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OCR for page 117
Ovarian Stimulation ~ Nonhuman Primal;
P0ert F. Williams, MAD.
IN~JCllON
-this article ~~l refries ~ - As of ovarian stimOa~cion In mailman
primates. Sing the majority of reproductive biology Awards with
roan primates is urxlertal~n with macaques (if. Platte - rhesus arm M.
fasia~ar~s - ~rKr~lgus), He fog of this article will be on ~e nonnal
and stimulated follir~~loger~ic prong In the gags Mdcaca. R~bly,
i~ regulating folli~ogenesis, avulatioa,, Aural fur~ic~n and He
Mensa 1~1 ~1 ~ AL an; an; 1 =_ : ~ ~1~ it ~~ ~ . _~ ~ ~~ __ ~ ~
~ ~~ _- - ~ & ~ ·_ &~ ~~ ~VV~ ~— ~~ ~11= ~ ' —~ ~ ~ ~
anew worlds primate have reproductive cycles shorter than the of the
old world Species (I). For reproductive biology, the ~t extensively
utilized Drew worlds Species are ,Saim~i sciureus (squirrel D~7S) and
Cr~1lithrix jac~hus (ma~6ets)e m=,9h the folla~ir~ explanation of the
mutual Cycle does not apply to rK!w world primates, the problems
aviated with ovarian stimulation are- applicable.
the i~mal Cycle
lhe menstrual cycle of macaques is ally fair ~ in
lath, being about Rally divided into folli~lar and lintel phases.
Bring the second week of the folli=~lar phase, a circle follicle ATE
grisly evident on one of the two ovaries; it continues maturation until
mad—ycle, when adulation arm transformation into a corms lu~ cxx~rs.
He major endocrine events (see Figure 1) of the trial cycle are a
gecxretric increase ~ peripilera1 An con~nt~tions of estradiol,
Arching fern the maturing follicle, midcycle surges of Ill and F5H,
irx~uced by the rising estradiol levels, and two ~ ; of pr ~ terone
secretion face, the corpus luteum, a differentiated structure derived foul
the ovulatory follicle. With diminished function of the corpus lubes,
progesterone levels decline and menstruation occurs. additionally, a
significant ~ ~ -pal FSH concentrations occurs in the last week
of one cycle and continues thrcogh the first week of the folli=~1ar phase
of the next cycle. Some reports have attributed the initiation of
follicle Grog for the next circle to this rise in me An;
(2) .
_ ~ ~ · _ ~ ~ _~ ~ ~ cc ~~ ~ .
The ~ interval for folli=~1ogenesis to occur ~ macaques is two
weeks. If the periovulatory follicle is lyzed (3), the corpus later
rove (3), or the trial Cycle s~ppr~ by pmg~s (4), the
interval for new follicle growth is approximately two weeks ~ duration,
equal in length to the follicular phase. However, it remains unknown f
what folli=~lar stage follicle growth is initiated at the beginning of
~ 17 -
OCR for page 118
this too week interval - primordial, primary, secxrl~lry, or tlot:LLry
(astral) follicles. Since an increase in mediumrsized antral follicles
(0.5-l.Om~) occurs at the transition from one cycle to another, it is
presumed that the ovulatory follicle develops from one of these
mP~iumrsized antral follicles. The two week folli~lar phase has been
divider into the intervals of recruitment, selection and ck~r~unoe.
Recruitment Is the process By a Curt of follicles begins to matte,
leadi~ to a follicle capable of avulati~. He size of the Art chasing
this first week of the ~sbrual cycle remains Be. Stir the
process of Election (appr~ima~=ly day 5-7 of the ~1 candle) the
girdle follicle, Rich may lead to ovulation, be; bi~ica~ly
distinct from all other follicles ~ bat ovaries. Finally, the pro=
of ~ ina ~ e is the ~ i ~ by which the selec ~ follicle and its
~KXy===or, the corpus luteum, dictates the course of events ~ the
hy ~ emus, the pituitary and ovaries. m e expression of dbllb}Lloe by
the preovulatory follicle has been hypothesized to be achieved by the
active secretion of an inhibitor of the development of other follicles
(5), or, coincident with a diminished need for FSH support by the dknLL~ant
follicle (2), the intuition of OH levels by es~actiol se~cic~n f m n
this follicle, thus dinting available FSH for follicles requiring
greater support than the dominant follicle. Irrespective of the
r~ch~urism, it is evident that the dominant follicle precludes the
development of other follicles daring the second week of the follic~1ar
phase. Thus, by this second week, an asymmetrical ovarian function occurs
In macaques; one ovary has ache primary game~enic role <3urir~ ache
interval of the dominant follicle and the other ovary is f~ioni~ as an
endocrine organ (5~. On fact, differential negative fed can FI;H
secretion occurs beaten the ~ ovaries, wit the ovary ~~ the
inant follicle having a Specific inhibition of ~ H secretion. obese
concepts of recruitment, selection and dominance must be considered in
planning treatments for the induction of folli~llogenesis. Such
treatments most be initiated prior to the expression of dcruu~D,ce by the
precvulatory follicle.
