A virus-free poly-promoter vector induces pluripotency in quiescent bovine cells under chemically defined conditions of dual kinase inhibition

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Huang, Ben ^a   Li, Tong ^a,b   Alonso Gonzalez, Lucia ^c   Gorre, Ruben ^d   Keatley, Sarah ^a   Green, Andria ^a   Turner, Pavla ^a   Kallingappa, Prasanna Kumar ^a   Verma, Vinod ^e   Oback, Björn ^a  

^a RUAKURA RESEARCH CENTRE   (New Zealand)

^b GUANGXI UNIVERSITY   (China)

^c UNIVERSITY OF OTAGO   (New Zealand)

^d Trenzyme GmbH   (Germany)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; CELL PROTEIN; GLYCOGEN SYNTHASE KINASE 3; KRUPPEL LIKE FACTOR 4; LEUKEMIA INHIBITORY FACTOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN DPPA3; PROTEIN ZFP42; STAGE SPECIFIC EMBRYO ANTIGEN 3; STAGE SPECIFIC EMBRYO ANTIGEN 4; SUPPRESSOR OF CYTOKINE SIGNALING 3; TELOMERASE; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; UVOMORULIN; BIOLOGICAL MARKER; PROTEIN KINASE INHIBITOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CONTROLLED STUDY; CULTURE MEDIUM; DNA SEQUENCE; DNA SYNTHESIS; EMBRYO; EMBRYONIC STEM CELL; ENZYME ACTIVITY; ENZYME INHIBITION; EXPRESSION VECTOR; FEMALE; FETUS; HUMAN; HUMAN CELL; HUMAN VERSUS ANIMAL COMPARISON; IN VITRO STUDY; KARYOTYPE; MALE; MOUSE; NON INVASIVE PROCEDURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; CATTLE; CELL LINE; CYTOLOGY; DRUG EFFECT; GENE VECTOR; GENETICS; METABOLISM; PATHOLOGY; PROMOTER REGION; TERATOMA;

ANIMALIA; BOVINAE;

ANIMALS; BIOLOGICAL MARKERS; CATTLE; CELL DIFFERENTIATION; CELL LINE; FEMALE; GENETIC VECTORS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; LEUKEMIA INHIBITORY FACTOR; MALE; MICE; PROMOTER REGIONS, GENETIC; PROTEIN KINASE INHIBITORS; TERATOMA;

EID: 80052425146     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024501     Document Type: Article

References (90)

