Pleiotropic Contributions of Phospholipase C-gamma 1 (PLC-gamma 1) to T-Cell Antigen Receptor-Mediated Signaling: Reconstitution Studies of a PLC-gamma 1-Deficient Jurkat T-Cell Line

doi:10.1128/MCB.20.24.9149-9161.2000

This Article

	Full Text
	Full Text (PDF)
	Alert me when this article is cited
	Alert me if a correction is posted

Services

	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new issues of the journal
	Download to citation manager
	Reprints and Permissions
	Copyright Information
	Books from ASM Press
	MicrobeWorld

Citing Articles

	Citing Articles via HighWire
	Citing Articles via Google Scholar

Google Scholar

	Articles by Irvin, B. J.
	Articles by Abraham, R. T.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Irvin, B. J.
	Articles by Abraham, R. T.

Previous Article | Next Article

Molecular and Cellular Biology, December 2000, p. 9149-9161, Vol. 20, No. 24
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Pleiotropic Contributions of Phospholipase C- $gamma$ 1 (PLC- $gamma$ 1) to T-Cell Antigen Receptor-Mediated Signaling: Reconstitution Studies of a PLC- $gamma$ 1-Deficient Jurkat T-Cell Line

Brenda J. Irvin,¹ Brandi L. Williams,² Allan E. Nilson,³ Hannah O. Maynor,¹ and Robert T. Abraham¹^,^*

Department of Pharmacology and Cancer Biology, Duke University Medical Center, Durham, North Carolina 27710¹; Wellcome/CRC Institute, University of Cambridge, Cambridge, United Kingdom²; and Department of Immunology, Mayo Clinic, Rochester, Minnesota 55905³

Received 17 July 2000/Returned for modification 15 August 2000/Accepted 26 September 2000

Phospholipase C- $gamma$ 1 (PLC- $gamma$ 1) plays a crucial role in the coupling of T-cell antigen receptor (TCR) ligation to interleukin-2(IL-2) gene expression in activated T lymphocytes. In this study,we have isolated and characterized two novel, PLC- $gamma$ 1-deficientsublines derived from the Jurkat T-leukemic cell line. The P98subline displays a >90% reduction in PLC- $gamma$ 1 expression, whilethe J.gamma1 subline contains no detectable PLC- $gamma$ 1 protein. Thelack of PLC- $gamma$ 1 expression in J.gamma1 cells caused profound defectsin TCR-dependent Ca²⁺ mobilization and NFAT activation. In contrast, both of theseresponses occurred at normal levels in PLC- $gamma$ 1-deficient P98 cells.Unexpectedly, the P98 cells displayed significant and selectivedefects in the activation of both the composite CD28 responseelement (RE/AP) and the full-length IL-2 promoter following costimulationwith anti-TCR antibodies and phorbol ester. These transcriptionaldefects were reversed by transfection of P98 cells with a wild-typePLC- $gamma$ 1 expression vector but not by expression of mutated PLC- $gamma$ 1constructs that lacked a functional, carboxyl-terminal SH2 [SH2(C)]domain or the major Tyr⁷⁸³ phosphorylation site. On the other hand, the amino-terminal SH2[SH2(N)] domain was not essential for reconstitution of RE/AP-or IL-2 promoter-dependent transcription but was required forthe association of PLC- $gamma$ 1 with LAT, as well as the tyrosine phosphorylationof PLC- $gamma$ 1 itself, in activated P98 cells. These studies demonstratethat the PLC- $gamma$ 1 SH2(N) and SH2(C) domains play functionally distinctroles during TCR-mediated signaling and identify a non-Ca²⁺-related signaling function linked to the SH2(C) domain, whichcouples TCR plus phorbol ester-CD28 costimulation to the activationof the IL-2 promoter in Tlymphocytes.

^* Corresponding author. Mailing address: Department of Pharmacology and Cancer Biology, Room C333B LSRC, Box 3813, Duke UniversityMedical Center, Durham, NC 27710. Phone: (919) 613-8650. Fax:(919) 681-8461. E-mail: abrah008{at}mc.duke.edu.

