Unusual regulation of a STAT protein by an SLC6 family transporter in C. elegans epidermal innate immunity

Cell Host and Microbe

Volumn 9, Issue 5, 2011, Pages 425-435

  Dierking, Katja ^a,b,c,d   Polanowska, Jolanta ^a,b,c   Omi, Shizue ^a,b,c   Engelmann, Ilka ^a,b,c   Gut, Marta ^e   Lembo, Frederique ^f   Ewbank, Jonathan J ^a,b,c   Pujol, Nathalie ^a,b,c  

^a CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITY OF KIEL   (Germany)

^e CENTRE NATIONAL DE GÉNOTYPAGE   (France)

^f AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; NEUROTRANSMITTER; PROTEIN SNF 12; PROTEIN STA 2; STAT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ENDOSOME; EPIDERMIS; GENE CONTROL; IMMUNOPRECIPITATION; INNATE IMMUNITY; MYCOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SKIN INFECTION;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; EPIDERMIS; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GENE EXPRESSION REGULATION; HYPOCREALES; IMMUNITY, INNATE; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; STAT TRANSCRIPTION FACTORS;

CAENORHABDITIS ELEGANS; DRECHMERIA CONIOSPORA;

EID: 79956075019     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2011.04.011     Document Type: Article

References (46)

