BIOLOGY

46, 328-334

REPRODUCTION

OF

(1992)

Human Endometrial Stromal Cells (CD) 13 Antigen/Aminopeptidase IUMITOSHI

Iivti,2’3

KARIYA,3

Department

MICHIYUKI

and

MAEDA,4

NOBUYUKI

EM!,3

KENJI

of Gynecology Kyoto

University,

and

Decidual Cells Express Cluster of Differentiation N and CD1O Antigen/Neutral Endopeptidase1

HIROSHI TAKAKURk,3

Obstetrics,3

54

Faculty Kawahara-cho,

FUJIWARA,3

NORIHIKO

HIDEHARU

KANZAKI,3

of Medicine,

and

OKAMOTO,3 and

Chest

Kyoto

Sakyo-ku,

MORI3

Research

Disease

606,

MASATOSHI

TAKAHIDE

Institute4

Japan

ABSTRACT With

specific

related

monoclonal

surface the

during

first

Indirect

trimester

of pregnancy

to aminopeptidase 93%

of

N and

the

enriched

examined

expressed

into

that

human

CD1O

activity

peptidase

and

was

on

detected

Human

endometrium

is composed

implantation ESC transform to play

of

an

origin

the fertilized into decidual

important

egg into cells (DC)

role(s)

of ESC

in the

and

DC is still

an other

increasing hemopoietic

dometrium

been

reported

whether ESC cells. By using

specific mouse and DC express

types

maintenance

in these

cell

we

and/or trimester

and

CD1O

antigen

the en-

were

Received

July

This

work

02857227,

supported

Japan and by the 1dorrespondence: rics,

Faculty

Shimizu Kimitoshi

of Medicine,

in part

by a Grant-in-Aid

the

Ministry

found that ESC (CD) 13 an-

shown

for

to be iden-

Scientific Science

Foundation Research Grant for 1990. lmai, M.D., Department of Gynecology Kvoto

University,

Sakyo.ku,

Kyoto

on

82cell-

stromal

on the

hydrolysis

606,

Research and

The was

peptidase activity also examined.

of

METHODS

prolapse deciduae

from

treatment

patients

who

of uterine

had

myoma

without hormonal therapy. were obtained from patients

First who

the date adjusted

ment

of the

of the last menstrual period and, by taking into account ultrasonic gestational

sac

and

fetal

if necessary, measure-

crown-rump

length.

1 shows

the

mouse

monoclonal

antibodies

used

tibody.

Indirect

frozen

(no.

Culture

obtained

for the

purchased from Becton Dickinson Immunocytometry Systems (Mountain View, CA). Fluorescein isothiocyanate (FITC)conjugated rabbit anti-mouse immunoglobulin (DAKOPAUS A/S, Glostrup, Denmark) was used as a second an-

and neutral enboth of which

of Education,

detected

legal abortions. Informed consent was obevery patient. Gestational age was calculated

from was

Immunofluorescence fresh

embedded

from

cells identical

in this study. My7 was purchased from Coulter Immunology (Hialeah, FL); MCS2, NU-Ni, NU-Ter, NTJ-B2, and Bear-i were purchased from Nichirei Co. (Tokyo, Japan), and LeuM3 was

1991.

03454396)

are

based

AND

were

hysterectomy

Table

with with

5, 1991.

was no,

Il,

which was

peptidases. suspension

cell

uterine human

The October

decidual

Antibodies

attempted

associated staining

3.4.11.2)[13] respectively,

function-

two

and

in endometrial

by an assay

endometria

had undergone tained from

stem is not

of studies on in the human

antibodies, we of differentiation

antigen,

3 antigen

cells

preparations

undergone

et al.

marrow that this

Here

CD1

examined

membrane-bound ESC-enriched

Human

of preg-

Kearns

number cells [8-121.

tical to aminopeptidase N (EC dopeptidase (EC 3.4.24.11)[14],

Accepted

analysis, the

CD1O

and

express cells

T&ues

through nutritional [11, [3] influences. reported on the surface of ESC and DC [4, 51, and

express antigens immunohistological

monoclonal both cluster

antigen

of

cells

stromal

MATERIALS

tigen and CD1O antigen. We also used flow cytometry to determine whether CD13 and CD1O antigens could be useful cell surface markers for ESC and DC in vitro. CD13

13 antigen

cytometric

75-93%

are the

the endometrium, and are considered

from bone evidence

the case. Recently, lymphocytes and to determine hemopoietic

of two

controversial.

