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Citations to this article

Germinal center exclusion of autoreactive B cells is defective in human systemic lupus erythematosus
Amedeo Cappione III, … , Gregg Silverman, Iñaki Sanz
Amedeo Cappione III, … , Gregg Silverman, Iñaki Sanz
Published November 1, 2005
Citation Information: J Clin Invest. 2005;115(11):3205-3216. https://doi.org/10.1172/JCI24179.
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Research Article Autoimmunity Article has an altmetric score of 6

Germinal center exclusion of autoreactive B cells is defective in human systemic lupus erythematosus

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Abstract

Breach of B cell tolerance is central to the pathogenesis of systemic lupus erythematosus (SLE). However, how B cell tolerance is subverted in human SLE is poorly understood due to difficulties in identifying relevant autoreactive B cells and in obtaining lymphoid tissue. We have circumvented these limitations by using tonsil biopsies to study autoreactive B cells (9G4 B cells), whose regulation is abnormal in SLE. Here we show that 9G4 B cells are physiologically excluded during the early stages of the GC reaction before acquiring a centroblast phenotype. Furthermore, we provide evidence to indicate that an anergic response to B cell receptor stimulation may be responsible for such behavior. In contrast, in SLE, 9G4 B cells progressed unimpeded through this checkpoint, successfully participated in GC reactions, and expanded within the post-GC IgG memory and plasma cell compartments. The faulty regulation of 9G4 B cells was not shared by RA patients. To our knowledge, this work represents the first comparative analysis of the fate of a specific autoreactive human B cell population. The results identify a defective tolerance checkpoint that appears to be specific for human SLE.

Authors

Amedeo Cappione III, Jennifer H. Anolik, Aimee Pugh-Bernard, Jennifer Barnard, Paul Dutcher, Gregg Silverman, Iñaki Sanz

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Altered BCR and TLR signals promote enhanced positive selection of autoreactive transitional B cells in Wiskott-Aldrich syndrome
NS Kolhatkar, A Brahmandam, CD Thouvenel, S Becker-Herman, HM Jacobs, MA Schwartz, EJ Allenspach, S Khim, AK Panigrahi, ET Prak, AJ Thrasher, LD Notarangelo, F Candotti, TR Torgerson, I Sanz, DJ Rawlings
Journal of Experimental Medicine 2015
B Cells, Antibodies, and More
W Hoffman, FG Lakkis, G Chalasani
Clinical journal of the American Society of Nephrology : CJASN 2015
Defects in Germinal Center Selection in SLE
M Woods, YR Zou, A Davidson
Frontiers in immunology 2015
Circulating Follicular Helper-Like T Cells in Systemic Lupus Erythematosus: Association With Disease Activity: Circulating Tfh-Like Cells in SLE
JY Choi, JH Ho, SG Pasoto, V Bunin, ST Kim, S Carrasco, EF Borba, CR Gonçalves, PR Costa, EG Kallas, E Bonfa, J Craft
Arthritis & Rheumatology 2015
B Cell-Intrinsic CD84 and Ly108 Maintain Germinal Center B Cell Tolerance
EB Wong, C Soni, AY Chan, PP Domeier, Shwetank, T Abraham, N Limaye, TN Khan, MJ Elias, SB Chodisetti, EK Wakeland, ZS Rahman
Journal of immunology (Baltimore, Md. : 1950) 2015
Absence of surrogate light chain results in spontaneous autoreactive germinal centres expanding VH81X-expressing B cells
O Grimsholm, W Ren, AI Bernardi, H Chen, G Park, A Camponeschi, D Chen, B Bergmann, N Höök, S Andersson, A Strömberg, I Gjertsson, S Cardell, U Yrlid, AD Riva, IL Mårtensson
Nature Communications 2015
Roles of B Cell-Intrinsic TLR Signals in Systemic Lupus Erythematosus
