Lessons from human teratomas to guide development of safe stem cell therapies

Nature Biotechnology

Volumn 30, Issue 9, 2012, Pages 849-857

  Cunningham, Justine J ^a   Ulbright, Thomas M ^b   Pera, Martin F ^c   Looijenga, Leendert H J ^d  

^a ALLERGAN INC   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d JOSEPHINE NEFKENS INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CLINICAL APPLICATION; EMBRYONIC STEM CELLS; HUMAN CELLS; HUMAN LIVES; NATURAL HISTORY; PLURIPOTENT STEM CELLS; POTENTIAL HAZARDS; SAFETY ASSESSMENTS; STEM CELL THERAPY; TUMOR FORMATION;

PATIENT MONITORING; STEM CELLS;

TUMORS;

FLUORODEOXYGLUCOSE F 18; NANOPARTICLE; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR SOX2;

BIOLUMINESCENCE; CANCER RISK; CANCER STEM CELL; CARCINOGENESIS; CATION EXCHANGE; CELL DIFFERENTIATION; DYSGERMINOMA; EMBRYONAL CARCINOMA STEM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIGENETICS; FLOW CYTOMETRY; GENOME IMPRINTING; GERM CELL TUMOR; HISTOPATHOLOGY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INOCULATION; KARYOTYPE; NON SEMINOMATOUS GERMINOMA; NUCLEAR MAGNETIC RESONANCE IMAGING; PATIENT MONITORING; PHENOTYPE; PLURIPOTENT STEM CELL; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SEMINOMA; SPERMATOCYTIC SEMINOMA; STEM CELL TRANSPLANTATION; SURFACE PLASMON RESONANCE; TERATOMA; TESTIS NONSEMINOMA CANCER; YOLK SAC TUMOR;

ANIMALS; FEMALE; HUMANS; MALE; MICE; PLURIPOTENT STEM CELLS; STEM CELL TRANSPLANTATION; TERATOMA;

ANIMALIA;

EID: 84866080418     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.2329     Document Type: Review

References (92)

