Canine distemper virus envelope protein interactions modulated by hydrophobic residues in the fusion protein globular head

Journal of Virology

Volumn 89, Issue 2, 2015, Pages 1445-1451

  Avila, Mislay ^a   Khosravi, Mojtaba ^a   Alves, Lisa ^a   Ader Ebert, Nadine ^a   Bringolf, Fanny ^a   Zurbriggen, Andreas ^a   Plemper, Richard K ^b   Plattet, Philippe ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS ENVELOPE PROTEIN F; VIRUS ENVELOPE PROTEIN F ENVELOPE PROTEIN H FUSION PROTEIN; VIRUS ENVELOPE PROTEIN H; VIRUS FUSION PROTEIN; PROTEIN BINDING;

AMINO ACID SUBSTITUTION; ARTICLE; CANINE DISTEMPER MORBILLIVIRUS; CONFORMATIONAL TRANSITION; HYDROPHOBICITY; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RESIDUE ANALYSIS; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS CELL TRANSFORMATION; VIRUS ENTRY; ANIMAL; CANINE DISTEMPER VIRUS; CHEMICAL STRUCTURE; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

CANINE DISTEMPER VIRUS; MORBILLIVIRUS;

ANIMALS; DISTEMPER VIRUS, CANINE; DNA MUTATIONAL ANALYSIS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EID: 84920811285     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01828-14     Document Type: Article

References (41)