K Ma, J Li, Y Fang, L Lu
International journal of molecular sciences 2015
Activation of TLR7 increases CCND3 expression via the downregulation of miR-15b in B cells of systemic lupus erythematosus
D Ren, F Liu, G Dong, M You, J Ji, Y Huang, Y Hou, H Fan
Cellular and Molecular Immunology 2015
Meta-analysis of shared genetic architecture across ten pediatric autoimmune diseases
YR Li, J Li, SD Zhao, JP Bradfield, FD Mentch, SM Maggadottir, C Hou, DJ Abrams, D Chang, F Gao, Y Guo, Z Wei, JJ Connolly, CJ Cardinale, M Bakay, JT Glessner, D Li, C Kao, KA Thomas, H Qiu, RM Chiavacci, CE Kim, F Wang, J Snyder, MD Richie, B Flatø, Ø Førre, LA Denson, SD Thompson, ML Becker, SL Guthery, A Latiano, E Perez, E Resnick, RK Russell, DC Wilson, MS Silverberg, V Annese, BA Lie, M Punaro, MC Dubinsky, DS Monos, C Strisciuglio, A Staiano, E Miele, S Kugathasan, JA Ellis, JE Munro, KE Sullivan, CA Wise, H Chapel, C Cunningham-Rundles, SF Grant, JS Orange, PM Sleiman, EM Behrens, AM Griffiths, J Satsangi, TH Finkel, A Keinan, ET Prak, C Polychronakos, RN Baldassano, H Li, BJ Keating, H Hakonarson
Nature Medicine 2015
Human embryonic stem cell-derived mesenchymal cells preserve kidney function and extend lifespan in NZB/W F1 mouse model of lupus nephritis
A Thiel, G Yavanian, MD Nastke, P Morales, NA Kouris, EA Kimbrel, R Lanza
Scientific Reports 2015
OX40/OX40L axis: not a friend in autoimmunity
H Ueno, P Blanco
Oncotarget 2015
Rationale for B cell targeting in SLE
I Sanz
Seminars in Immunopathology 2014
Chronic lymphocytic leukaemia: could immunological tolerance mechanisms be the origin of lymphoid neoplasms?
R García-Muñoz, L Llorente
Immunology 2014
Expression of the Inherently Autoreactive Idiotope 9G4 on Autoantibodies to Citrullinated Peptides and on Rheumatoid Factors in Patients with Early and Established Rheumatoid Arthritis
G Cambridge, RA Moura, T Santos, AA Khawaja, J Polido-Pereira, H Canhão, MJ Leandro, JE Fonseca, P Szodoray
PloS one 2014
Redemption of autoantibodies on anergic B cells by variable-region glycosylation and mutation away from self-reactivity
Z Sabouri, P Schofield, K Horikawa, E Spierings, D Kipling, KL Randall, D Langley, B Roome, R Vazquez-Lombardi, R Rouet, J Hermes, TD Chan, R Brink, DK Dunn-Walters, D Christ, CC Goodnow
Proceedings of the National Academy of Sciences 2014
Germinal Center B Cell Depletion Diminishes CD4+ Follicular T Helper Cells in Autoimmune Mice
I Yusuf, J Stern, TM McCaughtry, S Gallagher, H Sun, C Gao, T Tedder, G Carlesso, L Carter, R Herbst, Y Wang
PloS one 2014
Accumulation of Self-Reactive Naïve and Memory B Cell Reveals Sequential Defects in B Cell Tolerance Checkpoints in Sjögren’s Syndrome
E Corsiero, N Sutcliffe, C Pitzalis, M Bombardieri, J Reddy
PloS one 2014
B Cell-Intrinsic TLR7 Signaling Is Essential for the Development of Spontaneous Germinal Centers
C Soni, EB Wong, PP Domeier, TN Khan, T Satoh, S Akira, ZS Rahman
Journal of immunology (Baltimore, Md. : 1950) 2014
Fundamental roles of the innate-like repertoire of natural antibodies in immune homeostasis
J Vas, C Grönwall, GJ Silverman
Frontiers in immunology 2013
9G4+ autoantibodies are an important source of apoptotic cell reactivity associated with high levels of disease activity in systemic lupus erythematosus
SA Jenks, EM Palmer, EY Marin, L Hartson, AS Chida, C Richardson, I Sanz
Arthritis & Rheumatism 2013
Molecular basis of 9G4 B cell autoreactivity in human systemic lupus erythematosus
C Richardson, AS Chida, D Adlowitz, L Silver, E Fox, SA Jenks, E Palmer, Y Wang, J Heimburg-Molinaro, QZ Li, C Mohan, R Cummings, C Tipton, I Sanz
