"Every Cell is an Immune Cell; Contributions of Non-hematopoietic Cells to Anti-helminth Immunity"

Overview

Journal Mucosal Immunol

Publisher Elsevier

Specialty Allergy & Immunology

Date 2022 May 10

PMID 35538230

Authors

Juan M Inclan-Rico

Heather L Rossi

DeBroski R Herbert

Affiliations

Soon will be listed here.

Abstract

Helminths are remarkably successful parasites that can invade various mammalian hosts and establish chronic infections that can go unnoticed for years despite causing severe tissue damage. To complete their life cycles, helminths migrate through multiple barrier sites that are densely populated by a complex array of hematopoietic and non-hematopoietic cells. While it is clear that type 2 cytokine responses elicited by immune cells promote worm clearance and tissue healing, the actions of non-hematopoietic cells are increasingly recognized as initiators, effectors and regulators of anti-helminth immunity. This review will highlight the collective actions of specialized epithelial cells, stromal niches, stem, muscle and neuroendocrine cells as well as peripheral neurons in the detection and elimination of helminths at mucosal sites. Studies dissecting the interactions between immune and non-hematopoietic cells will truly provide a better understanding of the mechanisms that ensure homeostasis in the context of helminth infections.

Citing Articles

Application of Single-Cell Genomics to Animal Models of Periodontitis and Peri-Implantitis.

Hasuike A, Easter Q, Clark D, Byrd K J Clin Periodontol. 2024; 52(2):268-279.

PMID: 39695834 PMC: 11743042. DOI: 10.1111/jcpe.14093.

Single-cell and spatially resolved interactomics of tooth-associated keratinocytes in periodontitis.

Easter Q, Fernandes Matuck B, Beldorati Stark G, Worth C, Predeus A, Fremin B Nat Commun. 2024; 15(1):5016.

PMID: 38876998 PMC: 11178863. DOI: 10.1038/s41467-024-49037-y.

Targeting helminths: The expanding world of type 2 immune effector mechanisms.

Maizels R, Gause W J Exp Med. 2023; 220(10).

PMID: 37638887 PMC: 10460967. DOI: 10.1084/jem.20221381.

References

Inclan-Rico J, Siracusa M . First Responders: Innate Immunity to Helminths. Trends Parasitol. 2018; 34(10):861-880. PMC: 6168350. DOI: 10.1016/j.pt.2018.08.007. View

Coakley G, Harris N . The Intestinal Epithelium at the Forefront of Host-Helminth Interactions. Trends Parasitol. 2020; 36(9):761-772. DOI: 10.1016/j.pt.2020.07.002. View

Howitt M, Lavoie S, Michaud M, Blum A, Tran S, Weinstock J . Tuft cells, taste-chemosensory cells, orchestrate parasite type 2 immunity in the gut. Science. 2016; 351(6279):1329-33. PMC: 5528851. DOI: 10.1126/science.aaf1648. View

Taylor B, Zaph C, Troy A, Du Y, Guild K, Comeau M . TSLP regulates intestinal immunity and inflammation in mouse models of helminth infection and colitis. J Exp Med. 2009; 206(3):655-67. PMC: 2699121. DOI: 10.1084/jem.20081499. View

Boothby I, Kinet M, Boda D, Kwan E, Clancy S, Cohen J . Early-life inflammation primes a T helper 2 cell-fibroblast niche in skin. Nature. 2021; 599(7886):667-672. PMC: 8906225. DOI: 10.1038/s41586-021-04044-7. View

Dahlgren M, Jones S, Cautivo K, Dubinin A, Ortiz-Carpena J, Farhat S . Adventitial Stromal Cells Define Group 2 Innate Lymphoid Cell Tissue Niches. Immunity. 2019; 50(3):707-722.e6. PMC: 6553479. DOI: 10.1016/j.immuni.2019.02.002. View

McDermott J, Bartram R, Knight P, Miller H, Garrod D, Grencis R . Mast cells disrupt epithelial barrier function during enteric nematode infection. Proc Natl Acad Sci U S A. 2003; 100(13):7761-6. PMC: 164661. DOI: 10.1073/pnas.1231488100. View

Sharpe C, Thornton D, Grencis R . A sticky end for gastrointestinal helminths; the role of the mucus barrier. Parasite Immunol. 2018; 40(4):e12517. PMC: 5900928. DOI: 10.1111/pim.12517. View

10.

