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Measles pp 59-76 | Cite as

Measles Virus Glycoprotein Complex Assembly, Receptor Attachment, and Cell Entry

  • C. K. Navaratnarajah
  • V. H. J. Leonard
  • R. CattaneoEmail author
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 329)

Measles virus (MV) enters cells by membrane fusion at the cell surface at neutral pH. Two glycoproteins mediate this process: the hemagglutinin (H) and fusion (F) proteins. The H-protein binds to receptors, while the F-protein mediates fusion of the viral and cellular membranes. H naturally interacts with at least three different receptors. The wild-type virus primarily uses the signaling lymphocyte activation molecule (SLAM, CD150) expressed on certain lymphatic cells, while the vaccine strain has gained the ability to also use the ubiquitous membrane cofactor protein (MCP, CD46), a regulator of complement activation. Additionally, MV infects polarized epithelial cells through an unidentified receptor (EpR). The footprints of the three receptors on H have been characterized, and the focus of research is shifting to the characterization of receptor-specific conformational changes that occur in the H-protein dimer and how these are transmitted to the F-protein trimer. It was also shown that MV attachment and cell entry can be readily targeted to designated receptors by adding specificity determinants to the H-protein. These studies have contributed to our understanding of membrane fusion by the glycopro-tein complex of paramyxoviruses in general.

Keywords

Newcastle Disease Virus Measle Virus Cell Entry Purine Nucleoside Phosphorylase Fusion Activation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Alkhatib Briedis DJ (1986) The predicted primary structure of the measles virus hemagglutinin. Virology 150:479–490PubMedCrossRefGoogle Scholar
  2. Armstrong MA, Fraser KB, Dermott E, Shirodaria PV (1982) Immunoelectron microscopic studies on haemagglutinin and haemolysin of measles virus in infected HEp2 cells. J Gen Virol 59:187–192PubMedCrossRefGoogle Scholar
  3. Bartz R, Brinckmann U, Dunster LM, Rima B, ter Meulen V, Schneider-Schaulies J (1996) Mapping amino acids of the measles virus hemagglutinin responsible for receptor (CD46) downregulation. Virology 224:334–337PubMedCrossRefGoogle Scholar
  4. Bolt G, Pedersen IR (1998) The role of subtilisin-like proprotein convertases for cleavage of the measles virus fusion glycoprotein in different cell types. Virology 252:387–398PubMedCrossRefGoogle Scholar
  5. Bucheit AD, Kumar S, Grote DM, Lin Y, von Messling V, Cattaneo RB, Fielding AK (2003) An oncolytic measles virus engineered to enter cells through the CD20 antigen. Mol Ther 7:62–72PubMedCrossRefGoogle Scholar
  6. Buchholz CJ, Schneider U, Devaux P, Gerlier D, Cattaneo R (1996) Cell entry by measles virus: long hybrid receptors uncouple binding from membrane fusion. J Virol 70:3716–3723PubMedGoogle Scholar
  7. Buchholz CJ, Koller D, Devaux P, Mumenthaler C, Schneider-Schaulies J, Braun W, et al (1997) Mapping of the primary binding site of measles virus to its receptor CD46. J Biol Chem 272:22072–22079PubMedCrossRefGoogle Scholar
  8. Buckland R, Malvoisin E, Beauverger P, Wild F (1992) A leucine zipper structure present in the measles virus fusion protein is not required for its tetramerization but is essential for fusion. J Gen Virol 73:1703–1707PubMedCrossRefGoogle Scholar
  9. Buechi M, Bachi T (1982) Microscopy of internal structures of Sendai virus associated with the cytoplasmic surface of host membranes. Virology 120:349–359PubMedCrossRefGoogle Scholar
