Temporal and spatial expression of liver receptor homologue‐1 (LRH‐1) during embryogenesis suggests a potential role in gonadal development

Liver receptor homologue‐1 (LRH‐1), an orphan member of the nuclear receptor family highly expressed in adult mouse ovary, is closely related to steroidogenic factor 1 (SF‐1), known to be important in gonadal formation. To analyze the potential role of LRH‐1 in gonadal differentiation, we compared LRH‐1 and SF‐1 expression during mouse embryonic and postnatal development. LRH‐1 expression was first detected in the urogenital ridge before sexual determination, in primordial germ cells and surrounding somatic cells; expression persisted after differentiation into testes and ovaries. Of interest, LRH‐1 expression declined in the developing ovary and testis at embryonic day 15.5 but increased again just after birth in the ovary in granulosa cells and transiently in oocytes of developing follicles. By comparing and contrasting LRH and SF‐1 expression with the two tissue‐specific steroidogenic markers, cytochromes P450 aromatase and P450 17α‐hydroxylase/17,20 lyase, we provide evidence for a potential role for LRH‐1 in gonadal development, the initiation of folliculogenesis and regulation of estrogen biosynthesis within the ovary. Developmental Dynamics 234:159–168, 2005. © 2005 Wiley‐Liss, Inc.

[1]  J. Richardson,et al.  Transcriptional regulation of aromatase in placenta and ovary , 2005, The Journal of Steroid Biochemistry and Molecular Biology.

[2]  S. Kliewer,et al.  Orphan Nuclear Receptor LRH-1 Is Required To Maintain Oct4 Expression at the Epiblast Stage of Embryonic Development , 2005, Molecular and Cellular Biology.

[3]  J. Auwerx,et al.  Synergy between LRH-1 and beta-catenin induces G1 cyclin-mediated cell proliferation. , 2004, Molecular cell.

[4]  J. Brennan,et al.  One tissue, two fates: molecular genetic events that underlie testis versus ovary development , 2004, Nature Reviews Genetics.

[5]  J. Paré,et al.  The Fetoprotein Transcription Factor (FTF) Gene Is Essential to Embryogenesis and Cholesterol Homeostasis and Is Regulated by a DR4 Element* , 2004, Journal of Biological Chemistry.

[6]  S. Andò,et al.  Differential expression of steroidogenic factor-1/adrenal 4 binding protein and liver receptor homolog-1 (LRH-1)/fetoprotein transcription factor in the rat testis: LRH-1 as a potential regulator of testicular aromatase expression. , 2004, Endocrinology.

[7]  K. Molyneaux,et al.  Transcriptional profiling identifies genes differentially expressed during and after migration in murine primordial germ cells. , 2004, Gene expression patterns : GEP.

[8]  Df Albertini,et al.  Oocyte-somatic cell communication. , 2019, Reproduction (Cambridge, England) Supplement.

[9]  D. Mangelsdorf,et al.  Expression of LRH-1 and SF-1 in the mouse ovary: localization in different cell types correlates with differing function , 2003, Molecular and Cellular Endocrinology.

[10]  R. Lanz,et al.  Differential expression of steroidogenic factor-1 and FTF/LRH-1 in the rodent ovary. , 2003, Endocrinology.

[11]  Albertini Df,et al.  Oocyte-somatic cell communication. , 2003 .

[12]  D. Stocco,et al.  Liver receptor homologue-1 is expressed in human steroidogenic tissues and activates transcription of genes encoding steroidogenic enzymes. , 2002, The Journal of endocrinology.

[13]  J. Dean,et al.  Genetic control of early folliculogenesis in mice , 2002, Trends in Endocrinology & Metabolism.

[14]  S. Carreau The testicular aromatase: from gene to physiological role. , 2002, Reproductive biology.

[15]  K. Molyneaux,et al.  Time-lapse analysis of living mouse germ cell migration. , 2001, Developmental biology.

[16]  Martin M Matzuk,et al.  Analysis of Ovarian Gene Expression in Follicle-Stimulating Hormone β Knockout Mice. , 2001, Endocrinology.

[17]  R. Habert,et al.  Origin, differentiation and regulation of fetal and adult Leydig cells , 2001, Molecular and Cellular Endocrinology.

[18]  A. Spradling,et al.  Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. , 2001, Developmental biology.

[19]  S. Carreau Germ cells: a new source of estrogens in the male gonad , 2001, Molecular and Cellular Endocrinology.

[20]  J. Richards Perspective: The Ovarian Follicle-A Perspective in 2001. , 2001, Endocrinology.

[21]  J. Richards Perspective: the ovarian follicle--a perspective in 2001. , 2001, Endocrinology.

[22]  K. Burns,et al.  Analysis of ovarian gene expression in follicle-stimulating hormone beta knockout mice. , 2001, Endocrinology.

[23]  D. Boerboom,et al.  Expression and regulation of transcripts encoding two members of the NR5A nuclear receptor subfamily of orphan nuclear receptors, steroidogenic factor-1 and NR5A2, in equine ovarian cells during the ovulatory process. , 2000, Endocrinology.

