Embryonic stem cell differentiation models: Cardiogenesis, myogenesis, neurogenesis, epithelial and vascular smooth muscle cell differentiation in vitro

Cytotechnology

Volumn 30, Issue 1-3, 1999, Pages 211-226

  Guan, Kaomei ^a   Rohwedel, Jürgen ^a,b   Wobus, Anna M ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b UNIVERSITY OF LÜBECK   (Germany)

Author keywords

Cardiogenesis; Cell differentiation; Gene expression; Mouse embryonic stem cells; Myogenesis; Neurogenesis

Indexed keywords

CELL DIFFERENTIATION; IN VITRO STUDY; MODEL; MUSCLE CELL; ORGANOGENESIS; STEM CELL;

EID: 0032937142     PISSN: 09209069     EISSN: None     Source Type: Journal    
DOI: 10.1023/a:1008041420166     Document Type: Article

References (87)

1. 1 integrin-deficient cells. Dev Biol 179: 184-196.
2. Bain G, Kitchens D, Yao M, Huettner JE and Gottlieb DI(1995) Embryonic stem cells express neuronal properties in vitro. Dev Biol 168: 342-357.
3. Blank RS, Swartz EA, Thompson MM, Olson EN and Owens GK (1995) A retinoic acid-induced donal cell line derived from multipotential P19 embryonal carcinoma cells expresses smooth muscle characteristics. Circ Res 76: 742-749.
4. Boudjelal M, Taneja R, Matsubara S, Bouillet P, Dolle P and Chambon P (1997) Overexpression of Stra13, a novel retinoic acid-inducible gene of the basic helix-loop-helix family, inhibits mesodermal and promotes neuronal differentiation of P19 cells. Genes Dev 11: 2052-2065.
5. Bradley A, Evans M, Kaufman MH and Robertson E (1984) Formation of germ-line chimaeras from embryo-derived teratocaranoma cell lines. Nature 309: 255-256.
6. Brandon EP, Idzerda RL and McKnight GS (1995) Targeting the mouse genome: a compendium of knockouts (part I - III). Curr Biol 5: 625-634, 758-765, 873-881.
7. Chomczynski P and Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159.
8. Clarke AR (1994) Murine genetic modes of human disease. Curr Opin Genet Dev 4: 453-460.
9. Cormack BP, Valdivia RH and Falkow S (1996) FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173: 33-38.
10. Dani C, Smith AG, Dessolin S, Leroy P, Staccini L, Villageois P, Darimont C and Ailhaud G (1997) Differentiation of embryonic stem cells into adipocytes in vitro. J Cell Sci 110: 1279-1285.
11. Dinsmore J, Ratliff J, Deason T, Pakzaban P, Jacoby D, Galpern W and Isacson O (1996) Embryonic stem cells differentiated in vitro as a novel source of cells for transplantation. Cell Transplant 5: 131-143.
12. Dinsmore J, Ratcliff J, Jacoby D, Wunderlich M and Lindberg C (1998) Embryonic stem cells as a model for studying regulation of cellular differentiation. Theriogenology 49: 145-151.
13. Doetschman TC, Eistetter H, Katz M, Schmidt W and Kemler R (1985) The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 87: 27-45.
14. Drab M, Haller H, Bychkow R, Erdmann B, Lindschau C, Haase H, Morano I, Luft FC and Wobus AM (1997) From totipotent embryonic stem cells to spontaneously contracting vascular smooth muscle cells: a retinoic acid and db-cAMP in vitro differentiation model. FASEB J 11: 905-915.
15. Eistetter HR (1989) Pluripotent embryonal stem cell lines can be established from disaggregated mouse morulae. Dev GrowthDiffer 31: 275-282.
16. Evans MJ and Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292: 154-156.
17. 1 integrin gene expression in mice. Genes Dev 9:1896-1908.
18. 1 integrin. J Cell Sci 109: 2989-2999.
19. Forrester LM, Nagy A, Sam W, Watt A, Stevenson L, Bernstein A, Joyner AL and Wurst W (1996) An induction of gene trap screen in embryonic stem cells-identification of genes that respond to retinoic acid in vitro. Proc Natl Acad Sci USA 93: 1677-1682.
20. Fraichard A, Chassande O, Bilbaut G, Dehay C, Savatier P and Samarut J (1995) In vitro differentiation of embryonic stem cells into glial cells and functional neurons. J Cell Sci 108: 3181-3188.
21. Fürst DO, Osborn M, Nave R and Weber K (1988) The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line. J Cell Biol 106: 1563-1572.