1. Evans MJ, Kaufman MH, (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292: 154-156.
2. Martin GR, (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.
3. Kanatsu-Shinohara M, Inoue K, Lee J, Yoshimoto M, Ogonuki N, et al. (2004) Generation of pluripotent stem cells from neonatal mouse testis. Cell 119: 1001-1012.
4. Brons IG, Smithers LE, Trotter MW, Rugg-Gunn P, Sun B, et al. (2007) Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448: 191-195.
5. Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, et al. (2007) New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448: 196-199.
6. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, et al. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956.
7. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, et al. (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38: 431-440.
8. Wang J, Rao S, Chu J, Shen X, Levasseur DN, et al. (2006) A protein interaction network for pluripotency of embryonic stem cells. Nature 444: 364-368.
9. Nichols J, Smith A, (2009) Naive and primed pluripotent states. Cell Stem Cell 4: 487-492.
10. Guo G, Yang J, Nichols J, Hall JS, Eyres I, et al. (2009) Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 136: 1063-1069.
11. Hanna J, Cheng AW, Saha K, Kim J, Lengner CJ, et al. (2010) Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc Natl Acad Sci U S A 107: 9222-9227.
12. Yang J, van Oosten AL, Theunissen TW, Guo G, Silva JC, et al. (2010) Stat3 activation is limiting for reprogramming to ground state pluripotency. Cell Stem Cell 7: 319-328.
13. Bradley A, Evans M, Kaufman MH, Robertson E, (1984) Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 309: 255-256.
14. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, et al. (2008) The ground state of embryonic stem cell self-renewal. Nature 453: 519-523.
15. Silva J, Nichols J, Theunissen TW, Guo G, van Oosten AL, et al. (2009) Nanog is the gateway to the pluripotent ground state. Cell 138: 722-737.
16. Guo G, Smith A, (2010) A genome-wide screen in EpiSCs identifies Nr5a nuclear receptors as potent inducers of ground state pluripotency. Development 137: 3185-3192.
17. Takahashi K, Yamanaka S, (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
18. Blelloch R, Venere M, Yen J, Ramalho-Santos M, (2007) Generation of induced pluripotent stem cells in the absence of drug selection. Cell Stem Cell 1: 245-247.
19. Maherali N, Sridharan R, Xie W, Utikal J, Eminli S, et al. (2007) Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 1: 55-70.
20. Meissner A, Wernig M, Jaenisch R, (2007) Direct reprogramming of genetically unmodified fibroblasts into pluripotent stem cells. Nat Biotechnol 25: 1177-1181.
21. Okita K, Ichisaka T, Yamanaka S, (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448: 313-317.
22. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, et al. (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448: 318-324.
23. Stadtfeld M, Apostolou E, Akutsu H, Fukuda A, Follett P, et al. (2010) Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature 465: 175-181.
24. Mikkelsen TS, Hanna J, Zhang X, Ku M, Wernig M, et al. (2008) Dissecting direct reprogramming through integrative genomic analysis. Nature 454: 49-55.
25. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560.
26. Hanna J, Markoulaki S, Schorderet P, Carey BW, Beard C, et al. (2008) Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency. Cell 133: 250-264.
27. Kim JB, Zaehres H, Wu G, Gentile L, Ko K, et al. (2008) Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature 454: 646-650.
28. Boland MJ, Hazen JL, Nazor KL, Rodriguez AR, Gifford W, et al. (2009) Adult mice generated from induced pluripotent stem cells. Nature 461: 91-94.
29. Kang L, Wang J, Zhang Y, Kou Z, Gao S, (2009) iPS cells can support full-term development of tetraploid blastocyst-complemented embryos. Cell Stem Cell 5: 135-138.
30. Zhao XY, Li W, Lv Z, Liu L, Tong M, et al. (2009) iPS cells produce viable mice through tetraploid complementation. Nature 461: 86-90.
31. Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder JC, (1993) Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc Natl Acad Sci U S A 90: 8424-8428.
32. Li W, Wei W, Zhu S, Zhu J, Shi Y, et al. (2009) Generation of rat and human induced pluripotent stem cells by combining genetic reprogramming and chemical inhibitors. Cell Stem Cell 4: 16-19.
33. Liao J, Cui C, Chen S, Ren J, Chen J, et al. (2009) Generation of induced pluripotent stem cell lines from adult rat cells. Cell Stem Cell 4: 11-15.
34. Esteban MA, Xu J, Yang J, Peng M, Qin D, et al. (2009) Generation of induced pluripotent stem cell lines from Tibetan miniature pig. J Biol Chem 284: 17634-17640.
