close

Вход

Забыли?

вход по аккаунту

?

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

код для вставкиСкачать
THE ANATOMICAL RECORD 210:551-556 (1984)
Mesonephric Excretory Function Related to its influence on
Differentiation of Fetal Gonads
JQRGEN GRINSTED AND LO'ITE AAGESEN
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,
ABSTRACT
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
decade.
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
mammals.
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
gonads.
MESONEPHRIC INFLUENCE ON THE GONADS
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.,
1981).
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.
552
J. GRINSTED AND L. AAGESEN
TABLE I . List of tissues of different mammalian species in which MIS and MPS effect has been shown
MIS
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
ovary
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
clarified.
MPS
References
+
+
+
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
a,b).
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.
The
steroid
content
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).
MESONEPHROS: ONSET OF OVARIAN MEIOSIS
553
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
RELATION BETWEEN MESONEPHRIC
mesonephros increases estradiol content in
EXCRETORY
FUNCTION AND GONADAL
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;
THE MESONEPHRIC EXCRETORY FUNCTION IN
Davies, 1952; Shumkina, 1960; Tiedemann,
DIFFERENT SPECIES
1976).
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
554
J. GRINSTED AND L. AAGESEN
TABLE 2. Period
of
mesonephric degeneration and onset of meiosis in the ouary of different species
Morphological
regression
Start
Completed
Excretory function
Start
Ceased
Species
Pig
Sheep
Cattle
Cat
Rabbit
29'
16-219,10,'1
23-26''
35-38l
1219-211
45'
559
?
26-40'
?
451
27'O
3310
21'-36l
1319-1620
Guinea pig
Man
Rat
Mouse
23
2614
2514
453,435
?
?
54-611r2
5711.12
?
409-421
231,21,22oc19.20
First appearance
of meiotic germ
cells
Additional literature
concerning mesonephric
secretion and regression
40-483.4
524
75-804.16
40-504*'7
1-2 ( P . P . ) ~ , ~ ~
5, 9
9,13-15
9, 13
1, 14, 18
1, 9, 24, 30
3O-3Ei4x3l
5434
17- 184341
1342
2,5,35-40
11
43
Yc)
?
NoneL4
None'
?
?
?
'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.
2.
3.
4.
5.
6.
7.
8.
9.
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.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
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.
ACKNOWLEDGMENTS
Mrs. Inga Dybdahl is gratefully acknowledged for typing the manuscript.
LITERATURE CITED
Altschule, M.D. (1930) The changes in the mesonephric
tubules of human embryos ten to twelve weeks old.
Anat. Rec., 4681-91.
Baker, T.G. (1963) A quantitative and cytological study
of the germ cells in human ovaries. Proc. Roy. Soc.
Lond. rBio1.1, 158417-433.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
loannou, 1964.
Altschule, 1830.
De Martino and Zamboni, 1966
Baker, 1963.
Nagel, 1889.
Von Felix, 1911.
Starck, 1965.
Silverman, 1969
Cotrutz et al., 1971.
Koga, 1972.
Beaumont and Mandl, 1962.
Borum, 1961.
Brambell, 1927.
Beaumont, H.M., and A.M. Mandl (1962)A quantitative
and cvtoloeical studv of ooeonia and oocvtes in the
foeta1"andieonatal rat. Pr& Roy. SOC.Lond. [Biol.],
1.55:557-579.
~~.
~ . .
. ..
Bernier, N., and A. Beaumont (1964)Structure et regression du mesonephros du faetus de lapin. C.R. Soc. Biol.,
158:2227-2230.
Black, J.L., and B.H. Erickson (1968) Oogenesis and
ovarian development in the prenatal pig. Anat. Rec.,
161:45-56.
Borum, K. (1961)Oogenesis in the mouse. A study of the
meiotic prophase. Exp. Cell Res., 24:495-507.
Brambell, F.W.R. (1927) The development and morphology of the gonads of the mouse. 11. The development of
the Wolffian body and ducts. ROC.
Roy. Soc. Lond.
[Biol.], 102206-221.
Bremer, J.L. (1915) The mesonephric corpuscles of the
sheep, cow and deer. Anat. Rec., 101-6.
Bremer, J.L. (1916) The interrelations of the mesonephros, kidney and placenta in different classes of animals. Am. J. Anat., 19179-210.
