Instituto Nacional de Neurología y Neurocirugía, Mexico City, México
*
Author for correspondence: Graciela Cárdenas, E-mail: grace_goker@yahoo.de, gracielacardenas@yahoo.com.mx

Abstract

The central nervous system (CNS) has been recognized as an immunologically specialized microenvironment, where immune surveillance takes a distinctive character, and where delicate neuronal networks are sustained by anti-inflammatory factors that maintain local homeostasis. However, when a foreign agent such as a parasite establishes in the CNS, a set of immune defences is mounted and several immune molecules are released to promote an array of responses, which ultimately would control the infection and associated damage. Instead, a host–parasite relationship is established, in the context of which a close biochemical coevolution and communication at all organization levels between two complex organisms have developed. The ability of the parasite to establish in its host is associated with several evasion mechanisms to the immune response and its capacity for exploiting host-derived molecules. In this context, the CNS is deeply involved in modulating immune functions, either protective or pathogenic, and possibly in parasitic activity as well, via interactions with evolutionarily conserved molecules such as growth factors, neuropeptides and hormones. This review presents available evidence on some examples of CNS parasitic infections inducing different morbi-mortality grades in low- or middle-income countries, to illustrate how the CNS microenvironment affect pathogen establishment, growth, survival and reproduction in immunocompetent hosts. A better understanding of the influence of the CNS microenvironment on neuroinfections may provide relevant insights into the mechanisms underlying these pathologies.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2017 

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References

Adalid-Peralta, L, Fleury, A, García-Ibarra, TM, Hernández, M, Parkhouse, M, Crispín, JC, Voltaire-Proaño, J, Cárdenas, G, Fragoso, G and Sciutto, E (2012) Human neurocysticercosis: in vivo expansion of peripheral regulatory T cells and their recruitment in the central nervous system. Journal of Parasitology 98, 142148.CrossRefGoogle ScholarPubMed
Adalid-Peralta, L, Arce-Sillas, A, Fragoso, G, Cárdenas, G, Rosetti, M, Casanova-Hernández, D, Rangel-Escareño, C, Uribe-Figueroa, L, Fleury, A and Sciutto, E (2013) Cysticerci drive dendritic cells to promote in vitro and in vivo Tregs differentiation. Clinical and Developmental Immunology 2013, 981468.CrossRefGoogle ScholarPubMed
Adalid-Peralta, L, Rosas, G, Arce-Sillas, A, Bobes, RJ, Cárdenas, G, Hernández, M, Trejo, C, Meneses, G, Hernández, B, Estrada, K, Fleury, A, Laclette, JP, Larralde, C, Sciutto, E and Fragoso, G (2017) Effect of transforming growth factor-β upon Taenia solium and Taenia crassiceps cysticerci. Scientific Reports 7, 12345.Google Scholar
Adamo, SA (2013) Parasites: evolution's neurobiologists. Journal of Experimental Biology 216, 310.CrossRefGoogle ScholarPubMed
Almelli, T, Ndam, NT, Ezimegnon, S, Alao, MJ, Ahouansou, C, Sagbo, G, Amoussou, A, Deloron, P and Tahar, R (2014) Cytoadherence phenotype of Plasmodium falciparum-infected erythrocytes is associated with specific pfemp-1 expression in parasites from children with cerebral malaria. Malaria Journal 13, 333.CrossRefGoogle ScholarPubMed
Alvarez, JI and Teale, JM (2007) Evidence for differential changes of junctional complex proteins in murine neurocysticercosis dependent upon CNS vasculature. Brain Research 1169, 98111.CrossRefGoogle ScholarPubMed
Alvarez, JI, Londoño, DP, Alvarez, AL, Trujillo, J, Jaramillo, MM and Restrepo, BI (2002) Granuloma formation and parasite disintegration in porcine cysticercosis: comparison with human neurocysticercosis. Journal of Comparative Pathology 127, 186193.Google Scholar
Alvarez, JI, Mishra, BB, Gundra, UM, Mishra, PK and Teale, JM (2010) Mesocestoides corti intracranial infection as a murine model for neurocysticercosis. Parasitology 137, 359372.CrossRefGoogle ScholarPubMed
