PSCDGs of mouse multipotent adult germline stem cells can enter and progress through meiosis to form haploid male germ cells in vitro

Differentiation

Volumn 80, Issue 4-5, 2010, Pages 184-194

  Nolte, Jessica ^a   Michelmann, Hans W ^a   Wolf, Marieke ^b   Wulf, Gerald ^a   Nayernia, Karim ^c   Meinhardt, Andreas ^d   Zechner, Ulrich ^b   Engel, Wolfgang ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Multipotent adult germline stem cells; Pluripotent stem cell derived gametes; Spermatogenesis; Spermatogonial stem cells

Indexed keywords

EPIDERMAL GROWTH FACTOR; RETINOIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL RENEWAL; CONTROLLED STUDY; DEMETHYLATION; EMBRYONIC STEM CELL; EPIGENETICS; FLUORESCENCE ACTIVATED CELL SORTING; GAMETE; GENE EXPRESSION PROFILING; GENOTYPE; HAPLOIDY; IN VITRO STUDY; MALE; MEIOSIS; MOUSE; NONHUMAN; OOCYTE; PLURIPOTENT STEM CELL; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN METHYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOMATIC CELL; SPERMATOGENESIS; TRANSGENE;

ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; EMBRYO, MAMMALIAN; GERM CELLS; HAPLOIDY; MALE; MEIOSIS; MICE; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; MULTIPOTENT STEM CELLS; PLURIPOTENT STEM CELLS; SPERMATOGENESIS;

MAMMALIA; MUS MUSCULUS;

EID: 78049270270     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2010.08.001     Document Type: Article

References (43)

