Effect of Helminth-induced Immunity on Infections with Microbial Pathogens

Overview

Journal Nat Immunol

Date 2013 Oct 23

PMID 24145791

Citations 150

Authors

Padmini Salgame

George S Yap

William C Gause

Affiliations

Soon will be listed here.

Abstract

Helminth infections are ubiquitous worldwide and can trigger potent immune responses that differ from and potentially antagonize host protective responses to microbial pathogens. In this Review we focus on the three main killers in infectious disease-AIDS, tuberculosis and malaria-and critically assesses whether helminths adversely influence host control of these diseases. We also discuss emerging concepts for how M2 macrophages and helminth-modulated dendritic cells can potentially influence the protective immune response to concurrent infections. Finally, we present evidence advocating for more efforts to determine how and to what extent helminths interfere with the successful control of specific concurrent coinfections.

Citing Articles

Intestinal Protozoa, Helminth Infection, and Associated Factors among Tuberculosis Patients and Nontuberculosis Persons in Bobo-Dioulasso City, Burkina Faso.

Djibougou D, Mensah G, Cisse M, Inoussa T, Sawadogo L, Combary A Am J Trop Med Hyg. 2024; 111(6):1265-1272.

PMID: 39317180 PMC: 11619520. DOI: 10.4269/ajtmh.23-0346.

Host-associated helminth diversity and microbiome composition contribute to anti-pathogen defences in tropical frogs impacted by forest fragmentation.

Neely W, Souza K, Martins R, Marshall V, Buttimer S, Brito de Assis A R Soc Open Sci. 2024; 11(6):240530.

PMID: 39100162 PMC: 11296196. DOI: 10.1098/rsos.240530.

Immunological and Haematological Relevance of Helminths and Complex Coinfection among Newly Diagnosed Pulmonary Tuberculosis Patients from Bobo-Dioulasso, Burkina Faso.

Djibougou D, Mensah G, Kabore A, Toe I, Sawadogo L, Lompo P Biomedicines. 2024; 12(7).

PMID: 39062045 PMC: 11274831. DOI: 10.3390/biomedicines12071472.

Animal healer for refractory diseases: Myth or reality?.

Song M, Zhang C, Yang S, Lu J, Sun T, Li H Heliyon. 2024; 10(13):e33056.

PMID: 39027544 PMC: 11255451. DOI: 10.1016/j.heliyon.2024.e33056.

Acute Ascaris infection impairs the effector functions of natural killer cells in single and Salmonella co-infected pigs.

Mugo R, Oser L, Midha A, Adjah J, Kundik A, Laubschat A Sci Rep. 2024; 14(1):14586.

PMID: 38918457 PMC: 11199589. DOI: 10.1038/s41598-024-64497-4.

References

Lawn S, Karanja D, Mwinzia P, Andove J, Colley D, Folks T . The effect of treatment of schistosomiasis on blood plasma HIV-1 RNA concentration in coinfected individuals. AIDS. 2000; 14(16):2437-43. DOI: 10.1097/00002030-200011100-00004. View

Malhotra I, Mungai P, Wamachi A, Kioko J, Ouma J, Kazura J . Helminth- and Bacillus Calmette-Guérin-induced immunity in children sensitized in utero to filariasis and schistosomiasis. J Immunol. 1999; 162(11):6843-8. View

Mosser D, Edwards J . Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008; 8(12):958-69. PMC: 2724991. DOI: 10.1038/nri2448. View

Martinez F, Helming L, Gordon S . Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol. 2008; 27:451-83. DOI: 10.1146/annurev.immunol.021908.132532. View

Moreno Y, Gros P, Tam M, Segura M, Valanparambil R, Geary T . Proteomic analysis of excretory-secretory products of Heligmosomoides polygyrus assessed with next-generation sequencing transcriptomic information. PLoS Negl Trop Dis. 2011; 5(10):e1370. PMC: 3201918. DOI: 10.1371/journal.pntd.0001370. View

Babu S, Bhat S, Kumar N, Anuradha R, Kumaran P, Gopi P . Attenuation of toll-like receptor expression and function in latent tuberculosis by coexistent filarial infection with restoration following antifilarial chemotherapy. PLoS Negl Trop Dis. 2009; 3(7):e489. PMC: 2710006. DOI: 10.1371/journal.pntd.0000489. View

