Helminth Infections Decrease Host Susceptibility to Immune-mediated Diseases

Overview

Journal J Immunol

Specialty Allergy & Immunology

Date 2014 Sep 21

PMID 25240019

Citations 47

Authors

Joel V Weinstock

David E Elliott

Affiliations

Soon will be listed here.

Abstract

Helminthic infection has become rare in highly industrialized nations. Concurrent with the decline in helminthic infection has been an increase in the prevalence of inflammatory disease. Removal of helminths from our environment and their powerful effects on host immunity may have contributed to this increase. Several helminth species can abrogate disease in murine models of inflammatory bowel disease, type 1 diabetes, multiple sclerosis, and other conditions. Helminths evoke immune regulatory pathways often involving dendritic cells, regulatory T cells, and macrophages that help to control disease. Cytokines, such as IL-4, IL-10, and TGF-β, have a role. Notable is the helminthic modulatory effect on innate immunity, which impedes development of aberrant adaptive immunity. Investigators are identifying key helminth-derived immune modulatory molecules that may have therapeutic usefulness in the control of inflammatory disease.

Citing Articles

Helminth Lessons in Inflammatory Bowel Diseases (IBD).

Atagozli T, Elliott D, Ince M Biomedicines. 2023; 11(4).

PMID: 37189818 PMC: 10135676. DOI: 10.3390/biomedicines11041200.

COVID-19 morbidity in lower versus higher income populations underscores the need to restore lost biodiversity of eukaryotic symbionts.

Parker W, Patel E, Jirku-Pomajbikova K, Laman J iScience. 2023; 26(3):106167.

PMID: 36785786 PMC: 9908430. DOI: 10.1016/j.isci.2023.106167.

Echinococcus granulosus sensu stricto and antigen B may decrease inflammatory bowel disease through regulation of M1/2 polarization.

Bao J, Qi W, Sun C, Tian M, Jiao H, Guo G Parasit Vectors. 2022; 15(1):391.

PMID: 36289514 PMC: 9608937. DOI: 10.1186/s13071-022-05498-y.

Resistant Potato Starch Alters the Cecal Microbiome and Gene Expression in Mice Fed a Western Diet Based on NHANES Data.

Smith A, Chen C, Cheung L, Ward R, Hintze K, Dawson H Front Nutr. 2022; 9:782667.

PMID: 35392294 PMC: 8983116. DOI: 10.3389/fnut.2022.782667.

Helminth Therapy for Immune-Mediated Inflammatory Diseases: Current and Future Perspectives.

Shi W, Xu N, Wang X, Vallee I, Liu M, Liu X J Inflamm Res. 2022; 15:475-491.

PMID: 35087284 PMC: 8789313. DOI: 10.2147/JIR.S348079.

References

Hunter M, Wang A, Parhar K, Johnston M, van Rooijen N, Beck P . In vitro-derived alternatively activated macrophages reduce colonic inflammation in mice. Gastroenterology. 2010; 138(4):1395-405. DOI: 10.1053/j.gastro.2009.12.041. View

Graepel R, Leung G, Wang A, Villemaire M, Jirik F, Sharkey K . Murine autoimmune arthritis is exaggerated by infection with the rat tapeworm, Hymenolepis diminuta. Int J Parasitol. 2013; 43(7):593-601. DOI: 10.1016/j.ijpara.2013.02.006. View

Saunders K, Raine T, Cooke A, Lawrence C . Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection. Infect Immun. 2006; 75(1):397-407. PMC: 1828378. DOI: 10.1128/IAI.00664-06. View

Wang A, Fernando M, Leung G, Phan V, Smyth D, McKay D . Exacerbation of oxazolone colitis by infection with the helminth Hymenolepis diminuta: involvement of IL-5 and eosinophils. Am J Pathol. 2010; 177(6):2850-9. PMC: 2993289. DOI: 10.2353/ajpath.2010.100537. View

Hubner M, Shi Y, Torrero M, Mueller E, Larson D, Soloviova K . Helminth protection against autoimmune diabetes in nonobese diabetic mice is independent of a type 2 immune shift and requires TGF-β. J Immunol. 2011; 188(2):559-68. PMC: 3253252. DOI: 10.4049/jimmunol.1100335. View

