Paramyxovirus Entry

  • Katharine N. Bossart
  • Deborah L. Fusco
  • Christopher C. Broder
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 790)

Abstract

The family Paramyxoviridae consists of a group of large, enveloped, negative-sense, single-stranded RNA viruses and contains many important human and animal pathogens. Molecular and biochemical characterization over the past decade has revealed an extraordinary breadth of biological diversity among this family of viruses. Like all enveloped viruses, paramyxoviruses must fuse their membrane with that of a receptive host cell as a prerequisite for viral entry and infection. Unlike most other enveloped viruses, the vast majority of paramyxoviruses contain two distinctmembrane-anchored glycoproteins to mediate the attachment, membrane fusion and particle entry stages of host cell infection. The attachment glycoprotein is required for virion attachment and the fusion glycoprotein is directly involved in facilitating the merger of the viral and host cell membranes. Here we detail important functional, biochemical and structural features of the attachment and fusion glycoproteins from a variety of family members. Specifically, the three different classes of attachment glycoproteins are discussed, including receptor binding preference, their overall structure and fusion promotion activities. Recently solved atomic structures of certain attachment glycoproteins are summarized, and how they relate to both receptor binding and fusion mechanisms are described. For the fusion glycoprotein, specific structural domains and their proposed role in mediating membrane merger are illustrated, highlighting the important features of protease cleavage and associated tropism and virulence. The crystal structure solutions of both an uncleaved and a cleavage-activated metastable F are also described with emphasis on how small conformational changes can provide the necessary energy to mediate membrane fusion. Finally, the different proposed fusion models are reviewed, featuring recent experimental findings that speculate how the attachment and fusion glycoproteins work in concert to mediate virus entry.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Lamb RA, Parks GD. Paramyxoviridae: The viruses and their replication. In: Knipe DM, Howley PM eds. Fields Virology, 5 ed. Philadelphia: Lippincott Williams & Wilkins, 2007:1449–1496.Google Scholar
  2. 2.
    Alexander DJ. Newcastle disease and other avian paramyxoviruses. Rev Sci Tech 2000; 19(2):443–462.PubMedGoogle Scholar
  3. 3.
    Tambi EN, Maina OW, Mukhebi AW et al. Economic impact assessment of rinderpest control in Africa. Rev Sci Tech 1999; 18(2):458–477.PubMedGoogle Scholar
  4. 4.
    Eaton BT, Broder CC, Middleton D et al. Hendra and Nipah viruses: different and dangerous. Nat Rev Microbiol 2006; 4(1):23–35.PubMedCrossRefGoogle Scholar
  5. 5.
    Eaton BT, Mackenzie JS, Wang L-F. Henipaviruses. In: Knipe DM, Howley PM ed. Fields Virology, 5 ed. Philadelphia: Lippincott Williams & Wilkins, 2007:1587–1600.Google Scholar
  6. 6.
    Lamb RA. Mononegavirales. In: Knipe DM, Howley PM ed. Fields Virology, 5 ed. Philadelphia: Lippincott Williams and Wilkins, 2007:1357–1361.Google Scholar
  7. 7.
    Mayo MA. Asummary of taxonomic changes recently approvedby ICTV. Arch Virol 2002; 147(8):1655–1663.PubMedCrossRefGoogle Scholar
  8. 8.
    de Leeuw O, Peeters B. Complete nucleotide sequence of Newcastle disease virus: evidence for the existence of a new genus within the subfamily Paramyxovirinae. J Gen Virol 1999; 80(Pt 1):131–136.PubMedGoogle Scholar
  9. 9.
    Seal BS, Crawford JM, Sellers HS et al. Nucleotide sequence analysis of the Newcastle disease virus nucleocapsid protein gene and phylogenetic relationships among the Paramyxoviridae. Virus Res 2002; 83(1–2):119–129.PubMedCrossRefGoogle Scholar
  10. 10.
    Seal BS, King DJ, Meinersmann RJ. Molecular evolution of the Newcastle disease virus matrix protein gene and phylogenetic relationships among the paramyxoviridae. Virus Res 2000; 66(1):1–11.PubMedCrossRefGoogle Scholar
  11. 11.
    Wang LF, Yu M, Hansson E et al. The exceptionally large genome of Hendra virus: support for creation of a new genus within the family Paramyxoviridae. J Virol 2000; 74(21):9972–9979.PubMedCrossRefGoogle Scholar
  12. 12.
    Li Z, Yu M, Zhang H et al. Beilong virus, a novel paramyxovirus with the largest genome of non-segmented negative-stranded RNA viruses. Virology 2006; 346(1):219–228.PubMedCrossRefGoogle Scholar
  13. 13.
    Kurath G, Batts WN, Ahne W et al. Complete genome sequence of Fer-de-Lance virus reveals a novel gene in reptilian paramyxoviruses. J Virol 2004; 78(4):2045–2056.PubMedCrossRefGoogle Scholar
  14. 14.
    Marsh GA, de Jong C, Barr JA et al. Cedar virus: a novel Henipavirus isolated from Australian bats. PLoS Pathog 2012; 8(8):e1002836.PubMedCrossRefGoogle Scholar
  15. 15.
    Morrison TG. The three faces of paramyxovirus attachment proteins. Trends Microbiol 2001; 9(3):103–105.PubMedCrossRefGoogle Scholar
  16. 16.
    Lamb RA, Jardetzky TS. Structural basis of viral invasion: lessons from paramyxovirus F. Curr Opin Struct Biol 2007; 17(4):427–436.PubMedCrossRefGoogle Scholar
  17. 17.
    Parks GD, Lamb RA. Folding and oligomerization properties of asoluble and secreted form of the paramyxovirus hemagglutinin-neuraminidase glycoprotein. Virology 1990; 178(2):498–508.PubMedCrossRefGoogle Scholar
  18. 18.
    Scheid A, Caliguiri LA, Compans RW et al. Isolation of paramyxovirus glycoproteins. Association of both hemagglutinating and neuraminidase activities with the larger SV5 glycoprotein. Virology 1972; 50(3):640–652.PubMedCrossRefGoogle Scholar
  19. 19.
    Thompson SD, Portner A. Localization of functional sites on the hemagglutinin-neuraminidase glycoprotein of Sendai virus by sequence analysis of antigenic and temperature-sensitivemutants. Virology 1987; 160(1):1–8.PubMedCrossRefGoogle Scholar
  20. 20.
