HLA Class I Expression Is Associated with DNA Damage and Immune Cell Infiltration into Dysplastic and Neoplastic Lesions in Ulcerative Colitis

Human leukocyte antigen class I (HLA-I) is considered a genetic pathogen for ulcerative colitis (UC). This study aimed to investigate the significance of DNA damage and HLA-I expression in infiltrating immune cells and immune checkpoint protein PD-L1 expression in dysplasia/colitic cancer (CC) and s...

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Published inInternational journal of molecular sciences Vol. 24; no. 17; p. 13648
Main Authors Okami, Haruka, Ozawa, Naoya, Sohda, Makoto, Yokobori, Takehiko, Osone, Katsuya, Erkhem-Ochir, Bilguun, Dorjkhorloo, Gendensuren, Shiraishi, Takuya, Okada, Takuhisa, Sano, Akihiko, Sakai, Makoto, Miyazaki, Tatsuya, Ogawa, Hiroomi, Yao, Takashi, Oike, Takahiro, Sato, Hiro, Shirabe, Ken, Shibata, Atsushi, Saeki, Hiroshi
Format Journal Article
LanguageEnglish
Published Basel MDPI AG 01.09.2023
MDPI
Subjects
Anti-inflammatory agents
Antigen presentation
Antimitotic agents
Antineoplastic agents
Cancer
Cancer therapies
Cells
colitic cancer
Colon
Colorectal cancer
Cytotoxicity
DNA
DNA damage
Genetic aspects
Genetic research
Histocompatibility antigens
HLA histocompatibility antigens
human leukocyte antigen
immune cells
Immunohistochemistry
Inflammation
Inflammatory bowel disease
Lymphocytes
Medical colleges
Medical research
Proteins
T cells
Tumors
Ulcerative colitis
Japan
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Abstract Human leukocyte antigen class I (HLA-I) is considered a genetic pathogen for ulcerative colitis (UC). This study aimed to investigate the significance of DNA damage and HLA-I expression in infiltrating immune cells and immune checkpoint protein PD-L1 expression in dysplasia/colitic cancer (CC) and sporadic colorectal cancer (SCRC). We performed immunohistochemical staining for HLA-I, PD-L1, γH2AX (DNA damage marker), and immune cell markers such as CD8, FOXP3, CD68, and CD163 (in surgically resected specimens from 17 SCRC patients with 12 adjacent normal mucosa (NM) and 9 UC patients with 18 dysplasia/CC tumors. The ratio of membrane HLA-I-positive epithelial cells in UC and dysplasia/CC tissues was significantly higher than that in NM and SCRC. High HLA-I expression in dysplasia/CC was associated with high positivity of γH2AX and PD-L1 expression compared to SCRC. The infiltration of CD8-positive T cells and CD68-positive macrophages in HLA-I-high dysplasia/CC was significantly higher than in UC and SCRC. Dysplasia/CC specimens with DNA damage exhibited high levels of HLA-I-positive epithelial cells with high CD8- and CD68-positive immune cell infiltration compared to UC and SCRC specimens. Targeting DNA damage in UC may regulate immune cell infiltration, immune checkpoint proteins, and carcinogenesis by modulating DNA damage-induced HLA-I antigen presentation.
AbstractList Human leukocyte antigen class I (HLA-I) is considered a genetic pathogen for ulcerative colitis (UC). This study aimed to investigate the significance of DNA damage and HLA-I expression in infiltrating immune cells and immune checkpoint protein PD-L1 expression in dysplasia/colitic cancer (CC) and sporadic colorectal cancer (SCRC). We performed immunohistochemical staining for HLA-I, PD-L1, γH2AX (DNA damage marker), and immune cell markers such as CD8, FOXP3, CD68, and CD163 (in surgically resected specimens from 17 SCRC patients with 12 adjacent normal mucosa (NM) and 9 UC patients with 18 dysplasia/CC tumors. The ratio of membrane HLA-I-positive epithelial cells in UC and dysplasia/CC tissues was significantly higher than that in NM and SCRC. High HLA-I expression in dysplasia/CC was associated with high positivity of γH2AX and PD-L1 expression compared to SCRC. The infiltration of CD8-positive T cells and CD68-positive macrophages in HLA-I-high dysplasia/CC was significantly higher than in UC and SCRC. Dysplasia/CC specimens with DNA damage exhibited high levels of HLA-I-positive epithelial cells with high CD8- and CD68-positive immune cell infiltration compared to UC and SCRC specimens. Targeting DNA damage in UC may regulate immune cell infiltration, immune checkpoint proteins, and carcinogenesis by modulating DNA damage-induced HLA-I antigen presentation.