  10. Casali P, Sissons JG, Fujinami RS, Oldstone MB (1981) Purification of measles virus glycoproteins and their integration into artificial lipid membranes. J Gen Virol 54:161–171PubMedCrossRefGoogle Scholar
  11. Casasnovas JM, Larvie M, Stehle T (1999) Crystal structure of two CD46 domains reveals an extended measles virus-binding surface. EMBO J 18:2911–2922PubMedCrossRefGoogle Scholar
  12. Cathomen T, Mrkic B, Spehner D, Drillien R, Naef R, Pavlovic J, et al (1998) A matrix-less measles virus is infectious and elicits extensive cell fusion: consequences for propagation in the brain. EMBO J 17:3899–3908PubMedCrossRefGoogle Scholar
  13. Cattaneo R, Rose JK (1993) Cell fusion by the envelope glycoproteins of persistent measles viruses which caused lethal human brain disease. J Virol 67:1493–1502PubMedGoogle Scholar
  14. Cherry J (2003) Measles virus. In: Buck C, Demmler G, Kaplan S (eds) Textbook of pediatric infectious diseases. Elsevier, pp 2283–2304Google Scholar
  15. Cocks BG, Chang CC, Carballido JM, Yssel H, de Vries JE, Aversa G (1995) A novel receptor involved in T-cell activation. Nature 376:260–263PubMedCrossRefGoogle Scholar
  16. Colf LA, Juo ZS, Garcia KC (2007) Structure of the measles virus hemagglutinin. Nat Struct Mol Biol 14:1227–1228PubMedCrossRefGoogle Scholar
  17. Condack C, Grivel JC, Devaux P, Margolis L, Cattaneo R (2007) Measles virus vaccine attenuation: suboptimal infection of lymphatic tissue and tropism alteration. J Infect Dis 196:541–549PubMedCrossRefGoogle Scholar
  18. Corey EA, Iorio RM (2007) 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 81:9900–9910PubMedCrossRefGoogle Scholar
  19. Crennell S, Takimoto T, Portner A, Taylor G (2000) Crystal structure of the multifunctional para-myxovirus hemagglutinin-neuraminidase. Nat Struct Biol 7:1068–1074PubMedCrossRefGoogle Scholar
  20. de Swart RL, Ludlow M, de Witte L, Yanagi Y, van Amerongen G, McQuaid S, et al (2007) Predominant infection of CD150 + lymphocytes and dendritic cells during measles virus infection of macaques. PLoS Pathog 3:1771–1781CrossRefGoogle Scholar
  21. Devaux P, Buchholz CJ, Schneider U, Escoffier C, Cattaneo R, Gerlier D (1997) CD46 short consensus repeats III and IV enhance measles virus binding but impair soluble hemagglutinin binding. J Virol 71:4157–4160PubMedGoogle Scholar
  22. Dorig RE, Marcil A, Chopra A, Richardson CD (1993) The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75:295–305PubMedCrossRefGoogle Scholar
  23. Erlenhoefer C, Wurzer WJ, Loffler S, Schneider-Schaulies S, ter Meulen V, Schneider-Schaulies J (2001) CD150 (SLAM) is a receptor for measles virus but is not involved in viral contact-mediated proliferation inhibition. J Virol 75:4499–4505PubMedCrossRefGoogle Scholar
  24. Fournier P, Brons NH, Berbers GA, Wiesmuller KH, Fleckenstein BT, Schneider F, et al (1997) Antibodies to a new linear site at the topographical or functional interface between the hae-magglutinin and fusion proteins protect against measles encephalitis. J Gen Virol 78:1295–1302PubMedGoogle Scholar
  25. Funke S, Maisner A, Mühlebach MD, Koehl U, Grez M, Cattaneo R, et al (2008) Targeted cell entry of lentiviral vectors. Mol Ther 16(8):1427–1436PubMedCrossRefGoogle Scholar
  26. Griffin DE (2007) Measles virus. In: Knipe DM, Howley PM (eds) Fields' virology. Lippincott Williams and Wilkins, Philadelphia, pp 1551–1585Google Scholar
