Enzymes with extra talents: Moonlighting functions and catalytic promiscuity

Current Opinion in Chemical Biology

Volumn 7, Issue 2, 2003, Pages 265-272

  Copley, Shelley D ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGLYCOSIDE DERIVATIVE; AMINOGLYCOSIDE KINASE; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CARRIER PROTEIN; CYTOCHROME C; CYTOCHROME P450; ENZYME ANTIBODY; GEPHYRIN; GLUCOSE 6 PHOSPHATE ISOMERASE; GLUTATHIONE TRANSFERASE; ISOENZYME; PROTEIN; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TERPENE DERIVATIVE; TETRACHLOROHYDROQUINONE; TETRACHLOROHYDROQUINONE DEHALOGENASE; TYROSINE TRANSFER RNA LIGASE; UNCLASSIFIED DRUG;

CATALYSIS; ENZYME ANALYSIS; ENZYME BINDING; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYME SYNTHESIS; NEUROSPORA CRASSA; NONHUMAN; PROTEIN FUNCTION; REVIEW;

NEUROSPORA; NEUROSPORA CRASSA;

EID: 0037396292     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1367-5931(03)00032-2     Document Type: Review

References (55)

1. Jeffrey C.J. Moonlighting proteins. Trends Biochem. Sci. 24:1999;8-11.
2. O'Brien P.J., Herschlag D. Catalytic promiscuity and the evolution of new enzymatic activities. Chem. Biol. 6:1999;R91-R105.
3. Caprara M.G., Lehnert V., Lambowitz A.M., Westhof E. A tyrosyl-tRNA synthetase recognizes a conserved tRNA-like structural motif in the Group I intron catalytic core. Cell. 87:1996;1135-1145.
4. Mohr G., Rennard R., Cherniack A.D., Stryker J., Lambowitz A.M. Function of the Neurospora crassa mitochondrial tyrosyl-tRNA synthetase in RNA splicing. Role of the isiosyncratic N-terminal extension and different modes of interaction with different group I introns. J. Mol. Biol. 307:2001;75-92.
5. Faik P., Walker J.I.H., Redmill A.A.M., Morgan M.J. Mouse glucose-6-phosphate isomerase and neuroleukin have identical 3′ sequences. Nature. 332:1988;455-456.
6. Watanabe H., Takehana K., Date M., Shinozaki T., Raz A. Tumor cell autocrine motility factor is the neuroleukin/phosphohexose isomerase polypeptide. Cancer Res. 56:1996;2960-2963.
7. Xu W., Seiter K., Feldman E., Ahmed T., Chiao J.W. The differentiation and maturation mediator for human myeloid leukemia cells shares homology with neuroleukin or phosphoglucose isomerase. Blood. 87:1996;4502-4506.
8. Shimizu K., Tani M., Watanabe H., Nagamachi Y., Niinaka Y., Shiroishi T., Ohwada S., Raz A., Yokota J. The autocrine motility factor receptor gene encodes a novel type of seven transmembrane protein. FEBS Lett. 456:1999;295-300.
9. Leclerc N., Vallée A., Nabi I.R. Expression of the AMF/neuroleukin receptor in developing and adult brain cerebellum. J. Neurosci. Res. 60:2000;602-612.
10. Arsenieva D., Jeffery C.J. Conformational changes in phosphoglucose isomerase induced by ligand binding. J. Mol. Biol. 323:2002;77-84.
11. Tanaka N., Haga A., Uemura H., Akiyama H., Funasaka T., Nagase H., Raz A., Nakamura K.T. Inhibition mechanism of cytokine activity of human autocrine motility factor examined by crystal structure analyses and site-directed mutagenesis studies. J. Mol. Biol. 318:2002;985-997. • This and [10] demonstrate that binding of substrate analogues to phosphoglucose isomerase/autocrine motility factor causes only slight structural perturbations near the active site. Site-directed mutagenesis of two residues involved in binding erythrose-4-phosphate results in impaired autocrine motility factor activity, suggesting that the active site is involved in binding to the autocrine motility factor receptor.
