Morphological and biochemical repercussions of Toxoplasma gondii infection in a 3D human brain neurospheres model

Brain, Behavior, & Immunity - Health - Tập 11 - Trang 100190 - 2021
Paulo Emilio Correa Leite1,2, Juliana de Araujo Portes1, Mariana Rodrigues Pereira3, Fabiele Baldino Russo4, Erica S. Martins-Duarte1,5, Nathalia Almeida dos Santos4,6, Marcia Attias1, Francisco J. Barrantes7, Patricia Cristina Baleeiro Beltrão-Braga4,8, Wanderley de Souza1
1Institute of Biophysics Carlos Chagas Filho and National Center for Structural Biology and Bioimaging (CENABIO), Federal University of Rio de Janeiro, RJ, Brazil
2Directory of Metrology Applied to Life Sciences (Dimav), National Institute of Metrology Quality and Technology (INMETRO), Duque de Caxias, RJ, Brazil
3Biology Institute, Fluminense Federal University, Niteroi, RJ, Brazil
4Laboratory of Disease Modeling, Department of Microbiology, Institute of Biomedical Science, University of São Paulo, São Paulo, SP, Brazil
5Department of Parasitology, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil
6Centre for Stem Cells and Regenerative Medicine, King’s College London, Guy’s Hospital, London, UK
7Laboratory of Molecular Neurobiology, Institute for Biomedical Research (BIOMED), UCA-CONICET, Buenos Aires, Argentina
8Scientific Platform Pasteur-USP, São Paulo, SP, Brazil

Tài liệu tham khảo

Akdis, 2016, Interleukins (from IL-1 to IL-38), interferons, transforming growth factor beta, and TNF-alpha: receptors, functions, and roles in diseases, J. Allergy Clin. Immunol., 138, 984, 10.1016/j.jaci.2016.06.033 Albuquerque, 2013, Kynurenic acid as an antagonist of alpha7 nicotinic acetylcholine receptors in the brain: facts and challenges, Biochem. Pharmacol., 85, 1027, 10.1016/j.bcp.2012.12.014 Arling, 2009, Toxoplasma gondii antibody titers and history of suicide attempts in patients with recurrent mood disorders, J. Nerv. Ment. Dis., 197, 905, 10.1097/NMD.0b013e3181c29a23 Banerjee, 2012, Regulation of GABAergic inputs to CA1 pyramidal neurons by nicotinic receptors and kynurenic acid, J. Pharmacol. Exp. Therapeut., 341, 500, 10.1124/jpet.111.189860 Barbosa, 2020, Spontaneous T. gondii neuronal encystment induces structural neuritic network impairment associated with changes of tyrosine hydroxilase expression, Neurosci. Lett., 718, 10.1016/j.neulet.2019.134721 Benevides, 2008, CCR2 receptor is essential to activate microbicidal mechanisms to control Toxoplasma gondii infection in the central nervous system, Am. J. Pathol., 173, 741, 10.2353/ajpath.2008.080129 Berdoy, 2000, Fatal attraction in rats infected with Toxoplasma gondii, Proc. Biol. Sci., 267, 1591, 10.1098/rspb.2000.1182 Berenreiterova, 2011, The distribution of Toxoplasma gondii cysts in the brain of a mouse with latent toxoplasmosis: implications for the behavioral manipulation hypothesis, PloS One, 6, 10.1371/journal.pone.0028925 Berk, 2007, Dopamine dysregulation syndrome: implications for a dopamine hypothesis of bipolar disorder, Acta Psychiatr. Scandinavica. Supplementum, 41, 10.1111/j.1600-0447.2007.01058.x Bertoli, 1995, A spectrum in the pathology of toxoplasmosis in patients with acquired immunodeficiency syndrome, Arch. Pathol. Lab Med., 119, 214 Biswas, 2015, Ly6C(high) monocytes control cerebral toxoplasmosis, J. Immunol., 194, 3223, 10.4049/jimmunol.1402037 