Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-26T09:58:29.157Z Has data issue: false hasContentIssue false
  • English
  • Français

The resistance against Trichinella spiralis infection induced by primary infection with respiratory syncytial virus

Published online by Cambridge University Press:  05 November 2018

Ki-Back Chu ,
Dong-Hun Lee ,
Hae-Ji Kang  and
Fu-Shi Quan Open the ORCID record for Fu-Shi Quan [Opens in a new window]
Ki-Back Chu
Affiliation:
Department of Biomedical Science, Graduate School, Kyung Hee University, Seoul, Korea
Dong-Hun Lee
Affiliation:
Department of Biomedical Science, Graduate School, Kyung Hee University, Seoul, Korea
Hae-Ji Kang
Affiliation:
Department of Biomedical Science, Graduate School, Kyung Hee University, Seoul, Korea
Fu-Shi Quan*
Affiliation:
Department of Medical Zoology, Kyung Hee University School of Medicine, Seoul, Korea Biomedical Science Institute, Kyung Hee University, Seoul, Korea
*
Author for correspondence: Fu-Shi Quan, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Human infections with Trichinella spiralis and respiratory syncytial virus (RSV) are common, as T. spiralis infections are re-emerging in various parts of the world and RSV infections remain a threat for infants. Yet, studies investigating the relationship pertaining to the two are severely lacking. In particular, immune response induction via RSV and T. spiralis remain largely elusive. Here, we investigated the resistance against T. spiralis infection induced upon primary infection with RSV. RSV, notorious for causing severe inflammatory reaction in the lungs, were intranasally infected, followed with a T. spiralis infection in mice. Our results revealed that primary RSV infection in mice significantly raised T. spiralis-specific and total IgE, IgG and its subclass antibody responses upon T. spiralis challenge infection (RSV-Ts). Blood eosinophil levels were decreased in RSV-Ts, accompanied with significant increase in both Th1 and Th2 cytokines. Antibodies generated against RSV in RSV-infected mice were found to react with T. spiralis excretory/secretory antigen, showing several bands determined through immunoblotting. RSV-Ts also had a marked reduction of T. spiralis worm burden in diaphragm. These results indicate that immune responses induced by RSV infection contribute to resistance against subsequent T. spiralis infection.

Keywords

Antibody responseresistancerespiratory syncytial virusTrichinella spiralis
Type
Research Article
Information
Parasitology , Volume 146 , Issue 5 , April 2019 , pp. 634 - 642
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

