Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-27T11:32:41.127Z Has data issue: false hasContentIssue false
  • English
  • Français

Helminth-induced apoptosis: a silent strategy for immunosuppression

Published online by Cambridge University Press:  29 June 2017

AMIN ZAKERI
AMIN ZAKERI*
Affiliation:
Department of Pathobiology, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran
*
*Corresponding author. Department of Pathobiology, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran. E-mail: Aminzakeri7@gmail.com, Amin.zakeri@mail.um.ac.ir
Get access Rights & Permissions [Opens in a new window]

Summary

During microbial infections, both innate and adaptive immunity are activated. Viruses and bacteria usually induce an acute inflammation in the first setting of infection, which helps the eliciting an effective immune response. In contrast, macroparasites such as helminths are a highly successful group of invaders known to be capable of maintaining a chronic infestation with the minimum instigation. Undoubtedly, generating such an immunoregulatory environment requires the exploitation of various immunosuppressive mechanisms to debilitate host immunity supporting their survival and replication. Several mechanisms have been recognized whereby helminths prolong their infections including an increase of immunoregulatory cells, inhibition of Th1 or Th2 responses, targeting pattern recognition receptors (PRRs) and lowering the immune cells quantity via induction of apoptosis. Apoptosis is a programmed intracellular process involving a series of consecutive downstream signalling event evolved to cell death. It plays a pivotal role in several immunological reactions in particular deletion of autoreactive immune cells. Helminth-triggered apoptosis in immune cells exhausts host immunity, which paves the way for generating a permissive environment and chronic infection. This review provides a compilation of recent investigations discussing the apoptotic mechanisms exploited by different worms and the immunological consequences of immune cell death. Finally, the anti-cancer effects of some worm-derived molecules due to their apoptotic effects are discussed, highlighting as potentially druggable candidates to combat cancer.

Keywords

Apoptosishelminthhost–parasite interactionimmunosuppression
Type
Review Article
Information
Parasitology , Volume 144 , Issue 13 , November 2017 , pp. 1663 - 1676
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

REFERENCES

Albert, M. L. (2004). Death-defying immunity: do apoptotic cells influence antigen processing and presentation? Nature Reviews. Immunology 4, 223–231. doi: 10.1038/nri11308.CrossRefGoogle ScholarPubMed
Arce-Sillas, A., Alvarez-Luquin, D. D., Cardenas, G., Casanova-Hernandez, D., Fragoso, G., Hernandez, M., Proano Narvaez, J. V., Garcia-Vazquez, F., Fleury, A., Sciutto, E. and Adalid-Peralta, L. (2016). Interleukin 10 and dendritic cells are the main suppression mediators of regulatory T cells in human neurocysticercosis. Clinical & Experimental Immunology 183, 271–279. doi: 10.1111/cei.12709.CrossRefGoogle ScholarPubMed
Babal, P., Milcheva, R., Petkova, S., Janega, P. and Hurnikova, Z. (2011). Apoptosis as the adaptation mechanism in survival of Trichinella spiralis in the host. Parasitology Research 109, 997–1002. doi: 10.1007/s00436-011-2343-2.CrossRefGoogle ScholarPubMed
