Detailed morphological characterisation of Hendra virus infection of different cell types using super-resolution and conventional imaging

Virology Journal

Volumn 11, Issue 1, 2014, Pages

  Monaghan, Paul ^a   Green, Diane ^a   Pallister, Jackie ^a   Klein, Reuben ^a   White, John ^a   Williams, Catherine ^a   McMillan, Paul ^b,c,d   Tilley, Leann ^b,c,d   Lampe, Marko ^e,f,g   Hawes, Pippa ^h   Wang, Lin Fa ^a,i  

^a CSIRO   (Australia)

^b Department of Biochemistry and Molecular Biology ^*  (Australia)

^c LA TROBE UNIVERSITY   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e Leica Microsystems GmbH   (Germany)

^f EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^g UNIVERSITY OF HEIDELBERG   (Germany)

^h INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

ⁱ DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

Cell lines; Confocal microscopy; G protein; Hendra virus; M protein; Paramyxovirus; Super resolution microscopy

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; M PROTEIN;

A549 CELL LINE; ANIMAL CELL; ARTICLE; BAT; CELL CULTURE; CELL LABELING; CELL LINE; CELL NUCLEUS; CELL SURFACE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOTHELIUM CELL; HELA CELL LINE; HENDRA VIRUS; HENDRA VIRUS INFECTION; IN VITRO STUDY; MDBK CELL LINE; MICROSCOPY; NONHUMAN; OPTICAL RESOLUTION; PARAMYXOVIRIDAE; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SUPER RESOLUTION MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; VERO CELL LINE; VIRION; VIRUS ASSEMBLY; VIRUS ENVELOPE; VIRUS EXAMINATION; VIRUS LIKE AGENT; VIRUS MORPHOLOGY; ANIMAL; FLUORESCENCE IMAGING; HUMAN; PHYSIOLOGY; ULTRASTRUCTURE;

BOVINAE; HENDRA VIRUS; PARAMYXOVIRIDAE; SUS;

ANIMALS; CELL LINE; HENDRA VIRUS; HUMANS; MICROSCOPY; OPTICAL IMAGING; VIRUS ASSEMBLY;

EID: 84936855081     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/s12985-014-0200-5     Document Type: Article

References (42)

