Gene recombination in postmitotic cells: Targeted expression of Cre recombinase provokes cardiac-restricted, site-specific rearrangement in adult ventricular muscle in vivo

Journal of Clinical Investigation

Volumn 100, Issue 1, 1997, Pages 169-179

  Agah, Ramtin ^a   Frenkel, Peter A ^a   French, Brent A ^b   Michael, Lloyd H ^a   Overbeek, Paul A ^a   Schneider, Michael D ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b University of Louisville School of Medicine   (United States)

Author keywords

Adenovirus; Cardiac muscle; Cre recombinase; Homologous recombination; Transgenic mice

Indexed keywords

MYOSIN HEAVY CHAIN;

ADENOVIRUS; AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; EXPRESSION VECTOR; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC RECOMBINATION; GROWTH REGULATION; HEART VENTRICLE WALL; MITOSIS RATE; MOUSE; MUSCLE GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; TRANSGENIC MOUSE;

EID: 0030878260     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119509     Document Type: Article

References (54)

1. Rajewsky, K., H. Gu, R. Kuhn, U.A.K. Betz, W. Muller, J. Roes, and F. Schwenk. 1996. Conditional gene targeting. J. Clin. Invest. 98:600-603.
2. Lee, E.Y.H.P., C.Y. Chang, N.P. Hu, Y.C.J. Wang, C.C. Lai, K. Herrup, W.H. Lee, and A. Bradley. 1992. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature (Lond.). 359:288-294.
3. Letterio, J.J., A.G. Geiser, A.B. Kulkarni, N.S. Roche, M.B. Sporn, and A.B. Roberts. 1994. Maternal rescue of transforming growth factor-beta 1 null mice. Science (Wash. DC). 264:1936-1938.
4. Diebold, R.J., M.J. Eis, M. Yin, I. Ormsby, G.P. Boivin, B.J. Darrow, J.E. Saffitz, and T. Doetschman. 1995. Early-onset multifocal inflammation in the transforming growth factor β1-null mouse is lymphocyte mediated. Proc. Natl. Acad. Sci. USA. 92:12215-12219.
5. O'Gorman, S., D.T. Fox, and G.M. Wahl. 1991. Recombinase-mediated gene activation and site-specific integration in mammalian cells. Science (Wash. DC). 251:1351-1355.
6. Walters, M.C., W. Magis, S. Fiering, J. Eidemiller, D. Scalzo, M. Groudine, and D.I. Martin. 1996. Transcriptional enhancers act in cis to suppress position-effect variegation. Genes Dev. 10:185-195.
7. Dymecki, S.M. 1996. Flp recombinase promotes site-specific DNA recombination in embryonic stem cells and transgenic mice. Proc. Natl. Acad. Sci. USA. 93:6191-6196.
8. Sauer, B., and N. Henderson. 1988. Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. Proc. Natl. Acad. Sci. USA. 85:5166-5170.
9. Fukushige, S., and B. Sauer. 1992. Genomic targeting with a positive-selection lox integration vector allows highly reproducible gene expression in mammalian cells. Proc. Natl. Acad. Sci. USA. 89:7905-7909.
10. Lakso, M., B. Sauer, B. Mosinger, Jr., E.J. Lee, R.W. Manning, S.H. Yu, K.L. Mulder, and H. Westphal. 1992. Targeted oncogene activation by site-specific recombination in transgenic mice. Proc. Natl. Acad. Sci. USA. 89:6232-6236.
11. Orban, P.C., D. Chui, and J.D. Marth. 1992. Tissue-and site-specific DNA recombination in transgenic mice. Proc. Natl. Acad. Sci. USA. 89:6861-6865.
12. Baubonis, W., and B. Sauer. 1993. Genomic targeting with purified Cre recombinase. Nucleic Acids Res. 21:2025-2029.
13. Sauer, B. 1993. Manipulation of transgenes by site-specific recombination: use of Cre recombinase. Methods Enzymol. 225:890-900.
14. Van. D.J., M. Fornerod, R.B. Van, and G. Grosveld. 1995. Cre-mediated site-specific translocation between nonhomologous mouse chromosomes. Proc. Natl. Acad. Sci. USA. 92:7376-7380.
15. Smith, A.J., S.M.A. De, B. Kwabi-Addo, A. Heppell-Parton, H. Impey, and P. Rabbitts. 1995. A site-directed chromosomal translocation induced in embryonic stem cells by Cre-loxP recombination. Nat. Genet. 9:376-385.
