Crimean-Congo Hemorrhagic Fever Virus Entry into Host Cells Occurs through the Multivesicular Body and Requires ESCRT Regulators

PLoS Pathogens

Volumn 10, Issue 9, 2014, Pages

  Shtanko, Olena ^a   Nikitina, Raisa A ^b   Altuntas, Cengiz Z ^c   Chepurnov, Alexander A ^b   Davey, Robert A ^a  

^a SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

^b INSTITUTE OF CLINICAL IMMUNOLOGY   (Russian Federation)

^c Universal American   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN INTERACTING PROTEIN 1; ALIX PROTEIN; BAFILOMYCIN; COMPLEMENTARY DNA; ENHANCED GREEN FLUORESCENT PROTEIN; ESCRT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAB PROTEIN; RAB7 PROTEIN; SMALL INTERFERING RNA; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UNCLASSIFIED DRUG; VACUOLAR PROTEIN SORTING 4 HOMOLOG B; VACUOLAR PROTEIN SORTING ASSOCIATED PROTEIN 24; MESSENGER RNA;

ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; CRIMEAN CONGO HEMORRHAGIC FEVER; DISEASE TRANSMISSION; ENZYME ACTIVITY; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MEMBRANE FUSION; MULTIVESICULAR BODY; PATHOGENESIS; QUANTITAVE ASSAY; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VESICULAR STOMATITIS VIRUS; VIRUS CELL INTERACTION; VIRUS ENTRY; ADRENAL TUMOR; ENDOCYTOSIS; ENZYME IMMUNOASSAY; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; NAIROVIRUS; PATHOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL CULTURE; VIROLOGY; WESTERN BLOTTING;

CRIMEAN-CONGO HEMORRHAGIC FEVER VIRUS;

ADRENAL GLAND NEOPLASMS; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; ENDOCYTOSIS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HEMORRHAGIC FEVER VIRUS, CRIMEAN-CONGO; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOENZYME TECHNIQUES; MULTIVESICULAR BODIES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN TRANSPORT; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED; VIRUS INTERNALIZATION;

EID: 84907587657     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004390     Document Type: Article

References (90)

