Overlapping and unique signatures in the proteomic and transcriptomic responses of the nematode Caenorhabditis elegans toward pathogenic Bacillus thuringiensis

Developmental and Comparative Immunology

Volumn 51, Issue 1, 2015, Pages 1-9

  Yang, Wentao ^a   Dierking, Katja ^a   Esser, Daniela ^a   Tholey, Andreas ^a   Leippe, Matthias ^a   Rosenstiel, Philip ^a   Schulenburg, Hinrich ^a  

^a UNIVERSITY OF KIEL   (Germany)

Author keywords

Bacillus thuringiensis; C type lectins; Caenorhabditis elegans; Innate immunity; Proteomics; RNA Seq

Indexed keywords

ADENYLATE KINASE; C TYPE LECTIN DOMAIN CONTAINING PROTEIN; MESSENGER RNA; PROTEOME; REGULATOR PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; ADENOSINE PHOSPHATE; CAENORHABDITIS ELEGANS PROTEIN; LECTIN; PROTEIN KINASE;

ARTICLE; BACILLUS THURINGIENSIS; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ENZYME ASSAY; GENE EXPRESSION; GENE PRODUCT; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; INNATE IMMUNITY; MICROARRAY ANALYSIS; MOLECULAR DYNAMICS; NONHUMAN; PARASITE IDENTIFICATION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEOMICS; QUANTITATIVE ANALYSIS; RNA SEQUENCE; SEQUENCE ANALYSIS; TRANSCRIPTOMICS; ANIMAL; GENE EXPRESSION PROFILING; GENETICS; GRAM POSITIVE INFECTION; IMMUNOLOGY; METABOLISM; RNA PROCESSING; SPECIES DIFFERENCE;

BACILLUS THURINGIENSIS; CAENORHABDITIS ELEGANS; POSIBACTERIA;

ADENOSINE MONOPHOSPHATE; ANIMALS; BACILLUS THURINGIENSIS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; GENE EXPRESSION PROFILING; GRAM-POSITIVE BACTERIAL INFECTIONS; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; LECTINS, C-TYPE; PROTEIN KINASES; PROTEOME; RNA PROCESSING, POST-TRANSCRIPTIONAL; SPECIES SPECIFICITY; TRANSCRIPTOME;

EID: 84924237678     PISSN: 0145305X     EISSN: 18790089     Source Type: Journal    
DOI: 10.1016/j.dci.2015.02.010     Document Type: Article

References (76)

