Caenorhabditis elegans recognizes a bacterial quorum-sensing signal molecule through theawcon neuron

Journal of Biological Chemistry

Volumn 289, Issue 38, 2014, Pages 26566-26573

  Werner, Kristen M ^a   Perez, Lark J ^b   Ghosh, Rajarshi ^c   Semmelhack, Martin F ^a   Bassler, Bonnie L ^a,d  

^a PRINCETON UNIVERSITY   (United States)

^b ROWAN UNIVERSITY   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA;

CAENORHABDITIS ELEGANS; CHEMICAL INTERACTIONS; CHEMOSENSORY NEURONS; ELEGANS; FOOD SOURCES; QUORUM-SENSING; VIBRIO CHOLERAE;

MOLECULES;

BACTERIAL PROTEIN; KETONE; PROTEIN CAI 1; UNCLASSIFIED DRUG; 3-HYDROXYTRIDECAN-4-ONE;

ARTICLE; BACTERIAL CELL; CAENORHABDITIS ELEGANS; CHEMOSENSITIVITY; CHEMOTAXIS ASSAY; CONTROLLED STUDY; NONHUMAN; ORGANISMAL INTERACTION; PROTEIN MOTIF; PROTEIN SYNTHESIS; QUORUM SENSING; SIGNAL DETECTION; SIGNAL TRANSDUCTION; VIBRIO CHOLERAE; ANIMAL; CHEMISTRY; CHEMORECEPTOR CELL; CHEMOTAXIS; CYTOLOGY; METABOLISM; PHYSIOLOGY;

ANIMALS; CAENORHABDITIS ELEGANS; CHEMORECEPTOR CELLS; CHEMOTAXIS; KETONES; QUORUM SENSING; VIBRIO CHOLERAE;

EID: 84907190329     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.573832     Document Type: Article

References (51)