1. Estrada-Pena A, Ruiz-Fons F, Acevedo P, Gortazar C, de la Fuente J, (2013) Factors driving the circulation and possible expansion of Crimean-Congo haemorrhagic fever virus in the western Palearctic. J Appl Microbiol 114: 278–286.
2. Whitehouse CA, (2004) Crimean-Congo hemorrhagic fever. Antiviral Res 64: 145–160.
3. Ergonul O, (2006) Crimean-Congo haemorrhagic fever. Lancet Infect Dis 6: 203–214.
4. Vorou R, Pierroutsakos IN, Maltezou HC, (2007) Crimean-Congo hemorrhagic fever. Curr Opin Infect Dis 20: 495–500.
5. Schmaljohn CS, Nichol S T. (2007) Bunyaviridae. In: Knipe DM, Howley P M., editor. Fields Virology. Philadelphia: Lippincott Williams & Wilkins. pp. 1741–1789.
6. Sanchez AJ, Vincent MJ, Nichol ST, (2002) Characterization of the glycoproteins of Crimean-Congo hemorrhagic fever virus. J Virol 76: 7263–7275.
7. Sanchez AJ, Vincent MJ, Erickson BR, Nichol ST, (2006) Crimean-congo hemorrhagic fever virus glycoprotein precursor is cleaved by Furin-like and SKI-1 proteases to generate a novel 38-kilodalton glycoprotein. J Virol 80: 514–525.
8. Bergeron E, Vincent MJ, Nichol ST, (2007) Crimean-Congo hemorrhagic fever virus glycoprotein processing by the endoprotease SKI-1/S1P is critical for virus infectivity. J Virol 81: 13271–13276.
9. Erickson BR, Deyde V, Sanchez AJ, Vincent MJ, Nichol ST, (2007) N-linked glycosylation of Gn (but not Gc) is important for Crimean Congo hemorrhagic fever virus glycoprotein localization and transport. Virology 361: 348–355.
10. Bente DA, Forrester NL, Watts DM, McAuley AJ, Whitehouse CA, et al. (2013) Crimean-Congo hemorrhagic fever: history, epidemiology, pathogenesis, clinical syndrome and genetic diversity. Antiviral Res 100: 159–189.
11. Bertolotti-Ciarlet A, Smith J, Strecker K, Paragas J, Altamura LA, et al. (2005) Cellular localization and antigenic characterization of crimean-congo hemorrhagic fever virus glycoproteins. J Virol 79: 6152–6161.
12. Xiao X, Feng Y, Zhu Z, Dimitrov DS, (2011) Identification of a putative Crimean-Congo hemorrhagic fever virus entry factor. Biochem Biophys Res Commun 411: 253–258.
13. Garrison AR, Radoshitzky SR, Kota KP, Pegoraro G, Ruthel G, et al. (2013) Crimean-Congo hemorrhagic fever virus utilizes a clathrin- and early endosome-dependent entry pathway. Virology 444: 45–54.
14. Simon M, Johansson C, Mirazimi A, (2009) Crimean-Congo hemorrhagic fever virus entry and replication is clathrin-, pH- and cholesterol-dependent. J Gen Virol 90: 210–215.
15. Flick R, Flick K, Feldmann H, Elgh F, (2003) Reverse genetics for crimean-congo hemorrhagic fever virus. J Virol 77: 5997–6006.
16. Dumas JJ, Merithew E, Sudharshan E, Rajamani D, Hayes S, et al. (2001) Multivalent endosome targeting by homodimeric EEA1. Mol Cell 8: 947–958.
17. Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, et al. (1992) The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70: 715–728.
18. Li G, Stahl PD, (1993) Structure-function relationship of the small GTPase rab5. J Biol Chem 268: 24475–24480.
19. Stenmark H, Parton RG, Steele-Mortimer O, Lutcke A, Gruenberg J, et al. (1994) Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J 13: 1287–1296.
20. Hirota Y, Kuronita T, Fujita H, Tanaka Y, (2007) A role for Rab5 activity in the biogenesis of endosomal and lysosomal compartments. Biochem Biophys Res Commun 364: 40–47.
21. Rosenfeld JL, Moore RH, Zimmer KP, Alpizar-Foster E, Dai W, et al. (2001) Lysosome proteins are redistributed during expression of a GTP-hydrolysis-defective rab5a. J Cell Sci 114: 4499–4508.
22. Lozach PY, Mancini R, Bitto D, Meier R, Oestereich L, et al. (2010) Entry of bunyaviruses into mammalian cells. Cell Host Microbe 7: 488–499.
23. Woodman PG, Futter CE, (2008) Multivesicular bodies: co-ordinated progression to maturity. Curr Opin Cell Biol 20: 408–414.
24. Gruenberg J, Stenmark H, (2004) The biogenesis of multivesicular endosomes. Nat Rev Mol Cell Biol 5: 317–323.
25. Pasqual G, Rojek JM, Masin M, Chatton JY, Kunz S, (2011) Old world arenaviruses enter the host cell via the multivesicular body and depend on the endosomal sorting complex required for transport. PLoS Pathog 7: e1002232.
26. Khor R, McElroy LJ, Whittaker GR, (2003) The ubiquitin-vacuolar protein sorting system is selectively required during entry of influenza virus into host cells. Traffic 4: 857–868.
27. Le Blanc I, Luyet PP, Pons V, Ferguson C, Emans N, et al. (2005) Endosome-to-cytosol transport of viral nucleocapsids. Nat Cell Biol 7: 653–664.
28. Luyet PP, Falguieres T, Pons V, Pattnaik AK, Gruenberg J, (2008) The ESCRT-I subunit TSG101 controls endosome-to-cytosol release of viral RNA. Traffic 9: 2279–2290.
29. Kobayashi T, Vischer UM, Rosnoblet C, Lebrand C, Lindsay M, et al. (2000) The tetraspanin CD63/lamp3 cycles between endocytic and secretory compartments in human endothelial cells. Mol Biol Cell 11: 1829–1843.
