Journal of General Virology (1994), 75, 3742. Printed in Great Brita#l 37
A small percentage of influenza virus M1 protein contains zinc but zinc
does not influence in vitro M1-RNA interaction
Christine Elster, ~ Eric Fourest, 2 Florence Baudin, ~ Kjeld Larsen, ~ Stephen Cusack 1
and Rob W. H. Ruigrok 1.
1 EMBL Grenoble Outstation, c/o ILL, BP 156, 38042 Grenoble Cedex 9 and 2 CEN-G/DBMS/TSV, BP 85X,
38041 Grenoble Cedex, France
A peptide containing the CCHH motif, the putative
zinc-binding sequence of influenza virus M1 protein,
was found to bind zinc in a one-to-one complex with the
characteristics of a typical zinc-binding peptide. Intact
influenza virus also contained zinc and we show that this
zinc is bound to the M1 protein in the virus. However,
only a small proportion of M1 contained zinc: 4% in
virus and 6 to 9 % in isolated protein. One strain,
B/Yamagata/16/88, consistently contained more zinc:
15 to 20% both in virus and in isolated protein. We
also determined the RNA binding and transcription in-
hibition activities of various M1 proteins and found that
the zinc content of M1 had no influence on either
activity. We suggest that the zinc in M1 has a structural
role in the virion other than nucleic acid binding.
Introduction
Influenza viruses are enveloped viruses with a segmented
negative strand RNA genome. Each vRNA segment is
complexed with the major RNA-binding protein nucleo-
protein (NP) and carries a copy of the polymerase
complex. These structures, called ribonucleoprotein
particles (RNPs), are independent active transcription
units. The total genome consists of eight RNPs which are
contained within a shell of M1 protein which lines the
inside of the viral lipid bilayer. Embedded in this lipid
bilayer are the viral glycoproteins which are essential for
entry into and release from the host cell.
The structure of the virion suggests an important role
for the M 1 protein. M 1 may interact with the cytoplasmic
tails of the glycoproteins, the lipid membrane and the
RNPs and so form the 'glue' between them. Interaction
of M 1 with lipid has been shown in intact virus using
light-activated cross-linking (Gregoriades & Frangione,
1981) and also in vitro using isolated M1 and liposomes
(Bucher et al., 1980). Contact between M1 and the
glycoproteins has not yet been shown but interaction of
M1 with RNP is suggested by the fact that purified M1,
when added to transcribing RNPs, inhibits transcription
(Zvonarjev & Ghendon, 1980; Ye et al., 1989). hi vitro
interaction of M 1 with RNA has been shown with filter-
binding assays and a blotting technique (Wakefield &
Brownlee, 1989; Ye et al., 1989).
The primary sequence of all influenza A and B M1
proteins contains the putative zinc-binding sequence
CysXaa~-CysXaa 7 His-Xaa~ His (CCHH motif)
(residues 148 to 162 of A/PR/8/34 M1 protein; Allen et
al., 1980), first remarked upon by Wakefield & Brownlee
(1989), which could be involved in RNA binding. This
CCHH motif is situated in a part of the M1 sequence
that may be involved in transcription inhibition (Ye et
al., 1989). Zinc-binding sequences have been implicated
in specific protein-nucleic acid interactions and protein
dimerization domains (see references in Discussion). In
this paper we describe the zinc-binding activity of a 27
amino acid peptide containing the CCHH motif and
have determined the zinc content of intact influenza virus
and purified M 1. We further show that the zinc content
of M1 does not influence the in vitro RNA binding and
transcription inhibition activities of M1.
Methods
Virus and M1 protein. InfluenzavirusesA/PR/8/34, B/Beijing/1/87
and B/Yamagata/16/88 were grown in embryonated hen's eggs and
obtained in purified form from Pasteur-Mrrieux, Marcy L'Etoile,
France. M1 protein was isolated from spikeless virus. Spikes were
removed by bromelain digestion (Brand & Skehel, 1972) which was
stopped by addition of 100 mM-iodoacetamide. Spikeless virus was
then purified by pelleting through 14% sucrosein PBS. The virus was
then disrupted with 1% Triton X-I00 in PBS and centrifugedon a 10
to 30 % continuousglycerol gradientin PBS (SW41rotor, 36000 r.p.m.,
4 °C, 16 h). M1 was collectedfrom the upper fractions of the gradient
and stored immediatelyat -20 °C. The purity was judged to be higher
than 90% by PAGE (Fig. 1).
Virus protein concentrationswere determinedby the Lowry method
(Lowry et al., 1951) using BSA as a standard. The concentration of
isolated M 1 protein was determinedwith the Lowry and the Bradford
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