Arce-Sillas, A, Álvarez-Luquín, DD, Cárdenas, G, Casanova-Hernández, D, Fragoso, G, Hernández, M, Proaño Narváez, JV, García-Vázquez, F, Fleury, A, Sciutto, E and Adalid-Peralta, L (2016) Interleukin 10 and dendritic cells are the main suppression mediators of regulatory T cells in human neurocysticercosis. Clinical and Experimental Immunology 183, 271279.Google Scholar
Armah, H, Wired, EK, Dodoo, AK, Adjei, AA, Tettey, Y and Gyasi, R (2005) Cytokines and adhesion molecules expression in the brain in human cerebral malaria. International Journal of Environmental Research and Public Health 2, 123131.CrossRefGoogle ScholarPubMed
Arora, N, Tripathi, S, Kumar, P, Mondal, P, Mishra, A and Prasad, A (2017) Recent advancements and new perspectives in animal models for neurocysticercosis immunopathogenesis. Parasite Immunology 39. doi: 10.1111/pim.12439.CrossRefGoogle ScholarPubMed
Barbier, M, Faille, D, Loriod, B, Textoris, J, Camus, C, Puthier, D, Flori, L, Wassmer, SC, Victorero, G, Alessi, MC, Fusaï, T, Nguyen, C, Grau, GE and Rihet, P (2011) Platelets alter gene expression profile in human brain endothelial cells in an in vitro model of cerebral malaria. PLoS ONE 6, e19651.Google Scholar
Barragan, A and Sibley, LD (2003) Migration of Toxoplasma gondii across biological barriers. Trends in Microbiology 11, 426430.CrossRefGoogle ScholarPubMed
Barragan, A, Brossier, F and Sibley, LD (2005) Transepithelial migration of Toxoplasma gondii involves an interaction of intercellular adhesion molecule 1 (ICAM-1) with the parasite adhesin MIC2. Cellular Microbiology 7, 561568.Google Scholar
Basu, S and Dasgupta, PS (2000) Dopamine, a neurotransmitter, influences the immune system. Journal of Neuroimmunology 102, 113124.Google Scholar
Bayoumi, NK, Elhassan, EM, Elbashir, MI and Adam, I (2009) Cortisol, prolactin, cytokines and the susceptibility of pregnant Sudanese women to Plasmodium falciparum malaria. Annals of Tropical Medicine and Parasitology 103, 111117.Google Scholar
Berriman, M, Haas, BJ, LoVerde, PT, Wilson, RA, Dillon, GP, Cerqueira, GC, Mashiyama, ST, Al-Lazikani, B, Andrade, LF, Ashton, PD, Aslett, MA, Bartholomeu, DC, Blandin, G, Caffrey, CR, Coghlan, A, Coulson, R, Day, TA, Delcher, A, DeMarco, R, Djikeng, A, Eyre, T, Gamble, JA, Ghedin, E, Gu, Y, Hertz-Fowler, C, Hirai, H, Hirai, Y, Houston, R, Ivens, A, Johnston, DA, Lacerda, D, Macedo, CD, McVeigh, P, Ning, Z, Oliveira, G, Overington, JP, Parkhill, J, Pertea, M, Pierce, RJ, Protasio, AV, Quail, MA, Rajandream, MA, Rogers, J, Sajid, M, Salzberg, SL, Stanke, M, Tivey, AR, White, O, Williams, DL, Wortman, J, Wu, W, Zamanian, M, Zerlotini, A, Fraser-Liggett, CM, Barrell, BG and El-Sayed, NM (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460, 352358.CrossRefGoogle ScholarPubMed
Blader, IJ, Manger, ID and Boothroyd, JC (2001) Microarray analysis reveals previously unknown changes in Toxoplasma gondii-infected human cells. Journal of Biological Chemistry 276, 2422324231.CrossRefGoogle ScholarPubMed
Cangalaya, C, Bustos, JA, Calcina, J, Vargas-Calla, A, Suarez, D, Gonzalez, AE, Chacaltana, J, Guerra-Giraldez, C, Mahanty, S, Nash, TE, García, HH and Peru, CWGI (2016) Perilesional inflammation in neurocysticercosis – relationship between contrast-enhanced magnetic resonance imaging, Evans blue staining and histopathology in the pig model. PLoS Neglected Tropical Diseases 10, e0004869.Google Scholar
Cárdenas, G, Valdez, R, Sáenz, B, Bottasso, O, Fragoso, G, Sciutto, E, Romano, MC and Fleury, A (2012) Impact of Taenia solium neurocysticercosis upon endocrine status and its relation with immuno-inflammatory parameters. International Journal for Parasitology 42, 171176.CrossRefGoogle ScholarPubMed
Cetinkaya, Z, Yazar, S, Gecici, O and Namli, MN (2007) Anti-Toxoplasma gondii antibodies in patients with schizophrenia – preliminary findings in a Turkish sample. Schizophrenia Bulletin 33, 789791.Google Scholar
Chavarría, A, Fleury, A, García, E, Márquez, C, Fragoso, G and Sciutto, E (2005) Relationship between the clinical heterogeneity of neurocysticercosis and the immune-inflammatory profiles. Clinical Immunology 116, 271278.Google Scholar
Clark, IA, Chaudhri, G and Cowden, WB (1989) Roles of tumour necrosis factor in the illness and pathology of malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 436440.Google Scholar
