Advertisement

Pluripotent Stem Cell Banks

  • Begoña Aran
  • Ángel Raya
  • Anna Veiga
Chapter

Abstract

 Embryonic stem cells (ESCs) are pluripotent stem cells that can be obtained from the inner cell mass (ICM) of blastocyst-stage pre-implantation embryos. The first lines of human ESC (hESC) were derived by Thomson et al. in 1998. These cells can be indefinitely cultured in vitro and differentiated into different cell types. These cell lines constitute an excellent source of cells for the study of human genetics and gene expression patterns and as a tool to understand the events that take place during human embryo development. These cell lines can also be useful for drug screening and for the disease modelling. In 2006, Takahashi and Yamanaka first introduced the technology of induced reprogramming to pluripotency in the mouse and later in human cells. These induced pluripotent stem cells (iPSCs) are generated through the reprogramming of somatic cells back to an embryonic-like state. The reprogramming process is induced by the addition of exogenous reprogramming factors. Human iPSC (hiPSC) technology avoids the destruction of human embryos and the ethical debate involved. Moreover, patient-specific iPSC can be obtained by this technology providing unprecedented opportunities, not only in regenerative medicine but also in basic research as disease models, drug discovery and toxicology. The emerging demands of stem cell research and applications require the establishment and cooperation of centralized banks at a translational and even global scale. This will ensure the availability of high-quality hPSC using standardized state-of-the-art methods and strategies to deal with a heterogeneous regulatory, ethical and legal landscape. Furthermore, stem cell banks are essential for the distribution of cell lines among research centres, promoting scientific collaboration and facilitating widespread use of the cells for research and clinical applications.

Keywords

Embryonic stem cells Induced pluripotent stem cells Banking Clinical trials Disease models 

References

  1. 1.
    Aasen T, Raya A, Barrero MJ, Garreta E, Consiglio A, Gonzalez F et al (2008) Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol 26(11):1276–1284CrossRefGoogle Scholar
  2. 2.
    Allegrucci C, Young LE (2007) Differences between human embryonic stem cell lines. Hum Reprod Update 13(2):103–120PubMedCrossRefGoogle Scholar
  3. 3.
    Amit M, Shariki C, Margulets V, Itskovitz-Eldor J (2004) Feeder layer- and serum-free culture of human embryonic stem cells. Biol Reprod 70(3):837–845PubMedCrossRefGoogle Scholar
  4. 4.
    Andrews PW, Baker D, Benvinisty N, Miranda B, Bruce K, Brustle O et al (2015) Points to consider in the development of seed stocks of pluripotent stem cells for clinical applications: International Stem Cell Banking Initiative (ISCBI). Regen Med 10(2 Suppl):1–44PubMedCrossRefGoogle Scholar
  5. 5.
    Aran B, Rodriguez-Piza I, Raya A, Consiglio A, Munoz Y, Barri PN et al (2010) Derivation of human embryonic stem cells at the Center of Regenerative Medicine in Barcelona. In Vitro Cell Dev Biol Anim 46(3–4):356–366PubMedCrossRefGoogle Scholar
  6. 6.
    Avior Y, Sagi I, Benvenisty N (2016) Pluripotent stem cells in disease modelling and drug discovery. Nat Rev Mol Cell Biol 17(3):170–182PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Baghbaderani BA, Tian X, Neo BH, Burkall A, Dimezzo T, Sierra G et al (2015) cGMP-manufactured human induced pluripotent stem cells are available for pre-clinical and clinical applications. Stem Cell Rep 5(4):647–659CrossRefGoogle Scholar
  8. 8.
    Bellin M, Marchetto MC, Gage FH, Mummery CL (2012) Induced pluripotent stem cells: the new patient? Nat Rev Mol Cell Biol 13(11):713–726PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Bongso A, Fong CY, Ng SC, Ratnam S (1994) Isolation and culture of inner cell mass cells from human blastocysts. Hum Reprod 9(11):2110–2117PubMedCrossRefGoogle Scholar
  10. 10.
    Borstlap J, Luong MX, Rooke HM, Aran B, Damaschun A, Elstner A et al (2010) International stem cell registries. In Vitro Cell Dev Biol Anim 46(3–4):242–246PubMedCrossRefGoogle Scholar
  11. 11.
