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Table of Contents
The
Journal of
Immunology
VOL. 194 | NO. 7 | April 1, 2015 | Pages 2957–3530
IN THIS ISSUE
2957 Eyeing Regulation of Uveitis See article p. 3011
MKP7 Manages T Cells See article p. 3088
NK CARte Blanche in Tumor Targeting See article p. 3201
STINGing Sensors See article p. 3236
Wnt Winds Down Neuroinflammation See article p. 3295
OSCAR-Binding Key to Lectin Function See article p. 3317
E. coli EVs Elicit Emphysema See article p. 3361
PILLARS OF IMMUNOLOGY
2959 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: 655–669
Susanne J. Szabo, Sean T. Kim, Gina L. Costa, Xiankui Zhang, C. Garrison Fathman, and Laurie H. Glimcher
BRIEF REVIEWS
2977 The Role of PTPN22 Risk Variant in the Development of Autoimmunity: Finding Common Ground
between Mouse and Human
David J. Rawlings, Xuezhi Dai, and Jane H. Buckner
2985 Tumor-Infiltrating Dendritic Cells in Cancer Pathogenesis
Jo Marie Tran Janco, Purushottam Lamichhane, Lavakumar Karyampudi, and Keith L. Knutson
CUTTING EDGE
2993 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 with
specific 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 Helicobacter
pylori–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: New
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Copyright Ó 2015 by The American Association of Immunologists, Inc.
ANTIGEN RECOGNITION AND RESPONSES
2999 IL-4–Secreting Secondary T Follicular Helper (Tfh) Cells Arise from Memory T Cells, Not Persisting Tfh
Cells, through a B Cell–Dependent Mechanism
Keke C. Fairfax, Bart Everts, Eyal Amiel, Amber M. Smith, Gabriele Schramm, Helmut Haas, Gwendalyn J. Randolph,
Justin J. Taylor, and Edward J. Pearce
AUTOIMMUNITY
3011 Retina-Specific T Regulatory Cells Bring About Resolution and Maintain 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 RelA
Taro Fukazawa, Noriko Hiraiwa, Takeshi Umemura, Setsuko Mise-Omata, Yuichi Obata, and Takahiro Doi
3029 Functional Analysis of a Complement Polymorphism (rs17611) Associated with Rheumatoid Arthritis
Joanna L. Giles, Ernest Choy, Carmen van den Berg, B. Paul Morgan, and Claire L. Harris
CLINICAL AND HUMAN IMMUNOLOGY
3035 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 CD247
Expression
Petros 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 REGULATION
3054 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 Rab7 Mediates Induction of Activation-Induced Cytidine Deaminase Expression and Class-Switching
in T-Dependent and T-Independent Antibody Responses
Egest 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 Human
Monocytes
Banishree Saha, Johanna C. Bruneau, Karen Kodys, and Gyongyi Szabo
3088 MAPK Phosphatase 7 Regulates T Cell Differentiation via Inhibiting ERK-Mediated IL-2 Expression
Yongliang 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 Survival
Rika 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-3
with IFN-b Promoter
Mudan 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 of
Nonclassic Th1 Cells
Alessio 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 in
Cutaneous Immunosuppression
Erin Harberts, Hua Zhou, Rita Fishelevich, Juan Liu, and Anthony A. Gaspari
3136 TCAIM Decreases T Cell Priming Capacity of Dendritic Cells by Inhibiting TLR-Induced Ca2+ Influx
and IL-2 Production
Simone Z. Vogel, Stephan Schlickeiser, Karsten Ju¨rchott, Levent Akyuez, Julia Schumann, Christine Appelt, Katrin Vogt,
Martina Schro¨der, Martin Vaeth, Friederike Berberich-Siebelt, Manfred B. Lutz, Gerald Gru¨tz, and Birgit Sawitzki
3147 Therapeutic Regulatory T Cells Subvert Effector T Cell Function in Inflamed Islets To Halt Autoimmune
Diabetes
Ashley 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 Macrophages
Kenji 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 through
Osteoclast-Associated Receptor
Heidi 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 Maturation
Patricia 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 DEVELOPMENT
3191 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 VACCINES
3201 DAP12-Based Activating Chimeric Antigen Receptor for NK Cell Tumor Immunotherapy
Katrin To¨pfer, Marc Cartellieri, Susanne Michen, Ralf Wiedemuth, Nadja Mu¨ller, Dirk Lindemann, Michael Bachmann,
Monika Fu¨ssel, Gabriele Schackert, and Achim Temme
3213 Liver-Resident CD103+ Dendritic Cells Prime Antiviral CD8+ T Cells In Situ
Peter D. Krueger, Taeg S. Kim, Sun-Sang J. Sung, Thomas J. Braciale, and Young S. Hahn
INFECTIOUS DISEASE AND HOST RESPONSE
3223 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 Infection
Kelly M. Storek, Nina A. Gertsvolf, Maikke B. Ohlson, and Denise M. Monack
3246 Buprenorphine Decreases the CCL2-Mediated Chemotactic Response of Monocytes
Loreto 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 Gastritis
Pavle Matak, Myl
ene Heinis, Jacques R. R. Mathieu, Ross Corriden, Sylvain Cuvellier, St
