CD4+ T Cell Tolerance to Parenchymal Self-Antigens Requires Presentation by Bone Marrow-derived Antigen-presenting Cells

doi:10.1084/jem.187.10.1555

This Article

	Full Text
	Full Text (PDF, 130K)
	PPT slides of all figures
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JEM
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Adler, A. J.
	Articles by Pardoll, D. M.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Adler, A. J.
	Articles by Pardoll, D. M.


Social Bookmarking

	What's this?

J. Exp. Med., Volume 187, Number 10, May 18, 1998 1555-1564

CD4⁺ T Cell Tolerance to Parenchymal Self-Antigens Requires Presentation by Bone Marrow-derived Antigen-presenting Cells

By Adam J. Adler,^* David W. Marsh,^* Gregory S. Yochum,^* James L. Guzzo,^* Ankesh Nigam, William G. Nelson,^* and Drew M. Pardoll^*

From the ^* Department of Oncology and the Department of Surgery, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205

T cell tolerance to parenchymal self-antigens is thought to be induced by encounter of the T cell with its cognate peptide-majorhistocompatibility complex (MHC) ligand expressed on the parenchymalcell, which lacks appropriate costimulatory function. We haveused a model system in which naive T cell receptor (TCR) transgenichemagglutinin (HA)-specific CD4⁺ T cells are adoptively transferred into mice expressing HA asa self-antigen on parenchymal cells. After transfer, HA-specificT cells develop a phenotype indicative of TCR engagement and arerendered functionally tolerant. However, T cell tolerance is notinduced by peptide-MHC complexes expressed on parenchymal cells.Rather, tolerance induction requires that HA is presented by bonemarrow (BM)-derived cells. These results indicate that toleranceinduction to parenchymal self-antigens requires transfer to aBM-derived antigen-presenting cell that presents it to T cellsin a tolerogenic fashion.

Key words: peripheral tolerance; CD4⁺ T cells; antigen-presenting cells; adoptive T cell transfer; transgenic mice

Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

This article has been cited by other articles:

Grosso, J. F., Goldberg, M. V., Getnet, D., Bruno, T. C., Yen, H.-R., Pyle, K. J., Hipkiss, E., Vignali, D. A. A., Pardoll, D. M., Drake, C. G. (2009). Functionally Distinct LAG-3 and PD-1 Subsets on Activated and Chronically Stimulated CD8 T Cells. J. Immunol. 182: 6659-6669 [Abstract] [Full Text]
Getnet, D., Maris, C. H., Hipkiss, E. L., Grosso, J. F., Harris, T. J., Yen, H.-R., Bruno, T. C., Wada, S., Adler, A., Georgantas, R. W., Jie, C., Goldberg, M. V., Pardoll, D. M., Drake, C. G. (2009). Tumor Recognition and Self-Recognition Induce Distinct Transcriptional Profiles in Antigen-Specific CD4 T Cells. J. Immunol. 182: 4675-4685 [Abstract] [Full Text]
Solvason, N., Lou, Y.-P., Peters, W., Evans, E., Martinez, J., Ramirez, U., Ocampo, A., Yun, R., Ahmad, S., Liu, E., Yu, L., Eisenbarth, G., Leviten, M., Steinman, L., Garren, H. (2008). Improved Efficacy of a Tolerizing DNA Vaccine for Reversal of Hyperglycemia through Enhancement of Gene Expression and Localization to Intracellular Sites. J. Immunol. 181: 8298-8307 [Abstract] [Full Text]
Le Saout, C., Mennechet, S., Taylor, N., Hernandez, J. (2008). Memory-like CD8+ and CD4+ T cells cooperate to break peripheral tolerance under lymphopenic conditions. Proc. Natl. Acad. Sci. USA 105: 19414-19419 [Abstract] [Full Text]
Martin-Fontecha, A., Baumjohann, D., Guarda, G., Reboldi, A., Hons, M., Lanzavecchia, A., Sallusto, F. (2008). CD40L+ CD4+ memory T cells migrate in a CD62P-dependent fashion into reactive lymph nodes and license dendritic cells for T cell priming. JEM 205: 2561-2574 [Abstract] [Full Text]
Bos, R., van Duikeren, S., Morreau, H., Franken, K., Schumacher, T. N.M., Haanen, J. B., van der Burg, S. H., Melief, C. J.M., Offringa, R. (2008). Balancing between Antitumor Efficacy and Autoimmune Pathology in T-Cell-Mediated Targeting of Carcinoembryonic Antigen. Cancer Res. 68: 8446-8455 [Abstract] [Full Text]
Turner, M. J., Jellison, E. R., Lingenheld, E. G., Puddington, L., Lefrancois, L. (2008). Avidity maturation of memory CD8 T cells is limited by self-antigen expression. JEM 205: 1859-1868 [Abstract] [Full Text]
Cools, N., Ponsaerts, P., Van Tendeloo, V. F. I., Berneman, Z. N. (2007). Balancing between immunity and tolerance: an interplay between dendritic cells, regulatory T cells, and effector T cells. J. Leukoc. Biol. 82: 1365-1374 [Abstract] [Full Text]
Long, M., Slaiby, A. M., Wu, S., Hagymasi, A. T., Mihalyo, M. A., Bandyopadhyay, S., Vella, A. T., Adler, A. J. (2007). Histone Acetylation at the Ifng Promoter in Tolerized CD4 Cells Is Associated with Increased IFN-{gamma} Expression during Subsequent Immunization to the Same Antigen. J. Immunol. 179: 5669-5677 [Abstract] [Full Text]
Hagymasi, A. T., Slaiby, A. M., Mihalyo, M. A., Qui, H. Z., Zammit, D. J., Lefrancois, L., Adler, A. J. (2007). Steady State Dendritic Cells Present Parenchymal Self-Antigen and Contribute to, but Are Not Essential for, Tolerization of Naive and Th1 Effector CD4 Cells. J. Immunol. 179: 1524-1531 [Abstract] [Full Text]
Goldberg, M. V., Maris, C. H., Hipkiss, E. L., Flies, A. S., Zhen, L., Tuder, R. M., Grosso, J. F., Harris, T. J., Getnet, D., Whartenby, K. A., Brockstedt, D. G., Dubensky, T. W. Jr, Chen, L., Pardoll, D. M., Drake, C. G. (2007). Role of PD-1 and its ligand, B7-H1, in early fate decisions of CD8 T cells. Blood 110: 186-192 [Abstract] [Full Text]
Skoberne, M., Somersan, S., Almodovar, W., Truong, T., Petrova, K., Henson, P. M., Bhardwaj, N. (2006). The apoptotic-cell receptor CR3, but not {alpha}vbeta5, is a regulator of human dendritic-cell immunostimulatory function. Blood 108: 947-955 [Abstract] [Full Text]