    Langedijk JP, Daus FJ, van Oirschot JT. Sequence and structure alignment of Paramyxoviridae attachment proteins and discovery of enzymatic activity for a morbillivirus hemagglutinin. J Virol 1997;71(8):6155–6167.PubMedGoogle Scholar
  21. 21.
    Yu M, Hansson E, Langedijk JP et al. The attachment protein of Hendra virus has high structural similarity but limited primary sequence homology compared with viruses in the genus Paramyxovirus. Virology 1998; 251(2):227–233.PubMedCrossRefGoogle Scholar
  22. 22.
    Iorio RM, Melanson VR, Mahon PJ. Glycoprotein interactions in paramyxovirus fusion. Future Virol 2009; 4(4):335–351.PubMedCrossRefGoogle Scholar
  23. 23.
    Colman PM, Hoyne PA, Lawrence MC. Sequence and structure alignment of paramyxovirus hemagglutinin-neuraminidase with influenza virus neuraminidase. J Virol 1993; 67(6):2972–2980.PubMedGoogle Scholar
  24. 24.
    Crennell S, Takimoto T, Portner A et al. Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase. Nat Struct Biol 2000; 7(11):1068–1074.PubMedCrossRefGoogle Scholar
  25. 25.
    Lawrence MC, Borg NA, Streltsov VA et al. Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J Mol Biol 2004; 335(5):1343–1357.PubMedCrossRefGoogle Scholar
  26. 26.
    Yuan P, Thompson TB, Wurzburg BA et al. Structural studies of the parainfluenza virus 5 hemagglutinin-neuraminidase tetramer in complex with its receptor, sialyllactose. Structure (Camb) 2005; 13(5):803–815.CrossRefGoogle Scholar
  27. 27.
    Yuan P, Swanson KA, Leser GP et al. Structure of the Newcastle disease virus hemagglutinin-neuraminidase (HN) ectodomain reveals a four-helix bundle stalk. Proc Natl Acad Sci USA 2011; 108(36):14920–14925.PubMedCrossRefGoogle Scholar
  28. 28.
    Hashiguchi T, Kajikawa M, Maita N et al. Crystal structure of measles virus hemagglutinin provides insight into effective vaccines. Proc Natl Acad Sci USA 2007; 104(49):19535–19540.PubMedCrossRefGoogle Scholar
  29. 29.
    Colf LA, Juo ZS, Garcia KC. Structure of the measles virus hemagglutinin. Nat Struct Mol Biol 2007; 14(12):1227–1228.PubMedCrossRefGoogle Scholar
  30. 30.
    Bowden TA, Aricescu AR, Gilbert RJ et al. Structural basis of Nipah and Hendra virus attachment to their cell-surface receptor ephrin-B2. Nat Struct Mol Biol 2008; 15(6):567–572.PubMedCrossRefGoogle Scholar
  31. 31.
    Xu K, Rajashankar KR, Chan YP et al. Host cell recognition by the henipaviruses: crystal structures of the Nipah G attachment glycoprotein and its complex with ephrin-B3. Proc Natl Acad Sci USA 2008; 105(29):9953–9958.PubMedCrossRefGoogle Scholar
  32. 32.
    Thompson SD, Laver WG, Murti KG et al. Isolation of a biologically active soluble form of the hemagglutinin-neuraminidase protein of Sendai virus. J Virol 1988; 62(12):4653–4660.PubMedGoogle Scholar
  33. 33.
    Markwell MA, Fox CF. Protein-protein interactions within paramyxoviruses identified by native disulfide bonding or reversible chemical cross-linking. J Virol 1980; 33(1):152–166.PubMedGoogle Scholar
  34. 34.
    Morrison TG, McQuain C, O’Connell KF et al. Mature, cell-associated HN protein of Newcastle disease virus exists in two forms differentiated by posttranslational modifications. Virus Res 1990; 15(2):113–133.PubMedCrossRefGoogle Scholar
  35. 35.
    Ng DT, Randall RE, Lamb RA. Intracellular maturation and transport of the SV5 type II glycoprotein hemagglutinin-neuraminidase: specific and transient association with GRP78-BiP in the endoplasmic reticulum and extensive internalization from the cell surface. J Cell Biol 1989; 109(6 Pt 2):3273–3289.PubMedCrossRefGoogle Scholar
  36. 36.
    Russell R, Paterson RG, Lamb RA. Studies with cross-linking reagents on the oligomeric form of the paramyxovirus fusion protein. Virology 1994; 199(1):160–168.PubMedCrossRefGoogle Scholar
  37. 37.
    Ng DT, Hiebert SW, Lamb RA. Different roles of individual N-linked oligosaccharide chains in folding, assembly, and transport of the simian virus 5 hemagglutinin-neuraminidase. Mol Cell Biol 1990; 10(5):1989–2001.PubMedGoogle Scholar
  38. 38.
    Zaitsev V, von Itzstein M, Groves D et al. Second sialic acid binding site in Newcastle disease virus hemagglutinin-neuraminidase: implications for fusion. J Virol 2004; 78(7):3733–3741.PubMedCrossRefGoogle Scholar
  39. 39.
    Plemper RK, Hammond AL, Cattaneo R. Characterization of a region of the measles virus hemagglutinin sufficient for its dimerization. J Virol 2000; 74(14):6485–6493.PubMedCrossRefGoogle Scholar
  40. 40.
    Brindley MA, Plemper RK. Blue native PAGE and biomolecular complementation reveal a tetrameric or higher-order oligomer organization of the physiological measles virus attachment protein H. J Virol 2010; 84(23):12174–12184.PubMedCrossRefGoogle Scholar
  41. 41.
    Bossart KN, Crameri G, Dimitrov AS et al. Receptor binding, fusion inhibition and induction of cross-reactive neutralizing antibodies by a soluble G glycoprotein of Hendra virus. J Virol 2005; 79(11):6690–6702.PubMedCrossRefGoogle Scholar
  42. 42.
    Maar D, Harmon B, Chu D et al. Cysteines in the stalk of the Nipah virus G glycoprotein are located in a distinct subdomain critical for fusion activation. J Virol 2012; 86(12):6632–6642.PubMedCrossRefGoogle Scholar
  43. 43.
    Steffen DL, Xu K, Nikolov DB et al. Henipavirus Mediated Membrane Fusion, Virus Entry and Targeted Therapeutics. Viruses 2012; 4(2):280–308.PubMedCrossRefGoogle Scholar
  44. 44.
    Choppin PW, Scheid A. The role of viral glycoproteins in adsorption, penetration, and pathogenicity of viruses. Rev Infect Dis 1980; 2(1):40–61.PubMedCrossRefGoogle Scholar
  45. 45.
