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Defining the caprine γδ T cell WC1 multigenic array and evaluation of its expressed sequences and gene structure conservation among goat breeds and relative to cattle

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Abstract

Workshop cluster 1 (WC1) molecules are part of the scavenger receptor cysteine-rich (SRCR) superfamily and act as hybrid co-receptors for the γδ T cell receptor and as pattern recognition receptors for binding pathogens. These members of the CD163 gene family are expressed on γδ T cells in the blood of ruminants. While the presence of WC1+ γδ T cells in the blood of goats has been demonstrated using monoclonal antibodies, there was no information available about the goat WC1 gene family. The caprine WC1 multigenic array was characterized here for number, structure and expression of genes, and similarity to WC1 genes of cattle and among goat breeds. We found sequence for 17 complete WC1 genes and evidence for up to 30 SRCR a1 or d1 domains which represent distinct signature domains for individual genes. This suggests substantially more WC1 genes than in cattle. Moreover, goats had seven different WC1 gene structures of which 4 are unique to goats. Caprine WC1 genes also had multiple transcript splice variants of their intracytoplasmic domains that eliminated tyrosines shown previously to be important for signal transduction. The most distal WC1 SRCR a1 domains were highly conserved among goat breeds, but fewer were conserved between goats and cattle. Since goats have a greater number of WC1 genes and unique WC1 gene structures relative to cattle, goat WC1 molecules may have expanded functions. This finding may impact research on next-generation vaccines designed to stimulate γδ T cells.

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Abbreviations

ARS1:

Agricultural research service 1

BR:

Boer

ICD:

Intracytoplasmic domains

ID:

Interdomain

IFNγ:

Interferon-γ

IL:

Interleukin

MHC:

Major histocompatibility complex

PBMC:

Peripheral blood mononuclear cells

PCR:

Polymerase chain reaction

PRR:

Pattern recognition receptor

SC:

San Clemente

SRCR:

Scavenger receptor cysteine-rich

TCR:

T cell receptor

WC1:

Workshop cluster 1

YN:

Yunnan

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Acknowledgements

We thank Drs. John Hammond and John Schwartz with advice and assistance for annotation and Ms. Alice Newth and UMass Amherst Veterinary and Animal Sciences undergraduate students working at the farm for their help in blood collection. The USDA is an equal opportunity provider and employer.

Funding

This work was funded by the U.S. Department of Agriculture and National Institute for Food and Agriculture’s Agriculture and Food Research initiative (AFRI-NIFA-USDA) grant no. 2015–06970 and 2016–67015-24913 and the Center for Agriculture, Food, and the Environment and the Department of Veterinary and Animal Sciences at University of Massachusetts Amherst, under project #MAS00572. DB was supported by USDA appropriated project 5090–31000-026–00-D. TS was supported by USDA appropriated project 3040–31000-100–00-D.

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Authors and Affiliations

  1. Department of Veterinary and Animal Sciences, University of Massachusetts, Amherst, MA, 01003, USA

    Alehegne W. Yirsaw, Alexandra Gillespie, Fengqiu Zhang, Maria Amir, Haeree Park, Janice C. Telfer & Cynthia L. Baldwin

  2. United States Department of Agriculture, Agricultural Research Service, United States Meat Animal Research Center, Clay Center, NE, 68933, USA

    Timothy P. L. Smith

  3. United States Department of Agriculture, Agricultural Research Service, United States Dairy Forage Research Center, Madison, WI, 53706, USA

    Derek M. Bickhart

  4. College of Information and Computer Sciences, University of Massachusetts, Amherst, MA, 01003, USA

    Karthick P. Gunasekaran

  5. Program in Molecular and Cellular Biology, University of Massachusetts, Amherst, MA, 01003, USA

    Janice C. Telfer & Cynthia L. Baldwin

  6. College of Veterinary Medicine, University of Minnesota, 1365 Gortner Ave, St Paul, MN, 55108, USA

    Haeree Park

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  1. Alehegne W. Yirsaw
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Contributions

AY conducted the annotation studies, obtained full-length WC1 cDNA sequences, and identified the splice variants; AG gave technical oversight throughout and conducted phylogenetic analyses; FZ conducted PacBio sequencing of cDNA; TS and DB sequenced and assembled the ARS1 genome; KG developed the computer annotation capabilities; MA and HP obtained full-length cDNA sequences; JT and CB were the co-principal investigators who conceived of the study, obtained funding, and oversaw the analysis of the work and writing of the manuscript. All authors have read and approved the manuscript.

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Correspondence to Cynthia L. Baldwin.

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251_2022_1254_MOESM1_ESM.pdf

Supplementary file1 (PDF 1395 KB) Fig. S1. Goat WC1 gene number estimation using Venn diagram summary. All of the unique a1 domains and the single d1 domain sequences were grouped as found in each breed with corresponding names in the compartments within this figure. CHIR2.0 assembly of Yunnan (YN), ARS1 assembly of San Clemente (SC) and Boer (BR) goats. The relationships of a1 domains among goat breeds was made using sequence alignment and phylogenetic trees as shown in Fig. 5. Fig. S2. Alignment of the deduced amino acid sequences of the complete WC1 cDNA sequences. (A) Agarose gels of the amplicons obtained by RT-PCR for WC1 transcripts. Significant bands are indicated with an asterisk on the left-hand gel: lane 1, size markers; lane 2, ICD type I/II, 5800 bp (faint band) and 4400 bp; lane 4, ICD type III, 2900 bp and 2200 bp; right-hand gel: lane 1, size markers; lane 2, ICD type I/II, 4400 bp and 2700 bp. Full-length deduced amino acid sequences of the annotated WC1 genes from the ARS1 San Clemente assembly and WC1 transcript sequences from Boer goat DNA were aligned. Identities are indicated by dots (.), gaps resulting from the alignment are indicated by tildes (~), gaps resulting from lack of cDNA are indicated by dashes (-) and the N nucleotide sequences show as “x” when converted to deduced amino acids. Sequences shown are (B) SCgoatWC1-1-GA vs BRgoatWC1-1-cDNA sequences, (C) SCgoatWC1-9-GA vs BRgoatWC1-9-cDNA sequences, (D) SCgoatWC1-23-GA vs BRgoatWC1-23-cDNA sequences, (E) SCgoatWC1-22-GA vs BRgoatWC1-22-cDNA sequences, (F) SCgoatWC1-13-GA vs BRgoatWC1-13-cDNA sequences, (G) SCgoatWC1-4-GA vs BRgoatWC1-4-cDNA sequences, (H) SCgoatWC1-15-GA vs BRgoatWC1-15-cDNA sequences, and (I) SCgoatWC1-2-GA vs BRgoatWC1-2-cDNA sequences.

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Yirsaw, A.W., Gillespie, A., Zhang, F. et al. Defining the caprine γδ T cell WC1 multigenic array and evaluation of its expressed sequences and gene structure conservation among goat breeds and relative to cattle. Immunogenetics 74, 347–365 (2022). https://doi.org/10.1007/s00251-022-01254-9

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