Retinoic Acid Determines the Fate of Spermatogonia
محورهای موضوعی : Camel
A. Yilmaz
1
(Department of Animal Science, Hizan Vocational School, Bitlis Eren University, TR 13000, Bitlis, Turkey)
A. Ozdal Gokdal
2
(Department of Plant and Animal Production, Cine Vocational School, Adnan Menderes University, TR 09500, Aydin, Turkey)
کلید واژه: Spermatogenesis, Testis, retinoic acid, spermatogonia,
چکیده مقاله :
In this review, we aim to examine the effect of extrinsic and intrinsic factors on spermatogenesis process taking into account a complex signaling pathway. Primarily, it is suggested that retinoic acid (RA) has a vital function in spermatogenesis process and it is considered to be essential for completion of spermatogonia into mature spermatozoa. In the present review, the key effects of retinoic acid (RA) on spermatogenesis process were evaluated in the perspective of studies done, particularly at molecular level. Thus, this review will provide re look the spermatogenesis process in an outlook of new studies.
Abu Abed S.S., Becktt B.R., Chiba H., Chithalen J.V., Jones G., Metzger D., Champon P. and Petkovich P.M. (1998). Mouse P450RAI (CYP26) expression and retinoic acid-inducible retinoic acid metabolism in F9 cells are regulated by retinoic acid receptor γ and retinoid x receptor α. J. Biol. Chem. 273(4), 2409-2415.
Akmal K.M., Dufour J.M. and Kim K.H. (1996). Region-specific localization of retinoic acid receptor-α expression in the rat epididymis. Biol. Reprod. 54, 1111-1119.
Akmal K.M., Dufour J.M. and Kim K.H. (1997). Retinoic acid receptor α gene expression in the rat testis: potential role during the prophase of meiosis and in the transition from round to elongating spermatids. Biol. Reprod. 56, 549-556.
Akmal K.M., Dufour J.M., Higginson S. and Kim K.H. (1998). Ligand-dependent regulation of retinoic acid receptor α in rat testis: in vivo response to depletion and repletion of vitamin A. Endocrinology. 139, 1239-1248.
Appling D.R. and Chytil F. (1981). Evidence of a role of retinoic acid (vitamin A-acid) in the maintenance of testosterone production in male rats. Endocrinology. 108, 2120-2124.
Blaner W.S., Galdieri M. and Goodman D.S. (1987). Distribution and levels of cellular retinol and cellular retinoic acid-binding protein in various types of rat testis cells. Biol. Reprod. 36, 130-137.
Blomhoff R. and Blomhoff H.K. (2006). Overview of retinoid metabolism and function. J. Neurobiol. 66, 606-630.
Boulogne B., Levacher C., Durand P. and Habert R. (1999). Retinoic acid receptors and retinoic × receptors in the rat testis during fetal and postnatal development: immunolocalization and implication in the control of the number of gonocytes.Biol. Reprod. 61, 1548-1557.
Bowles J., Knight D., Smith C., Wilhelm D., Richman J., Mamiya S., Yashiro K., Chawengsaksophak K., Wilson M.J., Rossant J., Hamada H. and Koopman P. (2006). Retinoid signaling determines germ cell fate in mice. Science. 312, 596-600.
Bowles J. and Koopman P. (2007). Retinoic acid, meiosis and germ cell fate in mammals. Development. 134, 3401-3411.
Braun K.W., Tribley W.A., Griswold M.D. and Kim K.H. (2000). Follicle stimulating hormone inhibits all trans retinoic acid-induced retinoic acid receptor α nuclear localization and transcriptional activation in (?) mouse sertoli cell lines. J. Biol. Chem. 275(6), 4145-4151.
Chaudhary L.R., Hutson J.C. and Stocco D.M. (19890. Effect of retinol and retinoic acid on testosterone production by rat leydig cells in primary culture. Biochim. Biophys. Res. Comm. 158(2), 400-406.
Creemers L.B., Den Ouden K., Van Pelt A.M.M. and De Rooij D.G. (2002). Maintenance of adult mouse type a spermatogonia in vitro: influence of serum and growth factors and comparison with prepubertal spermatogonia cell culture. Reproduction. 124, 791-799.
Cupp A.S., Dufour J.M., Kim G., Skinner M.K. and Kim K.H. (1999). Action of retinoids on embryonic and early postnatal testis development. Endocrinology. 140, 2343-2352.