Blader, 2015, Lytic cycle of toxoplasma gondii: 15 Years later, Annu. Rev. Microbiol., 69, 463, 10.1146/annurev-micro-091014-104100 Boillat, 2020, Neuroinflammation-associated aspecific manipulation of mouse predator fear by toxoplasma gondii, Cell Rep., 30, 320, 10.1016/j.celrep.2019.12.019 Boyle, 2007, Toxoplasma gondii: inconsistent dissemination patterns following oral infection in mice, Exp. Parasitol., 116, 302, 10.1016/j.exppara.2007.01.010 Brenier-Pinchart, 2004, Infection of human astrocytes and glioblastoma cells with Toxoplasma gondii: monocyte chemotactic protein-1 secretion and chemokine expression in vitro, Acta Neuropathol., 107, 245, 10.1007/s00401-003-0804-0 Brisch, 2014, The role of dopamine in schizophrenia from a neurobiological and evolutionary perspective: old fashioned, but still in vogue, Front. Psychiatr., 5, 47 Brito, 2012, Expression of A1 adenosine receptors in the developing avian retina: in vivo modulation by A(2A) receptors and endogenous adenosine, J. Neurochem., 123, 239, 10.1111/j.1471-4159.2012.07909.x Brooks, 2015, Toxoplasma gondii infections alter GABAergic synapses and signaling in the central nervous system, mBio, 6, 10.1128/mBio.01428-15 Cabral, 2014, 3-D imaging and analysis of neurons infected in vivo with Toxoplasma gondii, J. Vis. Exp., 94 Caton, 2020, The role of nicotinic cholinergic neurotransmission in delusional thinking, NPJ Schizophrenia, 6, 16, 10.1038/s41537-020-0105-9 Chaves, 2001, IL-4 and IL-13 regulate the induction of indoleamine 2,3-dioxygenase activity and the control of Toxoplasma gondii replication in human fibroblasts activated with IFN-gamma, Eur. J. Immunol., 31, 333, 10.1002/1521-4141(200102)31:2<333::AID-IMMU333>3.0.CO;2-X Chumpitazi, 1998, Human platelet inhibition of Toxoplasma gondii growth, Clin. Exp. Immunol., 111, 325, 10.1046/j.1365-2249.1998.00499.x Coppin, 2003, Developmentally regulated biosynthesis of carbohydrate and storage polysaccharide during differentiation and tissue cyst formation in Toxoplasma gondii, Biochimie, 85, 353, 10.1016/S0300-9084(03)00076-2 David, 2016, GLT-1-Dependent disruption of CNS glutamate homeostasis and neuronal function by the Protozoan parasite toxoplasma gondii, PLoS Pathog., 12, 10.1371/journal.ppat.1005643 Deckert-Schluter, 1997, Interleukin-10 downregulates the intracerebral immune response in chronic Toxoplasma encephalitis, J. Neuroimmunol., 76, 167, 10.1016/S0165-5728(97)00047-7 Del Grande, 2017, Is toxoplasma gondii a trigger of bipolar disorder?, Pathogens, 6, 10.3390/pathogens6010003 Dickerson, 2018, Clinical and serological predictors of suicide in schizophrenia and major mood disorders, J. Nerv. Ment. Dis., 206, 173, 10.1097/NMD.0000000000000772 Dickerson, 2014, Antibodies to Toxoplasma gondii and cognitive functioning in schizophrenia, bipolar disorder, and nonpsychiatric controls, J. Nerv. Ment. Dis., 202, 589, 10.1097/NMD.0000000000000166 Dickerson, 2017, Suicide attempts and markers of immune response in individuals with serious mental illness, J. Psychiatr. Res., 87, 37, 10.1016/j.jpsychires.2016.11.011 Donley, 2016, Huntingtons disease mice infected with toxoplasma gondii demonstrate early kynurenine pathway activation, altered CD8+ T-cell responses, and premature mortality, PloS One, 11, 10.1371/journal.pone.0162404 Elsheikha, 