1. Akmal K.M., Dufour J.M., Kim K.H. Retinoic acid receptor alpha gene expression in the rat testis: potential role during the prophase of meiosis and in the transition from round to elongating spermatids. Biol. Reprod. 1997, 56:549-556.
2. Bowles J., Knight D., Smith C., Wilhelm D., Richman J., Mamiya S., Yashiro K., Chawengsaksophak K., Wilson M.J., Rossant J., Hamada H., Koopman P. Retinoid signaling determines germ cell fate in mice. Science 2006, 312:596-600.
3. Bucay N., Yebra M., Cirulli V., Afrikanova I., Kaido T., Hayek A., Montgomery A.M. A novel approach for the derivation of putative primordial germ cells and sertoli cells from human embryonic stem cells. Stem Cells 2009, 27:68-77.
4. Chen H.F., Kuo H.C., Chien C.L., Shun C.T., Yao Y.L., Ip P.L., Chuang C.Y., Wang C.C., Yang Y.S., Ho H.N. Derivation, characterization and differentiation of human embryonic stem cells: comparing serum-containing versus serum-free media and evidence of germ cell differentiation. Hum. Reprod. 2007, 22:567-577.
5. Clark A.T., Bodnar M.S., Fox M., Rodriquez R.T., Abeyta M.J., Firpo M.T., Pera R.A. Spontaneous differentiation of germ cells from human embryonic stem cells in vitro. Hum. Mol. Genet. 2004, 13:727-739.
6. Eguizabal C., Shovlin T.C., Durcova-Hills G., Surani A., McLaren A. Generation of primordial germ cells from pluripotent stem cells. Differentiation 2009, 78:116-123.
7. Farini D., Scaldaferri M.L., Iona S., La Sala G., De Felici M. Growth factors sustain primordial germ cell survival, proliferation and entering into meiosis in the absence of somatic cells. Dev. Biol. 2005, 285:49-56.
8. Geijsen N., Horoschak M., Kim K., Gribnau J., Eggan K., Daley G.Q. Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature 2004, 427:148-154.
9. Guan K., Nayernia K., Maier L.S., Wagner S., Dressel R., Lee J.H., Nolte J., Wolf F., Li M., Engel W., Hasenfuss G. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 2006, 440:1199-1203.
10. Guan K., Wagner S., Unsöld B., Maier L.S., Kaiser D., Hemmerlein B., Nayernia K., Engel W., Hasenfuss G. Generation of functional cardiomyocytes from adult mouse spermatogonial stem cells. Circ. Res. 2007, 100:1615-1625.
11. Hajkova P., Erhardt S., Lane N., Haaf T., El-Maarri O., Reik W., Walter J., Surani M.A. Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev. 2002, 117:15-23.
12. Hinxton Group, 2008. http://www.hinxtongroup.org/Consensus_HG08_FINAL.pdf.
13. Hua J., Sidhu K. Recent advances in the derivation of germ cells from the embryonic stem cells. Stem Cells Dev. 2008, 17:399-411.
14. Kee K., Gonsalves J.M., Clark A.T., Pera R.A. Bone morphogenetic proteins induce germ cell differentiation from human embryonic stem cells. Stem Cells Dev. 2006, 15:831-837.
15. Kerkis A., Fonseca S.A., Serafim R.C., Lavagnolli T.M., Abdelmassih S., Abdelmassih R., Kerkis I. In vitro differentiation of male mouse embryonic stem cells into both presumptive sperm cells and oocytes. Cloning Stem Cells 2007, 9:535-548.
16. Koshimizu U., Watanabe M., Nakatsuji N. Retinoic acid is a potent growth activator of mouse primordial germ cells in vitro. Dev. Biol. 1995, 168:683-685.
17. Kurrasch D.M, Huang J., Wilkie T.M., Repa J.J. Quantitative real-time polymerase chain reaction measurement of regulators of G-protein signaling mRNA levels in mouse tissues. Meth. Enzymol. 2004, 389:3-15.
18. Lacham-Kaplan O., Chy H., Trounson A. Testicular cell conditioned medium supports differentiation of embryonic stem cells into ovarian structures containing oocytes. Stem Cells 2006, 24:266-273.
19. Lavagnolli T.M., Fonseca S.A., Serafim R.C., Pereira V.S., Santos E.J., Abdelmassih S., Kerkis A., Kerkis I. Presumptive germ cells derived from mouse pluripotent somatic cell hybrids. Differentiation 2009, 78:124-130.
20. Leid M., Kastner P., Chambon P. Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem. Sci. 1992, 17:427-433.
21. Lucifero D., Mertineit C., Clarke H.J., Bestor T.H., Trasler J.M. Methylation dynamics of imprinted genes in mouse germ cells. Genomics 2002, 79:530-538.
22. Lucifero D., Reik W. Artificial sperm and epigenetic reprogramming. Nat. Biotechnol. 2006, 24:1097-1098.
