CYP26 enzymes are necessary within the postnatal seminiferous epithelium for normal murine spermatogenesis

Biology of Reproduction

Volumn 93, Issue 1, 2015, Pages

  Hogarth, Cathryn A ^a   Evans, Elizabeth ^a   Onken, Jennifer ^a   Kent, Travis ^a   Mitchell, Debra ^a   Petkovich, Martin ^b   Griswold, Michael D ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

CYP26; Retinoic acid; Sertoli cells; Spermatogenesis; Testis

Indexed keywords

CYTOCHROME; CYTOCHROME P450 26A1; CYTOCHROME P450 26B1; UNCLASSIFIED DRUG; CYP26A1 PROTEIN, MOUSE; CYP26B1 PROTEIN, MOUSE; CYTOCHROME P450; CYTOCHROME P450 FAMILY 26; SIGNAL TRANSDUCING ADAPTOR PROTEIN; STRA8 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BASEMENT MEMBRANE; BODY WEIGHT; CELL VACUOLE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GERM CELL; IMMUNOHISTOCHEMISTRY; MALE; MALE FERTILITY; MOUSE; NONHUMAN; PERINATAL PERIOD; PHENOTYPIC VARIATION; PRIORITY JOURNAL; SEMINIFEROUS TUBULE; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; SPERMATID; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON; SUBFERTILITY; TESTIS; ANIMAL; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALIA; MURINAE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CYTOCHROME P-450 ENZYME SYSTEM; GERM CELLS; MALE; MICE; MICE, KNOCKOUT; RETINOIC ACID 4-HYDROXYLASE; SEMINIFEROUS EPITHELIUM; SERTOLI CELLS; SPERMATOGENESIS; SPERMATOGONIA; SPERMATOZOA;

EID: 84938925785     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.115.129718     Document Type: Article

References (38)