Babu, S. and Nutman, T. B. (2012). Immunopathogenesis of lymphatic filarial disease. Seminars in Immunopathology 34, 847–861. doi: 10.1007/s00281-012-0346-4.CrossRefGoogle ScholarPubMed
Babu, S. and Nutman, T. B. (2014). Immunology of lymphatic filariasis. Parasite Immunology 36, 338–346. doi: 10.1111/pim.12081.CrossRefGoogle ScholarPubMed
Babu, S., Blauvelt, C. P. and Nutman, T. B. (2007). Filarial parasites induce NK cell activation, type 1 and type 2 cytokine secretion, and subsequent apoptotic cell death. Journal of Immunology 179, 2445–2456.CrossRefGoogle ScholarPubMed
Bai, L. and Wang, S. (2014). Targeting apoptosis pathways for new cancer therapeutics. Annual Review of Medicine 65, 139–155. doi: 10.1146/annurev-med-010713-141310.CrossRefGoogle ScholarPubMed
Barsoum, R. S., Esmat, G. and El-Baz, T. (2013). Human schistosomiasis: clinical perspective: review. Journal of Advanced Research 4, 433–444. doi: 10.1016/j.jare.2013.01.005.CrossRefGoogle ScholarPubMed
Bienvenu, A. L., Gonzalez-Rey, E. and Picot, S. (2010). Apoptosis induced by parasitic diseases. Parasites & Vectors 3, 106. doi: 10.1186/1756-3305-3-106.CrossRefGoogle ScholarPubMed
Brindley, P. J., da Costa, J. M. C. and Sripa, B. (2015). Why does infection with some helminths cause cancer?. Trends in Cancer 1, 174–182.CrossRefGoogle ScholarPubMed
Brunetti, E., Garcia, H. H., Junghanss, T. and International Ce Workshop in Lima, P. (2011). Cystic echinococcosis: chronic, complex, and still neglected. PLOS Neglected Tropical Diseases 5, e1146. doi: 10.1371/journal.pntd.0001146.CrossRefGoogle ScholarPubMed
Burke, M. L., Jones, M. K., Gobert, G. N., Li, Y. S., Ellis, M. K. and McManus, D. P. (2009). Immunopathogenesis of human schistosomiasis. Parasite Immunology 31, 163–176. doi: 10.1111/j.1365-3024.2009.01098.x.CrossRefGoogle ScholarPubMed
Carneiro-Santos, P., Martins-Filho, O., Alves-Oliveira, L. F., Silveira, A. M., Coura-Filho, P., Viana, I. R., Wilson, R. A. and Correa-Oliveira, R. (2000). Apoptosis: a mechanism of immunoregulation during human Schistosomiasis mansoni . Parasite Immunology 22, 267–277.CrossRefGoogle ScholarPubMed
Carrero, J. A. and Unanue, E. R. (2006). Lymphocyte apoptosis as an immune subversion strategy of microbial pathogens. Trends in Immunology 27, 497–503. doi: 10.1016/j.it.2006.09.005.CrossRefGoogle ScholarPubMed
Chen, K. M., Lee, H. H., Lai, S. C., Hsu, L. S., Wang, C. J. and Liu, J. Y. (2008). Apoptosis in meningoencephalitis of Angiostrongylus cantonensis-infected mice. Experimental Parasitology 119, 385–390. doi: 10.1016/j.exppara.2008.03.013.CrossRefGoogle ScholarPubMed
Chen, L., Rao, K. V., He, Y. X. and Ramaswamy, K. (2002). Skin-stage schistosomula of Schistosoma mansoni produce an apoptosis-inducing factor that can cause apoptosis of T cells. Journal of Biological Chemistry 277, 34329–34335. doi: 10.1074/jbc.M201344200.CrossRefGoogle ScholarPubMed
Chow, S. C., Brown, A. and Pritchard, D. (2000). The human hookworm pathogen Necator americanus induces apoptosis in T lymphocytes. Parasite Immunology 22, 21–29.CrossRefGoogle ScholarPubMed
Cliffe, L. J., Potten, C. S., Booth, C. E. and Grencis, R. K. (2007). An increase in epithelial cell apoptosis is associated with chronic intestinal nematode infection. Infection and Immunity 75, 1556–1564. doi: 10.1128/IAI.01375-06.CrossRefGoogle ScholarPubMed
