CYP26B1 promotes male germ cell differentiation by suppressing STRA8-dependent meiotic and STRA8-independent mitotic pathways

Developmental Biology

Volumn 389, Issue 2, 2014, Pages 173-181

  Saba, Rie ^a   Wu, Quan ^a,b   Saga, Yumiko ^a,b,c  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Cyp26b1; Germ cell; Kit; Meiosis; Mitosis; Retinoic acid; Stra8

Indexed keywords

DNA; RETINOIC ACID;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYP26B1 GENE; DNA REPLICATION; DNMT3L GENE; EMBRYO; FEMALE; GENE; GENE DELETION; GENE EXPRESSION; GENE SILENCING; GERM CELL; IMMUNOHISTOCHEMISTRY; KIT GENE; MALE; MEIOSIS; MICROARRAY ANALYSIS; MITOSIS; MOUSE; NANOS2 GENE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STRA8 GENE;

CYP26B1; GERM CELL; KIT; MEIOSIS; MITOSIS; RETINOIC ACID; STRA8;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL DIFFERENTIATION; CYTOCHROME P-450 ENZYME SYSTEM; GENE EXPRESSION REGULATION; GERM CELLS; MALE; MEIOSIS; MICE; MICE, KNOCKOUT; MITOSIS; PROTO-ONCOGENE PROTEINS C-KIT; RNA-BINDING PROTEINS; TRETINOIN;

EID: 84897545418     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.02.013     Document Type: Article

References (34)

