Transition Metals in Control of Gene Expression

American Association for the Advancement of Science (AAAS) - Tập 261 Số 5122 - Trang 715-725 - 1993
Thomas V. O’Halloran1
1Department of Chemistry, Northwestern University, Evanston, IL 60208-3113.

Tóm tắt

Metalloproteins play structural and catalytic roles in gene expression. The metalloregulatory proteins are a subclass that exerts metal-responsive control of genes involved in respiration, metabolism, and metal-specific homeostasis or stress-response systems, such as iron uptake and storage, copper efflux, and mercury detoxification. Two allosteric mechanisms for control of gene expression were first discovered in metalloregulatory systems: an iron-responsive translational control mechanism for ferritin production and a mercury-responsive DNA-distortion mechanism for transcriptional control of detoxification genes. These otherwise unrelated mechanisms give rise to a rapid physiological response when metal ion concentrations exceed a dangerous threshold. Molecular recognition in these allosteric metal ion receptors is achieved through atypical coordination geometries, cluster formation, or complexes with prosthetic groups, such as sulfide and heme. Thus, many of the inorganic assemblies that otherwise buttress the structure of biopolymers or catalyze substrate transformation in active sites of enzymes have also been adapted to serve sensor functions in the metalloregulatory proteins. Mechanistic studies of these metal-sensor protein interactions are providing new insights into fundamental aspects of inorganic chemistry, molecular biology, and cellular physiology.

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Tài liệu tham khảo

ADMAN, E.T., STRUCTURAL MODEL OF RUBREDOXIN FROM DESULFOVIBRIO-VULGARIS 2 A-RESOLUTION, JOURNAL OF MOLECULAR BIOLOGY 112: 113 (1977).

ANSARI, A.Z., ALLOSTERIC UNDERWINDING OF DNA IS A CRITICAL STEP IN POSITIVE CONTROL OF TRANSCRIPTION BY HG-MERR, NATURE 355: 87 (1992).

AVERILL, B.A., SYNTHETIC ANALOGS OF ACTIVE-SITES OF IRON-SULFUR PROTEINS .2. SYNTHESIS AND STRUCTURE OF TETRA[MERCAPTO-MU3-SULFIDO-IRON] CLUSTERS, [FE4S4(SR)4]2-, JOURNAL OF THE AMERICAN CHEMICAL SOCIETY 95: 3523 (1973).

BAGG, A, MOLECULAR MECHANISM OF REGULATION OF SIDEROPHORE-MEDIATED IRON ASSIMILATION, MICROBIOLOGICAL REVIEWS 51: 509 (1987).

BERG, J.M., METAL-BINDING DOMAINS IN NUCLEIC ACID-BINDING AND GENE-REGULATORY PROTEINS, PROGRESS IN INORGANIC CHEMISTRY 37: 143 (1989).

10.1126/science.2421409

BHASKER, C.R., THE PUTATIVE IRON-RESPONSIVE ELEMENT IN THE HUMAN ERYTHROID 5-AMINOLEVULINATE SYNTHASE MESSENGER-RNA MEDIATES TRANSLATIONAL CONTROL, JOURNAL OF BIOLOGICAL CHEMISTRY 268: 12699 (1993).

BROWN N.L. unpublished data.

BROWN, P.H., REQUIREMENTS FOR THE TRANSLATIONAL REPRESSION OF FERRITIN TRANSCRIPTS IN WHEAT-GERM EXTRACTS BY A 90-KDA PROTEIN FROM RABBIT LIVER, JOURNAL OF BIOLOGICAL CHEMISTRY 264: 13383 (1989).

10.1016/0014-5793(85)80723-7

Bryson, J. W., Bioinorganic Chemistry of Copper: 101 (1993).

BUCHMAN, C, A SINGLE AMINO-ACID CHANGE IN CUP2 ALTERS ITS MODE OF DNA-BINDING, MOLECULAR AND CELLULAR BIOLOGY 10: 4778 (1990).

BYRD, J, CHARACTERIZATION OF THE COPPER-THIOLATE CLUSTER IN YEAST METALLOTHIONEIN AND 2 TRUNCATED MUTANTS, JOURNAL OF BIOLOGICAL CHEMISTRY 263: 6688 (1988).