  27. Hallak LK, Merchan JR, Storgard CM, Loftus JC, Russell SJ (2005) Targeted measles virus vector displaying Echistatin infects endothelial cells via alpha(v)beta3 and leads to tumor regression. Cancer Res 65:5292–5300PubMedCrossRefGoogle Scholar
  28. Hammond AL, Plemper RK, Zhang J, Schneider U, Russell SJ, Cattaneo R (2001) Single-chain antibody displayed on a recombinant measles virus confers entry through the tumor-associated carcinoembryonic antigen. J Virol 75:2087–2096PubMedCrossRefGoogle Scholar
  29. Hashiguchi T, Kajikawa M, Maita N, Takeda M, Kuroki K, Sasaki K, et al (2007) Crystal structure of measles virus hemagglutinin provides insight into effective vaccines. Proc Natl Acad Sci U S A 104:19535–19540PubMedCrossRefGoogle Scholar
  30. Hsu EC, Sarangi F, Iorio C, Sidhu MS, Udem SA, Dillehay DL, et al (1998) A single amino acid change in the hemagglutinin protein of measles virus determines its ability to bind CD46 and reveals another receptor on marmoset B cells. J Virol 72:2905–2916PubMedGoogle Scholar
  31. Hsu EC, Sabatinos S, Hoedemaeker FJ, Rose DR, Richardson CD (1999) Use of site-specific mutagenesis and monoclonal antibodies to map regions of CD46 that interact with measles virus H protein. Virology 258:314–326PubMedCrossRefGoogle Scholar
  32. Hsu EC, Iorio C, Sarangi F, Khine AA, Richardson CD (2001) CDw150(SLAM) is a receptor for a lymphotropic strain of measles virus and may account for the immunosuppressive properties of this virus. Virology 279:9–21PubMedCrossRefGoogle Scholar
  33. Hu A, Cathomen T, Cattaneo R, Norrby E (1995) Influence of N-linked oligosaccharide chains on the processing, cell surface expression and function of the measles virus fusion protein. J Gen Virol 76:705–710PubMedCrossRefGoogle Scholar
  34. Kielian M, Rey FA (2006) Virus membrane-fusion proteins: more than one way to make a hairpin. Nat Rev Microbiol 4:67–76PubMedCrossRefGoogle Scholar
  35. Lamb RA (1993) Paramyxovirus fusion: a hypothesis for changes. Virology 197:1–11PubMedCrossRefGoogle Scholar
  36. Lamb RA, Parks GD (2007) Paramyxoviridae: the viruses and their replication. In: Knipe DM, Howley PM (eds) Fields virology. Lippincott Williams and Wilkins, Philadelphia, pp 1449–1496Google Scholar
  37. Lawrence MC, Borg NA, Streltsov VA, Pilling PA, Epa VC, Varghese JN, et al (2004) Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J Mol Biol 335:1343–1357PubMedCrossRefGoogle Scholar
  38. Lecouturier V, Fayolle J, Caballero M, Carabana J, Celma ML, Fernandez-Munoz R, et al (1996) Identification of two amino acids in the hemagglutinin glycoprotein of measles virus (MV) that govern hemadsorption HeLa cell fusion, and CD46 downregulation: phenotypic markers that differentiate vaccine and wild-type MV strains. J Virol 70:4200–4204PubMedGoogle Scholar
  39. Leonard VHJ, Sinn PL, Hodge G, Miest T, Devaux P, Oezguen N, et al (2008) Epithelial cell receptor-blind measles virus remains virulent but cannot cross epithelia and is not shed. J Clin Invest 118(7):2448–2458PubMedGoogle Scholar
  40. Liu TC, Galanis E, Kirn D (2007) Clinical trial results with oncolytic virotherapy: a century of promise, a decade of progress. Nat Clin Pract Oncol 4:101–117PubMedCrossRefGoogle Scholar
  41. Ludwig Schade B, Bottcher C, Korte T, Ohlwein N, Baljinnyam B, et al (2008) Electron cryo-microscopy reveals different F1+F2 protein states in intact parainfluenza virions. J Virol 82:3775–3781PubMedCrossRefGoogle Scholar