Cwiklinski, K., O'Neill, S. M., Donnelly, S. and Dalton, J. P. (2016). A prospective view of animal and human Fasciolosis. Parasite Immunology 38, 558–568. doi: 10.1111/pim.12343.CrossRefGoogle ScholarPubMed
Das Mohapatra, A., Panda, S. K., Pradhan, A. K., Prusty, B. K., Satapathy, A. K. and Ravindran, B. (2014). Filarial antigens mediate apoptosis of human monocytes through Toll-like receptor 4. Journal of Infectious Diseases 210, 1133–1144. doi: 10.1093/infdis/jiu208.CrossRefGoogle ScholarPubMed
Devitt, A. and Marshall, L. J. (2011). The innate immune system and the clearance of apoptotic cells. Journal of Leukocyte Biology 90, 447–457. doi: 10.1189/jlb.0211095.CrossRefGoogle ScholarPubMed
Diaz, A., Casaravilla, C., Barrios, A. A. and Ferreira, A. M. (2016). Parasite molecules and host responses in cystic echinococcosis. Parasite Immunology 38, 193–205. doi: 10.1111/pim.12282.CrossRefGoogle ScholarPubMed
Dimri, U., Singh, S. K., Sharma, M. C., Behera, S. K., Kumar, D. and Tiwari, P. (2012). Oxidant/antioxidant balance, minerals status and apoptosis in peripheral blood of dogs naturally infected with Dirofilaria immitis . Research in Veterinary Science 93, 296–299. doi: 10.1016/j.rvsc.2011.04.022.CrossRefGoogle Scholar
Duan, Y., Gu, X., Zhu, D., Sun, W., Chen, J., Feng, J., Song, K., Xu, F., He, X. and He, X. (2014). Schistosoma japonicum soluble egg antigens induce apoptosis and inhibit activation of hepatic stellate cells: a possible molecular mechanism. International Journal for Parasitology 44, 217–224. doi: 10.1016/j.ijpara.2013.11.003.CrossRefGoogle ScholarPubMed
Escamilla, A., Bautista, M. J., Zafra, R., Pacheco, I. L., Ruiz, M. T., Martinez-Cruz, S., Mendez, A., Martinez-Moreno, A., Molina-Hernandez, V. and Perez, J. (2016). Fasciola hepatica induces eosinophil apoptosis in the migratory and biliary stages of infection in sheep. Veterinary Parasitology 216, 84–88. doi: 10.1016/j.vetpar.2015.12.013.CrossRefGoogle ScholarPubMed
Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y. and Henson, P. M. (1998). Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. Journal of Clinical Investigation 101, 890–898. doi: 10.1172/JCI1112.CrossRefGoogle ScholarPubMed
Felton, J. M., Lucas, C. D., Rossi, A. G. and Dransfield, I. (2014). Eosinophils in the lung – modulating apoptosis and efferocytosis in airway inflammation. Frontiers in Immunology 5, 302. doi: 10.3389/fimmu.2014.00302.CrossRefGoogle ScholarPubMed
Fernald, K. and Kurokawa, M. (2013). Evading apoptosis in cancer. Trends in Cell Biology 23, 620–633. doi: 10.1016/j.tcb.2013.07.006.CrossRefGoogle ScholarPubMed
Fleury, A., Cardenas, G., Adalid-Peralta, L., Fragoso, G. and Sciutto, E. (2016). Immunopathology in Taenia solium neurocysticercosis. Parasite Immunology 38, 147–157. doi: 10.1111/pim.12299.CrossRefGoogle ScholarPubMed
Gazzinelli-Guimaraes, P. H., Souza-Fagundes, E. M., Cancado, G. G., Martins, V. G., Dhom-Lemos, L. C., Ricci, N. D., Fiuza, J. A., Bueno, L. L., Miranda, R. R., Guatimosim, S., Gazzinelli, A., Correa-Oliveira, R., Bartholomeu, D. C. and Fujiwara, R. T. (2013). Cell apoptosis induced by hookworm antigens: a strategy of immunomodulation. Frontiers in Bioscience (Elite Ed) 5, 662–675.Google ScholarPubMed