CASASFINET, J.R., CHARACTERIZATION OF THE COPPER-THIOLATE AND SILVER-THIOLATE CLUSTERS IN N-TERMINAL FRAGMENTS OF THE YEAST ACE1 TRANSCRIPTION FACTOR CAPABLE OF BINDING TO ITS SPECIFIC DNA RECOGNITION SEQUENCE, BIOCHEMISTRY 31: 6617 (1992).

COLEMAN, J.E., ZINC PROTEINS - ENZYMES, STORAGE PROTEINS, TRANSCRIPTION FACTORS, AND REPLICATION PROTEINS, ANNUAL REVIEW OF BIOCHEMISTRY 61: 897 (1992).

CONDEE, C.W., A MER-LUX TRANSCRIPTIONAL FUSION FOR REAL-TIME EXAMINATION OF INVIVO GENE-EXPRESSION KINETICS AND PROMOTER RESPONSE TO ALTERED SUPERHELICITY, JOURNAL OF BACTERIOLOGY 174: 8094 (1992).

COOKSEY, D.A., COPPER UPTAKE AND RESISTANCE IN BACTERIA, MOLECULAR MICROBIOLOGY 7: 1 (1993).

COX, L.A., POSTTRANSCRIPTIONAL REGULATION OF CHIMERIC HUMAN TRANSFERRIN GENES BY IRON, BIOCHEMISTRY 32: 4738 (1993).

COX, T.C., HUMAN ERYTHROID 5-AMINOLEVULINATE SYNTHASE - PROMOTER ANALYSIS AND IDENTIFICATION OF AN IRON-RESPONSIVE ELEMENT IN THE MESSENGER-RNA, EMBO JOURNAL 10: 1891 (1991).

COY, M, STRUCTURAL DYNAMICS AND FUNCTIONAL DOMAINS OF THE FUR PROTEIN, BIOCHEMISTRY 30: 8201 (1991).

DAMERON, C.T., A COPPER THIOLATE POLYNUCLEAR CLUSTER IN THE ACE1 TRANSCRIPTION FACTOR, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 6127 (1991).

DANDEKAR, T, IDENTIFICATION OF A NOVEL IRON-RESPONSIVE ELEMENT IN MURINE AND HUMAN ERYTHROID DELTA-AMINOLEVULINIC-ACID SYNTHASE MESSENGER-RNA, EMBO JOURNAL 10: 1903 (1991).

DELORENZO, V, OPERATOR SEQUENCES OF THE AEROBACTIN OPERON OF PLASMID-COLV-K30 BINDING THE FERRIC UPTAKE REGULATION (FUR) REPRESSOR, JOURNAL OF BACTERIOLOGY 169: 2624 (1987).

DEMPLE, B, REGULATION OF BACTERIAL OXIDATIVE STRESS GENES, ANNUAL REVIEW OF GENETICS 25: 315 (1991).

DOBOSON, N.J., NATURE 249: 425 (1973).

DUBOIS, R.N., A GROWTH FACTOR-INDUCIBLE NUCLEAR-PROTEIN WITH A NOVEL CYSTEINE HISTIDINE REPETITIVE SEQUENCE, JOURNAL OF BIOLOGICAL CHEMISTRY 265: 19185 (1990).

EICHHORN, G.L., ADV INORG BIOCHEM 3: 1 (1981).

EMERYGOODMAN, A, IRON REGULATORY FACTOR EXPRESSED FROM RECOMBINANT BACULOVIRUS - CONVERSION BETWEEN THE RNA-BINDING APOPROTEIN AND FE-S CLUSTER CONTAINING ACONITASE, NUCLEIC ACIDS RESEARCH 21: 1457 (1993).

ERDMAN, S.E., THE DROSOPHILA DOUBLESEX PROTEINS SHARE A NOVEL ZINC FINGER RELATED DNA-BINDING DOMAIN, EMBO JOURNAL 12: 527 (1993).

FISCHER, H.M., ESSENTIAL AND NON-ESSENTIAL DOMAINS IN THE BRADYRHIZOBIUM-JAPONICUM NIFA PROTEIN - IDENTIFICATION OF INDISPENSABLE CYSTEINE RESIDUES POTENTIALLY INVOLVED IN REDOX REACTIVITY AND OR METAL-BINDING, NUCLEIC ACIDS RESEARCH 16: 2207 (1988).

