Xenopus oocytes reactivate muscle gene transcription in transplanted somatic nuclei independently of myogenic factors

Development

Volumn 136, Issue 16, 2009, Pages 2695-2703

  Biddle, Adrian ^a,b,c   Simeoni, Ilenia ^a,b   Gurdon, J B ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Muscle genes; Reprogramming; Xenopus oocytes

Indexed keywords

ALPHA AMANITIN; INHIBITOR OF DIFFERENTIATION PROTEIN; MESSENGER RNA; MYOD PROTEIN; MYODA PROTEIN; MYODB PROTEIN; MYOGENIC FACTOR; MYOGENIN; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL NUCLEUS TRANSPLANTATION; CONTROLLED STUDY; EMBRYO; GENE ACTIVATION; GENE EXPRESSION; GENE INDUCTION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HALF LIFE TIME; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN CONTENT; SOMATIC CELL; TRANSCRIPTION INITIATION; XENOPUS LAEVIS;

ANIMALS; CELL NUCLEUS; CELLS, CULTURED; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MUSCLES; MYOD PROTEIN; MYOGENIC REGULATORY FACTORS; NUCLEAR TRANSFER TECHNIQUES; OOCYTES; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; XENOPUS LAEVIS; XENOPUS PROTEINS;

AMPHIBIA;

EID: 69049093919     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.036327     Document Type: Article

References (38)

