Self-renewal and scalability of human embryonic stem cells for human therapy

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Bibliography

• 1  Thomson JA, Itskovitz-Eldor J, Shapiro SS et al.: Embryonic stem cell lines derived from human blastocysts. Science282,1145–1147 (1998).▪▪ Important paper that describes the first successful derivation of human embryonic stem cells (hESCs) from human blastocysts.
  Medline CASGoogle Scholar
• 2  Chambers I, Smith A: Self-renewal of teratocarcinoma and embryonic stem cells. Oncogene23(43),7150–7160 (2004).
  Medline CASGoogle Scholar
• 3  Humphrey RK, Beattie GM, Lopez AD et al.: Maintenance of pluripotency in human embryonic stem cells is STAT3 independent. Stem Cells22(4),522–530 (2004).
  Medline CASGoogle Scholar
• 4  Chadwick K, Wang LS, Li L et al.: Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood102(3),906–915 (2003).
  Medline CASGoogle Scholar
• 5  Zhang PB, Li JA, Tan ZJ et al.: Short-term BMP-4 treatment initiates mesoderm induction in human embryonic stem cells. Blood111(4),1933–1941 (2008).
  Medline CASGoogle Scholar
• 6  Nichols J, Smith A: The origin and identity of embryonic stem cells. Development138(1),3–8 (2010).
  Google Scholar
• 7  Eiselleova L, Matulka K, Kriz V et al.: A complex role for FGF-2 in self-renewal, survival, and adhesion of human embryonic stem cells. Stem Cells27(8),1847–1857 (2009).
  Medline CASGoogle Scholar
• 8  Besser D: Expression of nodal, lefty-A, and lefty-B in undifferentiated human embryonic stem cells requires activation of Smad2/3. J. Biol. Chem.279(43),45076–45084 (2004).
  Medline CASGoogle Scholar
• 9  Vallier L, Alexander M, Pedersen RA: Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J. Cell Sci.118(19),4495–4509 (2005).
  Medline CASGoogle Scholar
• 10  Lee KW, Yook JY, Son MY et al.: Rapamycin promotes the osteoblastic differentiation of human embryonic stem cells by blocking the mTOR pathway and stimulating the BMP/Smad pathway. Stem Cells Dev.19(4),557–568 (2010).
  Medline CASGoogle Scholar
• 11  Jiaxi ZX, Su P, Wang L et al.: mTOR supports long-term self-renewal and suppresses mesoderm and endoderm activities of human embryonic stem cells. Proc. Natl Acad. Sci. USA106(19),7840–7845 (2009).
  MedlineGoogle Scholar
• 12  Easley CA, Ben-Yehudah A, Redinger CJ et al.: mTOR-mediated activation of p70 S6K induces differentiation of pluripotent human embryonic stem cells. Cell. Reprogram.12(3),263–273 (2010).
  Medline CASGoogle Scholar
• 13  Valdimarsdottir G, Mummery C: Functions of the TGF-β superfamily in human embryonic stem cells. APMIS113(11–12),773–789 (2005).
  Medline CASGoogle Scholar
• 14  Na J, Andrews P: The balancing action between Activin A/TGF-β, FGF, Writ and BMP signalling instructs human embryonic stem cell fate decisions. Mech. Dev.126,S207 (2009).
  Google Scholar
• 15  Chambers I, Colby D, Robertson M et al.: Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell113(5),643–655 (2003).▪▪ Describes the cloning of the critical pluripotency factor Nanog.
  Medline CASGoogle Scholar
• 16  Mitsui K, Tokuzawa Y, Itoh H et al.: The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell113(5),631–642. (2003).▪▪ Describes the cloning of the critical pluripotency factor Nanog.
  Medline CASGoogle Scholar
• 17  Zaehres H, Lensch MW, Daheron L, Stewart SA, Itskovitz-Eldor J, Daley GQ: High-efficiency RNA interference in human embryonic stem cells. Stem Cells23(3),299–305 (2005).
