viruses
Article
Analysis of the Immune Responses in the Ileum of Gnotobiotic
Pigs Infected with the Recombinant GII.p12_GII.3 Human
Norovirus by mRNA Sequencing
Byung-Joo Park
1
, Hee-Seop Ahn
1
, Sang-Hoon Han
1
, Hyeon-Jeong Go
1
, Dong-Hwi Kim
1
, Changsun Choi
2
,
Soontag Jung
2
, Jinjong Myoung
3
, Joong-Bok Lee
1
, Seung-Yong Park
1
, Chang-Seon Song
1
, Sang-Won Lee
1
,
Hoon-Taek Lee
4
and In-Soo Choi
1,
*
Citation: Park, B.-J.; Ahn, H.-S.; Han,
S.-H.; Go, H.-J.; Kim, D.-H.; Choi, C.;
Jung, S.; Myoung, J.; Lee, J.-B.; Park,
S.-Y.; et al. Analysis of the Immune
Responses in the Ileum of Gnotobiotic
Pigs Infected with the Recombinant
GII.p12_GII.3 Human Norovirus by
mRNA Sequencing. Viruses 2021, 13,
92. https://doi.org/10.3390/
v13010092
Academic Editor: Lennart Svensson
Received: 7 December 2020
Accepted: 8 January 2021
Published: 11 January 2021
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Copyright: © 2021 by the authors. Li-
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This article is an open access article
distributed under the terms and con-
ditions of the Creative Commons At-
tribution (CC BY) license (https://
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4.0/).
1
Department of Infectious Diseases, College of Veterinary Medicine, Konkuk University, Gwangjin-gu,
Seoul 05029, Korea; twilightsd@naver.com (B.-J.P.); heesuob2@naver.com (H.-S.A.);
hansh11@naver.com (S.-H.H.); misilseju@naver.com (H.-J.G.); opeean0@naver.com (D.-H.K.);
virus@konkuk.ac.kr(J.-B.L.); paseyo@konkuk.ac.kr (S.-Y.P.); songcs@konkuk.ac.kr (C.-S.S.);
odssey@konkuk.ac.kr (S.-W.L.)
2
Department of Food and Nutrition, College of Biotechnology and Natural Resources, Chung-Ang University,
Anseong, Gyeonggi 17546, Korea; cchoi@cau.ac.kr (C.C.); amazing2257@gmail.com (S.J.)
3
Korea Zoonosis Research Institute, Chonbuk National University, Jeonju, Jeollabuk-do 54896, Korea;
jinjong.myoung@jbnu.ac.kr
4
Department of Bioscience and Biotechnology, Konkuk University, Seoul 05029, Korea; htl3675@konkuk.ac.kr
* Correspondence: ischoi@konkuk.ac.kr; Tel.: +82-2049-6228
Abstract: Norovirus genogroup II (NoV GII) induces acute gastrointestinal food-borne illness in
humans. Because gnotobiotic pigs can be infected with human norovirus (HuNoV) GII, they are
frequently used to analyze the associated pathogenic mechanisms and immune responses, which
remain poorly understood. Recently, mRNA sequencing analysis (RNA-Seq) has been used to
identify cellular responses to viruses. In this study, we investigated the host immune response
and possible mechanisms involved in virus evasion in the ileum of gnotobiotic pigs infected with
HuNoV by RNA-Seq. HuNoV was detected in the feces, blood, and tissues of the jejunum, ileum,
colon, mesenteric lymph node, and spleen of pigs infected with HuNoV. In analysis of mRNA
sequencing, expression of anti-viral protein genes such as OAS1, MX1, and MX2 were largely
decreased, whereas type I IFN was increased in pigs infected with HuNoV. In addition, expression of
TNF and associated anti-inflammatory cytokine genes such as IL10 was increased in HuNoV-infected
pigs. Expression of genes related to natural killer (NK) cell cytotoxicity and CD8
+
T cell exhaustion
was increased, whereas that of MHC class I genes was decreased. Expression profiles of selected
genes were further confirmed by qRT-PCR and Western blot. These results suggest that infection with
HuNoV induces NK cell-mediated cytotoxicity but suppresses type I IFN- and CD8
+
T cell-mediated
antiviral responses.
Keywords: human norovirus; gnotobiotic pig; immune response; high-throughput mRNA sequencing
1. Introduction
Norovirus (NoV) constitutes an important pathogen of food-borne illnesses in humans.
Human norovirus (HuNoV) is transmitted by the fecal–oral route and generally causes
self-limiting acute gastroenteritis characterized by diarrhea, vomiting, stomach pain, and
fever [1]. HuNoV infection leads to approximately 20 million illnesses, 60,000 hospitaliza-
tions, and 700 deaths annually in the United States [2,3]. NoVs comprise non-enveloped
single-stranded positive-sense RNA viruses belonging to the family Caliciviridae [1]. They
are putatively classified into ten genogroups and further divided into at least 49 geno-
types [4], with NoVs of genogroups I (GI), II (GII), and IV (GIV) representing the main
causative agents of most human infections [5].
Viruses 2021, 13, 92. https://doi.org/10.3390/v13010092 https://www.mdpi.com/journal/viruses