Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-28T15:27:43.888Z Has data issue: false hasContentIssue false
  • English
  • Français

Female Prostate Development: Morphological Analysis of the Budding Dynamic

Published online by Cambridge University Press:  18 January 2022

Fernanda C. A. dos Santos Open the ORCID record for Fernanda C. A. dos Santos [Opens in a new window] ,
Ana F. P. Negre ,
Daniel A. O. Rodríguez ,
Géssica C. de Sousa ,
Giovanna A. Rodrigues ,
Bruno D. A. Sanches ,
Hernandes F. Carvalho Open the ORCID record for Hernandes F. Carvalho [Opens in a new window] ,
Sebastião R. Taboga  and
Manoel F. Biancardi Open the ORCID record for Manoel F. Biancardi [Opens in a new window]
Fernanda C. A. dos Santos
Affiliation:
Department of Histology, Embryology, and Cell Biology, Federal University of Goiás, Campus Samambaia, Goiânia, Goiás 74690-900, Brazil
Ana F. P. Negre
Affiliation:
Department of Histology, Embryology, and Cell Biology, Federal University of Goiás, Campus Samambaia, Goiânia, Goiás 74690-900, Brazil
Daniel A. O. Rodríguez
Affiliation:
Department of Structural and Functional Biology, State University of Campinas, Campinas, São Paulo 13083-862, Brazil
Géssica C. de Sousa
Affiliation:
Department of Histology, Embryology, and Cell Biology, Federal University of Goiás, Campus Samambaia, Goiânia, Goiás 74690-900, Brazil
Giovanna A. Rodrigues
Affiliation:
Department of Histology, Embryology, and Cell Biology, Federal University of Goiás, Campus Samambaia, Goiânia, Goiás 74690-900, Brazil
Bruno D. A. Sanches
Affiliation:
Department of Structural and Functional Biology, State University of Campinas, Campinas, São Paulo 13083-862, Brazil
Hernandes F. Carvalho
Affiliation:
Department of Structural and Functional Biology, State University of Campinas, Campinas, São Paulo 13083-862, Brazil
Sebastião R. Taboga
Affiliation:
Department of Biology, State University of São Paulo, São José do Rio Preto, São Paulo 15054-000, Brazil
Manoel F. Biancardi*
Affiliation:
Department of Histology, Embryology, and Cell Biology, Federal University of Goiás, Campus Samambaia, Goiânia, Goiás 74690-900, Brazil
*
*Corresponding author: Manoel F. Biancardi, E-mail: [email protected]
Get access

Abstract

The presence of the prostate in female mammals has long been known. However, pieces of information related to its development are still lacking. The aim of this study was to explore the budding dynamic during the initial prostate development in female gerbils. Pregnant females were timed, the fetuses were euthanized, and the urogenital sinus was dissected out between the embryonic days 20 and 24 (E20–E24 groups). Newborn pups (1-day-old; P1 group) underwent the same procedures. The female prostate development was based on epithelial buds which arose far from the paraurethral mesenchyme (PAM). The epithelial buds reached the PAM at prenatal day 24, crossing a small gap in the smooth muscle layer between the periurethral mesenchyme (PEM) and the PAM. Steroid nuclear receptors such as the androgen receptor and estrogen receptor alpha were localized in the PEM through the urethral wall, although some epithelial labeling was also present in the urogenital sinus epithelium (UGE). P63-positive cells were found only in the UGE, becoming restricted to the basal compartment after the 23rd prenatal day. The results showed that the gerbil female prostate exhibits a distinct budding pattern as compared to the male prostate development.

