Tissue-Specific Activities of an Immune Signaling Module Regulate Physiological Responses to Pathogenic and Nutritional Bacteria in C. elegans

Cell Host and Microbe

Volumn 6, Issue 4, 2009, Pages 321-330

  Shivers, Robert P ^a   Kooistra, Tristan ^a   Chu, Stephanie W ^a   Pagano, Daniel J ^a   Kim, Dennis H ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

MICROBIO; MOLIMMUNO

Indexed keywords

ADAPTOR PROTEIN; GENE PRODUCT; PROTEIN NSY 1; PROTEIN SARM; PROTEIN SEK 1; PROTEIN TPH 1; TOLL INTERLEUKIN 1 RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; EGG LAYING; GENE EXPRESSION REGULATION; HOST PATHOGEN INTERACTION; HOST RESISTANCE; IMMUNE RESPONSE; INFECTION RESISTANCE; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY;

ANIMALS; BACTERIA; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CYTOSKELETAL PROTEINS; IMMUNITY, INNATE; MAP KINASE KINASE 3; MAP KINASE KINASE KINASE 5; NERVE TISSUE; SIGNAL TRANSDUCTION;

CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 72649094825     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2009.09.001     Document Type: Article

References (53)

1. Akira S., Uematsu S., and Takeuchi O. Pathogen recognition and innate immunity. Cell 124 (2006) 783-801
2. Anyanful A., Easley K.A., Benian G.M., and Kalman D. Conditioning protects C. elegans from lethal effects of enteropathogenic E. coli by activating genes that regulate lifespan and innate immunity. Cell Host Microbe 5 (2009) 450-462
3. Avery L. The genetics of feeding in Caenorhabditis elegans. Genetics 133 (1993) 897-917
4. Bargmann, C. (2006). Chemosensation in C. elegans. In WormBook, The C. elegans Research Community, ed. 10.1895/wormbook.1.123.1, http://www.wormbook.org.
5. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77 (1974) 71-94
6. Carty M., Goodbody R., Schroder M., Stack J., Moynagh P.N., and Bowie A.G. The human adaptor SARM negatively regulates adaptor protein TRIF-dependent Toll-like receptor signaling. Nat. Immunol. 7 (2006) 1074-1081
7. Chen G., Zhuchenko O., and Kuspa A. Immune-like phagocyte activity in the social amoeba. Science 317 (2007) 678-681
8. Chuang C.F., and Bargmann C.I. A Toll-interleukin 1 repeat protein at the synapse specifies asymmetric odorant receptor expression via ASK1 MAPKKK signaling. Genes Dev. 19 (2005) 270-281
9. Couillault C., Pujol N., Reboul J., Sabatier L., Guichou J.F., Kohara Y., and Ewbank J.J. 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 (2004) 488-494
10. Dethlefsen L., McFall-Ngai M., and Relman D.A. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449 (2007) 811-818
11. Haycraft C.J., Swoboda P., Taulman P.D., Thomas J.H., and Yoder B.K. The C. elegans homolog of the murine cystic kidney disease gene Tg737 functions in a ciliogenic pathway and is disrupted in osm-5 mutant worms. Development 128 (2001) 1493-1505
12. Hobert O. PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32 (2002) 728-730
13. Hoffmann J.A., Kafatos F.C., Janeway C.A., and Ezekowitz R.A. Phylogenetic perspectives in innate immunity. Science 284 (1999) 1313-1318
14. Hotamisligil G.S. Inflammation and metabolic disorders. Nature 444 (2006) 860-867
15. Hotamisligil G.S., and Erbay E. Nutrient sensing and inflammation in metabolic diseases. Nat. Rev. Immunol. 8 (2008) 923-934
16. Kawli T., and Tan M.W. Neuroendocrine signals modulate the innate immunity of Caenorhabditis elegans through insulin signaling. Nat. Immunol. 9 (2008) 1415-1424
17. 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., and Ausubel F.M. A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297 (2002) 623-626
18. Kim D.H., Liberati N.T., Mizuno T., Inoue H., Hisamoto N., Matsumoto K., and Ausubel F.M. Integration of Caenorhabditis elegans MAPK pathways mediating immunity and stress resistance by MEK-1 MAPK kinase and VHP-1 MAPK phosphatase. Proc. Natl. Acad. Sci. USA 101 (2004) 10990-10994
19. Kim Y., Zhou P., Qian L., Chuang J.Z., Lee J., Li C., Iadecola C., Nathan C., and Ding A. MyD88-5 links mitochondria, microtubules, and JNK3 in neurons and regulates neuronal survival. J. Exp. Med. 204 (2007) 2063-2074
20. Liberati N.T., Fitzgerald K.A., Kim D.H., Feinbaum R., Golenbock D.T., and Ausubel F.M. Requirement for a conserved Toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response. Proc. Natl. Acad. Sci. USA 101 (2004) 6593-6598
21. Liberles S.D., Horowitz L.F., Kuang D., Contos J.J., Wilson K.L., Siltberg-Liberles J., Liberles D.A., and Buck L.B. Formyl peptide receptors are candidate chemosensory receptors in the vomeronasal organ. Proc. Natl. Acad. Sci. USA 106 (2009) 9842-9847
22. Maduro M., and Pilgrim D. Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141 (1995) 977-988
23. Mallo G.V., Kurz C.L., Couillault C., Pujol N., Granjeaud S., Kohara Y., and Ewbank J.J. Inducible antibacterial defense system in C. elegans. Curr. Biol. 12 (2002) 1209-1214
24. Matsuzawa A., Saegusa K., Noguchi T., Sadamitsu C., Nishitoh H., Nagai S., Koyasu S., Matsumoto K., Takeda K., and Ichijo H. ROS-dependent activation of the TRAF6-ASK1-p38 pathway is selectively required for TLR4-mediated innate immunity. Nat. Immunol. 6 (2005) 587-592