[6] reported that DC are derived cells, but Fowlis et al. [7] provided

have

(CD)

decidual

and

endometrial

stromal cells (ESC) and endometrial The growth and differentiation of ESC of ovarian steroid hormones. After

nancy at the maternofetal interface endocrine [2], and immunological Only a few studies have been markers or functional parameters the

mainly

cells

both

alanine.

INTRODUCTION

of cells, endometrial glandular cells (EGC). are under the control

that

By flow

detected

was

stromal

revealed

of differentiation

respectively.

antigen

p-nitroaniline

endomethal

staining cluster

endopeptidase,

and

Furthermore,

of alanine-p-nitroanilide

found

immunofluorescence

neutral

cells,

preparations.

we

antibodies,

antigens.

tissue in OCT.

with

liquid

Staining

samples

were

compound nitrogen,

cut (Miles

and

kept

into Inc.,

small

pieces,

Elkhart,

at -80#{176}Cuntil

IN), sec-

tioning. Cryostat sections, about 6 tm thick, were air-dried and fixed with acetone at 20#{176}C for 5 mm. Nonspecific im-

of

-

and ObstetJapan.

munoglobulin 5% normal

FAX: 81-

75-761-3967.

328

binding was blocked rabbit serum in PBS (pH

by preincubation 7.4) for 15 mm.

with Excess

CD13 TABLE

1.

Monoclonal

antibodies

Antibody/CDa

used

MCS2/CD13 NU-N1/CD1O NU-B2/CD2O NU-Ter/CD2 Bear-1/CD11b LeuM3/CD14

as above neutral endopeptidase, Bgp135 sheep RBC receptor CR3, C3bi receptor, phosphoinositol-linked

serum

was

removed.

N

at an

first

antibody

appropriate

was

were Tokyo, replaced

on

Mac-i protein

ESC-enriched cell described elsewhere

suspension [23] with

cells

cALL,c

Dilution

granulocytes

natural keller macrophages

Subclass

1:40 1:40 1:40 1:10 1:40 1:10 1:10

cells

Reference

lgGl IgGi IgGi lgG2b IgGi IgGi lgG2b

15 15, 16 17 18 19 20, 21 21, 22

antigen.

The

sections

examined Japan). with

were

antibody three washes

then

FITC-conjugated another three For

incu-

in a moist with PBS, rabwashes

with a fluorescence negative controls,

normal

mouse

serum

dilution.

of ESC-Enriched

329

CELLS

leukemias

myeloid

the

endometria

with

scissors,

and

ring

in RPMI

1640

Cell Suspension was minor

prepared by a method modifications. Briefly,

FIG. 1. Indirect immunofluorescence staining of human as follows: a, MCS2/CD13; b, NU-Ni/CD1O; c, LeuM3/CD14; glands (G) are not (a,b). CD14 antigen-bearing cells, which dometrium Ic). The gland is elongated and slightly tortuous, Id). The black bar indicates 50 m. All pictures are enlarged

were

washed

incubated medium

times

in PBS,

at 37#{176}C with

three

continuous

(Flow

Laboratories,

minced

Irvine,

containing 1 mg/mI collagenase (Wako Pure Chemical dustries, LTD., Osaka, Japan), 0.005% deoxyribonuclease I (Sigma Chemical Company, St. Louis, MO), 100 U/mI icillin, 100 i.g/ml streptomycin (Flow Laboratories), and fetal calf serum (Flow RPM! 1640 medium, 1640

Preparation

STROMAL

hemopoietic

granulocytes,

as above lymphoid progenitor cells, B cells T cells granulocytes, monocytes, monocytes, granulocytes,

CALLAb

they were incubated for 30 mm with bit anti-mouse immunoglobulin. After sections (Nikon,

ENDOMETRIAL

reactivity

monocytes,

bated for 1 h with each monoclonal chamber at room temperature. After

the

HUMAN

in this study.

