Expression profile of male germ cell-associated genes in mouse embryonic stem cell cultures treated with all-trans retinoic acid and testosterone

Molecular Reproduction and Development

Volumn 76, Issue 1, 2009, Pages 11-21

  Silva, Celso ^a,b   Wood, Jennifer R ^c   Salvador, Lisa ^b   Zhang, Zhibing ^d   Kostetskii, Igor ^b   Williams, Carmen J ^b   Strauss III, Jerome F ^d,e  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^d VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e 1 071 Sanger Hall ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOIC ACID; TESTOSTERONE;

ACT GENE; AKAP3 GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DAZL GENE; DEVELOPMENTAL STAGE; DPPA3 GENE; EMBRYONIC STEM CELL; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; GERM CELL; MALE; MOUSE; MSY2 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; ODF2 GENE; PIWIL2 GENE; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PRM1 GENE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPERMATOGENESIS; STRA8 GENE; SYCP1 GENE; SYCP3 GENE; TEX14 GENE;

ANIMALS; BIOLOGICAL MARKERS; CELL ADHESION; CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MALE; MICE; SPERMATOZOA; TESTOSTERONE; TRETINOIN;

MURINAE;

EID: 58449087949     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.20925     Document Type: Article

References (47)

1. Chang CY, Hsuuw YD, Huang FJ, Shyr CR, Chang SY, Huang CK, Kang HY, Huang KE. 2006. Androgenic and antiandrogenic effects and expression of androgen receptor in mouse embryonic stem cells. Fertil Steril 85:1195-1203.
2. Dani C, Smith AG, Dessolin S, Leroy P, Staccini L, Villageois P, Darimont C, Ailhaud G. 1997. Differentiation of embryonic stem cells into adipocytes in vitro. J Cell Sci 110:1279-1285.
3. De Felici M, Pesce M. 1994. Growth factors in mouse primordial germ cell migration and proliferation. Prog Growth Factor Res 5:135-143.
4. Di Carlo AD, Travia G, De Felici M. 2000. The meiotic specific synaptonemal complex protein SCP3 is expressed by female and male primordial germ cells of the mouse embryo. Int J Dev Biol 44:241-244.
5. Donovan PJ, Stott D, Cairns LA, Heasman J, Wylie CC. 1986. Migratory and postmigratory mouse primordial germ cells behave differently in culture. Cell 44:831-838.
6. Drab M, Haller H, Bychkov R, Erdmann B, Lindschau C, Haase H, Morano I, Luft FC, Wobus AM. 1997. From totipotent embryonic stem cells to spontaneously contracting smooth muscle cells: A retinoic acid and db-cAMP in vitro differentiation model. FASEB J 11:905-915.
7. Dyce PW, Wen L, Li J. 2006. In vitro germline potential of stem cells derived from fetal porcine skin. Nat Cell Biol 8:384-390.
8. Eddy EM. 2002. Male germ cell gene expression. Recent Prog Horm Res 57:103-128.
9. Evans MJ, Kaufman MH. 1981. Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154-156.
10. Evans JP, Schultz RM, Kopf GS. 1995. Identification and localization of integrin subunits in oocytes and eggs of the mouse. Mol Reprod Dev 40:211-220.
11. Fimia GM, Morlon A, Macho B, De Cesare D, Sassone-Corsi P. 2001. Transcriptional cascades during spermatogenesis: Pivotal role of CREM and ACT. Mol Cell Endocrinol 179:17-23.
12. Geijsen N, Horoschak M, Kim K, Gribnau J, Eggan K, Daley GQ. 2004. Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature 427:148-154.