    Borstlap J, Stacey G, Kurtz A, Elstner A, Damaschun A, Aran B et al (2008) First evaluation of the European hESCreg. Nat Biotechnol 26(8):859–860PubMedCrossRefGoogle Scholar
  12. 12.
    Bradley JA, Bolton EM, Pedersen RA (2002) Stem cell medicine encounters the immune system. Nat Rev Immunol 2(11):859–871PubMedCrossRefGoogle Scholar
  13. 13.
    Brennand KJ, Simone A, Jou J, Gelboin-Burkhart C, Tran N, Sangar S et al (2011) Modelling schizophrenia using human induced pluripotent stem cells. Nature 473(7346):221–225PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Brito A, Russo FB, Muotri AR, Beltrao-Braga PCB. Autism spectrum disorders and disease modeling using stem cells. Cell Tissue Res 2018;371(1):153–60PubMedCrossRefGoogle Scholar
  15. 15.
    Chen AE, Egli D, Niakan K, Deng J, Akutsu H, Yamaki M et al (2009) Optimal timing of inner cell mass isolation increases the efficiency of human embryonic stem cell derivation and allows generation of sibling cell lines. Cell Stem Cell 4(2):103–106PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Chou BK, Mali P, Huang X, Ye Z, Dowey SN, Resar LM et al (2011) Efficient human iPS cell derivation by a non-integrating plasmid from blood cells with unique epigenetic and gene expression signatures. Cell Res 21(3):518–529PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Crook JM, Hei D, Stacey G (2010) The International Stem Cell Banking Initiative (ISCBI): raising standards to bank on. In Vitro Cell Dev Biol Anim 46(3–4):169–172PubMedCrossRefGoogle Scholar
  18. 18.
    Crook JM, Peura TT, Kravets L, Bosman AG, Buzzard JJ, Horne R et al (2007) The generation of six clinical-grade human embryonic stem cell lines. Cell Stem Cell 1(5):490–494PubMedCrossRefGoogle Scholar
  19. 19.
    De Sousa PA, Downie JM, Tye BJ, Bruce K, Dand P, Dhanjal S et al (2016) Development and production of good manufacturing practice grade human embryonic stem cell lines as source material for clinical application. Stem Cell Res 17(2):379–390PubMedCrossRefGoogle Scholar
  20. 20.
    Devine MJ, Ryten M, Vodicka P, Thomson AJ, Burdon T, Houlden H et al (2011) Parkinson's disease induced pluripotent stem cells with triplication of the alpha-synuclein locus. Nat Commun 2:440PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    DiStefano T, Chen HY, Panebianco C, Kaya KD, Brooks MJ, Gieser L, et al. Accelerated and Improved differentiation of retinal organoids from pluripotent stem cells in Rotating-Wall vessel bioreactors. Stem cell reports. 2018;10(1):300–13PubMedCrossRefGoogle Scholar
  22. 22.
    Dowey SN, Huang X, Chou BK, Ye Z, Cheng L (2012) Generation of integration-free human induced pluripotent stem cells from postnatal blood mononuclear cells by plasmid vector expression. Nat Protoc 7(11):2013–2021PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Drukker M, Katchman H, Katz G, Even-Tov Friedman S, Shezen E, Hornstein E et al (2006) Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells. Stem Cells 24(2):221–229PubMedCrossRefGoogle Scholar
  24. 24.
    Durruthy-Durruthy J, Briggs SF, Awe J, Ramathal CY, Karumbayaram S, Lee PC et al (2014) Rapid and efficient conversion of integration-free human induced pluripotent stem cells to GMP-grade culture conditions. PLoS One 9(4):e94231PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Ellerstrom C, Strehl R, Moya K, Andersson K, Bergh C, Lundin K et al (2006) Derivation of a xeno-free human embryonic stem cell line. Stem Cells 24(10):2170–2176PubMedCrossRefGoogle Scholar
  26. 26.
    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(8):348–362PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Genbacev O, Krtolica A, Zdravkovic T, Brunette E, Powell S, Nath A et al (2005) Serum-free derivation of human embryonic stem cell lines on human placental fibroblast feeders. Fertil Steril 83(5):1517–1529PubMedCrossRefGoogle Scholar
  28. 28.