30. Metzelaar MJ, Wijngaard PL, Peters PJ, Sixma JJ, Nieuwenhuis HK, et al. (1991) CD63 antigen. A novel lysosomal membrane glycoprotein, cloned by a screening procedure for intracellular antigens in eukaryotic cells. J Biol Chem 266: 3239–3245.
31. Sadoul R, (2006) Do Alix and ALG-2 really control endosomes for better or for worse? Biol Cell 98: 69–77.
32. Vanlandingham PA, Ceresa BP, (2009) Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. J Biol Chem 284: 12110–12124.
33. Vonderheit A, Helenius A, (2005) Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 3: e233.
34. Zerial M, McBride H, (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2: 107–117.
35. Feng Y, Press B, Wandinger-Ness A, (1995) Rab 7: an important regulator of late endocytic membrane traffic. J Cell Biol 131: 1435–1452.
36. Buchholz UJ, Finke S, Conzelmann KK, (1999) Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 73: 251–259.
37. Bowman EJ, Siebers A, Altendorf K, (1988) Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci U S A 85: 7972–7976.
38. Fretz M, Jin J, Conibere R, Penning NA, Al-Taei S, et al. (2006) Effects of Na+/H+ exchanger inhibitors on subcellular localisation of endocytic organelles and intracellular dynamics of protein transduction domains HIV-TAT peptide and octaarginine. J Control Release 116: 247–254.
39. Akaike N, Harata N, (1994) Nystatin perforated patch recording and its applications to analyses of intracellular mechanisms. Jpn J Physiol 44: 433–473.
40. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, et al. (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10: 839–850.
41. Wang LH, Rothberg KG, Anderson RG, (1993) Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 123: 1107–1117.
42. Fernandez-Borja M, Wubbolts R, Calafat J, Janssen H, Divecha N, et al. (1999) Multivesicular body morphogenesis requires phosphatidyl-inositol 3-kinase activity. Curr Biol 9: 55–58.
43. Futter CE, Collinson LM, Backer JM, Hopkins CR, (2001) Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J Cell Biol 155: 1251–1264.
44. Vlahos CJ, Matter WF, Hui KY, Brown RF, (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 269: 5241–5248.
45. Fader CM, Colombo MI, (2009) Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ 16: 70–78.
46. Bishop N, Woodman P, (2000) ATPase-defective mammalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking. Mol Biol Cell 11: 227–239.
47. Liscum L, Faust JR, (1989) The intracellular transport of low density lipoprotein-derived cholesterol is inhibited in Chinese hamster ovary cells cultured with 3-beta-[2-(diethylamino)ethoxy]androst-5-en-17-one. J Biol Chem 264: 11796–11806.
48. Beatty WL, (2008) Late endocytic multivesicular bodies intersect the chlamydial inclusion in the absence of CD63. Infect Immun 76: 2872–2881.
49. Higgins ME, Davies JP, Chen FW, Ioannou YA, (1999) Niemann-Pick C1 is a late endosome-resident protein that transiently associates with lysosomes and the trans-Golgi network. Mol Genet Metab 68: 1–13.
50. Kobayashi T, Beuchat MH, Lindsay M, Frias S, Palmiter RD, et al. (1999) Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat Cell Biol 1: 113–118.
51. Simon M, Johansson C, Lundkvist A, Mirazimi A, (2009) Microtubule-dependent and microtubule-independent steps in Crimean-Congo hemorrhagic fever virus replication cycle. Virology 385: 313–322.
52. Sokol J, Blanchette-Mackie J, Kruth HS, Dwyer NK, Amende LM, et al. (1988) Type C Niemann-Pick disease. Lysosomal accumulation and defective intracellular mobilization of low density lipoprotein cholesterol. J Biol Chem 263: 3411–3417.
53. Carette JE, Raaben M, Wong AC, Herbert AS, Obernosterer G, et al. (2011) Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477: 340–343.
54. Cote M, Misasi J, Ren T, Bruchez A, Lee K, et al. (2011) Small molecule inhibitors reveal Niemann-Pick C1 is essential for Ebola virus infection. Nature 477: 344–348.
55. Jae LT, Raaben M, Herbert AS, Kuehne AI, Wirchnianski AS, et al. (2014) Virus entry. Lassa virus entry requires a trigger-induced receptor switch. Science 344: 1506–1510.
56. Trowbridge IS, Collawn JF, Hopkins CR, (1993) Signal-dependent membrane protein trafficking in the endocytic pathway. Annu Rev Cell Biol 9: 129–161.
57. Mellman I, (1996) Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 12: 575–625.
58. Mellman I, Warren G, (2000) The road taken: past and future foundations of membrane traffic. Cell 100: 99–112.
59. Lakadamyali M, Rust MJ, Zhuang X, (2006) Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124: 997–1009.
60. Pearse BM, Smith CJ, Owen DJ, (2000) Clathrin coat construction in endocytosis. Curr Opin Struct Biol 10: 220–228.
61. Wasano K, Hirakawa Y, (1994) Lamellar bodies of rat alveolar type 2 cells have late endosomal marker proteins on their limiting membranes. Histochemistry 102: 329–335.
62. Calafat J, Nijenhuis M, Janssen H, Tulp A, Dusseljee S, et al. (1994) Major histocompatibility complex class II molecules induce the formation of endocytic MIIC-like structures. J Cell Biol 126: 967–977.
