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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Influence of postnatal prolactin modulation on the development and maturation of ventral prostate in young rats

Ana C. L. Camargo A , Flávia B. Constantino A , Sérgio A. A. Santos A , Ketlin T. Colombelli A , Maeli Dal-Pai-Silva A , Sérgio L. Felisbino and Luis A. Justulin A B
+ Author Affiliations
- Author Affiliations

A Department of Morphology, Institute of Biosciences, Sao Paulo State University, Prof. Dr. Antonio Celso Wagner Zanin Street, 250, Botucatu, SP, 18618-689, Brazil.

B Corresponding author. Email: justulin@ibb.unesp.br

Reproduction, Fertility and Development 30(7) 969-979 https://doi.org/10.1071/RD17343
Submitted: 30 August 2017  Accepted: 15 November 2017   Published: 6 December 2017

Abstract

Besides androgenic dependence, other hormones also influence the prostate biology. Prolactin has been described as an important hormone associated with maintenance of prostatic morphophysiology; however, there is a lack of information on the involvement of prolactin during prostate development and growth. This study aimed to evaluate whether perinatal prolactin modulation interferes with rat ventral prostate (VP) development and maturation. Therefore, prolactin or bromocriptine (an inhibitor of prolactin release from the pituitary) were administered to Sprague Dawley rats from postnatal Day (PND) 12 to PND 21 or 35. Animals were then killed and serum hormonal quantification, VP morphological–stereological and immunohistochemical analyses and western blotting reactions were employed. Our results demonstrate that prolactin blockage increased serum testosterone on PND 21, which reflected an increase in anogenital distance. Although prolactin modulation did not interfere with VP weight, it modified VP morphology by dilating the acinar lumen and reducing epithelial cell height. Prolactin activated the signal transducer and activator of transcription (STAT) downstream pathway, increased androgen receptor expression and epithelial proliferation. In addition, prolactin and bromocriptine also increased expression of cytokeratin 18, a marker of luminal-differentiated cells. In conclusion, the VP responds to prolactin modulation through a mechanism of increasing the epithelial proliferative response and dynamics of cell differentiation, especially in animals treated for a more prolonged period.

Additional keyword: bromocriptine.


References

Ahonen, T. J., Härkönen, P. L., Laine, J., Rui, H., Martikainen, P. M., and Nevalainen, M. T. (1999). Prolactin is a survival factor for androgen-deprived rat dorsal and lateral prostate epithelium in organ culture. Endocrinology 140, 5412–5421.
Prolactin is a survival factor for androgen-deprived rat dorsal and lateral prostate epithelium in organ culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFemur8%3D&md5=6b474ca72e5637725a3fec5aa4465775CAS |

Aruldhas, M. M., Thampi, L. T., Kumari, T. M., and Govindarajulu, P. (1994). Prolactin and bromocriptine induced changes in liver, adipose tissue and blood lipids of mature male bonnet monkeys, Macaca radiata (Geoffroy). Endocr. J. 41, 207–212.
Prolactin and bromocriptine induced changes in liver, adipose tissue and blood lipids of mature male bonnet monkeys, Macaca radiata (Geoffroy).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXksFSns7g%3D&md5=5c111ca4b8e65dcc831108dce87a1379CAS |

Bartke, A., and Klemcke, H. M. K. (1986). Effects of physiological and abnormally elevated prolactin levels on the pituitary–testicular axis. Med. Biol. 63, 264–272.
| 1:STN:280:DyaL283gt1ShtQ%3D%3D&md5=d69afd543364dbfaaa2c52cef266b58bCAS |

Biancardi, M. F., Perez, A. P., Caires, C. R., Falleiros, L. R., Góes, R. M., Vilamaior, P. S., Freitas, D. R., Santos, F. C., and Taboga, S. R. (2017). Prenatal and pubertal testosterone exposure imprint permanent modifications in the prostate that predispose to the development of lesions in old Mongolian gerbils. Asian J. Androl. 19, 160–167.
Prenatal and pubertal testosterone exposure imprint permanent modifications in the prostate that predispose to the development of lesions in old Mongolian gerbils.Crossref | GoogleScholarGoogle Scholar |

Bole-Feysot, C., Goffin, V., Edery, M., Binart, N., and Kelly, P. A. (1998). Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr. Rev. 19, 225–268.
| 1:CAS:528:DyaK1cXktVWhs7k%3D&md5=881d964b72f4c69fc961689e02978e89CAS |

