Overviews of Stem Cells for Gonadal and Adrenal Steroidogenic Cells
American Journal of Life Sciences
Volume 3, Issue 3-2, May 2015, Pages: 58-64
Received: Mar. 29, 2015; Accepted: Mar. 31, 2015; Published: May 6, 2015
Views 5399      Downloads 191
Authors
Takashi Yazawa, Department of Biochemistry, Asahikawa Medical University, Hokkaido, Japan
Yoshitaka Imamichi, Department of Biochemistry, Faculty of Medical Sciences, University of Fukui, Matsuoka, Eiheiji-cho, Fukui, Japan
Kaoru Miyamoto, Department of Biochemistry, Faculty of Medical Sciences, University of Fukui, Matsuoka, Eiheiji-cho, Fukui, Japan
Junsuke Uwada, Department of Biochemistry, Asahikawa Medical University, Hokkaido, Japan
Md Rafiqul Islam Khan, Department of Biochemistry, Asahikawa Medical University, Hokkaido, Japan
Takanobu Taniguchi, Department of Biochemistry, Asahikawa Medical University, Hokkaido, Japan
Article Tools
Follow on us
Abstract
Gonads and adrenal glands are the primary organs for the production of steroid hormones in mammals. Steroid hormones play important roles in development and are essential for the maintenance of homeostasis during adult life. To supply sufficient amounts of hormones, gonads and adrenal glands maintain their functions by replenishment of steroidogenic cells. It has been hypothesized that stem/progenitor cells of steroidogenic cells are important for this phenomenon. In fact, such cells have been recently identified in gonads and adrenal glands. However, steroid hormone production decreases progressively with age, causing problems such as menopausal disorders in women. Although steroid hormones are administered to these patients, induction of steroidogenic cells from stem cells is a potential strategy to prevent menopausal disorders. Here, we review the current knowledge on stem cells that replenish steroid hormone-producing cells in the gonads and adrenal glands. We also discuss induction of steroidogenic cells from stem cells derived from non-steroidogenic organs.
Keywords
Steroid Hormone, Stem Cell, Adrenal, Testis, Ovary
To cite this article
Takashi Yazawa, Yoshitaka Imamichi, Kaoru Miyamoto, Junsuke Uwada, Md Rafiqul Islam Khan, Takanobu Taniguchi, Overviews of Stem Cells for Gonadal and Adrenal Steroidogenic Cells, American Journal of Life Sciences. Special Issue:Biology and Medicine of Peptide and Steroid Hormones. Vol. 3, No. 3-2, 2015, pp. 58-64. doi: 10.11648/j.ajls.s.2015030302.21
References
[1]
W. L. Miller, Molecular biology of steroid hormone synthesis. Endocr Rev, 1988, 9, pp. 295-318.
[2]
W. L. Miller, R. J. Auchus, The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocr Rev, 2011, 32, pp. 81-151.
[3]
W. E. Rainey, Y. Nakamura, Regulation of the adrenal androgen biosynthesis. J Steroid Biochem Mol Biol, 2008, 108, pp. 281-286.
[4]
P. J. Hornsby, Adrenarche: a cell biological perspective. J Endocrinol, 2012, 214, pp. 113-119.
[5]
O. Hatano, A. Takakusu, M. Nomura, K. Morohashi, Identical origin of adrenal cortex and gonad revealed by expression profiles of Ad4BP/SF-1. Genes Cells, 1996, 1, pp. 663-671.
[6]
K. Morohashi, The ontogenesis of the steroidogenic tissues. Genes Cells, 1997, 2, pp. 95-106.
[7]
P. Val, J. P. Martinez-Barbera, A. Swain, Adrenal development is initiated by Cited2 and Wt1 through modulation of Sf-1 dosage. Development, 2007, 134, pp. 2349-2358.
[8]
Y. Ikeda, W. H. Shen, H. A. Ingraham, K. L. Parker, Developmental expression of mouse steroidogenic factor-1, an essential regulator of the steroid hydroxylases. Mol Endocrinol, 1994, 8, pp. 654-662.
[9]
O. Hatano, K. Takayama, T. Imai, M. R. Waterman, A. Takakusu, T. Omura, K. Morohashi, Sex-dependent expression of a transcription factor, Ad4BP, regulating steroidogenic P-450 genes in the gonads during prenatal and postnatal rat development. Development, 1994, 120, pp. 2787-2797.
[10]
X. Luo, Y. Ikeda, K. L. Parker, A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell, 1994, 77, pp. 481-490.
[11]
K. L. Parker, B. P. Schimmer, Steroidogenic factor 1: a key determinant of endocrine development and function. Endocr Rev, 1997, 18, pp. 361-377.
