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From the Departments of Physiology and Internal Medicine, Southern Illinois University School of Medicine, Springfield, Illinois.
| Correspondence to: Dr Andrzej Bartke, Departments of Physiology and Internal Medicine, Southern Illinois University School of Medicine, 801 N Rutledge, Springfield, IL 62794-9628 (e-mail: abartke{at}siumed.edu). |
| Received for publication May 7, 2004; accepted for publication May 8, 2004. |
Role of PRL in the Control of Seasonal Breeding in the Male Hamster
Studies conducted in our laboratory following the above-referenced report
of the effects of bromocriptine (Bartke et
al, 1980) reaffirmed the role of photoperiod-induced alterations
in plasma PRL levels in the control of seasonal transitions between periods of
full testicular activity and testicular quiescence in the golden hamster and
identified a number of mechanisms involved in the actions of PRL. In the male
golden hamster, PRL acts at multiple levels of the
hypothalamic-pituitary-testicular axis. In the hypothalamus, it modifies the
turnover of neurotransmitters involved in the control of the pituitary (Steger
et al, 1982,
1984,
1986). In the pituitary, it
influences the number of androgen receptors
(Prins et al, 1988). Actions
of PRL on the hypothalamic-adenohypophyseal system result in the stimulation
of follicle-stimulating hormone (FSH) synthesis and release
(Bartke et al, 1981;
Steger et al, 1983;
Carrillo et al, 1984) and
reduction of the sensitivity of gonadotropin release to negative testosterone
feedback (Bartke et al, 1984;
Matt et al, 1984). This latter
effect is of particular interest, because the major shifts observed in the
sensitivity of luteinizing hormone (LH) and FSH release to feedback control by
gonadal steroids accompany annual cycles of reproductive activity in both
sexes of many (presumably all) seasonal breeders and are critically important
for transitions between reproductive activity and quiescence. Reduced
sensitivity of the hypothalamus and the pituitary to negative feedback of sex
steroids during annual reactivation of the gonads resembles the endocrine
changes that take place during puberty in both seasonal and nonseasonal
breeders, including humans.
In the hamster testis, PRL, along with the gonadotropins, regulates the expression of its own receptors (Klemcke et al, 1984, 1986; Amador et al, 1985) and LH receptors (Bex et al, 1978; Klemcke et al, 1981) and enhances the responsiveness of Leydig cells to LH stimulation (Klemcke et al, 1986).
The net result of the actions of PRL can be very striking. Golden hamsters with regression of the testes that was induced by 2 months of exposure to short photoperiods are found to respond to 2 months of treatment with PRL-secreting ectopic pituitary transplants by the restoration of their fertility (Bartke et al, 1979). Our earlier studies of hypophysectomized rats (Hafiez et al, 1972) and mice (Bartke, 1971) and of hypopituitary dwarf mice (Bartke, 1966; Bartke and Lloyd, 1970) demonstrated the similar, although generally far less dramatic, stimulatory effects that PRL has on testicular activity. These studies also suggested that increases in the number of LH receptors and in the sensitivity of testicular steroidogenesis to LH stimulation are important in mediating the effects of PRL on male reproductive function in these species of rodents.
The obvious and important question raised by these findings was whether the results obtained in hamsters, mice, and rats also apply to other mammalian species. It was also not entirely clear how to relate the results of our research probing the physiological role of PRL in the male to the rapidly accumulating evidence that pathologically elevated levels of PRL, hyperprolactinemia (hyperPRL), can interfere with testicular function, libido, potency, and fertility. This article will briefly review the highlights of studies that have addressed the role of PRL in different species of seasonally breeding mammals and studies that have used targeted silencing or overexpression of PRL or PRL receptor (PRL-R) genes to identify the physiological role of PRL in the control of male reproductive functions. The concluding section will address differences between the responses to normal and abnormally elevated levels of PRL and differences between the role of PRL in males of different species.
