Evidence that hyperprolactinaemia is associated with ovarian acyclicity in female zoo African elephants
T. L. Dow A B and J. L. Brown A C
+ Author Affiliations
- Author Affiliations
A Smithsonian Conservation Biology Institute, National Zoological Park, 1500 Remount Road, Front Royal, VA 22630, USA.
B West Virginia University, Department of Animal and Nutritional Sciences, PO Box 6108, Morgantown, West VA 26506, USA.
C Corresponding author. Email: brownjan@si.edu
Reproduction, Fertility and Development 24(8) 1019-1027 https://doi.org/10.1071/RD11302
Submitted: 6 December 2011 Accepted: 15 February 2012 Published: 30 March 2012
Abstract
African elephants of reproductive age in zoos are experiencing high rates of ovarian cycle problems (>40%) and low reproductive success. Previously, our laboratory found that 1/3 of acyclic females exhibit hyperprolactinaemia, a likely cause of ovarian dysfunction. This follow-up study re-examined hyperprolactinaemia in African elephants and found the problem has increased significantly to 71% of acyclic females. Circulating serum progestagens and prolactin were analysed in 31 normal cycling, 13 irregular cycling and 31 acyclic elephants for 12 months. In acyclic females, overall mean prolactin concentrations differed from cycling females (P < 0.05), with concentrations being either higher (n = 22; 54.90 ± 13.31 ng mL–1) or lower (n = 9; 6.47 ± 1.73 ng mL–1) than normal. No temporal patterns of prolactin secretion were evident in elephants that lacked progestagen cycles. In cycling females, prolactin was secreted in a cyclical manner, with higher concentrations observed during nonluteal (34.38 ± 1.77 and 32.75 ± 2.61 ng mL–1) than luteal (10.51 ± 0.30 and 9.67 ± 0.42 ng mL–1) phases for normal and irregular females, respectively. Of most concern was that over two-thirds of acyclic females now are hyperprolactinemic, a dramatic increase over that observed 7 years earlier. Furthermore, females of reproductive age constituted 45% of elephants with hyperprolactinaemia. Until the cause of this problem is identified and a treatment is developed, reproductive rates will remain suboptimal and the population nonsustaining.
Additional keywords: gonadal dysfunction, ovarian cyclicity, progestagens.
References
Ajika, K., Krulich, L., Fawcett, C. P., and McCann, S. M. (1972). Effects of oestrogen on plasma and pituitary gonadotrophins and prolactin, and on hypothalamic releasing and inhibiting factors. Neuroendocrinology 9, 304–315.| Effects of oestrogen on plasma and pituitary gonadotrophins and prolactin, and on hypothalamic releasing and inhibiting factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XksFKqt7k%3D&md5=907ab0d48f1229177acb2cea44cb1ef5CAS | 4555305PubMed |
Ange, K., Crissey, S. D., Doyle, C., Lance, K., and Hintz, H. (2001). A survey of African (Loxodonta africana) and Asian (Elephas maximus) elephant diets and measured body dimensions compared to their estimated nutrient requirements. In ‘Proceedings of the Association of Zoos and Aquariums Nutritional Advisory Group’. pp. 5–14. (Association of Zoos and Aquariums Nutritional Advisory Group: Orlando, FL.)
Bachelot, A., and Binart, N. (2007). Reproductive role of prolactin. Reproduction 133, 361–369.
| Reproductive role of prolactin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvVOjtro%3D&md5=05466edb1f7320935e919e42344a4759CAS | 17307904PubMed |
Ball, R., and Brown, J. L. (2006). Preliminary results of a cabergoline trial in captive elephants with hyperprolactinaemia. In ‘Proceedings, International Elephant Conservation and Research Symposium, Copenhagen’. p. 9. (International Elephant Foundation: Copenhagen.)