Regulation of Follicul ~ enesis
Both AH and FSH are required for sur~===ful follic`~ogenes~s.
Nhmercus studies of episodic secretion of OH secretion have dk~T~:strated
the association of hourly pull of TH with su~essfu] folli~1ogenes~
acuminating in ovulation and the at of such se retcry patterns with
anavulation (6~. ~ini~ation of AH and reactant inn of Sue
patterns of IN seareticn In monkeys with either arcuate Ales lesions
(7) or juvenile stately (~) result; In the induction of ovulatory trust
- :les. Incus, the ppisalic secretion of ~ a` - ars to be an integral
cant of the processes r~ating-folli~1c~;~s. Ye patterns of
AH secretion Reid for folli~1og~;is are less cafes. Perfuse of
the larder circulating half-life of AH, Ponds or AH ink
episodic patterns of FSH secretion are not as evident as those of Ill. Ye
- ~ ~ ~
OCR for page 119
late luteal/~arly folli='lar phase increase ~ Huron F5H csrKY3ntrations
has been proposed as the determinant of folli~1ogenes~s for the next
ovulation (2~. moughFsH accretion during this interval to critics?` for
normal folliculogenesis culminating in ovulation and normal lethal
function, the specific increase in FSH which occurs during this transition
from one cycle to another is not essential. Such a r.?~- dces not OrCU'
prior to the first ovulatory cycle bullring sexual maturation, the first
ovulatory cycle FxY~3xtrtum, nor during the folli~ar phase following
repeated follicular destructions by cautery (9~. Thus, this elevation of
ASH secretion ~ not essential for normal folli~llogenes~s culminating in
ovulation. However, some degree of FSH secretion during this interval [c
c~iti~1 for noun folli~llogenes=. Both inadequate ad Cod lueeal
Cases have been described as spontaneously occurring In macaques (10~.
E~bly, these luteal dysfunctions reflect aberrant folliallogenesis
(111. In monkeys having these spontaneous luteal defects, FSH
~ntrati~s in the early folli=~lar Erase are below ache normal rare.
Coveys treaty during the first week of the Dual Die with porcine
folli~1ar fluid had a transient inhibition of ASH Otis;
adulation was followed by aberrant lineal function, Ably induced by
the Greasy AH concentrations In the early follic~1ar phase (12~.
Thus, during the interval of normally elevate ~ I sea ration in the
transition from one cycle to the next, FSH plays a significant role in the
maturation of the developing follicle, but the elevation in FSH
concentrations is not essential.
Ovarian Stimulation
Any treatment regimen designed to induce multiple follicular
development most override a physiologic system operating to permit only a
single follicle to mature to copulation. thus, taint Nat be initiated
prior to the e~rgerxx of the danirent follicle. Additionally, the
stimulation must not only pate follicular clevelc~ hat At also
pride for normal devel~nt of granulosa arm ~ cells so that
1~ faction Is normal.
