Teratoma formation: A tool for monitoring pluripotency in stem cell research

Current Protocols in Stem Cell Biology

Volumn 2015, Issue , 2015, Pages 4a.8.1-4a.8.17

  Nelakanti, Raman V ^a   Kooreman, Nigel G ^a,b   Wu, Joseph C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Embryonic stem cell; Induced pluripotent stem cell; Pluripotency; Pluripotent stem cell; Teratoma; Tumorigenicity

Indexed keywords

PARAFFIN; PARAFORMALDEHYDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL MONITORING; CARCINOGENESIS; CELL ASSAY; CELL TRANSPLANTATION; CLINICAL PROTOCOL; CONTROLLED STUDY; CRYOPRESERVATION; ECTODERM; EMBEDDING; EMBRYONAL TISSUE; EMBRYONIC STEM CELL; ENDODERM; EXPLANT; FETUS; GASTROCNEMIUS MUSCLE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MEDICAL RESEARCH; MESODERM; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; SURGICAL ANATOMY; TERATOMA; TISSUE FIXATION; TUMOR GROWTH; ANIMAL; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; INJECTION; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; STEM CELL RESEARCH;

ANIMALS; CRYOPRESERVATION; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INJECTIONS; MICE, INBRED NOD; MICE, SCID; PARAFFIN EMBEDDING; PLURIPOTENT STEM CELLS; STEM CELL RESEARCH; TERATOMA; TISSUE FIXATION;

EID: 84942852568     PISSN: 19417322     EISSN: 19388969     Source Type: Journal    
DOI: 10.1002/9780470151808.sc04a08s32     Document Type: Article

References (51)