Journal of immunology (Baltimore, Md. : 1950) 2013
9G4+ antibodies isolated from HIV-infected patients neutralize HIV-1 and have distinct autoreactivity profiles
DC Alcéna, JJ Kobie, DA Kaminski, AF Rosenberg, JL Mattiacio, M Brewer, S Dewhurst, C Dykes, X Jin, MC Keefer, I Sanz
PloS one 2013
Protein Kinase Cβ Is Required for Lupus Development in Sle Mice
D Oleksyn, M Pulvino, J Zhao, R Misra, A Vosoughi, S Jenks, C Tipton, F Lund, G Schwartz, B Goldman, C Mohan, K Mehta, M Mehta, M Leitgets, I Sanz, L Chen
Arthritis & Rheumatism 2013
Contributions of B cells to lupus pathogenesis
A Sang, YY Zheng, L Morel
Molecular Immunology 2013
Neuropilin-1 expression characterizes T follicular helper (Tfh) cells activated during B cell differentiation in human secondary lymphoid organs
A Renand, P Milpied, J Rossignol, J Bruneau, F Lemonnier, M Dussiot, S Coulon, O Hermine
PloS one 2013
Rheumatoid factor B cell memory leads to rapid, switched antibody-forming cell responses
RA Sweet, JL Cullen, MJ Shlomchik
Journal of immunology (Baltimore, Md. : 1950) 2013
Development of autoantibodies due to regulator of G-protein signaling 13-induced delay in Germinal center B cell differentiation to plasmablasts: RGS13 Induces Germinal Center Program Extension
JH Wang, JS New, S Xie, PA Yang, Q Wu, J Li, B Luo, Y Ding, KM Druey, HC Hsu, JD Mountz
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Expansion of HIV-specific T follicular helper cells in chronic HIV infection
Madelene Lindqvist, Jan van Lunzen, Damien Soghoian, Bjorn Kuhl, Srinika Ranasinghe, Gregory Kranias, Michael Flanders, Sam Cutler, Naomi Yudanin, Matthias Muller, Isaiah Davis, Donna Farber, Philip Hartjen, Friedrich Haag, Galit Alter, Julian Schulze Zur Wiesch, Hendrik Streeck
Journal of Clinical Investigation 2012
Autoimmunity
A Perl
Autoimmunity 2012
Immunological aspects in chronic lymphocytic leukemia (CLL) development
R García-Muñoz, VR Galiacho, L Llorente
Annals of Hematology 2012
Serum from patients with SLE instructs monocytes to promote IgG and IgA plasmablast differentiation
H Joo, C Coquery, Y Xue, I Gayet, SR Dillon, M Punaro, G Zurawski, J Banchereau, V Pascual, S Oh
Journal of Experimental Medicine 2012
9G4 Autoreactivity Is Increased in HIV-Infected Patients and Correlates with HIV Broadly Neutralizing Serum Activity
JJ Kobie, DC Alcena, B Zheng, P Bryk, JL Mattiacio, M Brewer, C Labranche, FM Young, S Dewhurst, DC Montefiori, AF Rosenberg, C Feng, X Jin, MC Keefer, I Sanz
PloS one 2012
Antibody Repertoires in Humanized NOD-scid-IL2Rγnull Mice and Human B Cells Reveals Human-Like Diversification and Tolerance Checkpoints in the Mouse
GC Ippolito, KH Hoi, ST Reddy, SM Carroll, X Ge, T Rogosch, M Zemlin, LD Shultz, AD Ellington, CL Vandenberg, G Georgiou
PloS one 2012
Advances in human B cell phenotypic profiling
DA Kaminski, C Wei, Y Qian, AF Rosenberg, I Sanz
Frontiers in immunology 2012
Follicular helper T cells in immunity and systemic autoimmunity
JE Craft
Nature reviews. Rheumatology 2012
Taming lupus-a new understanding of pathogenesis is leading to clinical advances
Z Liu, A Davidson
Nature Medicine 2012
The lupus-prone NZM2410/NZW strain-derived Sle1b sublocus alters the germinal center checkpoint in female mice in a B cell-intrinsic manner
EB Wong, TN Khan, C Mohan, ZS Rahman
Journal of immunology (Baltimore, Md. : 1950) 2012
Regulation of Humoral Immunity by Complement
MC Carroll, DE Isenman
Immunity 2012
Treatment targets in systemic lupus erythematosus: biology and clinical perspective
V Marian, JH Anolik
Arthritis Research & Therapy 2012
