Istinct regulatory elements control muscle-specific, fiber-type-selective, and axially graded expression of a myosin light-chain gene in transgenic mice

Molecular and Cellular Biology

Volumn 16, Issue 7, 1996, Pages 3909-3922

  Rao, Mala V ^a,b   Donoghue, Maria J ^a,c   Merlie, John P ^a   Sanes, Joshua R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUS MUSCULUS;

ALPHA ACTIN; BETA GALACTOSIDASE; DEOXYRIBONUCLEASE I; HOMEODOMAIN PROTEIN; MYOGENIC FACTOR; MYOSIN LIGHT CHAIN;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; DNA FOOTPRINTING; EMBRYO; ENHANCER REGION; FAST MUSCLE FIBER; GENE EXPRESSION REGULATION; GENE MAPPING; INTERCOSTAL MUSCLE; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATOR GENE; SLOW MUSCLE FIBER; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; BASE SEQUENCE; CHLORAMPHENICOL O-ACETYLTRANSFERASE; CROSSES, GENETIC; DEOXYRIBONUCLEASE I; DNA FOOTPRINTING; DNA PRIMERS; EMBRYO; EMBRYONIC AND FETAL DEVELOPMENT; ENHANCER ELEMENTS (GENETICS); FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; MUSCLE FIBERS; MUSCLE, SKELETAL; MUTAGENESIS, SITE-DIRECTED; MYOSIN LIGHT CHAINS; ORGAN SPECIFICITY; POLYMERASE CHAIN REACTION; PROMOTER REGIONS (GENETICS); RECOMBINANT PROTEINS; REGULATORY SEQUENCES, NUCLEIC ACID; TRANSFECTION;

EID: 0030006881     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.7.3909     Document Type: Article

References (95)

1. Amacher, S. L., J. N. Buskin, and S. D. Hauschka. 1993. Multiple regulatory elements contribute differentially to muscle creatine kinase enhancer activity in skeletal and cardiac muscle. Mol. Cell. Biol. 13:2753-2764.
2. Aronow, B. J., C. A. Ebert, M. T. Valerius, S. S. Potter, D. A. Wiginton, D. P. Witte, and J. J. Hutton. 1995. Dissecting a locus control region: facilitation of enhancer function by extended enhancer-flanking sequences. Mol. Cell. Biol. 15:1123-1135.
3. Asakura, A., A. Fujisawa-Sehara, T. Komiya, Y. Nabeshima, and Y.-I. Nabeshima. 1993. MyoD and myogenin act on the chicken myosin light-chain 1 gene as distinct transcriptional factors. Mol. Cell. Biol. 13:7153-7162.
4. Banerjee-Basu, S., and A. Buonanno. 1993. cis-acting sequences of the rat troponin I slow gene confer tissue- and development-specific transcription in cultured muscle cells as well as fiber type specificity in transgenic mice. Mol. Cell. Biol. 13:7019-7028.
5. r gene cap sites is sufficient for differentiation-dependent expression. Mol. Cell. Biol. 8:1361-1365.
6. Black, B. L., J. F. Martin, and E. N. Olson. 1995. The mouse MRF4 promoter is transactivated directly and indirectly by muscle-specific transcription factors. J. Biol. Chem. 270:2889-2892.
7. Bradford, M. M. 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.
8. Braun, T., E. Tannich, G. Buschhausen-Denker, and H.-H. Arnold. 1989. Promoter upstream elements of the chicken cardiac myosin light-chain 2-A gene interact with trans-acting regulatory factors for muscle-specific transcription. Mol. Cell. Biol. 9:2513-2515.
9. Brennan, K. J., and E. C. Hardeman. 1993. Quantitative analysis of the human α-skeletal actin gene in transgenic mice. J. Biol. Chem. 268:719-725.
10. Buckingham, M. 1992. Making muscle in mammals. Trends Genet. 8:144-149.
11. Buskin, J. N., and S. D. Hauschka. 1989. Identification of a myocyte nuclear factor that binds to the muscle-specific enhancer of the mouse muscle creatine kinase gene. Mol. Cell. Biol. 9:2627-2640.
12. Chen, C., and H. Okayama. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
13. Cheng, T.-C., M. C. Wallace, J. P. Merlie, and E. N. Olson. 1993. Separable regulatory elements governing myogenin transcription in mouse embryogenesis. Science 261:215-218.
