Recruitment of the Major Vault Protein by InlK: A Strategy to Avoid Autophagy

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L.
monocytogenes is a facultative intracellular bacterium responsible for listeriosis. It is able to invade, survive and replicate in phagocytic and non-phagocytic cells. The infectious process at the cellular level has been extensively studied and many virulence factors have been identified. Yet, the role of InlK, a member of the internalin family specific to L. monocytogenes, remains unknown. Here, we first show using deletion analysis and in vivo infection, that InlK is a bona fide virulence factor, poorly expressed in vitro and well expressed in vivo, and that it is anchored to the bacterial surface by sortase A. We then demonstrate by a yeast two hybrid screen using InlK as a bait, validated by pulldown experiments and immunofluorescence analysis that intracytosolic bacteria via an interaction with the protein InlK interact with the Major Vault Protein (MVP), the main component of cytoplasmic ribonucleoproteic particules named vaults. Although vaults have been implicated in several cellular processes, their role has remained elusive. Our analysis demonstrates that MVP recruitment disguises intracytosolic bacteria from autophagic recognition, leading to an increased survival rate of InlK over-expressing bacteria compared to InlK⁻ bacteria. Together these results reveal that MVP is hijacked by L. monocytogenes in order to counteract the autophagy process, a finding that could have major implications in deciphering the cellular role of vault particles.

Vyšlo v časopise: Recruitment of the Major Vault Protein by InlK: A Strategy to Avoid Autophagy. PLoS Pathog 7(8): e32767. doi:10.1371/journal.ppat.1002168
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002168

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Zdroje

1. DortetLVeiga-ChaconECossartP 2009 Listeria monocytogenes. SchaechterM Encyclopedia of Microbiology 3rd ed. Oxford Elsevier 182 198

2. DissonOGrayoSHuilletENikitasGLanga-VivesF 2008 Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis. Nature 455 1114 1118

3. HamonMBierneHCossartP 2006 Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol 4 423 434

4. LecuitM 2007 Human listeriosis and animal models. Microbes Infect 9 1216 1225

5. CossartPSansonettiPJ 2004 Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304 242 248

6. BierneHGouinERouxPCaroniPYinHL 2001 A role for cofilin and LIM kinase in Listeria-induced phagocytosis. J Cell Biol 155 101 112

7. BonazziMVeigaEPizarro-CerdaJCossartP 2008 Successive post-translational modifications of E-cadherin are required for InlA-mediated internalization of Listeria monocytogenes. Cell Microbiol 10 2208 2222

8. KocksCGouinETabouretMBerchePOhayonH 1992 L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68 521 531

9. MostowySCossartP 2011 Autophagy and the cytoskeleton: New links revealed by intracellular pathogens. Autophagy 7 780 782

10. CossartP 2000 Actin-based motility of pathogens: the Arp2/3 complex is a central player. Cell Microbiol 2 195 205

11. YoshikawaYOgawaMHainTYoshidaMFukumatsuM 2009 Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat Cell Biol 11 1233 1240

12. ThurstonTLRyzhakovGBloorSvon MuhlinenNRandowF 2009 The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat Immunol 10 1215 1221

13. BirminghamCLCanadienVGouinETroyEBYoshimoriT 2007 Listeria monocytogenes evades killing by autophagy during colonization of host cells. Autophagy 3 442 451

14. PerrinAJJiangXBirminghamCLSoNSBrumellJH 2004 Recognition of bacteria in the cytosol of Mammalian cells by the ubiquitin system. Curr Biol 14 806 811

15. BierneHCossartP 2007 Listeria monocytogenes surface proteins: from genome predictions to function. Microbiol Mol Biol Rev 71 377 397

16. TanakaHKatoKYamashitaESumizawaTZhouY 2009 The structure of rat liver vault at 3.5 angstrom resolution. Science 323 384 388

17. RomeLKedershaNChuganiD 1991 Unlocking vaults: organelles in search of a function. Trends Cell Biol 1 47 50

18. AndersonDHKickhoeferVASieversSARomeLHEisenbergD 2007 Draft crystal structure of the vault shell at 9-A resolution. PLoS Biol 5 e318

19. MikyasYMakabiMRaval-FernandesSHarringtonLKickhoeferVA 2004 Cryoelectron microscopy imaging of recombinant and tissue derived vaults: localization of the MVP N termini and VPARP. J Mol Biol 344 91 105

20. StephenAGRaval-FernandesSHuynhTTorresMKickhoeferVA 2001 Assembly of vault-like particles in insect cells expressing only the major vault protein. J Biol Chem 276 23217 23220

21. KickhoeferVALiuYKongLBSnowBEStewartPL 2001 The Telomerase/vault-associated protein TEP1 is required for vault RNA stability and its association with the vault particle. J Cell Biol 152 157 164

22. KickhoeferVASivaACKedershaNLInmanEMRulandC 1999 The 193-kD vault protein, VPARP, is a novel poly(ADP-ribose) polymerase. J Cell Biol 146 917 928

