Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-19T06:11:08.170Z Has data issue: false hasContentIssue false
  • English
  • Français

Differential immune responses in mice infected with the tissue-dwelling nematode Trichinella zimbabwensis

Published online by Cambridge University Press:  21 August 2015

W.N. Onkoba ,
M.J. Chimbari ,
J.M. Kamau  and
S. Mukaratirwa
W.N. Onkoba*
Affiliation:
College of Health Sciences, School of Nursing and Public Health, University of KwaZulu-Natal, Howard Campus, Durban, South Africa Tropical Infectious Diseases, Institute of Primate Research, Karen, Nairobi, Kenya
M.J. Chimbari
Affiliation:
College of Health Sciences, School of Nursing and Public Health, University of KwaZulu-Natal, Howard Campus, Durban, South Africa
J.M. Kamau
Affiliation:
Tropical Infectious Diseases, Institute of Primate Research, Karen, Nairobi, Kenya School of Medicine, Department of Biochemistry, University of Nairobi, Kenya School of Life Sciences, University of KwaZulu-Natal, Westville Campus, Durban, South Africa
S. Mukaratirwa
Affiliation:
School of Life Sciences, University of KwaZulu-Natal, Westville Campus, Durban, South Africa
*
*E-mail: bwonkoba@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

To improve diagnostic tools, immunotherapies and vaccine development for trichinellosis surveillance and control there is a need to understand the host immune responses induced during infection with Trichinella zimbabwensis, a tissue-dwelling nematode. In this study, we sought to determine immune responses induced in mice during T. zimbabwensis infection. The parasite strain used (Code ISS1209) was derived from a naturally infected crocodile (Crocodylus niloticus) and is the main Trichinella species prevalent in southern Africa. Sixty 6- to 8-week-old female BALB/c mice were randomly assigned to two equal groups: T. zimbabwensis-infected (n= 30) and the non-infected control group (n= 30). Levels of serum tumour necrosis factor-alpha (TNF-α), interleukin-10 (IL-10), interleukin-4 (IL-4) as well as parasite-specific IgM, IgG, IgG1, IgG2a, IgG2b and IgG3 antibody responses were determined using enzyme-linked immunosorbent assay (ELISA). The cytokines and antibodies provided information on T-helper 1 (Th1)- and Th2-type, T-regulatory and antibody responses. Results showed that during the intestinal stage of infection, higher levels of parasite-specific IgM, IgG, IgG1 (P <  0.05) and IL-10 and TNF-α (P <  0.001) were observed in the Trichinella-infected group compared with the non-infected control group. In the parasite establishment and tissue migration phases, levels of IgG1 and IgG3 were elevated (P <  0.001), while those of IgM (P <  0.01) declined on days 21 and 35 post infection (pi) compared to the enteric phase. Our findings show that distinct differences in Th1- and Th2-type and T-regulatory responses are induced during the intestinal, tissue migration and larval establishment stages of T. zimbabwensis infection.