1. Apfeld J., O'Connor G., McDonagh T., DiStefano P.S., Curtis R. The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans. Genes Dev 2004, 18:3004-3009.
2. Barrett T., Wilhite S.E., Ledoux P., Evangelista C., Kim I.F., Tomashevsky M., et al. NCBI GEO: archive for functional genomics data sets - update. Nucleic Acids Res 2013, 41:D991-D995.
3. Bartee E., McCormack A., Früh K. Quantitative membrane proteomics reveals new cellular targets of viral immune modulators. PLoS Pathog 2006, 2:e107.
4. Bhavsar A.P., Guttman J.A., Finlay B.B. Manipulation of host-cell pathways by bacterial pathogens. Nature 2007, 449:827-834.
5. Bischof L.J., Kao C.-Y., Los F.C., Gonzalez M.R., Shen Z., Briggs S.P., et al. Activation of the unfolded protein response is required for defenses against bacterial pore-forming toxin in vivo. PLoS Pathog 2008, 4:e1000176.
6. Boehnisch C., Wong D., Habig M., Isermann K., Michiels N.K., Roeder T., et al. Protist-type lysozymes of the nematode Caenorhabditis elegans contribute to resistance against pathogenic Bacillus thuringiensis. PLoS ONE 2011, 6:e24619.
7. Bogaerts A., Temmerman L., Boerjan B., Husson S.J., Schoofs L., Verleyen P. A differential proteomics study of Caenorhabditis elegans infected with Aeromonas hydrophila. Dev. Comp. Immunol 2010, 34:690-698.
8. Boutros M., Agaisse H., Perrimon N. Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev. Cell 2002, 3:711-722.
9. Brown G.D., Gordon S. Immune recognition: a new receptor for β-glucans. Nature 2001, 413:36-37.
10. Chen Z., Hagler J., Palombella V.J., Melandri F., Scherer D., Ballard D., et al. Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev 1995, 9:1586-1597.
11. Couillault C., Pujol N., Reboul J., Sabatier L., Guichou J.-F., 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, 5:488-494.
12. Couillault C., Fourquet P., Pophillat M., Ewbank J.J. A UPR-independent infection-specific role for a BiP/GRP78 protein in the control of antimicrobial peptide expression in C. elegans epidermis. Virulence 2012, 3:299-308.
13. de Hoon M.J., Imoto S., Nolan J., Miyano S. Open source clustering software. Bioinformatics 2004, 20:1453-1454.
14. De Gregorio E., Spellman P.T., Rubin G.M., Lemaitre B. Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. PNAS 2001, 98:12590-12595.
15. De Gregorio E., Spellman P.T., Tzou P., Rubin G.M., Lemaitre B. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J. 2002, 21:2568-2579.
16. Dramsi S., Cossart P. Intracellular pathogens and the actin cytoskeleton. Annu. Rev. Cell Dev. Biol 1998, 14:137-166.
17. Dustin M.L., Cooper J.A. The immunological synapse and the actin cytoskeleton: molecular hardware for T cell signaling. Nat. Immunol 2000, 1:23-29.
18. Eden E., Navon R., Steinfeld I., Lipson D., Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 2009, 10:48.
19. Edgar R., Domrachev M., Lash A.E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30:207-210.
20. Encinas P., Rodriguez-Milla M.A., Novoa B., Estepa A., Figueras A., Coll J. Zebrafish fin immune responses during high mortality infections with viral haemorrhagic septicemia rhabdovirus. A proteomic and transcriptomic approach. BMC Genomics 2010, 11:518.
21. Engelmann I., Griffon A., Tichit L., Montanana-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.
22. Ghazalpour A., Bennett B., Petyuk V.A., Orozco L., Hagopian R., Mungrue I.N., et al. Comparative analysis of proteome and transcriptome variation in mouse. PLoS Genet 2011, 7:e1001393.
23. Griffitts J.S., Haslam S.M., Yang T., Garczynski S.F., Mulloy B., Morris H., et al. Glycolipids as receptors for Bacillus thuringiensis crystal toxin. Science 2005, 307:922-925.
24. Gygi S.P., Rochon Y., Franza B.R., Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol 1999, 19:1720-1730.
25. Halaschek-Wiener J., Khattra J.S., McKay S., Pouzyrev A., Stott J.M., Yang G.S., et al. Analysis of long-lived C. elegans daf-2 mutants using serial analysis of gene expression. Genome Res 2005, 15:603-615.
26. Hasshoff M., Böhnisch C., Tonn D., Hasert B., Schulenburg H. The role of Caenorhabditis elegans insulin-like signaling in the behavioral avoidance of pathogenic Bacillus thuringiensis. FASEB J. 2007, 21:1801-1812.
