Human Metapneumovirus Is Capable of Entering Cells by Fusion with Endosomal Membranes

PLoS Pathogens

Volumn 11, Issue 12, 2015, Pages

  Cox, Reagan G ^a   Mainou, Bernardo A ^b   Johnson, Monika ^c   Hastings, Andrew K ^a   Schuster, Jennifer E ^d   Dermody, Terence S ^a   Williams, John V ^c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d CHILDREN S MERCY HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; DYNAMIN; INTEGRIN; NEUTRALIZING ANTIBODY; SMALL INTERFERING RNA; VIRUS PROTEIN; VIRUS FUSION PROTEIN;

ACTIN POLYMERIZATION; ANTIBODY RESPONSE; ARTICLE; BRONCHUS MUCOSA; CELL FUSION; CONFOCAL MICROSCOPY; DNA TRANSFECTION; ENDOCYTOSIS; ENDOSOME; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN METAPNEUMOVIRUS; MEMBRANE TRANSPORT; NONHUMAN; PATHOGENESIS; PROTEIN BINDING; QUANTITATIVE ASSAY; RNA INTERFERENCE; VIRUS ENTRY; VIRUS NEUTRALIZATION; BRONCHUS; CELL LINE; GENETIC TRANSFECTION; HUMAN; METABOLISM; METAPNEUMOVIRUS; PARAMYXOVIRUS INFECTION; PHYSIOLOGY; RESPIRATORY MUCOSA; VIROLOGY;

BRONCHI; CELL LINE; ENDOSOMES; FLOW CYTOMETRY; HUMANS; METAPNEUMOVIRUS; MICROSCOPY, CONFOCAL; PARAMYXOVIRIDAE INFECTIONS; RESPIRATORY MUCOSA; RNA, SMALL INTERFERING; TRANSFECTION; VIRAL FUSION PROTEINS; VIRUS INTERNALIZATION;

EID: 84953209970     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005303     Document Type: Article

References (76)

1. van den Hoogen BG, de Jong JC, Groen J, Kuiken T, de Groot R, et al. (2001) A newly discovered human pneumovirus isolated from young children with respiratory tract disease. Nat Med 7: 719–724. 11385510
2. Boivin G, De Serres G, Cote S, Gilca R, Abed Y, et al. (2003) Human metapneumovirus infections in hospitalized children. Emerg Infect Dis 9: 634–640. 12781001
3. Williams JV, Wang CK, Yang CF, Tollefson SJ, House FS, et al. (2006) The role of human metapneumovirus in upper respiratory tract infections in children: a 20-year experience. J Infect Dis 193: 387–395. 16388486
4. Williams JV, Harris PA, Tollefson SJ, Halburnt-Rush LL, Pingsterhaus JM, et al. (2004) Human metapneumovirus and lower respiratory tract disease in otherwise healthy infants and children. N Engl J Med 350: 443–450. 14749452
5. van den Hoogen BG, van Doornum GJ, Fockens JC, Cornelissen JJ, Beyer WE, et al. (2003) Prevalence and clinical symptoms of human metapneumovirus infection in hospitalized patients. J Infect Dis 188: 1571–1577. 14624384
6. Peiris JS, Tang WH, Chan KH, Khong PL, Guan Y, et al. (2003) Children with respiratory disease associated with metapneumovirus in Hong Kong. Emerg Infect Dis 9: 628–633. 12781000
7. Mullins JA, Erdman DD, Weinberg GA, Edwards K, Hall CB, et al. (2004) Human metapneumovirus infection among children hospitalized with acute respiratory illness. Emerg Infect Dis 10: 700–705. 15200863
8. McAdam AJ, Hasenbein ME, Feldman HA, Cole SE, Offermann JT, et al. (2004) Human metapneumovirus in children tested at a tertiary-care hospital. J Infect Dis 190: 20–26. 15195239
9. Mackay IM, Bialasiewicz S, Jacob KC, McQueen E, Arden KE, et al. (2006) Genetic diversity of human metapneumovirus over 4 consecutive years in Australia. J Infect Dis 193: 1630–1633. 16703505
