Influence of activin a supplementation during human embryonic stem cell derivation on germ cell differentiation potential

Stem Cells and Development

Volumn 22, Issue 23, 2013, Pages 3141-3155

  Duggal, Galbha ^a   Heindryckx, Björn ^a   Warrier, Sharat ^a   O'Leary, Thomas ^a   Van Der Jeught, Margot ^a   Lierman, Sylvie ^a   Vossaert, Liesbeth ^b   Deroo, Tom ^a   Deforce, Dieter ^b   Chuva De Sousa Lopes, Susana M ^c   De Sutter, Petra ^a  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; BONE MORPHOGENETIC PROTEIN 4; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSCRIPTION FACTOR GATA 6;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYOID BODY; EMBRYONIC STEM CELL; GENE EXPRESSION; GERM CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

ACTIVINS; ANIMALS; BIOLOGICAL MARKERS; BONE MORPHOGENETIC PROTEIN 4; CELL DIFFERENTIATION; CELL LINE; EMBRYOID BODIES; EMBRYONIC STEM CELLS; ENDODERM; FLUORESCENT ANTIBODY TECHNIQUE; GATA6 TRANSCRIPTION FACTOR; GENE EXPRESSION PROFILING; GERM CELLS; HUMANS; MICE; PLURIPOTENT STEM CELLS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84888609209     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0024     Document Type: Article

References (63)

1. Clark AT, MS Bodnar, M Fox, RT Rodriquez, MJ Abeyta, MT Firpo and RA Pera. (2004). Spontaneous differentiation of germ cells from human embryonic stem cells in vitro. Hum Mol Genet 13:727-739.
2. Kee K, JM Gonsalves, AT Clark and RA Pera. (2006). Bone morphogenetic proteins induce germ cell differentiation from human embryonic stem cells. Stem Cells Dev 15:831-837.
3. Aflatoonian B, L Ruban, M Jones, R Aflatoonian, A Fazeli and HD Moore. (2009). In vitro post-meiotic germ cell development from human embryonic stem cells. Hum Reprod 24:3150-3159.
4. Eguizabal C, N Montserrat, R Vassena, M Barragan, E Garreta, L Garcia-Quevedo, F Vidal, A Giorgetti, A Veiga and JC Izpisua Belmonte. (2011). Complete meiosis from human induced pluripotent stem cells. Stem Cells 29:1186-1195.
5. Chuang CY, KI Lin, M Hsiao, L Stone, HF Chen, YH Huang, SP Lin, HN Ho and HC Kuo. (2012). Meiotic Competent Human Germ Cell-like Cells Derived from Human Embryonic Stem Cells Induced by BMP4/WNT3A Signaling and OCT4/EpCAM (Epithelial Cell Adhesion Molecule) Selection. J Biol Chem 287:14389-14401.
6. Bucay N, M Yebra, V Cirulli, I Afrikanova, T Kaido, A Hayek and AM Montgomery. (2009). A novel approach for the derivation of putative primordial germ cells and sertoli cells from human embryonic stem cells. Stem Cells 27:68-77.
7. Park TS, Z Galic, AE Conway, A Lindgren, BJ van Handel, M Magnusson, L Richter, MA Teitell, HK Mikkola, et al. (2009). 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 27:783-795.
8. Kee K, VT Angeles, M Flores, HN Nguyen and RA Reijo Pera. (2009). Human DAZL, DAZ and BOULE genes modulate primordial germ-cell and haploid gamete formation. Nature 462:222-225.
9. Tilgner K, SP Atkinson, S Yung, A Golebiewska, M Stojkovic, R Moreno, M Lako and L Armstrong. (2010). Expression of GFP under the control of the RNA helicase VASA permits fluorescence-activated cell sorting isolation of human primordial germ cells. Stem Cells 28:84-92.
10. Tilgner K, SP Atkinson, A Golebiewska, M Stojkovic, M Lako and L Armstrong. (2008). Isolation of primordial germ cells from differentiating human embryonic stem cells. Stem Cells 26:3075-3085.