1. Smith I, Broos A, De Jong C, Zeddeman A, Smith C, Smith G, Moore F, Barr J, Crameri G, Marsh GA, Tachedjian M, Yu M, Kung YH, Wang LF, Field H: Identifying Hendra virus diversity in Pteropid bats. PLoS One 2011, 6:1-8.
2. Pallister J, Middleton D, Broder CC, Wang L-F: Henipavirus vaccine development. Journal of Bioterrorism and Biodefense 2011, S1:005.
3. Broder C, Geisbert T, Xu K, Nikolov D, Wang L-F, Middleton D, Pallister J, Bossart K: Immunization Strategies Against Henipaviruses. In Henipavirus. 359th edition. Edited by Lee B, Rota PA. Berlin Heidelberg: Springer; 2012:197-223. Current Topics in Microbiology and Immunology.
4. Lyles DS: Assembly and Budding of Negative-Strand RNA Viruses. In Advances in Virus Research. 85th edition. Edited by Maramorosch K, Murphy FA. 2013:57-90. Advances in Virus Research.
5. Harrison MS, Sakaguchi T, Schmitt AP: Paramyxovirus assembly and budding: building particles that transmit infections. International Journal of Biochemistry & Cell Biology 2010, 42:1416-1429.
6. Wang LF, Michalski WP, Yu M, Pritchard LI, Crameri G, Shiell B, Eaton BT: A novel P/V/C gene in a new member of the Paramyxoviridae family, which causes lethal infection in humans, horses, and other animals. J Virol 1998, 72:1482-1490.
7. Lo MK, Harcourt BH, Mungall BA, Tamin A, Peeples ME, Bellini WJ, Rota PA: Determination of the henipavirus phosphoprotein gene mRNA editing frequencies and detection of the C, V and W proteins of Nipah virus in virus-infected cells. J Gen Virol 2009, 90:398-404.
8. Sleeman K, Bankamp B, Hummel KB, Lo MK, Bellini WJ, Rota PA: The C, V and W proteins of Nipah virus inhibit minigenome replication. J Gen Virol 2008, 89:1300-1308.
9. Bonaparte MI, Dimitrov AS, Bossart KN, Crameri G, Mungal BA, Bishop KA, Choudhry V, Dimitrov DS, Wang LF, Eaton BT, Broder CC: Ephrin-B2 ligand is a functional receptor for Hendra virus and Nipah virus. Proc Natl Acad Sci U S A 2005, 102:10652-10657.
10. Negrete OA, Levroney EL, Aguilar HC, Bertolotti-Ciarlet A, Nazarian R, Tajyar S, Lee B: EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus. Nature 2005, 436:401-405.
11. Bishop KA, Stantchev TS, Hickey AC, Khetawat D, Bossart KN, Krasnoperov V, Gill P, Feng YR, Wang L, Eaton BT, Wang LF, Broder CC: Identification of Hendra virus G glycoprotein residues that are critical for receptor binding. J Virol 2007, 81:5893-5901.
12. Wang B, Zhang N, Qian KX, Geng JG: Conserved molecular players for axon guidance and angiogenesis. Curr Protein Pept Sci 2005, 6:473-478.
13. Zhang J, Hughes S: Role of the ephrin and Eph receptor tyrosine kinase families in angiogenesis and development of the cardiovascular system. J Pathol 2006, 208:453-461.
14. Adams RH, Wilkinson GA, Weiss C, Diella F, Gale NW, Deutsch U, Risau W, Klein R: Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev 1999, 13:295-306.
15. Hickey AC, Broder CC: The mechanism of henipavirus fusion: examining the relationships beween the attachment and fusion glycoproteins. Virol Sin 2009, 24:110-120.
16. Diederich S, Sauerhering L, Weis M, Altmeppen H, Schaschke N, Reinheckel T, Erbar S, Maisner A: Activation of the Nipah virus fusion protein in MDCK cells is mediated by cathepsin B within the endosome-recycling compartment. J Virol 2012, 86:3736-3745.
17. Popa A, Carter JR, Smith SE, Hellman L, Fried MG, Dutch RE: Residues in the hendra virus fusion protein transmembrane domain are critical for endocytic recycling. J Virol 2012, 86:3014-3026.
18. Ciancanelli MJ, Basler CF: Mutation of YMYL in the Nipah virus matrix protein abrogates budding and alters subcellular localization. J Virol 2006, 80:12070-12078.
19. Subramanian SK, Tey BT, Hamid M, Tan WS: Production of the matrix protein of Nipah virus in Escherichia coli: Virus-like particles and possible application for diagnosis. J Virol Methods 2009, 162:179-183.
20. Patch JR, Han Z, McCarthy SE, Yan L, Wang LF, Harty RN, Broder CC: The YPLGVG sequence of the Nipah virus matrix protein is required for budding. Virol J 2008, 5:137.
21. Ghildyal R, Ho A, Dias M, Soegiyono L, Bardin PG, Tran KC, Teng MN, Jans DA: The respiratory syncytial virus matrix protein possesses a Crm1-mediated nuclear export mechanism. J Virol 2009, 83:5353-5362.