Gonzales, I., Rivera, J. T., Garcia, H. H. and Cysticercosis Working Group in P. (2016). Pathogenesis of Taenia solium taeniasis and cysticercosis. Parasite Immunology 38, 136–146. doi: 10.1111/pim.12307.CrossRefGoogle Scholar
Gottstein, B., Pozio, E. and Nöckler, K. (2009). Epidemiology, diagnosis, treatment, and control of trichinellosis. Clinical microbiology reviews 22, 127–145.CrossRefGoogle ScholarPubMed
Gouveia, M. J., Santos, J., Brindley, P. J., Rinaldi, G., Lopes, C., Santos, L. L., da Costa, J. M. and Vale, N. (2015). Estrogen-like metabolites and DNA-adducts in urogenital schistosomiasis-associated bladder cancer. Cancer Letters 359, 226–232.CrossRefGoogle ScholarPubMed
Guasconi, L., Serradell, M. C. and Masih, D. T. (2012). Fasciola hepatica products induce apoptosis of peritoneal macrophages. Veterinary Immunology and Immunopathology 148, 359–363. doi: 10.1016/j.vetimm.2012.06.022.CrossRefGoogle ScholarPubMed
Hartmann, W., Brenz, Y., Kingsley, M. T., Ajonina-Ekoti, I., Brattig, N. W., Liebau, E. and Breloer, M. (2013). Nematode-derived proteins suppress proliferation and cytokine production of antigen-specific T cells via induction of cell death. PLoS ONE 8, e68380. doi: 10.1371/journal.pone.0068380.CrossRefGoogle ScholarPubMed
Herold, S., Ludwig, S., Pleschka, S. and Wolff, T. (2012). Apoptosis signaling in influenza virus propagation, innate host defense, and lung injury. Journal of Leukocyte Biology 92, 75–82. doi: 10.1189/jlb.1011530.CrossRefGoogle ScholarPubMed
Huang, L. and Appleton, J. A. (2016). Eosinophils in Helminth infection: defenders and dupes. Trends in Parasitology 32, 798–807. doi: 10.1016/j.pt.2016.05.004.CrossRefGoogle ScholarPubMed
Jenson, J. S., O'Connor, R., Osborne, J. and Devaney, E. (2002). Infection with Brugia microfilariae induces apoptosis of CD4(+) T lymphocytes: a mechanism of immune unresponsiveness in filariasis. European Journal of Immunology 32, 858–867. doi: 10.1002/1521-4141(200203)32:3<60;858::AID-IMMU858><60;858::AID-IMMU858>3.0.CO;2-E.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Jusakul, A., Loilome, W., Namwat, N., Haigh, W. G., Kuver, R., Dechakhamphu, S., Sukontawarin, P., Pinlaor, S., Lee, S. P. and Yongvanit, P. (2012). Liver fluke-induced hepatic oxysterols stimulate DNA damage and apoptosis in cultured human cholangiocytes. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 731, 48–57.CrossRefGoogle ScholarPubMed
Kang, Y. J., Jo, J. O., Cho, M. K., Yu, H. S., Leem, S. H., Song, K. S., Ock, M. S. and Cha, H. J. (2013). Trichinella spiralis infection reduces tumor growth and metastasis of B16-F10 melanoma cells. Veterinary Parasitology 196, 106–113. doi: 10.1016/j.vetpar.2013.02.021.CrossRefGoogle ScholarPubMed
Kuroda, A., Uchikawa, R., Matsuda, S., Yamada, M., Tegoshi, T. and Arizono, N. (2002). Up-regulation of Fas (CD95) and induction of apoptosis in intestinal epithelial cells by nematode-derived molecules. Infection and immunity 70, 4002–4008.CrossRefGoogle ScholarPubMed
Kushwah, R. and Hu, J. (2010). Dendritic cell apoptosis: regulation of tolerance versus immunity. Journal of Immunology 185, 795–802. doi: 10.4049/jimmunol.1000325.CrossRefGoogle ScholarPubMed
Lopez-Briones, S., Sciutto, E., Ventura, J. L., Zentella, A. and Fragoso, G. (2003). CD4+ and CD19+ splenocytes undergo apoptosis during an experimental murine infection with Taenia crassiceps . Parasitology Research 90, 157–163. doi: 10.1007/s00436-003-0829-2.CrossRefGoogle ScholarPubMed