Davis K.D. and Lazar M.A. (1993). Induction of retinoic acid receptor-β by retinoic acid is cell specific. Endocrinology. 132(4), 1469-1474.
Davis J.T. and Ong D.E. (1995). Retinol processing by the peritubular cell from rat testis. Biol. Reprod. 52, 356-364.
Deltour L., Haselbeck R.J., Ang H.L. and Duester G. (1997). Localization of class I and class IV alcohol dehydrogenases in mouse testis and epididymis: potential retinol dehydrogenases for endogenous retinoic acid synthesis. Biol. Reprod. 56, 102-109.
Delva L., Bastie J.N., Rochette Egly C., Kraiba R., Balitrand N., Despouy P., Chambon P. and Chomienne C. (1999). Physical and functional interactions between cellular retinoic acid binding protein II and the retinoic acid-dependent nuclear complex. Mol. Cell. Biol. 19(10), 7158-7167.
Doyle T.J., Braun K.W., Mclean D.J., Wright R.W., Griswold M.D. and Kim K.H. (2007). Potential functions of retinoic acid receptor A in sertoli cells and germ cells during spermatogenesis. Ann. New York. Acad. Sci. 1120, 114-130.
Dufour J.M. and Kim K.H. (1999). Cellular and subcellular localization of six retinoid receptors in rat testis during postnatal development: identification of potential heterodimeric receptors. Biol. Reprod. 61, 1300-1308.
Eskild W., Ree A.H., Levy F.O., Jahnsen T. and Hansson V. (1991). Cellular localization of mRNAs for retinoic acid receptor-α, cellular etinol binding protein, and cellular retinoic acid-binding protein in rat testis: evidence for germ cell-specific mRNAs. Biol. Reprod. 44, 53-61. Gaemers I.C., Van Pelt A.M.M., Van Der Saag P.T. and De Rooij D.G. (1996). All trans-4-oxo-retinoic acid: a potent inducer of in vivo proliferation of growth-arrested A spermatogonia in the vitamin A deficient mouse testis. Endocrinology.137, 479-485.
Gaemers I.C., Van Pelt A.M.M., Van Der Saag P.T., Hoogerbrugge J.W., Themmen A.P.N. and De Rooij D.G. (1997). Effect of retinoid status on the messenger ribonucleic acid expression of nuclear retinoid receptors α, β, and γ in the mouse testis. Endocrinology. 138, 1544-1551.
Gaemers I.C., SonnoveldE.,Van Pelt A.M.M., Schrans B.H.G.J., Themmen A.P.N., Van Der Saag P.T. and De Rooij D.G. (1998a). The effect of 9-cis-retinoic acid on proliferation and differentiation of a spermatogonia and retinoid receptor gene expression in the vitamin A deficient mouse testis. Endocrinology. 139, 4269-4276.
Gaemers I.C., van Pelt A.M.M., Themmen A.P.N. and De Rooij D.G. (1998b). Isolation and characterization of all trans-retinoic acid-responsive genes in the rat testis. Mol. Reprod. Devel. 50, 1-6.
Galdieri M. and Nistico L. (1994). Retinoids regulate gonadotropin action in cultured rat sertoli cells. Biol. Reprod. 50, 171-177.
Ghyselinck N.B., Vernet N., Dennefeld C., Giese N., Nau H., Champon P., Viville S. and Mark M. (2006). Retinoids and spermatogenesis: lessons from mutant mice lacking the plasma retinol binding protein. Dev. Dyn. 235, 1608-1622.
Griswold M.D., Bishop P.D., Kim K.H., Ping R., Siiteri J.E. and Morales C. (1989). Function of vitamin A in normal and synchronized seminiferous tubules. Ann. New York. Acad. Sci. 546, 154-172.
Griswold M.D., Hogarth C.A., Bowles J. and Koopman P. (2012). Initiating meiosis: the case for retinoic acid. Biol. Reprod. 86(2), 1-7.
Guo X., Morris P.L. and Gudas L.J. (2001). Follicle stimulating hormone and leukemia inhibitory factor regulate sertoli cell retinol metabolism. Endocrinology. 142(3), 1024-1032.
Huang H.F.S. and Marshall G.R. (1983). Failure of spermatid release under various vitamins A states-an indication of delayed spermiation. Biol. Reprod. 28, 1163-1172.
