Effects of High-Mobility Group Box-1 on Mucosal Immunity and Epithelial Differentiation in Colitic Carcinoma
Abnormalities in mucosal immunity are involved in the onset and progression of ulcerative colitis (UC), resulting in a high incidence of colorectal cancer (CRC). While high-mobility group box-1 (HMGB1) is overexpressed during colorectal carcinogenesis, its role in UC-related carcinogenesis remains u...
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| Veröffentlicht in: | International journal of molecular sciences 2024-07, Vol.25 (13), p.6846 |
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| creator | Sasaki, Takamitsu Fujiwara-Tani, Rina Luo, Yi Ogata, Ruiko Sasaki, Rika Ikemoto, Ayaka Nishiguchi, Yukiko Nakashima, Chie Kishi, Shingo Fujii, Kiyomu Ohmori, Hitoshi Oue, Naohide Kuniyasu, Hiroki |
| description | Abnormalities in mucosal immunity are involved in the onset and progression of ulcerative colitis (UC), resulting in a high incidence of colorectal cancer (CRC). While high-mobility group box-1 (HMGB1) is overexpressed during colorectal carcinogenesis, its role in UC-related carcinogenesis remains unclear. In the present study, we investigated the role of HMGB1 in UC-related carcinogenesis and sporadic CRC. Both the azoxymethane colon carcinogenesis and dextran sulfate sodium colitis carcinogenesis models demonstrated temporal increases in mucosal HMGB1 levels. Activated CD8+ cells initially increased and then decreased, whereas exhausted CD8+ cells increased. Additionally, we observed increased regulatory CD8+ cells, decreased naïve CD8+ cells, and decreased mucosal epithelial differentiation. In the in vitro study, HMGB1 induced energy reprogramming from oxidative phosphorylation to glycolysis in CD8+ cells and intestinal epithelial cells. Furthermore, in UC dysplasia, UC-related CRC, and hyperplastic mucosa surrounding human sporadic CRC, we found increased mucosal HMGB1, decreased activated CD8+ cells, and suppressed mucosal epithelial differentiation. However, we observed increased activated CD8+ cells in active UC mucosa. These findings indicate that HMGB1 plays an important role in modulating mucosal immunity and epithelial dedifferentiation in both UC-related carcinogenesis and sporadic CRC. |
| doi_str_mv | 10.3390/ijms25136846 |
| format | Article |
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While high-mobility group box-1 (HMGB1) is overexpressed during colorectal carcinogenesis, its role in UC-related carcinogenesis remains unclear. In the present study, we investigated the role of HMGB1 in UC-related carcinogenesis and sporadic CRC. Both the azoxymethane colon carcinogenesis and dextran sulfate sodium colitis carcinogenesis models demonstrated temporal increases in mucosal HMGB1 levels. Activated CD8+ cells initially increased and then decreased, whereas exhausted CD8+ cells increased. Additionally, we observed increased regulatory CD8+ cells, decreased naïve CD8+ cells, and decreased mucosal epithelial differentiation. In the in vitro study, HMGB1 induced energy reprogramming from oxidative phosphorylation to glycolysis in CD8+ cells and intestinal epithelial cells. Furthermore, in UC dysplasia, UC-related CRC, and hyperplastic mucosa surrounding human sporadic CRC, we found increased mucosal HMGB1, decreased activated CD8+ cells, and suppressed mucosal epithelial differentiation. However, we observed increased activated CD8+ cells in active UC mucosa. These findings indicate that HMGB1 plays an important role in modulating mucosal immunity and epithelial dedifferentiation in both UC-related carcinogenesis and sporadic CRC.