Generation and characterization of transgene-free human induced pluripotent stem cells and conversion to putative clinical-grade status

Stem Cell Research and Therapy

Volumn 4, Issue 4, 2013, Pages

  Awe, Jason P ^a   Lee, Patrick C ^a   Ramathal, Cyril ^b   Vega Crespo, Agustin ^a   Durruthy Durruthy, Jens ^b   Cooper, Aaron ^c   Karumbayaram, Saravanan ^d   Lowry, William E ^d   Clark, Amander T ^d   Zack, Jerome A ^d   Sebastiano, Vittorio ^b   Kohn, Donald B ^d   Pyle, April D ^d   Martin, Martin G ^e   Lipshutz, Gerald S ^f   Phelps, Patricia E ^c   Pera, Renee A Reijo ^b   Byrne, James A ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Immunology and Molecular Genetics ^*  (United States)

^d Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research   (United States)

^e Division of Gastroenterology   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; LENTIVIRUS VECTOR; POLYCISTRONIC STEM CELL CASSETTE; UNCLASSIFIED DRUG;

'PRPF39 GENE; ADULT; ARTICLE; CELL DIFFERENTIATION; CELL TYPE; CLINICAL PROTOCOL; CONTROLLED STUDY; DNA MODIFICATION; EMBRYONIC STEM CELL; FOOD AND DRUG ADMINISTRATION; GENE EXPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; GOOD MANUFACTURING PRACTICE; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; INTRON; KARYOTYPING; LIVER CELL; OLIGODENDROGLIA; PLURIPOTENT STEM CELL; PRACTICE GUIDELINE; PRIORITY JOURNAL; PRPF39 GENE; RNA SPLICING; SKIN FIBROBLAST; TERATOMA; TRANSGENE; ANIMAL; GENOMICS; METABOLISM; MOUSE; NUCLEAR REPROGRAMMING;

ANIMALS; CELL DIFFERENTIATION; CELLULAR REPROGRAMMING; GENE EXPRESSION; GENOMICS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; TRANSGENES;

EID: 84880935695     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/scrt246     Document Type: Article

References (57)

