Behavioral and immune responses to infection require Gαq- RhoA signaling in C. elegans

PLoS Pathogens

Volumn 8, Issue 2, 2012, Pages

  McMullan, Rachel ^a,b   Anderson, Alexandra ^b   Nurrish, Stephen ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; G ALPHA Q RHOA PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; RAF PROTEIN; RAS PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT;

ARTICLE; BACTERIAL INFECTION; BACTERIUM; BEHAVIOR; CAENORHABDITIS ELEGANS; CELL STRUCTURE; CONTROLLED STUDY; EPITHELIUM CELL; IMMUNE RESPONSE; LOCOMOTION; MICROBACTERIUM NEMATOPHILUM; MOTONEURON; NONHUMAN; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL BEHAVIOR; CORYNEBACTERIUM INFECTION; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; TRANSGENIC ANIMAL;

CAENORHABDITIS ELEGANS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; CORYNEBACTERIUM INFECTIONS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 84860903825     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002530     Document Type: Article

References (69)

1. Beutler B, (2004) Innate immunity: an overview. Mol Immunol 40: 845-859.
2. Beutler B, Crozat K, Koziol JA, Georgel P, (2005) Genetic dissection of innate immunity to infection: the mouse cytomegalovirus model. Curr Opin Immunol 17: 36-43.
3. Boman HG, (2000) Innate immunity and the normal microflora. Immunol Rev 173: 5-16.
4. Irazoqui JE, Ausubel FM, (2010) 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: Caenorhabditis elegans as a model to study tissues involved in host immunity and microbial pathogenesis. Clin Exp Immunol 160: 48-57.
5. Irazoqui JE, Troemel ER, Feinbaum RL, Luhachack LG, Cezairliyan BO, et al. (2010) Distinct pathogenesis and host responses during infection of C. elegans by P. aeruginosa and S. aureus. PLoS Pathog 6: e1000982.
6. Pradel E, Ewbank JJ, (2004) Genetic models in pathogenesis. Annu Rev Genet 38: 347-363.
7. Tan MW, Shapira M, (2011) Genetic and molecular analysis of nematode-microbe interactions. Cell Microbiol 13: 497-507.
8. Gravato-Nobre MJ, Hodgkin J, (2005) Caenorhabditis elegans as a model for innate immunity to pathogens. Cell Microbiol 7: 741-751.
9. Hodgkin J, Kuwabara PE, Corneliussen B, (2000) A novel bacterial pathogen, Microbacterium nematophilum, induces morphological change in the nematode C. elegans. Curr Biol 10: 1615-1618.
10. O'Callaghan D, Vergunst A, (2010) Non-mammalian animal models to study infectious disease: worms or fly fishing? Curr Opin Microbiol 13: 79-85.
11. Sifri CD, Begun J, Ausubel FM, (2005) The worm has turned-microbial virulence modeled in Caenorhabditis elegans. Trends Microbiol 13: 119-127.
12. Tan MW, Mahajan-Miklos S, Ausubel FM, (1999) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci U S A 96: 715-720.
13. Tan MW, Rahme LG, Sternberg JA, Tompkins RG, Ausubel FM, (1999) Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc Natl Acad Sci U S A 96: 2408-2413.
14. Engelmann I, Griffon A, Tichit L, Montanana-Sanchis F, Wang G, et al. (2011) A comprehensive analysis of gene expression changes provoked by bacterial and fungal infection in C. elegans. PLoS One 6: e19055.
15. Ewbank JJ, Zugasti O, (2011) C. elegans: model host and tool for antimicrobial drug discovery. Dis Model Mech 4: 300-304.
16. Philpott DJ, Girardin SE, Sansonetti PJ, (2001) Innate immune responses of epithelial cells following infection with bacterial pathogens. Curr Opin Immunol 13: 410-416.
17. Sternberg EM, (2006) Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nat Rev Immunol 6: 318-328.
18. Curtis V, de Barra M, Aunger R, (2011) Disgust as an adaptive system for disease avoidance behaviour. Philos Trans R Soc Lond B Biol Sci 366: 389-401.
19. Pradel E, Zhang Y, Pujol N, Matsuyama T, Bargmann CI, et al. (2007) Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. Proc Natl Acad Sci USA 104: 2295-2300.
20. Pujol N, Link EM, Liu LX, Kurz CL, Alloing G, et al. (2001) A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Curr Biol 11: 809-821.
