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The Murine Coronavirus Hemagglutinin-esterase Receptor-binding Site: A Major Shift in Ligand Specificity through Modest Changes in Architecture


The hemagglutinin-esterases (HEs), envelope glycoproteins of corona-, toro- and orthomyxoviruses, mediate reversible virion attachment to O-acetylated sialic acids (O-Ac-Sias). They do so through concerted action of distinct receptor-binding (“lectin”) and receptor-destroying sialate O-acetylesterase (”esterase”) domains. Most HEs target 9-O-acetylated Sias. In one lineage of murine coronaviruses, however, HE esterase substrate and lectin ligand specificity changed dramatically as these viruses evolved to use 4-O-acetylated Sias instead. Here we present the crystal structure of the lectin domain of mouse hepatitis virus (MHV) strain S HE, resolved both in its native state and in complex with a receptor analogue. The data show that the shift from 9-O- to 4-O-Ac-Sia receptor usage primarily entailed a change in ligand binding topology and, surprisingly, only modest changes in receptor-binding site architecture. Our findings illustrate the ease with which viruses can change receptor-binding specificity with potential consequences for host-, organ and/or cell tropism, and for pathogenesis.


Vyšlo v časopise: The Murine Coronavirus Hemagglutinin-esterase Receptor-binding Site: A Major Shift in Ligand Specificity through Modest Changes in Architecture. PLoS Pathog 8(1): e32767. doi:10.1371/journal.ppat.1002492
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002492

Souhrn

The hemagglutinin-esterases (HEs), envelope glycoproteins of corona-, toro- and orthomyxoviruses, mediate reversible virion attachment to O-acetylated sialic acids (O-Ac-Sias). They do so through concerted action of distinct receptor-binding (“lectin”) and receptor-destroying sialate O-acetylesterase (”esterase”) domains. Most HEs target 9-O-acetylated Sias. In one lineage of murine coronaviruses, however, HE esterase substrate and lectin ligand specificity changed dramatically as these viruses evolved to use 4-O-acetylated Sias instead. Here we present the crystal structure of the lectin domain of mouse hepatitis virus (MHV) strain S HE, resolved both in its native state and in complex with a receptor analogue. The data show that the shift from 9-O- to 4-O-Ac-Sia receptor usage primarily entailed a change in ligand binding topology and, surprisingly, only modest changes in receptor-binding site architecture. Our findings illustrate the ease with which viruses can change receptor-binding specificity with potential consequences for host-, organ and/or cell tropism, and for pathogenesis.


Zdroje

1. AngataTVarkiA 2002 Chemical diversity in the sialic acids and related alpha-keto acids: an evolutionary perspective. Chem Rev 102 439 469

2. KleinARousselP 1998 O-acetylation of sialic acids. Biochimie 80 49 57

3. DumermuthEBeuretNSpiessMCrottetP 2002 Ubiquitous 9-O-acetylation of sialoglycoproteins restricted to the Golgi complex. J Biol Chem 277 18687 18693

4. KleinAKrishnaMVarkiNMVarkiA 1994 9-O-acetylated sialic acids have widespread but selective expression: analysis using a chimeric dual-function probe derived from influenza C hemagglutinin-esterase. Proc Natl Acad Sci U S A 91 7782 7786

5. RogersGNHerrlerGPaulsonJCKlenkHD 1986 Influenza C virus uses 9-O-acetyl-N-acetylneuraminic acid as a high affinity receptor determinant for attachment to cells. J Biol Chem 261 5947 5951

6. de GrootRJ 2006 Structure, function and evolution of the hemagglutinin-esterase proteins of corona- and toroviruses. Glycoconj J 23 59 72

7. HerrlerGSzepanskiSSchultzeB 1991 9-O-acetylated sialic acid, a receptor determinant for influenza C virus and coronaviruses. Behring Inst Mitt 177 184

8. HaselhorstTFlemingFEDyasonJCHartnellRDYuX 2009 Sialic acid dependence in rotavirus host cell invasion. Nat Chem Biol 5 91 93

9. OlofssonSBergstromT 2005 Glycoconjugate glycans as viral receptors. Ann Med 37 154 172

10. KremplCSchultzeBLaudeHHerrlerG 1997 Point mutations in the S protein connect the sialic acid binding activity with the enteropathogenicity of transmissible gastroenteritis coronavirus. J Virol 71 3285 3287

11. AlexanderDADimockK 2002 Sialic acid functions in enterovirus 70 binding and infection. J Virol 76 11265 11272

12. ArnbergNKiddAHEdlundKOlfatFWadellG 2000 Initial interactions of subgenus D adenoviruses with A549 cellular receptors: sialic acid versus alpha(v) integrins. J Virol 74 7691 7693

13. LiptonHLKumarASHertzlerSReddiHV 2006 Differential usage of carbohydrate co-receptors influences cellular tropism of Theiler's murine encephalomyelitis virus infection of the central nervous system. Glycoconj J 23 39 49

14. OlofssonSKumlinUDimockKArnbergN 2005 Avian influenza and sialic acid receptors: more than meets the eye? Lancet Infect Dis 5 184 188

15. BauerPHBronsonRTFungSCFreundRStehleT 1995 Genetic and structural analysis of a virulence determinant in polyomavirus VP1. J Virol 69 7925 7931