Coccaro, EF, Lee, R, Groer, MW, Can, A, Coussons-Read, M and Postolache, TT (2016) Toxoplasma gondii infection: relationship with aggression in psychiatric subjects. Journal of Clinical Psychiatry 77, 334341.Google Scholar
Colley, DG, Bustinduy, AL, Secor, WE and King, CH (2014) Human schistosomiasis. Lancet 383, 22532264.CrossRefGoogle ScholarPubMed
Consortium, S. j. G. S. a. F. A. (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460, 345351.Google Scholar
Cosentino, M, Fietta, AM, Ferrari, M, Rasini, E, Bombelli, R, Carcano, E, Saporiti, F, Meloni, F, Marino, F and Lecchini, S (2007) Human CD4 + CD25 + regulatory T cells selectively express tyrosine hydroxylase and contain endogenous catecholamines subserving an autocrine/paracrine inhibitory functional loop. Blood 109, 632642.CrossRefGoogle ScholarPubMed
Courret, N, Darche, S, Sonigo, P, Milon, G, Buzoni-Gâtel, D and Tardieux, I (2006) CD11c- and CD11b-expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood 107, 309316.Google Scholar
Del Brutto, OH (2014) Neurocysticercosis. Neurohospitalist 4, 205212.Google Scholar
Dewalick, S, Bexkens, ML, van Balkom, BW, Wu, YP, Smit, CH, Hokke, CH, de Groot, PG, Heck, AJ, Tielens, AG and van Hellemond, JJ (2011) The proteome of the insoluble Schistosoma mansoni eggshell skeleton. International Journal for Parasitology 41, 523532.Google Scholar
Dewalick, S, Hensbergen, PJ, Bexkens, ML, Grosserichter-Wagener, C, Hokke, CH, Deelder, AM, de Groot, PG, Tielens, AG and van Hellemond, JJ (2014) Binding of von Willebrand factor and plasma proteins to the eggshell of Schistosoma mansoni. International Journal for Parasitology 44, 263268.CrossRefGoogle Scholar
Dickerson, F, Boronow, J, Stallings, C, Origoni, A and Yolken, R (2007) Toxoplasma gondii in individuals with schizophrenia: association with clinical and demographic factors and with mortality. Schizophrenia Bulletin 33, 737740.Google Scholar
Dissous, C, Khayath, N, Vicogne, J and Capron, M (2006) Growth factor receptors in helminth parasites: signalling and host-parasite relationships. FEBS Letters 580, 29682975.Google Scholar
El-Assaad, F, Wheway, J, Mitchell, AJ, Lou, J, Hunt, NH, Combes, V and Grau, GE (2013) Cytoadherence of Plasmodium berghei-infected red blood cells to murine brain and lung microvascular endothelial cells in vitro. Infection and Immunity 81, 39843991.Google Scholar
El-Shehabi, F and Ribeiro, P (2010) Histamine signalling in Schistosoma mansoni: immunolocalisation and characterisation of a new histamine-responsive receptor (SmGPR-2). International Journal for Parasitology 40, 13951406.CrossRefGoogle ScholarPubMed
Escobedo, G, Camacho-Arroyo, I, Hernández-Hernández, OT, Ostoa-Saloma, P, García-Varela, M and Morales-Montor, J (2010) Progesterone induces scolex evagination of the human parasite Taenia solium: evolutionary implications to the host-parasite relationship. Journal of Biomedicine & Biotechnology 2010, 591079.Google Scholar
Everts, B, Perona-Wright, G, Smits, HH, Hokke, CH, van der Ham, AJ, Fitzsimmons, CM, Doenhoff, MJ, van der Bosch, J, Mohrs, K, Haas, H, Mohrs, M, Yazdanbakhsh, M and Schramm, G (2009) Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. Journal of Experimental Medicine 206, 16731680.CrossRefGoogle ScholarPubMed
Fairfax, K, Nascimento, M, Huang, SC, Everts, B and Pearce, EJ (2012) Th2 responses in schistosomiasis. Seminars in Immunopathology 34, 863871.Google Scholar
Ferrari, TC and Moreira, PR (2011) Neuroschistosomiasis: clinical symptoms and pathogenesis. Lancet Neurology 10, 853864.CrossRefGoogle Scholar
Ferrari, TC, Gazzinelli, G and Corrêa-Oliveira, R (2008) Immune response and pathogenesis of neuroschistosomiasis mansoni. Acta Tropica 108, 8388.Google Scholar
Flegr, J, Zitková, S, Kodym, P and Frynta, D (1996) Induction of changes in human behaviour by the parasitic protozoan Toxoplasma gondii. Parasitology 113(Pt 1), 4954.CrossRefGoogle ScholarPubMed
Flegr, J, Preiss, M, Klose, J, Havlícek, J, Vitáková, M and Kodym, P (2003) Decreased level of psychobiological factor novelty seeking and lower intelligence in men latently infected with the protozoan parasite Toxoplasma gondii dopamine, a missing link between schizophrenia and toxoplasmosis? Biological Psychology 63, 253268.Google Scholar
