|
|
||||||||
The Journal of Immunology, Vol 155, Issue 1 45-57, Copyright © 1995 by American Association of Immunologists
ARTICLES |
C Dubey, M Croft and SL Swain
Department of Biology, University of California, at San Diego, La Jolla 92093, USA.
Efficient initiation of a CD4 T cell response requires both activation through the TCR and costimulation provided by molecules on APC with counterreceptors on the T cell. We investigated the relative contribution of the ICAM-1:LFA-1 and B7:CD28/CTLA-4 costimulatory pathways in naive T cell activation, using either anti-CD28 Ab or fibroblast cell lines transfected with I-Ek, which express either no costimulatory molecules, ICAM-1 alone, B7-1 alone, or ICAM-1 and B7-1 together. Peptide Ag or immobilized anti-CD3 was used to provide the TCR signal. CD4 T cells from mice transgenic for the V beta 3/V alpha 11 TCR, which recognize a peptide of pigeon cytochrome c complexed to I- Ek, were used as a source of naive T cells. Naive T cells stimulated with Ag or anti-CD3 responded well to high numbers of APC expressing either ICAM-1 alone or B7-1 alone. However, APC expressing both ICAM-1 and B7-1 were much better stimulators of proliferation and IL-2 secretion at low cell numbers, and were far superior inducers of IL-2 at higher numbers, indicating a synergy between the two pathways. Stimulation provided by ICAM-1 could not be solely attributed to adhesive strengthening of other pathways, since costimulation was seen when immobilized anti-CD3 was used and when ICAM-1 only APC were added, indicating that ICAM-1 was in fact acting as a classic costimulatory molecule. Both the magnitude of the response and the amount of costimulation required for response were dependent on the intensity of TCR interaction. These results suggest that an efficient naive T cell response requires both a strong TCR signal and more than one costimulatory signal that will synergize with the TCR signal. This offers an explanation as to why APC such as dendritic cells and activated B cells, which express high levels of multiple costimulatory/adhesion molecules, are the only APC that elicit naive T cell responses.
This article has been cited by other articles:
![]() |
K. K. McKinstry, S. Golech, W.-H. Lee, G. Huston, N.-P. Weng, and S. L. Swain Rapid default transition of CD4 T cell effectors to functional memory cells J. Exp. Med., September 3, 2007; 204(9): 2199 - 2211. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Graf, T. Bushnell, and J. Miller LFA-1-Mediated T Cell Costimulation through Increased Localization of TCR/Class II Complexes to the Central Supramolecular Activation Cluster and Exclusion of CD45 from the Immunological Synapse J. Immunol., August 1, 2007; 179(3): 1616 - 1624. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Ke, D. Sun, P. Zhang, G. Jiang, H. J. Kaplan, and H. Shao Suppression of Established Experimental Autoimmune Uveitis by Anti-LFA-1{alpha} Ab Invest. Ophthalmol. Vis. Sci., June 1, 2007; 48(6): 2667 - 2675. [Abstract] [Full Text] [PDF] |
||||
![]() |
J.-J. Goval, R. Greimers, J. Boniver, and L. de Leval Germinal Center Dendritic Cells Express More ICAM-1 Than Extrafollicular Dendritic Cells and ICAM-1/LFA-1 Interactions are Involved in the Capacity of Dendritic Cells to Induce PBMCs Proliferation J. Histochem. Cytochem., January 1, 2006; 54(1): 75 - 84. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Parameswaran, R. Suresh, V. Bal, S. Rath, and A. George Lack of ICAM-1 on APCs during T Cell Priming Leads to Poor Generation of Central Memory Cells J. Immunol., August 15, 2005; 175(4): 2201 - 2211. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. P. Olcott, J. Tian, V. Walker, H. Dang, B. Middleton, L. Adorini, L. Washburn, and D. L. Kaufman Antigen-Based Therapies Using Ignored Determinants of {beta} Cell Antigens Can More Effectively Inhibit Late-Stage Autoimmune Disease in Diabetes-Prone Mice J. Immunol., August 1, 2005; 175(3): 1991 - 1999. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Haynes, S. M. Eaton, E. M. Burns, T. D. Randall, and S. L. Swain Newly generated CD4 T cells in aged animals do not exhibit age-related defects in response to antigen J. Exp. Med., March 21, 2005; 201(6): 845 - 851. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Blois, M. Tometten, J. Kandil, E. Hagen, B. F. Klapp, R. A. Margni, and P. C. Arck Intercellular Adhesion Molecule-1/LFA-1 Cross Talk Is a Proximate Mediator Capable of Disrupting Immune Integration and Tolerance Mechanism at the Feto-Maternal Interface in Murine Pregnancies J. Immunol., February 15, 2005; 174(4): 1820 - 1829. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. M. Eaton, E. M. Burns, K. Kusser, T. D. Randall, and L. Haynes Age-related Defects in CD4 T Cell Cognate Helper Function Lead to Reductions in Humoral Responses J. Exp. Med., December 20, 2004; 200(12): 1613 - 1622. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Metzler, P. Gfeller, M. Bigaud, J. Li, G. Wieczorek, C. Heusser, P. Lake, and A. Katopodis Combinations of Anti-LFA-1, Everolimus, Anti-CD40 Ligand, and Allogeneic Bone Marrow Induce Central Transplantation Tolerance through Hemopoietic Chimerism, Including Protection from Chronic Heart Allograft Rejection J. Immunol., December 1, 2004; 173(11): 7025 - 7036. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Kandula and C. Abraham LFA-1 on CD4+ T Cells Is Required for Optimal Antigen-Dependent Activation In Vivo J. Immunol., October 1, 2004; 173(7): 4443 - 4451. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Havari, A. M. Lennon-Dumenil, L. Klein, D. Neely, J. A. Taylor, M. F. McInerney, K. W. Wucherpfennig, and M. A. Lipes Expression of the B7.1 Costimulatory Molecule on Pancreatic {beta} Cells Abrogates the Requirement for CD4 T Cells in the Development of Type 1 Diabetes J. Immunol., July 15, 2004; 173(2): 787 - 796. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. D. Weinberg, D. E. Evans, C. Thalhofer, T. Shi, and R. A. Prell The generation of T cell memory: a review describing the molecular and cellular events following OX40 (CD134) engagement J. Leukoc. Biol., June 1, 2004; 75(6): 962 - 972. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Haynes, S. M. Eaton, E. M. Burns, M. Rincon, and S. L. Swain Inflammatory Cytokines Overcome Age-Related Defects in CD4 T Cell Responses In Vivo J. Immunol., May 1, 2004; 172(9): 5194 - 5199. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. T. A. Marques Jr., P. Chikhlikar, L. B. de Arruda, I. C. Leao, Y. Lu, J. Wong, J.-S. Chen, B. Byrne, and J. T. August HIV-1 p55Gag Encoded in the Lysosome-associated Membrane Protein-1 as a DNA Plasmid Vaccine Chimera Is Highly Expressed, Traffics to the Major Histocompatibility Class II Compartment, and Elicits Enhanced Immune Responses J. Biol. Chem., September 26, 2003; 278(39): 37926 - 37936. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. A. Wetzel, T. W. McKeithan, and D. C. Parker Live-Cell Dynamics and the Role of Costimulation in Immunological Synapse Formation J. Immunol., December 1, 2002; 169(11): 6092 - 6101. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. P. Banerjee, D. S. Vinay, A. Mathew, M. Raje, V. Parekh, D. V. R. Prasad, A. Kumar, D. Mitra, and G. C. Mishra Evidence That Glycoprotein 96 (B2), a Stress Protein, Functions as a Th2-Specific Costimulatory Molecule J. Immunol., October 1, 2002; 169(7): 3507 - 3518. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. M. Sutherland, B. S. McKenzie, Y. Zhan, A. J. Corbett, A. Fox-Marsh, H. M. Georgiou, L. C. Harrison, and A. M. Lew Anti-CD45RB antibody deters xenograft rejection by modulating T cell priming and homing Int. Immunol., August 1, 2002; 14(8): 953 - 962. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. H. Yen, N. Lepak, and S. L. Swain Induction of CD4 T Cell Changes in Murine AIDS Is Dependent on Costimulation and Involves a Dysregulation of Homeostasis J. Immunol., July 15, 2002; 169(2): 722 - 731. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Chirathaworn, J. E. Kohlmeier, S. A. Tibbetts, L. M. Rumsey, M. A. Chan, and S. H. Benedict Stimulation Through Intercellular Adhesion Molecule-1 Provides a Second Signal for T Cell Activation J. Immunol., June 1, 2002; 168(11): 5530 - 5537. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. K. Takahashi, H. Iwagaki, T. Yoshino, S. Mori, T. Morichika, H. Itoh, M. Yokoyama, S. Kubo, E. Kondo, T. Akagi, et al. Prostaglandin E2 Inhibits IL-18-Induced ICAM-1 and B7.2 Expression Through EP2/EP4 Receptors in Human Peripheral Blood Mononuclear Cells J. Immunol., May 1, 2002; 168(9): 4446 - 4454. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. H. Smits, E. C. de Jong, J. H. N. Schuitemaker, T. B. H. Geijtenbeek, Y. van Kooyk, M. L. Kapsenberg, and E. A. Wierenga Intercellular Adhesion Molecule-1/LFA-1 Ligation Favors Human Th1 Development J. Immunol., February 15, 2002; 168(4): 1710 - 1716. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Hombach, A. Wieczarkowiecz, T. Marquardt, C. Heuser, L. Usai, C. Pohl, B. Seliger, and H. Abken Tumor-Specific T Cell Activation by Recombinant Immunoreceptors: CD3{zeta} Signaling and CD28 Costimulation Are Simultaneously Required for Efficient IL-2 Secretion and Can Be Integrated Into One Combined CD28/CD3{zeta} Signaling Receptor Molecule J. Immunol., December 1, 2001; 167(11): 6123 - 6131. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Abraham and J. Miller Molecular Mechanisms of IL-2 Gene Regulation Following Costimulation Through LFA-1 J. Immunol., November 1, 2001; 167(9): 5193 - 5201. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Yu, D. Leitenberg, B. Li, and R. A. Flavell Deficiency of Small GTPase Rac2 Affects T Cell Activation J. Exp. Med., September 24, 2001; 194(7): 915 - 926. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. M. Palmer, L. Farrokh-Siar, J. Maguire van Seventer, and G. A. van Seventer IL-12 Decreases Activation-Induced Cell Death in Human Naive Th Cells Costimulated by Intercellular Adhesion Molecule-1. I. IL-12 Alters Caspase Processing and Inhibits Enzyme Function J. Immunol., July 15, 2001; 167(2): 749 - 758. [Abstract] [Full Text] [PDF] |
||||
![]() |
H.-T. Ni, M. J. Deeths, and M. F. Mescher LFA-1-Mediated Costimulation of CD8+ T Cell Proliferation Requires Phosphatidylinositol 3-Kinase Activity J. Immunol., June 1, 2001; 166(11): 6523 - 6529. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Hombach, D. Sent, C. Schneider, C. Heuser, D. Koch, C. Pohl, B. Seliger, and H. Abken T-Cell Activation by Recombinant Receptors: CD28 Costimulation Is Required for Interleukin 2 Secretion and Receptor-mediated T-Cell Proliferation but Does Not Affect Receptor-mediated Target Cell Lysis Cancer Res., March 1, 2001; 61(5): 1976 - 1982. [Abstract] [Full Text] |
||||
![]() |
L. S. Cauley, E. E. Miller, M. Yen, and S. L. Swain Superantigen-Induced CD4 T Cell Tolerance Mediated by Myeloid Cells and IFN-{gamma} J. Immunol., December 1, 2000; 165(11): 6056 - 6066. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. L. Gaglia, E. A. Greenfield, A. Mattoo, A. H. Sharpe, G. J. Freeman, and V. K. Kuchroo Intercellular Adhesion Molecule 1 Is Critical for Activation of CD28-Deficient T Cells J. Immunol., December 1, 2000; 165(11): 6091 - 6098. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. M. Jelley-Gibbs, N. M. Lepak, M. Yen, and S. L. Swain Two Distinct Stages in the Transition from Naive CD4 T Cells to Effectors, Early Antigen-Dependent and Late Cytokine-Driven Expansion and Differentiation J. Immunol., November 1, 2000; 165(9): 5017 - 5026. [Abstract] [Full Text] [PDF] |
||||
![]() |