  42. Manchester M, Gairin JE, Patterson JB, Alvarez J, Liszewski MK, Eto DS, et al (1997) Measles virus recognizes its receptor CD46, via two distinct binding domains within SCR1–2. Virology 233:174–184PubMedCrossRefGoogle Scholar
  43. Masse N, Ainouze M, Neel B, Wild TF, Buckland R, Langedijk JP (2004) Measles virus (MV) hemagglutinin: evidence that attachment sites for MV receptors SLAM and CD46 overlap on the globular head. J Virol 78:9051–9063PubMedCrossRefGoogle Scholar
  44. McGinnes LW, Morrison TG (2006) Inhibition of receptor binding stabilizes Newcastle disease virus HN and F protein-containing complexes. J Virol 80:2894–2903PubMedCrossRefGoogle Scholar
  45. Mühlebach MD, Leonard VHJ, Cattaneo R (2008) The measles virus fusion protein transmem-brane region controls formation of an active glycoprotein complex and fusion efficiency. J Virol (in press)Google Scholar
  46. Nakamura T, Peng KW, Vongpunsawad S, Harvey M, Mizuguchi H, Hayakawa T, et al (2004) Antibody-targeted cell fusion. Nat Biotechnol 22:331–336PubMedCrossRefGoogle Scholar
  47. Nakamura T, Peng KW, Harvey M, Greiner S, Lorimer IA, James CD, Russell SJ (2005) Rescue and propagation of fully retargeted oncolytic measles viruses. Nat Biotechnol 23: 209–214PubMedCrossRefGoogle Scholar
  48. Naniche Varior-Krishnan G, Cervoni F, Wild TF, Rossi B, Rabourdin-Combe C, Gerlier D (1993) Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J Virol 67:6025–6032PubMedGoogle Scholar
  49. Navaratnarajah CK, Vongpunsawad S, Oezguen N, Stehle T, Braun W, Hashiguchi T, et al (2008) Dynamic Interaction of the measles virus hemagglutinin with its receptor signaling lym-phocytic activation molecule (SLAM, CD150). J Biol Chem 283:11763–11771PubMedCrossRefGoogle Scholar
  50. Ohno Seki F, Ono N, Yanagi Y (2003) Histidine at position 61 and its adjacent amino acid residues are critical for the ability of SLAM (CD150) to act as a cellular receptor for measles virus. J Gen Virol 84:2381–2388PubMedCrossRefGoogle Scholar
  51. Ono N, Tatsuo H, Hidaka Y, Aoki T, Minagawa H, Yanagi Y (2001a) Measles viruses on throat swabs from measles patients use signaling lymphocytic activation molecule (CDw150) but not CD46 as a cellular receptor. J Virol 75:4399–4401CrossRefGoogle Scholar
  52. Ono N, Tatsuo H, Tanaka K, Minagawa H, Yanagi Y (2001b) V domain of human SLAM (CDw150) is essential for its function as a measles virus receptor. J Virol 75:1594–1600CrossRefGoogle Scholar
  53. Panum P (1939) Observations made during the epidemic of measles on the Faroe Islands in the year 1846. Med Classics 3:803–886Google Scholar
  54. Peng KW, Donovan KA, Schneider U, Cattaneo R, Lust JA, Russell SJ (2003) Oncolytic measles viruses displaying a single-chain antibody against CD38, a myeloma cell marker. Blood 101:2557–2562PubMedCrossRefGoogle Scholar
  55. Plemper RK, Hammond AL, Cattaneo R (2000) Characterization of a region of the measles virus hemagglutinin sufficient for its dimerization. J Virol 74:6485–6493PubMedCrossRefGoogle Scholar
  56. Plemper RK, Hammond AL, Cattaneo R (2001) Measles virus envelope glycoproteins hetero-oli-gomerize in the endoplasmic reticulum. J Biol Chem 276:44239–44246PubMedCrossRefGoogle Scholar
  57. Plemper RK, Hammond AL, Gerlier D, Fielding AK, Cattaneo R (2002) Strength of envelope protein interaction modulates cytopathicity of measles virus. J Virol 76:5051–5061PubMedCrossRefGoogle Scholar
  58. Rager M, Vongpunsawad S, Duprex WP, Cattaneo R (2002) Polyploid measles virus with hexam-eric genome length. EMBO J 21:2364–2372PubMedCrossRefGoogle Scholar