27. Hooper L.V., Wong M.H., Thelin A., Hansson L., Falk P.G., Gordon J.I. Molecular analysis of commensal host-microbial relationships in the intestine. Science 2001, 291:881-884.
28. Hooper L.V., Stappenbeck T.S., Hong C.V., Gordon J.I. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat. Immunol 2003, 4:269-273.
29. Hosack D.A., Dennis G., Sherman B.T., Lane H.C., Lempicki R.A. Identifying biological themes within lists of genes with EASE. Genome Biol 2003, 4:R70.
30. Huffman D.L., Abrami L., Sasik R., Corbeil J., van der Goot F.G., Aroian R.V. Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:10995-11000.
31. Iatsenko I., Sinha A., Rödelsperger C., Sommer R.J. New role for DCR-1/dicer in Caenorhabditis elegans innate immunity against the highly virulent bacterium Bacillus thuringiensis DB27. Infect. Immun 2013, 81:3942-3957.
32. Irazoqui J.E., Troemel E.R., Feinbaum R.L., Luhachack L.G., Cezairliyan B.O., Ausubel F.M. Distinct pathogenesis and host responses during infection of C. elegans by P. aeruginosa and S. aureus. PLoS Pathog 2010, 6:e1000982.
33. Irving P., Troxler L., Heuer T.S., Belvin M., Kopczynski C., Reichhart J.-M., et al. A genome-wide analysis of immune responses in Drosophila. PNAS 2001, 98:15119-15124.
34. Izzi L., Attisano L. Regulation of the TGFβ signalling pathway by ubiquitin-mediated degradation. Oncogene 2004, 23:2071-2078.
35. Janeway C.A., Medzhitov R. Innate immune recognition. Annu. Rev. Immunol 2002, 20:197-216.
36. Kao C.-Y., Los F.C., Huffman D.L., Wachi S., Kloft N., Husmann M., et al. Global functional analyses of cellular responses to pore-forming toxins. PLoS Pathog 2011, 7:e1001314.
37. Kim D., Pertea G., Trapnell C., Pimentel H., Kelley R., Salzberg S.L. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 2013, 14:R36.
38. Kurz C.L., Ewbank J.J. Caenorhabditis elegans: an emerging genetic model for the study of innate immunity. Nat. Rev. Genet 2003, 4:380-390.
39. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25.
40. Mallo G.V., Kurz C.L., Couillault C., Pujol N., Granjeaud S., Kohara Y., et al. Inducible antibacterial defense system in C. elegans. Curr. Biol 2002, 12:1209-1214.
41. Marsh E.K., May R.C. Caenorhabditis elegans, a model organism for investigating immunity. Appl. Environ. Microbiol 2012, 78:2075-2081.
42. McElwee J., Bubb K., Thomas J.H. Transcriptional outputs of the Caenorhabditis elegans forkhead protein DAF-16. Aging Cell 2003, 2:111-121.
43. McElwee J.J., Schuster E., Blanc E., Thomas J.H., Gems D. Shared transcriptional signature in Caenorhabditis elegans Dauer larvae and long-lived daf-2 mutants implicates detoxification system in longevity assurance. J. Biol. Chem 2004, 279:44533-44543.
44. Mochii M., Yoshida S., Morita K., Kohara Y., Ueno N. Identification of transforming growth factor-β-regulated genes in Caenorhabditis elegans by differential hybridization of arrayed cDNAs. PNAS 1999, 96:15020-15025.
45. Mukherjee S., Zheng H., Derebe M.G., Callenberg K.M., Partch C.L., Rollins D., et al. Antibacterial membrane attack by a pore-forming intestinal C-type lectin. Nature 2013, 505:103-107.
46. Mukhopadhyay D., Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007, 315:201-205.
47. Murphy C.T., McCarroll S.A., Bargmann C.I., Fraser A., Kamath R.S., Ahringer J., et al. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 2003, 424:277-283.
48. 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, 16:1005-1016.
49. Pujol N., Zugasti O., Wong D., Couillault C., Kurz C.L., Schulenburg H., et al. Anti-fungal innate immunity in C. elegans is enhanced by evolutionary diversification of antimicrobial peptides. PLoS Pathog 2008, 4:e1000105.
50. Ragno S., Romano M., Howell S., Pappin D.J., Jenner P.J., Colston M.J. Changes in gene expression in macrophages infected with Mycobacterium tuberculosis: a combined transcriptomic and proteomic approach. Immunology 2001, 104:99-108.
51. Richardson C.E., Kooistra T., Kim D.H. An essential role for XBP-1 in host protection against immune activation in C. elegans. Nature 2010, 463:1092-1095.
