Assessing self-renewal and differentiation in human embryonic stem cell lines

Stem Cells

Volumn 24, Issue 3, 2006, Pages 516-530

  Cai, Jingli ^a   Chen, Jia ^b   Liu, Ying ^a   Miura, Takumi ^a   Luo, Yongquan ^a   Loring, Jeanne F ^c   Freed, William J ^b   Rao, Mahendra S ^d   Zeng, Xianmin ^b,e  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^c BURNHAM INSTITUTE   (United States)

^d INVITROGEN CORPORATION   (United States)

^e BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

Author keywords

Differentiation; Embryoid body; Human embryonic stem cell

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CD9 ANTIGEN; CELL NUCLEUS RECEPTOR; CLAUDIN; CREATINE KINASE; DECORIN; DNA METHYLTRANSFERASE; FIBRONECTIN; GALANIN; GAP JUNCTION PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; INTEGRIN; LAMININ; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; MOLECULAR MARKER; NESTIN; NEUROTENSIN; NOGGIN; PHOSPHATASE; RNA BINDING PROTEIN; SMAD PROTEIN; SULFOTRANSFERASE; TRANSCRIPTION FACTOR; TUBULIN; TYROSINE 3 MONOOXYGENASE; UNINDEXED DRUG; UVOMORULIN; VIMENTIN; ZINC FINGER PROTEIN; DIFFERENTIATION ANTIGEN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; CELL RENEWAL; CONTROLLED STUDY; EMBRYONIC STEM CELL; GENE EXPRESSION; GENE SEQUENCE; GERM CELL; IMMUNOCYTOCHEMISTRY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TROPHOBLAST; ANIMAL; BIOSYNTHESIS; CELL CULTURE; COCULTURE; COMPARATIVE STUDY; CYTOLOGY; DNA MICROARRAY; EMBRYO; FIBROBLAST; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METHODOLOGY; PHYSIOLOGY; STEM CELL;

ANIMALS; ANTIGENS, DIFFERENTIATION; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; EMBRYO; FIBROBLASTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELLS;

EID: 33744989977     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2005-0143     Document Type: Article

References (105)

1. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al. Embryonic stem cell lines derived from human blastocysts. Science 1998;282:1145-1147.
2. Carpenter MK, Rosler E, Rao MS. Characterization and differentiation of human embryonic stem cells. Cloning Stem Cells 2003;5:79-88.
3. Mitalipova M, Calhoun J, Shin S et al. Human embryonic stem cell lines derived from discarded embryos. STEM CELLS 2003;21:521-526.
4. Zeng X, Miura T, Luo Y et al. Properties of pluripotent human embryonic stem cells BG01 and BG02. STEM CELLS 2004;22:292-312.
5. Amit M, Itskovitz-Eldor J. Derivation and spontaneous differentiation of human embryonic stem cells. J Anat 2002;200:225-232.
6. Heins N, Englund MC, Sjoblom C et al. Derivation, characterization, and differentiation of human embryonic stem cells. STEM CELLS 2004;22:367-376.
7. Park JH, Kim SJ, Oh EJ et al. Establishment and maintenance of human embryonic stem cells on STO, a permanently growing cell line. Biol Reprod 2003;69:2007-2014.
8. Ginis I, Luo Y, Miura T et al. Differences between human and mouse embryonic stem cells. Dev Biol 2004;269:360-380.
9. Carpenter MK, Inokuma MS, Denham J et al. Enrichment of neurons and neural precursors from human embryonic stem cells. Exp Neurol 2001;172:383-397.
10. Kaufman DS, Hanson ET, Lewis RL et al. Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A 2001;98:10716-10721.
11. Kehat I, Kenyagin-Karsenti D, Snir M et al. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 2001;108:407-414.
12. Odorico JS, Kaufman DS, Thomson JA. Multilineage differentiation from human embryonic stem cell lines. STEM CELLS 2001;19:193-204.
13. Rambhatla L, Chiu CP, Kundu P et al. Generation of hepatocyte-like cells from human embryonic stem cells. Cell Transplant 2003;12:1-11.
14. Reubinoff BE, Itsykson P, Turetsky T et al. Neural progenitors from human embryonic stem cells. Nat Biotechnol 2001;19:1134-1140.
15. Xu C, Police S, Rao N et al. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res 2002;91:501-508.
16. Zhang SC, Wernig M, Duncan ID et al. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 2001;19:1129-1133.
17. Brandenberger R, Khrebtukova I, Thies RS et al. MPSS profiling of human embryonic stem cells. BMC Dev Biol 2004;4:10.
18. Bhattacharya B, Miura T, Brandenberger R et al. Gene expression in human embryonic stem cell lines: Unique molecular signature. Blood 2004;103:2956-2964.
19. Miura T, Luo Y, Khrebtukova I et al. Monitoring early differentiation events in human embryonic stem cells by massively parallel signature sequencing and expressed sequence tag scan. Stem Cells Dev 2004;13:694-715.
20. Sperger JM, Chen X, Draper JS et al. Gene expression patterns in human embryonic stem cells and human pluripotent germ cell tumors. Proc Natl Acad Sci U S A 2003;100:13350-13355.
21. Abeyta MJ, Clark AT, Rodriguez RT et al. Unique gene expression signatures of independently-derived human embryonic stem cell lines. Hum Mol Genet 2004;13:601-608.
22. Robson P. The maturing of the human embryonic stem cell transcriptome profile. Trends Biotechnol 2004;22:609-612.
23. Sato N, Sanjuan IM, Heke M et al. Molecular signature of human embryonic stem cells and its comparison with the mouse. Dev Biol 2003;260:404-413.
24. Richards M, Tan SP, Tan JH et al. The transcriptome profile of human embryonic stem cells as defined by SAGE. STEM CELLS 2004;22:51-64.
25. Brimble SN, Zeng X, Weiler DA et al. Karyotypic stability, genotyping, differentiation, feeder-free maintenance, and gene expression sampling in three human embryonic stem cell lines derived prior to August 9, 2001. Stem Cells Dev 2004;13:585-597.
26. Wei CL, Miura T, Robson P et al. Transcriptome profiling of human and murine ESCs identifies divergent paths required to maintain the stem cell state. STEM CELLS 2005;23:166-185.
27. Bhattacharya B, Luo Y, Miura T et al. Comparison of the gene expression profile of undifferentiated human embryonic stem cell lines and embryoid bodies. BMC Dev Biol 2005;5:22.
28. Humpherys D, Eggan K, Akutsu H et al. Epigenetic instability in ES cells and cloned mice. Science 2001;293:95-97.
