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The Journal of Immunology, 1999, 163: 5860-5870.
Copyright © 1999 by The American Association of Immunologists

Molecular and Functional Characterization of Mouse Signaling Lymphocytic Activation Molecule (SLAM): Differential Expression and Responsiveness in Th1 and Th2 Cells1

Antonio G. Castro2,*, Thomas M. Hauser2,*, Benjamin G. Cocks*, John Abrams*, Sandra Zurawski*, Tatyana Churakova*, Francesca Zonin*, Douglas Robinson*, Stuart G. Tangye*, Gregorio Aversa*, Kim E. Nichols{dagger}, Jan E. de Vries*, Lewis L. Lanier* and Anne O’Garra3,*

* Department of Immunobiology, DNAX Research Institute of Molecular and Cellular Biology, Palo Alto, CA 94304; and {dagger} Division of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA 02115


   Abstract
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 Abstract
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Optimal T cell activation and expansion require engagement of the TCR plus costimulatory signals delivered through accessory molecules. SLAM (signaling lymphocytic activation molecule), a 70-kDa costimulatory molecule belonging to the Ig superfamily, was defined as a human cell surface molecule that mediated CD28-independent proliferation of human T cells and IFN-{gamma} production by human Th1 and Th2 clones. In this study, we describe the cloning of mouse SLAM and the production of mAb against it which reveal its expression on primary mouse T and B cells. Mouse SLAM is expressed on highly polarized Th1 and Th2 populations, and is maintained on Th1, but not on Th2 clones. Anti-mouse SLAM mAb augmented IFN-{gamma} production by Th1 cells and Th1 clones stimulated through the TCR, but did not induce IFN-{gamma} production by Th2 cells, nor their production of IL-4 or their proliferation. Mouse SLAM is a 75-kDa glycoprotein that upon tyrosine phosphorylation associates with the src homology 2-domain-containing protein tyrosine phosphatase SHP-2, but not SHP-1. Mouse SLAM also associates with the recently described human SLAM-associated protein. These studies may provide new insights into the regulation of Th1 responses.


   Acknowledgments
 
We thank Franck Barrat and Victoria Heath for reviewing the manuscript; Jun Wu and Richard Murray for discussion; Linda Lucian and Chad Crain for technical assistance; Debbie Ligget for oligonucleotide synthesis; Dan Gorman and the DNAX sequencing facility for DNA sequencing; and Jim Cupp, Eleni Callas, Jennifer Maskrey, and Dixie Pollakoff for cell sorting. We thank Maribel Andonian for help with graphics.

Received for publication June 22, 1999. Accepted for publication September 15, 1999.


   References
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 Abstract
 References
 

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[Abstract] [Full Text] [PDF]

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G. G. Welstead, E. C. Hsu, C. Iorio, S. Bolotin, and C. D. Richardson
Mechanism of CD150 (SLAM) Down Regulation from the Host Cell Surface by Measles Virus Hemagglutinin Protein
J. Virol., September 15, 2004; 78(18): 9666 - 9674.
[Abstract] [Full Text] [PDF]

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 BloodHome page
E. Merck, C. Gaillard, D. M. Gorman, F. Montero-Julian, I. Durand, S. M. Zurawski, C. Menetrier-Caux, G. Carra, S. Lebecque, G. Trinchieri, et al.
OSCAR is an FcR{gamma}-associated receptor that is expressed by myeloid cells and is involved in antigen presentation and activation of human dendritic cells
Blood, September 1, 2004; 104(5): 1386 - 1395.
[Abstract] [Full Text] [PDF]

