Path to the clinic: Assessment of iPSC-based cell therapies in vivo in a nonhuman primate model

Cell Reports

Volumn 7, Issue 4, 2014, Pages 1298-1309

  Hong, So Gun ^a   Winkler, Thomas ^a   Wu, Chuanfeng ^a   Guo, Vicky ^a   Pittaluga, Stefania ^b   Nicolae, Alina ^b   Donahue, Robert E ^a   Metzger, Mark E ^a   Price, Sandra D ^a   Uchida, Naoya ^c   Kuznetsov, Sergei A ^d   Kilts, Tina ^d   Li, Li ^d   Robey, Pamela G ^d   Dunbar, Cynthia E ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; NERVE CELL ADHESION MOLECULE; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL THERAPY; CONTROLLED STUDY; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; INFLAMMATION; MESODERM; NONHUMAN; PLURIPOTENT STEM CELL; PRIMATE; PRIORITY JOURNAL; REGENERATIVE MEDICINE; RHESUS MONKEY; TERATOMA; ANIMAL TISSUE; AUTOLOGOUS STEM CELL TRANSPLANTATION; BONE CELL; CELL MATURATION; DOSE RESPONSE; FEMALE; HUMAN VERSUS NONHUMAN DATA; MALE; MESODERMAL CELL; MOUSE; STEM CELL TRANSPLANTATION; STROMA CELL; TREATMENT RESPONSE; ADVERSE EFFECTS; ANIMAL; BIOLOGICAL THERAPY; BONE REGENERATION; CYTOLOGY; INDUCED PLURIPOTENT STEM CELL; METABOLISM; PHYSIOLOGY; PROCEDURES; TRANSPLANTATION;

ANIMALIA; PRIMATES; RODENTIA;

ANIMALS; BONE REGENERATION; CELL DIFFERENTIATION; CELL- AND TISSUE-BASED THERAPY; FEMALE; INDUCED PLURIPOTENT STEM CELLS; MACACA MULATTA; MALE; MICE; MODELS, ANIMAL;

EID: 84901272219     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.04.019     Document Type: Article

References (47)