Lund M, OBrien B, Hutchinson A, Robinson M, Simpson A, Dalton J . Secreted proteins from the helminth Fasciola hepatica inhibit the initiation of autoreactive T cell responses and prevent diabetes in the NOD mouse. PLoS One. 2014; 9(1):e86289. PMC: 3897667. DOI: 10.1371/journal.pone.0086289. View

Knight J . Genomic modulators of the immune response. Trends Genet. 2012; 29(2):74-83. PMC: 3605582. DOI: 10.1016/j.tig.2012.10.006. View

Leavenworth J, Tang X, Kim H, Wang X, Cantor H . Amelioration of arthritis through mobilization of peptide-specific CD8+ regulatory T cells. J Clin Invest. 2013; 123(3):1382-9. PMC: 3582146. DOI: 10.1172/JCI66938. View

Sun X, Liu Y, Lv Z, Yang L, Hu S, Zheng H . rSj16, a recombinant protein of Schistosoma japonicum-derived molecule, reduces severity of the complete Freund's adjuvant-induced adjuvant arthritis in rats' model. Parasite Immunol. 2010; 32(11-12):739-48. DOI: 10.1111/j.1365-3024.2010.01240.x. View

10.

Elliott D, Li J, Blum A, Metwali A, Qadir K, Urban Jr J . Exposure to schistosome eggs protects mice from TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol. 2002; 284(3):G385-91. DOI: 10.1152/ajpgi.00049.2002. View

11.

Blum A, Hang L, Setiawan T, Urban Jr J, Stoyanoff K, Leung J . Heligmosomoides polygyrus bakeri induces tolerogenic dendritic cells that block colitis and prevent antigen-specific gut T cell responses. J Immunol. 2012; 189(5):2512-20. PMC: 3424321. DOI: 10.4049/jimmunol.1102892. View

12.

Schnoeller C, Rausch S, Pillai S, Avagyan A, Wittig B, Loddenkemper C . A helminth immunomodulator reduces allergic and inflammatory responses by induction of IL-10-producing macrophages. J Immunol. 2008; 180(6):4265-72. DOI: 10.4049/jimmunol.180.6.4265. View

13.

Cooke A, Tonks P, Jones F, OShea H, Hutchings P, Fulford A . Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol. 1999; 21(4):169-76. DOI: 10.1046/j.1365-3024.1999.00213.x. View

14.

Bishnupuri K, Luo Q, Sainathan S, Kikuchi K, Sureban S, Sabarinathan M . Reg IV regulates normal intestinal and colorectal cancer cell susceptibility to radiation-induced apoptosis. Gastroenterology. 2009; 138(2):616-26, 626.e1-2. PMC: 2819553. DOI: 10.1053/j.gastro.2009.10.050. View

15.

Grainger J, Smith K, Hewitson J, McSorley H, Harcus Y, Filbey K . Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway. J Exp Med. 2010; 207(11):2331-41. PMC: 2964568. DOI: 10.1084/jem.20101074. View

16.

Sancho D, Reis e Sousa C . Sensing of cell death by myeloid C-type lectin receptors. Curr Opin Immunol. 2013; 25(1):46-52. PMC: 4480265. DOI: 10.1016/j.coi.2012.12.007. View

17.

Song X, Shen J, Wen H, Zhong Z, Luo Q, Chu D . Impact of Schistosoma japonicum infection on collagen-induced arthritis in DBA/1 mice: a murine model of human rheumatoid arthritis. PLoS One. 2011; 6(8):e23453. PMC: 3152573. DOI: 10.1371/journal.pone.0023453. View

18.

Fumagalli M, Pozzoli U, Cagliani R, Comi G, Riva S, Clerici M . Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions. J Exp Med. 2009; 206(6):1395-408. PMC: 2715056. DOI: 10.1084/jem.20082779. View

19.

Hartmann W, Haben I, Fleischer B, Breloer M . Pathogenic nematodes suppress humoral responses to third-party antigens in vivo by IL-10-mediated interference with Th cell function. J Immunol. 2011; 187(8):4088-99. DOI: 10.4049/jimmunol.1004136. View

20.

La Flamme A, Ruddenklau K, Backstrom B . Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis. Infect Immun. 2003; 71(9):4996-5004. PMC: 187318. DOI: 10.1128/IAI.71.9.4996-5004.2003. View