22. Gardner RL and Brook FA (1997) Reflections on the biology of embryonic stem (ES) cells. Int J Dev Biol 41: 235-243.
23. Hamill OP, Marty A, Neher E, Sakmann B and Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391: 85-100.
24. Helgason CD, Sauvageau G, Lawrence HJ, Largman C and Humphries RK (1996) Overexpression of HOXB4 enhances the hematopoieti c potential of embryonic stem cells differentiated in vitro. Blood 87: 2740-2749.
25. Hescheler J, Fleischmann BK, Lentini S, Maltsev VA, Rohwedel J, Wobus AM and Addicks K (1997) Embryonic stem cells a model to study structural and functional properties in cardiomyogenesis. Cardiovasc Res 36: 149-162.
26. Hogan BLM, Thaller C and Eichele G (1992) Evidence that Hensen's node is a site of retinoic acid synthesis. Nature 359: 237-241.
27. Hole N and Smith AG (1994) Embryonic stem cells and hematopoiesis. In: Culture of hematopoietic cells, (pp. 235-249) Wiley-Liss, Inc.
28. Hong Y, Winkler C and Schartl M (1996) Pluripotentcy and differentiation of embryonic stem cell lines from the medakafish (Oryzias latipes). Mech Dev 60: 33-44.
29. Itoh F, Nakane T and Chiba S (1997) Gene expression of MASH-1, MATH-1, neuroD and NSCL-2, basic helix-loop-helix proteins, during neural differentiation in P19 embryonal carcinoma cells Tohoku J Exp Med 182: 327-336.
30. Jacob A, Budhiraja Sand Reichel RR (1997) Differential induction of HNF-3 transcription factors during neuronal differentiation. Exp Cell Res 234: 277-284.
31. Johansson BM and Wiles MW (1995) Evidence for involvement of Activin A and bone morphogenetic protein 4 in mammalian mesoderm and hematopoietic development. Mol Cell Biol 15: 141-151.
32. Keller GM (1995) In vitro differentiation of embryonic stem cells. Curr Opin Cell Biol 7: 862-869.
33. Klug MG, Soonpa MH, Koh GY and Field LJ(1996) Genetically selected cardiomyocytes from differentiating embryonic stem cells form stable intracardiac grafts. J Clin Invest 98: 216-224.
34. Koh GY, Kim S-J, Klug M, Park K, Soonpa MH and Field L (1995) Targeted expression of transforming growth factor-ß1 in intracardiac grafts promotes vascular endothelial cell DNA synthesis. J Clin Invest 95: 114-121.
35. Lin Q, Schwarz J, Bucana C and Olson EN (1997) Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276: 1404-1407.
36. Lints TJ, Parsons LM, Hartley L, Lyons I and Harvey RP (1993) Nkx-2.5: a nova murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119: 419-431.
37. Maltsev VA, Rohwedel J, Hescheler J and Wobus AM (1993) Embryonic stem cells differentiate in vitro into cardiomyocytes representing sinusnodal, atrial and ventricular cell types. Mech Dev 44: 41-50.
38. Maltsev VA, Wobus AM, Rohwedel J, Bader M and Hescheler J (1994) Cardiomyocytes differentiated in vitro from embryonic stem cells developmentally express cardiac-specific genes and ionic currents. Circ Res 75: 233-244.
39. Maltsev VA, Ji GJ, Wobus AM, Fleischmann BK and Hescheler J: Establishment of β-adrenergic modulation of L-type calcium current in the early stages of cardiomyocyte development (submitted)
40. Marshall H, Morrison A, Studer M, Pöpperl H and Krumlauf R (1996) Retinoids and Hox genes. FASEB J 10: 969-978.
41. Martin GR (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Nat Acad Sci USA 78: 7634-7638.
42. Martin GR and Evans M J (1975) Differentiation of donal lines of teratocarcinoma cells: formation of embryoid bodies in vitro. Proc Natl Acad Sci USA 72: 1441-1445.
43. Miano JM, Cserjesi P, Ligon KL, Periasamy M and Olson EN (1994) Smooth muscle myosin heavy chain exclusively marks the smooth muscle lineage during mouse embryogenesis. Circ Res 75: 803-812.
44. Miller-Hance WC, LaCorbiere M, Fuller SJ, Evans SM, Lyons G, Schmidt C, Robbins J and Chien KR (1993) In vitro chamber specification during embryonic stem cell cardiogenesis. J Biol Chem 268: 25244-25252.
45. Molkentin JD, Lin Q, Duncan SA and Olson EN (1997) Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev 11: 1061-1072.
46. Monk M (1990) Changes in DNA methylation during mouse embryonic development in relation to X-chromosome activity and imprinting. Philos Trans R Soc Lond B Biol Sci 326: 299-312.