  Medline CASGoogle Scholar
• 18  Boyer LA, Lee TI, Cole MF et al.: Core transcriptional regulatory circuitry in human embryonic stem cells. Cell122(6),947–956. (2005).
  Medline CASGoogle Scholar
• 19  Nichols J, Zevnik B, Anastassiadis K et al.: Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell95(3),379–391 (1998).
  Medline CASGoogle Scholar
• 20  Kuroda T, Tada M, Kubota H et al.: Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol. Cell. Biol.25(6),2475–2485 (2005).
  Medline CASGoogle Scholar
• 21  Adachi K, Suemori H, Yasuda S, Nakatsuji N, Kawase E: Role of SOX2 in maintaining pluripotency of human embryonic stem cells. Genes Cells15(5),455–469 (2010).
  Medline CASGoogle Scholar
• 22  Boiani M, Scholer HR: Regulatory networks in embryo-derived pluripotent stem cells. Nat. Rev. Mol. Cell Biol.6(11),872–884 (2005).
  Medline CASGoogle Scholar
• 23  Zhang PL, Andrianakos R, Yang Y, Liu CM, Lu WG: Kruppel-like factor 4 (Klf4) prevents embryonic stem (ES) cell differentiation by regulating Nanog gene expression. J. Biol. Chem.285(12),9180–9189 (2010).
  Medline CASGoogle Scholar
• 24  Chan KK, Zhang J, Chia NY et al.: KLF4 and PBX1 directly regulate NANOG expression in human embryonic stem cells. Stem Cells27(9),2114–2125 (2009).
  Medline CASGoogle Scholar
• 25  Lim Cy, Tam Wl, Zhang J et al.: Sall4 regulates distinct transcription circuitries in different blastocyst-derived stem cell lineages. Cell Stem Cell3(5),543–554 (2008).
  Medline CASGoogle Scholar
• 26  Wang ZX, Teh CHL, Chan CMY et al.: The Transcription factor Zfp281 controls embryonic stem cell pluripotency by direct activation and repression of target genes. Stem Cells26(11),2791–2799 (2008).
  Medline CASGoogle Scholar
• 27  Chen X, Fang F, Liou YC, Ng HH: Zfp143 regulates Nanog through modulation of Oct4 binding. Stem Cells26(11),2759–2767 (2008).
  Medline CASGoogle Scholar
• 28  Xu RH, Sampsell-Barron TL, Gu F et al.: NANOG is a direct target of TGF β/Activin-mediated SMAD signaling in human ESCs. Cell Stem Cell3(2),196–206 (2008).
  Medline CASGoogle Scholar
• 29  Liang J, Wan M, Zhang Y et al.: Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat. Cell Biol.10(6),731–739 (2008).
  Medline CASGoogle Scholar
• 30  Mallanna SK, Rizzino A: Emerging roles of microRNAs in the control of embryonic stem cells and the generation of induced pluripotent stem cells. Dev. Biol.344(1),16–25 (2010).
  Medline CASGoogle Scholar
• 31  Fujita J, Crane AM, Souza MK et al.: Caspase activity mediates the differentiation of embryonic stem cells. Cell Stem Cell2(6),595–601 (2008).
  Medline CASGoogle Scholar
• 32  Moretto-Zita M, Jin H, Shen ZX, Zhao TB, Briggs SP, Xu Y: Phosphorylation stabilizes Nanog by promoting its interaction with Pin1. Proc. Natl Acad. Sci. USA107(30),13312–13317 (2010).
  Medline CASGoogle Scholar
• 33  Tsuruzoe S, Ishihara K, Uchimura Y et al.: Inhibition of DNA binding of Sox2 by the SUMO conjugation. Biochem. Biophys. Res. Commun.351(4),920–926 (2006).
  Medline CASGoogle Scholar
• 34  Ohgushi M, Matsumura M, Eiraku M et al.: Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells. Cell Stem Cell7(2),225–239 (2010).
