Human biliverdin IXα reductase is a zinc-metalloprotein: Characterization of purified and Escherichia coli expressed enzymes

European Journal of Biochemistry

Volumn 235, Issue 1-2, 1996, Pages 372-381

  Maines, Mahin D ^a,b   Polevoda, Bogdan V ^a   Huang, Tian Jun ^a   Mccoubrey, William K Jr ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Bile pigment formation; Biliverdin reductase; Heme oxidation; Metalloprotein; Zinc finger

Indexed keywords

ESCHERICHIA COLI; ANIMALIA;

BILIVERDIN REDUCTASE; OXIDOREDUCTASE; UNCLASSIFIED DRUG; COMPLEMENTARY DNA; METALLOPROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RECOMBINANT PROTEIN; ZINC;

ARTICLE; DNA LIBRARY; ENZYME ACTIVITY; ENZYME ANALYSIS; ESCHERICHIA COLI; GENE EXPRESSION; HUMAN; HUMAN TISSUE; MOLECULAR CLONING; PLACENTA; PRIORITY JOURNAL; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; IN VITRO STUDY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; RAT;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING SITES; CLONING, MOLECULAR; DNA, COMPLEMENTARY; ESCHERICHIA COLI; GENE EXPRESSION; HUMANS; METALLOPROTEINS; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; NAD; NADP; OXIDOREDUCTASES; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; RATS; RECOMBINANT PROTEINS; ZINC;

EID: 0029671237     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1996.00372.x     Document Type: Article

References (48)