1. Amabile G., Welner R.S., Nombela-Arrieta C., D'Alise A.M., Di Ruscio A., Ebralidze A.K., Kraytsberg Y., Ye M., Kocher O., Neuberg D.S., et al. In vivo generation of transplantable human hematopoietic cells from induced pluripotent stem cells. Blood 2013, 121:1255-1264.
2. Araki R., Uda M., Hoki Y., Sunayama M., Nakamura M., Ando S., Sugiura M., Ideno H., Shimada A., Nifuji A., Abe M. Negligible immunogenicity of terminally differentiated cells derived from induced pluripotent or embryonic stem cells. Nature 2013, 494:100-104.
3. Atoui R., Chiu R.C. Concise review: immunomodulatory properties of mesenchymal stem cells in cellular transplantation: update, controversies, and unknowns. Stem Cells Transl. Med. 2012, 1:200-205.
4. Ben-David U., Gan Q.F., Golan-Lev T., Arora P., Yanuka O., Oren Y.S., Leikin-Frenkel A., Graf M., Garippa R., Boehringer M., et al. Selective elimination of human pluripotent stem cells by an oleate synthesis inhibitor discovered in a high-throughput screen. Cell Stem Cell 2013, 12:167-179.
5. Bianco P., Riminucci M., Gronthos S., Robey P.G. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 2001, 19:180-192.
6. Bianco P., Robey P.G., Simmons P.J. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell 2008, 2:313-319.
7. Bilousova G., Jun H., King K.B., De Langhe S., Chick W.S., Torchia E.C., Chow K.S., Klemm D.J., Roop D.R., Majka S.M. Osteoblasts derived from induced pluripotent stem cells form calcified structures in scaffolds both in vitro and in vivo. Stem Cells 2011, 29:206-216.
8. Cunningham J.J., Ulbright T.M., Pera M.F., Looijenga L.H. Lessons from human teratomas to guide development of safe stem cell therapies. Nat. Biotechnol. 2012, 30:849-857.
9. de Almeida P.E., Ransohoff J.D., Nahid A., Wu J.C. Immunogenicity of pluripotent stem cells and their derivatives. Circ. Res. 2013, 112:549-561.
10. Dhodapkar K.M., Feldman D., Matthews P., Radfar S., Pickering R., Turkula S., Zebroski H., Dhodapkar M.V. Natural immunity to pluripotency antigen OCT4 in humans. Proc. Natl. Acad. Sci. USA 2010, 107:8718-8723.
11. Di Stasi A., Tey S.K., Dotti G., Fujita Y., Kennedy-Nasser A., Martinez C., Straathof K., Liu E., Durett A.G., Grilley B., et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N. Engl. J. Med. 2011, 365:1673-1683.
12. Donahue R.E., Dunbar C.E. Update on the use of nonhuman primate models for preclinical testing of gene therapy approaches targeting hematopoietic cells. Hum. Gene Ther. 2001, 12:607-617.
13. Emborg M.E., Liu Y., Xi J., Zhang X., Yin Y., Lu J., Joers V., Swanson C., Holden J.E., Zhang S.C. Induced pluripotent stem cell-derived neural cells survive and mature in the nonhuman primate brain. Cell Rep. 2013, 3:646-650.
14. Guha P., Morgan J.W., Mostoslavsky G., Rodrigues N.P., Boyd A.S. Lack of immune response to differentiated cells derived from syngeneic induced pluripotent stem cells. Cell Stem Cell 2013, 12:407-412.
15. Hayashi T., Misawa H., Nakahara H., Noguchi H., Yoshida A., Kobayashi N., Tanaka M., Ozaki T. Transplantation of osteogenically differentiated mouse iPS cells for bone repair. Cell Transplant. 2012, 21:591-600.
16. Illich D.J., Demir N., Stojković M., Scheer M., Rothamel D., Neugebauer J., Hescheler J., Zöller J.E. Concise review: induced pluripotent stem cells and lineage reprogramming: prospects for bone regeneration. Stem Cells 2011, 29:555-563.
17. Kaneko S., Yamanaka S. To be immunogenic, or not to be: that's the iPSC question. Cell Stem Cell 2013, 12:385-386.
18. Kuznetsov S.A., Krebsbach P.H., Satomura K., Kerr J., Riminucci M., Benayahu D., Robey P.G. Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J. Bone Miner. Res. 1997, 12:1335-1347.
19. Kuznetsov S.A., Cherman N., Robey P.G. In vivo bone formation by progeny of human embryonic stem cells. Stem Cells Dev. 2011, 20:269-287.
20. Lackner A.A., Veazey R.S. Current concepts in AIDS pathogenesis: insights from the SIV/macaque model. Annu. Rev. Med. 2007, 58:461-476.
21. Lee A.S., Tang C., Rao M.S., Weissman I.L., Wu J.C. Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies. Nat. Med. 2013, 19:998-1004.
22. Lian Q., Zhang Y., Zhang J., Zhang H.K., Wu X., Zhang Y., Lam F.F., Kang S., Xia J.C., Lai W.H., et al. Functional mesenchymal stem cells derived from human induced pluripotent stem cells attenuate limb ischemia in mice. Circulation 2010, 121:1113-1123.
23. Lindsay R.M., Raisman G., Seeley P.J. Intracerebral transplantation of cultured neurons after reaggregation in a plasma clot. Neuroscience 1987, 21:685-698.
24. Liu H., Zhu F., Yong J., Zhang P., Hou P., Li H., Jiang W., Cai J., Liu M., Cui K., et al. Generation of induced pluripotent stem cells from adult rhesus monkey fibroblasts. Cell Stem Cell 2008, 3:587-590.