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

Bates, JT, Keefer, CJ, Slaughter, JC, Kulp, DW, Schief, WR and Crowe, JE Jr (2014) Escape from neutralization by the respiratory syncytial virus-specific neutralizing monoclonal antibody palivizumab is driven by changes in on-rate of binding to the fusion protein. Virology 454–455, 139–144.Google Scholar
Becker, Y (2006) Respiratory syncytial virus (RSV) evades the human adaptive immune system by skewing the Th1/Th2 cytokine balance toward increased levels of Th2 cytokines and IgE, markers of allergy – a review. Virus Genes 33, 235–252.Google Scholar
Beiting, DP, Gagliardo, LF, Hesse, M, Bliss, SK, Meskill, D and Appleton, JA (2007) Coordinated control of immunity to muscle stage Trichinella spiralis by IL-10, regulatory T cells, and TGF-beta. Journal of Immunology (Baltimore, MD.: 1950) 178, 1039–1047.Google Scholar
Bellelli, C, Frosi, A, Chiovoloni, M, Grelloni, V and Baldelli, B (1989) Trichinella spiralis as a modulator of Shope fibroma virus. Parassitologia 31, 145–152.Google Scholar
Bruschi, F and Chiumiento, L (2011) Trichinella inflammatory myopathy: host or parasite strategy? Parasites & Vectors 4, 42. doi: 10.1186/1756-3305-4-42.Google Scholar
Collins, PL and Graham, BS (2008) Viral and host factors in human respiratory syncytial virus pathogenesis. Journal of Virology 82, 2040–2055.Google Scholar
Cuperlovic, K, Djordjevic, M and Pavlovic, S (2005) Re-emergence of trichinellosis in Southeastern Europe due to political and economic changes. Veterinary Parasitology 132, 159–166.Google Scholar
Cypess, RH, Lubiniecki, AS and Hammon, WM (1973) Immunosuppression and increased susceptibility to Japanese B encephalitis virus in Trichinella spiralis-infected mice. Proceedings of the Society for Experimental Biology and Medicine (New York, NY) 143, 469–473.Google Scholar
Dakhama, A, Lee, YM, Ohnishi, H, Jing, X, Balhorn, A, Takeda, K and Gelfand, EW (2009) Virus-specific IgE enhances airway responsiveness on reinfection with respiratory syncytial virus in newborn mice. The Journal of Allergy and Clinical Immunology 123, 138–145.e5.Google Scholar
de Vos, T, Danell, G and Dick, TA (1992) Trichinella spiralis: dose dependence and kinetics of the mucosal immune response in mice. Experimental Parasitology 75, 99–111.Google Scholar
Drajac, C, Laubreton, D, Riffault, S and Descamps, D (2017) Pulmonary susceptibility of neonates to respiratory syncytial virus infection: a problem of innate immunity? Journal of Immunology Research 2017, 8734504.Google Scholar
Dvoroznakova, E, Hurnikova, Z and Kolodziej-Sobocinska, M (2011) Development of cellular immune response of mice to infection with low doses of Trichinella spiralis, Trichinella britovi and Trichinella pseudospiralis larvae. Parasitology Research 108, 169–176.Google Scholar
Else, KJ and Grencis, RK (1991) Cellular immune responses to the murine nematode parasite Trichuris muris. I. Differential cytokine production during acute or chronic infection. Immunology 72, 508–513.Google Scholar
Fabre, V, Beiting, DP, Bliss, SK, Gebreselassie, NG, Gagliardo, LF, Lee, NA, Lee, JJ and Appleton, JA (2009) Eosinophil deficiency compromises parasite survival in chronic nematode infection. Journal of Immunology (Baltimore, MD: 1950) 182, 1577–1583.Google Scholar
Finkelman, FD, Katona, IM, Urban, JF Jr, Snapper, CM, Ohara, J and Paul, WE (1986) Suppression of in vivo polyclonal IgE responses by monoclonal antibody to the lymphokine B-cell stimulatory factor 1. Proceedings of the National Academy of Sciences of the USA 83, 9675–9678.Google Scholar
Finkelman, FD, Shea-Donohue, T, Goldhill, J, Sullivan, CA, Morris, SC, Madden, KB, Gause, WC and Urban, JF Jr (1997) Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annual Review of Immunology 15, 505–533.Google Scholar
Franssen, FF, Fonville, M, Takumi, K, Vallee, I, Grasset, A, Koedam, MA, Wester, PW, Boireau, P and van der Giessen, JW (2011) Antibody response against Trichinella spiralis in experimentally infected rats is dose dependent. Veterinary Research 42, 113. doi: 10.1186/1297-9716-42-113.Google Scholar
Furze, RC, Hussell, T and Selkirk, ME (2006) Amelioration of influenza-induced pathology in mice by coinfection with Trichinella spiralis. Infection and Immunity 74, 1924–1932.Google Scholar
Gagliardo, LF, McVay, CS and Appleton, JA (2002) Molting, ecdysis, and reproduction of Trichinella spiralis are supported in vitro by intestinal epithelial cells. Infection and Immunity 70, 1853–1859.Google Scholar
Garraud, O, Perraut, R, Riveau, G and Nutman, TB (2003) Class and subclass selection in parasite-specific antibody responses. Trends in Parasitology 19, 300–304.Google Scholar
