Signatures of selection for resistance to  Haemonchus contortus  in sheep and goats

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Abstract

Background

Gastrointestinal nematode infection (GNI) is the most important disease affecting the small ruminant industry in U.S. The environmental conditions in the southern United States are ideal for the survival of the most pathogenic gastrointestinal nematode, Haemonchus contortus. Host genetic variation for resistance to H. contortus allows selective breeding for increased resistance of animals. This selection process increases the prevalence of particular alleles in sheep and goats and creates unique genetic patterns in the genome of these species. The aim of this study was to identify loci with divergent allelic frequencies in a candidate gene panel of 100 genes using two different approaches (frequentist and Bayesian) to estimate Fst outliers in three different breeds of sheep and goats exposed to H. contortus.

Results

Our results for sheep populations showed SNPs under selection in C3AR1, CSF3, SOCS2, NOS2, STAT5B, TGFB2 and IL2RA genes using frequentist and Bayesian approaches. For goats, SNPs in CD1D, ITGA9, IL12A, IL13RA1, CD86 and TGFB2 genes were under selection. Common signatures of selection in both species were observed in NOS2, TGFB2 and TLR4 genes. Directional selection was present in all SNPs evaluated in the present study.

Conclusions

A total of 13 SNPs within 7 genes of our candidate gene panel related to H. contortus exposure were identified under selection in sheep populations. For goats, 11 SNPs within 7 genes were identified under selection. Results from this study support the hypothesis that resistance to H. contortus is likely to be controlled by many loci. Shared signatures of selection related to mechanisms of immune protection against H. contortus infection in sheep and goats could be useful targets in breeding programs aimed to produce resistant animals with low FEC.

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Most cited references 31

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STAT5 is critical in Dendritic Cells for development of TH2- but not TH1-dependent Immunity

Bryan Bell, Masayuki Kitajima, Ryan Larson … (2013)

Dendritic cells (DCs) are a critical player in immune responses, linking innate and adaptive immunity. We show here that DC-specific deletion of the STAT5 was not critical for development, but was required for type-2, but not type-1, allergic responses in both the skin and lung. Loss of STAT5 in DCs led to the inability to respond to thymic stromal lymphopoietin (TSLP). STAT5 was required for TSLP-dependent DC activation, including upregulation of costimulatory molecules and chemokine production. Furthermore, type-2 responses in mice with DC-specific loss of STAT5resembled those seen in TSLPR-deficient mice. These results show that the TSLP- STAT5 axis in DCs is a critical component for the promotion of type-2 immunity at barrier surfaces.

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CD86 and CD80 differentially modulate the suppressive function of human regulatory T cells.

Megan Burke, David M. Sansom, Yong Zheng … (2004)

Regulatory T cells (Treg) are important in maintaining tolerance to self tissues. As both CD28 and CTLA-4 molecules are implicated in the function of Treg, we investigated the ability of their two natural ligands, CD80 and CD86, to influence the Treg-suppressive capacity. During T cell responses to alloantigens expressed on dendritic cells, we observed that Abs against CD86 potently enhanced suppression by CD4(+)CD25(+) Treg. In contrast, blocking CD80 enhanced proliferative responses by impairing Treg suppression. Intriguingly, the relative expression levels of CD80 and CD86 on dendritic cells are modulated during progression from an immature to a mature state, and this correlates with the ability of Treg to suppress responses. Our data show that CD80 and CD86 have opposing functions through CD28 and CTLA-4 on Treg, an observation that has significant implications for manipulation of immune responses and tolerance in vivo.

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Induction of regulatory cells by helminth parasites: exploitation for the treatment of inflammatory diseases.

Conor M Finlay, Kevin P Walsh, Kingston H. G. Mills (2014)

Helminth parasites are highly successful pathogens, chronically infecting a quarter of the world's population, causing significant morbidity but rarely causing death. Protective immunity and expulsion of helminths is mediated by T-helper 2 (Th2) cells, type 2 (M2) macrophages, type 2 innate lymphoid cells, and eosinophils. Failure to mount these type 2 immune responses can result in immunopathology mediated by Th1 or Th17 cells. Helminths have evolved a wide variety of approaches for immune suppression, especially the generation of regulatory T cells and anti-inflammatory cytokines interleukin-10 and transforming growth factor-β. This is a very effective strategy for subverting protective immune responses to prolong their survival in the host but has the bystander effect of modulating immune responses to unrelated antigens. Epidemiological studies in humans have shown that infection with helminth parasites is associated with a low incidence of allergy/asthma and autoimmunity in developing countries. Experimental studies in mice have demonstrated that regulatory immune responses induced by helminth can suppress Th2 and Th1/Th17 responses that mediate allergy and autoimmunity, respectively. This has provided a rational explanation of the 'hygiene hypothesis' and has also led to the exploitation of helminths or their immunomodulatory products in the development of new immunosuppressive therapies for inflammatory diseases in humans. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.

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Author and article information

Contributors

Zaira M. Estrada-Reyes:

ORCID: http://orcid.org/0000-0002-1541-5749

zestrada@ufl.edu

Yoko Tsukahara: yoko3t@gmail.com

Rodrigo R. Amadeu: rramadeu@ufl.edu

Arthur L. Goetsch: arthur.goetsch@langston.edu

Terry A. Gipson: terry.gipson@langston.edu

Tilahun Sahlu: tilahun.sahlu@langston.edu

Richard Puchala: puchala@langston.edu

Zaisen Wang: wzaisen@langston.edu

Steve P. Hart: shart@langston.edu

Raluca G. Mateescu: raluca@ufl.edu

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 15 October 2019

Publication date PMC-release: 15 October 2019

Publication date Collection: 2019

Volume: 20

Electronic Location Identifier: 735

Affiliations

[1 ]ISNI 0000 0004 1936 8091, GRID grid.15276.37, Department of Animal Sciences, , University of Florida, ; Gainesville, FL USA

[2 ]ISNI 0000 0001 0684 3891, GRID grid.258945.7, American Institute for Goat Research, , Langston University, ; Langston, OK USA

[3 ]ISNI 0000 0004 1936 8091, GRID grid.15276.37, Horticultural Sciences Department, , University of Florida, ; Gainesville, FL USA

Author information

Zaira M. Estrada-Reyes http://orcid.org/0000-0002-1541-5749

Article

Publisher ID: 6150

DOI: 10.1186/s12864-019-6150-y

PMC ID: 6792194

PubMed ID: 31615414

SO-VID: 1789aefa-7a4d-4322-b1c9-5505de4d085f

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 2 April 2019

Date accepted : 29 September 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100005825, National Institute of Food and Agriculture;

Award ID: 003673

Award ID: Project OKLXSAHLU12

Award Recipient : Zaira M. Estrada-Reyes

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: fst,haemonchus contortus,signatures of selection,snp,sheep,goats,immune response

Data availability:

ScienceOpen disciplines: Genetics

Keywords: fst, haemonchus contortus, signatures of selection, snp, sheep, goats, immune response

Signatures of selection for resistance to Haemonchus contortus in sheep and goats

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European Journal of Microbiology and Immunology

Most cited references 31

STAT5 is critical in Dendritic Cells for development of TH2- but not TH1-dependent Immunity

CD86 and CD80 differentially modulate the suppressive function of human regulatory T cells.

Induction of regulatory cells by helminth parasites: exploitation for the treatment of inflammatory diseases.

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