1. Lafamme, M.A. et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol. 25, 1015-1024 (2007).
2. Lu, B. et al. Long-term safety and function of RPE from human embryonic stem cells in preclinical models of macular degeneration. Stem Cells 27, 2126-2135 (2009).
3. Przyborski, S.A. Differentiation of human embryonic stem cells after transplantation in immune-defcient mice. Stem Cells 23, 1242-1250 (2005). (Pubitemid 41504912)
4. Cooke, M.J., Stojkovic, M. & Przyborski, S.A. Growth of teratomas derived from human pluripotent stem cells is infuenced by the graft site. Stem Cells Dev. 15, 254-259 (2006). (Pubitemid 43726503)
5. Prokhorova, T.A. et al. Teratoma formation by human embryonic stem cells is site-dependent and enhanced by the presence of Matrigel. Stem Cells Dev. 18, 47-54 (2009).
6. Hentze, H. et al. Teratoma formation by human embryonic stem cells: evaluation of essential parameters for future safety studies. Stem Cell Res. (Amst.) 2, 198-210 (2009).
7. Lee, A.S. et al. Effects of cell number on teratoma formation by human embryonic stem cells. Cell Cycle 8, 2608-2612 (2009).
8. Shih, C.C., Forman, S.J., Chu, P. & Slovak, M. Human embryonic stem cells are prone to generate primitive, undifferentiated tumors in engrafted human fetal tissues in severe combined immunodefcient mice. Stem Cells Dev. 16, 893-902 (2007).
9. Kelly, P.N., Dakic, A., Adams, J.M., Nutt, S.L. & Strasser, A. Tumor growth need not be driven by rare cancer stem cells. Science 317, 337 (2007). (Pubitemid 47106366)
10. Quintana, E. et al. Effcient tumour formation by single human melanoma cells. Nature 456, 593-598 (2008).
11. Gertow, K. et al. Early events in xenograft development from the human embryonic stem cell line HS181-resemblance with an initial multiple epiblast formation. PLoS ONE 6, e27741 (2011).
12. Griscelli, F. et al. Malignant germ cell-like tumors, expressing Ki-1 antigen (CD30), are revealed during in vivo differentiation of partially reprogrammed human-induced pluripotent stem cells. Am. J. Pathol. 180, 2084-2096 (2012).
13. Oosterhuis, J.W. & Looijenga, L.H. Testicular germ-cell tumours in a broader perspective. Nat. Rev. Cancer 5, 210-222 (2005). (Pubitemid 40314952)
14. Rossant, J. & Papaioannou, V.E. The relationship between embryonic, embryonal carcinoma and embryo-derived stem cells. Cell Differ. 15, 155-161 (1984). (Pubitemid 15140030)
15. Fu, W. et al. Residual undifferentiated cells during differentiation of induced pluripotent stem cells in vitro and in vivo. Stem Cells Dev. 21, 521-529 (2011).
16. Baker, D.E. et al. Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat. Biotechnol. 25, 207-215 (2007). (Pubitemid 46227120)
17. Harrison, N.J., Baker, D. & Andrews, P.W. Culture adaptation of embryonic stem cells echoes germ cell malignancy. Int. J. Androl. 30, 275-281 (2007). (Pubitemid 47254405)
18. Fazeli, A. et al. Altered patterns of differentiation in karyotypically abnormal human embryonic stem cells. Int. J. Dev. Biol. 55, 175-180 (2011).
19. Tavakoli, T. et al. Self-renewal and differentiation capabilities are variable between human embryonic stem cell lines I3, I6 and BG01V. BMC Cell Biol. 10, 44 (2009).
20. Moon, S.H. et al. Effect of chromosome instability on the maintenance and differentiation of human embryonic stem cells in vitro and in vivo. Stem Cell Res. 6, 50-59 (2011).
21. Adewumi, O. et al. Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat. Biotechnol. 25, 803-816 (2007). (Pubitemid 47052190)
22. Andrews, P.W. et al. Embryonic stem (ES) cells and embryonal carcinoma (EC) cells: opposite sides of the same coin. Biochem. Soc. Trans. 33, 1526-1530 (2005). (Pubitemid 41779730)
23. Akst, J. Cysts stall stem cell trial. Scientist (Aug). 27 (2009).
24. Roy, N.S. et al. Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat. Med. 12, 1259-1268 (2006). (Pubitemid 44706928)