10. Foulongne V, Guyon G, Rodiere M, Segondy M, (2006) Human metapneumovirus infection in young children hospitalized with respiratory tract disease. Pediatr Infect Dis J 25: 354–359. 16567989
11. Esper F, Martinello RA, Boucher D, Weibel C, Ferguson D, et al. (2004) A 1-year experience with human metapneumovirus in children aged <5 years. J Infect Dis 189: 1388–1396. 15073675
12. Ebihara T, Endo R, Kikuta H, Ishiguro N, Ishiko H, et al. (2004) Human metapneumovirus infection in Japanese children. J Clin Microbiol 42: 126–132. 14715742
13. Dollner H, Risnes K, Radtke A, Nordbo SA, (2004) Outbreak of human metapneumovirus infection in norwegian children. Pediatr Infect Dis J 23: 436–440. 15131467
14. Loughlin GM, Moscona A, (2006) The cell biology of acute childhood respiratory disease: therapeutic implications. Pediatr Clin North Am 53: 929–959, ix-x. 17027618
15. Bullough PA, Hughson FM, Skehel JJ, Wiley DC, (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371: 37–43. 8072525
16. Rucker P, Wieninger SA, Matthias Ullmann G, Sticht H, (2012) Ph-dependent molecular dynamics of vesicular stomatitis virus glycoprotein G. Proteins 80: 2601–2613. doi: 10.1002/prot.24145 22806964
17. Miyauchi K, Kim Y, Latinovic O, Morozov V, Melikyan GB, (2009) HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137: 433–444. doi: 10.1016/j.cell.2009.02.046 19410541
18. Gobeil LA, Lodge R, Tremblay MJ, (2012) Differential HIV-1 endocytosis and susceptibility to virus infection in human macrophages correlate with cell activation status. J Virol 86: 10399–10407. doi: 10.1128/JVI.01051-12 22787228
19. Gobeil LA, Lodge R, Tremblay MJ, (2013) Macropinocytosis-like HIV-1 internalization in macrophages is CCR5 dependent and leads to efficient but delayed degradation in endosomal compartments. J Virol 87: 735–745. doi: 10.1128/JVI.01802-12 23115275
20. Sloan RD, Kuhl BD, Mesplede T, Munch J, Donahue DA, et al. (2013) Productive entry of HIV-1 during cell-to-cell transmission via dynamin-dependent endocytosis. J Virol 87: 8110–8123. doi: 10.1128/JVI.00815-13 23678185
21. Grove J, Marsh M, (2011) The cell biology of receptor-mediated virus entry. The Journal of cell biology 195: 1071–1082. doi: 10.1083/jcb.201108131 22123832
22. Lamb RA, Jardetzky TS, (2007) Structural basis of viral invasion: lessons from paramyxovirus F. Curr Opin Struct Biol 17: 427–436. 17870467
23. Kolokoltsov AA, Deniger D, Fleming EH, Roberts NJ, Jr.Karpilow 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. 17494077
24. Krzyzaniak MA, Zumstein MT, Gerez JA, Picotti P, Helenius A, (2013) Host cell entry of respiratory syncytial virus involves macropinocytosis followed by proteolytic activation of the f protein. PLoS Pathog 9: e1003309. doi: 10.1371/journal.ppat.1003309 23593008
25. San-Juan-Vergara H, Sampayo-Escobar V, Reyes N, Cha B, Pacheco-Lugo L, et al. (2012) Cholesterol-rich microdomains as docking platforms for respiratory syncytial virus in normal human bronchial epithelial cells. J Virol 86: 1832–1843. doi: 10.1128/JVI.06274-11 22090136
26. Cseke G, Maginnis MS, Cox RG, Tollefson SJ, Podsiad AB, et al. (2009) Integrin alphavbeta1 promotes infection by human metapneumovirus. Proceedings of the National Academy of Sciences of the United States of America 106: 1566–1571. doi: 10.1073/pnas.0801433106 19164533