25. McGhee J.D., Birchall J.C., Chung M.A., Cottrell D.A., Edgar L.G., Svendsen P.C., and Ferrari D.C. Production of null mutants in the major intestinal esterase gene (ges-1) of the nematode Caenorhabditis elegans. Genetics 125 (1990) 505-514
26. Mello C.C., Kramer J.M., Stinchcomb D., and Ambros V. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10 (1991) 3959-3970
27. Migeotte I., Communi D., and Parmentier M. Formyl peptide receptors: a promiscuous subfamily of G protein-coupled receptors controlling immune responses. Cytokine Growth Factor Rev. 17 (2006) 501-519
28. Mink M., Fogelgren B., Olszewski K., Maroy P., and Csiszar K. A novel human gene (SARM) at chromosome 17q11 encodes a protein with a SAM motif and structural similarity to Armadillo/beta-catenin that is conserved in mouse, Drosophila, and Caenorhabditis elegans. Genomics 74 (2001) 234-244
29. Miyata S., Begun J., Troemel E.R., and Ausubel F.M. DAF-16-dependent suppression of immunity during reproduction in Caenorhabditis elegans. Genetics 178 (2008) 903-918
30. Nicholas H.R., and Hodgkin J. The ERK MAP kinase cascade mediates tail swelling and a protective response to rectal infection in C. elegans. Curr. Biol. 14 (2004) 1256-1261
31. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (2001) e45
32. Pradel E., Zhang Y., Pujol N., Matsuyama T., Bargmann C.I., and Ewbank J.J. Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 104 (2007) 2295-2300
33. 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. A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Curr. Biol. 11 (2001) 809-821
34. Pujol N., Cypowyj S., Ziegler K., Millet A., Astrain A., Goncharov A., Jin Y., Chisholm A.D., and Ewbank J.J. Distinct innate immune responses to infection and wounding in the C. elegans epidermis. Curr. Biol. 18 (2008) 481-489
35. Reddy K.C., Andersen E.C., Kruglyak L., and Kim D.H. A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans. Science 323 (2009) 382-384
36. Ren M., Feng H., Fu Y., Land M., and Rubin C.S. Protein kinase D is an essential regulator of C. elegans innate immunity. Immunity 30 (2009) 521-532
37. Ringstad N., and Horvitz H.R. FMRFamide neuropeptides and acetylcholine synergistically inhibit egg-laying by C. elegans. Nat. Neurosci. 11 (2008) 1168-1176
38. Riviere S., Challet L., Fluegge D., Spehr M., and Rodriguez I. Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors. Nature 459 (2009) 574-577
39. Sagasti A., Hisamoto N., Hyodo J., Tanaka-Hino M., Matsumoto K., and Bargmann C.I. The CaMKII UNC-43 activates the MAPKKK NSY-1 to execute a lateral signaling decision required for asymmetric olfactory neuron fates. Cell 105 (2001) 221-232
40. Sawin E.R., Ranganathan R., and Horvitz H.R. C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26 (2000) 619-631
41. Styer K.L., Singh V., Macosko E., Steele S.E., Bargmann C.I., and Aballay A. Innate immunity in Caenorhabditis elegans is regulated by neurons expressing NPR-1/GPCR. Science 322 (2008) 460-464
42. Sze J.Y., Victor M., Loer C., Shi Y., and Ruvkun G. Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403 (2000) 560-564
43. Tan M.W., Mahajan-Miklos S., and Ausubel F.M. Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc. Natl. Acad. Sci. USA 96 (1999) 715-720
44. Tanaka-Hino M., Sagasti A., Hisamoto N., Kawasaki M., Nakano S., Ninomiya-Tsuji J., Bargmann C.I., and Matsumoto K. SEK-1 MAPKK mediates Ca2+ signaling to determine neuronal asymmetric development in Caenorhabditis elegans. EMBO Rep. 3 (2002) 56-62
45. Trent C., Tsuing N., and Horvitz H.R. Egg-laying defective mutants of the nematode Caenorhabditis elegans. Genetics 104 (1983) 619-647
46. Troemel E.R., Chu S.W., Reinke V., Lee S.S., Ausubel F.M., and Kim D.H. p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet. 2 (2006) e183 10.1371/journal.pgen.0020183
47. Troemel E.R., Felix M.A., Whiteman N.K., Barriere A., and Ausubel F.M. Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans. PLoS Biol. 6 (2008) 2736-2752
48. Weiner H.L., and Selkoe D.J. Inflammation and therapeutic vaccination in CNS diseases. Nature 420 (2002) 879-884
49. Willems E., Leyns L., and Vandesompele J. Standardization of real-time PCR gene expression data from independent biological replicates. Anal. Biochem. 379 (2008) 127-129
50. Zhang X., and Zhang Y. Neural-immune communication in Caenorhabditis elegans. Cell Host Microbe 5 (2009) 425-429
51. Zhang Y., Lu H., and Bargmann C.I. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438 (2005) 179-184
52. Ziegler K., Kurz C.L., Cypowyj S., Couillault C., Pophillat M., Pujol N., and Ewbank J.J. Antifungal innate immunity in C. elegans: PKCdelta links G protein signaling and a conserved p38 MAPK cascade. Cell Host Microbe 5 (2009) 341-352
53. Zugasti O., and Ewbank J.J. Neuroimmune regulation of antimicrobial peptide expression by a noncanonical TGF-beta signaling pathway in Caenorhabditis elegans epidermis. Nat. Immunol. 10 (2009) 249-256