Measles fusion machinery is dysregulated in neuropathogenic variants

mBio

Volumn 6, Issue 1, 2015, Pages

  Jurgens, Eric M ^a   Mathieu, Cyrille ^a,b,e   Palermo, Laura M ^a   Hardie, Diana ^f   Horvat, Branka ^b,c,d   Moscona, Anne ^a   Porotto, Matteo ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^c UNIVERSITÉ LYON 1   (France)

^d UNIVERSITÉ DE LYON   (France)

^e Université de Lyon   (France)

^f NATIONAL HEALTH LABORATORY SERVICE   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

LEUCINE; TRYPTOPHAN; VIRUS FUSION PROTEIN; VIRUS HEMAGGLUTININ; HEMAGGLUTININ; VIRUS RECEPTOR;

AMINO ACID SUBSTITUTION; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; LIPID BILAYER; MEASLES; MEASLES INCLUSION BODY ENCEPHALITIS; MEASLES VIRUS; MUTATIONAL ANALYSIS; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SEQUENCE ANALYSIS; THERMOSTABILITY; VIROGENESIS; VIRUS RECOMBINANT; VIRUS STRAIN; CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM DISEASES; COMPLICATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MISSENSE MUTATION; PHYSIOLOGY; VIROLOGY; VIRUS ENTRY;

MEASLES VIRUS;

CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM DISEASES; HEMAGGLUTININS; HIV INFECTIONS; HUMANS; MEASLES; MEASLES VIRUS; MUTATION, MISSENSE; RECEPTORS, VIRUS; VIRAL FUSION PROTEINS; VIRUS INTERNALIZATION;

EID: 84924155887     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02528-14     Document Type: Article

References (66)

