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Brief Communication

Syphacia obvelata: A New Hope to Induction of Intestinal Immunological Tolerance in C57BL/6 Mice
Niloofar Taghipour, Nariman Mosaffa, Mohammad Rostami-Nejad, Mohamad Mohsen Homayoni, Esmaeil Mortaz, Hamid Asadzadeh Aghdaei, Mohammad Reza Zali
Korean J Parasitol 2017;55(4):439-444.
Published online August 31, 2017
DOI: https://doi.org/10.3347/kjp.2017.55.4.439
The ability of nematodes to manipulate the immune system of their host towards a Th2 and T regulatory responses has been proposed to suppress the inflammatory response. Clinical trials have proposed a useful effect of helminth infections on improvement of inflammatory disorders. In this study, we investigated the immunomodulatory effect of Syphacia obvelata infection to induce intestinal tolerance in C57BL/6 mice. Mice were infected through the cagemates with self-infected BALB/c mice. Four weeks post-infection, expression levels of IFN-γ, TNF-α, IL-17, and IL-10 were assessed in the supernatant of mesenteric lymph node (MLN) culture. Foxp3+Treg were measured in MLN cells by flow cytometry. In the S. obvelata-infected group, the percentage of Tregs (5.2±0.4) was significantly higher than the control (3.6±0.5) (P<0.05). The levels of IL-10 (55.3±2.2 vs 35.2±3.2), IL-17 (52.9±3.8 vs 41±1.8), IFN-γ (44.8±4.8 vs 22.3±2.3) and TNF-α (71.1±5.8 vs 60.1±3.3) were significantly increased in infected mice compared to the control group (P<0.05). The above results showed the potential effects of S. obvelata to induce intestinal tolerance. Therefore, it seems that S. obvelata may increase the immunological suppressive function in the intestinal tract.

Citations

Citations to this article as recorded by  Crossref logo
  • Syphacia obvelata antigens alter the FOXP3/RORɣt expression balance in isolated peripheral blood mononuclear cells of IBD patients
    Abbas Amin, Niloofar Taghipour, Mohammad Rostami-Nejad, Foroogh Alborzi Avanaki, Reyhaneh Jafarshad, Seyyed Javad Seyyed Tabaei, Nariman Mosaffa
    Scientific Reports.2025;[Epub]     CrossRef
  • Potential anthelmintic effect of chitosan on Syphacia muris infecting Wistar rats: biochemical, immunological, and histopathological studies
    Nesma A. Mostafa, Salwa A. H. Hamdi, Mona F. Fol
    Scientific Reports.2024;[Epub]     CrossRef
  • Immune response, oxidative stress, and histological changes of Wistar rats after being administered with Parascaris equorum antigen
    Salma Adel Yehia, Abeer Mahmoud Badr, Abdel-Rahman Bashtar, Mahmoud Abdel-Aziz Ibrahim, Mohamed Refat Mousa, Nesma Abbas Mostafa
    Scientific Reports.2024;[Epub]     CrossRef
  • Immunomodulatory effect of Dicrocoelium dendriticum ova on DSS-induced experimental colitis in C57BL/6 mouse
    Leila Mighani, Malihe Eilakinezhad, Seyed-Alireza Esmaeili, Majid Khazaei, Moein Eskandari, Seyedeh Elnaz Nazari, Mojtaba Mousavi Bazaz, Khatereh kharazmi, Elham Moghaddas, Mehdi Zarean
    Scientific Reports.2024;[Epub]     CrossRef
  • Isolation and Functions of Extracellular Vesicles Derived from Parasites: The Promise of a New Era in Immunotherapy, Vaccination, and Diagnosis