Keywords

femalegerbilorganogenesisparaurethral mesenchymeperiurethral mesenchyme
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 28 , Issue 1 , February 2022 , pp. 272 - 280
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of the Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aguiar, ACS, Rodrigues, MMP, Fonseca-Alves, CE, Santos, FCA, Vilamaior, PSL, Taboga, SR & Laufer-Amorim, R (2013). Female paraurethral prostate gland in bitches. Braz J Vet Pathol 6, 106–110.Google Scholar
Allgeier, SH, Lin, T-M, Moore, RW, Vezina, CM, Abler, LL & Peterson, RE (2010). Androgenic regulation of ventral epithelial bud number and pattern in mouse urogenital sinus. Dev Dyn 239, 373–385.CrossRefGoogle ScholarPubMed
Biancardi, MF, Perez, AP, Caires, CR, Góes, RM, Vilamaior, PS, Santos, FC & Taboga, SR (2015). Prenatal exposure to testosterone masculinises the female gerbil and promotes the development of lesions in the prostate (Skene's gland). Reprod Fertil Dev 27, 1000–1011.CrossRefGoogle Scholar
Biancardi, MF, Perez, APS, Góes, RM, Santos, FCA, Vilamaior, PSL & Taboga, SR (2012). Prenatal testosterone exposure as a model for the study of endocrine disrupting chemicals on the gerbil prostate. Exp Biol Med 237, 1298–1309.CrossRefGoogle Scholar
Biancardi, MF, Santos, FCA, Hernandes, FC, Sanches, BDA & Taboga, SR (2017). Female prostate: Historical, developmental, and morphological perspectives. Cell BiolInt 41, 1174–1183.Google ScholarPubMed
Biancardi, MF, Santos, FCA, Madi-Ravazzi, L, Góes, RM, Vilamaior, PSL, Felisbino, SL & Taboga, SR (2010). Testosterone promotes an anabolic increase in the rat female prostate (Skene's paraurethral gland) which acquires a male ventral prostate phenotype. Anat Rec (Roboken) 293, 2163–2175.CrossRefGoogle ScholarPubMed
Brambell, FWR & Davis, DHS (1940). The normal occurrence, structure and homology of prostate glands in adult female Mastomys erythroleucus Temm. J Anat 75, 64–74.Google ScholarPubMed
Elchlepp, JG (1952). The urogenital organs of the cottontail rabbit (Sylvilagus floridanus). J Morphol 91, 169–198.CrossRefGoogle Scholar
Evatt, EJ (1911). A contribution to the development of the prostate gland in the human female, and a study of the homologies of the urethra and vagina of the sexes. J Anat Physiol 45, 122–130.Google Scholar
Fiala, JC (2005). Reconstruct: A free editor for serial section microscopy. J Microsc 218, 52–61.CrossRefGoogle ScholarPubMed
Flamini, MA, Barbeito, CG, Díaz, AO & Portiansky, EL (2020). Comparison of the structural and ultrastructural characteristics of the female prostate between pregnant and non-pregnant plains viscacha (Lagostomus maximus). Tissue Cell. doi:10.1016/j.tice.2020.101458.Google Scholar
Flamini, MA, Barbeito, CG, Gimeno, EJ & Portiansky, EL (2002). Morphological characterization of the female prostate (Skene's gland or paraurethral gland) of Lagostomus maximus maximus. Ann Anat 184, 341–345.CrossRefGoogle ScholarPubMed
Francis, K & Palsson, BO (1997). Effective intercellular communication distances are determined by the relative time constants for cyto/chemokine secretion and diffusion. Proc Natl Acad Sci U S A 94, 12258–12262.CrossRefGoogle Scholar
Georgas, KM, Armstrong, J, Keast, JR, Larkinsm, CE, McHugh, KM, Southard-Smith, EM, Cohn, MJ, Batourina, E, Dan, H, Schneider, K, Buehler, DP, Wiese, CB, Brennan, J, Davies, JA, Harding, SD, Baldock, RA, Little, MH, Vezina, CM & Mendelsohn, C (2015). An illustrated anatomical ontology of the developing mouse lower urogenital tract. Development 142, 1893–1908.CrossRefGoogle ScholarPubMed
Gerdes, MJ, Larsen, M, Dang, TD, Ressler, SJ, Tuxhorn, JA & Rowley, DR (2004). Regulation of rat prostate stromal cell myodifferentiation by androgen and TGF-β1. Prostate 58, 299–307.CrossRefGoogle ScholarPubMed
Greene, RR, Burrill, MW & Ivy, AC (1939). Experimental intersexuality. The effect of antenatal androgens on sexual development of female rats. Am J Anat 65, 415–469.CrossRefGoogle Scholar
Gross, SA & Didio, LJA (1987). Comparative morphology of the prostate in adult male and female Praomys (Mastomys) natalensis studied with electron microscopy. J Submicrosc Cytol 19, 77–84.Google ScholarPubMed
Guo, X & Chen, S-Y (2012). Transforming growth factor-β and smooth muscle differentiation. World J Biol Chem 3, 41–52.CrossRefGoogle ScholarPubMed
Inomata, T, Ninomiya, H, Somiya, H, Saito, H & Mochizuki, K (1992). Histological observation on the female prostate in Mongolian gerbils (Meriones unguiculatus). Jikken Dobutsu 41, 383–386.Google Scholar
Korenchevsky, V (1937). The female prostatic gland and its reaction to male sexual compounds. J Physiol 90, 371–376.CrossRefGoogle ScholarPubMed
Mahoney, J (1940). The embryology and postnatal development of the prostate gland in the female rat. Anat Rec 77, 375–395.CrossRefGoogle Scholar
Mahoney, JJ (1942). Genetic and hormonal determination of prostate development in the female rat. J Exp Zool 90, 413–439.CrossRefGoogle Scholar