1. Azuara, V., Perry, P., Sauer, S., Spivakov, M., Jorgensen, H. F., John, R. M., Gouti, M., Casanova, M., Warnes, G., Merkenschlager, M. et al. (2006). Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8, 532-538.
2. Benezra, R., Davis, R. L., Lockshon, D., Turner, D. L. and Weintraub, H. (1990). The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61, 49-59.
3. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K. et al. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326.
4. Blau, H. M., Chiu, C. P. and Webster, C. (1983). Cytoplasmic activation of human nuclear genes in stable heterocaryons. Cell 32, 1171-1180.
5. Byrne, J. A., Simonsson, S., Western, P. S. and Gurdon, J. B. (2003). Nuclei of adult mammalian somatic cells are directly reprogrammed to oct-4 stem cell gene expression by amphibian oocytes. Curr. Biol. 13, 1206-1213.
6. Carlsson, S. A., Ringertz, N. R. and Savage, R. E. (1974). Intracellular antigen migration in interspecific myoblast heterokaryons. Exp. Cell Res. 84, 255-266.
7. Charbonnier, F., Gaspera, B. D., Armand, A. S., Van der Laarse, W. J., Launay, T., Becker, C., Gallien, C. L. and Chanoine, C. (2002). Two myogenin-related genes are differentially expressed in Xenopus laevis myogenesis and differ in their ability to transactivate muscle structural genes. J. Biol. Chem. 277, 1139-1147.
8. Ciosk, R., DePalma, M. and Priess, J. R. (2006). Translational regulators maintain totipotency in the Caenorhabditis elegans germline. Science 311, 851-853.
9. Davidson, E. H. (1986). Gene Activity in Early Development. Academic Press: New York.
10. De Robertis, E. M., Partington, G. A., Longthorne, R. F. and Gurdon, J. B. (1977). Somatic nuclei in amphibian oocytes: evidence for selective gene expression. J. Embryol. Exp. Morphol. 40, 199-214.
11. Della Gaspera, B., Sequeira, I., Charbonnier, F., Becker, C., Shi, D. L. and Chanoine, C. (2006). Spatio-temporal expression of MRF4 transcripts and protein during Xenopus laevis embryogenesis. Dev. Dyn. 235, 524-529.
12. Eddy, E. M. and O'Brien, D. A. (1998). Gene expression during mammalian meiosis. Curr. Top. Dev. Biol. 37, 141-200.
13. Efroni, S., Duttagupta, R., Cheng, J., Dehghani, H., Hoeppner, D. J., Dash, C., Bazett-Jones, D. P., Le Grice, S., McKay, R. D., Buetow, K. H. et al. (2008). Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2, 437-447.
14. Gurdon, J. B. (1962). The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. J. Embryol. Exp. Morphol. 10, 622-640.
15. Gurdon, J. B., Brennan, S., Fairman, S. and Mohun, T. J. (1984). Transcription of muscle-specific actin genes in early Xenopus development: nuclear transplantation and cell dissociation. Cell 38, 691-700.
16. Gurdon, J. B., Kao, K., Kato, K. and Hopwood, N. D. (1992). Muscle gene activation in Xenopus requires intercellular communication during gastrula as well as blastula stages. Dev. Suppl. 137-142.
17. Harvey, R. P. (1990). The Xenopus MyoD gene: an unlocalised maternal mRNA predates lineage-restricted expression in the early embryo. Development 108, 669-680.
18. Humpherys, D., Eggan, K., Akutsu, H., Friedman, A., Hochedlinger, K., Yanagimachi, R., Lander, E. S., Golub, T. R. and Jaenisch, R. (2002). Abnormal gene expression in cloned mice derived from embryonic stem cell and cumulus cell nuclei. Proc. Natl. Acad. Sci. USA 99, 12889-12894.
19. Jennings, C. G. (1992). Expression of the myogenic gene MRF4 during Xenopus development. Dev. Biol. 151, 319-332.
20. Kablar, B., Krastel, K., Ying, C., Asakura, A., Tapscott, S. J. and Rudnicki, M. A. (1997). MyoD and Myf-5 differentially regulate the development of limb versus trunk skeletal muscle. Development 124, 4729-4738.
21. Kleene, K. C. (2001). A possible meiotic function of the peculiar patterns of gene expression in mammalian spermatogenic cells. Mech. Dev. 106, 3-23.
22. Langlands, K., Yin, X., Anand, G. and Prochownik, E. V. (1997). Differential interactions of Id proteins with basic-helix-loop-helix transcription factors. J. Biol. Chem. 272, 19785-19793.
23. Lassar, A. B., Davis, R. L., Wright, W. E., Kadesch, T., Murre, C., Voronova, A., Baltimore, D. and Weintraub, H. (1991). Functional activity of myogenic HLH proteins requires hetero-oligomerization with E12/E47-like proteins in vivo. Cell 66, 305-315.
24. McKnight, S. L. and Gavis, E. R. (1980). Expression of the herpes thymidine kinase gene in Xenopus laevis oocytes: an assay for the study of deletion mutants constructed in vitro. Nucleic Acids Res. 8, 5931-5948.
25. Messenger, N. J., Kabitschke, C., Andrews, R., Grimmer, D., Nunez Miguel, R., Blundell, T. L., Smith, J. C. and Wardle, F. C. (2005). Functional specificity of the Xenopus T-domain protein Brachyury is conferred by its ability to interact with Smad1. Dev. Cell 8, 599-610.
26. Nicolas, N., Gallien, C. L. and Chanoine, C. (1998). Expression of myogenic regulatory factors during muscle development of Xenopus: myogenin mRNA accumulation is limited strictly to secondary myogenesis. Dev. Dyn. 213, 309-321.
27. Pomerantz, J. and Blau, H. M. (2004). Nuclear reprogramming: a key to stem cell function in regenerative medicine. Nat. Cell Biol. 6, 810-816.
28. Rashbass, J., Taylor, M. V. and Gurdon, J. B. (1992). The DNA-binding protein E12 co-operates with XMyoD in the activation of muscle-specific gene expression in Xenopus embryos. EMBO J. 11, 2981-2990.
29. Rupp, R. A. and Weintraub, H. (1991). Ubiquitous MyoD transcription at the midblastula transition precedes induction-dependent MyoD expression in presumptive mesoderm of X. laevis. Cell 65, 927-937.
30. Seydoux, G. and Braun, R. E. (2006). Pathway to totipotency: lessons from germ cells. Cell 127, 891-904.
31. Surani, M. A., Hayashi, K. and Hajkova, P. (2007). Genetic and epigenetic regulators of pluripotency. Cell 128, 747-762.
32. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K. and Yamanaka, S. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872.
33. Terranova, R., Pereira, C. F., Du Roure, C., Merkenschlager, M. and Fisher, A. G. (2006). Acquisition and extinction of gene expression programs are separable events in heterokaryon reprogramming. J. Cell Sci. 119, 2065-2072.
34. Wakefield, L. and Gurdon, J. B. (1983). Cytoplasmic regulation of 5S RNA genes in nuclear-transplant embryos. EMBO J. 2, 1613-1619.
35. Weintraub, H., Tapscott, S. J., Davis, R. L., Thayer, M. J., Adam, M. A., Lassar, A. B. and Miller, A. D. (1989). Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc. Natl. Acad. Sci. USA 86, 5434-5438.
36. Weintraub, H., Davis, R., Tapscott, S., Thayer, M., Krause, M., Benezra, R., Blackwell, T. K., Turner, D., Rupp, R., Hollenberg, S. et al. (1991). The myoD gene family: nodal point during specification of the muscle cell lineage. Science 251, 761-766.
37. Wickens, M. P. and Gurdon, J. B. (1983). Post-transcriptional processing of simian virus 40 late transcripts in injected frog oocytes. J. Mol. Biol. 163, 1-26.
38. Zhou, Q., Brown, J., Kanarek, A., Rajagopal, J. and Melton, D. A. (2008). In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455, 627-632.