Horna, P., Cuenca, A., Cheng, F., Brayer, J., Wang, H.-W., Borrello, I., Levitsky, H., Sotomayor, E. M. (2006). In vivo disruption of tolerogenic cross-presentation mechanisms uncovers an effective T-cell activation by B-cell lymphomas leading to antitumor immunity. Blood 107: 2871-2878 [Abstract] [Full Text]
Long, M., Slaiby, A. M., Hagymasi, A. T., Mihalyo, M. A., Lichtler, A. C., Reiner, S. L., Adler, A. J. (2006). T-bet Down-Modulation in Tolerized Th1 Effector CD4 Cells Confers a TCR-Distal Signaling Defect That Selectively Impairs IFN-{gamma} Expression. J. Immunol. 176: 1036-1045 [Abstract] [Full Text]
Huang, X., Zhu, J., Yang, Y. (2005). Protection against Autoimmunity in Nonlymphopenic Hosts by CD4+CD25+ Regulatory T Cells Is Antigen-Specific and Requires IL-10 and TGF-{beta}. J. Immunol. 175: 4283-4291 [Abstract] [Full Text]
Tan, J. K. H., O'Neill, H. C. (2005). Maturation requirements for dendritic cells in T cell stimulation leading to tolerance versus immunity. J. Leukoc. Biol. 78: 319-324 [Abstract] [Full Text]
Lin, Y.-L., Liang, Y.-C., Lee, S.-S., Chiang, B.-L. (2005). Polysaccharide purified from Ganoderma lucidum induced activation and maturation of human monocyte-derived dendritic cells by the NF-{kappa}B and p38 mitogen-activated protein kinase pathways. J. Leukoc. Biol. 78: 533-543 [Abstract] [Full Text]
Ercolini, A. M., Ladle, B. H., Manning, E. A., Pfannenstiel, L. W., Armstrong, T. D., Machiels, J.-P. H., Bieler, J. G., Emens, L. A., Reilly, R. T., Jaffee, E. M. (2005). Recruitment of latent pools of high-avidity CD8+ T cells to the antitumor immune response. JEM 201: 1591-1602 [Abstract] [Full Text]
Liadis, N., Murakami, K., Eweida, M., Elford, A. R., Sheu, L., Gaisano, H. Y., Hakem, R., Ohashi, P. S., Woo, M. (2005). Caspase-3-Dependent {beta}-Cell Apoptosis in the Initiation of Autoimmune Diabetes Mellitus. Mol. Cell. Biol. 25: 3620-3629 [Abstract] [Full Text]
Hurchla, M. A., Sedy, J. R., Gavrielli, M., Drake, C. G., Murphy, T. L., Murphy, K. M. (2005). B and T Lymphocyte Attenuator Exhibits Structural and Expression Polymorphisms and Is Highly Induced in Anergic CD4+ T Cells. J. Immunol. 174: 3377-3385 [Abstract] [Full Text]
Bruder, D., Westendorf, A. M., Geffers, R., Gruber, A. D., Gereke, M., Enelow, R. I., Buer, J. (2004). CD4 T Lymphocyte-mediated Lung Disease: Steady State between Pathological and Tolerogenic Immune Reactions. Am. J. Respir. Crit. Care Med. 170: 1145-1152 [Abstract] [Full Text]
Mihalyo, M. A., Doody, A. D. H., McAleer, J. P., Nowak, E. C., Long, M., Yang, Y., Adler, A. J. (2004). In Vivo Cyclophosphamide and IL-2 Treatment Impedes Self-Antigen-Induced Effector CD4 Cell Tolerization: Implications for Adoptive Immunotherapy. J. Immunol. 172: 5338-5345 [Abstract] [Full Text]
Goddard, S., Youster, J., Morgan, E., Adams, D. H. (2004). Interleukin-10 Secretion Differentiates Dendritic Cells from Human Liver and Skin. Am. J. Pathol. 164: 511-519 [Abstract] [Full Text]
Cuenca, A., Cheng, F., Wang, H., Brayer, J., Horna, P., Gu, L., Bien, H., Borrello, I. M., Levitsky, H. I., Sotomayor, E. M. (2003). Extra-Lymphatic Solid Tumor Growth Is Not Immunologically Ignored and Results in Early Induction of Antigen-Specific T-Cell Anergy: Dominant Role of Cross-Tolerance to Tumor Antigens. Cancer Res. 63: 9007-9015 [Abstract] [Full Text]
Chen, Y.-L., Chen, S.-H., Wang, J.-Y., Yang, B.-C. (2003). Fas Ligand on Tumor Cells Mediates Inactivation of Neutrophils. J. Immunol. 171: 1183-1191 [Abstract] [Full Text]