    Dorig RE, Marcil A, Chopra A et al. The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 1993; 75(2):295–305.PubMedCrossRefGoogle Scholar
  46. 46.
    Naniche D, Varior-Krishnan G, Cervoni F et al. Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J Virol 1993; 67(10):6025–6032.PubMedGoogle Scholar
  47. 47.
    Nussbaum O, Broder CC, Moss B et al. Functional and structural interactions between measles virus hemagglutinin and CD46. J Virol 1995; 69(6):3341–3349.PubMedGoogle Scholar
  48. 48.
    Tatsuo H, Ono N, Tanaka K et al. SLAM (CDw150) is a cellular receptor for measles virus. Nature 2000; 406(6798):893–897.PubMedCrossRefGoogle Scholar
  49. 49.
    Tatsuo H, Ono N, Yanagi Y. Morbilliviruses use signaling lymphocyte activation molecules (CD150) as cellular receptors. J Virol 2001; 75(13):5842–5850.PubMedCrossRefGoogle Scholar
  50. 50.
    Baron MD. Wild-type Rinderpest virus uses SLAM(CD150)as its receptor. J GenVirol 2005; 86(Pt 6):1753–1757.Google Scholar
  51. 51.
    Galbraith SE, Tiwari A, Baron MD et al. Morbillivirus downregulation of CD46. J Virol 1998; 72(12):10292–10297.PubMedGoogle Scholar
  52. 52.
    Welstead GG, Hsu EC, Iorio C et al. Mechanism of CD150 (SLAM) down regulation from the host cell surface by measles virus hemagglutinin protein. J Virol 2004; 78(18):9666–9674.PubMedCrossRefGoogle Scholar
  53. 53.
    Masse N, Ainouze M, Neel B et al. Measles virus (MV) hemagglutinin: evidence that attachment sites for MV receptors SLAM and CD46 overlap on the globular head. J Virol 2004; 78(17):9051–9063.PubMedCrossRefGoogle Scholar
  54. 54.
    Vongpunsawad S, Oezgun N, Braun W et al. 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 2004; 78(1):302–313.PubMedCrossRefGoogle Scholar
  55. 55.
    Leonard VH, Sinn PL, Hodge G et al. 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 2008; 118(7):2448–2458.PubMedGoogle Scholar
  56. 56.
    Tahara M, Takeda M, Shirogane Y et al. Measles virus infects both polarized epithelial and immune cells by using distinctive receptor-binding sites on its hemagglutinin. J Virol 2008; 82(9):4630–4637.PubMedCrossRefGoogle Scholar
  57. 57.
    Noyce RS, Bondre DG, Ha MN et al. Tumor cell marker PVRL4 (nectin 4) is an epithelial cell receptor for measles virus. PLoS Pathog 2011; 7(8):e1002240.PubMedCrossRefGoogle Scholar
  58. 58.
    Muhlebach MD, Mateo M, Sinn PL et al. Adherens junction protein nectin-4 is the epithelial receptor for measles virus. Nature 2011; 480(7378):530–533.PubMedGoogle Scholar
  59. 59.
    Noyce RS, Richardson CD. Nectin 4 is the epithelial cell receptor for measles virus. Trends Microbiol 2012; 20(9):429–439.PubMedCrossRefGoogle Scholar
  60. 60.
    Zhang X, Lu G, Qi J et al. Structure of measles virus hemagglutinin bound to its epithelial receptor nectin-4. Nat Struct Mol Biol 2012.Google Scholar
  61. 61.
    Santiago C, Celma ML, Stehle T et al. Structure of the measles virus hemagglutinin bound to the CD46 receptor. Nat Struct Mol Biol 2010; 17(1):124–129.PubMedCrossRefGoogle Scholar
  62. 62.
    Hashiguchi T, Ose T, Kubota M et al. Structure of the measles virus hemagglutinin bound to its cellular receptor SLAM. Nat Struct Mol Biol 2011; 18(2):135–141.PubMedCrossRefGoogle Scholar
  63. 63.
    Bossart KN, Wang LF, Flora MN et al. Membrane fusion tropism and heterotypic functional activities of the Nipah virus and Hendra virus envelope glycoproteins. J Virol 2002; 76(22): 11186–11198.PubMedCrossRefGoogle Scholar
  64. 64.
    Bossart KN, Wang LF, Eaton BT et al. Functional expression and membrane fusion tropism of the envelope glycoproteins of Hendra virus. Virology 2001; 290(1):121–135.PubMedCrossRefGoogle Scholar
  65. 65.
    Eaton BT, Wright PJ, Wang LF et al. Henipaviruses: recent observations on regulation of transcription and the nature of the cell receptor. Arch Virol Suppl 2004 (18):122–131.Google Scholar
  66. 66.
    Bonaparte MI, Dimitrov AS, Bossart KN et al. Ephrin-B2 ligand is a functional receptor for Hendra virus and Nipah virus. Proc Natl Acad Sci USA 2005; 102(30):10652–10657.PubMedCrossRefGoogle Scholar
  67. 67.
    Negrete OA, Levroney EL, Aguilar HC et al. EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus. Nature 2005; 436(7049):401–405.PubMedGoogle Scholar
  68. 68.
    Negrete OA, Wolf MC, Aguilar HC et al. Two key residues in EphrinB3 are critical for its use as an alternative receptor for Nipah virus. PLoS Pathog 2006; 2(2):e7.PubMedCrossRefGoogle Scholar
  69. 69.
    Bishop KA, Stantchev TS, Hickey AC et al. Identification of Hendra virus G glycoprotein residues that are critical for receptor binding. J Virol 2007; 81(11):5893–5901.PubMedCrossRefGoogle Scholar
  70. 70.
    Bossart KN, McEachern JA, Hickey AC et al. Neutralization assays for differential henipavirus serology using Bio-Plex Protein Array Systems. J Virol Methods 2007; 142(l–2):29–40.PubMedCrossRefGoogle Scholar
  71. 71.
    Bowden TA, Crispin M, Harvey DJ et al. Dimeric architecture of the Hendra virus attachment glycoprotein: evidence for a conserved mode of assembly. J Virol 2010; 84(12):6208–6217.PubMedCrossRefGoogle Scholar
  72. 72.
    Bowden TA, Crispin M, Harvey DJ et al. Crystal structure and carbohydrate analysis of Nipah virus attachment glycoprotein: a template for antiviral and vaccine design. J Virol 2008; 82(23):11628–11636.PubMedCrossRefGoogle Scholar
  73. 73.