Luder, C. G., Gross, U. and Lopes, M. F. (2001). Intracellular protozoan parasites and apoptosis: diverse strategies to modulate parasite-host interactions. Trends in Parasitology 17, 480–486.CrossRefGoogle ScholarPubMed
Lundy, S. K. and Boros, D. L. (2002). Fas ligand-expressing B-1a lymphocytes mediate CD4+-T-cell apoptosis during schistosomal infection: induction by interleukin 4 (IL-4) and IL-10. Infection and Immunity 70, 812–819.CrossRefGoogle ScholarPubMed
Lundy, S. K., Lerman, S. P. and Boros, D. L. (2001). Soluble egg antigen-stimulated T helper lymphocyte apoptosis and evidence for cell death mediated by FasL+ T and B cells during murine Schistosoma mansoni infection. Infection and Immunity 69, 271–280.CrossRefGoogle Scholar
Maizels, R. M. and McSorley, H. J. (2016). Regulation of the host immune system by helminth parasites. Journal of Allergy and Clinical Immunology 138, 666–675. doi: 10.1016/j.jaci.2016.07.007.CrossRefGoogle ScholarPubMed
McGuckin, M. A., Eri, R. D., Das, I., Lourie, R. and Florin, T. H. (2010). ER stress and the unfolded protein response in intestinal inflammation. American Journal of Physiology. Gastrointestinal and Liver Physiology 298, G820–832. doi: 10.1152/ajpgi.00063.2010.CrossRefGoogle ScholarPubMed
Min, D. Y., Lee, Y. A., Ryu, J. S., Ahn, M. H., Chung, Y. B., Sim, S. and Shin, M. H. (2004). Caspase-3-mediated apoptosis of human eosinophils by the tissue-invading helminth Paragonimus westermani . International Archives of Allergy and Immunology 133, 357–364. doi: 10.1159/000077355.CrossRefGoogle ScholarPubMed
Mishra, R., Panda, S. K., Sahoo, P. K., Bal, and Satapathy, A. K. (2017). Increased Fas ligand expression of peripheral B-1 cells correlated with CD4+ T cell apoptosis in filarial infected patients. Parasite Immunology 39, e12421. doi: 10.1111/pim.12421.CrossRefGoogle ScholarPubMed
Moreau, E. and Chauvin, A. (2010). Immunity against helminths: interactions with the host and the intercurrent infections. Journal of Biomedicine and Biotechnology 2010, 428593. doi: 10.1155/2010/428593.CrossRefGoogle ScholarPubMed
Narasimhan, P. B., Bennuru, S., Meng, Z., Cotton, R. N., Elliott, K. R., Ganesan, S., McDonald-Fleming, R., Veenstra, T. D., Nutman, T. B. and Semnani, R. T. (2016). Microfilariae of Brugia malayi inhibit the mTOR pathway and induce autophagy in human dendritic cells. Infection and Immunity 84, 2463–2472.CrossRefGoogle ScholarPubMed
Nono, J. K., Pletinckx, K., Lutz, M. B. and Brehm, K. (2012). Excretory/secretory-products of Echinococcus multilocularis larvae induce apoptosis and tolerogenic properties in dendritic cells in vitro . PLOS Neglected Tropical Diseases 6, e1516. doi: 10.1371/journal.pntd.0001516.CrossRefGoogle ScholarPubMed
Obieglo, K., Feng, X., Bollampalli, V. P., Dellacasa-Lindberg, I., Classon, C., Osterblad, M., Helmby, H., Hewitson, J. P., Maizels, R. M., Gigliotti Rothfuchs, A. and Nylen, S. (2016). Chronic gastrointestinal nematode infection mutes immune responses to mycobacterial infection distal to the gut. Journal of Immunology 196, 2262–2271. doi: 10.4049/jimmunol.1500970.CrossRefGoogle ScholarPubMed
