Multifaceted profiling of virus-specific CD8 T cells reveals distinct immune signatures against cytomegalovirus infection states during pregnancy

Summary: Anti-cytomegalovirus (CMV) serological testing, including the IgG avidity index (AI), is used to assess CMV infection phases during pregnancy. However, little is known about anti-CMV cellular immunity during pregnancy, particularly its relation to serological diagnosis. Herein, using MHC-de...

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Main Authors: Ayumi Taguchi, Fumi Misumi, Shunsuke Teraguchi, Takeshi Nagamatsu, Shuhei Sakakibara, Tomohiro Otani, Mari Ichinose, David Priest, Kazuki Nakajima, Junko Nakamura, Ryoko Sawada, Tatsuo Suzutani, Toshiyuki Ikeda, Yutaka Nagura, Takayuki Iriyama, Daisuke Okuzaki, Hitoshi Okazaki, James B. Wing, Yasushi Hirota, Yutaka Osuga
Format: Article
Language:English
Published: Elsevier 2025-05-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S2589004225006777
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author Ayumi Taguchi
Fumi Misumi
Shunsuke Teraguchi
Takeshi Nagamatsu
Shuhei Sakakibara
Tomohiro Otani
Mari Ichinose
David Priest
Kazuki Nakajima
Junko Nakamura
Ryoko Sawada
Tatsuo Suzutani
Toshiyuki Ikeda
Yutaka Nagura
Takayuki Iriyama
Daisuke Okuzaki
Hitoshi Okazaki
James B. Wing
Yasushi Hirota
Yutaka Osuga
author_facet Ayumi Taguchi
Fumi Misumi
Shunsuke Teraguchi
Takeshi Nagamatsu
Shuhei Sakakibara
Tomohiro Otani
Mari Ichinose
David Priest
Kazuki Nakajima
Junko Nakamura
Ryoko Sawada
Tatsuo Suzutani
Toshiyuki Ikeda
Yutaka Nagura
Takayuki Iriyama
Daisuke Okuzaki
Hitoshi Okazaki
James B. Wing
Yasushi Hirota
Yutaka Osuga
author_sort Ayumi Taguchi
collection DOAJ
description Summary: Anti-cytomegalovirus (CMV) serological testing, including the IgG avidity index (AI), is used to assess CMV infection phases during pregnancy. However, little is known about anti-CMV cellular immunity during pregnancy, particularly its relation to serological diagnosis. Herein, using MHC-dextramer single-cell RNA sequencing and flow cytometry, we characterized IE1 and pp65 CMV-antigen specific CD8 T cells from pregnant women with different anti-CMV serological patterns, including IgG+IgM+/AI-low, IgG+IgM+/AI-high, and IgG+IgM−. In IgG+IgM+/AI-low and IgG+IgM+/AI-high specimens, CMV-specific T cells consisted largely of effectors, with a minor but characteristic proportion of memory T cells, including HLA-DR-positive memory precursors and granzyme K-high memory cells reactive to IE1. Conversely, IgG+IgM− cases had a distinctive expansion of pp65-specific terminally differentiated T effector memory with a signature of convergent clonal selection. Our findings revealed that different CMV infection phases have characteristic patterns of CD8 cell phenotype and antigen recognition, potentially offering a new approach for assessing congenital infection risk.
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spelling doaj-art-45e6c74e4ebd4b1faf3bd85f152e00222025-08-20T03:14:06ZengElsevieriScience2589-00422025-05-0128511241610.1016/j.isci.2025.112416Multifaceted profiling of virus-specific CD8 T cells reveals distinct immune signatures against cytomegalovirus infection states during pregnancyAyumi Taguchi0Fumi Misumi1Shunsuke Teraguchi2Takeshi Nagamatsu3Shuhei Sakakibara4Tomohiro Otani5Mari Ichinose6David Priest7Kazuki Nakajima8Junko Nakamura9Ryoko Sawada10Tatsuo Suzutani11Toshiyuki Ikeda12Yutaka Nagura13Takayuki Iriyama14Daisuke Okuzaki15Hitoshi Okazaki16James B. Wing17Yasushi Hirota18Yutaka Osuga19Laboratory of Human Single Cell Immunology, WPI Immunology Frontier Research Center, The University of Osaka, Osaka 565-0871, Japan; Department of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo 113-8654, JapanDepartment of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo 113-8654, JapanFaculty of Data Science, Shiga University, Shiga 522-8522, Japan; Department of Genome Informatics, Research Institute for Microbial Diseases, The University of Osaka, Osaka 565-0871, JapanDepartment of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo 113-8654, Japan; Department of Obstetrics and Gynecology, International University of Health and Welfare, Narita 286-8686, Japan; Corresponding authorLaboratory of Systems Immunology, WPI Immunology Frontier Research Center, The University of Osaka, Osaka 565-0871, Japan; Graduate School of Medical Safety Management, Jikei University of Health Care Sciences, Osaka 532-0003, Japan; Corresponding authorDepartment of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo 113-8654, JapanDepartment of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo 113-8654, JapanLaboratory of Human Single Cell Immunology, WPI Immunology Frontier Research Center, The University of Osaka, Osaka 565-0871, JapanDepartment of Transfusion Medicine, The University of Tokyo, Tokyo 113-8655, JapanDepartment of Transfusion Medicine, The University of Tokyo, Tokyo 113-8655, Japan; Laboratory Sciences, Department of Health Sciences, School of Health and Social Service, Saitama Prefectural University, Saitama 343-0036, JapanDepartment of Transfusion Medicine, The University of Tokyo, Tokyo 113-8655, JapanDepartment of Microbiology, Fukushima Medical University School of Medicine, Fukushima 960-1295, JapanDepartment of Transfusion Medicine, The University of Tokyo, Tokyo 113-8655, JapanDepartment of Transfusion Medicine, The University of Tokyo, Tokyo 113-8655, JapanDepartment of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo 113-8654, JapanLaboratory of Human Immunology (Single Cell Genomics), WPI Immunology Frontier Research Center, The University of Osaka, Osaka 565-0871, Japan; Human Single Cell Immunology Team, Center for Infectious Disease Education and Research, The University of Osaka, Osaka 565-0871, JapanDepartment of Transfusion Medicine, The University of Tokyo, Tokyo 113-8655, JapanLaboratory of Human Single Cell Immunology, WPI Immunology Frontier Research Center, The University of Osaka, Osaka 565-0871, Japan; Human Single Cell Immunology Team, Center for Infectious Disease Education and Research, The University of Osaka, Osaka 565-0871, JapanDepartment of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo 113-8654, JapanDepartment of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo 113-8654, JapanSummary: Anti-cytomegalovirus (CMV) serological testing, including the IgG avidity index (AI), is used to assess CMV infection phases during pregnancy. However, little is known about anti-CMV cellular immunity during pregnancy, particularly its relation to serological diagnosis. Herein, using MHC-dextramer single-cell RNA sequencing and flow cytometry, we characterized IE1 and pp65 CMV-antigen specific CD8 T cells from pregnant women with different anti-CMV serological patterns, including IgG+IgM+/AI-low, IgG+IgM+/AI-high, and IgG+IgM−. In IgG+IgM+/AI-low and IgG+IgM+/AI-high specimens, CMV-specific T cells consisted largely of effectors, with a minor but characteristic proportion of memory T cells, including HLA-DR-positive memory precursors and granzyme K-high memory cells reactive to IE1. Conversely, IgG+IgM− cases had a distinctive expansion of pp65-specific terminally differentiated T effector memory with a signature of convergent clonal selection. Our findings revealed that different CMV infection phases have characteristic patterns of CD8 cell phenotype and antigen recognition, potentially offering a new approach for assessing congenital infection risk.http://www.sciencedirect.com/science/article/pii/S2589004225006777biological sciencesimmunologypregnancy
spellingShingle Ayumi Taguchi
Fumi Misumi
Shunsuke Teraguchi
Takeshi Nagamatsu
Shuhei Sakakibara
Tomohiro Otani
Mari Ichinose
David Priest
Kazuki Nakajima
Junko Nakamura
Ryoko Sawada
Tatsuo Suzutani
Toshiyuki Ikeda
Yutaka Nagura
Takayuki Iriyama
Daisuke Okuzaki
Hitoshi Okazaki
James B. Wing
Yasushi Hirota
Yutaka Osuga
Multifaceted profiling of virus-specific CD8 T cells reveals distinct immune signatures against cytomegalovirus infection states during pregnancy
iScience
biological sciences
immunology
pregnancy
title Multifaceted profiling of virus-specific CD8 T cells reveals distinct immune signatures against cytomegalovirus infection states during pregnancy
title_full Multifaceted profiling of virus-specific CD8 T cells reveals distinct immune signatures against cytomegalovirus infection states during pregnancy
title_fullStr Multifaceted profiling of virus-specific CD8 T cells reveals distinct immune signatures against cytomegalovirus infection states during pregnancy
title_full_unstemmed Multifaceted profiling of virus-specific CD8 T cells reveals distinct immune signatures against cytomegalovirus infection states during pregnancy
title_short Multifaceted profiling of virus-specific CD8 T cells reveals distinct immune signatures against cytomegalovirus infection states during pregnancy
title_sort multifaceted profiling of virus specific cd8 t cells reveals distinct immune signatures against cytomegalovirus infection states during pregnancy
topic biological sciences
immunology
pregnancy
url http://www.sciencedirect.com/science/article/pii/S2589004225006777
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