1. Induced pluripotent stem cell lines derived from human somatic cells. 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, Science 2007 318 1917 1920 10.1126/science.1151526 18029452
2. Generation of isogenic pluripotent stem cells. Byrne JA, Hum Mol Genet 2008 17 37 R41 10.1093/hmg/ddn053 18632695
3. Nuclear reprogramming and the current challenges in advancing personalized pluripotent stem cell-based therapies. Byrne J, Gene Ther Regul 2013 7 1230002
4. Advances in reprogramming somatic cells to induced pluripotent stem cells. Patel M, Yang S, Stem Cell Rev 2010 6 367 380 10.1007/s12015-010-9123-8 20336395
5. Generation of iPS cells using defined factors linked via the self-cleaving 2A sequences in a single open reading frame. Shao L, Feng W, Sun Y, Bai H, Liu J, Currie C, Kim J, Gama R, Wang Z, Qian Z, Liaw L, Wu WS, Cell Res 2009 19 296 306 10.1038/cr.2009.20 19238173
6. Generation of germline-competent induced pluripotent stem cells. Okita K, Ichisaka T, Yamanaka S, Nature 2007 448 313 317 10.1038/nature05934 17554338 (Pubitemid 47080336)
7. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, McCormack MP, Wulffraat N, Leboulch P, Lim A, Osborne CS, Pawliuk R, Morillon E, Sorensen R, Forster A, Fraser P, Cohen JI, de Saint BG, Alexander I, Wintergerst U, Frebourg T, Aurias A, Stoppa-Lyonnet D, Romana S, Radford-Weiss I, Gross F, Valensi F, Delabesse E, Macintyre E, Sigaux F, Soulier J, Leiva LE, Wissler M, et al. Science 2003 302 415 419 10.1126/science.1088547 14564000 (Pubitemid 37296260)
8. Human induced pluripotent stem cells free of vector and transgene sequences. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, Slukvin II, Thomson JA, Science 2009 324 797 801 10.1126/science.1172482 19325077
9. A nonviral minicircle vector for deriving human iPS cells. Jia F, Wilson KD, Sun N, Gupta DM, Huang M, Li Z, Panetta NJ, Chen ZY, Robbins RC, Kay MA, Longaker MT, Wu JC, Nat Methods 2010 7 197 199 10.1038/nmeth.1426 20139967
10. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Anokye-Danso F, Trivedi CM, Juhr D, Gupta M, Cui Z, Tian Y, Zhang Y, Yang W, Gruber PJ, Epstein JA, Morrisey EE, Cell Stem Cell 2011 8 376 388 10.1016/j.stem.2011.03.001 21474102
11. Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Miyoshi N, Ishii H, Nagano H, Haraguchi N, Dewi DL, Kano Y, Nishikawa S, Tanemura M, Mimori K, Tanaka F, Saito T, Nishimura J, Takemasa I, Mizushima T, Ikeda M, Yamamoto H, Sekimoto M, Doki Y, Mori M, Cell Stem Cell 2011 8 633 638 10.1016/j.stem.2011.05.001 21620789
12. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Kim D, Kim CH, Moon JI, Chung YG, Chang MY, Han BS, Ko S, Yang E, Cha KY, Lanza R, Kim KS, Cell Stem Cell 2009 4 472 476 10.1016/j.stem.2009.05.005 19481515
13. Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Fusaki N, Ban H, Nishiyama A, Saeki K, Hasegawa M, Proc Jpn Acad Ser B Phys Biol Sci 2009 85 348 362 10.2183/pjab.85.348 19838014
14. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Warren L, Manos PD, Ahfeldt T, Loh YH, Li H, Lau F, Ebina W, Mandal PK, Smith ZD, Meissner A, Daley GQ, Brack AS, Collins JJ, Cowan C, Schlaeger TM, Rossi DJ, Cell Stem Cell 2010 7 618 630 10.1016/j.stem.2010.08.012 20888316
15. Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Sommer CA, Stadtfeld M, Murphy GJ, Hochedlinger K, Kotton DN, Mostoslavsky G, Stem Cells 2009 27 543 549 10.1634/stemcells.2008-1075 19096035