Bast, J. D., and Melampy, R. M. (1972). Luteinising hormone, prolactin and ovarian 20α-hydroxysteroid dehydrogenase levels during pregnancy and pseudopregnancy in the rat. Endocrinology 91, 1499–1505.
| Luteinising hormone, prolactin and ovarian 20α-hydroxysteroid dehydrogenase levels during pregnancy and pseudopregnancy in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXlsF2hsw%3D%3D&md5=e9ac3164ef56a743a2187809cb3f30cbCAS | 5086142PubMed |
Bechert, U. S. (1998). Factors affecting prolactin secretion in the African elephant. Ph.D. Thesis, Oregon State University, Corvallis, Oregon.
Bechert, U. S., Swanson, L., Wasser, S. K., Hess, D. L., and Stormshak, F. (1999). Serum prolactin concentrations in the captive female African elephant (Loxodonta africana): potential effects of season and steroid hormone interactions. Gen. Comp. Endocrinol. 114, 269–278.
| Serum prolactin concentrations in the captive female African elephant (Loxodonta africana): potential effects of season and steroid hormone interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisVaisLg%3D&md5=2090721b0c3a258460f52bdca4aceb40CAS | 10208775PubMed |
Ben-Jonathan, N. (1994). Regulation of prolactin secretion. In ‘The Pituitary Gland’. (Ed. H. Imura.) pp. 261–283. (Raven Press: New York.)
Ben-Jonathan, N., LaPensee, C. R., and LaPensee, E. W. (2008). What can we learn from rodents about prolactin in humans? Endocr. Rev. 29, 1–41.
| What can we learn from rodents about prolactin in humans?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivFGqs7o%3D&md5=acee925e208eb52cc1dd9c3cf413b503CAS | 18057139PubMed |
Billings, H. J., Viguie, C., Karsch, F. J., Goodman, R. L., Connors, J. M., and Anderson, G. M. (2002). Temporal requirements of thyroid hormones for seasonal changes in LH secretion. Endocrinology 143, 2618–2625.
| Temporal requirements of thyroid hormones for seasonal changes in LH secretion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltVymsbk%3D&md5=f24ee3c3166db078846bb2c1bab6f598CAS | 12072394PubMed |
Brown, J. L. (2000). Reproductive endocrine monitoring of elephants: an essential tool for assisting captive management. Zoo Biol. 19, 347–367.
| Reproductive endocrine monitoring of elephants: an essential tool for assisting captive management.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXos12gs7o%3D&md5=9a0aa1cd7c9ede734acacc972e8103afCAS |
Brown, J. L., and Lehnhardt, J. (1997). Secretory patterns of serum prolactin in Asian (Elephas maximus) and African (Loxodonta africana) elephants during different reproductive states: comparison with concentrations in a noncycling African elephant. Zoo Biol. 16, 149–159.
| Secretory patterns of serum prolactin in Asian (Elephas maximus) and African (Loxodonta africana) elephants during different reproductive states: comparison with concentrations in a noncycling African elephant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtVKhur4%3D&md5=0ab6f2bde9a1935c870728fd5f641daeCAS |
Brown, J. L., Citino, S. B., Bush, M., Lehnhardt, J., and Phillips, L. G. (1991). Cyclic patterns of luteinising hormone, follicle-stimulating hormone, inhibin and progesterone secretion in the Asian elephant (Elephas maximus). J. Zoo Wildl. Med. 1, 49–57.
Brown, J. L., Schmitt, D. L., Bellum, A., Graham, L. H., and Lehnhardt, J. (1999). Hormone secretion in the Asian elephant (Elephas maximus): characterization of ovulatory and anovulatory luteinising hormone surges. Biol. Reprod. 61, 1294–1299.
| Hormone secretion in the Asian elephant (Elephas maximus): characterization of ovulatory and anovulatory luteinising hormone surges.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MvlvVOmsA%3D%3D&md5=48bbd7a7d72a67fa565412ca73c7b478CAS | 10529277PubMed |
Brown, J. L., Walker, S. L., and Moeller, T. (2004a). Comparative endocrinology of cycling and noncycling Asian (Elephas maximus) and African (Loxodonta africana) elephants. Gen. Comp. Endocrinol. 136, 360–370.