    Giorgetti A, Montserrat N, Aasen T, Gonzalez F, Rodriguez-Piza I, Vassena R et al (2009) Generation of induced pluripotent stem cells from human cord blood using OCT4 and SOX2. Cell Stem Cell 5(4):353–357PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Gourraud PA, Hollenbach JA, Barnetche T, Single RM, Mack SJ (2012) Standard methods for the management of immunogenetic data. Methods Mol Biol 882:197–213PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Gymrek M, McGuire AL, Golan D, Halperin E, Erlich Y (2013) Identifying personal genomes by surname inference. Science 339(6117):321–324PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Haidet-Phillips AM, Hester ME, Miranda CJ, Meyer K, Braun L, Frakes A et al (2011) Astrocytes from familial and sporadic ALS patients are toxic to motor neurons. Nat Biotechnol 29(9):824–828PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Hasegawa K, Pomeroy JE, Pera MF (2010) Current technology for the derivation of pluripotent stem cell lines from human embryos. Cell Stem Cell 6(6):521–531PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Heins N, Englund MC, Sjoblom C, Dahl U, Tonning A, Bergh C et al (2004) Derivation, characterization, and differentiation of human embryonic stem cells. Stem Cells 22(3):367–376PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Imaizumi K, Nishishita N, Muramatsu M, Yamamoto T, Takenaka C, Kawamata S et al (2014) A simple and highly effective method for slow-freezing human pluripotent stem cells using dimethyl sulfoxide, hydroxyethyl starch and ethylene glycol. PLoS One 9(2):e88696PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    International Stem Cell Banking I (2009) Consensus guidance for banking and supply of human embryonic stem cell lines for research purposes. Stem Cell Rev 5(4):301–314CrossRefGoogle Scholar
  36. 36.
    International Stem Cell I, Adewumi O, Aflatoonian B, Ahrlund-Richter L, Amit M, Andrews PW et al (2007) Characterization of human embryonic stem cell lines by the international stem cell initiative. Nat Biotechnol 25(7):803–816CrossRefGoogle Scholar
  37. 37.
    Isasi RM, Knoppers BM (2009) Governing stem cell banks and registries: emerging issues. Stem Cell Res 3(2–3):96–105PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Kim D, Kim CH, Moon JI, Chung YG, Chang MY, Han BS et al (2009) Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 4(6):472–476PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Kim JH, Kurtz A, Yuan BZ, Zeng F, Lomax G, Loring JF et al (2017) Report of the international stem cell banking initiative workshop activity: current hurdles and progress in seed-stock banking of human pluripotent stem cells. Stem Cells Transl Med 6(11):1956–1962PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Kimbrel EA, Lanza R (2016) Pluripotent stem cells: the last 10 years. Regen Med 11(8):831–847PubMedCrossRefGoogle Scholar
  41. 41.
    Klimanskaya I, Chung Y, Becker S, Lu SJ, Lanza R (2006) Human embryonic stem cell lines derived from single blastomeres. Nature 444(7118):481–485PubMedCrossRefGoogle Scholar
  42. 42.
    Klimanskaya I, Chung Y, Meisner L, Johnson J, West MD, Lanza R (2005) Human embryonic stem cells derived without feeder cells. Lancet 365(9471):1636–1641PubMedCrossRefGoogle Scholar
  43. 43.
    Knoppers BM, Isasi R (2010) Stem cell banking: between traceability and identifiability. Genome Med 2(10):73PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Knoppers BM, Isasi R, Benvenisty N, Kim OJ, Lomax G, Morris C et al (2011) Publishing SNP genotypes of human embryonic stem cell lines: policy statement of the international stem cell forum ethics working party. Stem Cell Rev 7(3):482–484PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Kondo T, Asai M, Tsukita K, Kutoku Y, Ohsawa Y, Sunada Y et al (2013) Modeling Alzheimer’s disease with iPSCs reveals stress phenotypes associated with intracellular Abeta and differential drug responsiveness. Cell Stem Cell 12(4):487–496PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Kucia M, Halasa M, Wysoczynski M, Baskiewicz-Masiuk M, Moldenhawer S, Zuba-Surma E et al (2007) Morphological and molecular characterization of novel population of CXCR4+ SSEA-4+ Oct-4+ very small embryonic-like cells purified from human cord blood: preliminary report. Leukemia 21(2):297–303PubMedCrossRefGoogle Scholar
  47. 47.