    Xu K, Chan YP, Rajashankar KR et al. New insights into the Hendra virus attachment and entry process from structures of the virus G glycoprotein and its complex with Ephrin-B2. PLoS One 2012; 7(11):e48742.PubMedCrossRefGoogle Scholar
  74. 74.
    Collins PL, Crowe J, J.E. Respiratory Syncytial Virus and Metapneumovirus. In: Knipe DM, Howley PM ed. Fields Virology, 5 ed. Philadelphia: Lippincott Williams & Wilkins, 2007:1601–1646.Google Scholar
  75. 75.
    Harris J, Werling D. Binding and entry of respiratory syncytial virus into host cells and initiation of the innate immune response. Cell Microbiol 2003; 5(10):671–680.PubMedCrossRefGoogle Scholar
  76. 76.
    van den Hoogen BG, Bestebroer TM, Osterhaus AD et al. Analysis of the genomic sequence of a human metapneumovirus. Virology 2002; 295(1):119–132.PubMedCrossRefGoogle Scholar
  77. 77.
    Teng MN, Whitehead SS, Collins PL. Contribution of the respiratory syncytial virus G glycoprotein and its secreted and membrane-boundforms to virus replication in vitro and in vivo. Virology 2001; 289(2):283–296.PubMedCrossRefGoogle Scholar
  78. 78.
    Karron RA, Buonagurio DA, Georgiu AF et al. Respiratory syncytial virus (RSV) SH and G proteins are not essential for viral replication in vitro: clinical evaluation and molecular characterization of a cold-passaged, attenuated RSV subgroup B mutant. Proc Natl Acad Sci USA 1997; 94(25):13961–13966.PubMedCrossRefGoogle Scholar
  79. 79.
    Karron RA, Thumar B, Schappell E et al. Evaluation of two chimeric bovine-human parainfluenza virus type 3 vaccines in infants and young children. Vaccine 2012; 30(26):3975–3981.PubMedCrossRefGoogle Scholar
  80. 80.
    Karger A, Schmidt U, Buchholz UJ. Recombinant bovine respiratory syncytial virus with deletions of the G or SH genes: G and F proteins bind heparin. J Gen Virol 2001; 82(Pt 3):631–640.PubMedGoogle Scholar
  81. 81.
    Techaarpornkul S, Barretto N, Peeples ME. Functional analysis of recombinant respiratory syncytial virus deletion mutants lackingthe small hydrophobic and/or attachment glycoprotein gene. J Virol 2001; 75(15):6825–6834.PubMedCrossRefGoogle Scholar
  82. 82.
    Teng MN, Collins PL. Identification of the respiratory syncytial virus proteins required for formation and passage of helper-dependent infectious particles. J Virol 1998; 72(7):5707–5716.PubMedGoogle Scholar
  83. 83.
    Feldman SA, Hendry RM, Beeler JA. Identification of a linear heparin binding domain for human respiratory syncytial virus attachment glycoprotein G. J Virol 1999; 73(8):6610–6617.PubMedGoogle Scholar
  84. 84.
    Cantin C, Holguera J, Ferreira L et al. Newcastle disease virus may enter cells by caveolae-mediated endocytosis. J Gen Virol 2007; 88(Pt 2):559–569.PubMedCrossRefGoogle Scholar
  85. 85.
    Kolokoltsov AA, Deniger D, Fleming EH et al. Small interfering RNA profiling reveals key role of clathrin-mediated endocytosis and early endosome formation for infection by respiratory syncytial virus. J Virol 2007; 81(14):7786–7800.PubMedCrossRefGoogle Scholar
  86. 86.
    Biacchesi S, Skiadopoulos MH, Yang L et al. Recombinant human Metapneumovirus lacking the small hydrophobic SH and/or attachment G glycoprotein: deletion of G yields a promising vaccine candidate. J Virol 2004; 78(23):12877–12887.PubMedCrossRefGoogle Scholar
  87. 87.
    Biacchesi S, Pham QN, Skiadopoulos MH et al. Infection of nonhuman primates with recombinant human metapneumovirus lacking the SH, G, or M2-2 protein categorizes each as a nonessential accessory protein and identifies vaccine candidates. J Virol 2005; 79(19):12608–12613.PubMedCrossRefGoogle Scholar
  88. 88.
    Chang A, Masante C, Buchholz UJ et al. Human metapneumovirus (HMPV) binding and infection are mediated by interactions between the HMPV fusion protein and heparan sulfate. J Virol 2012; 86(6):3230–3243.PubMedCrossRefGoogle Scholar
  89. 89.
    Cseke G, Maginnis MS, Cox RG et al. Integrin alphavbetal promotes infection by human metapneumovirus. Proc Natl Acad Sci USA 2009; 106(5):1566–1571.PubMedCrossRefGoogle Scholar
  90. 90.
    Schowalter RM, Smith SE, Dutch RE. Characterization of human metapneumovirus F protein-promoted membrane fusion: critical roles for proteolytic processing and low pH. J Virol 2006; 80(22):10931–10941.PubMedCrossRefGoogle Scholar
  91. 91.
    Schowalter RM, Chang A, Robach JG et al. Low-pH triggering of human metapneumovirus fusion: essential residues and importance in entry. J Virol 2009; 83(3):1511–1522.PubMedCrossRefGoogle Scholar
  92. 92.
    Jack PJM, Boyle DB, Eaton BT et al. The complete genome sequence of J-virus reveals a unique genome structure in the family Paramyxoviridae. J Virol 2005; In Press.Google Scholar
  93. 93.
    Jack PJ, Anderson DE, Bossart KN et al. Expression of novel genes encoded by the paramyxovirus J virus. J Gen Virol 2008; 89(Pt 6):1434–1441.PubMedCrossRefGoogle Scholar
  94. 94.
    Paterson RG, Johnson ML, Lamb RA. Paramyxovirus fusion (F) protein and hemagglutinin-neuraminidase (HN) protein interactions: intracellular retention of F and HN does not affect transport of the homotypic HN or F protein. Virology 1997; 237(1):1–9.PubMedCrossRefGoogle Scholar
  95. 95.
    Chan DC, Fass D, Berger JM et al. Core structure of gp41 from the HIV envelope glycoprotein. Cell 1997; 89(2):263–273.PubMedCrossRefGoogle Scholar
  96. 96.
    Fass D, Harrison SC, Kim PS. Retrovirus envelope domain at 1.7 angstrom resolution. Nat Struct Biol 1996; 3(5):465–469.PubMedCrossRefGoogle Scholar
  97. 97.
