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Science 29 May 1998:
Vol. 280. no. 5368, pp. 1432 - 1435
DOI: 10.1126/science.280.5368.1432
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Reports

Impairment of Mycobacterial Immunity in Human Interleukin-12 Receptor Deficiency

Frédéric Altare, Anne Durandy, David Lammas, Jean-François Emile, Salma Lamhamedi, Françoise Le Deist, Pam Drysdale, Emmanuelle Jouanguy, Rainer Döffinger, Françoise Bernaudin, Olle Jeppsson, Jared A. Gollob, Edgar Meinl, Antony W. Segal, Alain Fischer, Dinakantha Kumararatne, Jean-Laurent Casanova *

In humans, interferon gamma  (IFN-gamma ) receptor deficiency leads to a predisposition to mycobacterial infections and impairs the formation of mature granulomas. Interleukin-12 (IL-12) receptor deficiency was found in otherwise healthy individuals with mycobacterial infections. Mature granulomas were seen, surrounded by T cells and centered with epithelioid and multinucleated giant cells, yet reduced IFN-gamma concentrations were found to be secreted by activated natural killer and T cells. Thus, IL-12-dependent IFN-gamma secretion in humans seems essential in the control of mycobacterial infections, despite the formation of mature granulomas due to IL-12-independent IFN-gamma secretion.

F. Altare, A. Durandy, S. Lamhamedi, F. Le Deist, E. Jouanguy, R. Döffinger, INSERM U429, Hôpital Necker-Enfants Malades, Paris 75015, France.
D. Lammas, P. Drysdale, D. Kumararatne, Department of Immunology, University of Birmingham Medical School, Birmingham B15 2TT, UK.
J.-F. Emile, Service d'Anatomo-Pathologie, Hôpital Paul Brousse, Villejuif 94804, France.
F. Bernaudin, Service de Pédiatrie, Centre Hospitalier Intercommunal, Créteil 94010, France.
O. Jeppsson, Department of Pediatrics, University Hospital, Norsborg 145 01, Sweden.
J. A. Gollob, Dana-Farber Cancer Institute, Boston, MA 02115, USA.
E. Meinl, University of Erlangen-Nürnberg, Erlangen 91054, Germany.
A. W. Segal, Department of Medicine, University College, London WC1 E6JJ, UK.
A. Fischer and J.-L. Casanova, INSERM U429, Hôpital Necker-Enfants Malades, Paris 75015, France, and Unité d'Immunologie et d'Hématologie Pédiatriques, Hôpital Necker-Enfants Malades, Paris 75015, France.
*   To whom correspondence should be addressed. E-mail: casanova{at}ceylan.necker.fr

