Ovariectomy increases the phenotypic plasticity of the female prostate epithelium in the Mongolian gerbil (Meriones unguiculatus)
Marianna Zanatelli A , Ana M. G. Custodio A , Manoel F. Biancardi B , Fernanda C. A. Santos B , Rejane M. Góes A C , Luiz R. Falleiros-Jr C , Patricia S. L. Vilamaior C and Sebastião R. Taboga A C D
+ Author Affiliations
- Author Affiliations
A Department of Structural and Functional Biology, Institute of Biology, State University of Campinas, UNICAMP, Campinas, SP, Brazil.
B Department of Morphology, Federal University of Goiás, UFG, Goiânia, GO, Brazil.
C Laboratory of Microscopy and Microanalysis, Department of Biology, São Paulo State University, UNESP/IBILCE, R Cristovão Colombo, 2265, 15054-000, São José do Rio Preto, São Paulo, Brazil.
D Corresponding author. Email: taboga@ibilce.unesp.br
Reproduction, Fertility and Development 29(9) 1751-1762 https://doi.org/10.1071/RD16037
Submitted: 21 January 2016 Accepted: 7 September 2016 Published: 14 October 2016
Abstract
The female prostate is a reproductive gland that typically presents a morphology similar to that of the male gland and is highly developed in female Mongolian gerbils. Two main cell populations compose the epithelium gland: basal and secretory luminal cells. However, during postnatal development, diverse secretory cell phenotypes are distributed among the typical ones. Prostate homeostasis is under the control of sexual hormones, such as oestrogen and progesterone. After hormonal deprivation the female gland undergoes several morphophysiological changes. The objective of this study was to identify and characterise, structurally and ultrastructurally, the cellular heterogeneity of the female prostate epithelium in normal conditions and after ovariectomy. Histological routine stains, such as haematoxylin–eosin, periodic acid–Schiff and silver impregnation, as well as immunocytochemical techniques were used to enable identification of the different cell types. Some secretory cells types were identified and characterised as mucinous, basophil, clear, ciliated, droplet, spumous and neuroendocrine cells. Population tally data showed that the hormonal suppression caused by ovariectomy resulted in a decrease in the proportions of basophil and clear cells and an increase in spumous cells. Thus, the secretory epithelial cells of the female gerbil prostate are not morphologically and functionally uniform, presenting a phenotypical plasticity according to the hormonal environment in which they operate.
Additional keywords: cell types, electron microscopy, hormonal deprivation, immunocytochemistry, secretory cells.
References
Abrahamsson, P. A. (1999a). Neuroendocrine cells in tumor growth of the prostate. Endocr. Relat. Cancer 6, 503–519.| Neuroendocrine cells in tumor growth of the prostate.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ptlWntQ%3D%3D&md5=8c615c49b5257bd5022a754fc0d3cfcdCAS | 10730904PubMed |
Abrahamsson, P. A. (1999b). Neuroendocrine differentiation in prostatic carcinoma. Prostate 39, 135–148.
| Neuroendocrine differentiation in prostatic carcinoma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivF2gtL8%3D&md5=aee260bcf5734f3e5cf6fa02138696d3CAS | 10221570PubMed |
Addiego, F., Belzer, E. G., Comolli, J., Moger, W., Perry, J. D., and Whipple, B. (1981). Female ejaculation: a case study. J. Sex Res. 17, 13–21.
| Female ejaculation: a case study.Crossref | GoogleScholarGoogle Scholar |
Amorino, G. P., and Parsons, S. J. (2004). Neuroendocrine cells in prostate cancer. Crit. Rev. Eukaryot. Gene Expr. 14, 287–300.
| Neuroendocrine cells in prostate cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Gqtb8%3D&md5=0afd2b77bfde3f3c48d8d53d0cb30d02CAS | 15663358PubMed |
Bancroft, J. D., and Gamble, M. (2002). ‘Theory and Practice of Histological Techniques’. (Churchill Livingstone: New York.)
