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CD1d-restricted autoreactive natural killer
(NK1.1+) T cells function as regulatory cells in various
disease conditions. Usingimproved tetramer tracking methodology, we
identified a NK1.1- thymic precursor and followed its
differentiation and emigrationto tissues by direct cell transfer and
in situ cell labeling studies.A major lineage expansion occurred
within the thymus after positiveselection and before NK receptor
expression. Surprisingly, cytokineanalysis of the developmental
intermediates between NK and NK+ stages
showed a T helper cell TH2 to TH1 conversion,
suggestingthat the regulatory functions of NK T cells may be
developmentallycontrolled. These findings characterize novel thymic
and postthymicdevelopmental pathways that expand autoreactive cells
and differentiatethem into regulatory cells.
1 Department of Molecular Biology, Princeton
University, Princeton, NJ 08544, USA.
2 Department
of Immunology, Scripps Research Institute, La Jolla, CA 92037, USA.
*
To whom correspondence should be addressed. E-mail:
abendelac{at}molbio.princeton.edu
Aberrant Selection and Function of Invariant NKT Cells in the Absence of AP-1 Transcription Factor Fra-2.
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Cutting Edge: The Chemokine Receptor CXCR3 Retains Invariant NK T Cells in the Thymus.
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Skin and Peripheral Lymph Node Invariant NKT Cells Are Mainly Retinoic Acid Receptor-Related Orphan Receptor {gamma}t+ and Respond Preferentially under Inflammatory Conditions.
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PNAS
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The Adaptor Molecule Signaling Lymphocytic Activation Molecule-Associated Protein (SAP) Regulates IFN-{gamma} and IL-4 Production in V{alpha}14 Transgenic NKT Cells via Effects on GATA-3 and T-bet Expression.
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PNAS
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Enhanced Early Expansion and Maturation of Semi-Invariant NK T Cells Inhibited Autoimmune Pathogenesis in Congenic Nonobese Diabetic Mice.
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J. Immunol.
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Congenic Analysis of the NKT Cell Control Gene Nkt2 Implicates the Peroxisomal Protein Pxmp4.
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Thymic Emigration: When and How T Cells Leave Home.
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PNAS
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181, 907-917
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FASEB J
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Innate-Like Effector Differentiation of Human Invariant NKT Cells Driven by IL-7.
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180, 4415-4424
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180, 2276-2283
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FASEB J
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J. Immunol.
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Blood
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From the Cover: Normal development and function of invariant natural killer T cells in mice with isoglobotrihexosylceramide (iGb3) deficiency.
S. Porubsky, A. O. Speak, B. Luckow, V. Cerundolo, F. M. Platt, and H.-J. Grone (2007)
PNAS
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Mouse TCR{alpha}beta+CD8{alpha}{alpha} Intraepithelial Lymphocytes Express Genes That Down-Regulate Their Antigen Reactivity and Suppress Immune Responses.
T. L. Denning, S. Granger, D. Mucida, R. Graddy, G. Leclercq, W. Zhang, K. Honey, J. P. Rasmussen, H. Cheroutre, A. Y. Rudensky, et al. (2007)
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Streptococcus agalactiae GAPDH Is a Virulence-Associated Immunomodulatory Protein.
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J. Immunol.
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Sensitivity of NK1.1-Negative NKT Cells to Transgenic BATF Defines a Role for Activator Protein-1 in the Expansion and Maturation of Immature NKT Cells in the Thymus.
A. J. Zullo, K. Benlagha, A. Bendelac, and E. J. Taparowsky (2007)
J. Immunol.
178, 58-66
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GATA-3 Regulates the Development and Function of Invariant NKT Cells.
P. J. Kim, S.-Y. Pai, M. Brigl, G. S. Besra, J. Gumperz, and I-C. Ho (2006)
J. Immunol.
177, 6650-6659
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Impaired selection of invariant natural killer T cells in diverse mouse models of glycosphingolipid lysosomal storage diseases.
