Steroidogenesis during postnatal testicular development of Galea spixii.

The androgen/estrogen balance is essential for normal sexual development and reproduction in mammals. Studies performed herein investigated the potential for estrogen synthesis in cells of the testes of a hystricomorph rodent, Galea spixii The study characterized the expression of the key enzymes responsible for estrogen and androgen synthesis, cytochromes P450 aromatase (P450arom), 17α-hydroxylase/17,20-lyase (P450c17) respectively, as well as the redox partner NADPH cytochrome P450 oxido-reductase (CPR) required to support electron transfer and catalysis of these P450s, by immunohistochemistry (IHC) and quantitative polymerase chain reaction (qPCR) analysis, throughout postnatal sexual development. Testes (immature, pre-pubertal, pubertal and post-pubertal) were collected, fixed for IHC (CYP19, CYP17 and CPR) and stored frozen for qPCR for the relevant gene transcripts (Cyp19a1 and Cyp17a1). Expression of P450c17 was significantly elevated at the pre-pubertal and pubertal stages. Based on IHC, P450c17 was expressed only in Leydig cell clusters. The expression of P450arom was detectable at all stages of sexual development of Galea spixii IHC data suggest that estrogen synthesis was not restricted to somatic cells (Leydig cells/Sertoli cells), but that germ cells may also be capable of converting androgens into estrogens, important for testicular function and spermatogenesis.

[1]  T. Inaba,et al.  Testicular gene expression of steroidogenesis-related factors in prepubertal, postpubertal, and aging dogs. , 2017, Theriogenology.

[2]  R. Ramasamy,et al.  The role of estradiol in male reproductive function , 2016, Asian journal of andrology.

[3]  M. Miglino,et al.  Ultrastructure of spermatogenesis in Spix's yellow-toothed cavy (Galea spixii). , 2013, Reproduction.

[4]  T. Berger,et al.  Increased testicular Sertoli cell population induced by an estrogen receptor antagonist , 2013, Molecular and Cellular Endocrinology.

[5]  A. R. Silva,et al.  Development of spermatogenesis in captive-bred Spix's yellow-toothed cavy (Galea spixii). , 2012, Reproduction, fertility, and development.

[6]  B. Ball,et al.  Expression of steroidogenic enzymes during equine testicular development. , 2011, Reproduction.

[7]  B. Bilińska,et al.  Immunoexpression of aromatase in immature and adult males of the European bison (Bison bonasus, Linnaeus 1758). , 2010, Reproduction in domestic animals = Zuchthygiene.

[8]  Meiyu Xu,et al.  Seasonal changes in spermatogenesis and immunolocalization of cytochrome P450 17alpha-hydroxylase/c17-20 lyase and cytochrome P450 aromatase in the wild male ground squirrel (Citellus dauricus Brandt). , 2010, The Journal of reproduction and development.

[9]  S. Blottner,et al.  Estrogens are involved in seasonal regulation of spermatogenesis and sperm maturation in roe deer (Capreolus capreolus). , 2008, General and comparative endocrinology.

[10]  S. Carreau,et al.  Estrogens: a new player in spermatogenesis. , 2007, Folia histochemica et cytobiologica.

[11]  C. O'keefe,et al.  Immune-mediated bone marrow failure syndromes of progenitor and stem cells: molecular analysis of cytotoxic T cell clones. , 2007, Folia histochemica et cytobiologica.

[12]  N. Tagawa,et al.  Developmental changes of serum steroids produced by cytochrome P450c17 in rat , 2006, Steroids.

[13]  G. Watanabe,et al.  Immunolocalization of steroidogenic enzymes in the fetal, neonatal and adult testis of the Shiba goat. , 2005, Experimental animals.

[14]  B. Hoffmann,et al.  Expression of oestrogen receptors alpha and beta and of aromatase in the testis of immature and mature boars. , 2005, Reproduction in domestic animals = Zuchthygiene.

[15]  S. Lambard,et al.  The promoter(s) of the aromatase gene in male testicular cells. , 2004, Reproductive biology.

[16]  M. Kurosumi,et al.  Immunocytochemical localization of aromatase in rat testis , 1985, Histochemistry.

[17]  S. Carreau,et al.  Complementary approaches demonstrate that cellular aromatization in the bank vole testis is related to photoperiod. , 2009, European journal of histochemistry : EJH.

[18]  T. Tsubota,et al.  Seasonal changes in spermatogenesis and testicular steroidogenesis in wild male raccoon dogs (Nyctereutes procynoides). , 2003, The Journal of veterinary medical science.

