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is published twice each month byThe Journal of Immunology

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VOL. 194 | NO. 7 | April 1, 2015 | Pages 2957–3530

IN THIS ISSUE2957 Eyeing Regulation of Uveitis See article p. 3011

MKP7 Manages T Cells See article p. 3088NK CARte Blanche in Tumor Targeting See article p. 3201STINGing Sensors See article p. 3236Wnt Winds Down Neuroinflammation See article p. 3295OSCAR-Binding Key to Lectin Function See article p. 3317E. coli EVs Elicit Emphysema See article p. 3361

PILLARS OF IMMUNOLOGY2959 T-bet Transcendent: Unmasking the Faces of Multifarious Immunity

Steven L. Reiner

2961 Pillars Article: A Novel Transcription Factor, T-bet, Directs Th1 Lineage Commitment. Cell. 2000.100: 655–669Susanne J. Szabo, Sean T. Kim, Gina L. Costa, Xiankui Zhang, C. Garrison Fathman, and Laurie H. Glimcher

BRIEF REVIEWS2977 The Role of PTPN22 Risk Variant in the Development of Autoimmunity: Finding Common Ground

between Mouse and HumanDavid J. Rawlings, Xuezhi Dai, and Jane H. Buckner

2985 Tumor-Infiltrating Dendritic Cells in Cancer PathogenesisJo Marie Tran Janco, Purushottam Lamichhane, Lavakumar Karyampudi, and Keith L. Knutson

CUTTING EDGE2993 Cutting Edge: An In Vivo Reporter Reveals Active B Cell Receptor Signaling in the Germinal Center

James Mueller, Mehrdad Matloubian, and Julie Zikherman

On the cover: High macrophage infiltration (DAB staining) following Helicobacter pylori–induced gastritis in mice withspecific deletion of hypoxia inducible factor-1 (HIF-1) in the myeloid lineage. This figure illustrates a global increase in

inflammation, which leads to the worsening of the gastritis in the absence of myeloid HIF-1. Image credit: Andrija Matak.Matak, P., M. Heinis, J. R. R. Mathieu, R. Corriden, S. Cuvellier, S. Delga, R. Mounier, A. Rouquette, J. Raymond,D. Lamarque, J.-F. Emile, V. Nizet, E. Touati, and C. Peyssonnaux. 2015. Myeloid HIF-1 is protective in Helicobacterpylori–mediated gastritis. J. Immunol. 194: 3259–3266.

The Journal of Immunology (ISSN 0022-1767) is published twice each month by The American Association of Immunologists,

Inc., 9650 Rockville Pike, Bethesda, MD 20814-3994, Phone: 301-634-7197, Fax: 301-634-7829. Subscription terms: Newsubscriptions and renewals begin January 1 and expire one year later (see http://www.jimmunol.org/subscriptions for prices anddetails). A special rate is available to members of The American Association of Immunologists, Inc. (see http://www.aai.org/

membership). The American Association of Immunologists, Inc., is not responsible for undeliverable issues. Replacement issuescan be obtained, if available, at the regular price of single issues (see http://www.jimmunol.org/pdf/single_issue_purchase.pdf).Reprints of individual articles are available only from authors. Periodicals postage paid at Bethesda, MD 20814-3994, and at

additional mailing offices. Country of origin U.S.A. Printed on acid-free recyclable paper. Postmaster: Send address changes60 days in advance to The Journal of Immunology, Subscription Department, 9650 Rockville Pike, Bethesda, MD 20814-3994.Copyright � 2015 by The American Association of Immunologists, Inc.

Journal ofTh e

ImmunologyTable of Contents

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ANTIGEN RECOGNITION AND RESPONSES2999 IL-4–Secreting Secondary T Follicular Helper (Tfh) Cells Arise from Memory T Cells, Not Persisting Tfh

Cells, through a B Cell–Dependent MechanismKeke C. Fairfax, Bart Everts, Eyal Amiel, Amber M. Smith, Gabriele Schramm, Helmut Haas, Gwendalyn J. Randolph,

Justin J. Taylor, and Edward J. Pearce

AUTOIMMUNITY3011 Retina-Specific T Regulatory Cells Bring About Resolution andMaintain Remission of Autoimmune Uveitis

Phyllis Silver, Reiko Horai, Jun Chen, Yingyos Jittayasothorn, Chi-Chao Chan, Rafael Villasmil, Muge R. Kesen,

and Rachel R. Caspi

3020 Egress of Mature Murine Regulatory T Cells from the Thymus Requires RelATaro Fukazawa, Noriko Hiraiwa, Takeshi Umemura, Setsuko Mise-Omata, Yuichi Obata, and Takahiro Doi