21. Schulenburg H, Ewbank JJ, (2007) The genetics of pathogen avoidance in Caenorhabditis elegans. Mol Microbiol 66: 563-570.
22. Zhang Y, Lu H, Bargmann CI, (2005) Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438: 179-184.
23. Yook K, Hodgkin J, (2007) Mos1 mutagenesis reveals a diversity of mechanisms affecting response of Caenorhabditis elegans to the bacterial pathogen Microbacterium nematophilum. Genetics 175: 681-697.
24. Shivers RP, Kooistra T, Chu SW, Pagano DJ, Kim DH, (2009) Tissue-specific activities of an immune signaling module regulate physiological responses to pathogenic and nutritional bacteria in C. elegans. Cell Host Microbe 6: 321-330.
25. Zugasti O, Ewbank JJ, (2009) Neuroimmune regulation of antimicrobial peptide expression by a noncanonical TGF-beta signaling pathway in Caenorhabditis elegans epidermis. Nat Immunol 10: 249-256.
26. Anyanful A, Easley KA, Benian GM, Kalman D, (2009) Conditioning Protects C. elegans from Lethal Effects of Enteropathogenic E. coli by Activating Genes that Regulate Lifespan and Innate Immunity. Cell Host and Microbe 5: 450-462.
27. Rand JB, (2007) Acetylcholine. WormBook pp. 1-21.
28. Perez-Mansilla B, Nurrish S, (2009) A network of G-protein signaling pathways control neuronal activity in C. elegans. Adv Genet 65: 145-192.
29. Lackner MR, Nurrish SJ, Kaplan JM, (1999) Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 24: 335-346.
30. Ziegler K, Kurz CL, Cypowyj S, Couillault C, Pophillat M, et al. (2009) Antifungal innate immunity in C. elegans: PKCdelta links G protein signaling and a conserved p38 MAPK cascade. Cell Host Microbe 5: 341-352.
31. McMullan R, Hiley E, Morrison P, Nurrish SJ, (2006) Rho is a presynaptic activator of neurotransmitter release at pre-existing synapses in C. elegans. Genes Dev 20: 65-76.
32. Williams SL, Lutz S, Charlie NK, Vettel C, Ailion M, et al. (2007) Trio's Rho-Specific GEF Domain is the Missing Gaq Effector in C.elegans. Genes Dev 21: 2731-2746.
33. Bastiani CA, Gharib S, Simon MI, Sternberg PW, (2003) Caenorhabditis elegans Galphaq regulates egg-laying behavior via a PLCbeta-independent and serotonin-dependent signaling pathway and likely functions both in the nervous system and in muscle. Genetics 165: 1805-1822.
34. Steven R, Zhang L, Culotti J, Pawson T, (2005) The UNC-73/Trio RhoGEF-2 domain is required in separate isoforms for the regulation of pharynx pumping and normal neurotransmission in C. elegans. Genes Dev 19: 2016-2029.
35. Harris G, Mills H, Wragg R, Hapiak V, Castelletto M, et al. (2010) The monoaminergic modulation of sensory-mediated aversive responses in Caenorhabditis elegans requires glutamatergic/peptidergic cotransmission. J Neurosci 30: 7889-7899.
36. O'Rourke D, Baban D, Demidova M, Mott R, Hodgkin J, (2006) Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum. Genome Res 16: 1005-16.
37. Zhang X, Zhang Y, (2009) Neural-immune communication in Caenorhabditis elegans. Cell Host Microbe 5: 425-429.
38. Fleming JT, Squire MD, Barnes TM, Tornoe C, Matsuda K, et al. (1997) Caenorhabditis elegans levamisole resistance genes lev-1, unc-29, and unc-38 encode functional nicotinic acetylcholine receptor subunits. J Neurosci 17: 5843-5857.
39. Akimkina T, Yook K, Curnock S, Hodgkin J, (2006) Genome characterization, analysis of virulence and transformation of Microbacterium nematophilum, a coryneform pathogen of the nematode Caenorhabditis elegans. FEMS Microbiol Lett 264: 145-151.
40. Nurrish S, Segalat L, Kaplan JM, (1999) Serotonin inhibition of synaptic transmission: Galpha(0) decreases the abundance of UNC-13 at release sites. Neuron 24: 231-242.
41. Nguyen M, Alfonso A, Johnson CD, Rand JB, (1995) Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase. Genetics 140: 527-535.
42. Nicholas HR, Hodgkin J, (2004) The ERK MAP kinase cascade mediates tail swelling and a protective response to rectal infection in C. elegans. Curr Biol 14: 1256-1261.
