Moonlighting protein in Starkeyomyces koorchalomoides: Characterization of dihydrolipoamide dehydrogenase as a protein acetyltransferase utilizing acetoxycoumarin as the acetyl group donor

Biochimie

Volumn 91, Issue 7, 2009, Pages 868-875

  Tyagi, Tapesh K ^a   Ponnan, Prija ^a,b   Singh, Prabhjot ^a   Bansal, Seema ^a   Batra, Anoop ^b   Collin, Fabrice ^c   Guillonneau, Francois ^d   Jore, Daniel ^c   Patkar, Shamkant A ^e   Saxena, Rajendra K ^b   Parmar, Virinder S ^b   Rastogi, Ramesh C ^b   Raj, Hanumantharao G ^a  

^a UNIVERSITY OF DELHI   (India)

^b UNIVERSITY OF DELHI   (India)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e NOVOZYMES A S   (Denmark)

Author keywords

Acetoxycoumarin; Dihydrolipoamide dehydrogenase; Lipoyl domain; Protein acetyltransferase; Starkeyomyces koorchalomoides

Indexed keywords

ACYLTRANSFERASE; COUMARIN; DIHYDROLIPOAMIDE DEHYDROGENASE; GLUTATHIONE TRANSFERASE; LYSINE; MITOCHONDRIAL ENZYME; PYRUVATE DEHYDROGENASE COMPLEX;

ACETYLATION; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PURIFICATION; FUNGAL GENETICS; FUNGUS; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; STARKEYOMYCES KOORCHALOMOIDES; STREPTOCOCCUS PNEUMONIAE; TANDEM MASS SPECTROMETRY; TEMPERATURE;

ACETYLATION; ACETYLTRANSFERASES; COUMARINS; DIHYDROLIPOAMIDE DEHYDROGENASE; FUNGI; GLUTATHIONE TRANSFERASE; STREPTOCOCCUS PNEUMONIAE;

FUNGI; STREPTOCOCCUS PNEUMONIAE;

EID: 65749109070     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2009.04.007     Document Type: Article

References (57)