1. Moss WJ, Griffin DE. 2012. Measles. Lancet 379: 153-164. http://dx. doi. org/10. 1016/S0140-6736(10)62352-5.
2. Katz SL, Hinman AR. 2004. Summary and conclusions: measles elimination meeting, 16-17 March 2000. J Infect Dis 189(Suppl 1): S43-S47. http://dx. doi. org/10. 1086/377696.
3. Hutchins SS, Bellini WJ, Coronado V, Jiles R, Wooten K, Deladisma A. 2004. Population immunity to measles in the United States, 1999. J Infect Dis 189(Suppl 1): S91-S97. http://dx. doi. org/10. 1086/377713.
4. Simons E, Ferrari M, Fricks J, Wannemuehler K, Anand A, Burton A, Strebel P. 2012. Assessment of the 2010 global measles mortality reduction goal: results from a model of surveillance data. Lancet 379: 2173-2178. http://dx. doi. org/10. 1016/S0140-6736(12)60522-4.
5. De Vries RD, Mesman AW, Geijtenbeek TB, Duprex WP, de Swart RL. 2012. The pathogenesis of measles. Curr Opin Virol 2: 248-255. http://dx. doi. org/10. 1016/j. coviro. 2012. 03. 005.
6. Ferreira CS, Frenzke M, Leonard VH, Welstead GG, Richardson CD, Cattaneo R. 2010. Measles virus infection of alveolar macrophages and dendritic cells precedes spread to lymphatic organs in transgenic mice expressing human signaling lymphocytic activation molecule (SLAM, CD150). J Virol 84: 3033-3042. http://dx. doi. org/10. 1128/JVI. 01559-09.
7. Avota E, Koethe S, Schneider-Schaulies S. 2013. Membrane dynamics and interactions in measles virus dendritic cell infections. Cell Microbiol 15: 161-169. http://dx. doi. org/10. 1111/cmi. 12025.
8. Lemon K, de Vries RD, Mesman AW, McQuaid S, van Amerongen G, Yüksel S, Ludlow M, Rennick LJ, Kuiken T, Rima BK, Geijtenbeek TB, Osterhaus AD, Duprex WP, de Swart RL. 2011. Early target cells of measles virus after aerosol infection of non-human primates. PLoS Pathog 7: e1001263. http://dx. doi. org/10. 1371/journal. ppat. 1001263.
9. Sawatsky B, Wong XX, Hinkelmann S, Cattaneo R, von Messling V. 2012. Canine distemper virus epithelial cell infection is required for clinical disease but not for immunosuppression. J Virol 86: 3658-3666. http://dx. doi. org/10. 1128/JVI. 06414-11.
10. Mühlebach MD, Mateo M, Sinn PL, Prüfer S, Uhlig KM, Leonard VH, Navaratnarajah CK, Frenzke M, Wong XX, Sawatsky B, Ramachandran S, McCray PB, 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.
11. Griffin DE, Lin WH, Pan CH. 2012. Measles virus, immune control, and persistence. FEMS Microbiol Rev 36: 649-662. http://dx. doi. org/10. 1111/j. 1574-6976. 2012. 00330. x.
12. Lin WH, Kouyos RD, Adams RJ, Grenfell BT, Griffin DE. 2012. Prolonged persistence of measles virus RNA is characteristic of primary infection dynamics. Proc Natl Acad Sci U S A 109: 14989-14994. http://dx. doi. org/10. 1073/pnas. 1211138109.
13. Pampiglione G. 1964. Prodromal phase of measles: some neurophysiological studies. BMJ 2: 1296-1300. http://dx. doi. org/10. 1136/bmj. 2. 5420. 1296.
14. Gibbs FA, Gibbs EL, Carpenter PR, Spies HW. 1959. Electroencephalographic abnormality in "uncomplicated" childhood diseases. JAMA 171: 1050-1055. http://dx. doi. org/10. 1001/jama. 1959. 03010260006002.
15. Norrby E, Kristensson K. 1997. Measles virus in the brain. Brain Res Bull 44: 213-220. http://dx. doi. org/10. 1016/S0361-9230(97)00139-1.
16. Hashiguchi T, Maenaka K, Yanagi Y. 2011. Measles virus hemagglutinin: structural insights into cell entry and measles vaccine. Front Microbiol 2: 247. http://dx. doi. org/10. 3389/fmicb. 2011. 00247.
17. 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.
18. Noyce RS, Bondre DG, Ha MN, Lin LT, Sisson G, Tsao MS, Richardson CD. 2011. Tumor cell marker PVRL4 (nectin 4) is an epithelial cell receptor for measles virus. PLoS Pathog. 7: e1002240. http://dx. doi. org/10. 1371/journal. ppat. 1002240.