29. Dean W, Bowden L, Aitchison A et al. Altered imprinted gene methylation and expression in completely ES cell-derived mouse fetuses: Association with aberrant phenotypes. Development 1998;125:2273-2282.
30. Xu C, Inokuma MS, Denham J et al. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 2001;19:971-974.
31. Rosler ES, Fisk GJ, Ares X et al. Long-term culture of human embryonic stem cells in feeder-free conditions. Dev Dyn 2004;229:259-274.
32. Zeng X, Chen J, Sanchez JF et al. Stable expression of hrGFP by mouse embryonic stem cells: Promoter activity in the undifferentiated state and during dopaminergic neural differentiation. STEM CELLS 2003;21:647-653.
33. Kuhn K, Baker SC, Chudin E et al. A novel, high-performance random array platform for quantitative gene expression profiling. Genome Res 2004;14:2347-2356.
34. Wong RC, Pebay A, Nguyen LT et al. Presence of functional gap junctions in human embryonic stem cells. STEM CELLS 2004;22:883-889.
35. Amit M, Shariki C, Margulets V et al. Feeder layer- and serum-free culture of human embryonic stem cells. Biol Reprod 2004;70:837-845.
36. Draper JS, Moore HD, Ruban LN et al. Culture and characterization of human embryonic stem cells. Stem Cells Dev 2004;13:325-336.
37. Ramalho-Santos M, Yoon S, Matsuzaki Y et al. "Stemness": Transcriptional profiling of embryonic and adult stem cells. Science 2002;298:597-600.
38. Zaehres H, Lensch MW, Daheron L et al. High-efficiency RNA interference in human embryonic stem cells. STEM CELLS 2005;23:299-305.
39. Mitsui K, Tokuzawa Y, Itoh H et al. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003;113:631-642.
40. Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 2000;24:372-376.
41. Hart AH, Hartley L, Ibrahim M et al. Identification, cloning and expression analysis of the pluripotency promoting Nanog genes in mouse and human. Dev Dyn 2004;230:187-198.
42. Noaksson K, Zoric N, Zeng X et al. Monitoring differentiation of human embryonic stem cells using real-time PCR. STEM CELLS 2005;23:1460-1467.
43. Yang AX, Mejido J, Luo Y et al. Development of a focused microarray to assess human embryonic stem cell differentiation. Stem Cells Dev 2005;14:270-284.
44. Rosner MH, Vigano MA, Ozato K et al. A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature 1990;345:686-692.
45. Yuan H, Corbi N, Basilico C et al. Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev 1995;9:2635-2645.
46. Cui L, Johkura K, Yue F et al. Spatial distribution and initial changes of SSEA-1 and other cell adhesion-related molecules on mouse embryonic stem cells before and during differentiation. J Histochem Cytochem 2004;52:1447-1457.
47. Anisimov SV, Tarasov KV, Tweedie D et al. SAGE identification of gene transcripts with profiles unique to pluripotent mouse R1 embryonic stem cells. Genomics 2002;79:169-176.
48. Lee YS, Kim HK, Chung S et al. Depletion of human micro-RNA miR-125b reveals that it is critical for the proliferation of differentiated cells but not for the down-regulation of putative targets during differentiation. J Biol Chem 2005;280:16635-16641.
49. Okuda A, Fukushima A, Nishimoto M et al. UTF1, a novel transcriptional coactivator expressed in pluripotent embryonic stem cells and extra-embryonic cells. Embo J 1998;17:2019-2032.
50. Lei W, Hirose T, Zhang LX et al. Cloning of the human orphan receptor germ cell nuclear factor/retinoid receptor-related testis-associated receptor and its differential regulation during embryonal carcinoma cell differentiation. J Mol Endocrinol 1997;18:167-176.
51. Hanna LA, Foreman RK, Tarasenko IA et al. Requirement for Foxd3 in maintaining pluripotent cells of the early mouse embryo. Genes Dev 2002;16:2650-2661.
52. Chambers I, Colby D, Robertson M et al. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003;113:643-655.
53. Rogers MB, Hosler BA, Gudas LJ. Specific expression of a retinoic acid-regulated, zinc-finger gene, Rex-1, in preimplantation embryos, trophoblast and spermatocytes. Development 1991;113:815-824.
54. Feldman B, Poueymirou W, Papaioannou VE et al. Requirement of FGF-4 for postimplantation mouse development. Science 1995;267:246-249.