12. Amraei M., Nabi I.R. Species specificity of the cytokine function of phosphoglucose isomerase. FEBS Lett. 525:2002;151-155.
13. Kirsch J., Betz H. The postsynaptic localization of the glycine receptor-associated protein gephyrin is regulated by the cytoskeleton. J. Neurosci. 15:1995;4148-4156.
14. Meyer G., Kirsch J., Betz H., Langosch D. Identification of a gephyrin binding motif on the glycine receptor beta subunit. Neuron. 15:1995;563-572.
15. Kneussel M., Brandstatter J.H., Laube B., Stahl S., Muller U., Betz H. Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice. J. Neurosci. 19:1999;9289-9297.
16. Kneussel M., Betz H. Receptors, gephyrin and gephyrin-associate proteins: novel insights into the assembly of inhibitory postsynaptic membrane specializations. J. Physiol. 525.1:2000;1-9.
17. Fuhrmann J.C., Kins S., Rostaing P., El Far O., Kirsch J., Sheng M., Triller A., Betz H., Kneussel M. Gephyrin interacts with dynein light chains 1 and 2, components of motor protein complexes. J. Neurosci. 22:2002;5393-5402.
18. Stallmeyer B., Schwarz G., Schulze J., Reiss J., Kirsch J., Mendel R.R. The neurotransmitter receptor-anchoring protein gephyrin reconstitutes molybdenum cofactor biosynthesis in bacteria, plants, and mammalian cells. Proc. Natl. Acad. Sci. USA. 96:1999;1333-1338.
19. Reiss J., Gross-Hardt S., Christensen E., Schmidt P., Mendel R.R., Schwarz G. A mutation in the gene for the neurotransmitter receptor-clustering protein gephyrin causes a novel form of molybdenum cofactor deficiency. Am. J. Hum. Genet. 68:2001;208-213.
20. Feng G., Tintrup H., Kirsch J., Nichol M.C., Kuhse J., Betz H., Sanes J.R. Dual requirement for gephyrin in glycine receptor clustering and molybdoenzyme activity. Science. 282:1998;1321-1324.
21. Sola M., Kneussel M., Heck I.S., Betz H., Weissenhorn W. X-ray crystal structure of the trimeric N-terminal domain of gephyrin. J. Biol. Chem. 2001:2001;25294-25301.
22. Schwarz G., Schrader N., Mendel R.R., Hecht H.-J., Schindelin H. Crystal structures of human gephyrin and plant Cnx1 G domains: comparative analysis and functional implications. J. Mol. Biol. 312:2001;405-418.
23. Xiang S., Nichols J., Rajagopalan K.V., Schindelin H. The crystal structure of Escherichia coli MoeA and its relationship to the multifunctional protein gephyrin. Structure. 9:2001;299-310 MoeA, which is homologous to the C-terminal domain of gephyrin, forms a dimer in which each monomer has four distinct domains. This finding, in conjunction with the known trimeric structure of the N-terminal domain, leads to a model in which gephyrin forms a hexagonal scaffold under the post-synaptic membrane of neurons to which multiple binding partners may attach.
24. Meier J., De Chaldée M., Triller A., Vannier C. Functional heterogeneity of gephyrins. Mol. Cell. Neurosci. 16:2000;566-577.
25. Ramming M., Kins S., Werner N., Hermann A., Betz H., Kirsch J. Diversity and phylogeny of gephyrin: tissue-specific splice variants, gene structure, and sequence similarities to molybdenum cofactor-synthesizing and cytoskeleton-associated proteins. Proc. Natl. Acad. Sci. USA. 97:2000;10266-10271.
26. Lim M.L.R., Lum M.-G., Hansen T.M., Roucou X., Nagley P. On the release of cytochrome c from mitochondria during cell death signaling. J. Biomed. Sci. 9:2002;488-506.
