Genome-wide transcriptional analysis of drosophila larvae infected by entomopathogenic nematodes shows involvement of complement, recognition and extracellular matrix proteins

Journal of Innate Immunity

Volumn 6, Issue 2, 2014, Pages 192-204

  Arefin, Badrul ^a   Kucerova, Lucie ^b   Dobes, Pavel ^c   Markus, Robert ^a   Strnad, Hynek ^d   Wang, Zhi ^a   Hyrsl, Pavel ^c   Zurovec, Michal ^b   Theopold, Ulrich ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b INSTITUTE OF ENTOMOLOGY   (Czech Republic)

^c MASARYK UNIVERSITY   (Czech Republic)

^d INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

Author keywords

Basement membrane; Coagulation; Hemocyte; Insect immunity; Nematodes; Recognition molecule; Thioester containing proteins

Indexed keywords

COMPLEMENT; GLUTACTIN; MEMBRANE PROTEIN; SCLEROPROTEIN; THIOESTER; TRANSCRIPTOME; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; GLT PROTEIN, DROSOPHILA; PHOTOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DROSOPHILA; ENTOMOPATHOGENIC NEMATODE; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HEMOLYMPH; IMMUNE RESPONSE; LARVA; NEMATODIASIS; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BLOOD CELL; CLUSTER ANALYSIS; CONFOCAL MICROSCOPY; DNA MICROARRAY; DROSOPHILA MELANOGASTER; GENE ONTOLOGY; GENETICS; HOST PARASITE INTERACTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INSECT GENOME; METABOLISM; MICROBIOLOGY; PARASITOLOGY; PHOTORHABDUS; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHABDITOIDEA; RNA INTERFERENCE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CLUSTER ANALYSIS; COMPLEMENT SYSTEM PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EXTRACELLULAR MATRIX PROTEINS; GENE ONTOLOGY; GENOME, INSECT; HEMOCYTES; HOST-PARASITE INTERACTIONS; HOST-PATHOGEN INTERACTIONS; LARVA; LUMINESCENT PROTEINS; MEMBRANE GLYCOPROTEINS; MICROSCOPY, CONFOCAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOTORHABDUS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHABDITOIDEA; RNA INTERFERENCE; TRANSCRIPTOME;

EID: 84896374986     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000353734     Document Type: Article

References (52)

