In Vivo Footprinting of a Muscle Specific Enhancer by Ligation Mediated PCR
10.1126/science.2814500
Crossref journal-article
American Association for the Advancement of Science (AAAS)
Science (221)
Abstract

In vivo protein-DNA interactions at the developmentally regulated enhancer of the mouse muscle creatine kinase (MCK) gene were examined by a newly developed polymerase chain reaction (PCR) footprinting procedure. This ligation mediated, single-sided PCR technique permits the exponential amplification of an entire sequence ladder. Several footprints were detected in terminally differentiated muscle cells where the MCK gene is actively transcribed. None were observed in myogenic cells prior to differentiation or in nonmuscle cells. Two footprints appear to correspond to sites that can bind the myogenic regulator MyoD1 in vitro, whereas two others represent muscle specific use of apparently general factors. Because MyoD1 is synthesized by undifferentiated myoblasts, these data imply that additional regulatory mechanisms must restrict the interaction between this protein and its target site prior to differentiation.

Bibliography

Mueller, P. R., & Wold, B. (1989). In Vivo Footprinting of a Muscle Specific Enhancer by Ligation Mediated PCR. Science, 246(4931), 780–786.

Authors 2
  1. Paul R. Mueller (first)
  2. Barbara Wold (additional)
References 59 Referenced 718
  1. BANERJI, J, A LYMPHOCYTE-SPECIFIC CELLULAR ENHANCER IS LOCATED DOWNSTREAM OF THE JOINING REGION IN IMMUNOGLOBULIN HEAVY-CHAIN GENES, CELL 33: 729 (1983). (10.1016/0092-8674(83)90015-6) / CELL (1983)
  2. BRAUN, T, A NOVEL HUMAN-MUSCLE FACTOR RELATED TO BUT DISTINCT FROM MYOD1 INDUCES MYOGENIC CONVERSION IN 10T1/2 FIBROBLASTS, EMBO JOURNAL 8: 701 (1989). (10.1002/j.1460-2075.1989.tb03429.x) / EMBO JOURNAL (1989)
  3. BRAUN, T, PROMOTER UPSTREAM ELEMENTS OF THE CHICKEN CARDIAC MYOSIN LIGHT-CHAIN 2-A GENE INTERACT WITH TRANS-ACTING REGULATORY FACTORS FOR MUSCLE-SPECIFIC TRANSCRIPTION, MOLECULAR AND CELLULAR BIOLOGY 9: 2513 (1989). / MOLECULAR AND CELLULAR BIOLOGY (1989)
  4. BUSKIN, J. B., JOURNAL OF CELL BIOLOGY 107: 98a (1988). / JOURNAL OF CELL BIOLOGY (1988)
  5. BUSKIN, J.N., IDENTIFICATION OF A MYOCYTE NUCLEAR FACTOR THAT BINDS TO THE MUSCLE-SPECIFIC ENHANCER OF THE MOUSE MUSCLE CREATINE-KINASE GENE, MOLECULAR AND CELLULAR BIOLOGY 9: 2627 (1989). / MOLECULAR AND CELLULAR BIOLOGY (1989)
  6. CAUDY, M, DAUGHTERLESS, A DROSOPHILA GENE ESSENTIAL FOR BOTH NEUROGENESIS AND SEX DETERMINATION, HAS SEQUENCE SIMILARITIES TO MYC AND THE ACHAETE-SCUTE COMPLEX, CELL 55: 1061 (1988). (10.1016/0092-8674(88)90250-4) / CELL (1988)
  7. CHAMBERLAIN, J.S., REGULATION OF CREATINE-KINASE INDUCTION IN DIFFERENTIATING MOUSE MYOBLASTS, MOLECULAR AND CELLULAR BIOLOGY 5: 484 (1985). / MOLECULAR AND CELLULAR BIOLOGY (1985)