    Lambert JC, Ibrahim-Verbaas CA, Harold D, Naj AC, Sims R, Bellenguez C et al (2013) Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer’s disease. Nat Genet 45(12):1452–1458PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Lancaster MA, Knoblich JA (2014) Generation of cerebral organoids from human pluripotent stem cells. Nat Protoc 9(10):2329–2340PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Laustriat D, Gide J, Peschanski M (2010) Human pluripotent stem cells in drug discovery and predictive toxicology. Biochem Soc Trans 38(4):1051–1057PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Lerou PH, Yabuuchi A, Huo H, Takeuchi A, Shea J, Cimini T et al (2008) Human embryonic stem cell derivation from poor-quality embryos. Nat Biotechnol 26(2):212–214PubMedCrossRefGoogle Scholar
  51. 51.
    Li T, Zhou C, Liu C, Mai Q, Zhuang G (2008) Bulk vitrification of human embryonic stem cells. Hum Reprod 23(2):358–364PubMedCrossRefGoogle Scholar
  52. 52.
    Li T, Zhou CQ, Mai QY, Zhuang GL (2005) Establishment of human embryonic stem cell line from gamete donors. Chin Med J 118(2):116–122PubMedGoogle Scholar
  53. 53.
    Li Y, Tan JC, Li LS (2010) Comparison of three methods for cryopreservation of human embryonic stem cells. Fertil Steril 93(3):999–1005PubMedCrossRefGoogle Scholar
  54. 54.
    Loser P, Schirm J, Guhr A, Wobus AM, Kurtz A (2010) Human embryonic stem cell lines and their use in international research. Stem Cells 28(2):240–246PubMedPubMedCentralGoogle Scholar
  55. 55.
    Lu J, Hou R, Booth CJ, Yang SH, Snyder M (2006) Defined culture conditions of human embryonic stem cells. Proc Natl Acad Sci U S A 103(15):5688–5693PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Ludwig T, J AT. Defined, feeder-independent medium for human embryonic stem cell culture. Current protocols in stem cell biology. 2007;Chapter 1:Unit 1C 2Google Scholar
  57. 57.
    Ludwig TE, Levenstein ME, Jones JM, Berggren WT, Mitchen ER, Frane JL et al (2006) Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol 24(2):185–187PubMedCrossRefGoogle Scholar
  58. 58.
    Mandai M, Watanabe A, Kurimoto Y, Hirami Y, Morinaga C, Daimon T et al (2017) Autologous induced stem-cell-derived retinal cells for macular degeneration. N Engl J Med 376(11):1038–1046CrossRefPubMedGoogle Scholar
  59. 59.
    Marti M, Mulero L, Pardo C, Morera C, Carrio M, Laricchia-Robbio L et al (2013) Characterization of pluripotent stem cells. Nat Protoc 8(2):223–253PubMedCrossRefGoogle Scholar
  60. 60.
    McCracken KW, Cata EM, Crawford CM, Sinagoga KL, Schumacher M, Rockich BE et al (2014) Modelling human development and disease in pluripotent stem-cell-derived gastric organoids. Nature 516(7531):400–404PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Menasche P, Vanneaux V, Hagege A, Bel A, Cholley B, Cacciapuoti I et al (2015) Human embryonic stem cell-derived cardiac progenitors for severe heart failure treatment: first clinical case report. Eur Heart J 36(30):2011–2017PubMedCrossRefGoogle Scholar
  62. 62.
    Merling RK, Sweeney CL, Choi U, De Ravin SS, Myers TG, Otaizo-Carrasquero F, et al. Transgene-free iPSCs generated from small volume peripheral blood nonmobilized CD34+ cells. Blood 2013;121(14):e98–107PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Miller JD, Ganat YM, Kishinevsky S, Bowman RL, Liu B, Tu EY et al (2013) Human iPSC-based modeling of late-onset disease via progerin-induced aging. Cell Stem Cell 13(6):691–705PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Mitalipova M, Calhoun J, Shin S, Wininger D, Schulz T, Noggle S et al (2003) Human embryonic stem cell lines derived from discarded embryos. Stem Cells 21(5):521–526PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Moretti A, Bellin M, Welling A, Jung CB, Lam JT, Bott-Flugel L et al (2010) Patient-specific induced pluripotent stem-cell models for long-QT syndrome. N Engl J Med 363(15):1397–1409PubMedCrossRefGoogle Scholar
  66. 66.