14. Christ, B., and C. P. Ordahl. 1995. Early stages of chick somite development. Anal. Embryol. 191:381-396.
15. Corin, S. J., L. K. Levitt, J. V. O'Mahoney, J. E. Joya, E. C. Hardeman, and R. Wade. 1995. Delineation of a slow-twitch-myofiber-spccific transcriptional element by using in vivo somatic gene transfer. Proc. Natl. Acad. Sci. USA 92:6185-6189.
16. Cserjesi, P., and E. N. Olson. 1991. Myogenin induces the myocyte-specific enhancer binding factor MEF-2 independently of other muscle-specific gene products. Mol. Cell. Biol. 11:4854-4862.
17. Cunningham, J. M., K. K. Kaiser, and J. R. Sanes. 1991. Rostrocaudal variation of fiber type composition in rat intercostal muscles. Histochemistry 95:513-517.
18. Daubas, P., A. Klarsfeld, I. Farner, C. Pinset, R. Cox, and M. Buckingham. 1988. Functional activity of the two promoters of the myosin alkali light chain gene in primary muscle cell cultures: comparison with other muscle gene promoters and other culture systems. Nucleic Acids Res. 16:1251-1271.
19. Daubas, P., B. Robert, I. Garner, and M. Buckingham. 1985. A comparison between mammalian and avian fast skeletal muscle alkali myosin light chain genes: regulatory implications. Nucleic Acids Res. 13:4623-4643.
20. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
21. Donoghue, M. J., J. D. Alvarez, J. P. Merlie, and J. R. Sanes. 1991. Fiber-type- and position-dependent expression of a myosin light chain-chloram-phenicol acetyltransferase (CAT) transgene detected with a novel histochemical stain for CAT. J. Cell Biol. 115:423-434.
22. Donoghue, M., H. Ernst, B. Wentworth, B. Nadal Ginard, and N. Rosenthal. 1988. A muscle specific enhancer is located at the 3′ end of the myosin light chain 1/3 gene locus. Genes Dev. 2:1779-1790.
23. Donoghue, M. J., J. P. Merlie, N. Rosenthal, and J. R. Sanes. 1991. A rostrocaudal gradient of transgene expression in adult skeletal muscle. Proc. Natl. Acad. Sci. USA 88:5847-5851.
24. Donoghue, M. J., R. Morris-Valero, Y. R. Johnson, J. P. Merlie, and J. R. Sanes. 1992. Mammalian muscle cells bear a cell autonomous, heritable memory of their rostrocaudal position. Cell 69:67-77.
25. Donoghue, M. J., B. L. Patton, J. R. Sanes, and J. P. Merlie. 1992. An axial gradient of transgene methylation in murine skeletal muscle: genomic imprint of rostrocaudal position. Development 116:1101-1112.
26. Donoghue, M. J., and J. R. Sanes. 1994. All muscles are not created equal. Trends Genet. 10:396-401.
27. Forrester, W. C., C. V. Genderen, T. Jenuwin, and R. Grosschedl. 1994. Dependence of enhancer-mediated transcription of the immunoglobulin μ gene on nuclear matrix attachment regions. Science 265:1221-1225.
28. Fujisawa-Sehara, A., Y. Nabeshima, T. Komiya, T. Uetsuki, A. Asakura, and Y. Nabeshima. 1992. Differential trans-activation of muscle-specific regulatory elements including the myosin light chain box by chicken MyoD, myogenin, and MRF4. J. Biol. Chem. 267:10031-10038.
29. Gehring, W. J., Y. Q. Qian, M. Billeter, K. Furukubo-Tokunaga, A. F. Schier, D. Resendez-Perez, M. Affolter, G. Otting, and K. Wüthrich. 1994. Homeodomain-DNA recognition. Cell 78:211-223.
30. Gorman, C. M., L. F. Moffat, and B. H. Howard. 1982. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2:1044-1051.
31. Gossett, L., D. J. Kelvin, E. A. Sternberg, and E. N. Olson. 1989. A new myocyte-specific enhancer-binding factor that recognizes a conserved element associated with multiple muscle-specific genes. Mol. Cell. Biol. 9:5022-5033.