Role of PRL in the Control of the Annual Reproductive Cycles in the Black Bear and the Polar Bear
A series of elegant studies in Dr Bahr's laboratory used captive and
free-ranging bears to determine whether the role of PRL in the control of male
reproductive seasonality applies to species taxonomically distant from
rodents. In the black bear (Ursus americanus), serum PRL levels were
minimal in December, when animals were in the den, and increased beginning in
March, reaching maximal values in May
(Tsubota et al, 1995). Thus,
seasonal increases in serum PRL levels coincided with testicular recrudescence
and the onset of breeding season and preceded peak testosterone
concentrations, which were achieved in June
(Tsubota et al, 1995). The
expression of testicular gonadotropin and PRL-R genes was examined before and
during the breeding season (in January and May, respectively)
(Howell-Skalla et al, 2000a). The major PRL-R transcript was present in both January and May, whereas minor
transcripts were detected only in May, coinciding with the increased abundance
of LH receptor (LH-R) messenger RNA (mRNA). A subsequent study demonstrated an
increase in the abundance of LH-R and PRL-R mRNA between January and March
(Howell-Skalla et al, 2000b).
Suppression of serum PRL levels during testicular recrudescence by treatment
with a long-acting dopaminergic agonist prevented an increase in the
expression of LH-R and PRL-R in March, lowered serum testosterone levels in
March and April, and reduced testis size in May
(Howell-Skalla et al, 2000b).
These findings strongly imply that increased release of PRL before the onset
of the breeding season plays a physiological role in the ensuing stimulation
of testicular function in the black bear. Moreover, the mechanisms involved in
this effect of PRL appear to resemble those described in the hamster and in
nonseasonally breeding rodents.
In the follow-up of these studies, plasma hormone levels and testicular size were examined in free-ranging polar bears (Ursus maritimus) during the mating season in April and May and after the mating season in July and October (Howell-Skalla et al, 2002). Plasma LH and testosterone levels were maximal in April, highest levels of PRL were measured in April and May, and testes reached maximal size in May. Thus, seasonal elevation of PRL levels in polar bears coincides with the breeding season, but further studies are required to determine whether PRL plays a role in stimulating a seasonal increase in testicular activity in this species.
Does PRL Have a Role in Short-Day Breeders?
The release of PRL depends on the photoperiod, with long days being
stimulatory and short days inhibitory. This raises the possibility that in
short-day (fall) breeders, such as sheep or deer, PRL either has no role in
the control of reproduction or is involved in the seasonal inhibition rather
than the seasonal stimulation of testicular growth and activity. Several
laboratories probed the suspected involvement of PRL in mediating the effects
of photoperiod on testicular function in the ram. Most of these studies
involved treatment with bromocriptine, an inhibitor of PRL release, during
different phases of the annual cycle of reproductive activity. Although the
effects of bromocriptine were generally small and not always consistent
between the studies, they did include reductions in testis size, sperm
production, and testosterone secretion
(Sanford and Dickson, 1980;
Barenton et al, 1982; Yarney and Sanford, 1989;
Regisford and Katz, 1993) and
a delay in the response of the testes to a short (stimulatory) photoperiod
(Barenton and Pelletier, 1980;
Sanford and Dickson, 1980). Differences between the results of the various studies are probably related to
differences in the breed of the animals and in the experimental protocols. The
possibility that PRL exerts direct, rather than gonadotropin-mediated, effects
in the ovine testes is strongly supported by the presence of PRL-Rs in the
Leydig cells and the seminiferous tubules of this species
(Lincoln et al, 2001) and by
results obtained in rams with surgical disconnection of the pituitary from the
hypothalamus (Lincoln et al,
1996). This procedure suppresses gonadotropin release and disrupts
the inhibitory control of PRL release by tuberoinfundibular dopaminergic
neurons. In such animals, alterations in PRL release induced by photoperiod or
bromocriptine are followed, within 4–8 weeks, by corresponding changes
in the size of the testes (Lincoln et al,
1996; Lincoln and Clarke,
1997).
