Subfractionation of differentiating human embryonic stem cell populations allows the isolation of a mesodermal population enriched for intermediate mesoderm and putative renal progenitors

Stem Cells and Development

Volumn 19, Issue 10, 2010, Pages 1637-1648

  Lin, S Adelia ^a,b,c   Kolle, Gabriel ^d   Grimmond, Sean M ^d   Zhou, Qi ^b,c   Doust, Elizabeth ^b,c   Little, Melissa H ^d   Aronow, Bruce ^e   Ricardo, Sharon D ^a   Pera, Martin F ^f   Bertram, John F ^a   Laslett, Andrew L ^a,b,c  

^a MONASH UNIVERSITY   (Australia)

^b Australian Stem Cell Centre   (Australia)

^c CSIRO   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD24 ANTIGEN; PODOCALYXIN; TRANSCRIPTION FACTOR PAX2; TRANSCRIPTOME; WT1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL ISOLATION; CELL LINEAGE; CELL POPULATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FLOW CYTOMETRY; FRACTIONATION; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KIDNEY CELL; KIDNEY DEVELOPMENT; KIDNEY DISEASE; MESENCHYMAL STEM CELL; MESODERM; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; UPREGULATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL SEPARATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; GENE EXPRESSION; HUMANS; KIDNEY; MALE; MESODERM; MICE; MICE, SCID; MICROARRAY ANALYSIS; STEM CELL TRANSPLANTATION; TERATOMA;

MURINAE;

EID: 77957587734     PISSN: 15473287     EISSN: None     Source Type: Journal    
DOI: 10.1089/scd.2010.0017     Document Type: Article

References (47)

