Old World Arenaviruses Enter the Host Cell via the Multivesicular Body and Depend on the Endosomal Sorting Complex Required for Transport

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The highly pathogenic Old World arenavirus Lassa virus (LASV) and the prototypic arenavirus lymphocytic choriomeningitis virus (LCMV) use α-dystroglycan as a cellular receptor and enter the host cell by an unusual endocytotic pathway independent of clathrin, caveolin, dynamin, and actin. Upon internalization, the viruses are delivered to acidified endosomes in a Rab5-independent manner bypassing classical routes of incoming vesicular trafficking. Here we sought to identify cellular factors involved in the unusual and largely unknown entry pathway of LASV and LCMV. Cell entry of LASV and LCMV required microtubular transport to late endosomes, consistent with the low fusion pH of the viral envelope glycoproteins. Productive infection with recombinant LCMV expressing LASV envelope glycoprotein (rLCMV-LASVGP) and LCMV depended on phosphatidyl inositol 3-kinase (PI3K) as well as lysobisphosphatidic acid (LBPA), an unusual phospholipid that is involved in the formation of intraluminal vesicles (ILV) of the multivesicular body (MVB) of the late endosome. We provide evidence for a role of the endosomal sorting complex required for transport (ESCRT) in LASV and LCMV cell entry, in particular the ESCRT components Hrs, Tsg101, Vps22, and Vps24, as well as the ESCRT-associated ATPase Vps4 involved in fission of ILV. Productive infection with rLCMV-LASVGP and LCMV also critically depended on the ESCRT-associated protein Alix, which is implicated in membrane dynamics of the MVB/late endosomes. Our study identifies crucial cellular factors implicated in Old World arenavirus cell entry and indicates that LASV and LCMV invade the host cell passing via the MVB/late endosome. Our data further suggest that the virus-receptor complexes undergo sorting into ILV of the MVB mediated by the ESCRT, possibly using a pathway that may be linked to the cellular trafficking and degradation of the cellular receptor.

Vyšlo v časopise: Old World Arenaviruses Enter the Host Cell via the Multivesicular Body and Depend on the Endosomal Sorting Complex Required for Transport. PLoS Pathog 7(9): e32767. doi:10.1371/journal.ppat.1002232
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002232

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1. GeisbertTWJahrlingPB 2004 Exotic emerging viral diseases: progress and challenges. Nat Med 10 S110 121

2. McCormickJBFisher-HochSP 2002 Lassa fever. Curr Top Microbiol Immunol 262 75 109

3. RichmondJKBagloleDJ 2003 Lassa fever: epidemiology, clinical features, and social consequences. BMJ 327 1271 1275

4. McCormickJBKingIJWebbPAJohnsonKMO'SullivanR 1987 A case-control study of the clinical diagnosis and course of Lassa fever. J Infect Dis 155 445 455

5. Fisher-HochSPTomoriONasidiAPerez-OronozGIFakileY 1995 Review of cases of nosocomial Lassa fever in Nigeria: the high price of poor medical practice. BMJ 311 857 859

6. BartonLLMetsMBBeauchampCL 2002 Lymphocytic choriomeningitis virus: emerging fetal teratogen. Am J Obstet Gynecol 187 1715 1716

7. JahrlingPBPetersCJ 1992 Lymphocytic choriomeningitis virus. A neglected pathogen of man. Arch Pathol Lab Med 116 486 488

8. MetsMBBartonLLKhanASKsiazekTG 2000 Lymphocytic choriomeningitis virus: an underdiagnosed cause of congenital chorioretinitis. Am J Ophthalmol 130 209 215

9. FischerSAGrahamMBKuehnertMJKottonCNSrinivasanA 2006 Transmission of lymphocytic choriomeningitis virus by organ transplantation. N Engl J Med 354 2235 2249

10. PetersCJ 2006 Lymphocytic choriomeningitis virus–an old enemy up to new tricks. N Engl J Med 354 2208 2211

11. BuchmeierMJde la TorreJCPetersCJ 2007 Arenaviridae: the viruses and their replication. KnipeDLHowleyPM Fields Virology. 4th ed Philadelphia Lippincott-Raven 1791 1828

12. MarshMHeleniusA 2006 Virus entry: open sesame. Cell 124 729 740

13. SmithAEHeleniusA 2004 How viruses enter animal cells. Science 304 237 242

14. CaoWHenryMDBorrowPYamadaHElderJH 1998 Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus [see comments]. Science 282 2079 2081

15. BarresiRCampbellKP 2006 Dystroglycan: from biosynthesis to pathogenesis of human disease. J Cell Sci 119 199 207

16. SpiropoulouCFKunzSRollinPECampbellKPOldstoneMB 2002 New World arenavirus clade C, but not clade A and B viruses, utilizes alpha-dystroglycan as its major receptor. J Virol 76 5140 5146