S. D. Gadola, J. D. Silk, A. Jeans, P. A. Illarionov, M. Salio, G. S. Besra, R. Dwek, T. D. Butters, F. M. Platt, and V. Cerundolo (2006)
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203, 2293-2303
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Rapid Development of a Gamma Interferon-Secreting Glycolipid/CD1d-Specific V{alpha}14+ NK1.1- T-Cell Subset after Bacterial Infection..
M. Emoto, I. Yoshizawa, Y. Emoto, M. Miamoto, R. Hurwitz, and S. H. E. Kaufmann (2006)
Infect. Immun.
74, 5903-5913
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A unique lymphotoxin {alpha}beta-dependent pathway regulates thymic emigration of V{alpha}14 invariant natural killer T cells.
A. S. Franki, K. Van Beneden, P. Dewint, K. J. L. Hammond, S. Lambrecht, G. Leclercq, M. Kronenberg, D. Deforce, and D. Elewaut (2006)
PNAS
103, 9160-9165
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DOCK2 Is Required in T Cell Precursors for Development of V{alpha}14 NK T Cells..
Y. Kunisaki, Y. Tanaka, T. Sanui, A. Inayoshi, M. Noda, T. Nakayama, M. Harada, M. Taniguchi, T. Sasazuki, and Y. Fukui (2006)
J. Immunol.
176, 4640-4645
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Long-Term Retention of Mature NK1.1+ NKT Cells in the Thymus.
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J. Immunol.
176, 4059-4065
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T-bet concomitantly controls migration, survival, and effector functions during the development of V{alpha}14i NKT cells.
J. L. Matsuda, Q. Zhang, R. Ndonye, S. K. Richardson, A. R. Howell, and L. Gapin (2006)
Blood
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A Cell-Type Specific CD1d Expression Program Modulates Invariant NKT Cell Development and Function.
M. I. Zimmer, A. Colmone, K. Felio, H. Xu, A. Ma, and C.-R. Wang (2006)
J. Immunol.
176, 1421-1430
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Targeted Expression of Human CD1d in Transgenic Mice Reveals Independent Roles for Thymocytes and Thymic APCs in Positive and Negative Selection of V{alpha}14i NKT Cells.
J. Schumann, P. Pittoni, E. Tonti, H. R. MacDonald, P. Dellabona, and G. Casorati (2005)
J. Immunol.
175, 7303-7310
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CD1d-Independent Developmental Acquisition of Prompt IL-4 Gene Inducibility in Thymus CD161(NK1)-CD44lowCD4+CD8- T Cells Is Associated with Complementarity Determining Region 3-Diverse and Biased V{beta}2/V{beta}7/V{beta}8/V{alpha}3.2 T Cell Receptor Usage.
Differential antitumor immunity mediated by NKT cell subsets in vivo.
N. Y. Crowe, J. M. Coquet, S. P. Berzins, K. Kyparissoudis, R. Keating, D. G. Pellicci, Y. Hayakawa, D. I. Godfrey, and M. J. Smyth (2005)
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202, 1279-1288
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The Influence of CD1d in Postselection NKT Cell Maturation and Homeostasis.
F. W. McNab, S. P. Berzins, D. G. Pellicci, K. Kyparissoudis, K. Field, M. J. Smyth, and D. I. Godfrey (2005)
J. Immunol.
175, 3762-3768
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Characterization of the early stages of thymic NKT cell development.
K. Benlagha, D. G. Wei, J. Veiga, L. Teyton, and A. Bendelac (2005)
J. Exp. Med.
202, 485-492
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D. G. Wei, H. Lee, S.-H. Park, L. Beaudoin, L. Teyton, A. Lehuen, and A. Bendelac (2005)
J. Exp. Med.
202, 239-248
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Expansion and Hyperactivity of CD1d-Restricted NKT Cells during the Progression of Systemic Lupus Erythematosus in (New Zealand Black x New Zealand White)F1 Mice.