E = r gonadotropic preparations in c ~ ination with Han * =rionic
gc~LkJtno pin are each successful in inducing multiple folli='lar
development: human menopausal gonadotropin (UPS Figure 2; 13), human
follicle stimulating hormone (l4), pregnant mare's serum gYxeKkstrqpin
(15), and porcine ESH (16~. Treatment with the=- gonadotropin
preparations in combination with hog results in multiple follicular
develc~nt and Adaption of meiosis ~t the Ocher. OF - #; may be
aspirated fmn the follicles prior to 36 ham; post hoe or flub fed
the soviet after 36 hairs; ~t ha; treatment. Ocx~e maturatic~
variable err] will range freon indenture (phrase I) Ash mature
(database IT). Ye hot is typically a~inist~ after An estradiol
corm ntratic~ns have achier at last 600 pg/ml. Rehash folli~lar
development and oocyte maturation occurs with there treatment regimens,
luteal function is not the same as in normal nY~s:rua1 cycles. PP-~U=- of
the multiple folli=~1ar develcpment and correspondingly inr~1#lsed amount
_ l] 9 _
OCR for page 120
of lute1 tissue following hCG treatment, pmg~tercrm Ratio are
markedly greasy ~ the luteal phase of slime cycles relative t:o
Be It's pycle (13~. Hover, despite ideas Procter
Sties, the faction of the luteal tissue is diminish relative
to normal t;=C~e. Following gonadotrc~i~ir~u~ ovarian st;~1atic~, ~
bit sites arx] IlI-bi=li~ site coupling to ache adenylate ~:la~ in
are ~ (17~.
lYpi~ly, Pugh net uniformly, 1H surges do no: for tin
fin stimulated cycles, despite serum Rations of estradiol
nonna1ly ass aviated with the irruption of IRISH surges. Scantly,
ir~ibi1:ory products of the stimulated follicles block Be
iti~f~c3: action of estradiol on I~/FSH sedation (18~. Be
ovarian factor which blocks the positive f~ck action of estradiol has
been refeed to as gonaclotr~p=-surg~ir~ibitir~ factor (GnSIF); whether
GnSIF activity is due ~ a ~ clistinct freon Irvin remains to be
detail (19~.
: A proportion of mar~ceys treated with exagerx~us gonadotr~ins do have
a spas If surge in rinse Deco ache rewire elevation of estractiol.
Since Be ire reasing estrogen oorx~trations are due to Be collective
production of estrogens, by a multitude of follicles, the degree of
folli~lar maturation which has normally Purrs when ~=itive~
f~= occurs In the spontaneous cycles has not yet ~ ~ Prey
stiumlated folliculogenesis. thus, when a spontaneous gonadatrop~n
surge cars in a gonadotropin stimulated monkey, the surge is not
Raze to folliallar maturation, resulting in premature
luteinization of the gravelly with atter~nt inrush progesterone
production (13~. me pr~ials station of pmgesterc)r~e pracl~:
normal follim~1ar Veldt arm Ante maturation.
Even among those subjects which do not have a premature Ill surge,
there ~ a hetemgeT~s follim,Qar response to gonad~ropic stagnation.
Typically' bash on estrogen rinse to gonadotmpic Estimation, the
females have ret~:tively bad classified as "low", 'Sian" and 'high"
rq~rs to gonadc~ic stimulation (20) . No Ethos has Ben developed
for predicting the z~nse of a given subject to goradc~tr - ~ treatment.
Be latter two problems (i.e., premature If surge and heter~s
response to gc~nadatropins) can be ameliorated by adjuncti~re ~ era ~ with a
gonadoLr~vin releasing hormone (GnRH) analog for the inhibition of
endogenous gonadotrop ~ secretion (20). Agonists of GnEH, t
initially pealing pituitary gonadakropin secretion will induce
~down-regulation" of pituitary function and inhibition of gonadotropin
rep when administerel at a sufficient frequency and duration.
Without the initial stipulatory phase, GnRH antagonists will imrPAR~t~ly
inhibit gonadotrop ~ secretion. Simultaneous treatment with GnRH
antagonist and exogenous gonadotropin will prevent the premature OH surge
and will increase the response to exogenous gonadotropin. The estradiol
response of 'tedium responders" Hal been observed to be greater with
adjunctive antagonist treatment than without such treatment.
- 120
-
OCR for page 121
AN sequela of ovarian stim~atic~n with qua dins
the develc~rent of hyperprnlactinemia during to luteal phase of He
~imOa~ced Cole. math no present in all stim~la~ cues, this
transi~t hyperprolactir~nia is prevalerIt when ~tr~ ~t~tians
have been profanely elevated Uric the folli~1ar phase arm
elevate id the luteal phase (13~. Quash ~tr~ me, fee
hyperprolactinmia is not idol by the Hen milieu, but rather by
Be syrwryistic Inaction of estrogen arx! progestin (21~. Firstly at
least cue week of es~adiol <~ntrations In excess of 250 ~ is
red for prig of the pituitary, follows by Austria estradiol
Trains coincideic with progesteror~e levels at physiologic
trations between 2 arm 4 ng/ml. In this ~1, hyperpr~lactin~ia
~3eve~q?s coincident with Be proges~ne elevation; estradiol or
preserve alone do not irx~uce this hyp~prolactinemia. In Be
stimulates Accrual cycles, these conditional pa err; of estradiol and
pa - esterane will occasionally occur with attendant hyperprolactinernia.