1. Kouzarides T. Acetylation: a regulatory modification to rival phosphorylation?. EMBO J. 19 (2000) 1176-1179
2. Grant P.A. A tale of histone modifications. Genome Biol. 2 (2001) 0003.1-0003.6
3. Loidl P. Histone acetylation: facts and questions. Chromosoma 103 (1994) 441-449
4. Vidali G., Gershey E.L., and Allfrey V.G. Chemical studies of histone acetylation. The distribution of epsilon-N-acetyllysine in calf thymus histones. J. Biol. Chem. 243 (1968) 6361-6366
5. Yang X. The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res. 32 (2004) 959-976
6. Yang X.J. Lysine acetylation and the bromodomain: a new partnership for signaling. Bioassays 26 (2004) 1076-1087
7. Thompson P.R., Wang D., Wang L., et al. Regulation of the p300 HAT domain via a novel activation loop. Nat. Struct. Mol. Biol. 11 (2004) 308-315
8. Santos-Rosa H., Valls E., Kouzarides T., and Martinez-Balbas M. Mechanisms of P/CAF auto-acetylation. Nucleic Acids Res. 31 (2003) 4285-4292
9. Glozak M.A., Sengupta N., Zhang X., and Seto E. Acetylation and deacetylation of nonhistone proteins. Gene 363 (2005) 15-23
10. Vane J.R. Inhibition of prostaglandins synthesis as a mechanism of action for aspirin-like drugs. Nature (New Biol.) 231 (1971) 232-234
11. Lee T.C., Uemura Y., and Snyder F. A novel CoA-independent transacetylase produces the ethanolamine plasmalogen and acyl analogs of platelet-activating factor (PAF) with PAF as the acetates donor in HL-60 cells. J. Biol. Chem. 267 (1992) 19992-20001
12. Hein D.W. Molecular genetics and function of NAT1 and NAT2: role in aromatic amine metabolism and carcinogenesis. Mut. Res. 506 (2002) 65-77
13. Kumari R., Kohli E., Gupta G., et al. Microsomal acetoxy drug: protein transacetylase of placenta: part 1. Characterization of DAMC: GST transacetylase. Placenta 23 (2002) 352-357
14. Kohli E., Gaspari M., Raj H.G., et al. Establishment of the enzymatic protein acetylation independent of acetyl CoA: recombinant glutathione S-transferase 3-3 is acetylated by a novel membrane-bound transacetylase using 7,8-diacetoxy 4-methyl coumarin as the acetyl donor. FEBS Lett. 530 (2002) 139-142
15. Kohli E., Gaspari M., Raj H.G., et al. Acetoxy drug: protein transacetylase of buffalo liver-characterization and mass spectrometry of the acetylated protein product. Biochim. Biophys. Acta 1698 (2004) 55-66
16. Bansal S., Gaspari M., Raj H.G., et al. Calreticulin transacetylase mediates the acetylation of nitric oxide synthase by polyphenolic acetate. Appl. Biochem. Biotechnol. 144 (2008) 37-45
17. Raj H.G., Parmar V.S., Jain S.C., et al. Mechanism of biochemical action of substituted 4-methylbenzopyran-2-one. Part 4: hyperbolic activation of rat liver microsomal NADPH-cytochrome C reductase by the novel acetylator 7,8-diacetoxy-4-methylcoumarin. Bioorg. Med. Chem. 7 (1999) 369-373
18. Raj H.G., Parmar V.S., Jain S.C., et al. Mechanism of biochemical action of substituted 4-methylbenzopyran-2-one. Part 7: assay and characterization of 7, 8-diacetoxy-4-methylcoumarin: protein transacetylase from rat liver microsomes based on the irreversible inhibition of cytosolic glutathione S-transacetylase. Bioorg. Med. Chem. 8 (2000) 1707-1712
19. Raj H.G., Kohli E., Rohil V., et al. Acetoxy-4-methycoumarins confer differential protection from aflatoxin B1-induced micronuclei and apoptosis in lung and bone marrow cells. Mut. Res. 494 (2001) 31-40
20. Raj H.G., Parmar V.S., Jain S.C., et al. Mechanism of biochemical action of substituted 4-methylbenzopyren-2-one. Part II: mechanism-based inhibition of rat liver microsomal-mediated aflatoxin B1-DNA binding by the candidate antimutagen 7,8-diacetoxy-4-methylcoumarin. Bioorg. Med. Chem. 6 (1998) 1895-1904
21. Kumar A., Tyagi Y.K., Seema, et al. Ellagic acid peracetate is superior to ellagic acid in the prevention of genotoxicity due to aflatoxin B1 in bone marrow and lung cells. J. Pharm. Pharmacol. 1 (2007) 81-86
22. Khurana P., Kumari R., Vohra P., et al. Acetoxy drug: protein transacetyalse catalyzed activation of human platelet nitric oxide synthase by polyphenolic peracetates. Bioorg. Med. Chem. 14 (2006) 575-583
23. Gulati R., Kumar A., Bansal S., et al. Calreticulin transacetylase (CRTAase): identifications of novel substrates and CRTAase mediated modification of protein kinase C activity in lymphocytes of asthmatic patients by polyphenolic acetates. Pure Appl. Chem. 79 (2007) 729-737
24. Raj H.G., Kumari R., Seema, et al. Novel function of calreticulin: characterization of calreticulin as a transacetylase-mediating protein acetylator independent of acetyl coA using polyphenolic acetates. Pure Appl. Chem. 78 (2006) 985-992
25. Seema, Kumari R., Gupta G., et al. Characterization of protein transacetylase from human placenta as a signaling molecule calreticulin using polyphenolic peracetates as the acetyl group donors. Cell Biochem. Biophys. 47 (2007) 53-64
26. Michalak M., Corbett E.F., Mesaeli N., Nakamura K., and Opas M. Calreticulin: one protein, one gene, many functions. Biochem. J. 344 (1999) 281-292