O'Connell, E. M. and Nutman, T. B. (2015). Eosinophilia in infectious diseases. Immunology and Allergy Clinics of North America 35, 493–522. doi: 10.1016/j.iac.2015.05.003.CrossRefGoogle ScholarPubMed
O'Connor, R. A., Jenson, J. S., Osborne, J. and Devaney, E. (2003). An enduring association? Microfilariae and immunosuppression [correction of immunosupression] in lymphatic filariasis. Trends in Parasitology 19, 565–570.CrossRefGoogle ScholarPubMed
Ohshima, H., Bandaletova, T. Y., Brouet, I., Bartsch, H., Kirby, G., Ogunbiyi, F., Vatanasapt, V. and Pipitgool, V. (1994). Increased nitrosamine and nitrate biosynthesis mediated by nitric oxide synthase induced in hamsters infected with liver fluke (Opisthorchis viverrini). Carcinogenesis 15, 271–275.CrossRefGoogle ScholarPubMed
Opferman, J. T. (2008). Apoptosis in the development of the immune system. Cell Death & Differentiation 15, 234–242. doi: 10.1038/sj.cdd.4402182.CrossRefGoogle ScholarPubMed
Pearce, E. J. and MacDonald, A. S. (2002). The immunobiology of schistosomiasis. Nature Reviews Immunology 2, 499–511. doi: 10.1038/nri843.CrossRefGoogle ScholarPubMed
Peón, A. N., Espinoza-Jiménez, A. and Terrazas, L. I. (2013). Immunoregulation by Taenia crassiceps and its antigens. BioMed Research International 2013, 498583. doi: 10.1155/2013/498583.CrossRefGoogle ScholarPubMed
Piekarska, J., Michalski, A., Szczypka, M. and Obminska-Mrukowicz, B. (2009 a). Trichinella spiralis: effect of thymus factor X on apoptosis and necrosis in mice. Experimental Parasitology 123, 128–133. doi: 10.1016/j.exppara.2009.06.009.CrossRefGoogle ScholarPubMed
Piekarska, J., Szczypka, M., Obminska-Mrukowicz, B. and Gorczykowski, M. (2009 b). Effect of phytohaemagglutinin-P on apoptosis and necrosis in Trichinella spiralis infected mice. Veterinary Parasitology 159, 240–244. doi: 10.1016/j.vetpar.2008.10.050.CrossRefGoogle ScholarPubMed
Prendergast, C. T., Sanin, D. E., Cook, P. C. and Mountford, A. P. (2015). CD4+ T cell hyporesponsiveness after repeated exposure to Schistosoma mansoni larvae is dependent upon interleukin-10. Infection and Immunity 83, 1418–1430. doi: 10.1128/IAI.02831-14.CrossRefGoogle ScholarPubMed
Robinson, M. W. and Dalton, J. P. (2009). Zoonotic helminth infections with particular emphasis on fasciolosis and other trematodiases. Philosophical transactions of the Royal Society of London. Series B, Biological Sciences 364, 2763–2776. doi: 10.1098/rstb.2009.0089.CrossRefGoogle ScholarPubMed
Sciutto, E., Chavarria, A., Fragoso, G., Fleury, A. and Larralde, C. (2007). The immune response in Taenia solium cysticercosis: protection and injury. Parasite Immunology 29, 621–636. doi: 10.1111/j.1365-3024.2007.00967.x.CrossRefGoogle ScholarPubMed
Semnani, R. T. and Nutman, T. B. (2004). Toward an understanding of the interaction between filarial parasites and host antigen-presenting cells. Immunological Reviews 201, 127–138. doi: 10.1111/j.0105-2896.2004.00196.x.CrossRefGoogle ScholarPubMed
Semnani, R. T., Venugopal, P. G., Mahapatra, L., Skinner, J. A., Meylan, F., Chien, D., Dorward, D. W., Chaussabel, D., Siegel, R. M. and Nutman, T. B. (2008). Induction of TRAIL- and TNF-alpha-dependent apoptosis in human monocyte-derived dendritic cells by microfilariae of Brugia malayi . Journal of Immunology 181, 7081–7089.CrossRefGoogle ScholarPubMed