Collectively, the results obtained in different breeds of sheep suggest that PRL contributes to the control of seasonal alterations in testicular function in short-day breeders, although the magnitude of its effects is much smaller than in some rodents and carnivores that breed in the spring.
Physiological Role of PRL in the Male Revisited; PRL-R Knockout and PRL Knockout Mice
The availability of mice with targeted disruption (knockout [KO]) of the
gene responsible for the production of PRL or PRL-R
(Horseman et al, 1997;
Ormandy et al, 1997) provided
an exciting opportunity to reexamine the physiological functions of PRL
signaling, including its role in the control of male reproduction. The absence
of functional PRL-Rs in PRL-R-KO mice was originally reported to be associated
with infertility or reduced fertility in approximately half of the males
(Ormandy et al, 1997). However, subsequent studies of male reproductive functions in these animals
produced conflicting results. Binart et al
(2003) reported no alterations
in the weight of the testes, epididymides, and sex accessory glands, in the
plasma levels of gonadotropins and testosterone, or in the fertility of
PRL-R-KO males and concluded that "the absence of PRL signaling is not
detrimental to male testicular function and to fertility in the mouse."
However, in a paper published during the same year, Robertson et al
(2003) reported an increased
rate in the total infertility of PRL-R-KO mice, along with an increased
latency to produce a first pregnancy.
Isolated PRL deficiency in PRL-KO mice was associated with reductions in the weight of the seminal vesicles and the ventral prostate, in the levels of plasma LH, and in the pituitary release of LH and FSH in vitro (Steger et al, 1998). However, plasma testosterone levels, in vitro testosterone release, and fertility were not affected. It is unclear why the lack of PRL signaling in PRL-R-KO and PRL-KO mice affects the reproductive function of the male mouse in such a way that the expected results are marginal compared with those obtained in hypophysectomized or PRL-deficient hereditary dwarf mice or even absent. Perhaps normal or near-normal reproductive function in PRL-R-KO and PRL-KO animals is due to compensatory mechanisms and/or alternate signaling pathways (eg, growth hormone [GH]) that are absent in both hypophysectomized animals and hereditary dwarf mice. Such a possibility is consistent with the observation that plasma PRL levels are increased in GH-R-KO mice (Chandrashekar et al, 1999). That the male reproductive functions appear to be more vulnerable to deletions of the gene responsible for producing PRL-R than to deletion of the gene responsible for producing PRL could be due to developmental effects in PRL-R-KO animals, which are presumably unable to respond to placental lactogens or maternal PRL, including the PRL present in the milk.
Recent Progress in Understanding the Action of PRL on the Prostate
The action of PRL on the male accessory reproductive glands, including the
prostate, has been extensively studied for more than 50 years, and a
comprehensive review of the advances in this field during the past 25 years is
outside the scope of this brief article. However, we note how much progress
was made possible by the development of methods for gene knockout and for
production of transgenic animals, especially when it became possible to target
gene expression to specific organs.
A report on the reduced weight of the ventral prostate and seminal vesicles in PRL-KO mice without changes in plasma testosterone levels (Steger et al, 1998) indicates that PRL has a physiological role in the structural maintenance of these organs and that it acts directly on the male accessory reproductive glands. Unexpectedly, the weight of seminal vesicles and prostate was not altered in PRL-R-KO mice (Binart et al, 2003). However, the number of epithelial cells in the dorsal prostate was diminished in these animals, and simian virus 40 T-induced neoplasia was reduced in the ventral lobe (Robertson et al, 2003).