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms25136846</identifier><identifier>PMID: 38999957</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Analysis ; Animals ; Antibodies ; Cancer ; Carcinogenesis - immunology ; Carcinogenesis - metabolism ; Carcinogenesis - pathology ; CD8-Positive T-Lymphocytes - immunology ; CD8-Positive T-Lymphocytes - metabolism ; Cell Differentiation ; Cell growth ; Chromosomal proteins ; Colitis, Ulcerative - chemically induced ; Colitis, Ulcerative - immunology ; Colitis, Ulcerative - metabolism ; Colitis, Ulcerative - pathology ; Colon ; Colon cancer ; Colorectal cancer ; Colorectal Neoplasms - immunology ; Colorectal Neoplasms - metabolism ; Colorectal Neoplasms - pathology ; Development and progression ; Dextran ; Disease ; Epithelial Cells - metabolism ; Epithelial Cells - pathology ; Ethylenediaminetetraacetic acid ; HMGB1 Protein - metabolism ; Humans ; Immunity, Mucosal ; Inflammatory bowel disease ; Intestinal Mucosa - immunology ; Intestinal Mucosa - metabolism ; Intestinal Mucosa - pathology ; Lymphocytes ; Male ; Mice ; Mice, Inbred C57BL ; Peptides ; Phosphatase ; Proteins ; Respiration ; Sulfates ; Ulcerative colitis</subject><ispartof>International journal of molecular sciences, 2024-07, Vol.25 (13), p.6846</ispartof><rights>COPYRIGHT 2024 MDPI AG</rights><rights>2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c311t-ec64871ba97bfffe1667988e0cf18d70ed6eb60dd7fc6d6556cd69728d16bc233</cites><orcidid>0000-0003-2298-8825</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38999957$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sasaki, Takamitsu</creatorcontrib><creatorcontrib>Fujiwara-Tani, Rina</creatorcontrib><creatorcontrib>Luo, Yi</creatorcontrib><creatorcontrib>Ogata, Ruiko</creatorcontrib><creatorcontrib>Sasaki, Rika</creatorcontrib><creatorcontrib>Ikemoto, Ayaka</creatorcontrib><creatorcontrib>Nishiguchi, Yukiko</creatorcontrib><creatorcontrib>Nakashima, Chie</creatorcontrib><creatorcontrib>Kishi, Shingo</creatorcontrib><creatorcontrib>Fujii, Kiyomu</creatorcontrib><creatorcontrib>Ohmori, Hitoshi</creatorcontrib><creatorcontrib>Oue, Naohide</creatorcontrib><creatorcontrib>Kuniyasu, Hiroki</creatorcontrib><title>Effects of High-Mobility Group Box-1 on Mucosal Immunity and Epithelial Differentiation in Colitic Carcinoma</title><title>International journal of molecular sciences</title><addtitle>Int J Mol Sci</addtitle><description>Abnormalities in mucosal immunity are involved in the onset and progression of ulcerative colitis (UC), resulting in a high incidence of colorectal cancer (CRC). While high-mobility group box-1 (HMGB1) is overexpressed during colorectal carcinogenesis, its role in UC-related carcinogenesis remains unclear. In the present study, we investigated the role of HMGB1 in UC-related carcinogenesis and sporadic CRC. Both the azoxymethane colon carcinogenesis and dextran sulfate sodium colitis carcinogenesis models demonstrated temporal increases in mucosal HMGB1 levels. Activated CD8+ cells initially increased and then decreased, whereas exhausted CD8+ cells increased. Additionally, we observed increased regulatory CD8+ cells, decreased naïve CD8+ cells, and decreased mucosal epithelial differentiation. In the in vitro study, HMGB1 induced energy reprogramming from oxidative phosphorylation to glycolysis in CD8+ cells and intestinal epithelial cells. Furthermore, in UC dysplasia, UC-related CRC, and hyperplastic mucosa surrounding human sporadic CRC, we found increased mucosal HMGB1, decreased activated CD8+ cells, and suppressed mucosal epithelial differentiation. However, we observed increased activated CD8+ cells in active UC mucosa. These findings indicate that HMGB1 plays an important role in modulating mucosal immunity and epithelial dedifferentiation in both UC-related carcinogenesis and sporadic CRC.