17. BorrowPOldstoneMB 1994 Mechanism of lymphocytic choriomeningitis virus entry into cells. Virology 198 1 9

18. KlewitzCKlenkHDter MeulenJ 2007 Amino acids from both N-terminal hydrophobic regions of the Lassa virus envelope glycoprotein GP-2 are critical for pH-dependent membrane fusion and infectivity. J Gen Virol 88 2320 2328

19. QuirinKEschliBScheuIPoortLKartenbeckJ 2008 Lymphocytic choriomeningitis virus uses a novel endocytic pathway for infectious entry via late endosomes. Virology 378 21 33

20. RojekJMPerezMKunzS 2008 Cellular entry of lymphocytic choriomeningitis virus. J Virol 82 1505 1517

21. RojekJMSanchezABNguyenNTde la TorreJCKunzS 2008 Different mechanisms of cell entry by human-pathogenic Old World and New World arenaviruses. J Virol 82 7677 7687

22. VonderheitAHeleniusA 2005 Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 3 e233

23. Le BlancILuyetPPPonsVFergusonCEmansN 2005 Endosome-to-cytosol transport of viral nucleocapsids. Nat Cell Biol 7 653 664

24. TakadaARobisonCGotoHSanchezAMurtiKG 1997 A system for functional analysis of Ebola virus glycoprotein. Proc Natl Acad Sci U S A 94 14764 14769

25. KunzSRojekJPerezMSpiropoulouCMBO 2005 Characterization of the interaction of Lassa fever virus with its cellular receptor α-dystroglycan. J Virol 79 5979 5987

26. LylesDSRupprechtCE 2007 Rhabdoviridae. KnipeDMHowleyPM Fields Virology. 5th ed Philadelphia Lippincott 1363

27. PinschewerDDPerezMJeetendraEBachiTHorvathE 2004 Kinetics of protective antibodies are determined by the viral surface antigen. J Clin Invest 114 988 993

28. ClementeRde la TorreJC 2009 Cell entry of Borna disease virus follows a clathrin-mediated endocytosis pathway that requires Rab5 and microtubules. J Virol 83 10406 10416

29. JohannsdottirHKManciniRKartenbeckJAmatoLHeleniusA 2009 Host cell factors and functions involved in vesicular stomatitis virus entry. J Virol 83 440 453

30. OhkumaSPooleB 1978 Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc Natl Acad Sci U S A 75 3327 3331

31. OhkumaSPooleB 1981 Cytoplasmic vacuolation of mouse peritoneal macrophages and the uptake into lysosomes of weakly basic substances. J Cell Biol 90 656 664

32. ShahWAPengHCarbonettoS 2006 Role of non-raft cholesterol in lymphocytic choriomeningitis virus infection via alpha-dystroglycan. J Gen Virol 87 673 678

33. VelaEMZhangLColpittsTMDaveyRAAronsonJF 2007 Arenavirus entry occurs through a cholesterol-dependent, non-caveolar, clathrin-mediated endocytic mechanism. Virology 13 13

34. BenmerahALamazeCBegueBSchmidSLDautry-VarsatA 1998 AP-2/Eps15 interaction is required for receptor-mediated endocytosis. J Cell Biol 140 1055 1062

35. NicholsBJ 2002 A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat Cell Biol 4 374 378

36. DamkeHBabaTWarnockDESchmidSL 1994 Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127 915 934

37. OhPMcIntoshDPSchnitzerJE 1998 Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J Cell Biol 141 101 114

38. van der BliekAMRedelmeierTEDamkeHTisdaleEJMeyerowitzEM 1993 Mutations in human dynamin block an intermediate stage in coated vesicle formation. J Cell Biol 122 553 563

39. GruenbergJ 2001 The endocytic pathway: a mosaic of domains. Nat Rev Mol Cell Biol 2 721 730

40. ZerialMMcBrideH 2001 Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2 107 117

41. RaiborgCStenmarkH 2009 The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458 445 452

42. MatsuoHChevallierJMayranNLe BlancIFergusonC 2004 Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science 303 531 534

43. HenryMDCampbellKP 1998 A role for dystroglycan in basement membrane assembly. Cell 95 859 870

44. HallKBlair ZajdelMEBlairGE 2010 Unity and diversity in the human adenoviruses: exploiting alternative entry pathways for gene therapy. Biochem J 431 321 336

45. MeierOGreberUF 2004 Adenovirus endocytosis. J Gene Med 6 Suppl 1 S152 163

46. BacheKGBrechAMehlumAStenmarkH 2003 Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J Cell Biol 162 435 442

47. BabstMOdorizziGEstepaEJEmrSD 2000 Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1 248 258

48. RaziMFutterCE 2006 Distinct roles for Tsg101 and Hrs in multivesicular body formation and inward vesiculation. Mol Biol Cell 17 3469 3483