Huang H.F.S. (1994). Induction of enrichment of the stages of the seminiferous epithelial cycle in prepubertal rats. Biol. Reprod. 51, 24-33.
Huang F.J., Wu T.C.J. and Tsai M.Y. (2001). Effect of retinoic acid on implantation and post-implantation development of mouse embryos in vitro. Hum. Reprod. 16(10), 2171-2176.
Ismail N., Morales C. and Clermont Y. (1990). Role of spermatogonia in the stage synchronization of the seminiferous epithelium in vitamin A deficient rats. Am. J. Anat. 188(1), 57-63.
Kastner P., Mark M., Leid M., Gansmuller A., Chin W., Grondona J.M., Decimo D., Krezel W., Dierich A. and Champon P. (1996). Abnormal spermatogenesis in RXRβ mutant mice. Gen. Dev. 10, 80-92.
Kim K.H. and Griswold M.D. (1990). The regulation of retinoic acid receptor mRNA levels during spermatogenesis. Mol. Endocrinol. 4, 1679-1688.
Kubova J., Menke D.B., Zhou Q., Capel B., Griswold M.D. and Page D.C. (2006). Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc. Natl. Acad. Sci. USA. 103(8), 2474-2479.
Krezel W., Dupe V., Mark M., Dierich A., Kastner P. and Champon P. (1996). RXRγ null mice are apparently normal and compound RXRα+/- / RXRβ-/- / RXRγ-/- mutant mice are viable. Proc. Natl. Acad. Sci. Dev. Biol. 93, 9010-9014.
Kurlandsky S.B., Gamble M.V., Ramakrishnan R. and Blaner W.S. (1995). Plasma delivery of retinoic acid to tissues in the rat. J. Biol. Chem. 270(30), 17850-17857.
Lambrot R., Coffigny H., Pairault C., Donnadieu A.C., Frydman R., Habert R. and Fabre V.R. (2006). Use of organ culture to study the human fetal testis development: effect of retinoic acid. J. Clin. Endocrinol. Metab. 91, 2696-2703.
Lampron C., Rochette Egly C., Gorry P., Dolle P., Mark M., Lufkin T., Le Meyr M. and Champon P. (1995). Mice Multiple deficient in cellular retinoic acid binding protein II (CRABPII) or in both CRABPI and CRBPII are essentially normal. Development. 121, 539-548.
Li H., Palczewski K., Baehr W. and Clagett Dame M. (2011). Vitamin A deficiency results in meiotic failure and accumulation of undifferentiated spermatogonia in prepubertal mouse testis. Biol. Reprod. 84, 336-341.
Livera G., Rouiler Fabre V., Durand P. and Habert R. (2000). Multiple effects of retinoids on the development of sertoli, germ, and leydig cells of fetal and neonatal rat testis in culture. Biol. Reprod. 62, 1303-1314.
Livera G., Rouiller Fabre V. and Habert R. (2001). Retinoid receptors involved in the effects of retinoic acid on rat testis development. Biol. Reprod. 64,1307-1314.
Livera G., Rouiller Fabre V., Pairault C., Levacher C. and Habert R. (2002). Regulation and perturbation of testicular functions by vitamin A. Reprod. 124, 173-180.
Livera G., Pairault C., Lambrot R., Lelievre Pegorier M., Sáez, J.M., Habert R. and Rouiller Fabre V. (2004). Retinoids-sensitive steps in steroidogenesis in featal and neonatal rat testes: in vitroand in vivo studies. Biol. Reprod. 82, 1814-1821.
Lufkin T., Lohnes D., Mark M., Dierich A., Gorry P., Gaup M.P., LeMeur M. and Champon P. (1993). High postnatal lethality and testis degeneration in retinoic acid recptor α mutant mice. Proc. Natl. Acad. Sci. Dev. Biol. 90, 7225-7229.
Maekawa M., Kamimura K. and Nagano T. (1996). Peritubular myoid cells in the testis: their structure and function. Arch. Histol. Cytol. 59(1), 1-13.
Marinos E., Kulukussa M., Zotos A. and Kitas C. (1995). Retinoic acid affects basement membrane formation of the seminiferous cords in 14-day male rat gonads in vitro. Differention. 9, 87-94.
