Teratomas from pluripotent stem cells: A clinical hurdle

Journal of Cellular Biochemistry

Volumn 111, Issue 4, 2010, Pages 769-781

  Fong, Chui Yee ^a   Gauthaman, Kalamegam ^a   Bongso, Ariff ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Clinical hurdles; HESC; HiPSC; NTSC; Teratomas; Tumorigenesis; Wharton's jelly stem cells

Indexed keywords

CELL ANTIBODY; CERAMIDE DERIVATIVE; GANCICLOVIR; HLA A ANTIGEN; HLA B ANTIGEN; HLA DR ANTIGEN; KRUPPEL LIKE FACTOR 4; LIN28 PROTEIN; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN; SPHINGOSINE DERIVATIVE; THYMIDINE KINASE; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BLASTOCYST; BLOOD GROUP TYPING; CANCER GROWTH; CANCER RISK; CANCER SIZE; CARCINOGENESIS; CELL ASSAY; CELL CULTURE; CELL DEATH; CELL DIFFERENTIATION; CELL LINEAGE; CELL NUCLEUS TRANSPLANTATION; CELL RENEWAL; CELL SELECTION; DENSITY GRADIENT; EMBRYONAL CARCINOMA STEM CELL; EMBRYONIC STEM CELL; ENCAPSULATION; ENGRAFTMENT; FLUORESCENCE ACTIVATED CELL SORTING; GRAFT REJECTION; HEMATOPOIETIC STEM CELL; HLA TYPING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MAGNETIC ACTIVATED CELL SORTING; MALIGNANT TRANSFORMATION; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; NEURAL STEM CELL; NON INVASIVE PROCEDURE; NUCLEAR REPROGRAMMING; PARACRINE SIGNALING; PATHOGENESIS; PATIENT SAFETY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SOMATIC CELL; STEM CELL PLASTICITY; STEM CELL TRANSPLANTATION; SUICIDE GENE; TERATOCARCINOMA; TERATOMA;

BIOLOGICAL ASSAY; HUMANS; NUCLEAR TRANSFER TECHNIQUES; PLURIPOTENT STEM CELLS; STEM CELL TRANSPLANTATION; TERATOMA; TRANSLATIONAL RESEARCH;

EID: 78049239513     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22775     Document Type: Article

References (120)

1. Adewumi O, Aflatoonian B, Ahrlund-Richter L, Amit M, Andrews PW, Beighton G, Bello PA, Benvenisty N, Berry LS, Bevan S, Blum B, Brooking J, Chen KG, Choo AB, Churchill GA, Corbel M, Damjanov I, Draper JS, Dvorak P, Emanuelsson K, Fleck RA, Ford A, Gertow K, Gertsenstein M, Gokhale PJ, Hamilton RS, Hampl A, Healy LE, Hovatta O, Hyllner J, Imreh MP, Itskovitz-Eldor J, Jackson J, Johnson JL, Jones M, Kee K, King BL, Knowles BB, Lako M, Lebrin F, Mallon BS, Manning D, Mayshar Y, McKay RD, Michalska AE, Mikkola M, Mileikovsky M, Minger SL, Moore HD, Mummery CL, Nagy A, Nakatsuji N, O'Brien CM, Oh SK, Olsson C, Otonkoski T, Park KY, Passier R, Patel H, Patel M, Pedersen R, Pera MF, Piekarczyk MS, Pera RA, Reubinoff BE, Robins AJ, Rossant J, Rugg-Gunn P, Schulz TC, Semb H, Sherrer ES, Siemen H, Stacey GN, Stojkovic M, Suemori H, Szatkiewicz J, Turetsky T, Tuuri T, van den Brink S, Vintersten K, Vuoristo S, Ward D, Weaver TA, Young LA, Zhang W. 2007. Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol 25: 803-816.
2. Amano S, Hagiwara A. 1976. In vivo study on the process of solid tumor formation from embryoid bodies of mouse teratocarcinoma. Dev Growth Differ 18: 95-104.
