Strength in numbers: "Omics" studies of C. elegans innate immunity

Virulence

Volumn 3, Issue 6, 2012, Pages 477-484

  Simonsen, Karina T ^a   Gallego, Sandra F ^b   Færgeman, Nils J ^b   Kallipolitis, Birgitte H ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

C. elegans; Innate immunity; Model host; Proteomics; Transcriptomics

Indexed keywords

BACILLUS THURINGIENSIS TOXIN; COLLAGEN; CYTOCHROME P450; GLUCURONOSYLTRANSFERASE; HELMINTH PROTEIN; LYSOZYME; METALLOTHIONEIN I; METALLOTHIONEIN II; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE C DELTA; TRANSCRIPTION FACTOR DAF 16; TRANSCRIPTION FACTOR FOXO; TRANSFORMING GROWTH FACTOR BETA; CAENORHABDITIS ELEGANS PROTEIN; PROTEOME; TRANSCRIPTOME;

ARTICLE; BACILLUS THURINGIENSIS; BACTERIAL INFECTION; CAENORHABDITIS ELEGANS; CRYPTOCOCCUS NEOFORMANS; DOMAIN OF UNKNOWN FUNCTION 274 GENE; DOWN REGULATION; ENTEROCOCCUS FAECALIS; GENE; GENOME ANALYSIS; HOST PATHOGEN INTERACTION; HUMAN; INNATE IMMUNITY; MASS SPECTROMETRY; METRIDIN LIKE SHK TOXIN DOMAIN; MICROARRAY ANALYSIS; MICROCYSTIS AERUGINOSA; MYCOSIS; NONHUMAN; PECTOBACTERIUM CAROTOVORUM; PHOTORHABDUS LUMINESCENS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEOMICS; RNA INTERFERENCE; RNA SEQUENCE; SERRATIA MARCESCENS; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; UPREGULATION; ANIMAL; BACTERIUM; FUNGUS; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; REVIEW;

ANIMALS; BACTERIA; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; FUNGI; GENE EXPRESSION PROFILING; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; PROTEOME; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84870534296     PISSN: 21505594     EISSN: 21505608     Source Type: Journal    
DOI: 10.4161/viru.21906     Document Type: Article

References (71)