Staveley-O'Carroll, K., Schell, T. D., Jimenez, M., Mylin, L. M., Tevethia, M. J., Schoenberger, S. P., Tevethia, S. S. (2003). In Vivo Ligation of CD40 Enhances Priming Against the Endogenous Tumor Antigen and Promotes CD8+ T Cell Effector Function in SV40 T Antigen Transgenic Mice. J. Immunol. 171: 697-707 [Abstract] [Full Text]
Veeraswamy, R. K., Cella, M., Colonna, M., Unanue, E. R. (2003). Dendritic Cells Process and Present Antigens Across A Range of Maturation States. J. Immunol. 170: 5367-5372 [Abstract] [Full Text]
Huang, C.-T., Huso, D. L., Lu, Z., Wang, T., Zhou, G., Kennedy, E. P., Drake, C. G., Morgan, D. J., Sherman, L. A., Higgins, A. D., Pardoll, D. M., Adler, A. J. (2003). CD4+ T Cells Pass Through an Effector Phase During the Process of In Vivo Tolerance Induction. J. Immunol. 170: 3945-3953 [Abstract] [Full Text]
Ackerman, A. L., Cresswell, P. (2003). Regulation of MHC Class I Transport in Human Dendritic Cells and the Dendritic-Like Cell Line KG-1. J. Immunol. 170: 4178-4188 [Abstract] [Full Text]
Bouzahzah, F., Jung, S., Craft, J. (2003). CD4+ T Cells from Lupus-Prone Mice Avoid Antigen-Specific Tolerance Induction In Vivo. J. Immunol. 170: 741-748 [Abstract] [Full Text]
Morelli, A. E., Larregina, A. T., Shufesky, W. J., Zahorchak, A. F., Logar, A. J., Papworth, G. D., Wang, Z., Watkins, S. C., Falo, L. D. Jr, Thomson, A. W. (2003). Internalization of circulating apoptotic cells by splenic marginal zone dendritic cells: dependence on complement receptors and effect on cytokine production. Blood 101: 611-620 [Abstract] [Full Text]
de Jersey, J., Carmignac, D., Barthlott, T., Robinson, I., Stockinger, B. (2002). Activation of CD8 T Cells by Antigen Expressed in the Pituitary Gland. J. Immunol. 169: 6753-6759 [Abstract] [Full Text]
Noessner, E., Gastpar, R., Milani, V., Brandl, A., Hutzler, P. J. S., Kuppner, M. C., Roos, M., Kremmer, E., Asea, A., Calderwood, S. K., Issels, R. D. (2002). Tumor-Derived Heat Shock Protein 70 Peptide Complexes Are Cross-Presented by Human Dendritic Cells. J. Immunol. 169: 5424-5432 [Abstract] [Full Text]
Gonzalez, M., Quezada, S. A., Blazar, B. R., Panoskaltsis-Mortari, A., Rudensky, A. Y., Noelle, R. J. (2002). The Balance Between Donor T Cell Anergy and Suppression Versus Lethal Graft-Versus-Host Disease Is Determined by Host Conditioning. J. Immunol. 169: 5581-5589 [Abstract] [Full Text]
Mougneau, E., Hugues, S., Glaichenhaus, N. (2002). Antigen Presentation by Dendritic Cells In Vivo. JEM 196: 1013-1016 [Full Text]
Higgins, A. D., Mihalyo, M. A., Adler, A. J. (2002). Effector CD4 Cells Are Tolerized Upon Exposure to Parenchymal Self-Antigen. J. Immunol. 169: 3622-3629 [Abstract] [Full Text]
Heckelsmiller, K., Rall, K., Beck, S., Schlamp, A., Seiderer, J., Jahrsdorfer, B., Krug, A., Rothenfusser, S., Endres, S., Hartmann, G. (2002). Peritumoral CpG DNA Elicits a Coordinated Response of CD8 T Cells and Innate Effectors to Cure Established Tumors in a Murine Colon Carcinoma Model. J. Immunol. 169: 3892-3899 [Abstract] [Full Text]
Prasad, S. J., Goodnow, C. C. (2002). Cell-intrinsic effects of non-MHC NOD genes on dendritic cell generation in vivo. Int Immunol 14: 677-684 [Abstract] [Full Text]
Higgins, A. D., Mihalyo, M. A., McGary, P. W., Adler, A. J. (2002). CD4 Cell Priming and Tolerization Are Differentially Programmed by APCs upon Initial Engagement. J. Immunol. 168: 5573-5581 [Abstract] [Full Text]
Auffermann-Gretzinger, S., Lossos, I. S., Vayntrub, T. A., Leong, W., Grumet, F. C., Blume, K. G., Stockerl-Goldstein, K. E., Levy, R., Shizuru, J. A. (2002). Rapid establishment of dendritic cell chimerism in allogeneic hematopoietic cell transplant recipients. Blood 99: 1442-1448 [Abstract] [Full Text]