23. LiuYSnowBEKickhoeferVAErdmannNZhouW 2004 Vault poly(ADP-ribose) polymerase is associated with mammalian telomerase and is dispensable for telomerase function and vault structure in vivo. Mol Cell Biol 24 5314 5323

24. Raval-FernandesSKickhoeferVAKitchenCRomeLH 2005 Increased susceptibility of vault poly(ADP-ribose) polymerase-deficient mice to carcinogen-induced tumorigenesis. Cancer Res 65 8846 8852

25. StadlerPFChenJJHackermullerJHoffmannSHornF 2009 Evolution of vault RNAs. Mol Biol Evol 26 1975 1991

26. van ZonAMossinkMHSchoesterMSchefferGLScheperRJ 2001 Multiple human vault RNAs. Expression and association with the vault complex. J Biol Chem 276 37715 37721

27. BergerWSteinerEGruschMElblingLMickscheM 2009 Vaults and the major vault protein: novel roles in signal pathway regulation and immunity. Cell Mol Life Sci 66 43 61

28. SteinerEHolzmannKElblingLMickscheMBergerW 2006 Cellular functions of vaults and their involvement in multidrug resistance. Curr Drug Targets 7 923 934

29. SchroeijersABReursAWSchefferGLStamAGde JongMC 2002 Up-regulation of drug resistance-related vaults during dendritic cell development. J Immunol 168 1572 1578

30. KowalskiMPDubouix-BourandyABajmocziMGolanDEZaidiT 2007 Host resistance to lung infection mediated by major vault protein in epithelial cells. Science 317 130 132

31. MrazekJKreutmayerSBGrasserFAPolacekNHuttenhoferA 2007 Subtractive hybridization identifies novel differentially expressed ncRNA species in EBV-infected human B cells. Nucleic Acids Res 35 e73

32. KimELeeSMianMFYunSUSongM 2006 Crosstalk between Src and major vault protein in epidermal growth factor-dependent cell signalling. FEBS J 273 793 804

33. KolliSZitoCIMossinkMHWiemerEABennettAM 2004 The major vault protein is a novel substrate for the tyrosine phosphatase SHP-2 and scaffold protein in epidermal growth factor signaling. J Biol Chem 279 29374 29385

34. LiangPWanYYanYWangYLuoN 2010 MVP interacts with YPEL4 and inhibits YPEL4-mediated activities of the ERK signal pathway. Biochem Cell Biol 88 445 450

35. YuZFotouhi-ArdakaniNWuLMaouiMWangS 2002 PTEN associates with the vault particles in HeLa cells. J Biol Chem 277 40247 40252

36. RyuSJParkSC 2009 Targeting major vault protein in senescence-associated apoptosis resistance. Expert Opin Ther Targets 13 479 484

37. MossinkMHde GrootJvan ZonAFranzel-LuitenESchoesterM 2003 Unimpaired dendritic cell functions in MVP/LRP knockout mice. Immunology 110 58 65

38. MossinkMHvan ZonAFranzel-LuitenESchoesterMKickhoeferVA 2002 Disruption of the murine major vault protein (MVP/LRP) gene does not induce hypersensitivity to cytostatics. Cancer Res 62 7298 7304

39. GlaserPFrangeulLBuchrieserCRusniokCAmendA 2001 Comparative genomics of Listeria species. Science 294 849 852

40. BierneHSabetCPersonnicNCossartP 2007 Internalins: a complex family of leucine-rich repeat-containing proteins in Listeria monocytogenes. Microbes Infect 9 1156 1166

41. BierneHMazmanianSKTrostMPucciarelliMGLiuG 2002 Inactivation of the srtA gene in Listeria monocytogenes inhibits anchoring of surface proteins and affects virulence. Mol Microbiol 43 869 881

42. BonazziMCossartP 2006 Bacterial entry into cells: a role for the endocytic machinery. FEBS Lett 580 2962 2967

43. CamejoABuchrieserCCouveECarvalhoFReisO 2009 In vivo transcriptional profiling of Listeria monocytogenes and mutagenesis identify new virulence factors involved in infection. PLoS Pathog 5 e1000449

44. Toledo-AranaADussurgetONikitasGSestoNGuet-RevilletH 2009 The Listeria transcriptional landscape from saprophytism to virulence. Nature 459 950 956

45. AubryCGoulardCNahoriMADecalfJBonecaIG 2011 OatA, a peptidoglycan O-acetyltransferase involved in Listeria monocytogenes immune escape and critical for virulence. J Infect Dis Accepted

46. PucciarelliMGCalvoESabetCBierneHCossartP 2005 Identification of substrates of the Listeria monocytogenes sortases A and B by a non-gel proteomic analysis. Proteomics 5 4808 4817

47. McGannPRaengpradubSIvanekRWiedmannMBoorKJ 2008 Differential regulation of Listeria monocytogenes internalin and internalin-like genes by sigmaB and PrfA as revealed by subgenomic microarray analyses. Foodborne Pathog Dis 5 417 435