Audience Academic
Author Miyazaki, Tatsuya
Sohda, Makoto
Yokobori, Takehiko
Erkhem-Ochir, Bilguun
Okada, Takuhisa
Dorjkhorloo, Gendensuren
Shibata, Atsushi
Saeki, Hiroshi
Ogawa, Hiroomi
Sato, Hiro
Okami, Haruka
Sano, Akihiko
Shiraishi, Takuya
Yao, Takashi
Shirabe, Ken
Ozawa, Naoya
Sakai, Makoto
Oike, Takahiro
Osone, Katsuya
AuthorAffiliation 5 Department of Radiation Oncology, Graduate School of Medicine, Gunma University, Maebashi 371-8510, Japan; oiketakahiro@gunma-u.ac.jp (T.O.); hiro.sato@gunma-u.ac.jp (H.S.)
6 Division of Molecular Oncological Pharmacy, Faculty of Pharmacy, Keio University, Minato-ku 108-8345, Japan; shibata.at@keio.jp
1 Department of General Surgical Science, Graduate School of Medicine, Gunma University, Maebashi 371-8510, Japan; m2220010@gunma-u.ac.jp (H.O.); a050055asahi@gmail.com (N.O.); okatsuya@gunma-u.ac.jp (K.O.); m2220603@gunma-u.ac.jp (G.D.); whityshiro@gmail.com (T.S.); t.okd@gunma-u.ac.jp (T.O.); ak_sano@outlook.jp (A.S.); maksakai@gunma-u.ac.jp (M.S.); hiroomio@gunma-u.ac.jp (H.O.); kshirabe@gunma-u.ac.jp (K.S.); h-saeki@gunma-u.ac.jp (H.S.)
2 Division of Integrated Oncology Research, Gunma University, Initiative for Advanced Research (GIAR), Maebashi 371-8511, Japan; bilguun.e@gunma-u.ac.jp
3 Department of Surgery Japanese Red Cross Maebashi Hospital, Maebashi 371-0811, Japan; tatsuyamiyaza
AuthorAffiliation_xml – name: 2 Division of Integrated Oncology Research, Gunma University, Initiative for Advanced Research (GIAR), Maebashi 371-8511, Japan; bilguun.e@gunma-u.ac.jp
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– name: 6 Division of Molecular Oncological Pharmacy, Faculty of Pharmacy, Keio University, Minato-ku 108-8345, Japan; shibata.at@keio.jp
– name: 1 Department of General Surgical Science, Graduate School of Medicine, Gunma University, Maebashi 371-8510, Japan; m2220010@gunma-u.ac.jp (H.O.); a050055asahi@gmail.com (N.O.); okatsuya@gunma-u.ac.jp (K.O.); m2220603@gunma-u.ac.jp (G.D.); whityshiro@gmail.com (T.S.); t.okd@gunma-u.ac.jp (T.O.); ak_sano@outlook.jp (A.S.); maksakai@gunma-u.ac.jp (M.S.); hiroomio@gunma-u.ac.jp (H.O.); kshirabe@gunma-u.ac.jp (K.S.); h-saeki@gunma-u.ac.jp (H.S.)
– name: 3 Department of Surgery Japanese Red Cross Maebashi Hospital, Maebashi 371-0811, Japan; tatsuyamiyazaki4126@gmail.com
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Snippet Human leukocyte antigen class I (HLA-I) is considered a genetic pathogen for ulcerative colitis (UC). This study aimed to investigate the significance of DNA...
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StartPage 13648
SubjectTerms Anti-inflammatory agents
Antigen presentation
Antimitotic agents
Antineoplastic agents
Cancer
Cancer therapies
Cells
colitic cancer
Colon
Colorectal cancer
Cytotoxicity
DNA
DNA damage
Genetic aspects
Genetic research
Histocompatibility antigens
HLA histocompatibility antigens
human leukocyte antigen
immune cells
Immunohistochemistry
Inflammation
Inflammatory bowel disease
Lymphocytes
Medical colleges
Medical research
Proteins
T cells
Tumors
Ulcerative colitis
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Title HLA Class I Expression Is Associated with DNA Damage and Immune Cell Infiltration into Dysplastic and Neoplastic Lesions in Ulcerative Colitis
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https://search.proquest.com/docview/2863294028
https://pubmed.ncbi.nlm.nih.gov/PMC10487850
https://doaj.org/article/93c8d5ffedd545f096334e9c74868a24
Volume 24
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