3029 Functional Analysis of a Complement Polymorphism (rs17611) Associated with Rheumatoid ArthritisJoanna L. Giles, Ernest Choy, Carmen van den Berg, B. Paul Morgan, and Claire L. Harris

CLINICAL AND HUMAN IMMUNOLOGY3035 TLR7- and TLR9-Responsive Human B Cells Share Phenotypic and Genetic Characteristics

Noa Simchoni and Charlotte Cunningham-Rundles

3045 A Novel Thymoma-Associated Immunodeficiency with Increased Naive T Cells and Reduced CD247ExpressionPetros Christopoulos, Elaine P. Dopfer, Miroslav Malkovsky, Philipp R. Esser, Hans-Eckart Schaefer, Alexander Marx,

Sylvia Kock, Nicole Rupp, Myriam R. Lorenz, Klaus Schwarz, Jan Harder, Stefan F. Martin, Martin Werner,

Christian Bogdan, Wolfgang W. A. Schamel, and Paul Fisch

IMMUNE REGULATION3054 Cellular Mechanisms of CCL22-Mediated Attenuation of Autoimmune Diabetes

Loraine Bischoff, Sigrid Alvarez, Derek L. Dai, Galina Soukhatcheva, Paul C. Orban, and C. Bruce Verchere

3065 B Cell Rab7Mediates Induction of Activation-Induced Cytidine Deaminase Expression and Class-Switchingin T-Dependent and T-Independent Antibody ResponsesEgest J. Pone, Tonika Lam, Zheng Lou, Rui Wang, Yuhui Chen, Dongfang Liu, Aimee L. Edinger, Zhenming Xu,

and Paolo Casali

3079 Alcohol-Induced miR-27a Regulates Differentiation and M2 Macrophage Polarization of Normal HumanMonocytesBanishree Saha, Johanna C. Bruneau, Karen Kodys, and Gyongyi Szabo

3088 MAPK Phosphatase 7 Regulates T Cell Differentiation via Inhibiting ERK-Mediated IL-2 ExpressionYongliang Zhang, Kalyan C. Nallaparaju, Xin Liu, Huipeng Jiao, Joseph M. Reynolds, Zhi-Xin Wang, and Chen Dong

3096 FcmR Interacts and Cooperates with the B Cell Receptor To Promote B Cell SurvivalRika Ouchida, Qing Lu, Jun Liu, Yingqian Li, Yiwei Chu, Takeshi Tsubata, and Ji-Yang Wang

3102 HSV-2 Immediate-Early Protein US1 Inhibits IFN-b Production by Suppressing Association of IRF-3with IFN-b PromoterMudan Zhang, Yalan Liu, Ping Wang, Xinmeng Guan, Siyi He, Sukun Luo, Chang Li, Kai Hu, Wei Jin, Tao Du,

Yan Yan, Zhenfeng Zhang, Zhenhua Zheng, Hanzhong Wang, and Qinxue Hu

3116 Demethylation of the RORC2 and IL17A in Human CD4+ T Lymphocytes Defines Th17 Origin ofNonclassic Th1 CellsAlessio Mazzoni, Veronica Santarlasci, Laura Maggi, Manuela Capone, Maria Caterina Rossi, Valentina Querci,

Raffaele De Palma, Hyun-Dong Chang, Andreas Thiel, Rolando Cimaz, Francesco Liotta, Lorenzo Cosmi, Enrico Maggi,

Andreas Radbruch, Sergio Romagnani, Jun Dong, and Francesco Annunziato

3127 Ultraviolet Radiation Signaling through TLR4/MyD88 Constrains DNA Repair and Plays a Role inCutaneous ImmunosuppressionErin Harberts, Hua Zhou, Rita Fishelevich, Juan Liu, and Anthony A. Gaspari

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3136 TCAIM Decreases T Cell Priming Capacity of Dendritic Cells by Inhibiting TLR-Induced Ca2+ Influxand IL-2 ProductionSimone Z. Vogel, Stephan Schlickeiser, Karsten Jurchott, Levent Akyuez, Julia Schumann, Christine Appelt, Katrin Vogt,

Martina Schroder, Martin Vaeth, Friederike Berberich-Siebelt, Manfred B. Lutz, Gerald Grutz, and Birgit Sawitzki