C. Forestier, A. Molano, J. S. Im, Y. Dutronc, B. Diamond, A. Davidson, P. A. Illarionov, G. S. Besra, and S. A. Porcelli (2005)
J. Immunol.
175, 763-770
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Invariant V{alpha}14+ NKT Cells Participate in the Early Response to Enteric Listeria monocytogenes Infection.
T. Ranson, S. Bregenholt, A. Lehuen, O. Gaillot, M. C. Leite-de-Moraes, A. Herbelin, P. Berche, and J. P. Di Santo (2005)
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175, 1137-1144
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Commitment toward the natural T (iNKT) cell lineage occurs at the CD4+8+ stage of thymic ontogeny.
J. S. Bezbradica, T. Hill, A. K. Stanic, L. Van Kaer, and S. Joyce (2005)
PNAS
102, 5114-5119
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Defective NKT cell development in mice and humans lacking the adapter SAP, the X-linked lymphoproliferative syndrome gene product.
B. Pasquier, L. Yin, M.-C. Fondaneche, F. Relouzat, C. Bloch-Queyrat, N. Lambert, A. Fischer, G. de Saint-Basile, and S. Latour (2005)
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201, 695-701
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Modulation of CD1d-restricted NKT cell responses by using N-acyl variants of {alpha}-galactosylceramides.
K. O. A. Yu, J. S. Im, A. Molano, Y. Dutronc, P. A. Illarionov, C. Forestier, N. Fujiwara, I. Arias, S. Miyake, T. Yamamura, et al. (2005)
PNAS
102, 3383-3388
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The Human CD1-Restricted T Cell Repertoire Is Limited to Cross-Reactive Antigens: Implications for Host Responses against Immunologically Related Pathogens.
P. A. Sieling, J. B. Torrelles, S. Stenger, W. Chung, A. E. Burdick, T. H. Rea, P. J. Brennan, J. T. Belisle, S. A. Porcelli, and R. L. Modlin (2005)
J. Immunol.
174, 2637-2644
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The Fourth Way? Harnessing Aggressive Tendencies in the Thymus.
T. A. Baldwin, K. A. Hogquist, and S. C. Jameson (2004)
J. Immunol.
173, 6515-6520
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Increase in Hepatic NKT Cells in Leukocyte Cell-Derived Chemotaxin 2-Deficient Mice Contributes to Severe Concanavalin A-Induced Hepatitis.
T. Saito, A. Okumura, H. Watanabe, M. Asano, A. Ishida-Okawara, J. Sakagami, K. Sudo, Y. Hatano-Yokoe, J. S. Bezbradica, S. Joyce, et al. (2004)
J. Immunol.
173, 579-585
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Restoration of NK T Cell Development in fyn-Mutant Mice by a TCR Reveals a Requirement for Fyn During Early NK T Cell Ontogeny.
P. Gadue, L. Yin, S. Jain, and P. L. Stein (2004)
J. Immunol.
172, 6093-6100
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Development of innate CD4+ {alpha}-chain variable gene segment 24 (V{alpha}24) natural killer T cells in the early human fetal thymus is regulated by IL-7.
J. K. Sandberg, C. A. Stoddart, F. Brilot, K. A. Jordan, and D. F. Nixon (2004)
PNAS
101, 7058-7063
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Distinct cell types control lymphoid subset development by means of IL-15 and IL-15 receptor {alpha} expression.
K. S. Schluns, E. C. Nowak, A. Cabrera-Hernandez, L. Puddington, L. Lefrancois, and H. L. Aguila (2004)
PNAS
101, 5616-5621
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NF-{kappa}B Controls Cell Fate Specification, Survival, and Molecular Differentiation of Immunoregulatory Natural T Lymphocytes.