3. Amariglio N, Hirshberg A, Scheithauer BW, Amariglio N, Hirshberg A, Scheithauer BW, Cohen Y, Loewenthal R, Trakhtenbrot L, Paz N, Koren-Michowitz M, Waldman D, Leider-Trejo L, Toren A, Constantini S, Rechavi G. 2009. Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med 6: e1000029.
4. Amit M, Carpenter MK, Inokuma MS, Chiu CP, Harris CP, Waknitz MA, Itskovitz-Eldor J, Thomson JA. 2000. Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolong periods of culture. Dev Biol 227: 271-278.
5. Amit M, Shariki C, Margulets V, Itskovitz-Eldor J. 2004. Feeder layer- and serum-free culture of human embryonic stem cells. Biol Reprod 70: 837-845.
6. Andrews PW. 2002. From teratocarcinomas to embryonic stem cells. Philos Trans R Soc Lond B Biol Sci 357: 405-417.
7. Andrews PW, Matin MM, Bahrami AR, Damjanov I, Gokhale P, Draper JS. 2005. Embryonic stem (ES) cells and embryonal carcinoma (EC) cells: Opposite sides of the same coin. Biochem Soc Trans 33: 1526-1530.
8. Ayuzawa R, Doi C, Rachakatla RS, Pyle MM, Maurya DK, Troyer D, Tamura M. 2009. Naïve human umbilical cord matrix derived stem cells significantly attenuate growth of human breast cancer cells in vitro and in vivo. Cancer Lett 280: 31-37.
9. Bailey AS, Jiang S, Afentoulis M, Baumann CI, Schroeder DA, Olson SB, Wong MH, Fleming WH. 2004. Transplanted adult hematopoietic stems cells differentiate into functional endothelial cells. Blood 103: 13-19.
10. Balsam LB, Wagers AJ, Christensen JL, Kofidis T, Weissman IL, Robbins RC. 2004. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428: 668-673.
11. Ben-Hur T, Idelson M, Khaner H, Pera M, Reinhartz E, Itzik A, Reubinoff BE. 2004. Transplantation of human embryonic stem cell-derived neural progenitors improves behavioral deficit in Parkinsonian rats. Stem Cells 22: 1246-1255.
12. Bieberich E, Silva J, Wang G, Krishnamurthy K, Condie BG. 2004. Selective apoptosis of pluripotent mouse and human stem cells by novel ceramide analogues prevents teratoma formation and enriches for neural precursors in ES cell-derived neural transplants. J Cell Biol 167: 723-734.
13. Bielby RC, Boccaccini AR, Polak JM, Buttery LD. 2004. In vitro differentiation and in vivo mineralization of osteogenic cells derived from human embryonic stem cells. Tissue Eng 10: 1518-1525.
14. Blum B, Benvenisty N. 2008. The tumorigenicity of human embryonic stem cells. Adv Cancer Res 100: 133-158.
15. Bongso A, Lee EH. 2005. Stem cells: From bench to bedside. Singapore: World Scientific Publishing Co. Pte. Ltd.
16. Bongso A, Fong CY, Ng SC, Ratnam S. 1994. Isolation and culture of inner cell mass cells from human blastocysts. Hum Reprod 9: 2110-2117.
17. Brederlau A, Correia AS, Anisimov SV, Elmi M, Paul G, Roybon L, Morizane A, Bergquist F, Riebe I, Nannmark U, Carta M, Hanse E, Takahashi J, Sasai Y, Funa K, Brundin P, Eriksson PS, Li JY. 2006. Transplantation of human embryonic stem cell-derived cells to a rat model of Parkinson's disease: Effect of in vitro differentiation on graft survival and teratoma formation. Stem Cells 24: 1433-1440.
18. Byrne JA, Pedersen DA, Clepper LL, Nelson M, Sanger WG, Gokhale S, Wolf DP, Mitalipov SM. 2007. Producing primate embryonic stem cells by somatic cell nuclear transfer. Nature 450: 497-502.