3147 Therapeutic Regulatory T Cells Subvert Effector T Cell Function in Inflamed Islets To Halt AutoimmuneDiabetesAshley E. Mahne, Joanna E. Klementowicz, Annie Chou, Vinh Nguyen, and Qizhi Tang

3156 IL-1 Receptor Type 2 Suppresses Collagen-Induced Arthritis by Inhibiting IL-1 Signal on MacrophagesKenji Shimizu, Akiko Nakajima, Katsuko Sudo, Yang Liu, Atsuhiko Mizoroki, Tetsuro Ikarashi, Reiko Horai,

Shigeru Kakuta, Toshiki Watanabe, and Yoichiro Iwakura

3169 Collagen Induces Maturation of Human Monocyte-Derived Dendritic Cells by Signaling throughOsteoclast-Associated ReceptorHeidi S. Schultz, Louise M. Nitze, Louise H. Zeuthen, Pernille Keller, Albrecht Gruhler, Jesper Pass, Jianhe Chen, Li Guo,

Andrew J. Fleetwood, John A. Hamilton, Martin W. Berchtold, and Svetlana Panina

3180 Inhibiting STAT5 by the BET Bromodomain Inhibitor JQ1 Disrupts Human Dendritic Cell MaturationPatricia A. Toniolo, Suhu Liu, Jennifer E. Yeh, Pedro M. Moraes-Vieira, Sarah R. Walker, Vida Vafaizadeh,

Jos�e Alexandre M. Barbuto, and David A. Frank

IMMUNE SYSTEM DEVELOPMENT3191 Repression of Ccr9 Transcription in Mouse T Lymphocyte Progenitors by the Notch Signaling Pathway

Veena Krishnamoorthy, Tiffany Carr, Renee F. de Pooter, Emanuelle Olumide Akinola, Fotini Gounari, and Barbara L. Kee

IMMUNOTHERAPY AND VACCINES3201 DAP12-Based Activating Chimeric Antigen Receptor for NK Cell Tumor Immunotherapy

Katrin Topfer, Marc Cartellieri, Susanne Michen, Ralf Wiedemuth, Nadja Muller, Dirk Lindemann, Michael Bachmann,

Monika Fussel, Gabriele Schackert, and Achim Temme

3213 Liver-Resident CD103+ Dendritic Cells Prime Antiviral CD8+ T Cells In SituPeter D. Krueger, Taeg S. Kim, Sun-Sang J. Sung, Thomas J. Braciale, and Young S. Hahn

INFECTIOUS DISEASE AND HOST RESPONSE3223 Ly6Chigh Monocytes Control Cerebral Toxoplasmosis

Aindrila Biswas, Dunja Bruder, Susanne A. Wolf, Andreas Jeron, Matthias Mack, Markus M. Heimesaat,

and Ildiko Rita Dunay

3236 cGAS and Ifi204 Cooperate To Produce Type I IFNs in Response to Francisella InfectionKelly M. Storek, Nina A. Gertsvolf, Maikke B. Ohlson, and Denise M. Monack

3246 Buprenorphine Decreases the CCL2-Mediated Chemotactic Response of MonocytesLoreto Carvallo, Lillie Lopez, Fa-Yun Che, Jihyeon Lim, Eliseo A. Eugenin, Dionna W. Williams, Edward Nieves,

Tina M. Calderon, Carlos Madrid-Aliste, Andras Fiser, Louis Weiss, Ruth Hogue Angeletti, and Joan W. Berman

3259 Myeloid HIF-1 Is Protective in Helicobacter pylori–Mediated GastritisPavle Matak, Myl�ene Heinis, Jacques R. R. Mathieu, Ross Corriden, Sylvain Cuvellier, St�ephanie Delga, R�emi Mounier,

Alexandre Rouquette, Josette Raymond, Dominique Lamarque, Jean-Francois Emile, Victor Nizet, Eliette Touati,

and Carole Peyssonnaux

3267 Blimp-1, an Intrinsic Factor that Represses HIV-1 Proviral Transcription in Memory CD4+ T CellsKatarzyna Kaczmarek Michaels, Malini Natarajan, Zelda Euler, Galit Alter, Gregory Viglianti, and Andrew J. Henderson

3275 Proinflammatory Responses and Higher IL-10 Production by T Cells Correlate with Protection againstMalaria during Pregnancy and Delivery OutcomesPilar Requena, Diana Barrios, Leanne J. Robinson, Paula Samol, Alexandra J. Umbers, Regina Wangnapi,

Maria Ome-Kaius, Anna Rosanas-Urgell, Alfredo Mayor, Marta L�opez, Elisa de Lazzari, Myriam Ar�evalo-Herrera,