1. Blasius, A.L., and Beutler, B. (2010). Intracellular toll-like receptors. Immunity 32, 305-315.
2. Boutros, M., Agaisse, H., and Perrimon, N. (2002). Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev. Cell 3, 711-722. (Pubitemid 35339488)
3. Bromberg, J.F. (2001). Activation of STAT proteins and growth control. Bioessays 23, 161-169.
4. Chase, D.L., and Koelle, M.R. (2007). Biogenic amine neurotransmitters in C. elegans. In WormBook, The C. elegans Research Community, ed. 10.1895/wormbook.1.132.1, http://www.wormbook.org.
5. Couillault, C., Pujol, N., Reboul, J., Sabatier, L., Guichou, J.F., Kohara, Y., and Ewbank, J.J. (2004). TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat. Immunol. 5, 488-494.
6. Dijksterhuis, J., Veenhuis, M., and Harder, W. (1990). Ultrastructural study of adhesion and initial stages of infection of the nematode by conidia of Drechmeria coniospora. Mycol. Res. 94, 1-8.
7. Estes, K.A., Dunbar, T.L., Powell, J.R., Ausubel, F.M., and Troemel, E.R. (2010). bZIP transcription factor zip-2 mediates an early response to Pseudomonas aeruginosa infection in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 107, 2153-2158.
8. Ewbank, J.J. (2002). Tackling both sides of the host-pathogen equation with Caenorhabditis elegans. Microbes Infect. 4, 247-256.
9. Greener, T., Grant, B., Zhang, Y., Wu, X., Greene, L.E., Hirsh, D., and Eisenberg, E. (2001). Caenorhabditis elegans auxilin: a J-domain protein essential for clathrin-mediated endocytosis in vivo. Nat. Cell Biol. 3, 215-219.
10. Huang, H.R., Chen, Z.J., Kunes, S., Chang, G.D., and Maniatis, T. (2010). Endocytic pathway is required for Drosophila Toll innate immune signaling. Proc. Natl. Acad. Sci. USA 107, 8322-8327.
11. Irazoqui, J.E., Urbach, J.M., and Ausubel, F.M. (2010). Evolution of host innate defence: insights from Caenorhabditis elegans and primitive invertebrates. Nat. Rev. Immunol. 10, 47-58.
12. Kawli, T., and Tan, M.W. (2008). Neuroendocrine signals modulate the innate immunity of Caenorhabditis elegans through insulin signaling. Nat. Immunol. 9, 1415-1424.
13. Kim, D.H., Feinbaum, R., Alloing, G., Emerson, F.E., Garsin, D.A., Inoue, H., Tanaka-Hino, M., Hisamoto, N., Matsumoto, K., Tan, M.W., et al. (2002). A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297, 623-626. (Pubitemid 34815350)
14. Kurz, C.L., Shapira, M., Chen, K., Baillie, D.L., and Tan, M.W. (2007). Caenorhabditis elegans pgp-5 is involved in resistance to bacterial infection and heavy metal and its regulation requires TIR-1 and a p38 map kinase cascade. Biochem. Biophys. Res. Commun. 363, 438-443.
15. Lamitina, T., Huang, C.G., and Strange, K. (2006). Genome-wide RNAi screening identifies protein damage as a regulator of osmoprotective gene expression. Proc. Natl. Acad. Sci. USA 103, 12173-12178.
16. Lee, K.Z., Kniazeva, M., Han, M., Pujol, N., and Ewbank, J.J. (2010). The fatty acid synthase fasn-1 acts upstream of WNK and Ste20/GCK-VI kinases to modulate antimicrobial peptide expression in C. elegans epidermis. Virulence 1, 113-122.
17. Lemaitre, B., and Hoffmann, J. (2007). The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25, 697-743.
18. Lenfant, N., Polanowska, J., Bamps, S., Omi, S.Z., Borg, J.P., and Reboul, J. (2010). A genome-wide study of PDZ-domain interactions in C. elegans reveals a high frequency of non-canonical binding. BMC Genomics 11, 671.
19. Liberati, N.T., Fitzgerald, K.A., Kim, D.H., Feinbaum, R., Golenbock, D.T., and Ausubel, F.M. (2004). Requirement for a conserved Toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response. Proc. Natl. Acad. Sci. USA 101, 6593-6598.
20. Liegeois, S., Benedetto, A., Garnier, J.M., Schwab, Y., and Labouesse, M. (2006). The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J. Cell Biol. 173, 949-961.
21. McMahon, L., Legouis, R., Vonesch, J.L., and Labouesse, M. (2001). Assembly of C. elegans apical junctions involves positioning and compaction by LET-413 and protein aggregation by the MAGUK protein DLG- 1. J. Cell Sci. 114, 2265-2277. (Pubitemid 32633698)
22. Means, T.K., Mylonakis, E., Tampakakis, E., Colvin, R.A., Seung, E., Puckett, L., Tai, M.F., Stewart, C.R., Pukkila-Worley, R., Hickman, S.E., et al. (2009). Evolutionarily conserved recognition and innate immunity to fungal pathogens by the scavenger receptors SCARF1 and CD36. J. Exp. Med. 206, 637-653.
23. Melikian, H.E. (2004). Neurotransmitter transporter trafficking: endocytosis, recycling, and regulation. Pharmacol. Ther. 104, 17-27.
24. Nelson, N. (1998). The family of Na+/Cl- neurotransmitter transporters. J. Neurochem. 71, 1785-1803.