Mahoney, JJ & Witschi, E (1947). Genetics of the female prostate in rats. Genetics 32, 369–378.CrossRefGoogle ScholarPubMed
Manso, LA, Medeiros, BCM, Rodrigues, GA, Ramos, JG, Marques, MR, Taboga, SR, Santos, FCA & Biancardi, MF (2021). Testosterone exposure in prenatal life disrupts epithelial nuclear morphology, smooth muscle layer pattern, and FGF10 and Shh expression in prostate. Life Sci. doi:10.1016/j.lfs.2021.119198.CrossRefGoogle ScholarPubMed
Matthews, LH (1942). Notes on the genitalia and reproduction of some African bats. Proc Zool Soc Lond B111(3-4), 289–346.CrossRefGoogle Scholar
Prins, GS & Putz, O (2008). Molecular signaling pathways that regulate prostate gland development. Differentiation 76, 641–659.CrossRefGoogle ScholarPubMed
Ramos, JG, Silva, JPA, Manso, LA, Rodrigues, GA, Taboga, SR, Carvalho, HF, Santos, FCA & Biancardi, MF (2020). Developmental changes induced by exogenous testosterone during early phases of prostate organogenesis. Exp Mol Pathol. doi:10.1016/j.yexmp.2020.104473.CrossRefGoogle ScholarPubMed
Rodríguez, DAO, Lima, RF, Campos, MS, Costa, JR, Biancardi, MF, Marques, MR, Taboga, SR & Santos, FCA (2016). Intrauterine exposure to bisphenol A promotes different effects in both neonatal and adult prostate of male and female gerbils (Meriones unguiculatus). Environ Toxicol 31, 1740–1750.CrossRefGoogle Scholar
Sanches, BDA, Biancardi, MF, Santos, FCA, Góes, RM, Vilamaior, PSL & Taboga, SR (2014). Budding process during the organogenesis of the ventral prostatic lobe in Mongolian gerbil. Microsc Res Tech 77, 458–466.CrossRefGoogle ScholarPubMed
Sanches, BDA, Zani, BC, Maldarine, JS, Biancardi, MF, Santos, FCA, Góes, RM, Vilamaior, PSL & Taboga, SR (2016). Postnatal development of Mongolian gerbil female prostate: An immunohistochemical and 3D modeling study. Microsc Res Tech 79, 438–446.CrossRefGoogle ScholarPubMed
Santos, FCA, Leite, RP, Custódio, AMG, Carvalho, KP, Monteiro-Leal, LH, Santos, AB, Góes, RM, Carvalho, HF & Taboga, SR (2006). Testosterone stimulates growth and secretory activity of the female prostate in the adult gerbil (Meriones unguiculatus). Biol Reprod 75, 370–379.CrossRefGoogle Scholar
Schaeffer, EM, Marchionni, L, Huang, Z, Simons, B, Blackman, A, Yu, W, Parmigiani, G & Berman, DM (2008). Androgen-induced programs for prostate epithelial growth and invasion arise in embryogenesis and are reactivated in cancer. Oncogene 27, 7180–7191.CrossRefGoogle ScholarPubMed
Shehata, R (1972). Female prostate in the house rat Rattus rattus. Acta Anat (Basel) 83, 426–434.CrossRefGoogle ScholarPubMed
Shehata, R (1975). Female prostate in Arvicanthis niloticus and Meriones lybicus. Acta Anat (Basel) 92, 513–523.CrossRefGoogle Scholar
Shehata, R (1980). Female prostate and urethral glands in the home rat, Rattus norvegicus. Acta Anat (Basel) 107, 286–288.CrossRefGoogle ScholarPubMed
Skene, AJC (1880). The anatomy and pathology of two important glands of the female urethra. Amer J Obstet Dis Women Child 13, 265–270.Google Scholar
Sloboda, J, Zaviačič, M, Jakubovský, J, Hammar, E & 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.CrossRefGoogle ScholarPubMed
Staack, A, Donjacour, AA, Brody, J, Cunha, GR & Carroll, P (2003). Mouse urogenital development: A practical approach. Differentiation 71, 402–413.CrossRefGoogle ScholarPubMed
Thomson, AA (2008). Mesenchymal mechanisms in prostate organogenesis. Differentiation 76, 587–598.CrossRefGoogle ScholarPubMed
Thomson, AA & Marker, PC (2006). Branching morphogenesis in the prostate gland and seminal vesicles. Differentiation 74, 382–392.CrossRefGoogle ScholarPubMed
Thomson, AA, Timms, BG, Barton, L, Cunha, GR & Grace, OC (2002). The role of smooth muscle in regulating prostatic induction. Development 129, 1905–1912.CrossRefGoogle ScholarPubMed
Timms, BG (2008). Prostate development: A historical perspective. Differentiation 76, 565–577.CrossRefGoogle ScholarPubMed
Timms, BG, Lee, CW, Aumüller, G & Seitz, J (1995). Instructive induction of prostate growth and differentiation by a defined urogenital sinus mesenchyme. Microsc Res Tech 30, 319–332.CrossRefGoogle ScholarPubMed
Timms, BG, Mohs, TJ & Didio, LJA (1994). Ductal budding and branching patterns in the developing prostate. J Urol 151, 1427–1432.CrossRefGoogle ScholarPubMed
Timms, BG, Petersen, SL & vom Saal, FS (1999). Prostate gland growth during development is stimulated in both male and female rat fetuses by intrauterine proximity to female fetuses. J Urol 161, 1694–1701.CrossRefGoogle ScholarPubMed
Toivanen, R & Shen, MM (2017). Prostate organogenesis: Tissue induction, hormonal regulation and cell type specification. Development 144, 1382–1398.CrossRefGoogle ScholarPubMed
Zaviačič, M (1999). The Female Prostate: From Vestigial Skene's Parauretral Glands and Ducts to Woman's Functional Prostate. Bratislava, Slovakia: Slovack Academic Press.Google Scholar