    Mojdeh Khosravi, Elnaz Sadat Mirsamadi, Hamed Mirjalali, Mohammad Reza Zali
    International Journal of Nanomedicine.2020; Volume 15: 2957.     CrossRef
  • Immunomodulatory effect of Syphacia obvelata in treatment of experimental DSS-induced colitis in mouse model
    Niloofar Taghipour, Nariman Mosaffa, Hamid Asadzadeh Aghdaei, Mohammad Rostami-Nejad, Joel V. Weinstock, Sarira Shahnavaz, Mohammad Reza Zali
    Scientific Reports.2019;[Epub]     CrossRef
  • Hypothesis: Multiple sclerosis is caused by three-hits, strictly in order, in genetically susceptible persons
    Patrick K A Kearns, Helen A Casey, John Paul Leach
    Multiple Sclerosis and Related Disorders.2018; 24: 157.     CrossRef
  • 8,614 View
  • 137 Download
  • 7 Web of Science
  • Crossref

Original Articles

Activation and Recruitment of Regulatory T Cells via Chemokine Receptor Activation in Trichinella spiralis-Infected Mice
Jeong-Bin Ahn, Shin Ae Kang, Dong-Hee Kim, Hak Sun Yu
Korean J Parasitol 2016;54(2):163-171.
Published online April 30, 2016
DOI: https://doi.org/10.3347/kjp.2016.54.2.163
As most infections by the helminth parasite elicit the recruitment of CD4+CD25+Foxp3+ T (Treg) cells, many scientists have suggested that these cells could be used for the treatment of immune-mediated inflammation and associated diseases. In order to investigate the distribution and alteration of activated Treg cells, we compared the expression levels of Treg cell activation markers in the ileum and gastrocnemius tissues 1, 2, and 4 weeks after infection. The number of Treg cells was monitored using GFP-coded Foxp3 transgenic mice. In mice at 1 week after Trichinella spiralis infection, the number of activated Treg cells was higher than in the control group. In mice at 2 weeks after infection, there was a significant increase in the number of cells expressing Foxp3 and CTLA-4 when compared to the control group and mice at 1 week after infection. At 4 weeks after infection, T. spiralis was easily identifiable in nurse cells in mouse muscles. In the intestine, the expression of Gzmb and Klrg1 decreased over time and that of Capg remained unchanged for the first and second week, then decreased in the 4th week. However, in the muscles, the expression of most chemokine genes was increased due to T. spiralis infection, in particular the expression levels of Gzmb, OX40, and CTLA-4 increased until week 4. In addition, increased gene expression of all chemokine receptors in muscle, CXCR3, CCR4, CCR5, CCR9, and CCR10, was observed up until the 4th week. In conclusion, various chemokine receptors showed increased expressions combined with recruitment of Treg cells in the muscle tissue.