2016, The known and missing links between Toxoplasma gondii and schizophrenia, Metab. Brain Dis., 31, 749, 10.1007/s11011-016-9822-1 Evans, 2014, Patterns of Toxoplasma gondii cyst distribution in the forebrain associate with individual variation in predator odor avoidance and anxiety-related behavior in male Long-Evans rats, Brain Behav. Immun., 37, 122, 10.1016/j.bbi.2013.11.012 Eyles, 2012, Schizophrenia: do all roads lead to dopamine or is this where they start? Evidence from two epidemiologically informed developmental rodent models, Transl. Psychiatry, 2, e81, 10.1038/tp.2012.6 Fischer, 1997, Host cells of Toxoplasma gondii encystation in infected primary culture from mouse brain, Parasitol. Res., 83, 637, 10.1007/s004360050311 Fischer, 1997, Cytokine responses induced by Toxoplasma gondii in astrocytes and microglial cells, Eur. J. Immunol., 27, 1539, 10.1002/eji.1830270633 Flegr, 2002, Increased risk of traffic accidents in subjects with latent toxoplasmosis: a retrospective case-control study, BMC Infect. Dis., 2, 11, 10.1186/1471-2334-2-11 Flegr, 2018, Toxoplasmosis, but not borreliosis, is associated with psychiatric disorders and symptoms, Schizophr. Res., 197, 603, 10.1016/j.schres.2018.02.008 Flegr, 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?, Biol. Psychol., 63, 253, 10.1016/S0301-0511(03)00075-9 Fond, 2018, Latent toxoplasma infection in real-world schizophrenia: results from the national FACE-SZ cohort, Schizophr. Res., 201, 373, 10.1016/j.schres.2018.05.007 Gazzinelli, 1993, Acute cerebral toxoplasmosis is induced by in vivo neutralization of TNF-alpha and correlates with the down-regulated expression of inducible nitric oxide synthase and other markers of macrophage activation, J. Immunol., 151, 3672, 10.4049/jimmunol.151.7.3672 Gazzinelli, 1996, In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha, J. Immunol., 157, 798, 10.4049/jimmunol.157.2.798 Halonen, 1996, Growth and development of Toxoplasma gondii in human neurons and astrocytes, JNEN (J. Neuropathol. Exp. Neurol.), 55, 1150, 10.1097/00005072-199611000-00006 Hamdani, 2017, Effects of cumulative herpesviridae and toxoplasma gondii infections on cognitive function in healthy, bipolar, and schizophrenia subjects, J. Clin. Psychiatr., 78, e18, 10.4088/JCP.15m10133 Havlicek, 2001, Decrease of psychomotor performance in subjects with latent ’asymptomatic’ toxoplasmosis, Parasitology, 122, 515, 10.1017/S0031182001007624 Hay, 1983, The effect of congenital and adult-acquired Toxoplasma infections on the motor performance of mice, Ann. Trop. Med. Parasitol., 77, 261, 10.1080/00034983.1983.11811707 Hermes, 2008, Neurological and behavioral abnormalities, ventricular dilatation, altered cellular functions, inflammation, and neuronal injury in brains of mice due to common, persistent, parasitic infection, J. Neuroinflammation, 5, 48, 10.1186/1742-2094-5-48 Hunter, 1994, Production of gamma interferon by natural killer cells from Toxoplasma gondii-infected SCID mice: regulation by interleukin-10, interleukin-12, and tumor necrosis factor alpha, Infect. Immun., 62, 2818, 10.1128/IAI.62.7.2818-2824.1994 Ingram, 2013, Mice infected with low-virulence strains of Toxoplasma gondii lose their innate aversion to cat urine, even after extensive parasite clearance, PloS One, 8, 10.1371/journal.pone.0075246 