Carón, R. W., Jahn, G. A., and Deis, R. P. (1994). Lactogenic actions of different growth hormone preparations in pregnant and lactating rats. J. Endocrinol. 142, 535–545.
Lactogenic actions of different growth hormone preparations in pregnant and lactating rats.Crossref | GoogleScholarGoogle Scholar |

Chambon, M., Grizard, G., and Boucher, D. (1985). Bromocriptine, a dopamine agonist, directly inhibits testosterone production by rat Leydig cells. Andrologia 17, 172–177.
Bromocriptine, a dopamine agonist, directly inhibits testosterone production by rat Leydig cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXkvVaiu7w%3D&md5=8a14be57f252f22e3029379661246ca5CAS |

Colombelli, K. T., Santos, S. A. A., Camargo, A. C. L., Constantino, F. B., Barquilha, C. N., Rinaldi, J. C., Felisbino, S. L., and Justulin, L. A. (2017). Impairment of microvascular angiogenesis is associated with delay in prostatic development in rat offspring of maternal protein malnutrition. Gen. Comp. Endocrinol. 246, 258–269.
Impairment of microvascular angiogenesis is associated with delay in prostatic development in rat offspring of maternal protein malnutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXjvFOhsw%3D%3D&md5=dc43ac394333a105ba3a9e82389f9f7bCAS |

Crépin, A., Bidaux, G., Vanden-Abeele, F., Dewailly, E., Goffin, V., Prevarskaya, N., and Slomianny, C. (2007). Prolactin stimulates prostate cell proliferation by increasing endoplasmic reticulum content due to SERCA 2b over-expression. Biochem. J. 401, 49–55.
Prolactin stimulates prostate cell proliferation by increasing endoplasmic reticulum content due to SERCA 2b over-expression.Crossref | GoogleScholarGoogle Scholar |

Cunha, G. R. R., Bigsby, R. M. M., Cooke, P. S. S., and Sugimura, Y. (1985). Stromal–epithelial interactions in adult organs. Cell Differ. 17, 137–148.
Stromal–epithelial interactions in adult organs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL28%2FivVWqtg%3D%3D&md5=ccb109fdaa5892cbc6c3d26d2c45dd3bCAS |

Dorshkind, K., and Horseman, N. D. (2000). The roles of prolactin, growth hormone, insulin-like growth factor-I, and thyroid hormones in lymphocyte development and function: insights from genetic models of hormone and hormone receptor deficiency. Endocr. Rev. 21, 292–312.
| 1:CAS:528:DC%2BD3cXlsF2gt7o%3D&md5=a06b1a4f33d0daf4a60858bb6dd8e244CAS |

Ferraris, J., Boutillon, F., Bernadet, M., Seilicovich, A., Goffin, V., and Pisera, D. (2012). Prolactin receptor antagonism in mouse anterior pituitary: effects on cell turnover and prolactin receptor expression. Am. J. Physiol. Endocrinol. Metab. 302, E356–E364.
Prolactin receptor antagonism in mouse anterior pituitary: effects on cell turnover and prolactin receptor expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsFKgsr8%3D&md5=f204b8eee009cfa7f2db6b3428caf0a9CAS |

Fischbeck, K. L., and Rasmussen, K. M. (1987). Effect of repeated reproductive cycles on maternal nutritional status, lactational performance and litter growth in ad libitum-fed and chronically food-restricted rats. J. Nutr. 117, 1967–1975.
| 1:CAS:528:DyaL1cXlsVynug%3D%3D&md5=255683a377140a26fac5991bbb2097ccCAS |

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=290fe1513e12072216f2cda44513dcf9CAS |

Gandelman, R., and Graham, S. (1986). Development of the surgically produced singleton mouse fetus. Dev. Psychobiol. 19, 343–350.
Development of the surgically produced singleton mouse fetus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL283nsFKnsA%3D%3D&md5=4db80343b6d039b3be5127a149740753CAS |

Gilleran, J. P., Putz, O., DeJong, M., DeJong, S., Birch, L., Pu, Y., Huang, L., and Prins, G. S. (2003). The role of prolactin in the prostatic inflammatory response to neonatal estrogen. Endocrinology 144, 2046–2054.
The role of prolactin in the prostatic inflammatory response to neonatal estrogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt1Witrs%3D&md5=e04ce043f7cf038feb73d91a115d7ebbCAS |