Cluster of differentiation antigen. bCommon acute lymphoblastic leukemia CCommon acute lymphoblastic leukemia.

the

ON

Main

aminopeptidase

with PBS, microscope

CD1O

Antigen

My7/CD13

rabbit

AND

medium,

and

Laboratories). the cells were ESC were

After three resuspended

separated

cell clumps by differential sedimentation bility of the cells was examined using exclusion test, and viability was always

from

stirUK) Intype pen10%

washes with in RPM! the

glandular

at 1 g. The viathe trypan blue dye greater than 95%.

endometrium in mid-proliferative phase using monoclonal antibodies. Tissues were stained d, hematoxylin and eosin. ESC are positively stained with CD13 and CD1O, but endometrial are considered to be tissue macrophages or granulocytes, are sparsely distributed in the enand the spindle-shaped ESC possess little cytoplasm, giving the appearance of naked nuclei equally.

330

IMAI

FIG. 2. Indirect stained as follows: endometrial glands gland is convoluted

Flow

Cytometric

A pellet ice with

immunofluorescence staining of human endometrium in secretory phase (cycle date 24) using monoclonal a, MCS2/CD13; b, NU-N1/CD1O; C, Bear-1/CD11b; d, hematoxylin and eosin. ESC are positively stained (G) are not (a,b). CD11b antigen-bearing cells are sparsely distributed Ic). The cytoplasm of ESC is enlarged (d). The black bar indicates 50 m. All pictures are enlarged equally.

of ESC-Enriched

Analysis

of 5 x

i05

cells

10 .tl of undiluted

was

incubated

primary

antibody

Preparation for

30 mm

listed

on

in Table

1. After two washes with Hanks’ solution containing 0.1% BSA (Sigma Chemical Company) and 0.1% NaN3, the cells were incubated for 30 mm with FITC-conjugated rabbit antimouse immunoglobulin on ice in the dark. The cells were then washed three times and suspended in Hanks’ solution to be analyzed by flow cytometry (FACscan, Becton Dickinson were

Immunocytometly stained with only

the first antibody was ulosa cell monoclonal published

results).

sity of the

endometria,

for each

Assay

prewarmed PBS (Merck, Darmstadt,

examined enzymatically of alanine-p-nitroanilide [24]. The ESC-enriched times with PBS and

containing Germany).

0.4

by a method into p-nicell suspenresuspended in

mM alanine-p-nitroanilide The incubation was carried

out in a water bath, with gende agitation, 37#{176}C. The reaction was stopped by addition

for 20 mm at of ice-cold 1.0

Japan).

Giken,

with The

cells den-

a specamount

by a standard

curve.

menstrual

cycles,

RESULTS

pausal

analyzed

examined

Tokyo,

formed was determined done in duplicate.

yr of age, of gestation,

were

4.2), and the The optical

nm was

of p-nitroanilmne All assays were

35-48 12 wk

cells

at 385

(Union

Endometria

secretory the basal ing

Staining

Immunofluorescence

in secretory and CD1O

and alanmne washed three

supernatant

replaced by mouse anti-porcine granantibodies (Fujiwara H. et al., un3000

antibodies. Tissues were with CD13 and CD1O, but and eosinophilic, and the

acid buffer (pH by centrifugation.

trophotometer

Indirect

At least

Peptidase activity was based on the hydrolysis troaniline sion was

M sodium acetate-acetic were rapidly removed

cells or

Systems). As negative controls, FITC-conjugated second antibody

sample. Enzyme

ET AL.

of 13 women and

7 were

phase. antigens

with

in proliferative

ESC, but not in proliferative

phase (Fig. 2a,b) layer also expressed

CDI1b

or

CD14

rophages

or

endometria hum and

(Figs. ic myometrium

granulocytes,

antigens (data not nancy, DC, which with round nuclei,

normal

deciduae from 11 women, were examined. Among the

of the menstrual both antigens.

antigens, were

phase,

EGC, expressed phase (Fig.

probably observed

and 2c). Endometrial were negative for

at 6 and premenoand

6 were

both CD13 la,b) and in cycle. ESC in Cells express-

monocytes/macsparsely

in the

surface epitheCD13 and CD1O

shown). In the first trimester of pregare identified as large, polygonal cells expressed both CD13 and CD1O anti-

CD13

AND

CD1O

ON

HUMAN

ENDOMETRIAL

STROMAL

FIG. 3. Indirect immnofluorescence staining of human decidua of 7 wk gestation. Tissues c, Bear-i /CD11b; d, hematoxylin and eosin. All pictures are enlarged equally. DC are positively antigen seems weak (a,b). The glands (G) are negative for CD13 antigens. Sparsely distributed the large and polygonal DC Id). The black bar indicates 50 p.m.

gens

(Fig.