[12]
B. P. Schimmer, P. C. White, Minireview: steroidogenic factor 1: its roles in differentiation, development, and disease. Mol Endocrinol, 2010, 24, pp. 1322-1337.
[13]
D. S. Lala, D. A. Rice, K. L. Parker, Steroidogenic factor I, a key regulator of steroidogenic enzyme expression, is the mouse homolog of fushi tarazu-factor I. Mol Endocrinol, 1992, 6, pp. 1249-1258.
[14]
K. Morohashi, S. Honda, Y. Inomata, H. Handa, T. Omura, A common trans-acting factor, Ad4-binding protein, to the promoters of steroidogenic P-450s. J Biol Chem, 1992, 267, pp. 17913-17919.
[15]
T. Yazawa, Y. Imamichi, K. Miyamoto, M. Khan, J. Uwada, A. Umezawa, T. Taniguchi, Regulation of Steroidogenesis, Development and Cell Differentiation by Steroidogenic Factor-1 and Liver Receptor Homolog-1. Zoological Science, (in press)
[16]
K. Kawabe, T. Shikayama, H. Tsuboi, S. Oka, K. Oba, T. Yanase, H. Nawata, K. Morohashi, Dax-1 as one of the target genes of Ad4BP/SF-1. Mol Endocrinol, 1999, 13, pp. 1267-1284.
[17]
C. Zhang, M. J. Large, R. Duggavathi, F. J. DeMayo, J. P. Lydon, K. Schoonjans, E. Kovanci, B. D. Murphy, Liver receptor homolog-1 is essential for pregnancy. Nat Med, 2013, 19, pp. 1061-1066.
[18]
K. Bertolin, J. Gossen, K. Schoonjans, B. D. Murphy, The orphan nuclear receptor Nr5a2 is essential for luteinization in the female mouse ovary. Endocrinology, 2014, 155, pp. 1931-1943.
[19]
H. Chen, R. S. Ge, B. R. Zirkin, Leydig cells: From stem cells to aging. Mol Cell Endocrinol, 2009, 306, pp. 9-16.
[20]
M. C. Beattie, L. Adekola, V. Papadopoulos, H. Chen, B. R. Zirkin, Leydig cell aging and hypogonadism. Exp Gerontol, 2015, pp.
[21]
S. Jabara, L. K. Christenson, C. Y. Wang, J. M. McAllister, N. B. Javitt, A. Dunaif, J. F. Strauss, 3rd, Stromal cells of the human postmenopausal ovary display a distinctive biochemical and molecular phenotype. J Clin Endocrinol Metab, 2003, 88, pp. 484-492.
[22]
F. Labrie, All sex steroids are made intracellularly in peripheral tissues by the mechanisms of intracrinology after menopause. J Steroid Biochem Mol Biol, 2015, 145, pp. 133-138.
[23]
P. J. Hornsby, Aging of the human adrenal cortex. Sci Aging Knowledge Environ, 2004, 2004, pp. re6.
[24]
T. Yazawa, Y. Imamichi, K. Miyamoto, A. Umezawa, T. Taniguchi, Differentiation of mesenchymal stem cells into gonad and adrenal steroidogenic cells. World J Stem Cells, 2014, 6, pp. 203-212.
[25]
R. Habert, H. Lejeune, J. M. Saez, Origin, differentiation and regulation of fetal and adult Leydig cells. Mol Cell Endocrinol, 2001, 179, pp. 47-74.
[26]
P. J. O'Shaughnessy, P. J. Baker, H. Johnston, The foetal Leydig cell-- differentiation, function and regulation. Int J Androl, 2006, 29, pp. 90-95; discussion 105-108.
[27]
Y. Shima, K. Miyabayashi, S. Haraguchi, T. Arakawa, H. Otake, T. Baba, S. Matsuzaki, Y. Shishido, H. Akiyama, T. Tachibana, K. Tsutsui, K. Morohashi, Contribution of Leydig and Sertoli cells to testosterone production in mouse fetal testes. Mol Endocrinol, 2013, 27, pp. 63-73.
[28]
P. J. O'Shaughnessy, P. J. Baker, M. Heikkila, S. Vainio, A. P. McMahon, Localization of 17beta-hydroxysteroid dehydrogenase/17-ketosteroid reductase isoform expression in the developing mouse testis--androstenedione is the major androgen secreted by fetal/neonatal leydig cells. Endocrinology, 2000, 141, pp. 2631-2637.
[29]
H. B. Siril Ariyaratne, S. Chamindrani Mendis-Handagama, D. Buchanan Hales, J. Ian Mason, Studies on the onset of Leydig precursor cell differentiation in the prepubertal rat testis. Biol Reprod, 2000, 63, pp. 165-171.