19. Cao F, Lin S, Xie X, Ray P, Patel M, Zhang X, Drukker M, Dylla SJ, Connolly AJ, Chen X, Weissman IL, Gambhir SS, Wu JC. 2006. In vivo visualization of embryonic stem cell survival, proliferation and migration after cardiac delivery. Circulation 113: 1005-1014.
20. Cao F, Drukker M, Lin S, Sheikh AY, Xie X, Li Z, Connolly AJ, Weissman IL, Wu JC. 2007. Molecular imaging of embryonic stem cell misbehavior and suicide gene ablation. Cloning Stem Cells 9: 107-117.
21. Carpenedo RL, Sargent CY, McDevitt TC. 2007. Rotary suspension culture enhances the efficiency, yield and homogeneity of embryoid body differentiation. Stem Cells 25: 2224-2234.
22. Chao KC, Chao KF, Fu YS, Liu SH. 2009. Islet-like clusters derived from mesenchymal stem cells in Wharton's Jelly of the human umbilical cord for transplantation to control type 1 diabetes. PLoS ONE 3: e1451.
23. Chen M, Bongso A. 1999. Comparative evaluation of two density gradient preparations for sperm separation for medically assisted conception. Hum Reprod 14: 759-764.
24. Cheng L, Hammond H, Ye Z, Zhan X, Dravid G. 2003. Human adult marrow cells support prolonged expansion of human embryonic stem cells in culture. Stem Cells 21: 131-142.
25. Choo AB, Tan HL, Ang SN, Fong WJ, Chin A, Lo J, Zheng L, Hentze H, Philp RJ, Oh SK, Yap M. 2008. Selection against undifferentiated human embryonic stem cells by a cytotoxic antibody recognizing podocalyxin-like protein-1. Stem Cells 26: 1454-1463.
26. Clevers H. 2005. Stem cells, asymmetric division and cancer. Nat Genet 37: 1027-1028.
27. Condic ML, Rao M. 2008. Regulatory issues for personalized pluripotent cells. Stem Cells 26: 2753-2758.
28. Cooke MJ, Stojkovic M, Przyborski SA. 2006. Growth of teratomas derived from human pluripotent stem cells is influenced by the graft site. Stem Cells Dev 15: 254-259.
29. Damjanov I, Andrews PW. 2007. The terminology of teratocarcinomas and teratomas. Nat Biotechnol 25: 1212.
30. Dean SK, Yulyana Y, Williams G, Sidhu KS, Tuch BE. 2006. Differentiation of encapsulated embryonic stem cells after transplantation. Transplantation 82: 1175-1184.
31. Dimmeler S, Burchfield J, Zeiher AM. 2008. Cell-based therapy of myocardial infarction. Arterioscler Thromb Vasc Biol 28: 208-216.
32. Ellerström C, Strehl R, Noaksson K, Hyllner J, Semb H. 2007. Facilitated expansion of human embryonic stem cells by single-cell enzymatic dissociation. Stem Cells 25: 1690-1696.
33. Feng Q, Lu SJ, Klimanskaya I, Gomes I, Kim D, Chung Y, Honig GR, Kim KS, Lanza R. 2010. Hemangioblastic derivatives from human induced pluripotent stem cells exhibit limited expansion and early senescence. Stem Cells 28: 704-712.
34. Fiegel HC, Lange C, Kneser U, Lambrecht W, Zander AR, Rogiers X, Kluth D. 2006. Fetal and adult liver stem cells for liver regeneration and tissue engineering. J Cell Mol Med 10: 577-587.
35. Fong CY, Sathananthan AH, Wong PC, Bongso A. 2004. Nine-day-old human embryo cultured in vitro: A clue to the origins of embryonic stem cells. Reprod BioMed Online 9: 321-325.
36. Fong CY, Richards M, Manasi N, Biswas A, Bongso A. 2007. Comparative growth behaviour and characterization of stem cells from human Wharton's jelly. Reprod BioMed Online 15: 708-718.
