Quantitative Proteomic Identification of Six4 as the Trex-Binding Factor in the Muscle Creatine kinase Enhancer

Molecular and Cellular Biology

Volumn 24, Issue 5, 2004, Pages 2132-2143

  Himeda, Charis L ^a   Ranish, Jeffrey A ^b   Angello, John C ^a   Maire, Pascal ^c   Aebersold, Ruedi ^b   Hauschka, Stephen D ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^c INSTITUT COCHIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BINDING PROTEIN; CREATINE KINASE MM; DNA FRAGMENT; MICROSPHERE; OLIGONUCLEOTIDE; REGULATOR PROTEIN; SIX4 PROTEIN; TRANSCRIPTION FACTOR; TREX BINDING FACTOR; UNCLASSIFIED DRUG;

ADOLESCENT; ALDOLASE A GENE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CARDIAC TROPONIN C GENE; CELL CULTURE; CHICK EMBRYO; EMBRYO; ENHANCER REGION; GEL MOBILITY SHIFT ASSAY; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE MUTATION; HEART MUSCLE; HUMAN; HUMAN CELL; MAGNET; MAGNETIC BEAD; MCK GENE; MOUSE; MUSCLE; MUSCLE CELL; MUSCLE DEVELOPMENT; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN FAMILY; PROTEIN PURIFICATION; PROTEOMICS; QUANTITATIVE ANALYSIS; QUANTITATIVE PROTEOMICS; REGULATOR GENE; SKELETAL MUSCLE; TRANSCRIPTION REGULATION; TRANSCRIPTION REGULATORY ELEMENT X; TRANSGENICS;

ANIMALS; CELLS, CULTURED; CHICK EMBRYO; CREATINE KINASE; CREATINE KINASE, MM FORM; DNA-BINDING PROTEINS; ENHANCER ELEMENTS (GENETICS); GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, REGULATOR; HELA CELLS; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOMAGNETIC SEPARATION; ISOENZYMES; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; MYOCYTES, CARDIAC; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PROTEOMICS; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 1342282907     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.5.2132-2143.2004     Document Type: Article

References (54)