1. Mahajan-Miklos S, Tan MW, Rahme LG, Ausubel FM. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 1999; 96:47-56; PMID:9989496; http://dx.doi.org/10.1016/S0092-8674(00)80958-7
2. Tan MW, Rahme LG, Sternberg JA, Tompkins RG, Ausubel FM. Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc Natl Acad Sci U S A 1999; 96: 2408-13; PMID:10051655; http://dx.doi.org/10. 1073/pnas.96.5.2408
3. Félix MA, Braendle C. The natural history of Caenorhabditis elegans. Curr Biol 2010; 20:R965-9; PMID:21093785; http://dx.doi.org/10.1016/j.cub.2010.09.050
4. Sifri CD, Begun J, Ausubel FM. The worm has turned-microbial virulence modeled in Caenorhabditis elegans. Trends Microbiol 2005; 13:119-27; PMID:15737730; http://dx.doi.org/10.1016/j.tim.2005.01.003
5. Nicholas HR, Hodgkin J. Responses to infection and possible recognition strategies in the innate immune system of Caenorhabditis elegans. Mol Immunol 2004; 41:479-93; PMID:15183927; http://dx.doi.org/10. 1016/j.molimm.2004.03.037
6. Pukkila-Worley R, Peleg AY, Tampakakis E, Mylonakis E. Candida albicans hyphal formation and virulence assessed using a Caenorhabditis elegans infection model. Eukaryot Cell 2009; 8:1750-8; PMID:19666778; http://dx.doi.org/10.1128/EC.00163-09
7. Engelmann I, Griffon A, Tichit L, Montañana-Sanchis F, Wang G, Reinke V, et al. A comprehensive analysis of gene expression changes provoked by bacterial and fungal infection in C. elegans. PLoS One 2011; 6: e19055; PMID:21602919; http://dx.doi.org/10.1371/journal.pone.0019055
8. Pukkila-Worley R, Ausubel FM, Mylonakis E. Candida albicans infection of Caenorhabditis elegans induces antifungal immune defenses. PLoS Pathog 2011; 7: e1002074; PMID:21731485; http://dx.doi.org/10. 1371/journal.ppat.1002074
9. Jia K, Thomas C, Akbar M, Sun Q, Adams-Huet B, Gilpin C, et al. Autophagy genes protect against Salmonella typhimurium infection and mediate insulin signaling-regulated pathogen resistance. Proc Natl Acad Sci U S A 2009; 106:14564-9; PMID:19667176
10. Irazoqui JE, Troemel ER, Feinbaum RL, Luhachack LG, Cezairliyan BO, Ausubel FM. Distinct pathogenesis and host responses during infection of C. elegans by P. aeruginosa and S. aureus. PLoS Pathog 2010; 6: e1000982; PMID:20617181; http://dx.doi.org/10. 1371/journal.ppat.1000982
11. Troemel ER, Félix MA, Whiteman NK, Barrière A, Ausubel FM. Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans. PLoS Biol 2008; 6:2736-52; PMID:19071962; http://dx.doi. org/10.1371/journal.pbio.0060309
12. Mallo GV, Kurz CL, Couillault C, Pujol N, Granjeaud S, Kohara Y, et al. Inducible antibacterial defense system in C. elegans. Curr Biol 2002; 12:1209-14; PMID:12176330; http://dx.doi.org/10.1016/S0960-9822(02)00928-4
13. Pujol N, Cypowyj S, Ziegler K, Millet A, Astrain A, Goncharov A, et al. Distinct innate immune responses to infection and wounding in the C. elegans epidermis. Curr Biol 2008; 18:481-9; PMID:18394898; http://dx.doi.org/10.1016/j.cub.2008.02.079
14. O'Rourke D, Baban D, Demidova M, Mott R, Hodgkin J. Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum. Genome Res 2006; 16:1005-16; PMID: 16809667; http://dx.doi.org/10.1101/gr.50823006
15. Shapira M, Hamlin BJ, Rong J, Chen K, Ronen M, Tan MW. A conserved role for a GATA transcription factor in regulating epithelial innate immune responses. Proc Natl Acad Sci U S A 2006; 103:14086-91; PMID:16968778; http://dx.doi.org/10.1073/pnas.0603424103
16. Troemel ER, Chu SW, Reinke V, Lee SS, Ausubel FM, Kim DH. p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet 2006; 2:e183; PMID:17096597; http://dx.doi.org/10.1371/journal.pgen.0020183
17. Bolz DD, Tenor JL, Aballay A. A conserved PMK-1/p38 MAPK is required in caenorhabditis elegans tissuespecific immune response to Yersinia pestis infection. J Biol Chem 2010; 285:10832-40; PMID:20133945; http://dx.doi.org/10.1074/jbc.M109.091629
18. Boehnisch C, Wong D, Habig M, Isermann K, Michiels NK, Roeder T, et al. Protist-type lysozymes of the nematode Caenorhabditis elegans contribute to resistance against pathogenic Bacillus thuringiensis. PLoS One 2011; 6:e24619; PMID:21931778; http://dx.doi.org/10.1371/journal.pone.0024619