FORSBURG, S.L., COMMUNICATION BETWEEN MITOCHONDRIA AND THE NUCLEUS IN REGULATION OF CYTOCHROME GENES IN THE YEAST SACCHAROMYCES-CEREVISIAE, ANNUAL REVIEW OF CELL BIOLOGY 5: 153 (1989).

FOSTER, J.W., EFFECT OF SALMONELLA-TYPHIMURIUM FERRIC UPTAKE REGULATOR (FUR) MUTATIONS ON IRON-REGULATED AND PH-REGULATED PROTEIN-SYNTHESIS, JOURNAL OF BACTERIOLOGY 174: 4317 (1992).

FRANTZ, B, DNA DISTORTION ACCOMPANIES TRANSCRIPTIONAL ACTIVATION BY THE METAL-RESPONSIVE GENE-REGULATORY PROTEIN MERR, BIOCHEMISTRY 29: 4747 (1990).

10.1016/0092-8674(88)90229-2

FURST, P, COOPERATIVE ACTIVATION OF A EUKARYOTIC TRANSCRIPTION FACTOR - INTERACTION BETWEEN CU(I) AND YEAST ACE1 PROTEIN, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 86: 5267 (1989).

GARDNER, P.R., CONTROLS ON THE BIOSYNTHESIS OF THE MANGANESE-CONTAINING SUPEROXIDE-DISMUTASE OF ESCHERICHIA-COLI - EFFECTS OF THIOLS, JOURNAL OF BIOLOGICAL CHEMISTRY 262: 17591 (1987).

GOLDBERG, M.B., TRANSCRIPTIONAL REGULATION BY IRON OF A VIBRIO-CHOLERAE VIRULENCE GENE AND HOMOLOGY OF THE GENE TO THE ESCHERICHIA-COLI FUR SYSTEM, JOURNAL OF BACTERIOLOGY 172: 6863 (1990).

GROSSMAN, S.R., E6-PROTEIN OF HUMAN PAPILLOMAVIRUS TYPE-18 BINDS ZINC, ONCOGENE 4: 1089 (1989).

GRUFF, E.S., TRIGONAL-PLANAR [M(SR)3]1- COMPLEXES OF CADMIUM AND MERCURY - STRUCTURAL SIMILARITIES BETWEEN MERCURY-CYSTEINE AND CADMIUM-CYSTEINE COORDINATION CENTERS, JOURNAL OF THE AMERICAN CHEMICAL SOCIETY 112: 1245 (1990).

GUARENTE L COMMUNICATION.

HAILE, D.J., CELLULAR-REGULATION OF THE IRON-RESPONSIVE ELEMENT BINDING-PROTEIN - DISASSEMBLY OF THE CUBANE IRON-SULFUR CLUSTER RESULTS IN HIGH-AFFINITY RNA-BINDING, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 89: 11735 (1992).

HAILE, D.J., RECIPROCAL CONTROL OF RNA-BINDING AND ACONITASE ACTIVITY IN THE REGULATION OF THE IRON-RESPONSIVE ELEMENT BINDING-PROTEIN - ROLE OF THE IRON-SULFUR CLUSTER, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 89: 7536 (1992).

HAMED, M. Y., JOURNAL OF INORGANIC BIOCHEMISTRY 50: 193 (1993).

Hantke, K., Molecular & General Genetics 197: 337 (1984).

Harrison, P. M., Iron Carriers and Iron Proteins 5: 123 (1989).

HARRISON, S.C., A STRUCTURAL TAXONOMY OF DNA-BINDING DOMAINS, NATURE 353: 715 (1991).

HELMANN, J.D., ADV INORG BIOCHEM 8: 33 (1990).

10.1126/science.2305262

HELTZEL, A, ACTIVATOR-DEPENDENT PREINDUCTION BINDING OF SIGMA-70 RNA-POLYMERASE AT THE METAL-REGULATED MER PROMOTER, BIOCHEMISTRY 29: 9572 (1990).

10.1126/science.3685996

HOLM, R. H., ADVANCES IN INORGANIC CHEMISTRY 38: 1 (1992).

HOOBER, J.K., LIGHT-DEREPRESSIBLE GENES ARE REGULATED BY METAL-PROTEIN COMPLEXES - A HYPOTHESIS, CARLSBERG RESEARCH COMMUNICATIONS 53: 27 (1988).