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. 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.
3. 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.
4. 2+/GTP sensor in exocytotic secretion. Proc. Natl. Acad. Sci. USA 93:10797-10802.
5. Chen, C. Y., and R. J. Schwartz. 1997. Competition between negative acting YY1 versus positive acting serum response factor and tinman homologue Nkx-2.5 regulates cardiac alpha-actin promoter activity. Mol. Endocrinol. 11:812-822.
6. Christensen, T., and L. Kedes. 1999. The myogenic regulatory circuit that controls cardiac/slow twitch troponin C gene transcription in skeletal muscle involves E-box, MEF-2, and MEF-3 motifs. Gene Expr. 8:247-261.
7. 1 phase and is repressed by fibroblast growth factor. J. Cell Biol. 105:949-956.
8. Davidson, I., C. Fromental, P. Augereau, A. Wildeman, M. Zenke, and P. Chambon. 1986. Cell-type specific protein binding to the enhancer of simian virus 40 in nuclear extracts. Nature 323:544-548.
9. 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.
10. Donoviel, D. B., M. A. Shield, J. N. Buskin, H. S. Haugen, C. H. Clegg, and S. D. Hauschka. 1996. Analysis of muscle creatine kinase gene regulatory elements in skeletal and cardiac muscles of transgenic mice. Mol. Cell. Biol. 16:1649-1658.
11. Eng, J. K., A. L. McCormack, and J. R. Yates. 1994. An approach to correlate tandem spectral data of peptides with amino acid sequences in protein databases. J. Am. Soc. Mass Spectrom. 5:976-989.
12. Fabre-Suver, C., and S. D. Hauschka. 1996. A novel site in the muscle creatine kinase enhancer is required for expression in skeletal but not cardiac muscle. J. Biol. Chem. 271:4646-4652.
13. Farrance, I. K. G., J. H. Mar, and C. P. Ordahl. 1992. M-CAT binding factor is related to the SV40 enhancer binding factor, TEF-1. J. Biol. Chem. 267:17234-17240.
14. Flink, I. L., and E. Morkin. 1995. Alternatively processed isoforms of cellular nucleic acid-binding protein interact with a suppressor region of the human β-myosin heavy chain gene. J. Biol. Chem. 270:6959-6965.
15. Fougerousse, F., M. Durand, S. Lopez, L. Suel, J. Demignon, C. Thornton, H. Ozaki, K. Kawakami, P. Barbet, J. S. Beckmann, and P. Maire. 2002. Six and Eya expression during human somitogenesis and MyoD gene family activation. J. Muscle Res. Cell. Motil. 23:255-264.
16. Gabrielsen, O. S., and J. Huet. 1993. Magnetic DNA affinity purification of yeast transcription factor. Methods Enzymol. 218:508-525.
17. Gygi, S. P., B. Rist, S. A. Gerber, F. Turecek, M. H. Gelb, and R. Aebersold. 1999. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 17:994-999.
18. Hamburger, V., and H. L. Hamilton. 1992. A series of normal stages in the development of the chick embryo. Dev. Dyn. 195:231-272.
19. Han, D. K., J. Eng, H. Zhou, and R. Aebersold. 2001. Quantitative profiling of differentiation-induced microsomal proteins using isotope-coded affinity tags and mass spectrometry. Nat. Biotechnol. 19:946-951.
20. Hauser, M. A., A. Robinson, D. Hartigan-O'Connor, D. A. Williams-Gregory, J. N. Buskin, S. Apone, C. J. Kirk, S. Hardy, S. D. Hauschka, and J. S. Chamberlain. 2000. Analysis of muscle creatine kinase regulatory elements in recombinant adenoviral vectors. Mol. Ther. 2:16-25.
21. Hidaka, K., I. Yamamoto, Y. Arai, and T. Mukai. 1993. The MEF-3 motif is required for MEF-2-mediated skeletal muscle-specific induction of the rat aldolase A gene. Mol. Cell. Biol. 13:6469-6478.
22. Horlick, R. A., and P. A. Benfield. 1989. The upstream muscle-specific enhancer of the rat muscle creatine kinase gene is composed of multiple elements. Mol. Cell. Biol. 9:2396-2413.
23. Itoh, S., Y. Katoh, H. Konishi, N. Takaya, T. Kimura, M. Periasamy, and H. Yamaguchi. 2001. Nitric oxide regulates smooth-muscle-specific myosin heavy chain gene expression at the transcriptional level-possible role of SRF and YY1 through CArG element. J. Mol. Cell. Cardiol. 33:95-107.
24. Jaynes, J. B., J. E. Johnson, J. N. Buskin, C. L. Gartside, and S. D. Hauschka. 1988. The muscle creatine kinase gene is regulated by multiple upstream elements, including a muscle-specific enhancer. Mol. Cell. Biol. 8:62-70.
25. 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.
26. Karasseva, N., G. Tsika, J. Ji, A. Zhang, X. Mao, and R. Tsika. 2003. Transcription enhancer factor-1 binds multiple muscle MEF2 and A/T-rich elements during fast-to-slow skeletal muscle fiber type transitions. Mol. Cell. Biol. 23:5143-5164.
27. Kawakami, K., H. Ohto, K. Ikeda, and R. G. Roeder. 1996. Structure, function and expression of a murine homeobox protein AREC3, a homologue of Drosophila sine oculis gene product, and implication in development. Nucleic Acids Res. 24:303-310.
28. Keller, A., A. I. Nesvizhskii, E. Kolker, and R. Aebersold. 2002. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74:5383-5392.
29. 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.
30. Martin, K. A., A. Gualberto, M. F. Kolman, J. Lowry, and K. Walsh. 1997. A competitive mechanism of CArG element regulation by YY1 and SRF: implications for assessment of Phox1/MHox transcription factor interactions at CArG elements. DNA Cell Biol. 16:653-661.