55. Kim SK, Suh MR, Yoon HS et al. Identification of developmental pluripotency associated 5 expression in human pluripotent stem cells. STEM CELLS 2005;23:458-462.
56. Schmid E, Tapscott S, Bennett GS et al. Differential location of different types of intermediate-sized filaments in various tissues of the chicken embryo. Differentiation 1979;15:27-40.
57. Sharma MK, Saxena V, Liu RZ et al. Differential expression of the duplicated cellular retinoic acid-binding protein 2 genes (crabp2a and crabp2b) during zebrafish embryonic development. Gene Expr Patterns 2005;5:371-379.
58. Kolodkin AL, Matthes DJ, Goodman CS. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 1993;75:1389-1399.
59. Good P, Yoda A, Sakakibara S et al. The human Musashi homolog 1 (MSI1) gene encoding the homologue of Musashi/Nrp-1, a neural RNA-binding protein putatively expressed in CNS stem cells and neural progenitor cells. Genomics 1998;52:382-384.
60. Garner CC, Tucker RP, Matus A. Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature 1988;336:674-677.
61. Reeves SA, Helman LJ, Allison A et al. Molecular cloning and primary structure of human glial fibrillary acidic protein. Proc Natl Acad Sci U S A 1989;86:5178-5182.
62. Zhou Q, Wang S, Anderson DJ. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 2000;25:331-343.
63. Malas S, Duthie SM, Mohri F et al. Cloning and mapping of the human SOX1: A highly conserved gene expressed in the developing brain. Mamm Genome 1997;8:866-868.
64. Hockfield S, McKay RD. Identification of major cell classes in the developing mammalian nervous system. J Neurosci 1985;5:3310-3328.
65. Lee JE, Hollenberg SM, Snider L et al. Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 1995;268:836-844.
66. Masserano JM, Weiner N. Tyrosine hydroxylase regulation in the central nervous system. Mol Cell Biochem 1983;53-54:129-152.
67. Burgoyne RD, Cambray-Deakin MA, Lewis SA et al. Differential distribution of beta-tubulin isotypes in cerebellum. Embo J 1988;7:2311-2319.
68. Kornblihtt AR, Vibe-Pedersen K, Baralle FE. Isolation and characterization of cDNA clones for human and bovine fibronectins. Proc Natl Acad Sci U S A 1983;80:3218-3222.
69. Fisher LW, Hawkins GR, Tuross N et al. Purification and partial characterization of small proteoglycans I and II, bone sialoproteins I and II, and osteonectin from the mineral compartment of developing human bone. J Biol Chem 1987;262:9702-9708.
70. Ruoslahti E, Pihko H, Seppala M. Alpha-fetoprotein: Immunochemical purification and chemical properties. Expression in normal state and in malignant and non-malignant liver disease. Transplant Rev 1974;20:38-60.
71. Lohi J, Leivo I, Franssila K et al. Changes in the distribution of integrins and their basement membrane ligands during development of human thyroid follicular epithelium. Histochem J 1997;29:337-345.
72. Smyth N, Vatansever HS, Murray P et al. Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J Cell Biol 1999;144:151-160.
73. Wozney JM, Rosen V, Celeste AJ et al. Novel regulators of bone formation: molecular clones and activities. Science 1988;242:1528-1534.
74. Kurachi K, Chandra T, Degen SJ et al. Cloning and sequence of cDNA coding for alpha 1-antitrypsin. Proc Natl Acad Sci U S A 1981;78:6826-6830.
75. Kendall RL, Thomas KA. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci U S A 1993;90:10705-10709.
76. ten Dijke P, Ichijo H, Franzen P et al. Activin receptor-like kinases: A novel subclass of cell-surface receptors with predicted serine/threonine kinase activity. Oncogene 1993;8:2879-2887.
77. Arceci RJ, King AA, Simon MC et al. Mouse GATA-4: A retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol Cell Biol 1993;13:2235-2246.
78. Novak U, Wilks A, Buell G et al. Identical mRNA for preproglucagon in pancreas and gut. Eur J Biochem 1987;164:553-558.
79. Andik I, Donhoffer S. The effect of insulin on food intake and selection of mice. Z Vitam Horm Fermentforsch 1949;3:208-212.
80. Newman PJ, Berndt MC, Gorski J et al. PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 1990;247:1219-1222.