19. Harrison SC. 2008. Viral membrane fusion. Nat Struct Mol Biol 15: 690-698. http://dx. doi. org/10. 1038/nsmb. 1456.
20. Chang A, Dutch RE. 2012. Paramyxovirus fusion and entry: multiple paths to a common end. Viruses 4: 613-636. http://dx. doi. org/10. 3390/v4040613.
21. White JM, Delos SE, Brecher M, Schornberg K. 2008. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit Rev Biochem Mol Biol 43: 189-219. http://dx. doi. org/10. 1080/10409230802058320.
22. Sapir A, Avinoam O, Podbilewicz B, Chernomordik LV. 2008. Viral and developmental cell fusion mechanisms: conservation and divergence. Dev Cell 14: 11-21. http://dx. doi. org/10. 1016/j. devcel. 2007. 12. 008.
23. Young VA, Rall GF. 2009. Making it to the synapse: measles virus spread in and among neurons. Curr Top Microbiol Immunol 330: 3-30. http://dx. doi. org/10. 1007/978-3-540-70617-5_1.
24. Watanabe S, Shirogane Y, Suzuki SO, Ikegame S, Koga R, Yanagi Y. 2013. Mutant fusion proteins with enhanced fusion activity promote measles virus spread in human neuronal cells and brains of suckling hamsters. J Virol 87: 2648-2659. http://dx. doi. org/10. 1128/JVI. 02632-12.
25. O'Donnell LA, Rall GF. 2010. Blue moon neurovirology: the merits of studying rare CNS diseases of viral origin. J Neuroimmune Pharmacol 5: 443-455. http://dx. doi. org/10. 1007/s11481-010-9200-4.
26. Makhortova NR, Askovich P, Patterson CE, Gechman LA, Gerard NP, Rall GF. 2007. Neurokinin-1 enables measles virus trans-synaptic spread in neurons. Virology 362: 235-244. http://dx. doi. org/10. 1016/j. virol. 2007. 02. 033.
27. Palmer SG, DeVito I, Jenkins SG, Niewiesk S, Porotto M, Moscona A. 2014. Circulating clinical strains of human parainfluenza virus reveal the viral entry requirements for in vivo infection. J Virol 88: 13495-13502. http://dx. doi. org/10. 1128/JVI. 01965-14.
28. Xu R, Palmer SG, Porotto M, Palermo LM, Niewiesk S, Wilson IA, Moscona A. 2013. Interaction between the hemagglutinin-neuraminidase and fusion glycoproteins of human parainfluenza virus type III regulates viral growth in vivo. mBio 4(5): e00803-00813. http://dx. doi. org/10. 1128/mBio. 00803-13.
29. Hardie DR, Albertyn C, Heckmann JM, Smuts HE. 2013. Molecular characterisation of virus in the brains of patients with measles inclusion body encephalitis (MIBE). Virol J 10: 283. http://dx. doi. org/10. 1186/1743-422X-10-283.
30. Rota J, Lowe L, Rota P, Bellini W, Redd S, Dayan G, van Binnendijk R, Hahné S, Tipples G, Macey J, Espinoza R, Posey D, Plummer A, Bateman J, Gudiño J, Cruz-Ramirez E, Lopez-Martinez I, Anaya-Lopez L, Holy Akwar T, Giffin S, Carrion V, de Filippis AM, Vicari A, Tan C, Wolf B, Wytovich K, Borus P, Mbugua F, Chege P, Kombich J, Akoua-Koffi C, Smit S, Bukenya H, Bwogi J, Baliraine FN, Kremer J, Muller C, Santibanez S. 2006. Identical genotype B3 sequences from measles patients in 4 countries, 2005. Emerg Infect Dis 12: 1779-1781. http://dx. doi. org/10. 3201/eid1211. 060635.
31. Combredet C, Labrousse V, Mollet L, Lorin C, Delebecque F, Hurtrel B, McClure H, Feinberg MB, Brahic M, Tangy F. 2003. A molecularly cloned Schwarz strain of measles virus vaccine induces strong immune responses in macaques and transgenic mice. J Virol 77: 11546-11554. http://dx. doi. org/10. 1128/JVI. 77. 21. 11546-11554. 2003.
32. Takeda M, Takeuchi K, Miyajima N, Kobune F, Ami Y, Nagata N, Suzaki Y, Nagai Y, Tashiro M. 2000. Recovery of pathogenic measles virus from cloned cDNA. J Virol 74: 6643-6647. http://dx. doi. org/10. 1128/JVI. 74. 14. 6643-6647. 2000.
33. Talekar A, DeVito I, Salah Z, Palmer SG, Chattopadhyay A, Rose JK, Xu R, Wilson IA, Moscona A, Porotto M. 2013. Identification of a region in the stalk domain of the Nipah virus receptor binding protein that is critical for fusion activation. J Virol 87: 10980-10996. http://dx. doi. org/10. 1128/JVI. 01646-13.