1. Singleton, J. W. & Laster, L. (1965) Biliverdin reductase of pig liver, J. Biol. Chem. 240, 4780-4789.
2. Watt, J. & O'Carra, P. (1976) Affinity chromatography of biliverdin reductase, Biochem. Soc. Trans. 4, 866-868.
3. Tenhunen, R., Ross, M. E., Marver, H. S. & Schmid, R. (1970) Reduced nicotinamide-adenine dinucleotide phosphate dependent biliverdin reductase: partial purification and characterization, Biochemistry 9, 298-303.
4. Kutty, R. K. & Maines, M. D. (1981) Purification and characterization of biliverdin reductase from the rat liver, J. Biol. Chem. 256, 3956-3962.
5. Rigney, E., Mantle, T. J. & Dickinson, M. F. (1989) The kinetics of ox kidney biliverdin reductase in the pre-ready state, Biochem. J. 259, 709-713.
6. Cascone, O., Frydman, R. B., Ferrara, P., Tomaro, M. L. & Rosenfield, J. (1989) Molecular differences between rat-liver and rat-kidney biliverdin reductase. Implications for their in vivo regulation, Eur. J. Biochem. 179, 123-130.
7. Maines, M. D., Trakshel, G. M. & Kutty, R. K. (1986) Characterization of two constitutive forms of rat liver microsomal heme oxygenase: only one molecular species of the enzyme is inducible, J. Biol. Chem. 261, 411-419.
8. Cruse, I. & Maines, M. D. (1988) Evidence suggesting that the two forms of heme oxygenase are products of different genes, J. Biol. Chem. 263, 3348-3353.
9. Stocker, R., Yamamoto, Y., McDonagh, A. F., Glazer, A. N. & Ames, B. N. (1987) Bilirubin is an antioxidant of possible physiological importance, Science 235, 1043-1047.
10. Heyman, E., Ohlsson, A. & Girschek, P. (1989) Retinopathy of prematurity and bilirubin, N. Engl. J. Med. 302, 256.
11. Tiribelli, C. & Ostrow, D. (1993) New concepts in bilirubin chemistry, transport, and metabolism, Hematology 17, 715-736.
12. Maines, M. D. & Trakshel, G. M. (1993) Purification and characterization of human biliverdin reductase, Arch. Biochem. Biophys. 300, 320-326.
13. Yamaguchi, T., Komoda, Y. & Nakajima, H. (1994) Biliverdin IXα reductase and biliverdin IXβ reductase from human liver: purification and characterization, J. Biol. Chem. 269, 24 343-24 348.
14. Fakhrai, H. & Maines, M. D. (1992) Expression and characterization of a cDNA for rat kidney biliverdin reductase: evidence suggesting the liver and kidney enzymes are the same transcript product, J. Biol. Chem. 267, 4023-4029.
15. Huang, T. J., Trakshel, G. M. & Maines, M. D. (1989) Detection of ten variants of biliverdin reductase in rat liver by two-dimensional gel electrophoresis, J. Biol. Chem. 264, 7844-7849.
16. Huang, T. J., Trakshel, G. M. & Maines, M. D. (1989) Microheterogeneity of biliverdin reductase in rat liver and spleen: selective suppression of enzyme variants in liver by bromobenzene, Arch. Biochem. Biophys. 274, 617-625.
17. McCoubrey, W. K. Jr & Maines, M. D. (1994) Site-directed mutagenesis of cysteine residues in biliverdin reductase: roles in substrate and cofactor binding, Eur. J. Biochem. 222, 597-603.
18. Ewing, J. F. & Maines, M. D. (1991) Rapid induction of heme oxygenase-1 DNA and protein by hyperthermia in rat brain: heme oxygenase-2 is not a heat shock protein, Proc. Natl Acad. Sci. USA 88, 5364-5368.
19. Ewing, J. F., Weber, C. M. & Maines, M. D. (1993) Biliverdin reductase is heat resistant and co-expressed with constitutive and heat shock form of heme oxygenase, J. Neurochem. 61, 1015-1023.
20. Shibahara S., Müller, R. M. & Taguchi, H. (1987) Transcriptional control of the rat heme oxygenase by heat shock, J. Biol. Chem. 262, 12 889-12 892.
21. Lindquist, S. & Craig, E. A. (1988) The heat shock proteins, Annu. Rev. Genet. 22, 631-637.
22. Morimoto, R. I. & Tissieres, A. (1990) Stress proteins in biology and medicine, Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY.
23. Schlesinger, M. J. (1990) Heat shock proteins, J. Biol. Chem. 265, 12 111-12 114.
24. Maines, M. D. (1992) Heme oxygenase: Clinical applications and functions, CRC Press, Boca Raton FL.
25. Chen, E. Y. & Seeburg, P. H. (1985) Supercoil sequencing: a fast and simple method for sequencing plasmid DNA, DNA 4, 165-170.
26. Feinberg, A. P. & Vogelstein, B. (1983) A technique for radio-labelling DNA restriction endonuclease fragments to high specific activity, Anal. Biochem. 132, 6-13.
27. Sambrook, J., Fritsch, E. F. & Maniatis, T (1989) Extraction and purification of plasmid DNA in Molecular cloning: a laboratory manual, pp. 1.21-1.43, Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY.
28. Chirgwin, J. M., Przybyla, A. E., MacDonald, R. J. & Rutter, W. J. (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease, Biochemistry 18, 5294-5299.
29. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Smith, J. A., Seidman, J. G. & Struhl, K. (1987) Preparation and analysis of RNA in Current protocols in molecular biology, pp. 4.0.3-4.10.7, John Wiley and Sons, New York.
30. Sun, Y., Rotenberg, M. O. & Maines, M. D.(1990) Developmental expression of heme oxygenase isozymes in rat brain: two HO-2 mRNAs are detected, J. Biol. Chem. 265, 8212-8217.
31. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
32. Towbin, H., Staehelin, T. & Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gets to nitrocellulose sheets: Procedure and some applications, Proc. Natl Acad. Sci. USA 76, 4350-4354.
33. Scopes, R. (1982) Making an extract in Protein purification principles and practice (Cantor, C. R., ed.) pp. 21-37, Springer-Verlag, New York.
34. 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.
35. Mazen, A., Gradwohl, G. & DeMurcia, G. (1988) Zn binding proteins detected by protein blotting, Anal. Biochem. 172, 39-42.
36. Kozak, M. (1987) An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs, Nucleic Acids Res. 15, 8125-8133.
37. Pearson, J. D., Dewald, B. D., Mathews, W. R., Mozier, N. M., Zurcher-Neely, H. A., Heinrickson, R. L., Morris, M. A., McCubbin, W. D., McDonald, J. R. & Fraser, E. D. (1990) Amino acid sequence and characterization of a protein inhibitor of protein kinase C, J. Biol. Chem. 265, 4583-4591.
38. Bell, J. E. & Maines, M. D. (1988) Kinetic properties and regulation of biliverdin reductase, Arch. Biochem. Biophys, 263, 1-9.
39. Nyman, P. O. (1961) Purification and properties of carbonic anhydrase from human ethrocytes, Biochim. Biophys. Acta 52, 1-12.
40. Blanckaert, N., Degroote, J., Heirwegh, K. P. M., Verwilghen, R. & Zaman, Z. (1976) Comparison of the biliary excretion of the four isomers of bilirubin IX in Wistar rats and homozygous Gunn rat, Gastroenterology 71, 897-901.
41. Blumenthal, S. G., Taggart, D. B., Ikeda, R., Ruebner, B. & Bergstrom, D. E. (1977) Conjugated and unconjugated bilirubins in bile of humans and rhesus monkeys. Structure of adult human and Rhesus-monkey bilirubins compared with dog bilirubins, Biochem. J. 167, 535-548.
42. Kutty, R. K. & Maines, M. D. (1982) Oxidation of heme c derivatives by purified heme oxygenase: evidence for the presence of one molecular species of heme oxygenase in rat liver, J. Biol. Chem. 257, 9944-9952.
43. Prasad, A. S. & Oberleas, D. (1970) Binding of Zn to amino acids and serum proteins in vitro, J. Lab. Clin. Med. 76, 416-425.
44. 2O of Zn enzymes, Proc. Natl Acad. Sci. USA 87, 220-224.
45. Miller, J., McLachlan, A. D. & Klug, A. (1985) Repetitive Zn binding domains in the protein transcription factor IIIA from Xenopus oocytes, EMBO J. 4, 1609-1614.
46. Brown, R. S., Sander, C. & Argos, P. (1985) The primary structure of transcription factor TFIIIA has 12 consecutive repeats, FEBS Lett. 186, 271-274.
47. Frydman, J., Tomaro, M. L., Rosenfield, J. & Frydman, R. B. (1990) Identification of the amino acid residues essential for the activity and the interconversion of the molecular forms of biliverdin reductase, Biochim. Biophys. Acta. 1040, 119-129.
48. Pabo, C. O. & Sauer, R. T. (1992) Transcription factors: Structural families and principles of DNA recognition, Ann. Rev. Biochem. 61, 1053-1095.