e phanie Delga, R
e mi Mounier,
Alexandre Rouquette, Josette Raymond, Dominique Lamarque, Jean-Franc¸ois Emile, Victor Nizet, Eliette Touati,
and Carole Peyssonnaux
3267 Blimp-1, an Intrinsic Factor that Represses HIV-1 Proviral Transcription in Memory CD4+ T Cells
Katarzyna 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 against
Malaria during Pregnancy and Delivery Outcomes
Pilar 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
e valo-Herrera,
Carmen Fern
andez-Becerra, Hernando del Portillo, Chetan E. Chitnis, Peter M. Siba, Stephen Rogerson, Ivo Mueller,
Azucena Bardaj´i, Clara Men
e ndez, and Carlota Doban~o
INNATE IMMUNITY AND INFLAMMATION
3286 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 Autoimmune
Neuroinflammation
Amol 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 Molecular
and Pathophysiological Determinants of Complement Activity
Georgia 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 Monocytes
Alexander 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 Mediates
Phagocytosis via Hydrolysis of Ethanolamine Phospholipids
Julio M. Rubio, Juan P. Rodr´iguez, Luis Gil-de-G
omez, Carlos Guijas, Mar´ia A. Balboa, and Jesus
Balsinde
3340 Basal Cells Contribute to Innate Immunity of the Airway Epithelium through Production of the
Antimicrobial Protein RNase 7
Gimano D. Amatngalim, Yolanda van Wijck, Yvonne de Mooij-Eijk, Renate M. Verhoosel, Ju¨rgen Harder,
Annemarie N. Lekkerkerker, Richard A. J. Janssen, and Pieter S. Hiemstra
3351 WNT-Inflammasome Signaling Mediates NOD2-Induced Development of Acute Arthritis in Mice
Vikas Singh, Sahana Holla, Subbaraya G. Ramachandra, and Kithiganahalli Narayanaswamy Balaji
3361 Extracellular Vesicles Derived from Gram-Negative Bacteria, such as Escherichia coli, Induce Emphysema
Mainly via IL-17A–Mediated Neutrophilic Inflammation
You-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 Tumorigenesis
Tere 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 Receptors
without Eliciting Melanogenic Effects
Trinidad 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 Regeneration
Julien Gondin, Marine Th
e ret, Guillaume Duhamel, Katarina Pegan, Jacques R. R. Mathieu, Carole Peyssonnaux,
Sylvain Cuvellier, Claire Latroche, B
e n
e dicte Chazaud, David Bendahan, and R
e mi Mounier
3400 CXCL10 Triggers Early Microglial Activation in the Cuprizone Model
Tim Clarner, Katharina Janssen, Lara Nellessen, Martin Stangel, Thomas Skripuletz, Barbara Krauspe, Franz-Martin Hess,
Bernd Denecke, Clara Beutner, Bettina Linnartz-Gerlach, Harald Neumann, Luc Vallieres,
Sandra Amor, Kim Ohl,
Klaus Tenbrock, Cordian Beyer, and Markus Kipp
3414 Properdin Provides Protection from Citrobacter rodentium–Induced Intestinal Inflammation in a
C5a/IL-6–Dependent Manner
Umang Jain, Qi Cao, Nikhil A. Thomas, Trent M. Woodruff, Wilhelm J. Schwaeble, Cordula M. Stover,
and Andrew W. Stadnyk
MOLECULAR AND STRUCTURAL IMMUNOLOGY
3422 Noncanonical STAT3 Activation Regulates Excess TGF-b1 and Collagen I Expression in Muscle of
Stricturing Crohn’s Disease
Chao 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 Locus
Joaquin Zacar´ias-Cabeza, Mohamed Belhocine, Laurent Vanhille, Pierre Cauchy, Frederic Koch, Aleksandra Pekowska,
Romain Fenouil, Aur
e lie 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 Pathway
Ming-Xiao He and You-Wen He
TUMOR IMMUNOLOGY
3452 Differential Response of Myeloid-Derived Suppressor Cells to the Nonsteroidal Anti-Inflammatory Agent
Indomethacin in Tumor-Associated and Tumor-Free Microenvironments
Ada 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 Human
Mesenchymal Stem Cell Recruitment to Tumors
Sofia 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 Cells
and a Prognostic Factor for Survival in Lung Cancer Patients
Fayc¸al Djenidi, Julien Adam, A¨icha Goubar, Aur
e lie Durgeau, Guillaume Meurice, Vincent de Montpr
e ville,
Pierre Validire, Benjamin Besse, and Fathia Mami-Chouaib
3487 Specific Roles of Each TCR Hemichain in Generating Functional Chain-Centric TCR
Munehide 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 Neoantigen
H
e lo¨ise Flament, Ruby Alonso Ramirez, Virginie Pr
e mel, Nathalie T. Joncker, Alexandra Jacquet, Suzy Scholl,
and Olivier Lantz
NOVEL IMMUNOLOGICAL METHODS
3513 Predominant Development of Mature and Functional Human NK Cells in a Novel Human IL-2–Producing
Transgenic NOG Mouse
Ikumi Katano, Takeshi Takahashi, Ryoji Ito, Tsutomu Kamisako, Takuma Mizusawa, Yuyo Ka, Tomoyuki Ogura,
Hiroshi Suemizu, Yutaka Kawakami, and Mamoru Ito
CORRECTIONS
3526 Correction: Stat3 Activation Is Responsible for IL-6–Dependent T Cell Proliferation through Preventing
Apoptosis: Generation and Characterization of T Cell–Specific Stat3-Deficient Mice
Kiyoshi Takeda, Tsuneyasu Kaisho, Nobuaki Yoshida, Junji Takeda, Tadamitsu Kishimoto, and Shizuo Akira
3527 AUTHOR INDEX