Drosophila peptidoglycan recognition protein LC (PGRP-LC) acts as a signal-transducing innate immune receptor - PubMed (original) (raw)
Drosophila peptidoglycan recognition protein LC (PGRP-LC) acts as a signal-transducing innate immune receptor
Kwang-Min Choe et al. Proc Natl Acad Sci U S A. 2005.
Abstract
Drosophila peptidoglycan recognition protein LC (PGRP-LC), a transmembrane protein required for the response to bacterial infection, acts at the top of a cytoplasmic signaling cascade that requires the death-domain protein Imd and an IkappaB kinase to activate Relish, an NF-kappaB family member. It is not clear how binding of peptidoglycan to the extracellular domain of PGRP-LC activates intracellular signaling because its cytoplasmic domain has no homology to characterized proteins. Here, we demonstrate that PGRP-LC binds Imd and that its cytoplasmic domain is critical for its activity, suggesting that PGRP-LC acts as a signal-transducing receptor. The PGRP-LC cytoplasmic domain is also essential for the formation of dimers, and results suggest that dimerization may be required for receptor activation. The PGRP-LC cytoplasmic domain can mediate formation of heterodimers between different PGRP-LC isoforms, thereby potentially expanding the diversity of ligands that can be recognized by the receptor.
Figures
Fig. 1.
Domains of PGRP-LCx required for antimicrobial peptide gene induction. (a) PGRP-LC deletion constructs. PGRP-LC is a type II transmembrane protein with a previously uncharacterized N-terminal cytoplasmic domain, a transmembrane domain (TM) and a C-terminal PGRP domain. A V5 epitope was added in the C terminus of full-length and deletion constructs. (b) Protein expression in transiently transfected S2 cells was confirmed by Western blotting with anti-V5 antibody. (c) Induction of CecA1 was measured on Northern blots with RNA samples prepared from S2 cells expressing the PGRP-LCx deletion constructs. RNAs were purified from the cells after protein expression and, as shown in lanes 9–16, treatment with E. coli (102-fold dilution of OD600 = 1.5, 6 h of incubation). Rp49 was used as a loading control.
Fig. 2.
Domains of Imd required for antimicrobial peptide gene induction. (a) Imd deletion constructs. The C-terminal 80-aa death domain (DD) is shown. V5 tag was added in the C terminus of full-length and deletion constructs. (b) Protein expression in transiently transfected S2 cells was confirmed by Western blotting with anti-V5 antibody. (c) Induction of CecA1 was measured on Northern blots. Deletion of the N-terminal half, the C-terminal half including the death domain, or only the death domain all abolished CecA1 induction.
Fig. 3.
Physical interaction of PGRP-LC and Imd. Lysates were prepared from S2 cells transiently transfected with expression vectors for V5-tagged Imd and c-Myc-tagged PGRP-LCa or PGRP-LCx (20 μg each). Anti-c-Myc antibody was used to immunoprecipitate PGRP-LC, and anti-V5 antibody was used to detect Imd on Western blots.
Fig. 4.
Identification of the domain of Imd that interacts with PGRP-LC. Lysates were prepared from cells transiently transfected with expression vectors for a V5-tagged Imd deletion construct and c-Myc-tagged PGRP-LCx (20 μg each). Anti-c-Myc antibody was used to immunoprecipitate the full-length PGRP-LCx, and anti-V5 antibody was used to detect Imd on Western blots. Deletion of the N-terminal half of Imd abolished the interaction, whereas deletion of the C-terminal half did not prevent interaction, suggesting that the N-terminal part is responsible for the interaction with PGRP-LC.
Fig. 5.
Homotypic and heterotypic interactions between PGRP-LCa and PGRP-LCx. Lysates were prepared from cells transiently transfected with expression vectors for the two PGRP-LC isoforms tagged with either V5 or c-Myc (20 μg each) and subjected to coimmunoprecipitation.
Fig. 6.
Mapping of the region of PGRP-LCx required for homotypic interactions. Lysates derived from cells transiently transfected with expression vectors for a V5-tagged deletion construct and the c-Myc-tagged full-length PGRP-LCx (20 μg each) were prepared and subjected to coimmunoprecipitation. Anti-c-Myc antibody was used to immunoprecipitate the full-length PGRP-LCx and anti-V5 antibody was used to detect the deletion constructs of PGRP-LCx by Western blotting. Note that deletion of the extracellular domain did not significantly affect the interaction, whereas deletion of the cytoplasmic domain abolished it (arrows mark IP products in lanes 7, 8, 10, and 11). Deletion of the distal half of the cytoplasmic domain did not prevent the interaction (lane 8), suggesting that the proximal half of the cytoplasmic domain is crucial for the interaction.
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References
- Janeway, C. A., Jr., (1989) Cold Spring Harbor Symp. Quant. Biol. 54, 1–13. - PubMed
- Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J. M. & Hoffmann, J. A. (1996) Cell 86, 973–983. - PubMed
- Rutschmann, S., Kilinc, A. & Ferrandon, D. (2002) J. Immunol. 168, 1542–1546. - PubMed
- Levashina, E. A., Langley, E., Green, C., Gubb, D., Ashburner, M., Hoffmann, J. A. & Reichhart, J. M. (1999) Science 285, 1917–1919. - PubMed
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