Matsuda M., Hyoudou T., Kadowaki M., Onuki K., Masushige S. and Kida S. (2005). The administration of retinoic acid down-regulation cAMP-responsive element modulator (CREM) mRNA in vitamin A-deficient testes.Biosci. Biotechnol. Biochem. 69(2), 261-266.
Mc Lean G., Abu Abed S., Dolle P., Tahayato A., Champon P. and Petkovich M. (2001). Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1, and comparative expression analysis with Cyp26A1 during early murine development. Mech. Dev. 10, 195-201.
Mc Lean G., Li H., Metzger D., Champon P. and Petkovich M. (2007). Apoptotic extinction of germ cells in testes of Cyp26b1 knockout mice. Endocrinology. 10, 4560-4567.
Molotkov A., Fan X., Deltour L., Foglio M.H., Martras S., Farres J., Pares X. and Duester G. (2002). Stimulation of retinoic acid production and growth by ubiquitously expressed alcohol dehydrogenases Adh3. Proc. Natl. Acad. Sci. USA. 99, 5337-5342.
Morales C. and Griswold M.D. (1987). Retinol induced stage synchronization in seminiferous tubules of the rat. Endocrinology. 121(1), 423-434.
Napoli J.L. (1996). Retinoic acid biosynthesis and metabolism. FASEB. J. 10, 993-1001.
Ohta K., Lin Y., Hogg N., Yamamoto M. and Yamazaki Y. (2010). Direct effects of retinoic acid on entry of fetal male germ cells into meiosis in mice. Biol. Reprod. 83,1056-1063.
Oulad Abdelghani M., Bouillet P., Decime D., Gansmuller A., Heyberger S., Dolle P., Bronner S., Lutz Y. and Chambon P. (1996). Characterization of a premeiotic germ cell specific cytoplasmic protein encoded by Stra8, a novel retinoic acid-responsive gene. J. Cell. Biol. 135(2), 469-477.
Pfahl M. and Chytil F. (1996). Regulation of metabolism by retinoic acid and its nuclear receptors. Annu. Rev. Nutr. 16, 257-283.
Porter S.B., Ong D.E., Chytil F. and Crist M.C.O. (1985). Localization of cellular retinol binding protein and cellular retinoic acid binding protein in the rat testis and epididymis. J. Androl. 6, 197-212.
Rajan N., Kidd G.L., Talmage D.A., Blaner W.S., Suhara A. and Goodan D.S. (1991). Cellular retinoic acid binding protein messenger RNA: levels in rat tissues and localization in rat testis. J. Lipid. Res. 32, 1195-1204.
Ross A.C. (1993). Cellular metabolism and activation of retinoids: roles of cellular retinoid-binding proteins. FASEB J. 7, 317-327.
Rouiller Fabre V., Levacher C., Pairault C., Racine C., Moreau E., Olaso R., Livera G., Migrenne S., Delbes G. and Habert R. (2003). Development of the foetal and neonatal testis. Andrology. 35, 79-83.
Ruberte E., Friederich V., Morriss Kay G. and Champon P. (1992). Differential distribution patterns of CRABP I and CRABP II transcripts during mouse embriyogenesis. Development. 115, 973-987.
Russel L.D., Ettlin R.A., Sinha Hikim A.P. and Clegg E.D. (1990). Histological and Histopathological Evaluation of the Testis. Int. J. Andr. 20, 119-161.
Sato H., Tanji N., Tsuji M., Terada N., Yamasaki K., Wang J., Sakayama K. and Yokoyama M. (2005). Inhibitory effect of all-trans retinoic acid on androgen induced growth of mouse seminal vesicles in vivo and its mechanism. Hum. Exper. Toxicol. 24, 467-474.
Schmitt M.C. and Ong D.E. (1993). Expression of cellular retiol-binding protein and lecithin-retinol acyltransferase in develophing rat testis. Biol. Reprod. 49, 972-979.
Silva C., Wood J.R., Salvador L., Zhang Z., Kostetskii I., Williams C.J. and Straussiii J.F. (2008). Expression profile of male germ cell associated genes in embryonic stem cell cultures treated with all-trans retinoic acid and testosterone. Mol. Reprod. Dev. 79,11-21. www. interscience.wiley.com.
Snyder E.M., Small C. and Griswold M.D. (2010). Retinoic acid availability drives the asynchronous initiation of spermatogonial differentiation in the mouse. Biol. Reprod. 83, 783-790.