A massive enlargement of accessory reproductive glands was described in old transgenic mice that overexpressed human GH or human placental GH variant hormones, which signal via both GH receptors and PRL-Rs in the mouse (Prins et al, 1992). These findings reaffirm the stimulatory actions of PRL on the male reproductive system, because the overexpression of bovine GH, which is not lactogenic in the mouse, failed to produce similar changes (Prins et al, 1992). In more recent studies, transgenic mice with a ubiquitous overexpression of PRL that was driven by a metallothionein-1 promoter had elevated serum androgen levels and a dramatic enlargement of the prostate (Wennbo et al, 1997). Prostate-specific expression of rat PRL that was under the control of rat probasin (Pb) promoter led to stromal hyperplasia, ductal dilatation, focal epithelial dysplasia, and an increased stromal-to-epithelial ratio without changes in serum androgen levels (Kindblom et al, 2003). Microarray analysis of hyperplastic prostates from Pb-PRL transgenic mice showed altered expression of more than 250 genes and provided evidence for reduced apoptosis, increased tissue remodeling, and activation of the stroma (Dillner et al, 2003). These changes, together with the evidence for local expression of PRL in the prostate (Nevalainen et al, 1997; Härkönen, 2003), raise many new and important questions about the potential role of PRL in prostatic hyperplasia and cancer in men.
New Information on the Role of PRL in Men
A discussion of the progress in the understanding of the role of PRL in
male reproductive functions would not be complete without reference to
findings in the human. Research results reported during the past 25 years have
added to the evidence that pathological hypersecretion of PRL (hyperPRL) in
men is associated with hypogonadism and/or impotence and that the effects of
PRL on the central nervous system control of gonadotropin release and sexual
behavior are important in the etiology of these disorders (see reviews in
Bartke and Shrenker, 1987;
DeRosa et al, 2003).
Identifying the physiological role that PRL has on male sexual function, endocrine regulation, and fertility in our own species continues to be an interesting challenge. Indirect support for the involvement of PRL in controlling the steroidogenic and gametogenic functions of the human testis and influencing the male reproductive tract was provided by studies of PRL binding. Hair et al (2002) reported localization of PRL-Rs in human Leydig cells, spermatocytes, and spermatids and in the epithelium of the epididymis, vas deferens, prostate, and seminal vesicles. Studies of various steps of PRL signaling in fresh samples of vas deferens have suggested the functional activation of PRL-Rs in this tissue (Hair et al, 2002). Other investigators have described the beneficial effects of PRL and metoclopromide (a PRL releaser) on sperm characteristics in infertile men (Ufearo and Orisakwe, 1995), and in men with prostatic cancer, investigators have described the potentiation of antigonadal effects of a gonadotropin-releasing hormone agonist by bromocriptine, an inhibitor of PRL release (Huhtaniemi et al, 1991).
Krüger et al (2003a) reported that plasma PRL levels in men increase immediately after orgasm. The same investigators examined the consequences of pharmacological manipulation of PRL release on arousal, orgasm, and refractory period (Krüger et al, 2003b). Suppression of PRL secretion with cabergoline enhanced all of the examined parameters of sexual drive and function. Stimulation of PRL release with protirelin had no significant effects on these parameters but completely prevented the effects of cabergoline. The authors suggested that post-orgasmic PRL release has a function in inhibiting sexual drive and behavior (Krüger et al, 2003b).
Effects of PRL in Hamsters vs Current View of the Role of PRL in the Male
By studying the effects that treatment with bromocriptine, PRL, or
PRL-secreting ectopic pituitary transplants has on male golden hamsters, we
have obtained evidence that PRL is involved in the control of seasonal
breeding in this species. What can be said about the significance of these
findings from the perspective of 25 years? First, these findings firmly
establish that PRL can have a major role in mediating the effects of
photoperiod on male reproductive functions and that PRL can facilitate the
identification of the mechanisms involved in these effects. Work in other
laboratories indicates that the conclusions concerning the role of PRL in the
seasonal breeding of male golden hamsters apply to other, but clearly not all
(DiGregorio et al, 1994),
seasonal breeders. The strongest evidence for the importance of PRL in the
control of the annual cycle of testicular activity in a species other than
golden hamsters was obtained in studies of black bears
(Howell-Skalla et al, 2000b).