19. Wong D, Bazopoulou D, Pujol N, Tavernarakis N, Ewbank JJ. Genome-wide investigation reveals pathogen-specific and shared signatures in the response of Caenorhabditis elegans to infection. Genome Biol 2007; 8:R194; PMID:17875205; http://dx.doi.org/10.1186/gb-2007-8-9-r194
20. Huffman DL, Abrami L, Sasik R, Corbeil J, van der Goot FG, Aroian RV. Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. Proc Natl Acad Sci U S A 2004; 101:10995-1000; PMID:15256590; http://dx.doi.org/10.1073/pnas. 0404073101
21. Bogaerts A, Beets I, Temmerman L, Schoofs L, Verleyen P. Proteome changes of Caenorhabditis elegans upon a Staphylococcus aureus infection. Biol Direct 2010; 5:11; PMID:20163716; http://dx.doi.org/10. 1186/1745-6150-5-11
22. Bogaerts A, Temmerman L, Boerjan B, Husson SJ, Schoofs L, Verleyen P. A differential proteomics study of Caenorhabditis elegans infected with Aeromonas hydrophila. Dev Comp Immunol 2010; 34:690-8; PMID:20149819; http://dx.doi.org/10.1016/j.dci. 2010.02.003
23. Simonsen KT, Møller-Jensen J, Kristensen AR, Andersen JS, Riddle DL, Kallipolitis BH. Quantitative proteomics identifies ferritin in the innate immune response of C. elegans. Virulence 2011; 2:120-30; PMID:21389771; http://dx.doi.org/10.4161/viru.2.2.15270
24. Jensen VL, Simonsen KT, Lee YH, Park D, Riddle DL. RNAi screen of DAF-16/FOXO target genes in C. elegans links pathogenesis and dauer formation. PLoS One 2010; 5:e15902; PMID:21209831; http://dx.doi. org/10.1371/journal.pone.0015902
25. Zeitoun-Ghandour S, Charnock JM, Hodson ME, Leszczyszyn OI, Blindauer CA, Stürzenbaum SR. The two Caenorhabditis elegans metallothioneins (CeMT-1 and CeMT-2) discriminate between essential zinc and toxic cadmium. FEBS J 2010; 277:2531-42; PMID: 20553489; http://dx.doi.org/10.1111/j.1742-4658.2010.07667.x
26. Canpolat E, Lynes MA. In vivo manipulation of endogenous metallothionein with a monoclonal antibody enhances a T-dependent humoral immune response. Toxicol Sci 2001; 62:61-70; PMID: 11399794; http://dx.doi.org/10.1093/toxsci/62.1.61
27. Zugasti O, Ewbank JJ. Neuroimmune regulation of antimicrobial peptide expression by a noncanonical TGF-beta signaling pathway in Caenorhabditis elegans epidermis. Nat Immunol 2009; 10:249-56; PMID: 19198592; http://dx.doi.org/10.1038/ni.1700
28. Evans EA, Kawli T, Tan MW. Pseudomonas aeruginosa suppresses host immunity by activating the DAF-2 insulin-like signaling pathway in Caenorhabditis elegans. PLoS Pathog 2008; 4:e1000175; PMID:18927620; http://dx.doi.org/10.1371/journal.ppat.1000175
29. Alper S, McBride SJ, Lackford B, Freedman JH, Schwartz DA. Specificity and complexity of the Caenorhabditis elegans innate immune response. Mol Cell Biol 2007; 27:5544-53; PMID:17526726; http://dx.doi.org/10.1128/MCB.02070-06
30. Zelensky AN, Gready JE. The C-type lectin-like domain superfamily. FEBS J 2005; 272:6179-217; PMID:16336259; http://dx.doi.org/10.1111/j.1742-4658.2005.05031.x
31. Drickamer K, Dodd RB. C-Type lectin-like domains in Caenorhabditis elegans: predictions from the complete genome sequence. Glycobiology 1999; 9:1357-69; PMID:10561461; http://dx.doi.org/10.1093/glycob/9.12.1357
32. Schulenburg H, Hoeppner MP, Weiner J, 3rd, Bornberg-Bauer E. Specificity of the innate immune system and diversity of C-type lectin domain (CTLD) proteins in the nematode Caenorhabditis elegans. Immunobiology 2008; 213:237-50; PMID:18406370; http://dx.doi.org/10.1016/j.imbio.2007.12.004
33. Cash HL, Whitham CV, Behrendt CL, Hooper LV. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 2006; 313:1126-30; PMID: 16931762; http://dx.doi.org/10.1126/science.1127119
34. Bork P, Beckmann G. The CUB domain. A widespread module in developmentally regulated proteins. J Mol Biol 1993; 231:539-45; PMID:8510165; http://dx.doi. org/10.1006/jmbi.1993.1305
35. Nandakumar M, Tan MW. Gamma-linolenic and stearidonic acids are required for basal immunity in Caenorhabditis elegans through their effects on p38 MAP kinase activity. PLoS Genet 2008; 4:e1000273; PMID:19023415; http://dx.doi.org/10.1371/journal. pgen.1000273