A. K. Stanic, J. S. Bezbradica, J.-J. Park, N. Matsuki, A. L. Mora, L. Van Kaer, M. R. Boothby, and S. Joyce (2004)
J. Immunol.
172, 2265-2273
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Differential regulation of NK cell proliferation by type I and type II IFN.
Control of NKT Cell Differentiation by Tissue-Specific Microenvironments.
Y. Yang, A. Ueno, M. Bao, Z. Wang, J. S. Im, S. Porcelli, and J.-W. Yoon (2003)
J. Immunol.
171, 5913-5920
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Glycolipid Antigen Drives Rapid Expansion and Sustained Cytokine Production by NK T Cells.
N. Y. Crowe, A. P. Uldrich, K. Kyparissoudis, K. J. L. Hammond, Y. Hayakawa, S. Sidobre, R. Keating, M. Kronenberg, M. J. Smyth, and D. I. Godfrey (2003)
J. Immunol.
171, 4020-4027
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T Cell Development in Mice Expressing CD1d Directed by a Classical MHC Class II Promoter.
C. Forestier, S.-H. Park, D. Wei, K. Benlagha, L. Teyton, and A. Bendelac (2003)
J. Immunol.
171, 4096-4104
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Repeated {alpha}-Galactosylceramide Administration Results in Expansion of NK T Cells and Alleviates Inflammatory Dermatitis in MRL-lpr/lpr Mice.
J.-Q. Yang, V. Saxena, H. Xu, L. Van Kaer, C.-R. Wang, and R. R. Singh (2003)
J. Immunol.
171, 4439-4446
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Constitutive Cytokine mRNAs Mark Natural Killer (NK) and NK T Cells Poised for Rapid Effector Function.
D. B. Stetson, M. Mohrs, R. L. Reinhardt, J. L. Baron, Z.-E. Wang, L. Gapin, M. Kronenberg, and R. M. Locksley (2003)
J. Exp. Med.
198, 1069-1076
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The response of natural killer T cells to glycolipid antigens is characterized by surface receptor down-modulation and expansion.
M. T. Wilson, C. Johansson, D. Olivares-Villagomez, A. K. Singh, A. K. Stanic, C.-R. Wang, S. Joyce, M. J. Wick, and L. Van Kaer (2003)
PNAS
100, 10913-10918
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Differential Chemokine Responses and Homing Patterns of Murine TCR{alpha}{beta} NKT Cell Subsets.
B. Johnston, C. H. Kim, D. Soler, M. Emoto, and E. C. Butcher (2003)
J. Immunol.
171, 2960-2969
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Most IL-4-Producing {gamma}{delta} Thymocytes of Adult Mice Originate from Fetal Precursors.
K. Grigoriadou, L. Boucontet, and P. Pereira (2003)
J. Immunol.
171, 2413-2420
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An Anti-Inflammatory Role for V{alpha}14 NK T cells in Mycobacterium bovis Bacillus Calmette-Guerin-Infected Mice.
F. Dieli, M. Taniguchi, M. Kronenberg, S. Sidobre, J. Ivanyi, L. Fattorini, E. Iona, G. Orefici, G. De Leo, D. Russo, et al. (2003)
J. Immunol.
171, 1961-1968
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Differential Requirement for Rel/Nuclear Factor {kappa}B Family Members in Natural Killer T Cell Development.
V. Sivakumar, K. J.L. Hammond, N. Howells, K. Pfeffer, and F. Weih (2003)
J. Exp. Med.
197, 1613-1621
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NIK-dependent RelB Activation Defines a Unique Signaling Pathway for the Development of V{alpha}14i NKT Cells.
D. Elewaut, R. B. Shaikh, K. J. L. Hammond, H. De Winter, A. J. Leishman, S. Sidobre, O. Turovskaya, T. I. Prigozy, L. Ma, T. A. Banks, et al. (2003)
J. Exp. Med.
197, 1623-1633
|Abstract »|Full Text »|PDF »
CD1d-expressing Dendritic Cells but Not Thymic Epithelial Cells Can Mediate Negative Selection of NKT Cells.
