Qualitative proteomic analysis of Tipula oleracea nudivirus occlusion bodies Annie Bézier, Grégoire Harichaux, Karine Musset, Valérie Labas, Elisabeth A. Herniou

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Annie Bézier, Grégoire Harichaux, Karine Musset, Valérie Labas, Elisabeth A. Herniou. Qualita- tive proteomic analysis of Tipula oleracea nudivirus occlusion bodies. Journal of General Virology, Microbiology Society, 2017, 98 (2), pp.284-295. ￿10.1099/jgv.0.000661￿. ￿hal-01595093￿

HAL Id: hal-01595093 https://hal.archives-ouvertes.fr/hal-01595093 Submitted on 26 May 2020

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Version postprint Order ofAuthors: First Author: Corresponding Author: Section/Category: Article Type: Full Title: Manuscript Number: Abstract: Qualitative proteomicanalysisofTipulaoleraceanudivirus(ToNV)occlusionbodies Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), Powered byEditorialManager® and ProduXionManager® fromAries SystemsCorporation 284-295. DOI :10.1099/jgv.0.000661 Comment citer cedocument: Journal ofGeneralVirology Downloaded from www.microbiologyresearch.org by newly identifiednudiviruscoregeneproduct. protein VP39homolog)and11K(Hz2V025);thehypotheticalHz2V079,a proteins: thetwovirionstructuralproteins34K(Hz2V052,baculoviruscapsid of baculoviruspolyhedrin/granulinandthehomologsthreeHzNV-2predicted composed of52viralproteins,themostabundantwhicharefunctionalhomolog tandem highresolutionmassspectrometryrevealedToNVocclusionbodiesare 25 and12kDa.Proteomicanalysisusingon-linenanoflowliquidchromatography those observedforothernudiviruseswithfivemajorproteinbandsofabout75,48,35, bodies. ProteinprofilerevealedbyCoomassie-stainedSDS-PAGEisquitesimilarto ToNV isthesecondfullysequencednudivirustobedescribedasformingocclusion nudivirus (ToNV)isthecausativeagentofcraneflynucleopolyhedrosis.WithPmNV, from baculovirusesorendogenousnudiviruses(i.e.bracoviruses).Tipulaoleracea (HzNV-2). Functionofpredictednudiviralproteinsisstillinferredfromwhatknown nudivirus (PmNV)andfournucleocapsidproteinsfromHelicoverpazea2 data totheexceptionofmajorocclusionbodyproteinfromPenaeusmonodon However, onlyfewdirectmatcheswerecompletedbetweengenomicandproteomic nudivirus particlesweremainlycharacterizedbypolyacrylamidegelelectrophoresis. fully sequencednudiviralgenomesareavailableindatabasesandproteinprofilefrom to baculoviruses,whichreplicateinthenucleusofcellstheyinfect.Updatesix Nudiviruses arearthropod-specificlargedouble-strandedcircularDNAviruses,related Elisabeth A.Herniou Valérie Labas Karine Musset Grégoire Harichaux Anne Bézier Anne Bézier FRANCE Univ. ofTours,France Anne Bézier Insect Viruses-DNA Standard Qualitative proteomicanalysisofTipulaoleraceanudivirus(ToNV)occlusionbodies JGV-D-16-00587R1

On: Mon, 28 Nov2016 13:16:47 --Manuscript Draft-- IP: 138.102.192.62

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Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), Table number: Figure number: Categories: Proteomics countWord countWord (Abstract): Keywords: Fax number Phone number Correspondence:Bézier Annie etdePhénomique des Animaux d’IntérêtBio 2 1 Annie Running title: bodies Title: Section/Category: Article type: Standard INRA, PRC UMR85 INRA, PRC Institut deRecherche la sur Biologie del’Insecte Qualitative Bézier

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Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), gene product. and 11K two baculovirus of composed are tandem chromatography bands SDS as described be nucleopolyhedrosis fly crane nudiviruses nudiviral from proteins nucleocapsid from protein body occlusion major the matches direct few particles sequenced which baculoviruses, arthropod are Nudiviruses ABSTRACT virion structural proteins structural virion - PAGE of about 75, 48, 75, about of

