Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-26T01:05:00.412Z Has data issue: false hasContentIssue false

Infection with Trypanosoma lewisi or Trypanosoma musculi may promote the spread of Toxoplasma gondii

Published online by Cambridge University Press:  04 February 2021

Jiang-Mei Gao
Affiliation:
Center for Parasitic Organisms, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou510275, China Institute of Zoology, Guangdong Academy of Sciences, Guangzhou510260, China
Si-Qi Yi
Affiliation:
Center for Parasitic Organisms, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou510275, China
Guo-Qing Geng
Affiliation:
Center for Parasitic Organisms, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou510275, China
Zhi-Shen Xu
Affiliation:
Center for Parasitic Organisms, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou510275, China
Geoff Hide
Affiliation:
Biomedical Research Centre and Ecosystems and Environment Research Centre, School of Science, Engineering and Environment, University of Salford, Salford, M5 4WT, UK
Zhao-Rong Lun
Affiliation:
Center for Parasitic Organisms, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou510275, China Biomedical Research Centre and Ecosystems and Environment Research Centre, School of Science, Engineering and Environment, University of Salford, Salford, M5 4WT, UK
De-Hua Lai*
Affiliation:
Center for Parasitic Organisms, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-Sen University, Guangzhou510275, China
*
Author for correspondence: De-Hua Lai, E-mail: [email protected]