16. Metzger, D., J. Clifford, H. Chiba, and P. Chambon. 1995. Conditional site-specific recombination in mammalian cells using a ligand-dependent chimeric Cre recombinase. Proc. Natl. Acad. Sci. USA. 92:6991-6995.
17. Gu, H., J.D. Marth, P.C. Orban, H. Mossman, and K. Rajewsky. 1994. Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science (Wash. DC). 265:103-106.
18. Kühn, R., F. Schwenk, M. Aguet, and K. Rajewsky. 1995. Inducible gene targeting in mice. Science (Wash. DC). 269:1427-1429.
19. Soonpaa, M.H., K.K. Kim, L. Pajak, M. Franklin, and L.J. Field. 1996. Cardiomyocyte DNA synthesis and binucleation during murine development. Am. J. Physiol. 40:H2183-H2189.
20. Wang, P., M. Anton, F.L. Graham, and S. Bacchetti. 1995. High frequency recombination between loxP sites in human chromosomes mediated by an adenovirus vector expressing Cre recombinase. Somatic Cell Mol. Genet. 21:429-441.
21. Subramaniam, A., W.K. Jones, J. Gulick, S. Wert, J. Neumann, and J. Robbins. 1991. Tissue-specific regulation of the alpha-myosin heavy chain gene promoter in transgenic mice. J. Biol. Chem. 266:24613-24620.
22. Abdellatif, M., W.R. MacLellan, and M.D. Schneider. 1994. p21 Ras as a governor of global gene expression. J. Biol. Chem. 269:15423-15426.
23. Araki, K., M. Araki, J. Miyazaki, and P. Vassalli. 1995. Site-specific recombination of a transgene in fertilized eggs by transient expression of Cre recombinase. Proc. Natl. Acad. Sci. USA. 92:160-164.
24. Taketo, M., A.C. Schroeder, L.E. Mobraaten, K.B. Gunning, G. Hanten, R.R. Fox, T.H. Roderick, C.L. Stewart, F. Lilly, C.T. Hansen, and P.A. Overbeek. 1991. FVB/N: an inbred mouse strain preferable for transgenic analyses. Proc. Natl. Acad. Sci. USA. 88:2065-2069.
25. French, B.A., W. Mazur, N.M. Ali, R.S. Geske, J.P. Finnigan, G.P. Rodgers, R. Roberts, and A.E. Raizner. 1994. Percutaneous transluminal in vivo gene transfer by recombinant adenovirus in normal porcine coronary arteries, atherosclerotic arteries, and two models of coronary restenosis. Circulation. 90:2402-2413.
26. Bett, A.J., W. Haddara, L. Prevec, and F.L. Graham. 1994. An efficient and flexible system for construction of adenovirus vectors with insertions or deletions in early regions 1 and 3. Proc. Natl. Acad. Sci. USA. 91:8802-8806.
27. Graham, F.L., and L. Prevec. 1991. Manipulation of adenovirus vectors. In Gene Transfer and Expression Protocols. Vol. 7. E. J. Murray, editor. Humana Press, Inc., Totowa, NJ. 109-127.
28. Anton, M., and F.L. Graham. 1995. Site-specific recombination mediated by an adenovirus vector expressing the Cre recombinase protein: a molecular switch for control of gene expression. J. Virol. 69:4600-4606.
29. Michael, L.H., M.L. Entman, C.J. Hartley, K.A. Youker, J. Zhu, S.R. Hall, H.K. Hawkins, K. Bernes, and C.M. Ballantyne. 1995. Myocardial ischemia and reperfusion: a murine model. Am. J. Physiol. 269:H2147-H2154.
30. Brand, T., W.R. MacLellan, and M.D. Schneider. 1993. A dominant-negative receptor for type-beta transforming growth factors created by deletion of the kinase domain. J. Biol. Chem. 268:11500-11503.
31. Eustice, D.C., P.A. Feldman, P.A.M. Colberg, R.M. Buckery, and R.H. Neubauer. 1991. A sensitive method for the detection of beta-galactosidase in transfected mammalian cells. Biotechniques. 11:739-740.
32. Bradford, M.A. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
33. Seed, B., and J.Y. Sheen. 1988. A simple phase-extraction assay for chloramphenicol acyltransferase activity. Gene (Amst.). 67:271-277.
34. Ausubel, F.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl. 1994. Current Protocols in Molecular Biology. John Wiley & Sons, Inc., New York.
35. Hogan, B., R. Beddington, F. Costantini, and E. Lacy. 1994. Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 497 pp.