11. Ramos-Mej?a V, AF Fernandez, V Ayllo n, PJ Real, C Bueno, P Anderson, F Mart?n, MF Fraga and P Menendez. (2012). Maintenance of human embryonic stem cells in mesenchymal stem cell-conditioned media augments hematopoietic specification. Stem Cells Dev 21:1549-1558.
12. Osafune K, L Caron, M Borowiak, RJ Martinez, CS Fitz- Gerald, Y Sato, CA Cowan, KR Chien and DA Melton. (2008). Marked differences in differentiation propensity among human embryonic stem cell lines. Nat Biotechnol 26:313-315.
13. Shi Y and J Massague. (2003). Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700.
14. James D, AJ Levine, D Besser and A Hemmati-Brivanlou. (2005). TGFbeta/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development 132:1273-1282.
15. Krummen LA, A Moore, TK Woodruff, R Covello, R Taylor, P Working and JP Mather. (1994). Localization of inhibin and activin binding sites in the testis during development by in situ ligand binding. Biol Reprod 50:734-744.
16. Mithraprabhu S, S Mendis, SJ Meachem, L Tubino, MM Matzuk, CW Brown and KL Loveland. (2010). Activin bioactivity affects germ cell differentiation in the postnatal mouse testis in vivo. Biol Reprod 82:980-990.
17. Meinhardt A, JR McFarlane, J Seitz and DM de Kretser. (2000). Activin maintains the condensed type of mitochondria in germ cells. Mol Cell Endocrinol 168:111-117.
18. Mendis SH, SJ Meachem, MA Sarraj and KL Loveland. (2011). Activin A balances Sertoli and germ cell proliferation in the fetal mouse testis. Biol Reprod 84:379-391.
19. Coutts SM, AJ Childs, N Fulton, C Collins, RA Bayne, AS McNeilly and RA Anderson. (2008). Activin signals via SMAD2/3 between germ and somatic cells in the human fetal ovary and regulates kit ligand expression. Dev Biol 314:189-199.
20. Bristol-Gould SK, PK Kreeger, CG Selkirk, SM Kilen, RW Cook, JL Kipp, LD Shea, KE Mayo and TK Woodruff. (2006). Postnatal regulation of germ cells by activin: the establishment of the initial follicle pool. Dev Biol 298: 132-148.
21. Kipp JL, A Golebiowski, G Rodriguez, M Demczuk, SM Kilen and KE Mayo. (2011). Gene expression profiling reveals Cyp26b1 to be an activin regulated gene involved in ovarian granulosa cell proliferation. Endocrinology 152: 303-312.
22. Tesar PJ, JG Chenoweth, FA Brook, TJ Davies, EP Evans, DL Mack, RL Gardner and RD McKay. (2007). New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448:196-199.
23. Xu RH, TL Sampsell-Barron, F Gu, S Root, RM Peck, G Pan, J Yu, J Antosiewicz-Bourget, S Tian, R Stewart and JA Thomson. (2008). NANOG is a direct target of TGFbeta/ activin-mediated SMAD signaling in human ESCs. Cell Stem Cell 3:196-206.
24. Hayashi K and MA Surani. (2009). Self-renewing epiblast stem cells exhibit continual delineation of germ cells with epigenetic reprogramming in vitro. Development 136:3549-3556.
25. Hanna J, AW Cheng, K Saha, J Kim, CJ Lengner, F Soldner, JP Cassady, J Muffat, BW Carey and R Jaenisch. (2010). Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc Natl Acad Sci U S A 107:9222-9227.
26. O'Leary T, B Heindryckx, S Lierman, D van Bruggen, JJ Goeman, M Vandewoestyne, D Deforce, SM de Sousa Lopes and P De Sutter. (2012). Tracking the progression of the human inner cell mass during embryonic stem cell derivation. Nat Biotechnol 30:278-282.
27. Brons IG, LE Smithers, MW Trotter, P Rugg-Gunn, B Sun, SM Chuva de Sousa Lopes, SK Howlett, A Clarkson, L Ahrlund-Richter, RA Pedersen and L Vallier. (2007). Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448:191-195.