  Medline CASGoogle Scholar
• 35  Watanabe K, Ueno M, Kamiya D et al.: A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotechnol.25(6),681–686 (2007).▪ Among the first approaches to effectively promote clonal expansion of hESCs.
  Medline CASGoogle Scholar
• 36  Emre N, Vidal JG, Elia J et al.: The ROCK inhibitor Y-27632 improves recovery of human embryonic stem cells after fluorescence-activated cell sorting with multiple cell surface markers. PLoS One5(8),e12148 (2010).
  MedlineGoogle Scholar
• 37  Baharvand H, Salekdeh GH, Taei A, Mollamohammadi S: An efficient and easy-to-use cryopreservation protocol for human ES and iPS cells. Nat. Protoc.5(3),588–594 (2010).
  Medline CASGoogle Scholar
• 38  Song H, Chung S-K, Xu Y: Modeling disease in human ESCs using an efficient BAC-based homologous recombination system. Cell Stem Cell6(1),80–89 (2010).▪ Describes the generation of the first homozygous mutant hESCs and the critical role of p53 in maintaining genomic stability in hESCs.
  Medline CASGoogle Scholar
• 39  Ferretti R, Palumbo V, Di Savino A et al.: Morgana/chp-1, a ROCK inhibitor involved in centrosome duplication and tumorigenesis. Dev. Cell18(3),486–495 (2010).
  Medline CASGoogle Scholar
• 40  Baxter MA, Camarasa MV, Bates N et al.: Analysis of the distinct functions of growth factors and tissue culture substrates necessary for the long-term self-renewal of human embryonic stem cell lines. Stem Cell Res.3(1),28–38 (2009).
  Medline CASGoogle Scholar
• 41  Xu Y, Zhu XW, Hahm HS et al.: Revealing a core signaling regulatory mechanism for pluripotent stem cell survival and self-renewal by small molecules. Proc. Natl Acad. Sci. USA107(18),8129–8134 (2010).
  Medline CASGoogle Scholar
• 42  Li D, Zhou JX, Wang L et al.: Integrated biochemical and mechanical signals regulate multifaceted human embryonic stem cell functions. J. Cell Biol.191(3),631–644 (2010).
  Medline CASGoogle Scholar
• 43  Li L, Wang SA, Jezierski A et al.: A Unique interplay between Rap1 and E-cadherin in the endocytic pathway regulates self-renewal of human embryonic stem cells. Stem Cells28(2),247–257 (2010).
  MedlineGoogle Scholar
• 44  Miura T, Mattson MP, Rao MS: Cellular lifespan and senescence signaling in embryonic stem cells. Aging Cell3(6),333–343 (2004).
  Medline CASGoogle Scholar
• 45  Kim SJ, Cheon SH, Yoo SJ et al.: Contribution of the PI3K/Akt/PKB signal pathway to maintenance of self-renewal in human embryonic stem cells. FEBS Lett.579(2),534–540 (2005).
  Medline CASGoogle Scholar
• 46  Bendall SC, Stewart MH, Menendez P et al.: IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro. Nature448(7157),1015–1021 (2007).
  Medline CASGoogle Scholar
• 47  Mattson MP, Meffert MK: Roles for NF-κB in nerve cell survival, plasticity, and disease. Cell Death Differ.13(5),852–860 (2006).
  Medline CASGoogle Scholar
• 48  Kang HB, Kim YE, Kwon HJ, Sok DE, Lee YH: Enhancement of NF-κB expression and activity upon differentiation of human embryonic stem cell line SNUhES3. Stem Cells Dev.16(4),615–623 (2007).
  Medline CASGoogle Scholar
• 49  Yang CB, Atkinson SP, Vilella F et al.: Opposing putative roles for canonical and noncanonical NF-κB signaling on the survival, proliferation, and differentiation potential of human embryonic stem cells. Stem Cells28(11),1970–1980 (2010).