37. Fong CY, Chak LL, Subramanian A, Tan JH, Biswas A, Gauthaman K, Choolani M, Chan WK, Bongso A. 2009a. A three dimensional anchorage independent in vitro system for the prolonged growth of embryoid bodies to study cancer cell behaviour and anticancer agents. Stem Cell Rev Rep 5: 410-419.
38. Fong CY, Peh GS, Subramanian A, Gauthaman K, Bongso A. 2009b. The use of discontinuous density gradients in stem cell research and application. Stem Cell Rev Rep 5: 428-434.
39. Fong CY, Peh GS, Gauthaman K, Bongso A. 2009c. Separation of SSEA-4 and TRA-1-60 labelled undifferentiated human embryonic stem cells from a heterogeneous cell population using magnetic-activated cell sorting (MACS) and fluorescence-activated cell sorting (FACS). Stem Cell Rev Rep 5: 72-80.
40. Fong CY, Subramanian A, Biswas A, Gauthaman K, Srikanth P, Hande PM, Bongso A. 2010a. Derivation efficiency, cell proliferation, frozen-thaw survival, 'stemness' properties, and differentiation of human Wharton's jelly stem cells. Reprod BioMed Online DOI: 10.1016/j.rbmo.2010.04.010.
41. Fong CY, Chak LL, Biswas A, Tan JH, Gauthaman K, Chan WK, Bongso A. 2010b. Human Wharton's jelly stem cells have unique transcriptome profiles compared to human embryonic stem cells and other mesenchymal stem cells. Stem Cells Rev Rep DOI: 10.1007/s12015-010-9166-x.
42. French AJ, Adams CA, Anderson LS, Kitchen JR, Hughes MR, Wood SH. 2008. Development of human cloned blastocysts following somatic cell nuclear transfer with adult fibroblasts. Stem Cells 26: 485-493.
43. Fujikawa T, Oh SH, Pi L, Hatch HM, Shupe T, Petersen BE. 2005. Teratoma formation leads to failure of treatment for type 1 diabetes using embryonic stem cell-derived insulin-producing cells. Am J Pathol 166: 1781-1791.
44. Ganta C, Chiyo D, Ayuzawa R, Rachakatla R, Pyle M, Andrews G, Weiss M, Tamura M, Troyer D. 2009. Rat umbilical cord stem cells completely abolish rat mammary carcinomas with no evidence of metastasis or recurrence 100 days post-tumor cell inoculation. Cancer Res 69: 1815-1820.
45. Gauthaman K, Fong CY, Bongso A. 2010a. Effect of ROCK inhibitor Y-27632 on normal and variant human embryonic stem cells (hESCs) in vitro: Its benefits in hESC expansion. Stem Cell Rev Rep 6: 86-95.
46. Gauthaman K, Fong CY, Bongso A. 2010b. Human embryonic stem cell-derived tissue transplantation therapy: Challenges ahead. In: Bongso A, Lee EH, editors. Stem cells: From bench to bedside. 2nd edition. Singapore: World Scientific Publishing Co. Pte. Ltd.
47. Gauthaman K, Venugopal JR, Fong CY, Peh GS, Ramakrishna S, Bongso A. 2010c. Nanofibrous substrates support colony formation and maintain stemness of human embryonic stem cells. J Cell Mol Med 13: 3475-3484.
48. Giorgetti A, Montserrat N, Aasen T, Gonzalez F, Rodriguez-Piza I, Vassena R, Raya A, Boue S, Barrero MJ, Corbella BA, Torrabadella M, Veiga A, Izpisua Belmonte JC. 2009. Generation of induced pluripotent stem cells from human cord blood using OCT4 and SOX2. Cell Stem Cell 5: 353-357.
49. Haase A, Olmer R, Schwanke K, Wunderlich S, Merkert S, Hess C, Zweigerdt R, Gruh I, Meyer J, Wagner S, Maier LS, Han DW, Glage S, Miller K, Fischer P, Schöler HR, Martin U. 2009. Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell 5: 434-441.