</description><subject>Analysis</subject><subject>Animals</subject><subject>Antibodies</subject><subject>Cancer</subject><subject>Carcinogenesis - immunology</subject><subject>Carcinogenesis - metabolism</subject><subject>Carcinogenesis - pathology</subject><subject>CD8-Positive T-Lymphocytes - immunology</subject><subject>CD8-Positive T-Lymphocytes - metabolism</subject><subject>Cell Differentiation</subject><subject>Cell growth</subject><subject>Chromosomal proteins</subject><subject>Colitis, Ulcerative - chemically induced</subject><subject>Colitis, Ulcerative - immunology</subject><subject>Colitis, Ulcerative - metabolism</subject><subject>Colitis, Ulcerative - pathology</subject><subject>Colon</subject><subject>Colon cancer</subject><subject>Colorectal cancer</subject><subject>Colorectal Neoplasms - immunology</subject><subject>Colorectal Neoplasms - 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Academic</collection><jtitle>International journal of molecular sciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sasaki, Takamitsu</au><au>Fujiwara-Tani, Rina</au><au>Luo, Yi</au><au>Ogata, Ruiko</au><au>Sasaki, Rika</au><au>Ikemoto, Ayaka</au><au>Nishiguchi, Yukiko</au><au>Nakashima, Chie</au><au>Kishi, Shingo</au><au>Fujii, Kiyomu</au><au>Ohmori, Hitoshi</au><au>Oue, Naohide</au><au>Kuniyasu, Hiroki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Effects of High-Mobility Group Box-1 on Mucosal Immunity and Epithelial Differentiation in Colitic Carcinoma</atitle><jtitle>International journal of molecular sciences</jtitle><addtitle>Int J Mol Sci</addtitle><date>2024-07-01</date><risdate>2024</risdate><volume>25</volume><issue>13</issue><spage>6846</spage><pages>6846-</pages><issn>1422-0067</issn><issn>1661-6596</issn><eissn>1422-0067</eissn><abstract>Abnormalities in mucosal immunity are involved in the onset and progression of ulcerative colitis (UC), resulting in a high incidence of colorectal cancer (CRC). While high-mobility group box-1 (HMGB1) is overexpressed during colorectal carcinogenesis, its role in UC-related carcinogenesis remains unclear. In the present study, we investigated the role of HMGB1 in UC-related carcinogenesis and sporadic CRC. Both the azoxymethane colon carcinogenesis and dextran sulfate sodium colitis carcinogenesis models demonstrated temporal increases in mucosal HMGB1 levels. Activated CD8+ cells initially increased and then decreased, whereas exhausted CD8+ cells increased. Additionally, we observed increased regulatory CD8+ cells, decreased naïve CD8+ cells, and decreased mucosal epithelial differentiation. In the in vitro study, HMGB1 induced energy reprogramming from oxidative phosphorylation to glycolysis in CD8+ cells and intestinal epithelial cells. Furthermore, in UC dysplasia, UC-related CRC, and hyperplastic mucosa surrounding human sporadic CRC, we found increased mucosal HMGB1, decreased activated CD8+ cells, and suppressed mucosal epithelial differentiation. However, we observed increased activated CD8+ cells in active UC mucosa. These findings indicate that HMGB1 plays an important role in modulating mucosal immunity and epithelial dedifferentiation in both UC-related carcinogenesis and sporadic CRC.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>38999957</pmid><doi>10.3390/ijms25136846</doi><orcidid>https://orcid.org/0000-0003-2298-8825</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Analysis Animals Antibodies Cancer Carcinogenesis - immunology Carcinogenesis - metabolism Carcinogenesis - pathology CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - metabolism Cell Differentiation Cell growth Chromosomal proteins Colitis, Ulcerative - chemically induced Colitis, Ulcerative - immunology Colitis, Ulcerative - metabolism Colitis, Ulcerative - pathology Colon Colon cancer Colorectal cancer Colorectal Neoplasms - immunology Colorectal Neoplasms - metabolism Colorectal Neoplasms - pathology Development and progression Dextran Disease Epithelial Cells - metabolism Epithelial Cells - pathology Ethylenediaminetetraacetic acid HMGB1 Protein - metabolism Humans Immunity, Mucosal Inflammatory bowel disease Intestinal Mucosa - immunology Intestinal Mucosa - metabolism Intestinal Mucosa - pathology Lymphocytes Male Mice Mice, Inbred C57BL Peptides Phosphatase Proteins Respiration Sulfates Ulcerative colitis |
| title | Effects of High-Mobility Group Box-1 on Mucosal Immunity and Epithelial Differentiation in Colitic Carcinoma |
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