Byskov, A.G. (1978a)Regulation of initiation of meiosis
in fetal gonads. Int. J. Androl. (Suppl.), 2:29-38.
Byskov, A.G. (1978b) The meiosis inducing interaction
between germ cells and rete cells in the fetal mouse
gonad. Ann. Biol. Anim. Biochem. Biophys.,
18(2B):327-334.
Byskov, A.G. (1979) Regulation of meiosis in mammals.
Ann. Biol. Anim. Biochem. Biophys., 19(4B):1251-1261.
Byskov, A.G., and J. Grinsted (1981) Feminizing effect of
mesonephros on cultured differentiating mouse gonads
MESONEPHROS: ONSET OF OVARIAN MEIOSIS
and ducts. Science, 212:817-818.
Byskov, A.G., and S.Lintern-Moore (1973) Follicle formation in the immature mouse ovary. The role of the
rete ovarii. J. Anat., 116207-217.
Byskov, A.G., and L. Saxen (1976) Induction of meiosis
in fetal mouse testis in vitro. Dev. Biol., 52:193-200.
Byskov, A.G., N.E. Skakkebaek, G. Stafanger, and H.
Peters (1977) Influence of ovarian surface epithelium
and rete ovarii on follicle formation. J. Anat., 123:7786.
Cotrutz, C., G. Mihalacke, C. Cotrutz, and D. Negru
(1971) La morphologie du mesonephros chez I’homme.
Arch. Anat. Histol. Embryol. Norm. Exp., 54:191-201.
Davies, J. (1951)Nephric development in the sheep with
reference to the problem of the ruminant pronephros.
J. Anat. (Lond.), 8.56-11.
Davies, J. (1952)Correlated anatomical and histochemical studies on the mesonephros and placenta of the
sheep. Am. J. Anat., 91:263-299.
Davies, J., and D.V. Davies (1950) The development of
the mesonephros of the sheep. Roc. Zool. Soc. Lond.,
12073-112.
Davies, J., and J.I. Routh (1957) Composition of the foetal fluids of the rabbit. J. Embryol. Exp. Morphol.,
5(1):32-39.
Dickerson, J.W.T., and A. McCance (1957) The composition and origin of the allantoic fluid in the rabbit. J.
Embryol. Exp. Morphol. 5:40-42.
Ericksou, B.H. (1966)Development and radioresponse of
the prenatal bovine ovary, J. Reprod. Fertil., 11:97105.
Evans, H.E., and W.O. Sack (1973) Prenatal development of domestic and laboratory mammals: Growth
curves, external features and selected references. Anat.
Histol. Embryol., 2:11-45.
Fajer, A.B., J.A. Schneider, D. McCall, I.G. Anges, and
E.S. Polakis (1979)The induction of meiosis by ovaries
of newborn hamsters and its relation to the action of
the extraovarian structures in the mesovarium (rete
ovarii). Ann. Biol. Anim. Biochem. Biophys.,
19(4B):1273-1278.
von Felix, W. (1911) Die entwicklung der Harn- und
geschlechtsorgane. In: Handbuch der Entwicklungsgeschichte der Menschen. F. Kleibel and F.P. Mall, eds.
S. Hirzel, Leipzig, Vol. 2, pp. 732-978.
Fraser, E.A. (1920) The pronephros and early development of the mesonephros in the cat. J. Anat. (Lond.),
54:287-304.
Gersh, J. (1937) The correlations of structure and function in the developing mesonephros and metanephros.
Contr. Embryol. (Carnegie Inst. XXVI), 153:33-58.
Giannelli, L. (1925)Contributo all0 studio della funzione
secretoria del mesonefro. Ann. Ostet. Ginecol., 7539544.
Grinsted, J. (1982)Influence of mesonephros on fetal and
neonatal rabbit gonads. II. Sex-steroid release by the
ovary, in vitro. Acta Endocrinol., 99281-287.
Grinsted, J., and A.G. Byskov (1981) Meiosis inducing
and meiosis preventing substances in human male reproductive organs. Fertil. Steril., 35199-204.
Grinsted, J., A.G. Byskov, and M.P. Andreasen (1979)
Induction of meiosis in fetal mouse testis in vitro by
rete testis tissue from pubertal mice and bulls. J. Reprod. Fertil., 56653-656.
Grinsted, J., A.G. Byskov, I.J. Christensen, and J.C.