32. Grieshammer, L., D. Sassonn, and N. Rosenthal. 1992. A transgene target for positional regulators marks early rostrocaudal specification of myogenic lineages. Cell 69:79-93.
33. Haack, H., and P. Gruss. 1993. The establishment of murine Hox-1 expression domains during patterning of the limb. Dev. Biol. 157:410-422.
34. Hallauer, P. L., H. L. Bradshaw, and K. E. M. Hastings. 1993. Complex fiber-type-specific expression of fast skeletal muscle troponin I gene constructs in transgenic mice. Development 119:691-701.
35. Hallauer, P. L., K. E. M. Hastings, and A. C. Peterson. 1988. Fast skeletal muscle-specific expression of a quail troponin I gene in transgenic mice. Mol. Cell. Biol. 8:5072-5079.
36. Hanley, T., and J. P. Merlie. 1991. Transgene detection in unpurified mouse tail DNA by polymerase chain reaction. BioTechniques 10:56.
37. Hayashi, S., and M. P. Scott. 1990. What determines the specificity of action of Drosophila homeodomain proteins? Cell 63:883-894.
38. Hemsley, A., N. Arnheim, M. D. Toney, G. Cortopossi, and D. J. Galas. 1989. A simple method for site-directed mutagenesis using polymerase chain reaction. Nucleic Acids Res. 17:6545-6551.
39. Hoey, T., and M. Levine. 1988. Divergent homeobox proteins recognize similar DNA sequences in Drosophila. Nature (London) 332:858-861.
40. Hogan, B., F. Constantini, and E. Lacy. 1986. Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
41. Hughes, S. M., J. M. Taylor, S. J. Tapscott, C. M. Gurley, W. J. Carter, and C. A. Peterson. 1993. Selective accumulation of MyoD and myogenin mRNAs in fast and slow adult skeletal muscle is controlled by innervation and hormones. Development 118:1137-1147.
42. Johnson, J. E., B. J. Wold, and S. D. Hauschka. 1989. Muscle creatine kinase sequence elements regulating skeletal and cardiac muscle expression in transgenic mice. Mol. Cell. Biol. 9:3393-3399.
43. Kelly, R., S. Alonso, S. Tajbakhsh, G. Cossu, and M. Buckingham. 1995. Myosin light chain 3F regulatory sequences confer regionalized cardiac and skeletal muscle expression in transgenic mice. J. Cell Biol. 129:383-396.
44. Knotts, S., H. Rindt, J. Neumann, and J. Robbins. 1994. In vivo regulation of the mouse β myosin heavy chain gene. J. Biol. Chem. 269:31275-31282.
45. Kothary, R., S. Clapoff, S. Darling, M. D. Perry, L. A. Moran, and J. Rossant. 1989. Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development 105:707-714.
46. Lamson, G., and F. E. Stockdale. 1989. Developmental and muscle-specific changes in methylation of the myosin light chain LC1f and LC3f promoters during avian myogenesis. Dev. Biol. 132:62-68.
47. Laskowski, M. B., and J. R. Sanes. 1987. Topographic mapping of motor pools onto skeletal muscles. J. Neurosci. 7:252-260.
48. Laskowski, M. B., and J. R. Sanes. 1988. Topographically selective reinnervation of adult mammalian skeletal muscles. J. Neurosci. 8:3094-3099.
49. Lassar, A. B., J. N. Buskin, D. Lockshon, R. L. Davis, S. Apone, S. D. Hauschka, and H. Weintraub. 1989. MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell 58:823-831.
50. Levi, G., M. T. Corsetti, E. Boncinelli, and G. Corte. 1993. Changes in the prevalence of an homeobox gene product during muscle differentiation. Mech. Dev. 43:111-120.
51. Levitt, L. K., J. V. O'Mahoney, K. J. Brennan, J. E. Joya, L. Zhu, R. P. Wade, and E. C. Hardeman. 1995. The human troponin I slow promoter directs slow fiber-specific expression in transgenic mice. DNA Cell Biol. 14:599-607.
52. Li, H., and Y. Capetanaki. 1994. An E box in the desmin promoter cooperates with the E box and MEF-2 sites of a distal enhancer to direct muscle-specific transcription. EMBO J. 13:3580-3589.
53. Lyons, G. E., M. Ontell, R. Cox, D. Sassoon, and M. Buckingham. 1990. The expression of myosin genes in developing skeletal muscle in the mouse embryo. J. Cell Biol. 111:1465-1476.
54. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
55. Maxam, A. M., and W. Gilbert. 1980. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 65:499-560.
56. Mercer, H. E., G. W. Hoyle, R. P. Kapur, R. I. Brinster, and R. D. Palmiter. 1991. Dopamine β-hydroxylase gene promoter directs expression of E. coli lacZ 10 sympathetic and other neurons in adult transgenic mice. Neuron 7:703-716.
57. Merlie, J. P., and J. M. Kornhauser. 1989. Neuronal regulation of gene expression by an acetylcholine receptor promoter in muscles of transgenic mice. Neuron 2:1295-1300.
58. Merlie, J. P., J. Mudd, T.-C. Cheng, and E. N. Olson. 1994. Myogenin and acetylcholine receptor α gene promoters mediate transcriptional regulation in response to motor innervation. J. Biol. Chem. 269:2461-2467.
59. Michelson, A. M. 1994. Muscle pattern diversification in Drosophila is determined by the autonomous function of homeotic genes in the embryonic mesoderm. Development 120:755-768.
60. Miner, J. H., J. B. Miller, and B. J. Wold. 1992. Skeletal muscle phenotypes initiated by ectopic MyoD in transgenic mouse heart. Development 114:853-860.
61. Mulle, C., P. Benoit, C. Pinset, M. Roa, and J.-P. Changeux. 1988. Calcitonin gene-related peptide enhances the rate of desensitization of the nicotinic acetylcholine receptor in cultured mouse muscle cells. Proc. Natl. Acad. Sci. USA 85:5728.
62. Murre, C., P. S. McCaw, and D. Baltimore. 1989. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 56:777-783.
63. Nabeshima, Y., Y. Fujii-Kuriyama, M. Muramatsu, and K. Ogata. 1984. Alternative transcription and two modes of splicing result in two myosin light chains from one gene. Nature (London) 308:333-338.
64. Naidu, P. S., D. C. Lndolph, R. Q. To, T. J. Hinterberger, and S. F. Konieczny. 1995. Myogenin and MEF2 function synergistically to activate the MRF4 promoter during myogenesis. Mol. Cell. Biol. 15:2707-2718.
65. Niederrelther, K., R. N. D'Souza, and B. de Crombrugge. 1992. Minimal DNA sequences that control the cell lineage-specific expression of the proalpha2(1) collagen promoter in transgenic mice. J. Cell Biol. 119:1361-1370.
66. Nikovits, W., Jr., J. H. Mar, and C. P. Ordahl. 1990. Muscle-specific activity of the skeletal troponin I promoter requires interaction between upstream regulatory sequences and elements contained within the first transcribed exon. Mol. Cell. Biol. 10:3468-3482.
67. 66a.Olson, E. N. Personal communication.
68. Olson, E. N., and W. H. Klein. 1994. bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev. 8:1-8.
69. Olson, E. N., M. Perry, and R. A. Schulz. 1995. Regulation of muscle differentiation by the MEF2 family of MADS box transcription factors. Dev. Biol. 172:2-14.
70. Ontell, M. P., M. M. Sopper, G. Lyons, M. Buckingham, and M. Ontell. 1993. Modulation of contractile protein gene expression in fetal murine crural muscles: emergence of muscle diversity. Dev. Dyn. 198:203-213.
71. Pajak, L., M. Mariappan, and D. F. Wieczorek. 1991. Reprognimming of myosin light chain 1/3 expression in muscle heterokaryons. Dev. Biol. 145:28-34.
72. Pankratz, M. J., and H. Jäckle. 1990. Making stripes in the Drosophila embryo. Trends Genet. 6:287-292.
73. Pellerin, I., C. Schnabel, K. M. Catron, and C. Abate. 1994. Hox proteins have different affinities for a consensus DNA site that correlate with the positions of their genes on the hox cluster. Mol. Cell. Biol. 14:4532-4545.
74. Periasamy, M., E. Strehler, L. Garfinkel, R. Gubtis, N. Ruiz-Opazo, and B. Nadal-Ginard. 1984. Fast skeletal muscle myosin light chains 1 and 3 are produced from a single gene by a combined process of differential RNA transcription and splicing. J. Biol. Chem. 259:13595-13604.