1. Ben-David, U., Mayshar, Y., and Benvenisty, N. 2013. Virtual karyotyping of pluripotent stem cells on the basis of their global gene expression profiles. Nat. Protoc. 8:989-997.
2. Bhattacharya, B., Miura, T., Brandenberger, R., Mejido, J., Luo, Y., Yang, A.X., Joshi, B.H., Ginis, I., Thies, R.S., Amit, M., Lyons, I., Condie, B.G., Itskovitz-Eldor, J., Rao, M.S., and Puri, R.K. 2004. Gene expression in human embryonic stem cell lines:Unique molecular signature. Blood 103:2956-2964.
3. Bock, C., Kiskinis, E., Verstappen, G., Gu, H., Boulting, G., Smith, Z.D., Ziller, M., Croft, G.F., Amoroso, M.W., Oakley, D.H., Gnirke, A., Eggan, K., and Meissner, A. 2011. Reference maps of human ES and iPS cell variation enable high-throughput characterization of pluripotent cell lines. Cell 144:439-452.
4. Brivanlou, A.H., Gage, F.H., Jaenisch, R., Jessell, T., Melton, D., and Rossant, J. 2003. Stem cells. Setting standards for human embryonic stem cells. Science 300:913-916.
5. Buchwalow, I.H. and Böcker, W. 2010. Probes processing in immunohistochemistry. In Immunohistochemistry: Basics and Methods, pp. 19-29. Springer-Verlag, Heidelberg.
6. Buta, C., David, R., Dressel, R., Emgård, M., Fuchs, C., Gross, U., Healy, L., Hescheler, J., Kolar, R., Martin, U., Mikkers, H., Müller, F.-J., Schneider, R.K., Seiler, A.E.M., Spielmann, H., and Weitzer, G. 2013. Reconsidering pluripotency tests: Do we still need teratoma assays? Stem Cell Res. 11:552-562.
7. Cao, F., Lin, S., Xie, X., Ray, P., Patel, M., Zhang, X., Drukker, M., Dylla, S.J., Connolly, A.J., Chen, X., Weissman, I.L., Gambhir, S.S., and Wu, J.C. 2006. In vivo visualization of embryonic stem cell survival, proliferation, and migration after cardiac delivery. Circulation 113:1005-1014.
8. Cao, F., van der Bogt, K.E.A., Sadrzadeh, A., Xie, X., Sheikh, A.Y., Wang, H., Connolly, A.J., Robbins, R.C., and Wu, J.C. 2007. Spatial and temporal kinetics of teratoma formation from murine embryonic stem cell transplantation. Stem Cells Dev. 16:883-891.
9. Cardiff, R.D., Miller, C.H., and Munn, R.J. 2014. Manual hematoxylin and eosin staining of mouse tissue sections. Cold Spring Harb. Protoc. 2014:655-658.
10. Cooke, M.J., Stojkovic, M., and Przyborski, S.A. 2006. Growth of teratomas derived from human pluripotent stem cells is influenced by the graft site. Stem Cells Dev. 15:254-259.
11. Daley, G.Q., Lensch, M.W., Jaenisch, R., Meissner, A., Plath, K., and Yamanaka, S. 2009. Broader implications of defining standards for the pluripotency of iPSCs. Cell Stem Cell 4:200-201; author reply 202.
12. Dressel, R. 2011. Effects of histocompatibility and host immune responses on the tumorigenicity of pluripotent stem cells. Semin. Immunopathol. 33:573-591.
13. Fawcett, D.W. 1950. Bilateral ovarian teratomas in a mouse. Cancer Res. 10:705-707.
14. Fekete, E. and Ferrigno, M.A. 1952. Studies on a transplantable teratoma of the mouse. Cancer Res. 12:438-440.
15. Fischer, A.H., Jacobson, K.A., Rose, J., and Zeller, R. 2008. Cryosectioning tissues. Cold Spring Harb. Protoc. doi:10.1101/pdb.prot4991.
16. Fraenkel-Conrat, H. and Olcott, H.S. 1948. The reaction of formaldehyde with proteins; crosslinking between amino and primary amide or guanidyl groups. J. Am. Chem. Soc. 70:2673-2684.
17. Gertow, K., Przyborski, S., Loring, J.F., Auerbach, J.M., Epifano, O., Otonkoski, T., Damjanov, I., and Ahrlund-Richter, L. 2007. Isolation of human embryonic stem cell-derived teratomas for the assessment of pluripotency. Curr. Protoc. Stem Cell Biol. 3:1B.4.1-1B.4.29.
18. Gropp, M., Shilo, V., Vainer, G., Gov, M., Gil, Y., Khaner, H., Matzrafi, L., Idelson, M., Kopolovic, J., Zak, N.B., and Reubinoff, B.E. 2012. Standardization of the teratoma assay for analysis of pluripotency of human ES cells and biosafety of their differentiated progeny. PLoS One 7:e45532.