50. Hanahan D, Weinberg RA. 2000. The hallmarks of cancer. Cell 100: 57-70.
51. Heile AMB, Wallrapp C, Klinge PM, Samii A, Kassem M. 2009. Cerebral transplantation of encapsulated mesenchymal stem cells improves cellular pathology after experimental traumatic brain injury. Neurosci Lett 463: 176-181.
52. Herszfeld D, Wolvetang E, Langton-Bunker E, Chung TL, Filipczyk AA, Houssami S, Jamshidi P, Koh K, Laslett AL, Michalska A, Nguyen L, Reubinoff BE, Tellis I, Auerbach JM, Ording CJ, Looijenga LH, Pera MF. 2006. CD30 is a survival factor and a biomarker for transformed human pluripotent stem cells. Nat Biotechnol 24: 351-357.
53. Hou T, Xu J, Wu X, Xie Z, Luo F, Zhang Z, Zeng L. 2009. Umbilical cord Wharton's Jelly: A new potential cell source of mesenchymal stromal cells for bone tissue engineering. Tissue Eng Part A 15: 2325-2334.
54. Houghton J, Stoicov C, Nomura S, Rogers AB, Carlson J, Li H, Cai X, Fox JG, Goldenring JR, Wang TC. 2004. Gastric cancer originating from bone marrow-derived cells. Science 306: 1568-1571.
55. Hu BY, Weick JP, Yu J, Ma LX, Zhang XQ, Thomson JA, Zhang SC. 2010. Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc Natl Acad Sci USA 107: 4335-4340.
56. Huangfu D, Osafune K, Maehr R, Guo W, Eijkelenboom A, Chen S, Muhlestein W, Melton DA. 2008. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol 26: 1269-1275.
57. Jang YY, Sharkis SJ. 2005. Stem cell plasticity: A rare cell, not a rare event. Stem Cell Rev Rep 1: 45-51.
58. Joannides A, Fiore-Hériché C, Westmore K, Caldwell M, Compston A, Allen N, Chandran S. 2006. Automated mechanical passaging: A novel and efficient method for human embryonic stem cell expansion. Stem Cells 24: 230-235.
59. Jung J, Hackett NR, Pergolizzi RG, Pierre-Destine L, Krause A, Crystal RG. 2007. Ablation of tumor-derived stem cells transplanted to the central nervous system by genetic modification of embryonic stem cells with a suicide gene. Hum Gene Ther 18: 1182-1192.
60. Kawai H, Yamashita T, Ohta Y, DeGuchi K, Nagotani S, Zhang X, Ikeda Y, Matsuura T, Abe K. 2010. Tridermal tumorigenesis of induced pluripotent stem cells transplanted in ischemic brain. J Cereb Blood Metab. DOI: 10.1038/jcbfm.2010.32.
61. Kim D, Kim CH, Moon JI, Chung YG, Chang MY, Han BS, Ko S, Yang E, Cha KY, Lanza R, Kim KS. 2009. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 4: 472-476.
62. Ko K, Tapia N, Wu G, Kim JB, Bravo MJ, Sasse P, Glaser T, Ruau D, Han DW, Greber B, Hausdörfer K, Sebastiano V, Stehling M, Fleischmann BK, Brüstle O, Zenke M, Scholer HR. 2009. Induction of pluripotency in adult unipotent germline stem cells. Cell Stem Cell 5: 87-96.
63. Kumashiro Y, Asahina K, Ozeki R, Shimizu-Saito K, Tanaka Y, Kida Y, Inoue K, Kaneko M, Sato T, Teramoto K, Arii S, Teraoka H. 2005. Enrichment of hepatocytes differentiated from mouse embryonic stem cells as a transplantable source. Transplantation 79: 550-557.
64. Laflamme MA, Chen KY, Naumova AV. 2007. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25: 1015-1024.
65. Lawrenz B, Schiller H, Willbold E, Ruediger M, Muhs A, Esser S. 2004. Highly sensitive biosafety model for stem-cell-derived grafts. Cytotherapy 6: 212-222.
66. Lensch MW, Schlaeger TM, Zon LI, Daley GQ. 2007. Teratoma formation assays with human embryonic stem cells: A rationale for one type of human-animal chimera. Cell Stem Cell 1: 253-258.