T. Chun, M. J. Page, L. Gapin, J. L. Matsuda, H. Xu, H. Nguyen, H.-S. Kang, A. K. Stanic, S. Joyce, W. A. Koltun, et al. (2003)
J. Exp. Med.
197, 907-918
|Abstract »|Full Text »|PDF »
Ligand-dependent Inhibition of CD1d-restricted NKT Cell Development in Mice Transgenic for the Activating Receptor Ly49D.
R. B. Voyle, F. Beermann, R. K. Lees, J. Schumann, J. Zimmer, W. Held, and H. R. MacDonald (2003)
J. Exp. Med.
197, 919-925
|Abstract »|Full Text »|PDF »
Human NKT Cells Express Granulysin and Exhibit Antimycobacterial Activity.
J. L. Gansert, V. Kiebler, M. Engele, F. Wittke, M. Rollinghoff, A. M. Krensky, S. A. Porcelli, R. L. Modlin, and S. Stenger (2003)
J. Immunol.
170, 3154-3161
|Abstract »|Full Text »|PDF »
IL-15 availability conditions homeostasis of peripheral natural killer T cells.
T. Ranson, C. A. J. Vosshenrich, E. Corcuff, O. Richard, V. Laloux, A. Lehuen, and J. P. Di Santo (2003)
PNAS
100, 2663-2668
|Abstract »|Full Text »|PDF »
Human Invariant V{alpha}24-J{alpha}Q TCR Supports the Development of CD1d-Dependent NK1.1+ and NK1.1- T Cells in Transgenic Mice.
M. Capone, D. Cantarella, J. Schumann, O. V. Naidenko, C. Garavaglia, F. Beermann, M. Kronenberg, P. Dellabona, H. R. MacDonald, and G. Casorati (2003)
J. Immunol.
170, 2390-2398
|Abstract »|Full Text »|PDF »
BATF Transgenic Mice Reveal a Role for Activator Protein-1 in NKT Cell Development.
K. L. Williams, A. J. Zullo, M. H. Kaplan, R. R. Brutkiewicz, C. D. Deppmann, C. Vinson, and E. J. Taparowsky (2003)
J. Immunol.
170, 2417-2426
|Abstract »|Full Text »|PDF »
Extrathymic T Cell Lymphopoiesis: Ontogeny and Contribution to Gut Intraepithelial Lymphocytes in Athymic and Euthymic Mice.
D. Guy-Grand, O. Azogui, S. Celli, S. Darche, M. C. Nussenzweig, P. Kourilsky, and P. Vassalli (2003)
J. Exp. Med.
197, 333-341
|Abstract »|Full Text »|PDF »
The Contribution of NKT Cells, NK Cells, and Other {gamma}-Chain-Dependent Non-T Non-B Cells to IL-12-Mediated Rejection of Tumors.
S.-H. Park, T. Kyin, A. Bendelac, and C. Carnaud (2003)
J. Immunol.
170, 1197-1201
|Abstract »|Full Text »|PDF »
TCR{gamma}{delta}+ and CD161+ Thymocytes Express HIV-1 in the SCID-hu Mouse, Potentially Contributing to Immune Dysfunction in HIV Infection.
K. B. Gurney, O. O. Yang, S. B. Wilson, and C. H. Uittenbogaart (2002)
J. Immunol.
169, 5338-5346
|Abstract »|Full Text »|PDF »
NK T Cell Precursors Exhibit Differential Cytokine Regulation and Require Itk for Efficient Maturation.
and NK+ stages
showed a T helper cell TH2 to TH1 conversion,
suggesting that the regulatory functions of NK T cells may be
developmentally controlled. These findings characterize novel thymic
and postthymic developmental pathways that expand autoreactive cells
and differentiate them into regulatory cells.