The darker side of follicular helper T cells: from autoimmunity to immunodeficiency
S Shekhar, X Yang
Cellular and Molecular Immunology 2012
Resolve, revise, and relax: The 3 Rs of B cell repertoire adjustment
JL Scholz, MP Cancro
Immunology Letters 2012
T Cells That Promote B-Cell Maturation in Systemic Autoimmunity
JS Weinstein, SG Hernandez, J Craft
Immunological Reviews 2012
The pathogenesis of systemic lupus erythematosus-an update
J Choi, ST Kim, J Craft
Current Opinion in Immunology 2012
The XX sex chromosome complement in mice is associated with increased spontaneous lupus compared with XY
MV Sasidhar, N Itoh, SM Gold, GW Lawson, RR Voskuhl
Annals of the rheumatic diseases 2012
B Cell Tolerance and Positive Selection in Lupus
D Eilat, M Wabl
Journal of immunology (Baltimore, Md. : 1950) 2012
Naive antibody gene-segment frequencies are heritable and unaltered by chronic lymphocyte ablation
J Glanville, TC Kuo, HC Büdingen, L Guey, J Berka, PD Sundar, G Huerta, GR Mehta, JR Oksenberg, SL Hauser, DR Cox, A Rajpal, J Pons
Proceedings of the National Academy of Sciences 2011
Anergic Responses Characterize a Large Fraction of Human Autoreactive Naive B Cells Expressing Low Levels of Surface IgM
TD Quach, N Manjarrez-Orduno, DG Adlowitz, L Silver, H Yang, C Wei, EC Milner, I Sanz
Journal of immunology (Baltimore, Md. : 1950) 2011
Long-lived autoreactive plasma cells drive persistent autoimmune inflammation
F Hiepe, T Dörner, AE Hauser, BF Hoyer, H Mei, A Radbruch
Nature Reviews Rheumatology 2011
Mechanisms of B cell autoimmunity in SLE
T Dörner, C Giesecke, PE Lipsky
Arthritis Research & Therapy 2011
OMIP-003: phenotypic analysis of human memory B cells
C Wei, J Jung, I Sanz
Cytometry Part A 2011
Invariant NKT cells limit activation of autoreactive CD1d-positive B cells
F Wermeling, SM Lind, ED Jordö, SL Cardell, MC Karlsson
Journal of Experimental Medicine 2010
B-cell Biology and Related Therapies in Systemic Lupus Erythematosus
S Ahmed, JH Anolik
Rheumatic Disease Clinics of North America 2010
Complement receptor 2/CD21− human naive B cells contain mostly autoreactive unresponsive clones
I Isnardi, YS Ng, L Menard, G Meyers, D Saadoun, I Srdanovic, J Samuels, J Berman, JH Buckner, C Cunningham-Rundles, E Meffre
Blood 2010
Memory B cells from a subset of treatment naïve relapsing remitting multiple sclerosis patients elicit CD4+ T cell proliferation and IFN-γ production in response to MBP and MOG
CT Harp, S Ireland, LS Davis, G Remington, B Cassidy, PD Cravens, O Stuve, AE Lovett-Racke, TN Eagar, BM Greenberg, MK Racke, LG Cowell, NJ Karandikar, EM Frohman, NL Monson
European Journal of Immunology 2010
Systems biology of lupus: Mapping the impact of genomic and environmental factors on gene expression signatures, cellular signaling, metabolic pathways, hormonal and cytokine imbalance, and selecting targets for treatment
A Perl
Autoimmunity 2010
Signals that influence T follicular helper cell differentiation and function
MA Linterman, CG Vinuesa
Seminars in Immunopathology 2010
Decreased frequency and activated phenotype of blood CD27 IgD IgM B lymphocytes is a permanent abnormality in systemic lupus erythematosus patients
B Rodríguez-Bayona, A Ramos-Amaya, JJ Pérez-Venegas, C Rodríguez, JA Brieva
Arthritis Research & Therapy 2010
The Ubiquitin Modifying Enayme A20 Restricts B cell Survival and Prevents Autoimmunity
RM Tavares, EE Turer, CL Liu, R Advincula, P Scapini, L Rhee, J Barrera, CA Lowell, PJ Utz, BA Malynn, A Ma
Immunity 2010
Deletion of IgG-Switched Autoreactive B Cells and Defects in Fas lpr Lupus Mice