    Wilson IA, Skehel JJ, Wiley DC. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Aresolution. Nature 1981; 289(5796):366–373.PubMedCrossRefGoogle Scholar
  98. 98.
    Chen L, Colman PM, Cosgrove LJ et al. Cloning, expression, and crystallization of the fusion protein of Newcastle disease virus. Virology 2001; 290(2):290–299.PubMedCrossRefGoogle Scholar
  99. 99.
    Yin HS, Paterson RG, Wen X et al. Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc Natl Acad Sci USA 2005.Google Scholar
  100. 100.
    Yin HS, Wen X, Paterson RG et al. Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 2006; 439(7072):38–44.PubMedCrossRefGoogle Scholar
  101. 101.
    Cao J, Bergeron L, Helseth E et al. Effects of amino acid changes in the extracellular domain ofthe human immunodeficiency virus type 1 gp41 envelope glycoprotein. J Virol 1993; 67:2747–2755.PubMedGoogle Scholar
  102. 102.
    Hernandez LD, Hoffman LR, Wolfsberg TG et al. Virus-cell and cell-cell fusion. Annu Rev Cell Dev Biol 1996; 12:627–661.PubMedCrossRefGoogle Scholar
  103. 103.
    Lescar J, Roussel A, Wien MW et al. The Fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 2001; 105(1):137–148.PubMedCrossRefGoogle Scholar
  104. 104.
    White JM, Delos SE, Brecher M et al. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit Rev Biochem Mol Biol 2008; 43(3):189–219.PubMedCrossRefGoogle Scholar
  105. 105.
    Scheid A, Choppin PW. Identification of biological activities of paramyxovirus glycoproteins. Activation of cell fusion, hemolysis, and infectivity of proteolytic cleavage of an inactive precursor protein of Sendai virus. Virology 1974; 57(2):475–490.PubMedCrossRefGoogle Scholar
  106. 106.
    Klenk HD, Garten W. Host cell proteases controlling virus pathogenicity. Trends Microbiol 1994; 2(2):39–43.PubMedCrossRefGoogle Scholar
  107. 107.
    Gotoh B, Yamauchi F, Ogasawara T et al. Isolation offactor Xa from chick embryo as the amniotic endoprotease responsible for paramyxovirus activation. FEBS Lett 1992; 296(3):274–278.PubMedCrossRefGoogle Scholar
  108. 108.
    Nagai Y, Klenk HD. Activation of precursors to both glycoporteins of Newcastle disease virus by proteolytic cleavage. Virology 1977; 77(1):125–134.PubMedCrossRefGoogle Scholar
  109. 109.
    Pager CT, Dutch RE. Cathepsin L is involved in proteolytic processing of the hendra virus fusion protein. J Virol 2005; 79(20):12714–12720.PubMedCrossRefGoogle Scholar
  110. 110.
    Pager CT, Craft WW, Jr., Patch J et al. A mature and fusogenic form ofthe Nipah virus fusion protein requires proteolytic processing by cathepsin L. Virology 2006; 346(2):251–257.PubMedCrossRefGoogle Scholar
  111. 111.
    Baker KA, Dutch RE, Lamb RA et al. Structural basis for paramyxovirus-mediated membrane fusion. Mol Cell 1999; 3(3):309–319.PubMedCrossRefGoogle Scholar
  112. 112.
    Hunter E. Viral entry and receptors. In: Coffin SH, Hughes SH, and Varmus HE, eds. Retroviruses. New York: Cold Spring Harbor Laboratory Press, 1997:71–119.Google Scholar
  113. 113.
    Novick SL, Hoekstra D. Membrane penetration of Sendai virus glycoproteins during the early stages of fusion with liposomes as determined by hydrophobic photoaffinity labeling. Proc Natl Acad Sci USA 1988; 85(20):7433–7437.PubMedCrossRefGoogle Scholar
  114. 114.
    Dutch RE, Jardetzky TS, Lamb RA. Virus membrane fusion proteins: biological machines that undergo a metamorphosis. Biosci Rep 2000; 20(6):597–612.PubMedCrossRefGoogle Scholar
  115. 115.
    Singh M, Berger B, Kim PS. LearnCoil-VMF: computational evidence for coiled-coil-like motifs in many viral membrane-fusion proteins. J Mol Biol 1999; 290(5):1031–1041.PubMedCrossRefGoogle Scholar
  116. 116.
    Hughson FM. Enveloped viruses: a common mode of membrane fusion? Curr Biol 1997; 7(9):R565–569.PubMedCrossRefGoogle Scholar
  117. 117.
    Plemper RK, Compans RW. Mutations in the putative HR-C region of the measles virus F2 glycoprotein modulate syncytium formation. J Virol 2003; 77(7):4181–4190.PubMedCrossRefGoogle Scholar
  118. 118.
    Wild CT, Shugars DC, Greenwell TK et al. Peptides corresponding to a predictive alpha-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infection. Proc Natl Acad Sci USA 1994; 91(21):9770–9774.PubMedCrossRefGoogle Scholar
  119. 119.
    Jiang S, Lin K, Strick N et al. HIV-1 inhibition by a peptide. Nature 1993; 365:113.PubMedCrossRefGoogle Scholar
  120. 120.
    Lambert DM, Barney S, Lambert AL et al. Peptides from conserved regions of paramyxovirus fusion (F) proteins are potent inhibitors of viral fusion. Proc Natl Acad Sci USA 1996; 93(5):2186–2191.PubMedCrossRefGoogle Scholar
  121. 121.
    Joshi SB, Dutch RE, Lamb RA. A core trimer of the paramyxovirus fusion protein: parallels to influenza virus hemagglutinin and HIV-1 gp41. Virology 1998; 248(1):20–34.PubMedCrossRefGoogle Scholar
  122. 122.
    Wild TF, Buckland R. Inhibition of measles virus infection and fusion with peptides corresponding to the leucine zipper region of the fusion protein. JGen Virol 1997; 78(Pt 1):107–111.Google Scholar
  123. 123.
    Young JK, Li D, Abramowitz MC et al. Interaction of peptides with sequences from the Newcastle disease virus fusion protein heptad repeat regions. J Virol 1999; 73(7):5945–5956.PubMedGoogle Scholar
  124. 124.
    Young JK, Hicks RP, Wright GE et al. Analysis of apeptide inhibitor of paramyxovirus (NDV) fusion using biological assays, NMR, and molecular modeling. Virology 1997; 238(2):291–304.PubMedCrossRefGoogle Scholar
  125. 125.