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 5 , September 2016 , pp. 547 - 554
Copyright
Copyright © Cambridge University Press 2015 

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

Anthony, R.M., Rutitzky, L.I., Urban, J.F. Jr, Stadecker, M.J. & Gause, W.C. (2007) Protective immune mechanisms in helminth infection. Nature Reviews in Immunology 7, 975–987.Google Scholar
Aranzamendi, C., Fransen, F., Langelaar, M., Franssen, F., van der Ley, P., van Putten, J.P.M., Rutten, V. & Pinelli, E. (2012) Trichinella spiralis-secreted products modulate DC functionality and expand regulatory T cells in vitro . Parasite Immunology 34, 210–223.CrossRefGoogle ScholarPubMed
Artavanis-Tsakonas, K., Tongren, J.E. & Riley, E.M. (2003) The war between the malaria parasite and the immune system: immunity, immunoregulation and immunopathology. Clinical and Experimental Immunology 133, 145–152.Google Scholar
Artis, D., Humphreys, N.E., Bancroft, A.J., Rothwell, N.J., Potten, C.S. & Grencis, R.K. (1999) Tumor necrosis factor is a critical component of interleukin 13-mediated protective T helper cell type 2 responses during helminth infection. Journal of Experimental Medicine 190, 953–962.Google Scholar
Ashour, D.S. (2013) Trichinella spiralis immunomodulation: an interactive multifactorial process. Expert Review of Clinical Immunology 9, 669–675.Google Scholar
Beiting, D.P., Bliss, S.K., Schlafer, D.H., Roberts, V.L. & Appleton, J.A. (2004) Interleukin-10 limits local and body cavity inflammation during infection with muscle-stage Trichinella spiralis . Infection and Immunity 72, 3129–3137.CrossRefGoogle ScholarPubMed
Beiting, D.P., Gagliardo, L.F., Hesse, M., Bliss, S.K., Meskill, D. & Appleton, J.A. (2007) Coordinated control of immunity to muscle stage Trichinella spiralis by IL-10, regulatory T cells, and TGF-beta. Journal of Immunology 178, 1039–1047.CrossRefGoogle ScholarPubMed
Bień, J. (2007) The usefulness of ELISA test for early serological detection of Trichinella spp. infection in pigs. Wiadomosci Parazytologiczne 53, 149–151.Google Scholar
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Chai, J.Y., Murrell, K.D. & Lymbery, A.J. (2005) Fish-borne parasitic zoonoses: Status and issues. International Journal for Parasitology 35, 1233–1254.Google Scholar
Dabanch, P. (2003) Zoonoses. Zoonosis 20, S47–S51.Google Scholar
De Merode, E., Homewood, K. & Cowlishaw, G. (2004) The value of bushmeat and other wild foods to rural households living in extreme poverty in Democratic Republic of Congo. Biological Conservation 118, 573–581.Google Scholar
Deville, S., De Pooter, A., Aucouturier, J., Lainé-Prade, V., Cote, M., Boireau, P. & Vallée, I. (2005) Influence of adjuvant formulation on the induced protection of mice immunized with total soluble antigen of Trichinella spiralis . Veterinary Parasitology 132, 75–80.CrossRefGoogle ScholarPubMed
Dupouy-Camet, J. (2009) Presidential address of ICT12 Conference: ‘Trichinella and trichinellosis – A never ending story’. Veterinary Parasitology 159, 194–196.Google Scholar
Else, K. & Finkelman, F.D. (1998) Invited review: Intestinal nematode parasites, cytokines and effector mechanisms. International Journal for Parasitology 28, 1145–1158.CrossRefGoogle Scholar
Escalante, M., Romarís, F., Rodríguez, M., Rodríguez, E., Ga, M.T. & Ubeira, F.M. (2004) Evaluation of Trichinella spiralis larva Group 1 antigens for serodiagnosis of human trichinellosis. Journal of Clinical Microbiology 42, 4060–4066.CrossRefGoogle ScholarPubMed