Jones, 2001, Congenital toxoplasmosis: a review, Obstet. Gynecol. Surv., 56, 296, 10.1097/00006254-200105000-00025 Khan, 2000, IP-10 is critical for effector T cell trafficking and host survival in Toxoplasma gondii infection, Immunity, 12, 483, 10.1016/S1074-7613(00)80200-9 Kusbeci, 2011, Could Toxoplasma gondii have any role in Alzheimer disease?, Alzheimer Dis. Assoc. Disord., 25, 1, 10.1097/WAD.0b013e3181f73bc2 Lang, 2018, Chronic Toxoplasma infection is associated with distinct alterations in the synaptic protein composition, J. Neuroinflammation, 15, 216, 10.1186/s12974-018-1242-1 Leite, 2019, Suitability of 3D human brain spheroid models to distinguish toxic effects of gold and poly-lactic acid nanoparticles to assess biocompatibility for brain drug delivery, Part. Fibre Toxicol., 16, 22, 10.1186/s12989-019-0307-3 Luft, 1992, Toxoplasmic encephalitis in AIDS, Clin. Infect. Dis. : Off. Publ. Infect. Dis. Soc. Am., 15, 211, 10.1093/clinids/15.2.211 Mahmoudvand, 2015, The possible association between Toxoplasma gondii infection and risk of anxiety and cognitive disorders in BALB/c mice, Pathog. Glob. Health, 109, 369, 10.1080/20477724.2015.1117742 Mahmoudvand, 2016, Toxoplasma gondii infection promotes neuroinflammation through cytokine networks and induced hyperalgesia in BALB/c mice, Inflammation, 39, 405, 10.1007/s10753-015-0262-6 Markovitz, 2015, Toxoplasma gondii and anxiety disorders in a community-based sample, Brain Behav. Immun., 43, 192, 10.1016/j.bbi.2014.08.001 Martin, 2015, Effect of parasitic infection on dopamine biosynthesis in dopaminergic cells, Neuroscience, 306, 50, 10.1016/j.neuroscience.2015.08.005 Martynowicz, 2019, Guanabenz reverses a key behavioral change caused by latent toxoplasmosis in mice by reducing neuroinflammation, mBio, 10, 10.1128/mBio.00381-19 McConkey, 2013, Toxoplasma gondii infection and behaviour - location, location, location?, J. Exp. Biol., 216, 113, 10.1242/jeb.074153 Mitra, 2013, Toxoplasma gondii infection induces dendritic retraction in basolateral amygdala accompanied by reduced corticosterone secretion, Dis. Models Mechan., 6, 516, 10.1242/dmm.009928 Montoya, 2004, Toxoplasmosis, Lancet, 363, 1965, 10.1016/S0140-6736(04)16412-X Nissen, 2017, The disease burden of congenital toxoplasmosis in Denmark, PloS One, 12, 10.1371/journal.pone.0178282 Pamies, 2017, A human brain microphysiological system derived from induced pluripotent stem cells to study neurological diseases and toxicity, ALTEX, 34, 362, 10.14573/altex.1609122 Pamies, 2014, Biological and medical applications of a brain-on-a-chip, Exp. Biol. Med., 239, 1096, 10.1177/1535370214537738 Pedersen, 2012, Toxoplasma gondii infection and self-directed violence in mothers, Arch. Gen. Psychiatr., 69, 1123, 10.1001/archgenpsychiatry.2012.668 Penzes, 2011, Dendritic spine pathology in neuropsychiatric disorders, Nat. Neurosci., 14, 285, 10.1038/nn.2741 Prandovszky, 2011, The neurotropic parasite Toxoplasma gondii increases dopamine metabolism, PloS One, 6, 10.1371/journal.pone.0023866 Quan, 2020, VEGF production is regulated by the AKT/ERK1/2 signaling pathway and controls the proliferation of toxoplasma gondii in ARPE-19 cells, Front. Cellular Infect. Microbiol., 10, 184, 10.3389/fcimb.2020.00184 Robert-Gangneux, 2015, Molecular diagnosis of toxoplasmosis in