36. Subramaniam, A., J. Gulick, J. Neumann, S. Knotts, and J. Robbins. 1993. Transgenic analysis of the thyroid-responsive elements in the alpha-cardiac myosin heavy chain gene promoter. J. Biol. Chem. 268:4331-4336.
37. Yang, Y., K.U. Jooss, Q. Su, H.C.J. Ertl, and J.M. Wilson. 1996. Immune responses to viral antigens versus transgene product in the elimination of recombinant adenovirus-infected hepatocytes in vivo. Gene Ther. 3:137-144.
38. Kirshenbaum, L.A., W.R. MacLellan, W. Mazur, B.A. French, and M.D. Schneider. 1993. Highly efficient gene transfer to adult rat ventricular myocytes by recombinant adenovirus. J. Clin. Invest. 92:381-387.
39. Kass-Eisler, A., E. Falck-Pedersen, M. Alvira, J. Rivera, P.M. Buttrick, B.A. Wittenberg, L. Cipriani, and L.A. Leinwand. 1993. Quantitative determination of adenovirus-mediated gene delivery to rat cardiac myocytes in vitro and in vivo. Proc. Natl. Acad. Sci. USA. 90:11498-11502.
40. Stratford-Perricaudet, L.D., I. Makeh, M. Perricaudet, and P. Briand. 1992. Widespread long-term gene transfer to mouse skeletal muscles and heart. J. Clin. Invest. 90:626-630.
41. Fishman, G.I., M.L. Kaplan, and P.M. Buttrick. 1994. Tetracycline-regulated cardiac gene expression in vivo. J. Clin. Invest. 93:1864-1868.
42. Leiden, J.M. 1995. Gene therapy - promise, pitfalls, and prognosis. N. Engl. J. Med. 333:871-873.
43. Fisher, K.J., H. Choi, J. Burda, S.J. Chen, and J.M. Wilson. 1996. Recombinant adenovirus deleted of all viral genes for gene therapy of cystic fibrosis. Virology. 217:11-22.
44. Kochanek, S., P.R. Clemens, K. Mitani, H.H. Chen, S. Chan, and C.T. Caskey. 1996. A new adenoviral vector: replacement of all viral coding sequences with 28 kb of DNA independently expressing both full-length dystrophin and beta-galactosidase. Proc. Natl. Acad. Sci. USA. 93:5731-5736.
45. Gilgenkrantz, H., D. Duboc, V. Juillard, D. Couton, A. Pavirani, J.G. Guillet, P. Briand, and A. Kahn. 1995. Transient expression of genes transferred in vivo into heart using first-generation adenoviral vectors: role of the immune response. Hum. Gene Ther. 6:1265-1274.
46. Yang, Y., and J.M. Wilson. 1996. CD40 ligand-dependent T cell activation: requirement of B7-CD28 signaling through CD40. Science (Wash. DC). 273:1862-1864.
47. Kass-Eisler, A., E. Falckpedersen, D.H. Elfenbein, M. Alvira, P.M. Buttrick, and L.A. Leinwand. 1994. The impact of developmental stage, route of administration and the immune system on adenovirus-mediated gene transfer. Gene Ther. 1:395-402.
48. Yang, Y.P., Q. Su, I.S. Grewal, R. Schilz, R.A. Flavell, and J.M. Wilson. 1996. Transient subversion of CD40 ligand function diminishes immune responses to adenovirus vectors in mouse liver and lung tissues. J. Virol. 70:6370-6377.
49. Yang, Y., G. Trinchieri, and J.M. Wilson. 1995. Recombinant IL-12 prevents formation of blocking IgA antibodies to recombinant adenovirus and allows repeated gene therapy to mouse lung. Nat. Med. 1:890-893.
50. Lyons, G.E., S. Schiaffino, S. Sassoon, P. Barton, and M. Buckingham. 1990. Developmental regulation of myosin gene expression in normal mouse cardiac muscle. J. Cell Biol. 111:2427-2436.
51. Sands, A.T., T.N. Hansen, F.J. Demayo, L.A. Stanley, L. Xin, and R.J. Schwartz. 1993. Cytoplasmic beta-actin promoter produces germ cell and preimplantation embryonic transgene expression. Mol. Reprod. Dev. 34:117-126.
52. Soonpaa, M.H., G.Y. Koh, M.G. Klug, and L.J. Field. 1994. Formation of nascent intercalated disks between grafted fetal cardiomyocytes and host myocardium. Science (Wash. DC). 264:98-101.
53. Bronson, S.K., E.G. Plaehn, K.D. Kluckman, J.R. Hagaman, N. Maeda, and O. Smithies. 1996. Single-copy transgenic mice with chosen-site integration. Proc. Natl. Acad Sci. USA. 93:9067-9072.
54. Wang, Y., L.A. Krushel, and G.M. Edelman. 1996. Targeted DNA recombination in vivo using an adenovirus carrying the Cre recombinase gene. Proc. Natl. Acad. Sci. USA. 93:3932-3936.