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Early immune responses and parasite tissue distribution in mice experimentally infected with oocysts of either archetypal or non-archetypal genotypes of Toxoplasma gondii

Published online by Cambridge University Press:  14 December 2020

Daniela P. Chiebao*
Department of Preventive Veterinary Medicine, Faculty of Veterinary Medicine and Animal Science – FMVZ, University of Sao Paulo, 87 Professor Doutor Orlando Marques de Paiva Avenue, 05508-270São Paulo, Brazil
Paul M. Bartley
Moredun Research Institute, Pentland Science Park, Bush Loan, EdinburghEH26 0PZ, UK
Francesca Chianini
Moredun Research Institute, Pentland Science Park, Bush Loan, EdinburghEH26 0PZ, UK
Lauren E. Black
Moredun Research Institute, Pentland Science Park, Bush Loan, EdinburghEH26 0PZ, UK
Alison Burrells
Moredun Research Institute, Pentland Science Park, Bush Loan, EdinburghEH26 0PZ, UK
Hilda F. J. Pena
Department of Preventive Veterinary Medicine, Faculty of Veterinary Medicine and Animal Science – FMVZ, University of Sao Paulo, 87 Professor Doutor Orlando Marques de Paiva Avenue, 05508-270São Paulo, Brazil
Rodrigo M. Soares
Department of Preventive Veterinary Medicine, Faculty of Veterinary Medicine and Animal Science – FMVZ, University of Sao Paulo, 87 Professor Doutor Orlando Marques de Paiva Avenue, 05508-270São Paulo, Brazil
Elisabeth A. Innes
Moredun Research Institute, Pentland Science Park, Bush Loan, EdinburghEH26 0PZ, UK
Frank Katzer
Moredun Research Institute, Pentland Science Park, Bush Loan, EdinburghEH26 0PZ, UK
Author for correspondence: Daniela P. Chiebao, E-mail:


In most of the world Toxoplasma gondii is comprised of archetypal types (types I, II and III); however, South America displays several non-archetypal strains. This study used an experimental mouse model to characterize the immune response and parasite kinetics following infection with different parasite genotypes. An oral inoculation of 50 oocysts per mouse from T. gondii M4 type II (archetypal, avirulent), BrI or BrIII (non-archetypal, virulent and intermediate virulent, respectively) for groups (G)2, G3 and G4, respectively was used. The levels of mRNA expression of cytokines, immune compounds, cell surface markers and receptor adapters [interferon gamma (IFNγ), interleukin (IL)-12, CD8, CD4, CD25, CXCR3 and MyD88] were quantified by SYBR green reverse transcription-quantitative polymerase chain reaction. Lesions were characterized by histology and detection by immunohistochemistry established distribution of parasites. Infection in G2 mice was mild and characterized by an early MyD88-dependent pathway. In G3, there were high levels of expression of pro-inflammatory cytokines IFNγ and IL-12 in the mice showing severe clinical symptoms at 8–11 days post infection (dpi), combined with the upregulation of CD25, abundant tachyzoites and tissue lesions in livers, lungs and intestines. Significant longer expression of IFNγ and IL-12 genes, with other Th1-balanced immune responses, such as increased levels of CXCR3 and MyD88 in G4, resulted in survival of mice and chronic toxoplasmosis, with the occurrence of tissue cysts in brain and lungs, at 14 and 21 dpi. Different immune responses and kinetics of gene expression appear to be elicited by the different strains and non-archetypal parasites demonstrated higher virulence.