27. Cox RG, Livesay SB, Johnson M, Ohi MD, Williams JV, (2012) The Human Metapneumovirus Fusion Protein Mediates Entry via an Interaction with RGD-Binding Integrins. Journal of virology 86: 12148–12160. doi: 10.1128/JVI.01133-12 22933271
28. Stewart PL, Nemerow GR, (2007) Cell integrins: commonly used receptors for diverse viral pathogens. Trends Microbiol 15: 500–507. 17988871
29. Connolly SA, Lamb RA, (2006) Paramyxovirus fusion: real-time measurement of parainfluenza virus 5 virus-cell fusion. Virology 355: 203–212. 16916528
30. Pedroso de Lima MC, Ramalho-Santos J, Martins MF, Pato de Carvalho A, Bairos V, et al. (1992) Kinetic modeling of Sendai virus fusion with PC-12 cells. Effect of pH and temperature on fusion and viral inactivation. Eur J Biochem 205: 181–186. 1313363
31. Schowalter RM, Chang A, Robach JG, Buchholz UJ, Dutch RE, (2009) Low-pH triggering of human metapneumovirus fusion: essential residues and importance in entry. Journal of virology 83: 1511–1522. doi: 10.1128/JVI.01381-08 19036821
32. Puri A, Grimaldi S, Blumenthal R, (1992) Role of viral envelope sialic acid in membrane fusion mediated by the vesicular stomatitis virus envelope glycoprotein. Biochemistry 31: 10108–10113. 1327132
33. Clague MJ, Schoch C, Zech L, Blumenthal R, (1990) Gating kinetics of pH-activated membrane fusion of vesicular stomatitis virus with cells: stopped-flow measurements by dequenching of octadecylrhodamine fluorescence. Biochemistry 29: 1303–1308. 2157487
34. Cox RG, Livesay SB, Johnson M, Ohi MD, Williams JV, (2012) The human metapneumovirus fusion protein mediates entry via an interaction with RGD-binding integrins. J Virol 86: 12148–12160. doi: 10.1128/JVI.01133-12 22933271
35. Lanzetti L, (2007) Actin in membrane trafficking. Current opinion in cell biology 19: 453–458. 17616384
36. 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. 8245121
37. Bose S, Zokarkar A, Welch BD, Leser GP, Jardetzky TS, et al. (2012) Fusion activation by a headless parainfluenza virus 5 hemagglutinin-neuraminidase stalk suggests a modular mechanism for triggering. Proceedings of the National Academy of Sciences of the United States of America 109: E2625–2634. 22949640
38. Superti F, Seganti L, Ruggeri FM, Tinari A, Donelli G, et al. (1987) Entry pathway of vesicular stomatitis virus into different host cells. J Gen Virol 68 (Pt 2): 387–399. 3029282
39. Dautry-Varsat A, (1986) Receptor-mediated endocytosis: the intracellular journey of transferrin and its receptor. Biochimie 68: 375–381. 2874839
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. 16740485
41. Huotari J, Helenius A, (2011) Endosome maturation. The EMBO journal 30: 3481–3500. doi: 10.1038/emboj.2011.286 21878991
42. Marshansky V, Futai M, (2008) The V-type H+-ATPase in vesicular trafficking: targeting, regulation and function. Current opinion in cell biology 20: 415–426. doi: 10.1016/j.ceb.2008.03.015 18511251
43. Schowalter RM, Smith SE, Dutch RE, (2006) Characterization of human metapneumovirus F protein-promoted membrane fusion: critical roles for proteolytic processing and low pH. Journal of virology 80: 10931–10941. 16971452