1. Chen SY, Anderson S, Kutty PK, Lugo F, McDonald M, Rota PA, Ortega-Sanchez IR, Komatsu K, Armstrong GL, Sunenshine R, Seward JF. 2011. Health care-associated measles outbreak in the United States after an importation: challenges and economic impact. J Infect Dis 203: 1517-1525. http://dx.doi.org/10.1093/infdis/jir115.
2. Sakai K, Nagata N, Ami Y, Seki F, Suzaki Y, Iwata-Yoshikawa N, Suzuki T, Fukushi S, Mizutani T, Yoshikawa T, Otsuki N, Kurane I, Komase K, Yamaguchi R, Hasegawa H, Saijo M, Takeda M, Morikawa S. 2013. Lethal canine distemper virus outbreak in cynomolgus monkeys in Japan in 2008. J Virol 87:1105-1114. http://dx.doi.org/10.1128/JVI.02419-12.
3. Roelke-Parker ME, Munson L, Packer C, Kock R, Cleaveland S, Carpenter M, O'Brien SJ, Pospischil A, Hofmann-Lehmann R, Lutz H, Mwamengele GL, Mgasa MN, Machange GA, Summers BA, Appel MJ. 1996. A canine distemper virus epidemic in Serengeti lions (Panthera leo). Nature 379:441-445. http://dx.doi.org/10.1038/379441a0.
4. Domingo M, Ferrer L, Pumarola M, Marco A, Plana J, Kennedy S, McAliskey M, Rima BK. 1990. Morbillivirus in dolphins. Nature 348:21. http://dx.doi.org/10.1038/348021a0.
5. Lamb RA, Parks GD. 2007. Paramyxoviridae: the viruses and their replication, p 1449-1496. In Fields B, Knipe DM, Howley PM (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
6. Tatsuo H, Ono N, Tanaka K, Yanagi Y. 2000. SLAM (CDw150) is a cellular receptor for measles virus. Nature 406:893-897. http://dx.doi.org/10.1038/35022579.
7. Muhlebach MD, Mateo M, Sinn PL, Prufer S, Uhlig KM, Leonard VH, Navaratnarajah CK, Frenzke M, Wong XX, Sawatsky B, Ramachandran S, McCray PB, Jr, Cichutek K, von Messling V, Lopez M, Cattaneo R. 2011. Adherens junction protein nectin-4 is the epithelial receptor for measles virus. Nature 480:530-533. http://dx.doi.org/10.1038/nature10639.
8. Vongpunsawad S, Oezgun N, Braun W, Cattaneo R. 2004. Selectively receptor-blind measles viruses: identification of residues necessary for SLAM-or CD46-induced fusion and their localization on a new hemagglutinin structural model. J Virol 78:302-313. http://dx.doi.org/10.1128/JVI.78.1.302-313.2004.
9. von Messling V, Oezguen N, Zheng Q, Vongpunsawad S, Braun W, Cattaneo R. 2005. Nearby clusters of hemagglutinin residues sustain SLAM-dependent canine distemper virus entry in peripheral blood mononuclear cells. J Virol 79:5857-5862. http://dx.doi.org/10.1128/JVI.79.9.5857-5862.2005.
10. Langedijk JP, Janda J, Origgi FC, Orvell C, Vandevelde M, Zurbriggen A, Plattet P. 2011. Canine distemper virus infects canine keratinocytes and immune cells by using overlapping and distinct regions located on one side of the attachment protein. J Virol 85:11242-11254. http://dx.doi.org/10.1128/JVI.05340-11.
11. Brindley MA, Takeda M, Plattet P, Plemper RK. 2012. Triggering the measles virus membrane fusion machinery. Proc Natl Acad Sci USA 109:E3018-E3027. http://dx.doi.org/10.1073/pnas.1210925109.
12. Ader N, Brindley MA, Avila M, Origgi FC, Langedijk JP, Orvell C, Vandevelde M, Zurbriggen A, Plemper RK, Plattet P. 2012. Structural rearrangements of the central region of the morbillivirus attachment protein stalk domain trigger F protein refolding for membrane fusion. J Biol Chem 287:16324-16334. http://dx.doi.org/10.1074/jbc.M112.342493.
13. Navaratnarajah CK, Negi S, Braun W, Cattaneo R. 2012. Membrane fusion triggering: three modules with different structure and function in the upper half of the measles virus attachment protein stalk. J Biol Chem 287:38543-38551. http://dx.doi.org/10.1074/jbc.M112.410563.
14. Ader N, Brindley M, Avila M, Orvell C, Horvat B, Hiltensperger G, Schneider-Schaulies J, Vandevelde M, Zurbriggen A, Plemper RK, Plattet P. 2013. Mechanism for active membrane fusion triggering by morbillivirus attachment protein. J Virol 87:314-326. http://dx.doi.org/10.1128/JVI.01826-12.
15. Avila M, Alves L, Khosravi M, Ader-Ebert N, Origgi F, Schneider-Schaulies J, Zurbriggen A, Plemper RK, Plattet P. 2014. Molecular determinants defining the triggering range of prefusion F complexes of canine distemper virus. J Virol 88:2951-2966. http://dx.doi.org/10.1128/JVI.03123-13.
16. Russell CJ, Jardetzky TS, Lamb RA. 2001. Membrane fusion machines of paramyxoviruses: capture of intermediates of fusion. EMBO J 20:4024-4034. http://dx.doi.org/10.1093/emboj/20.15.4024.
17. Plemper RK, Hammond AL, Cattaneo R. 2001. Measles virus envelope glycoproteins hetero-oligomerize in the endoplasmic reticulum. J Biol Chem 276:44239-44246. http://dx.doi.org/10.1074/jbc.M105967200.
18. Lee JK, Prussia A, Paal T, White LK, Snyder JP, Plemper RK. 2008. Functional interaction between paramyxovirus fusion and attachment proteins. J Biol Chem 283:16561-16572. http://dx.doi.org/10.1074/jbc.M801018200.
19. Paal T, Brindley MA, St Clair C, Prussia A, Gaus D, Krumm SA, Snyder JP, Plemper RK. 2009. Probing the spatial organization of measles virus fusion complexes. J Virol 83:10480-10493. http://dx.doi.org/10.1128/JVI.01195-09.
20. Apte-Sengupta S, Negi S, Leonard VH, Oezguen N, Navaratnarajah CK, Braun W, Cattaneo R. 2012. Base of the measles virus fusion trimer head receives the signal that triggers membrane fusion. J Biol Chem 287:33026-33035. http://dx.doi.org/10.1074/jbc.M112.373308.