Abstract

Toxoplasma gondii can infect almost all warm-blooded vertebrates with pathogensis being largely influenced by the host immune status. As important epidemiological hosts, rodents are globally distributed and are also commonly found infected with haemoflagellates, such as those in the genus Trypanosoma. We here address whether and how co-infection with trypanosomes can influence T. gondii infection in laboratory models. Rats of five strains, co-infected with T. lewisi and mice of four strains, co-infected with T. musculi, were found to be more or less susceptible to T. gondii infection, respectively, with corresponding increased or decreased brain cyst burdens. Downregulation of iNOS expression and decreased NO production or reverse were observed in the peritoneal macrophages of rats or mice, infected with trypanosomes, respectively. Trypanosoma lewisi and T. musculi can modulate host immune responses, either by enhancement or suppression and influence the outcome of Toxoplasma infection.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albright, JW and Albright, JF (1980) Trypanosome-mediated suppression of murine humoral immunity independent of typical suppressor cells. Journal of Immunology 124, 24812484.Google ScholarPubMed
Beura, LK, Hamilton, SE, Bi, K, Schenkel, JM, Odumade, OA, Casey, KA, Thompson, EA, Fraser, KA, Rosato, PC, Filali-Mouhim, A, Sekaly, RP, Jenkins, MK, Vezys, V, Haining, WN, Jameson, SC and Masopust, D (2016) Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature 532, 512516.CrossRefGoogle ScholarPubMed
Brinkmann, V, Remington, JS and Sharma, SD (1987) Protective immunity in toxoplasmosis: correlation between antibody response, brain cyst formation, T-cell activation, and survival in normal and B-cell-deficient mice bearing the H-2k haplotype. Infection and Immunity 55, 990994.CrossRefGoogle ScholarPubMed
Carrera, NJ, Carmona, MC, Guerrero, OM and Castillo, AC (2009) The immunosuppressant effect of T. lewisi (Kinetoplastidae) infection on the multiplication of Toxoplasma gondii (Sarcocystidae) on alveolar and peritoneal macrophages of the white rat. Revista de Biologia Tropical 57, 1322.Google Scholar
Catarinella Arrea, G, Chinchilla Carmona, M, Guerrero Bermúdez, OM and Abrahams, E (1998) Effect of Trypanosoma lewisi (Kinetoplastida: Trypanosomatidae) on the infection of white rats with Toxoplasma Gondii (Eucoccidia: Sarcocystidae) oocysts. Revista de Biologia Tropical 46, 11211123.Google ScholarPubMed
Corraliza, IM, Campo, ML, Soler, G and Modolell, M (1994) Determination of arginase activity in macrophages: a micromethod. Journal of Immunological Methods 174, 231235.CrossRefGoogle ScholarPubMed
Desquesnes, M, Ravel, S and Cuny, G (2002) PCR Identification of Trypanosoma Lewisi, a common parasite of laboratory rats. Kinetoplastid Biology and Disease 1, 2.CrossRefGoogle ScholarPubMed
Ding, AH, Nathan, CF and Stuehr, DJ (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. Journal of Immunology 141, 24072412.Google ScholarPubMed
Dobigny, G, Gauthier, P, Houéménou, G, Dossou, HJ, Badou, S, Etougbétché, J, Tatard, C and Truc, P (2019) Spatio-temporal survey of small mammal-borne Trypanosoma lewisi in Cotonou, Benin, and the potential risk of human infection. Infection Genetics and Evolution 75, 103967.CrossRefGoogle ScholarPubMed
Dubey, JP and Frenkel, JK (1998) Toxoplasmosis of rats: a review, with considerations of their value as an animal model and their possible role in epidemiology. Veterinary Parasitology 77, 132.CrossRefGoogle ScholarPubMed
El-Mahmoudy, A, Matsuyama, H, Borgan, MA, Shimizu, Y, El-Sayed, MG, Minamoto, N and Takewaki, T (2002) Thymoquinone suppresses expression of inducible nitric oxide synthase in rat macrophages. International Immunopharmacology 2, 16031611.CrossRefGoogle ScholarPubMed
Gao, JM, Yi, SQ, Wu, MS, Geng, GQ, Shen, JL, Lu, FL, Hide, G, Lai, DH and Lun, ZR (2015) Investigation of infectivity of neonates and adults from different rat strains to Toxoplasma gondii Prugniaud shows both variations which correlates with iNOS and Arginase-1 activity and increased susceptibility of neonates to infection. Experimental Parasitology 149, 4753.CrossRefGoogle Scholar
Glas, AS, Lijmer, JG, Prins, MH, Bonsel, GJ and Bossuyt, PM (2003) The diagnostic odds ratio: a single indicator of test performance. Journal of Clinical Epidemiology 56, 11291135.CrossRefGoogle ScholarPubMed
Gross, NT, Guerrero, OM, Chinchilla, M and Jarstrand-Hall, C (2006) Trypanosoma lewisi-induced immunosuppression: the effects on alveolar macrophage activities against Cryptococcus neoformans. Experimental Parasitology 113, 262266.CrossRefGoogle ScholarPubMed