34. Talekar A, Moscona A, Porotto M. 2013. Measles virus fusion machinery activated by sialic acid binding globular domain. J Virol 87: 13619-13627. http://dx. doi. org/10. 1128/JVI. 02256-13.
35. 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.
36. Mateo M, Navaratnarajah CK, Syed S, Cattaneo R. 2013. The measles virus hemagglutinin beta-propeller head beta4-beta5 hydrophobic groove governs functional interactions with nectin-4 and CD46 but not those with the signaling lymphocytic activation molecule. J Virol 87: 9208-9216. http://dx. doi. org/10. 1128/JVI. 01210-13.
37. Parks CL, Lerch RA, Walpita P, Wang HP, Sidhu MS, Udem SA. 2001. Analysis of the noncoding regions of measles virus strains in the Edmonston vaccine lineage. J Virol 75: 921-933. http://dx. doi. org/10. 1128/JVI. 75. 2. 921-933. 2001.
38. Otani S, Ayata M, Takeuchi K, Takeda M, Shintaku H, Ogura H. 2014. Biased hypermutation occurred frequently in a gene inserted into the IC323 recombinant measles virus during its persistence in the brains of nude mice. Virology 462-463: 91-97. http://dx. doi. org/10. 1016/j. virol. 2014. 05. 035.
39. Plemper RK, Doyle J, Sun A, Prussia A, Cheng LT, Rota PA, Liotta DC, Snyder JP, Compans RW. 2005. Design of a small-molecule entry inhibitor with activity against primary measles virus strains. Antimicrob Agents Chemother 49: 3755-3761. http://dx. doi. org/10. 1128/AAC. 49. 9. 3755-3761. 2005.
40. Watanabe S, Shirogane Y, Suzuki SO, Ikegame S, Koga R, Yanagi Y. 2013. Mutant fusion proteins with enhanced fusion activity promote measles virus spread in human neuronal cells and brains of suckling hamsters. J Virol 87: 2648-2659. http://dx. doi. org/10. 1128/JVI. 02632-12.
41. Moscona A, Peluso RW. 1993. Relative affinity of the human parainfluenza virus type 3 hemagglutinin-neuraminidase for sialic acid correlates with virus-induced fusion activity. J Virol 67: 6463-6468.
42. Porotto M, Salah Z, Devito I, Talekar A, Palmer SG, Xu R, Wilson IA, Moscona A. 2012. The second receptor binding site of the globular head of the Newcastle disease virus (NDV) hemagglutinin-neuraminidase activates the stalk of multiple paramyxovirus receptor binding proteins to trigger fusion. J Virol 86: 5730-5741. http://dx. doi. org/10. 1128/JVI. 06793-11.
43. Porotto M, Salah ZW, Gui L, Devito I, Jurgens EM, Lu H, Yokoyama CC, Palermo LM, Lee KK, Moscona A. 2012. Regulation of paramyxovirus fusion activation: the hemagglutinin-neuraminidase protein stabilizes the fusion protein in a pretriggered state. J Virol 86: 12838-12848. http://dx. doi. org/10. 1128/JVI. 01965-12.
44. Greengard O, Poltoratskaia N, Leikina E, Zimmerberg J, Moscona A. 2000. The anti-influenza virus agent 4-GU-DANA (zanamivir) inhibits cell fusion mediated by human parainfluenza virus and influenza virus HA. J Virol 74: 11108-11114. http://dx. doi. org/10. 1128/JVI. 74. 23. 11108-11114. 2000.
45. 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.
46. Porotto M, Palmer SG, Palermo LM, Moscona A. 2012. Mechanism of fusion triggering by human parainfluenza virus type III: communication between viral glycoproteins during entry. J Biol Chem 287: 778-793. http://dx. doi. org/10. 1074/jbc. M111. 298059.
47. Ader N, Brindley M, Avila M, Örvell 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.
48. Welsch JC, Talekar A, Mathieu C, Pessi A, Moscona A, Horvat B, Porotto M. 2013. Fatal measles virus infection prevented by brainpenetrant fusion inhibitors. J Virol 87: 13785-13794. http://dx. doi. org/10. 1128/JVI. 02436-13.
49. Rima BK, Duprex WP. 2005. Molecular mechanisms of measles virus persistence. Virus Res 111: 132-147. http://dx. doi. org/10. 1016/j. virusres. 2005. 04. 005.
