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Mesonephric excretory function related to its influence on differentiation of fetal gonads.

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THE ANATOMICAL RECORD 210:551-556 (1984)
Mesonephric Excretory Function Related to its influence on
Differentiation of Fetal Gonads
The Finsen Laboratory, The Finsen Institute, DK-2100Copenhagen (J.G.)
and Department of Obstetrics and Gynecology, Hvidovre University
Hospital, DK-2650 Huidovre (L.A.),Denmark
The mammalian intermediate fetal kidney, the mesonephros,
is known in different species to excrete body waste products during a limited
period of fetal life. Recently, the mesonephros and its derivatives have been
shown to influence gonadal functions in several ways. Thus, the mesonephric
cells are responsible for regulating the onset of meiosis in different mammals
by the secretion of two substances, a meiosis-inducing substance (MIS) and a
meiosis-preventing substance (MPS).
In this paper, the relation between mesonephric kidney function and its
influence on the gonads is reviewed through literature studies. It seems that
cessation of mesonephric excretion precedes onset of meiosis in the ovary in
different species.
It is suggested that the mesonephric renal function interferes with synthesis
and/or secretion of MIS or that the excreted products may interfere with the
responsiveness to MIS of the germ cells.
The influence of the intermediate fetal kidney, the mesonephros on the gonads, has
gained much attention during the last
It has been shown that the mesonephros
and its derivatives influence the developing
gonads in the following ways (for review, see
Grinsted and Fajer, 1983):
1) The mesonephros donates cells to the
embryonic gonadal anlage in both sexes.
2) The mesonephros secretes substances
that influence the onset of meiosis in
3) The mesonephros influences gonadal sex
differentiation in mice in vitro.
4)The mesonephros influences gonadal sex
steroid production in fetal and neonatal rabbit gonads.
The mesonephros is known to be a fetal
excretory organ in several species (a fetal
kidney), a function that we have reviewed in
relation to the mesonephric influence on the
Point 1
Through electron microscopic evaluations,
it has been shown in sheep and in mice that
in the male, the mesonephric cells are inti-
0 1984 ALAN R. LISS, INC.
mately connected to the developing seminiferous cords of the testis. It is thus believed
that the Sertoli cells are mesonephric in origin (Zamboni et al., 1981; Upadhyay et al.,
In culture experiments, we have measured
the amounts of sex steroids in culture media
of rabbit testes grown alone and in media of
testes grown with attached mesonephric tissue. These studies also indicated that the
steroid-producing Leydig cells could be of mesonephric origin, since only the youngest
testes, grown with the mesonephros, developed with adequate numbers of Leydig cells
and with adequate steroid production in vitro
(Grinsted et al., 1982).
In the female mouse, the granulosa cells of
the follicular wall are shown to be of mesonephric origin: in experiments with cultures
of fetal ovaries with and without attached
mesonephric tissue, only the ovaries cultured
with the mesonephros develop follicles in culture (Byskov and Lintern-Moore, 1973; Byskov et al., 1977). Electron microscopic
examinations support these experimental
findings: a direct connection between the meReceived December 30, 1983; accepted July 13,1984.
TABLE I . List of tissues of different mammalian species in which MIS and MPS effect has been shown
Fetal mouse ovary
Fetal and neonatal hamster ovary
Rete ovarii of hamster before ovarian onset
of meiosis
Rete ovarii of hamster after ovarian onset
of meiosis
Follicular fluid of preovulatory human
Fetal mouse testis
Fetal mouse rete testis and epididymis
Fetal human testis
Fetal human epididymis
Pubertal mouse testis
Pubertal mouse rete testis and epididymis
Pubertal bull testis
Pubertal bull rete testis and epididymis
Adult human testis
Adult human epididymis
Adult rat testis
sonephric structures and the cells forming
the follicular wall has been demonstrated in
mice and sheep (Zamboni et al., 1979; Upadhyay et al., 1979). An influence, however,
by the surface epithelium on the gonadal
development cannot be excluded, as shown
by autoradiography. At the time when the
basement membrane of the surface epithelium becomes discontinuous, marked cells of
this epithelium are found in the gonadal
stroma in fetal rats (Merchant-Larios, 1979).
