Structural and Mechanistic Studies of Measles Virus Illuminate Paramyxovirus Entry

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Measles virus (MeV), a member of the paramyxovirus family of enveloped RNA viruses and one of the most infectious viral pathogens identified, accounts for major pediatric morbidity and mortality worldwide although coordinated efforts to achieve global measles control are in place. Target cell entry is mediated by two viral envelope glycoproteins, the attachment (H) and fusion (F) proteins, which form a complex that achieves merger of the envelope with target cell membranes. Despite continually expanding knowledge of the entry strategies employed by enveloped viruses, our molecular insight into the organization of functional paramyxovirus fusion complexes and the mechanisms by which the receptor binding by the attachment protein triggers the required conformational rearrangements of the fusion protein remain incomplete. Recently reported crystal structures of the MeV attachment protein in complex with its cellular receptors CD46 or SLAM and newly developed functional assays have now illuminated some of the fundamental principles that govern cell entry by this archetype member of the paramyxovirus family. Here, we review these advances in our molecular understanding of MeV entry in the context of diverse entry strategies employed by other members of the paramyxovirus family.

Vyšlo v časopise: Structural and Mechanistic Studies of Measles Virus Illuminate Paramyxovirus Entry. PLoS Pathog 7(6): e32767. doi:10.1371/journal.ppat.1002058
Kategorie: Review
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002058

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1. GriffinDE 2007 Measles Virus. KnipeDMHowleyPM Fields Virology 5 ed. Philadelphia Wolters Kluwer/Lippincott Williams & Wilkins 1551 1585

2. LambRAParksGD 2007 Paramyxoviridae: The viruses and their replication. KnipeDMHowleyPM Fields Virology 5 ed. Philadelphia Wolters Kluwer/Lippincott Williams & Wilkins 1449 1496

3. TatsuoHOnoNYanagiY 2001 Morbilliviruses use signaling lymphocyte activation molecules (CD150) as cellular receptors. J Virol 75 5842 5850

4. TatsuoHOnoNTanakaKYanagiY 2000 SLAM (CDw150) is a cellular receptor for measles virus. Nature 406 893 897

5. DorigREMarcilAChopraARichardsonCD 1993 The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75 295 305

6. NanicheDVarior-KrishnanGCervoniFWildTFRossiB 1993 Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J Virol 67 6025 6032

7. ManchesterMEtoDSValsamakisALitonPBFernandez-MunozR 2000 Clinical isolates of measles virus use CD46 as a cellular receptor. J Virol 74 3967 3974

8. TaharaMTakedaMShiroganeYHashiguchiTOhnoS 2008 Measles virus infects both polarized epithelial and immune cells by using distinctive receptor-binding sites on its hemagglutinin. J Virol 82 4630 4637

9. LeonardVHSinnPLHodgeGMiestTDevauxP 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

10. BonaparteMIDimitrovASBossartKNCrameriGMungallBA 2005 Ephrin-B2 ligand is a functional receptor for Hendra virus and Nipah virus. Proc Natl Acad Sci U S A 102 10652 10657

11. NegreteOALevroneyELAguilarHCBertolotti-CiarletANazarianR 2005 EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus. Nature 436 401 405

12. NegreteOAWolfMCAguilarHCEnterleinSWangW 2006 Two key residues in ephrinB3 are critical for its use as an alternative receptor for Nipah virus. PLoS Pathog 2 e7 doi:10.1371/journal.ppat.0020007

13. LambRAJardetzkyTS 2007 Structural basis of viral invasion: lessons from paramyxovirus F. Curr Opin Struct Biol 17 427 436

14. MelikyanGBMarkosyanRMHemmatiHDelmedicoMKLambertDM 2000 Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusion. J Cell Biol 151 413 423

15. PeisajovichSGSamuelOShaiY 2000 Paramyxovirus F1 protein has two fusion peptides: implications for the mechanism of membrane fusion. J Mol Biol 296 1353 1365

16. Ben-EfraimIKligerYHermeshCShaiY 1999 Membrane-induced step in the activation of Sendai virus fusion protein. J Mol Biol 285 609 625