Thompson J.N., Howell J.M. and Pitt G.A.J. 1964. Vitamin A and reproduction in rats. Proc. Royal. Soc. Lond. Ser. Biol. Sci. 159, 510-516.
Trautmann E., Guerquin M.J., Duquenne C., Lahaye B., Habert R. and Livera G. (2000). Retinoic acid prevents germ cell mitotic arrest in mouse fetal testes. Cell. Cycle. 7(5), 56-66.
Van Beek M.E. and Meistrich M.C. (1992). Spermatogenesis in retinol-deficient rats maintained on retinoic acid. J. Reprod. Fertil. 94(2), 327-336.
Van Pelt A.M.M. and De Rooij D.G. (1990). The origin of the synchronization of the seminiferous epithelium in vitamin A-deficient rats after vitamin A replacement. Biol. Reprod. 42, 677-682.
Van Pelt A.M.M. and De Rooij D.G. (1991). Retinoic acid is able to reinitiate spermatogenesis in vitamin A deficient rats and high replicate doses support the full development of spermatogenic cells. Endocrinology. 128, 697-704.
Van Pelt A.M.M., Van Den Brink C.E., De Rooij D.G. and Van der Saag P.T. (1992). Changes in retinoic acid receptor messenger ribonucleic acid levels in the vitamin A deficient rat testis after administration of retinoids.Endocrinology. 131, 344-350.
Van Pelt A.M.M., Van Dissel-Emiliani F.M.F., Gaemers I.C., Van Der Burg M.J.M., Tanke H.J. and De Rooij D.G. (1995). Characteristics of A spermatogonia and preleptotene spermatocyetes in the vitamin A deficient rat testis. Biol. Reprod. 53, 570-578.
Van Pelt A.M.M., Morena A.R., van Dissel Emiliani F.M.F., Boitani C., Gaemers I.C., De Rooij D.G. and Stefanini M. (1996). Isolation of the synchronized A spermatogonia from adult vitamin A deficient rat testes. Biol. Reprod. 55, 439-444.
Vernet N., Dennefeld C., Guillou F., Champon P., Ghyselinck N.B. and Mark M. (2006a). Prepubertal testis development relies on retinoic acid but rexinoid receptors in sertoli cells. European Mol. Biol. Organ. J. 25, 5816-5825.
Vernet N., Dennefeld C., Rochette-Egly C., Oulad Abdelghani M., Champon P., Ghyselinck N.B. and Mark M. (2006b). Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis. Endocrinology. 147, 96-110.
Wright W.W. (2010). New insights into the regulation of gametogenesis by retinoic acid. Biol. Reprod. 83, 890-892.
Yamamoto Y., Zolfaghari R. and Ross A.C. (2000). Regulation of CYP26 (cytochrome P450RAI) mRNA expression and retinoic acid metabolism by retinoids and dietary vitamin A in liver of mice and mice. Fed. Am. Soc. Exper. Biol. J. 14, 2119-2127.
Yashiro K., Zhao X., Uehara M., Yamashito K., Nishijima M., Nishino J., Saijoh Y., Sakai Y. and Hamada H. (2004). Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev. Cell. 6, 411-422.
Zhai Y., Sperkova Z. and Napoli J.L. (2001). Cellula expression of retinal dehydrogenase types 1 and 2: effects of vitamin A status on testis mRNA. J. Cell. Physiol. 186, 220-232.
Zhang, F.P., Pakarainen T., Zh F., Poutanen M. and Huhtaniemi I. (2004). Molecular characterization of postnatal development of testicular sterodiogenesis in luteinizing hormone receptor knockout mice. Endocrinology. 145, 1453-1463.
Zheng W.L., Bucco R.A., Schmitt M.C., Wardlaw S.A. and Ong D.E. (1996). Localization of cellular retinoic acid-binding protein (CRABP) II and CRABP in developing rat testis. Endocrinology. 137, 5028-5035.
Zhou Q., Li Y., Nie R., Friel P., Mitchell D., Evanoff R.M., Pounchnik D., Banasik B., Mc Carrey J.R., Small C. and Griswold M.D. (2008). Expression of stimulated by retinoic acid gene 8 (Stra8) and maturation of murine gonocytes and spermatonia induced by retinoic acid in vitro. Biol. Reprod. 78, 537-545.