[30]
J. B. Kerr, C. M. Knell, The fate of fetal Leydig cells during the development of the fetal and postnatal rat testis. Development, 1988, 103, pp. 535-544.
[31]
J. B. Kerr, K. Donachie, F. F. Rommerts, Selective destruction and regeneration of rat Leydig cells in vivo. A new method for the study of seminiferous tubular-interstitial tissue interaction. Cell Tissue Res, 1985, 242, pp. 145-156.
[32]
H. Chen, I. Huhtaniemi, B. R. Zirkin, Depletion and repopulation of Leydig cells in the testes of aging brown Norway rats. Endocrinology, 1996, 137, pp. 3447-3452.
[33]
K. C. Lo, Z. Lei, V. Rao Ch, J. Beck, D. J. Lamb, De novo testosterone production in luteinizing hormone receptor knockout mice after transplantation of leydig stem cells. Endocrinology, 2004, 145, pp. 4011-4015.
[34]
R. S. Ge, Q. Dong, C. M. Sottas, V. Papadopoulos, B. R. Zirkin, M. P. Hardy, In search of rat stem Leydig cells: identification, isolation, and lineage-specific development. Proc Natl Acad Sci U S A, 2006, 103, pp. 2719-2724.
[35]
L. Landreh, K. Spinnler, K. Schubert, M. R. Hakkinen, S. Auriola, M. Poutanen, O. Soder, K. Svechnikov, A. Mayerhofer, Human testicular peritubular cells host putative stem Leydig cells with steroidogenic capacity. J Clin Endocrinol Metab, 2014, 99, pp. E1227-1235.
[36]
J. M. Young, A. S. McNeilly, Theca: the forgotten cell of the ovarian follicle. Reproduction, 2010, 140, pp. 489-504.
[37]
J. A. Parrott, M. K. Skinner, Kit ligand actions on ovarian stromal cells: effects on theca cell recruitment and steroid production. Mol Reprod Dev, 2000, 55, pp. 55-64.
[38]
C. T. Huang, S. R. Weitsman, B. N. Dykes, D. A. Magoffin, Stem cell factor and insulin-like growth factor-I stimulate luteinizing hormone-independent differentiation of rat ovarian theca cells. Biol Reprod, 2001, 64, pp. 451-456.
[39]
M. Orisaka, T. Mizutani, K. Tajima, S. Orisaka, K. Shukunami, K. Miyamoto, F. Kotsuji, Effects of ovarian theca cells on granulosa cell differentiation during gonadotropin-independent follicular growth in cattle. Mol Reprod Dev, 2006, 73, pp. 737-744.
[40]
A. Honda, M. Hirose, K. Hara, S. Matoba, K. Inoue, H. Miki, H. Hiura, M. Kanatsu-Shinohara, Y. Kanai, T. Kono, T. Shinohara, A. Ogura, Isolation, characterization, and in vitro and in vivo differentiation of putative thecal stem cells. Proc Natl Acad Sci U S A, 2007, 104, pp. 12389-12394.
[41]
M. Kanatsu-Shinohara, K. Inoue, J. Lee, M. Yoshimoto, N. Ogonuki, H. Miki, S. Baba, T. Kato, Y. Kazuki, S. Toyokuni, M. Toyoshima, O. Niwa, M. Oshimura, T. Heike, T. Nakahata, F. Ishino, A. Ogura, T. Shinohara, Generation of pluripotent stem cells from neonatal mouse testis. Cell, 2004, 119, pp. 1001-1012.
[42]
E. M. Walczak, G. D. Hammer, Regulation of the adrenocortical stem cell niche: implications for disease. Nat Rev Endocrinol, 2015, 11, pp. 14-28.
[43]
A. C. Kim, G. D. Hammer, Adrenocortical cells with stem/progenitor cell properties: recent advances. Mol Cell Endocrinol, 2007, 265-266, pp. 10-16.
[44]
A. C. Kim, F. M. Barlaskar, J. H. Heaton, T. Else, V. R. Kelly, K. T. Krill, J. O. Scheys, D. P. Simon, A. Trovato, W. H. Yang, G. D. Hammer, In search of adrenocortical stem and progenitor cells. Endocr Rev, 2009, 30, pp. 241-263.
[45]
M. A. Wood, G. D. Hammer, Adrenocortical stem and progenitor cells: unifying model of two proposed origins. Mol Cell Endocrinol, 2011, 336, pp. 206-212.
[46]
F. Beuschlein, C. Mutch, D. L. Bavers, Y. M. Ulrich-Lai, W. C. Engeland, C. Keegan, G. D. Hammer, Steroidogenic factor-1 is essential for compensatory adrenal growth following unilateral adrenalectomy. Endocrinology, 2002, 143, pp. 3122-3135.