| Comparative endocrinology of cycling and noncycling Asian (Elephas maximus) and African (Loxodonta africana) elephants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtVegsbg%3D&md5=59a546814cba056c07805f476ff4f998CAS | 15081836PubMed |
Brown, J. L., Olson, D., Keele, M., and Freeman, E. W. (2004b). Survey of the reproductive status of Asian and African elephants in North America. Zoo Biol. 23, 309–321.
| Survey of the reproductive status of Asian and African elephants in North America.Crossref | GoogleScholarGoogle Scholar |
Clubb, R., Rowcliffe, M., Lee, P., Mar, K. U., Moss, C., and Mason, G. J. (2009). Fecundity and population viability in female zoo elephants: problems and possible solutions. Anim. Welf. 114, 237–247.
Dekkers, O. M., Lagro, J., Burman, P., Jørgensen, J. O., Romijn, J. A., and Pereira, A. M. (2010). Recurrence of hyperprolactinaemia after withdrawal of dopamine agonists: systematic review and meta-analysis. J. Clin. Endocrinol. Metab. 95, 43–51.
| Recurrence of hyperprolactinaemia after withdrawal of dopamine agonists: systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGhsro%3D&md5=deda038b81ea1ca29a3174e6ae6facf1CAS | 19880787PubMed |
Doknic, M., Pekic, S., Zarkovic, M., Medic-Stojanoska, M., Dieguez, C., Casanueva, F., and Popovic, V. (2002). Dopaminergic tone and obesity: an insight from prolactinomas treated with bromocriptine. Eur. J. Endocrinol. 147, 77–84.
| Dopaminergic tone and obesity: an insight from prolactinomas treated with bromocriptine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvVCksb4%3D&md5=952fd6f2cc1dcced827dd59190ad38b1CAS | 12088923PubMed |
Dow, T. L., Holásková, I., and Brown, J. L. (2011). Results of the third reproductive assessment survey of North American Asian (Elephas maximus) and African (Loxodonta africana) female elephants. Zoo Biol. 29, 1–13.
Faust, L. J., Thompson, S. D., and Earnhardt, J. M. (2006). Is reversing the decline of Asian elephants in North American zoos possible? An individual-based modelling approach. Zoo Biol. 25, 201–218.
| Is reversing the decline of Asian elephants in North American zoos possible? An individual-based modelling approach.Crossref | GoogleScholarGoogle Scholar |
Freeman, E. W., Guangnano, G., Olson, D., Keele, M., and Brown, J. L. (2009). Social factors influence ovarian acyclicity in captive African elephants (Loxodonta africana). Zoo Biol. 28, 1–15.
| Social factors influence ovarian acyclicity in captive African elephants (Loxodonta africana).Crossref | GoogleScholarGoogle Scholar | 19358314PubMed |
Freeman, M. E., Kanyicska, B., Lerant, A., and Nagy, G. (2000). Prolactin: structure, function and regulation of secretion. Physiol. Rev. 80, 1523–1631.
| 1:CAS:528:DC%2BD3cXnsVKisLY%3D&md5=5c7b4b3358e526d59c059526953dd53cCAS | 11015620PubMed |
Gitay-Goren, H., Lindenbaum, E. S., and Kraiem, Z. (1989). Effects of prolactin on steroidogenesis and cAMP accumulation in rat luteal cell cultures. Mol. Cell. Endocrinol. 65, 195–201.
| Effects of prolactin on steroidogenesis and cAMP accumulation in rat luteal cell cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlt1OgtL0%3D&md5=76ca4e6ad43e9b4f068e9e5ba4fa8551CAS | 2476349PubMed |
Hermes, R., Olson, D., Goeritz, F., Brown, J. L., Schmitt, D. L., Hagan, D., Peterson, J. S., Fritsch, G., and Hildebrandt, T. B. (2000). Ultrasonography of the sexual cycle in female African elephants (Loxodonta africana). Zoo Biol. 19, 369–382.