Citations

Citations to this article as recorded by  Crossref logo
  • Trichinella spiralis adult excretory-secretory antigen promotes peripheral regulatory T cell differentiation and attenuates experimental colitis via TGF-β-like mechanisms
    Xi-Meng Sun, Ze-Ni Luo, Wei Wang, Chun-Yue Hao, Zhi-Ang Li, Saeed El-Ashram, Xin-Ping Zhu
    Parasites & Vectors.2025;[Epub]     CrossRef
  • Chemokines and chemokine receptors: Insights from human disease and experimental models of helminthiasis
    Lucas Kraemer, Derek M. McKay, Remo Castro Russo, Ricardo Toshio Fujiwara
    Cytokine & Growth Factor Reviews.2022; 66: 38.     CrossRef
  • Trichinella-induced immunomodulation: Another tale of helminth success
    F. Bruschi, D.S. Ashour, A.A. Othman
    Food and Waterborne Parasitology.2022; 27: e00164.     CrossRef
  • Regulatory T‐cells in helminth infection: induction, function and therapeutic potential
    Madeleine P. J. White, Caitlin M. McManus, Rick M. Maizels
    Immunology.2020; 160(3): 248.     CrossRef
  • Trichinella spiralis:inflammation modulator
    Jing Ding, Xiaolei Liu, Xue Bai, Yang Wang, Jian Li, Chun Wang, Shicun Li, Mingyuan Liu, Xuelin Wang
    Journal of Helminthology.2020;[Epub]     CrossRef
  • Effect of Cytotoxic T-Lymphocyte Antigen-4 on the Efficacy of the Fatty Acid-Binding Protein Vaccine Against Schistosoma japonicum
    Chun-lian Tang, Qun Pan, Ya-ping Xie, Ying Xiong, Rong-hui Zhang, Jin Huang
    Frontiers in Immunology.2019;[Epub]     CrossRef
  • Regulatory effect of two Trichinella spiralis serine protease inhibitors on the host’s immune system
    Jingyun Xu, Pengcheng Yu, Lijia Wu, Mingxu Liu, Yixin Lu
    Scientific Reports.2019;[Epub]     CrossRef
  • The opposite roles of PAS-5 and Galectin-1 in immune response during the early infection of Angiostrongylus cantonensis
    Lan-Zhu Yan, Xiao-Meng Shi, Yan-Wen Zu, Yuan-Yuan Shen, Xi-Xi Chen, Meng-Jing Zhao, Xing-Pan Li, Bao-Long Yan, Hui-Cong Huang
    Parasites & Vectors.2018;[Epub]     CrossRef
  • 10,189 View
  • 129 Download
  • 8 Web of Science
  • Crossref
Age-Related CD4+CD25+Foxp3+ Regulatory T-Cell Responses During Plasmodium berghei ANKA Infection in Mice Susceptible or Resistant to Cerebral Malaria
Ying Shan, Jun Liu, Yan-Yan Pan, Yong-Jun Jiang, Hong Shang, Ya-Ming Cao
Korean J Parasitol 2013;51(3):289-295.
Published online June 30, 2013
DOI: https://doi.org/10.3347/kjp.2013.51.3.289