To what extent the cells of the developing
gonads are derived from the mesonephros or
the surface epithelium is not yet completely
Byskov and Saxen, 1976
0 and Baker, 1976
Fajer et al., 1979
Fajer et al., 1979
Fajer et al., 1979
Yding-Andersen et al., 1981c
Westergaard et al., 1984
Byskov, 1978a
Byskov, 1978a
Grinsted and Byskov, 1981
Grinsted and Byskov, 1981
Grinsted et al., 1979
Grinsted et al., 1979
Grinsted et al., 1979
Grinsted et al., 1979
Grinsted and Byskov, 1981
Grinsted and Byskov, 1981
Parvinen et al.. 1982
MIS is probably a substance closely related
to steroids. MPS is a substance with the biochemical characteristics of a polypeptide,
possessing a molecular weight of more than
5,000 daltons (Yding Andersen et al., 1981
Point 3
In cultures of differentiating embryonic
mice gonads, grown with and without attached mesonephric tissue, the gonads of sexually undifferentiated male fetuses become
feminized, i.e., develop into ovarianlike structures, if they are cultured in the presence of
mesonephric tissue.
The control group of male gonads cultured
Point 2
without mesonephric tissue develop norIn culture it has been shown that the me- mally in the masculine way (Byskov and
sonephros and its derivatives secrete at least Grinsted, 1981).
From these experiments, we concluded that
two substances in vitro: 1)A meiosis-inducing substance (MIS), able to trigger undiffer- the mesonephros influences the gonadal sex
entiated fetal mouse and hamster germ cells differentiation in a feminine direction, in
to enter the meiotic prophase; and 2) a vitro.
meiosis-preventing substance (MPS), able to
Point 4
prevent the germ cells from entering meiosis.
in the media of coculThe tissues in which activity of MIS and
MPS has been shown in vitro are listed in tures from fetal rabbit gonads with attached
mesonephros has been compared to the meTable 1.
An indication of the presence of MIS in dia from gonads cultured alone. From these
vivo has been shown histologically: within a experiments it is concluded that the male
short period, germ cells of the fetal mouse and the female mesonephros influence the
testis have been found in meiotic prophase steroid content differently (Grinsted, 1982).
In the male, the mesonephros cannot sewhen situated outside the testicular cords,
but close to the MIS-secreting, developing crete steroids but may decrease the amount
of testosterone secreted by the testis cultured
epididymis (Byskov, 1978b).
with the mesonephros. The young and prim- composition of the excretion is hypotonic, owitive sex-differentiating male gonads are de- ing to low sodium and chloride content, but
pendent on the presence of the mesonephros, has a high content of urea and potassium
morphologically as well as endocrinologi- (Davies and Routh, 1957). Morphological evically (Grinsted et al, 1982).
dence of a n endocrine function of the mesoIn the female, the mesonephros of the fetal nephros, like the secretion of renin from the
rabbit secretes sex steroids into the culture juxtaglomerular complex of the metanemedia. In addition, it is able to lower as well phros, has been found only in pig and rat
as increase gonadel sex steroids in the media (Kaplan and Friedman, 1942; Sutherland and
of the cocultures, at different stages. Before Hartroft, 1968), but not in man (De Martino
meiosis is initiated, the steroid content is and Zamboni, 1966; Cotrutz et al., 1971;
lowered by the mesonephros. After meiosis is Koga, 19721, cat or sheep (Tiedemann, 1976).
initiated after birth (at day 3 postpartum) the
mesonephros increases estradiol content in
media of the cocultures. The mesonephric inORGANIZING ACTION
fluence on the ovarian steroid production is
thus altered simultaneously with onset of
In Table 2, cessation of mesonephric excremeiosis in the ovary (at the first day after tory capacity and regression and onset of ovarbirth). It is suggested that MIS secretion by ian meiosis are given in the species in which
the mesonephric cells is associated with the these functions presently are described.
mesonephric influence on the gonadal steroid
The species listed in Table 2 are arranged
production (Grinsted, 1982).