| Ultrasonography of the sexual cycle in female African elephants (Loxodonta africana).Crossref | GoogleScholarGoogle Scholar |
Hodges, J. K. (1998). Endocrinology of the ovarian cycle and pregnancy in the Asian (Elephas maximus) and African (Loxodonta africana) elephant. Anim. Reprod. Sci. 53, 3–18.
| Endocrinology of the ovarian cycle and pregnancy in the Asian (Elephas maximus) and African (Loxodonta africana) elephant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXns1yksLs%3D&md5=77469f34397684ad46b00b8391d154b1CAS | 9835363PubMed |
Hodges, J. K., van Aarde, R. J., Heistermann, M., and Hoppen, H. O. (1994). Progestin content and biosynthetic potential of the corpus luteum of the African elephant (Loxodonta africana). J. Reprod. Fertil. 102, 163–168.
| Progestin content and biosynthetic potential of the corpus luteum of the African elephant (Loxodonta africana).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXit12rtLY%3D&md5=1653733d38e73c531d5b43f428f10803CAS | 7799309PubMed |
Hodges, J. K., Heistermann, M., Beard, A., and van Aarde, R. J. (1997). Concentrations of progesterone and the 5-α-reduced progestins, 5-α-pregnane-3, 20-dione and 3-α-hydroxy-5-α-pregnan-20-one, in luteal tissue and circulating blood, and their relationship to luteal function in the African elephant. Biol. Reprod. 56, 640–646.
| Concentrations of progesterone and the 5-α-reduced progestins, 5-α-pregnane-3, 20-dione and 3-α-hydroxy-5-α-pregnan-20-one, in luteal tissue and circulating blood, and their relationship to luteal function in the African elephant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXht1GjtLk%3D&md5=ce328e766cc940a088c9f393b0c07f56CAS | 9047008PubMed |
Jones, E. E. (1989). Hyperprolactinaemia and female infertility. J. Reprod. Med. 34, 117–126.
| 1:STN:280:DyaL1M7nvVeguw%3D%3D&md5=8627bd0a016563bcd7ec70100236c978CAS | 2647973PubMed |
Kapustin, N., Critser, J. K., Olson, D., and Malven, P. V. (1996). Nonluteal oestrous cycles of 3-week duration are initiated by anovulatory luteinising hormone peaks in African elephants. Biol. Reprod. 55, 1147–1154.
| Nonluteal oestrous cycles of 3-week duration are initiated by anovulatory luteinising hormone peaks in African elephants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmtlaqtb0%3D&md5=0e3d17bd0a1e0f18f601fb976f044d80CAS | 8902228PubMed |
Lamprecht, S. A., Lindner, H. R., and Strauss, J. F. (1969). Induction of 20α-hydroxysteroid dehydrogenase in rat corpora lutea by pharmacological blockage of pituitary prolactin secretion. Biochim. Biophys. Acta 187, 133–143.
| 1:CAS:528:DyaF1MXksl2ntbs%3D&md5=e4f95b02bf658502bdda590d74b88e6cCAS | 5811200PubMed |
Larsen, J. L., Bhana, A., and Odell, W. D. (1990). Prolactin inhibition of pregnant mare’s serum stimulated follicle development in the rat ovary. Endocrinol. Res. 16, 449–459.
| Prolactin inhibition of pregnant mare’s serum stimulated follicle development in the rat ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsFWjtrs%3D&md5=f10a057ea2ada1e7350d946c751a8d4eCAS |
La Torre, D., and Falorni, A. (2007). Pharmacological causes of hyperprolactinaemia. Ther. Clin. Risk Manage. 3, 929–951.