52. Robinson M.D., Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 2010, 11:R25.
53. Sahu S.N., Lewis J., Patel I., Bozdag S., Lee J.H., LeClerc J.E., et al. Genomic analysis of immune response against Vibrio cholerae hemolysin in Caenorhabditis elegans. PLoS ONE 2012, 7:e38200.
54. Saijo S., Ikeda S., Yamabe K., Kakuta S., Ishigame H., Akitsu A., et al. Dectin-2 recognition of α-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 2010, 32:681-691.
55. Saldanha A.J. Java Treeview-extensible visualization of microarray data. Bioinformatics 2004, 20:3246-3248.
56. Scherl A., François P., Charbonnier Y., Deshusses J.M., Koessler T., Huyghe A., et al. Exploring glycopeptide-resistance in Staphylococcus aureus: a combined proteomics and transcriptomics approach for the identification of resistance-related markers. BMC Genomics 2006, 7:296.
57. Schulenburg H., Müller S. Natural variation in the response of Caenorhabditis elegans towards Bacillus thuringiensis. Parasitology 2004, 128:433-443.
58. Schulenburg H., Hoeppner M.P., Weiner J., 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, 213:237-250.
59. Shapira M., Hamlin B.J., Rong J., Chen K., Ronen M., Tan M.-W. A conserved role for a GATA transcription factor in regulating epithelial innate immune responses. PNAS 2006, 103:14086-14091.
60. Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37:1-13.
61. Simonsen K.T., Møller-Jensen J., Kristensen A.R., Andersen J.S., Riddle D.L., Kallipolitis B.H. Quantitative proteomics identifies ferritin in the innate immune response of C. elegans. Virulence 2011, 2:120-130.
62. Sinha A., Rae R., Iatsenko I., Sommer R.J. System wide analysis of the evolution of innate immunity in the nematode model species Caenorhabditis elegans and Pristionchus pacificus. PLoS ONE 2012, 7:e44255.
63. Stein L., Sternberg P., Durbin R., Thierry-Mieg J., Spieth J. WormBase: network access to the genome and biology of Caenorhabditis elegans. Nucleic Acids Res 2001, 29:82-86.
64. Stiernagle T. Maintenance of C. elegans. WormBook 2006, The C. elegans Research Community. WormBook.
65. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:15545-15550.
66. Team R.C. R: a language and environment for statistical computing 2012.
67. Trapnell C., Hendrickson D.G., Sauvageau M., Goff L., Rinn J.L., Pachter L. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat. Biotechnol 2013, 31:46-53.
68. Treitz C., Cassidy L., Höckendorf A., Leippe M., Tholey A. Quantitative proteome analysis of Caenorhabditis elegans upon exposure to nematicidal Bacillus thuringiensis. J. Proteomics 2015, 113:337-350.
69. Troemel E.R., Chu S.W., Reinke V., Lee S.S., Ausubel F.M., Kim D.H. p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet 2006, 2:e183.
70. van Die I., van Vliet S.J., Nyame A.K., Cummings R.D., Bank C.M., Appelmelk B., et al. The dendritic cell-specific C-type lectin DC-SIGN is a receptor for Schistosoma mansoni egg antigens and recognizes the glycan antigen Lewis x. Glycobiology 2003, 13:471-478.
71. Vierstraete E., Verleyen P., Baggerman G., D'Hertog W., Van den Bergh G., Arckens L., et al. A proteomic approach for the analysis of instantly released wound and immune proteins in Drosophila melanogaster hemolymph. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:470-475.
72. Vogel C., Marcotte E.M. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet 2012, 13:227-232.
73. Wang J., Nakad R., Schulenburg H. Activation of the Caenorhabditis elegans FOXO family transcription factor DAF-16 by pathogenic Bacillus thuringiensis. Dev. Comp. Immunol 2012, 37:193-201.
74. Wang Z., Gerstein M., Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet 2009, 10:57-63.
75. Weis W.I., Taylor M.E., Drickamer K. The C-type lectin superfamily in the immune system. Immunol. Rev 1998, 163:19-34.
76. Ziegler K., Kurz C.L., Cypowyj S., Couillault C., Pophillat M., Pujol N., et al. Antifungal innate immunity in C. elegans: PKCδ links G protein signaling and a conserved p38 MAPK cascade. Cell Host Microbe 2009, 5:341-352.