50. Cattaneo R, Schmid A, Billeter MA, Sheppard RD, Udem SA. 1988. Multiple viral mutations rather than host factors cause defective measles virus gene expression in a subacute sclerosing panencephalitis cell line. J Virol 62: 1388-1397.
51. Griffin DE. 2014. Measles virus and the nervous system. Handb Clin Neurol 123: 577-590. http://dx. doi. org/10. 1016/B978-0-444-53488-0. 00027-4.
52. Fisher DL, Defres S, Solomon T. May 2014. Measles-induced encephalitis. QJM http://dx. doi. org/10. 1093/qjmed/hcu113.
53. Bale JF, Jr. 2014. Measles, mumps, rubella, and human parvovirus B19 infections and neurologic disease. Hand Clin Neurol 121: 1345-1353. http://dx. doi. org/10. 1016/B978-0-7020-4088-7. 00091-2.
54. Albertyn C, van der Plas H, Hardie D, Candy S, Tomoka T, Leepan EB, Heckmann JM. 2011. Silent casualties from the measles outbreak in South Africa. S Afr Med J 101: 313-314, 316-317.
55. Porotto M, Devito I, Palmer SG, Jurgens EM, Yee JL, Yokoyama CC, Pessi A, Moscona A. 2011. Spring-loaded model revisited: paramyxovirus fusion requires engagement of a receptor binding protein beyond initial triggering of the fusion protein. J Virol 85: 12867-12880. http://dx. doi. org/10. 1128/JVI. 05873-11.
56. Plattet P, Plemper RK. 2013. Envelope protein dynamics in paramyxovirus entry. mBio 4(4): e00413-130. http://dx. doi. org/10. 1128/mBio. 00413-13.
57. 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.
58. Kweder H, Ainouze M, Cosby SL, Muller CP, Lévy C, Verhoeyen E, Cosset FL, Manet E, Buckland R. 2014. Mutations in the H, F, or M proteins Can facilitate resistance of measles virus to neutralizing human anti-MV Sera. Adv Virol 2014: 205617. http://dx. doi. org/10. 1155/2014/205617.
59. Leonard VH, Sinn PL, Hodge G, Miest T, Devaux P, Oezguen N, Braun W, McCray PB, Jr, McChesney MB, Cattaneo R. 2008. Measles virus blind to its epithelial cell receptor remains virulent in rhesus monkeys but cannot cross the airway epithelium and is not shed. J Clin Invest 118: 2448-2458. http://dx. doi. org/10. 1172/JCI35454.
60. Palermo LM, Porotto M, Yokoyama CC, Palmer SG, Mungall BA, Greengard O, Niewiesk S, Moscona A. 2009. Human parainfluenza virus infection of the airway epithelium: the viral hemagglutininneuraminidase regulates fusion protein activation and modulates infectivity. J Virol 83: 6900-6908. http://dx. doi. org/10. 1128/JVI. 00475-09.
61. Porotto M, Fornabaio M, Kellogg GE, Moscona A. 2007. A second receptor binding site on human parainfluenza virus type 3 hemagglutininneuraminidase contributes to activation of the fusion mechanism. J Virol 81: 3216-3228. http://dx. doi. org/10. 1128/JVI. 02617-06.
62. Moosmann P, Rusconi S. 1996. Alpha complementation of LacZ in mammalian cells. Nucleic Acids Res 24: 1171-1172. http://dx. doi. org/10. 1093/nar/24. 6. 1171.
63. Porotto M, Rockx B, Yokoyama CC, Talekar A, DeVito I, Palermo LM, Liu J, Cortese R, Lu M, Feldmann H, Pessi A, Moscona A. 2010. Inhibition of Nipah virus infection in vivo: targeting an early stage of paramyxovirus fusion activation during viral entry. PLoS Pathog. 6: http://dx. doi. org/10. 1371/journal. ppat. 1001168.
64. Hashimoto K, Ono N, Tatsuo H, Minagawa H, Takeda M, Takeuchi K, Yanagi Y. 2002. SLAM (CD150)-independent measles virus entry as revealed by recombinant virus expressing green fluorescent protein. J Virol 76: 6743-6749. http://dx. doi. org/10. 1128/JVI. 76. 13. 6743-6749. 2002.
65. Radecke F, Spielhofer P, Schneider H, Kaelin K, Huber M, Dötsch C, Christiansen G, Billeter MA. 1995. Rescue of measles viruses from cloned DNA. EMBO J 14: 5773-5784.
66. Mathieu C, Huey D, Jurgens E, Welsch JC, DeVito I, Talekar A, Horvat B, Niewiesk S, Moscona A, Porotto M. 2015. Prevention of measles Infection by intranasal delivery of fusion inhibitory peptides. J Virol 89: 1143-1155. http://dx. doi. org/10. 1128/JVI. 02417-14.