  59. Richardson C, Hull D, Greer P, Hasel K, Berkovich A, Englund G, et al (1986) The nucleotide sequence of the mRNA encoding the fusion protein of measles virus (Edmonston strain): a comparison of fusion proteins from several different paramyxoviruses. Virology 155:508–523PubMedCrossRefGoogle Scholar
  60. Schneider U, Bullough F, Vongpunsawad S, Russell SJ, Cattaneo R (2000) Recombinant measles viruses efficiently entering cells through targeted receptors. J Virol 74:9928–9936PubMedCrossRefGoogle Scholar
  61. Schneider-Schaulies Schnorr JJ, Brinckmann U, Dunster LM, Baczko K, Liebert UG, et al (1995) Receptor usage and differential downregulation of CD46 by measles virus wild-type and vaccine strains. Proc Natl Acad Sci USA 92:3943–3947PubMedCrossRefGoogle Scholar
  62. Springfeld C, von Messling V, Frenzke M, Ungerechts G, Buchholz CJ, Cattaneo R (2006) Oncolytic efficacy and enhanced safety of measles virus activated by tumor-secreted matrix metalloproteinases. Cancer Res 66:7694–7700PubMedCrossRefGoogle Scholar
  63. Tahara M, Takeda M, Shirogane Y, Hashiguchi T, Ohno S, Yanagi Y (2008) Measles virus infects both polarized epithelial and immune cells by using distinctive receptor-binding sites on its hemagglutinin. J Virol 82:4630–4637PubMedCrossRefGoogle Scholar
  64. Tatsuo H, Ono N, Tanaka K, Yanagi Y (2000) SLAM (CDw150) is a cellular receptor for measles virus. Nature 406:893–897PubMedCrossRefGoogle Scholar
  65. Ungerechts G, Springfeld C, Frenzke ME, Lampe J, Johnston PB, Parker WB, et al (2007a) Lymphoma chemovirotherapy: CD20-targeted and convertase-armed measles virus can syner-gize with fludarabine. Cancer Res 67:10939–10947CrossRefGoogle Scholar
  66. Ungerechts G, Springfeld C, Frenzke ME, Lampe J, Parker WB, Sorscher EJ, Cattaneo R (2007b) An immunocompetent murine model for oncolysis with an armed and targeted measles virus. Mol Ther 15:1991–1997CrossRefGoogle Scholar
  67. von Messling V, Svitek N, Cattaneo R (2006) Receptor (SLAM [CD150]) recognition and the V protein sustain swift lymphocyte-based invasion of mucosal tissue and lymphatic organs by a morbillivirus. J Virol 80:6084–6092CrossRefGoogle Scholar
  68. 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 78:302–313PubMedCrossRefGoogle Scholar
  69. Watanabe Hirano A, Stenglein S, Nelson J, Thomas G, Wong TC (1995) Engineered serine protease inhibitor prevents furin-catalyzed activation of the fusion glycoprotein and production of infectious measles virus. J Virol 69:3206–3210PubMedGoogle Scholar
  70. Wild TF, Malvoisin E, Buckland R (1991) Measles virus: both the haemagglutinin and fusion glycoproteins are required for fusion. J Gen Virol 72:439–442PubMedCrossRefGoogle Scholar
  71. Yanagi Y, Takeda M, Ohno S (2006) Measles virus: cellular receptors, tropism and pathogenesis. J Gen Virol 87:2767–2779PubMedCrossRefGoogle Scholar
  72. Yin HS, Wen X, Paterson RG, Lamb RA, Jardetzky TS (2006) Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439:38–44PubMedCrossRefGoogle Scholar
  73. Yuan P, Thompson TB, Wurzburg BA, Paterson RG, Lamb RA, Jardetzky TS (2005) Structural studies of the parainfluenza virus 5 hemagglutinin-neuraminidase tetramer in complex with its receptor, sialyllactose. Structure 13:803–815PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  • C. K. Navaratnarajah
    • 1
  • V. H. J. Leonard
    • 1
  • R. Cattaneo
    • 1
    Email author
  1. 1.Mayo Clinic College of Medicine, Dept. of Molecular MedicineVirology and Gene Therapy Graduate Track, 200 1st St SWRochesterUSA

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