[19]  S. Moslemi,et al.  Immunolocalization of Aromatase in Stallion Leydig Cells and Seminiferous Tubules , 2003, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[20]  S. Carreau,et al.  Photoperiod-dependent capability of androgen aromatization and the role of estrogens in the bank vole testis visualized by means of immunohistochemistry , 2001, Molecular and Cellular Endocrinology.

[21]  A. Conley,et al.  Mammalian aromatases. , 2001, Reproduction.

[22]  A. McMahon,et al.  Localization of 17β-Hydroxysteroid Dehydrogenase/17-Ketosteroid Reductase Isoform Expression in the Developing Mouse Testis-Androstenedione Is the Major Androgen Secreted by Fetal/Neonatal Leydig Cells. , 2000, Endocrinology.

[23]  B. Bilińska,et al.  Immunolocalization of androgen receptors in testicular cells during postnatal development of the bank vole (Clethrionomys glareolus, S.). , 1999, Tissue & cell.

[24]  S. Carreau,et al.  Sources of oestrogen in the testis and reproductive tract of the male. , 1999, International Journal of Andrology.

[25]  W. Boon,et al.  Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  P. Saunders,et al.  Immunoexpression of the steroidogenic enzymes 3-beta hydroxysteroid dehydrogenase and 17 alpha-hydroxylase, C17,20 lyase and the receptor for luteinizing hormone (LH) in the fetal rat testis suggests that the onset of Leydig cell steroid production is independent of LH action. , 1998, Biology of reproduction.

[27]  J. Bahr,et al.  Rat testicular germ cells and epididymal sperm contain active P450 aromatase. , 1998, Journal of andrology.

[28]  I. Bird,et al.  The role of cytochrome P450 17 alpha-hydroxylase and 3 beta-hydroxysteroid dehydrogenase in the integration of gonadal and adrenal steroidogenesis via the delta 5 and delta 4 pathways of steroidogenesis in mammals. , 1997, Biology of reproduction.

[29]  G. Shetty,et al.  Effect of estrogen deprivation on the reproductive physiology of male and female primates , 1997, The Journal of Steroid Biochemistry and Molecular Biology.

[30]  V. Papadopoulos,et al.  Printed in U.S.A. Copyright © 1997 by The Endocrine Society Regulation of Rat Testis Gonocyte Proliferation by Platelet-Derived Growth Factor and Estradiol: Identification of Signaling Mechanisms Involved* , 2022 .

[31]  J. Bahr,et al.  Seasonal changes in spermatogenesis and testicular steroidogenesis in the male black bear Ursus americanus. , 1997, Journal of reproduction and fertility.

[32]  B. Bilińska,et al.  Are ovine Leydig cells able to aromatize androgens? , 1997, Reproduction, fertility, and development.

[33]  J. Bahr,et al.  Mouse Epididymal Sperm Contain Active P 450 Aromatase Which Decreases as Sperm Traverse the Epididymis , 2004 .

[34]  N. Harada,et al.  Functional aromatase expression in porcine adrenal gland and testis. , 1996, Biology of reproduction.

[35]  J. Gaillard,et al.  Immunohistochemical localization of cytochrome P450 aromatase in equine gonads. , 1995, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[36]  J. Roser,et al.  Localization of aromatase in equine Leydig cells. , 1994, Domestic animal endocrinology.

[37]  K. Toda,et al.  Germ cells of the mouse testis express P450 aromatase. , 1993, Endocrinology.

[38]  C. Nolan,et al.  Genotype at the P450scc locus determines differences in the amount of P450scc protein and maximal testosterone production in mouse Leydig cells. , 1990, Molecular endocrinology.

[39]  J. Saez,et al.  Insulin-like growth factor-I and insulin increase the stimulatory guanine nucleotide binding protein (Gs) in cultured bovine adrenal cells , 1989, Molecular and Cellular Endocrinology.

[40]  F. Rommerts.  How much androgen is required for maintenance of spermatogenesis? , 1988, The Journal of endocrinology.

[41]  M. Hammar,et al.  Testosterone Production in Vitro in Human Testicular Tissue , 2009, Andrologia.

[42]  C. Tsai-Morris,et al.  Cellular localization of rat testicular aromatase activity during development. , 1985, Endocrinology.

[43]  J. Raeside,et al.  Estrogen and androgen production by purified Leydig cells of mature boars. , 1983, Biology of reproduction.