Reduction of annexin-V (placental anticoagulant protein-I)
on placental villi of women with antiphospholipid
antibodies and recurrent spontaneous abortion
Jacob H. Rand, MD, Xiao-Xuan Wu, MD, Seth Guller, PhD, Joan Gil, MD, Arabinda Guha, PhD,
Jonathan Scher, MD, and Charles J. Lockwood, MD
New York, New York
OBJECTIVE: The mechanism by which anti phospholipid antibodies are associated with pregnancy loss
and thromboembolic conditions has yet to be elucidated. Annexin-V, an anticoagulant
phospholipid-binding protein, is normally present in syncytiotrophoblasts lining the placental villi, where it
may playa role in the maintenance of intervillous blood fluidity. We therefore investigated the distribution
of annexin-V in placentas of patients with anti phospholipid antibodies in situ and then used short-term
villous cultures to study the direct effect of antiphospholipid antibodies on the immunolocation of
annexin-V.
STUDY DESIGN: We performed a blinded study by means of computerized morphometric analysis of
placental tissues that were stained for annexin-V with affinity-purified polyclonal antibody in an
avidin-biotin peroxidase system. The distribution of villous surface annexin-V on cross sections of
placentas of patients with antiphospholipid antibodies was compared with that of placentas from patients
with uncomplicated pregnancies, elective abortions, and pregnancy losses not associated with
anti phospholipid antibodies (n = 8 for each group). We quantitated villous surface annexin-V in cultured
placental villi that were incubated with antiphospholipid antibodies immunoglobulin G compared with
normal immunoglobulin G and measured annexin-V levels by enzyme-linked immunosorbent assay in
conditioned media and in the villi.
RESULTS: The mean villous surface annexin-V of the group with antiphospholipid antibodies was
26.2% ± 17% (SO) versus 93.9% ± 5.7% in the normal control group (p < 0.0001). Villi from patients
undergoing elective abortions and with pregnancy losses that were not attributed to anti phospholipid
antibodies also showed higher mean villous surface annexin-V levels (86.9% ± 10.6% and
83.5% ± 11.3%, respectively, p < 0.0001). Organ culture of normal placental villi with affinity-purified
immunoglobulin G from patients with antiphospholipid antibodies showed a dose-dependent decrease of
villous surface annexin-V over a concentration range of 1.5 IJ.g/ml to 1.5 mg/ml. Annexin-V concentrations
in conditioned media were significantly lower in the presence of anti phospholipid antibodies
immunoglobulin G compared with normal immunoglobulin G (49.4 ± 8.9 ng/gm wet weight vs
57.2 ± 11.5 ng/gm, respectively, p < 0.05). In contrast, the mean level of annexin-V in placental villi
incubated with anti phospholipid antibodies immunoglobulin G was greater than in villi incubated with
normal immunoglobulin G, 1328 ± 130 ng/gm wet weight versus 1183 ± 165 ng/gm (p < 0.02).
CONCLUSIONS: Patients with anti phospholipid antibodies and a history of previous pregnancy losses
have a significant reduction in annexin-V immunostaining on placental villous surfaces, and
antiphospholipid antibodies immunoglobulin G can directly decrease levels of villous surface annexin-V
on cultured placental villi. Assays of annexin-V in the conditioned media and cell pellets of cultured
placental villi suggest that the mechanism for antiphospholipid antibodies-mediated reduced annexin-V
surface staining is an inhibition of annexin-V transport to the villous surface rather than displacement by
anti phospholipid antibodies from the surface. This anti phospholipid antibodies-induced deficiency of
placental surface annexin-V may contribute to the placental thrombosis observed in these patients. (AM J
OBSTET GYNECOL 1994;171 :1566-72.)
Key words: Annexin-V, placental anticoagulant protein-I, placental villi, antiphospholipid
antibodies, recurrent spontaneous abortion, thrombosis, syncytiotrophoblast
From the Departments of Medicine; Obstetrics, Gynecology, and Repro-
ductive Science; and Pathology; Mount Sinai School of Medicine.
Presented in part at the Fourteenth Congress of the International
Society of Thrombosis and Haemostasis, July 7, 1993, and at the
Thirty-fifth Annual Meeting of the American Society of Hematology,
December 6, 1993.
Received for publication January 27, 1994; revised March 30,
1994; accepted July 13, 1994.
1566
Reprint requests: Jacob H. Rand, MD, Hematology Division, Box
1079, Mount Sinai School of Medicine, One Gustave Levy Place,
New York, NY 10029.
Copyright © 1994 by Mosby-Year Book, Inc.
0002-9378194 $3.00 + 0 6/1/59103