31. Merika, M., and S. H. Orkin. 1993. DNA-binding specificity of GATA family transcription factors. Mol. Cell. Biol. 13:3999-4010.
32. Michelotti, E. F., T. Tomonaga, H. Krutzsch, and D. Levens. 1995. Cellular nucleic acid binding protein regulates the CT element of the human c-myc protooncogene. J. Biol. Chem. 270:9494-9499.
33. Molkentin, J. D., B. L. Black, J. F. Martin, and E. N. Olson. 1995. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 83:1125-1136.
34. Mueller, P. R., and B. Wold. 1989. In vivo footprinting of a muscle specific enhancer by ligation mediated PCR. Science 246:780-786.
35. Nesvizhskii, A. I., A. Keller, E. Kolker, and R. Aebersold. 2003. A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75:4646-4658.
36. Nguyen, Q.-G. V., J. N. Buskin, C. L. Himeda, C. Fabre-Suver, and S. D. Hauschka. 2003. Transgenic and tissue culture analyses of the muscle creatine kinase enhancer Trex control element in skeletal and cardiac muscle indicate differences in gene expression between muscle types. Transgenic Res. 12:337-349.
37. Niiya, A., H. Ohto, K. Kawakami, and M. Araki. 1998. Localization of Six4/AREC3 in the developing mouse retina; implications in mammalian retinal development. Exp. Eye Res. 67:699-707.
38. Ohto, H., S. Kamada, K. Tago, S. I. Tominaga, H. Ozaki, S. Sato, and K. Kawakami. 1999. Cooperation of Six and Eya in activation of their target genes through nuclear translocation of Eya. Mol. Cell. Biol. 19:6815-6824.
39. Ohto, H., T. Takizawa, T. Saito, M. Kobayashi, K. Ikeda, and K. Kawakami. 1998. Tissue and developmental distribution of Six family gene products. Int. J. Dev. Biol. 42:141-148.
40. Parmacek, M. S., H. I. Ip, F. Jung, T. L. Shen, J. F. Martin, A. J. Vora, E. N. Olson, and J. M. Leiden. 1994. A novel myogenic regulatory circuit controls slow/cardiac troponin C gene transcription in skeletal muscle. Mol. Cell. Biol. 14:1870-1885.
41. Rajavashisth, T. B., A. K. Taylor, A. Andalibi, K. L. Svenson, and A. J. Lusis. 1989. Identification of a zinc finger protein that binds to the sterol regulatory element. Science 245:640-643.
42. Ranish, J. A., E. C. Yi, D. M. Leslie, S. O. Purvine, D. R. Goodlett, J. Eng, and R. Aebersold. 2003. The study of macromolecular complexes by quantitative proteomics. Nat. Genet. 33:349-355.
43. Salminen, M., S. Lopez, P. Maire, A. Kahn, and D. Daegelen. 1996. Fast-muscle-specific DNA-protein interactions occurring in vivo at the human aldolase A M promoter are necessary for correct promoter activity in transgenic mice. Mol. Cell. Biol. 16:76-85.
44. Shield, M. A., H. S. Haugen, C. H. Clegg, and S. D. Hauschka. 1996. E-box sites and a proximal regulatory region of the muscle creatine kinase gene differentially regulate expression in diverse skeletal muscles and cardiac muscle of transgenic mice. Mol. Cell. Biol. 16:5058-5068.
45. Spitz, F., J. Demignon, A. Poreu, A. Kahn, J.-P. Concordet, D. Daegelen, and P. Maire. 1998. Expression of myogenin during embryogenesis is controlled by Six/sine oculis homeoproteins through a conserved MEF3 binding site. Proc. Natl. Acad. Sci. USA 95:14220-14225.
46. Spitz, F., M. Salminen, J. Demignon, A. Kahn, D. Daegelen, and P. Maire. 1997. A combination of MEF3 and NFI proteins activates transcription in a subset of fast-twitch muscles. Mol. Cell. Biol. 17:656-666.
47. Sternberg, E. A., G. Spizz, W. M. Perry, D. Vizard, T. Weil, and E. N. Olson. 1988. Identification of upstream and ihtragenic regulatory elements that confer cell-type-restricted and differentiation-specific expression on the muscle creatine kinase gene. Mol. Cell. Biol. 8:2896-2909.
48. Stewart, A. F. R., S. B. Larkin, I. K. G. Farrance, J. H. Mar, D. E. Hall, and C. P. Ordahl. 1994. Muscle-enriched TEF-1 isoforms bind M-CAT elements from muscle-specific promoters and differentially activate transcription. J. Biol. Chem. 269:3147-3150.
49. Suzuki-Yagawa, Y., K. Kawakami, and K. Nagano. 1992. Housekeeping Na, K-ATPase alpha 1 subunit gene promoter is composed of multiple cis elements to which common and cell type-specific factors bind. Mol. Cell. Biol. 12:4046-4055.
50. Trask, R. V., A. W. Strauss, and J. J. Billadello. 1988. Developmental regulation and tissue-specific expression of the human muscle creatine kinase gene. J. Biol. Chem. 263:17142-17149.
51. Xiao, J. H., I. Davidson, H. Matthes, J. M. Garnier, and P. Chambon. 1991. Cloning, expression, and transcriptional properties of the human enhancer factor TEF-1. Cell 65:551-568.
52. Xu, P. X., I. Woo, H. Her, D. R. Beier, and R. L. Maas. 1997. Mouse Eya homologues of the Drosophila eyes absent gene require Pax6 for expression in lens and nasal placode. Development 124:219-231.
53. Yi, J.-M., K. Walsh, and P. Schimmel. 1991. Rabbit muscle creatine kinase: genomic cloning, sequencing, and analysis of upstream sequences important for expression in myocytes. Nucleic Acids Res. 19:3027-3033.
54. Zahradka, P., D. E. Larson, and B. H. Sells. 1989. RNA polymerase II-directed gene transcription by rat skeletal muscle nuclear extracts. Exp. Cell Res. 185:8-20.