27. Yu T., Wang X., Purring-Koch C., Wei Y., McLendon G. A mutational epitope for cytochrome c binding to the apoptosis protease activation factor-1. J. Biol. Chem. 276:2001;13034-13038 Site-directed mutagenesis shows that several residues, including 7, 25, 39, 62-65 and 72, are involved in binding of cyt c to apoptosis protease activation factor-1. These data suggest a very large interface between the two proteins that encompasses a large part of the surface of cyt c.
28. Kranz R., Roland L., Goldman B., Bonnard G., Sabeeha M. Molecular mechanisms of cytochrome c biogenesis: three distinct systems. Mol. Microbiol. 29:1998;383-396.
29. van Loo G., Saelens X., van Gurp M., MacFarlane M., Martin S.J., Vandenabeele P. The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell. Death Differ. 9:2002;1031-1042.
30. Steele C.L., Crock J., Bohlmann J., Croteau R. Sesquiterpene synthases from grand fir (Abies grandis). J. Biol. Chem. 273:1998;2078-2089.
31. Langenheim J.H. Higher plant terpenoids: a phytocentric overview of their ecological roles. J. Chem. Ecol. 20:1994;1223-1280.
32. Hollfelder F., Kirby A.J., Tawfik D.S., Kikuchi K., Hilvert D. Characterization of proton-transfer catalysis by serum albumins. J. Am. Chem. Soc. 122:2000;1022-1029.
33. Rafikova O., Rafikov R., Nudler E. Catalysis of S-nitrosothiols formation by serum albumin: the mechanism and implication in vascular control. Proc. Natl. Acad. Sci. USA. 99:2002;5913-5918.
34. Yang J., Petersen C.E., Ha C.-E., Bhagavan N.V. Structural insights into human serum albumin-mediated prostaglandin catalysis. Protein Sci. 11:2002;538-545.
35. Sogorb M.A., Carrera V., Benabent M., Vilanova E. Rabbit serum albumin hydrolyzes the carbamate carbaryl. Chem. Res. Toxicol. 15:2002;520-526.
36. Cooper A.J.L., Bruschi S.A., Iriarte A., Martinez-Carrion M. Mitochondrial aspartate aminotransferase catalyzes cysteine S-conjugate β-lyase reactions. Biochem. J. 368:2002;253-261.
37. Fong D.H., Berghuis A.M. Substrate promiscuity of an aminoglycoside antibiotic resistance enzyme via target mimicry. EMBO J. 10:2002;2323-2331 The structures of aminoglycoside kinase APH(3′)-IIIa complexed with kanamycin A or neomycin A show that the promiscuous binding of substrates involves use of two sub-sites, a flexible loop that forms part of the aminoglycoside-binding pocket, and several acidic residues that can form many hydrogen bonds to substrates.
38. Benach J., Atrian S., Gonzàlez-Duarte R., Ladenstein R. The catalytic reaction and inhibition mechanism of Drosophila alcohol dehydrogenase: observation of an enzyme-bound NAD-ketone adduct at 1.4 Å resolution by X-ray crystallography. J. Mol. Biol. 289:1999;335-355.
39. Charnock S.J., Bolam D.N., Nurizzo D., Szabó L., McKie V.A., Gilbert H.J., Davies G.J. Promiscuity in ligand-binding: the three-dimensional structure of a Piromyces carbohydrate-binding module, CBM29-2, in complex with cello- and mannohexaose. Proc. Natl. Acad. Sci. USA. 99:2002;14077-14082.
40. Pilkington SJ, Dalton H: In Methods in Enzymology, Vol. 188. Edited by Lidstrom ME. San Diego: Academic Press; 1990.
41. Knapp M., Seebeck F.P., Klinman J.P. Steric control of oxygenation regiochemistry in soybean lipoxygenase-1. J. Am. Chem. Soc. 123:2001;2931-2932.