  8. 10.1073/pnas.81.7.1991
  9. 10.1126/science.3353714
  10. CRONMILLER, C, MOLECULAR CHARACTERIZATION OF DAUGHTERLESS, A DROSOPHILA SEX DETERMINATION GENE WITH MULTIPLE ROLES IN DEVELOPMENT, GENES & DEVELOPMENT 2: 1666 (1988). (10.1101/gad.2.12a.1666) / GENES & DEVELOPMENT (1988)
  11. DAVIDSON, I, CELL-TYPE SPECIFIC PROTEIN-BINDING TO THE ENHANCER OF SIMIAN VIRUS-40 IN NUCLEAR EXTRACTS, NATURE 323: 544 (1986). (10.1038/323544a0) / NATURE (1986)
  12. DAVIS, R.L., EXPRESSION OF A SINGLE TRANSFECTED CDNA CONVERTS FIBROBLASTS TO MYOBLASTS, CELL 51: 987 (1987). (10.1016/0092-8674(87)90585-X) / CELL (1987)
  13. DEPINHO, R.A., THE HUMAN MYC GENE FAMILY - STRUCTURE AND ACTIVITY OF L-MYC AND AN L-MYC PSEUDOGENE, GENES & DEVELOPMENT 1: 1311 (1987). (10.1101/gad.1.10.1311) / GENES & DEVELOPMENT (1987)
  14. DESPLAN, C, THE SEQUENCE SPECIFICITY OF HOMEODOMAIN-DNA INTERACTION, CELL 54: 1081 (1988). (10.1016/0092-8674(88)90123-7) / CELL (1988)
  15. EDMONDSON, D.G., A GENE WITH HOMOLOGY TO THE MYC SIMILARITY REGION OF MYOD1 IS EXPRESSED DURING MYOGENESIS AND IS SUFFICIENT TO ACTIVATE THE MUSCLE DIFFERENTIATION PROGRAM, GENES & DEVELOPMENT 3: 628 (1989). (10.1101/gad.3.5.628) / GENES & DEVELOPMENT (1989)
  16. 10.1126/science.3917574
  17. FORS L unpublished data.
  18. FROHMAN, M.A., RAPID PRODUCTION OF FULL-LENGTH CDNAS FROM RARE TRANSCRIPTS - AMPLIFICATION USING A SINGLE GENE-SPECIFIC OLIGONUCLEOTIDE PRIMER, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 85: 8998 (1988). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1988)
  19. Gilbert, W., Conttrol of Ribosome Sytnthesis: 139 (1976). / Conttrol of Ribosome Sytnthesis (1976)
  20. GINIGER, E, SPECIFIC DNA-BINDING OF GAL4, A POSITIVE REGULATORY PROTEIN OF YEAST, CELL 40: 767 (1985). (10.1016/0092-8674(85)90336-8) / CELL (1985)
  21. GUNNING, P, DIFFERENTIAL PATTERNS OF TRANSCRIPT ACCUMULATION DURING HUMAN MYOGENESIS, MOLECULAR AND CELLULAR BIOLOGY 7: 4100 (1987). / MOLECULAR AND CELLULAR BIOLOGY (1987)
  22. HOEY, T, DIVERGENT HOMEO BOX PROTEINS RECOGNIZE SIMILAR DNA-SEQUENCES IN DROSOPHILA, NATURE 332: 858 (1988). (10.1038/332858a0) / NATURE (1988)
  23. 10.1126/science.3310230
  24. HORLICK, R.A., THE UPSTREAM MUSCLE-SPECIFIC ENHANCER OF THE RAT MUSCLE CREATINE-KINASE GENE IS COMPOSED OF MULTIPLE ELEMENTS, MOLECULAR AND CELLULAR BIOLOGY 9: 2396 (1989). / MOLECULAR AND CELLULAR BIOLOGY (1989)
  25. HUIBREGTSE, J.M., DIRECT IDENTIFICATION OF SMALL SEQUENCE CHANGES IN CHROMOSOMAL DNA, GENE 44: 151 (1986). (10.1016/0378-1119(86)90056-9) / GENE (1986)
  26. 10.1016/0092-8674(87)90152-8
