Elimination of tumorigenic stem cells from differentiated progeny and selection of definitive endoderm reveals a Pdx1+ foregut endoderm stem cell lineage

Stem Cell Research

Volumn 6, Issue 2, 2011, Pages 143-157

  Kahan, Brenda ^a   Magliocca, Joseph ^a,b   Merriam, Fabiola ^a   Treff, Nathan ^a,c   Budde, Melisa ^a   Nelson, Jeffrey ^a,d   Browning, Victoria ^a   Ziehr, Benjamin ^a   Odorico, Jon ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c REPRODUCTIVE MEDICINE ASSOCIATES OF NEW JERSEY   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CELL PROTEIN; EPITHELIAL CELL ADHESION MOLECULE; TRANSCRIPTION FACTOR PDX 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER STEM CELL; CARCINOGENICITY; CELL DIFFERENTIATION; CELL LINEAGE; CELL POPULATION; CELL PROLIFERATION; CELL SELECTION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENDODERM; GENE EXPRESSION; GENETIC MANIPULATION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIGENS, CD15; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; CELL DIFFERENTIATION; CELL LINEAGE; CELL SEPARATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; ENDODERM; GASTROINTESTINAL TRACT; HOMEODOMAIN PROTEINS; HUMANS; MALE; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM TRANSPLANTATION; STAGE-SPECIFIC EMBRYONIC ANTIGENS; TERATOMA; TRANS-ACTIVATORS;

MURINAE; MUS;

EID: 79951512282     PISSN: 18735061     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.scr.2010.10.003     Document Type: Article

References (48)