Research Article
Copyright © The Author(s) 2020. Published by Cambridge University Press

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Ajioka, JW and Soldati, D (2007). Genetics and genome organization of Toxoplasma gondii. In Ajioka, JW and Soldati, D (eds), Toxoplasma: Molecular and Cellular Biology. Wymondham: Horizon Bioscience, pp. 193207.Google Scholar
Ajzenberg, D, Cogné, N, Paris, L, Bessières, M-H, Thulliez, P, Filisetti, D, Pelloux, H, Marty, P and Dardé, M-L (2002) Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical findings. The Journal of Infectious Diseases 186, 684689.CrossRefGoogle ScholarPubMed
Barragan, A and Sibley, LD (2002) Transepithelial migration of Toxoplasma gondii is linked to parasite motility and virulence. Journal of Experimental Medicine 195, 16251633.CrossRefGoogle ScholarPubMed
Bartley, PM, Katzer, F, Rocchi, MS, Maley, SW, Benavides, J, Nath, M, Pang, Y, Cantón, G, Thomson, J, Chianini, F and Innes, EA (2013 a) Development of maternal and foetal immune responses in cattle following experimental challenge with Neospora caninum at day 210 of gestation. Veterinary Research 44, 91.CrossRefGoogle ScholarPubMed
Bartley, PM, Wright, SE, Zimmer, IA, Roy, S, Kitchener, AC, Meredith, A, Innes, EA and Katzer, F (2013 b) Detection of Neospora caninum in wild carnivorans in Great Britain. Veterinary Parasitology 192, 279283.CrossRefGoogle ScholarPubMed
Bartley, PM, Burrells, A, Benavides, J, Canton, G, Garcia, JL, Thomson, J, Chianini, F, Innes, EA and Katzer, F (2019) Cell mediated and innate immune responses in pigs following vaccination and challenge with Toxoplasma Parasites. Veterinary Parasitology 275, 108963.CrossRefGoogle ScholarPubMed
Benavides, J, Maley, S, Pang, Y, Palarea, J, Eaton, S, Katzer, F, Innes, EA, Buxton, D and Chianini, F (2011) Development of lesions and tissue distribution of parasite in lambs orally infected with sporulated oocysts of Toxoplasma gondii. Veterinary Parasitology 179, 209215.CrossRefGoogle ScholarPubMed
Bezerra, ECM, dos Santos, SV, dos Santos, TCC, de Andrade, HF and Meireles, LR (2019) Behavioral evaluation of BALB/c (Mus musculus) mice infected with genetically distinct strains of Toxoplasma gondii. Microbial Pathogenesis 126, 279286.CrossRefGoogle ScholarPubMed
Burrells, A, Bartley, PM, Zimmer, IA, Roy, S, Kitchener, AC, Meredith, A, Wright, SE, Innes, EA and Katzer, F (2013) Evidence of the three main clonal Toxoplasma gondii lineages from wild mammalian carnivores in the UK. Parasitology 140, 17681776.CrossRefGoogle ScholarPubMed
Buxton, D, Wright, S, Maley, SW, Rae, AG, Lundén, A and Innes, EA (2001) Immunity to experimental neosporosis in pregnant sheep. Parasite Immunology 23, 8591.CrossRefGoogle ScholarPubMed
Chiebao, DP, Pena, HFDJ, Cabral, AD, Rocca, MP, Lopes, EG, Valadas, SYOB, Keid, LB, Grisi Filho, JHH and Soares, RM (2016) Infection of mice with oocysts of Toxoplasma gondii by oral route showed differences of virulence from Brazilian RFLP genotypes BrI and BrIII. Research in Veterinary Science 107, 257260.CrossRefGoogle ScholarPubMed
Chiebao, DP, Pena, HF, Passarelli, D, Santín, T, Pulz, LH, Strefezzi, RF, Sevá, AP, Martins, CM, Lopes, EG, Grisi-Filho, JHH, Gennari, SM and Soares, RM (2019) Congenital transmission of Toxoplasma gondii after experimental reinfection with Brazilian typical strains in chronically infected sheep. Frontiers in Veterinary Science 6, 111.CrossRefGoogle ScholarPubMed
Chiu, BC, Martin, BE, Stolberg, VR and Chensue, SW (2013) Cutting edge: central memory CD8T cells in aged mice are virtual memory cells. The Journal of Immunology 191, 57935796.CrossRefGoogle Scholar