| 1:CAS:528:DC%2BD2sXhsVGrtLjM&md5=1e9a48e4ed386428ac6d54abe1919839CAS |
Lebedeva, I. Y., Denisenko, V. U., Leebedeva, V. A., and Kuzmina, T. I. (1998). Prolactin in follicular fluid and intracellular store calcium in follicular cells are related to morphological signs of ovarian follicle atresia in cows: work in progress. Theriogenology 49, 509–519.
| Prolactin in follicular fluid and intracellular store calcium in follicular cells are related to morphological signs of ovarian follicle atresia in cows: work in progress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtFShurY%3D&md5=54480d26995b8c05de8b0d2db15eaabbCAS | 10732030PubMed |
Li, C. H., Chung, D., Bewley, T. A., and Cabrera, C. M. (1987). Elephant prolactin: isolation and characterization. Int. J. Pept. Protein Res. 29, 472–477.
| Elephant prolactin: isolation and characterization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXktlegtrk%3D&md5=f731c1e4fee373101c23c4d96ce110bfCAS | 3596899PubMed |
Li, C. H., Oosthuizen, M. M. J., and Chung, D. (1989). Primary structure of elephant pituitary prolactin. Int. J. Pept. Protein Res. 33, 67–69.
| Primary structure of elephant pituitary prolactin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlt1Oitbg%3D&md5=0807361bc24f13a0125ac6293f829b05CAS | 2722400PubMed |
Li, W. L., Liu, Y., Yu, Y. C., Huang, Y. M., Liang, S. D., and Shi, Z. D. (2011). Prolactin plays a stimulatory role in ovarian follicular development and egg-laying in chicken hens. Domest. Anim. Endocrinol. 41, 57–66.
| Prolactin plays a stimulatory role in ovarian follicular development and egg-laying in chicken hens.Crossref | GoogleScholarGoogle Scholar | 21600726PubMed |
Lieberman, M. E., Maurer, R. A., and Gorski, J. (1978). Oestrogen control of prolactin synthesis in vitro. Proc. Natl. Acad. Sci. USA 75, 5946–5949.
| Oestrogen control of prolactin synthesis in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXotFaiuw%3D%3D&md5=0c3718dd94943853513ca111ec9e6464CAS | 282615PubMed |
Lueders, I., Niemuller, C., Gray, C., Rich, P., and Hildebrandt, T. (2010). Luteogenesis during the oestrous cycle in Asian elephants (Elephas maximus). Reproduction 140, 777–786.
| Luteogenesis during the oestrous cycle in Asian elephants (Elephas maximus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFCntr7I&md5=999607110e5197edf333298e61a42db6CAS | 20798219PubMed |
Mah, P. M., and Webster, J. (2002). Hyperprolactinaemia: aetiology, diagnosis, and management. Semin. Reprod. Med. 20, 365–374.
| Hyperprolactinaemia: aetiology, diagnosis, and management.Crossref | GoogleScholarGoogle Scholar | 12536359PubMed |
Martel, C., Labrie, C., Couët, J., Dupont, E., Trudel, C., Luu-The, V., Takahashi, M., Pelletier, G., and Labrie, F. (1990). Effects of human chorionic gonadotropin (hCG) and prolactin (PRL) on 3 beta-hydroxy-5-ene-steroid dehydrogenase/delta 5-delta 4 isomerase (3beta-HSD) expression and activity in the rat ovary. Mol. Cell. Endocrinol. 72, R7–R13.
| Effects of human chorionic gonadotropin (hCG) and prolactin (PRL) on 3 beta-hydroxy-5-ene-steroid dehydrogenase/delta 5-delta 4 isomerase (3beta-HSD) expression and activity in the rat ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXls1Glt7o%3D&md5=bcd41de292369007063da32a3338b857CAS | 2149342PubMed |
Matsuyama, S., Shiota, K., and Takahashi, M. (1990). Possible role of transforming growth factor-beta as a mediator of luteotropic action of prolactin in rat luteal cell cultures. Endocrinology 127, 1561–1567.