Goffin, V., Bernichtein, S., Touraine, P., and Kelly, P. A. (2005). Development and potential clinical uses of human prolactin receptor antagonists. Endocr. Rev. 26, 400–422.
Development and potential clinical uses of human prolactin receptor antagonists.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltVWru7k%3D&md5=b3ca297ba6608530ddadf3c2fc2c0416CAS |

Grattan, D. R. (2015). 60 years of neuroendocrinology: the hypothalamo–prolactin axis. J. Endocrinol. 226, T101–T122.
60 years of neuroendocrinology: the hypothalamo–prolactin axis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFKjsLvM&md5=768220024dee276e8063dbb52d7d4098CAS |

Gualillo, O., Lago, F., García, M., Menéndez, C., Señarís, R., Casanueva, F. F., and Diéguez, C. (1999). Prolactin stimulates leptin secretion by rat white adipose tissue. Endocrinology 140, 5149–5153.
Prolactin stimulates leptin secretion by rat white adipose tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFemt78%3D&md5=8aedbc07bc5b7055a1c88a234184aa71CAS |

Hernandez, M. E., Soto-Cid, A., Rojas, F., Pascual, L. I., Aranda-Abreu, G. E., Toledo, R., Garcia, L. I., Quintanar-Stephano, A., and Manzo, J. (2006). Prostate response to prolactin in sexually active male rats. Reprod. Biol. Endocrinol. 4, 28–39.
Prostate response to prolactin in sexually active male rats.Crossref | GoogleScholarGoogle Scholar |

Herrera-Covarrubias, D., Coria-Avila, G. A., Xicoténcatl, P. C., Fernández-Pomares, C., Manzo, J., Aranda-Abreu, G. E., and Hernández, M. E. (2015). Long-term administration of prolactin or testosterone induced similar precancerous prostate lesions in rats. Exp. Oncol. 37, 13–18.
| 1:STN:280:DC%2BC2Mnns1emsw%3D%3D&md5=28afddd889cab96bc7a2be068ba4b833CAS |

Ingelmo, I., Gomez, V., Martín, R., Codesal, J., Rodríguez, R., Pozuelo, J. M., and Santamara, L. (2007). Effect of prolactin and bromocriptine on the population of prostate neuroendocrine cells from intact and cyproterone acetate-treated rats: stereological and immunohistochemical study. Anat. Rec. (Hoboken) 290, 855–861.
Effect of prolactin and bromocriptine on the population of prostate neuroendocrine cells from intact and cyproterone acetate-treated rats: stereological and immunohistochemical study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXovFahtb0%3D&md5=92de85b51b99c5848e6b0430aae3c264CAS |

Janssen, T., Darro, F., Petein, M., Raviv, G., Pasteels, J. L., Kiss, R., and Schulman, C. C. (1996). In vitro characterization of prolactin-induced effects on proliferation in the neoplastic LNCaP, DU145, and PC3 models of the human prostate. Cancer 77, 144–149.
In vitro characterization of prolactin-induced effects on proliferation in the neoplastic LNCaP, DU145, and PC3 models of the human prostate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlsV2ntg%3D%3D&md5=63cbc7325d763911d5f6d8aba211c012CAS |

Kumar, V. S. H., M. B., V., A. N., P., Aithal, S., Baleed, S. R., and Patil, U. N. (2013). Bromocriptine, a dopamine (d2) receptor agonist, used alone and in combination with glipizide in sub-therapeutic doses to ameliorate hyperglycaemia. J. Clin. Diagn. Res. 7, 1904–1907.