23. Marques-Mari A.I., Lacham-Kaplan O., Medrano J.V., Pellicer A., Simón C. Differentiation of germ cells and gametes from stem cells. Hum. Reprod. Update 2009, 15:379-390.
24. Mathews D.J., Donovan P.J., Harris J., Lovell-Badge R., Savulescu J., Faden R. Pluripotent stem cell-derived gametes: truth and (potential) consequences. Cell Stem Cell 2009, 5:11-14.
25. McLaren A. Germ and somatic cell lineages in the developing gonad. Mol. Cell. Endocrinol. 2000, 163:3-9.
26. Mikkola M., Olsson C., Palgi J., Ustinov J., Palomaki T., Horelli-Kuitunen N., Knuutila S., Lundin K., Otonkoski T., Tuuri T. Distinct differentiation characteristics of individual human embryonic stem cell lines. BMC Dev. Biol. 2006, 6:40.
27. Nagano M.C. In vitro gamete derivation from pluripotent stem cells: progress and perspective. Biol. Reprod. 2007, 76:546-551.
28. Nayernia K., Li M., Jaroszynski L., Khusainov R., Wulf G., Schwandt I., Korabiowska M., Michelmann H.W., Meinhardt A., Engel W. Stem cell based therapeutical approach of male infertility by teratocarcinoma derived germ cells. Hum. Mol. Genet. 2004, 13:1451-1460.
29. Nayernia K., Nolte J., Michelmann H.W., Lee J.H., Rathsack K., Drusenheimer N., Dev A., Wulf G., Ehrmann I.E., Elliott D.J., Okpanyi V., Zechner U., Haaf T., Meinhardt A., Engel W. In vitro-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice. Dev. Cell 2006, 11:125-132.
30. Oulad-Abdelghani M., Bouillet P., Décimo D., Gansmuller A., Heyberger S., Dollé P., Bronner S., Lutz Y., Chambon P. Characterization of a premeiotic germ cell-specific cytoplasmic protein encoded by Stra8, a novel retinoic acid-responsive gene. J. Cell Biol. 1996, 135:469-477.
31. Park T.S., Galic Z., Conway A.E., Lindgren A., van Handel B.J., Magnusson M., Richter L., Teitell M.A., Mikkola H.K., Lowry W.E., Plath K., Clark A.T. Derivation of primordial germ cells from human embryonic and induced pluripotent stem cells is significantly improved by coculture with human fetal gonadal cells. Stem Cells 2009, 27:783-795.
32. Reijo R.A., Dorfman D.M., Slee R., Renshaw A.A., Loughlin K.R., Cooke H., Page D.C. DAZ family proteins exist throughout male germ cell development and transit from nucleus to cytoplasm at meiosis in humans and mice. Biol. Reprod. 2000, 63:1490-1496.
33. Saitou M., Barton S.C., Surani M.A. A molecular programme for the specification of germ cell fate in mice. Nature 2002, 418:293-300.
34. Suzuki K., Yanagimachi R. Beneficial effect of medium with high concentration serum for direct sperm injection into mouse oocytes using a conventional pipette. Zygote 1997, 5:111-116.
35. Tanaka S.S., Toyooka Y., Akasu R., Katoh-Fukui Y., Nakahara Y., Suzuki R., Yokoyama M., Noce T. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev. 2000, 14:841-853.
36. Tegelenbosch R.A., de Rooij D.G. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat. Res. 1993, 290:193-200.
37. Tilgner K., Atkinson S.P., Golebiewska A., Stojkovic M., Lako M., Armstrong L. Isolation of primordial germ cells from differentiating human embryonic stem cells. Stem Cells 2008, 26:3075-3085.
38. Toyooka Y., Tsunekawa N., Akasu R., Noce T. Embryonic stem cells can form germ cells in vitro. Proc. Natl. Acad. Sci. USA 2003, 100:11457-11462.
39. Wang P.J., McCarrey J.R., Yang F., Page D.C. An abundance of X-linked genes expressed in spermatogonia. Nat. Genet. 2001, 27:422-426.
40. Wei W., Qing T., Ye X., Liu H., Zhang D., Yang W., Deng H. Primordial germ cell specification from embryonic stem cells. PLoS One 2008, 3:e4013.
41. Yu Z., Ji P., Cao J., Zhu S., Li Y., Zheng L., Chen X., Feng L. Dazl promotes germ cell differentiation from embryonic stem cells. J. Mol. Cell Biol. 2009, 1:93-103.
42. Zechner U., Nolte J., Wolf M., Shirneshan K., Hajj N.E., Weise D., Kaltwasser B., Zovoilis A., Haaf T., Engel W. Comparative methylation profiles and telomerase biology of mouse multipotent adult germline stem cells and embryonic stem cells. Mol. Hum. Reprod. 2009, 15:345-353.
43. Zovoilis A., Nolte J., Drusenheimer N., Zechner U., Hada H., Guan K., Hasenfuss G., Nayernia K., Engel W. Multipotent adult germline stem cells and embryonic stem cells have similar microRNA profiles. Mol. Hum. Reprod. 2008, 14:521-529.