It is interesting that photoinducible changes in PRL release in Japanese quail
are associated with corresponding changes in testicular growth
(Yasuo et al, 2004). From the
evidence available to date, it appears that golden hamsters are not unique in
using PRL for the purpose of mediating the effects of photoperiod on the
testis but that the magnitude of these effects of PRL on male gonadal function
in this species may be exceptional. In the gonadally regressed hamsters, PRL
acts on the hypothalamus and pituitary to stimulate gonadotropin release, and
a combination of this effect with the direct effects of PRL on the testis
leads to dramatic stimulation of testicular growth and function. gonadally
active adult male hamsters, experimentally creasing plasma PRL to levels above
the physiological range produced significant increases in plasma FSH
testosterone levels, testicular weight, and release of and testosterone in
vitro (Bartke et al, 1982). Stimulation of gonadotropin release by hyperPRL is not unique to golden
hamster, since it also occurs in the nonseasonally breeding mouse
(Klemcke and Bartke, 1981),
but it stands in sharp contrast to the inhibitory action of hyperPRL
gonadotropin release in the rat and the human (for views, see
Bartke and Shrenker, 1987;
De Rosa et 2003).
It is unclear whether, and to what extent, the dramatic differences observed between species in their responses to hyperPRL coincide with differences in the physiological role of PRL in the regulation of the testis. Stimulatory, potentiating, and synergistic effects of PRL on ious aspects of testicular growth and function were demonstrated in hamsters and mice in which hyperPRL stimulatory, as well as in rats, in which it is inhibitory (for a review, see Bartke et al, 1985). Similar to the uation in the rat, both hypo- and hyperprolactinemia detrimental to testicular function in the domestic (Jedlinska et al, 1995).
In the human, there is mounting evidence that normally acts on the Leydig cells, germ cells, prostate, vas deferens, and other regions of the male reproductive tract, but the role of these actions in the normal remains to be clearly defined.
Acknowledgments
I would like to thank Drs Harold Klemcke, Richard Steger, Kathleen Matt, Frederic Bex, and Armando Amador as well as other colleagues and students who contributed to this work and to apologize to the countless individuals whose work pertinent to this topic was not mentioned in this brief retrospective.
Footnotes
? Our studies of the role of PRL in seasonal breeders were supported by
NICHD. 
References
Amador A, Klemcke HG, Bartke A, Soares MJ, Siler-Khodr TM, Talamantes F. Effects of different numbers of ectopic pituitary transplants on regulation of testicular LH/hCG and prolactin receptors in the hamster (Mesocricetus auratus). J Reprod Fertil. 1985; 73: 483 -489.
Barenton B, Hochereau-de Reviers MT, Perreau C, Poirier JC. Effects of induced hypoprolactinemia in the ram: plasma gonadotropin levels, LH and FSH receptors and histology of the testis. Reprod Nutr Dev. 1982;22: 621 -630.
Barenton B, Pelletier J. Prolactin, testicular growth and LH
receptors in the ram following light and 2-Br-
-ergocryptine (CB-154)
treatments. Biol Reprod. 1980; 22: 781
-790.[Abstract]
Bartke A. Influence of prolactin on male fertility in dwarf mice. J Endocrinol. 1966; 35: 419 -420.
Bartke A. Effects of prolactin on spermatogenesis in
hypophysectomized mice. J Endocrinol. 1971; 49: 311
-316.
Bartke A, Hogan MP, Cutty GB. Effects of human chorionic gonadotropin, prolactin, and bromocriptine on photoperiod-induced testicular regression and recrudescence in golden hamsters. J Androl. 1980;1: 115 -120.[Abstract]
Bartke A, Klemcke H, Matt K. Effects of physiological and abnormally elevated prolactin levels on the pituitary-testicular axis. Med Biol. 1985;63: 264 -272.
Bartke A, Lloyd CW. Influence of prolactin and pituitary isografts
on spermatogenesis in dwarf mice and hypophysectomized rats. J
Endocrinol. 1970;46: 321
-329.