81. Lowe JB, Boguski MS, Sweetser DA et al. Human liver fatty acid binding protein. Isolation of a full length cDNA and comparative sequence analyses of orthologous and paralogous proteins. J Biol Chem 1985;260:3413-3417.
82. Chartier FL, Bossu JP, Laudet V et al. Cloning and sequencing of cDNAs encoding the human hepatocyte nuclear factor 4 indicate the presence of two isoforms in human liver. Gene 1994;147:269-272.
83. Crossley PH, Martin GR. The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 1995;121:439-451.
84. Zarnegar R, Michalopoulos G. Purification and biological characterization of human hepatopoietin A, a polypeptide growth factor for hepatocytes. Cancer Res 1989;49:3314-3320.
85. Yamada S, Zhu Q, Aihara Y et al. Cloning of cDNA and the gene encoding human hepatocyte nuclear factor (HNF)-3 beta and mutation screening in Japanese subjects with maturity-onset diabetes of the young. Diabetologia 2000;43:121-124.
86. Termine JD, Kleinman HK, Whitson SW et al. Osteonectin, a bone-specific protein linking mineral to collagen. Cell 1981;26:99-105.
87. Russell MW, Baker P, Izumo S. Cloning, chromosomal mapping, and expression of the human eHAND gene. Mamm Genome 1997;8:863-865.
88. Robert B, Sassoon D, Jacq B et al. Hox-7, a mouse homeobox gene with a novel pattern of expression during embryogenesis. Embo J 1989;8:91-100.
89. Gunning P, Ponte P, Blau H et al. Alpha-skeletal and alpha-cardiac actin genes are coexpressed in adult human skeletal muscle and heart. Mol Cell Biol 1983;3:1985-1995.
90. Suzuki E, Evans T, Lowry J et al. The human GATA-6 gene: Structure, chromosomal location, and regulation of expression by tissue-specific and mitogen-responsive signals. Genomics 1996;38:283-290.
91. Glant TT, Hadhazy C, Mikecz K et al. Appearance and persistence of fibronectin in cartilage. Specific interaction of fibronectin with collagen type II. Histochemistry 1985;82:149-158.
92. Lau ET, Kwok YK, Chui DH et al. Embryonic and fetal globins are expressed in adult erythroid progenitor cells and in erythroid cell cultures. Prenat Diagn 2001;21:529-539.
93. Herrmann BG. Action of the Brachyury gene in mouse embryogenesis. Ciba Found Symp 1992;165:78-86; discussion 86-91.
94. Call KM, Glaser T, Ito CY et al. Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms' tumor locus. Cell 1990;60:509-520.
95. Braun T, Buschhausen-Denker G, Bober E et al. A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts. Embo J 1989;8:701-709.
96. Li ZL, Lilienbaum A, Butler-Browne G et al. Human desmin-coding gene: Complete nucleotide sequence, characterization and regulation of expression during myogenesis and development. Gene 1989;78:243-254.
97. Kangawa K, Matsuo H. Purification and complete amino acid sequence of alpha-human atrial natriuretic polypeptide (alpha-hANP). Biochem Biophys Res Commun 1984;118:131-139.
98. Marotta CA, Forget BG, Cohen-Solal M et al. Nucleotide sequence analysis of coding and noncoding regions of human beta-globin mRNA. Prog Nucleic Acid Res Mol Biol 1976;19:165-175.
99. Ogawa E, Maruyama M, Kagoshima H et al. PEBP2/PEA2 represents a family of transcription factors homologous to the products of the Drosophila runt gene and the human AML1 gene. Proc Natl Acad Sci U S A 1993;90:6859-6863.
100. Bell GI, Merryweather JP, Sanchez-Pescador R et al. Sequence of a cDNA clone encoding human preproinsulin-like growth factor II. Nature 1984;310:775-777.
101. Ryan K, Garrett N, Mitchell A et al. Eomesodermin, a key early gene in Xenopus mesoderm differentiation. Cell 1996;87:989-1000.
102. Suh E, Chen L, Taylor J et al. A homeodomain protein related to caudal regulates intestine-specific gene transcription. Mol Cell Biol 1994;14:7340-7351.
103. Yamada K, Ogawa H, Honda S et al. A GCM motif protein is involved in placenta-specific expression of human aromatase gene. J Biol Chem 1999;274:32279-32286.
104. Cserhalmi-Friedman PB, Squeo R, Gordon D et al. Epidermolytic hyperkeratosis in a Hispanic family resulting from a mutation in the keratin 1 gene. Clin Exp Dermatol 2000;25:241-243.
105. Yuan L, Liu JG, Zhao J et al. The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol Cell 2000;5:73-83.