D Aït-Azzouzene, DH Kono, R Gonzalez-Quintial, LJ McHeyzer-Williams, M Lim, D Wickramarachchi, T Gerdes, AL Gavin, P Skog, MG McHeyzer-Williams, D Nemazee, AN Theofilopoulos
Journal of immunology (Baltimore, Md. : 1950) 2010
Altered B-cell homeostasis and excess BAFF in human chronic graft-versus-host disease
S Sarantopoulos, KE Stevenson, HT Kim, CS Cutler, NS Bhuiya, M Schowalter, VT Ho, EP Alyea, J Koreth, BR Blazar, RJ Soiffer, JH Antin, J Ritz
Blood 2009
B Cells and Immunological Tolerance
N Manjarrez-Orduño, TD Quách, I Sanz
Journal of Investigative Dermatology 2009
Insights into the heterogeneity of human B cells: diverse functions, roles in autoimmunity, and use as therapeutic targets
JH Anolik, RJ Looney, FE Lund, TD Randall, I Sanz
Immunologic Research 2009
B cells in autoimmunity
T Dörner, AM Jacobi, PE Lipsky
Arthritis Research & Therapy 2009
The role of B cells in lupus pathogenesis
E Nashi, YH Wang, B Diamond
The International Journal of Biochemistry & Cell Biology 2009
Follicular helper T cells are required for systemic autoimmunity
MA Linterman, RJ Rigby, RK Wong, D Yu, R Brink, JL Cannons, PL Schwartzberg, MC Cook, GD Walters, CG Vinuesa
Journal of Experimental Medicine 2009
TLR4 signaling augments B lymphocyte migration and overcomes the restriction that limits access to germinal center dark zones
IY Hwang, C Park, K Harrison, JH Kehrl
Journal of Experimental Medicine 2009
Anti-nuclear antibody reactivity in lupus may be partly hard-wired into the primary B-cell repertoire
S Chang, L Yang, YM Moon, YG Cho, SY Min, TJ Kim, YJ Kim, W Patrick, HY Kim, C Mohan
Molecular Immunology 2009
Molecular hallmarks of anti-chromatin antibodies associated with the lupus susceptibility locus, Sle1
Z Liang, S Chang, MS Youn, C Mohan
Molecular Immunology 2009
B cells and transplantation: an educational resource
TN Small, WH Robinson, DB Miklos
Biology of Blood and Marrow Transplantation 2009
The Lupus Susceptibility Locus Sle1 Breaches Peripheral B Cell Tolerance at the Antibody-Forming Cell and Germinal Center Checkpoints
R Vuyyuru, C Mohan, T Manser, ZS Rahman
Journal of immunology (Baltimore, Md. : 1950) 2009
Functional anergy in a subpopulation of naive B cells from healthy humans that express autoreactive immunoglobulin receptors
JA Duty, P Szodoray, NY Zheng, KA Koelsch, Q Zhang, M Swiatkowski, M Mathias, L Garman, C Helms, B Nakken, K Smith, AD Farris, PC Wilson
Journal of Experimental Medicine 2008
Phenotypic and functional heterogeneity of human memory B cells
I Sanz, C Wei, FE Lee, J Anolik
Seminars in Immunology 2008
How the study of children with rheumatic diseases identified interferon-alpha and interleukin-1 as novel therapeutic targets
V Pascual, F Allantaz, P Patel, AK Palucka, D Chaussabel, J Banchereau
Immunological Reviews 2008
Developments in the scientific understanding of lupus
SP Ardoin, DS Pisetsky
Arthritis Research & Therapy 2008
Role of B cells in systemic lupus erythematosus and rheumatoid arthritis
L Mandik-Nayak, N Ridge, M Fields, AY Park, J Erikson
Current Opinion in Immunology 2008
Interleukin-6 is responsible for aberrant B-cell receptor-mediated regulation of RAG expression in systemic lupus erythematosus
S Hillion, S Garaud, V Devauchelle, A Bordron, C Berthou, P Youinou, C Jamin
Immunology 2007
Autoreactivity in human IgG+ memory B cells
T Tiller, M Tsuiji, S Yurasov, K Velinzon, MC Nussenzweig, H Wardemann
Immunity 2007
Understanding B-cell tolerance through the use of immunoglobulin transgenic models
KR Kumar, C Mohan
Immunologic Research 2007

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