28. Hayashi K, H Ohta, K Kurimoto, S Aramaki and M Saitou. (2011). Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146: 519-532.
29. Hayashi K, S Ogushi, K Kurimoto, S Shimamoto, H Ohta and M Saitou. (2012). Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science 338:971-975.
30. Stephenson EL, PR Braude and C Mason. (2006). Proposal for a universal minimum information convention for the reporting on the derivation of human embryonic stem cell lines. Regen Med 1:739-750.
31. O'Leary T, B Heindryckx, S Lierman, M Van der Jeught, B Menten, D Deforce, R Cornelissen, SC de Sousa Lopes and P De Sutter. (2011). The influence of early embryo traits on human embryonic stem cell derivation efficiency. Stem Cells Dev 20:785-793.
32. O'Leary T, G Duggal, S Lierman, E Van den Abbeel, B Heindryckx and P De Sutter. (2012). The influence of patient and cohort parameters on the incidence and developmental potential of embryos with poor quality traits for use in human embryonic stem cell derivation. Hum Reprod 27:1581-1589.
33. Van der Jeught M, T O'Leary, S Ghimire, S Lierman, G Duggal, K Versieren, D Deforce, S Chuva de Sousa Lopes, B Heindryckx and P De Sutter. (2013). The combination of inhibitors of FGF/MEK/Erk and GSK3b signaling increases the number of OCT3/4- and NANOG-positive cells in the human inner cell mass, but does not improve stem cell derivation. Stem Cells Dev 22:296-306.
34. Meisner LF and JA Johnson. (2008). Protocols for cytogenetic studies of human embryonic stem cells. Methods 45:133-141.
35. Inman GJ, FJ Nicola s, JF Callahan, JD Harling, LM Gaster, AD Reith, NJ Laping and CS Hill. (2002). SB-431542 is a potent and specific inhibitor of transforming growth factorbeta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol 62:65-74.
36. Nichols J and A Smith. (2009). Naive and primed pluripotent states. Cell Stem Cell 4:487-492.
37. Mazaheri Z, M Movahedin, F Rahbarizadeh and S Amanpour. (2011). Different doses of bone morphogenetic protein 4 promote the expression of early germ cell-specific gene in bone marrow mesenchymal stem cells. In Vitro Cell Dev Biol Anim 47:521-525.
38. Young JC, VL Dias and KL Loveland. (2010). Defining the window of germline genesis in vitro from murine embryonic stem cells. Biol Reprod 82:390-401.
39. Teo AK, Y Ali, KY Wong, H Chipperfield, A Sadasivam, Y Poobalan, EK Tan, ST Wang, S Abraham, et al. (2012). Activin and BMP4 synergistically promote formation of definitive endoderm in human embryonic stem cells. Stem Cells 30:631-642.
40. Unger C, H Skottman, P Blomberg, MS Dilber and O Hovatta. (2008). Good manufacturing practice and clinicalgrade human embryonic stem cell lines. Hum Mol Genet 17:R48-R53.
41. Thomson JA, J Itskovitz-Eldor, SS Shapiro, MA Waknitz, JJ Swiergiel, VS Marshall and JM Jones. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147.
42. Reubinoff BE, MF Pera, CY Fong, A Trounson and A Bongso. (2000). Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol 18:399-404.
43. Cowan CA, I Klimanskaya, J McMahon, J Atienza, J Witmyer, JP Zucker, S Wang, CC Morton, AP McMahon, D Powers and DA Melton. (2004). Derivation of embryonic stem-cell lines from human blastocysts. N Engl J Med 350:1353-1356.
44. Andrews PW, N Benvenisty, R McKay, MF Pera, J Rossant, H Semb, GN Stacey and SCotISC Initiative. (2005). The International Stem Cell Initiative: toward benchmarks for human embryonic stem cell research. Nat Biotechnol 23: 795-797.