| Possible role of transforming growth factor-beta as a mediator of luteotropic action of prolactin in rat luteal cell cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmtVGnsb0%3D&md5=5f5bf1721288b0e2128c30626c20e7e7CAS | 2401226PubMed |
Meites, J., Lu, K. H., Wuttke, W., Welsch, C. W., Nagasawa, H., and Quadri, S. K. (1972). Recent studies on functions and control of prolactin secretion in rats. Recent Prog. Horm. Res. 28, 471–526.
| 1:STN:280:DyaE3s7itlShug%3D%3D&md5=c7ebbc35f1595fd19d250ebf4c1885abCAS | 4569231PubMed |
Meyer, J., Ball, R., and Brown, J. L. (2004). Why are so many elephants in captivity not cycling? Evidence of an association between ovarian inactivity and hyperprolactinaemia. JEMA 15, 9–15.
Morishige, W. K., and Rothchild, I. (1974). Temporal aspects of regulation of corpus luteum function by luteinising hormone, prolactin and placental luteotropin during the first half of pregnancy in the rat. Endocrinology 95, 260–274.
| Temporal aspects of regulation of corpus luteum function by luteinising hormone, prolactin and placental luteotropin during the first half of pregnancy in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXlsVKiu7g%3D&md5=ddb0a259179b898b06ad04cc87e6d5f5CAS | 4857736PubMed |
Nicosia, S., Olivia, D., Giannattasio, G., and Spada, A. (1983). The role of vasoactive intestinal polypeptide (VIP) as a hypothalamic neurohormone. J. Endocrinol. Invest. 6, 235–240.
| 1:CAS:528:DyaL3sXlsFaisLk%3D&md5=4d320858478f34e1f8bec666905546d1CAS | 6311891PubMed |
Prado-Oviedo, N. (2011). Role of oestrogens in hyperprolactinaemia: induced acyclicity in African female elephants. M.Sc. Thesis, American University, Washington, DC.
Rillema, J. A. (1994). Development of the mammary gland and lactation. Trends Endocrinol. Metab. 5, 149–154.
| Development of the mammary gland and lactation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlslSmu7o%3D&md5=ab3e9e546a6fa5c97060caef3d00ba5fCAS | 18407201PubMed |
Rillema, J. A. (1998). Actions of prolactin. In ‘Encyclopedia of Reproduction. Vol. 4’. 3rd edn. (Eds E. Knobil and J. Neill.) pp. 39–43. (Academic Press: London.)
Smith, M. F., McIntush, E. W., Ricke, W. A., Kojima, F. N., and Smith, G. W. (1999). Regulation of ovarian extracellular matrix remodelling by metalloproteases and their tissue inhibitors: effects on follicular development, ovulation and luteal function. J. Reprod. Fertil. Suppl. 54, 367–381.
| 1:CAS:528:DyaK1MXnslSit7o%3D&md5=be226d22e93261c6d62abe035755ee95CAS | 10692869PubMed |
Tashjian, A. H., Barowsky, N. J., and Jensen, D. K. (1971). Thyrotropin-releasing hormone: direct evidence for stimulation of prolactin production by pituitary cells in culture. Biochem. Biophys. Res. Commun. 43, 516–523.
| Thyrotropin-releasing hormone: direct evidence for stimulation of prolactin production by pituitary cells in culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXktlSlurc%3D&md5=1365e64812b00f5740be2b535c5e1a0eCAS | 4327442PubMed |
Tsai-Morris, C. H., Ghosh, M., Hirshfield, A. N., Wise, P. M., and Brodie, A. M. (1983). Inhibition of ovarian aromatase by prolactin in vivo. Biol. Reprod. 29, 342–346.
| Inhibition of ovarian aromatase by prolactin in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlsFamsLw%3D&md5=cb0bb47df9eb1ca34083913370cc956aCAS | 6685537PubMed |
Webster, J., and Scanlon, M. F. (1997). Prolactinomas. In ‘Clinical Endocrine Oncology’. (Eds R. Sheaves, P. J. Jenkins and J. A. Wass.) pp. 189–194. (Blackwell Science: Oxford, UK.)