1. Eleftherianos I, ffrench-Constant RH, ClarkeDJ, Dowling AJ, Reynolds SE: Dissecting theimmune response to the entomopathogenPhotorhabdus. Trends Microbiol 2010; 18:552-560.
2. Balasubramanian N, Nascimento G, FerreiraR, Martinez M, Simoes N: Pepsin-like asparticprotease (Sc-ASP155) cloning, molecularcharacterization and gene expression analysisin developmental stages of nematodeSteinernema carpocapsae. Gene 2012; 500:164-171.
3. Lang AE, Schmidt G, Schlosser A, Hey TD,Larrinua IM, Sheets JJ, Mannherz HG, AktoriesK: Photorhabdus luminescens toxinsADP-ribosylate actin and RhoA to force actinclustering. Science 2010; 327: 1139-1142.
4. Castillo JC, Reynolds SE, Eleftherianos I: Insectimmune responses to nematode parasites.Trends Parasitol 2011; 27: 537-547.
5. Hallem EA, Rengarajan M, Ciche TA, SternbergPW: Nematodes, bacteria, and flies: a tripartitemodel for nematode parasitism. CurrBiol 2007; 17: 898-904.
6. Hyrsl P, Dobes P, Wang Z, Hauling T, WilhelmssonC, Theopold U: Clotting factors andeicosanoids protect against nematode infections.J Innate Immun 2011; 3: 65-70.
7. Castillo JC, Shokal U, Eleftherianos I: A novelmethod for infecting Drosophila adult flieswith insect pathogenic nematodes. Virulence2012; 3: 339-347.
8. Castillo JC, Shokal U, Eleftherianos I: Immunegene transcription in Drosophila adultflies infected by entomopathogenic nematodesand their mutualistic bacteria. J InsectPhysiol 2013; 59: 179-185.
9. Wang R, Liang Z, Hal M, Soderhall K: A transglutaminaseinvolved in the coagulation systemof the freshwater crayfish, Pacifastacusleniusculus. Tissue localisation and cDNAcloning. Fish Shellfish Immunol 2001; 11:623-637. (Pubitemid 34000089)
10. Kim Y, Ji D, Cho S, Park Y: Two groups ofentomopathogenic bacteria, Photorhabdusand Xenorhabdus, share an inhibitory actionagainst phospholipase A2 to induce host immunodepression.J Invertebr Pathol 2005; 89:258-264. (Pubitemid 41219462)
11. Aliota MT, Fuchs JF, Mayhew GF, Chen CC,Christensen BM: Mosquito transcriptomechanges and filarial worm resistance in Armigeressubalbatus. BMC Genomics 2007; 8:463.
12. Aliota MT, Fuchs JF, Rocheleau TA, ClarkAK, Hillyer JF, Chen CC, Christensen BM:Mosquito transcriptome profiles and filarialworm susceptibility in Armigeres subalbatus.PLoS Negl Trop Dis 2010; 4:e666.
13. Erickson SM, Xi Z, Mayhew GF, Ramirez JL,Aliota MT, Christensen BM, Dimopoulos G:Mosquito infection responses to developingfilarial worms. PLoS Negl Trop Dis 2009;3:e529.
14. Dobes P, Wang Z, Markus R, Theopold U,Hyrsl P: An improved method for nematodeinfection assays in Drosophila larvae. Fly(Austin) 2012; 6: 75-79.
15. Dietzl G, Chen D, Schnorrer F, Su KC, BarinovaY, Fellner M, Gasser B, Kinsey K, OppelS, Scheiblauer S, Couto A, Marra V, KelemanK, Dickson BJ: A genome-wide transgenicRNAi library for conditional gene inactivationin Drosophila. Nature 2007; 448: 151-156. (Pubitemid 47067374)
16. Gottar M, Gobert V, Matskevich AA, ReichhartJM, Wang C, Butt TM, Belvin M, HoffmannJA, Ferrandon D: Dual detection offungal infections in Drosophila via recognitionof glucans and sensing of virulence factors.Cell 2006; 127: 1425-1437. (Pubitemid 44960414)
17. Michel T, Reichhart JM, Hoffmann JA, RoyetJ: Drosophila Toll is activated by Gram-positivebacteria through a circulating peptidoglycanrecognition protein. Nature 2001; 414:756-759. (Pubitemid 34000773)
18. Gottar M, Gobert V, Michel T, Belvin M,Duyk G, Hoffmann JA, Ferrandon D, Royet J:The Drosophila immune response againstGram-negative bacteria is mediated by a peptidoglycanrecognition protein. Nature 2002;416: 640-644. (Pubitemid 34406765)