Molecular and Cellular Biology, December 2000, p. 9149-9161, Vol. 20, No. 24
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

This article has been cited by other articles:

Baumann, S., Fas, S. C., Giaisi, M., Muller, W. W., Merling, A., Gulow, K., Edler, L., Krammer, P. H., Li-Weber, M. (2008). Wogonin preferentially kills malignant lymphocytes and suppresses T-cell tumor growth by inducing PLC{gamma}1- and Ca2+-dependent apoptosis. Blood 111: 2354-2363 [Abstract] [Full Text]
Ruiz, S., Santos, E., Bustelo, X. R. (2007). RasGRF2, a Guanosine Nucleotide Exchange Factor for Ras GTPases, Participates in T-Cell Signaling Responses. Mol. Cell. Biol. 27: 8127-8142 [Abstract] [Full Text]
Heo, S.-K., Yoon, M.-A, Lee, S.-C., Ju, S.-A, Choi, J.-H., Suh, P.-G., Kwon, B. S., Kim, B.-S. (2007). HVEM Signaling in Monocytes Is Mediated by Intracellular Calcium Mobilization. J. Immunol. 179: 6305-6310 [Abstract] [Full Text]
Zhou, Z., Yin, J., Dou, Z., Tang, J., Zhang, C., Cao, Y. (2007). The Calponin Homology Domain of Vav1 Associates with Calmodulin and Is Prerequisite to T Cell Antigen Receptor-induced Calcium Release in Jurkat T Lymphocytes. J. Biol. Chem. 282: 23737-23744 [Abstract] [Full Text]
Schneider, O. D., Weiss, A. A., Miller, W. E. (2007). Pertussis Toxin Utilizes Proximal Components of the T-Cell Receptor Complex To Initiate Signal Transduction Events in T Cells. Infect. Immun. 75: 4040-4049 [Abstract] [Full Text]
Kaminski, M., Kiessling, M., Suss, D., Krammer, P. H., Gulow, K. (2007). Novel Role for Mitochondria: Protein Kinase C{theta}-Dependent Oxidative Signaling Organelles in Activation-Induced T-Cell Death. Mol. Cell. Biol. 27: 3625-3639 [Abstract] [Full Text]
Bartolo, V. D., Montagne, B., Salek, M., Jungwirth, B., Carrette, F., Fourtane, J., Sol-Foulon, N., Michel, F., Schwartz, O., Lehmann, W. D., Acuto, O. (2007). A novel pathway down-modulating T cell activation involves HPK-1-dependent recruitment of 14-3-3 proteins on SLP-76. J. Exp. Med. 204: 681-691 [Abstract] [Full Text]
Stoevesandt, O., Kohler, K., Wolf, S., Andre, T., Hummel, W., Brock, R. (2007). A Network Analysis of Changes in Molecular Interactions in Cellular Signaling. Mol. Cell. Proteomics 6: 503-513 [Abstract] [Full Text]
Espagnolle, N., Depoil, D., Zaru, R., Demeur, C., Champagne, E., Guiraud, M., Valitutti, S. (2007). CD2 and TCR synergize for the activation of phospholipase C{gamma}1/calcium pathway at the immunological synapse. Int Immunol 19: 239-248 [Abstract] [Full Text]
Beach, D., Gonen, R., Bogin, Y., Reischl, I. G., Yablonski, D. (2007). Dual Role of SLP-76 in Mediating T Cell Receptor-induced Activation of Phospholipase C-{gamma}1. J. Biol. Chem. 282: 2937-2946 [Abstract] [Full Text]
DeBell, K., Graham, L., Reischl, I., Serrano, C., Bonvini, E., Rellahan, B. (2007). Intramolecular Regulation of Phospholipase C-{gamma}1 by Its C-Terminal Src Homology 2 Domain. Mol. Cell. Biol. 27: 854-863 [Abstract] [Full Text]
Wozniak, A. L., Wang, X., Stieren, E. S., Scarbrough, S. G., Elferink, C. J., Boehning, D. (2006). Requirement of biphasic calcium release from the endoplasmic reticulum for Fas-mediated apoptosis. J. Cell Biol. 175: 709-714 [Abstract] [Full Text]
Lovatt, M., Filby, A., Parravicini, V., Werlen, G., Palmer, E., Zamoyska, R. (2006). Lck Regulates the Threshold of Activation in Primary T Cells, While both Lck and Fyn Contribute to the Magnitude of the Extracellular Signal-Related Kinase Response. Mol. Cell. Biol. 26: 8655-8665 [Abstract] [Full Text]