16. BauerPHCuiCLiuWRStehleTHarrisonSC 1999 Discrimination between sialic acid-containing receptors and pseudoreceptors regulates polyomavirus spread in the mouse. J Virol 73 5826 5832

17. Lopez-BuenoARubioMPBryantNMcKennaRAgbandje-McKennaM 2006 Host-selected amino acid changes at the sialic acid binding pocket of the parvovirus capsid modulate cell binding affinity and determine virulence. J Virol 80 1563 1573

18. NamHJGurda-WhitakerBGanWYIlariaSMcKennaR 2006 Identification of the sialic acid structures recognized by minute virus of mice and the role of binding affinity in virulence adaptation. J Biol Chem 281 25670 25677

19. VinesAWellsKMatrosovichMCastrucciMRItoT 1998 The role of influenza A virus hemagglutinin residues 226 and 228 in receptor specificity and host range restriction. J Virol 72 7626 7631

20. HelleboAVilasUFalkKVlasakR 2004 Infectious salmon anemia virus specifically binds to and hydrolyzes 4-O-acetylated sialic acids. J Virol 78 3055 3062

21. CornelissenLAWierdaCMvan der MeerFJHerreweghAAHorzinekMC 1997 Hemagglutinin-esterase, a novel structural protein of torovirus. J Virol 71 5277 5286

22. SnijderEJden BoonJAHorzinekMCSpaanWJ 1991 Comparison of the genome organization of toro- and coronaviruses: evidence for two nonhomologous RNA recombination events during Berne virus evolution. Virology 180 448 452

23. ZengQLangereisMAvan VlietALHuizingaEGde GrootRJ 2008 Structure of coronavirus hemagglutinin-esterase offers insight into corona and influenza virus evolution. Proc Natl Acad Sci U S A 105 9065 9069

24. LangereisMAZengQGerwigGJFreyBvon ItzsteinM 2009 Structural basis for ligand and substrate recognition by torovirus hemagglutinin esterases. Proc Natl Acad Sci U S A 106 15897 15902

25. SmitsSLGerwigGJvan VlietALLissenbergABrizaP 2005 Nidovirus sialate-O-acetylesterases: evolution and substrate specificity of coronaviral and toroviral receptor-destroying enzymes. J Biol Chem 280 6933 6941

26. ReglGKaserAIwersenMSchmidHKohlaG 1999 The hemagglutinin-esterase of mouse hepatitis virus strain S is a sialate-4-O-acetylesterase. J Virol 73 4721 4727

27. LangereisMAvan VlietALBootWde GrootRJ 2010 Attachment of mouse hepatitis virus to O-acetylated sialic acid is mediated by hemagglutinin-esterase and not by the spike protein. J Virol 84 8970 8974

28. RosenthalPBZhangXFormanowskiFFitzWWongCH 1998 Structure of the haemagglutinin-esterase-fusion glycoprotein of influenza C virus. Nature 396 92 96

29. HanaokaKPritchettTJTakasakiSKochibeNSabesanS 1989 4-O-acetyl-N-acetylneuraminic acid in the N-linked carbohydrate structures of equine and guinea pig alpha 2-macroglobulins, potent inhibitors of influenza virus infection. J Biol Chem 264 9842 9849

30. ReuterGPfeilRStollSSchauerRKamerlingJP 1983 Identification of new sialic acids derived from glycoprotein of bovine submandibular gland. Eur J Biochem 134 139 143

31. KaziLLissenbergAWatsonRde GrootRJWeissSR 2005 Expression of hemagglutinin esterase protein from recombinant mouse hepatitis virus enhances neurovirulence. J Virol 79 15064 15073

32. WilliamsRKJiangGSHolmesKV 1991 Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc Natl Acad Sci U S A 88 5533 5536

33. DvekslerGSPensieroMNCardellichioCBWilliamsRKJiangGS 1991 Cloning of the mouse hepatitis virus (MHV) receptor: expression in human and hamster cell lines confers susceptibility to MHV. J Virol 65 6881 6891

34. BoschBJRottierPJM 2008 Nidovirus entry into cells. PerlmanSGallagherTSnijderEJ Nidoviruses Washington D.C. ASM Press 157 177

35. LiWMooreMJVasilievaNSuiJWongSK 2003 Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426 450 454

36. ReevesPJCallewaertNContrerasRKhoranaHG 2002 Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc Natl Acad Sci U S A 99 13419 13424

37. KamerlingJPVliegenthartJFG 1989 Carbohydrates. LawsonAM Clinical Biochemistry - Principles, Methods, Applications, Vol 1, Mass Spectrometry Berlin Walter de Gruyter 176 263

38. KabschW 1993 Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Cryst 26 795 800

39. Collaborative Computational Project, Number 4 1994 The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50 760 763

40. EmsleyPCowtanK 2004 Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60 2126 2132

41. WinnMDIsupovMNMurshudovGN 2001 Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr D Biol Crystallogr 57 122 133

42. KamerlingJPSchauerRShuklaAKStollSVan HalbeekH 1987 Migration of O-acetyl groups in N,O-acetylneuraminic acids. Eur J Biochem 162 601 607

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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