10.1126/science.1763327

10.1126/science.7384796

10.1016/0092-8674(87)90594-0

KAPTEIN, R, CURRENT OPINION IN STRUCTURAL BIOLOGY 2: 109 (1992).

KENNEDY, M.C., THE STATE OF CLUSTER SH AND S2- OF ACONITASE DURING CLUSTER INTERCONVERSIONS AND REMOVAL - A CONVENIENT PREPARATION OF APOENZYME, JOURNAL OF BIOLOGICAL CHEMISTRY 263: 8194 (1988).

KENNEDY, M.C., PURIFICATION AND CHARACTERIZATION OF CYTOSOLIC ACONITASE FROM BEEF-LIVER AND ITS RELATIONSHIP TO THE IRON-RESPONSIVE ELEMENT BINDING-PROTEIN, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 89: 11730 (1992).

KLAUSNER, R.D., REGULATING THE FATE OF MESSENGER-RNA - THE CONTROL OF CELLULAR IRON-METABOLISM, CELL 72: 19 (1993).

KLEVIT, R. E., PROTEINS-STRUCTURE FUNCTION AND GENETICS 7: 215 (1990).

KO, L.J., MURINE AND HUMAN LYMPHOCYTE-T GATA-3 FACTORS MEDIATE TRANSCRIPTION THROUGH A CIS-REGULATORY ELEMENT WITHIN THE HUMAN T-CELL RECEPTOR DELTA GENE ENHANCER, MOLECULAR AND CELLULAR BIOLOGY 11: 2778 (1991).

KRIWACKI, R.W., SEQUENCE-SPECIFIC RECOGNITION OF DNA BY ZINC-FINGER PEPTIDES DERIVED FROM THE TRANSCRIPTION FACTOR SP1, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 89: 9759 (1992).

KRIZEK, B.A., LIGAND VARIATION AND METAL-ION BINDING-SPECIFICITY IN ZINC FINGER PEPTIDES, INORGANIC CHEMISTRY 32: 937 (1993).

KUHN, L.C., COORDINATION OF CELLULAR IRON-METABOLISM BY POSTTRANSCRIPTIONAL GENE-REGULATION, JOURNAL OF INORGANIC BIOCHEMISTRY 47: 183 (1992).

10.1126/science.1411536

10.1126/science.8424176

LAUBLE, H, CRYSTAL-STRUCTURES OF ACONITASE WITH ISOCITRATE AND NITROISOCITRATE BOUND, BIOCHEMISTRY 31: 2735 (1992).

10.1126/science.2503871

LEWIS, C.D., HIGHER-ORDER METAPHASE CHROMOSOME STRUCTURE - EVIDENCE FOR METALLOPROTEIN INTERACTIONS, CELL 29: 171 (1982).

LI, P.M., THE LIM REGION OF A PRESUMPTIVE CAENORHABDITIS-ELEGANS TRANSCRIPTION FACTOR IS AN IRON-SULFUR-CONTAINING AND ZINC-CONTAINING METALLODOMAIN, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 9210 (1991).

LOVERING, R, IDENTIFICATION AND PRELIMINARY CHARACTERIZATION OF A PROTEIN MOTIF RELATED TO THE ZINC FINGER, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 90: 2112 (1993).

LUISI, B, DNA-TRANSCRIPTION - ZINC STANDARD FOR ECONOMY, NATURE 356: 379 (1992).

10.1038/352497a0

LUND, P.A., REGULATION OF TRANSCRIPTION IN ESCHERICHIA-COLI FROM THE MER AND MERR PROMOTERS IN THE TRANSPOSON TN501, JOURNAL OF MOLECULAR BIOLOGY 205: 343 (1989).

MARMORSTEIN, R, DNA RECOGNITION BY GAL4 - STRUCTURE OF A PROTEIN DNA COMPLEX, NATURE 356: 408 (1992).

Martell A. E. Critical Stability Constants 5 (1982).

MERCHANT, S, DYNAMIC INTERPLAY BETWEEN 2 COPPER-TITRATING COMPONENTS IN THE TRANSCRIPTIONAL REGULATION OF CYT C6, EMBO JOURNAL 10: 1383 (1991).

MEYES, A.M., J BIOL CHEM 262: 16822 (1987).