1. Alper J. Geron gets green light for human trial of ES cell-derived product. Nat. Biotechnol. 2009, 27:213-214.
2. Amariglio N., Hirshberg A., Scheithauer B.W., Cohen Y., Loewenthal R., Trakhtenbrot L., Paz N., Koren-Michowitz M., Waldman D., Leider-Trejo L., Toren A., Constantini S., Rechavi G. Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med. 2009, 6:e1000029.
3. Anderson R., Schaible K., Heasman J., Wylie C. Expression of the homophilic adhesion molecule, Ep-CAM, in the mammalian germ line. J. Reprod. Fertil. 1999, 116:379-384.
4. Anderson D., Self T., Mellor I.R., Goh G., Hill S.J., Denning C. Transgenic enrichment of cardiomyocytes from human embryonic stem cells. Mol. Ther. 2007, 15:2027-2036.
5. Baharvand H., Ashtiani S.K., Taee A., Massumi M., Valojerdi M.R., Yazdi P.E., Moradi S.Z., Farrokhi A. Generation of new human embryonic stem cell lines with diploid and triploid karyotypes. Dev. Growth Differ. 2006, 48:117-128.
6. Besnard V., Wert S.E., Hull W.M., Whitsett J.A. Immunohistochemical localization of Foxa1 and Foxa2 in mouse embryos and adult tissues. Gene Expr. Patterns 2004, 5:193-208.
7. Bhushan A., Itoh N., Kato S., Thiery J.P., Czernichow P., Bellusci S., Scharfmann R. Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 2001, 128:5109-5117.
8. Borowiak M., Maehr R., Chen S., Chen A.E., Tang W., Fox J.L., Schreiber S.L., Melton D.A. Small molecules efficiently direct endodermal differentiation of mouse and human embryonic stem cells. Cell Stem Cell 2009, 4:348-358.
9. Burke Z., Oliver G. Prox1 is an early specific marker for the developing liver and pancreas in the mammalian foregut endoderm. Mech. Dev. 2002, 118:147-155.
10. Chen S., Borowiak M., Fox J.L., Maehr R., Osafune K., Davidow L., Lam K., Peng L.F., Schreiber S.L., Rubin L.L., Melton D. A small molecule that directs differentiation of human ESCs into the pancreatic lineage. Nat. Chem. Biol. 2009, 5:258-265.
11. Chung S., Shin B.S., Hedlund E., Pruszak J., Ferree A., Kang U.J., Isacson O., Kim K.S. Genetic selection of sox1GFP-expressing neural precursors removes residual tumorigenic pluripotent stem cells and attenuates tumor formation after transplantation. J. Neurochem. 2006, 97:1467-1480.
12. Cirulli V., Ricordi C., Hayek A. E-cadherin, NCAM, and EpCAM expression in human fetal pancreata. Transplant. Proc. 1995, 27:3335.
13. Cirulli V., Crisa L., Beattie G.M., Mally M.I., Lopez A.D., Fannon A., Ptasznik A., Inverardi L., Ricordi C., Deerinck T., Ellisman M., Reisfeld R.A., Hayek A. KSA antigen Ep-CAM mediates cell-cell adhesion of pancreatic epithelial cells: morphoregulatory roles in pancreatic islet development. J. Cell Biol. 1998, 140:1519-1534.
14. D'Amour K.A., Agulnick A.D., Eliazer S., Kelly O.G., Kroon E., Baetge E.E. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat. Biotechnol. 2005, 23:1534-1541.
15. D'Amour K.A., Bang A.G., Eliazer S., Kelly O.G., Agulnick A.D., Smart N.G., Moorman M.A., Kroon E., Carpenter M.K., Baetge E.E. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat. Biotechnol. 2006, 24:1392-1401.
16. Dufort D., Schwartz L., Harpal K., Rossant J. The transcription factor HNF3beta is required in visceral endoderm for normal primitive streak morphogenesis. Development 1998, 125:3015-3025.
17. Fox N.W., Damjanov I., Knowles B.B., Solter D. Stage-specific embryonic antigen 3 as a marker of visceral extraembryonic endoderm. Dev. Biol. 1984, 103:263-266.
18. Fujikawa T., Oh S.H., Pi L., Hatch H.M., Shupe T., Petersen B.E. Teratoma formation leads to failure of treatment for type I diabetes using embryonic stem cell-derived insulin-producing cells. Am. J. Pathol. 2005, 166:1781-1791.
19. Fukuda H., Takahashi J., Watanabe K., Hayashi H., Morizane A., Koyanagi M., Sasai Y., Hashimoto N. Fluorescence-activated cell sorting-based purification of embryonic stem cell-derived neural precursors averts tumor formation after transplantation. Stem Cells 2006, 24:763-771.
20. Gonzalez B., Denzel S., Mack B., Conrad M., Gires O. EpCAM is involved in maintenance of the murine embryonic stem cell phenotype. Stem Cells 2009, 27:1782-1791.
21. Gouon-Evans V., Boussemart L., Gadue P., Nierhoff D., Koehler C.I., Kubo A., Shafritz D.A., Keller G. BMP-4 is required for hepatic specification of mouse embryonic stem cell-derived definitive endoderm. Nat. Biotechnol. 2006, 24:1402-1411.
22. Hadjantonakis A.K., Macmaster S., Nagy A. Embryonic stem cells and mice expressing different GFP variants for multiple non-invasive reporter usage within a single animal. BMC Biotechnol. 2002, 2:11.
23. Hentze H., Soong P.L., Wang S.T., Phillips B.W., Putti T.C., Dunn N.R. Teratoma formation by human embryonic stem cells: evaluation of essential parameters for future safety studies. Stem Cell Res. 2009, 2:198-210.
24. Hou J., Charters A.M., Lee S.C., Zhao Y., Wu M.K., Jones S.J., Marra M.A., Hoodless P.A. A systematic screen for genes expressed in definitive endoderm by serial analysis of gene expression (SAGE). BMC Dev. Biol. 2007, 7:92.