Flegr, J, Prandota, J, Sovičková, M and Israili, ZH (2014) Toxoplasmosis – a global threat. Correlation of latent toxoplasmosis with specific disease burden in a set of 88 countries. PLoS ONE 9, e90203.Google Scholar
Fuks, JM, Arrighi, RB, Weidner, JM, Kumar Mendu, S, Jin, Z, Wallin, RP, Rethi, B, Birnir, B and Barragan, A (2012) GABAergic signaling is linked to a hypermigratory phenotype in dendritic cells infected by Toxoplasma gondii. PLoS Pathogens 8, e1003051.Google Scholar
Galea, I, Bechmann, I and Perry, VH (2007) What is immune privilege (not)? Trends in Immunology 28, 1218.CrossRefGoogle ScholarPubMed
Gimenez, F, Barraud de Lagerie, S, Fernandez, C, Pino, P and Mazier, D (2003) Tumor necrosis factor alpha in the pathogenesis of cerebral malaria. Cellular and Molecular Life Sciences 60, 16231635.Google Scholar
Golcu, D, Gebre, RZ and Sapolsky, RM (2014) Toxoplasma gondii influences aversive behaviors of female rats in an estrus cycle dependent manner. Physiology & Behavior 135, 98103.Google Scholar
Gregg, B, Taylor, BC, John, B, Tait-Wojno, ED, Girgis, NM, Miller, N, Wagage, S, Roos, DS and Hunter, CA (2013) Replication and distribution of Toxoplasma gondii in the small intestine after oral infection with tissue cysts. Infection and Immunity 81, 16351643.Google Scholar
Guerra-Giraldez, C, Marzal, M, Cangalaya, C, Balboa, D, Orrego, M, Paredes, A, Gonzales-Gustavson, E, Arroyo, G, García, HH, González, AE, Mahanty, S and Nash, TE and Peru, c. w. g. i. (2013) Disruption of the blood-brain barrier in pigs naturally infected with Taenia solium, untreated and after anthelmintic treatment. Experimental Parasitology 134, 443446.Google Scholar
Gundra, UM, Mishra, BB, Wong, K and Teale, JM (2011) Increased disease severity of parasite-infected TLR2−/- mice is correlated with decreased central nervous system inflammation and reduced numbers of cells with alternatively activated macrophage phenotypes in a murine model of neurocysticercosis. Infection and Immunity 79, 25862596.Google Scholar
Halonen, SK, Chiu, F and Weiss, LM (1998) Effect of cytokines on growth of Toxoplasma gondii in murine astrocytes. Infection and Immunity 66, 49894993.Google Scholar
Hamdan, FF and Ribeiro, P (1999) Characterization of a stable form of tryptophan hydroxylase from the human parasite Schistosoma mansoni. Journal of Biological Chemistry 274, 2174621754.Google Scholar
Havlícek, J, Gasová, ZG, Smith, AP, Zvára, K and Flegr, J (2001) Decrease of psychomotor performance in subjects with latent ‘asymptomatic’ toxoplasmosis. Parasitology 122, 515520.Google Scholar
Hinze-Selch, D, Däubener, W, Eggert, L, Erdag, S, Stoltenberg, R and Wilms, S (2007) A controlled prospective study of Toxoplasma gondii infection in individuals with schizophrenia: beyond seroprevalence. Schizophrenia Bulletin 33, 782788.CrossRefGoogle ScholarPubMed
Huerta, L, Terrazas, LI, Sciutto, E and Larralde, C (1992) Immunological mediation of gonadal effects on experimental murine cysticercosis caused by Taenia crassiceps metacestodes. Journal of Parasitology 78, 471476.Google Scholar
John, CC, Carabin, H, Montano, SM, Bangirana, P, Zunt, JR and Peterson, PK (2015) Global research priorities for infections that affect the nervous system. Nature 527, S178S186.Google Scholar
Keswani, T, Sarkar, S, Sengupta, A and Bhattacharyya, A (2016) Role of TGF-β and IL-6 in dendritic cells, Treg and Th17 mediated immune response during experimental cerebral malaria. Cytokine 88, 154166.CrossRefGoogle ScholarPubMed
Kristensson, K, Masocha, W and Bentivoglio, M (2013) Mechanisms of CNS invasion and damage by parasites. Handbook of Clinical Neurology 114, 1122.CrossRefGoogle ScholarPubMed
Kuesap, J and Na-Bangchang, K (2010) Possible role of heme oxygenase-1 and prostaglandins in the pathogenesis of cerebral malaria: heme oxygenase-1 induction by prostaglandin D(2) and metabolite by a human astrocyte cell line. Korean Journal of Parasitology 48, 1521.Google Scholar
Lachenmaier, SM, Deli, MA, Meissner, M and Liesenfeld, O (2011) Intracellular transport of Toxoplasma gondii through the blood-brain barrier. Journal of Neuroimmunology 232, 119130.Google Scholar