43. Teng Y, Girard L, Ferreira HB, Sternberg PW, Emmons SW, (2004) Dissection of cis-regulatory elements in the C. elegans Hox gene egl-5 promoter. Dev Biol 276: 476-492.
44. Brundage L, Avery L, Katz A, Kim UJ, Mendel JE, et al. (1996) Mutations in a C. elegans Gqalpha gene disrupt movement, egg laying, and viability. Neuron 16: 999-1009.
45. McMullan R, Nurrish SJ, (2007) Rho deep in thought. Genes Dev 21: 2677-2682.
46. Motegi F, Sugimoto A, (2006) Sequential functioning of the ECT-2 RhoGEF, RHO-1 and CDC-42 establishes cell polarity in Caenorhabditis elegans embryos. Nat Cell Biol 8: 978-985.
47. Norman KR, Fazzio RT, Mellem JE, Espelt MV, Strange K, et al. (2005) The Rho/Rac-family guanine nucleotide exchange factor VAV-1 regulates rhythmic behaviors in C. elegans. Cell 123: 119-132.
48. Spencer AG, Orita S, Malone CJ, Han M, (2001) A RHO GTPase-mediated pathway is required during P cell migration in Caenorhabditis elegans. Proc Natl Acad Sci U S A 98: 13132-13137.
49. Lundquist EA, (2006) Small GTPases. WormBook pp. 1-18.
50. Braga V, (2000) Epithelial cell shape: cadherins and small GTPases. Exp Cell Res 261: 83-90.
51. Gravato-Nobre MJ, Hodgkin J, (2008) The acyltransferase gene bus-1 exhibits conserved and specific expression in nematode rectal cells and reveals pathogen-induced cell swelling. Dev Dyn 237: 3762-3776.
52. Bargmann CI, (2006) Chemosensation in C. elegans. WormBook pp. 1-29.
53. Qiu RG, Chen J, McCormick F, Symons M, (1995) A role for Rho in Ras transformation. Proc Natl Acad Sci U S A 92: 11781-11785.
54. Canevascini S, Marti M, Frohli E, Hajnal A, (2005) The Caenorhabditis elegans homologue of the proto-oncogene ect-2 positively regulates RAS signalling during vulval development. EMBO Rep 6: 1169-1175.
55. Kawli T, Tan M, (2008) Neuroendocrine signals modulate the innate immunity of Caenorhabditis elegans through insulin signaling. Nat Immunol pp. 1415-1424.
56. Ha HI, Hendricks M, Shen Y, Gabel CV, Fang-Yen C, et al. (2010) Functional organization of a neural network for aversive olfactory learning in Caenorhabditis elegans. Neuron 68: 1173-1186.
57. Li W, Chong H, Guan KL, (2001) Function of the Rho family GTPases in Ras-stimulated Raf activation. J Biol Chem 276: 34728-34737.
58. Bar-Sagi D, Hall A, (2000) Ras and Rho GTPases: a family reunion. Cell 103: 227-238.
59. Pujol N, Cypowyj S, Ziegler K, Millet A, Astrain A, et al. (2008) Distinct innate immune responses to infection and wounding in the C. elegans epidermis. Curr Biol 18: 481-489.
60. Pujol N, Zugasti O, Wong D, Couillault C, Kurz CL, et al. (2008) Anti-fungal innate immunity in C. elegans is enhanced by evolutionary diversification of antimicrobial peptides. PLoS Pathog 4: e1000105.
61. Han M, Aroian RV, Sternberg PW, (1990) The let-60 locus controls the switch between vulval and nonvulval cell fates in Caenorhabditis elegans. Genetics 126: 899-913.
62. Beitel GJ, Clark SG, Horvitz HR, (1990) Caenorhabditis elegans ras gene let-60 acts as a switch in the pathway of vulval induction. Nature 348: 503-509.
63. Barbacid M, (1987) ras genes. Annu Rev Biochem 56: 779-827.
64. Toda T, Uno I, Ishikawa T, Powers S, Kataoka T, et al. (1985) In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 40: 27-36.
65. Hawasli AH, Saifee O, Liu C, Nonet ML, Crowder CM, (2004) Resistance to volatile anesthetics by mutations enhancing excitatory neurotransmitter release in Caenorhabditis elegans. Genetics 168: 831-843.
66. Bokoch GM, (2005) Regulation of innate immunity by Rho GTPases. Trends Cell Biol 15: 163-171.
67. Kawli T, He F, Tan MW, (2010) It takes nerves to fight infections: insights on neuro-immune interactions from C. elegans. Dis Model Mech 3: 721-731.
68. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
69. Segalat L, Elkes DA, Kaplan JM, (1995) Modulation of serotonin-controlled behaviors by Go in Caenorhabditis elegans. Science 267: 1648-1651.