Guerrero, OM, Chinchilla, M and Abrahams, E (1997) Increasing of Toxoplasma Gondii (Coccidia, Sarcocystidae) infections by Trypanosoma lewisi (Kinetoplastida, Trypanosomatidae) in white rats. Revista de Biologia Tropical 45, 877882.Google Scholar
Hill, DE, Chirukandoth, S and Dubey, JP (2005) Biology and epidemiology of Toxoplasma gondii in man and animals. Animal Health Research Reviews 6, 4161.CrossRefGoogle ScholarPubMed
Letscher-Bru, V, Pfaff, AW, Abou-Bacar, A, Filisetti, D, Antoni, E, Villard, O, Klein, JP and Candolfi, E (2003) Vaccination with Toxoplasma gondii SAG-1 protein is protective against congenital toxoplasmosis in BALB/c mice but not in CBA/J mice. Infection and Immunity 71, 66156619.CrossRefGoogle ScholarPubMed
Li, Z, Zhao, ZJ, Zhu, XQ, Ren, QS, Nie, FF, Gao, JM, Gao, XJ, Yang, TB, Zhou, WL, Shen, JL, Wang, Y, Lu, FL, Chen, XG, Hide, G, Ayala, FJ and Lun, ZR (2012) Differences in iNOS and arginase expression and activity in the macrophages of rats are responsible for the resistance against T. gondii Infection. PloS one 7, e35834.CrossRefGoogle ScholarPubMed
Lin, RH, Lai, DH, Zheng, LL, Wu, J, Lukeš, J, Hide, G and Lun, ZR (2015) Analysis of the mitochondrial maxicircle of Trypanosoma Lewisi, a neglected human pathogen. Parasites & Vectors 8, 665.CrossRefGoogle ScholarPubMed
Liu, JH and Liu, AQ (1990) The prevalence of Trypanosome lewisi in monkey and human in Changchun, China. Chinese Journal of Zoonoses 6, 4041. In Chinese.Google Scholar
Lun, ZR, Reid, SA, Lai, DH and Li, FJ (2009) Atypical human trypanosomiasis: a neglected disease or just an unlucky accident? Trends in Parasitology 25, 107108.CrossRefGoogle ScholarPubMed
Lun, ZR, Wen, YZ, Uzureau, P, Lecordier, L, Lai, DH, Lan, YG, Desquesnes, M, Geng, GQ, Yang, TB, Zhou, WL, Jannin, JG, Simarro, PP, Truc, P, Vincendeau, P and Pays, E (2015) Resistance to normal human serum reveals Trypanosoma lewisi as an underestimated human pathogen. Molecular and Biochemical Parasitology 199, 5861.CrossRefGoogle ScholarPubMed
Montoya, JG and Liesenfeld, O (2004) Toxoplasmosis. Lancet (London, England) 363, 19651976.CrossRefGoogle ScholarPubMed
Nielsen, K, Sheppard, J, Holmes, W and Tizard, I (1978) Increased susceptibility of Trypanosoma lewisi infected, or decomplemented rats to Salmonella typhimurium. Experientia 34, 118119.CrossRefGoogle ScholarPubMed
Nishikawa, Y, Xuenan, X, Makala, L, Vielemeyer, O, Joiner, KA and Nagasawa, H (2003) Characterisation of Toxoplasma gondii engineered to express mouse interferon-gamma. International Journal for Parasitology 33, 15251535.CrossRefGoogle ScholarPubMed
Onah, DN and Wakelin, D (1999) Trypanosome-induced suppression of responses to Trichinella spiralis in vaccinated mice. International Journal for Parasitology 29, 10171026.CrossRefGoogle ScholarPubMed
Piccolo-Johanning, L, Kellerman-Guterman, V, Valerio-Campos, I and Chinchilla-Carmona, M (2013) Immunosuppressor effect of Trypanosoma musculi (Mastigophora: Trypanosomatidae) on experimental toxoplasmosis. Revista de Biologia Tropical 61, 981990.Google ScholarPubMed
Sztein, MB and Kierszenbaum, F (1992) Suppression by Trypanosoma cruzi of T-cell receptor expression by activated human lymphocytes. Immunology 77, 277283.Google ScholarPubMed
Tang, HJ, Lan, YG, Wen, YZ, Zhang, XC, Desquesnes, M, Yang, TB, Hide, G and Lun, ZR (2012) Detection of Trypanosoma lewisi from wild rats in Southern China and its genetic diversity based on the ITS1 and ITS2 sequences. Infection Genetics and Evolution 12, 10461051.CrossRefGoogle ScholarPubMed
Tenter, AM, Heckeroth, AR and Weiss, LM (2000) Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 12171258.CrossRefGoogle ScholarPubMed
Truc, P, Büscher, P, Cuny, G, Gonzatti, MI, Jannin, J, Joshi, P, Juyal, P, Lun, ZR, Mattioli, R, Pays, E, Simarro, PP, Teixeira, MM, Touratier, L, Vincendeau, P and Desquesnes, M (2013) Atypical human infections by animal trypanosomes. PLoS Neglected Tropical Diseases 7, e2256.CrossRefGoogle ScholarPubMed
Vincendeau, P, Caristan, A and Pautrizel, R (1981) Macrophage function during Trypanosoma musculi infection in mice. Infection and Immunity 34, 378381.CrossRefGoogle ScholarPubMed
Wang, T, Gao, JM, Yi, SQ, Geng, GQ, Gao, XJ, Shen, JL, Lu, FL, Wen, YZ, Hide, G and Lun, ZR (2014) Toxoplasma gondii infection in the peritoneal macrophages of rats treated with glucocorticoids. Parasitology Research 113, 351358.CrossRefGoogle ScholarPubMed
Zhao, ZJ, Zhang, J, Wei, J, Li, Z, Wang, T, Yi, SQ, Shen, JL, Yang, TB, Hide, G and Lun, ZR (2013) Lower expression of inducible nitric oxide synthase and higher expression of arginase in rat alveolar macrophages are linked to their susceptibility to Toxoplasma gondii infection. PloS one 8, e63650.CrossRefGoogle ScholarPubMed
Supplementary material: File

Gao et al. supplementary material

Gao et al. supplementary material

Download Gao et al. supplementary material(File)
File 1.2 MB