19. Gutierrez-Aranda, I., Ramos-Mejia, V., Bueno, C., Munoz-Lopez, M., Real, P.J., Mácia, A., Sanchez, L., Ligero, G., Garcia-Parez, J.L., and Menendez, P. 2010. Human induced pluripotent stem cells develop teratoma more efficiently and faster than human embryonic stem cells regardless the site of injection. Stem Cells 28:1568-1570.
20. Hentze, H., Soong, P.L., Wang, S.T., Phillips, B.W., Putti, T.C., and Dunn, N.R. 2009. Teratoma formation by human embryonic stem cells: Evaluation of essential parameters for future safety studies. Stem Cell Res. 2:198-210.
21. Karlsson, C., Emanuelsson, K., Wessberg, F., Kajic, K., Axell, M.Z., Eriksson, P.S., Lindahl, A., Hyllner, J., and Strehl, R. 2009. Human embryonic stem cell-derived mesenchymal progenitors-potential in regenerative medicine. Stem Cell Res. 3:39-50.
22. Kim, J.B., Zaehres, H., Wu, G., Gentile, L., Ko, K., Sebastiano, V., Araúzo-Bravo, M.J., Ruau, D., Han, D.W., Zenke, M., and Schöler, H.R. 2008. Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature 454:646-650.
23. Koehler, K.R., Tropel, P., Theile, J.W., Kondo, T., Cummins, T.R., Viville, S., and Hashino, E. 2011. Extended passaging increases the efficiency of neural differentiation from induced pluripotent stem cells. BMC Neurosci. 12:82.
24. Kooreman, N.G. and Wu, J.C. 2010. Tumorigenicity of pluripotent stem cells: Biological insights from molecular imaging. J. R. Soc. Interface 7 Suppl 6:S753-S763.
25. Lan, F., Lee, A.S., Liang, P., Sanchez-Freire, V., Nguyen, P.K., Wang, L., Han, L., Yen, M., Wang, Y., Sun, N., Abilez, O.J., Hu, S., Ebert, A.D., Navarrete, E.G., Simmons, C.S., Wheeler, M., Pruitt, B., Lewis, R., Yamaguchi, Y., Ashley, E.A., Bers, D.M., Robbins, R.C., Longaker, M.T., and Wu, J.C. 2013. Abnormal calcium handling properties underlie familial hypertrophic cardiomyopathy pathology in patientspecific induced pluripotent stem cells. Cell Stem Cell 12:101-113.
26. Laurent, L.C., Ulitsky, I., Slavin, I., Tran, H., Schork, A., Morey, R., Lynch, C., Harness, J. V, Lee, S., Barrero, M.J., Ku, S., Martynova, M., Semechkin, R., Galat, V., Gottesfeld, J., Izpisua Belmonte, J.C., Murry, C., Keirstead, H.S., Park, H.-S., Schmidt, U., Laslett, A.L., Muller, F.-J., Nievergelt, C.M., Shamir, R., and Loring, J.F. 2011. Dynamic changes in the copy number of pluripotency and cell proliferation genes in human ESCs and iPSCs during reprogramming and time in culture. Cell Stem Cell 8:106-118.
27. Lee, A.S., Tang, C., Cao, F., Xie, X., van der Bogt, K., Hwang, A., Connolly, A.J., Robbins, R.C., and Wu, J.C. 2009. Effects of cell number on teratoma formation by human embryonic stem cells. Cell Cycle 8:2608-2612.
28. Lee, A.S., Tang, C., Rao, M.S., Weissman, I.L., and Wu, J.C. 2013. Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies. Nat. Med. 19:998-1004.
29. Lees, J.G., Lim, S.A., Croll, T., Williams, G., Lui, S., Cooper-White, J., McQuade, L.R., Mathiyalagan, B., and Tuch, B.E. 2007. Transplantation of 3D scaffolds seeded with human embryonic stem cells: Biological features of surrogate tissue and teratoma-forming potential. Regen. Med. 2:289-300.
30. Li, X.-Y., Jia, Q., Di, K.-Q., Gao, S.-M., Wen, X.-H., Zhou, R.-Y., Wei, W., and Wang, L.-Z. 2007. Passage number affects the pluripotency of mouse embryonic stem cells as judged by tetraploid embryo aggregation. Cell Tissue Res. 327:607-614.
31. Lister, R., Pelizzola, M., Kida, Y.S., Hawkins, R.D., Nery, J.R., Hon, G., Antosiewicz-Bourget, J., O'Malley, R., Castanon, R., Klugman, S., Downes, M., Yu, R., Stewart, R., Ren, B., Thomson, J.a., Evans, R.M., and Ecker, J.R. 2011. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471:68-73.
32. Marks, H., Kalkan, T., Menafra, R., Denissov, S., Jones, K., Hofemeister, H., Nichols, J., Kranz, A., Stewart, A.F., Smith, A., and Stunnenberg, H.G. 2012. The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149:590-604.