[47]
R. D. Perrone, H. H. Bengele, E. A. Alexander, Sodium retention after adrenal enucleation. Am J Physiol, 1986, 250, pp. E1-12.
[48]
A. S. Belloni, G. Neri, F. G. Musajo, P. G. Andreis, M. Boscaro, D. D'Agostino, P. Rebuffat, D. P. Boshier, G. Gottardo, G. Mazzocchi, et al., Investigations on the morphology and function of adrenocortical tissue regenerated from gland capsular fragments autotransplanted in the musculus gracilis of the rat. Endocrinology, 1990, 126, pp. 3251-3262.
[49]
P. King, A. Paul, E. Laufer, Shh signaling regulates adrenocortical development and identifies progenitors of steroidogenic lineages. Proc Natl Acad Sci U S A, 2009, 106, pp. 21185-21190.
[50]
M. A. Wood, A. Acharya, I. Finco, J. M. Swonger, M. J. Elston, M. D. Tallquist, G. D. Hammer, Fetal adrenal capsular cells serve as progenitor cells for steroidogenic and stromal adrenocortical cell lineages in M. musculus. Development, 2013, 140, pp. 4522-4532.
[51]
T. Yazawa, T. Mizutani, K. Yamada, H. Kawata, T. Sekiguchi, M. Yoshino, T. Kajitani, Z. Shou, A. Umezawa, K. Miyamoto, Differentiation of adult stem cells derived from bone marrow stroma into Leydig or adrenocortical cells. Endocrinology, 2006, 147, pp. 4104-4111.
[52]
S. Gondo, T. Okabe, T. Tanaka, H. Morinaga, M. Nomura, R. Takayanagi, H. Nawata, T. Yanase, Adipose tissue-derived and bone marrow-derived mesenchymal cells develop into different lineage of steroidogenic cells by forced expression of steroidogenic factor 1. Endocrinology, 2008, 149, pp. 4717-4725.
[53]
T. Tanaka, S. Gondo, T. Okabe, K. Ohe, H. Shirohzu, H. Morinaga, M. Nomura, K. Tani, R. Takayanagi, H. Nawata, T. Yanase, Steroidogenic factor 1/adrenal 4 binding protein transforms human bone marrow mesenchymal cells into steroidogenic cells. J Mol Endocrinol, 2007, 39, pp. 343-350.
[54]
S. Gojo, A. Umezawa, Plasticity of mesenchymal stem cells--regenerative medicine for diseased hearts. Hum Cell, 2003, 16, pp. 23-30.
[55]
D. G. Phinney, D. J. Prockop, Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair--current views. Stem Cells, 2007, 25, pp. 2896-2902.
[56]
J. A. Kode, S. Mukherjee, M. V. Joglekar, A. A. Hardikar, Mesenchymal stem cells: immunobiology and role in immunomodulation and tissue regeneration. Cytotherapy, 2009, 11, pp. 377-391.
[57]
M. C. Hu, S. J. Chou, Y. Y. Huang, N. C. Hsu, H. Li, B. C. Chung, Tissue-specific, hormonal, and developmental regulation of SCC-LacZ expression in transgenic mice leads to adrenocortical zone characterization. Endocrinology, 1999, 140, pp. 5609-5618.
[58]
T. Yazawa, Y. Inaoka, R. Okada, T. Mizutani, Y. Yamazaki, Y. Usami, M. Kuribayashi, M. Orisaka, A. Umezawa, K. Miyamoto, PPAR-gamma coactivator-1alpha regulates progesterone production in ovarian granulosa cells with SF-1 and LRH-1. Mol Endocrinol, 2010, 24, pp. 485-496.
[59]
X. Wei, G. Peng, S. Zheng, X. Wu, Differentiation of umbilical cord mesenchymal stem cells into steroidogenic cells in comparison to bone marrow mesenchymal stem cells. Cell Prolif, 2012, 45, pp. 101-110.
[60]
T. Yazawa, S. Kawabe, Y. Inaoka, R. Okada, T. Mizutani, Y. Imamichi, Y. Ju, Y. Yamazaki, Y. Usami, M. Kuribayashi, A. Umezawa, K. Miyamoto, Differentiation of mesenchymal stem cells and embryonic stem cells into steroidogenic cells using steroidogenic factor-1 and liver receptor homolog-1. Mol Cell Endocrinol, 2011, 336, pp. 127-132.
ADDRESS
Science Publishing Group
1 Rockefeller Plaza,
10th and 11th Floors,
New York, NY 10020
U.S.A.
Tel: (001)347-983-5186