Combined Activin A/LiCl/Noggin treatment improves production of mouse embryonic stem cell-derived definitive endoderm cells

Journal of Cellular Biochemistry

Volumn 112, Issue 4, 2011, Pages 1022-1034

  Li, Fuming ^a,b   He, Zhiying ^c   Li, Yangfang ^c   Liu, Pingyu ^a,b   Chen, Fei ^c   Wang, Minjun ^c   Zhu, Haiying ^a   Ding, Xiaoyan ^a   Wangensteen, Kirk J ^d   Hu, Yiping ^c   Wang, Xin ^a,e  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c SECOND MILITARY MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF MINNESOTA   (United States)

^e UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Definitive endoderm; Differentiation; Embryonic body; Mouse embryonic stem cells; Suspension culture

Indexed keywords

ACTIVIN A; BONE MORPHOGENETIC PROTEIN 4; LITHIUM CHLORIDE; NOGGIN; PROTEIN NODAL; WNT PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENDODERM; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MONOLAYER CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEM CELL;

ACTIVINS; ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CARRIER PROTEINS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; CULTURE MEDIA, SERUM-FREE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; EMBRYONIC STEM CELLS; ENDODERM; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; LITHIUM CHLORIDE; LIVER; MICE; PANCREAS; PROTO-ONCOGENE PROTEINS C-KIT; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; RECEPTORS, CXCR4; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TIME FACTORS; WNT PROTEINS;

EID: 79952569130     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22962     Document Type: Article

References (44)

