[CANCER RESEARCH 47, 2763-2766, June 1, 1987]
Presence of Cytidine S'-Monophospho-TV-acetylneuraminic Acid:Gal/21-
3GalNAc-R a(2-3)-Sialyltransferase in Normal Human Leukocytes and
Increased Activity of This Enzyme in Granulocytes from Chronic
Myelogenous Leukemia Patients1
M. A. Baker,2 A. Kanani, I. Brockhausen, H. Schachter, A. Hindenburg, and R. N. Taub
Department of Medicine, Toronto General Hospital, University of Toronto, Tarato, Ontario, M5G IL7 fM. A, B., A. K.J, the Department of Biochemistry, University of
Toronto, and the Research Institute, Hospital for Sick Children, Toronto, Ontario, M5G 1X8 [I. B., H. SJ, and the Department of Medicine, Columbia University,
New York, New York 10032
ABSTRACT
We have examined granulocytes from patients with chronic myeloge-
nous leukemia (CML) and from normal subjects to determine whether
activity of a specific sialyltransferase might account for the aberrant
sialylation of CMinked membrane oligosaccharides in CML cells. Total
membrane preparations of morphologically mature CML and normal
granulocytes were tested for sialyltransferase activity using the substrates
galactosy!-/31-3-A'-acetyl-D-galactosamine-a-O-nitrophenyl and A'-ace-
tyl-D-galactosamine-a-phenyl. W-Acetyl-D-galactosamine-a-phenyl was
not an acceptor with either CML or normal cells. With galactosyl-j81-3-
Af-acetyl-D-galactosamine-a-O-nitrophenyl, sialyltransferase activity was
2.8 times higher in CML cells compared to normal cells. Product iden
tification by high performance liquid chromatography showed that en
zyme from both normal and CML granulocytes linked sialic acid to
galactosyl-fll-S-AT-acetyl-D-galactosamine-R by the o(2-3) and not the
a(2-f>) linkage. The enzyme CMP-/V-acetylneuraminic acid: galactosyl-
01-3-,/V-acetyl-D-galactosamine-R a(2-3)-sialyltransferase has not pre
viously been described in human granulocytes. The marked increase in
activity of this enzyme in CML and the resulting increase in sialylation
may contribute to the pathophysiological behavior of CML granulocytes.
INTRODUCTION
Chronic myelogenous leukemia is characterized by inappro
priate early release of immature granulocyte precursors from
the bone marrow and by a major delay of exit of mature
granulocytes from the blood into the tissues (1). CML3 granu
locytes show a marked decrease in binding to PNA when
compared to normal granulocytes; they are less adhesive to
nylon wool (2) than normal cells; their cell membranes show
decreased labeling after treatment with galactose oxidase-
NaB3H4 and increased labeling after sodium periodate-NaB3H4
treatment (3). All these effects can be partially or completely
reversed by treatment with Vibrio cholera neuraminidase. These
studies suggest that the cell surface oligosaccharides are more
fully sialylated in CML cells and this may account in part for
Received 8/25/86; revised 12/22/86; accepted 2/18/87.
The costs of publication of this article were defrayed in part by the payment
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1This research was supported by Medical Research Council of Canada Grant
MT-3285 to H. S., by National Cancer Institute (United States) Grants CA 31761
and CA 37162, a grant from the William J. Matheson Foundation to R. N. T.
and A. H., and by National Cancer Institute of Canada and Medical Research
Council of Canada Grants to M. A. B. M. A. B. is a Research Associate of the
Ontario Cancer Treatment and Research Foundation. A. H. is a Fellow of the
Leukemia Society of America. I. B. did this work while holding a Canadian Cystic
Fibrosis Foundation Studentship.
2To whom requests for reprints should be addressed, at Toronto General
Hospital, Mulock Larkin Wing 1-005, Toronto, Ontario M5G 1L7, Toronto,
Ontario, Canada.
3 The abbreviations used are: CML, chronic myelogenous leukemia; Gal, r>-
galactose; GalNAc, W-acetyl-D-galactosamine; GalNAcOH, JV-acetylgalactosa-
minitol; NANA, /V-acetylneuraminic acid; PNA, peanut agglutinin; HPLC, high
performance liquid chromatography, Gal/31-3GalNAc, galactosyl-/31-3-Ar-acetyl-
D-galactosamine; NeuAc, JV-acetylneuraminic acid; FMLP, formyl-methionine-
leucine-phenylalanine.
the pathophysiological behavior of the circulating cells. The
aberrant sialylation involves the major granulocyte glycoprotein
with a molecular weight of 150,000 which has been shown to
be important for granulocyte adhesion (4,5). CML granulocytes
show decreased binding of the synthetic chemotactic peptide
FMLP (6).
Sialylation of glycoproteins is effected by sialyltransferases
specific to the structure of the substrate (Table 1; Ref. 7). Two
enzymes are known to transfer sialic acid from CMP-NANA
to Gal/31-3GalNAc-R: (a) CMP-NANA:Gal/31-3-GalNAc-R
a(2-3)-sialyltransferase (sialic acid to galactose) (EC 2.4.99.4),
where R can be polypeptide or a nitrophenyl group, and (h)
CMP-NANA:R,/31-3GalNAc-R2 a(2-6)-sialyltransferase I
(sialic acid to ./V-acetylgalactosamine (EC 2.4.99.3), where RI
can be H-, Gal-, or sialyla2-3Gal-and R2 must be a polypeptide.
The «3-sialyltransferase has been reported in rat, porcine and
fetal calf liver, human placenta, and porcine and ovine submax-
illary glands (8-12). The a6-sialyltransferase I has been found
in the submaxillary glands of several species (9, 11, 13-16).
The structures formed by these enzymes, sialyla-2-3-GaljSl-
3GalNAc- and Galj81-3(sialyla2-6)GalNAc-, respectively, have
been detected on many mucins and on glycoproteins such as
antifreeze glycoprotein, RBC glycophorins, etc. (7). Addition
ally, a third sialyltransferase has been described which acts
on O-glycosyl oligosaccharides. This enzyme, CMP-NANA:si-
alyla2-3Galj31-3GalNAc-R a(2-6)-sialyltransferase II, also
transfers a residue of sialic acid to W-acetylgalactosamine (EC
2.4.99.7); R can be a polypeptide or a nitrophenyl group (10,
14). This enzyme has been found in fetal calf liver, but is
probably quite widely distributed (10, 14). It can act neither on
Gal,81-3GalNAc-R nor on GalNAc-R.
In a previous study (17) we compared the sialyltransferase
activities of membranes prepared from CML granulocytes that
appeared mature by microscopic criteria and from normal gran
ulocytes of identical morphology. The CML preparations
showed significantly higher sialyltransferase activities toward
asialofetuin, asialo fucose-free blood group A-negative porcine
submaxillary mucin and antifreeze glycoprotein, all of which
are known to contain appreciable amounts of O-linked Gal/31-
3GalNAc oligosaccharides. Asialo-ovine submaxillary mucin,
which contains mainly O-linked GalNAc residues and only a
small amount of Galj81-3GalNAc, was a poor sialyltransferase
substrate with either normal or CML cells. There was no
significant difference in sialyltransferase activity between CML
and normal cells when asialo-o, acid glycoprotein was used as
an acceptor; this substrate contains only TV-linked oligosaccha
rides with terminal Gal residues. These observations suggested
that the increased sialyltransferase activity in CML cells was
acting on O-linked Gal|81-3GalNAc groups.
The present studies were carried out to prove this hypothesis
and to establish the nature of the sialic acid linkage to Gal/31-
2763
Research.
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