36. Wang Q, Hasan G, Pikielny CW. Preferential expression of biotransformation enzymes in the olfactory organs of Drosophila melanogaster, the antennae. J Biol Chem 1999; 274:10309-15; PMID:10187818; http://dx.doi.org/10.1074/jbc.274.15.10309
37. Beale E, Li G, Tan MW, Rumbaugh KP. Caenorhabditis elegans senses bacterial autoinducers. Appl Environ Microbiol 2006; 72:5135-7; PMID: 16820523; http://dx.doi.org/10.1128/AEM.00611-06
38. Rumbaugh KP. Fatal attraction: bacterial bait lures worms to their death. Proc Natl Acad Sci U S A 2010; 107:16411-2; PMID:20823245; http://dx.doi.org/10. 1073/pnas.1011935107
39. Zhang Y, Lu H, Bargmann CI. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 2005; 438:179-84; PMID:16281027; http://dx.doi.org/10.1038/nature04216
40. Ideo H, Fukushima K, Gengyo-Ando K, Mitani S, Dejima K, Nomura K, et al. A Caenorhabditis elegans glycolipid-binding galectin functions in host defense against bacterial infection. J Biol Chem 2009; 284: 26493-501; PMID:19635802; http://dx.doi.org/10. 1074/jbc.M109.038257
41. Shivers RP, Youngman MJ, Kim DH. Transcriptional responses to pathogens in Caenorhabditis elegans. Curr Opin Microbiol 2008; 11:251-6; PMID:18567532; http://dx.doi.org/10.1016/j.mib.2008.05.014
42. Schulenburg H, Boehnisch C. Diversification and adaptive sequence evolution of Caenorhabditis lysozymes (Nematoda: Rhabditidae). BMC Evol Biol 2008; 8:114; PMID:18423043; http://dx.doi.org/10.1186/1471-2148-8-114
43. Marsh EK, van den Berg MC, May RC. A two-gene balance regulates Salmonella typhimurium tolerance in the nematode Caenorhabditis elegans. PLoS One 2011; 6:e16839; PMID:21399680; http://dx.doi.org/10. 1371/journal.pone.0016839
44. Irazoqui JE, Urbach JM, Ausubel FM. Evolution of host innate defence: insights from Caenorhabditis elegans and primitive invertebrates. Nat Rev Immunol 2010; 10:47-58; PMID:20029447; http://dx.doi.org/10.1038/nri2689
45. Pujol N, Link EM, Liu LX, Kurz CL, Alloing G, Tan MW, et al. A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Curr Biol 2001; 11:809-21; PMID:11516642; http://dx.doi.org/10.1016/S0960-9822(01)00241-X
46. Tenor JL, Aballay A. A conserved Toll-like receptor is required for Caenorhabditis elegans innate immunity. EMBO Rep 2008; 9:103-9; PMID:17975555; http://dx.doi.org/10.1038/sj.embor.7401104
47. Couillault C, Pujol N, Reboul J, Sabatier L, Guichou JF, Kohara Y, et al. TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat Immunol 2004; 5:488-94; PMID:15048112; http://dx.doi.org/10.1038/ni1060
48. Kim DH, Feinbaum R, Alloing G, Emerson FE, Garsin DA, Inoue H, et al. A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 2002; 297:623-6; PMID:12142542; http://dx. doi.org/10.1126/science.1073759
49. Shivers RP, Pagano DJ, Kooistra T, Richardson CE, Reddy KC, Whitney JK, et al. Phosphorylation of the conserved transcription factor ATF-7 by PMK-1 p38 MAPK regulates innate immunity in Caenorhabditis elegans. PLoS Genet 2010; 6:e1000892; PMID: 20369020; http://dx.doi.org/10.1371/journal.pgen. 1000892
50. Liberati NT, Fitzgerald KA, Kim DH, Feinbaum R, Golenbock DT, Ausubel FM. Requirement for a conserved Toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response. Proc Natl Acad Sci U S A 2004; 101:6593-8; PMID:15123841; http://dx.doi.org/10.1073/pnas.0308625101
51. Ren M, Feng H, Fu Y, Land M, Rubin CS. Protein kinase D is an essential regulator of C. elegans innate immunity. Immunity 2009; 30:521-32; PMID: 19371715; http://dx.doi.org/10.1016/j.immuni.2009.03.007
52. Ziegler K, Kurz CL, Cypowyj S, Couillault C, Pophillat M, Pujol N, et al. Antifungal innate immunity in C. elegans: PKCdelta links G protein signaling and a conserved p38 MAPK cascade. Cell Host Microbe 2009; 5:341-52; PMID:19380113; http://dx.doi.org/10.1016/j.chom.2009.03.006
53. Roberts AF, Gumienny TL, Gleason RJ, Wang H, Padgett RW. Regulation of genes affecting body size and innate immunity by the DBL-1/BMP-like pathway in Caenorhabditis elegans. BMC Dev Biol 2010; 10:61; PMID:20529267; http://dx.doi.org/10.1186/1471-213X-10-61