Mahnke, Guo, Lee, Sepulveda, S. Swain, Nussenzweig, and R. Steinman The Dendritic Cell Receptor for Endocytosis, DEC-205, Can Recycle and Enhance Antigen Presentation via Major Histocompatibility Complex Class II-positive Lysosomal Compartments J. Cell Biol., October 30, 2000; 151(3): 673 - 684. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. W. Hodge, A. N. Rad, D. W. Grosenbach, H. Sabzevari, A. G. Yafal, L. Gritz, and J. Schlom Enhanced Activation of T Cells by Dendritic Cells Engineered to Hyperexpress a Triad of Costimulatory Molecules J Natl Cancer Inst, August 2, 2000; 92(15): 1228 - 1239. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. E. Woodhead, T. J. Stonehouse, M. H. Binks, K. Speidel, D. A. Fox, A. Gaya, D. Hardie, A. J. Henniker, V. Horejsi, K. Sagawa, et al. Novel molecular mechanisms of dendritic cell-induced T cell activation Int. Immunol., July 1, 2000; 12(7): 1051 - 1061. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. A. Muraro, M. Pette, B. Bielekova, H. F. McFarland, and R. Martin Human Autoreactive CD4+ T Cells from Naive CD45RA+ and Memory CD45RO+ Subsets Differ with Respect to Epitope Specificity and Functional Antigen Avidity J. Immunol., May 15, 2000; 164(10): 5474 - 5481. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. R. Rogers, C. Dubey, and S. L. Swain Qualitative Changes Accompany Memory T Cell Generation: Faster, More Effective Responses at Lower Doses of Antigen J. Immunol., March 1, 2000; 164(5): 2338 - 2346. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. E. Evans, M. W. Munks, J. M. Purkerson, and D. C. Parker Resting B Lymphocytes as APC for Naive T Lymphocytes: Dependence on CD40 Ligand/CD40 J. Immunol., January 15, 2000; 164(2): 688 - 697. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Wen, F. S. Wong, J. Tang, N.-Y. Chen, M. Altieri, C. David, R. Flavell, and R. Sherwin In Vivo Evidence for the Contribution of Human Histocompatibility Leukocyte Antigen (HLA)-DQ Molecules to the Development of Diabetes J. Exp. Med., January 3, 2000; 191(1): 97 - 104. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Cerwenka, T. M. Morgan, and R. W. Dutton Naive, Effector, and Memory CD8 T Cells in Protection Against Pulmonary Influenza Virus Infection: Homing Properties Rather Than Initial Frequencies Are Crucial J. Immunol., November 15, 1999; 163(10): 5535 - 5543. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. L. Swain, H. Hu, and G. Huston Class II-Independent Generation of CD4 Memory T Cells from Effectors Science, November 12, 1999; 286(5443): 1381 - 1383. [Abstract] [Full Text] |
||||
![]() |
J. W. Hodge, H. Sabzevari, A. Gomez Yafal, L. Gritz, M. G. O. Lorenz, and J. Schlom A Triad of Costimulatory Molecules Synergize to Amplify T-Cell Activation Cancer Res., November 1, 1999; 59(22): 5800 - 5807. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Sprent Presidential Address to The American Association of Immunologists : Stimulating Naive T Cells J. Immunol., November 1, 1999; 163(9): 4629 - 4636. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Shier, K. Ngo, and W.-P. Fung-Leung Defective CD8+ T Cell Activation and Cytolytic Function in the Absence of LFA-1 Cannot Be Restored by Increased TCR Signaling J. Immunol., November 1, 1999; 163(9): 4826 - 4832. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. S. Liwski and T. D. G. Lee Nematode Infection Enhances Survival of Activated T Cells by Modulating Accessory Cell Function J. Immunol., November 1, 1999; 163(9): 5005 - 5012. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Haynes, P.-J. Linton, S. M. Eaton, S. L. Tonkonogy, and S. L. Swain Interleukin 2, but Not Other Common {gamma} Chain–binding Cytokines, Can Reverse the Defect in Generation of CD4 Effector T Cells from Naive T Cells of Aged Mice J. Exp. Med., October 4, 1999; 190(7): 1013 - 1024. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. W. Hodge and J. Schlom Comparative Studies of a Retrovirus versus a Poxvirus Vector in Whole Tumor-Cell Vaccines Cancer Res., October 1, 1999; 59(20): 5106 - 5111. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. E Donovan and P. W Finn Immune mechanisms of childhood asthma Thorax, October 1, 1999; 54(10): 938 - 946. [Full Text] |