Campos, S. G., Gonçalves, B. F., Scarano, W. R., Corradi, L. S., Santos, F. C., Custodio, A. M., Vilamaior, P. S., Góes, R. M., and Taboga, S. R. (2010). Tissue changes in senescent gerbil prostate after hormone deprivation leads to acquisition of androgen insensitivity. Int. J. Exp. Pathol. 91, 394–407.
| Tissue changes in senescent gerbil prostate after hormone deprivation leads to acquisition of androgen insensitivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjslelsQ%3D%3D&md5=334743c4b0320cc15f2704d9b8669319CAS | 20353424PubMed |
Cozzi, P. J., Wang, J., Delprado, W., Perkins, A. C., Allen, B. J., Russel, P. J., and Li, Y. (2005). MUC1, MUC2, MUC4, MUC5AC and MUC6 expression in the progression of prostate cancer. Clin. Exp. Metastasis 22, 565–573.
| MUC1, MUC2, MUC4, MUC5AC and MUC6 expression in the progression of prostate cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsVyiu7c%3D&md5=d3ed12d3f469c6e35d4119133147ddaeCAS | 16475027PubMed |
Custódio, A. M. G., Góes, R. M., and Taboga, S. R. (2004). Acid phosphatase activity in gerbil prostate: comparative study in male and female during postnatal development. Cell Biol. Int. 28, 335–344.
| Acid phosphatase activity in gerbil prostate: comparative study in male and female during postnatal development.Crossref | GoogleScholarGoogle Scholar |
Custodio, A. M., Santos, F. C., Campos, S. G., Vilamaior, P. S., Góes, R. M., and Taboga, S. R. (2008). Aging effects on the Mongolian gerbil female prostate (Skene’s paraurethral glands): structural, ultrastructural, quantitative, and hormonal evaluations. Anat. Rec. (Hoboken) 291, 463–474.
| Aging effects on the Mongolian gerbil female prostate (Skene’s paraurethral glands): structural, ultrastructural, quantitative, and hormonal evaluations.Crossref | GoogleScholarGoogle Scholar | 18231985PubMed |
Custodio, A. M., Santos, F. C., Campos, S. G., Vilamaior, P. S., Oliveira, S. M., Góes, R. M., and Taboga, S. R. (2010). Disorders related with ageing in the gerbil female prostate (Skene’s paraurethral glands). Int. J. Exp. Pathol. 91, 132–143.
| Disorders related with ageing in the gerbil female prostate (Skene’s paraurethral glands).Crossref | GoogleScholarGoogle Scholar | 20041966PubMed |
Da Silva, D. A., Zanatelli, M., Shinohara, F. Z., Góes, R. M., Dos Santos, F. C., Vilamaior, P. S., and Taboga, S. R. (2013). Effects of exposure to estradiol and estradiol plus testosterone on the Mongolian gerbil (Meriones unguiculatus) female prostate. Microsc. Res. Tech. 76, 486–495.
| Effects of exposure to estradiol and estradiol plus testosterone on the Mongolian gerbil (Meriones unguiculatus) female prostate.Crossref | GoogleScholarGoogle Scholar | 23529937PubMed |
Di Sant’Agnese, P. A. (1992). Neuroendocrine differentiation in human prostatic carcinoma. Hum. Pathol. 23, 287–296.
| Neuroendocrine differentiation in human prostatic carcinoma.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383htVWisg%3D%3D&md5=be267bec2262d4384e8ca956d0b28f48CAS | 1313390PubMed |
Dodson, M. K., Cliby, W. A., Pettavel, P. P., Keeney, G. L., and Podratz, K. C. (1995). Female urethral adenocarcinoma: evidence for more than one tissue of origin? Gynecol. Oncol. 59, 352–357.
| Female urethral adenocarcinoma: evidence for more than one tissue of origin?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28%2FpsFOnuw%3D%3D&md5=a30e996e7406b262d7b9480bb0458346CAS | 8522254PubMed |
Fochi, R. A., Perez, A. P., Bianchi, C. V., Rochel, S. S., Góes, R. M., Vilamaior, P. S., Taboga, S. R., and Santos, F. C. (2008). Hormonal oscillations during the estrous cycle influence the morphophysiology of the gerbil (Meriones unguiculatus) female prostate (Skene paraurethral glands). Biol Reprod. 79, 1084–1091.
| Hormonal oscillations during the estrous cycle influence the morphophysiology of the gerbil (Meriones unguiculatus) female prostate (Skene paraurethral glands).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVCltL%2FI&md5=89f871b2340534831d8cbf3f39cc6004CAS | 18685125PubMed |
Fochi, R. A., Santos, F. C., Goes, R. M., and Taboga, S. R. (2013). Progesterone as a morphological regulatory factor of the male and female gerbil prostate. Int. J. Exp. Pathol. 94, 373–386.
| Progesterone as a morphological regulatory factor of the male and female gerbil prostate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslKnsrnF&md5=a4e92c56d89644ed6bf4e8fa33fc037fCAS | 24205795PubMed |
Gross, S. A., and Didio, L. J. A. (1987). Comparative morphology of the prostate in adult male and female of Praomys (mastomys) natalensis studies with electron microscopy. J. Submicrosc. Cytol. 19, 77–84.