3a,b).

the expression whereas that parison with secretory

Judging

from

the

fluorescence

intensity,

of the CDIO antigen on DC appeared weak of the CD13 antigen appeared strong in comantigen expression on ESC in proliferative or

phase.

The

glands

in the

decidua

expressed

ther CD13 nor CD1O antigens. The cells expressing or CD14 antigens were observed sparsely in the and they could be large DC (Fig. 3c). CD2 antigen-bearing

distinguished cells,

antigen-bearing

cells,

served

in both

sparsely

likely

from likely

the

and

CD11b and

Peptidase

were

immunoglobulmn,

Actimy

of the ESC-Enriched

amount

ofp-nitroanihmne

to the

number

of ESC

lation lated

also

ob-

0.994)

(data

not

coefficient: r to the incubation (data

not

Cytometric

The

Analysis

ESC-enriched

endometria secretory CD13

or

cell

women,

39-48

suspension

from

yr of age,

were

10

tact and

normally

analyzed.

Three

were in late proliferative phase, and 7 were in phase. No difference was observed between phases.

antigen and

fluorescence 4). CD1Ib, less than CD2

not

bind

antisame to

the

=

(from 0.998; time

Cell Suspension

formed 0.5

x

was 106

linearly

to 4 x

related

106;

corre-

Fig. 5. It was also linearly rebetween 5 and 60 mm (r =

DISCUSSION

menstruating

cells,

did

mouse to the

shown).

shown).

Flow

by the fact that which belong

of murine

The

CD2O

and

deciduae

was excluded cell antibodies,

nei-

polygonal

B lymphocytes,

were stained as follows: a, MCS2/CD13; b, NU-N1/CD1O; stained with C013 and CD1O, but the expression of CD1O CDilb antigen-bearing cells (c) can be distinguished from

to ESC granulosa

subclass ESC.

deciduae

T lymphocytes,

endometria

tibodies porcine

331

CELLS

CD1O

was

detected

antigen

was

on detected

82-93%

of the

on 75-93%.

examined Their

intensity seemed to be relatively strong CD14, CD2, or CD2O antigens were positive 10% of the examined cells (data not shown CD2O).

Nonspecific

binding

of CD13

and

CDIO

mean (Fig. on for an-

ESC and their direct descendants, DC, keep direct conwith semiallogeneic fetal antigens during pregnancy, are considered to play a very important role(s) in suc-

cessful pregnancy. There is no distinct functional parameter for ESC/DC, and only a few surface markers for ESC and DC have been reported [4, 5]. Therefore, with CD-series monoclonal antibodies, we attempted to determine whether ESC

and

DC

express

hemopoietic

cell-associated

and found that ESC and DC expressed nopeptidase N and CD1O antigen/neutral It is well established that lymphocytes, macrophages

are

distributed

in the

antigens

CD13 antigen/amiendopeptidase. granulocytes, and human

endometrium

332

IMAI

EF

AL.

400

a

FLI

FLI

FLI

U 400

400

TTT..,0

#{149}

0

ie FL

I

FL

Fluorescence FIG. 4. Flow cytometric analysis of stained as follows: a, a second antibody CD11b. Percent positivity was as follows:

Ie

I

o2 FL

io2

i#{248}

I

intensity

human ESC-enriched preparation from the endometrium in late-proliferative phase (cycle date 14). Cells were only as one of the negative controls; b, My7/CD13; c, MCS2/CD13; d, NU-N1/CD1O; e, LeuM3/CD14; f, Bear-li a, 2.1; b, 92.8; c, 93.1; d, 92.2; e, 3.9; f, 3.3. Over 90% of the cells were positive for CD13 and CD1O antigens.

C a) C C

(‘S 0 I-

z

& 1

2

No.

of

FIG. 5. Assay of peptidase activity of ESC-enriched (cycle date 23). The amount of p-nitroaniline hydrolyzed of ESC. Incubation time: 20 mm.