MICHELSEN, J.W., THE LIM MOTIF DEFINES A SPECIFIC ZINC-BINDING PROTEIN DOMAIN, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 90: 4404 (1993).

10.1002/j.1460-2075.1985.tb03825.x

MILLS, S.D., A 2-COMPONENT REGULATORY SYSTEM REQUIRED FOR COPPER INDUCIBLE EXPRESSION OF THE COPPER RESISTANCE OPERON OF PSEUDOMONAS-SYRINGAE, JOURNAL OF BACTERIOLOGY 175: 1656 (1993).

MORBY, A.P., SMTB IS A METAL-DEPENDENT REPRESSOR OF THE CYANOBACTERIAL METALLOTHIONEIN GENE SMTA - IDENTIFICATION OF A ZN INHIBITED DNA-PROTEIN COMPLEX, NUCLEIC ACIDS RESEARCH 21: 921 (1993).

Neilands, J. B., Metal-Ion Induced Regulation of Gene Expression 8: 63 (1990).

NICKOL, J, ZINC INDUCES A BEND WITHIN THE TRANSCRIPTION FACTOR-IIIA-BINDING REGION OF THE 5-S RNA GENE, JOURNAL OF MOLECULAR BIOLOGY 228: 1115 (1992).

NIES, D.H., RESISTANCE TO CADMIUM, COBALT, ZINC, AND NICKEL IN MICROBES, PLASMID 27: 17 (1992).

10.1126/science.3798107

OHALLORAN, T.V., THE MERR HEAVY-METAL RECEPTOR MEDIATES POSITIVE ACTIVATION IN A TOPOLOGICALLY NOVEL TRANSCRIPTION COMPLEX, CELL 56: 119 (1989).

O'Halloran, T. V., Metal Ions in Biological Systems 25: 105 (1989).

OMICHINSKI, J.G., A SMALL SINGLE-FINGER PEPTIDE FROM THE ERYTHROID TRANSCRIPTION FACTOR GATA-1 BINDS SPECIFICALLY TO DNA AS A ZINC OR IRON COMPLEX, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 90: 1676 (1993).

PAN, T, SEQUENTIAL ASSIGNMENTS OF THE H-1-NMR RESONANCES OF ZN(II)2 AND CD-113(II)2 DERIVATIVES OF THE DNA-BINDING DOMAIN OF THE GAL4 TRANSCRIPTION FACTOR REVEAL A NOVEL STRUCTURAL MOTIF FOR SPECIFIC DNA RECOGNITION, BIOCHEMISTRY 30: 4212 (1991).

PARKHILL, J, CONSTRUCTION AND CHARACTERIZATION OF A MERCURY-INDEPENDENT MERR ACTIVATOR (MERR(AC)) - TRANSCRIPTIONAL ACTIVATION IN THE ABSENCE OF HG(II) IS ACCOMPANIED BY DNA DISTORTION, EMBO JOURNAL 12: 413 (1993).

10.1126/science.2028256

PFEIFER, K, FUNCTIONAL DISSECTION AND SEQUENCE OF YEAST HAP1 ACTIVATOR, CELL 56: 291 (1989).

PRIVALLE, C.T., IRON SPECIFICITY OF THE FUR-DEPENDENT REGULATION OF THE BIOSYNTHESIS OF THE MANGANESE-CONTAINING SUPEROXIDE-DISMUTASE IN ESCHERICHIA-COLI, JOURNAL OF BIOLOGICAL CHEMISTRY 268: 5178 (1993).

RALSTON D unpublished data.

RALSTON, D.M., ADV INORG BIOCHEM 8: 1 (1990).

RALSTON, D.M., ULTRASENSITIVITY AND HEAVY-METAL SELECTIVITY OF THE ALLOSTERICALLY MODULATED MERR TRANSCRIPTION COMPLEX, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 87: 3846 (1990).

Rhodes, D., Scientific American 268:56 (1993).

RICE, W.G., INHIBITION OF HIV-1 INFECTIVITY BY ZINC-EJECTING AROMATIC C-NITROSO COMPOUNDS, NATURE 361: 473 (1993).

RICHARDSON, D.R., INTERMEDIATE STEPS IN CELLULAR IRON UPTAKE FROM TRANSFERRIN - DETECTION OF A CYTOPLASMIC POOL OF IRON, FREE OF TRANSFERRIN, JOURNAL OF BIOLOGICAL CHEMISTRY 267: 21384 (1992).