Nguyen, L. T., Elford, A. R., Murakami, K., Garza, K. M., Schoenberger, S. P., Odermatt, B., Speiser, D. E., Ohashi, P. S. (2002). Tumor Growth Enhances Cross-Presentation Leading to Limited T Cell Activation without Tolerance. JEM 195: 423-435 [Abstract] [Full Text]
Kawahata, K., Misaki, Y., Yamauchi, M., Tsunekawa, S., Setoguchi, K., Miyazaki, J.-i., Yamamoto, K. (2002). Peripheral Tolerance to a Nuclear Autoantigen: Dendritic Cells Expressing a Nuclear Autoantigen Lead to Persistent Anergic State of CD4+ Autoreactive T Cells After Proliferation. J. Immunol. 168: 1103-1112 [Abstract] [Full Text]
Kammerer, R., Stober, D., Riedl, P., Oehninger, C., Schirmbeck, R., Reimann, J. (2002). Noncovalent Association with Stress Protein Facilitates Cross-Priming of CD8+ T Cells to Tumor Cell Antigens by Dendritic Cells. J. Immunol. 168: 108-117 [Abstract] [Full Text]
Steinman, R. M., Nussenzweig, M. C. (2002). Avoiding horror autotoxicus: The importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. USA 10.1073/pnas.231606698v1 [Abstract] [Full Text]
Hawiger, D., Inaba, K., Dorsett, Y., Guo, M., Mahnke, K., Rivera, M., Ravetch, J. V., Steinman, R. M., Nussenzweig, M. C. (2001). Dendritic Cells Induce Peripheral T Cell Unresponsiveness Under Steady State Conditions In Vivo. JEM 194: 769-780 [Abstract] [Full Text]
Hernandez, J., Aung, S., Redmond, W. L., Sherman, L. A. (2001). Phenotypic and Functional Analysis of CD8+ T Cells Undergoing Peripheral Deletion in Response to Cross-Presentation of Self-Antigen. JEM 194: 707-718 [Abstract] [Full Text]
Sotomayor, E. M., Borrello, I., Rattis, F.-M., Cuenca, A. G., Abrams, J., Staveley-O'Carroll, K., Levitsky, H. I. (2001). Cross-presentation of tumor antigens by bone marrow-derived antigen-presenting cells is the dominant mechanism in the induction of T-cell tolerance during B-cell lymphoma progression. Blood 98: 1070-1077 [Abstract] [Full Text]
Bittencourt, M. d. C., Perruche, S., Contassot, E., Fresnay, S., Baron, M.-H., Angonin, R., Aubin, F., Herve, P., Tiberghien, P., Saas, P. (2001). Intravenous injection of apoptotic leukocytes enhances bone marrow engraftment across major histocompatibility barriers. Blood 98: 224-230 [Abstract] [Full Text]
Jooss, K., Gjata, B., Danos, O., von Boehmer, H., Sarukhan, A. (2001). Regulatory function of in vivo anergized CD4+ T cells. Proc. Natl. Acad. Sci. USA 10.1073/pnas.151088898v1 [Abstract] [Full Text]
Li, M., Davey, G. M., Sutherland, R. M., Kurts, C., Lew, A. M., Hirst, C., Carbone, F. R., Heath, W. R. (2001). Cell-Associated Ovalbumin Is Cross-Presented Much More Efficiently than Soluble Ovalbumin In Vivo. J. Immunol. 166: 6099-6103 [Abstract] [Full Text]
Eck, S. C., Turka, L. A. (2001). Adoptive Transfer Enables Tumor Rejection Targeted against a Self-Antigen without the Induction of Autoimmunity. Cancer Res. 61: 3077-3083 [Abstract] [Full Text]
Anderson, C. C., Carroll, J. M., Gallucci, S., Ridge, J. P., Cheever, A. W., Matzinger, P. (2001). Testing Time-, Ignorance-, and Danger-Based Models of Tolerance. J. Immunol. 166: 3663-3671 [Abstract] [Full Text]
den Haan, J. M.M., Lehar, S. M., Bevan, M. J. (2000). CD8+ but Not CD8- Dendritic Cells Cross-prime Cytotoxic T Cells In Vivo. JEM 192: 1685-1696 [Abstract] [Full Text]
Reilly, R. T., Gottlieb, M. B. C., Ercolini, A. M., Machiels, J.-P. H., Kane, C. E., Okoye, F. I., Muller, W. J., Dixon, K. H., Jaffee, E. M. (2000). HER-2/neu Is a Tumor Rejection Target in Tolerized HER-2/neu Transgenic Mice. Cancer Res. 60: 3569-3576 [Abstract] [Full Text]