Different functions have been attributed to CD4+CD25+Foxp3+ regulatory T-cells (Tregs) during malaria infection. Herein, we describe the disparity in Treg response and pro- and anti-inflammatory cytokines during infection with Plasmodium berghei ANKA between young (3-week-old) and middle-aged (8-month-old) C57BL/6 mice. Young mice were susceptible to cerebral malaria (CM), while the middle-aged mice were resistant to CM and succumbed to hyperparasitemia and severe anemia. The levels of pro-inflammatory cytokines, such as TNF-α, in young CM-susceptible mice were markedly higher than in middle-aged CM-resistant mice. An increased absolute number of Tregs 3-5 days post-inoculation, co-occurring with elevated IL-10 levels, was observed in middle-aged CM-resistant mice but not in young CM-susceptible mice. Our findings suggest that Treg proliferation might be associated with the suppression of excessive pro-inflammatory Th1 response during early malaria infection, leading to resistance to CM in the middle-aged mice, possibly in an IL-10-dependent manner.

Citations

Citations to this article as recorded by  Crossref logo
  • Contribution of Magnetic Resonance Imaging Studies to the Understanding of Cerebral Malaria Pathogenesis
    Alicia Comino Garcia-Munoz, Isabelle Varlet, Georges Emile Grau, Teodora-Adriana Perles-Barbacaru, Angèle Viola
    Pathogens.2024; 13(12): 1042.     CrossRef
  • Mechanistic insights into immunopathogenesis of murine cerebral malaria: Cues from “young” C57BL/6J and BALB/c mice
    Shweta Rai, Meetali Girdhar, Fouzia Siraj, Sheetal Sharma, Mukesh Kumar, Anju Katyal
    Immunology Letters.2023; 256-257: 9.     CrossRef
  • G6pd-Deficient Mice Are Protected From Experimental Cerebral Malaria and Liver Injury by Suppressing Proinflammatory Response in the Early Stage of Plasmodium berghei Infection
    Haoan Yi, Weiyang Jiang, Fang Yang, Fan Li, Yirong Li, Wenjing Zhu, Qing Li, Syed Hassam Fakhar, Yaming Cao, Lan Luo, Wen Zhang, Yongshu He
    Frontiers in Immunology.2021;[Epub]     CrossRef
  • The role of regulatory T cells during Plasmodium chabaudi chabaudi AS infection in BALB/c mice
    W. Pang, X. Sun, H. Feng, J. Wang, L. Cui, Y. Cao
    Parasite Immunology.2016; 38(7): 439.     CrossRef
  • Phenylhydrazine administration accelerates the development of experimental cerebral malaria
    Xiaotong Zhu, Jun Liu, Yonghui Feng, Wei Pang, Zanmei Qi, Yongjun Jiang, Hong Shang, Yaming Cao
    Experimental Parasitology.2015; 156: 1.     CrossRef
  • Myeloid expression of the AP‐1 transcription factor JUNB modulates outcomes of type 1 and type 2 parasitic infections
    M. F. Fontana, A. Baccarella, D. Kellar, T. K. Oniskey, P. Terinate, S. D. Rosenberg, E. J. Huang, D. R. Herbert, C. C. Kim
    Parasite Immunology.2015; 37(9): 470.     CrossRef
  • Parasite densities modulate susceptibility of mice to cerebral malaria during co-infection with Schistosoma japonicum and Plasmodium berghei
    Mei-lian Wang, Yong-hui Feng, Wei Pang, Zan-mei Qi, Ying Zhang, Ya-jun Guo, En-jie Luo, Ya-ming Cao
    Malaria Journal.2014;[Epub]     CrossRef
  • 9,159 View
  • 89 Download
  • Crossref
Brief Communication
Trichinella spiralis Infection Suppressed Gut Inflammation with CD4+CD25+Foxp3+ T Cell Recruitment
Min Kyoung Cho, Mi Kyung Park, Shin Ae Kang, Seon Hee Choi, Soon Cheol Ahn, Hak Sun Yu
Korean J Parasitol 2012;50(4):385-390.
Published online November 26, 2012
DOI: https://doi.org/10.3347/kjp.2012.50.4.385

In order to know the effect of pre-existing Trichinella spiralis infection on experimentally induced intestinal inflammation and immune responses, we induced colitis in T. spiralis-infected mice and observed the severity of colitis and the levels of Th1, Th2, and regulatory cytokines and recruitment of CD4+CD25+Foxp3+ T (regulatory T; Treg) cells. Female C57BL/6 mice were infected with 250 muscle larvae; after 4 weeks, induction of experimental colitis was performed using 3% dextran sulfate sodium (DSS). During the induction period, we observed severity of colitis, including weight loss and status of stool, and evaluated the disease activity index (DAI). A significantly low DAI and degree of weight loss were observed in infected mice, compared with uninfected mice. In addition, colon length in infected mice was not contracted, compared with uninfected mice. We also observed a significant increase in production of pro-inflammatory cytokines, IL-6 and IFN-γ, in spleen lymphocytes treated with DSS; however, such an increase was not observed in infected mice treated with DSS. Of particular interest, production of regulatory cytokines, IL-10 and transforming growth factor (TGF)-β, in spleen lymphocytes showed a significant increase in mice infected with T. spiralis. A similar result was observed in mesenteric lymph nodes (MLN). Subsets of the population of Treg cells in MLN and spleen showed significant increases in mice infected with T. spiralis. In conclusion, T. spiralis infection can inhibit the DSS-induced colitis in mice by enhancing the regulatory cytokine and Treg cells recruitment.

