The Transcription Factor T-bet Resolves Memory B Cell Subsets with Distinct Tissue Distributions and Antibody Specificities in Mice and Humans

被引：152

作者：

Johnson, John L. ^{[1
]}

Rosenthal, Rebecca L. ^{[1
]}

Knox, James J. ^{[1
]}

Myles, Arpita ^{[1
]}

Naradikian, Martin S. ^{[2
]}

Madej, Joanna ^{[1
]}

Kostiv, Mariya ^{[1
]}

Rosenfeld, Aaron M. ^{[1
]}

Meng, Wenzhao ^{[1
]}

Christensen, Shannon R. ^{[3
]}

Hensley, Scott E. ^{[3
]}

Yewdell, Jonathan ^{[4
]}

Canaday, David H. ^{[5
,6
]}

Zhu, Jinfang ^{[7
]}

McDermott, Adrian B. ^{[8
]}

Dori, Yoav ^{[9
]}

Itkin, Max ^{[10
]}

Wherry, E. John ^{[11
,12
]}

Pardi, Norbert ^{[13
]}

Weissman, Drew ^{[13
]}

Naji, Ali ^{[14
]}

Prak, Eline T. Luning ^{[1
]}

Betts, Michael R. ^{[3
]}

Cancro, Michael P. ^{[1
]}

机构：

[1] Univ Penn, Dept Pathol & Lab Med, Philadelphia, PA 19104 USA

[2] La Jolla Inst Allergy & Immunol, La Jolla, CA 92037 USA

[3] Univ Penn, Dept Microbiol, Philadelphia, PA 19104 USA

[4] NIAID, Lab Viral Dis, NIH, 9000 Rockville Pike, Bethesda, MD 20892 USA

[5] Case Western Reserve Univ, Sch Med, Div Infect Dis, Cleveland, OH 45106 USA

[6] Cleveland VA Hosp, Cleveland, OH 45106 USA

[7] NIAID, Lab Immune Syst Biol, NIH, 9000 Rockville Pike, Bethesda, MD 20892 USA

[8] NIAID, Vaccine Res Ctr, NIH, 9000 Rockville Pike, Bethesda, MD 20892 USA

[9] Childrens Hosp Philadelphia, Ctr Lymphat Imaging & Intervent, Philadelphia, PA 19104 USA

[10] Hosp Univ Penn, Dept Radiol, Div Intervent Radiol, 3400 Spruce St, Philadelphia, PA 19104 USA

[11] Univ Penn, Parker Inst Canc Immunotherapy, Inst Immunol, Philadelphia, PA 19104 USA

[12] Univ Penn, Dept Syst Pharmacol & Translat Therapeut, Philadelphia, PA 19104 USA

[13] Univ Penn, Dept Med, Philadelphia, PA 19104 USA

[14] Hosp Univ Penn, Dept Surg, 3400 Spruce St, Philadelphia, PA 19104 USA

来源：

IMMUNITY | 2020年 / 52卷 / 05期

基金：

美国国家卫生研究院;

关键词：

INFLUENZA-VIRUS; EXPRESSION; DIFFERENTIATION; HEMAGGLUTININ; REPERTOIRE; INFECTION; RESPONSES; PATTERNS; PROGRAM; VACCINE;

D O I：

10.1016/j.immuni.2020.03.020

中图分类号：

R392 [医学免疫学]; Q939.91 [免疫学];

学科分类号：

100102 ;

摘要：

B cell subsets expressing the transcription factor T-bet are associated with humoral immune responses and autoimmunity. Here, we examined the anatomic distribution, clonal relationships, and functional properties of T-bet(+) and T-bet(-) memory B cells (MBCs) in the context of the influenza-specific immune response. In mice, both T-bet(-) and T-bet(+) hemagglutinin (HA)-specific B cells arose in germinal centers, acquired memory B cell markers, and persisted indefinitely. Lineage tracing and IgH repertoire analyses revealed minimal interconversion between T-bet(-) and T-bet(+) MBCs, and parabionts showed differential tissue residency and recirculation properties. T-bet(+) MBCs could be subdivided into recirculating T-bet(lo) MBCs and spleen-resident T-bet(hi) MBCs. Human MBCs displayed similar features. Conditional gene deletion studies revealed that T-bet expression in B cells was required for nearly all HA stalk-specific IgG2c antibodies and for durable neutralizing titers to influenza. Thus, T-bet expression distinguishes MBC subsets that have profoundly different homing, residency, and functional properties, and mediate distinct aspects of humoral immune memory.

引用

页码：842 / +

页数：20

共 68 条

[21] THE IGG SUBCLASS RESPONSES TO INFLUENZA-VIRUS HEMAGGLUTININ IN THE MOUSE - EFFECT OF ROUTE OF INOCULATION [J].

HOCART, MJ ;

MACKENZIE, JS ;

STEWART, GA .

JOURNAL OF GENERAL VIROLOGY, 1989, 70 :809-818

[22] A genome-wide regulatory network identifies key transcription factors for memory CD8+ T-cell development [J].

Hu, Guangan ;

Chen, Jianzhu .