42. Funa N., Ohnishi Y., Ebizuka Y., Horinouchi S. Properties and substrate specificity of RppA, a chalcone synthase-related polyketide synthase in Streptomyces griseus. J. Biol. Chem. 277:2002;4628-4635.
43. Thornburg L.D., Lai M.-T., Wishnok J.S., Stubbe J. A non-heme iron protein with heme tendencies: an investigation of the substrate specificity of thymine hydroxylase. Biochemistry. 32:1993;14023-14033.
44. Palmer D.R., Garrett J.B., Sharma V., Meganathan R., Babbitt P.C., Gerlt J.A. Unexpected divergence of enzyme function and sequence: "N-acylamino acid racemase" is o-succinylbenzoate synthase. Biochemistry. 38:1999;4252-4258.
45. Anandarajah K., Kiefer P.M., Copley S.D. Recruitment of a double bond isomerase to serve as a reductive dehalogenase during biodegradation of pentachlorophenol. Biochemistry. 39:2000;5303-5311.
46. Kiefer P.M. Jr., McCarthy D.L., Copley S.D. The reaction catalyzed by tetrachlorohydroquinone dehalogenase does not involve nucleophilic aromatic substitution. Biochemistry. 41:2002;1308-1314.
47. Kiefer P.M. Jr., Copley S.D. Characterization of the initial steps in the reductive dehalogenation catalyzed by tetrachlorohydroquinone dehalogenase. Biochemistry. 41:2002;1315-1322 The mechanism of tetrachlorohydroquinone dehalogenase is described, and a potential mechanism for the promiscuous maleylacetone isomerase activity is proposed. In spite of the dramatically different transformations involved in these two reactions, the proposed mechanisms involve formation and reaction of structurally similar intermediates at the active site.
48. Wagner J., Lerner R.A., Barbas C.F. III Efficient aldolase catalytic antibodies that use the enamine mechanism of natural enzymes. Science. 270:1995;1797-1800.
49. Barbas C.F. III, Heine A., Zhong G., Hoffman T., Gramatikova S., Björnestedt R., List B., Anderson J., Stura E.A., Wilson I.A., Lerner R.A. Immune versus natural selection: antibody aldolases with enzymic rates but broader scope. Science. 278:1997;2085-2092.
50. James L.C., Tawfik D.S. Catalytic and binding poly-reactivities shared by two unrelated proteins: the potential role of promiscuity in enzyme evolution. Protein Sci. 10:2001;2600-2607 Aldolase antibody 38C2 catalyzes the Kemp elimination using a Lys residue as a general base. The role of Lys in this reaction differs from that previously characterized in aldolase-type reactions, in which the Lys acts as a nucleophile and forms a Schiff base with a wide variety of substrates.
51. 1-pyrroline-5-carboxylate dehydrogenase activity and the ability to associate with membranes, suggesting that the latter abilities are conferred by the C-terminal region of the protein.
52. Fernández-Canón J.M., Hejna J., Reifsteck C., Olson S., Grompe M. Gene structure, chromosomal location, and expression pattern of maleylacetoacetate isomerase. Genomics. 58:1999;263-269.
53. Canada K.A., Iwashita S., Shim H., Wood T.K. Directed evolution of toluene ortho-monooxygenase for enhanced 1-naphthol synthesis and chlorinated ethene degradation. J. Bacteriol. 184:2002;344-349.
54. Zheng W., Scheibner K.A., Ho A.K., Cole P.A. Mechanistic studies on the alkyltransferase activity of serotonin N-acetyl transferase. Chem. Biol. 8:2001;379-389.
55. Spreitzer R., Salvucci M.E. RUBISCO: structure, regulatory interactions, and possibilities for a better enzyme. Annu. Rev. Plant Biol. 53:2002;449-475.