    Rapaport D, Ovadia M, Shai Y. A synthetic peptide corresponding to a conserved heptad repeat domain is a potent inhibitor of Sendai virus-cell fusion: an emerging similarity with functional domains of other viruses. Embo J 1995; 14(22):5524–5531.PubMedGoogle Scholar
  126. 126.
    Bossart KN, Mungall BA, Crameri G et al. Inhibition of Henipavirus fusion and infection by heptad-derived peptides of the Nipah virus fusion glycoprotein. Virol J 2005; 2:57.PubMedCrossRefGoogle Scholar
  127. 127.
    Dutch RE, Hagglund RN, Nagel MA et al. Paramyxovirus fusion (F) protein: a conformational change on cleavage activation. Virology 2001; 281(1):138–150.PubMedCrossRefGoogle Scholar
  128. 128.
    Zhao X, Singh M, Malashkevich VN et al. Structural characterization of the human respiratory syncytial virus fusion protein core. Proc Natl Acad Sci USA 2000; 97(26):14172–14177.PubMedCrossRefGoogle Scholar
  129. 129.
    Zhu J, Zhang CW, Qi Y et al. The fusion protein core of measles virus forms stable coiled-coil trimer. Biochem Biophys Res Commun 2002; 299(5):897–902.PubMedCrossRefGoogle Scholar
  130. 130.
    Liu Y, Xu Y, Zhu J et al. Crystallization and preliminary X-ray diffraction analysis of central structure domains from mumps virus F protein. Acta Crystallograph Sect F Struct Biol Cryst Commun 2005; 61(Pt9):855–857.CrossRefGoogle Scholar
  131. 131.
    Xu Y, Lou Z, Liu Yet al. Crystallization and preliminary crystallographic analysis of the fusion core from two new zoonotic paramyxoviruses, Nipah virus and Hendra virus. Acta Crystallogr D Biol Crystallogr 2004; 60(Pt 6):1161–1164.PubMedCrossRefGoogle Scholar
  132. 132.
    Chen L, Gorman JJ, McKimm-Breschkin J et al. The structure of the fusion glycoprotein of Newcastle disease virus suggests a novel paradigm for the molecular mechanism of membrane fusion. Structure (Camb) 2001; 9(3):255–266.CrossRefGoogle Scholar
  133. 133.
    Lamb RA, Paterson RG, Jardetzky TS. Paramyxovirus membrane fusion: Lessons from the F and HN atomic structures. Virology 2006; 344(1):30–37.PubMedCrossRefGoogle Scholar
  134. 134.
    Russell CJ, Kantor KL, Jardetzky TS et al. A dual-functional paramyxovirus F protein regulatory switch segment: activation and membrane fusion. J Cell Biol 2003; 163(2):363–374.PubMedCrossRefGoogle Scholar
  135. 135.
    Harbury PB, Kim PS, Alber T. Crystal structure of an isoleucine-zipper trimer. Nature 1994;371(6492):80–83.PubMedCrossRefGoogle Scholar
  136. 136.
    Welch BD, Liu Y, Kors CA et al. Structure of the cleavage-activated prefusion form of the parainfluenza virus 5 fusion protein. Proc Natl Acad Sci USA 2012; 109(41):16672–16677.PubMedCrossRefGoogle Scholar
  137. 137.
    Chan YP, Lu M, Dutta S et al. Biochemical, conformational, and immunogenic analysis of soluble trimeric forms of henipavirus fusion glycoproteins. J Virol 2012; 86(21):11457–11471.PubMedCrossRefGoogle Scholar
  138. 138.
    Russell CJ, Jardetzky TS, Lamb RA. Membrane fusionmachines of paramyxoviruses: capture of intermediates of fusion. Embo J 2001; 20(15):4024–4034.PubMedCrossRefGoogle Scholar
  139. 139.
    Steinhauer DA, Plemper RK. Structure of the primed paramyxovirus fusion protein. Proc Natl Acad Sci USA 2012; 109(41):16404–16405.PubMedCrossRefGoogle Scholar
  140. 140.
    Aguilar HC, Matreyek KA, Choi DY et al. Polybasic KKR motif in the cytoplasmic tail of Nipah virus fusion protein modulates membrane fusion by inside-out signaling. J Virol 2007; 81(9):4520–4532.PubMedCrossRefGoogle Scholar
  141. 141.
    Paterson RG, Russell CJ, Lamb RA. Fusion protein of the paramyxovirus SV5: destabilizing and stabilizing mutants of fusion activation. Virology 2000; 270(1):17–30.PubMedCrossRefGoogle Scholar
  142. 142.
    Waning DL, Russell CJ, Jardetzky TS et al. Activation of a paramyxovirus fusion protein is modulated by inside-out signaling from the cytoplasmic tail. Proc Natl Acad Sci USA 2004; 101(25):9217–9222.PubMedCrossRefGoogle Scholar
  143. 143.
    Smith EC, Culler MR, Hellman LM et al. Beyond anchoring: the expanding role of the hendra virus fusion protein transmembrane domain in protein folding, stability, and function. J Virol 2012; 86(6):3003–3013.PubMedCrossRefGoogle Scholar
  144. 144.
    Skehel JJ, Wiley DC. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 2000; 69:531–569.PubMedCrossRefGoogle Scholar
  145. 145.
    Hu XL, Ray R, Compans RW. Functional interactions between the fusion protein and hemagglutinin-neuraminidase of human parainfluenza viruses [published erratum appears in J Virol 1992 Aug;66(8):5176]. J Virol 1992; 66(3):1528–1534.PubMedGoogle Scholar
  146. 146.
    Bagai S, Lamb RA. Quantitative measurement of paramyxovirus fusion: differences in requirements of glycoproteins between simian virus 5 and human parainfluenza virus 3 or Newcastle disease virus. J Virol 1995; 69(11):6712–6719.PubMedGoogle Scholar
  147. 147.
    Bousse T, Takimoto T, Gorman WL et al. Regions on the hemagglutinin-neuraminidase proteins of human parainfluenza virus type-1 and Sendai virus important for membrane fusion. Virology 1994; 204(2):506–514.PubMedCrossRefGoogle Scholar
  148. 148.
    Deng R, Wang Z, Mirza AM et al. Localization of a domain on the paramyxovirus attachment protein required for the promotion of cellular fusion by its homologous fusion protein spike. Virology 1995; 209(2):457–469.PubMedCrossRefGoogle Scholar
  149. 149.
    Tanabayashi K, Compans RW. Functional interaction of paramyxovirus glycoproteins: identification of a domain in Sendai virus HN which promotes cell fusion. J Virol 1996; 70(9):6112–6118.PubMedGoogle Scholar
  150. 150.