13. Goldman-Johnson DR, de Kretser DM, Morrison JR. 2008. Evidence that androgens regulate early developmental events, prior to sexual differentiation. Endocrinology 149:5-14.
14. Griswold MD. 1998. The central role of Sertoli cells in spermatogenesis. Semin Cell Dev Biol 9:411-416.
15. Gu W, Tekur S, Reinbold R, Eppig JJ, Choi YC, Zheng JZ, Murray MT, Hecht NB. 1998. Mammalian male and female germ cells express a germ cell-specific Y-Box protein, M SY2. Biol Reprod 59:1266-1274.
16. Horowitz E, Zhang Z, Jones BH, Moss SB, Ho C, Wood JR, Wang X, Sammel MD, Strauss JF III. 2005. Patterns of expression of sperm flagellar genes: Early expression of genes encoding axonemal proteins during the spermatogenic cycle and shared features of promoters of genes encoding central apparatus proteins. Mol Hum Reprod 11:307-317.
17. Huang H, Zhao X, Chen L, Xu C, Yao X, Lu Y, Dai L, Zhang M. 2006. Differentiation of human embryonic stem cells into smooth muscle cells in adherent monolayer culture. Biochem Biophys Res Commun 351:321-327.
18. Hubner K, Fuhrmann G, Christenson LK, Kehler J, Reinbold R, De La Fuente R, Wood J, Strauss JF III, Boiani M, Scholer HR. 2003. Derivation of oocytes from mouse embryonic stem cells. Science 300:1251-1256.
19. Kehler J, Tolkunova E, Koschorz B, Pesce M, Gentile L, Boiani M, Lomeli H, Nagy A, McLaughlin KJ, Scholer HR, Tomilin A. 2004. Oct4 is required for primordial germ cell survival. EMBO Rep 5:1078-1083.
20. Keller G. 2005. Embryonic stem cell differentiation: Emergence of a new era in biology and medicine. Genes Dev 19:1129-1155.
21. Kleene KC, Distel RJ, Hecht NB. 1984. Translational regulation and deadenylation of a protamine mRNA during spermiogenesis in the mouse. Dev Biol 105:71-79.
22. Koshimizu U, Watanabe M, Nakatsuji N. 1995. Retinoic acid is a potent growth activator of mouse primordial germ cells in vitro. Dev Biol 168:683-685.
23. Lacham-Kaplan O, Chy H, Trounson A. 2006. Testicular cell conditioned medium supports differentiation of embryonic stem cells into ovarian structures containing oocytes. Stem Cells (Dayton, Ohio) 24:266-273.
24. Lee JH, Engel W, Nayernia K. 2006. Stem cell protein Piwil2 modulates expression of murine spermatogonial stem cell expressed genes. Mol Reprod Dev 73:173-179.
25. Micallef SJ, Janes ME, Knezevic K, Davis RP, Elefanty AG, Stanley EG. 2005. Retinoic acid induces Pdx1-positive endoderm in differentiating mouse embryonic stem cells. Diabetes 54:301-305.
26. Morriss-Kay GM, Sokolova N. 1996. Embryonic development and pattern formation. FASEB J 10:961-968.
27. Nagano MC. 2007. In vitro gamete derivation from pluripotent stem cells: Progress and perspective. Biol Reprod 76:546-551.
28. Nayernia K, Nolte J, Michelmann HW, Lee JH, Rathsack K, Drusenheimer N, Dev A, Wulf G, Ehrmann IE, Elliott DJ, Okpanyi V, Zechner U, Haaf T, Meinhardt A, Engel W. 2006. In vitro-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice. Dev cell 11:125-132.
29. Nelson VL, Qin KN, Rosenfield RL, Wood JR, Penning TM, Legro RS, Strauss JF III, McAllister JM. 2001. The biochemical basis for increased testosterone production in theca cells propagated from patients with polycystic ovary syndrome. J Clin Endocrinol Metab 86:5925-5933.
30. Ohinata Y, Payer B, O'Carroll D, Ancelin K, Ono Y, Sano M, Barton SC, Obukhanych T, Nussenzweig M, Tarakhovsky A, Saitou M, Surani MA. 2005. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436:207-213.