Lambert, H and Barragan, A (2010) Modelling parasite dissemination: host cell subversion and immune evasion by Toxoplasma gondii. Cellular Microbiology 12, 292300.Google Scholar
Lambert, H, Dellacasa-Lindberg, I and Barragan, A (2011) Migratory responses of leukocytes infected with Toxoplasma gondii. Microbes and Infection 13, 96102.CrossRefGoogle ScholarPubMed
Larralde, C, Sciutto, E, Huerta, L, Terrazas, I, Fragoso, G, Trueba, L, Lemus, D, Lomelí, C, Tapia, G and Montoya, RM (1989) Experimental cysticercosis by Taenia crassiceps in mice: factors involved in susceptibility. Acta Leiden 57, 131134.Google Scholar
Larralde, C, Morales, J, Terrazas, I, Govezensky, T and Romano, MC (1995) Sex hormone changes induced by the parasite lead to feminization of the male host in murine Taenia crassiceps cysticercosis. Journal of Steroid Biochemistry and Molecular Biology 52, 575580.Google Scholar
Libonati, RM, de Mendonça, BB, Maués, JA, Quaresma, JA and de Souza, JM (2006) Some aspects of the behavior of the hypothalamus-pituitary-adrenal axis in patients with uncomplicated Plasmodium falciparum malaria: cortisol and dehydroepiandrosterone levels. Acta Tropica 98, 270276.CrossRefGoogle ScholarPubMed
Lindgren, M, Torniainen-Holm, M, Härkänen, T, Dickerson, F, Yolken, RH and Suvisaari, J (2017) The association between toxoplasma and the psychosis continuum in a general population setting. Schizophrenia Research. pii: S0920-9964(17)30391-2. doi: 10.1016/j.schres.2017.06.052.Google Scholar
Lingnau, A, Margos, G, Maier, WA and Seitz, HM (1993) The effects of hormones on the gametocytogenesis of Plasmodium falciparum in vitro. Applied Parasitology 34, 153160.Google Scholar
Livneh, E, Glazer, L, Segal, D, Schlessinger, J and Shilo, BZ (1985) The Drosophila EGF receptor gene homolog: conservation of both hormone binding and kinase domains. Cell 40, 599607.Google Scholar
Long, E, Harrison, R, Bickle, Q, Bain, J, Nelson, G and Doenhoff, M (1980) Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. The effect of varying the route and the number of primary infections, and the correlation between the size of the primary infection and the degree of resistance that is acquired. Parasitology 81, 355371.Google Scholar
Lourembam, SD, Sawian, CE and Baruah, S (2013) Dysregulation of cytokines expression in complicated falciparum malaria with increased TGF-β and IFN-γ and decreased IL-2 and IL-12. Cytokine 64, 503508.Google Scholar
Madkhali, AM, Alkurbi, MO, Szestak, T, Bengtsson, A, Patil, PR, Wu, Y, Al-Harthi, SA, Alharthi, S, Jensen, AT, Pleass, R and Craig, AG (2014) An analysis of the binding characteristics of a panel of recently selected ICAM-1 binding Plasmodium falciparum patient isolates. PLoS ONE 9, e111518.Google Scholar
Mahanty, S, Orrego, MA, Mayta, H, Marzal, M, Cangalaya, C, Paredes, A, Gonzales-Gustavson, E, Arroyo, G, Gonzalez, AE, Guerra-Giraldez, C, García, HH and Nash, TE and Peru, C. W. G. i. (2015) Post-treatment vascular leakage and inflammatory responses around brain cysts in porcine neurocysticercosis. PLoS Neglected Tropical Diseases 9, e0003577.Google Scholar
Maswoswe, SM, Peters, W and Warhurst, DC (1985) Corticosteroid stimulation of the growth of Plasmodium falciparum gametocytes in vitro. Annals of Tropical Medicine & Parasitology 79, 607616.Google Scholar
Matos-Silva, H, Reciputti, BP, Paula, EC, Oliveira, AL, Moura, VB, Vinaud, MC, Oliveira, MA and Lino-Júnior, RES (2012) Experimental encephalitis caused by Taenia crassiceps cysticerci in mice. Arquivos de Neuro-psiquiatria 70, 287292.Google Scholar
Meibalan, E and Marti, M (2017) Biology of malaria transmission. Cold Spring Harbor Perspectives in Medicine 7, pii: a025452. doi: 10.1101/cshperspect.a025452.Google Scholar
Melzer, TC, Cranston, HJ, Weiss, LM and Halonen, SK (2010) Host cell preference of Toxoplasma gondii cysts in murine brain: a confocal study. Journal of Neuroparasitology 1, pii: N100505.Google Scholar
Mercier, C and Cesbron-Delauw, MF (2015) Toxoplasma secretory granules: one population or more? Trends in Parasitology 31, 6071.Google Scholar