Carmen Fern�andez-Becerra, Hernando del Portillo, Chetan E. Chitnis, Peter M. Siba, Stephen Rogerson, Ivo Mueller,

Azucena Bardaji, Clara Men�endez, and Carlota Doban~o

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INNATE IMMUNITY AND INFLAMMATION3286 CIKS/DDX3X Interaction Controls the Stability of the Zc3h12a mRNA Induced by IL-17

Domenico Somma, Paola Mastrovito, Marianeve Grieco, Alfonso Lavorgna, Angelica Pignalosa, Luigi Formisano,

Anna Maria Salzano, Andrea Scaloni, Francesco Pacifico, Ulrich Siebenlist, and Antonio Leonardi

3295 Canonical Wnt Signaling in Dendritic Cells Regulates Th1/Th17 Responses and Suppresses AutoimmuneNeuroinflammationAmol Suryawanshi, Indumathi Manoharan, Yuan Hong, Daniel Swafford, Tanmay Majumdar, M. Mark Taketo,

Balaji Manicassamy, Pandelakis A. Koni, Muthusamy Thangaraju, Zuoming Sun, Andrew L. Mellor, David H. Munn,

and Santhakumar Manicassamy

3305 Rare Loss-of-Function Mutation in Complement Component C3 Provides Insight into Molecularand Pathophysiological Determinants of Complement ActivityGeorgia Sfyroera, Daniel Ricklin, Edimara S. Reis, Hui Chen, Emilia L. Wu, Yiannis N. Kaznessis, Kristina N. Ekdahl,

Bo Nilsson, and John D. Lambris

3317 OSCAR Is a Receptor for Surfactant Protein D That Activates TNF-a Release from Human CCR2+

Inflammatory MonocytesAlexander D. Barrow, Yaseelan Palarasah, Mattia Bugatti, Alex S. Holehouse, Derek E. Byers, Michael J. Holtzman,

William Vermi, Karsten Skjødt, Erika Crouch, and Marco Colonna

3327 Group V Secreted Phospholipase A2 Is Upregulated by IL-4 in Human Macrophages and MediatesPhagocytosis via Hydrolysis of Ethanolamine PhospholipidsJulio M. Rubio, Juan P. Rodriguez, Luis Gil-de-G�omez, Carlos Guijas, Maria A. Balboa, and Jes �us Balsinde

3340 Basal Cells Contribute to Innate Immunity of the Airway Epithelium through Production of theAntimicrobial Protein RNase 7Gimano D. Amatngalim, Yolanda van Wijck, Yvonne de Mooij-Eijk, Renate M. Verhoosel, Jurgen Harder,

Annemarie N. Lekkerkerker, Richard A. J. Janssen, and Pieter S. Hiemstra

3351 WNT-Inflammasome Signaling Mediates NOD2-Induced Development of Acute Arthritis in MiceVikas Singh, Sahana Holla, Subbaraya G. Ramachandra, and Kithiganahalli Narayanaswamy Balaji

3361 Extracellular Vesicles Derived from Gram-Negative Bacteria, such as Escherichia coli, Induce EmphysemaMainly via IL-17A–Mediated Neutrophilic InflammationYou-Sun Kim, Won-Hee Lee, Eun-Jeong Choi, Jun-Pyo Choi, Young Joo Heo, Yong Song Gho, Young-Koo Jee,

Yeon-Mok Oh, and Yoon-Keun Kim

3369 The NLRP1 Inflammasome Attenuates Colitis and Colitis-Associated TumorigenesisTere M. Williams, Rachel A. Leeth, Daniel E. Rothschild, Sheryl L. Coutermarsh-Ott, Dylan K. McDaniel,

Alysha E. Simmons, Bettina Heid, Thomas E. Cecere, and Irving C. Allen

3381 Biased Agonism as a Novel Strategy To Harness the Proresolving Properties of Melanocortin Receptorswithout Eliciting Melanogenic EffectsTrinidad Montero-Melendez, Thomas Gobbetti, Sadani N. Cooray, Thomas E. N. Jonassen, and Mauro Perretti

3389 Myeloid HIFs Are Dispensable for Resolution of Inflammation during Skeletal Muscle RegenerationJulien Gondin, Marine Th�eret, Guillaume Duhamel, Katarina Pegan, Jacques R. R. Mathieu, Carole Peyssonnaux,

Sylvain Cuvellier, Claire Latroche, B�en�edicte Chazaud, David Bendahan, and R�emi Mounier