~lems with Stimulated Ovarian Fashion
As described above, the response to exoqenals ganadotr~in therapy
maybe he~en~us, with varying degrees of folliallar develc~ and
variable ~ maturation. Earl of this heterugenei~r Is due to Be
endocrine milieu of the subject ardor the errs of a premature In
surge. Additional variability may be Truce by He human c~orionic
gonadotropin therapy administered to induce final folli~llar development
and oocyte maturation. HCG has a long he f-life relative to EH.
Follcr~ing the injection of ha; in monkeys, if follicles are net aspirated,
but are permitted to ovulate, final follicular maturation continues for
days and ovulations will I from 48 to 120 hours after hog treatment
(22~. This response is probable due to hCG acting on a heterogenous
population of follicles, with the least mature follicles at the top of
hod treatment being those which ovulate last.
Despite the problems with inducing follicular and oocybe maturation
and management of the endocrine milieu, the greatest difficulty limiter
r~ In primate folli~llogenesis and oogenes~s Is the availability of
Sleazy subjects. Non-human primates are of a such Ore limited supply
Han laboratory or domestic species. Allis Xylem ~1H ~ APT ~
· · · . . ~
~ ~ a~
reach lZatlOn Of HIM subjects tor Ovarian sti~aticn prowls;
hover, the gonadotropin preparations utilized at this tine are of human
or n~primate origin, thus the treated irxlividu21s develop neutralizing
annuities to the gonadotropin preparations (23, 24), precluding
reutilization of the subject with the saIre gonadotropin pr~pezatic~n. Even
if He immune recense togonadotropins did not cover, orc=~dbe
bled, ethical considerations of how many ti~ chard a In
primate be utilized In research protocols arm he many turgid Tours
Child be perform weld benzene limiting factors;. gently, OCCUR;
Hat be revered freon rx:,n-h~nan private= by either laparat~y or
lab; ethical considerations encourage restriction of the
- 121
OCR for page 122
performance of multiple surging procures on antes utilized ~
r~h. -thus, the limit availability of nonhuman primate=, he
unavailab;li~ of non-h~n primate acnadc~r~ins, and the limit
__ en, . _ do.
. a _ ~ . a _ Ha ~ a . ~ ~ _ a
reutilization of r~ subjects are' greater E~1eE; in he
i~estigatic~n of folliallogenesis art oogenesis than are he biologic
problems Aviated with irx~ucing follia~ar growth and axle maturation.
~ol~ic~ns for Emblems with Stimulated Ovarian Lice
He variable ovarian Dense to gc~nado~z~ic '~i~1ati~ may be
art corers by a~itianal rearm into the basic ~i~
r~ulatir~ folliallogenesis in nc~n-h~nan primates. NUT dices
remain unanswered relative to primate follia~logenesis:
a) Hat ~ the tine Curse for develc~rent of a primordial
follicle into a periovulatory follicle?
b)
c)
d)
e)
f)
Cat stages of follia~ogenesis are gonad~rcp~n
dependent? ~t are ache specific roles of ~ and PI;H?
Is folli~1a~enesis a continues pro=, or can it be
argots without atresia ooa~rring?
During recruitment, Cat is the size of the c *Hart of
follicles from which the dot follicle is selected?
By what n~x~nism dog "selection" of the dominant
follicle occur and how is dcminanm" of the periovulatory
follicle sustained?
When ovarian function is stimulated by exogenous
gonadotro pies, what pool of follicles is responsive to
this ~crea~nent?
go How are oocybe and follicu1ar maturation inberl inked?
h) Can mechanisms of follimllogenesis be extrapolated f``xll
nonprimate species to printer? Estrogen race pbors have
been demonstrated ~ the granulosa cells of rats (25);
in ViVO' rat granulosa call proliferate following DEN
treatment (26). In macaques, estradiol receptors have
not been demonstrated in granulosA cells (27), and
monkeys do not exhibit a granulosa roll proliferation
when treated with DES (28). Thus, are reohanis=s of
folliculogenesis different ~ primates then in non-
primate species?