25. De Backer, A., Madern, G.C., van de Ven, C.P., Tibboel, D. & Hazebroek, F.W. Strategy for management of newborns with cervical teratoma. J. Perinat. Med. 32, 500-508 (2004). (Pubitemid 39576869)
26. De Backer, A. et al. Study of the factors associated with recurrence in children with sacrococcygeal teratoma. J. Pediatr. Surg. 41, 173-181 (2006). (Pubitemid 43067513)
27. Oosterhuis, J.W., Looijenga, HJ., van Echten, J. & de Jong, B. Chromosomal constitution and developmental potential of human germ cell tumors and teratomas. Cancer Genet. Cytogenet. 95, 96-102 (1997). (Pubitemid 27188452)
28. Simmonds, P.D. et al. Primary pure teratoma of the testis. J. Urol. 155, 939-942 (1996). (Pubitemid 26052684)
29. de Graaff, W.E. et al. Ploidy of testicular carcinoma in situ. Lab. Invest. 66, 166-168 (1992).
30. Gobel, U. et al. Germ-cell tumors in childhood and adolescence. GPOH MAKEI and the MAHO study groups. Ann. Oncol. 11, 263-271 (2000). (Pubitemid 30214662)
31. Runyan, C, Gu, Y., Shoemaker, A., Looijenga, L. & Wylie, C. The distribution and behavior of extragonadal primordial germ cells in Bax mutant mice suggest a novel origin for sacrococcygeal germ cell tumors. Int. J. Dev. Biol. 52, 333-344 (2008). (Pubitemid 351792163)
32. Vortmeyer, A.O. et al. Microdissection-based analysis of mature ovarian teratoma. Am. J. Pathol. 154, 987-991 (1999).
33. Gertow, K. et al. Organized development from human embryonic stem cells after injection into immunodefcient mice. Stem Cells Dev. 13, 421-435 (2004). (Pubitemid 39223293)
34. Blum, B. & Benvenisty, N. Clonal analysis of human embryonic stem cell differentiation into teratomas. Stem Cells 25, 1924-1930 (2007). (Pubitemid 47258170)
35. Busch, C., Oppitz, M., Wehrmann, M., Schweizer, P. & Drews, U. Immunohistochemical localization of Nanog and Oct4 in stem cell compartments of human sacrococcygeal teratomas. Histopathology 52, 717-730 (2008). (Pubitemid 351600054)
36. Busch, C. et al. Isolation of three stem cell lines from human sacrococcygeal teratomas. J. Pathol. 217, 589-596 (2009).
37. Rijlaarsdam, M.A. et al. Specifc detection of OCT3/4 isoform A/B/B1 expression in solid (germ cell) tumours and cell lines: confrmation of OCT3/4 specifcity for germ cell tumours. Br. J. Cancer 105, 854-863 (2011).
38. Zwaka, T.P. & Thomson, J.A. A germ cell origin of embryonic stem cells? Development 132, 227-233 (2005). (Pubitemid 40268273)
39. West, J.A., Park, I.H., Daley, G.Q. & Geijsen, N. In vitro generation of germ cells from murine embryonic stem cells. Nat. Protoc. 1, 2026-2036 (2006). (Pubitemid 46773327)
40. Chu, L.F., Surani, M.A., Jaenisch, R. & Zwaka, T.P. Blimp1 expression predicts embryonic stem cell development in vitro. Curr. Biol. 21, 1759-1765 (2011).
41. O'Rahilly, R. & Muller, F. Neurulation in the normal human embryo. Ciba Found. Symp. 181, 70-82 (1994).
42. Sano, K. Pathogenesis of intracranial germ cell tumors reconsidered. J. Neurosurg. 90, 258-264 (1999). (Pubitemid 29068127)
43. Oosterhuis, J.W., Stoop, H., Honecker, F. & Looijenga, L.H. Why human extragonadal germ cell tumours occur in the midline of the body: old concepts, new perspectives. Int. J. Androl. 30, 256-264 (2007).
44. Blum, B. & Benvenisty, N. The tumorigenicity of human embryonic stem cells. Adv. Cancer Res. 100, 133-158 (2008). (Pubitemid 351932182)
45. Heifetz, S.A. et al. Immature teratomas in children: pathologic considerations: a report from the combined Pediatric Oncology Group/Children's Cancer Group. Am. J. Surg. Pathol. 22, 1115-1124 (1998). (Pubitemid 28411070)
46. Veltman, I.M., Schepens, M.T., Looijenga, L.H., Strong, L.C. & van Kessel, A.G. Germ cell tumours in neonates and infants: a distinct subgroup? APMIS 111, 152-160 (2003). (Pubitemid 36566685)
47. Spits, C. et al. Recurrent chromosomal abnormalities in human embryonic stem cells. Nat. Biotechnol. 26, 1361-1363 (2008).