(Hz2V025) ee any hrceie b plarlmd gl electrophoresis gel polyacrylamide by characterized mainly were proteins nudiviral

ie bracoviruses (i.e. polyhedrin/granulin is quite similar to those observed for other nudiviruses with five major five with nudiviruses other for observed those to similar quite is

52 forming

s tl ifre from inferred still is were completed were

284-295. DOI :10.1099/jgv.0.000661 ; viral proteins viral

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and the and elct i te nucleus the in replicate Comment citer cedocument: 35 high resolution high

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Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), databases: (Huger Araneina in suspected ( virus bacilliform intranuclear ( nucleopolyhedrovirus single with ( Huger 1985, NV paludosa Burand 2002 Lepidoptera orders insect more infect they Nudiviruses (Jehle new the Jehle viruses) filamentous nuclear virusesarthropodcircular dsDNA large that group diverse highly a form described Formerly INTRODUCTION OrNV) ( OrNV)

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Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), OrNV of virions occluded al., et virions occluded (Yang TpNV enveloped as transmitted are viruses some family in interest particular of point A (Cheng that evidence canescens Venturia ToNV 100 since the especially (Raina tissues ( cells host in genome Nudivirus and (HzNV tissues reproductive concerns and variable is tropism tissue The (HzNV sterility and malformations induce also and OrNV), a and larvae both adults) stages developmental All transmitted. orally or sexually are Nudiviruses ToNV ( GbNV 2012), OrNV), mid OrNV),

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Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), 25 ( bands protein 4.10 approximately of Separation Coomassie RESULTS furtherother characterizedcomponents. all identified we chromatography qualitative (Bézier matrix protein enveloped 2013) Rohrmann, and assembly, and packaging transcription, processing, and baculoviruses,t similaritysequenceBasedwith on ToNV (Bézier (ORFs) frames reading open genome The genomicand proteomicof data nudiviruses HzNV from 34K) (Chaivisuthangkura PmNV 30 than Bonami 1985; Sheehan, & Crawford 2015)

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Version postprint 220 219 218 217 216 215 214 213 212 211 210 209 208 207 206 205 204 203 202 201 200 199 198 197 196

Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), peptides (http://web.expasy.org/peptide_cutter) acids, amino 119 of composed al al et were they Surprisingly a crucial Burke nudiviruses endogenous of components (Gauthier (Garcia hytrosaviruses PIFs baculoviruses A fromin nudiviral DNAand excision integration its genome. host Li 2004; most also but maturation, virion and/or DNA FEN and INT nudiviral the integrase/recombinase, an also hyt (Burke bracoviruses in protein associated particles as identified been already Bambara, & Balakrishnan FEN probably endonuclease FLAP the and INT integrase the proteins, core nudiviral two Vc ll ., 2016) ., VLP rosaviruses (GpSGHVORF30; Kariithi (GpSGHVORF30; rosaviruses I poen ( proteins PIF ., 2010; Hou 2010; ., are conserved in exogenous nudiviruses (Bézier (Bézier nudiviruses exogenous in conserved are et al , ranging in size in ranging , component role et al et . et al et novd n N mtbls (rig & aaa, 99 Liu 1999; Jayaram, & (Grainge metabolism DNA in involved both

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Version postprint 243 242 241 240 239 238 237 236 235 234 233 232 231 230 229 228 227 226 225 224 223 222 221

Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), ToNV anddescribedas therefore are particle genuine are they that ( identified been already have ( Eukaryota Bacteriaand in found also sequence a on based identity sequence peptide 100% a on relies detection its as confirmed be to need relevant Lastly detected as well as nudiviruses inendogenous HzNV ( p as characterized been exclusively far so had HzNVORF9) and HzNVORF64 HzNVorf106, PmV, (PmNVORF62, proteins nudiviral be to time first the for shown were PmNVORF64) and PmNVORF7 proteins Twenty 2010 ( baculoviruses other as described previously been not LEF OBs the peptides two ClanGV Bézier mass spectrometry method spectrometry mass - . ;