Bunnell, S. C., Singer, A. L., Hong, D. I., Jacque, B. H., Jordan, M. S., Seminario, M.-C., Barr, V. A., Koretzky, G. A., Samelson, L. E. (2006). Persistence of cooperatively stabilized signaling clusters drives T-cell activation.. Mol. Cell. Biol. 26: 7155-7166 [Abstract] [Full Text]
Navarrete, C., Sancho, R., Caballero, F. J., Pollastro, F., Fiebich, B. L., Sterner, O., Appendino, G., Munoz, E. (2006). Basiliolides, a Class of Tetracyclic C19 Dilactones from Thapsia garganica, Release Ca2+ from the Endoplasmic Reticulum and Regulate the Activity of the Transcription Factors Nuclear Factor of Activated T Cells, Nuclear Factor-{kappa}B, and Activator Protein 1 in T Lymphocytes. J. Pharmacol. Exp. Ther. 319: 422-430 [Abstract] [Full Text]
Houtman, J. C. D., Houghtling, R. A., Barda-Saad, M., Toda, Y., Samelson, L. E. (2005). Early Phosphorylation Kinetics of Proteins Involved in Proximal TCR-Mediated Signaling Pathways. J. Immunol. 175: 2449-2458 [Abstract] [Full Text]
Tassi, I., Presti, R., Kim, S., Yokoyama, W. M., Gilfillan, S., Colonna, M. (2005). Phospholipase C-{gamma}2 Is a Critical Signaling Mediator for Murine NK Cell Activating Receptors. J. Immunol. 175: 749-754 [Abstract] [Full Text]
Upshaw, J. L., Schoon, R. A., Dick, C. J., Billadeau, D. D., Leibson, P. J. (2005). The Isoforms of Phospholipase C-{gamma} Are Differentially Used by Distinct Human NK Activating Receptors. J. Immunol. 175: 213-218 [Abstract] [Full Text]
Kiyokawa, E., Baba, T., Otsuka, N., Makino, A., Ohno, S., Kobayashi, T. (2005). Spatial and Functional Heterogeneity of Sphingolipid-rich Membrane Domains. J. Biol. Chem. 280: 24072-24084 [Abstract] [Full Text]
Serrano, C. J., Graham, L., DeBell, K., Rawat, R., Veri, M. C., Bonvini, E., Rellahan, B. L., Reischl, I. G. (2005). A New Tyrosine Phosphorylation Site in PLC{gamma}1: The Role of Tyrosine 775 in Immune Receptor Signaling. J. Immunol. 174: 6233-6237 [Abstract] [Full Text]
Gonen, R., Beach, D., Ainey, C., Yablonski, D. (2005). T Cell Receptor-induced Activation of Phospholipase C-{gamma}1 Depends on a Sequence-independent Function of the P-I Region of SLP-76. J. Biol. Chem. 280: 8364-8370 [Abstract] [Full Text]
Liu, X. K., Lin, X., Gaffen, S. L. (2004). Crucial Role for Nuclear Factor of Activated T Cells in T Cell Receptor-mediated Regulation of Human Interleukin-17. J. Biol. Chem. 279: 52762-52771 [Abstract] [Full Text]
Kim, Y. J., Sekiya, F., Poulin, B., Bae, Y. S., Rhee, S. G. (2004). Mechanism of B-Cell Receptor-Induced Phosphorylation and Activation of Phospholipase C-{gamma}2. Mol. Cell. Biol. 24: 9986-9999 [Abstract] [Full Text]
Humphries, L. A., Dangelmaier, C., Sommer, K., Kipp, K., Kato, R. M., Griffith, N., Bakman, I., Turk, C. W., Daniel, J. L., Rawlings, D. J. (2004). Tec Kinases Mediate Sustained Calcium Influx via Site-specific Tyrosine Phosphorylation of the Phospholipase C{gamma} Src Homology 2-Src Homology 3 Linker. J. Biol. Chem. 279: 37651-37661 [Abstract] [Full Text]
Koonpaew, S., Janssen, E., Zhu, M., Zhang, W. (2004). The Importance of Three Membrane-distal Tyrosines in the Adaptor Protein NTAL/LAB. J. Biol. Chem. 279: 11229-11235 [Abstract] [Full Text]
Katagiri, K., Shimonaka, M., Kinashi, T. (2004). Rap1-mediated Lymphocyte Function-associated Antigen-1 Activation by the T Cell Antigen Receptor Is Dependent on Phospholipase C-{gamma}1. J. Biol. Chem. 279: 11875-11881 [Abstract] [Full Text]