17. ZhaoXSinghMMalashkevichVNKimPS 2000 Structural characterization of the human respiratory syncytial virus fusion protein core. Proc Natl Acad Sci U S A 97 14172 14177

18. IorioRMMahonPJ 2008 Paramyxoviruses: different receptors - different mechanisms of fusion. Trends Microbiol 16 135 137

19. SmithECPopaAChangAMasanteCDutchRE 2009 Viral entry mechanisms: the increasing diversity of paramyxovirus entry. FEBS J 276 7217 7227

20. IorioRMMelansonVRMahonPJ 2009 Glycoprotein interactions in paramyxovirus fusion. Future Virol 4 335 351

21. PatersonRGJohnsonMLLambRA 1997 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 237 1 9

22. LiJQuinlanEMirzaAIorioRM 2004 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 78 5299 5310

23. ConnollySALeserGPJardetzkyTSLambRA 2009 Bimolecular complementation of paramyxovirus fusion and hemagglutinin-neuraminidase proteins enhances fusion: implications for the mechanism of fusion triggering. J Virol 83 10857 10868

24. PlemperRKHammondALCattaneoR 2001 Measles virus envelope glycoproteins hetero-oligomerize in the endoplasmic reticulum. J Biol Chem 276 44239 44246

25. PlemperRKHammondALGerlierDFieldingAKCattaneoR 2002 Strength of envelope protein interaction modulates cytopathicity of measles virus. J Virol 76 5051 5061

26. AguilarHCMatreyekKAChoiDYFiloneCMYoungS 2007 Polybasic KKR motif in the cytoplasmic tail of Nipah virus fusion protein modulates membrane fusion by inside-out signaling. J Virol 81 4520 4532

27. AguilarHCMatreyekKAFiloneCMHashimiSTLevroneyEL 2006 N-glycans on Nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry. J Virol 80 4878 4889

28. BishopKAStantchevTSHickeyACKhetawatDBossartKN 2007 Identification of Hendra virus G glycoprotein residues that are critical for receptor binding. J Virol 81 5893 5901

29. CoreyEAIorioRM 2009 Measles virus attachment proteins with impaired ability to bind CD46 interact more efficiently with the homologous fusion protein. Virology 383 1 5

30. SantiagoCCelmaMLStehleTCasasnovasJM 2010 Structure of the measles virus hemagglutinin bound to the CD46 receptor. Nat Struct Mol Biol 17 124 129

31. HashiguchiTOseTKubotaMMaitaNKamishikiryoJ 2011 Structure of the measles virus hemagglutinin bound to its cellular receptor SLAM. Nat Struct Mol Biol 18 135 141

32. BrindleyMAPlemperRK 2010 Blue native PAGE and biomolecular complementation reveal a tetrameric or higher-order oligomer organization of the physiological measles virus attachment protein H. J Virol 84 12174 12184

33. PaalTBrindleyMASt ClairCPrussiaAGausD 2009 Probing the spatial organization of measles virus fusion complexes. J Virol 83 10480 10493

34. LeeJKPrussiaAPaalTWhiteLKSnyderJP 2008 Functional interaction between paramyxovirus fusion and attachment proteins. J Biol Chem 283 16561 16572

35. YuanPLeserGPDemelerBLambRAJardetzkyTS 2008 Domain architecture and oligomerization properties of the paramyxovirus PIV 5 hemagglutinin-neuraminidase (HN) protein. Virology

36. DengRWangZMahonPJMarinelloMMirzaA 1999 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 253 43 54

37. TsurudomeMKawanoMYuasaTTabataNNishioM 1995 Identification of regions on the hemagglutinin-neuraminidase protein of human parainfluenza virus type 2 important for promoting cell fusion. Virology 213 190 203

38. TanabayashiKCompansRW 1996 Functional interaction of paramyxovirus glycoproteins: identification of a domain in Sendai virus HN which promotes cell fusion. J Virol 70 6112 6118