4 , Abd N polymerase RNA and P47 P47 and -

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Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), MOBP the also and ToNV in protein major second the as identified a as determined (Hz2V025) ( 34K proteins structural respectively main other The The MOBP that revealed (Ishihama 4.6.1 software Q+ Scaffold using emPAI the calculating al (Deng proteins structural major GV and NPV the for observed already bands major were 2015). by encoded Lundgren 2010; Inc) bas the On Protein to ToNV (Bézier one least at in homologs had Overall ., 2007; Wang Wang 2007; ., , second the relative quantity of each each of quantity relative the found within all within found MOBP represented MOBP ,

amount Abundance from all these 52 identified proteins, proteins, identified 52 these all from is

component Km 20) ad to and 2009), (Kim, .

orf059 ooos o he HzNV three to homologs second of the of The identification of single proteins proteins single of identification The

et al et to et al t al et uiiu cr gene core nudivirus OB te ucinl ooo o te auoiu plhdi (Bézier polyhedrin baculovirus the of homolog functional the , 284-295. DOI :10.1099/jgv.0.000661 ~61%

total represented ., 2010; Wang 2010; ., main ., 2015). , 2010) ., gel components components

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Version postprint 293 292 291 290 289 288 287 286 285 284 283 282 281 280 279 278 277 276 275 274 273 272 271 270 269

Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), (Bézier family multigenic ORF032 specific ToNV the to belongs ORF034, putative except function, proteins (Table al nudiviruses in function (HzNVORF9), orf Eight Alla Braunagel s However represented PIF the of members three the All ( bands, major remaining Burke 2010; homologs as suspected was 1 ORF053, and kDa 8.7 (ORF041, weight molecular proportion same the in band nudiviruses and 2009) (Kim, baculovirus in protein structural ~ , 09 Wetterwald 2009; ., 0.2%) and 031 et al

proteins

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did and Fig and ., 2016) and endogenous ( nudiviruses (HzNVORF124 & Summers, & uch . with 13 to 278 total spectr total 278 to 13 with not have any have not 11K is a nudiviral specific core protein core specific nudiviral a is 11K with MOBP and the VP39in with MOBP t al et , infectivity factors infectivity ecdd by encoded , had orf o abundance low . endogenous ( endogenous

2 a 049 , 2013) ., ) homologs already identified as particle components with no other known known other no with components particle as identified already homologs 284-295. DOI :10.1099/jgv.0.000661 . osbe ia evlp cmoet Km 2009) (Kim, component envelope viral possible They

(HzNVORF106)

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orf 0.7 kDa). kDa). 0.7 ; Thiem & Miller, 1989 Miller, & Thiem ; This protein was found in the 12 the in found was protein This baculovirus OBs ( ~ ~ 027 , were 2%) 2% of all identified all of 2% et al et n VcVLP and orf et al , but only two (b and c) out of the of out c) and (b two only but ,

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did ., 2010), hytrosavirus 2010), ., ., 2010). found. PIFs PIFs found. spectrum counts spectrum The The

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kDa , 117

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Version postprint 318 317 316 315 314 313 312 311 310 309 308 307 306 305 304 303 302 301 300 299 298 297 296 295 294

Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), al baculovirus I ( bracovirus, cesium and (sucrose unusual respectively assoc be to shown were ODV and BV (HearNPV) therefore might Braconi other for shown was it as contaminants proteins host DNA 99 (over confidence host Nine Associated counts identified all of 80% and 20% respectively represented genes accessory and genes gene accessory counts spectrum components. which particular n unpublished ., 2014; Zhang 2014; ., or

(not shown). ny two only ,

t al et mRNA processing, mRNA vn among even - cell derived proteins were identified to be associated with ToNV ToNV with associated be to identified were proteins derived cell

arthropod

ODV

oti ha sok rtis ATP proteins, shock heat contain , ( data) , 2014 .,

Hou T but they but might a hese hese products play a crucial role in role crucial a play ctin

(ORF032 and ORF034) out of the three members members three the of out ORF034) and (ORF032 et al et ( and .

t al et Lanier & Vol & Lanier

bt tubulin, beta , 284-295. DOI :10.1099/jgv.0.000661 ) They %). o unrelated or ) 20 ae en co been have chloride ., 2015) ., might might uiiue a large at nudiviruses proteins about Comment citer cedocument: , 2013 .,

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represent spectrum 2). , 2013 .,

