viruses
Article
Characterization of Adaptive-like γδ T Cells in Ugandan
Infants during Primary Cytomegalovirus Infection
Jessica Tuengel
1
, Sanya Ranchal
1
, Alexandra Maslova
2
, Gurpreet Aulakh
1
, Maria Papadopoulou
3,4,5
,
Sibyl Drissler
6
, Bing Cai
1
, Cetare Mohsenzadeh-Green
1
, Hugo Soudeyns
7,8
, Sara Mostafavi
1,2
,
Peter van den Elzen
1
, David Vermijlen
3,4,5
, Laura Cook
1,9
and Soren Gantt
7,8,
*
Citation: Tuengel, J.; Ranchal, S.;
Maslova, A.; Aulakh, G.;
Papadopoulou, M.; Drissler, S.; Cai,
B.; Mohsenzadeh-Green, C.;
Soudeyns, H.; Mostafavi, S.; et al.
Characterization of Adaptive-like γδ
T Cells in Ugandan Infants during
Primary Cytomegalovirus Infection.
Viruses 2021, 13, 1987. https://
doi.org/10.3390/v13101987
Academic Editor: Graciela Andrei
Received: 10 July 2021
Accepted: 27 September 2021
Published: 3 October 2021
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Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
1
BC Children’s Hospital Research Institute, University of British Columbia, Vancouver, BC V5Z 4H4, Canada;
jessicaharli@gmail.com (J.T.); sranchal@student.ubc.ca (S.R.); gsaulakh@alumni.ubc.ca (G.A.);
caibing@bcchr.ubc.ca (B.C.); cetarehmg@gmail.com (C.M.-G.); saram@stat.ubc.ca (S.M.);
pvde@mail.ubc.ca (P.v.d.E.); l.cook@unimelb.edu.au (L.C.)
2
Department of Bioinformatics, University of British Columbia, Vancouver, BC V5T 4S6, Canada;
sasha113@gmail.com
3
Department of Pharmacotherapy and Pharmaceutics, Université Libre de Bruxelles (ULB),
6041 Gosselies, Belgium; mpapadop@ulb.ac.be (M.P.); dvermijl@ulb.ac.be (D.V.)
4
Institute for Medical Immunology, Université Libre de Bruxelles (ULB), 1050 Brussels, Belgium
5
ULB Center for Research in Immunology, Université Libre de Bruxelles (ULB), 1050 Brussels, Belgium
6
Terry Fox Laboratory, British Columbia Cancer Agency, Vancouver, BC V5Z 1L3, Canada; sdrissler@bccrc.ca
7
Department of Microbiology, Infectiology and Immunology, Université de Montréal, Montréal, QC H3C 3J7,
Canada; hugo.soudeyns@umontreal.ca
8
CHU Sainte-Justine Research Centre, Montréal, QC H3T 1C5, Canada
9
Department of Microbiology and Immunology, The Peter Doherty Institute for Infection and Immunity,
University of Melbourne, Melbourne, VIC 3000, Australia
* Correspondence: soren.gantt@umontreal.ca
Abstract: Gamma-delta (γδ) T cells are unconventional T cells that help control cytomegalovirus
(CMV) infection in adults. γδ T cells develop early in gestation, and a fetal public γδ T cell receptor
(TCR) clonotype is detected in congenital CMV infections. However, age-dependent γδ T cell
responses to primary CMV infection are not well-understood. Flow cytometry and TCR sequencing
was used to comprehensively characterize γδ T cell responses to CMV infection in a cohort of
32 infants followed prospectively from birth. Peripheral blood γδ T cell frequencies increased during
infancy, and were higher among CMV-infected infants relative to uninfected. Clustering analyses
revealed associations between CMV infection and activation marker expression on adaptive-like Vδ1
and Vδ3, but not innate-like Vγ9Vδ2 γδ T cell subsets. Frequencies of NKG2C
+
CD57
+
γδ T cells were
temporally associated with the quantity of CMV shed in saliva by infants with primary infection.
The public γδ TCR clonotype was only detected in CMV-infected infants <120 days old and at lower
frequencies than previously described in fetal infections. Our findings support the notion that CMV
infection drives age-dependent expansions of specific γδ T cell populations, and provide insight for
novel strategies to prevent CMV transmission and disease.
Keywords: CMV; gamma delta T cell; gammadelta; Vδ1; Vδ3; Vγ8; Vγ9
neg
Vδ2; cCMV; NKG2C;
immune ontogeny
1. Introduction
Cytomegalovirus (CMV) infects most of the world’s population, beginning in early
childhood [1]. Postnatal CMV infection is frequently asymptomatic and rarely causes
disease in immunocompetent individuals; however, population-based studies have indi-
cated an association between CMV infection and all-cause mortality [2]. Congenital CMV
infection (cCMV) is a major cause of childhood deafness and other neurodevelopmental
disabilities [3]. Immunological changes during early life likely play an important role in the
Viruses 2021, 13, 1987. https://doi.org/10.3390/v13101987 https://www.mdpi.com/journal/viruses