21. Bose S, Heath CM, Shah PA, Alayyoubi M, Jardetzky TS, Lamb RA. 2013. Mutations in the parainfluenza virus 5 fusion protein reveal domains important for fusion triggering and metastability. J Virol 87:13520-13531. http://dx.doi.org/10.1128/JVI.02123-13.
22. Plattet P, Langedijk JP, Zipperle L, Vandevelde M, Orvell C, Zurbriggen A. 2009. Conserved leucine residue in the head region of morbillivirus fusion protein regulates the large conformational change during fusion activity. Biochemistry 48:9112-9121. http://dx.doi.org/10.1021/bi9008566.
23. Plattet P, Plemper RK. 2013. Envelope protein dynamics in paramyxovirus entry. mBio 4(4):e00413-13. http://dx.doi.org/10.1128/mBio.00413-13.
24. Jardetzky TS, Lamb RA. 2014. Activation of paramyxovirus membrane fusion and virus entry. Curr Opin Virol 5:24-33. http://dx.doi.org/10.1016/j.coviro.2014.01.005.
25. Mateo M, Navaratnarajah CK, Cattaneo R. 2014. Structural basis of efficient contagion: measles variations on a theme by parainfluenza viruses. Curr Opin Virol 5:16-23. http://dx.doi.org/10.1016/j.coviro.2014.01.004.
26. Palmer SG, Porotto M, Palermo LM, Cunha LF, Greengard O, Moscona A. 2012. Adaptation of human parainfluenza virus to airway epithelium reveals fusion properties required for growth in host tissue. mBio 3(3): e00137-12. http://dx.doi.org/10.1128/mBio.00137-12.
27. Aguilar HC, Matreyek KA, Filone CM, Hashimi ST, Levroney EL, Negrete OA, Bertolotti-Ciarlet A, Choi DY, McHardy I, Fulcher JA, Su SV, Wolf MC, Kohatsu L, Baum LG, Lee B. 2006. N-glycans on Nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry. J Virol 80:4878-4889. http://dx.doi.org/10.1128/JVI.80.10.4878-4889.2006.
28. Bishop KA, Hickey AC, Khetawat D, Patch JR, Bossart KN, Zhu Z, Wang LF, Dimitrov DS, Broder CC. 2008. Residues in the stalk domain of the Hendra virus G glycoprotein modulate conformational changes associated with receptor binding. J Virol 82:11398-11409. http://dx.doi.org/10.1128/JVI.02654-07.
29. Plemper RK, Hammond AL, Gerlier D, Fielding AK, Cattaneo R. 2002. Strength of envelope protein interaction modulates cytopathicity of measles virus. J Virol 76:5051-5061. http://dx.doi.org/10.1128/JVI.76.10.5051-5061.2002.
30. Melanson VR, Iorio RM. 2004. Amino acid substitutions in the F-specific domain in the stalk of the Newcastle disease virus HN protein modulate fusion and interfere with its interaction with the F protein. J Virol 78: 13053-13061. http://dx.doi.org/10.1128/JVI.78.23.13053-13061.2004.
31. Iorio RM, Melanson VR, Mahon PJ. 2009. Glycoprotein interactions in paramyxovirus fusion. Future Virol 4:335-351. http://dx.doi.org/10.2217/fvl.09.17.
32. Iorio RM, Mahon PJ. 2008. Paramyxoviruses: different receptors-different mechanisms of fusion. Trends Microbiol 16:135-137. http://dx.doi.org/10.1016/j.tim.2008.01.006.
33. Hashiguchi T, Ose T, Kubota M, Maita N, Kamishikiryo J, Maenaka K, Yanagi Y. 2011. Structure of the measles virus hemagglutinin bound to its cellular receptor SLAM. Nat Struct Mol Biol 18:135-141. http://dx.doi.org/10.1038/nsmb.1969.
34. Welch BD, Yuan P, Bose S, Kors CA, Lamb RA, Jardetzky TS. 2013. Structure of the parainfluenza virus 5 (PIV5) hemagglutininneuraminidase (HN) ectodomain. PLoS Pathog 9:e1003534. http://dx.doi.org/10.1371/journal.ppat.1003534.
35. Yuan P, Swanson KA, Leser GP, Paterson RG, Lamb RA, Jardetzky TS. 2011. Structure of the Newcastle disease virus hemagglutininneuraminidase (HN) ectodomain reveals a four-helix bundle stalk. Proc Natl Acad Sci USA 108:14920-14925. http://dx.doi.org/10.1073/pnas.1111691108.
36. Bose S, Song AS, Jardetzky TS, Lamb RA. 2014. Fusion activation through attachment protein stalk domains indicates a conserved core mechanism of paramyxovirus entry into cells. J Virol 88:3925-3941. http://dx.doi.org/10.1128/JVI.03741-13.
37. Liu Q, Stone JA, Bradel-Tretheway B, Dabundo J, Avides Montano JA, Santos-Montanez J, Biering SB, Nicola AV, Iorio RM, Lu X, Aguilar HC. 2013. Unraveling a three-step spatiotemporal mechanism of triggering of receptor-induced Nipah virus fusion and cell entry. PLoS Pathog 9:e1003770. http://dx.doi.org/10.1371/journal.ppat.1003770.
38. Apte-Sengupta S, Navaratnarajah CK, Cattaneo R. 2013. Hydrophobic and charged residues in the central segment of the measles virus hemagglutinin stalk mediate transmission of the fusion-triggering signal. J Virol 87:10401-10404. http://dx.doi.org/10.1128/JVI.01547-13.
39. Brindley MA, Suter R, Schestak I, Kiss G, Wright ER, Plemper RK. 2013. A stabilized headless measles virus attachment protein stalk efficiently triggers membrane fusion. J Virol 87:11693-11703. http://dx.doi.org/10.1128/JVI.01945-13.
40. Orvell C, Sheshberadaran H, Norrby E. 1985. Preparation and characterization of monoclonal antibodies directed against four structural components of canine distemper virus. J Gen Virol 66:443-456. http://dx.doi.org/10.1099/0022-1317-66-3-443.
41. Cherpillod P, Beck K, Zurbriggen A, Wittek R. 1999. Sequence analysis and expression of the attachment and fusion proteins of canine distemper virus wild-type strain A75/17. J Virol 73:2263-2269.