T . as

Such Such NPV hey hey OB 13 et ; ,

Version postprint 343 342 341 340 339 338 337 336 335 334 333 332 331 330 329 328 327 326 325 324 323 322 321 320 319

Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), (Gattoni conditions 2002). type considered the on depending specificitytarget involved in type M (hnRNP) Hrp59 infection. SOD cellular many SOD function cellularSOD host the counteract al et al (Thézé entomopoxviruses in v as such (NCLDV) viruses DNA (Th eukaryota release Cu 2007; membrane cytoplasmic the through budding and nucleus nucleus, the and cytoplasm the between transit nucleocapsid in involved directly is actin cellular infection, (Saphire virus ., 1991 ., the - é n ueoie imts (O) s novd n eoiyn sprxd fe radicals free superoxide detoxifying in involved is (SOD) dismutase superoxide Zn ., 2011) and and 2011) ., z protein é Marek Megavirus d Human s ncer rti that protein nuclear a is et al et

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s et al et 284-295. DOI :10.1099/jgv.0.000661 , 2005) ., tes response stress ,

or (Almazan (Almazan described as associated with ODV in ODV with associated as described Comment citer cedocument: homolog is implicated in premRNA splicing regulation under stress under regulation splicing premRNA in implicated is homolog ., 1996) ., ) . by

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t al et infected cells contained cells infected found in the genome of genome the in found

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Version postprint 368 367 366 365 364 363 362 361 360 359 358 357 356 355 354 353 352 351 350 349 348 347 346 345 344

Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), regarding for specific date insect. within hytrosaviruses, and baculoviruses nudiviruses, main the of conservation Thus, viruses. enveloped other in component particle as identified previously were proteins release. and assembly packaging, and infectivity oral in involved homologs nudiviruses prot oleracea Tipula exhaustive time first the Comprehensive CONCLUSION remain real the response, stress preventing cytoskeleton component the because ToNV with associated be also might proteins host Other by virus DNA about known is nothing (Jorba eins s t al et

largely unknown were whether s , 08 Dechtawewat 2008; ., immuno ,

as well as well as both demonstrated cases of nudivirus nudivirus of casesdemonstrated both and structural host host structural and rn fly crane

es However, led ietfe a pril component particle as identified already . qualitative qualitative

S contained contained

Tipula these 284-295. DOI :10.1099/jgv.0.000661

od labelling gold in baculoviruses and hytrosaviruses. and baculoviruses in Comment citer cedocument: genome is not sequenced. sequenced. not is genome proteins hnRNP hnRNP

each virus each .

oleracea opsto of composition proteomic analysis on proteomic using protein Downloaded from www.microbiologyresearch.org by 52 viral proteins and 9 host proteins. About half of the viral viral the of half About proteins. host 9 and proteins viral 52 proteins association with association are associated with associated are

strengthens On: Mon, 28 Nov2016 13:16:47 uiiu. This nudivirus. t al. et

components through various various through components

retains

implication of these host factors in nudivirus life cycle life nudivirus in factors host these of implication nlss f hs proteins these of analyses IP: 138.102.192.62 21; Jagdeo 2015; , could nudivirus nudivirus specificity

the idea of a similar basic similar a of idea the

be involved in virus entry and other protein in protein other and entry virus in involved be DNA endogenization study does not provide any information information any provide not does study

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T . n te eoeos r endogenous or exogenous other in over

, These mainly concern baculovirus baculovirus concern mainly These OBs

e cldd uiiu infecting nudivirus occluded he t , 2015) ., o be confirmed as ToNV ToNV as confirmed be o half identified proteins are to are proteins identified half ht ol nt be not could that

hud e done. be should ia entities, viral ( bracoviruses - HR s b , , with cell cell - ut MS/MS MS/MS to our knowledge knowledge our to entry mechanism mechanism entry the envelope the Alm

and n particular in revealed exploitation ost all host host all ost

identified Although Although Vc VLP s OB , or , for 15 ) ,

Version postprint 393 392 391 390 389 388 387 386 385 384 383 382 381 380 379 378 377 376 375 374 373 372 371 370 369

Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), In components remaining Coom (Biorad). marker weight molecular Kaleidoscope with along gel, stacking 5% a to combined gel running polyacrylamide 12.5% a on 70V at 3h during electrophoresed sample PAGE Technologies Life AssayKit, Protein of microliters Five SDS studythis (NERC Hydrology and Ecology for Centre Council, Research Environment Natural the at held collection virus insect ( sample archival ToNV Viral sample M electronproteins microscopy andscanning transmission particles P Nonidet different these with ATERIAL - gel digestion - Page and h poen mat protein the assie blue, major bandmajor blue, assie n to and was the same as those used foras genomic thesame previous was analy - lane lane 40 in the study . S ,

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rce to proceed uiid iu ( virus purified 284-295. DOI :10.1099/jgv.0.000661 r i x - Comment citer cedocument: ETHODS CEH, Wallingford, England). Wallingford, CEH, .

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min at 95°C in 1x PBS and SDS and PBS 1x in 95°C at min . treat ccluded particles particles ccluded o iciiae ute between further discriminate To proteins o s o include to as so also reveal the ses (Bézier ses (Bézier OBs

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Version postprint 418 417 416 415 414 413 412 411 410 409 408 407 406 405 404 403 402 401 400 399 398 397 396 395 394

Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2), nano LCPackings aC PepMap (Acclaim using conducted was separation peptide The B. solvent 4% 84% water, % 15.9 acid, formic 10 for preconcentrated and desalted 0.1% were Peptides (v/v/v). acetonitrile (B) and (v/v/v) acetonitrile 2% water, % 97.9 2 C 100 PepMap (Acclaim column trap LCPackings an on loaded Dionex). SR11; 6.8 (version Software Liquid 3000 RSLCHigh Pressure by Ultra controlled (Dionex) Chromatographer Chromeleon Velos Orbitrap LTQ resolution were mixtures Peptide NanoLC for (Thermofisher) 5 for (1:1) using acetonitrile gel acid, formic the 0.1% from in extracted incubation were peptides resulting The Roche). Grade, (Sequencing in overnight digested were Proteins bicarbonate by washed were slices Gelrespectively. dark, the in temperature and 56°C of solutions in incubations for acetonitrile for (1:1) acetonitrile water, in washed was band Each

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proteomics Departmentof Microbiology,University Massachusetts,MA. Amherst, of

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Length major (aa) Comment citer cedocument: 362 398 364 385 388 421 408 450 479 497 494 527 561 597 704 690 742 763 765 808 major component major

and associated associated and (kDa) 60.04 66.18 68.85 81.16 81.88 86.95 87.20 88.28 94.99 40.96 43.27 43.40 44.81 45.23 47.74 47.81 51.94 56.85 57.75 58.96 MW .

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32

Version postprint Bézier, A., Harichaux,G., Musset,K., Labas,V.,Herniou, E.A.(2017). Qualitative proteomic analysis ofTipulaoleracea nudivirusocclusion bodies. Journalof General Virology, 98(2),

100 122 114 124 106 117 119 115 107 41 53 28 42 30 56 34 13 32 89 23 62 26 59 54 31 27 99 63 49 87 43

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* 284-295. DOI :10.1099/jgv.0.000661

Comment citer cedocument: 115 105 133 139 144 143 188 180 193 205 203 218 225 224 226 237 241 254 272 291 289 291 307 324 327 333 331 336 74 93 92

30.124 21.86 22.47 23.37 25.29 26.20 26.31 27.00 27.31 27.36 31.78 34.12 34.70 35.02 36.30 37.77 38.31 39.09 39.15 39.58 10.70 10.73 12.39 12.65 15.68 15.76 16.77 16.81 20.64 21.27 8.70

10.13 9.37 9.38 6.41 9.70 9.92 4.36 7.25 5.60 7.16 8.24 4.83 6.14 4.88 9.82 6.19 6.43 4.97 4.82 6.31 8.51 5.75 8.35 8.85 9.03 4.88 6.19 5.76 7.75 8.31 7.76

10 10 13 19 44 13 13 47 14 16 5 2 3 9 1 1 1 1 2 5 7 6 1 1 8 8 1 3 7 1 1

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284-295. DOI :10.1099/jgv.0.000661

Comment citer cedocument: 53

MW and pI and MW 6.53 Myosin filament organization Response to oxidative stressResponse tooxidative stressResponse tooxidative stressResponse tooxidative Microtubule GO

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