Bartke A, Matt KS, Siler-Khodr TM, Soares MJ, Talamantes F, Goldman BD, Hogan MP, Hebert A. Does prolactin modify testosterone feedback in the hamster? Pituitary grafts alter the ability of testosterone to suppress luteinizing hormone and follicle-stimulating hormone release in castrated male hamsters. Endocrinology. 1984; 115: 1506 -1510.[Abstract]
Bartke A, Shrenker P. Effects of naturally occurring and experimentally induced hyperprolactinemia on male hypothalamic, pituitary, and reproductive functions. In: Paparo AA, ed. CRC Critical Reviews in Anatomical Science. Boca Raton, Fla: CRC Press; 1987 : 37-62.
Bartke A, Siler-Khodr TM, Hogan MP, Roychoudhury P. Ectopic pituitary transplants stimulate synthesis and release of follicle-stimulating hormone in golden hamsters. Endocrinology. 1981; 108: 133 -139.[Abstract]
Bartke A, Smith MS, Dalterio S. Reversal of short photoperiod–induced sterility in male hamsters by ectopic pituitary homografts. Int J Androl. 1979; 2: 257 -262.
Bartke A, Steger RW, Klemcke HG, Siler-Khodr TM, Goldman BD. Effects of experimentally induced hyperprolactinemia on the hypothalamus, pituitary, and testes in the golden hamster. J Androl. 1982; 3: 172 -177.[Abstract]
Bex F, Bartke A, Goldman BD, Dalterio S. Prolactin, growth hormone, luteinizing hormone receptors, and seasonal changes in testicular activity in the golden hamster. Endocrinology. 1978; 103: 2069 -2080.[Abstract]
Binart N, Melaine N, Pineau C, Kercret H, Touzalin AM,
Imbert-Bollore P, Kelly PA, Jegou B. Male reproductive function is not
affected in prolactin receptor-deficient mice.
Endocrinology. 2003; 144: 3779
-3782.
Carrillo AJ, Goldman BD, Bartke A. Hypothalamic deafferentation inhibits the stimulatory influence of prolactin on follicle-stimulating hormone release in the golden hamster. Endocrinology. 1984; 114: 87 -91.[Abstract]
Chandrashekar V, Bartke A, Coschigano KT, Kopchick JJ. Pituitary
and testicular function in growth hormone receptor gene knockout mice.
Endocrinology. 1999; 140: 1082
-1088.
De Rosa M, Zarrilli S, Di Sarno A, Milano N, Gaccione M, Boggia B, Lombardi G, Colao A. Hyperprolactinemia in men: clinical and biochemical features and response to treatment. Endocrine. 2003; 20: 75 -82.[Medline]
DiGregorio GB, Gonzalez Reyna A, Murphy BD. Roles of melatonin and prolactin in testicular crudescence in mink (Mustela vison). J Reprod Fertil. 1994;102: 1 -5.
Dillner K, Kindblom J, Flores-Morales A, Shao R, Tornell J,
Norstedt G, Wennbo H. Gene expression analysis of prostrate hyperplasia in
mice overexpressing the prolactin gene specifically in the prostrate.
Endocrinology. 2003; 144: 4955
-4966.
Hafiez AA, Lloyd CW, Bartke A. The role of prolactin in the
regulation of testis function. The effects of prolactin and luteinizing
hormone on the plasma levels of testosterone and androstenedione in
hypophysectomized rats. J Endocrinol. 1972; 52: 327
-332.
Hair WM, Gubbay O, Jabbour HN, Lincoln GA. Prolactin receptor
expression in human testis and accessory tissues: localization and function.
Mol Hum Reprod. 2002; 8: 606
-611.
Härkönen P. Paracrine prolactin may cause prostatic
problems. Endocrinology. 2003; 144: 2266
-2268.
Horseman ND, Zhao W, Montecino-Rodriquez E, et al. Defective mammopoiesis, but normal hematopoiesis, in mice with a targeted disruption of the prolactin gene. EMBO J. 1997; 16: 101 -110.