  Medline CASGoogle Scholar
• 50  Cervantes RB, Stringer JR, Shao C, Tischfield JA, Stambrook PJ: Embryonic stem cells and somatic cells differ in mutation frequency and type. Proc. Natl Acad. Sci. USA99(6),3586–3590 (2002).
  Medline CASGoogle Scholar
• 51  Narva E, Autio R, Rahkonen N et al.: High-resolution DNA analysis of human embryonic stem cell lines reveals culture-induced copy number changes and loss of heterozygosity. Nat. Biotechnol.28(4),371–377 (2010).▪ Among the first papers to describe the genomic instability in hESCs using high-resolution genomic analysis.
  MedlineGoogle Scholar
• 52  Laurent LC, Ulitsky I, Slavin I et al.: Dynamic changes in the copy number of pluripotency and cell proliferation genes in human ESCs and iPSCs during reprogramming and time in culture. Cell Stem Cell8(1),106–118 (2011).▪ One of the first articles to describe genomic instability in hESCs and induced pluripotent stem cells using high-resolution genomic analysis.
  Medline CASGoogle Scholar
• 53  Momcilovic O, Choi S, Varum S, Bakkenist C, Schatten G, Navara C: Ionizing radiation induces ataxia telangiectasia mutated-dependent checkpoint signaling and cell cycle arrest in pluripotent human embryonic stem cells. Stem Cells27(8),1822–1835 (2009).
  Medline CASGoogle Scholar
• 54  Vousden KH, Prives C: Blinded by the light: the growing complexity of p53. Cell137(3),413–431 (2009).
  Medline CASGoogle Scholar
• 55  Lin T, Chao C, Saito SI et al.: p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat. Cell Biol.7(2),165–171 (2005).▪▪ Describes an important role of p53 in maintaining genomic stability in ESCs.
  Medline CASGoogle Scholar
• 56  Liu DP, Ou LD, Clemenson GD et al.: Puma is required for p53-induced depletion of adult stem cells. Nat. Cell Biol.12(10),993–998 (2010).
  Medline CASGoogle Scholar
• 57  Martin MJ, Muotri A, Gage F, Varki A: Human embryonic stem cells express an immunogenic nonhuman sialic acid. Nat. Med.11(2),228–232 (2005).
  Medline CASGoogle Scholar
• 58  Crook JM, Peura TT, Kravets L et al.: The generation of six clinical-grade human embryonic stem cell lines. Cell Stem Cell1(5),490–494 (2007).
  Medline CASGoogle Scholar
• 59  Sivarajah S, Raj GS, Mathews AJV, Sahib NBE, Hwang WS, Crook JM: The generation of GLP-grade human embryonic stem cell banks from four clinical-grade cell lines for preclinical research. In Vitro Cell. Dev. Biol. Anim.46(3–4),210–216 (2010).
  MedlineGoogle Scholar
• 60  Englund MCO, Caisander G, Noaksson K et al.: The establishment of 20 different human embryonic stem cell lines and subclones; a report on derivation, culture, characterisation and banking. In Vitro Cell. Dev. Biol. Anim.46(3–4),217–230 (2010).
  MedlineGoogle Scholar
• 61  Meng GL, Liu SY, Li XY, Krawetz R, Rancourt DE: Extracellular matrix isolated from foreskin fibroblasts supports long-term xeno-free human embryonic stem cell culture. Stem Cells Dev.19(4),547–556 (2010).
  Medline CASGoogle Scholar
• 62  Aguilar-Gallardo C, Poo M, Gomez E et al.: Derivation, characterization, differentiation, and registration of seven human embryonic stem cell lines (VAL-3, -4, -5, -6M, -7, -8, and -9) on human feeder. In Vitro Cell. Dev. Biol. Anim.46(3–4),317–326 (2010).