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Bacillus Calmette-Guerin sepsis: shift of an intended local toward a detrimental systemic cytotoxic immune response.
S. Zeerleder, C. E. Hack, C. Caliezi, R. Hebeisen, and W. A. Wuillemin (2001)
Blood 98, 890-891
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A Role for IL-12 Receptor Expression and Signal Transduction in Host Defense in Leprosy.
J. Kim, K. Uyemura, M. K. Van Dyke, A. J. Legaspi, T. H. Rea, K. Shuai, and R. L. Modlin (2001)
J. Immunol. 167, 779-786
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Impairment of Mycobacterial But Not Viral Immunity by a Germline Human STAT1 Mutation.
S. Dupuis, C. Dargemont, C. Fieschi, N. Thomassin, S. Rosenzweig, J. Harris, S. M. Holland, R. D. Schreiber, and J.-L. Casanova (2001)
Science 293, 300-303
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Enhanced Protection Against Fatal Mycobacterial Infection in SCID Beige Mice by Reshaping Innate Immunity with IFN-{{gamma}} Transgene.
Z. Xing, A. Zganiacz, J. Wang, and S. K. Sharma (2001)
J. Immunol. 167, 375-383
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Mannosylated Lipoarabinomannans Inhibit IL-12 Production by Human Dendritic Cells: Evidence for a Negative Signal Delivered Through the Mannose Receptor.
J. Nigou, C. Zelle-Rieser, M. Gilleron, M. Thurnher, and G. Puzo (2001)
J. Immunol. 166, 7477-7485
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Culture at High Density Improves the Ability of Human Macrophages to Control Mycobacterial Growth.
N. Boechat, F. Bouchonnet, M. Bonay, A. Grodet, V. Pelicic, B. Gicquel, and A. J. Hance (2001)
J. Immunol. 166, 6203-6211
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Interleukin-12 as successful adjuvant in tuberculosis treatment.
U. Greinert, M. Ernst, M. Schlaak, and P. Entzian (2001)
Eur. Respir. J. 17, 1049-1051
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A Heritable Defect in IL-12 Signaling in B10.Q/J Mice. I. In Vitro Analysis.
R. Ortmann, R. Smeltz, G. Yap, A. Sher, and E. M. Shevach (2001)
J. Immunol. 166, 5712-5719
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A Heritable Defect in IL-12 Signaling in B10.Q/J Mice. II. Effect on Acute Resistance to Toxoplasma gondii and Rescue by IL-18 Treatment.
G. S. Yap, R. Ortmann, E. Shevach, and A. Sher (2001)
J. Immunol. 166, 5720-5725
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Missense mutation of the interleukin-12 receptor {beta}1 chain-encoding gene is associated with impaired immunity against Mycobacterium avium complex infection.
T. Sakai, M. Matsuoka, M. Aoki, K. Nosaka, and H. Mitsuya (2001)
Blood 97, 2688-2694
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Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha /beta.
C. Manca, L. Tsenova, A. Bergtold, S. Freeman, M. Tovey, J. M. Musser, C. E. Barry III, V. H. Freedman, and G. Kaplan (2001)
PNAS
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Genetics of Susceptibility to Infectious Diseases: Tuberculosis and Leprosy as Examples.
S. Marquet and E. Schurr (2001)
Drug Metab. Dispos. 29, 479-483
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Gamma Interferon-Producing CD4+ T Lymphocytes in the Lung Correlate with Resistance to Infection with Mycobacterium tuberculosis.
A. A. Chackerian, T. V. Perera, and S. M. Behar (2001)
Infect. Immun. 69, 2666-2674
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High Levels of Interferon Gamma in the Plasma of Children With Complete Interferon Gamma Receptor Deficiency.
C. Fieschi, S. Dupuis, C. Picard, C. I. E. Smith, S. M. Holland, and J.-L. Casanova (2001)
Pediatrics 107, e48
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M. tuberculosis: immunology and vaccination.
G.A.W. Rook, G. Seah, and A. Ustianowski (2001)
Eur. Respir. J. 17, 537-557
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Factors Influencing Numbers of Mycobacterium avium, Mycobacterium intracellulare, and Other Mycobacteria in Drinking Water Distribution Systems.
J. O. Falkinham III, C. D. Norton, and M. W. LeChevallier (2001)
Appl. Envir. Microbiol. 67, 1225-1231
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Non-Major Histocompatibility Complex Control of Antibody Isotype and Th1 versus Th2 Cytokines during Experimental Infection of Mice with Mycobacterium avium.
V. Nagabhushanam and C. Cheers (2001)
Infect. Immun. 69, 1708-1713
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Contribution of Th1 and Th2 Cells to Protection and Pathology in Experimental Models of Granulomatous Lung Disease.
A. Wangoo, T. Sparer, I. N. Brown, V. A. Snewin, R. Janssen, J. Thole, H. T. Cook, R. J. Shaw, and D. B. Young (2001)
J. Immunol. 166, 3432-3439
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Interleukin 12 P40 Production by Barrier Epithelial Cells during Airway Inflammation.
M. J. Walter, N. Kajiwara, P. Karanja, M. Castro, and M. J. Holtzman (2001)
J. Exp. Med. 193, 339-352
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A Point Mutation in a Domain of Gamma Interferon Receptor 1 Provokes Severe Immunodeficiency.
L. M. Allende, A. Lopez-Goyanes, E. Paz-Artal, A. Corell, M. A. Garcia-Perez, P. Varela, A. Scarpellini, S. Negreira, E. Palenque, and A. Arnaiz-Villena (2001)
Clin. Vaccine Immunol. 8, 133-137
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Stat4 Regulates Multiple Components of IFN-{gamma}-Inducing Signaling Pathways.
V. A. Lawless, S. Zhang, O. N. Ozes, H. A. Bruns, I. Oldham, T. Hoey, M. J. Grusby, and M. H. Kaplan (2000)
J. Immunol. 165, 6803-6808
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Immunodeficiency Diseases Caused by Defects in Phagocytes.
J. A. Lekstrom-Himes and J. I. Gallin (2000)
N. Engl. J. Med. 343, 1703-1714
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Interleukin-18 (IL-18) Enhances Innate IL-12-Mediated Resistance to Toxoplasma gondii.
G. Cai, R. Kastelein, and C. A. Hunter (2000)
Infect. Immun. 68, 6932-6938
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The Sympathetic Nerve---An Integrative Interface between Two Supersystems: The Brain and the Immune System.
I. J. Elenkov, R. L. Wilder, G. P. Chrousos, and E. S. Vizi (2000)
Pharmacol. Rev. 52, 595-638
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IL-12 Receptor {beta}2 (IL-12R{beta}2)-Deficient Mice Are Defective in IL-12-Mediated Signaling Despite the Presence of High Affinity IL-12 Binding Sites.
C.-y. Wu, X. Wang, M. Gadina, J. J. O'Shea, D. H. Presky, and J. Magram (2000)
J. Immunol. 165, 6221-6228
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Comparative Analysis of T Lymphocytes Recovered from the Lungs of Mice Genetically Susceptible, Resistant, and Hyperresistant to Mycobacterium tuberculosis-Triggered Disease.
I. V. Lyadova, E. B. Eruslanov, S. V. Khaidukov, V. V. Yeremeev, K. B. Majorov, A. V. Pichugin, B. V. Nikonenko, T. K. Kondratieva, and A. S. Apt (2000)
J. Immunol. 165, 5921-5931
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Adenosine inhibits IL-12 and TNF-{alpha} production via adenosine A2a receptor-dependent and independent mechanisms.
G. HASKÓ, D. G. KUHEL, J.-F. CHEN, M. A. SCHWARZSCHILD, E. A. DEITCH, J. G. MABLEY, A. MARTON, and C. SZABÓ (2000)
FASEB J 14, 2065-2074
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