Serradell, M. C., Guasconi, L., Cervi, L., Chiapello, L. S. and Masih, D. T. (2007). Excretory-secretory products from Fasciola hepatica induce eosinophil apoptosis by a caspase-dependent mechanism. Veterinary Immunology and Immunopathology 117, 197–208. doi: 10.1016/j.vetimm.2007.03.007.CrossRefGoogle ScholarPubMed
Serradell, M. C., Guasconi, L. and Masih, D. T. (2009). Involvement of a mitochondrial pathway and key role of hydrogen peroxide during eosinophil apoptosis induced by excretory-secretory products from Fasciola hepatica . Molecular and Biochemical Parasitology 163, 95–106. doi: 10.1016/j.molbiopara.2008.10.005.CrossRefGoogle ScholarPubMed
Sikasunge, C. S., Phiri, I. K., Johansen, M. V., Willingham, A. L. 3rd and Leifsson, P. S. (2008). Host-cell apoptosis in Taenia solium-induced brain granulomas in naturally infected pigs. Parasitology 135, 1237–1242. doi: 10.1017/S0031182008004678.CrossRefGoogle ScholarPubMed
Smith, P., Walsh, C. M., Mangan, N. E., Fallon, R. E., Sayers, J. R., McKenzie, A. N. and Fallon, P. G. (2004). Schistosoma mansoni worms induce anergy of T cells via selective up-regulation of programmed death ligand 1 on macrophages. Journal of Immunology 173, 1240–1248.CrossRefGoogle ScholarPubMed
Sofronic-Milosavljevic, L., Ilic, N., Pinelli, E. and Gruden-Movsesijan, A. (2015). Secretory products of Trichinella spiralis muscle larvae and immunomodulation: implication for autoimmune diseases, allergies, and malignancies. Journal of Immunology Research 2015, 523875. doi: 10.1155/2015/523875.CrossRefGoogle ScholarPubMed
Solano, S., Cortes, I. M., Copitin, N. I., Tato, P. and Molinari, J. L. (2006). Lymphocyte apoptosis in the inflammatory reaction around Taenia solium metacestodes in porcine cysticercosis. Veterinary Parasitology 140, 171–176. doi: 10.1016/j.vetpar.2006.03.006.CrossRefGoogle ScholarPubMed
Tato, P., Fernandez, A. M., Solano, S., Borgonio, V., Garrido, E., Sepulveda, J. and Molinari, J. L. (2004). A cysteine protease from Taenia solium metacestodes induce apoptosis in human CD4+ T-cells. Parasitology Research 92, 197–204. doi: 10.1007/s00436-003-1008-1.CrossRefGoogle ScholarPubMed
Valanparambil, R. M., Tam, M., Jardim, A., Geary, T. G. and Stevenson, M. M. (2017). Primary Heligmosomoides polygyrus bakeri infection induces myeloid-derived suppressor cells that suppress CD4+ Th2 responses and promote chronic infection. Mucosal Immunology, 10, 238–249. doi: 10.1038/mi.2016.36.CrossRefGoogle ScholarPubMed
Vasilev, S., Ilic, N., Gruden-Movsesijan, A., Vasilijic, S., Bosic, M. and Sofronic-Milosavljevic, L. (2015). Necrosis and apoptosis in Trichinella spiralis-mediated tumour reduction. Central European Journal of Immunology 40, 42–53. doi: 10.5114/ceji.2015.50832.CrossRefGoogle ScholarPubMed
Voll, R. E., Herrmann, M., Roth, E. A., Stach, C., Kalden, J. R. and Girkontaite, I. (1997). Immunosuppressive effects of apoptotic cells. Nature 390, 350–351. doi: 10.1038/37022.CrossRefGoogle ScholarPubMed
Wang, J., Xu, F., Zhu, D., Duan, Y., Chen, J., Sun, X., He, X., Li, P., Sun, W. and Feng, J. (2014). Schistosoma japonicum soluble egg antigens facilitate hepatic stellate cell apoptosis by downregulating Akt expression and upregulating p53 and DR5 expression. PLOS Neglected Tropical Diseases 8, e3106.CrossRefGoogle ScholarPubMed