Citations

Citations to this article as recorded by  Crossref logo
  • Helminths in alternative therapeutics of inflammatory bowel disease
    Himani Pandey, Daryl W. T. Tang, Sunny H. Wong, Devi Lal
    Intestinal Research.2025; 23(1): 8.     CrossRef
  • Cathepsin L of Fasciola hepatica meliorates colitis by altering the gut microbiome and inflammatory macrophages
    Jing-Zhi Gong, Jun-Jie Huang, Ming Pan, Qi-Wang Jin, Yi-Min Fan, Wen-Qian Shi, Si-Yang Huang
    International Journal of Biological Macromolecules.2025; 286: 138270.     CrossRef
  • Improved antiparasitic effects of mebendazole using chitosan and zinc oxide nanocomposites for drug delivery in Trichinella spiralis infected mice during the muscular phase
    Nabila M. Mira, Aya M. Henaish, Eman A. Moussa, Ibrahim B. Helal, Shaimaa M. Kasem
    Acta Tropica.2025; 263: 107565.     CrossRef
  • Therapeutic potentials of Trichinella spiralis in immune disorders: From allergy to autoimmunity
    Minkyoung Cho, Hak Sun Yu
    Parasites, Hosts and Diseases.2025; 63(2): 123.     CrossRef
  • Trichinella-derived protein ameliorates colitis by altering the gut microbiome and improving intestinal barrier function
    Shao Rong Long, Wen Xuan Shang, Hui Ran Zhang, Miao Jiang, Jing Jing Wang, Ruo Dan Liu, Zhong Quan Wang, Jing Cui, Hualei Sun
    International Immunopharmacology.2024; 127: 111320.     CrossRef
  • The gut microbiota is essential for Trichinella spiralis—evoked suppression of colitis
    Hualei Sun, Shao Rong Long, Miao Jiang, Hui Ran Zhang, Jing Jing Wang, Zi Xuan Liao, Jing Cui, Zhong Quan Wang, Subbaraman Babu
    PLOS Neglected Tropical Diseases.2024; 18(11): e0012645.     CrossRef
  • The Underrated Gut Microbiota Helminths, Bacteriophages, Fungi, and Archaea
    Maria Jose Garcia-Bonete, Anandi Rajan, Francesco Suriano, Elena Layunta
    Life.2023; 13(8): 1765.     CrossRef
  • Helminth-derived biomacromolecules as therapeutic agents for treating inflammatory and infectious diseases: What lessons do we get from recent findings?
    Pritha Chakraborty, Vivekanandhan Aravindhan, Suprabhat Mukherjee
    International Journal of Biological Macromolecules.2023; 241: 124649.     CrossRef
  • Potential of human helminth therapy for resolution of inflammatory bowel disease: The future ahead
    Toshio Arai, Fernando Lopes
    Experimental Parasitology.2022; 232: 108189.     CrossRef
  • Trichinella-induced immunomodulation: Another tale of helminth success
    F. Bruschi, D.S. Ashour, A.A. Othman
    Food and Waterborne Parasitology.2022; 27: e00164.     CrossRef
  • Trichinella Infection Ameliorated Vincristine-Induced Neuroinflammation in Mice
    Young Rae Jo, Hwan Tae Park, Hak Sun Yu, Hyun-Hee Kong
    The Korean Journal of Parasitology.2022; 60(4): 247.     CrossRef
  • Immune Protection of a Helminth Protein in the DSS-Induced Colitis Model in Mice
    Shao Rong Long, Ruo Dan Liu, Deepak Vijaya Kumar, Zhong Quan Wang, Chien-Wen Su
    Frontiers in Immunology.2021;[Epub]     CrossRef
  • Trichinella spiralis:inflammation modulator
    Jing Ding, Xiaolei Liu, Xue Bai, Yang Wang, Jian Li, Chun Wang, Shicun Li, Mingyuan Liu, Xuelin Wang
    Journal of Helminthology.2020;[Epub]     CrossRef
  • Infection with Toxocara canis Inhibits the Production of IgE Antibodies to α-Gal in Humans: Towards a Conceptual Framework of the Hygiene Hypothesis?
    Adnan Hodžić, Lourdes Mateos-Hernández, Emilie Fréalle, Patricia Román-Carrasco, Pilar Alberdi, Muriel Pichavant, Veronica Risco-Castillo, Delphine Le Roux, Jérôme Vicogne, Wolfgang Hemmer, Herbert Auer, Ines Swoboda, Georg Duscher, José de la Fuente, Ale
    Vaccines.2020; 8(2): 167.     CrossRef