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T. Chtanova, S. G. Tangye, R. Newton, N. Frank, M. R. Hodge, M. S. Rolph, and C. R. Mackay
T Follicular Helper Cells Express a Distinctive Transcriptional Profile, Reflecting Their Role as Non-Th1/Th2 Effector Cells That Provide Help for B Cells
J. Immunol., July 1, 2004; 173(1): 68 - 78.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
R. Chen, F. Relouzat, R. Roncagalli, A. Aoukaty, R. Tan, S. Latour, and A. Veillette
Molecular Dissection of 2B4 Signaling: Implications for Signal Transduction by SLAM-Related Receptors
Mol. Cell. Biol., June 15, 2004; 24(12): 5144 - 5156.
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A. Veillette
SLAM Family Receptors Regulate Immunity with and without SAP-related Adaptors
J. Exp. Med., May 3, 2004; 199(9): 1175 - 1178.
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N. Wang, A. Satoskar, W. Faubion, D. Howie, S. Okamoto, S. Feske, C. Gullo, K. Clarke, M. R. Sosa, A. H. Sharpe, et al.
The Cell Surface Receptor SLAM Controls T Cell and Macrophage Functions
J. Exp. Med., May 3, 2004; 199(9): 1255 - 1264.
[Abstract] [Full Text] [PDF]

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 Int ImmunolHome page
M. Simarro, A. Lanyi, D. Howie, F. Poy, J. Bruggeman, M. Choi, J. Sumegi, M. J. Eck, and C. Terhorst
SAP increases FynT kinase activity and is required for phosphorylation of SLAM and Ly9
Int. Immunol., May 1, 2004; 16(5): 727 - 736.
[Abstract] [Full Text] [PDF]

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P. A. Valdez, H. Wang, D. Seshasayee, M. van Lookeren Campagne, A. Gurney, W. P. Lee, and I. S. Grewal
NTB-A, a New Activating Receptor in T Cells That Regulates Autoimmune Disease
J. Biol. Chem., April 30, 2004; 279(18): 18662 - 18669.
[Abstract] [Full Text] [PDF]

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V. Pasquinelli, M. F. Quiroga, G. J. Martinez, L. C. Zorrilla, R. M. Musella, M. M. Bracco, L. Belmonte, A. Malbran, L. Fainboim, P. A. Sieling, et al.
Expression of Signaling Lymphocytic Activation Molecule- Associated Protein Interrupts IFN-{gamma} Production in Human Tuberculosis
J. Immunol., January 15, 2004; 172(2): 1177 - 1185.
[Abstract] [Full Text] [PDF]

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F. Seki, N. Ono, R. Yamaguchi, and Y. Yanagi
Efficient Isolation of Wild Strains of Canine Distemper Virus in Vero Cells Expressing Canine SLAM (CD150) and Their Adaptability to Marmoset B95a Cells
J. Virol., September 15, 2003; 77(18): 9943 - 9950.
[Abstract] [Full Text] [PDF]

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 J. Gen. Virol.Home page
S. Ohno, F. Seki, N. Ono, and Y. Yanagi
Histidine at position 61 and its adjacent amino acid residues are critical for the ability of SLAM (CD150) to act as a cellular receptor for measles virus
J. Gen. Virol., September 1, 2003; 84(9): 2381 - 2388.
[Abstract] [Full Text] [PDF]

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S. G. Tangye, K. E. Nichols, N. J. Hare, and B. C. M. van de Weerdt
Functional Requirements for Interactions Between CD84 and Src Homology 2 Domain-Containing Proteins and Their Contribution to Human T Cell Activation
J. Immunol., September 1, 2003; 171(5): 2485 - 2495.
[Abstract] [Full Text] [PDF]

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J. M. Del Valle, P. Engel, and M. Martin
The Cell Surface Expression of SAP-binding Receptor CD229 Is Regulated via Its Interaction with Clathrin-associated Adaptor Complex 2 (AP-2)
J. Biol. Chem., May 2, 2003; 278(19): 17430 - 17437.
[Abstract] [Full Text] [PDF]

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D. Howie, S. Okamoto, S. Rietdijk, K. Clarke, N. Wang, C. Gullo, J. P. Bruggeman, S. Manning, A. J. Coyle, E. Greenfield, et al.
The role of SAP in murine CD150 (SLAM)-mediated T-cell proliferation and interferon gamma production
Blood, September 26, 2002; 100(8): 2899 - 2907.
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S. Hannier, C. Bitegye, and S. Demotz
Early Events of TCR Signaling Are Distinct in Human Th1 and Th2 Cells
J. Immunol., August 15, 2002; 169(4): 1904 - 1911.
[Abstract] [Full Text] [PDF]