Wang, X. L., Fu, B. Q., Yang, S. J., Wu, X. P., Cui, G. Z., Liu, M. F., Zhao, Y., Yu, Y. L., Liu, X. Y., Deng, H. K., Chen, Q. J. and Liu, M. Y. (2009). Trichinella spiralis–a potential anti-tumor agent. Veterinary Parasitology 159, 249–252. doi: 10.1016/j.vetpar.2008.10.052.CrossRefGoogle ScholarPubMed
Wang, X. L., Liu, M. Y., Sun, S. M., Liu, X. L., Yu, L., Wang, X. R., Chu, L. X., Rosenthal, B., Shi, H. N., Boireau, P., Wang, F., Zhao, Y. and Wu, X. P. (2013). An anti-tumor protein produced by Trichinella spiralis induces apoptosis in human hepatoma H7402 cells. Veterinary Parasitology 194, 186–188. doi: 10.1016/j.vetpar.2013.01.052.CrossRefGoogle ScholarPubMed
Yan, H. L., Xue, G., Mei, Q., Ding, F. X., Wang, Y. Z. and Sun, S. H. (2008). Calcium-dependent proapoptotic effect of Taenia solium metacestodes annexin B1 on human eosinophils: a novel strategy to prevent host immune response. International Journal of Biochemistry & Cell Biology 40, 2151–2163. doi: 10.1016/j.biocel.2008.02.018.CrossRefGoogle ScholarPubMed
Yang, F., Sun, X., Shen, J., Yu, L. P., Liang, J. Y., Zheng, H. Q. and Wu, Z. D. (2013). A recombined protein (rSj16) derived from Schistosoma japonicum induces cell cycle arrest and apoptosis of murine myeloid leukemia cells. Parasitology Research 112, 1261–1272. doi: 10.1007/s00436-012-3260-8.CrossRefGoogle ScholarPubMed
Yu, Y. R., Deng, M. J., Lu, W. W., Zhang, J. S., Jia, M. Z., Huang, J. and Qi, Y. F. (2014). Endoplasmic reticulum stress-mediated apoptosis is activated in intestines of mice with Trichinella spiralis infection. Experimental Parasitology 145, 1–6. doi: 10.1016/j.exppara.2014.06.017.CrossRefGoogle ScholarPubMed
Zakeri, A., Borji, H. and Haghparast, A. (2016). Interaction between helminths and toll-like receptors: possibilities and potentials for asthma therapy. International Reviews of Immunology 35, 219–248. doi: 10.3109/08830185.2015.1096936.CrossRefGoogle ScholarPubMed
Zepeda, N., Solano, S., Copitin, N., Fernandez, A. M., Hernandez, L., Tato, P. and Molinari, J. L. (2010). Decrease of peritoneal inflammatory CD4(+), CD8(+), CD19(+) lymphocytes and apoptosis of eosinophils in a murine Taenia crassiceps infection. Parasitology Research 107, 1129–1135. doi: 10.1007/s00436-010-1980-1.CrossRefGoogle Scholar
Zepeda, N., Tirado, R., Copitin, N., Solano, S., Fernandez, A. M., Tato, P. and Molinari, J. L. (2016). A Taenia crassiceps factor induces apoptosis of spleen CD4+T cells and TFG-β and Foxp3 gene expression in mice. Journal of Helminthology 90, 223–231. doi: 10.1017/S0022149X1500022X.CrossRefGoogle ScholarPubMed
Zepeda, N., Solano, S., Copitin, N., Chavez, J. L., Fernandez, A. M., Garcia, F., Tato, P. and Molinari, J. L. (2017). Apoptosis of mouse hippocampal cells induced by Taenia crassiceps metacestode factor. Journal of Helminthology 91, 215–221. doi: 10.1017/S0022149X16000146.CrossRefGoogle ScholarPubMed
Zhang, C., Wang, J., Lu, G., Li, J., Lu, X., Mantion, G., Vuitton, D. A., Wen, H. and Lin, R. (2012). Hepatocyte proliferation/growth arrest balance in the liver of mice during E. multilocularis infection: a coordinated 3-stage course. PLoS ONE 7, e30127. doi: 10.1371/journal.pone.0030127.CrossRefGoogle Scholar
Zhang, W., Ross, A. G. and McManus, D. P. (2008). Mechanisms of immunity in hydatid disease: implications for vaccine development. Journal of Immunology 181, 6679–6685.CrossRefGoogle ScholarPubMed