| 1:STN:280:DyaL2s7mvFyrtA%3D%3D&md5=70a2426e8ae66d60d706a7d856973948CAS | 3560297PubMed |
Hines, T. M. (2001). The G-spot: a modern gynecologic myth. Am. J. Obstet. Gynecol. 185, 359–362.
| The G-spot: a modern gynecologic myth.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvnsFWkug%3D%3D&md5=565ed3ad454cb0981732da40239cec75CAS | 11518892PubMed |
Howell, W. M., and Black, D. A. (1980). Controlled silver staining of nucleolus organizer regions with protective colloidal developer. I. Step method. Experientia 36, 1014–1015.
| Controlled silver staining of nucleolus organizer regions with protective colloidal developer. I. Step method.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M%2Fms12kug%3D%3D&md5=022ef46da8f16ebb3764b4dc4be406b7CAS | 6160049PubMed |
Ingelmo, I., Gomez, V., Martin, R., Codesal, J., Rodriguez, R., Pozuelo, J. M., and Santamaria, 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=e95fed84e19197b691dee79b190488d1CAS | 17541972PubMed |
Legrier, M. E., Pinieux, G. D., Boye, K., Arvelo, F., Judde, J. G., Fontaine, J. J., Bara, J., and Poupon, M. F. (2004). Mucinous differentiation features associated with hormonal escape in a human prostate cancer xenograft. Br. J. Cancer 90, 720–727.
| Mucinous differentiation features associated with hormonal escape in a human prostate cancer xenograft.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXoslKjtQ%3D%3D&md5=6e96ce73e2e1be2879dde1f96b2d2c1cCAS | 14760390PubMed |
Montuenga, L. M., Guembe, L., Burrell, M. A., Bodegas, M. E., Calvo, A., Sola, J. J., Sesma, P., and Villaro, A. C. (2003). The diffuse endocrine system: from embryogenesis to carcinogenesis. Prog. Histochem. Cytochem. 38, 153–272.
| The diffuse endocrine system: from embryogenesis to carcinogenesis.Crossref | GoogleScholarGoogle Scholar |
Oliveira, S. M., Santos, F. C., Corradi, L. S., Goes, R. M., Vilamaior, P. S., and Taboga, S. R. (2011). Microscopic evaluation of proliferative disorders in the gerbil female prostate: evidence of aging and the influence of multiple pregnancies. Micron. 42, 712–717.
| Microscopic evaluation of proliferative disorders in the gerbil female prostate: evidence of aging and the influence of multiple pregnancies.Crossref | GoogleScholarGoogle Scholar | 21531142PubMed |
Perez, A. P., Biancardi, M. F., Góes, R. M., dos Santos, F. A., and Taboga, S. R. (2011). Exposure to ethinylestradiol during prenatal development and postnatal supplementation with testosterone causes morphophysiological alterations in the prostate of male and female adult gerbils. Int. J. Exp. Pathol. 92, 121–130.
| Exposure to ethinylestradiol during prenatal development and postnatal supplementation with testosterone causes morphophysiological alterations in the prostate of male and female adult gerbils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtVKjsrk%3D&md5=64be7b3aaddbac5bee594b846afb6cffCAS | 21314741PubMed |
Rochel, S. S., Bruni-Cardoso, A., Taboga, S. R., Vilamaior, P. S., and Góes, R. M. (2007). Lobe identity in the Mongolian gerbil prostatic complex: a new rodent model for prostate study. Anat. Rec. (Hoboken) 290, 1233–1247.
| Lobe identity in the Mongolian gerbil prostatic complex: a new rodent model for prostate study.Crossref | GoogleScholarGoogle Scholar | 17724712PubMed |
Rodríguez, R., Pozuelo, J. M., Martín, R., Henriques-Gil, N., Haro, M., Arriazu, R., and Santamaría, L. (2003). Presence of neuroendocrine cells during postnatal development in rat prostate: immunohistochemical, molecular, and quantitative study. Prostate 57, 176–185.
| Presence of neuroendocrine cells during postnatal development in rat prostate: immunohistochemical, molecular, and quantitative study.Crossref | GoogleScholarGoogle Scholar | 12949942PubMed |
Santos, F. C. A., and Taboga, S. R. (2006). Female prostate: a review about the biological repercussions of this gland in humans and rodents. Anim. Reprod. 3, 3–18.