European Food Safety Authority, (2011) The European Union Summary Report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2009. EFSA Journal 9, 1–378.Google Scholar
Fabre, M.V., Beiting, D.P., Bliss, S.K. & Appleton, J.A. (2009) Immunity to Trichinella spiralis muscle infection. Veterinary Parasitology 159, 245–248.CrossRefGoogle ScholarPubMed
Fabre, V., Beiting, D.P., Bliss, S.K., Gebreselassie, N.G., Gagliardo, L.F., Lee, N.A., Lee, J.J. & Appleton, J.A. (2009) Eosinophil deficiency compromises parasite survival in chronic nematode infection. Journal of Immunology 182, 1577–1583.Google Scholar
Feng, S., Wu, X., Wang, X., Bai, X., Shi, H., Tang, B., Liu, X., Song, Y., Boireau, P., Wang, F., Zhao, Y. & Liu, M. (2013) Vaccination of mice with an antigenic serine protease-like protein elicits a protective immune response against Trichinella spiralis infection. Journal of Parasitology 99, 426–432.CrossRefGoogle ScholarPubMed
Frey, C.F., Schuppers, M.E., Nöckler, K., Marinculić, A., Pozio, E., Kihm, U. & Gottstein, B. (2009) Validation of a Western Blot for the detection of anti-Trichinella spp. antibodies in domestic pigs. Parasitology Research 104, 1269–1277.CrossRefGoogle ScholarPubMed
Fu, Y., Wang, W., Tong, J., Pan, Q., Long, Y., Qian, W. & Hou, X. (2009) Th17: a new participant in gut dysfunction in mice infected with Trichinella spiralis . Mediators of Inflammation 517052.Google Scholar
Furze, R.C. & Selkirk, M.E. (2005) Comparative dynamics and phenotype of the murine immune response to Trichinella spiralis and Trichinella pseudospiralis . Parasite Immunology 27, 181–188.Google Scholar
Gao, F., Liu, X., Wu, X.-P., Wang, X.-L., Gong, D., Lu, H., Xia, Y., Song, Y., Wang, J., Du, J., Liu, S., Han, X., Tang, Y., Yang, H., Jin, Q., Zhang, X. & Liu, M. (2012) Differential DNA methylation in discrete developmental stages of the parasitic nematode Trichinella spiralis . Genome Biology 13, R100.Google Scholar
Gao, F., Wang, R. & Liu, M. (2014) Trichinella spiralis, potential model nematode for epigenetics and its implication in metazoan parasitism. Frontiers in Physiology 4, 410.Google Scholar
Gottstein, B., Pozio, E. & Nöckler, K. (2009) Epidemiology, diagnosis, treatment, and control of trichinellosis. Clinical Microbiology Reviews 22, 127–145.Google Scholar
Goyal, P.K. & Wakelin, D. (1993) Influence of variation in host strain and parasite isolate on inflammatory and antibody responses to Trichinella spiralis in mice. Parasitology 106, 371–378.CrossRefGoogle ScholarPubMed
Gruden-Movsesijan, A., Ilic, N., Mostarica-Stojkovic, M., Stosic-Grujicic, S., Milic, M. & Sofronic-Milosavljevic, L. (2008) Trichinella spiralis: modulation of experimental autoimmune encephalomyelitis in DA rats. Experimental Parasitology 118, 641–647.Google Scholar
Gruden-Movsesijan, A., Ilic, N., Colic, M., Majstorovic, I., Vasilev, S., Radovic, I. & Sofronic-Milosavljevic, L.J. (2011) The impact of Trichinella spiralis excretory-secretory products on dendritic cells. Comparative Immunology, Microbiology and Infectious Diseases 34, 429–439.Google Scholar
Harnett, W. & Harnett, M.M. (2010) Helminth-derived immunomodulators: can understanding the worm produce the pill? Nature Reviews. Immunology 10, 278–284.CrossRefGoogle ScholarPubMed
Helmby, H. & Grencis, R.K. (2003) IFN-gamma-independent effects of IL-12 during intestinal nematode infection. Journal of Immunology 171, 3691–3696.Google Scholar
Hewitson, J.P., Grainger, J.R. & Maizels, R.M. (2009) Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Molecular and Biochemical Parasitology 167, 1–11.Google Scholar