  MedlineGoogle Scholar
• 63  Tecirlioglu RT, Nguyen L, Koh K, Trounson AO, Michalska AE: Derivation and maintenance of human embryonic stem cell line on human adult skin fibroblast feeder cells in serum replacement medium. In Vitro Cell. Dev. Biol. Anim.46(3–4),231–235 (2010).
  MedlineGoogle Scholar
• 64  Park Y, Choi IY, Lee SJ et al.: Undifferentiated propagation of the human embryonic stem cell lines, H1 and HSF6, on human placenta-derived feeder cells without basic fibroblast growth factor supplementation. Stem Cells Dev.19(11),1713–1722 (2010).
  Medline CASGoogle Scholar
• 65  Rodin S, Domogatskaya A, Strom S et al.: Long-term self-renewal of human pluripotent stem cells on human recombinant laminin-511. Nat. Biotechnol.28(6),611–615 (2010).
  Medline CASGoogle Scholar
• 66  Prowse ABJ, Doran MR, Cooper-White JJ et al.: Long term culture of human embryonic stem cells on recombinant vitronectin in ascorbate free media. Biomaterials31(32),8281–8288 (2010).
  Medline CASGoogle Scholar
• 67  Ludwig TE, Bergendahl V, Levenstein ME, Yu J, Probasco MD, Thomson JA: Feeder-independent culture of human embryonic stem cells. Nat. Meth.3(8),637–646 (2006).
  Medline CASGoogle Scholar
• 68  Wang L, Schulz TC, Sherrer ES et al.: Self-renewal of human embryonic stem cells requires insulin-like growth factor-1 receptor and ERBB2 receptor signaling. Blood110(12),4111–4119 (2007).
  Medline CASGoogle Scholar
• 69  Yao S, Chen S, Clark J et al.: Long-term self-renewal and directed differentiation of human embryonic stem cells in chemically defined conditions. Proc. Natl Acad. Sci. USA103(18),6907–6912 (2006).
  Medline CASGoogle Scholar
• 70  Melkoumian Z, Weber JL, Weber DM et al.: Synthetic peptide-acrylate surfaces for long-term self-renewal and cardiomyocyte differentiation of human embryonic stem cells. Nat. Biotechnol.28(6),606–695 (2010).▪ One of the first articles to develop a bioactive surface for long-term expansion of hESCs.
  Medline CASGoogle Scholar
• 71  Yoon BS, Jun EK, Park G et al.: Optimal suppression of protein phosphatase 2A activity is critical for maintenance of human embryonic stem cell self-renewal. Stem Cells28(5),874–884 (2010).
  Medline CASGoogle Scholar
• 72  Wu DM, Pang YH, Ke YH et al.: A conserved mechanism for control of human and mouse embryonic stem cell pluripotency and differentiation by Shp2 tyrosine phosphatase. PLoS One4(3),e4914 (2009).
  MedlineGoogle Scholar
• 73  Villa-Diaz LG, Nandivada H, Ding J et al.: Synthetic polymer coatings for long-term growth of human embryonic stem cells. Nat. Biotechnol.28(6),581–583 (2010).▪ One of the first studies to develop a bioactive surface to support the long-term culture of hESCs.
  Medline CASGoogle Scholar
• 74  Mohamet L, Lea ML, Ward CM: Abrogation of E-cadherin-mediated cellular aggregation allows proliferation of pluripotent mouse embryonic stem cells in shake flask bioreactors. PLoS One5(9),e12921 (2010).
  MedlineGoogle Scholar
• 75  Serra M, Brito C, Sousa MFQ et al.: Improving expansion of pluripotent human embryonic stem cells in perfused bioreactors through oxygen control. J. Biotechnol.148(4),208–215 (2010).
  Medline CASGoogle Scholar
• 76  Steiner D, Khaner H, Cohen M et al.: Derivation, propagation and controlled differentiation of human embryonic stem cells in suspension. Nat. Biotechnol.28(4),361–364 (2010).▪ The first successful derivation of hESCs in suspension culture.
  Medline CASGoogle Scholar