Group 2 coronaviruses are characterized within the order Nidovirales by a unique genome organization. A characteristic feature of group 2 coronaviruses is the presence of a gene encoding the haemagglutinin–esterase (HE) protein, which is absent in coronaviruses of groups 1 and 3. At least three coronavirus strains within group 2 expressed a structural protein with sialate-4-O-acetylesterase activity, distinguishing them from other members of group 2, which encode an enzyme specific for 5-N-acetyl-9-O-acetylneuraminic acid. The esterases of mouse hepatitis virus (MHV) strains S and JHM and puffinosis virus (PV) specifically hydrolysed 5-N-acetyl-4-O-acetylneuraminic acid (Neu4,5Ac2) as well as the synthetic substrates p-nitrophenyl acetate, 4-methylumbelliferyl acetate and fluorescein diacetate. The Km values of the MHV-like esterases for the latter substrates were two- to tenfold lower than those of the sialate-9-O-acetylesterases of influenza C viruses. Another unspecific esterase substrate, α-naphthyl acetate, was used for the in situ detection of the dimeric HE proteins in SDS–polyacrylamide gels. MHV-S, MHV-JHM and PV bound to horse serum glycoproteins containing Neu4,5Ac2. De-O-acetylation of the glycoproteins by alkaline treatment or incubation with the viral esterases resulted in a complete loss of recognition, indicating a specific interaction of MHV-like coronaviruses with Neu4,5Ac2. Combined with evidence for distinct phylogenetic lineages of group 2 coronaviruses, subdivision into subgroups 2a (MHV-like viruses) and 2b (bovine coronavirus-like viruses) is suggested.
BosE. C.,
LuytjesW.,
van der MeulenH. V.,
KoertenH. K.,
SpaanW. J.1996; The production of recombinant infectious DI-particles of a murine coronavirus in the absence of helper virus. Virology 218:52–60
CornelissenL. A.,
WierdaC. M.,
van der MeerF. J.,
HerreweghA. A.,
HorzinekM. C.,
EgberinkH. F.,
de GrootR. J.1997; Hemagglutinin–esterase, a novel structural protein of torovirus. Journal of Virology 71:5277–5286
DuckmantonL.,
TellierR.,
RichardsonC.,
PetricM.1999; The novel hemagglutinin–esterase genes of human torovirus and Breda virus. Virus Research 64:137–149
EnjuanesL.,
BrianD.,
CavanaghD.,
HolmesK.,
LaiM. M.,
LaudeH.,
MastersP. S.,
RottierP.,
SiddellS.,
SpaanW.,
TaguchiF.,
TalbotP.2000; Coronaviridae . In Virus Taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses pp 835–849 Edited by
van RegenmortelM. H. V.,
FauquetC. M.,
BishopD. H. L.,
CarstensE. B.,
EstesM. K.,
LemonS. M.,
ManiloffJ.,
MayoM. A.,
McGeochD. J.,
PringleC. R.,
WicknerR. B.
New York: Academic Press;
Garcia-SastreA.,
VillarE.,
ManuguerraJ. C.,
HannounC.,
CabezasJ. A.1991; Activity of influenza C virus O -acetylesterase with O -acetyl-containing compounds. Biochemical Journal 273:435–441
KlauseggerA.,
StroblB.,
ReglG.,
KaserA.,
LuytjesW.,
VlasakR.1999; Identification of a coronavirus hemagglutinin–esterase with a substrate specificity different from those of influenza C virus and bovine coronavirus. Journal of Virology 73:3737–3743
KruegerD. K.,
KellyS. M.,
LewickiD. N.,
RuffoloR.,
GallagherT. M.2001; Variations in disparate regions of the murine coronavirus spike protein impact the initiation of membrane fusion. Journal of Virology 75:2792–2802
NakadaS.,
CreagerR. S.,
KrystalM.,
AaronsonR. P.,
PaleseP.1984; Influenza C virus hemagglutinin: comparison with influenza A and B virus hemagglutinins. Journal of Virology 50:118–124
NuttallP. A.,
HarrapK. A.1982; Isolation of a coronavirus during studies on puffinosis, a disease of the Manx shearwater ( Puffinus puffinus ). Archives of Virology 73:1–13
ReglG.,
KaserA.,
IwersenM.,
SchmidH.,
KohlaG.,
StroblB.,
VilasU.,
SchauerR.,
VlasakR.1999; The hemagglutinin–esterase of mouse hepatitis virus strain S is a sialate-4- O -acetylesterase. Journal of Virology 73:4721–4727
RobitailleJ.,
IzziL.,
DanielsE.,
ZelusB.,
HolmesK. V.,
BeaucheminN.1999; Comparison of expression patterns and cell adhesion properties of the mouse biliary glycoproteins Bbgp1 and Bbgp2. European Journal of Biochemistry 264:534–544
SchultzeB.,
GrossH. J.,
BrossmerR.,
HerrlerG.1991a; The S protein of bovine coronavirus is a hemagglutinin recognizing 9- O -acetylated sialic acid as a receptor determinant. Journal of Virology 65:6232–6237
SchultzeB.,
WahnK.,
KlenkH.-D.,
HerrlerG.1991b; Isolated HE-protein from hemagglutinating encephalomyelitis virus and bovine coronavirus has receptor-destroying and receptor-binding activity. Virology 180:221–228
SugawaraK.,
OhuchiM.,
NakamuraK.,
HommaM.1981; Effects of various proteases on the glycoprotein composition and the infectivity of influenza C virus. Archives of Virology 68:147–151
VlasakR.,
LuytjesW.,
LeiderJ.,
SpaanW.,
PaleseP.1988a; The E3 protein of bovine coronavirus is a receptor-destroying enzyme with acetylesterase activity. Journal of Virology 62:4686–4690
VlasakR.,
LuytjesW.,
SpaanW.,
PaleseP.1988b; Human and bovine coronaviruses recognize sialic acid-containing receptors similar to those of influenza C viruses. Proceedings of the National Academy of Sciences, USA 85:4526–4529
VolzD.,
ReidP. E.,
ParkC. M.,
OwenD. A.,
DunnW. L.1987; A new histochemical method for the selective periodate oxidation of total tissue sialic acids. Histochemical Journal 19:311–318
WessnerD. R.,
ShickP. C.,
LuJ. H.,
CardellichioC. B.,
GagnetenS. E.,
BeaucheminN.,
HolmesK. V.,
DvekslerG. S.1998; Mutational analysis of the virus and monoclonal antibody binding sites in MHVR, the cellular receptor of the murine coronavirus mouse hepatitis virus strain A59. Journal of Virology 72:1941–1948
YokomoriK.,
BannerL. R.,
LaiM. M.1991; Heterogeneity of gene expression of the hemagglutinin–esterase (HE) protein of murine coronaviruses. Virology 183:647–657
YokomoriK.,
StohlmanS. A.,
LaiM. M.1993; The detection and characterization of multiple hemagglutinin–esterase (HE)-defective viruses in the mouse brain during subacute demyelination induced by mouse hepatitis virus. Virology 192:170–178