47. Muscat GE, Rea S and Downes M (1995) Identification of a regulatory function for an orphan receptor in muscle: COUPTF II affects the expression of the myoD gene family during myogenesis. Nucleic Acids Res 23: 1311-1318.
48. Nagy A, Rossant J, Nagy R, Abramow-Newerly W and Roder JC (1993) Derivation of completely cell culture-derived mice from early passage embryonic stem cells. Proc Natl Acad Sci USA 90: 8424-8428.
49. Okabe S, Forsberg-Nilsson K, Spiro AC, Segal M and McKay RD (1996) Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech Dev 59: 89-102.
50. Pain B, Clark ME, Shen M, Nakazawa H, Sakurai M, Samarut J and Etches RJ (1996) Long-term in vitro culture and characterization of avian embryonic stem cells with multiple morphogenetic potentialities. Development 122: 2339-2348.
51. Palmiter RD, Brinster RL, Hammer RE, Trumbauer ME, Rosenfeld MG, Birnberg NC and Evans RM (1982) Dramatic growth of mice that develop from eggs microinjected with metallothioneingrowth hormone fusion genes. Nature 300: 611-615.
52. Reh U, Pütz D and Wobus AM (1997) Screening method for the measurement of chronotropic effects on cardiac cells. Bioforum 20: 536-540.
53. Potocnik AJ, Kohler H and Eichmann K (1997) Hemato-lymphoid in vivo reconstitution potential of subpopulations derived from in vitro differentiated embryonic stem cells. Proc Natl Acad USA 94: 10295-10300.
54. Resnick JL, Bixler LS, Cheng L and Donovan PJ (1992) Long-term proliferation of mouse primordial germ cells in culture. Nature 359: 550-551.
55. Risau W, Sariola H, Zerwes HG, Sasse J, Ekblom P, Kemler R and Doetschman T (1988) Vasculogenesis and angiogenesis in embryonic stem cell-derived embryoid bodies. Development 102: 471-478.
56. Rohwedel J, Maltsev V, Bober E, Arnold HH, Hescheler J and Wobus AM (1994) Muscle cell differentiation of embryonic stem cells reflects myogenesis in vivo: Developmentally regulated expression of myogenic determination genes and functional expression of ionic currents. Dev Biol 164: 87-101.
57. Rohwedel J, Horak V, Hebrok M, Füchtbauer EM and Wobus AM (1995) M-twist expression inhibits mouse embryonic stem cell-derived myogenic differentiation in vitro. Exp Cell Res 220: 92-100.
58. Rohwedel J, Sehlmeyer U, Jin S, Meister A and Wobus AM (1996) Primordial germ cell-derived mouse embryonic germ (EG) cells in vitro resemble undifferentiated stem cells with respect to differentiation capacity and cell cycle distribution. Cell Biol Inter 20: 579-587.
59. Rohwedel J, Kleppisch T, Pich U, Guan K, Jin S, Zuschratter W, Hopf C, Hoch W, Hescheler J, Witzemann V and Wobus AM (1998a) Formation of postsynaptic-like membranes during differentiation of embryonic stem cells in vitro. Exp Cell Res 239: 214-225.
60. 1 integrin function results in a retardation of myogenic, but an acceleration of neuronal differentiation of embryonic stem cells in vitro. Dev Biol 201 (in press).
61. Rose O, Rohwedel J, Reinhardt S, Bachmann M, Cramer M, Rotter M, Wobus AM, Starzinski-Powitz A (1994) Expression of M-cadherin protein in myogenic cells during prenatal mouse development and differentiation of embryonic stem cells in culture. Dev Dyn 201: 245-259.
62. Rudnicki MA and McBurney MW (1987) Cell culture methods and induction of differentiation of embryonal carcinoma cell lines. In: Robertson EJ (ed.) Teratocarcinomas and embryonic stem cells - a practical approach, (pp. 19-49) IRL Press Oxford, Washington DC, USA.
63. Rust EM, Westfall MV, Samuelson LC and Metzger JM (1997) Gene transfer into mouse embryonic stem cell-derived cardiac myocytes mediated by recombinant adenovirus. In Vitro Cell Dev Biol, Anim 33: 270-276.
64. Sauer H, Hofmann C, Wartenberg M, Wobus AM and Hescheler J (1998) Spontaneous calcium oscillations in embryonic stem cell-derived primitive endodermal cells. Exp Cell Res 238: 13-22.
65. Scholer HR, Dressler GR, Balling R, Rohdewohld H and Gruss P (1990) Oct-4: A germline-specific transcription factor mapping to the mouset-complex. EMBO J 9: 2185-2195.