44. Herfst S, Mas V, Ver LS, Wierda RJ, Osterhaus AD, et al. (2008) Low-pH-induced membrane fusion mediated by human metapneumovirus F protein is a rare, strain-dependent phenomenon. Journal of virology 82: 8891–8895. doi: 10.1128/JVI.00472-08 18596097
45. Mas V, Herfst S, Osterhaus AD, Fouchier RA, Melero JA, (2011) Residues of the human metapneumovirus fusion (F) protein critical for its strain-related fusion phenotype: implications for the virus replication cycle. Journal of virology 85: 12650–12661. doi: 10.1128/JVI.05485-11 21937649
46. Cantin C, Holguera J, Ferreira L, Villar E, Munoz-Barroso I, (2007) Newcastle disease virus may enter cells by caveolae-mediated endocytosis. J Gen Virol 88: 559–569. 17251575
47. Sanchez-Felipe L, Villar E, Munoz-Barroso I, (2014) Entry of Newcastle Disease Virus into the host cell: role of acidic pH and endocytosis. Biochim Biophys Acta 1838: 300–309. doi: 10.1016/j.bbamem.2013.08.008 23994097
48. Yoshimura A, Kuroda K, Kawasaki K, Yamashina S, Maeda T, et al. (1982) Infectious cell entry mechanism of influenza virus. J Virol 43: 284–293. 7109028
49. Rossman JS, Leser GP, Lamb RA, (2012) Filamentous influenza virus enters cells via macropinocytosis. J Virol 86: 10950–10960. 22875971
50. Matlin KS, Reggio H, Helenius A, Simons K, (1981) Infectious entry pathway of influenza virus in a canine kidney cell line. J Cell Biol 91: 601–613. 7328111
51. Mercer J, Schelhaas M, Helenius A, (2010) Virus entry by endocytosis. Annu Rev Biochem 79: 803–833. doi: 10.1146/annurev-biochem-060208-104626 20196649
52. Wei Y, Zhang Y, Cai H, Mirza AM, Iorio RM, et al. (2014) Roles of the putative integrin-binding motif of the human metapneumovirus fusion (f) protein in cell-cell fusion, viral infectivity, and pathogenesis. J Virol 88: 4338–4352. doi: 10.1128/JVI.03491-13 24478423
53. Chang A, Masante C, Buchholz UJ, Dutch RE, (2012) Human metapneumovirus (HMPV) binding and infection are mediated by interactions between the HMPV fusion protein and heparan sulfate. J Virol 86: 3230–3243. doi: 10.1128/JVI.06706-11 22238303
54. Hynes RO, (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110: 673–687. 12297042
55. Greber UF, (2002) Signalling in viral entry. Cell Mol Life Sci 59: 608–626. 12022470
56. Stergiou L, Bauer M, Mair W, Bausch-Fluck D, Drayman N, et al. (2013) Integrin-mediated signaling induced by simian virus 40 leads to transient uncoupling of cortical actin and the plasma membrane. PloS one 8: e55799. doi: 10.1371/journal.pone.0055799 23409046
57. Maginnis MS, Mainou BA, Derdowski A, Johnson EM, Zent R, et al. (2008) NPXY motifs in the beta1 integrin cytoplasmic tail are required for functional reovirus entry. Journal of virology 82: 3181–3191. doi: 10.1128/JVI.01612-07 18216114
58. Gustavsson A, Armulik A, Brakebusch C, Fassler R, Johansson S, et al. (2002) Role of the beta1-integrin cytoplasmic tail in mediating invasin-promoted internalization of Yersinia. Journal of cell science 115: 2669–2678. 12077358
59. Agerer F, Lux S, Michel A, Rohde M, Ohlsen K, et al. (2005) Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. Journal of cell science 118: 2189–2200. 15855238
60. Slanina H, Hebling S, Hauck CR, Schubert-Unkmeir A, (2012) Cell invasion by Neisseria meningitidis requires a functional interplay between the focal adhesion kinase, Src and cortactin. PloS one 7: e39613. doi: 10.1371/journal.pone.0039613 22768099