  27. JACKSON, P.D., A METHOD FOR MAPPING INTRANUCLEAR PROTEIN - DNA INTERACTIONS AND ITS APPLICATION TO A NUCLEASE HYPERSENSITIVE SITE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 82: 2296 (1985). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1985)
  28. JAYNES, J.B., TRANSCRIPTIONAL REGULATION OF THE MUSCLE CREATINE-KINASE GENE AND REGULATED EXPRESSION IN TRANSFECTED MOUSE MYOBLASTS, MOLECULAR AND CELLULAR BIOLOGY 6: 2855 (1986). / MOLECULAR AND CELLULAR BIOLOGY (1986)
  29. JAYNES, J.B., THE MUSCLE CREATINE-KINASE GENE IS REGULATED BY MULTIPLE UPSTREAM ELEMENTS, INCLUDING A MUSCLE-SPECIFIC ENHANCER, MOLECULAR AND CELLULAR BIOLOGY 8: 62 (1988). / MOLECULAR AND CELLULAR BIOLOGY (1988)
  30. JAYNES, J.B., ACTIVATION AND REPRESSION OF TRANSCRIPTION BY HOMEODOMAIN-CONTAINING PROTEINS THAT BIND A COMMON SITE, NATURE 336: 744 (1988). (10.1038/336744a0) / NATURE (1988)
  31. JOHNSON, J.E., EXPRESSION OF A TRANSFECTED MOUSE MUSCLE-CREATINE KINASE GENE IS INDUCED UPON GROWTH-FACTOR DEPRIVATION OF MYOGENIC BUT NOT OF NONMYOGENIC CELLS, DEVELOPMENTAL BIOLOGY 134: 258 (1989). (10.1016/0012-1606(89)90095-X) / DEVELOPMENTAL BIOLOGY (1989)
  32. JOHNSON, J.E., MUSCLE CREATINE-KINASE SEQUENCE ELEMENTS REGULATING SKELETAL AND CARDIAC-MUSCLE EXPRESSION IN TRANSGENIC MICE, MOLECULAR AND CELLULAR BIOLOGY 9: 3393 (1989). / MOLECULAR AND CELLULAR BIOLOGY (1989)
  33. JOHNSON J.E. THESIS U WASHINGTON (1989).
  34. JOHNSRUD, L, CONTACTS BETWEEN ESCHERICHIA-COLI RNA-POLYMERASE AND A LAC OPERON PROMOTER, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 75: 5314 (1978). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1978)
  35. LASSAR, A.B., TRANSFECTION OF A DNA LOCUS THAT MEDIATES THE CONVERSION OF 10T1/2 FIBROBLASTS TO MYOBLASTS, CELL 47: 649 (1986). (10.1016/0092-8674(86)90507-6) / CELL (1986)
  36. LASSAR, A.B., 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 (1989). (10.1016/0092-8674(89)90935-5) / CELL (1989)
  37. LIM, R.W., EGF RESPONSIVENESS AND RECEPTOR REGULATION IN NORMAL AND DIFFERENTIATION-DEFECTIVE MOUSE MYOBLASTS, DEVELOPMENTAL BIOLOGY 105: 48 (1984). (10.1016/0012-1606(84)90260-4) / DEVELOPMENTAL BIOLOGY (1984)
  38. LINDHART, T.A., J SUPRAMOL STRUCT 14: 483 (1980). (10.1002/jss.400140407) / J SUPRAMOL STRUCT (1980)
  39. 10.1126/science.2463672
  40. 10.1016/S0076-6879(80)65059-9
  41. MEESE, E, SIMULTANEOUS ISOLATION OF HIGH-MOLECULAR-WEIGHT RNA AND DNA FROM LIMITED AMOUNTS OF TISSUES AND CELLS, GENE ANALYSIS TECHNIQUES 4: 45 (1987). (10.1016/0735-0651(87)90017-3) / GENE ANALYSIS TECHNIQUES (1987)
  42. 10.1016/0092-8674(87)90512-5
  43. MUELLER, P.R., CONSTITUTIVE AND METAL-INDUCIBLE PROTEIN - DNA INTERACTIONS AT THE MOUSE METALLOTHIONEIN-I PROMOTER EXAMINED BY INVIVO AND INVITRO FOOTPRINTING, GENES & DEVELOPMENT 2: 412 (1988). (10.1101/gad.2.4.412) / GENES & DEVELOPMENT (1988)