67. Li Y, Chopp M. 2009. Marrow stromal cell transplantation in stroke and traumatic brain injury. Neurosci Lett 456: 120-123.
68. Lin G, OuYang Q, Zhou X, Lin G, OuYang Q, Zhou X, Gu Y, Yuan D, Li W, Liu G, Liu T, Lu G. 2007. A highly homozygous and parthenogenetic human embryonic stem cell line derived from a one-pronuclear oocyte following in vitro fertilization procedure. Cell Res 17: 999-1007.
69. Looijenga LH, Gillis AJ, Stoop HJ, Hersmus R, Oosterhuis JW. 2007. Chromosomes and expression in human testicular germ-cell tumors: Insight into their cell of origin and pathogenesis. Ann N Y Acad Sci 1120: 187-214.
70. Ludwig TE, Levenstein ME, Jones JM, Berggren WT, Mitchen ER, Frane JL, Crandall LJ, Daigh CA, Conard KR, Piekarczyk MS, Conard KR, Piekarczyk MS, Llanas RA, Thomson JA. 2006. Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol 24: 185-187.
71. Luong MX, Smith KP, Stein GS. 2008. Human embryonic stem cell registries: Value, challenges and opportunities. J Cell Biochem 105: 625-632.
72. Martin R. 2003. Adult stem cell plasticity. Fact or artifact? Annu Rev Cell Dev Biol 19: 1-22.
73. Martin-Ibañez R, Unger C, Strömberg A, Baker D, Canals JM, Hovatta O. 2008. Novel cryopreservation method for dissociated human embryonic stem cells in the presence of a ROCK inhibitor. Hum Reprod 23: 2744-2754.
74. Meirelles L, Chagastelles PC, Nardi NB. 2006. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119: 2204-2213.
75. Mummery CL. 2005. Cardiology: Solace for the broken-hearted? Nature 433: 585-587.
76. Mummery C, Ward-van Oostwaard D, Doevendans P, Spijker R, van den Brink S, Hassink R, van der Heyden M, Opthof T, Pera M, de la Riviere AB, Passier R, Tertoolen L. 2003. Differentiation of human embryonic stem cells to cardiomyocytes: Role of coculture with visceral endoderm-like cells. Circulation 107: 2733-2740.
77. Murry CE, Soonpaa MH, Reinecke H, Nakajima H, Nakajima HO, Rubart M, Pasumarthi KBS, Virag JI, Bartelmez SH, Poppa V, Bradford G, Dowell JD, Williams DA, Field LJ. 2004. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428: 664-668.
78. Nakajima F, Tokunaga K, Nakatsuji N. 2007. Human leukocyte antigen matching estimations in a hypothetical bank of human embryonic stem cell lines in the Japanese population for use in cell transplantation therapy. Stem Cells 25: 983-985.
79. Naujok O, Kaldrack J, Taivankhuu T, Jörns A, Lenzen S. 2010. Selective removal of undifferentiated embryonic stem cells from differentiation cultures through HSV1 thymidine kinase and ganciclovir treatment. Stem Cell Rev Rep. DOI: 10.1007/s12015-010-9148-z.
80. Ng ES, Davis RP, Azzola L, Edouard G, Stanley EG, Elefanty AG. 2005. Forced aggregation of defined numbers of human embryonic stem cells into embryoid bodies fosters robust, reproducible hematopoietic differentiation. Blood 106: 1601-1603.
81. Oosterhuis JW, Stoop H, Honecker F, Looijenga LH. 2007. Why human extragonadal germ cell tumours occur in the midline of the body: Old concepts, new perspectives. Int J Androl 30: 256-263.
82. Osafune K, Caron L, Borowiak M, Martinez RJ, Fitz-Gerald CS, Sato Y, Cowan CA, Chien KR, Melton DA. 2008. Marked differences in differentiation propensity among human embryonic stem cell lines. Nat Biotechnol 26: 313-315.