35. Wu Z, Chen J, Ren J, Bao L, Liao J, et al. (2009) Generation of pig induced pluripotent stem cells with a drug-inducible system. J Mol Cell Biol 1: 46-54.
36. Bao L, He L, Chen J, Wu Z, Liao J, et al. (2011) Reprogramming of ovine adult fibroblasts to pluripotency via drug-inducible expression of defined factors. Cell Res 21: 600-608.
37. Nagy K, Sung HK, Zhang P, Laflamme S, Vincent P, et al. (2011) Induced Pluripotent Stem Cell Lines Derived from Equine Fibroblasts. Stem Cell Rev 7: 693-702.
38. Honda A, Hirose M, Hatori M, Matoba S, Miyoshi H, et al. (2010) Generation of induced pluripotent stem cells in rabbits: potential experimental models for human regenerative medicine. J Biol Chem 285: 31362-31369.
39. Liu H, Zhu F, Yong J, Zhang P, Hou P, et al. (2008) Generation of induced pluripotent stem cells from adult rhesus monkey fibroblasts. Cell Stem Cell 3: 587-590.
40. Tomioka I, Maeda T, Shimada H, Kawai K, Okada Y, et al. (2010) Generating induced pluripotent stem cells from common marmoset (Callithrix jacchus) fetal liver cells using defined factors, including Lin28. Genes Cells 15: 959-969.
41. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
42. Heng JC, Feng B, Han J, Jiang J, Kraus P, et al. (2010) The nuclear receptor Nr5a2 can replace Oct4 in the reprogramming of murine somatic cells to pluripotent cells. Cell Stem Cell 6: 167-174.
43. Brambrink T, Foreman R, Welstead GG, Lengner CJ, Wernig M, et al. (2008) Sequential expression of pluripotency markers during direct reprogramming of mouse somatic cells. Cell Stem Cell 2: 151-159.
44. Kaji K, Norrby K, Paca A, Mileikovsky M, Mohseni P, et al. (2009) Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature 458: 771-775.
45. Stadtfeld M, Nagaya M, Utikal J, Weir G, Hochedlinger K, (2008) Induced pluripotent stem cells generated without viral integration. Science 322: 945-949.
46. Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S, (2008) Generation of mouse induced pluripotent stem cells without viral vectors. Science 322: 949-953.
47. Soldner F, Hockemeyer D, Beard C, Gao Q, Bell GW, et al. (2009) Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 136: 964-977.
48. Yusa K, Rad R, Takeda J, Bradley A, (2009) Generation of transgene-free induced pluripotent mouse stem cells by the piggyBac transposon. Nat Methods 6: 363-369.
49. Woltjen K, Michael IP, Mohseni P, Desai R, Mileikovsky M, et al. (2009) piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458: 766-770.
50. Silva J, Barrandon O, Nichols J, Kawaguchi J, Theunissen TW, et al. (2008) Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS Biol 6: e253.
51. Buehr M, Meek S, Blair K, Yang J, Ure J, et al. (2008) Capture of authentic embryonic stem cells from rat blastocysts. Cell 135: 1287-1298.
52. Li P, Tong C, Mehrian-Shai R, Jia L, Wu N, et al. (2008) Germline competent embryonic stem cells derived from rat blastocysts. Cell 135: 1299-1310.
53. Keefer CL, Pant D, Blomberg L, Talbot NC, (2007) Challenges and prospects for the establishment of embryonic stem cell lines of domesticated ungulates. Anim Reprod Sci 98: 147-168.
54. Renard JP, Maruotti J, Jouneau A, Vignon X, (2007) Nuclear reprogramming and pluripotency of embryonic cells: Application to the isolation of embryonic stem cells in farm animals. Theriogenology 68 (Suppl 1): S196-205.
55. Oback B, Wells D, (2002) Practical Aspects of Donor Cell Selection for Nuclear Cloning. Cloning Stem Cells 4: 169-175.
56. Doerfler W, Schubbert R, Heller H, Kammer C, Hilger-Eversheim K, et al. (1997) Integration of foreign DNA and its consequences in mammalian systems. Trends Biotechnol 15: 297-301.
57. Fusaki N, Ban H, Nishiyama A, Saeki K, Hasegawa M, (2009) 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. Proc Jpn Acad Ser B Phys Biol Sci 85: 348-362.
58. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, et al. (2009) Human induced pluripotent stem cells free of vector and transgene sequences. Science 324: 797-801.
59. Thomas CE, Ehrhardt A, Kay MA, (2003) Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet 4: 346-358.
60. Carey BW, Markoulaki S, Hanna J, Saha K, Gao Q, et al. (2009) Reprogramming of murine and human somatic cells using a single polycistronic vector. Proc Natl Acad Sci U S A 106: 157-162.
61. Gonzalez F, Barragan Monasterio M, Tiscornia G, Montserrat Pulido N, Vassena R, et al. (2009) Generation of mouse-induced pluripotent stem cells by transient expression of a single nonviral polycistronic vector. Proc Natl Acad Sci U S A 106: 8918-8922.
62. Smith ZD, Nachman I, Regev A, Meissner A, (2010) Dynamic single-cell imaging of direct reprogramming reveals an early specifying event. Nat Biotechnol 28: 521-526.