19. Takehana A, Yano T, Mita S, Kotani A, OshimaY, Kurata S: Peptidoglycan recognitionprotein (PRGP)-LE and PGRP-LC act synergisticallyin Drosophila immunity. EMBO J2004; 23: 4690-4700. (Pubitemid 39657868)
20. Maillet F, Bischoff V, Vignal C, Hoffmann J,Royet J: The Drosophila peptidoglycan recognitionprotein PGRP-LF blocks PFRP-LC andIMD/JNK pathway activation. Cell Host Microbe2008; 3: 293-303. (Pubitemid 351637430)
21. Wang Z, Wilhelmsson C, Hyrsl P, Loof TG,Dobes P, Klupp M, Loseva O, Morgelin M,Ikle J, Cripps RM, Herwald H, Theopold U:Pathogen entrapment by transglutaminase -a conserved early innate immune mechanism.PLoS Pathog 2010; 6:e1000763.
22. Smyth GK: Linear models and empiricalbayes methods for assessing differential expressionin microarray experiments. StatAppl Genet Mol Biol 2004; 3:article3.
23. Storey JD, Tibshirani R: Statistical significancefor genomewide studies. Proc NatlAcad Sci USA 2003; 100: 9440-9445.
24. Gentleman RC, Carey VJ, Bates DM, BolstadB, Dettling M, Dudoit S, Ellis B, Gautier L, GeY, Gentry J, Hornik K, Hothorn T, Huber W,Iacus S, Irizarry R, Leisch F, Li C, Maechler M,Rossini AJ, Sawitzki G, Smith C, Smyth G,Tierney L, Yang JY, Zhang J: Bioconductor:open software development for computationalbiology and bioinformatics. Genome Biol2004; 5:R80.
25. Kanehisa M, Goto S: Kegg: Kyoto encyclopediaof genes and genomes. Nucleic Acids Res2000; 28: 27-30. (Pubitemid 30047706)
26. Ashburner M, Ball CA, Blake JA, Botstein D,Butler H, Cherry JM, Davis AP, Dolinski K,Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC,Richardson JE, Ringwald M, Rubin GM, SherlockG: Gene ontology: tool for the unificationof biology. The gene ontology consortium.Nat Genet 2000; 25: 25-29. (Pubitemid 30257031)
27. Tian L, Greenberg SA, Kong SW, AltschulerJ, Kohane IS, Park PJ: Discovering statisticallysignificant pathways in expression profilingstudies. Proc Natl Acad Sci USA 2005; 102:13544-13549. (Pubitemid 41420885)
28. Zettervall CJ, Anderl I, Williams MJ, PalmerR, Kurucz E, Ando I, Hultmark D: A directedscreen for genes involved in Drosophila bloodcell activation. Proc Natl Acad Sci USA 2004;101: 14192-14197. (Pubitemid 39305052)
29. Lemaitre B, Hoffmann J: The host defense ofDrosophila melanogaster. Annu Rev Immunol2007; 25: 697-743.
30. Bou Aoun R, Hetru C, Troxler L, Doucet D,Ferrandon D, Matt N: Analysis of thioestercontainingproteins during the innate immuneresponse of Drosophila melanogaster. JInnate Immun 2011; 3: 52-64.
31. Lavine MD, Strand MR: Insect hemocytes andtheir role in immunity. Insect Biochem MolBiol 2002; 32: 1295-1309.
32. Irving P, Ubeda JM, Doucet D, Troxler L, LagueuxM, Zachary D, Hoffmann JA, Hetru C,Meister M: New insights into Drosophila larvalhaemocyte functions through genomewideanalysis. Cell Microbiol 2005; 7: 335-350. (Pubitemid 40277914)
33. Wertheim B, Kraaijeveld AR, Schuster E,Blanc E, Hopkins M, Pletcher SD, Strand MR,Partridge L, Godfray HC: Genome-wide geneexpression in response to parasitoid attack inDrosophila. Genome Biol 2005; 6:R94.
34. Vodovar N, Vinals M, Liehl P, Basset A, DegrouardJ, Spellman P, Boccard F, Lemaitre B:Drosophila host defense after oral infection byan entomopathogenic Pseudomonas species.Proc Natl Acad Sci USA 2005; 102: 11414-11419. (Pubitemid 41153834)
35. Schlenke TA, Morales J, Govind S, Clark AG:Contrasting infection strategies in generalistand specialist wasp parasitoids of Drosophilamelanogaster. PLoS Pathog 2007; 3: 1486-1501. (Pubitemid 350085613)