27. Lowry O.H., Rosebrough N.J., Farr A.T., and Randall R.J. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
28. Bradford M.M. A rapid and sensitive method for the quantitation of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
29. Habig W.H., Pabst M.J., and Jacoby W.B. Glutathione S-transferase: the first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249 (1974) 7130-7139
30. 5 reductase. Anal. Biochem. 110 (1981) 373-379
31. Ornstein L. Disc electrophoresis - I: background and theory. Ann. N. Y. Acad. Sci. 121 (1964) 321-349
32. Davis B.J. Disc electrophoresis - II: method and application to human serum proteins. Ann. N. Y. Acad. Sci. 121 (1964) 404-427
33. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227 (1970) 680-685
34. Weber K., and Osborn M. The reliability of molecular weight determination by dodecyl sulphate-polyacrylamide gel electrophoresis. J. Biol. Chem. 244 (1969) 4406-4412
35. 2+ reverse staining: a method for detection and quantification of protein in PAGE. Anal. Biochem. 213 (1993) 206-212
36. Håkansson A.P., and Smith A.W. Enzymatic characterization of dihydrolipoamide dehydrogenase from Streptococcus pneumoniae harboring its own substrate. J. Biol. Chem. 282 (2007) 29521-29530
37. Perkins D.N., Pappin D.J.C., Creasy D.M., and Cottrell J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20 (1999) 3551-3567
38. Serrano A. Purification, characterization and function of dihydrolipoamide dehydrogenase from the cyanobacterium Anabaena sp. strain P.C.C 7119. Biochem. J. 288 (1992) 823-830
39. Dietrichs D., and Andreesen J.R. Purification and comparative studies of dihydrolipoamide dehydrogenase from the anaerobic, glycine-utilizing bacteria Peptostreptococcus glycinophilus, Clostridium cylindrosporum and Clostridium sporogenes. J. Bacteriol. 172 (1990) 243-251
40. Yan L.J., Yang S.H., Shu H., Prokai L., and Forster M.J. Histochemical staining and quantification of dihydrolipoamide dehydrogenase diaphorase activity using blue native PAGE. Electrophoresis 28 (2007) 1036-1045
41. Batista A.P., Kletzin A., and Pereira M.M. The dihydrolipoamide dehydrogenase from the crenarchaeon Acidianus ambivalens. FEMS Microb. Lett. 281 (2008) 147-154
42. Schoneck R., Mulot O.B., Numrich P., et al. Cloning, sequencing and functional expression of dihydrolipoamide dehydrogenase from the human pathogen Trypanosoma cruzi. Eur. J. Biochem. 243 (1997) 739-747
43. Fehrmann H., and Veeger C. Lipoamide dehydrogenase of the phytopathogenic fungi Pythium ultimum and Phytophthora erythroseptica. Biochim. Biophys. Acta 350 (1974) 292-303
44. Agnihothrudu V. Fungi isolated from rhizosphere II Starkeyomyces: a new genus of the Tuberculariaceae. J. Indian Bot. Soc. 35 (1956) 38-42
45. Williams Jr. C.H. In: Muller F. (Ed). Chemistry and Biochemistry of Flavoenzymes vol. 3 (1992), CRC Press, Boca Raton, Florida
46. Castro M.E., Molina R., Díaz W., Pichuantes S.E., and Vásquez C.C. The dihydrolipoamide dehydrogenase of Aeromonas caviae ST exhibits NADH-dependent tellurite reductase activity. Biochem. Biophys. Res. Commun. 375 (2008) 91-94
47. Babady N.E., Pang Y.P., Elpeleg O., and Isaya G. Cryptic proteolytic activity of dihydrolipoamide dehydrogenase. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 6158-6163
48. Richarme G., and Heine H.G. Galactose- and maltose-stimulated lipoamide dehydrogenase activities related to the binding-protein-dependant transport of galactose and maltose in toluenized cells of Escherichia coli. Eur. J. Biochem. 156 (1986) 399-405
49. Jang Y.J., Chung K.S., Park C., and Yoo H.S. Fission yeast dihydrolipoamide dehydrogenase gene is involved in G1/S cell cycle progression. Biochim. Biophys. Acta 1358 (1997) 229-239
50. Igamberdieva A.U., Bykovab N.V., Ensb W., and Hill R.D. Dihydrolipoamide dehydrogenase from porcine heart catalyzes NADH-dependent scavenging of nitric oxide. FEBS Lett. 568 (2004) 146-150
51. Bansal S., Ponnan P., Raj H.G., et al. Autoacetylation of purified calreticulin transacetylase utilizing acetoxycoumarin as the acetyl group donor. Appl. Biochem. Biotechnol. (2008) 10.1007/s12010-008-8357-2
52. Berg A., Westphal A.H., Bosma H.J., and Kok A.D. Kinetics and specificity of reductive acylation of wild-type and mutated lipoyl domains of 2-oxo-acid dehydrogenase complexes from Azotobacter vinelandii. Eur. J. Biochem. 252 (1998) 45-50
53. Reed L.J. A trail of research from lipoic acid to α-keto acid dehydrogenase complexes. J. Biol. Chem. 276 (2001) 38329-38336
54. Bringas R., and Fernandez J. A lipoamide dehydrogenase from Neisseria meningitidis has a lipoyl domain. Proteins 21 (1995) 303-306
55. Zhu P.P., and Peterkofsky A. Sequence and organization of genes encoding enzymes involved in pyruvate metabolism in Mycoplasma capricolum. Protein Sci. 5 (1996) 1719-1736
56. Smith A.W., Roche H., Trombe M.C., Briles D.E., and Håkansson A. Characterization of the dihydrolipoamide dehydrogenase from Streptococcus pneumoniae and its role in pneumococcal infection. Mol. Microbiol. 44 (2002) 431-448
57. Jeffery C.J. Moonlighting proteins. Trends Biochem. Sci. 24 (1999) 8-11