1. Arnold SJ, Robertson EJ. 2009. Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat Rev Mol Cell Biol 10:91-103.
2. Basma H, Soto-Gutierrez A, Yannam GR, Liu L, Ito R, Yamamoto T, Ellis E, Carson SD, Sato S, Chen Y, Muirhead D, Navarro-Alvarez N, Wong RJ, Roy-Chowdhury J, Platt JL, Mercer DF, Miller JD, Strom SC, Kobayashi N, Fox IJ. 2009. Differentiation and transplantation of human embryonic stem cell-derived hepatocytes. Gastroenterology 136:990-999.
3. Bondue A, Lapouge G, Paulissen C, Semeraro C, Iacovino M, Kyba M, Blanpain C. 2008. Mesp1 acts as a master regulator of multipotent cardiovascular progenitor specification. Cell Stem Cell 3:69-84.
4. Borowiak M, Maehr R, Chen S, Chen AE, Tang W, Fox JL, Schreiber SL, Melton DA. 2009. Small molecules efficiently direct endodermal differentiation of mouse and human embryonic stem cells. Cell Stem Cell 4:348-358.
5. Cai J, Zhao Y, Liu Y, Ye F, Song Z, Qin H, Meng S, Chen Y, Zhou R, Song X, Guo Y, Ding M, Deng H. 2007. Directed differentiation of human embryonic stem cells into functional hepatic cells. Hepatology 45:1229-1239. (Pubitemid 46775786)
6. Chen S, Borowiak M, Fox JL, Maehr R, Osafune K, Davidow L, Lam K, Peng LF, Schreiber SL, Rubin LL, Melton D. 2009. A small molecule that directs differentiation of human ESCs into the pancreatic lineage. Nat Chem Biol 5:258-265.
7. Clement-Lacroix P, Ai M, Morvan F, Roman-Roman S, Vayssiere B, Belleville C, Estrera K, Warman ML, Baron R, Rawadi G. 2005. Lrp5-independent activation of Wnt signaling by lithium chloride increases bone formation and bone mass in mice. Proc Natl Acad Sci U S A 102:17406-17411. (Pubitemid 41740879)
8. Clevers H. 2006. Wnt/beta-catenin signaling in development and disease. Cell 127:469-480.
9. Duan Y, Catana A, Meng Y, Yamamoto N, He S, Gupta S, Gambhir SS, Zern MA. 2007. Differentiation and enrichment of hepatocyte-like cells from human embryonic stem cells in vitro and in vivo. Stem Cells 25:3058-3068. (Pubitemid 350294431)
10. Duan Y, Ma X, Zou W, Wang C, Behbahan IS, Ahuja TP, Tolstikov V, Zern MA. 2010. Differentiation and characterization of metabolically functioning hepatocytes from human embryonic stem cells. Stem Cells 28:674-686.
11. Evans MJ, Kaufman MH. 1981. Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154-156. (Pubitemid 11050741)
12. Gadue P, Huber TL, Paddison PJ, Keller GM. 2006. Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc Natl Acad Sci U S A 103: 16806-16811. (Pubitemid 44737334)
13. Galceran J, Hsu SC, Grosschedl R. 2001. Rescue of a Wnt mutation by an activated form of LEF-1: regulation of maintenance but not initiation of Brachyury expression. Proc Natl Acad Sci U S A 98:8668-8673. (Pubitemid 32678085)
14. Gouon-Evans V, Boussemart L, Gadue P, Nierhoff D, Koehler CI, Kubo A, Shafritz DA, Keller GM. 2006. BMP-4 is required for hepatic specification of mouse embryonic stem cell-derived definitive endoderm. Nat Biotechnol 24:1402-1411. (Pubitemid 44722104)
15. Hay DC, Zhao D, Fletcher J, Hewitt ZA, McLean D, Urruticoechea-Uriguen A, Black JR, Elcombe C, Ross JA, Wolf R, Cui W. 2008. Efficient differentiation of hepatocytes from human embryonic stem cells exhibiting markers recapitulating liver development in vivo. Stem Cells 26:894-902.
16. Heo J, Factor VM, Uren T, Takahama Y, Lee JS, Major M, Feinstone SM, Thorgeirsson SS. 2006. Hepatic precursors derived from murine embryonic stem cells contribute to regeneration of injured liver. Hepatology 44:1478-1486. (Pubitemid 44953653)
17. Kattman SJ, Huber TL, Keller GM. 2006. Multipotent flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev Cell 11:723-732. (Pubitemid 44644969)
18. Kelly OG, Pinson KI, Skarnes WC. 2004. The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 131:2803-2815. (Pubitemid 39004073)
19. Klein PS, Melton DA. 1996. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci U S A 93:8455-8459. (Pubitemid 26269579)
20. Kroon E, Martinson LA, Kadoya K, Bang AG, Kelly OG, Eliazer S, Young H, Richardson M, Smart NG, Cunningham J, Agulnick AD, D'Amour KA, Carpenter MK, Baetge EE. 2008. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 26:443-452. (Pubitemid 351501814)
21. Kubo A, Shinozaki K, Shannon JM, Kouskoff V, Kennedy M, Woo S, Fehling HJ, Keller G. 2004. Development of definitive endoderm from embryonic stem cells in culture. Development 131:51-62.
22. Latinkic BV, Umbhauer M, Neal KA, Lerchner W, Smith JC, Cunliffe V. 1997. The Xenopus Brachyury promoter is activated by FGF and low concentrations of activin and suppressed by high concentrations of activin and by paired-type homeodomain proteins. Genes Dev 11:3265-3276.