61. Lozach PY, Huotari J, Helenius A, (2011) Late-penetrating viruses. Curr Opin Virol 1: 35–43. doi: 10.1016/j.coviro.2011.05.004 22440565
62. Hurtado-Lorenzo A, Skinner M, El Annan J, Futai M, Sun-Wada GH, et al. (2006) V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nature cell biology 8: 124–136. 16415858
63. Piyaratna R, Tollefson SJ, Williams JV, (2011) Genomic analysis of four human metapneumovirus prototypes. Virus Res 160: 200–205. doi: 10.1016/j.virusres.2011.06.014 21740936
64. Yang CF, Wang CK, Tollefson SJ, Piyaratna R, Lintao LD, et al. (2009) Genetic diversity and evolution of human metapneumovirus fusion protein over twenty years. Virol J 6: 138. doi: 10.1186/1743-422X-6-138 19740442
65. Chang A, Hackett BA, Winter CC, Buchholz UJ, Dutch RE, (2012) Potential electrostatic interactions in multiple regions affect human metapneumovirus F-mediated membrane fusion. J Virol 86: 9843–9853. doi: 10.1128/JVI.00639-12 22761366
66. Chaiwatpongsakorn S, Epand RF, Collins PL, Epand RM, Peeples ME, (2011) Soluble respiratory syncytial virus fusion protein in the fully cleaved, pretriggered state is triggered by exposure to low-molarity buffer. Journal of virology 85: 3968–3977. doi: 10.1128/JVI.01813-10 21307202
67. Scott CC, Gruenberg J, (2010) Ion flux and the function of endosomes and lysosomes: pH is just the start: the flux of ions across endosomal membranes influences endosome function not only through regulation of the luminal pH. Bioessays 33: 103–110.
68. Gerasimenko JV, Tepikin AV, Petersen OH, Gerasimenko OV, (1998) Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr Biol 8: 1335–1338. 9843688
69. Diederich S, Moll M, Klenk HD, Maisner A, (2005) The nipah virus fusion protein is cleaved within the endosomal compartment. J Biol Chem 280: 29899–29903. 15961384
70. Meulendyke KA, Wurth MA, McCann RO, Dutch RE, (2005) Endocytosis plays a critical role in proteolytic processing of the Hendra virus fusion protein. J Virol 79: 12643–12649. 16188966
71. Campbell EM, Nunez R, Hope TJ, (2004) Disruption of the actin cytoskeleton can complement the ability of Nef to enhance human immunodeficiency virus type 1 infectivity. J Virol 78: 5745–5755. 15140972
72. Marsh M, Bron R, (1997) SFV infection in CHO cells: cell-type specific restrictions to productive virus entry at the cell surface. J Cell Sci 110 (Pt 1): 95–103. 9010788
73. Sodeik B, (2000) Mechanisms of viral transport in the cytoplasm. Trends Microbiol 8: 465–472. 11044681
74. Williams JV, Tollefson SJ, Johnson JE, Crowe JE, Jr. (2005) The cotton rat (Sigmodon hispidus) is a permissive small animal model of human metapneumovirus infection, pathogenesis, and protective immunity. J Virol 79: 10944–10951. 16103146
75. Takada A, Robison C, Goto H, Sanchez A, Murti KG, et al. (1997) A system for functional analysis of Ebola virus glycoprotein. Proceedings of the National Academy of Sciences of the United States of America 94: 14764–14769. 9405687
76. Wen X, Krause JC, Leser GP, Cox RG, Lamb RA, et al. (2012) Structure of the human metapneumovirus fusion protein with neutralizing antibody identifies a pneumovirus antigenic site. Nat Struct Mol Biol 19: 461–463. doi: 10.1038/nsmb.2250 22388735