Hlaka, L., Chitanga, S. & Mukaratirwa, S. (2015) Host sex influences the establishment of Trichinella zimbabwensis in Sprague–Dawley rats. International Journal of Applied Research in Veterinary Medicine 13, 141–146.Google Scholar
Hübner, M.P., Shi, Y., Torrero, M.N., Mueller, E., Larson, D., Soloviova, K., Gondorf, F., Hoerauf, A., Killoran, K.E., Stocker, J.T., Davies, S.J., Tarbell, K.V. & Mitre, E. (2012) Helminth protection against autoimmune diabetes in nonobese diabetic mice is independent of a type 2 immune shift and requires TGF-β. Journal of Immunology 188, 559–568.Google Scholar
Hurnikova, Z., Dubinsky, P., Mukaratirwa, S., Foggin, C.M. & Kapel, C.M.O. (2004) Infectivity and temperature tolerance of non-encapsulating Trichinella zimbabwensis in experimentally infected red foxes (Vulpes vulpes). Helminthologia 41, 189–192.Google Scholar
Ilic, N., Colic, M., Gruden-Movsesijan, A., Majstorovic, I., Vasilev, S. & Sofronic-Milosavljevic, L. (2008) Characterization of rat bone marrow dendritic cells initially primed by Trichinella spiralis antigens. Parasite Immunology 30, 491–495.Google Scholar
Ilic, N., Worthington, J.J., Gruden-Movsesijan, A., Travis, M.A., Sofronic-Milosavljevic, L. & Grencis, R.K. (2011) Trichinella spiralis antigens prime mixed Th1/Th2 response but do not induce de novo generation of Foxp3(+) T cells in vitro . Parasite Immunology 33, 572–582.Google Scholar
Ilic, N., Gruden-Movsesijan, A. & Sofronic-Milosavljevic, L. (2012) Trichinella spiralis: shaping the immune response. Immunology Research 52, 111–119.Google Scholar
Kapel, C.M.O. & Gamble, H.R. (2000) Infectivity, persistence, and antibody response to domestic and sylvatic Trichinella spp. in experimentally infected pigs. International Journal of Parasitology 30, 215–221.Google Scholar
Khumjui, C., Choomkasien, P., Dekumyoy, P., Kusolsuk, T., Kongkaew, W., Chalamaat, M. & Jones, J.L. (2008) Outbreak of trichinellosis caused by Trichinella papuae, Thailand, 2006. Emerging Infectious Diseases 14, 1913–1915.Google Scholar
Kilkenny, C., Browne, W.J., Cuthill, I.C., Emerson, M. & Altman, D.G. (2013) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. Animals 4, 35–44.Google Scholar
La Grange, L.J., Marucci, G. & Pozio, E. (2009) Trichinella zimbabwensis in wild Nile crocodiles (Crocodylus niloticus) of South Africa. Veterinary Parasitology 161, 88–91.Google Scholar
La Grange, L.J., Marucci, G. & Pozio, E. (2010) Trichinella zimbabwensis in a naturally infected mammal. Journal of Helminthology 84, 35–38.Google Scholar
La Grange, L.J., Govender, D., Mukaratirwa, S. & Hughes, D.M. (2012) The occurrence of Trichinella zimbabwensis in naturally infected wild crocodiles (Crocodylus niloticus) from the Kruger National Park, South Africa. Development and Change 32, 1–6.Google Scholar
La Rosa, G., Marucci, G. & Pozio, E. (2003) Biochemical analysis of encapsulated and non-encapsulated species of Trichinella (Nematoda, Trichinellidae) from cold- and warm-blooded animals reveals a high genetic divergence in the genus. Parasitology Research 91, 462–466.Google Scholar
Li, X., Yao, J., Pan, A., Liu, W., Hu, X., Wu, Z. & Zhou, X. (2013) An antigenic recombinant serine protease from Trichinella spiralis induces protective immunity in BALB/c mice. Parasitology Research 112, 3229–3238.Google Scholar
Ludovisi, A., La Grange, L.J., Gómez Morales, M.A. & Pozio, E. (2013) Development of an ELISA to detect the humoral immune response to Trichinella zimbabwensis in Nile crocodiles (Crocodylus niloticus). Veterinary Parasitology 194, 189–192.Google Scholar
Magwedere, K., Hemberger, M.Y., Hoffman, L.C. & Dziva, F. (2012) Zoonoses: a potential obstacle to the growing wildlife industry of Namibia. Infection Ecology & Epidemiology. doi:10.3402/iee.v2i0.18365.Google Scholar