25. Huber I., Itzhaki I., Caspi O., Arbel G., Tzukerman M., Gepstein A., Habib M., Yankelson L., Kehat I., Gepstein L. Identification and selection of cardiomyocytes during human embryonic stem cell differentiation. FASEB J. 2007, 21:2551-2563.
26. Ishii T., Yasuchika K., Machimoto T., Kamo N., Komori J., Konishi S., Suemori H., Nakatsuji N., Saito M., Kohno K., Uemoto S., Ikai I. Transplantation of embryonic stem cell-derived endodermal cells into mice with induced lethal liver damage. Stem Cells 2007, 25:3252-3260.
27. Johannesson M., Stahlberg A., Ameri J., Sand F.W., Norrman K., Semb H. FGF4 and retinoic acid direct differentiation of hESCs into PDX1-expressing foregut endoderm in a time- and concentration-dependent manner. PLoS ONE 2009, 4:e4794.
28. Kahan B.W., Jacobson L.M., Hullett D.A., Ochoada J.M., Oberley T.D., Lang K.M., Odorico J.S. Pancreatic precursors and differentiated islet cell types from murine embryonic stem cells: an in vitro model to study islet differentiation. Diabetes 2003, 52:2016-2024.
29. Kanai-Azuma M., Kanai Y., Gad J.M., Tajima Y., Taya C., Kurohmaru M., Sanai Y., Yonekawa H., Yazaki K., Tam P.P., Hayashi Y. Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 2002, 129:2367-2379.
30. Kattman S.J., Huber T.L., Keller G.M. Multipotent flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev. Cell 2006, 11:723-732.
31. Knoepfler P.S. Deconstructing stem cell tumorigenicity: a roadmap to safe regenerative medicine. Stem Cells 2009, 27:1050-1056.
32. Kroon E., Martinson L.A., Kadoya K., Bang A.G., Kelly O.G., Eliazer S., Young H., Richardson M., Smart N.G., Cunningham J., Agulnick A.D., D'Amour K.A., Carpenter M.K., Baetge E.E. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat. Biotechnol. 2008, 26:443-452.
33. Leor J., Gerecht S., Cohen S., Miller L., Holbova R., Ziskind A., Shachar M., Feinberg M.S., Guetta E., Itskovitz-Eldor J. Human embryonic stem cell transplantation to repair the infarcted myocardium. Heart 2007, 93:1278-1284.
34. Li G., Luo R., Zhang J., Yeo K.S., Lian Q., Xie F., Tan E.K., Caille D., Kon O.L., Salto-Tellez M., Meda P., Lim S.K. Generating mESC-derived insulin-producing cell lines through an intermediate lineage-restricted progenitor line. Stem Cell Res. 2009, 2:41-55.
35. McGrath K.E., Koniski A.D., Maltby K.M., McGann J.K., Palis J. Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev. Biol. 1999, 213:442-456.
36. Miller R.J., Banisadr G., Bhattacharyya B.J. CXCR4 signaling in the regulation of stem cell migration and development. J. Neuroimmunol. 2008, 198:31-38.
37. Nagy A., Rossant J., Nagy R., Abramow-Newerly W., Roder J.C. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl Acad. Sci. USA 1993, 90:8424-8428.
38. Phillips B.W., Hentze H., Rust W.L., Chen Q.P., Chipperfield H., Tan E.K., Abraham S., Sadasivam A., Soong P.L., Wang S.T., Lim R., Sun W., Colman A., Dunn N.R. Directed differentiation of human embryonic stem cells into the pancreatic endocrine lineage. Stem Cells Dev. 2007, 16:561-578.
39. Roy N.S., Cleren C., Singh S.K., Yang L., Beal M.F., Goldman S.A. Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat. Med. 2006, 12:1259-1268.
40. Saldeen J., Kriz V., Agren N., Welsh M. SHB and angiogenic factors promote ES cell differentiation to insulin-producing cells. Biochem. Biophys. Res. Commun. 2006, 344:517-524.
41. Seguin C.A., Draper J.S., Nagy A., Rossant J. Establishment of endoderm progenitors by SOX transcription factor expression in human embryonic stem cells. Cell Stem Cell 2008, 3:182-195.
42. Sherwood R.I., Jitianu C., Cleaver O., Shaywitz D.A., Lamenzo J.O., Chen A.E., Golub T.R., Melton D.A. Prospective isolation and global gene expression analysis of definitive and visceral endoderm. Dev. Biol. 2007, 304:541-555.
43. Sherwood R.I., Chen T.Y., Melton D.A. Transcriptional dynamics of endodermal organ formation. Dev. Dyn. 2009, 238:29-42.
44. Shi Y., Hou L., Tang F., Jiang W., Wang P., Ding M., Deng H. Inducing embryonic stem cells to differentiate into pancreatic beta cells by a novel three-step approach with activin A and all-trans retinoic acid. Stem Cells 2005, 23:656-662.
45. Solter D., Knowles B.B. Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc. Natl Acad. Sci. USA 1978, 75:5565-5569.
46. Soria B., Roche E., Berna G., Leon-Quinto T., Reig J.A., Martin F. Insulin-secreting cells derived from embryonic stem cells normalize glycemia in streptozotocin-induced diabetic mice. Diabetes 2000, 49:157-162.
47. Yasunaga M., Tada S., Torikai-Nishikawa S., Nakano Y., Okada M., Jakt L.M., Nishikawa S., Chiba T., Era T., Nishikawa S. Induction and monitoring of definitive and visceral endoderm differentiation of mouse ES cells. Nat. Biotechnol. 2005, 23:1542-1550.
48. Ying Q.L., Stavridis M., Griffiths D., Li M., Smith A. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 2003, 21:183-186.