49. BacheKGStuffersSMalerodLSlagsvoldTRaiborgC 2006 The ESCRT-III subunit hVps24 is required for degradation but not silencing of the epidermal growth factor receptor. Mol Biol Cell 17 2513 2523

50. MalerodLStuffersSBrechAStenmarkH 2007 Vps22/EAP30 in ESCRT-II mediates endosomal sorting of growth factor and chemokine receptors destined for lysosomal degradation. Traffic 8 1617 1629

51. PerezMCravenRCde la TorreJC 2003 The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc Natl Acad Sci U S A 100 12978 12983

52. KanagawaMSaitoFKunzSYoshida-MoriguchiTBarresiR 2004 Molecular recognition by LARGE is essential for expression of functional dystroglycan. Cell 117 953 964

53. ScheuringSRohrichtRASchoning-BurkhardtBBeyerAMullerS 2001 Mammalian cells express two VPS4 proteins both of which are involved in intracellular protein trafficking. J Mol Biol 312 469 480

54. BishopNWoodmanP 2000 ATPase-defective mammalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking. Mol Biol Cell 11 227 239

55. FujitaHYamanakaMImamuraKTanakaYNaraA 2003 A dominant negative form of the AAA ATPase SKD1/VPS4 impairs membrane trafficking out of endosomal/lysosomal compartments: class E vps phenotype in mammalian cells. J Cell Sci 116 401 414

56. UrataSNodaTKawaokaYYokosawaHYasudaJ 2006 Cellular factors required for Lassa virus budding. J Virol 80 4191 4195

57. KunzSSevillaNRojekJMOldstoneMB 2004 Use of alternative receptors different than alpha-dystroglycan by selected isolates of lymphocytic choriomeningitis virus. Virology 325 432 445

58. PiresRHartliebBSignorLSchoehnGLataS 2009 A crescent-shaped ALIX dimer targets ESCRT-III CHMP4 filaments. Structure 17 843 856

59. McCulloughJFisherRDWhitbyFGSundquistWIHillCP 2008 ALIX-CHMP4 interactions in the human ESCRT pathway. Proc Natl Acad Sci U S A 105 7687 7691

60. AbramiLLindsayMPartonRGLepplaSHvan der GootFG 2004 Membrane insertion of anthrax protective antigen and cytoplasmic delivery of lethal factor occur at different stages of the endocytic pathway. J Cell Biol 166 645 651

61. SchmidtMHHoellerDYuJFurnariFBCaveneeWK 2004 Alix/AIP1 antagonizes epidermal growth factor receptor downregulation by the Cbl-SETA/CIN85 complex. Mol Cell Biol 24 8981 8993

62. Chatellard-CausseCBlotBCristinaNTorchSMissottenM 2002 Alix (ALG-2-interacting protein X), a protein involved in apoptosis, binds to endophilins and induces cytoplasmic vacuolization. J Biol Chem 277 29108 29115

63. StrackBCalistriACraigSPopovaEGottlingerHG 2003 AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114 689 699

64. ChenCVincentOJinJWeiszOAMontelaroRC 2005 Functions of early (AP-2) and late (AIP1/ALIX) endocytic proteins in equine infectious anemia virus budding. J Biol Chem 280 40474 40480

65. ZhaiQFisherRDChungHYMyszkaDGSundquistWI 2008 Structural and functional studies of ALIX interactions with YPX(n)L late domains of HIV-1 and EIAV. Nat Struct Mol Biol 15 43 49

66. SevillaNKunzSHolzALewickiHHomannD 2000 Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells. J Exp Med 192 1249 1260

67. SmeltSCBorrowPKunzSCaoWTishonA 2001 Differences in affinity of binding of lymphocytic choriomeningitis virus strains to the cellular receptor alpha-dystroglycan correlate with viral tropism and disease kinetics. J Virol 75 448 457

68. RojekJMPasqualGSanchezABNguyenNTde la TorreJC 2010 Targeting the proteolytic processing of the viral glycoprotein precursor is a promising novel antiviral strategy against arenaviruses. J Virol 84 573 584

69. CossetFLMarianneauPVerneyGGallaisFTordoN 2009 Characterization of Lassa virus cell entry and neutralization with Lassa virus pseudoparticles. J Virol 83 3228 3237

70. Puig-KrogerASerrano-GomezDCaparrosEDominguez-SotoARellosoM 2004 Regulated expression of the pathogen receptor dendritic cell-specific intercellular adhesion molecule 3 (ICAM-3)-grabbing nonintegrin in THP-1 human leukemic cells, monocytes, and macrophages. J Biol Chem 279 25680 25688