Lee, H.-S. S. (2015). Impact of maternal diet on the epigenome during in utero life and the developmental programming of diseases in childhood and adulthood. Nutrients 7, 9492–9507.
Impact of maternal diet on the epigenome during in utero life and the developmental programming of diseases in childhood and adulthood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XitVGltr3M&md5=f354fc69bb3bee121428d7eecb8a4aacCAS |

Lee, R. C., Walters, J. A., Reyland, M. E., and Anderson, S. M. (1999). Constitutive activation of the prolactin receptor results in the induction of growth factor-independent proliferation and constitutive activation of signaling molecules. J. Biol. Chem. 274, 10024–10034.
Constitutive activation of the prolactin receptor results in the induction of growth factor-independent proliferation and constitutive activation of signaling molecules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXis1GjsbY%3D&md5=8a1f8c97de712c2de46ee262a60817afCAS |

Liu, M., Xu, Y.-F. F., Feng, Y., Zhai, W., Che, J.-P. P., Xia, S.-Q. Q., Wang, G.-C. C., and Zheng, J.-H. H. (2013). Androgen-STAT3 activation may contribute to gender disparity in human simply renal cysts. Int. J. Clin. Exp. Pathol. 6, 686–694.
| 1:CAS:528:DC%2BC3sXlsFCru7c%3D&md5=093921f0e9dc3603e8c8a9cafd28f805CAS |

Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=27001fc4d390214adec9d2e6245c9fd6CAS |

Marano, R. J., and Ben-Jonathan, N. (2014). Minireview: extrapituitary prolactin: an update on the distribution, regulation, and functions. Mol. Endocrinol. 28, 622–633.
Minireview: extrapituitary prolactin: an update on the distribution, regulation, and functions.Crossref | GoogleScholarGoogle Scholar |

Nevalainen, M. T., Valve, E. M., Mäkelä, S. I., Bläuer, M., Tuohimaa, P. J., and Härkönen, P. L. (1991). Estrogen and prolactin regulation of rat dorsal and lateral prostate in organ culture. Endocrinology 129, 612–622.
Estrogen and prolactin regulation of rat dorsal and lateral prostate in organ culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltVKnsbg%3D&md5=f9f18f6c23da789e17e72d6caceb4ed6CAS |

Nevalainen, M. T., Valve, E. M., Ingleton, P. M., Nurmi, M., Martikainen, P. M., and Härkönen, P. L. (1997). Prolactin and prolactin receptors are expressed and functioning in human prostate. J. Clin. Invest. 99, 618–627.
Prolactin and prolactin receptors are expressed and functioning in human prostate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtlSqu7s%3D&md5=53e36bf50ff044b5d31681a891f4f367CAS |

Pérez-Villamil, B., Bordiú, E., and Puente-Cueva, M. (1992). Involvement of physiological prolactin levels in growth and prolactin receptor content of prostate glands and testes in developing male rats. J. Endocrinol. 132, 449–459.
Involvement of physiological prolactin levels in growth and prolactin receptor content of prostate glands and testes in developing male rats.Crossref | GoogleScholarGoogle Scholar |

Prins, G. S. (1992). Neonatal estrogen exposure induces lobe-specific alterations in adult rat prostate androgen receptor expression. Endocrinology 130, 3703–3714.
Neonatal estrogen exposure induces lobe-specific alterations in adult rat prostate androgen receptor expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XksVSrsrs%3D&md5=bf08c96e9e6e1b7b6c487f3cf6842801CAS |

Prins, G. S., and Putz, O. (2008). Molecular signaling pathways that regulate prostate gland development. Differentiation 76, 641–659.
Molecular signaling pathways that regulate prostate gland development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSrsLfO&md5=93a71e739a617f1c68278ace944b76f5CAS |

Prins, G. S., Birch, L., Habermann, H., Chang, W. Y., Tebeau, C., Putz, O., and Bieberich, C. (2001). Influence of neonatal estrogens on rat prostate development. Reprod. Fertil. Dev. 13, 241–252.
Influence of neonatal estrogens on rat prostate development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlslE%3D&md5=a83921106664ae92b15ce11c2cf3093bCAS |

Puchtler, H., Waldrop, F. S., Meloan, S. N., Terry, M. S., and Conner, H. M. (1970). Methacarn (methanol-Carnoy) fixation. Practical and theoretical considerations. Histochemie 21, 97–116.
Methacarn (methanol-Carnoy) fixation. Practical and theoretical considerations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXhtFygtbk%3D&md5=fb8d3d4546cefb41fc4efed7feea39d6CAS |