45. Ware CB, AM Nelson and CA Blau. (2006). A comparison of NIH-approved human ESC lines. Stem Cells 24:2677-2684.
46. Adewumi O, B Aflatoonian, L Ahrlund-Richter, M Amit, PW Andrews, G Beighton, PA Bello, N Benvenisty, LS Berry, et al. (2007). Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol 25:803-816.
47. Lerou PH, A Yabuuchi, H Huo, JD Miller, LF Boyer, TM Schlaeger and GQ Daley. (2008). Derivation and maintenance of human embryonic stem cells from poor-quality in vitro fertilization embryos. Nat Protoc 3:923-933.
48. Fraga AM, E Souza de Arau jo, R Stabellini, N Vergani and LV Pereira. (2011). A survey of parameters involved in the establishment of new lines of human embryonic stem cells. Stem Cell Rev 7:775-781.
49. Camarasa MV, VM Galvez, DR Brison and D Bachiller. (2012). Optimized protocol for derivation of human embryonic stem cell lines. Stem Cell Rev 8:1011-1020.
50. Tannenbaum SE, TT Turetsky, O Singer, E Aizenman, S Kirshberg, N Ilouz, Y Gil, Y Berman-Zaken, TS Perlman, et al. (2012). Derivation of xeno-free and GMP-grade human embryonic stem cells-platforms for future clinical applications. PLoS One 7:e35325.
51. Rajala K, B Lindroos, SM Hussein, RS Lappalainen, M Pekkanen-Mattila, J Inzunza, B Rozell, S Miettinen, S Narkilahti, et al. (2010). A defined and xeno-free culture method enabling the establishment of clinical-grade human embryonic, induced pluripotent and adipose stem cells. PLoS One 5:e10246.
52. Skottman H. (2010). Derivation and characterization of three new human embryonic stem cell lines in Finland. In Vitro Cell Dev Biol Anim 46:206-209.
53. Allegrucci C and LE Young. (2007). Differences between human embryonic stem cell lines. Hum Reprod Update 13:103-120.
54. Abeyta MJ, AT Clark, RT Rodriguez, MS Bodnar, RA Pera and MT Firpo. (2004). Unique gene expression signatures of independently-derived human embryonic stem cell lines. Hum Mol Genet 13:601-608.
55. Skottman H, AM Stromberg, E Matilainen, J Inzunza, O Hovatta and R Lahesmaa. (2006). Unique gene expression signature by human embryonic stem cells cultured under serum-free conditions correlates with their enhanced and prolonged growth in an undifferentiated stage. Stem Cells 24:151-167.
56. Aflatoonian B and H Moore. (2006). Germ cells from mouse and human embryonic stem cells. Reproduction 132: 699-707.
57. Matsui Y. (2010). The molecular mechanisms regulating germ cell development and potential. J Androl 31:61-65.
58. Wongtrakoongate P, M Jones, PJ Gokhale and PW Andrews. (2013). STELLA facilitates differentiation of germ cell and endodermal lineages of human embryonic stem cells. PLoS One 8:e56893.
59. West FD, DW Machacek, NL Boyd, K Pandiyan, KR Robbins and SL Stice. (2008). Enrichment and differentiation of human germ-like cells mediated by feeder cells and basic fibroblast growth factor signaling. Stem Cells 26:2768-2776.
60. de Sousa Lopes SM, BA Roelen, RM Monteiro, R Emmens, HY Lin, E Li, KA Lawson and CL Mummery. (2004). BMP signaling mediated by ALK2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryo. Genes Dev 18:1838-1849.
61. Lewis SL and PP Tam. (2006). Definitive endoderm of the mouse embryo: formation, cell fates, and morphogenetic function. Dev Dyn 235:2315-2329.
62. Lawson KA, NR Dunn, BA Roelen, LM Zeinstra, AM Davis, CV Wright, JP Korving and BL Hogan. (1999). Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 13:424-436.
63. Dudley B, C Palumbo, J Nalepka and K Molyneaux. (2010). BMP signaling controls formation of a primordial germ cell niche within the early genital ridges. Dev Biol 343:84-93.