Morales, J, Velasco, T, Tovar, V, Fragoso, G, Fleury, A, Beltrán, C, Villalobos, N, Aluja, A, Rodarte, LF, Sciutto, E and Larralde, C (2002) Castration and pregnancy of rural pigs significantly increase the prevalence of naturally acquired Taenia solium cysticercosis. Veterinary Parasitology 108, 4148.Google Scholar
Mortensen, PB, Nørgaard-Pedersen, B, Waltoft, BL, Sørensen, TL, Hougaard, D and Yolken, RH (2007) Early infections of Toxoplasma gondii and the later development of schizophrenia. Schizophrenia Bulletin 33, 741744.Google Scholar
Nagineni, CN, Detrick, B and Hooks, JJ (2002) Transforming growth factor-beta expression in human retinal pigment epithelial cells is enhanced by Toxoplasma gondii: a possible role in the immunopathogenesis of retinochoroiditis. Clinical and Experimental Immunology 128, 372378.Google Scholar
Ngô, HM, Zhou, Y, Lorenzi, H, Wang, K, Kim, TK, El Bissati, K, Mui, E, Fraczek, L, Rajagopala, SV, Roberts, CW, Henriquez, FL, Montpetit, A, Blackwell, JM, Jamieson, SE, Wheeler, K, Begeman, IJ, Naranjo-Galvis, C, Alliey-Rodriguez, N, Davis, RG, Soroceanu, L, Cobbs, C, Steindler, DA, Boyer, K, Noble, AG, Swisher, CN, Heydemann, PT, Rabiah, P, Withers, S, Soteropoulos, P, Hood, L et al. McLeod, R (2017) Toxoplasma modulates signature pathways of human epilepsy, neurodegeneration & cancer. Scientific Reports 7, 11496.Google Scholar
Nishimura, K, Kitamura, Y, Inoue, T, Umesono, Y, Sano, S, Yoshimoto, K, Inden, M, Takata, K, Taniguchi, T, Shimohama, S and Agata, K (2007) Reconstruction of dopaminergic neural network and locomotion function in planarian regenerates. Developmental Neurobiology 67, 10591078.Google Scholar
Omer, FM, de Souza, JB, Corran, PH, Sultan, AA and Riley, EM (2003) Activation of transforming growth factor beta by malaria parasite-derived metalloproteinases and a thrombospondin-like molecule. Journal of Experimental Medicine 198, 18171827.Google Scholar
Ousman, SS and Kubes, P (2012) Immune surveillance in the central nervous system. Nature Neuroscience 15, 10961101.Google Scholar
Pacheco, R, Prado, CE, Barrientos, MJ and Bernales, S (2009) Role of dopamine in the physiology of T-cells and dendritic cells. Journal of Neuroimmunology 216, 819.CrossRefGoogle ScholarPubMed
Pal, P, Daniels, BP, Oskman, A, Diamond, MS, Klein, RS and Goldberg, DE (2016) Plasmodium falciparum histidine-rich protein II compromises brain endothelial barriers and may promote cerebral malaria pathogenesis. MBio 7, pii: e00617-16. doi: 10.1128/mBio.00617-16.Google Scholar
Pax, RA, Siefker, C and Bennett, JL (1984) Schistosoma mansoni: differences in acetylcholine, dopamine, and serotonin control of circular and longitudinal parasite muscles. Experimental Parasitology 58, 314324.Google Scholar
Peña, N, Morales, J, Morales-Montor, J, Vargas-Villavicencio, A, Fleury, A, Zarco, L, de Aluja, AS, Larralde, C, Fragoso, G and Sciutto, E (2007) Impact of naturally acquired Taenia solium cysticercosis on the hormonal levels of free ranging boars. Veterinary Parasitology 149, 134137.Google Scholar
Perry, GH (2014) Parasites and human evolution. Evolutionary Anthropology 23, 218228.Google Scholar
Persson, CM, Lambert, H, Vutova, PP, Dellacasa-Lindberg, I, Nederby, J, Yagita, H, Ljunggren, HG, Grandien, A, Barragan, A and Chambers, BJ (2009) Transmission of Toxoplasma gondii from infected dendritic cells to natural killer cells. Infection and Immunity 77, 970976.Google Scholar
Piguet, PF, Kan, CD, Vesin, C, Rochat, A, Donati, Y and Barazzone, C (2001) Role of CD40-CVD40L in mouse severe malaria. American Journal of Pathology 159, 733742.Google Scholar
Prandovszky, E, Gaskell, E, Martin, H, Dubey, JP, Webster, JP and McConkey, GA (2011) The neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PLoS ONE 6, e23866.Google Scholar
Radke, JR, Donald, RG, Eibs, A, Jerome, ME, Behnke, MS, Liberator, P and White, MW (2006) Changes in the expression of human cell division autoantigen-1 influence Toxoplasma gondii growth and development. PLoS Pathogens 2, e105.Google Scholar
Rajaram, S, Baylink, DJ and Mohan, S (1997) Insulin-like growth factor-binding proteins in serum and other biological fluids: regulation and functions. Endocrine Reviews 18, 801831.Google Scholar
Ransohoff, RM and Engelhardt, B (2012) The anatomical and cellular basis of immune surveillance in the central nervous system. Nature Reviews. Immunology 12, 623635.Google Scholar