ROGERS, J, TRANSLATION OF FERRITIN LIGHT AND HEAVY SUBUNIT MESSENGER-RNAS IS REGULATED BY INTRACELLULAR CHELATABLE IRON LEVELS IN RAT HEPATOMA-CELLS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 84: 2277 (1987).

ROSS, W, GENETIC-ANALYSIS OF TRANSCRIPTIONAL ACTIVATION AND REPRESSION IN THE TN21 MER OPERON, JOURNAL OF BACTERIOLOGY 171: 4009 (1989).

ROUAULT, T.A., STRUCTURAL RELATIONSHIP BETWEEN AN IRON-REGULATED RNA-BINDING PROTEIN (IRE-BP) AND ACONITASE - FUNCTIONAL IMPLICATIONS, CELL 64: 881 (1991).

10.1126/science.3413484

SAITO, T, SOME STRUCTURAL FEATURES OF THE IRON-UPTAKE REGULATION PROTEIN, EUROPEAN JOURNAL OF BIOCHEMISTRY 197: 29 (1991).

SANFRANCISCO, MJD, IDENTIFICATION OF THE METALLOREGULATORY ELEMENT OF THE PLASMID-ENCODED ARSENICAL RESISTANCE OPERON, NUCLEIC ACIDS RESEARCH 18: 619 (1990).

SCHIERING, N, STRUCTURE OF THE DETOXIFICATION CATALYST MERCURIC ION REDUCTASE FROM BACILLUS SP STRAIN-RC607, NATURE 352: 168 (1991).

SCHMITT, M.P., IRON-DEPENDENT REGULATION OF DIPHTHERIA-TOXIN AND SIDEROPHORE EXPRESSION BY THE CLONED CORYNEBACTERIUM-DIPHTHERIAE REPRESSOR GENE DTXR IN C-DIPHTHERIAE C7 STRAINS, INFECTION AND IMMUNITY 59: 1899 (1991).

SILVER, S, GENE-REGULATION OF PLASMID-DETERMINED AND CHROMOSOME-DETERMINED INORGANIC-ION TRANSPORT IN BACTERIA, MICROBIOLOGICAL REVIEWS 56: 195 (1992).

SOUTH, T. L., PROTEIN SCIENCE 2: 3 (1993).

South, T. L., Metal-Ion Induced Regulation of Gene Expression 8: 199 (1990).

SPIRO, S, FNR-DEPENDENT REPRESSION OF THE NDH GENE OF ESCHERICHIA-COLI AND METAL-ION REQUIREMENT FOR FNR-REGULATED GENE-EXPRESSION, MOLECULAR MICROBIOLOGY 3: 601 (1989).

SUKEGAWA, J, A NUCLEAR-PORE COMPLEX PROTEIN THAT CONTAINS ZINC FINGER MOTIFS, BINDS DNA, AND FACES THE NUCLEOPLASM, CELL 72: 29 (1993).

SUMMERS, A.O., UNTWIST AND SHOUT - A HEAVY METAL-RESPONSIVE TRANSCRIPTIONAL REGULATOR, JOURNAL OF BACTERIOLOGY 174: 3097 (1992).

SUMMERS, M.F., NUCLEOCAPSID ZINC FINGERS DETECTED IN RETROVIRUSES - EXAFS STUDIES OF INTACT VIRUSES AND THE SOLUTION-STATE STRUCTURE OF THE NUCLEOCAPSID PROTEIN FROM HIV-1, PROTEIN SCIENCE 1: 563 (1992).

SZCZYPKA, M.S., A CYSTEINE-RICH NUCLEAR-PROTEIN ACTIVATES YEAST METALLOTHIONEIN GENE-TRANSCRIPTION, MOLECULAR AND CELLULAR BIOLOGY 9: 421 (1989).

10.1126/science.8446898

TAO, X, J BIOL CHEM 267: 21761 (1992).

TAO, X, SPECIFIC BINDING OF THE DIPHTHERIA TOX REGULATORY ELEMENT DTXR TO THE TOX OPERATOR REQUIRES DIVALENT HEAVY-METAL IONS AND A 9-BASE-PAIR INTERRUPTED PALINDROMIC SEQUENCE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 89: 5897 (1992).