25. Partridge, F.A., Gravato-Nobre, M.J., and Hodgkin, J. (2010). Signal transduction pathways that function in both development and innate immunity. Dev. Dyn. 239, 1330-1336.
26. Plowman, G.D., Sudarsanam, S., Bingham, J., Whyte, D., and Hunter, T. (1999). The protein kinases of Caenorhabditis elegans: a model for signal transduction in multicellular organisms. Proc. Natl. Acad. Sci. USA 96, 13603-13610.
27. Powell, J.R., and Ausubel, F.M. (2008). Models of Caenorhabditis elegans infection by bacterial and fungal pathogens. Methods Mol. Biol. 415, 403-427.
28. Pujol, N., Link, E.M., Liu, L.X., Kurz, C.L., Alloing, G., Tan, M.W., Ray, K.P., Solari, R., Johnson, C.D., and Ewbank, J.J. (2001). A reverse genetic analysis of components of the Toll signalling pathway in Caenorhabditis elegans. Curr. Biol. 11, 809-821.
29. Pujol, N., Cypowyj, S., Ziegler, K., Millet, A., Astrain, A., Goncharov, A., Jin, Y., Chisholm, A.D., and Ewbank, J.J. (2008a). Distinct innate immune responses to infection and wounding in the C. elegans epidermis. Curr. Biol. 18, 481-489.
30. Pujol, N., Zugasti, O., Wong, D., Couillault, C., Kurz, C.L., Schulenburg, H., and Ewbank, J.J. (2008b). Anti-fungal innate immunity in C. elegans is enhanced by evolutionary diversification of antimicrobial peptides. PLoS Pathog. 4, e1000105. 10.1371/journal.ppat.1000105.
31. Ren, M., Feng, H., Fu, Y., Land, M., and Rubin, C.S. (2009). Protein kinase D (DKF-2), a diacylglycerol effector, is an essential regulator of C. elegans innate immunity. Immunity 30, 521-532.
32. Rohlfing, A.K., Miteva, Y., Hannenhalli, S., and Lamitina, T. (2010). Genetic and physiological activation of osmosensitive gene expression mimics transcriptional signatures of pathogen infection in C. elegans. PLoS ONE 5, e9010. 10.1371/journal.pone.0009010.
33. Sato, K., Ernstrom, G.G., Watanabe, S., Weimer, R.M., Chen, C.-H., Sato, M., Siddiqui, A., Jorgensen, E.M., and Grant, B.D. (2009). Differential requirements for clathrin in receptor-mediated endocytosis and maintenance of synaptic vesicle pools. Proc. Natl. Acad. Sci. USA 106, 1139-1144.
34. Sehgal, P.B. (2008). Paradigm shifts in the cell biology of STAT signaling. Semin. Cell Dev. Biol. 19, 329-340.
35. Shivers, R.P., Youngman, M.J., and Kim, D.H. (2008). Transcriptional responses to pathogens in Caenorhabditis elegans. Curr. Opin. Microbiol. 11, 251-256.
36. Shivers, R.P., Pagano, D.J., Kooistra, T., Richardson, C.E., Reddy, K.C., Whitney, J.K., Kamanzi, O., Matsumoto, K., Hisamoto, N., and Kim, D.H. (2010). Phosphorylation of the conserved transcription factor ATF-7 by PMK-1 p38 MAPK regulates innate immunity in Caenorhabditis elegans. PLoS Genet. 6, e1000892. 10.1371/journal.pgen.1000892.
37. Stiernagle, T. (2006). Maintenance of C. elegans. In WormBook, The C. elegans Research Community, ed. 10.1895/wormbook.1.101.1, http://www.wormbook. org.
38. Stringham, E., Pujol, N., Vandekerckhove, J., and Bogaert, T. (2002). unc-53 controls longitudinal migration in C. elegans. Development 129, 3367-3379.
39. Tong, A., Lynn, G., Ngo, V., Wong, D., Moseley, S.L., Ewbank, J.J., Goncharov, A., Wu, Y.C., Pujol, N., and Chisholm, A.D. (2009). Negative regulation of Caenorhabditis elegans epidermal damage responses by death-associated protein kinase. Proc. Natl. Acad. Sci. USA 106, 1457-1461.
40. Troemel, E.R., Chu, S.W., Reinke, V., Lee, S.S., Ausubel, F.M., and Kim, D.H. (2006). p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet. 2, e183. 10.1371/journal.pgen.0020183.
41. Wang, Y., and Levy, D.E. (2006). C. elegans STAT: evolution of a regulatory switch. FASEB J. 20, 1641-1652. (Pubitemid 44943801)
42. Wong, D., Bazopoulou, D., Pujol, N., Tavernarakis, N., and Ewbank, J.J. (2007). Genome-wide investigation reveals pathogen-specific and shared signatures in the response of Caenorhabditis elegans to infection. Genome Biol. 8, R194.
43. Wood, W.B., ed. (1988). The nematode Caenorhabditis elegans (Plainview, NY: Cold Spring Harbor Laboratory Press).
44. Xu, L., Wei, Y., Reboul, J., Vaglio, P., Shin, T.-H., Vidal, M., Elledge, S.J., and Harper, J.W. (2003). BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 425, 316-321. (Pubitemid 37158409)
45. Ziegler, K., Kurz, C.L., Cypowyj, S., Couillault, C., Pophillat, M., Pujol, N., and Ewbank, J.J. (2009). Antifungal innate immunity in C. elegans: PKCdelta linksG protein signaling and a conserved p38 MAPK cascade. Cell Host Microbe 5, 341-352.
46. Zugasti, O., and Ewbank, J.J. (2009). Neuroimmune regulation of antimicrobial peptide expression by a noncanonical TGF-beta signaling pathway in Caenorhabditis elegans epidermis. Nat. Immunol. 10, 249-256.