3400 CXCL10 Triggers Early Microglial Activation in the Cuprizone ModelTim Clarner, Katharina Janssen, Lara Nellessen, Martin Stangel, Thomas Skripuletz, Barbara Krauspe, Franz-Martin Hess,

Bernd Denecke, Clara Beutner, Bettina Linnartz-Gerlach, Harald Neumann, Luc Valli�eres, Sandra Amor, Kim Ohl,

Klaus Tenbrock, Cordian Beyer, and Markus Kipp

3414 Properdin Provides Protection from Citrobacter rodentium–Induced Intestinal Inflammation in aC5a/IL-6–Dependent MannerUmang Jain, Qi Cao, Nikhil A. Thomas, Trent M. Woodruff, Wilhelm J. Schwaeble, Cordula M. Stover,

and Andrew W. Stadnyk

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MOLECULAR AND STRUCTURAL IMMUNOLOGY3422 Noncanonical STAT3 Activation Regulates Excess TGF-b1 and Collagen I Expression in Muscle of

Stricturing Crohn’s DiseaseChao Li, Audra Iness, Jennifer Yoon, John R. Grider, Karnam S. Murthy, John M. Kellum, and John F. Kuemmerle

3432 Transcription-Dependent Generation of a Specialized Chromatin Structure at the TCRb LocusJoaquin Zacarias-Cabeza, Mohamed Belhocine, Laurent Vanhille, Pierre Cauchy, Frederic Koch, Aleksandra Pekowska,

Romain Fenouil, Aur�elie Bergon, Marta Gut, Ivo Gut, Dirk Eick, Jean Imbert, Pierre Ferrier, Jean-Christophe Andrau,

and Salvatore Spicuglia

3444 c-FLIP Protects T Lymphocytes from Apoptosis in the Intrinsic PathwayMing-Xiao He and You-Wen He

TUMOR IMMUNOLOGY3452 Differential Response of Myeloid-Derived Suppressor Cells to the Nonsteroidal Anti-Inflammatory Agent

Indomethacin in Tumor-Associated and Tumor-Free MicroenvironmentsAda G. Blidner, Mariana Salatino, Ivan D. Mascanfroni, Miriam J. Diament, Elisa Bal de Kier Joff�e, Maria A. Jasnis,

Slobodanka M. Klein, and Gabriel A. Rabinovich

3463 Macrophage Migration Inhibitory Factor–CXCR4 Is the Dominant Chemotactic Axis in HumanMesenchymal Stem Cell Recruitment to TumorsSofia Lourenco, Vitor H. Teixeira, Tammy Kalber, Ricardo J. Jose, R. Andres Floto, and Sam M. Janes

3475 CD8+CD103+ Tumor–Infiltrating Lymphocytes Are Tumor-Specific Tissue-Resident Memory T Cellsand a Prognostic Factor for Survival in Lung Cancer PatientsFaycal Djenidi, Julien Adam, Aicha Goubar, Aur�elie Durgeau, Guillaume Meurice, Vincent de Montpr�eville,

Pierre Validire, Benjamin Besse, and Fathia Mami-Chouaib

3487 Specific Roles of Each TCR Hemichain in Generating Functional Chain-Centric TCRMunehide Nakatsugawa, Yuki Yamashita, Toshiki Ochi, Shinya Tanaka, Kenji Chamoto, Tingxi Guo, Marcus O. Butler,

and Naoto Hirano

3501 Modeling the Specific CD4+ T Cell Response against a Tumor NeoantigenH�eloise Flament, Ruby Alonso Ramirez, Virginie Pr�emel, Nathalie T. Joncker, Alexandra Jacquet, Suzy Scholl,

and Olivier Lantz

NOVEL IMMUNOLOGICAL METHODS3513 Predominant Development of Mature and Functional Human NKCells in a Novel Human IL-2–Producing

Transgenic NOG MouseIkumi Katano, Takeshi Takahashi, Ryoji Ito, Tsutomu Kamisako, Takuma Mizusawa, Yuyo Ka, Tomoyuki Ogura,

Hiroshi Suemizu, Yutaka Kawakami, and Mamoru Ito

CORRECTIONS3526 Correction: Stat3 Activation Is Responsible for IL-6–Dependent T Cell Proliferation through Preventing

Apoptosis: Generation and Characterization of T Cell–Specific Stat3-Deficient MiceKiyoshi Takeda, Tsuneyasu Kaisho, Nobuaki Yoshida, Junji Takeda, Tadamitsu Kishimoto, and Shizuo Akira

3527 AUTHOR INDEX

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