Dadimoghaddam, Y, Daryani, A, Sharif, M, Ahmadpour, E and Hossienikhah, Z (2014) Tissue tropism and parasite burden of Toxoplasma gondii RH strain in experimentally infected mice. Asian Pacific Journal of Tropical Medicine 7, 521524.CrossRefGoogle ScholarPubMed
Dardé, ML (2008) Toxoplasma gondii, ‘new’ genotypes and virulence. Parasite 15, 366371.CrossRefGoogle ScholarPubMed
Detavernier, A, Azouz, A, Shehade, H, Splittgerber, M, Van Maele, L, Nguyen, M, Thomas, S, Achouri, Y, Svec, D, Calonne, E, Fuks, F, Oldenhove, G and Goriely, S (2019) Monocytes undergo multi-step differentiation in mice during oral infection by Toxoplasma gondii. Communications Biology 2, 114.CrossRefGoogle ScholarPubMed
Dubey, JP (2010) Toxoplasmosis of Animals and Humans, 2nd Edn. Boca Raton: CRC Press.Google Scholar
Dubey, JP and Beattie, CP (1988) Toxoplasmosis of Animals and Man. Boca Raton: CRC Press.Google Scholar
Dubey, JP, Lago, EG, Gennari, SM, Su, C and Jones, JL (2012) Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology 139, 13751424.CrossRefGoogle ScholarPubMed
Elbez-Rubinstein, A, Ajzenberg, D, Dardé, M-L, Cohen, R, Dumètre, A, Yera, H, Gondon, E, Janaud, JC and Thulliez, P (2009) Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection and review. Journal of Infectious Diseases 199, 280285.CrossRefGoogle ScholarPubMed
Fournier, GFDSR, Lopes, MG, Marcili, A, Ramirez, DG, Acosta, ICL, Giuli da Silva Ferreira, JI, Cabral, AD, Ribeiro de Lima, JT, Fatima de Jesus Pena, H, Dias, RA and Gennari, SM (2014) Toxoplasma gondii in domestic and wild animals from forest fragments of the municipality of Natal, Northeastern Brazil. Revista Brasileira de Parasitologia Veterinaria 23, 501508.CrossRefGoogle Scholar
Fox, BA, Rommerein, LM, Guevara, RB, Falla, A, Triana, MAH, Sun, Y and Bzik, DJ (2016) The Toxoplasma gondii rhoptry kinome is essential for chronic infection. mBio 7, e00193–16.CrossRefGoogle ScholarPubMed
Ganesan, AP, Johansson, M, Ruffell, B, Yagui-Beltran, A, Lau, J, Jablons, DM and Coussens, LM (2013) Tumor-infiltrating regulatory T cells inhibit endogenous cytotoxic T cell responses to lung adenocarcinoma. The Journal of Immunology 191, 20092017.CrossRefGoogle ScholarPubMed
Gazzinelli, RT, Mendonça-Neto, R, Lilue, J, Howard, J and Sher, A (2014) Innate resistance against Toxoplasma gondii: an evolutionary tale of mice, cats, and men. Cell Host and Microbe 15, 132138.CrossRefGoogle ScholarPubMed
Guiton, PS, Sagawa, JM, Fritz, HM and Boothroyd, JC (2017) An in vitro model of intestinal infection reveals a developmentally regulated transcriptome of Toxoplasma sporozoites and a NF-κB-like signature in infected host cells. PLoS ONE 12, 129.CrossRefGoogle Scholar
Hamilton, C, Robins, R, Thomas, R, Oura, C, Oliveira, S, Villena, I, Innes, EA, Katzer, F and Kelly, PJ (2019) Prevalence and genetic diversity of Toxoplasma gondii in free-ranging chickens from the Caribbean. Acta Parasitologica 64, 738744.CrossRefGoogle ScholarPubMed
Herrmann, DC, Maksimov, P, Hotop, A, Groß, U, Däubener, W, Liesenfeld, O, Pleyer, U, Conraths, FJ and Schares, G (2014) Genotyping of samples from German patients with ocular, cerebral and systemic toxoplasmosis reveals a predominance of Toxoplasma gondii type II. International Journal of Medical Microbiology 304, 911916.CrossRefGoogle ScholarPubMed
Hide, G, Morley, EK, Hughes, JM, Gerwash, O, Elmahaishi, MS, Elmahaishi, KH, Thomasson, D, Wright, EA, Williams, RH, Murphy, RG and Smith, JE (2009) Evidence for high levels of vertical transmission in Toxoplasma gondii. Parasitology 136, 18771885.CrossRefGoogle ScholarPubMed