Plattner, R., Koleske, A. J., Kazlauskas, A., Pendergast, A. M. (2004). Bidirectional Signaling Links the Abelson Kinases to the Platelet-Derived Growth Factor Receptor. Mol. Cell. Biol. 24: 2573-2583 [Abstract] [Full Text]
Jullien, P., Cron, R. Q., Dabbagh, K., Cleary, A., Chen, L., Tran, P., Stepick-Biek, P., Lewis, D. B. (2003). Decreased CD154 expression by neonatal CD4+ T cells is due to limitations in both proximal and distal events of T cell activation. Int Immunol 15: 1461-1472 [Abstract] [Full Text]
Diaz-Flores, E., Siliceo, M., Martinez-A., C., Merida, I. (2003). Membrane Translocation of Protein Kinase C{theta} during T Lymphocyte Activation Requires Phospholipase C-{gamma}-generated Diacylglycerol. J. Biol. Chem. 278: 29208-29215 [Abstract] [Full Text]
Ishikawa, J., Ohga, K., Yoshino, T., Takezawa, R., Ichikawa, A., Kubota, H., Yamada, T. (2003). A Pyrazole Derivative, YM-58483, Potently Inhibits Store-Operated Sustained Ca2+ Influx and IL-2 Production in T Lymphocytes. J. Immunol. 170: 4441-4449 [Abstract] [Full Text]
Zhu, M., Janssen, E., Zhang, W. (2003). Minimal Requirement of Tyrosine Residues of Linker for Activation of T Cells in TCR Signaling and Thymocyte Development. J. Immunol. 170: 325-333 [Abstract] [Full Text]
Dienz, O., Moller, A., Strecker, A., Stephan, N., Krammer, P. H., Droge, W., Schmitz, M. L. (2003). Src Homology 2 Domain-Containing Leukocyte Phosphoprotein of 76 kDa and Phospholipase C{gamma}1 Are Required for NF-{kappa}B Activation and Lipid Raft Recruitment of Protein Kinase C{theta} Induced by T Cell Costimulation. J. Immunol. 170: 365-372 [Abstract] [Full Text]
Zhong, X.-P., Hainey, E. A., Olenchock, B. A., Zhao, H., Topham, M. K., Koretzky, G. A. (2002). Regulation of T Cell Receptor-induced Activation of the Ras-ERK Pathway by Diacylglycerol Kinase zeta. J. Biol. Chem. 277: 31089-31098 [Abstract] [Full Text]
Villalba, M., Bi, K., Hu, J., Altman, Y., Bushway, P., Reits, E., Neefjes, J., Baier, G., Abraham, R. T., Altman, A. (2002). Translocation of PKC{theta} in T cells is mediated by a nonconventional, PI3-K- and Vav-dependent pathway, but does not absolutely require phospholipase C. J. Cell Biol. 157: 253-263 [Abstract] [Full Text]
Watanabe, D., Hashimoto, S., Ishiai, M., Matsushita, M., Baba, Y., Kishimoto, T., Kurosaki, T., Tsukada, S. (2001). Four Tyrosine Residues in Phospholipase C-gamma 2, Identified as Btk-dependent Phosphorylation Sites, Are Required for B Cell Antigen Receptor-coupled Calcium Signaling. J. Biol. Chem. 276: 38595-38601 [Abstract] [Full Text]
Manninen, A., Saksela, K. (2002). HIV-1 Nef Interacts with Inositol Trisphosphate Receptor to Activate Calcium Signaling in T Cells. J. Exp. Med. 195: 1023-1032 [Abstract] [Full Text]
Villalba, M., Bi, K., Hu, J., Altman, Y., Bushway, P., Reits, E., Neefjes, J., Baier, G., Abraham, R. T., Altman, A. (2002). Translocation of PKC{theta} in T cells is mediated by a nonconventional, PI3-K- and Vav-dependent pathway, but does not absolutely require phospholipase C. J. Cell Biol. 157: 253-263 [Abstract] [Full Text]

J. Bacteriol.	J. Virol.	Eukaryot. Cell

Microbiol. Mol. Biol. Rev.	Clin. Vaccine Immunol.	All ASM Journals

Pleiotropic Contributions of Phospholipase C-1 (PLC-1) to T-Cell Antigen Receptor-Mediated Signaling: Reconstitution Studies of a PLC-1-Deficient Jurkat T-Cell Line

Pleiotropic Contributions of Phospholipase C- $gamma$ 1 (PLC- $gamma$ 1) to T-Cell Antigen Receptor-Mediated Signaling: Reconstitution Studies of a PLC- $gamma$ 1-Deficient Jurkat T-Cell Line