1. Surette, M. G., and Bassler, B.L.(1998) Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc. Natl. Acad. Sci. U.S.A. 95, 7046-7050
2. Surette, M. G., Miller, M. B., and Bassler, B. L. (1999) Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc. Natl. Acad. Sci. U.S.A. 96, 1639-1644
3. Miller, M. B., Skorupski, K., Lenz, D. H., Taylor, R. K., and Bassler, B. L. (2002) Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110, 303-314
4. Chen, X., Schauder, S., Potier, N., Van Dorsselaer, A., Pelczer, I., Bassler, B. L., and Hughson, F. M. (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415, 545-549
5. Mok, K. C., Wingreen, N. S., and Bassler, B. L. (2003) Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. EMBO J. 22, 870-881
6. Henke, J. M., and Bassler, B. L. (2004) Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J. Bacteriol. 186, 6902-6914
7. Higgins, D. A., Pomianek, M. E., Kraml, C. M., Taylor, R. K., Semmelhack, M. F., and Bassler, B. L. (2007) The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 450, 883-886
8. Kelly, R. C., Bolitho, M. E., Higgins, D. A., Lu, W., Ng, W.-L., Jeffrey, P. D., Rabinowitz, J. D., Semmelhack, M. F., Hughson, F. M., and Bassler, B. L. (2009) The Vibrio cholerae quorum-sensing autoinducer CAI-1: analysis of the biosynthetic enzyme CqsA. Nat. Chem. Biol. 5, 891-895
9. Ng, W.-L., Perez, L. J., Wei, Y., Kraml, C., Semmelhack, M. F., and Bassler, B. L. (2011) Signal production and detection specificity in Vibrio CqsA/CqsS quorum-sensing systems. Mol. Microbiol. 79, 1407-1417
10. Wei, Y., Perez, L.J., Ng, W.-L., Semmelhack, M.F., and Bassler, B.L. (2011) Mechanism of Vibrio cholerae autoinducer-1 biosynthesis. ACS Chem. Biol. 6, 356-365
11. Schauder, S., Shokat, K., Surette, M. G., and Bassler, B. L. (2001) The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 41, 463-476
12. Waters, C. M., Lu, W., Rabinowitz, J. D., and Bassler, B. L. (2008) Quorum sensing controls biofilm formation inVibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J. Bacteriol. 190, 2527-2536
13. Hammer, B. K., and Bassler, B. L. (2009) Distinct sensory pathways in Vibrio cholerae El Tor and classical biotypes modulate cyclic dimeric GMP levels to control biofilm formation. J. Bacteriol. 191, 169-177
14. Ward, S. (1973) Chemotaxis by the nematode Caenorhabditis elegans: identification ofattractants and analysis ofthe response by use ofmutants. Proc. Natl. Acad. Sci. U.S.A. 70, 817-821
15. Dusenbery, D. B.(1974) Analysis of chemotaxisin the nematodeCaenorh-abditis elegans by countercurrent separation. J. Exp. Zool. 188, 41-47
16. Horvitz, H. R., Chalfie, M., Trent, C., Sulston, J. E., and Evans, P. D. (1982) Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 216, 1012-1014
17. Avery, L., and Horvitz, H. R. (1990) Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. J. Exp. Zool. 253, 263-270
18. Thomas, J. H. (1990) Genetic analysis of defecation in Caenorhabditis elegans. Genetics 124, 855-872
19. Bargmann, C. I., Hartwieg, E., and Horvitz, H. R. (1993) Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74, 515-527
20. Beale, E., Li, G., Tan, M.-W., and Rumbaugh, K. P. (2006) Caenorhabditis elegans senses bacterial autoinducers. Appl. Environ. Microbiol. 72, 5135-5137
21. Pradel, E., Zhang, Y., Pujol, N., Matsuyama, T., Bargmann, C. I., and Ew-bank, J. J. (2007) Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 104, 2295-2300
22. Niu, Q., Huang, X., Zhang, L., Xu, J., Yang, D., Wei, K., Niu, X., An, Z., Bennett, J. W., Zou, C., Yang, J., and Zhang, K.-Q. (2010) A Trojan horse mechanismof bacterial pathogenesis against nematodes. Proc. Natl. Acad. Sci. U.S.A. 107, 16631-16636
23. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94
24. Troemel, E. R., Kimmel, B. E., and Bargmann, C. I. (1997) Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans. Cell 91, 161-169
25. Denk, W., Strickler, J. H., and Webb, W. W. (1990) Two-photon laser scanning fluorescence microscopy. Science 248, 73-76
26. Pologruto, T. A., Sabatini, B. L., and Svoboda, K. (2003) ScanImage: flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2, 13
27. Thelin, K. H., and Taylor, R. K. (1996) Toxin-coregulated pilus, but not mannose-sensitive hemagglutinin, is required for colonization by Vibrio cholerae O1 El Tor biotype and O139 strains. Infect. Immun. 64, 2853-2856
28. Bolitho, M. E., Perez, L. J., Koch, M. J., Ng, W.-L., Bassler, B. L., and Semmelhack, M. F. (2011) Small molecule probes of the receptor binding site in the Vibrio cholerae CAI-1 quorum sensing circuit. Bioorg. Med. Chem. 19, 6906-6918