immunocompromised patients: a 3-year multicenter retrospective study, J. Clin. Microbiol., 53, 1677, 10.1128/JCM.03282-14 Samojlowicz, 2019, Presence of Toxoplasma gondii infection in brain as a potential cause of risky behavior: a report of 102 autopsy cases, Eur. J. Clin. Microbiol. Infect. Dis. : Off. Publ. Eur. Soc. Clin. Microbiol., 38, 305, 10.1007/s10096-018-3427-z Schluter, 2019, Advances and challenges in understanding cerebral toxoplasmosis, Front. Immunol., 10, 242, 10.3389/fimmu.2019.00242 Schluter, 2001, Toxoplasma gondii infection of neurons induces neuronal cytokine and chemokine production, but gamma interferon- and tumor necrosis factor-stimulated neurons fail to inhibit the invasion and growth of T. gondii, Infect. Immun., 69, 7889, 10.1128/IAI.69.12.7889-7893.2001 Schwarcz, 2012, Kynurenines in the mammalian brain: when physiology meets pathology, Nat. Rev. Neurosci., 13, 465, 10.1038/nrn3257 Stone, 2020, Does kynurenic acid act on nicotinic receptors? An assessment of the evidence, J. Neurochem., 152, 627, 10.1111/jnc.14907 Strack, 2002, Chemokines are differentially expressed by astrocytes, microglia and inflammatory leukocytes in Toxoplasma encephalitis and critically regulated by interferon-gamma, Acta Neuropathol., 103, 458, 10.1007/s00401-001-0491-7 Sutterland, 2015, Beyond the association. Toxoplasma gondii in schizophrenia, bipolar disorder, and addiction: systematic review and meta-analysis, Acta Psychiatr. Scand., 132, 161, 10.1111/acps.12423 Takahashi, 2006, Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors, Cell, 126, 663, 10.1016/j.cell.2006.07.024 Tonin, 2014, Influence of toxoplasmosis on acetylcholinesterase activity, nitric oxide levels and cellular lesion on the brain of mice, Pathol. Res. Pract., 210, 526, 10.1016/j.prp.2014.04.025 Torrey, 2007, Antibodies to Toxoplasma gondii in patients with schizophrenia: a meta-analysis, Schizophr. Bull., 33, 729, 10.1093/schbul/sbl050 Trevizan, 2019, Acute Toxoplasma gondii infection alters the number of neurons and the proportion of enteric glial cells in the duodenum in Wistar rats, Neuro Gastroenterol. Motil. : Off. J. Eur. Gastrointest. Motility Soc., 31 Tyebji, 2019, Toxoplasmosis: a pathway to neuropsychiatric disorders, Neurosci. Biobehav. Rev., 96, 72, 10.1016/j.neubiorev.2018.11.012 Vyas, 2007, Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors, Proc. Natl. Acad. Sci. U. S. A, 104, 6442, 10.1073/pnas.0608310104 Wang, 2019, From inflammatory reactions to neurotransmitter changes: implications for understanding the neurobehavioral changes in mice chronically infected with Toxoplasma gondii, Behav. Brain Res., 359, 737, 10.1016/j.bbr.2018.09.011 Witting, 1979, Learning capacity and memory of normal and Toxoplasma-infected laboratory rats and mice, Zeitschrift Parasitenkunde, 61, 29, 10.1007/BF00927085 Xiao, 2014, MicroRNA-132 dysregulation in Toxoplasma gondii infection has implications for dopamine signaling pathway, Neuroscience, 268, 128, 10.1016/j.neuroscience.2014.03.015 Zafeiriou, 2020, Developmental GABA polarity switch and neuronal plasticity in Bioengineered Neuronal Organoids, Nat. Commun., 11, 3791, 10.1038/s41467-020-17521-w Zhang, 2001, Initial characterization of CST1, a Toxoplasma gondii cyst wall glycoprotein, Infect. Immun., 69, 501, 10.1128/IAI.69.1.501-507.2001