48. Golas, M.M., Gunawan, B., Raab, B.W., Fuzesi, L. & Lange, B. Malignant transformation of an untreated congenital sacrococcygeal teratoma: a amplifcation at 8q and 12p detected by comparative genomic hybridization. Cancer Genet. Cytogenet. 197, 95-98 (2010).
49. Hong, H. et al. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 460, 1132-1135 (2009).
50. Norris, HJ., Zirkin, H.J. & Benson, W.L. Immature (malignant) teratoma of the ovary: a clinical and pathologic study of 58 cases. Cancer 37, 2359-2372 (1976).
51. O'Connor, D.M. & Norris, H.J. The infuence of grade on the outcome of stage I ovarian immature (malignant) teratomas and the reproducibility of grading. Int. J. Gynecol. Pathol. 13, 283-289 (1994). (Pubitemid 24309715)
52. Gonzalez-Crussi, F., Winkler, R.F. & Mirkin, D.L. Sacrococcygeal teratomas in infants and children: relationship of histology and prognosis in 40 cases. Arch. Pathol. Lab. Med. 102, 420-425 (1978). (Pubitemid 9004031)
53. Surti, U., Hoffner, L., Chakravarti, A. & Ferrell, R.E. Genetics and biology of human ovarian teratomas. I. Cytogenetic analysis and mechanism of origin. Am. J. Hum. Genet. 47, 635-643 (1990).
54. Baker, B.A. et al. DNA content of ovarian immature teratomas and malignant germ cell tumors. Gynecol. Oncol. 71, 14-18 (1998). (Pubitemid 28492387)
55. Mostert, M. et al. Comparative genomic and in situ hybridization of germ cell tumors of the infantile testis. Lab. Invest. 80, 1055-1064 (2000). (Pubitemid 30483223)
56. Schneider, D.T. et al. Genetic analysis of childhood germ cell tumors with comparative genomic hybridization. Klin. Padiatr. 213, 204-211 (2001). (Pubitemid 32801573)
57. Schneider, D.T. et al. Genetic analysis of mediastinal nonseminomatous germ cell tumors in children and adolescents. Genes Chromosom. Cancer 34, 115-125 (2002). (Pubitemid 34260603)
58. Schneider, D.T. et al. Molecular genetic analysis of central nervous system germ cell tumors with comparative genomic hybridization. Mod. Pathol. 19, 864-873 (2006). (Pubitemid 43780457)
59. Voorhoeve, P.M. et al. A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 124, 1169-1181 (2006).
60. Herszfeld, D. et al. CD30 is a survival factor and a biomarker for transformed human pluripotent stem cells. Nat. Biotechnol. 24, 351-357 (2006). (Pubitemid 43372160)
61. Werbowetski-Ogilvie, T.E. et al. Characterization of human embryonic stem cells with features of neoplastic progression. Nat. Biotechnol. 27, 91-97 (2009).
62. Gopalakrishna-Pillai, S. & Iverson, L.E. Astrocytes derived from trisomic human embryonic stem cells express markers of astrocytic cancer cells and premalignant stem-like progenitors. BMC Med. Genomics 3, 12 (2010).
63. Furukawa, S. et al. Yolk sac tumor but not seminoma or teratoma is associated with abnormal epigenetic reprogramming pathway and shows frequent hypermethylation of various tumor suppressor genes. Cancer Sci. 100, 698-708 (2009).
64. Sauvageau, M. & Sauvageau, G. Polycomb group genes: keeping stem cell activity in balance. PLoS Biol. 6, e113 (2008).
65. Ohm, J.E. et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat. Genet. 39, 237-242 (2007). (Pubitemid 46184356)
66. Netto, G.J. et al. Global DNA hypomethylation in intratubular germ cell neoplasia and seminoma, but not in nonseminomatous male germ cell tumors. Mod. Pathol. 21, 1337-1344 (2008).
67. Wermann, H. et al. Global DNA methylation in fetal human germ cells and germ cell tumours: association with differentiation and cisplatin resistance. J. Pathol. 221, 433-442 (2010).
68. Minami, K. et al. DNMT3L is a novel marker and is essential for the growth of human embryonal carcinoma. Clin. Cancer Res. 16, 2751-2759 (2010).
69. Tang, C. et al. An antibody against SSEA-5 glycan on human pluripotent stem cells enables removal of teratoma-forming cells. Nat. Biotechnol. 29, 829-834 (2011).