Potian J, Rafi W, Bhatt K, McBride A, Gause W, Salgame P . Preexisting helminth infection induces inhibition of innate pulmonary anti-tuberculosis defense by engaging the IL-4 receptor pathway. J Exp Med. 2011; 208(9):1863-74. PMC: 3171086. DOI: 10.1084/jem.20091473. View

Resende Co T, Hirsch C, Toossi Z, Dietze R, Ribeiro-Rodrigues R . Intestinal helminth co-infection has a negative impact on both anti-Mycobacterium tuberculosis immunity and clinical response to tuberculosis therapy. Clin Exp Immunol. 2006; 147(1):45-52. PMC: 1810442. DOI: 10.1111/j.1365-2249.2006.03247.x. View

Mkhize-Kwitshana Z, Taylor M, Jooste P, Mabaso M, Walzl G . The influence of different helminth infection phenotypes on immune responses against HIV in co-infected adults in South Africa. BMC Infect Dis. 2011; 11:273. PMC: 3213674. DOI: 10.1186/1471-2334-11-273. View

10.

Mikovits J, Meyers A, Ortaldo J, Minty A, Caput D, Ferrara P . IL-4 and IL-13 have overlapping but distinct effects on HIV production in monocytes. J Leukoc Biol. 1994; 56(3):340-6. DOI: 10.1002/jlb.56.3.340. View

11.

Verhagen L, Hermans P, Warris A, de Groot R, Maes M, Villalba J . Helminths and skewed cytokine profiles increase tuberculin skin test positivity in Warao Amerindians. Tuberculosis (Edinb). 2012; 92(6):505-12. DOI: 10.1016/j.tube.2012.07.004. View

12.

Dickson J, Oeggl K, Holden T, Handley L, OConnell T, Preston T . The omnivorous Tyrolean Iceman: colon contents (meat, cereals, pollen, moss and whipworm) and stable isotope analyses. Philos Trans R Soc Lond B Biol Sci. 2001; 355(1404):1843-9. PMC: 1692906. DOI: 10.1098/rstb.2000.0739. View

13.

Chaussabel D, Tolouei Semnani R, McDowell M, Sacks D, Sher A, Nutman T . Unique gene expression profiles of human macrophages and dendritic cells to phylogenetically distinct parasites. Blood. 2003; 102(2):672-81. DOI: 10.1182/blood-2002-10-3232. View

14.

Metenou S, Kovacs M, Dembele B, Coulibaly Y, Klion A, Nutman T . Interferon regulatory factor modulation underlies the bystander suppression of malaria antigen-driven IL-12 and IFN-γ in filaria-malaria co-infection. Eur J Immunol. 2012; 42(3):641-50. PMC: 3430845. DOI: 10.1002/eji.201141991. View

15.

Lustigman S, Prichard R, Gazzinelli A, Grant W, Boatin B, McCarthy J . A research agenda for helminth diseases of humans: the problem of helminthiases. PLoS Negl Trop Dis. 2012; 6(4):e1582. PMC: 3335854. DOI: 10.1371/journal.pntd.0001582. View

16.

Babu S, Kumaraswami V, Nutman T . Alternatively activated and immunoregulatory monocytes in human filarial infections. J Infect Dis. 2009; 199(12):1827-37. PMC: 3440875. DOI: 10.1086/599090. View

17.

Belyaev N, Brown D, Diaz A, Rae A, Jarra W, Thompson J . Induction of an IL7-R(+)c-Kit(hi) myelolymphoid progenitor critically dependent on IFN-gamma signaling during acute malaria. Nat Immunol. 2010; 11(6):477-85. DOI: 10.1038/ni.1869. View

18.

Downs J, Mguta C, Kaatano G, Mitchell K, Bang H, Simplice H . Urogenital schistosomiasis in women of reproductive age in Tanzania's Lake Victoria region. Am J Trop Med Hyg. 2011; 84(3):364-9. PMC: 3042809. DOI: 10.4269/ajtmh.2011.10-0585. View

19.

Gallagher M, Malhotra I, Mungai P, Wamachi A, Kioko J, Ouma J . The effects of maternal helminth and malaria infections on mother-to-child HIV transmission. AIDS. 2005; 19(16):1849-55. DOI: 10.1097/01.aids.0000189846.90946.5d. View

20.

Anthony R, Rutitzky L, Urban Jr J, Stadecker M, Gause W . Protective immune mechanisms in helminth infection. Nat Rev Immunol. 2007; 7(12):975-87. PMC: 2258092. DOI: 10.1038/nri2199. View