23. Lickert H, Kutsch S, Kanzler B, Tamai Y, Taketo MM, Kemler R. 2002. Formation of multiple hearts in mice following deletion of beta-catenin in the embryonic endoderm. Dev Cell 3:171-181.
24. Li FM, Liu PY, Liu CC, Xiang D, Deng L, Li WL, Wangensteen K, Song JG, Ma Y, Hui LJ, Wei LX, Li LS, Ding XY, Hu YP, He ZY, Wang X. 2010. Hepatoblast-like progenitor cells derived from embryonic stem cells can repopulate livers of mice. Gastroenterology 139:2158-2169.
25. McGrath KE, Koniski AD, Maltby KM, McGann JK, Palis J. 1999. Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev Biol 15:442-456. (Pubitemid 29444352)
26. Mfopou JK, Chen B, Mateizel I, Sermon K, Bouwens L. 2010. Noggin, retinoids, and fibroblast growth factor regulate hepatic or pancreatic fate of human embryonic stem cells. Gastroenterology 138:2233-2245.
27. Morrison GM, Oikonomopoulou I, Migueles RP, Soneji S, Livigni A, Enver T, Brickman JM. 2008. Anterior definitive endoderm from ESCs reveals a role for FGF signaling. Cell Stem Cell 3:402-415.
28. Murry CE, Keller G. 2008. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132:661-680. (Pubitemid 351260059)
29. Nakanishi M, Kurisaki A, Hayashi Y, Warashina M, Ishiura S, Kusuda-Furue M, Asashima M. 2009. Directed induction of anterior and posterior primitive streak by Wnt from embryonic stem cells cultured in a chemically defined serum-free medium. FASEB J 23:114-122.
30. Nostro MC, Cheng X, Keller GM, Gadue P. 2008. Wnt, Activin, and BMP signaling regulate distinct stages in the developmental pathway from embryonic stem cells to blood. Cell Stem Cell 2:60-71.
31. Sherwood RI, Jitianu C, Cleaver O, Shaywitz DA, Lamenzo JO, Chen AE, Golub TR, Melton DA. 2007. Prospective isolation and global gene expression analysis of definitive and visceral endoderm. Dev Biol 304:541-555. (Pubitemid 46527567)
32. Snykers S, De Kock J, Rogiers V, Vanhaecke T. 2009. In vitro differentiation of embryonic and adult stem cells into hepatocytes: state of the art. Stem Cells 27:577-605.
33. Soto-Gutierrez A, Kobayashi N, Rivas-Carrillo JD, Navarro-Alvarez N, Zhao D, Okitsu T, Noguchi H, Basma H, Tabata Y, Chen Y, Tanaka K, Narushima M, Miki A, Ueda T, Jun HS, Yoon JW, Lebkowski J, Tanaka N, Fox IJ. 2006. Reversal of mouse hepatic failure using an implanted liver-assist device containing ES cell-derived hepatocytes. Nat Biotechnol 24:1412-1419. (Pubitemid 44722105)
34. Steiner D, Khaner H, Cohen M, Even-Ram S, Gil Y, Itsykson P, Turetsky T, Idelson M, Aizenman E, Ram R, Berman-Zaken Y, Reubinoff B. 2010. Derivation, propagation and controlled differentiation of human embryonic stem cells in suspension. Nat Biotechnol 28:361-364.
35. Sumi T, Tsuneyoshi N, Nakatsuji N, Suemori H. 2008. Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/beta-catenin, Activin/Nodal and BMP signaling. Development 135:2969-2979.
36. Tada S, Era T, Furusawa C, Sakurai H, Nishikawa S, Kinoshita M, Nakao K, Chiba T. 2005. Characterization of mesendoderm: a diverging point of the definitive endoderm and mesoderm in embryonic stem cell differentiation culture. Development 132:4363-4374. (Pubitemid 41576697)
37. Tam PP, Loebel DA. 2007. Gene function in mouse embryogenesis: get set for gastrulation. Nat Rev Genet 8:368-381. (Pubitemid 46625808)
38. Touboul T, Hannan NR, Corbineau S, Martinez A, Martinet C, Branchereau S, Mainot S, Strick-Marchand H, Pedersen R, Di Santo J, Weber A, Vallier L. 2010. Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development. Hepatology 51:1754-1765.
39. Xu Y, Shi Y, Ding S. 2008. A chemical approach to stem-cell biology and regenerative medicine. Nature 453:338-344. (Pubitemid 351693140)
40. Yamaguchi TP, Takada S, Yoshikawa Y, Wu N, McMahon AP. 1999. T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm speci- fication. Genes Dev 13:3185-3190. (Pubitemid 30030440)
41. Yasunaga M, Tada S, Torikai-Nishikawa S, Nakano Y, Okada M, Jakt LM, Nishikawa S, Chiba T, Era T, Nishikawa S. 2005. Induction and monitoring of definitive and visceral endoderm differentiation of mouse ES cells. Nat Biotechnol 23:1542-1550. (Pubitemid 41752932)
42. Zaret KS. 2008. Genetic programming of liver and pancreas progenitors: lessons for stem-cell differentiation. Nat Rev Genet 9:329-340. (Pubitemid 351556060)
43. Zaret KS, Grompe M. 2008. Generation and regeneration of cells of the liver and pancreas. Science 322:1490-1494.
44. Zhu S, Wurdak H, Wang J, Lyssiotis CA, Peters EC, Cho CY, Wu X, Schultz PG. 2009. A small molecule primes embryonic stem cells for differentiation. Cell Stem Cell 4:416-426.