22. Ghildyal R, Baulch-Brown C, Mills J, Meanger J: The matrix protein of human respiratory syncytial virus localises to the nucleus of infected cells and inhibits transcription. Arch Virol 2003, 148:1419-1429.
23. Yoshida T, Nagai Y, Yoshii S, Maeno K, Matsumoto T, Hoshino M: Membrane (M) protein of HJV (Sendai virus) - its role in virus assembly. Virology 1976, 71:143-161.
24. Peeples ME, Can W, Gupta KC, Coleman N: Nuclear entry and nucleolar localisation of the Newcastle-Disease Virus (NDV) matrix protein occur early in infection and do not require othe NDV proteins. J Virol 1992, 66:3263-3269.
25. Wang YE, Park A, Lake M, Pentecost M, Torres B, Yun TE, Wolf MC, Holbrook MR, Freiberg AN, Lee B: Ubiquitin-regulated nuclear-cytoplasmic trafficking of the nipah virus matrix protein is important for viral budding. Plos Pathogens 2010, 6(11):e1001186. doi:10.1371/journal.ppat.1001186.
26. Hooper P, Zaki S, Daniels P, Middleton D: Comparative pathology of the diseases caused by Hendra and Nipah viruses. Microbes Infect 2001, 3:315-322.
27. Aljofan M, Saubern S, Meyer AG, Marsh G, Meers J, Mungall BA: Characteristics of Nipah virus and Hendra virus replication in different cell lines and their suitability for antiviral screening. Virus Res 2009, 142:92-99.
28. Crameri G, Todd S, Grimley S, McEachern JA, Marsh GA, Smith C, Tachedjian M, De Jong C, Virtue ER, Yu M, Bulach D, Liu JP, Michalski WP, Middleton D, Field HE, Wang LF: Establishment, immortalisation and characterisation of pteropid bat cell lines. PLoS One 2009, 4:e8266.
29. Loney C, Mottet-Osman G, Roux L, Bhella D: Paramyxovirus ultrastructure and genome packaging: cryo-electron tomography of Sendai virus. J Virol 2009, 83:8191-8197.
30. Liljeroos L, Huiskonen JT, Ora A, Susi P, Butcher SJ: Electron cryotomography of measles virus reveals how matrix protein coats the ribonucleocapsid within intact virions. Proc Natl Acad Sci U S A 2011, 108:18085-18090.
31. Emeny JM, Morgan MJ: Regulation of the interferon system - evidence that Vero cells have a genetic defect in interferon production. J Gen Virol 1979, 43:247-252.
32. Erbar S, Diederich S, Maisner A: Selective receptor expression restricts Nipah virus infection of endothelial cells. Virol J 2008, 5:Article 142.
33. Horsington J, Turnbull L, Whitchurch CB, Newsome TP: Sub-viral imaging of vaccinia virus using super-resolution microscopy. J Virol Methods 2012, 186:132-136.
34. Folling J, Bossi M, Bock H, Medda R, Wurm CA, Hein B, Jakobs S, Eggeling C, Hell SW: Fluorescence nanoscopy by ground-state depletion and single-molecule return. Nat Methods 2008, 5:943-945.
35. Heilemann M, van de Linde S, Schuttpelz M, Kasper R, Seefeldt B, Mukherjee A, Tinnefeld P, Sauer M: Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angewandte Chemie-International Edition 2008, 47:6172-6176.
36. Gustafsson MGL, Shao L, Carlton PM, Wang CJR, Golubovskaya IN, Cande WZ, Agard DA, Sedat JW: Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys J 2008, 94:4957-4970.
37. Halpin K, Young PL, Field HE, Mackenzie JS: Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. J Gen Virol 2000, 81:1927-1932.
38. Pallister J, Middleton D, Wang LF, Klein R, Haining J, Robinson R, Yamada M, White J, Payne J, Feng YR, Chan YP, Broder CC: A recombinant Hendra virus G glycoprotein-based subunit vaccine protects ferrets from lethal Hendra virus challenge. Vaccine 2011, 29:5623-5630.
39. Marsh GA, Haining J, Hancock TJ, Robinson R, Foord AJ, Barr JA, Riddell S, Heine HG, White JR, Crameri G, Field HE, Wang LF, Middleton D: Experimental infection of horses with Hendra virus/Australia/horse/2008/Redlands. Emerg Infect Dis 2011, 17:2232-2238.
40. Monaghan P, Cook H, Jackson T, Ryan M, Wileman T: The ultrastructure of the developing replication site in foot-and-mouth disease virus-infected BHK-38 cells. J Gen Virol 2004, 85:933-946.
41. Zhu Z, Bossart KN, Bishop KA, Crameri G, Dimitrov AS, McEachern JA, Feng Y, Middleton D, Wang LF, Broder CC, Dimitrov DS: Exceptionally potent cross-reactive neutralization of Nipah and Hendra viruses by a human monoclonal antibody. J Infect Dis 2008, 197:846-853.
42. White JR, Boyd V, Crameri GS, Duch CJ, van Laar RK, Wang LF, Eaton BT: Location of, immunogenicity of and relationships between neutralization epitopes on the attachment protein (G) of Hendra virus. J Gen Virol 2005, 86:2839-2848.