71. KunzSRojekJMPerezMSpiropoulouCFOldstoneMB 2005 Characterization of the interaction of lassa fever virus with its cellular receptor alpha-dystroglycan. J Virol 79 5979 5987

72. ReignierTOldenburgJNobleBLambERomanowskiV 2006 Receptor use by pathogenic arenaviruses. Virology 353 111 120 Epub 2006 Jun 21

73. KunzSSevillaNMcGavernDBCampbellKPOldstoneMB 2001 Molecular analysis of the interaction of LCMV with its cellular receptor [alpha]-dystroglycan. J Cell Biol 155 301 310

74. TengMNBorrowPOldstoneMBde la TorreJC 1996 A single amino acid change in the glycoprotein of lymphocytic choriomeningitis virus is associated with the ability to cause growth hormone deficiency syndrome. J Virol 70 8438 8443

75. TrombettaESMellmanI 2005 Cell biology of antigen processing in vitro and in vivo. Annu Rev Immunol 23 975 1028

76. BurgdorfSKurtsC 2008 Endocytosis mechanisms and the cell biology of antigen presentation. Curr Opin Immunol 20 89 95

77. AbramiLReigNvan der GootFG 2005 Anthrax toxin: the long and winding road that leads to the kill. Trends Microbiol 13 72 78

78. KhorRMcElroyLJWhittakerGR 2003 The ubiquitin-vacuolar protein sorting system is selectively required during entry of influenza virus into host cells. Traffic 4 857 868

79. LuyetPPFalguieresTPonsVPattnaikAKGruenbergJ 2008 The ESCRT-I subunit TSG101 controls endosome-to-cytosol release of viral RNA. Traffic 9 2279 2290

80. MahantySHutchinsonKAgarwalSMcRaeMRollinPE 2003 Cutting edge: impairment of dendritic cells and adaptive immunity by Ebola and Lassa viruses. J Immunol 170 2797 2801

81. BaizeSKaplonJFaureCPannetierDGeorges-CourbotMC 2004 Lassa virus infection of human dendritic cells and macrophages is productive but fails to activate cells. J Immunol 172 2861 2869

82. BeutlerBJiangZGeorgelPCrozatKCrokerB 2006 Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu Rev Immunol 24 353 389

83. BuchmeierMJLewickiHATomoriOOldstoneMB 1981 Monoclonal antibodies to lymphocytic choriomeningitis and pichinde viruses: generation, characterization, and cross-reactivity with other arenaviruses. Virology 113 73 85

84. KobayashiTStangEFangKSde MoerloosePPartonRG 1998 A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392 193 197

85. LefrancoisLLylesDS 1982 The interaction of antibody with the major surface glycoprotein of vesicular stomatitis virus. II. Monoclonal antibodies of nonneutralizing and cross-reactive epitopes of Indiana and New Jersey serotypes. Virology 121 168 174

86. AhmedRSalmiAButlerLDChillerJMOldstoneMB 1984 Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J Exp Med 160 521 540

87. DutkoFJOldstoneMB 1983 Genomic and biological variation among commonly used lymphocytic choriomeningitis virus strains. J Gen Virol 64 Pt 8 1689 1698

88. CaoWHenryMDBorrowPYamadaHElderJH 1998 Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282 2079 2081

89. BenmerahABayrouMCerf-BensussanNDautry-VarsatA 1999 Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J Cell Sci 112 Pt 9 1303 1311

90. SieczkarskiSBWhittakerGR 2002 Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J Virol 76 10455 10464

91. SieczkarskiSBWhittakerGR 2003 Differential requirements of Rab5 and Rab7 for endocytosis of influenza and other enveloped viruses. Traffic 4 333 343

92. RojekJMLeeAMNguyenNSpiropoulouCFKunzS 2008 Site 1 protease is required for proteolytic processing of the glycoproteins of the South American hemorrhagic fever viruses Junin, Machupo, and Guanarito. J Virol 82 6045 6051

93. BishopNHormanAWoodmanP 2002 Mammalian class E vps proteins recognize ubiquitin and act in the removal of endosomal protein-ubiquitin conjugates. J Cell Biol 157 91 101

94. LivakKJSchmittgenTD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25 402 408

95. KimSKimHChangBAhnNHwangS 2006 Regulation of transferrin recycling kinetics by PtdIns[4,5]P2 availability. FASEB J 20 2399 2401

96. LiLLiaoJRulandJMakTWCohenSN 2001 A TSG101/MDM2 regulatory loop modulates MDM2 degradation and MDM2/p53 feedback control. Proc Natl Acad Sci U S A 98 1619 1624