4

3

celis(x106) preparation from the from alanine-p-nitroanilide

endometrium is linearly

in mid-secretory related to the

phase number

CD13

and

decidua.

Using

specific

AND

monoclonal

that

ESC

and

DC

ON

antibodies,

be identified immunohistochemically tometry [12]. Our immunohistological clearly

CD1O

ENDOMETRIAL

HUMAN

they

can

18-111 or by flow cyfindings showed

express

both

CD13

and

CD1O

an-

tigens. Although CD13 and CD1O antigens are also expressed on granulocytes, monocytes and lymphoid cells [1517], these cells could be distinguished from ESC and DC with other specific CD11b, and CD14 ings on these works [8-12]. Judging

cell surface markers, such as CD2, antigens. Our immunohistological

hemopoietic from

the

cells

were

fluorescence

consistent

antigen

appeared that

to become

molecules expression

should

be

after

ascertained

by

CD13 antigen that of CD1O

a more

cytometric

analysis,

CD13

This

quantitative

antigen

Their

fluorescence that

intensity

CD13

and

was

CD1O

was

cells antigen

antigens

detected

in the ESC-enon more than

relatively

strong.

can

be

This

useful

cell surface markers for ESC. CD13 antigen has been shown to be identical nopeptidase N (EC 3.4.11.2) [13]. Ammnopeptidase integral, single-chain membrane glycoprotein that

of these

by ammnopeptidase ample, met-enkephalin,

der

intensively

membrane

on [25].

the

This

intestinal antigen

ulocytes, monocytes, myeloid [15, 16]. It is an ectoenzyme, on cell surface tive peptides,

and is also

kidney expressed

several

secretory

endometrium,

in

vitro

trimester dopeptidase

to amiN is an has been brush

on gran-

nm, tides

oxytocin,

enzyme activity.

1 (IL-i) [27]. and CD1O antigens are or not as ESC-enriched

activity in vitro, and found This does not necessarily

themselves

have

peptidase

activity

as enkephahins,

bradyki-

peptidases, we cell suspension

examhad

enzyme

The

authors

the flow

in the

female

genital

tract,

and

their

roles

has

day of the of human

secretion

[31]. In addition, to affect the

by

first

neutral immune

ensys-

successful

implantation

and

maintenance

may be useful for assessing en-

role(s)

of these

en-

wish

have

to thank

ytometric

Ms. Yumiko

been

Tomita

for

her

assistance

with

technical

analysis.

REFERENCES I. Krehbiel

RI-I. Cytochemical

pregnancy

of the decidual

studies

in the

and

production

reaction

of deciduomata.

in the

Physiol

early

rat during

Zool

1937;

10:212-

235. 2. Riddick AmJ

DH,

Kusmik

Obstet

TG,

human

PlC Suppression

Lala

Cell

S, Asano

M, Parhar

RS, Lala

monoclonal

of amniotic

S, Kano

1988;

fluid

prolactin.

J

on

Reprod

endometnial

Immunol

cell-specific

and

tissue

by early

alloreacuvity

116:392-410.

K. Studies

PK. Decidual

antobodies:

of lymphocyte

Immunol

antibodies.

by monoclonal

source

127:187-190.

decidua.

E., Mon

5. Kearns by

1977;

ItS, Kennedy

a possible

Decidua:

WF.

Gynecol

pregnancy

in human

10:1-14.

recognized J Immunol 1985;

surface

species

cells

1987; antigen(s)

distribution.

135:1046-1052. 6. Kearns,

M, Lala

dopregnant

PK. Bone

mouse

7. Powlis

DJ,

marrow.

Ansell

JD.

BR, Isaacson

11.

13.

Tabibzadeh Starkey

PM,

nancy

decidua: cytometty.

Look

Immunology

AT, Ashmun

glycoprotein

RA, Shapiro

CDI3

83:1299-1307. 14. Letarte M, Vera 1988;

cycle.

(gplSO)

5, Iran

leukemia

168:1247-1253.

of

in the

pseu.

from

bone

1988;

of leukocytic

Cell

evidence cells

in

Metab

populations

of large

isolation

of the

decidual

in early

J Pathol

lymphoid

sub-

127:66-73.

epithelium

Endocrinol

CWG.

and

human

that

1987;

leupreg-

endometrial

153:281-288.

human

endometrium

70:437-443. in human early preggranular lymphocytes by 1990;

65:129-134.

