Immunologic and chemical targeting of the tight-junction protein Claudin-6 eliminates tumorigenic human pluripotent stem cells

Nature Communications

Volumn 4, Issue , 2013, Pages

  Ben David, Uri ^a   Nudel, Neta ^a   Benvenisty, Nissim ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 6; CYTOTOXIN; ENTEROTOXIN; PROTEIN ANTIBODY;

ADULT; ANTIBODY; BIOTECHNOLOGY; DISEASE TREATMENT; IMMUNE SYSTEM; MEDICINE; PROTEIN; TOXIN; TUMOR;

ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL KILLING; CELL POPULATION; CELL RENEWAL; CELL SURVIVAL; CHEMICAL PROCEDURES; CLOSTRIDIUM PERFRINGENS; CONJUGATE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOLOGICAL PROCEDURES; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; SEPARATION TECHNIQUE; TERATOMA;

ANIMALS; CARCINOGENESIS; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CLAUDINS; DOWN-REGULATION; EMBRYONIC STEM CELLS; ENTEROTOXINS; FIBROBLASTS; HUMANS; MICE; PLURIPOTENT STEM CELLS; TERATOMA; TIGHT JUNCTION PROTEINS;

CLOSTRIDIUM PERFRINGENS;

EID: 84879905939     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2992     Document Type: Article

References (37)

1. Yamanaka, S. Induced pluripotent stem cells: past, present, and future. Cell Stem Cell 10, 678-684 (2012).
2. Ben-David, U., Kopper, O. & Benvenisty, N. Expanding the boundaries of embryonic stem cells. Cell Stem Cell 10, 666-677 (2012).
3. Ben-David, U. & Benvenisty, N. The tumorigenicity of human embryonic and induced pluripotent stem cells. Nat. Rev. Cancer 11, 268-277 (2011).
4. Lee, A. S. et al. Effects of cell number on teratoma formation by human embryonic stem cells. Cell Cycle 8, 2608-2612 (2009).
5. Hentze, H. et al. Teratoma formation by human embryonic stem cells: evaluation of essential parameters for future safety studies. Stem Cell Res. 2, 198-210 (2009).
6. Miura, K. et al. Variation in the safety of induced pluripotent stem cell lines. Nat. Biotechnol. 27, 743-745 (2009).
7. 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 (2012).
8. Bieberich, E., Silva, J., Wang, G., Krishnamurthy, K. & Condie, B. G. 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 (2004). (Pubitemid 39565152)
9. Schuldiner, M., Itskovitz-Eldor, J. & Benvenisty, N. Selective ablation of human embryonic stem cells expressing a "suicide" gene. Stem Cells 21, 257-265 (2003). (Pubitemid 36623167)
10. Choo, A. B. et al. Selection against undifferentiated human embryonic stem cells by a cytotoxic antibody recognizing podocalyxin-like protein-1. Stem Cells 26, 1454-1463 (2008).
11. Blum, B., Bar-Nur, O., Golan-Lev, T. & Benvenisty, N. The anti-apoptotic gene survivin contributes to teratoma formation by human embryonic stem cells. Nat. Biotechnol. 27, 281-287 (2009).
12. Fong, C. Y., Peh, G. S., Gauthaman, K. & Bongso, A. 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. 5, 72-80 (2009).
13. 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).
14. 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)
15. Bhattacharya, B. et al. Gene expression in human embryonic stem cell lines: unique molecular signature. Blood 103, 2956-2964 (2004). (Pubitemid 38451667)
16. 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)
17. Hewitt, K. J., Agarwal, R. & Morin, P. J. The claudin gene family: expression in normal and neoplastic tissues. BMC Cancer 6, 186 (2006).
18. Wu, Q. et al. Tight junction protein, claudin-6, downregulates the malignant phenotype of breast carcinoma. Eur. J. Cancer. Prev. 19, 186-194 (2010).
19. Zavala-Zendejas, V. E. et al. Claudin-6, 7, or 9 overexpression in the human gastric adenocarcinoma cell line AGS increases its invasiveness, migration, and proliferation rate. Cancer Invest. 29, 1-11 (2011).
20. Ushiku, T., Shinozaki-Ushiku, A., Maeda, D., Morita, S. & Fukayama, M. Distinct expression pattern of claudin-6, a primitive phenotypic tight junction molecule, in germ cell tumours and visceral carcinomas. Histopathology 61, 1043-1056 (2012).
21. Wang, L. et al. Claudin 6: a novel surface marker for characterizing mouse pluripotent stem cells. Cell Res. 22, 1082-1085 (2012).
22. Turksen, K. & Troy, T. C. Claudin-6: a novel tight junction molecule is developmentally regulated in mouse embryonic epithelium. Dev. Dyn. 222, 292-300 (2001). (Pubitemid 32937601)
23. Anderson, W. J. et al. Genetic targeting of the endoderm with claudin-6CreER. Dev. Dyn. 237, 504-512 (2008).
24. Suzuki, M. et al. Therapeutic antitumor efficacy of monoclonal antibody against Claudin-4 for pancreatic and ovarian cancers. Cancer Sci. 100, 1623-1630 (2009).
25. Kohls, M. D. & Lappi, D. A. Mab-ZAP: a tool for evaluating antibody efficacy for use in an immunotoxin. Biotechniques 28, 162-165 (2000). (Pubitemid 30036834)
26. McClane, B. A. & Chakrabarti, G. New insights into the cytotoxic mechanisms of Clostridium perfringens enterotoxin. Anaerobe 10, 107-114 (2004). (Pubitemid 38519811)
27. Kim, D. S. et al. Robust enhancement of neural differentiation from human ES and iPS cells regardless of their innate difference in differentiation propensity. Stem Cell Rev. 6, 270-281 (2010).
28. Matsumoto, T. et al. Isolation and characterization of human anterior cruciate ligament-derived vascular stem cells. Stem Cells Dev. 21, 859-872 (2012).
29. 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)
30. Ben-David, U. et al. Selective elimination of human pluripotent stem cells by an oleate synthesis inhibitor discovered in a high-throughput screen. Cell Stem Cell 12, 167-179 (2013).
31. Thomson, J. A. et al. Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147 (1998). (Pubitemid 28516247)
32. Kopper, O. & Benvenisty, N. Stepwise differentiation of human embryonic stem cells into early endoderm derivatives and their molecular characterization. Stem Cell Res. 8, 335-345 (2012).
33. Pick, M. et al. Clone-and gene-specific aberrations of parental imprinting in human induced pluripotent stem cells. Stem Cells 27, 2686-2690 (2009).
34. Ma, Y. et al. High-efficiency siRNA-based gene knockdown in human embryonic stem cells. RNA. 16, 2564-2569 (2010).
35. Marteyn, A. et al. Mutant human embryonic stem cells reveal neurite and synapse formation defects in type 1 myotonic dystrophy. Cell Stem Cell 8, 434-444 (2011).
36. Fishman, B. et al. Targeting pancreatic progenitor cells in human embryonic stem cell differentiation for the identification of novel cell surface markers. Stem Cell Rev. 8, 792-802 (2012).
37. Si-Tayeb, K. et al. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology. 51, 297-305 (2010).