75. Petropoulos, C. J., M. P. Rosenberg, N. A. Jenkins, N. G. Copeland, and S. H. Hughes. 1989. The chicken skeletal alpha-actin promoter is tissue specific in transgenic mice. Mol. Cell. Biol. 9:3785-3792.
76. Pette, D., and U. Schnez. 1977. Myosin light chain patterns of individual fast and slow-twitch fibres of rabbit muscles. Histochemistry 54:97-107.
77. Pette, D., and R. S. Staron. 1993. The molecular diversity of mammalian muscle fibers. News Phys. Sci. 8:153-157.
78. 76a.Rao, M. V. Unpublished data.
79. Robert, B., P. Daubas, M.-A. Akimenko, A. Cohen, I. Garner, J.-L. Guenet, and M. Buckingham. 1984. A single locus in the mouse encodes both myosin light chains 1 and 3, a second locus corresponds to a related pseudogene. Cell 39:129-140.
80. Rosenthal, N., E. B. Berglund, B. M. Wentworth, M. Donoghue, B. Winter, E. Bober, T. Braun, and H. H. Arnold. 1990. A highly conserved enhancer downstream of the human MLC1/3 locus is a target for multiple myogenic determination factors. Nucleic Acids Res. 18:6239-6246.
81. Rosenthal, N., J. M. Kornhauser, M. Donoghue, K. Rosen, and J. P. Merlie. 1989. Myosin light chain enhancer activates muscle specific, developmentally regulated gene expression in transgenic mice. Proc. Natl. Acad. Sci. USA 86:7780-7784.
82. Rudnicki, M. A., T. Braun, S. Hinuma, and R. Jaenisch. 1992. Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71:383-390.
83. Salminen, M., P. Maire, J.-P. Concordet, C. Moch, A. Porteu, A. Kahn, and D. Daegelen. 1994. Fast-muscle-specific expression of human aldolase A transgenes. Mol. Cell. Biol. 14:6797-6808.
84. Sanes, J. R., M. J. Donoghue, M. C. Wallace, and J. P. Merlie. 1992. Rostrocaudal differences among muscles revealed by a transgene: graded expression at low copy number. Cold Spring Harbor Symp. Quant. Biol. 57:451-460.
85. Sanes, J. R., P. T. Kotzbauer, J. Mudd, T. Hanley, J.-C. Martinou, and J. P. Merlie. 1991. Selective expression of an acetylcholine receptor-lacZ transgene in synaptic nuclei of adult muscle fibers. Development 113:1181-1191.
86. Sanes, J. R., J. L. R. Rubenstein, and J.-F. Nicolas. 1986. Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J. 5:3133-3142.
87. Schoenherr, C. J., and D. J. Anderson. 1995. Silencing is golden: negative regulation in the control of neuronal gene transcription. Curr. Opinion Neurobiol. 5:566-571.
88. Seidel, U., and H. H. Arnold. 1989. Identification of the functional promoter regions in the human gene encoding the myosin alkali light chains MLC1 and MLC3 of fast skeletal muscle. J. Biol. Chem. 264:16109-16117.
89. Shani, M. 1985. Tissue-specific expression of rat myosin light-chain 2 gene in transgenic mice. Nature (London) 314:283-286.
90. Staron, R. S., and D. Pette. 1987. The multiplicity of combinations of myosin light chains and heavy chains in histochemically typed single fibres. Biochem. J. 243:695-699.
91. Slockdale, F. E. 1992. Myogenic cell lineages. Dev. Biol. 154:284-298.
92. Wentworth, B., M. Donoghue, J. C. Engert, E. B. Berglund, and N. Rosenthal. 1991. Paired MyoD binding sites regulate myosin light chain gene expression. Proc. Natl. Acad. Sci. USA 88:1242-1246.
93. Wigston, D. J., and J. R. Sanes. 1982. Selective reinnervation of adult mammalian muscles by axons from different segmental levels. Nature (London) 299:464-467.
94. Wigston, D. J., and J. R. Sanes. 1985. Selective reinnervation of rat intercostal muscles transplanted from different segmental levels to a common site. J. Neurosci. 5:1208-1221.
95. Yu, L., R. J. LaPilla, and N. Davidson. 1986. Mouse muscle nicotinic acetylcholine receptor gamma subunit: cDNA sequence and gene expression. Nucleic Acids Res. 14:3539-3555.