    Murdoch A, Braude P, Courtney A, Brison D, Hunt C, Lawford-Davies J et al (2012) The procurement of cells for the derivation of human embryonic stem cell lines for therapeutic use: recommendations for good practice. Stem Cell Rev 8(1):91–99PubMedCrossRefGoogle Scholar
  67. 67.
    Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H et al (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10(5):615–622PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Nakatsuji N, Nakajima F, Tokunaga K (2008) HLA-haplotype banking and iPS cells. Nat Biotechnol 26(7):739–740PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Nguyen HN, Byers B, Cord B, Shcheglovitov A, Byrne J, Gujar P et al (2011) LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress. Cell Stem Cell 8(3):267–280PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Ohmine S, Dietz AB, Deeds MC, Hartjes KA, Miller DR, Thatava T et al (2011) Induced pluripotent stem cells from GMP-grade hematopoietic progenitor cells and mononuclear myeloid cells. Stem Cell Res Ther 2(6):46PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Okita K, Matsumura Y, Sato Y, Okada A, Morizane A, Okamoto S et al (2011a) A more efficient method to generate integration-free human iPS cells. Nat Methods 8(5):409–412PubMedCrossRefGoogle Scholar
  72. 72.
    Okita K, Nagata N, Yamanaka S (2011b) Immunogenicity of induced pluripotent stem cells. Circ Res 109(7):720–721PubMedCrossRefGoogle Scholar
  73. 73.
    Ota A, Matsumura K, Lee JJ, Sumi S, Hyon SH (2017) StemCell keep is effective for cryopreservation of human embryonic stem cells by vitrification. Cell Transplant 26(5):773–787PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Pera MF, Trounson AO (2004) Human embryonic stem cells: prospects for development. Development 131(22):5515–5525PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Pistollato F, Bremer-Hoffmann S, Healy L, Young L, Stacey G (2012) Standardization of pluripotent stem cell cultures for toxicity testing. Expert Opin Drug Metab Toxicol 8(2):239–257PubMedCrossRefGoogle Scholar
  76. 76.
    Rajala K, Hakala H, Panula S, Aivio S, Pihlajamaki H, Suuronen R et al (2007) Testing of nine different xeno-free culture media for human embryonic stem cell cultures. Hum Reprod 22(5):1231–1238PubMedCrossRefGoogle Scholar
  77. 77.
    Raya A, Rodriguez-Piza I, Aran B, Consiglio A, Barri PN, Veiga A et al (2008) Generation of cardiomyocytes from new human embryonic stem cell lines derived from poor-quality blastocysts. Cold Spring Harb Symp Quant Biol 73:127–135PubMedCrossRefGoogle Scholar
  78. 78.
    Reubinoff BE, Pera MF, Fong CY, Trounson A, Bongso A (2000) Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol 18(4):399–404PubMedCrossRefGoogle Scholar
  79. 79.
    Reubinoff BE, Pera MF, Vajta G, Trounson AO (2001) Effective cryopreservation of human embryonic stem cells by the open pulled straw vitrification method. Hum Reprod 16(10):2187–2194PubMedCrossRefGoogle Scholar
  80. 80.
    Richards M, Fong CY, Chan WK, Wong PC, Bongso A (2002) Human feeders support prolonged undifferentiated growth of human inner cell masses and embryonic stem cells. Nat Biotechnol 20(9):933–936PubMedCrossRefGoogle Scholar
  81. 81.
    Rodin S, Domogatskaya A, Strom S, Hansson EM, Chien KR, Inzunza J et al (2010) Long-term self-renewal of human pluripotent stem cells on human recombinant laminin-511. Nat Biotechnol 28(6):611–615PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Sanchez-Danes A, Richaud-Patin Y, Carballo-Carbajal I, Jimenez-Delgado S, Caig C, Mora S et al (2012) Disease-specific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson’s disease. EMBO Mol Med 4(5):380–395PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Santos DM, Tiscornia G (2017) Induced pluripotent stem cell modeling of Gaucher’s disease: what have we learned? Int J Mol Sci 18(4):888PubMedCentralCrossRefPubMedGoogle Scholar
  84. 84.