according to the evolutionary size of their
mesonephroi (Bremer, 1916; Gersh, 1937;
Davies, 1952; Shumkina, 1960; Tiedemann,
The mesonephros has been termed “the
The largest mesonephroi develop in species
principal excretory organ in embryonic life” in which sexual differentiation precedes the
(Patten and Carlson, 19741, although it devel- onset of meiosis in the ovary (termed “species
ops unevenly in different species (reviewed with delayed type of meiosis,” e.g., pig, sheep,
recently in Tiedemann, 1976).In species with and rabbit [Byskov, 19791). In animals in
prominent mesonephroi, numerous nephrons which the mesonephric anlage is small, the
exist. Each nephron consists of a glomerulus, gonads differentiate sexually almost simula glomerular capsule, a proximal and a dis- taneously with appearance of meiotic germ
tal tubule, and a collecting duct. The loop of cells in the ovary (termed “species with imHenle, which is present in the permanent mediate type of meiosis,” e.g., man, rat and
kidney, the metanephros, is always absent in mouse [Byskov, 19791).
the mammalian mesonephros (Tiedemann,
It seems that onset of meiosis in the ovary,
1979).In species with small mesonephroi, the and thereby probably MIS secretion, is corexcretory apparatus may be underdeveloped related with cessation of mesonephric excreor completely missing (Bremer, 1916; Tiede- tory capacity and regression (Table 2).
mann, 1979). Bremer (1916) has listed the
No correlation could be demonstrated
mesonephros according to decreasing size in through the literature between mesonephric
different species as follows: pig, sheep, cat, regression and the other mesonephric influrabbit, guinea pig, man, rat and mouse.
ence on the gonads. It is shown in vitro, howThe excretory function has been correlated ever, that mesonephric influence on the
to the developmental stage and type of pla- gonadal steroid secretion changes, when
centation (Bremer, 1916; Davies, 1952; Ham- meiotic cells appear in the ovary (Grinsted,
ilton et al., 1972). In species with a more 1982).
primitive type of placentation (epitheliochorIn cultures of undifferentiated fetal mouse
ial or endochorial), the mesonephros is said gonads and parts of adult kidney tissue, exto possess excretory capacity, whereas in spe- tensive degeneration of the germ cells take
cies with a more developed placentation type place and meiotic cells do not appear in the
(hemochorial) only small and nonfunctional fetal gonads of both sexes in a n experiment
mesonephroi are formed. The onset of func- (Grinsted and Byskov, not published) carried
tional excretory capacity occurs when the out like the previous studies (see Grinsted
mesonephric tubules differentiate into proxi- and Byskov, 1981).This observation supports
mal and distal portions (Davies, 1952). The the hypothesis of a n inhibiting influence by
TABLE 2. Period
mesonephric degeneration and onset of meiosis in the ouary of different species
Excretory function
Guinea pig
First appearance
of meiotic germ
Additional literature
concerning mesonephric
secretion and regression
1-2 ( P . P . ) ~ , ~ ~
5, 9
9, 13
1, 14, 18
1, 9, 24, 30
17- 184341
'Days post coitum or post partum (p.p.1.
The species are arranged according to decreasing evolutionary size of the mesonephros. The periods in which the mesonephros
possesses excretory capacity and regresses and the age at which the first meiotic germ cells are seen in the ovary are given in the
table. The length of gestations are calculated in days post coitum according to Evans and Sack (19731, or Streeter (19211, if not given
by the authors. The authors referred to are given below:
1. Gersh, 1937.
MacCallum, 1902.
Black and Erickson. 1968
Mauleon, 1969.
Weber, 1897.
Mihalkovics, 1885.
Stanier, 1960.
Sutherland and Hartroft, 1968
Tiedemann, 1976.
10. Shumkina, 1960.
11. Davies, 1952.
12. Davies and Davies, 1950.
13. Bremer, 1915.
14. Bremer, 1916.
15. Davies. 1951.
Erickson, 1966.
Winiwarter and Sainmont, 1909.
Fraser, 1920.
Davies and Routh, 1957
Bernier and Beaumont, 1964.
Leeson and Baxter, 1957.
Giannelli, 1925.
Peters et al., 1965.
von Kolliker, 1879.
Leeson, 1957.
Leeson, 1959.
Leeson, 1960.
Strauser, 1928.
Tiedemann, 1979.
30. Tiedemann and Wettstein, 1980.
kidney tissue on undifferentiated germ cells,
although this particular experiment was carried out with tissues of the permanent kidney, the metanephros and not the mesonephros .
Thus, it is proposed that the mesonephric
kidney function or perhaps its excretory
products may interfere with the onset of
meiosis. The reasons for such connection can
only be speculative. Whether the interference is exerted by decreased secretion of MIS
or by decreased responsiveness of the germ
cells to MIS is still completely unknown.
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