31. Okada Y, Shimazaki T, Sobue G, Okano H. 2004. Retinoic-acid- concentration-dependent acquisition of neural cell identity during in vitro differentiation of mouse embryonic stem cells. Dev Biol 275:124-142.
32. Oulad-Abdelghani M, Bouillet P, Decimo D, Gansmuller A, Heyberger S, Dolle P, Bronner S, Lutz Y, Chambon P. 1996. Characterization of a premeiotic germ cell-specific cytoplasmic protein encoded by Stra8, a novel retinoic acid-responsive gene. J Cell Biol 135:469-477.
33. Rocchietti-March M, Weinbauer GF, Page DC, Nieschlag E, Gromoll J. 2000. Dazl protein expression in adult rat testis is up-regulated at meiosis and not hormonally regulated. Int J Androl 23:51-56.
34. Rohwedel J, Guan K, Wobus AM. 1999. Induction of cellular differentiation by retinoic acid in vitro. Cells Tissues Organs 165:190-202.
35. Saitou M, Barton SC, Surani MA. 2002. A molecular programme for the specification of germ cell fate in mice. Nature 418:293-300.
36. Salero E, Hatten ME. 2007. Differentiation of ES cells into cerebellar neurons. Proc Natl Acad Sci USA 104:2997-3002.
37. Strubing C, Ahnert-Hilger G, Shan J, Wiedenmann B, Hescheler J, Wobus AM. 1995. Differentiation of pluripotent embryonic stem cells into the neuronal lineage in vitro gives rise to mature inhibitory and excitatory neurons. Mech Dev 53:275-287.
38. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. 1998. Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147.
39. Tighe AP, Gudas LJ. 2004. Retinoic acid inhibits leukemia inhibitory factor signaling pathways in mouse embryonic stem cells. J Cell Physiol 198:223-229.
40. Toyooka Y, Tsunekawa N, Akasu R, Noce T. 2003. Embryonic stem cells can form germ cells in vitro. Proc Natl Acad Sci USA 100:11457-11462.
41. West JA, Park IH, Daley GQ, Geijsen N. 2006. In vitro generation of germ cells from murine embryonic stem cells. Nature Protoc 1:2026-2036.
42. Wobus AM, Kleppisch T, Maltsev V, Hescheler J. 1994. Cardiomyocyte-like cells differentiated in vitro from embryonic carcinoma cells P19 are characterized by functional expression of adrenoceptors and Ca2+ channels. In Vitro Cell Dev Biol 30:425-434.
43. Wolgemuth DJ, Chung SS. 2007. Retinoid signaling during spermatogenesis as revealed by genetic and metabolic manipulations of retinoic acid receptor alpha. Soc Reprod Fertil Suppl 63:11-23.
44. Wood JR, Nelson VL, Ho C, Jansen E, Wang CY, Urbanek M, McAllister JM, Mosselman S, Strauss JF III. 2003. The molecular phenotype of polycystic ovary syndrome (PCOS) theca cells and new candidate PCOS genes defined by microarray analysis. J Biol Chem 278:26380-26390.
45. Wu MH, Rajkovic A, Burns KH, Yan W, Lin YN, Matzuk MM. 2003. Sequence and expression of testis-expressed gene 14 (Tex14): A gene encoding a protein kinase preferentially expressed during spermatogenesis. Gene Expr Patterns 3:231-236.
46. Zhang Z, Kostetskii I, Moss SB, Jones BH, Ho C, Wang H, Kishida T, Gerton GL, Radice GL, Strauss JF III. 2004. Haploinsufficiency for the murine orthologue of Chlamydomonas PF20 disrupts spermatogenesis. Proc Natl Acad Sci USA 101:12946-12951.
47. Zhang Z, Kostetskii I, Tang W, Haig-Ladewig L, Sapiro R, Wei Z, Patel AM, Bennett J, Gerton GL, Moss SB, Radice GL, Strauss JF III. 2006. Deficiency of SPAG16L causes male infertility associated with impaired sperm motility. Biol Reprod 74:751-759.