    Schwartz SD, Hubschman JP, Heilwell G, Franco-Cardenas V, Pan CK, Ostrick RM et al (2012) Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 379(9817):713–720PubMedCrossRefGoogle Scholar
  85. 85.
    Schwartz SD, Regillo CD, Lam BL, Eliott D, Rosenfeld PJ, Gregori NZ et al (2015) Human embryonic stem cell-derived retinal pigment epithelium in patients with age-related macular degeneration and Stargardt's macular dystrophy: follow-up of two open-label phase 1/2 studies. Lancet 385(9967):509–516PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Seltmann S, Lekschas F, Muller R, Stachelscheid H, Bittner MS, Zhang W et al (2016) hPSCreg–the human pluripotent stem cell registry. Nucleic Acids Res 44(D1):D757–D763PubMedCrossRefGoogle Scholar
  87. 87.
    Shi Y, Inoue H, Wu JC, Yamanaka S (2017) Induced pluripotent stem cell technology: a decade of progress. Nat Rev Drug Discov 16(2):115–130PubMedCrossRefGoogle Scholar
  88. 88.
    Silva M, Daheron L, Hurley H, Bure K, Barker R, Carr AJ et al (2015) Generating iPSCs: translating cell reprogramming science into scalable and robust biomanufacturing strategies. Cell Stem Cell 16(1):13–17PubMedCrossRefGoogle Scholar
  89. 89.
    Sjogren A, Hardarson T, Andersson K, Caisander G, Lundquist M, Wikland M et al (2004) Human blastocysts for the development of embryonic stem cells. Reprod Biomed Online 9(3):326–329PubMedCrossRefGoogle Scholar
  90. 90.
    Soldner F, Stelzer Y, Shivalila CS, Abraham BJ, Latourelle JC, Barrasa MI et al (2016) Parkinson-associated risk variant in distal enhancer of alpha-synuclein modulates target gene expression. Nature 533(7601):95–99PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Song WK, Park KM, Kim HJ, Lee JH, Choi J, Chong SY et al (2015) Treatment of macular degeneration using embryonic stem cell-derived retinal pigment epithelium: preliminary results in Asian patients. Stem Cell Rep 4(5):860–872CrossRefGoogle Scholar
  92. 92.
    Stacey GN, Crook JM, Hei D, Ludwig T (2013) Banking human induced pluripotent stem cells: lessons learned from embryonic stem cells? Cell Stem Cell 13(4):385–388PubMedCrossRefGoogle Scholar
  93. 93.
    Strelchenko N, Verlinsky O, Kukharenko V, Verlinsky Y (2004) Morula-derived human embryonic stem cells. Reprod Biomed Online 9(6):623–629PubMedCrossRefGoogle Scholar
  94. 94.
    Strom S, Inzunza J, Grinnemo KH, Holmberg K, Matilainen E, Stromberg AM et al (2007) Mechanical isolation of the inner cell mass is effective in derivation of new human embryonic stem cell lines. Hum Reprod 22(12):3051–3058PubMedCrossRefGoogle Scholar
  95. 95.
    Sun N, Yazawa M, Liu J, Han L, Sanchez-Freire V, Abilez OJ et al (2012) Patient-specific induced pluripotent stem cells as a model for familial dilated cardiomyopathy. Sci Transl Med 4(130):130ra47PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Takahashi Y, Sato S, Kurashima Y, Yamamoto T, Kurokawa S, Yuki Y, Takemura N, Uematsu S, Lai C-Y, Otsu M, Matsuno H, Osawa H, Mizushima T, Nishimura J, Hayashi M, Yamaguchi T, Kiyono H (2018) A refined culture system for human induced pluripotent stem cell-derived intestinal epithelial organoids. Stem Cell Reports 10(1):314–328PubMedCrossRefGoogle Scholar
  97. 97.
    Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K et al (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861–872PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Takebe T, Sekine K, Enomura M, Koike H, Kimura M, Ogaeri T et al (2013) Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 499(7459):481–484PubMedCrossRefGoogle Scholar
  100. 100.
    Tannenbaum SE, Turetsky TT, Singer O, Aizenman E, Kirshberg S, Ilouz N et al (2012) Derivation of xeno-free and GMP-grade human embryonic stem cells–platforms for future clinical applications. PLoS One 7(6):e35325PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Taylor CJ, Bolton EM, Pocock S, Sharples LD, Pedersen RA, Bradley JA (2005) Banking on human embryonic stem cells: estimating the number of donor cell lines needed for HLA matching. Lancet 366(9502):2019–2025PubMedCrossRefGoogle Scholar
  102. 102.