NATURE COMMUNICATIONS, 2013, 4

[23] Anomalous type 17 response to viral infection by CD8+ T cells lacking T-bet and eomesodermin [J].

Intlekofer, Andrew M. ;

Banerjee, Arnob ;

Takemoto, Naofumi ;

Gordon, Scott M. ;

DeJong, Caitlin S. ;

Shin, Haina ;

Hunter, Christopher A. ;

Wherry, E. John ;

Lindsten, Tullia ;

Reiner, Steven L. .

SCIENCE, 2008, 321 (5887) :408-411

[24] Complement receptor 2/CD21- human naive B cells contain mostly autoreactive unresponsive clones [J].

Isnardi, Isabelle ;

Ng, Yen-Shing ;

Menard, Laurence ;

Meyers, Greta ;

Saadoun, David ;

Srdanovic, Iva ;

Samuels, Jonathan ;

Berman, Jessica ;

Buckner, Jane H. ;

Cunningham-Rundles, Charlotte ;

Meffre, Eric .

BLOOD, 2010, 115 (24) :5026-5036

[25] Distinct Effector B Cells Induced by Unregulated Toll-like Receptor 7 Contribute to Pathogenic Responses in Systemic Lupus Erythematosus [J].

Jenks, Scott A. ;

Cashman, Kevin S. ;

Zumaquero, Esther ;

Marigorta, Urko M. ;

Patel, Aakash V. ;

Wang, Xiaoqian ;

Tomar, Deepak ;

Woodruff, Matthew C. ;

Simon, Zoe ;

Bugrovsky, Regina ;

Blalock, Emily L. ;

Scharer, Christopher D. ;

Tipton, Christopher M. ;

Wei, Chungwen ;

Lim, S. Sam ;

Petri, Michelle ;

Niewold, Timothy B. ;

Anolik, Jennifer H. ;

Gibson, Greg ;

Lee, F. Eun-Hyung ;

Boss, Jeremy M. ;

Lund, Frances E. ;

Sanz, Ignacio .

IMMUNITY, 2018, 49 (04) :725-+

[26] Different T-bet expression patterns characterize particular reactive lymphoid tissue lesions [J].

Jöhrens, K ;

Anagnostopoulos, I ;

Dürkop, H ;

Stein, H .

HISTOPATHOLOGY, 2006, 48 (04) :343-352

[27] Vaccine-Induced Antibodies that Neutralize Group 1 and Group 2 Influenza A Viruses [J].

Joyce, M. Gordon ;

Wheatley, Adam K. ;

Thomas, Paul V. ;

Chuang, Gwo-Yu ;

Soto, Cinque ;

Bailer, Robert T. ;

Druz, Aliaksandr ;

Georgiev, Ivelin S. ;

Gillespie, Rebecca A. ;

Kanekiyo, Masaru ;

Kong, Wing-Pui ;

Leung, Kwanyee ;

Narpala, Sandeep N. ;

Prabhakaran, Madhu S. ;

Yang, Eun Sung ;

Zhang, Baoshan ;

Zhang, Yi ;

Asokan, Mangaiarkarasi ;

Boyington, Jeffrey C. ;

Bylund, Tatsiana ;

Darko, Sam ;

Lees, Christopher R. ;

Ransier, Amy ;

Shen, Chen-Hsiang ;

Wang, Lingshu ;

Whittle, James R. ;

Wu, Xueling ;

Yassine, Hadi M. ;

Santos, Celia ;

Matsuoka, Yumiko ;

Tsybovsky, Yaroslav ;

Baxa, Ulrich ;

Mullikin, James C. ;

Subbarao, Kanta ;

Douek, Daniel C. ;

Graham, Barney S. ;

Koup, Richard A. ;

Ledgerwood, Julie E. ;

Roederer, Mario ;

Shapiro, Lawrence ;

Kwong, Peter D. ;

Mascola, John R. ;

McDermott, Adrian B. .

CELL, 2016, 166 (03) :609-623

[28] Parabiosis in Mice: A Detailed Protocol [J].

Kamran, Paniz ;

Sereti, Konstantina-Ioanna ;

Zhao, Peng ;

Ali, Shah R. ;

Weissman, Irving L. ;

Ardehali, Reza .

JOVE-JOURNAL OF VISUALIZED EXPERIMENTS, 2013, (80)

[29] T-Bet+ IgM Memory Cells Generate Multi-lineage Effector B Cells [J].

Kenderes, Kevin J. ;

Levack, Russell C. ;

Papillion, Amber M. ;

Cabrera-Martinez, Berenice ;

Dishaw, Lisa M. ;

Winslow, Gary M. .

CELL REPORTS, 2018, 24 (04) :824-+

[30] Age-Associated B Cells Express a Diverse Repertoire of VH and Vκ Genes with Somatic Hypermutation [J].

Knode, Lisa M. Russell ;

Naradikian, Martin S. ;

Myles, Arpita ;

Scholz, Jean L. ;

Hao, Yi ;

Liu, Danya ;

Ford, Mandy L. ;

Tobias, John W. ;

Cancro, Michael P. ;

Gearhart, Patricia J. .

JOURNAL OF IMMUNOLOGY, 2017, 198 (05) :1921-1927

← 1 2 3 4 5 6 7 →