16. Generation of transgene-free lung disease-specific human induced pluripotent stem cells using a single excisable lentiviral stem cell cassette. Somers A, Jean JC, Sommer CA, Omari A, Ford CC, Mills JA, Ying L, Sommer AG, Jean JM, Smith BW, Lafyatis R, Demierre MF, Weiss DJ, French DL, Gadue P, Murphy GJ, Mostoslavsky G, Kotton DN, Stem Cells 2010 28 1728 1740 10.1002/stem.495 20715179
17. Methods for making induced pluripotent stem cells: reprogramming a la carte. Gonzalez F, Boue S, Izpisua Belmonte JC, Nat Rev Genet 2011 12 231 242 21339765
18. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S, Cell 2007 131 861 872 10.1016/j.cell.2007.11.019 18035408 (Pubitemid 350138099)
19. The evolving field of induced pluripotency: recent progress and future challenges. Sommer CA, Mostoslavsky G, J Cell Physiol 2013 228 267 275 10.1002/jcp.24155 22767332
20. Excision of reprogramming transgenes improves the differentiation potential of iPS cells generated with a single excisable vector. Sommer CA, Sommer AG, Longmire TA, Christodoulou C, Thomas DD, Gostissa M, Alt FW, Murphy GJ, Kotton DN, Mostoslavsky G, Stem Cells 2010 28 64 74 19904830
21. From skin biopsy to neurons through a pluripotent intermediate under good manufacturing practice protocols. Karumbayaram S, Lee P, Azghadi SF, Cooper AR, Patterson M, Kohn DB, Pyle A, Clark A, Byrne J, Zack JA, Plath K, Lowry WE, Stem Cells Transl Med 2012 1 36 43 10.5966/sctm.2011-0001 23197638
22. Comparative study of human-induced pluripotent stem cells derived from bone marrow cells, hair keratinocytes, and skin fibroblasts. Streckfuss-Bomeke K, Wolf F, Azizian A, Stauske M, Tiburcy M, Wagner S, Hubscher D, Dressel R, Chen S, Jende J, Wulf G, Lorenz V, Schon MP, Maier LS, Zimmermann WH, Hasenfuss G, Guan K, Eur Heart J 2012 12 12
23. Reprogramming of T cells from human peripheral blood. Loh YH, Hartung O, Li H, Guo C, Sahalie JM, Manos PD, Urbach A, Heffner GC, Grskovic M, Vigneault F, Lensch MW, Park IH, Agarwal S, Church GM, Collins JJ, Irion S, Daley GQ, Cell Stem Cell 2010 7 15 19 10.1016/j.stem.2010.06.004 20621044
24. The first reported generation of several induced pluripotent stem cell lines from homozygous and heterozygous Huntington's disease patients demonstrates mutation related enhanced lysosomal activity. Camnasio S, Carri AD, Lombardo A, Grad I, Mariotti C, Castucci A, Rozell B, Riso PL, Castiglioni V, Zuccato C, Rochon C, Takashima Y, Diaferia G, Biunno I, Gellera C, Jaconi M, Smith A, Hovatta O, Naldini L, Di Donato S, Feki A, Cattaneo E, Neurobiol Dis 2012 46 41 51 10.1016/j.nbd.2011.12.042 22405424
25. Derivation and cardiomyocyte differentiation of induced pluripotent stem cells from heart failure patients. Zwi-Dantsis L, Huber I, Habib M, Winterstern A, Gepstein A, Arbel G, Gepstein L, Eur Heart J 2012 22 22
26. Induced pluripotent stem cells: a novel frontier in the study of human primary immunodeficiencies. Pessach IM, Ordovas-Montanes J, Zhang SY, Casanova JL, Giliani S, Gennery AR, Al-Herz W, Manos PD, Schlaeger TM, Park IH, Rucci F, Agarwal S, Mostoslavsky G, Daley GQ, Notarangelo LD, J Allergy Clin Immunol 2011 127 1400 1407 e4 10.1016/j.jaci.2010.11.008 21185069
27. Induced pluripotent stem cells from hair follicles as a cellular model for neurodevelopmental disorders. Petit I, Kesner NS, Karry R, Robicsek O, Aberdam E, Muller FJ, Aberdam D, Ben-Shachar D, Stem Cell Res 2012 8 134 140 10.1016/j.scr.2011.09.003 22099027
28. HIV-1 integration in the human genome favors active genes and local hotspots. Schroder AR, Shinn P, Chen H, Berry C, Ecker JR, Bushman F, Cell 2002 110 521 529 10.1016/S0092-8674(02)00864-4 12202041 (Pubitemid 35232295)