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P. L. Sinn, G. Williams, S. Vongpunsawad, R. Cattaneo, and P. B. McCray Jr.
Measles Virus Preferentially Transduces the Basolateral Surface of Well-Differentiated Human Airway Epithelia
J. Virol., March 1, 2002; 76(5): 2403 - 2409.
[Abstract] [Full Text] [PDF]

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 Sci SignalHome page
A. Veillette
The SAP Family: A New Class of Adaptor-Like Molecules That Regulates Immune Cell Functions
Sci. Signal., February 19, 2002; 2002(120): pe8 - pe8.
[Abstract] [Full Text] [PDF]

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D. Howie, M. Simarro, J. Sayos, M. Guirado, J. Sancho, and C. Terhorst
Molecular dissection of the signaling and costimulatory functions of CD150 (SLAM): CD150/SAP binding and CD150-mediated costimulation
Blood, February 1, 2002; 99(3): 957 - 965.
[Abstract] [Full Text] [PDF]

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V. E. Garcia, M. F. Quiroga, M. T. Ochoa, L. Ochoa, V. Pasquinelli, L. Fainboim, L. M. Olivares, R. Valdez, D. O. Sordelli, G. Aversa, et al.
Signaling Lymphocytic Activation Molecule Expression and Regulation in Human Intracellular Infection Correlate with Th1 Cytokine Patterns
J. Immunol., November 15, 2001; 167(10): 5719 - 5724.
[Abstract] [Full Text] [PDF]

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M. Martin, X. Romero, M. A. de la Fuente, V. Tovar, N. Zapater, E. Esplugues, P. Pizcueta, J. Bosch, and P. Engel
CD84 Functions as a Homophilic Adhesion Molecule and Enhances IFN-{gamma} Secretion: Adhesion Is Mediated by Ig-Like Domain 1
J. Immunol., October 1, 2001; 167(7): 3668 - 3676.
[Abstract] [Full Text] [PDF]

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A. E. Morelli, A. F. Zahorchak, A. T. Larregina, B. L. Colvin, A. J. Logar, T. Takayama, L. D. Falo, and A. W. Thomson
Cytokine production by mouse myeloid dendritic cells in relation to differentiation and terminal maturation induced by lipopolysaccharide or CD40 ligation
Blood, September 1, 2001; 98(5): 1512 - 1523.
[Abstract] [Full Text] [PDF]

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M. Kruse, E. Meinl, G. Henning, C. Kuhnt, S. Berchtold, T. Berger, G. Schuler, and A. Steinkasserer
Signaling Lymphocytic Activation Molecule Is Expressed on Mature CD83+ Dendritic Cells and Is Up-Regulated by IL-1{beta}
J. Immunol., August 15, 2001; 167(4): 1989 - 1995.
[Abstract] [Full Text] [PDF]

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H. Tatsuo, N. Ono, and Y. Yanagi
Morbilliviruses Use Signaling Lymphocyte Activation Molecules (CD150) as Cellular Receptors
J. Virol., July 1, 2001; 75(13): 5842 - 5850.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
M. J. Czar, E. N. Kersh, L. A. Mijares, G. Lanier, J. Lewis, G. Yap, A. Chen, A. Sher, C. S. Duckett, R. Ahmed, et al.
Altered lymphocyte responses and cytokine production in mice deficient in the X-linked lymphoproliferative disease gene SH2D1A/DSHP/SAP
PNAS, June 7, 2001; (2001) 131193098.
[Abstract] [Full Text] [PDF]

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L. M. Shlapatska, S. V. Mikhalap, A. G. Berdova, O. M. Zelensky, T. J. Yun, K. E. Nichols, E. A. Clark, and S. P. Sidorenko
CD150 Association with Either the SH2-Containing Inositol Phosphatase or the SH2-Containing Protein Tyrosine Phosphatase Is Regulated by the Adaptor Protein SH2D1A
J. Immunol., May 1, 2001; 166(9): 5480 - 5487.
[Abstract] [Full Text] [PDF]

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