Journal of General Virology (1992), 73, 2591-2600. Printed in Great Britain 2591
Synthesis and processing of the haemagglutinin-esterase glycoprotein of
bovine coronavirus encoded in the E3 region of adenovirus
Dongwan Yoo, 1. Frank L. Graham, 3 Ludvik Prevec, 3 Michael D. Parker, l~ Maria Benk6,1
Tim Zamb ~ and Lorne A. Babiuk 1,2
Veterinary Infectious Disease Organization and 2Department of Veterinary Microbiology, University of Saskatchewan,
Saskatoon, Saskatchewan S7N 0 WO and 3Departments of Biology and Pathology, McMaster University, Hamilton,
Ontario, Canada LSS 4K1
The haemagglutinin-esterase gene (HE) of bovine
coronavirus (BCV) encodes a major viral membrane
glycoprotein that elicits BCV-neutralizing antibodies.
The BCV HE gene was cloned into a human adenovirus
serotype 5 (Ad5) transfer vector in place of early
transcription region 3, and a helper-independent
recombinant virus was constructed by rescue of the
transcription unit by homologous in vivo recombi-
nation between the vector and Ad5 genomic DNA. The
BCV HE polypeptide expressed by this recombinant
Ad was characterized in vivo and in vitro. A 65K
polypeptide was identified using an anti-BCV antibody
in both human (293) and bovine (MDBK) cells infected
with the recombinant Ad. In the absence of a reducing
agent, migration of the 65K polypeptide was shifted to
130K, indicating that the recombinant HE polypeptide
existed in a dimeric form. The HE polypeptide was
glycosylated, as demonstrated by labelling with
[aH]glucosamine, and was immunoreactive with three
distinct groups of conformation-specific anti-HE
monoclonal antibodies (MAbs). Cells infected with
recombinant Ad expressing BCV HE exhibited both
haemadsorption activity and acetylesterase activity. In
addition, the anti-HE group A MAbs HC10-5 and
KD9-40 inhibited both the haemadsorption activity
and esterase activity of the recombinant HE polypep-
tide, suggesting that the antigenic domain responsible
for BCV neutralization may overlap (or is closely
associated with) the domain(s) responsible for haem-
agglutination and/or acetylesterase activities. When
mice were inoculated intraperitoneally with live recom-
binant Ad, a significant level of BCV-neutralizing
HE-specific antibody was induced. These results
indicate that the recombinant Ad replicates and directs
the synthesis of the BCV HE polypeptide in vivo.
Introduction
Coronaviruses contain a large, positive-sense ssRNA of
approximately 30 kb in length that is associated with
nucleocapsid (N) protein (55K) in a helical ribonucleo-
protein complex (MacNaughton et al., 1978). In addition
to the N protein, two membrane glycoproteins are found
in virions: the spike (S) protein (180K) and the integral
membrane (M) protein (23K). The S glycoprotein forms
surface peplomers and functions in virus attachment
(Collins et al., 1982) and cell fusion (Sturman et al., 1985;
de Groots et al., 1989; Yoo et al., 1991), whereas the M
protein determines the site of virus maturation (Tooze et
al., 1984; Rottier & Rose, 1987). A third membrane
glycoprotein, haemagglutinin-esterase (HE; 65K), is
found only in certain species of coronaviruses, such as
bovine coronavirus (BCV) (King & Brian, 1982; King et
t Present address: VirologyAnnex, USAMRIID, Fort Detrick,
Frederick, Maryland21701-5000, U.S.A.
al., 1985; Deregt et al., 1987), haemagglutinating
encephalomyelitis virus (Callebaut & Pensaert, 1980)
and human coronavirus OC43 (Hogue & Brian, 1986). In
strains of mouse hepatitis virus (MHV), the HE gene is
present but is expressed in only a few isolates (Makino &
Lai, 1989; Shieh et al., 1989). It appears that the HE gene
in MHV-JHM is a pseudogene which is not essential for
virus replication (Yokomori et al., 1991). Moreover, the
HE gene does not exist at all in avian infectious
bronchitis virus (Stern & Sefton, 1982; Boursnell et al.,
1987) or porcine transmissible gastroenteritis virus
(Garwes & Reynolds, 1981). In contrast, the HE protein
of BCV is a major membrane-associated glycoprotein
and is essential for virus replication (Vlasak et al.,
1988b). The BCV HE has been reported to exhibit
significant sequence homology with the haemagglutinin
of type C human influenza virus (Nakada et al., 1984;
Luytjes et al., 1988; Parker et al., 1989, 1990b), having
known haemagglutination and acetylesterase functions
0001-0928 © 1992SGM