70. Visvader, J.E. & Lindeman, G.J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer 8, 755-768 (2008).
71. Lawrenz, B. et al. Highly sensitive biosafety model for stem-cell-derived grafts. Cytotherapy 6, 212-222 (2004). (Pubitemid 38868094)
72. Crabbe, A. et al. Effects of MRI contrast agents on the stem cell phenotype. Cell Transplant. 19, 919-936 (2010).
73. Havranek, P. et al. Sacrococcygeal teratoma in Sweden: a 10-year national retrospective study. J. Pediatr. Surg. 27, 1447-1450 (1992).
74. Lebkowski, J.S. et al. Human embryonic stem cells: culture, differentiation, and genetic modifcation for regenerative medicine applications. Cancer J. 7 (suppl. 2), S83-S93 (2001).
75. Kelly, O.G. et al. Cell-surface markers for the isolation of pancreatic cell types derived from human embryonic stem cells. Nat. Biotechnol. 29, 750-756 (2011).
76. Roche, S. et al. Comparative analysis of protein expression of three stem cell populations: models of cytokine delivery system in vivo. Int. J. Pharm. advance online publication, doi: 10.1016/j.ijpharm.2011.12.041 (20 January 2012).
77. Chambers, I. et al. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113, 643-655 (2003). (Pubitemid 36694189)
78. Boyer, L.A. et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122, 947-956 (2005). (Pubitemid 41345211)
79. Assou, S. et al. A meta-analysis of human embryonic stem cells transcriptome integrated into a web-based expression atlas. Stem Cells 25, 961-973 (2007). (Pubitemid 46572593)
80. Suh, M.R. et al. Human embryonic stem cells express a unique set of microRNAs. Dev. Biol. 270, 488-498 (2004).
81. Morin, R.D. et al. Application of massively parallel sequencing to microRNA profling and discovery in human embryonic stem cells. Genome Res. 18, 610-621 (2008). (Pubitemid 351482785)
82. Curado, M.P. et al. Cancer Incidence in Five Continents, Vol IX (IARC Scientifc Publications No. 160, Lyon, France, 2007).
83. Sarasquete, M.E. et al. Minimal residual disease monitoring in multiple myeloma: a comparison between allelic-specifc oligonucleotide real-time quantitative polymerase chain reaction and fow cytometry. Haematologica 90, 1365-1372 (2005). (Pubitemid 41503652)
84. Mason, K.D. & Juneja, S. Go with the fow for monitoring response in myeloma with minimal residual disease. Leuk. Lymphoma 49, 177-178 (2008). (Pubitemid 351193908)
85. St. Ledger, K. et al. Analytical validation of a highly sensitive microparticle-based immunoassay for the quantitation of IL-13 in human serum using the Erenna immunoassay system. J. Immunol. Methods 350, 161-170 (2009).
86. Eriksson, L. et al. An investigation of sensitivity limits in PET scanners. Nucl. Instrum. Methods Phys. Res. A 580, 836-842 (2007). (Pubitemid 47379900)
87. Schmittgen, T.D. et al. Real-time PCR quantifcation of precursor and mature microRNA. Methods 44, 31-38 (2008). (Pubitemid 350297984)
88. Gillis, A.J. et al. Expression and interdependencies of pluripotency factors LIN28, OCT3/4, NANOG and SOX2 in human testicular germ cells and tumours of the testis. Int. J. Androl. 34, e160-e174 (2011).
89. Li, J., Schachermeyer, S., Wang, Y., Yin, Y. & Zhong, W. Detection of microRNA by fuorescence amplifcation based on cation-exchange in nanocrystals. Anal. Chem. 81, 9723-9729 (2009).
90. Zhou, W.J., Chen, Y. & Corn, R.M. Ultrasensitive microarray detection of short RNA sequences with enzymatically modifed nanoparticles and surface plasmon resonance imaging measurements. Anal. Chem. 83, 3897-3902 (2011).
91. Cao, F. et al. Noninvasive de novo imaging of human embryonic stem cell-derived teratoma formation. Cancer Res. 69, 2709-2713 (2009).
92. Su, W. et al. Bioluminescence reporter gene imaging characterize human embryonic stem cell-derived teratoma formation. J. Cell. Biochem. 112, 840-848 (2011).