Schell, T. D., Knowles, B. B., Tevethia, S. S. (2000). Sequential Loss of Cytotoxic T Lymphocyte Responses to Simian Virus 40 Large T Antigen Epitopes in T Antigen Transgenic Mice Developing Osteosarcomas. Cancer Res. 60: 3002-3012 [Abstract] [Full Text]
Steinman, R. M., Turley, S., Mellman, I., Inaba, K. (2000). The Induction of Tolerance by Dendritic Cells That Have Captured Apoptotic Cells. JEM 191: 411-416 [Full Text]
Huang, F.-P., Platt, N., Wykes, M., Major, J. R., Powell, T. J., Jenkins, C. D., MacPherson, G. G. (2000). A Discrete Subpopulation of Dendritic Cells Transports Apoptotic Intestinal Epithelial Cells to T Cell Areas of Mesenteric Lymph Nodes. JEM 191: 435-444 [Abstract] [Full Text]
Lu, Z., Yuan, L., Zhou, X., Sotomayor, E., Levitsky, H. I., Pardoll, D. M. (2000). CD40-independent Pathways of T Cell Help for Priming of CD8+ Cytotoxic T Lymphocytes. JEM 191: 541-550 [Abstract] [Full Text]
Adler, A. J., Huang, C.-T., Yochum, G. S., Marsh, D. W., Pardoll, D. M. (2000). In Vivo CD4+ T Cell Tolerance Induction Versus Priming Is Independent of the Rate and Number of Cell Divisions. J. Immunol. 164: 649-655 [Abstract] [Full Text]
Sotomayor, E. M., Borrello, I., Tubb, E., Allison, J. P., Levitsky, H. I. (1999). In vivo blockade of CTLA-4 enhances the priming of responsive T cells but fails to prevent the induction of tumor antigen-specific tolerance. Proc. Natl. Acad. Sci. USA 96: 11476-11481 [Abstract] [Full Text]
Miller, C., Ragheb, J. A., Schwartz, R. H. (1999). Anergy and Cytokine-mediated Suppression as Distinct Superantigen-induced Tolerance Mechanisms In Vivo. JEM 190: 53-64 [Abstract] [Full Text]
Doan, T., Herd, K., Street, M., Bryson, G., Fernando, G., Lambert, P., Tindle, R. (1999). Human Papillomavirus Type 16�E7 Oncoprotein Expressed in Peripheral Epithelium Tolerizes E7-Directed Cytotoxic T-Lymphocyte Precursors Restricted through Human (and Mouse) Major Histocompatibility Complex Class I Alleles. J. Virol. 73: 6166-6170 [Abstract] [Full Text]
Singh-Jasuja, H., Toes, R. E.M., Spee, P., Munz, C., Hilf, N., Schoenberger, S. P., Ricciardi-Castagnoli, P., Neefjes, J., Rammensee, H.-G., Arnold-Schild, D., Schild, H. (1999). Cross-Presentation of Glycoprotein 96-associated Antigens on Major Histocompatibility Complex Class I Molecules Requires Receptor-mediated Endocytosis. JEM 191: 1965-1974 [Abstract] [Full Text]
Morgan, D. J., Kurts, C., Kreuwel, H. T.�C., Holst, K. L., Heath, W. R., Sherman, L. A. (1999). Ontogeny of T cell tolerance to peripherally expressed antigens. Proc. Natl. Acad. Sci. USA 96: 3854-3858 [Abstract] [Full Text]
Toes, R. E.M., Ossendorp, F., Offringa, R., Melief, C. J.M. (1999). CD4 T Cells and Their Role in Antitumor Immune Responses. JEM 189: 753-756 [Full Text]
Wise, M. P., Bemelman, F., Cobbold, S. P., Waldmann, H. (1998). Cutting Edge: Linked Suppression of Skin Graft Rejection Can Operate Through Indirect Recognition. J. Immunol. 161: 5813-5816 [Abstract] [Full Text]
Jooss, K., Gjata, B., Danos, O., von Boehmer, H., Sarukhan, A. (2001). Regulatory function of in vivo anergized CD4+ T cells. Proc. Natl. Acad. Sci. USA 98: 8738-8743 [Abstract] [Full Text]
Steinman, R. M., Nussenzweig, M. C. (2002). Inaugural Article: Avoiding horror autotoxicus: The importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. USA 99: 351-358 [Abstract] [Full Text]
Maccioni, M., Zeder-Lutz, G., Huang, H., Ebel, C., Gerber, P., Hergueux, J., Marchal, P., Duchatelle, V., Degott, C., van Regenmortel, M., Benoist, C., Mathis, D. (2002). Arthritogenic Monoclonal Antibodies from K/BxN Mice. JEM 195: 1071-1077 [Abstract] [Full Text]