25. Marolt D., Campos I.M., Bhumiratana S., Koren A., Petridis P., Zhang G., Spitalnik P.F., Grayson W.L., Vunjak-Novakovic G. Engineering bone tissue from human embryonic stem cells. Proc. Natl. Acad. Sci. USA 2012, 109:8705-8709.
26. Merling R.K., Sweeney C.L., Choi U., De Ravin S.S., Myers T.G., Otaizo-Carrasquero F., Pan J., Linton G., Chen L., Koontz S., et al. Transgene-free iPSCs generated from small volume peripheral blood nonmobilized CD34+ cells. Blood 2013, 121:e98-e107.
27. Mitalipov S., Kuo H.C., Byrne J., Clepper L., Meisner L., Johnson J., Zeier R., Wolf D. Isolation and characterization of novel rhesus monkey embryonic stem cell lines. Stem Cells 2006, 24:2177-2186.
28. Nasef A., Ashammakhi N., Fouillard L. Immunomodulatory effect of mesenchymal stromal cells: possible mechanisms. Regen. Med. 2008, 3:531-546.
29. Okita K., Yamanaka S. Intracellular signaling pathways regulating pluripotency of embryonic stem cells. Curr. Stem Cell Res. Ther. 2006, 1:103-111.
30. Picker L.J., Hansen S.G., Lifson J.D. New paradigms for HIV/AIDS vaccine development. Annu. Rev. Med. 2012, 63:95-111.
31. Prokhorova T.A., Harkness L.M., Frandsen U., Ditzel N., Schrøder H.D., Burns J.S., Kassem M. Teratoma formation by human embryonic stem cells is site dependent and enhanced by the presence of Matrigel. Stem Cells Dev. 2009, 18:47-54.
32. Quarto R., Mastrogiacomo M., Cancedda R., Kutepov S.M., Mukhachev V., Lavroukov A., Kon E., Marcacci M. Repair of large bone defects with the use of autologous bone marrow stromal cells. N. Engl. J. Med. 2001, 344:385-386.
33. Rao M. Conserved and divergent paths that regulate self-renewal in mouse and human embryonic stem cells. Dev. Biol. 2004, 275:269-286.
34. Robey P.G. Cell sources for bone regeneration: the good, the bad, and the ugly (but promising). Tissue Eng. Part B Rev. 2011, 17:423-430.
35. Roobrouck V.D., Ulloa-Montoya F., Verfaillie C.M. Self-renewal and differentiation capacity of young and aged stem cells. Exp. Cell Res. 2008, 314:1937-1944.
36. Schnerch A., Cerdan C., Bhatia M. Distinguishing between mouse and human pluripotent stem cell regulation: the best laid plans of mice and men. Stem Cells 2010, 28:419-430.
37. Seok J., Warren H.S., Cuenca A.G., Mindrinos M.N., Baker H.V., Xu W., Richards D.R., McDonald-Smith G.P., Gao H., Hennessy L., et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. USA 2013, 110:3507-3512. Inflammation and Host Response to Injury, Large Scale Collaborative Research Program.
38. Sommer C.A., Sommer A.G., Longmire T.A., Christodoulou C., Thomas D.D., Gostissa M., Alt F.W., Murphy G.J., Kotton D.N., Mostoslavsky G. Excision of reprogramming transgenes improves the differentiation potential of iPS cells generated with a single excisable vector. Stem Cells 2010, 28:64-74.
39. Steinert A.F., Rackwitz L., Gilbert F., Nöth U., Tuan R.S. Concise review: the clinical application of mesenchymal stem cells for musculoskeletal regeneration: current status and perspectives. Stem Cells Transl. Med. 2012, 1:237-247.
40. Tang C., Lee A.S., Volkmer J.P., Sahoo D., Nag D., Mosley A.R., Inlay M.A., Ardehali R., Chavez S.L., Pera R.R., et al. An antibody against SSEA-5 glycan on human pluripotent stem cells enables removal of teratoma-forming cells. Nat. Biotechnol. 2011, 29:829-834.
41. Tang C., Weissman I.L., Drukker M. Immunogenicity of in vitro maintained and matured populations: potential barriers to engraftment of human pluripotent stem cell derivatives. Methods Mol. Biol. 2013, 1029:17-31.
42. Tesar P.J., Chenoweth J.G., Brook F.A., Davies T.J., Evans E.P., Mack D.L., Gardner R.L., McKay R.D. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 2007, 448:196-199.
43. Villa-Diaz L.G., Brown S.E., Liu Y., Ross A.M., Lahann J., Parent J.M., Krebsbach P.H. Derivation of mesenchymal stem cells from human induced pluripotent stem cells cultured on synthetic substrates. Stem Cells 2012, 30:1174-1181.
44. Vodyanik M.A., Yu J., Zhang X., Tian S., Stewart R., Thomson J.A., Slukvin I.I. A mesoderm-derived precursor for mesenchymal stem and endothelial cells. Cell Stem Cell 2010, 7:718-729.
45. Wu C., Jares A., Winkler T., Xie J., Metais J.Y., Dunbar C.E. High efficiency restriction enzyme-free linear amplification-mediated polymerase chain reaction approach for tracking lentiviral integration sites does not abrogate retrieval bias. Hum. Gene Ther. 2013, 24:38-47.
46. Zhao T., Zhang Z.N., Rong Z., Xu Y. Immunogenicity of induced pluripotent stem cells. Nature 2011, 474:212-215.
47. Zhong B., Watts K.L., Gori J.L., Wohlfahrt M.E., Enssle J., Adair J.E., Kiem H.P. Safeguarding nonhuman primate iPS cells with suicide genes. Mol. Ther. 2011, 19:1667-1675.