Santos, F. C., Carvalho, H. F., Góes, R. M., and Taboga, S. R. (2003). Structure, histochemistry, and ultrastructure of the epithelium and stroma in the gerbil (Meriones unguiculatus) female prostate. Tissue Cell 35, 447–457.
| Structure, histochemistry, and ultrastructure of the epithelium and stroma in the gerbil (Meriones unguiculatus) female prostate.Crossref | GoogleScholarGoogle Scholar | 14580358PubMed |
Santos, F. C., Leite, R. P., Custodio, A. M., Carvalho, K. P., Monteiro-Leal, L. H., Santos, A. B., Goes, R. M., Carvalho, H. F., and Taboga, S. R. (2006). Testosterone stimulates growth and secretory activity of the female prostate in the adult gerbil (Meriones unguiculatus). Biol. Reprod. 75, 370.
| Testosterone stimulates growth and secretory activity of the female prostate in the adult gerbil (Meriones unguiculatus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVWmtbg%3D&md5=2d8a3d084d944e8eb937775c31a5290aCAS | 16707769PubMed |
Santos, F. C. A., Falleiros-Júnior, L. R., Corradi, L. S., Vilamaior, P. S., and Taboga, S. R. (2007). Experimental endocrine therapies promote epithelial cytodifferentiation and ciliogenesis in the gerbil female prostate. Cell Tissue Res. 328, 617–624.
| Experimental endocrine therapies promote epithelial cytodifferentiation and ciliogenesis in the gerbil female prostate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkslWnsb4%3D&md5=b2f360ad373543f205a2289584d70369CAS |
Santos, F. C., Custodio, A. M., Campos, S. G., Vilamaior, P. S., Góes, R. M., and Taboga, S. R. (2008). Antiestrogen therapies affect tissue homeostasis of the gerbil (Meriones unguiculatus) female prostate and ovaries. Biol Reprod. 79, 674–685.
| Antiestrogen therapies affect tissue homeostasis of the gerbil (Meriones unguiculatus) female prostate and ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFCqtbbE&md5=2418d1fd6c7033797269d318272cb427CAS | 18495680PubMed |
Schmidt, S., Franke, M., Lehmann, J., Loch, T., Stöckle, M., and Weicher t-Jacobsen, K. (2001). Prostate-specific antigen in female urine: a prospective study involving 217 women. Urology 57, 717–720.
| Prostate-specific antigen in female urine: a prospective study involving 217 women.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M3ms1ajsQ%3D%3D&md5=017b869b2a4a331d6ba727adc41e7db4CAS | 11306389PubMed |
Schubach, G. (2002). The G-spot is the female prostate. Am. J. Obstet. Gynecol. 186, 850.
| The G-spot is the female prostate.Crossref | GoogleScholarGoogle Scholar | 11967519PubMed |
Shehata, R. (1975). Female prostate in Arvicantihis niloticus and Meriones lybicus. Acta Anat. (Basel) 92, 513–523.
| Female prostate in Arvicantihis niloticus and Meriones lybicus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE28%2FlvVersA%3D%3D&md5=c9e1cc54f912ad37defc4c915c88c7a8CAS | 1237983PubMed |
Shehata, R. (1980). Female prostate and urethral glands in the home rat, Rattus novergicus. Acta Anat. (Basel) 107, 286–288.
| Female prostate and urethral glands in the home rat, Rattus novergicus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c3jvVKgsw%3D%3D&md5=9e94665385405fdf0c6397cecf3e5bf2CAS | 7190348PubMed |
Shinohara, F. Z., Silva, D. A., Zanatelli, M., Góes, R. M., Vilamaior, P. S., Santos, F. C., and Taboga, S. R. (2013). Progesterone restores the female prostate activity in ovariectomized gerbil and may act as competitor of testosterone in intraprostatic environment. Life Sci. 92, 957–966.
| Progesterone restores the female prostate activity in ovariectomized gerbil and may act as competitor of testosterone in intraprostatic environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmsVGitrk%3D&md5=55ac4613750eb095db0303bf28a04a40CAS | 23454442PubMed |
Sloboda, J., Zaviačič, M., Jakubovský, J., Hammar, E., and Johnsen, J. (1998). Metastasizing adenocarcinoma of the female prostate (Skene’s paraurethral glands). Histological and immunohistochemical prostate markers studies and first ultrastructural observation. Pathol. Res. Pract. 194, 129–136.
| Metastasizing adenocarcinoma of the female prostate (Skene’s paraurethral glands). Histological and immunohistochemical prostate markers studies and first ultrastructural observation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3ksFejtw%3D%3D&md5=747ce1ec85066bfd9ff3b67d32ab9c0cCAS | 9584326PubMed |
Tepper, S. L., Jagirdar, J., Heath, D., and Geller, S. A. (1984). Homology between the female paraurethral (Skenes’s) glands and the prostate. Arch. Pathol. Lab. Med. 108, 423–425.