Rezende, SA, Miranda, TC, Ferreira, MG and Goes, AM (1993) In vitro granuloma modulation induced by immune complexes in human Schistosomiasis mansoni. Brazilian Journal of Medical and Biological Research 26, 207211.Google Scholar
Ribeiro, P, El-Shehabi, F and Patocka, N (2005) Classical transmitters and their receptors in flatworms. Parasitology 131(Suppl.), S19S40.Google Scholar
Ross, AG, McManus, DP, Farrar, J, Hunstman, RJ, Gray, DJ and Li, YS (2012) Neuroschistosomiasis. Journal of Neurology 259, 2232.CrossRefGoogle ScholarPubMed
Sáenz, B, Fleury, A, Chavarría, A, Hernández, M, Crispin, JC, Vargas-Rojas, MI, Fragoso, G and Sciutto, E (2012) Neurocysticercosis: local and systemic immune-inflammatory features related to severity. Medical Microbiology and Immunology 201, 7380.Google Scholar
Sambo, MR, Trovoada, MJ, Benchimol, C, Quinhentos, V, Gonçalves, L, Velosa, R, Marques, MI, Sepúlveda, N, Clark, TG, Mustafa, S, Wagner, O, Coutinho, A and Penha-Gonçalves, C (2010) Transforming growth factor beta 2 and heme oxygenase 1 genes are risk factors for the cerebral malaria syndrome in Angolan children. PLoS ONE 5, e11141.Google Scholar
Schramm, G, Mohrs, K, Wodrich, M, Doenhoff, MJ, Pearce, EJ, Haas, H and Mohrs, M (2007) Cutting edge: IPSE/alpha-1, a glycoprotein from Schistosoma mansoni eggs, induces IgE-dependent, antigen-independent IL-4 production by murine basophils in vivo. Journal of Immunology 178, 60236027.Google Scholar
Schuindt, SH, Oliveira, BC, Pimentel, PM, Resende, TL, Retamal, CA, DaMatta, RA, Seipel, D and Arnholdt, AC (2012) Secretion of multi-protein migratory complex induced by Toxoplasma gondii infection in macrophages involves the uPA/uPAR activation system. Veterinary Parasitology 186, 207215.Google Scholar
Sciutto, E, Fragoso, G, Fleury, A, Laclette, JP, Sotelo, J, Aluja, A, Vargas, L and Larralde, C (2000) Taenia solium disease in humans and pigs: an ancient parasitosis disease rooted in developing countries and emerging as a major health problem of global dimensions. Microbes and Infection 2, 18751890.Google Scholar
Scrimgeour, EM and Gajdusek, DC (1985) Involvement of the central nervous system in Schistosoma mansoni and S. haematobium infection. A review. Brain 108(Pt 4), 10231038.CrossRefGoogle ScholarPubMed
Seipel, D, Oliveira, BC, Resende, TL, Schuindt, SH, Pimentel, PM, Kanashiro, MM and Arnholdt, AC (2010) Toxoplasma gondii infection positively modulates the macrophages migratory molecular complex by increasing matrix metalloproteinases, CD44 and alpha v beta 3 integrin. Veterinary Parasitology 169, 312319.Google Scholar
Shi, Y and Massagué, J (2003) Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113, 685700.Google Scholar
Shrivastava, SK, Dalko, E, Delcroix-Genete, D, Herbert, F, Cazenave, PA and Pied, S (2017) Uptake of parasite-derived vesicles by astrocytes and microglial phagocytosis of infected erythrocytes may drive neuroinflammation in cerebral malaria. Glia 65, 7592.Google Scholar
Sikasunge, CS, Johansen, MV, Phiri, IK, Willingham, AL and Leifsson, PS (2009) The immune response in Taenia solium neurocysticercosis in pigs is associated with astrogliosis, axonal degeneration and altered blood-brain barrier permeability. Veterinary Parasitology 160, 242250.Google Scholar
Sousa-Pereira, SR, Teixeira, AL, Silva, LC, Souza, AL, Antunes, CM, Teixeira, MM and Lambertucci, JR (2006) Serum and cerebral spinal fluid levels of chemokines and Th2 cytokines in Schistosoma mansoni myeloradiculopathy. Parasite Immunology 28, 473478.Google Scholar
Sun, XJ, Li, R, Sun, X, Zhou, Y, Wang, Y, Liu, XJ, Lu, Q, Zhou, CL and Wu, ZD (2012) Unique roles of Schistosoma japonicum protein Sj16 to induce IFN-γ and IL-10 producing CD4(+)CD25(+) regulatory T cells in vitro and in vivo. Parasite Immunology 34, 430439.Google Scholar
Taft, AS, Norante, FA and Yoshino, TP (2010) The identification of inhibitors of Schistosoma mansoni miracidial transformation by incorporating a medium-throughput small-molecule screen. Experimental Parasitology 125, 8494.Google Scholar
Taman, A and Ribeiro, P (2009) Investigation of a dopamine receptor in Schistosoma mansoni: functional studies and immunolocalization. Molecular & Biochemical Parasitology 168, 2433.Google Scholar