Maizels, R.M., Pearce, E.J., Artis, D., Yazdanbakhsh, M. & Wynn, T.A. (2009) Regulation of pathogenesis and immunity in helminth infections. Journal of Experimental Medicine 206, 2059–2066.CrossRefGoogle ScholarPubMed
Maizels, R.M., Hewitson, J.P. & Smith, K.A. (2012) Susceptibility and immunity to helminth parasites. Current Opinion in Immunology 24, 459–466.CrossRefGoogle ScholarPubMed
Matenga, E., Mukaratirwa, S., Bhebhe, E. & Willingham, A.L. (2006) Comparison of the infectivity of Trichinella zimbabwensis in indigenous Zimbabwean pigs (Mukota) and exotic Large White pigs. International Journal of Applied Research in Veterinary Medicine 4, 301–306.Google Scholar
Mukaratirwa, S. & Foggin, C.M. (1999) Infectivity of Trichinella sp. isolated from Crocodylus niloticus to the indigenous Zimbabwean pig (Mukota). International Journal of Parasitology 29, 1129–1131.Google Scholar
Mukaratirwa, S., Nkulungo, E., Matenga, E. & Bhebhe, E. (2003) Effect of host age in the distribution of adult Trichinella zimbabwensis in the small intestines of golden hamsters (Mesocricetus auratus) and Balb/C mice. Onderstepoort Journal of Veterinary Research 70, 169–173.Google Scholar
Mukaratirwa, S., Dzoma, B.M., Matenga, E., Ruziwa, S.D., Sacchi, L. & Pozio, E. (2008) Experimental infections of baboons (Papio spp.) and vervet monkeys (Cercopithecus aethiops) with Trichinella zimbabwensis and successful treatment with ivermectin. Onderstepoort Journal of Veterinary Research 75, 173–180.Google Scholar
Mukaratirwa, S., La Grange, L. & Pfukenyi, D.M. (2013) Trichinella infections in animals and humans in sub-Saharan Africa: a review. Acta Tropica 125, 82–89.Google Scholar
Mukaratirwa, S., Gcanga, L. & Kamau, J. (2015) Efficacy of maslinic acid and fenbendazole on muscle larvae of Trichinella zimbabwensis in laboratory rats. Journal of Helminthology. doi:10.1017/S0022149X14000923.Google Scholar
Murrell, K.D. & Pozio, E. (2011) Worldwide occurrence and impact of human trichinellosis, 1986–2009. Emerging Infectious Diseases 17, 2194–2202.Google Scholar
Murrell, K.D., Dorny, P., Flisser, A., Nash, T. & Pawlowski, Z. (2005) WHO/FAO/OIE Guidelines for the surveillance, prevention and control of taeniosis/cysticercosis. Paris, France, WHO/FAO/OIE.Google Scholar
Nagano, I., Wu, Z., Asano, K. & Takahashi, Y. (2011) Molecular cloning and characterization of transgelin-like proteins mainly transcribed in newborn larvae of Trichinella spp. Veterinary Parasitology 178, 134–142.CrossRefGoogle ScholarPubMed
Onkoba, W.N., Kamau, J.K., Chimbari, M.J. & Mukaratirwa, S. (2015) Metabolic and adaptive immune responses of BALB/c mice infected with Trichinella zimbabwensis . Acta Tropica, in press .Google Scholar
Picherot, M., Oswald, I.P., Cote, M., Noeckler, K., Le Guerhier, F., Boireau, P. & Vallée, I. (2007) Swine infection with Trichinella spiralis: Comparative analysis of the mucosal intestinal and systemic immune responses. Veterinary Parasitology 143, 122–130.Google Scholar
Pozio, E., Foggin, C.M., Gelanew, T., Marucci, G., Hailu, A., Rossi, P. & Morales, M.A.G. (2007) Trichinella zimbabwensis in wild reptiles of Zimbabwe and Mozambique and farmed reptiles of Ethiopia. Veterinary Parasitology 143, 305–310.Google Scholar
Pozio, E. & La Rosa, G. (2005) Evaluation of the infectivity of Trichinella papuae and Trichinella zimbabwensis for equatorial freshwater fishes. Veterinary Parasitology 132, 113–114.Google Scholar