[24]  S. Soyal,et al.  FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. , 2000, Development.

[25]  T. A. Kerr,et al.  Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. , 2000, Molecular cell.

[26]  G. Gil,et al.  Alpha 1-fetoprotein transcription factor is required for the expression of sterol 12alpha -hydroxylase, the specific enzyme for cholic acid synthesis. Potential role in the bile acid-mediated regulation of gene transcription. , 2000, The Journal of biological chemistry.

[27]  A. Mclaren,et al.  Germ and somatic cell lineages in the developing gonad , 2000, Molecular and Cellular Endocrinology.

[28]  J. Richardson,et al.  Microsomal triglyceride transfer protein expression during mouse development. , 2000, Journal of lipid research.

[29]  D. Mangelsdorf,et al.  The role of orphan nuclear receptors in the regulation of cholesterol homeostasis. , 2000, Annual review of cell and developmental biology.

[30]  T. O. Abney The potential roles of estrogens in regulating Leydig cell development and function: A review , 1999, Steroids.

[31]  M. Nitta,et al.  CPF: an orphan nuclear receptor that regulates liver-specific expression of the human cholesterol 7alpha-hydroxylase gene. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. Richardson,et al.  A 500-bp region, ≈40 kb upstream of the human CYP19 (aromatase) gene, mediates placenta-specific expression in transgenic mice , 1999 .

[33]  A. McMahon,et al.  Female development in mammals is regulated by Wnt-4 signalling , 1999, Nature.

[34]  J. Richardson,et al.  A 500-bp region, approximately 40 kb upstream of the human CYP19 (aromatase) gene, mediates placenta-specific expression in transgenic mice. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[35]  A. Spradling,et al.  Female mouse germ cells form synchronously dividing cysts. , 1998, Development.

[36]  S. Mellon,et al.  Orphan receptors, proto-oncogenes and other nuclear factors regulate P450C17 gene transcription. , 1998, Endocrine research.

[37]  A. Cooney,et al.  Characterization of germ cell-specific expression of the orphan nuclear receptor, germ cell nuclear factor. , 1997, Endocrinology.

[38]  S. Mellon,et al.  Multiple orphan nuclear receptors converge to regulate rat P450c17 gene transcription: novel mechanisms for orphan nuclear receptor action. , 1997, Molecular endocrinology.

[39]  M. Buehr The primordial germ cells of mammals: some current perspectives. , 1997, Experimental cell research.

[40]  J. Paré,et al.  The alpha1-fetoprotein locus is activated by a nuclear receptor of the Drosophila FTZ-F1 family , 1996, Molecular and cellular biology.

[41]  P. O’Shaughnessy,et al.  Development of cytochrome P450 aromatase mRNA levels and enzyme activity in ovaries of normal and hypogonadal (hpg) mice. , 1995, Journal of molecular endocrinology.

[42]  K. Morohashi,et al.  Function and distribution of a steroidogenic cell-specific transcription factor, Ad4BP , 1995, The Journal of Steroid Biochemistry and Molecular Biology.

[43]  S. Mellon,et al.  Transcriptional regulation of rat cytochrome P450c17 expression in mouse Leydig MA-10 and adrenal Y-1 cells: identification of a single protein that mediates both basal and cAMP-induced activities. , 1994, DNA and cell biology.

[44]  W. Shen,et al.  Nuclear receptor steroidogenic factor 1 regulates the müllerian inhibiting substance gene: A link to the sex determination cascade , 1994, Cell.

[45]  K. Parker,et al.  A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation , 1994, Cell.

[46]  W. Shen,et al.  Developmental expression of mouse steroidogenic factor-1, an essential regulator of the steroid hydroxylases. , 1994, Molecular endocrinology.

[47]  C. Mendelson,et al.  Genomic elements involved in transcriptional regulation of the rabbit surfactant protein-A gene. , 1993, Molecular endocrinology.

[48]  M. Moisan,et al.  Characterization of the mouse FTZ-F1 gene, which encodes a key regulator of steroid hydroxylase gene expression. , 1993, Molecular endocrinology.

[49]  O. Mathew,et al.  Effect of upper airway pressure pulses on breathing pattern. , 1986, Respiration physiology.

[50]  A. Byskov Differentiation of mammalian embryonic gonad. , 1986, Physiological reviews.

[51]  G. Moore,et al.  The initiation of follicle and oocyte growth in the mouse ovary. , 1979, Biology of reproduction.

[52]  J. McCarrey,et al.  Mechanisms of genetic sex determination, gonadal sex differentiation, and germ-cell development in animals. , 1979, Advances in genetics.

[53]  H. Peters,et al.  Follicular growth: the basic event in the mouse and human ovary. , 1975, Journal of reproduction and fertility.

[54]  T. Pedersen,et al.  Proposal for a classification of oocytes and follicles in the mouse ovary. , 1968, Journal of reproduction and fertility.