63. Berstine EG, Hooper ML, Grandchamp S, Ephrussi B, (1973) Alkaline phosphatase activity in mouse teratoma. Proc Natl Acad Sci U S A 70: 3899-3903.
64. Chan EM, Ratanasirintrawoot S, Park IH, Manos PD, Loh YH, et al. (2009) Live cell imaging distinguishes bona fide human iPS cells from partially reprogrammed cells. Nat Biotechnol 27: 1033-1037.
65. Meilinger D, Fellinger K, Bultmann S, Rothbauer U, Bonapace IM, et al. (2009) Np95 interacts with de novo DNA methyltransferases, Dnmt3a and Dnmt3b, and mediates epigenetic silencing of the viral CMV promoter in embryonic stem cells. EMBO Rep 10: 1259-1264.
66. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, et al. (1994) Specific association of human telomerase activity with immortal cells and cancer. Science 266: 2011-2015.
67. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, et al. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
68. Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, et al. (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279: 349-352.
69. Araki R, Jincho Y, Hoki Y, Nakamura M, Tamura C, et al. (2010) Conversion of ancestral fibroblasts to induced pluripotent stem cells. Stem Cells 28: 213-220.
70. Ruiz S, Panopoulos AD, Herrerias A, Bissig KD, Lutz M, et al. (2011) A high proliferation rate is required for cell reprogramming and maintenance of human embryonic stem cell identity. Curr Biol 21: 45-52.
71. Baxter J, Sauer S, Peters A, John R, Williams R, et al. (2004) Histone hypomethylation is an indicator of epigenetic plasticity in quiescent lymphocytes. EMBO J 23: 4462-4472.
72. Wells DN, Laible G, Tucker FC, Miller AL, Oliver JE, et al. (2003) Coordination between donor cell type and cell cycle stage improves nuclear cloning efficiency in cattle. Theriogenology 59: 45-59.
73. Oback B, (2009) Cloning from stem cells: different lineages, different species, same story. Reprod Fertil Dev 21: 83-94.
74. Oback B, (2010) Cloning from stem cells of different developmental potency. Encyclopedia of Biotechnology in Agriculture and Food pp. 167-170.
75. Buecker C, Chen HH, Polo JM, Daheron L, Bu L, et al. (2010) A murine ESC-like state facilitates transgenesis and homologous recombination in human pluripotent stem cells. Cell Stem Cell 6: 535-546.
76. Hockemeyer D, Soldner F, Beard C, Gao Q, Mitalipova M, et al. (2009) Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat Biotechnol 27: 851-857.
77. Zou J, Maeder ML, Mali P, Pruett-Miller SM, Thibodeau-Beganny S, et al. (2009) Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell 5: 97-110.
78. Trees AJ, Graham SP, Renz A, Bianco AE, Tanya V, (2000) Onchocerca ochengi infections in cattle as a model for human onchocerciasis: recent developments. Parasitology 120 (Suppl): S133-142.
79. Skvorak KJ, (2009) Animal models of maple syrup urine disease. J Inherit Metab Dis 32: 229-246.
80. Roberts S, Menage J, Sivan S, Urban JP, (2008) Bovine explant model of degeneration of the intervertebral disc. BMC Musculoskelet Disord 9: 24.
81. Lee B, Dennis JA, Healy PJ, Mull B, Pastore L, et al. (1999) Hepatocyte gene therapy in a large animal: a neonatal bovine model of citrullinemia. Proc Natl Acad Sci U S A 96: 3981-3986.
82. Dharmadhikari AS, Nardell EA, (2008) What animal models teach humans about tuberculosis. Am J Respir Cell Mol Biol 39: 503-508.
83. Tchakoute VL, Graham SP, Jensen SA, Makepeace BL, Nfon CK, et al. (2006) In a bovine model of onchocerciasis, protective immunity exists naturally, is absent in drug-cured hosts, and is induced by vaccination. Proc Natl Acad Sci U S A 103: 5971-5976.
84. Allen JE, Adjei O, Bain O, Hoerauf A, Hoffmann WH, et al. (2008) Of mice, cattle, and humans: the immunology and treatment of river blindness. PLoS Negl Trop Dis 2: e217.
85. Oback B, Wells DN, (2003) Cloning cattle. Cloning Stem Cells 5: 243-256.
86. Wells DN, Misica PM, Tervit HR, (1999) Production of cloned calves following nuclear transfer with cultured adult mural granulosa cells. Biol Reprod 60: 996-1005.
87. Oback B, Wiersema AT, Gaynor P, Laible G, Tucker FC, et al. (2003) Cloned cattle derived from a novel zona-free embryo reconstruction system. Cloning Stem Cells 5: 3-12.
88. Berg DK, Smith CS, Pearton DJ, Wells DN, Broadhurst R, et al. (2011) Trophectoderm lineage determination in cattle. Dev Cell 20: 244-255.
89. Misica-Turner PM, Oback FC, Eichenlaub M, Wells DN, Oback B, (2007) Aggregating embryonic but not somatic nuclear transfer embryos increases cloning efficiency in cattle. Biol Reprod 76: 268-278.
90. Hentze H, Soong PL, Wang ST, Phillips BW, Putti TC, et al. (2009) Teratoma formation by human embryonic stem cells: evaluation of essential parameters for future safety studies. Stem Cell Res 2: 198-210.