    Tsurudome M, Kawano M, Yuasa T et al. Identification of regions on the hemagglutinin-neuraminidase protein of human parainfluenza virus type 2 important for promoting cell fusion. Virology 1995; 213(1):190–203.PubMedCrossRefGoogle Scholar
  151. 151.
    Melanson VR, Iorio RM. 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 2004; 78(23):13053–13061.PubMedCrossRefGoogle Scholar
  152. 152.
    Melanson VR, Iorio RM. Addition of N-glycans in the stalk of the Newcastle disease virus HN protein blocks its interaction with the F protein and prevents fusion. J Virol 2006; 80(2):623–633.PubMedCrossRefGoogle Scholar
  153. 153.
    Lamb RA. Paramyxovirus fusion: A hypothesis for changes. Virology 1993; 197:1–11.PubMedCrossRefGoogle Scholar
  154. 154.
    McGinnes LW, Gravel K, Morrison TG. Newcastle disease virus HN protein alters the conformation of the F protein at cell surfaces. J Virol 2002; 76(24):12622–12633.PubMedCrossRefGoogle Scholar
  155. 155.
    Morrison T, McQuain C, McGinnes L. Complementation between avirulent Newcastle disease virus and a fusion protein gene expressed from a retro virus vector: requirements for membrane fusion. J Virol 1991; 65(2):813–822.PubMedGoogle Scholar
  156. 156.
    Connolly SA, Leser GP, Jardetzky TS et al. Bimolecular complementation of paramyxovirus fusion and hemagglutinin-neuraminidase proteins enhances fusion: implications for the mechanism of fusion triggering. J Virol 2009; 83(21):10857–10868.PubMedCrossRefGoogle Scholar
  157. 157.
    Yao Q, Hu X, Compans RW. Association of the parainfluenza virus fusion and hemagglutinin-neuraminidase glycoproteins on cell surfaces. J Virol 1997; 71(1):650–656.PubMedGoogle Scholar
  158. 158.
    McGinnes LW, Morrison TG. Inhibition of receptor binding stabilizes newcastle disease virus HN and F protein-containing complexes. J Virol 2006; 80(6):2894–2903.PubMedCrossRefGoogle Scholar
  159. 159.
    Li J, Quinlan E, Mirza A et al. Mutated form of the Newcastle disease virus hemagglutinin-neuraminidase interacts with the homologous fusion protein despite deficiencies in both receptor recognition and fusion promotion. J Virol 2004; 78(10):5299–5310.CrossRefPubMedGoogle Scholar
  160. 160.
    Deng R, Wang Z, Mahon PJ et al. Mutations in the Newcastle disease virus hemagglutinin-neuraminidase protein that interfere with its ability to interact with the homologous F protein in the promotion of fusion. Virology 1999; 253(1):43–54.PubMedCrossRefGoogle Scholar
  161. 161.
    Plemper RK, Hammond AL, Cattaneo R. Measles virus envelope glycoproteins hetero-oligomerize in the endoplasmic reticulum. J Biol Chem 2001; 276(47):44239–44246.PubMedCrossRefGoogle Scholar
  162. 162.
    Plemper RK, Hammond AL, Gerlier D et al. Strength of envelope protein interaction modulates cytopathicity of measles virus. J Virol 2002; 76(10):5051–5061.PubMedCrossRefGoogle Scholar
  163. 163.
    Corey EA, Iorio RM. Mutations in the stalk of the measles virus hemagglutinin protein decrease fusion but do not interfere with virus-specific interaction with the homologous fusion protein. J Virol 2007; 81(18):9900–9910.PubMedCrossRefGoogle Scholar
  164. 164.
    Corey EA, Iorio RM. Measles virus attachment proteins with impaired ability to bind CD46 interact more efficiently with the homologous fusion protein. Virology 2009; 383(1):1–5.PubMedCrossRefGoogle Scholar
  165. 165.
    Aguilar HC, Matreyek KA, Filone CM et al. N-glycans on Nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry. J Virol 2006; 80(10):4878–4889.PubMedCrossRefGoogle Scholar
  166. 166.
    Aguilar HC, Ataman ZA, Aspericueta V et al. A novel receptor-induced activation site in the Nipah virus attachment glycoprotein (G) involved in triggering the fusion glycoprotein (F). J Biol Chem 2009; 284(3):1628–1635.PubMedCrossRefGoogle Scholar
  167. 167.
    Whitman SD, Smith EC, Dutch RE. Differential rates of protein folding and cellular trafficking for the Hendra virus F and G proteins: implications for F-G complex formation. J Virol 2009; 83(17):8998–9001.CrossRefPubMedGoogle Scholar
  168. 168.
    Stone-Hulslander J, Morrison TG. Detection of an interaction between the HN and F proteins in Newcastle disease virus-infected cells. J Virol 1997; 71(9):6287–6295.PubMedGoogle Scholar
  169. 169.
    Tong S, Compans RW. Alternative mechanisms of interaction between homotypic and heterotypic parainfluenza virus HN and F proteins. J Gen Virol 1999; 80(Pt 1):107–115.PubMedGoogle Scholar
  170. 170.
    Whitman SD, Dutch RE. Surface density of the Hendra G protein modulates Hendra F protein-promoted membrane fusion: role for Hendra G protein trafficking and degradation. Virology 2007; 363(2):419–429.PubMedCrossRefGoogle Scholar
  171. 171.
    Lee B, Ataman ZA. Modes of paramyxovirus fusion: a Henipavirus perspective. Trends Microbiol 2011; 19(8):389–399.PubMedCrossRefGoogle Scholar
  172. 172.
    Chang A, Dutch RE. Paramyxovirus fusion and entry: multiple paths to a common end. Viruses 2012; 4(4):613–636.PubMedCrossRefGoogle Scholar
  173. 173.
    Zhu Q, Biering SB, Mirza AM et al. Individual N-glycans added at intervals along the stalk of the Nipah virus G protein prevent fusion, but do not block the interaction with the homologous F protein. J Virol 2013; Jan 2. [Epub ahead of print]Google Scholar
  174. 174.
    Paal T, Brindley MA, St Clair C et al. Probing the spatial organization of measles virus fusion complexes. J Virol 2009; 83(20):10480–10493.PubMedCrossRefGoogle Scholar
  175. 175.
    Brindley MA, Takeda M, Plattet P et al. Triggering the measles virus membrane fusion machinery. Proc Natl Acad Sci USA 2012; 109(44):E3018–3027.PubMedCrossRefGoogle Scholar
  176. 176.