    Taylor CJ, Peacock S, Chaudhry AN, Bradley JA, Bolton EM (2012) Generating an iPSC bank for HLA-matched tissue transplantation based on known donor and recipient HLA types. Cell Stem Cell 11(2):147–152PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Tedder RS, Zuckerman MA, Goldstone AH, Hawkins AE, Fielding A, Briggs EM et al (1995) Hepatitis B transmission from contaminated cryopreservation tank. Lancet 346(8968):137–140PubMedCrossRefGoogle Scholar
  104. 104.
    Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS et al (1998) Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145–1147PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Turetsky T, Aizenman E, Gil Y, Weinberg N, Shufaro Y, Revel A et al (2008) Laser-assisted derivation of human embryonic stem cell lines from IVF embryos after preimplantation genetic diagnosis. Hum Reprod 23(1):46–53PubMedCrossRefGoogle Scholar
  106. 106.
    Turner M, Leslie S, Martin NG, Peschanski M, Rao M, Taylor CJ et al (2013) Toward the development of a global induced pluripotent stem cell library. Cell Stem Cell 13(4):382–384PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Warren L, Manos PD, Ahfeldt T, Loh YH, Li H, Lau F et al (2010) Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7(5):618–630PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Wen Z, Nguyen HN, Guo Z, Lalli MA, Wang X, Su Y et al (2014) Synaptic dysregulation in a human iPS cell model of mental disorders. Nature 515(7527):414–418PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Woltjen K, Michael IP, Mohseni P, Desai R, Mileikovsky M, Hamalainen R et al (2009) piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458(7239):766–770PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Wong KG, Ryan SD, Ramnarine K, Rosen SA, Mann SE, Kulick A et al (2017) CryoPause: a new method to immediately initiate experiments after cryopreservation of pluripotent stem cells. Stem Cell Rep 9(1):355–365CrossRefGoogle Scholar
  111. 111.
    Young JE, Boulanger-Weill J, Williams DA, Woodruff G, Buen F, Revilla AC et al (2015) Elucidating molecular phenotypes caused by the SORL1 Alzheimer’s disease genetic risk factor using human induced pluripotent stem cells. Cell Stem Cell 16(4):373–385PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, Slukvin II, Thomson JA (2009) Human induced pluripotent stem cells free of vector and transgene sequences. Science 324(5928):797–801PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S et al (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318(5858):1917–1920PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Zhang X, Stojkovic P, Przyborski S, Cooke M, Armstrong L, Lako M et al (2006) Derivation of human embryonic stem cells from developing and arrested embryos. Stem Cells 24(12):2669–2676PubMedCrossRefGoogle Scholar
  115. 115.
    Zhou T, Benda C, Dunzinger S, Huang Y, Ho JC, Yang J et al (2012) Generation of human induced pluripotent stem cells from urine samples. Nat Protoc 7(12):2080–2089PubMedCrossRefGoogle Scholar
  116. 116.
    Reinhardt P, Schmid B, Burbulla LF, Schöndorf DC, Wagner L, Glatza M, Höing S, Hargus G, Heck SA, Dhingra A, Wu G, Müller S, Brockmann K, Kluba T, Maisel M, Krüger R, Berg D, Tsytsyura Y, Thiel CS, Psathaki OE, Klingauf J, Kuhlmann T, Klewin M, Müller H, Gasser T, Schöler HR, Sterneckert J (2013) Genetic correction of a LRRK2 mutation in human iPSCs links parkinsonian neurodegeneration to ERK-dependent changes in gene expression. Cell Stem Cell 12(3):354–367. doi: 10.1016/j.stem.2013.01.008CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Center of Regenerative Medicine in Barcelona (CMRB)BarcelonaSpain
  2. 2.National Stem Cell Bank-Barcelona Node, Biomolecular and Bioinformatics Resources Platform PRB2, ISCIII, CMRBBarcelonaSpain
  3. 3.Institució Catalana de Recerca I Estudis Avançats (ICREA)BarcelonaSpain
  4. 4.Center for Networked Biomedical Research on Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN)MadridSpain

Personalised recommendations