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The Journal of Immunology, Vol 155, Issue 1 45-57, Copyright © 1995 by American Association of Immunologists

ARTICLES

Costimulatory requirements of naive CD4+ T cells. ICAM-1 or B7-1 can costimulate naive CD4 T cell activation but both are required for optimum response

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.


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P. R. Rogers, H. M. Grey, and M. Croft
Modulation of Naive CD4 T Cell Activation with Altered Peptide Ligands: The Nature of the Peptide and Presentation in the Context of Costimulation Are Critical for a Sustained Response
J. Immunol., April 15, 1998; 160(8): 3698 - 3704.
[Abstract] [Full Text] [PDF]

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 JEMHome page
Y. Wu, Q. Zhou, P. Zheng, and Y. Liu
CD28-independent Induction of T Helper Cells and Immunoglobulin Class Switches Requires Costimulation by the Heat-stable Antigen
J. Exp. Med., April 6, 1998; 187(7): 1151 - 1156.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
J. S. Goldstein, T. Chen, M. Brunswick, H. Mostowsky, and S. Kozlowski
Purified MHC Class I and Peptide Complexes Activate Naive CD8+ T Cells Independently of the CD28/B7 and LFA-1/ICAM-1 Costimulatory Interactions
J. Immunol., April 1, 1998; 160(7): 3180 - 3187.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
L. A. Zuckerman, L. Pullen, and J. Miller
Functional Consequences of Costimulation by ICAM-1 on IL-2 Gene Expression and T Cell Activation
J. Immunol., April 1, 1998; 160(7): 3259 - 3268.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
I. M. Dozmorov and R. A. Miller
Generation of Antigen-Specific Th2 Cells from Unprimed Mice In Vitro: Effects of Dexamethasone and Anti-IL-10 Antibody
J. Immunol., March 15, 1998; 160(6): 2700 - 2705.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
C. S. Subauste, R. de Waal Malefyt, and F. Fuh
Role of CD80 (B7.1) and CD86 (B7.2) in the Immune Response to an Intracellular Pathogen
J. Immunol., February 15, 1998; 160(4): 1831 - 1840.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
J. N. Agrewala, S. Suvas, R. K. Verma, and G. C. Mishra
Differential Effect of Anti-B7-1 and Anti-M150 Antibodies in Restricting the Delivery of Costimulatory Signals from B Cells and Macrophages
J. Immunol., February 1, 1998; 160(3): 1067 - 1077.
[Abstract] [Full Text] [PDF]

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 JCBHome page
J. M.G. Higgins, D. A. Mandlebrot, S. K. Shaw, G. J. Russell, E. A. Murphy, Y.-T. Chen, W. J. Nelson, C. M. Parker, and M. B. Brenner
Direct and Regulated Interaction of Integrin {alpha}E{beta}7 with E-Cadherin
J. Cell Biol., January 12, 1998; 140(1): 197 - 210.
[Abstract] [Full Text] [PDF]

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 JEMHome page
L. S. Cauley, K. A. Cauley, F. Shub, G. Huston, and S. L. Swain
Transferable Anergy: Superantigen Treatment Induces CD4+ T Cell Tolerance That Is Reversible and Requires CD4-CD8- Cells and Interferon {gamma}
J. Exp. Med., July 7, 1997; 186(1): 71 - 81.
[Abstract] [Full Text] [PDF]

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 JEMHome page
Z. Cai, H. Kishimoto, A. Brunmark, M. R. Jackson, P. A. Peterson, and J. Sprent
Requirements for Peptide-induced T Cell Receptor Downregulation on Naive CD8+ T Cells
J. Exp. Med., February 17, 1997; 185(4): 641 - 652.
[Abstract] [Full Text] [PDF]

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 JEMHome page
Y. Liu, R. H. Wenger, M. Zhao, and P. J. Nielsen
Distinct Costimulatory Molecules Are Required for the Induction of Effector and Memory Cytotoxic T Lymphocytes
J. Exp. Med., January 20, 1997; 185(2): 251 - 262.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
Z. Cai, A. Brunmark, M. R. Jackson, D. Loh, P. A. Peterson, and J. Sprent
Transfected Drosophila cells as a probe for defining the minimal requirements for stimulating unprimed CD8+ T cells
PNAS, December 10, 1996; 93(25): 14736 - 14741.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
R. Wang, Y. Wang-Zhu, and H. Grey
Interactions between double positive thymocytes and high affinity ligands presented by cortical epithelial cells generate double negative thymocytes with T cell regulatory activity
PNAS, February 19, 2002; 99(4): 2181 - 2186.
[Abstract] [Full Text] [PDF]

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 BloodHome page
A. M. Girvin, K. B. Gordon, C. J. Welsh, N. A. Clipstone, and S. D. Miller
Differential abilities of central nervous system resident endothelial cells and astrocytes to serve as inducible antigen-presenting cells
Blood, May 15, 2002; 99(10): 3692 - 3701.
[Abstract] [Full Text] [PDF]


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