63. Finzi A, Brunet A, Xiao Y, Thibodeau J, Cohen EA, (2006) Major histocompatibility complex class II molecules promote human immunodeficiency virus type 1 assembly and budding to late endosomal/multivesicular body compartments. J Virol 80: 9789–9797.
64. Hutagalung AH, Novick PJ, (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91: 119–149.
65. Stenmark H, (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10: 513–525.
66. Gaullier JM, Simonsen A, D'Arrigo A, Bremnes B, Stenmark H, et al. (1998) FYVE fingers bind PtdIns(3)P. Nature 394: 432–433.
67. Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, et al. (2000) Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 19: 4577–4588.
68. Bache KG, Brech A, Mehlum A, Stenmark H, (2003) Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J Cell Biol 162: 435–442.
69. Cantley LC, (2002) The phosphoinositide 3-kinase pathway. Science 296: 1655–1657.
70. Fruman DA, Rommel C, (2014) PI3K and cancer: lessons, challenges and opportunities. Nat Rev Drug Discov 13: 140–156.
71. Xu H, Li X, Liu D, Li J, Zhang X, et al. (2013) Follicular T-helper cell recruitment governed by bystander B cells and ICOS-driven motility. Nature 496: 523–527.
72. National Institutes of Health (NIH). ClinicalTrials.gov. http://clinicaltrials.gov/ct2/show/NCT01297491. Accessed February 19, 2014.
73. Ogino M, Ebihara H, Lee BH, Araki K, Lundkvist A, et al. (2003) Use of vesicular stomatitis virus pseudotypes bearing hantaan or seoul virus envelope proteins in a rapid and safe neutralization test. Clin Diagn Lab Immunol 10: 154–160.
74. Higa MM, Petersen J, Hooper J, Doms RW, (2012) Efficient production of Hantaan and Puumala pseudovirions for viral tropism and neutralization studies. Virology 423: 134–142.
75. Brown KS, Safronetz D, Marzi A, Ebihara H, Feldmann H, (2011) Vesicular stomatitis virus-based vaccine protects hamsters against lethal challenge with Andes virus. J Virol 85: 12781–12791.
76. de Boer SM, Kortekaas J, de Haan CA, Rottier PJ, Moormann RJ, et al. (2012) Heparan sulfate facilitates Rift Valley fever virus entry into the cell. J Virol 86: 13767–13771.
77. Hollidge BS, Nedelsky NB, Salzano MV, Fraser JW, Gonzalez-Scarano F, et al. (2012) Orthobunyavirus entry into neurons and other mammalian cells occurs via clathrin-mediated endocytosis and requires trafficking into early endosomes. J Virol 86: 7988–8001.
78. Pobjecky N, Smith J, Gonzalez-Scarano F, (1986) Biological studies of the fusion function of California serogroup Bunyaviruses. Microb Pathog 1: 491–501.
79. Jin M, Park J, Lee S, Park B, Shin J, et al. (2002) Hantaan virus enters cells by clathrin-dependent receptor-mediated endocytosis. Virology 294: 60–69.
80. Santos RI, Rodrigues AH, Silva ML, Mortara RA, Rossi MA, et al. (2008) Oropouche virus entry into HeLa cells involves clathrin and requires endosomal acidification. Virus Res 138: 139–143.
81. Hofmann H, Li X, Zhang X, Liu W, Kuhl A, et al. (2013) Severe fever with thrombocytopenia virus glycoproteins are targeted by neutralizing antibodies and can use DC-SIGN as a receptor for pH-dependent entry into human and animal cell lines. J Virol 87: 4384–4394.
82. Kobasa D, Rodgers ME, Wells K, Kawaoka Y, (1997) Neuraminidase hemadsorption activity, conserved in avian influenza A viruses, does not influence viral replication in ducks. J Virol 71: 6706–6713.
83. Niwa H, Yamamura K, Miyazaki J, (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193–199.
84. Muhlberger E, Weik M, Volchkov VE, Klenk HD, Becker S, (1999) Comparison of the transcription and replication strategies of marburg virus and Ebola virus by using artificial replication systems. J Virol 73: 2333–2342.
85. Saeed MF, Kolokoltsov AA, Davey RA, (2006) Novel, rapid assay for measuring entry of diverse enveloped viruses, including HIV and rabies. J Virol Methods 135: 143–150.
86. Davey RA, Zuo Y, Cunningham JM, (1999) Identification of a receptor-binding pocket on the envelope protein of friend murine leukemia virus. J Virol 73: 3758–3763.
87. Kolokoltsov AA, Deniger D, Fleming EH, Roberts NJ, JrKarpilow JM, et al. (2007) Small interfering RNA profiling reveals key role of clathrin-mediated endocytosis and early endosome formation for infection by respiratory syncytial virus. J Virol 81: 7786–7800.
88. Kolokoltsov AA, Fleming EH, Davey RA, (2006) Venezuelan equine encephalitis virus entry mechanism requires late endosome formation and resists cell membrane cholesterol depletion. Virology 347: 333–342.
89. Miller ME, Adhikary S, Kolokoltsov AA, Davey RA, (2012) Ebolavirus requires acid sphingomyelinase activity and plasma membrane sphingomyelin for infection. J Virol 86: 7473–7483.
90. Kolokoltsov AA, Adhikary S, Garver J, Johnson L, Davey RA, et al. (2012) Inhibition of Lassa virus and Ebola virus infection in host cells treated with the kinase inhibitors genistein and tyrphostin. Arch Virol 157: 121–127.