  • Exposure time determines the protective effect of Trichinella spiralis on experimental colitis
    Wenxiao Zheng, Zhenrong Ma, Xi Sun, Yehong Huang, Bin Lu, Xiaogang Chen, Xiang Xue, Xuexian Yang, Xiang Wu
    Microbial Pathogenesis.2020; 147: 104263.     CrossRef
  • Effect of Trichinella spp. or derived antigens on chemically induced inflammatory bowel disease (IBD) in mouse models: A systematic review and meta-analysis
    Jian Li, Xiaolei Liu, Jing Ding, Bin Tang, Xue Bai, Yang Wang, Shicun Li, Mingyuan Liu, Xuelin Wang
    International Immunopharmacology.2020; 85: 106646.     CrossRef
  • Adoptive transfer of Trichinella spiralis-activated macrophages can ameliorate both Th1- and Th2-activated inflammation in murine models
    Shin Ae Kang, Mi-Kyung Park, Sang Kyun Park, Jun Ho Choi, Da In Lee, So Myong Song, Hak Sun Yu
    Scientific Reports.2019;[Epub]     CrossRef
  • Acute infection with Strongyloides venezuelensis increases intestine production IL-10, reduces Th1/Th2/Th17 induction in colon and attenuates Dextran Sulfate Sodium-induced colitis in BALB/c mice
    Vanessa Fernandes Rodrigues, Márcia Paulliny Soares Bahia, Núbia Rangel Cândido, João Marcelo Peixoto Moreira, Vinicius Gustavo Oliveira, Emília Souza Araújo, Jailza Lima Rodrigues Oliveira, Michelle de Carvalho Rezende, Ary Correa, Deborah Negrão-Corrêa
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  • Regulatory T Cell and Forkhead Box Protein 3 as Modulators of Immune Homeostasis
    Leonn Mendes Soares Pereira, Samara Tatielle Monteiro Gomes, Ricardo Ishak, Antonio Carlos Rosário Vallinoto
    Frontiers in Immunology.2017;[Epub]     CrossRef
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    Parasite Immunology.2017;[Epub]     CrossRef
  • Biodegradable Chitosan Decreases the Immune Response to Trichinella spiralis in Mice
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    Molecules.2017; 22(11): 2008.     CrossRef
  • Activation and Recruitment of Regulatory T Cells via Chemokine Receptor Activation in Trichinella spiralis-Infected Mice
    Jeong-Bin Ahn, Shin Ae Kang, Dong-Hee Kim, Hak Sun Yu
    The Korean Journal of Parasitology.2016; 54(2): 163.     CrossRef
  • Regulatory parameters of the lung immune response during the early phase of experimental trichinellosis
    Guido H. Falduto, Cecilia C. Vila, María P. Saracino, María V. Gentilini, Stella M. Venturiello
    Veterinary Parasitology.2016; 231: 47.     CrossRef
  • Helminth Regulation of Immunity
    Fernando Lopes, Chelsea Matisz, José L. Reyes, Humberto Jijon, Ahmed Al-Darmaki, Gilaad G. Kaplan, Derek M. McKay
    Inflammatory Bowel Diseases.2016; 22(10): 2499.     CrossRef
  • Immunomodulatory potential of particular Trichinella spiralis muscle larvae excretory–secretory components
    J. Cvetkovic, Lj. Sofronic-Milosavljevic, N. Ilic, M. Gnjatovic, I. Nagano, A. Gruden-Movsesijan
    International Journal for Parasitology.2016; 46(13-14): 833.     CrossRef
  • Allergenicity of two Anisakis simplex allergens evaluated in vivo using an experimental mouse model
    Min Kyoung Cho, Mi Kyung Park, Shin Ae Kang, Maria Luisa Caballero, Teresa Perez-Pinar, Rosa Rodriguez-Perez, Mee Sun Ock, Hee Jae Cha, Yeon Chul Hong, Hak Sun Yu
    Experimental Parasitology.2014; 146: 71.     CrossRef
  • Excretory/Secretory Products from Trichinella spiralis Adult Worms Ameliorate DSS-Induced Colitis in Mice
    Xiaodi Yang, Yaping Yang, Yunyun Wang, Bin Zhan, Yuan Gu, Yuli Cheng, Xinping Zhu, Udai P. Singh
    PLoS ONE.2014; 9(5): e96454.     CrossRef
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    Dalia S Ashour
    Expert Review of Clinical Immunology.2013; 9(7): 669.     CrossRef
  • 10,036 View
  • 94 Download
  • Crossref