1. Hogarth CA, Griswold MD. The key role of vitamin A in spermatogenesis. J Clin Invest 2010; 120:956-962.
2. McLean DJ, Russell LD, Griswold MD. Biological activity and enrichment of spermatogonial stem cells in vitamin A-deficient and hyperthermia-exposed testes from mice based on colonization following germ cell transplantation. Biol Reprod 2002; 66:1374-1379.
3. Mitranond V, Sobhon P, Tosukhowong P, Chindaduangrat W. Cytological changes in the testes of vitamin-A-deficient rats. I. Quantitation of germinal cells in the seminiferous tubules. Acta Anat (Basel) 1979; 103:159-168.
4. Griswold MD, Bishop PD, Kim KH, Ping R, Siiteri JE, Morales C. Function of vitamin A in normal and synchronized seminiferous tubules. Ann N Y Acad Sci 1989; 564:154-172.
5. Van Pelt AM, De Rooij DG. The origin of the synchronization of the seminiferous epithelium in vitamin A-deficient rats after vitamin A replacement. Biol Reprod 1990; 42:677-682.
6. van Pelt AM, de Rooij DG. Synchronization of the seminiferous epithelium after vitamin A replacement in vitamin A-deficient mice. Biol Reprod 1990; 43:363-367.
7. Snyder EM, Davis JC, Zhou Q, EvanoffR, Griswold MD. Exposure to retinoic acid in the neonatal but not adult mouse results in synchronous spermatogenesis. Biol Reprod 2011; 84:886-893.
8. Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci U S A 2006; 103:2474-2479.
9. Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, Yashiro K, Chawengsaksophak K, Wilson MJ, Rossant J, Hamada H, Koopman P. Retinoid signaling determines germ cell fate in mice. Science 2006; 312:596-600.
10. Snyder EM, Small C, Griswold MD. Retinoic acid availability drives the asynchronous initiation of spermatogonial differentiation in the mouse. Biol Reprod 2010; 83:783-790.
11. Sugimoto R, Nabeshima Y, Yoshida S. Retinoic acid metabolism links the periodical differentiation of germ cells with the cycle of Sertoli cells in mouse seminiferous epithelium. Mech Dev 2012; 128:610-624.
12. Hogarth CA, Arnold S, Kent T, Mitchell D, Isoherranen N, Griswold MD. Processive pulses of retinoic acid propel asynchronous and continuous murine sperm production. Biol Reprod 2015; 92:37.
13. Napoli JL. Physiological insights into all-trans-retinoic acid biosynthesis. Biochim Biophys Acta 2012; 1821:152-167.
14. Thatcher JE, Isoherranen N. The role of CYP26 enzymes in retinoic acid clearance. Expert Opin Drug Metab Toxicol 2009; 5:875-886.
15. Small CL, Shima JE, Uzumcu M, Skinner MK, Griswold MD. Profiling gene expression during the differentiation and development of the murine embryonic gonad. Biol Reprod 2005; 72:492-501.
16. Yashiro K, Zhao X, Uehara M, Yamashita K, Nishijima M, Nishino J, Saijoh Y, Sakai Y, Hamada H. Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev Cell 2004; 6:411-422.
17. Abu-Abed S, Dolle P, Metzger D, Beckett B, Chambon P, Petkovich M. The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures. Genes Dev 2001; 15:226-240.
18. Uehara M, Yashiro K, Mamiya S, Nishino J, Chambon P, Dolle P, Sakai Y. CYP26A1 and CYP26C1 cooperatively regulate anterior-posterior patterning of the developing brain and the production of migratory cranial neural crest cells in the mouse. Dev Biol 2007; 302:399-411.
19. Li H, MacLean G, Cameron D, Clagett-Dame M, Petkovich M. Cyp26b1 expression in murine Sertoli cells is required to maintain male germ cells in an undifferentiated state during embryogenesis. PLoS One 2009; 4:e7501.
20. Lecureuil C, Fontaine I, Crepieux P, Guillou F. Sertoli and granulosa cellspecific Cre recombinase activity in transgenic mice. Genesis 2002; 33:114-118.
21. Sanz E, Yang L, Su T, Morris DR, McKnight GS, Amieux PS. Cell-typespecific isolation of ribosome-associated mRNA from complex tissues. Proc Natl Acad Sci U S A 2009; 106:13939-13944.
22. Gallagher SJ, Kofman AE, Huszar JM, Dannenberg JH, DePinho RA, Braun RE, Payne CJ. Distinct requirements for Sin3a in perinatal male gonocytes and differentiating spermatogonia. Dev Biol 2013; 373:83-94.
23. Sadate-Ngatchou PI, Payne CJ, Dearth AT, Braun RE. Cre recombinase activity specific to postnatal, premeiotic male germ cells in transgenic mice. Genesis 2008; 46:738-742.
24. MacLean G, Li H, Metzger D, Chambon P, Petkovich M. Apoptotic extinction of germ cells in testes of Cyp26b1 knockout mice. Endocrinology 2007; 148:4560-4567.
25. Hogarth CA, Griswold MD. Immunohistochemical approaches for the study of spermatogenesis. Methods Mol Biol 2013; 927:309-320.
26. Russell LD, Ettlin RA, Sinha Hakim AP, Clegg ED. Histological and Histopathological Evaluation of the Testis. Clearwater, FL: Cache River Press; 1990.
27. Siiteri JE, Karl AF, Linder CC, Griswold MD. Testicular synchrony:evaluation and analysis of different protocols. Biol Reprod 1992; 46:284-289.
28. Van Beek ME, Meistrich ML. A method for quantifying synchrony in testes of rats treated with vitamin A deprivation and readministration. Biol Reprod 1990; 42:424-431.
29. Snyder EM, Davis JC, Zhou Q, EvanoffR, Griswold MD. Exposure to retinoic acid in the neonatal but not adult mouse results in synchronous spermatogenesis. Biol Reprod 2011; 84:886-893.
30. Davis JC, Snyder EM, Hogarth CA, Small C, Griswold MD. Induction of spermatogenic synchrony by retinoic acid in neonatal mice. Spermatogenesis 2013; 3:e23180.
31. Li H, Palczewski K, Baehr W, Clagett-Dame M. Vitamin A deficiency results in meiotic failure and accumulation of undifferentiated spermatogonia in prepubertal mouse testis. Biol Reprod 2011; 84:336-341.
32. van Pelt AM, de Rooij DG. Synchronization of the seminiferous epithelium after vitamin A replacement in vitamin A-deficient mice. Biol Reprod 1990; 43:363-367.
33. Hogarth CA, EvanoffR, Mitchell D, Kent T, Small C, Amory JK, Griswold MD. Turning a spermatogenic wave into a tsunami: synchronizing murine spermatogenesis using WIN 18,446. Biol Reprod 2013; 88:40.
34. Huang HF, Marshall GR. Failure of spermatid release under various vitamin A states-an indication of delayed spermiation. Biol Reprod 1983; 28:1163-1172.
35. Raverdeau M, Gely-Pernot A, Feret B, Dennefeld C, Benoit G, Davidson I, Chambon P, Mark M, Ghyselinck NB. Retinoic acid induces Sertoli cell paracrine signals for spermatogonia differentiation but cell autonomously drives spermatocyte meiosis. Proc Natl Acad Sci U S A 2012; 109:16582-16587.
36. Kumar S, Chatzi C, Brade T, Cunningham TJ, Zhao X, Duester G. Sexspecific timing of meiotic initiation is regulated by Cyp26b1 independent of retinoic acid signalling. Nat Commun 2011; 2:151.
37. Tong MH, Yang QE, Davis JC, Griswold MD. Retinol dehydrogenase 10 is indispensible for spermatogenesis in juvenile males. Proc Natl Acad Sci U S A 2013; 110:543-548.
38. Vernet N, Dennefeld C, Rochette-Egly C, Oulad-Abdelghani M, Chambon P, Ghyselinck NB, Mark M. Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis. Endocrinology 2006; 147:96-110.