33. Martí, M., Mulero, L., Pardo, C., Morera, C., Carrió, M., Laricchia-Robbio, L., Esteban, C.R., and Izpisua Belmonte, J.C. 2013. Characterization of pluripotent stem cells. Nat. Protoc. 8:223-253.
34. Martin, G.R. 1981. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. U.S.A. 78:7634-7638.
35. Masui, S., Nakatake, Y., Toyooka, Y., Shimosato, D., Yagi, R., Takahashi, K., Okochi, H., Okuda, A., Matoba, R., Sharov, A.A., Ko, M.S.H., and Niwa, H. 2007. Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat. Cell Biol. 9:625-635.
36. Mills, J.A., Wang, K., Paluru, P., Ying, L., Lu, L., Galvão, A.M., Xu, D., Yao, Y., Sullivan, S.K., Sullivan, L.M., Mac, H., Omari, A., Jean, J.-C., Shen, S., Gower, A., Spira, A., Mostoslavsky, G., Kotton, D.N., French, D.L., Weiss, M.J., and Gadue, P. 2013. Clonal genetic and hematopoietic heterogeneity among human-induced pluripotent stem cell lines. Blood 122:2047-2051.
37. Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M., Maeda, M., and Yamanaka, S. 2003. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113:631-642.
38. Müller, F.-J., Goldmann, J., Löser, P., and Loring, J.F. 2010. A call to standardize teratoma assays used to define human pluripotent cell lines. Cell Stem Cell 6:412-414.
39. Müller, F.-J., Schuldt, B.M., Williams, R., Mason, D., Altun, G., Papapetrou, E.P., Danner, S., Goldmann, J.E., Herbst, A., Schmidt, N.O., Aldenhoff, J.B., Laurent, L.C., and Loring, J.F. 2011. A bioinformatic assay for pluripotency in human cells. Nat. Methods 8:315-317.
40. Narsinh, K.H., Sun, N., Sanchez-Freire, V., Lee, A.S., Almeida, P., Hu, S., Jan, T., Wilson, K.D., Leong, D., Rosenberg, J., Yao, M., Robbins, R.C., and Wu, J.C. 2011. Single cell transcriptional profiling reveals heterogeneity of human induced pluripotent stem cells. J. Clin. Invest. 121:1217-1221.
41. Noaksson, K., Zoric, N., Zeng, X., Rao, M.S., Hyllner, J., Semb, H., Kubista, M., and Sartipy, P. 2005. Monitoring differentiation of human embryonic stem cells using real-time PCR. Stem Cells 23:1460-1467.
42. Park, Y.B., Kim, Y.Y., Oh, S.K., Chung, S.G., Ku, S.Y., Kim, S.H., Choi, Y.M., and Moon, S.Y. 2008. Alterations of proliferative and differentiation potentials of human embryonic stem cells during long-term culture. Exp. Mol. Med. 40:98-108.
43. Plaia, T.W., Josephson, R., Liu, Y., Zeng, X., Ording, C., Toumadje, A., Brimble, S.N., Sherrer, E.S., Uhl, E.W., Freed, W.J., Schulz, T.C., Maitra, A., Rao, M.S., and Auerbach, J.M. 2006. Characterization of a new NIHregistered variant human embryonic stem cell line, BG01V: A tool for human embryonic stem cell research. Stem Cells 24:531-546.
44. Prokhorova, T.A., Harkness, L.M., Frandsen, U., Ditzel, N., Schrøder, H.D., Burns, J.S., and 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.
45. Robinton, D.A. and Daley, G.Q. 2012. The promise of induced pluripotent stem cells in research and therapy. Nature 481:295-305.
46. Stevens, L.C. and Little, C.C. 1954. Spontaneous testicular teratomas in an inbred strain of mice. Proc. Natl. Acad. Sci. U.S.A. 40:1080-1087.
47. Takahashi, K. and Yamanaka, S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676.
48. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., and Yamanaka, S. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872.
49. Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., Waknitz, M.A., Swiergiel, J.J., Marshall, V.S., and Jones, J.M. 1998. Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147.
50. Xie, X., Hiona, A., Lee, A.S., Cao, F., Huang, M., Li, Z., Cherry, A., Pei, X., and Wu, J.C. 2011. Effects of long-term culture on human embryonic stem cell aging. Stem Cells Dev. 20:127-138.
51. Zeller, R. 1989. Fixation, embedding, and sectioning of tissues, embryos, and single cells. Curr. Protoc. Mol. Biol. 14:14.1.1-14.1.8.