29. Swem, L. R., Swem, D. L., O'Loughlin, C. T., Gatmaitan, R., Zhao, B., Ulrich, S. M., and Bassler, B. L. (2009) A quorum-sensing antagonist targets both membrane-bound and cytoplasmic receptors and controls bacterial pathogenicity. Mol. Cell 35, 143-153
30. Bargmann, C. I. (2006) Chemosensation in C. elegans. WormBook 1-29
31. Zhang, Y., Lu, H., and Bargmann, C. I. (2005) Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438, 179-184
32. Choe, A., Chuman, T., von Reuss, S. H., Dossey, A. T., Yim, J. J., Ajredini, R., Kolawa, A. A., Kaplan, F., Alborn, H. T., Teal, P. E., Schroeder, F. C., Sternberg, P.W., and Edison, A.S. (2012) Sex-specific mating pheromones in the nematode Panagrellus redivivus. Proc. Natl. Acad. Sci. U.S.A. 109, 20949-20954
33. Ng, W.-L., Wei, Y., Perez, L. J., Cong, J., Long, T., Koch, M., Semmelhack, M. F., Wingreen, N. S., and Bassler, B. L. (2010) Probing bacterial trans-membrane histidine kinase receptor-ligand interactions with natural and synthetic molecules. Proc. Natl. Acad. Sci. U.S.A. 107, 5575-5580
34. Chang, S., Johnston, R. J., Jr., and Hobert, O. (2003) A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans. Genes Dev. 17, 2123-2137
35. Lanjuin, A., VanHoven, M. K., Bargmann, C. I., Thompson, J. K., and Sengupta, P.(2003) Otx/otd homeobox genes specify distinct sensory neuron identities in C. elegans. Dev. Cell 5, 621-633
36. Lewis, J.A., and Hodgkin, J. A. (1977) Specific neuroanatomical changes in chemosensory mutants of the nematode Caenorhabditis elegans. J. Comp. Neurol. 172, 489-510
37. Uchida, O., Nakano, H., Koga, M., and Ohshima, Y. (2003) The C. elegans che-1 gene encodes a zinc finger transcription factor required for specification of the ASE chemosensory neurons. Development 130, 1215-1224
38. Chuang, C.-F., Vanhoven, M. K., Fetter, R. D., Verselis, V. K., and Barg-mann, C. I. (2007) An innexin-dependent cell network establishes left-right neuronal asymmetry in C. elegans. Cell 129, 787-799
39. Troemel, E. R., Sagasti, A., and Bargmann, C. I. (1999) Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odor-ant receptor expression in C. elegans. Cell 99, 387-398
40. Sagasti, A., Hisamoto, N., Hyodo, J., Tanaka-Hino, M., Matsumoto, K., and Bargmann, C. I.(2001) The CaMKII UNC-43 activates the MAPKKK NSY-1 to execute a lateral signaling decision required for asymmetric olfactory neuron fates. Cell 105, 221-232
41. Wes, P. D., and Bargmann, C. I. (2001) C. elegans odour discrimination requires asymmetric diversity in olfactory neurons. Nature 410, 698-701
42. Leinwand, S. G., and Chalasani, S. H. (2013) Neuropeptide signaling remodels chemosensory circuit composition in Caenorhabditis elegans. Nat. Neurosci. 16, 1461-1467
43. Golden, J. W., and Riddle, D. L. (1984) The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. Dev. Biol. 102, 368-378
44. Jeong, P.-Y., Jung, M., Yim, Y.-H., Kim, H., Park, M., Hong, E., Lee, W., Kim, Y. H., Kim, K., and Paik, Y.-K. (2005) Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone. Nature 433, 541-545
45. Butcher, R. A., Fujita, M., Schroeder, F. C., and Clardy, J. (2007) Small-molecule pheromones that control dauer development in Caenorhabditis elegans. Nat. Chem. Biol. 3, 420-422
46. Srinivasan, J., Kaplan, F., Ajredini, R., Zachariah, C., Alborn, H. T., Teal, P. E., Malik, R. U., Edison, A. S., Sternberg, P. W., and Schroeder, F. C. (2008) A blend ofsmall molecules regulates both mating and development in Caenorhabditis elegans. Nature 454, 1115-1118
47. Butcher, R. A., Ragains, J. R., Li, W., Ruvkun, G., Clardy, J., and Mak, H. Y. (2009) Biosynthesis ofthe Caenorhabditis elegans dauer pheromone. Proc. Natl. Acad. Sci. U.S.A. 106, 1875-1879
48. Zagoriy, V., Matyash, V., and Kurzchalia, T. (2010) Long-chain O-asca-rosyl-alkanediols are constitutive components of Caenorhabditis elegans but do not induce dauer larva formation. Chem. Biodivers. 7, 2016-2022
49. Artyukhin, A. B., Yim, J. J., Srinivasan, J., Izrayelit, Y., Bose, N., von Reuss, S. H., Jo, Y., Jordan, J. M., Baugh, L. R., Cheong, M., Sternberg, P. W., Avery, L., and Schroeder, F. C. (2013) Succinylated octopamine ascaro-sides and a new pathway of biogenic amine metabolism in C. elegans. J. Biol. Chem. 288, 18778-18783
50. Hanahan, D. (1985) DNA Cloning: A practical approach, pp. 109-135, IRL Press, Oxford, UK
51. Boyer, H.W., and Roulland-Dussoix, D. (1969) A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41, 459-472