Determination of answers to these questions will significantly
Improve cur understanding of folliculogenesis and should allow for greater
control of the folli~1ar response to stimulation regimens ~ th exogenous
gonadotropins and more homogencus folli~1ar and oocyte responses.
Additively, basic irn~estigations into oocyte maturation Laid prcF~ide
critical insights reed for the c~veloE~nt of Bathes for the In vied
maturation of Dotes. Ih,,~, when a heterogen~; distribution of opiates
is obtained, the in~nature opiates can be mature in vitro to a Encage of
ferti 1 inability.
- 122
-
OCR for page 123
Me i2Tterlir~ prc~lems of no non-h~nan primate dins for
ovarian sti~ndatio~ protocols, insane rinses to available
Mains, and limiter supply of r~on-h~nan primate preset a scenario
whim Is difficult ~ resolve. Were will rover be sufficient dandifies
of ohms primate pituitaries or urine to allow for the p~ifica~ of
Wins by cornrential technologies. C~11 lines are being premed
by recombinant INA technology to prcx~uce non-h~nan primate ~ins.
~ever, it would seem highly unlikely that ~antiti~ of grants - m
available or Scat of prelection wed permit the for~latic~n of
pzepa~tians for repine ovarian stinn~Jation. Art alternative to the use
of adds gonado~ins, is the augmentation of ~ fin
~ion. this can firstly be a~T~lishec] with the puisatile
~inis~tic~n of OH or clc~niphene citron tr`3at~nt, he the Free of
Ovarian stipulation is not as extensive as concurs with exager~;
adatropins, and the pulsatile a Ministration of GriPH is pa ~ lematic,
and thus not practical for routine ovarian stimulation. Possibly, active
(29), a member of the inhibin family which indurate= FSH secretion, may
be ~ eful for ovarian stimulation. In the future, when its actions are
understood and it is available, it or an agonistic analog may be fur An
prorating ovarian stimulation. Of course, if the structure of activin is
heter~gene~s between species, there inane response of recipient animals
will be a problen. Evolving rational norm will clictate the
appropriateness of reutilization of research subjects in multiple
stimulation protons. Certainly, the Ned for suryir=1 recovery of
dies can be eliminate ~ the fug by the continual improvers In
the resolution of son~phy equipment. den resolution has bed
significantly improved, Locates can be revved normal - idly by
sor~raphica3ly guided pry. Iben the ethical ccmsideration will
not be the perforate of multiple surgical pours, kilt ra~r the
reutilization of Norman primates ~ multiple ovarian stimulation
protocols e
In statuary, relative ~ ache Utilization of non-h~nan primates in
rearm on medically assisted conception, the major difficulties
associates] with the stimmation of folliculogenes~s are not biologi -
problems Assyrian winch the fiction of ache hy~halamic-pituitary-
ovarian axis, but rather are managerial and logistical problems cabby by
the limited availability of non-human primates, the unavailability of
ncnrhuman primate gonadotrc pins for ovarian stimulation, and the ethical
considerations of research subject reutilization. Thus, the majority of
tonic science research on mealy assisted conception will need to be
undertaken ~ laboratory or domesticated species and the non-human primate
utilized for only selected studies.
— 123 —
OCR for page 124
A~I~
We a==istar~e of Martha Forester, Dara I~azy, and Patricia R - se In
the preparation of grciEhics are We manuscript is sincerely ~r~ia~.
- 124
-
OCR for page 125
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ad
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em o
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is ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~
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- 125
Figure 1
-
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OCR for page 126
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at
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Figure 2
- 126
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OCR for page 127
~ENGF~
1. merir~ MJ tl986) Ovarian ar~hito during follicle maturation.
In: outlaw, WR arm J E:rw~ (ems) Repr~uctic~n arm Devel~nt
Volume 3 of Comparative PriTrste Biology, Alan R. Li~c, ma:, Now York,
p 215.
2. Zeleznik AJ arm SO Hillier (1984) The role of ganadc~tr~ins in the
selection of me preovula~ry follicle. Clinical C~etrics arm
Ecology 27 927 e
3. German AL, Em: Nixon, DK Johnson, and GD H - en (1977) P - ulaticnl
of follialloger=;is in the cycling rhesus By: Selection of the
dominant follicle. Endocrinology 100:155.