29. Analysis of self-inactivating lentiviral vector integration sites and flanking gene expression in human peripheral blood progenitor cells after alkylator chemotherapy. Grund N, Maier P, Giordano FA, Appelt JU, Zucknick M, Li L, Wenz F, Zeller WJ, Fruehauf S, Allgayer H, Laufs S, Hum Gene Ther 2010 21 943 956 10.1089/hum.2009.116 20210626
30. Genomic safe harbors permit high beta-globin transgene expression in thalassemia induced pluripotent stem cells. Papapetrou EP, Lee G, Malani N, Setty M, Riviere I, Tirunagari LM, Kadota K, Roth SL, Giardina P, Viale A, Leslie C, Bushman FD, Studer L, Sadelain M, Nat Biotechnol 2011 29 73 78 10.1038/nbt.1717 21151124
31. From skin biopsy to neurons through a pluripotent intermediate under good manufacturing practice protocols. Karumbayaram S, Lee P, Azghadi SF, Cooper AR, Patterson M, Kohn DB, Pyle A, Clark A, Byrne J, Zack JA, Stem Cells Translational Med 2012 1 36 43 10.5966/sctm.2011-0001
32. Enhanced generation of induced pluripotent stem cells from a subpopulation of human fibroblasts. Byrne JA, Nguyen HN, Reijo Pera RA, PLoS One 2009 4 7118 10.1371/journal.pone.0007118 19774082
33. Genome-wide high-throughput integrome analyses by nrLAM-PCR and next-generation sequencing. Paruzynski A, Arens A, Gabriel R, Bartholomae CC, Scholz S, Wang W, Wolf S, Glimm H, Schmidt M, von Kalle C, Nat Protoc 2010 5 1379 1395 10.1038/nprot.2010.87 20671722
34. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Langmead B, Trapnell C, Pop M, Salzberg SL, Genome Biol 2009 10 25 10.1186/gb-2009-10-3-r25 19261174
35. Human skin cells that express stage-specific embryonic antigen 3 associate with dermal tissue regeneration. Crespo AV, Awe JP, Pera RR, Byrne JA, BioResearch Open Access 2012 1 25 33 10.1089/biores.2012.0204 23514702
36. Gene Expression Omnibus http://www.ncbi.nlm.nih.gov/geo
37. ApE http://biologylabs.utah.edu/jorgensen/wayned/ape
38. Human oligodendrocytes derived from embryonic stem cells: effect of noggin on phenotypic differentiation in vitro and on myelination in vivo. Izrael M, Zhang P, Kaufman R, Shinder V, Ella R, Amit M, Itskovitz-Eldor J, Chebath J, Revel M, Mol Cell Neurosci 2007 34 310 323 10.1016/j.mcn.2006.11.008 17196394 (Pubitemid 46330036)
39. Mouse olfactory ensheathing glia enhance axon outgrowth on a myelin substrate in vitro. Runyan SA, Phelps PE, Exp Neurol 2009 216 95 104 10.1016/j.expneurol.2008.11.015 19100263
40. Ascorbic acid enhances the cardiac differentiation of induced pluripotent stem cells through promoting the proliferation of cardiac progenitor cells. Cao N, Liu Z, Chen Z, Wang J, Chen T, Zhao X, Ma Y, Qin L, Kang J, Wei B, Wang L, Jin Y, Yang HT, Cell Res 2012 22 219 236 10.1038/cr.2011.195 22143566
41. Long-term self-renewal and directed differentiation of human embryonic stem cells in chemically defined conditions. Yao S, Chen S, Clark J, Hao E, Beattie GM, Hayek A, Ding S, Proc Natl Acad Sci U S A 2006 103 6907 6912 10.1073/pnas.0602280103 16632596
42. Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Song Z, Cai J, Liu Y, Zhao D, Yong J, Duo S, Song X, Guo Y, Zhao Y, Qin H, Yin X, Wu C, Che J, Lu S, Ding M, Deng H, Cell Res 2009 19 1233 1242 10.1038/cr.2009.107 19736565
43. Defining the nature of human pluripotent stem cell progeny. Patterson M, Chan DN, Ha I, Case D, Cui Y, Van Handel B, Mikkola HK, Lowry WE, Cell Res 2012 22 178 193 10.1038/cr.2011.133 21844894