Jensenius (1982)Influence of mesonephros on fetal and
neonatal rabbit gonads. I. Sex-steroids release by the
testis, in vitro. Acta Endocrinol., 99:272-280.
Grinsted, J., and A.B. Fajer (1983)The role of hormones
on germ cell survival and meiosis in vivo and in vitro.
In: The Anterior Pituitary Gland. AS. Bhatnagar, ed.
Raven Press, New York, pp. 279-285.
555
Hamilton, W.J., J.D. Boyd, and H.W. Mossman (1972)
Human Embryology, 4th ed. W.J. Hamilton and H.W.
Mossman, eds. W. Heffer & Sons,Ltd. Cambridge, The
William and Wilkins Co., Baltimore.
Ioannou, J.M. (1964) Oogenesis in the guinea-pig. J. Embryol. Exp. Morphol., 12(4):673-691.
Kaplan, A,, and M. Friedman (1942) Studies concerning
the site of renin formation in the kidney. 111. The
apparant site of renin formation in the tubules of the
mesonephros and metanephros of the hog fetus. J. Exp.
Med., 76307-319.
Koga, A. (1972) Some observations on the fine structure
of the human mesonephros. Arch. Histol. Jpn.,
34(2):185-201.
von Kolliker, A. (1879) Entwicklungsgeschichte des
Menschen und der hoheren Thiere. 2. a d . W. Englemann, Leipzig.
Leeson, T.S. (1957)The fine structure of the mesonephros
of the 17-day rabbit embryo. Exp. Cell Res., 12:670672.
Leeson, T.S. (1959)An electron microscopic study of the
mesonephros and metanephros of the rabbit. Am. J.
Anat., 105165-195.
Leeson, T.S. (1960)Electron microscopy of the developing
kidney: An investigation into the fine structure of the
mesonephros and metanephros of the rabbit. J. Anat.
(Lond.), 94:lOO-106.
Leeson, T.S., and J.S. Baxter (1957) The correlation of
structure and function of the rabbit. J. Anat. (Lond.),
91 :383-390.
MacCallum, J.B. (1902) Notes on the Wolffian body of
higher mammals. Am. J. Anat., 1:1245-1259.
Martino, De C., and L. Zamboni (1966) A morphologic
study of the mesonephoros of the human embryo. J.
Ultrastruct. Res., 16:399427.
Mauleon, P. (1969) Oogenesis and folliculogenesis. In:
Reproduction in Domestic Animals, 2nd ed. H.H. Cole
and P.T. Cupps, eds. Academic Press, New York and
London, pp. 187-215.
McCance. R.A.. and J.W.T. Dickerson (1957)The comDosition and origin of the foetal fluids of the pig. J. Embryol. Exp. Morphol., 5:43-50.
Merchant-Larios,H. (1979)Origin of the somatic cells in
the rat gonad An autoradiographic approach. Ann.
Biol. Anim. Biochem. Biophys., 19(4B):1219-1229.
Mihalkovics, G. von (1885) Untersuchungen uber die
Entwicklung des Harn- und Geshclechtsapparates des
Amnioten. Mont. Int. J. Anat. Histol., 2:41-106.
Nagel, W. (1889)Ueber die Entwicklung des Urogenitalsystem des Menschen. Arch. Microsk. Anat., 34:269384.
0, W.S., and T.G. Baker (1976) Initiation and control of
meiosis in hamster gonads in vitro. J. Reprod. Fertil.,
48:399-401.
Patten, B.M., and B.M. Carlson (1974) Foundations of
Embryology, 3rd ed. McGraw-Hill Book Company, New
York, London.
Parvinen, H., A.G. Byskov, C . Yding Andersen, and J.
Grinsted (1982) Is the spermatogenic cycle regulated
by MIS and MF’S? Ann. N.Y. Acad. Sci., 383:483-484.
Peters, H., E. Levy, and M. Crone (1965) Oogenesis in
rabbits. J. Exp. Zool., 158(2):169-179.
Shumkina, O.B. (1960)Development of the mesonephros
in sheep and cow embryos (Ouis aries and Bos taurus).
Proc. Acad. Sci., USSR Biol. Sci., 127:618-622.
Silverman, H. (1969) Uber die entwicklung der epithelplatten in den corpuscula renalia der menchlichen urniere. Acta Anat., 74:36-43.
Stanier, M.W. (1960) The function of the mammalian
mesonephros. J. Physiol., 151 ~472-483.