4 German AL arm GD Hodgen (1977) Systemic versus intraovarian pr~es-
ter~ne replacement after Putty In rhesus Parleys: Differential
patterns of gonadotropins art follicle growth. J Clin Erxiocrinol
Myth 45:837.
Goodman AL arm GD Hodgen (1983) The ovarian triad of the primate
Anal cycle. Pant ~ Horm Res 39:1.
6. Cnxrley OF, M Filioori, D Spratt, and OF Santoro (1985) The
p~y~;iology of gonadat~-releasing hormone (Grind static in men
and women. Pant hag Horm R£s 41:473.
Xhc~il E, ~ Plant, L WilOt, PE Beldhetz, arm G Call (1980)
Neur~ocrine control of the rhesus Mornay dual cycle:
Permissive role of the hypothalamic gonado~p~n-~l^~=ir~ hormone.
Science 207:
8. Wildt L, G Marshall, arm E Knobil (1980) 1~peri~tal irx~uction of
ply ~ ache infantile female rhesus monkey. Science 207:1373.
9. disarm AS, WE Nixon, artful GO Hodgen (1980) Sterile serum
folliclfftimulating hormone elevations: Signifi~ In racrui~
am selection of the cock ant follicle err] ad of octopus
1lltelml normalcy. J Clill E~ldocrinol Match 50:1046.
10. William RF arm GD Hodgen (1982) the reproductive Cycle In f—Age
macaques. Aver J Prima=1 Suppl 1:181.
U. di.Z~a, GS art GD Bergen (1981) ILL base dysfur~tic~n
infertility: A sequel to a~rrar~c follies s. Fowl S~2:il
35:489.
OCR for page 128
12. Stouffer RL and GD Hodgen (1980) Induction of luteal phase defects
in rhesus monkeys by folli~1ar fluid administration at the onset of
the menstrual cycle. J Clan Endocrinol Mats 51:669.
13. Collins RL, RF Williams, and GO Hodgen (1984) Endocrine consequent es
of prolonged ovarian hyperstimulation: Hyperp~ulactinemia, folli~1ar
atresia, and premature luteinization. Fertil Sberil 42:436.
14. Supermen As, RF William, and GD Hodgen (1984) Ovulation iT~i~
using ''Ears'' follicle stimulating honoree in~eys. Fertil Ster
41:629.
15. Bavister, ED, BE Bowman, K Collins, DJ Diersc~ke, arm SG Finale
(1984) Birth of rhesus Morley infant after In vitro fertilization and
nonsu~ir=1 embryo transfer. Pax Natl- Acad Sol USA 81:2218.
16. Yano J and X~ Gould (1985) Suction of follicular grow In we
squirrel monkey (Saimiri sciure ,~) with human rarity follicle
stimulating hormone (Methodic). Fertil Steril 43:799.
17. Stuffer RL, GD Hodgerl, PE Grave=, DR Danforth, KM Eyster, are] JS
Ott~bre (1986) Characterization of corpora lutea in Parleys after
s~vulation with human menopa~~~1 gonadotropin or follicle
stimulating hormone. J Clin E~ocrinol Metab 62:833.
18. Schenken AS and GD Hodgen (1983) Follicle-stimwlating hormone inured
ovarian hyperstimulation In monkeys: Blockade of the luteinizing
hormone surge. J Clan Endocrinol Met 57 50.
19. Danforth DR, MJ Sinosich, TL Anderson, CY Cheng, CW Bardin, and GD
Hodgen (1987) Identification of gonadotrop m surge-inhibiting factor
(GnSIF) in follicular fluid and its differentiation frill inhib~n.
Biol Reprod 37:1075.
20. Hodgen GD, D Kenigsberg, RL Collins, and AS Schenken (1985) Selection
of the dominant follicle and hormonal enhancement of the natural
cycle. Ann NY Aca Sol 442:23.
21. Williams, RF, JG Gianfortoni, and-GD Hodgen (1985) Hyperprolactinemia
insured by an estrogen-progesterone synergy: Quantitative and
temporal effects of estrogen priming in monkeys. J Clin Endocrinol
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22.
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- 129
-
Representative terms from entire chapter:
stimulating hormone