LI-I, Peiper

SC. Human

myeloid

to aminopeptidase.

is identical

R, AddisJBL, antigen

derived

characterization gland

J Clin

characterization

flow

1987;

lymphocytes.

IL, Redman

Sargent

not

distribution Pathol

A. Immunocytochemical activity

menstrual

are

cells

J

Am

are granulated

S. Proliferative the

lymphocytic

decidual

immunocvtochemical

D, Ritson

precursors

39:445-446.

endometrium.

granulocytes

cell

155:1537-1554.

PM. Immunohistological

throughout 12.

1982;

related to endometrial 1985; 55:35-44.

Hollings

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Med that

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infiltrate Immunology

BulmerJN,

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Evidence

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9. BulmerJN,Johnson

10.

marrow

uterus.

Transplantation

populations

ac-

tivity in vitro may be due to peptidase(s)-bearing cells, such as macrophages, but suggests that peptides could be degraded locally by the cells in the human endometrium. Some biologically active peptides are known to be present

expression

hCG

dometrial function. The physiological zymes remains to be clarified.

8. Kamat

pepand

that it had peptidase indicate that the ESC the

stimulates

trophoblasts been reported

to the

cocytic nancy.

because

mRNA

of pregnancy. Furthermore, these enzymes as surface markers and as new parameters

3. Parhar

so forth [17]. at the amino

substance P, neurotensin, chemotactic (fMet-Leu-Phe), gastrin, atrial natriuretic peptide,

interleukmn As CD13 ined whether

IL-113

in humans by degrading IL-i [32]. Taken together, ammnopeptidase N and neutral endopeptidase, located on the surface of ESC and DC, may modulate the metabolism of biologically active peptides and may

4. Nakayama

such

locally For exby both

tem

ac-

CD1O antigen has been shown to be identical to neutral endopeptidase (EC 3.4.21.11) [14], and is also an integral membrane protein, expressed on lymphoid progenitor cells, acute lymphocytic leukemia cells, subsets of B lymphocytes,

residues,

degraded

after the twenty-third inhibits decidualization

and

bor-

hin [26].

of hydrophobic

and

[30]

human has

gestational

side

be

ACKNOWLEDGMENTS

biologically and met-enkepha-

renal glomeruhi, and tubular epithehium, and It is also an ectoenzyme and leaves peptides

may

neutral endopeptidase. which can be degraded

in

leukemic cells, and so forth which exposes its catalytic site

[25], and hydrolyzes such as met-lys-bradykinmn

peptides

N or

vitro

studied

333

peptidases, is present in the uterine fluid of fertile women, and its role as an immunomodulator has been suggested [28]. IL-113, which can be degraded by neutral endopeptidase, has been shown to be present in the first trimester human deciduae more abundantly than in proliferative and

ESC

immu-

decidualization.

Some

CELLS

been reported to appear menstrual cycle [29]. IL-i

other

be differentiation-related this change in antigen

on more than 82% of the examined riched cell suspension, and CD1O indicates

the

studied.

contribute

method. By flow

75%.

of

of the whereas

weak

these antigens might of ESC/DC. However,

suggests

with

intensity

nohistological staining, the expression on ESC appeared to become strong

CD2O, find-

STROMAL

Onizuka

is identical

RJ, Quackenbush to

neutral

plasma N.J

Clin

membrane Invest

EJ. Common

endopeptidase

J. Exp

1989; acute Med

334 15.

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Gadd

S. Cluster

Schmidt Cell

In:

dem

Borne

Antigens.

Knapp

W,

AEGKr

Oxford,

New

DOrken (eds.),

B, Gilks Leucocyte

York, Tokyo:

WIt,

Rieber

Typing

Oxford

EP,

man

University

HG,

antibody

17. I)flrkcn

Sagawa

K, Menon

MCS-2 Jpn

J Cancer

In:

Knapp

routine

Res

13, N1fllkr’ P, Ik/JLtIIi) 0)10,

M, MinowadaJ.

in the

(Gann)

‘Pan-myeloid”

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neutral endopeptidase.

With specific monoclonal antibodies, we found that human endometrial stromal cells and decidual cells express two function-related surface antigens. I...
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