66. Schoonjans L, Albright GM, Li JL, Collen D and Moreadith RW (1996) Pluripotential rabbit embryonic stem (ES) cells are capable of forming overt coat color chimeras following injection into blastocysts. Mol Reprod Dev 45: 439-443.
67. Solter D and Knowles BB (1978) Monodonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc Natl Acad Sci USA 75: 5565-5569.
68. Soudais C, Bielinska M, Heikinheimo M, MacArthur CA, Narita N, Saffitz JE, Simon MC, Leiden JM and Wilson DB (1995) Targeted mutagenesis of the transcription factor GATA-4 gene in mouse embryonic stem cells disrupts visceral endoderm differentiation in vitro. Development 121: 3877-3888.
69. Spielmann H, Pohl I, Döring B, Liebsch M and Moldenhauer F (1997) The embryonic stem cell test (EST), an in vitro embryotoxicity test using two permanent mouse cell lines: 3T3 fibroblasts and embryonic stem cells. In: Van Zutphen LFM and Balls M (eds) Animal Alternatives, Welfare and Ethics, (pp. 663-669) Elsevier Science Amsterdam.
70. Srivastava D, Cserjesi P and Olson EN (1995) A subclass of bHLH protei ns required for cardiac morphogenesis. Science 270: 1995-1999.
71. Stevens LC (1984) Germ cell origin of testicular and ovarian teratomas. Transplant Proc 16: 502-504.
72. Stewart CL, Gadi I and Bhatt H (1994) Stem cells from primordial germ cells can reenter the germ line. Dev Biol 161: 626-628.
73. Strübing C, Ahnert-Hilger G, Jin S, Wiedenmann B, Hescheler J and Wobus AM (1995) Differentiation of pluripotent embryonic stem cells into the neuronal lineage in vitro gives rise to mature inhibitory and excitatory neurons. Mech Dev 53: 275-287.
74. Thomas KR and Capecchi M R (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51 503-512.
75. Weitzer G, Milner DJ, Kim JU, Bradley A and Capetanaki Y (1995) Cytoskeletal control of myogenesis a desmin null mutation blocks the myogenic pathway during embryonic stem cell differentiation. Dev Biol 172: 422-439.
76. Wheeler MB (1994) Development and validation of swine embryonic stem cells a review. Reprod Fertil Dev 6: 563-568.
77. Wiles MV and Keller G (1991) Multiple hematopoietic lineages develop from embryonic stem (ES) cells in culture. Development 111: 259-267.
78. Wobus AM, Holzhausen H, Jäkel P and Schöneich J (1984) Characterization of a pluripotent stem cell line derived from a mouse embryo. Exp Cell Res 152: 212-219.
79. 2+ channel blockers. Differentiation 48: 173-182.
80. Wobus AM, Rohwedel J, Maltsev V and Hescheler J (1994a) In vitro differentiation of embryonic stem cells into cardiomyocytes or skeletal muscle cells is specifically modulated by retinoic acid. Roux's Arch Dev Biol 204: 36-45.
81. 2+ channels. In Vitro Cell Dev Biol, Anim 30A: 425-434.
82. Wobus AM, Rohwedel J, Maltsev V and Hescheler J (1995) Development of cardiomyocytes expressing cardiac-specific genes, action potentials, and ionic channels during embryonic stem cell-derived cardiogenesis. Ann N Y Acad Sci 752: 460-469.
83. Wobus AM, Rohwedel J, Strübing C, Jin S, Adler K, Maltsev V and Hescheler J (1997a) In vitro differentiation of embryonic stem cells In: Klug S and Thiel R (eds) Methods in Developmental Toxicology and Biology, (pp. 1-17) Blackwell Science Berlin Vienna.
84. Wobus AM, Guan K, Shan J, Wellner MC, Rohwedel J, Ji G, Fleischmann B, Katus HA, Hescheler J and Franz WM (1997b) Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J Mol Cell Cardiol 29: 1525-1539.
85. Wobus AM and Guan K (1998) Embryonic stem cell-derived cardiac differentiation: Modulation of differentiation and 'loss of function' analysis in vitro. Trends Cardiovasc Med 8: 64-74.
86. Wobus AM, Guan K and Pich U: In vitro differentiation of embryonic stem cells and analysis of cellular phenotypes, "Gene knockout protocols", In: Methods in Molecular Biology, Humana Press, Inc. (submitted).
87. Wong H, Anderson WD, Cheng T and Riabowol KT (1994) Monitoring mRNA expression by polymerase chain reaction: the "primer-dropping" method. Anal Biochem 223: 251-258.