Woolf, P. D. (1986). Differential diagnosis of hyperprolactinaemia: physiological and pharmacological factors. In ‘Prolactinomas: Contemporary Issues in Endocrinology and Metabolism. Vol 2’. (Eds J. M. Olefsky and R. J. Robbins.) pp. 43–65. (Churchill Livingstone: New York.)
Yamamoto, Y., Yamamoto, T., Watanabe, G., Yuto, N., Keio, M., Narushima, E., Katayanagi, M., Nakao, R., Morikubo, S., Sakurai, Y., Kaneko, M., Kaewmanee, S., and Taya, K. (2010). Prolactin secretion and ovarian function in cycling and non-cycling African female elephants (Loxodonta africana). J. Vet. Med. Sci. 72, 845–852.
| Prolactin secretion and ovarian function in cycling and non-cycling African female elephants (Loxodonta africana).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyktb7O&md5=cce2b1e97f9f3e5a7c67e828fc815bd9CAS | 20179385PubMed |
Yoshimura, Y., Tada, S., Oda, T., Nakamura, Y., Maruyama, K., Ichikawa, F., Ebihara, T., Hirota, Y., Sawada, T., and Kawakami, S. (1989). Direct inhibitory ovarian effects of prolactin in the process of ovulation. Nippon Sanka Fujinka Gakkai Zasshi 41, 83–89.
| 1:STN:280:DyaL1M7ns1GhsA%3D%3D&md5=d526bc3616af30f5ae0bfd7c897ebb32CAS | 2926197PubMed |
Yoshimura, Y., Maruyana, K., Shiraki, M., Kawakami, S., Fukushima, M., and Nakamura, Y. (1990). Prolactin inhibits plasminogen activator activity in the preovulatory follicles. Endocrinology 126, 631–636.
| Prolactin inhibits plasminogen activator activity in the preovulatory follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXntVCisA%3D%3D&md5=21a7665d5a1bd5c61711c684a1afd46fCAS | 2294009PubMed |
Yoshimura, Y., Nakamura, Y., Yamada, H., Ando, M., Ubukata, Y., Oda, T., and Suzuki, M. (1991). Possible contribution of prolactin in the process of ovulation and oocyte maturation. Horm. Res. 35, 22–32.
| Possible contribution of prolactin in the process of ovulation and oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlvFyqt7g%3D&md5=584df03f83dea1a22f9112768b4ae257CAS | 1752600PubMed |
Yoshimura, Y., Nakamura, Y., Oda, T., Ando, M., Ubukata, Y., Koyama, N., Karube, M., and Yamada, H. (1992). Effects of prolactin on ovarian plasmin generation in the process of ovulation. Biol. Reprod. 46, 322–327.
| Effects of prolactin on ovarian plasmin generation in the process of ovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhsVCgs7s%3D&md5=b4d12b16b18d31eda5b4aea157287dc6CAS | 1535514PubMed |
Yu, M. C., Gerkins, V. R., Henderson, B. E., Brown, J. B., and Pike, M. C. (1981). Elevated levels of prolactin in nulliparous women. Br. J. Cancer 43, 826–831.
| Elevated levels of prolactin in nulliparous women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXltlShu7k%3D&md5=618e75c4c4cb2af8764e6a9764aac0f0CAS | 7248160PubMed |
Zadworny, D., Shimada, K., Ishida, H., and Sato, K. (1989). Gonadotrophin-stimulated oestradiol production in small ovarian follicles of the hen is suppressed by physiological concentrations of prolactin in vitro. Gen. Comp. Endocrinol. 74, 468–473.
| Gonadotrophin-stimulated oestradiol production in small ovarian follicles of the hen is suppressed by physiological concentrations of prolactin in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXktVClt7Y%3D&md5=7b9ad3d1c517243f0f018585be6cf175CAS | 2744414PubMed |