Tan, IJ, Peeva, E and Zandman-Goddard, G (2015) Hormonal modulation of the immune system – a spotlight on the role of progestogens. Autoimmunity Reviews 14, 536542.Google Scholar
Tardieux, I and Ménard, R (2008) Migration of Apicomplexa across biological barriers: the Toxoplasma and Plasmodium rides. Traffic 9, 627635.Google Scholar
Terrazas, LI, Bojalil, R, Govezensky, T and Larralde, C (1994) A role for 17-beta-estradiol in immunoendocrine regulation of murine cysticercosis (Taenia crassiceps). Journal of Parasitology 80, 563568.Google Scholar
Togbe, D, de Sousa, PL, Fauconnier, M, Boissay, V, Fick, L, Scheu, S, Pfeffer, K, Menard, R, Grau, GE, Doan, BT, Beloeil, JC, Renia, L, Hansen, AM, Ball, HJ, Hunt, NH, Ryffel, B and Quesniaux, VF (2008) Both functional LTbeta receptor and TNF receptor 2 are required for the development of experimental cerebral malaria. PLoS ONE 3, e2608.CrossRefGoogle ScholarPubMed
Torrey, EF, Bartko, JJ, Lun, ZR and Yolken, RH (2007) Antibodies to Toxoplasma gondii in patients with schizophrenia: a meta-analysis. Schizophrenia Bulletin 33, 729736.CrossRefGoogle ScholarPubMed
Ueno, N and Lodoen, MB (2015) From the blood to the brain: avenues of eukaryotic pathogen dissemination to the central nervous system. Current Opinion in Microbiology 26, 5359.Google Scholar
Unno, A, Kitoh, K and Takashima, Y (2010) Up-regulation of hyaluronan receptors in Toxoplasma gondii-infected monocytic cells. Biochemical and Biophysical Research Communications 391, 477480.Google Scholar
Valdez, RA, Jiménez, P, Fernández Presas, AM, Aguilar, L, Willms, K and Romano, MC (2014) Taenia solium tapeworms synthesize corticosteroids and sex steroids in vitro. General and Comparative Endocrinology 205, 6267.Google Scholar
Van Den Ham, KM, Shio, MT, Rainone, A, Fournier, S, Krawczyk, CM and Olivier, M (2015) Iron prevents the development of experimental cerebral malaria by attenuating CXCR3-mediated T cell chemotaxis. PLoS ONE 10, e0118451.Google Scholar
Verastegui, MR, Mejia, A, Clark, T, Gavidia, CM, Mamani, J, Ccopa, F, Angulo, N, Chile, N, Carmen, R, Medina, R, García, HH, Rodriguez, S, Ortega, Y and Gilman, RH (2015) Novel rat model for neurocysticercosis using Taenia solium. American Journal of Pathology 185, 22592268.CrossRefGoogle ScholarPubMed
Vignali, DA, Collison, LW and Workman, CJ (2008) How regulatory T cells work. Nature Reviews. Immunology 8, 523532.Google Scholar
Vleugels, MP, Brabin, B, Eling, WM and de Graaf, R (1989) Cortisol and Plasmodium falciparum infection in pregnant women in Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 173177.CrossRefGoogle ScholarPubMed
Wang, HL, Wang, GH, Li, QY, Shu, C, Jiang, MS and Guo, Y (2006) Prevalence of Toxoplasma infection in first-episode schizophrenia and comparison between Toxoplasma-seropositive and Toxoplasma-seronegative schizophrenia. Acta Psychiatrica Scandinavica 114, 4048.Google Scholar
Wassmer, SC, Combes, V and Grau, GE (2003) Pathophysiology of cerebral malaria: role of host cells in the modulation of cytoadhesion. Annals of the New York Academy of Sciences 992, 3038.Google Scholar
Weidner, JM, Kanatani, S, Hernández-Castañeda, MA, Fuks, JM, Rethi, B, Wallin, RP and Barragan, A (2013) Rapid cytoskeleton remodelling in dendritic cells following invasion by Toxoplasma gondii coincides with the onset of a hypermigratory phenotype. Cellular Microbiology 15, 17351752.Google Scholar
White, AC (2000) Neurocysticercosis: updates on epidemiology, pathogenesis, diagnosis, and management. Annual Review of Medicine 51, 187206.Google Scholar
Wilson, RA (2012) Virulence factors of schistosomes. Microbes and Infection 14, 14421450.Google Scholar
Wu, JJ, Chen, G, Liu, J, Wang, T, Zheng, W and Cao, YM (2010) Natural regulatory T cells mediate the development of cerebral malaria by modifying the pro-inflammatory response. Parasitology International 59, 232241.Google Scholar
Zhou, S, Jin, X, Chen, X, Zhu, J, Xu, Z, Wang, X, Liu, F, Hu, W, Zhou, L and Su, C (2015) Heat shock protein 60 in eggs specifically induces Tregs and reduces liver immunopathology in mice with Schistosomiasis japonica. PLoS ONE 10, e0139133.Google Scholar