Howell-Skalla LA, Bunick D, Bleck G, Nelson RA, Bahr JM. Cloning and sequences analysis of the extracellular region of the polar bear (Ursus maritimus) luteinizing hormone receptor (LHr), follicle stimulating hormone receptor (FSHr), and prolactin receptor (PRLr) genes and their expression in the testis of the black bear (Ursus americanus). Mol Reprod Dev. 2000a;55: 136 -145.[Medline]
Howell-Skalla LA, Bunick D, Nelson RA, Bahr JM. Testicular
recrudescence in the male black bear (Ursus americanus): changes in testicular
luteinizing hormone-, follicle-stimulating hormone-, and prolactin-receptor
ribonucleic acid abundance and dependency on prolactin. Biol
Reprod. 2000b;63: 440
-447.
Howell-Skalla LA, Cattet MRL, Ramsay MA, Bahr JM. Seasonal changes in testicular size and serum LH, prolactin and testosterone concentrations in male polar bears (Ursus maritimus). Reproduction. 2002; 123: 729 -733.
Huhtaniemi I, Kurohmaru M, Venho P, Rannikko S. Combination of a GnRH against with an antiandrogen or bromocriptine in the treatment of prostatic cancer; slight potential for antigonadal effects. Int J Androl. 1991;14: 374 -386.[Medline]
Jedlinska M, Rozewiecka L, Ziecik AJ. Effect of hypoprolactinaemia and hyperprolactinaemia on LH secretion, endocrine function of testes and structure of seminiferous tubules in boars. J Reprod Fertil. 1995;103: 265 -272.
Kindblom J, Dillner K, Sahlin L, Robertson F, Ormandy C, Tornell J,
Wennbo H. Prostate hyperplasia in a transgenic mouse with prostate-specific
expression of prolactin. Endocrinology. 2003; 144: 2269
-2278.
Klemcke HG, Bartke A. Effects of chronic hyperprolactinemia in mice on plasma gonadotropin concentrations and testicular human chorionic gonadotropin binding sites. Endocrinology. 1981; 108: 1763 -1768.[Abstract]
Klemcke HG, Bartke A, Borer KT, Hogan MP. Regulation of testicular prolactin and luteinizing hormone receptors in golden hamsters. Endocrinology. 1984; 114: 594 -603.[Abstract]
Klemcke HG, Bartke A, Goldman BD. Plasma prolactin concentrations and testicular human chorionic gonadotropin binding sites during short photoperiod–induced testicular regression and recrudescence in the golden hamster. Biol Reprod. 1981; 25: 536 -548.[Abstract]
Klemcke HG, Bartke A, Steger R, Hodges S, Hogan MP. Prolactin (PRL), follicle-stimulating hormone, and luteinizing hormone are regulators of testicular PRL receptors in golden hamsters. Endocrinology. 1986; 118: 773 -782.[Abstract]
Krüger THC, Haake P, Chereath D, Knapp W, Janssen OE, Exton MS, Schedlowski M, Hartmann U. Specificity of the neuroendocrine response to orgasm during sexual arousal in men. J Endocrinol. 2003a; 177: 57 -64.[Abstract]
Krüger THC, Paake P, Haverkamp J, et al. Effects of acute prolactin manipulation on sexual drive and function in males. J Endocrinol. 2003b;179: 357 -365.[Abstract]
Lincoln GA, Clarke IJ. Refractoriness to a static melatonin signal develops in the pituitary gland for the control of prolactin secretion in the ram. Biol Reprod. 1997; 57: 460 -467.[Abstract]
Lincoln GA, Clarke IJ, Sweeney T. Hamster-like cycles in testicular size in the absence of gonadotrophin secretion in HPD rams exposed to long-term changes in photoperiod and treatment with melatonin. J Neuroendocrinol. 1996;8: 855 -866.[Medline]
Lincoln GA, Townsend J, Jabbour HN. Prolactin actions in the sheep
testis: a test of the priming hypothesis. Biol Reprod. 2001; 65: 936
-943.