39. MelansonVRIorioRM 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

40. BowdenTAAricescuARGilbertRJGrimesJMJonesEY 2008 Structural basis of Nipah and Hendra virus attachment to their cell-surface receptor ephrin-B2. Nat Struct Mol Biol 15 567 572

41. ColfLAJuoZSGarciaKC 2007 Structure of the measles virus hemagglutinin. Nat Struct Mol Biol 14 1227 1228

42. HashiguchiTKajikawaMMaitaNTakedaMKurokiK 2007 Crystal structure of measles virus hemagglutinin provides insight into effective vaccines. Proc Natl Acad Sci U S A 104 19535 19540

43. CrennellSTakimotoTPortnerATaylorG 2000 Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase. Nat Struct Biol 7 1068 1074

44. YuanPThompsonTBWurzburgBAPatersonRGLambRA 2005 Structural studies of the parainfluenza virus 5 hemagglutinin-neuraminidase tetramer in complex with its receptor, sialyllactose. Structure 13 803 815

45. ZaitsevVvon ItzsteinMGrovesDKiefelMTakimotoT 2004 Second sialic acid binding site in Newcastle disease virus hemagglutinin-neuraminidase: implications for fusion. J Virol 78 3733 3741

46. LawrenceMCBorgNAStreltsovVAPillingPAEpaVC 2004 Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J Mol Biol 335 1343 1357

47. XuKRajashankarKRChanYPHimanenJPBroderCC 2008 Host cell recognition by the henipaviruses: crystal structures of the Nipah G attachment glycoprotein and its complex with ephrin-B3. Proc Natl Acad Sci U S A 105 9953 9958

48. NavaratnarajahCKOezguenNRuppLKayLLeonardVH 2011 The heads of the measles virus attachment protein move to transmit the fusion-triggering signal. Nat Struct Mol Biol 18 128 134

49. von MesslingVOezguenNZhengQVongpunsawadSBraunW 2005 Nearby clusters of hemagglutinin residues sustain SLAM-dependent canine distemper virus entry in peripheral blood mononuclear cells. J Virol 79 5857 5862

50. BossartKNCrameriGDimitrovASMungallBAFengYR 2005 Receptor binding, fusion inhibition, and induction of cross-reactive neutralizing antibodies by a soluble G glycoprotein of Hendra virus. J Virol 79 6690 6702

51. SaphireEOOldstoneMB 2011 Measles virus fusion shifts into gear. Nat Struct Mol Biol 18 115 116

52. MahonPJMirzaAMMusichTAIorioRM 2008 Engineered intermonomeric disulfide bonds in the globular domain of the Newcastle disease virus hemagglutinin-neuraminidase protein: Implications for the mechanism of fusion promotion. J Virol 82 10386 10396

53. CoreyEAIorioRM 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 9910

54. BishopKAHickeyACKhetawatDPatchJRBossartKN 2008 Residues in the stalk domain of the Hendra virus G glycoprotein modulate conformational changes associated with receptor binding. J Virol 82 11398 11409

55. LeeJKPrussiaASnyderJPPlemperRK 2007 Reversible inhibition of the fusion activity of measles virus F protein by an engineered intersubunit disulfide bridge. J Virol 81 8821 8826

56. YinHSWenXPatersonRGLambRAJardetzkyTS 2006 Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439 38 44

57. PrussiaAJPlemperRKSnyderJP 2008 Measles virus entry inhibitors: a structural proposal for mechanism of action and the development of resistance. Biochemistry 47 13573 13583

58. PlemperRKLakdawalaASGernertKMSnyderJPCompansRW 2003 Structural features of paramyxovirus F protein required for fusion initiation. Biochemistry 42 6645 6655

59. YinHSPatersonRGWenXLambRAJardetzkyTS 2005 Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc Natl Acad Sci U S A 102 9288 9293

60. BirmannsSRusuMWriggersW 2011 Using Sculptor and Situs for simultaneous assembly of atomic components into low-resolution shapes. J Struct Biol 173 428 435

61. PattersonJBScheiflingerFManchesterMYilmaTOldstoneMB 1999 Structural and functional studies of the measles virus hemagglutinin: identification of a novel site required for CD46 interaction. Virology 256 142 151