Radhakrishnan, A., Raju, R., Tuladhar, N., Subbannayya, T., Thomas, J. K., Goel, R., Telikicherla, D., Palapetta, S. M., Rahiman, B. A., Venkatesh, D. D., Urmila, K. K., Harsha, H. C., Mathur, P. P., Prasad, T. S. K., Pandey, A., Shemanko, C., and Chatterjee, A. (2012). A pathway map of prolactin signaling. J. Cell Commun. Signal. 6, 169–173.
A pathway map of prolactin signaling.Crossref | GoogleScholarGoogle Scholar |

Ramaley, J. A. (1981). Serum prolactin levels in the prepubertal period in male and female rats. Control by photoperiod and gonadal status and relationship to puberty onset. Int. J. Androl. 4, 91–104.
Serum prolactin levels in the prepubertal period in male and female rats. Control by photoperiod and gonadal status and relationship to puberty onset.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhtlKrur0%3D&md5=a4f88b02b12478567adfab0ae834b901CAS |

Reiter, E., Lardinois, S., Klug, M., Sente, B., Hennuy, B., Bruyninx, M., Closset, J., and Hennen, G. (1995). Androgen-independent effects of prolactin on the different lobes of the immature rat prostate. Mol. Cell. Endocrinol. 112, 113–122.
Androgen-independent effects of prolactin on the different lobes of the immature rat prostate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXntl2msrg%3D&md5=b71a986ed83d95237b6ca4cdae99b719CAS |

Rinaldi, J. C., Justulin, L. A., Lacorte, L. M., Sarobo, C., Boer, P. A., Scarano, W. R., and Felisbino, S. L. (2013). Implications of intrauterine protein malnutrition on prostate growth, maturation and aging. Life Sci. 92, 763–774.
Implications of intrauterine protein malnutrition on prostate growth, maturation and aging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXks1SisLw%3D&md5=4576ccc4b22bf11fb5d05dc2807dc3a9CAS |

Rojas-Durán, F., Pascual-Mathey, L. I., Serrano, K., Aranda-Abreu, G. E., Manzo, J., Soto-Cid, A. H., and Hernandez, M. E. (2015). Correlation of prolactin levels and PRL-receptor expression with Stat and Mapk cell signaling in the prostate of long-term sexually active rats. Physiol. Behav. 138, 188–192.
Correlation of prolactin levels and PRL-receptor expression with Stat and Mapk cell signaling in the prostate of long-term sexually active rats.Crossref | GoogleScholarGoogle Scholar |

Rozenboim, I., Mobarky, N., Heiblum, R., Chaiseha, Y., Kang, S. W., Biran, I., Rosenstrauch, A., Sklan, D., and El Halawani, M. E. (2004). The role of prolactin in reproductive failure associated with heat stress in the domestic turkey. Biol. Reprod. 71, 1208–1213.
The role of prolactin in reproductive failure associated with heat stress in the domestic turkey.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqtLg%3D&md5=7ede3506fad49d1ed49c09b079e064e8CAS |

Ryníková, A., Koppel, J., Kuchár, S., Cikos, S., and Mozes, S. (1988). Effects of ovine prolactin in infant rats. Exp. Clin. Endocrinol. 92, 241–244.
Effects of ovine prolactin in infant rats.Crossref | GoogleScholarGoogle Scholar |

Sackmann-Sala, L., Guidotti, J.-E., and Goffin, V. (2015a). Minireview: prolactin regulation of adult stem cells. Mol. Endocrinol. 29, 667–681.
Minireview: prolactin regulation of adult stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXosV2rtrs%3D&md5=36dab69da2f26ed089728c405f566902CAS |

Sackmann-Sala, L., Angelergues, A., Boutillon, F., d’Acremont, B., Maidenberg, M., Oudard, S., and Goffin, V. (2015b). Human and murine prostate basal/stem cells are not direct targets of prolactin. Gen. Comp. Endocrinol. 220, 133–142.
Human and murine prostate basal/stem cells are not direct targets of prolactin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXms1Wksbs%3D&md5=d0199aa617d4777c295c48fd92055ea6CAS |

Santos, S. A. A., Rinaldi, J. C., Martins, A. E., Camargo, A. C. L., Leonelli, C., Delella, F. K., Felisbino, S. L., and Justulin, L. A. (2014). Impact of gestational diabetes and lactational insulin replacement on structure and secretory function of offspring rat ventral prostate. Gen. Comp. Endocrinol. 206, 60–71.
Impact of gestational diabetes and lactational insulin replacement on structure and secretory function of offspring rat ventral prostate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVyhurzF&md5=f97485a1c676ee14a87880b5364bcba3CAS |