    Ader N, Brindley M, Avila M et al. Mechanism for active membrane fusion triggering by morbillivirus attachment protein. J Virol 2013; 87(1):314–326.PubMedCrossRefGoogle Scholar
  177. 177.
    Porotto M, Devito I, Palmer SG et al. Spring-loadedmodelrevisited: paramyxovirus fusion requires engagement of areceptor binding protein beyond initial triggering of the fusion protein. J Virol 2011; 85(24):12867–12880.PubMedCrossRefGoogle Scholar
  178. 178.
    Porotto M, Palmer SG, Palermo LM et al. Mechanism of fusion triggering by human parainfluenza virus type III: communication between viral glycoproteins during entry. J Biol Chem 2012; 287(1):778–793.PubMedCrossRefGoogle Scholar
  179. 179.
    Sergei T, McGinnes LW, Peeples ME et al. The attachment function of the Newcastle disease virus hemagglutinin-neuraminidase protein can be separated from fusion promotion by mutation. Virology 1993; 193(2):717–726.CrossRefGoogle Scholar
  180. 180.
    Takimoto T, Taylor GL, Crennell SJ et al. Crystallization of Newcastle disease virus hemagglutinin-neuraminidase glycoprotein. Virology 2000; 270(1):208–214.PubMedCrossRefGoogle Scholar
  181. 181.
    Takimoto T, Taylor GL, Connaris HC et al. Role of the hemagglutinin-neuraminidase protein in the mechanism of paramyxovirus-cell membrane fusion. J Virol 2002; 76(24):13028–13033.PubMedCrossRefGoogle Scholar
  182. 182.
    Mishin VP, Watanabe M, Taylor G et al. N-linked glycan at residue 523 of human parainfluenza virus type 3 hemagglutinin-neuraminidase masks a second receptor-binding site. J Virol 2010; 84(6):3094–3100.PubMedCrossRefGoogle Scholar
  183. 183.
    Bousse T, Takimoto T. Mutation at residue 523 creates a second receptor binding site on human parainfluenza virus type 1 hemagglutinin-neuraminidase protein. J Virol 2006; 80(18):9009–9016.PubMedCrossRefGoogle Scholar
  184. 184.
    Porotto M, Fornabaio M, Kellogg GE et al. A second receptor binding site on human parainfluenza virus type 3 hemagglutinin-neuraminidase contributes to activation of the fusion mechanism. J Virol 2007; 81(7):3216–3228.PubMedCrossRefGoogle Scholar
  185. 185.
    Alymova IV, Portner A, Mishin VP et al. Receptor-binding specificity of the human parainfluenza virus type 1 hemagglutinin-neuraminidase glycoprotein. Glycobiology 2012; 22(2):174–180.PubMedCrossRefGoogle Scholar
  186. 186.
    Bousse TL, Taylor G, Krishnamurthy S et al. Biological significance of the second receptor binding site of Newcastle disease virus hemagglutinin-neuraminidase protein. J Virol 2004; 78(23):13351–13355.PubMedCrossRefGoogle Scholar
  187. 187.
    Mahon PJ, Mirza AM, Iorio RM. Role of the two sialic acid binding sites on the newcastle disease virus HN protein in triggering the interaction with the F protein required for the promotion of fusion. J Virol 2011;85(22):12079–12082.PubMedCrossRefGoogle Scholar
  188. 188.
    Porotto M, Salah Z, DeVito I et al. The second receptor binding site of the globular head of the Newcastle disease virus hemagglutinin-neuraminidase activates the stalk of multiple paramyxovirus receptor binding proteins to trigger fusion. J Virol 2012; 86(10):5730–5741.PubMedCrossRefGoogle Scholar
  189. 189.
    Mahon PJ, Mirza AM, Musich TA et al. Engineered intermonomeric disulfide bonds in the globular domain of Newcastle disease virus hemagglutinin-neuraminidase protein: implications for the mechanism of fusion promotion. J Virol 2008; 82(21):10386–10396.PubMedCrossRefGoogle Scholar
  190. 190.
    Navaratnarajah CK, Oezguen N, Rupp L et al. The heads of the measles virus attachment protein move to transmit the fusion-triggering signal. Nat Struct Mol Biol 2011; 18(2):128–134.PubMedCrossRefGoogle Scholar
  191. 191.
    Lee JK, Prussia A, Paal T et al. Functional interaction between paramyxovirus fusion and attachment proteins. J Biol Chem 2008; 283(24):16561–16572.PubMedCrossRefGoogle Scholar
  192. 192.
    Plemper RK, Brindley MA, Iorio RM. Structural and mechanistic studies of measles virus illuminate paramyxovirus entry. PLoS Pathog 2011; 7(6):e1002058.PubMedCrossRefGoogle Scholar
  193. 193.
    Ader N, Brindley MA, Avila M et al. Structural rearrangements of the central region of the morbillivirus attachment protein stalk domain trigger F protein refolding for membrane fusion. J Biol Chem 2012; 287(20):16324–16334.PubMedCrossRefGoogle Scholar
  194. 194.
    Navaratnarajah CK, Negi S, Braun W et al. Membrane fusion triggering: three modules with different structure and function in the upper half ofthe measles virus attachment protein stalk. J Biol Chem 2012.Google Scholar
  195. 195.
    Apte-Sengupta S, Negi S, Leonard VH et al. Base of the measles virus fusion trimer head receives the signal that triggers membrane fusion. J Biol Chem 2012; 287(39):33026–33035.PubMedCrossRefGoogle Scholar
  196. 196.
    Bose S, Zokarkar A, Welch BD et al. Fusion activation by a headless parainfluenza virus 5 hemagglutinin-neuraminidase stalk suggests a modular mechanism for triggering. Proc Natl Acad Sci USA 2012; 109(39):E2625–2634.PubMedCrossRefGoogle Scholar
  197. 197.
    Bishop KA, Hickey AC, Khetawat D et al. Residues in the stalk domain of the hendra virus g glycoprotein modulate conformational changes associated with receptor binding. J Virol 2008; 82(22):11398–11409.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2013

Authors and Affiliations

  • Katharine N. Bossart
    • 1
    • 2
  • Deborah L. Fusco
    • 3
  • Christopher C. Broder
    • 3
  1. 1.Department of MicrobiologyBoston University School of MedicineBostonUSA
  2. 2.National Emerging Infectious Diseases Laboratories InstituteBoston University School of MedicineBostonUSA
  3. 3.Department of Microbiology and ImmunologyUniformed Services UniversityBethesdaUSA

Personalised recommendations