
Secretion of a peripheral membrane protein, MFG-E8,
as a complex with membrane vesicles
A possible role in membrane secretion
Kenji Oshima
1
, Naohito Aoki
1
, Takeo Kato
2
, Ken Kitajima
1
and Tsukasa Matsuda
1
1
Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan;
2
Food Research Institute, Aichi Prefectural
Government, Nagoya, Japan
MFG-E8 (milk fat globule-EGF factor 8) is a peripheral
membrane glycoprotein, which is expressed abundantly in
lactating mammary glands and is secreted in association with
fat globules. This protein consists of two-repeated EGF-like
domains, a mucin-like domain and two-repeated discoidin-
like domains (C-domains), and contains an integrin-binding
motif (RGD sequence) in the EGF-like domain. To clarify
the role of each domain on the peripheral association with
the cell membrane, several domain-deletion mutants of
MFG-E8 were expressed in COS-7 cells. The immunofluo-
rescent staining of intracellular and cell-surface proteins and
biochemical analyses of cell-surface-biotinylated and secre-
ted proteins demonstrated that both of the two C-domains
were required for the membrane association. During the
course of these studies for domain functions, MFG-E8, but
not C-domain deletion mutants, was shown to be secreted as
membrane vesicle complexes. By size-exclusion chromato-
graphy and ultracentrifugation analyses, the complexes were
characterized to have a high-molecular mass, low density
and higher sedimentation velocity and to be detergent-
sensitive. Not only such a exogenously expressed MFG-E8
but also that endogenously expressed in a mammary epi-
thelial cell line, COMMA-1D, was secreted as the membrane
vesicle-like complex. Scanning electron microscopic analyses
revealed that MFG-E8 was secreted into the culture medium
in association with small membrane vesicles with a size from
100 to 200 nm in diameter. Furthermore, the expression of
MFG-E8 increased the number of these membrane vesicle
secreted into the culture medium. These results suggest a
possible role of MFG-E8 in the membrane vesicle secretion,
such as budding or shedding of plasma membrane (micro-
vesicles) and exocytosis of endocytic multivesicular bodies
(exosomes).
Keywords: MFG-E8; membrane secretion; exosome; per-
ipheral membrane protein; milk fat globule membrane.
MFG-E8 (milk fat globule-EGF factor 8) was cloned and
characterized as mouse milk 53- and 66-kDa glycoproteins
peripherally associated with the membrane surrounding the
lipid droplets and being referred to as milk fat globule
membrane (MFGM) [1]. MFG-E8 consists of two repeated
EGF-like domains on the N-terminal side and of two
repeated C (discoidin-like) domains homologous to the C1
and C2 domains of blood coagulation factors V and VIII.
Orthologous proteins have been isolated in bovine
(MGP57/53 or PAS-6/7) [2,3], human (BA46 or lacta-
dherin) [4,5] and rat (rAGS) [6].
Though the expression of MFG-E8 is upregulated in
lactating mammary gland, MFG-E8 has also been detected
in various other tissues, including brain, lung, heart, kidney
and spleen in some mammals such as mouse, human and
bovine [7–9]. The mouse and bovine MFG-E8 proteins
expressed in mammary gland were shown to be composed
of two isoforms [3,9]. In mouse, a Pro/Thr-rich domain is
inserted possibly by a mammary gland-specific alternative
splicing between EGF-like and C-domains, resulting in the
production of a long form of MFG-E8 (MFG-E8-L) in the
lactating mammary gland. In contrast, a short form (MFG-
E8-S) lacking the Pro/Thr-rich domain is ubiquitously
expressed in various tissues [9].
The second EGF-like domain of MFG-E8 contains an
integrin-binding Arg-Gly-Asp (RGD) sequence motif [10],
which is conserved in all known MFG-E8 sequences of
several species and binds to some integrins. The avb5
integrin was affinity-purified from lactating bovine udder
extracts by using its specific binding to bovine milk
MFG-E8 [7], and human and bovine MFG-E8 proteins
promoted cell adhesion through avb3andavb5 integrins
[11, 12]. Although MFG-E8 contains no apparent hydro-
phobic transmembrane regions, MFG-E8 has been shown
to be a peripheral membrane protein and bind directly to
the MFGM and cell membrane [7,13–15]. Both the native
and recombinant MFG-E8 proteins bind in vitro to anionic
phospholipids, especially phosphatidylserine (PtdSer)
[7,12,16]. This PtdSer-binding of MFG-E8 has been
reported to depend only on the second C-domain
(C2-domain), but not the first C-domain (C1-domain),
in the same manner as that of blood coagulation factors
V and VIII [17–19].
Correspondence to T. Matsuda, Department of Applied Molecular
Biosciences, Graduate School of Bioagricultural Sciences, Nagoya
University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan.
Fax: + 81 52 789 4128, Tel.: + 81 52 789 4129,
E-mail: tmatsuda@agr.nagoya-u.ac.jp
Abbreviations: MFGM, milk fat globule membrane; DMEM,
Dulbecco’s modified Eagle’s serum; DAPI, 4¢,6-diamidine-2-phenyl-
indole-dihydrochloride; ECL, enhanced chemiluminescence; MVBs,
endocytic multivesicular bodies; GST, glutathione S-transferase.
(Received 19 September 2001, revised 17 December 2001, accepted 2
January 2002)
Eur. J. Biochem. 269, 1209–1218 (2002) ÓFEBS 2002