Hill, RD, Gouffon, JS, Saxton, AM and Su, C (2012) Differential gene expression in mice infected with distinct toxoplasma strains. Infection and Immunity 80, 968974.CrossRefGoogle ScholarPubMed
Hochberg, Y (1988) A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75, 800802.CrossRefGoogle Scholar
Hoeman, CM, Dhakal, M, Zaghouani, AA, Cascio, JA, Wan, X, Khairallah, MT, Chen, W and Zaghouani, H (2013) Developmental expression of IL-12Rbeta2 on murine naive neonatal T cells counters the upregulation of IL-13Ralpha1 on primary Th1 cells and balances immunity in the newborn. The Journal of Immunology 190, 61556163.CrossRefGoogle ScholarPubMed
Howe, DK and Sibley, LD (1995) Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. Journal of Infectious Diseases 172, 15611566.CrossRefGoogle ScholarPubMed
Hurtado, A, Aduriz, G, Moreno, B, Barandika, J and Garcia-Perez, AL (2001) Single tube nested PCR for the detection of Toxoplasma gondii in fetal tissues from naturally aborted ewes. Veterinary Parasitology 102, 1727.CrossRefGoogle ScholarPubMed
Innes, EA and Vermeulen, AN (2006) Vaccination as a control strategy against the coccidial parasites Eimeria, Toxoplasma and Neospora. Parasitology 133, 145168.CrossRefGoogle ScholarPubMed
Jin, Y, Yao, Y, El-Ashram, S, Tian, J, Shen, J and Ji, Y (2019) The neurotropic parasite Toxoplasma gondii induces astrocyte polarization through NFκB pathway. Frontiers in Medicine 6, 17.Google ScholarPubMed
Johnson-Tardieu, JM, Walworth, EW, Cornelius, JG, Ye, X, Schuster, SM and Peck, AB (1996) Autoimmune diabetes-prone NOD mice express the Lyt2 alpha (Lyt2.1) and Lyt3 alpha (Lyt3.1) alleles of CD8. Immunogenetics 43, 612.Google ScholarPubMed
Katzer, F, Canton, G, Burrells, A, Palarea-Albaladejo, J, Horton, B, Bartley, PM, Pang, Y, Chianini, F, Innes, EA and Benavides, J (2014) Immunization of lambs with the S48 strain of Toxoplasma gondii reduces tissue cyst burden following oral challenge with a complete strain of the parasite. Veterinary Parasitology 205, 4656.CrossRefGoogle ScholarPubMed
Kawai, T and Akira, S (2005) Tool-like receptor downstream signaling. Arthritis Research and Therapy 7, 1219.CrossRefGoogle Scholar
Konecki, DS, Brennand, J, Fuscoe, JC, Caskey, CT and Chinault, AC (1982) Hypoxanthine-guanine phosphoribosyl transferase genes of mouse and Chinese hamster: construction and sequence analysis of cDNA recombinants. Nucleic Acids Research 10, 67636775.CrossRefGoogle Scholar
Lopes, FMR, Gonçalves, DD, dos Reis, CR, Breganó, RM, Freire, RL, de Freitas, JC and Navarro, IT (2009) Presence of domesticated cats and visual impairment associated to Toxoplasma gondii serum positive children at an elementary school in Jataizinho, state of Paraná, Brazil. Revista Brasileira de Parasitologia Veterinaria 17, 1215.CrossRefGoogle Scholar
Lu, YY, Dong, H, Feng, YJ, Wang, K, Jiang, YB, Zhang, LX and Yang, YR (2018) Avirulence and lysozyme secretion in Paneth cells after infection of BALB/c mice with oocysts of Toxoplasma gondii strains TgCatCHn2 (ToxoDB#17) and TgCatCHn4 (ToxoDB#9). Veterinary Parasitology 252, 18.CrossRefGoogle Scholar
Martins, GA, Tadokoro, CE, Silva, RB, Silva, JS and Rizzo, LV (2004) CTLA-4 blockage increases resistance to infection with the intracellular protozoan Trypanosoma cruzi. The Journal of Immunology 172, 48934901.CrossRefGoogle ScholarPubMed
Massad, E, Menezes, RX, Silveira, PSP and Ortega, NRS (2004) Métodos Quantitativos em Medicina. Barueri: Manole.Google Scholar