1. Erceg S, S Laínez, M Ronaghi, P Stojkovic, MA Pérez- Aragó, V Moreno-Manzano, R Moreno-Palanques, R Planells-Cases and M Stojkovic. (2008). Differentiation of human embryonic stem cells to regional specific neural precursors in chemically defined medium conditions. PLoS ONE 3:e2122.
2. CohenM A, P Itsykson and BE Reubinoff. (2007). Neural differentiation of human ES cells. Curr Protoc Cell Biol 36:23.7.1-23.7.20.
3. Ferreira LS, S Gerecht, HF Shieh, N Watson, MA Rupnick, SM Dallabrida, G Vunjak-Novakovic and R Langer. (2007). Vascular progenitor cells isolated from human embryonic stem cells give rise to endothelial and smooth muscle like cells and form vascular networks in vivo. Circ Res 101:286-294.
4. Nakagami H, N Nakagawa, Y Takeya, K Kashiwagi, C Ishida, S Hayashi, M Aoki, K Matsumoto, T Nakamura, T Ogihara and R Morishita. (2006). Model of vasculogenesis from embryonic stem cells for vascular research and regenerative medicine. Hypertension 48:112-119.
5. Kärner E., CM Bäckesjö, J Cedervall, RV Sugars, L Ahrlund-Richter and M Wendel. (2009). Dynamics of gene expression during bone matrix formation in osteogenic cultures derived from human embryonic stem cells in vitro. Biochim Biophys Acta 1790:110-118.
6. Kärner E., C Unger, AJ Sloan, L Ahrlund-Richter, RV Sugars and M Wendel. (2007). Bone matrix formation in osteogenic cultures derived from human embryonic stem cells in vitro. Stem Cells Dev 16:39-52.
7. Lee KW, JY Yook, MY Son, MJ Kim, DB Koo, YM Han and YS Cho. (2009). Rapamycin promotes the osteoblastic differentiation of human embryonic stem cells by blocking the mTOR pathway and stimulating the BMP/Smad pathway. Stem Cells Dev 19:557-568.
8. Bu L, X Jiang, S Martin-Puig, L Caron, S Zhu, Y Shao, DJ Roberts, PL Huang, IJ Domian and KR Chien. (2009). Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 460:113-117
9. Tran TH, X Wang, C Browne, Y Zhang, M Schinke, S Izumo and M Burcin. (2009). Wnt3a-induced mesoderm formation and cardiomyogenesis in human embryonic stem cells. Stem Cells 27:1869-1878.
10. Borowiak M, R Maehr, S Chen, AE Chen, W Tang, JL Fox, SL Schreiber and DA Melton. (2009). Small molecules efficiently direct endodermal differentiation of mouse and human embryonic stem cells. Cell Stem Cell 4:348-358.
11. Van Hoof D., KA D'Amour and MS German. (2009). Derivation of insulin-producing cells from human embryonic stem cells. Stem Cell Res 3:73-87
12. Sasaki K, H Ichikawa, S Takei, HS No, D Tomotsune, Y Kano, T Yokoyama, S Sirasawa, A Mogi, S Yoshie, S Sasaki, S Yamada, K Matsumoto, M Mizuguchi, F Yue and Y Tanaka. (2009). Hepatocyte differentiation from human ES cells using the simple embryoid body formation method and the staged-additional cocktail. Scientific World Journal 9:884-890.
13. Synnergren J, N Heins, G Brolen, G Eriksson, A Lindahl, J Hyllner, B Olsson, P Sartipy and P Bjorquist. (2009). Transcriptional profiling of human embryonic stem cells differentiating to definitive and primitive endoderm and further towards the hepatic lineage. Stem Cells Dev.
14. Ji L, BL Allen-Hoffmann, JJ de Pablo and SP Palecek. (2006). Generation and differentiation of human embryonic stem cell-derived keratinocyte precursors. Tissue Eng 12:665-679.
15. Metallo CM, L Ji., JJ de Pablo and SP Palecek. (2008). Retinoic acid and bone morphogenetic protein signaling synergize to efficiently direct epithelial differentiation of human embryonic stem cells. Stem Cells 26:372-380.
16. 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.
17. Park TS, Z Galic, AE Conway, A Lindgren, BJ van Handel, M Magnusson, L Richter, MA Teitell, HK Mikkola, WE Lowry, K Plath and AT Clark. (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.
18. Xu RH, X Chen, DS Li, R Li., GC Addicks, C Glennon, TP Zwaka and JA Thomson. (2002). BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol 20:1261-1264.
19. Xu RH. (2006). In vitro induction of trophoblast from human embryonic stem cells. Methods Mol Med 121:189-202.
20. Steenhard BM, KS Isom, P Cazcarro, JH Dunmore, AR Godwin, PL St John and DR Abrahamson. (2005). Integration of embryonic stem cells in metanephric kidney organ culture. J Am Soc Nephrol 16:1623-1631.
21. Kim D and GR Dressier. (2005). Nephrogenic factors promote differentiation of mouse embryonic stem cells into renal epithelia. J Am Soc Nephrol 16:3527-3534.
22. Vigneau C, K Polgar, G Striker, J Elliott, D Hyink, O Weber, HJ Fehling, G Keller, C Burrow and P Wilson. (2007). Mouse embryonic stem cell-derived embryoid bodies generate progenitors that integrate long term into renal proximal tubules in vivo. J Am Soc Nephrol 18:1709-1720.
23. 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
24. 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.
25. Gertow K, S Wolbank, B Rozell, R Sugars, M Andäng, CL Parish, MP Imreh, M Wendel and L Ahrlund-Richter. (2004). Organized development from human embryonic stem cells after injection into immunodeficient mice. Stem Cells Dev 13:421-435.
26. Schuldiner M, O Yanuka, J Itskovitz-Eldor, DA Melton and N Benvenisty. (2000). Effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 97:11307-11312.