  44. MUELLER P.R. unpublished data.
  45. MURRE, C, A NEW DNA-BINDING AND DIMERIZATION MOTIF IN IMMUNOGLOBULIN ENHANCER BINDING, DAUGHTERLESS, MYOD, AND MYC PROTEINS, CELL 56: 777 (1989). (10.1016/0092-8674(89)90682-X) / CELL (1989)
  46. 10.1126/science.2814502
  47. PICARD, D, A LYMPHOCYTE-SPECIFIC ENHANCER IN THE MOUSE IMMUNOGLOBULIN KAPPA-GENE, NATURE 307: 80 (1984). (10.1038/307080a0) / NATURE (1984)
  48. RIGGS, A.D., 5-METHYLCYTOSINE, GENE-REGULATION, AND CANCER, ADVANCES IN CANCER RESEARCH 40: 1 (1983). (10.1016/S0065-230X(08)60678-8) / ADVANCES IN CANCER RESEARCH (1983)
  49. 10.1126/science.2448875
  50. SCHUBERT, D, CHARACTERIZATION OF A UNIQUE MUSCLE-CELL LINE, JOURNAL OF CELL BIOLOGY 61: 398 (1974). (10.1083/jcb.61.2.398) / JOURNAL OF CELL BIOLOGY (1974)
  51. STERNBERG, E.A., IDENTIFICATION OF UPSTREAM AND INTRAGENIC REGULATORY ELEMENTS THAT CONFER CELL-TYPE-RESTRICTED AND DIFFERENTIATION-SPECIFIC EXPRESSION ON THE MUSCLE CREATINE-KINASE GENE, MOLECULAR AND CELLULAR BIOLOGY 8: 2896 (1988). / MOLECULAR AND CELLULAR BIOLOGY (1988)
  52. 10.1126/science.3175662
  53. TAYLOR, A, NUCLEOTIDE-SEQUENCE AND EXPRESSION OF THE HUMAN SKELETAL ALPHA-ACTIN GENE - EVOLUTION OF FUNCTIONAL REGULATORY DOMAINS, GENOMICS 3: 323 (1988). (10.1016/0888-7543(88)90123-1) / GENOMICS (1988)
  54. THISSE, B, SEQUENCE OF THE TWIST GENE AND NUCLEAR-LOCALIZATION OF ITS PROTEIN IN ENDOMESODERMAL CELLS OF EARLY DROSOPHILA EMBRYOS, EMBO JOURNAL 7: 2175 (1988). (10.1002/j.1460-2075.1988.tb03056.x) / EMBO JOURNAL (1988)
  55. VILLARES, R, THE ACHAETE-SCUTE GENE-COMPLEX OF DROSOPHILA-MELANOGASTER - CONSERVED DOMAINS IN A SUBSET OF GENES REQUIRED FOR NEUROGENESIS AND THEIR HOMOLOGY TO MYC, CELL 50: 415 (1987). (10.1016/0092-8674(87)90495-8) / CELL (1987)
  56. 10.1016/0092-8674(85)90267-3
  57. WHITE, T.J., THE POLYMERASE CHAIN-REACTION, TRENDS IN GENETICS 5: 185 (1989). (10.1016/0168-9525(89)90073-5) / TRENDS IN GENETICS (1989)
  58. WRIGHT, W.E., MYOGENIN, A FACTOR REGULATING MYOGENESIS, HAS A DOMAIN HOMOLOGOUS TO MYOD, CELL 56: 607 (1989). (10.1016/0092-8674(89)90583-7) / CELL (1989)
  59. ZINN, K, DETECTION OF FACTORS THAT INTERACT WITH THE HUMAN INTERFERON-BETA REGULATORY REGION INVIVO BY DNAASE-I FOOTPRINTING, CELL 45: 611 (1986). (10.1016/0092-8674(86)90293-X) / CELL (1986)
Dates
Type When
Created 18 years, 11 months ago (Oct. 5, 2006, 5:21 p.m.)
Deposited 1 year, 7 months ago (Jan. 12, 2024, 10:17 p.m.)
Indexed 2 days, 13 hours ago (Sept. 3, 2025, 6:33 a.m.)
Issued 35 years, 9 months ago (Nov. 10, 1989)
Published 35 years, 9 months ago (Nov. 10, 1989)
Published Print 35 years, 9 months ago (Nov. 10, 1989)
Funders 0

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@article{Mueller_1989, title={In Vivo Footprinting of a Muscle Specific Enhancer by Ligation Mediated PCR}, volume={246}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.2814500}, DOI={10.1126/science.2814500}, number={4931}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Mueller, Paul R. and Wold, Barbara}, year={1989}, month=nov, pages={780–786} }