Meireles, LR, Ekman, CCJ, De Andrade Júnior, HF and Luna, EJDA (2015) Human toxoplasmosis outbreaks and the agent infecting form. Findings from a systematic review. Journal of the Institute of Tropical Medicine of Sao Paulo 57, 369376.CrossRefGoogle ScholarPubMed
Mendes, NHD, Oliveira, CBS, Garcia, CA, Holanda, CMXC and Andrade-Neto, VF (2014) Epidemiological and serological profiles of ocular toxoplasmosis in the municipality of Natal, Northeastern Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 108, 656661.CrossRefGoogle Scholar
Miller, CM, Boulter, NR, Ikin, RJ and Smith, NC (2009) The immunobiology of the innate response to Toxoplasma gondii. International Journal for Parasitology 39, 2339.CrossRefGoogle ScholarPubMed
Minitab (2019) Suporte ao Minitab 18. Available at Scholar
Mordue, DG, Monroy, F, La Regina, M, Dinarello, CA and Sibley, LD (2001) Acute toxoplasmosis leads to lethal overproduction of Th1 cytokines. Journal of immunology (Baltimore, Md.: 1950) 167, 45744584.CrossRefGoogle ScholarPubMed
Pena, HFJ, Soares, RM, Amaku, M, Dubey, JP and Gennari, SM (2006) Toxoplasma gondii infection in cats from São Paulo state, Brazil: seroprevalence, oocyst shedding, isolation in mice, and biologic and molecular characterization. Research in Veterinary Science 81, 5867.CrossRefGoogle Scholar
Pena, HFJ, Gennari, SM, Dubey, JP and Su, C (2008) Population structure and mouse-virulence of Toxoplasma gondii in Brazil. International Journal for Parasitology 38, 561569.CrossRefGoogle ScholarPubMed
Pena, HFJ, Pinheiro, TM, Soares, HS, Oliveira, S, Alves, BF, Ferreira, MN and Gennari, SM (2018 a) Typical Brazilian genotype of Toxoplasma gondii isolated from a horse destined for human consumption in Europe from a slaughterhouse. Parasitology Research 117, 33053308.CrossRefGoogle ScholarPubMed
Pena, HFJ, Alves, BF, Soares, HS, Oliveira, S, Ferreira, MN, Bricarello, PA, Machado, TMP, Castro, BBP and Gennari, SM (2018 b) Free-range chickens from Santa Catarina state, southern Brazil, as asymptomatic intermediate hosts for Toxoplasma gondii clonal type I and typical Brazilian genotypes. Veterinary Parasitology: Regional Studies and Reports 13, 5559.Google Scholar
Saeij, JPJ, Boyle, JP and Boothroyd, JC (2005) Differences among the three major strains of Toxoplasma gondii and their specific interactions with the infected host. Trends in Parasitology 21, 476481.CrossRefGoogle ScholarPubMed
Sánchez-Sánchez, R, Ferre, I, Regidor-Cerrillo, J, Gutiérrez-Expósito, D, Ferrer, LM, Arteche-Villasol, N, Moreno-Gonzalo, J, Müller, J, Aguado-Martínez, A, Pérez, V, Hemphill, A, Ortega-Mora, LM and Benavides, J (2019) Virulence in mice of a Toxoplasma gondii type II isolate does not correlate with the outcome of experimental infection in pregnant sheep. Frontiers in Cellular and Infection Microbiology 9, 118.Google Scholar
Shaw, MH, Freeman, GJ, Scott, MF, Fox, BA, Bzik, DJ, Belkaid, Y and Yap, GS (2006) Tyk2 negatively regulates adaptive Th1 immunity by mediating IL-10 signaling and promoting IFN-gamma dependent IL-10 reactivation. Journal of immunology (Baltimore, Md.: 1950) 176, 72637271.CrossRefGoogle ScholarPubMed
Shibata, K, Yamada, H, Nakamura, M, Hatano, S, Katsuragi, Y, Kominami, R and Yoshikai, Y (2014) IFN-gamma-producing and IL-17-producing gammadelta T cells differentiate at distinct developmental stages in murine fetal thymus. The Journal of Immunology 192, 22102218.CrossRefGoogle ScholarPubMed
Shwab, EK, Zhu, XQ, Majumdar, D, Pena, HFJ, Gennari, SM, Dubey, JP and Su, C (2014) Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology 141, 453461.CrossRefGoogle ScholarPubMed