83. Phillips BW, Horne R, Lay TS, Rust WL, Teck TT, Crook JM. 2008. Attachment and growth of human embryonic stem cells on microcarriers. J Biotechnol 138: 24-32.
84. Plaia TW, Josephson R, Liu Y, Zeng X, Ording C, Toumadje A, Brimble SN, Sherrer ES, Uhl EW, Freed WJ, Schulz TC, Maitra A, Rao MS, Auerbach JM. 2006. Characterization of a new NIH-registered variant human embryonic stem cell line, BG01V: A tool for human embryonic stem cell research. Stem Cells 24: 531-546.
85. Pomper MG, Hammond H, Yu X, Ye Z, Foss CA, Lin DD, Fox JJ, Cheng L. 2009. Serial imaging of human embryonic stem-cell engraftment and teratoma formation in live mouse models. Cell Res 19: 370-379.
86. Prokhorova TA, Harkness LM, Frandsen U, Ditzel N, Schrøder HD, Burns JS, Kassem M. 2009. Teratoma formation by human embryonic stem cells is site dependent and enhanced by the presence of matrigel. Stem Cells Dev 18: 47-54.
87. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ. 2008. Efficient tumour formation by single human melanoma cells. Nature 456: 593-598.
88. Reubinoff B, Pera MF, Fong CY, Trounson A, Bongso A. 2000. Embryonic stem cell lines from human blastocysts: Somatic differentiation in vitro. Nat Biotechnol 18: 399-404.
89. Revazova ES, Turovets NA, Kochetkova OD, Kindarova LB, Kuzmichev LN, Janus JD, Pryzhkova MV. 2007. Patient-specific stem cell lines derived from human parthenogenetic blastocysts. Cloning Stem Cells 9: 432-449.
90. Richards M, Fong CY, Chan WK, Wong PC, Bongso A. 2002. Human feeders support prolonged undifferentiated growth of human inner cell masses and embryonic stem cells. Nat Biotechnol 20: 933-936.
91. Roche E, Soria B. 2005. Differentiation of human embryonic, fetal and adult stem cells to islets of the pancreas. In: Bongso A, Lee EH, editors. Stem cells: From bench to bedside. Singapore: World Scientific Press Publications.
92. Salem HK, Thiemermann C. 2010. Mesenchymal stromal cells: Current understanding and clinical status. Stem Cells 28: 585-596.
93. Schuldiner M, Eiges R, Eden A, Yanuka O, Itskovitz-Eldor J, Goldstein RS, Benvenisty N. 2001. Induced neuronal differentiation of human embryonic stem cells. Brain Res 913: 201-205.
94. Schuldiner M, Itskovitz-Eldor J, Benvenisty N. 2003. Selective ablation of human embryonic stem cells expressing a suicide gene. Stem Cells 21: 257-265.
95. Shibata H, Ageyama N, Tanaka Y, Kishi Y, Sasaki K, Nakamura S, Muramatsu S, Hayashi S, Kitano Y, Terao K, Hanazono Y. 2006. Improved safety of hematopoietic transplantation with monkey embryonic stem cells in the allogeneic setting. Stem Cells 24: 1450-1457.
96. Shih CC, Forman SJ, Chu P, Slovak M. 2007. Human embryonic stem cells are prone to generate primitive, undifferentiated tumors in engrafted human fetal tissues in severe combined immunodeficient mice. Stem Cells Dev 16: 893-902.
97. Shim JH, Kim SE, Woo DH, Kim SK, Oh CH, McKay R, Kim JH. 2007. Directed differentiation of human embryonic stem cells towards a pancreatic cell fate. Diabetologia 50: 1228-1238.
98. Smith KP, Luong MX, Stein GS. 2009. Pluripotency: Toward a gold standard for human ES and iPS cells. J Cell Physiol 220: 21-29.
99. Steiner D, Khaner H, Cohen M, Steiner S, 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.
100. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
101. Tan HL, Fong WJ, Lee EH, Yap M, Choo A. 2009. mAb 84, a cytotoxic antibody that kills undifferentiated human embryonic stem cells via oncosis. Stem Cells 27: 1792-1801.