27. Batchelder CA, CC Lee, DG Matsell, MC Yoder and AF Tarantal. (2009). Renal ontogeny in the rhesus monkey (Macaca mulatta) and directed differentiation of human embryonic stem cells towards kidney precursors. Differentiation 78:45-56.
28. Saxen L. (1987). Organogenesis of the Kidney. Cambridge University Press, Cambridge.
29. Rumballe B, K Georgas, LW ilkinson and M Little. (2010). Molecular anatomy of the kidney: what have we learned from gene expression and functional genomics? Pediatr Nephrol 25:1005-1016.
30. Challen GA, G Martinez, MJ Davis, DF Taylor, M Crowe, RD Teasdale, SM Grimmond and MH Little. (2004). Identifying the molecular phenotype of renal progenitor cells. J Am Soc Nephrol 15:2344-2357
31. Torres M, E Gómez-Pardo, GR Dressier and P Gruss. (1995). Pax-2 controls multiple steps of urogenital development. Development 121:4057-4065.
32. Kreidberg JA, H Sariola, JM Loring, M Maeda, J Pelletier, D Housman and R Jaenisch. (1993). WT-1 is required for early kidney development. Cell 74:679-691.
33. Carroll TJ and AP McMahon, eds. (2003). Overview: The Molecular Basis of Kidney Development. Academic Press, London.
34. Passier R, DW Oostwaard, J Snapper, J Kloots, RJ Hassink, E Kuijk, B Roelen, AB de la Riviere and C Mummery. (2005). Increased cardiomyocyte differentiation from human embryonic stem cells in serum-free cultures. Stem Cells 23:772-780.
35. D'Amour K.A., AD Agulnick, S Eliazer, OG Kelly, E Kroon and EE Baetge. (2005). Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 23:1534-1541.
36. D'Amour K.A., AG Bang, S Eliazer, OG Kelly, AD Agulnick, NG Smart, MA Moorman, E Kroon, MK Carpenter and EE Baetge. (2006). Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 24:1392-1401.
37. Adewumi O, B Aflatoonian, L Ahrlund-Richter, M Amit, PW Andrews, G Beighton, PA Bello, N Benvenisty, LS Berry, S Bevan, B Blum, J Brooking, KG Chen, AB Choo, GA Churchill, M Corbel, I Damjanov, JS Draper, P Dvorak, K Emanuelsson, RA Fleck, A Ford, K Gertow, M Gertsenstein, PJ Gokhale, RS Hamilton, A Hampl, LE Healy, O Hovatta, J Hyllner, MP Imreh, J Itskovitz-Eldor, J Jackson, JL Johnson, M Jones, K Kee, BL King, BB Knowles, M Lako, F Lebrin, BS Mallon, D Manning, Y Mayshar, RD McKay, AE Michalska, M Mikkola, M Mileikovsky, SL Minger, HD Moore, CL Mummery, A Nagy, N Nakatsuji, CM O'Brien, SK Oh, C Olsson, T Otonkoski, KY Park, R Passier, H Patel, M Patel, R Pedersen, MF Pera, MS Piekarczyk, RA Pera, BE Reubinoff, AJ Robins, J Rossant, P Rugg-Gunn, TC Schulz, H Semb, ES Sherrer, H Siemen, GN Stacey, M Stojkovic, H Suemori, J Szatkiewicz, T Turetsky, T Tuuri, S van den Brink, K Vintersten, S Vuoristo, D Ward, TA Weaver, LA Young and W Zhang; International Stem Cell Initiative. (2007). Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol 25:803-816.
38. Pera MF, AA Filipczyk, SM Hawes and AL Laslett. (2003). Isolation, characterization, and differentiation of human embryonic stem cells. Meth Enzymol 365:429-446.
39. Herszfeld D, E Wolvetang, E Langton-Bunker, TL Chung, AA Filipczyk, S Houssami, P Jamshidi, K Koh, AL Laslett, A Michalska, L Nguyen, BE Reubinoff, I Tellis, JM Auerbach, CJ Ording, LH Looijenga and MF Pera. (2006). CD30 is a survival factor and a biomarker for transformed human pluripotent stem cells. Nat Biotechnol 24:351-357
40. Wertz K and BG Herrmann. (1999). Kidney-specific Cadherin (cdh16) is expressed in embryonic kidney, lung, and sex ducts. Mech Dev 84:185-188.
41. Laslett AL, S Grimmond, B Gardiner, L Stamp, A Lin, SM Hawes, S Wormald, D Nikolic-Paterson, D Haylock and MF Pera. (2007). Transcriptional analysis of early lineage commitment in human embryonic stem cells. BMC Dev Biol 7:12.
42. Kolle G, M H.o., Q Zhou, HS Chy, K Krishnan, N Cloonan, I Bertoncello, AL Laslett and SM Grimmond. (2009). Identification of human embryonic stem cell surface markers by combined membrane-polysome translation state array analysis and immunotranscriptional profiling. Stem Cells 27:2446-2456.
43. Schopperle WM, DB Kershaw and WC DeWolf. (2003). Human embryonal carcinoma tumor antigen, Gp200/GCTM-2, is podocalyxin. Biochem Biophys Res Commun 300:285-290.
44. Brunskill EW, BJ Aronow, K Georgas, B Rumballe, MT Valerius, J Aronow, V Kaimal, AG Jegga, J Yu, S Grimmond, AP McMahon, LT Patterson, MH Little and SS Potter. (2008). Atlas of gene expression in the developing kidney at microanatomic resolution. Dev Cell 15:781-791.
45. McLean AB, KA DAmour, KL Jones, M Krishnamoorthy, MJ Kulik, DM Reynolds, AM Sheppard, H Liu, Y Xu, EE Baetge and S Dalton. (2007). Activin a efficiently specifies definitive endoderm from human embryonic stem cells only when phosphatidylinositol 3-kinase signaling is suppressed. Stem Cells 25:29-38.
46. Phillips BW, H Hentze, WL Rust, QP Chen, H Chipperfield, EK Tan, S Abraham, A Sadasivam, PL Soong, ST Wang, R Lim, W Sun, A Colman and NR Dunn. (2007). Directed differentiation of human embryonic stem cells into the pancreatic endocrine lineage. Stem Cells Dev 16:561-578.
47. Tropepe V, S Hitoshi, C Sirard, TW Mak, J Rossant and D van der Kooy. (2001). Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 30:65-78.