44. Lentiviral vector transduction of NOD/SCID repopulating cells results in multiple vector integrations per transduced cell: risk of insertional mutagenesis. Woods NB, Muessig A, Schmidt M, Flygare J, Olsson K, Salmon P, Trono D, von Kalle C, Karlsson S, Blood 2003 101 1284 1289 10.1182/blood-2002- 07-2238 12393514 (Pubitemid 36182497)
45. Functional consequences of PRPF39 on distant genes and cisplatin sensitivity. Stark AL, Delaney SM, Wheeler HE, Im HK, Dolan ME, Hum Mol Genet 2012 17 17
46. Schindler disease: the molecular lesion in the alpha-N- acetylgalactosaminidase gene that causes an infantile neuroaxonal dystrophy. Wang AM, Schindler D, Desnick R, J Clin Invest 1990 86 1752 1756 10.1172/JCI114901 2243144 (Pubitemid 20372630)
47. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Soldner F, Hockemeyer D, Beard C, Gao Q, Bell GW, Cook EG, Hargus G, Blak A, Cooper O, Mitalipova M, Isacson O, Jaenisch R, Cell 2009 136 964 977 10.1016/j.cell.2009.02.013 19269371
48. Experimental approaches for the generation of induced pluripotent stem cells. Sommer CA, Mostoslavsky G, Stem Cell Res Ther 2010 1 26 10.1186/scrt26 20699015
49. Differentiation of human oligodendrocytes from pluripotent stem cells. Hu BY, Du ZW, Zhang SC, Nat Protoc 2009 4 1614 1622 10.1038/nprot.2009.186 19834476
50. Human embryonic stem cells differentiate into oligodendrocytes in high purity and myelinate after spinal cord transplantation. Nistor GI, Totoiu MO, Haque N, Carpenter MK, Keirstead HS, Glia 2005 49 385 396 10.1002/glia.20127 15538751 (Pubitemid 40222916)
51. From skin biopsy to neurons through a pluripotent intermediate under good manufacturing practice protocols. Karumbayaram S, Lee P, Azghadi SF, Cooper AR, Patterson M, Kohn DB, Pyle A, Clark A, Byrne J, Zack JA, Plath K, Lowry WE, Stem Cells Trans Med 2012 1 36 43 10.5966/sctm.2011-0001
52. Sensitive and specific detection of the non-human sialic Acid N-glycolylneuraminic acid in human tissues and biotherapeutic products. Diaz SL, Padler-Karavani V, Ghaderi D, Hurtado-Ziola N, Yu H, Chen X, der Linden EC B-V, Varki A, Varki NM, PLoS One 2009 4 4241 10.1371/journal.pone.0004241 19156207
53. Human embryonic stem cells express an immunogenic nonhuman sialic acid. Martin MJ, Muotri A, Gage F, Varki A, Nat Med 2005 11 228 232 10.1038/nm1181 15685172 (Pubitemid 40321360)
54. Hematopoietic stem cell gene transfer in a tumor-prone mouse model uncovers low genotoxicity of lentiviral vector integration. Montini E, Cesana D, Schmidt M, Sanvito F, Ponzoni M, Bartholomae C, Sergi Sergi L, Benedicenti F, Ambrosi A, Di Serio C, Doglioni C, von Kalle C, Naldini L, Nat Biotechnol 2006 24 687 696 10.1038/nbt1216 16732270 (Pubitemid 43882120)
55. Woodchuck post-transcriptional element induces nuclear export of myotonic dystrophy 3′ untranslated region transcripts. Mastroyiannopoulos NP, Feldman ML, Uney JB, Mahadevan MS, Phylactou LA, EMBO Rep 2005 6 458 463 10.1038/sj.embor.7400390 15832171 (Pubitemid 40767079)
56. Transplanted oligodendrocytes and motoneuron progenitors generated from human embryonic stem cells promote locomotor recovery after spinal cord transection. Erceg S, Ronaghi M, Oria M, Rosello MG, Arago MA, Lopez MG, Radojevic I, Moreno-Manzano V, Rodriguez-Jimenez FJ, Bhattacharya SS, Cordoba J, Stojkovic M, Stem Cells 2010 28 1541 1549 10.1002/stem.489 20665739
57. Geron Receives FDA Clearance to begin World's First Human Clinical Trial of Embryonic Stem Cell-based Therapy http://ir.geron.com/phoenix.zhtml?c= 67323&p=irol-newsArticle&ID=1636192&highlight