Starck, D. (1965) Embryologie, Ein Lehrbuch auf allgemein Biologischer Grundlage 2. a d . G. Thieme,
556
J. GRINSTED AND L. AAGESEN
Stuttgart.
Strauser, E.R. (1928) Evidence concerning the functional
capacity of the mesonephros of the rabbit. Anat. Rec.,
38:30.
Streeter, G.L. (1921) Weight, sitting height, head size,
foot length and menstrual age of the human embryo.
Contr. Embryol. No. 55 (Carnegie Inst. Washington),
IO:143-170.
Sutherland, L.E., and P.M. Hartroft (1968) Comparative
morphology of the juxtaglomerular cells. 11. The presence of juxtaglomerular cells in embryos. Can. J. Zool.,
46:257-263.
Tiedemann, K. (1976)The Mesonephros of Cat and Sheep,
Comparative Morphological and Histochemical Studies. Springer-Verlag,Berlin, Heidelberg, New York.
Tiedemann, K. (1979) Architecture of the mesonephric
nephron in pig and rabbit. Anat. Embryol., 157:105112.
Tiedemann, K., and R. Wettstein (1980) The mature mesonephric nephron of the rabbit Embryo I. SEM-studies. Cell Tissue Res., 209:95-109.
Upadhyay, S., J.M. Luciani, and L. Zamboni (1979) The
role of the mesonephros in the development of indifferent gonads and ovaries of the mouse. Ann. Biol. Anim.
Biochem. Biophys., 19(4B):1179-1196.
Upadhyay, S., J.M. Luciani, and L. Zamboni (1981) The
role of the mesonephros in the development of the
mouse testis and its excurrent pathways. In: Development and Function of the Reproductive Organs. A.G.
Byskov and H. Peters, eds. Excerpta Medica, Int. Congress. Ser. 559, pp. 19-27.
Weber, S. (1897) Zur Entwicklungsgeschichte des Uropoetischen Apparates bei Saugern, mit besonderer Berdcksicktigung der Urniere zur Zeit des Auftretens der
Bleibenden Niere. Schwalbe’s Morphol. Arb., 7611-
691.
Westergaard, L.G., A.G. Byskov, C. Yding Andersen, J.
Grinsted, and K.P. McNatty (1984) Is resumption of
meiosis in the human preovulatory oocyte triggered by
a meiosis inducing substance (MIS) in the follicular
fluid? Fertil Steril41,3:377-384.
Winiwarter, H., von, and G. Sainmont (1908-1909) Nouvelles recherches sur l’ovogenese et l’organogenese
del’ovaire des mammiferes (chat). Arch. biol., 24:373431.
Yding Andersen, C., A.G. Byskov, and J. Grinsted (1981a)
Initial purification of the meiosis inducing substance
(MIS) and the meiosis preventing substance (MPS).
Acta Endocrinol. (Suppl.), 97243-343.
Yding Andersen, C., A.G. Byskov, and J. Grinsted (1981b)
Partial purification of the meiosis inducing substance
(MIS). In: Development and function of the Reproductive Organs. A.G. Byskov and H. Peters, eds. Excerpta
Medica, Int. Congr. Ser. 559, pp. 73-80.
Yding Andersen, C., L.G. Westergaard, A.G. Byskov, J.
Grinsted, and G.L. Lauritsen (1981~)Possible regulation of meiosis in the human ovary. In: Human Reproduction. K. Semm and L. Mettler, eds. Excerpta
Medica, Int. Congr. Ser. 551, pp. 449-452.
Zamboni, L., J. Bezard, and P. Mauleon (1979) The role
of the mesoneuhros in the develoument of the sheeu
fetal ovary. i n n . Biol. Anim. Biochem. Biophys:,
19(4B):1153-1178.
Zamboni, L, S . Upadhyay, J. Bezard, and P. Mauleon
(1981)The role of the mesonephros in the development
of the sheep testis and its excurrent pathways. In:
Development and Function of the Reproductive Organs. A.G. Byskov and H. Peters, eds. Excerpta Medica, Int. Congr. Ser. 559, pp. 31-40.
Документ
Категория
Без категории
Просмотров
0
Размер файла
527 Кб
Теги
excretory, gonads, differentiation, mesonephros, related, function, influence, fetal
1/--страниц
Пожаловаться на содержимое документа