Zhao A, McDermott J, Urban Jr J, Gause W, Madden K, Au Yeung K . Dependence of IL-4, IL-13, and nematode-induced alterations in murine small intestinal smooth muscle contractility on Stat6 and enteric nerves. J Immunol. 2003; 171(2):948-54. DOI: 10.4049/jimmunol.171.2.948. View

11.

Cliffe L, Humphreys N, Lane T, Potten C, Booth C, Grencis R . Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science. 2005; 308(5727):1463-5. DOI: 10.1126/science.1108661. View

12.

Nusse Y, Savage A, Marangoni P, Rosendahl-Huber A, Landman T, de Sauvage F . Parasitic helminths induce fetal-like reversion in the intestinal stem cell niche. Nature. 2018; 559(7712):109-113. PMC: 6042247. DOI: 10.1038/s41586-018-0257-1. View

13.

Sato T, van Es J, Snippert H, Stange D, Vries R, van den Born M . Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature. 2010; 469(7330):415-8. PMC: 3547360. DOI: 10.1038/nature09637. View

14.

Veiga-Fernandes H, Artis D . Neuronal-immune system cross-talk in homeostasis. Science. 2018; 359(6383):1465-1466. DOI: 10.1126/science.aap9598. View

15.

Donnelly S, Stack C, ONeill S, A Sayed A, Williams D, Dalton J . Helminth 2-Cys peroxiredoxin drives Th2 responses through a mechanism involving alternatively activated macrophages. FASEB J. 2008; 22(11):4022-32. PMC: 3980656. DOI: 10.1096/fj.08-106278. View

16.

Gnanasekar M, Velusamy R, He Y, Ramaswamy K . Cloning and characterization of a high mobility group box 1 (HMGB1) homologue protein from Schistosoma mansoni. Mol Biochem Parasitol. 2005; 145(2):137-46. DOI: 10.1016/j.molbiopara.2005.09.013. View

17.

McGinty J, Ting H, Billipp T, Nadjsombati M, Khan D, Barrett N . Tuft-Cell-Derived Leukotrienes Drive Rapid Anti-helminth Immunity in the Small Intestine but Are Dispensable for Anti-protist Immunity. Immunity. 2020; 52(3):528-541.e7. PMC: 7469474. DOI: 10.1016/j.immuni.2020.02.005. View

18.

Oyesola O, Shanahan M, Kanke M, Mooney B, Webb L, Smita S . PGD2 and CRTH2 counteract Type 2 cytokine-elicited intestinal epithelial responses during helminth infection. J Exp Med. 2021; 218(9). PMC: 8294949. DOI: 10.1084/jem.20202178. View

19.

Inaba A, Arinaga A, Tanaka K, Endo T, Hayatsu N, Okazaki Y . Interleukin-4 Promotes Tuft Cell Differentiation and Acetylcholine Production in Intestinal Organoids of Non-Human Primate. Int J Mol Sci. 2021; 22(15). PMC: 8348364. DOI: 10.3390/ijms22157921. View

20.

Cheng X, Voss U, Ekblad E . Tuft cells: Distribution and connections with nerves and endocrine cells in mouse intestine. Exp Cell Res. 2018; 369(1):105-111. DOI: 10.1016/j.yexcr.2018.05.011. View

21.

Krasteva G, Canning B, Hartmann P, Veres T, Papadakis T, Muhlfeld C . Cholinergic chemosensory cells in the trachea regulate breathing. Proc Natl Acad Sci U S A. 2011; 108(23):9478-83. PMC: 3111311. DOI: 10.1073/pnas.1019418108. View