102. Taylor CJ, Bolton EM, Pocock S, Sharples LD, Pedersen RA, Bradley JA. 2005. Banking on human embryonic stem cells: Estimating the number of donor cell lines needed for HLA matching. Lancet 366: 2019-2025.
103. Thomas RJ, Anderson D, Chandra A, Smith NM, Young LE, Williams D, Denning C. 2009. Automated, scalable culture of human embryonic stem cells in feeder-free conditions. Biotechnol Bioeng 102: 1636-1644.
104. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. 1998. Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
105. Tolar J, Nauta AJ, Osborn MJ, Panoskaltsis Mortari A, McElmurry RT, Bell S, Xia L, Zhou N, Riddle M, Schroeder TM, Westendorf JJ, McIvor RS, Hogendoorn PC, Szuhai K, Oseth L, Hirsch B, Yant SR, Kay MA, Peister A, Prockop DJ, Fibbe WE, Blazar BR. 2007. Sarcoma derived from cultured mesenchymal stem cells. Stem Cells 25: 371-379.
106. Troyer DL, Weiss ML. 2008. Concise review: Wharton's jelly-derived cells are a primitive stromal cell population. Stem Cells 26: 591-599.
107. Ulbright TM. 2005. Germ cell tumors of the gonads: A selective review emphasizing problems in differential diagnosis, newly appreciated, and controversial issues. Mod Pathol 18: S61-S79.
108. Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Südhof TC, Wernig M. 2010. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463: 1035-1041.
109. Voelkel C, Galla M, Maetzig T, Warlich E, Kuehle J, Zychlinski D, Bode J, Cantz T, Schambach A, Baum C. 2010. Protein transduction from retroviral Gag precursors. Proc Natl Acad Sci USA 107: 7805-7810.
110. Wang L, Tran I, Seshareddy K, Weiss ML, Detamore MS. 2009. A comparison of human bone marrow-derived mesenchymal stem cells and human umbilical cord-derived mesenchymal stromal cells for cartilage tissue engineering. Tissue Eng Part A 8: 2259-2266.
111. Watanabe K, Ueno M, Kamiya D, Nishiyama A, Matsumura M, Wataya T, Takahashi JB, Nishikawa S, Nishikawa S, Muguruma K, Sasai Y. 2007. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 25: 681-686.
112. Weissman IL. 2000. Stem cells: Units of development, units of regeneration and units in evolution. Cell 100: 157-168.
113. Woltjen K, Michael IP, Mohseni P, Desai R, Mileikovsky M, Hämäläinen R, Cowling R, Wang W, Liu P, Gertsenstein M, Kaji K, Sung HK, Nagy A. 2009. piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458: 766-770.
114. Xu C, Inokuma MS, Denham J, Golds K, Kundu P, Gold JD, Carpenter MK. 2001. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 19: 971-974.
115. Yang D, Zhang ZJ, Oldenburg M. 2008. Human embryonic stem cell-derived dopaminergic neurons reverse functional deficit in Parkinsonian rats. Stem Cells 26: 55-63.
116. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA. 2007. Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
117. Zapata AG. 2009. Stem cell populations in adult bone marrow: Phenotypes and biological relevance for production of somatic stem cells. In: Simon C, Pellicer A, editors. Stem cells in human reproduction. London: Informa Healthcare UK Ltd. pp 177-186.
118. Zhang SC, Wernig M, Duncan ID, Brüstle O, Thomson JA. 2001. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19: 1129-1133.
119. Zhang X, Zhu T, Chen Y, Mertani HC, Lee KO, Lobie PE. 2003. Human growth hormone-regulated HOXA1 is a human mammary epithelial oncogene. J Biol Chem 278: 7580-7590.
120. Zhou H, Wu S, Joo JY, Zhu S, Han DW, Lin T, Trauger S, Bien G, Yao S, Zhu Y, Siuzdak G, Schöler HR, Duan L, Ding S. 2009. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4: 381-384.