Sibley, DL, Mordue, D and Howe, DK (1999) Experimental approaches to understanding virulence in toxoplasmosis. Immunobiology 201, 210224.CrossRefGoogle ScholarPubMed
Silva, MA, Pena, HFJ, Soares, HS, Aizawa, J, Oliveira, S, Alves, BF, Souza, DS, Melo, RPB, Gennari, SM, Mota, RA and Silva, JCR (2018) Isolation and genetic characterization of Toxoplasma gondii from free-ranging and captive birds and mammals in Pernambuco State, Brazil. Revista Brasileira de Parasitologia Veterinaria 27, 481487.CrossRefGoogle ScholarPubMed
Strausberg, RL, Feingold, EA, Grouse, LH, Derge, JG, Klausner, RD, Collins, FS, Wagner, L, Shenmen, CM, Schuler, GD, Altschul, SF, Zeeberg, B, Buetow, KH, Schaefer, CF, Bhat, NK, Hopkins, RF, Jordan, H, Moore, T, Max, SI, Wang, J, Hsieh, F, Diatchenko, L, Marusina, K, Farmer, AA, Rubin, GM, Hong, L, Stapleton, M, Soares, MB, Bonaldo, MF, Casavant, TL, Scheetz, TE, Brownstein, MJ, Usdin, TB, Toshiyuki, S, Carninci, P, Prange, C, Raha, SS, Loquellano, NA, Peters, GJ, Abramson, RD, Mullahy, SJ, Bosak, SA, McEwan, PJ, McKernan, KJ, Malek, JA, Gunaratne, PH, Richards, S, Worley, KC, Hale, S, Garcia, AM, Gay, LJ, Hulyk, SW, Villalon, DK, Muzny, DM, Sodergren, EJ, Lu, X, Gibbs, RA, Fahey, J, Helton, E, Ketteman, M, Madan, A, Rodrigues, S, Sanchez, A, Whiting, M, Madan, A, Young, AC, Shevchenko, Y, Bouffard, GG, Blakesley, RW, Touchman, JW, Green, ED, Dickson, MC, Rodriguez, AC, Grimwood, J, Schmutz, J, Myers, RM, Butterfield, YS, Krzywinski, MI, Skalska, U, Smailus, DE, Schnerch, A, Schein, JE, Jones, SJ and Marra, MA (2002) Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proceedings of the National Academy of Sciences of the United States of America 99, 1689916903.Google ScholarPubMed
Sukhumavasi, W, Egan, CE, Amy, L, Taylor, GA, Fox, BA, David, J, Denkers, EY, Warren, AL and Bzik, DJ (2008) TLR Adaptor MyD88 is essential for pathogen control during oral Toxoplasma gondii infection but not adaptive immunity induced by a vaccine strain of the parasite. The Journal of Immunology 181, 34643473. Scholar
Torres, M, Guiton, R, Lacroix-Lamandé, S, Ryffel, B, Leman, S and Dimier-Poisson, I (2013) Myd88 is crucial for the development of a protective CNS immune response to Toxoplasma gondii infection. Journal of Neuroinflammation 10, 19.CrossRefGoogle ScholarPubMed
Tuladar, S, Kochanowsky, JA, Bhaskara, A, Ghotmi, Y, Chandrasekaran, S and Koshy, AA (2019) The ROP16 III -dependent early immune response determines the subacute CNS immune response and type III Toxoplasma gondii survival. PLoS Pathogens 15, e1007856.CrossRefGoogle Scholar
Tzanidakis, N, Maksimov, P, Conraths, FJ, Kiossis, E, Brozos, C, Sotiraki, S and Schares, G (2012) Toxoplasma gondii in sheep and goats: seroprevalence and potential risk factors under dairy husbandry practices. Veterinary Parasitology 190, 340348.CrossRefGoogle ScholarPubMed
Wang, Z, Filgueiras, LR, Wang, S, Serezani, AP, Peters-Golden, M, Jancar, S and Serezani, CH (2014) Leukotriene B4 enhances the generation of proinflammatory microRNAs to promote MyD88-dependent macrophage activation. The Journal of Immunology 192, 23492356.CrossRefGoogle ScholarPubMed
Watson, WA and Beverley, JKA (1971) Epizootics of toxoplasmosis causing ovine abortion. Veterinary Records 88, 120124.CrossRefGoogle ScholarPubMed
Zhang, Y, Jiang, N, Zhang, T, Wang, D, Feng, Y, Sang, X, Yang, N and Chen, Q (2018) Toxoplasma gondii genotype determines Tim-3 expression levels in splenic and circulatory T cells in mice. Frontiers in Microbiology 9, 19.CrossRefGoogle ScholarPubMed
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