36. Wang S, Tsarouhas V, Xylourgidis N, Sabri N,Tiklova K, Nautiyal N, Gallio M, SamakovlisC: The tyrosine kinase stitcher activatesgrainy head and epidermal wound healing inDrosophila. Nat Cell Biol 2009; 11: 890-895.
37. Razzell W, Wood W, Martin P: Swatting flies:modelling wound healing and inflammationin Drosophila. Dis Model Mech 2011; 4: 569-574.
38. Shaw TJ, Martin P: Wound repair at a glance.J Cell Sci 2009; 122: 3209-3213.
39. Sonnemann KJ, Bement WM: Wound repair:toward understanding and integration of single-cell and multicellular wound responses.Annu Rev Cell Dev Biol 2011; 27: 237-263.
40. Adachi T, Tomita M, Yoshizato K: Synthesisof prolyl 4-hydroxylase alpha subunit andtype IV collagen in hemocytic granular cellsof silkworm, Bombyx mori: Involvement oftype IV collagen in self-defense reaction andmetamorphosis. Matrix Biol 2005; 24: 136-154. (Pubitemid 40693637)
41. Stramer B, Wood W, Galko MJ, Redd MJ, JacintoA, Parkhurst SM, Martin P: Live imagingof wound inflammation in Drosophilaembryos reveals key roles for small GTPasesduring in vivo cell migration. J Cell Biol 2005;168: 567-573. (Pubitemid 40271022)
42. Lesch C, Jo J, Wu Y, Fish GS, Galko MJ: Atargeted UAS-RNAi screen in Drosophila larvaeidentifies wound closure genes regulatingdistinct cellular processes. Genetics 2010; 186:943-957.
43. Adachi T, Tomita M, Yoshizato K: Synthesisof prolyl 4-hydroxylase alpha subunit andtype IV collagen in hemocytic granular cellsof silkworm, Bombyx mori: Involvement oftype IV collagen in self-defense reaction andmetamorphosis. Matrix Biol 2005; 24: 136-154. (Pubitemid 40693637)
44. Stramer B, Wood W, Galko MJ, Redd MJ, JacintoA, Parkhurst SM, Martin P: Live imagingof wound inflammation in Drosophilaembryos reveals key roles for small GTPasesduring in vivo cell migration. J Cell Biol 2005;168: 567-573. (Pubitemid 40271022)
45. Lesch C, Jo J, Wu Y, Fish GS, Galko MJ: Atargeted UAS-RNAi screen in Drosophila larvaeidentifies wound closure genes regulatingdistinct cellular processes. Genetics 2010; 186:943-957.
46. Basbous N, Coste F, Leone P, Vincentelli R,Royet J, Kellenberger C, Roussel A: The Drosophilapeptidoglycan-recognition protein LFinteracts with peptidoglycan-recognitionprotein LC to downregulate the Imd pathway.EMBO Rep 2011; 12: 327-333.
47. Zhong D, Wang MH, Pai A, Yan G: Transcriptionprofiling of immune genes duringparasite infection in susceptible and resistantstrains of the flour beetles (Tribolium castaneum). Exp Parasitol 2013; 134: 61-67.
48. Ramos R, Silva JP, Rodrigues AC, Costa R,Guardao L, Schmitt F, Soares R, Vilanova M,Domingues L, Gama M: Wound healingactivity of the human antimicrobial peptideLL37. Peptides 2011; 32: 1469-1476.
49. Vandamme D, Landuyt B, Luyten W, Schoofs L: A comprehensive summary of LL-37, thefactotum human cathelicidin peptide. CellImmunol 2012; 280: 22-35.
50. Nikolajsen CL, Scavenius C, Enghild JJ: Humancomplement C3 is a substrate for transglutaminases.A functional link between nonprotease-based members of the coagulationand complement cascades. Biochemistry2012; 51: 4735-4742.
51. Cronin SJ, Nehme NT, Limmer S, Liegeois S,Pospisilik JA, Schramek D, Leibbrandt A, SimoesRde M, Gruber S, Puc U, EbersbergerI, Zoranovic T, Neely GG, von Haeseler A,Ferrandon D, Penninger JM: Genome-wideRNAi screen identifies genes involved in intestinalpathogenic bacterial infection. Science2009; 325: 340-343.
52. Lee MJ, Mondal A, Small C, Paddibhatla I,Kawaguchi A, Govind S: A database for theanalysis of immunity genes in Drosophila :Padma database. Fly (Austin) 2011; 5: 155-161.