Schauwecker, S. M., Kim, J. J., Licht, J. D., and Clevenger, C. V. (2017). Histone H1 and chromosomal protein HMGN2 regulate prolactin-induced STAT5 transcription factor recruitment and function in breast cancer cells. J. Biol. Chem. 292, 2237–2254.
Histone H1 and chromosomal protein HMGN2 regulate prolactin-induced STAT5 transcription factor recruitment and function in breast cancer cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXisVGisb0%3D&md5=60b2135879628cdf26c34d89dd44c038CAS |

Shapiro, A., Ron, M., Caine, M., and Kramer, J. (1980). The pharmacological action of bromocriptine on the human prostate. Urol. Res. 8, 25–28.
The pharmacological action of bromocriptine on the human prostate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXktF2jt78%3D&md5=2eca0b841cdfca3970ce7f9e79f8b9f6CAS |

Stoker, T. E., Robinette, C. L., and Cooper, R. L. (1999). Maternal exposure to atrazine during lactation suppresses suckling-induced prolactin release and results in prostatitis in the adult offspring. Toxicol. Sci. 52, 68–79.
Maternal exposure to atrazine during lactation suppresses suckling-induced prolactin release and results in prostatitis in the adult offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns1egtr4%3D&md5=670d1fcbb77f2bd7a59cc3bf137da6b2CAS |

Swan, S. H., Main, K. M., Liu, F., Stewart, S. L., Kruse, R. L., Calafat, A. M., Mao, C. S., Redmon, J. B., Ternand, C. L., Sullivan, S., Teague, J. L., Study for Future Families Research Team (2005). Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ. Health Perspect. 113, 1056–1061.
Decrease in anogenital distance among male infants with prenatal phthalate exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpslSku74%3D&md5=ca07c21e26bead9887599dfa5bffc4f1CAS |

Thankamony, A., Pasterski, V., Ong, K. K., Acerini, C. L., and Hughes, I. A. (2016). Anogenital distance as a marker of androgen exposure in humans. Andrology 4, 616–625.
Anogenital distance as a marker of androgen exposure in humans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtFOkur7E&md5=eb55ed1259eaf5a4d4d8c9547e4f7a13CAS |

Timms, B. G., Mohs, T. J., and Didio, L. J. (1994). Ductal budding and branching patterns in the developing prostate. J. Urol. 151, 1427–1432.
Ductal budding and branching patterns in the developing prostate.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c3htVKltQ%3D%3D&md5=64bd0916e7b7a01362be071951f007d5CAS |

Van Coppenolle, F., Slomianny, C., Carpentier, F., Le Bourhis, X., Ahidouch, A., Croix, D., Legrand, G., Dewailly, E., Fournier, S., Cousse, H., Authie, D., Raynaud, J. P., Beauvillain, J. C., Dupouy, J. P., and Prevarskaya, N. (2001). Effects of hyperprolactinemia on rat prostate growth: evidence of androgeno-dependence. Am. J. Physiol. Endocrinol. Metab. 280, E120–E129.
| 1:CAS:528:DC%2BD3MXjtVWls74%3D&md5=756cefe5dc7d92b283169c533b7641a9CAS |

Weibel, E. R., Kistler, G. S., and Scherle, W. F. (1966). Practical stereological methods for morphometric cytology. J. Cell Biol. 30, 23–38.
Practical stereological methods for morphometric cytology.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF2s7msFersg%3D%3D&md5=967c7377ba236190104bcada610f6226CAS |

Zhang, C., Guo, Y., Cui, J., Zhu, H. H., and Gao, W.-Q. (2013). Cytokeratin 18 is not required for morphogenesis of developing prostates but contributes to adult prostate regeneration. BioMed Res. Int. 2013, 576472.

Zhang, R., Jiao, J., Zhang, W., Zhang, Z., Zhang, W., Qin, L. Q., and Han, S. F. (2016). Effects of cereal fiber on leptin resistance and sensitivity in C57BL/6J mice fed a high-fat/cholesterol diet. Food Nutr. Res. 60, 31690.
Effects of cereal fiber on leptin resistance and sensitivity in C57BL/6J mice fed a high-fat/cholesterol diet.Crossref | GoogleScholarGoogle Scholar |