Pozio, E., Marucci, G., Casulli, A., Sacchi, L., Mukaratirwa, S., Foggin, C.M. & La Rosa, G. (2004) Trichinella papuae and Trichinella zimbabwensis induce infection in experimentally infected varans, caimans, pythons and turtles. Parasitology 128, 333–342.Google Scholar
Pozio, E. & Murrell, K.D. (2006) Systematics and epidemiology of Trichinella . Advances in Parasitology 63, 367–439.Google Scholar
Pozio, E. & Rossi, P. (2008) Guidelines for the identification and development of sampling methods and design of suitable protocols for monitoring of Trichinella infection in indicator species. Annali dell'Istituto Superiore Di Sanita 44, 200–204.Google Scholar
Pozio, E., Sofronic-Milosavljevic, L., Gomez Morales, M.A., Boireau, P. & Nöckler, K. (2002) Evaluation of ELISA and Western Blot Analysis using three antigens to detect anti-Trichinella IgG in horses. Veterinary Parasitology 108, 163–178.Google Scholar
Ranque, S., Faugère, B., Pozio, E., La Rosa, G., Tamburrini, A., Pellissier, J.F. & Brouqui, P. (2000) Trichinella pseudospiralis outbreak in France. Emerging Infectious Diseases 6, 543–547.Google Scholar
Ruangkunaporn, Y., Watt, G., Karnasuta, C., Jongsakul, K., Mahannop, P., Chongsa-nguan, M. & Chaicumpa, W. (1994) Immunodiagnosis of trichinellosis: efficacy of somatic antigen in early detection of human trichinellosis. Asian Pacific Journal of Allergy and Immunology 12, 39–42.Google Scholar
Sadaow, L., Intapan, P.M., Boonmars, T., Morakote, N. & Maleewong, W. (2013) Susceptibility of laboratory rodents to Trichinella papuae . Korean Journal of Parasitology 51, 629–632.CrossRefGoogle ScholarPubMed
Slifko, T.R., Smith, H.V. & Rose, J.B. (2000) Emerging parasite zoonoses associated with water and food. International Journal of Parasitology 30, 1379–1393.CrossRefGoogle ScholarPubMed
Sofronic-Milosavljevic, L., Ilic, N., Pinelli, E. & Gruden-Movsesijan, A. (2015) Secretory products of Trichinella spiralis muscle larvae and immunomodulation: implication for autoimmune diseases, allergies, and malignancies. Journal of Immunology Research. doi:10.1155/2015/523875.Google Scholar
Wakelin, D. & Goyal, P.K. (1996) Trichinella isolates: parasite variability and host responses. International Journal of Parasitology 26, 471–481.Google Scholar
Wakelin, D., Goyal, P.K., Dehlawi, M.S. & Hermanek, J. (1994) Immune responses to Trichinella spiralis and T. pseudospiralis in mice. Immunology 81, 475–479.Google Scholar
Wu, Z., Nagano, I., Asano, K. & Takahashi, Y. (2010) Infection of non-encapsulated species of Trichinella ameliorates experimental autoimmune encephalomyelitis involving suppression of Th17 and Th1 response. Parasitology Research 107, 1173–1188.Google Scholar
Yang, J., Gu, Y., Yang, Y., Wei, J., Wang, S., Cui, S., Pan, J., Li, Q. & Zhu, X. (2010) Trichinella spiralis: immune response and protective immunity elicited by recombinant paramyosin formulated with different adjuvants. Experimental Parasitology 124, 403–408.Google Scholar
Yazdanbakhsh, M., Van Den Biggelaar, A. & Maizels, R.M. (2001) Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends in Immunology 22, 372–377.Google Scholar
Yépez-Mulia, L., Hernández-Bello, R., Arizmendi-Puga, N., Fonseca-Liñán, R. & Ortega-Pierres, G. (2007) Contributions to the study of Trichinella spiralis TSL-1 antigens in host immunity. Parasite Immunology 29, 661–670.Google Scholar
Yépez-Mulia, L., Montaño-Escalona, C., Fonseca-Liñán, R., Muñoz-Cruz, S., Arizmendi-Puga, N., Boireau, P. & Ortega-Pierres, G. (2009) Differential activation of mast cells by antigens from Trichinella spiralis muscle larvae, adults, and newborn larvae. Veterinary Parasitology 159, 253–257.Google Scholar