THEIL, E.C., REGULATION OF FERRITIN AND TRANSFERRIN RECEPTOR MESSENGER-RNAS, JOURNAL OF BIOLOGICAL CHEMISTRY 265: 4771 (1990).

THIELE, D.J., METAL-REGULATED TRANSCRIPTION IN EUKARYOTES, NUCLEIC ACIDS RESEARCH 20: 1183 (1992).

THOMSON, A.J., DOES FERREDOXIN-I (AZOTOBACTER) REPRESENT A NOVEL CLASS OF DNA-BINDING PROTEINS THAT REGULATE GENE-EXPRESSION IN RESPONSE TO CELLULAR IRON(II), FEBS LETTERS 285: 230 (1991).

TRAGESER, M, ROLE OF CYSTEINE RESIDUES AND OF METAL-IONS IN THE REGULATORY FUNCTIONING OF FNR, THE TRANSCRIPTIONAL REGULATOR OF ANAEROBIC RESPIRATION IN ESCHERICHIA-COLI, MOLECULAR MICROBIOLOGY 3: 593 (1989).

VALLEE, B.L., THE BIOCHEMICAL BASIS OF ZINC PHYSIOLOGY, PHYSIOLOGICAL REVIEWS 73: 79 (1993).

VANHOVE, B, NOVEL 2-COMPONENT TRANSMEMBRANE TRANSCRIPTION CONTROL - REGULATION OF IRON-DICITRATE TRANSPORT IN ESCHERICHIA-COLI K-12, JOURNAL OF BACTERIOLOGY 172: 6749 (1990).

WALDEN, W.E., TRANSLATIONAL REPRESSION IN EUKARYOTES - PARTIAL-PURIFICATION AND CHARACTERIZATION OF A REPRESSOR OF FERRITIN MESSENGER-RNA TRANSLATION, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 85: 9503 (1988).

WATENPAUGH, K.D., STRUCTURE OF RUBREDOXIN AT 1.2 A RESOLUTION, JOURNAL OF MOLECULAR BIOLOGY 131: 509 (1979).

WATTON, S.P., TRIGONAL MERCURIC COMPLEX OF AN ALIPHATIC THIOLATE - A SPECTROSCOPIC AND STRUCTURAL MODEL FOR THE RECEPTOR-SITE IN THE HG(II) BIOSENSOR MERR, JOURNAL OF THE AMERICAN CHEMICAL SOCIETY 112: 2824 (1990).

ALSINA, T., JOURNAL OF THE CHEMICAL SOCIETY, DALTON TRANSACTIONS: 1393 (1992).

WEBSTER, L.C., CONVERSION OF THE E1A CYS4 ZINC FINGER TO A NONFUNCTIONAL HIS2, CYS2 ZINC FINGER BY A SINGLE POINT MUTATION, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 9989 (1991).

WILLIAMS, RJP, THE MINERAL ELEMENTS IN HOMEOSTASIS AND MORPHOGENESIS, BIOCHEMICAL SOCIETY TRANSACTIONS 18: 689 (1990).

Wright, J. G., Progress in Inorganic Chemistry 38: 328 (1990).

ZAHRINGER, J, NOVEL MECHANISM FOR TRANSLATIONAL CONTROL IN REGULATION OF FERRITIN SYNTHESIS BY IRON, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 73: 857 (1976).

ZENG, J, THIONEIN (APOMETALLOTHIONEIN) CAN MODULATE DNA-BINDING AND TRANSCRIPTION ACTIVATION BY ZINC FINGER CONTAINING FACTOR-SP1, FEBS LETTERS 279: 310 (1991).

ZENG, J, ZINC TRANSFER FROM TRANSCRIPTION FACTOR-IIIA FINGERS TO THIONEIN CLUSTERS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 9984 (1991).

ZHANG, L, ANTIBODY-PROMOTED DIMERIZATION BYPASSES THE REGULATION OF DNA-BINDING BY THE HEME DOMAIN OF THE YEAST TRANSCRIPTIONAL ACTIVATOR HAP1, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 90: 2851 (1993).

ZHOU, P.B., ISOLATION OF A METAL-ACTIVATED TRANSCRIPTION FACTOR GENE FROM CANDIDA-GLABRATA BY COMPLEMENTATION IN SACCHAROMYCES-CEREVISIAE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 6112 (1991).

Watton S. P. unpublished data.