Matt KS, Bartke A, Soares MJ, Talamantes F, Hebert A, Hogan MP. Does prolactin modify testosterone feedback in the hamster? Suppression of plasma prolactin inhibits photoperiod-induced decreases in testosterone feedback sensitivity. Endocrinology. 1984; 115: 2098 -2103.[Abstract]
Nevalainen MT, Valve EM, Ingleton PM, Nurmi M, Martikainen PM, Härkönen PL. Prolactin and prolactin receptors are expressed and functioning in human prostate. J Clin Invest. 1997; 99: 618 -627.[Medline]
Ormandy CJ, Camus A, Barra J, et al. Null mutation of the prolactin
receptor gene produces multiple reproductive defects in the mouse.
Genes Dev. 1997; 11: 167
-178.
Prins GS, Bartke A, Chandrashekar V, Reiher J, Hodges S, Meyers R. Effects of bromocriptine and ectopic pituitary transplants on pituitary and hypothalamic nuclear androgen receptors in the male hamster. Neuroendocrinology. 1988; 47: 236 -240.[Medline]
Prins GS, Cecim M, Birch L, Wagner TE, Bartke A. Growth response and androgen receptor expression in seminal vesicles from aging transgenic mice expressing human or bovine growth hormone genes. Endocrinology. 1992; 131: 2016 -2023.[Abstract]
Regisford EGC, Katz LS. Effects of bromocriptine-induced hypoprolactinemia on gonadotrophin secretion and testicular function in rams (Ovis aries) during two seasons. J Reprod Fertil. 1993; 99: 529 -537.
Robertson FG, Harris J, Naylor MJ, et al. Prostate development and
carcinogenesis in prolactin receptor knockout mice.
Endocrinology. 2003; 144: 3196
-3205.
Sanford LM, Dickson KA. Seasonality in reproductive processes in rams with suppressed prolactin secretion. Fertil Steril. 1980;34: 192 -193.
Steger RW, Bartke A, Goldman BD. Alterations in neuroendocrine function during photoperiod induced testicular atrophy and recrudescence in the golden hamster. Biol Reprod. 1982; 26: 437 -444.[Abstract]
Steger RW, Bartke A, Goldman BD, Soares MJ, Talamantes F. Effects of short photoperiod on the ability of golden hamster pituitaries to secrete prolactin and gonadotropins in vitro. Biol Reprod. 1983; 29: 872 -878.[Abstract]
Steger RW, Bartke A, Matt KS, Soares MJ, Talamantes F. Neuroendocrine changes in male hamsters following photostimulation. J Exp Zool. 1984; 229: 467 -474.[Medline]
Steger RW, Chandrashekar V, Zhao W, Bartke A, Horseman N.
Neuroendocrine and reproductive functions in male mice with targeted
disruption of the prolactin gene. Endocrinology. 1998; 139: 3691
-3695.
Steger RW, Matt KS, Bartke A. Interactions of testosterone and short-photoperiod exposure on the neuroendocrine axis of the male Syrian hamster. Neuroendocrinology. 1986; 43: 69 -74.[Medline]
Tsubota T, Nelson RA, Thulin JD, Howell L, Bahr JM. Annual changes in serum concentrations of prolactin in captive male black bears (Ursus americanus). J Reprod Fertil. 1995; 104: 187 -191.
Ufearo CS, Orisakwe OE. Restoration of normal sperm characteristics in hypoprolactineamic infertile men treated with metaclopromide and exogenous prolactin. Clin Pharmacol Ther. 1995; 58: 354 -359.[Medline]
Wennbo H, Kinblom J, Isaksson OGP, Törnell J. Transgenic mice
over-expressing the prolactin gene develop dramatic enlargement in the
prostate gland. Endocrinology. 1997; 138: 4410
-4415.
Yarney TA, Sanford LM. Pubertal changes in the secretion of gonadotrophic hormones, testicular gonadotrophic receptors and testicular function in the ram. Domest Anim Endocrinol. 1989; 6: 219 -229.[Medline]
Yasuo S, Watanabe M, Tsukada A, Takagi T, Iigo M, Shimada K,
Ebihara S, Yoshimura T. Photoinducible phase-specific light induction of Cry1
gene in the pars tuberalis of Japanese quail.
Endocrinology. 2004; 145: 1612
-1616.
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