54. Dong MQ, Venable JD, Au N, Xu T, Park SK, Cociorva D, et al. Quantitative mass spectrometry identifies insulin signaling targets in C. elegans. Science 2007; 317:660-3; PMID:17673661; http://dx.doi.org/10.1126/science.1139952
55. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, et al. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 2003; 424:277-83; PMID:12845331; http://dx.doi.org/10.1038/nature01789
56. Oh SW, Mukhopadhyay A, Dixit BL, Raha T, Green MR, Tissenbaum HA. Identification of direct DAF-16 targets controlling longevity, metabolism and diapause by chromatin immunoprecipitation. Nat Genet 2006; 38:251-7; PMID:16380712; http://dx.doi.org/10. 1038/ng1723
57. Chen CS, Bellier A, Kao CY, Yang YL, Chen HD, Los FC, et al. WWP-1 is a novel modulator of the DAF-2 insulin-like signaling network involved in pore-forming toxin cellular defenses in Caenorhabditis elegans. PLoS One 2010; 5:e9494; PMID:20209166; http://dx.doi. org/10.1371/journal.pone.0009494
58. Garsin DA, Villanueva JM, Begun J, Kim DH, Sifri CD, Calderwood SB, et al. Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 2003; 300:1921; PMID:12817143; http://dx.doi.org/10.1126/science.1080147
59. Evans EA, Chen WC, Tan MW. The DAF-2 insulinlike signaling pathway independently regulates aging and immunity in C. elegans. Aging Cell 2008; 7:879-93; PMID:18782349; http://dx.doi.org/10.1111/j. 1474-9726.2008.00435.x
60. Estes KA, Dunbar TL, Powell JR, Ausubel FM, Troemel ER. bZIP transcription factor zip-2 mediates an early response to Pseudomonas aeruginosa infection in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2010; 107:2153-8; PMID:20133860; http://dx.doi.org/10. 1073/pnas.0914643107
61. Dunbar TL, Yan Z, Balla KM, Smelkinson MG, Troemel ER. C. elegans detects pathogen-induced translational inhibition to activate immune signaling. Cell Host Microbe 2012; 11:375-86; PMID: 22520465; http://dx.doi.org/10.1016/j.chom.2012.02. 008
62. McEwan DL, Kirienko NV, Ausubel FM. Host translational inhibition by Pseudomonas aeruginosa Exotoxin A Triggers an immune response in Caenorhabditis elegans. Cell Host Microbe 2012; 11: 364-74; PMID:22520464; http://dx.doi.org/10.1016/j.chom.2012.02.007
63. Kleino A, Silverman N. UnZIPping mechanisms of effector-triggered immunity in animals. Cell Host Microbe 2012; 11:320-2; PMID:22520459; http://dx.doi.org/10.1016/j.chom.2012.04.002
64. Melo JA, Ruvkun G. Inactivation of conserved C. elegans genes engages pathogen-and xenobiotic-associated defenses. Cell 2012; 149:452-66; PMID: 22500807; http://dx.doi.org/10.1016/j.cell.2012.02. 050
65. Mohri-Shiomi A, Garsin DA. Insulin signaling and the heat shock response modulate protein homeostasis in the Caenorhabditis elegans intestine during infection. J Biol Chem 2008; 283:194-201; PMID:17951251; http://dx.doi.org/10.1074/jbc.M707956200
66. Rohlfing AK, Miteva Y, Hannenhalli S, Lamitina T. Genetic and physiological activation of osmosensitive gene expression mimics transcriptional signatures of pathogen infection in C. elegans. PLoS One 2010; 5: e9010; PMID:20126308; http://dx.doi.org/10.1371/journal.pone.0009010
67. Singh V, Aballay A. Heat-shock transcription factor (HSF)-1 pathway required for Caenorhabditis elegans immunity. Proc Natl Acad Sci U S A 2006; 103:13092-7; PMID:16916933; http://dx.doi.org/10.1073/pnas. 0604050103
68. Kudlow BA, Zhang L, Han M. Systematic analysis of tissue-restricted miRISCs reveals a broad role for microRNAs in suppressing basal activity of the C. elegans pathogen response. Mol Cell 2012; 46:530-41; PMID:22503424; http://dx.doi.org/10.1016/j.molcel.2012.03.011
69. Welker NC, Habig JW, Bass BL. Genes misregulated in C. elegans deficient in Dicer, RDE-4, or RDE-1 are enriched for innate immunity genes. RNA 2007; 13: 1090-102; PMID:17526642; http://dx.doi.org/10. 1261/rna.542107
70. Larance M, Bailly AP, Pourkarimi E, Hay RT, Buchanan G, Coulthurst S, et al. Stable-isotope labeling with amino acids in nematodes. Nat Methods 2011; 8: 849-51; PMID:21874007; http://dx.doi.org/10.1038/nmeth.1679
71. Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4:44-57; PMID:19131956; http://dx.doi.org/10.1038/nprot.2008.211