| 1:STN:280:DyaL2c7nslyrtg%3D%3D&md5=48e65b85a7427fca8075e155887397eeCAS | 6546868PubMed |
Uzoaru, I., Akang, E. E., Aghadiuno, P. U., and Nadimpalli, V. R. (1992). Benign cystic ovarian teratomas with prostatic tissue: a report of two cases. Teratology 45, 235–239.
| Benign cystic ovarian teratomas with prostatic tissue: a report of two cases.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38zjs1Wmsw%3D%3D&md5=60a5eb7e91f3c3eed05da807913325f8CAS | 1631777PubMed |
Wernert, N., Gerdes, J., Loy, V., Seitz, G., Scherr, O., and Dhom, G. (1988). Investigations of the estrogen (ER-ICA-test) and progesterone receptor in the prostate and prostatic carcinoma on immunohistochemical basis. Virchows. Archiv. A Pathol. Anat. Histopathol. 412, 387–391.
| Investigations of the estrogen (ER-ICA-test) and progesterone receptor in the prostate and prostatic carcinoma on immunohistochemical basis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c7ks1Gksg%3D%3D&md5=f2c45473f7446fe06bb5e9c7e2013b34CAS |
Wernert, N., Albrecht, M., Sesterhenn, I., Goebbels, R., Bonkhoff, H., Seitz, G., Inniger, R., and Remberger, K. (1992). The ‘female prostate’: location, morphology, immunohistochemical characteristics and significance. Eur. Urol. 22, 64–69.
| 1:STN:280:DyaK3s%2FkvFGnsA%3D%3D&md5=ef29e535959e9852c58dd91cad54c91bCAS | 1385145PubMed |
Zanatelli, M., Silva, D. A., Shinohara, F. Z., Góes, R. M., Santos, F. C., Vilamaior, P. S., and Taboga, S. R. (2014). Actions of oestradiol and progesterone on the prostate in female gerbils: reversal of the histological effects of castration. Reprod. Fertil. Dev. 26, 540–550.
| Actions of oestradiol and progesterone on the prostate in female gerbils: reversal of the histological effects of castration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtVWlsrs%3D&md5=fb030b24cb4ec302055afd00d96bc906CAS | 23677028PubMed |
Zaviačič, M. (1999). ‘The Female Prostate: From Vestigial Skene’s Paraurethral Glands and Ducts to Woman’s Functional Prostate’. (Slovack Academic Press: Slovakia.)
Zaviačič, M., and Ablin, R. J. (2000). The female prostate and prostate-specific antigen. Imunohistochemical localization, implications of this prostate marker in women and reasons for using the term ‘prostate’ in human female. Histol. Histopathol. 15, 131–142.
| 10668204PubMed |
Zaviačič, M., Sidlo, J., and Borovský, M. (1993). Prostate specific antigen and prostate specific acid phosphatase in adenocarcinoma of Skene’s paraurethral glands and ducts. Virchows Arch. A Pathol. Anat. Histopathol. 423, 503–505.
| Prostate specific antigen and prostate specific acid phosphatase in adenocarcinoma of Skene’s paraurethral glands and ducts.Crossref | GoogleScholarGoogle Scholar | 7507278PubMed |
Zaviačič, M., Danihel, L., Ružičková, M., Blažeková, J., Itoh, Y., Okutani, R., and Kaway, T. (1997). Immunohistochemical localization of human protein 1 in the female prostate (Skene’s gland) and the male prostate. Histochem. J. 29, 219–227.
| Immunohistochemical localization of human protein 1 in the female prostate (Skene’s gland) and the male prostate.Crossref | GoogleScholarGoogle Scholar | 9472384PubMed |
Zaviačič, M., Jakubovská, V., Belošovič, J., and Breza, J. (2000a). Ultrastrucuture of the normal adult human female prostate gland (Skene’s gland). Anat. Embryol. (Berl.) 201, 51–61.
| 10603093PubMed |
Zaviačič, M., Zajíčková, M., Blažeková, J., Donárová, L., Stvrtina, S., Mikulecký, M., Zaviačič, T., Holomáň, K., and Breza, J. (2000b). Weight, size, macroanatomy, and histology of the normal prostate in the adult human female: a minireview. J. Histotechnol. 23, 61–69.
| Weight, size, macroanatomy, and histology of the normal prostate in the adult human female: a minireview.Crossref | GoogleScholarGoogle Scholar |