Gebreselassie, NG, Moorhead, AR, Fabre, V, Gagliardo, LF, Lee, NA, Lee, JJ and Appleton, JA (2012) Eosinophils preserve parasitic nematode larvae by regulating local immunity. Journal of Immunology (Baltimore, MD: 1950) 188, 417–425.Google Scholar
Gottstein, B, Pozio, E and Nockler, K (2009) Epidemiology, diagnosis, treatment, and control of trichinellosis. Clinical Microbiology Reviews 22, 127–145, Table of Contents.Google Scholar
Grieves, JL, Yin, Z, Garcia-Sastre, A, Mena, I, Peeples, ME, Risman, HP, Federman, H, Sandoval, MJ, Durbin, RK and Durbin, JE (2018) A viral-vectored RSV vaccine induces long-lived humoral immunity in cotton rats. Vaccine 36, 3842–3852.Google Scholar
Gruden-Movsesijan, A, Ilic, N, Colic, M, Majstorovic, I, Vasilev, S, Radovic, I and Sofronic-Milosavljevic, L (2011) The impact of Trichinella spiralis excretory-secretory products on dendritic cells. Comparative Immunology, Microbiology and Infectious Diseases 34, 429–439.Google Scholar
Gurish, MF, Bryce, PJ, Tao, H, Kisselgof, AB, Thornton, EM, Miller, HR, Friend, DS and Oettgen, HC (2004) Ige enhances parasite clearance and regulates mast cell responses in mice infected with Trichinella spiralis. Journal of Immunology (Baltimore, MD: 1950) 172, 1139–1145.Google Scholar
Helmby, H and Grencis, RK (2003) Contrasting roles for IL-10 in protective immunity to different life cycle stages of intestinal nematode parasites. European Journal of Immunology 33, 2382–2390.Google Scholar
Huang, L, Gebreselassie, NG, Gagliardo, LF, Ruyechan, MC, Lee, NA, Lee, JJ and Appleton, JA (2014) Eosinophil-derived IL-10 supports chronic nematode infection. Journal of Immunology (Baltimore, MD: 1950) 193, 4178–4187.Google Scholar
Huang, L, Gebreselassie, NG, Gagliardo, LF, Ruyechan, MC, Luber, KL, Lee, NA, Lee, JJ and Appleton, JA (2015) Eosinophils mediate protective immunity against secondary nematode infection. Journal of Immunology (Baltimore, MD: 1950) 194, 283–290.Google Scholar
Jiang, J, Fisher, EM, Concannon, M, Lustigman, S, Shen, H and Murasko, DM (2016) Enhanced humoral response to influenza vaccine in aged mice with a novel adjuvant, rOv-ASP-1. Vaccine 34, 887–892.Google Scholar
Kerzner, MS and Redmon, W (1964) Neurotrichinosis. Rhode Island Medical Journal 47, 388–391.Google Scholar
Kim, KS, Kim, AR, Piao, Y, Lee, JH and Quan, FS (2017) A rapid, simple, and accurate plaque assay for human respiratory syncytial virus (HRSV). Journal of Immunological Methods 446, 15–20.Google Scholar
Lal, RB, Rudolph, D, Alpers, MP, Sulzer, AJ, Shi, YP and Lal, AA (1994) Immunologic cross-reactivity between structural proteins of human T-cell lymphotropic virus type I and the blood stage of Plasmodium falciparum. Clinical and Diagnostic Laboratory Immunology 1, 5–10.Google Scholar
Lambert, L, Sagfors, AM, Openshaw, PJ and Culley, FJ (2014) Immunity to RSV in early-life. Frontiers in Immunology 5, 466.Google Scholar
Lee, CM and Best, Y (1983) Trichinella spiralis: changes in leucocytes during infection. Journal of the National Medical Association 75, 1205–1214.Google Scholar
Lee, DL and Shivers, RR (1987) A freeze-fracture study of muscle fibres infected with Trichinella spiralis. Tissue & Cell 19, 665–671.Google Scholar
Lee, YT, Ko, EJ, Kim, KH, Hwang, HS, Lee, Y, Kwon, YM, Kim, MC, Lee, YN, Jung, YJ and Kang, SM (2017) Cellular immune correlates preventing disease against respiratory syncytial virus by vaccination with virus-like nanoparticles carrying fusion proteins. Journal of Biomedical Nanotechnology 13, 84–98.Google Scholar
Lubiniecki, AS, Cypess, RH and Lucas, JP (1974) Synergistic interaction of two agents in mice: Japanese B encephalitis virus and Trichinella spiralis. The American Journal of Tropical Medicine and Hygiene 23, 235–241.Google Scholar
Masters, A and Harrison, P (2014) Platelet counting with the BD Accuri(TM) C6 flow cytometer. Platelets 25, 175–180.Google Scholar
McFarlane, AJ, McSorley, HJ, Davidson, DJ, Fitch, PM, Errington, C, Mackenzie, KJ, Gollwitzer, ES, Johnston, CJC, MacDonald, AS, Edwards, MR, Harris, NL, Marsland, BJ, Maizels, RM and Schwarze, J (2017) Enteric helminth-induced type I interferon signaling protects against pulmonary virus infection through interaction with the microbiota. The Journal of Allergy and Clinical Immunology 140, 1068–1078.e6.Google Scholar
Moon, E, Lee, S, Soh, Y, Guo, Y, Piao, Y and Quan, F (2018) Correlates of immune response in Trichinella spiralis infection. Immunological Investigations 47, 605–614.Google Scholar
Murrell, KD and Pozio, E (2011) Worldwide occurrence and impact of human trichinellosis, 1986–2009. Emerging Infectious Diseases 17, 2194–2202.Google Scholar
Openshaw, PJ and Tregoning, JS (2005) Immune responses and disease enhancement during respiratory syncytial virus infection. Clinical Microbiology Reviews 18, 541–555.Google Scholar