||||
![]() |
H. Kishimoto and J. Sprent Strong TCR Ligation Without Costimulation Causes Rapid Onset of Fas-Dependent Apoptosis of Naive Murine CD4+ T Cells J. Immunol., August 15, 1999; 163(4): 1817 - 1826. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Sepulveda, A. Cerwenka, T. Morgan, and R. W. Dutton CD28, IL-2-Independent Costimulatory Pathways for CD8 T Lymphocyte Activation J. Immunol., August 1, 1999; 163(3): 1133 - 1142. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. R. Rogers and M. Croft Peptide Dose, Affinity, and Time of Differentiation Can Contribute to the Th1/Th2 Cytokine Balance J. Immunol., August 1, 1999; 163(3): 1205 - 1213. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. de Zoeten, V. Carr-Brendel, D. Markovic, J. Taylor-Papadimitriou, and E. P. Cohen Treatment of Breast Cancer with Fibroblasts Transfected with DNA from Breast Cancer Cells J. Immunol., June 1, 1999; 162(11): 6934 - 6941. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. L. Constant B Lymphocytes as Antigen-Presenting Cells for CD4+ T Cell Priming In Vivo J. Immunol., May 15, 1999; 162(10): 5695 - 5703. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Geginat, G. Bossi, J. R. Bender, and R. Pardi Anchorage Dependence of Mitogen-Induced G1 to S Transition in Primary T Lymphocytes J. Immunol., May 1, 1999; 162(9): 5085 - 5093. [Abstract] [Full Text] [PDF] |
||||
![]() |
H.-T. Ni, M. J. Deeths, W. Li, D. L. Mueller, and M. F. Mescher Signaling Pathways Activated by Leukocyte Function-Associated Ag-1-Dependent Costimulation J. Immunol., May 1, 1999; 162(9): 5183 - 5189. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Abraham, J. Griffith, and J. Miller The Dependence for Leukocyte Function-Associated Antigen-1/ICAM-1 Interactions in T Cell Activation Cannot Be Overcome by Expression of High Density TCR Ligand J. Immunol., April 15, 1999; 162(8): 4399 - 4405. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. R. Luksch, O. Winqvist, M. E. Ozaki, L. Karlsson, M. R. Jackson, P. A. Peterson, and S. R. Webb Intercellular adhesion molecule-1 inhibits interleukin 4 production by naive T cells PNAS, March 16, 1999; 96(6): 3023 - 3028. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. Gramaglia, D. N. Mauri, K. T. Miner, C. F. Ware, and M. Croft Lymphotoxin {alpha}{beta} Is Expressed on Recently Activated Naive and Th1-Like CD4 Cells but Is Down-Regulated by IL-4 During Th2 Differentiation J. Immunol., February 1, 1999; 162(3): 1333 - 1338. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. D. Weinberg, K. W. Wegmann3, C. Funatake, and R. H. Whitham Blocking OX-40/OX-40 Ligand Interaction In Vitro and In Vivo Leads to Decreased T Cell Function and Amelioration of Experimental Allergic Encephalomyelitis J. Immunol., February 1, 1999; 162(3): 1818 - 1826. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. A. ROSSINI, D. L. GREINER, and J. P. MORDES Induction of Immunologic Tolerance for Transplantation Physiol Rev, January 1, 1999; 79(1): 99 - 141. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. B. Samoilova, J. L. Horton, B. Hilliard, T.-S. T. Liu, and Y. Chen IL-6-Deficient Mice Are Resistant to Experimental Autoimmune Encephalomyelitis: Roles of IL-6 in the Activation and Differentiation of Autoreactive T Cells J. Immunol., December 15, 1998; 161(12): 6480 - 6486. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. Gramaglia, A. D. Weinberg, M. Lemon, and M. Croft Ox-40 Ligand: A Potent Costimulatory Molecule for Sustaining Primary CD4 T Cell Responses J. Immunol., December 15, 1998; 161(12): 6510 - 6517. [Abstract] [Full Text] [PDF] |
||||