1. Baltus A.E., Menke D.B., Hu Y.-C., Goodheart M.L., Carpenter A.E., De Rooij D.G., Page D.C. In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat. Genet. 2006, 38:1430-1434. 10.1038/ng1919.
2. Bourc'his D., Xu G.L., Lin C.S., Bollman B., Bestor T.H. Dnmt3L and the establishment of maternal genomic imprints. Science 2001, 294:2536-2539. 10.1126/science.1065848.
3. Bowles J., Kight D., Smith C., Wilhelm D., Richman J., Mamiya S., Yashiro K., Chawensaksophak K., Wilson M.J., Rossant J., Hamada H., Koopman P. Retinoid signaling determines germ cell fate in mice. Science 2006, 312:596. 10.1126/science.1125691.
4. Bowles J., Feng C.W., Spiller C., Davidson T.L., Jackson A., Koopman P. FGF9 suppresses meiosis and promotes male germ cell fate in mice. Dev. Cell. 2010, 19:440-449. 10.1016/j.devcel.2010.08.010.
5. Buaas F.W., Kirsh A.L., Sharma M., McLean D.J., Morris J.L., Griswold M.D., de Rooji D.G., Braun R.E. Plzf is required in adult male germ cells for stem cell self-renewal. Nat. Genet. 2004, 36(6):647-652. 10.1038/ng1366.
6. Cheung C.T., Singh R., Yoon A.R., Hasan M.K., Yaguchi T., Kaul S.C., Yun C.O., Wadhwa R. Molecular characterization of apoptosis induced by CARF silencing in human cancer cells. Cell Death Differ. 2011, 18:589-601. 10.1038/cdd.2010.129.
7. Colvin J.S., Green R.P., Schmahl J., Capel B., Ornitz D.M. Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 2001, 104:875-889. 10.1016/S0092-8674(01)00284-7.
8. Costoya J.A., Hobbs R.M., Barna M., Cattoretti G., Manova K., Sukhwani M., Orwig K.E., Wolgemuth D.J., Pandolfi P.P. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat. Genet. 2004, 36(6):653-659. 10.1038/ng1367.
9. Fernandez-Capetillo O., Mahadevaiah S.K., Celeste A., Romanienko P.J., Camerini-Otero R.D., Bonner W.M., Manova K., Burgoyne P., Nussenzweig A. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell. 2003, 4:497-508. 10.1016/S1534-5807(03)00093-5.
10. Hiramatsu R., Kanai Y., Mizukami T., Ishii M., Matoba S., Kanai-azuma M., Kurohmaru M., Kawakami H., Hayashi Y. Regionally distinct potencies of mouse XY genital ridge to initiate testis differentiation dependent on anteroposterior axis. Dev. Dyn. 2003, 228:247-253. 10.1002/dvdy.
11. Kohoutek J., Dvorák P., Hampl A. Temporal distribution of CDK4, CDK6, D-type cyclins, and p27 in developing mouse oocytes. Biol. Reprod. 2004, 70:139-145. 10.1095/biolreprod.103.017335.
12. Koubova J., Menke D.B., Zhou Q., Capel B., Griswold M.D., Page D.C. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc. Natl. Acad. Sci. USA 2006, 103:2474-2479. 10.1073/pnas.0510813103.
13. Kumar S., Chatzi C., Brade T., Cunningham T.J., Zhao X., Duester G. Sex-specific timing of meiotic initiation is regulated by Cyp26b1 independent of retinoic acid signalling. Nat. Commun. 2011, 2:151. 10.1038/ncomms1136.
14. 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. 10.1371/journal.pone.0007501.
15. 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. 10.1210/en.2007-0492.
16. McClelland K., Bowles J., Koopman P. Male sex determination: insights into molecular mechanisms. Asian J. Adrol. 2012, 14:164-171. 10.1038/aja.2011.169.
17. Morita-Fujimura Y., Tokitake Y., Matsui Y. Heterogeneity of mouse primordial germ cells reflecting the distinct status of their differentiation, proliferation and apoptosis can be classified by the expression of cell surface proteins integrin α6 and c-Kit. Dev. Growth Differ. 2009, 51:567-583. 10.1111/j.1440-169X.2009.01119.x.
18. Ottolenghi C., Pelosi E., Tran J., Colombino M., Douglass E., Nedorezov T., Cao A., Forabosco A., Schlessinger D. Loss of Wnt4 and Foxl2 leads to female-to-male sex reversal extending to germ cells. Hum. Mol. Genet. 2007, 16:2795-2804. 10.1093/hmg/ddm235.
19. Pellegrini M., Filipponi D., Gori M., Barrios F., Lolicato F., Grimaldi P., Rossi P., Jannini E.A., Geremia R., Dolci S. ATRA and KL promote differentiation toward the meiotic program of male germ cells. Cell Cycle 2008, 7:3878-3888.
20. Roig M.B., Roset R., Ortet L., Balsiger N.A., Anfosso A., Cabellos L., Garrido M., Alameda F., Brady H.J.M., Gil-Gómez G. Identification of a novel cyclin required for the intrinsic apoptosis pathway in lymphoid cells. Cell Death Differ. 2009, 16:230-243. 10.1038/cdd.2008.145.
21. Saba R., Kato Y., Saga Y. NANOS2 promotes male germ cell development independent of meiosis suppression. Dev. Biol. 2014, 385(1):32-40. 10.1016/j.ydbio.2013.10.018.
22. Schrans-Stassen B.H.G.J., van de Kant H.J., de Rooij D.G., van Pelt A.M. Differential expression of c- kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology 1999, 140(12):5894-5900. 10.1210/en.140.12.5894.
23. Spiller C.M., Koopman P. Cell Cycle Control of Germ Cell Differentiation. Cell Cycle in Development 2011, 269-308. Springer, Berlin Heidelberg. 10.1007/978-3-642-19065-0.
24. Suzuki A., Saga Y. Nanos2 suppresses meiosis and promotes male germ cell differentiation service. Genes Dev. 2008, 22:430-435. 10.1101/gad.1612708.
25. Suzuki A., Tsuda M., Saga Y. Functional redundancy among Nanos proteins and a distinct role of Nanos2 during male germ cell development. Development 2007, 83:77-83. 10.1242/dev.02697.
26. Suzuki H., Sada A., Yoshida S., Saga Y. The heterogeneity of spermatogonia is revealed by their topology and expression of marker proteins including the germ cell-specific proteins Nanos2 and Nanos3. Dev. Biol. 2009, 336:222-231. 10.1016/j.ydbio.2009.10.002.
27. Traut W., Endl E., Scholzen T., Gerdes J., Winking H. The temporal and spatial distribution of the proliferation associated Ki-67 protein during female and male meiosis. Chromosoma 2002, 111:156-164. 10.1007/s00412-002-0202-8.
28. Trautmann E., Guerquin M., Duquenne C., Lahaye J., Habert R. Retinoic acid prevents germ cell mitotic arrest in mouse fetal testis. Cell Cycle 2008, 7(5):656-664. 10.4161/cc.7.5.5482.
29. Tsuda M., Sasaoka Y., Kiso M., Abe K., Haraguchi S., Kobayashi S., Saga Y. Conserved role of nanos proteins in germ cell development. Science 2003, 301:1239-1241. 10.1126/science.1085222.
30. Western P.S., Miles D.C., Van den Bergen J.A., Burton M., Sinclair A.H. Dynamic regulation of mitotic arrest in fetal male germ cells. Stem Cells 2008, 26:339-347. 10.1634/stemcells.2007-0622.
31. Wu Q., Kanata K., Saba R., Deng C.-X., Hamada H., Saga Y. Nodal/activin signaling promotes male germ cell fate and suppresses female programming in somatic cells. Development 2013, 140:291-300. 10.1242/dev.087882.
32. Yashiro K., Zhao X., Uehara M., Yamashita K., Nishijima M., Nishino J., Saijoh Y., Sakai Y. Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev. Cell 2004, 6:411-422. 10.1016/S1534-5807(04)00062-0.
33. Yoshida S., Takakura A., Ohbo K., Abe K., Wakabayashi J., Yamamoto M., Suda T., Nabeshima Y.-I. Neurogenin3 delineates the earliest stages of spermatogenesis in the mouse testis. Dev. Biol. 2004, 269:447-458. 10.1016/j.ydbio.2004.01.036.
34. Yuan L., Liu J.G., Zhao J., Brundell E., Daneholt B., Höög C. The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol. Cell 2000, 5:73-83. 10.1016/S1097-2765(00)80404-9.