Osborne, LC, Monticelli, LA, Nice, TJ, Sutherland, TE, Siracusa, MC, Hepworth, MR, Tomov, VT, Kobuley, D, Tran, SV, Bittinger, K, Bailey, AG, Laughlin, AL, Boucher, JL, Wherry, EJ, Bushman, FD, Allen, JE, Virgin, HW and Artis, D (2014) Coinfection. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science (New York, NY) 345, 578–582.Google Scholar
Porter, KR, Anthony, RL, Solihin, A and Hayes, CG (1995) Mapping of a human T-lymphotropic virus type I gag protein epitope that cross-reacts with anti-Plasmodium falciparum antibodies. Journal of Medical Virology 45, 469–474.Google Scholar
Pozio, E (2007) World distribution of Trichinella spp. infections in animals and humans. Veterinary Parasitology 149, 3–21.Google Scholar
Pozio, E and Zarlenga, DS (2013) New pieces of the Trichinella puzzle. International Journal for Parasitology 43, 983–997.Google Scholar
Purkerson, M and Despommier, D (1974) Fine structure of the muscle phase of Trichinella spiralis in the mouse. In Kim, C (ed.) Trichinellosis. New York: Intext Educational Publishers, pp. 7–24.Google Scholar
Rosca, EC and Simu, M (2018) Border zone brain lesions due to neurotrichinosis. International Journal of Infectious Diseases 67, 43–45.Google Scholar
Schmidt, ME and Varga, SM (2018) The CD8T cell response to respiratory virus infections. Frontiers in Immunology 9, 678.Google Scholar
Shin, K, Watts, GF, Oettgen, HC, Friend, DS, Pemberton, AD, Gurish, MF and Lee, DM (2008) Mouse mast cell tryptase mMCP-6 is a critical link between adaptive and innate immunity in the chronic phase of Trichinella spiralis infection. Journal of Immunology (Baltimore, MD: 1950) 180, 4885–4891.Google Scholar
Sztein, MB, Cuna, WR and Kierszenbaum, F (1990) Trypanosoma cruzi inhibits the expression of CD3, CD4, CD8, and IL-2R by mitogen-activated helper and cytotoxic human lymphocytes. Journal of Immunology (Baltimore, MD: 1950) 144, 3558–3562.Google Scholar
Tanaka, M, Iwamura, Y, Amanuma, H, Irie, Y, Watanabe, M, Watanabe, T, Uchiyama, Y and Yasuraoka, K (1989) Integration and expression of murine retrovirus-related sequences in schistosomes. Parasitology 99(Pt 1), 31–38.Google Scholar
Van Milligen, FJ, Cornelissen, JB, Hendriks, IM, Gaasenbeek, CP and Bokhout, BA (1998) Protection of Fasciola hepatica in the gut mucosa of immune rats is associated with infiltrates of eosinophils, IgG1 and IgG2a antibodies around the parasites. Parasite Immunology 20, 285–292.Google Scholar
Wakelin, D and Donachie, AM (1983) Genetic control of eosinophilia. Mouse strain variation in response to antigens of parasite origin. Clinical and Experimental Immunology 51, 239–246.Google Scholar
Webb, BA and Luckhart, S (1994) Evidence for an early immunosuppressive role for related Campoletis sonorensis venom and ovarian proteins in Heliothis virescens. Archives of Insect Biochemistry and Physiology 26, 147–163.Google Scholar
Webb, BA and Summers, MD (1990) Venom and viral expression products of the endoparasitic wasp Campoletis sonorensis share epitopes and related sequences. Proceedings of the National Academy of Sciences of the USA 87, 4961–4965.Google Scholar
Welliver, RC, Wong, DT, Sun, M, Middleton, E Jr, Vaughan, RS and Ogra, PL (1981) The development of respiratory syncytial virus-specific IgE and the release of histamine in nasopharyngeal secretions after infection. The New England Journal of Medicine 305, 841–846.Google Scholar
Wilson, NO, Hall, RL, Montgomery, SP and Jones, JL (2015) Trichinellosis surveillance – United States, 2008–2012. Morbidity and Mortality Weekly Report. Surveillance Summaries (Washington, DC: 2002) 64, 1–8.Google Scholar
Zepeda, N, Solano, S, Copitin, N, Fernandez, AM, Hernandez, L, Tato, P and Molinari, JL (2010) Decrease of peritoneal inflammatory CD4(+), CD8(+), CD19(+) lymphocytes and apoptosis of eosinophils in a murine Taenia crassiceps infection. Parasitology Research 107, 1129–1135.Google Scholar
Zhu, Q, McAuliffe, JM, Patel, NK, Palmer-Hill, FJ, Yang, CF, Liang, B, Su, L, Zhu, W, Wachter, L, Wilson, S, MacGill, RS, Krishnan, S, McCarthy, MP, Losonsky, GA and Suzich, JA (2011) Analysis of respiratory syncytial virus preclinical and clinical variants resistant to neutralization by monoclonal antibodies palivizumab and/or motavizumab. The Journal of Infectious Diseases 203, 674–682.Google Scholar
Zhu, Q, Patel, NK, McAuliffe, JM, Zhu, W, Wachter, L, McCarthy, MP and Suzich, JA (2012) Natural polymorphisms and resistance-associated mutations in the fusion protein of respiratory syncytial virus (RSV): effects on RSV susceptibility to palivizumab. The Journal of Infectious Diseases 205, 635–638.Google Scholar