48. BalestrinoDHamonMADortetLNahoriMAPizarro-CerdaJ 2010 Single-cell techniques using chromosomally tagged fluorescent bacteria to study Listeria monocytogenes infection processes. Appl Environ Microbiol 76 3625 3636

49. SabetCToledo-AranaAPersonnicNLecuitMDubracS 2008 The Listeria monocytogenes virulence factor InlJ is specifically expressed in vivo and behaves as an adhesin. Infect Immun 76 1368 1378

50. BronPAMonkIRCorrSCHillCGahanCG 2006 Novel luciferase reporter system for in vitro and organ-specific monitoring of differential gene expression in Listeria monocytogenes. Appl Environ Microbiol 72 2876 2884

51. KickhoeferVAVasuSKRomeLH 1996 Vaults are the answer, what is the question? Trends Cell Biol 6 174 178

52. van ZonAMossinkMHScheperRJSonneveldPWiemerEA 2003 The vault complex. Cell Mol Life Sci 60 1828 1837

53. HenryRShaughnessyLLoessnerMJAlberti-SeguiCHigginsDE 2006 Cytolysin-dependent delay of vacuole maturation in macrophages infected with Listeria monocytogenes. Cell Microbiol 8 107 119

54. MizushimaNYoshimoriTLevineB 2010 Methods in mammalian autophagy research. Cell 140 313 326

55. PankivSClausenTHLamarkTBrechABruunJA 2007 p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282 24131 24145

56. LevineBMizushimaNVirginHW 2011 Autophagy in immunity and inflammation. Nature 469 323 335

57. IzquierdoMASchefferGLFlensMJGiacconeGBroxtermanHJ 1996 Broad distribution of the multidrug resistance-related vault lung resistance protein in normal human tissues and tumors. Am J Pathol 148 877 887

58. SunnaramBLGandemerVSebillotMGrandgirardNAmiotL 2003 LRP overexpression in monocytic lineage. Leuk Res 27 755 759

59. CossartPToledo-AranaA 2008 Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect 10 1041 1050

60. LebretonALakisicGJobVFritschLThamTN 2011 A Bacterial Protein Targets the BAHD1 Chromatin Complex to Stimulate Type III Interferon Response. Science 331 1319 1321

61. KedershaNLRomeLH 1986 Isolation and characterization of a novel ribonucleoprotein particle: large structures contain a single species of small RNA. J Cell Biol 103 699 709

62. PerssonHKvistAVallon-ChristerssonJMedstrandPBorgA 2009 The non-coding RNA of the multidrug resistance-linked vault particle encodes multiple regulatory small RNAs. Nat Cell Biol 11 1268 1271

63. SuprenantKA 2002 Vault ribonucleoprotein particles: sarcophagi, gondolas, or safety deposit boxes? Biochemistry 41 14447 14454

64. NandyCMrazekJStoiberHGrasserFAHuttenhoferA 2009 Epstein-barr virus-induced expression of a novel human vault RNA. J Mol Biol 388 776 784

65. SakakiYTerashiKYamaguchiAKawamataNTokitoY 2002 Human T-cell lymphotropic virus type I Tax activates lung resistance-related protein expression in leukemic clones established from an adult T-cell leukemia patient. Exp Hematol 30 340 345

66. OgawaMYoshikawaYMimuroHHainTChakrabortyT 2011 Autophagy targeting of Listeria monocytogenes and the bacterial countermeasure. Autophagy 7 310 314

67. ArnaudMChastanetADebarbouilleM 2004 New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70 6887 6891

68. Boujemaa-PaterskiRGouinEHansenGSamarinSLe ClaincheC 2001 Listeria protein ActA mimics WASp family proteins: it activates filament barbed end branching by Arp2/3 complex. Biochemistry 40 11390 11404

69. VeigaEGuttmanJABonazziMBoucrotEToledo-AranaA 2007 Invasive and adherent bacterial pathogens co-Opt host clathrin for infection. Cell Host Microbe 2 340 351

70. van ZonAMossinkMHSchoesterMHoutsmullerABSchefferGL 2003 The formation of vault-tubes: a dynamic interaction between vaults and vault PARP. J Cell Sci 116 4391 4400

71. MostowySBonazziMHamonMAThamTNMalletA 2010 Entrapment of intracytosolic bacteria by septin cage-like structures. Cell Host Microbe 8 433 444

72. GouinEMengaudJCossartP 1994 The virulence gene cluster of Listeria monocytogenes is also present in Listeria ivanovii, an animal pathogen, and Listeria seeligeri, a nonpathogenic species. Infect Immun 62 3550 3553

73. LevraudJPDissonOKissaKBonneICossartP 2009 Real-time observation of Listeria monocytogenes-phagocyte interactions in living zebrafish larvae. Infect Immun 77 3651 3660