Kinetic and physical characterisation of recombinant wild-type and mutant human protoporphyrinogen oxidases

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1650, Issue 1-2, 2003, Pages 10-21

  Maneli, Mbulelo H ^a   Corrigall, Anne V ^a   Klump, Horst H ^b   Davids, Lester M ^a   Kirsch, Ralph E ^a   Meissner, Peter N ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Haem biosynthesis; Porphyria; R59W; Variegate porphyria

Indexed keywords

ARGININE; BINDING PROTEIN; GLYCINE; PROTOPORPHYRINOGEN OXIDASE; QUERCETIN; RECOMBINANT PROTEIN; ENZYME INHIBITOR; FLAVINE ADENINE NUCLEOTIDE; FLAVOPROTEIN; MITOCHONDRIAL PROTEIN; OXIDOREDUCTASE; PPOX PROTEIN, HUMAN;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CATALYSIS; CODON; DENATURATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME PURIFICATION; ENZYME SUBSTRATE COMPLEX; GENE DISRUPTION; NUCLEOTIDE SEQUENCE; PORPHYRIA VARIEGATA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; STRAIN DIFFERENCE; WILD TYPE; CHEMISTRY; GENETICS; HEAT; HUMAN; KINETICS; METABOLISM; MISSENSE MUTATION; MUTATION; PHYSIOLOGY; PROTEIN DENATURATION; STRUCTURE ACTIVITY RELATION;

ENZYME INHIBITORS; FLAVIN-ADENINE DINUCLEOTIDE; FLAVOPROTEINS; HEAT; HUMANS; KINETICS; MITOCHONDRIAL PROTEINS; MUTATION; MUTATION, MISSENSE; OXIDOREDUCTASES; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; PROTEIN DENATURATION; PROTOPORPHYRINOGEN OXIDASE; RECOMBINANT PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 0141872474     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1570-9639(03)00186-9     Document Type: Article

References (61)

1. Poulsen R., Polglase W.J. The enzymic conversion of protoporphyrinogen IX to protoporphyrin IX. Protoporphyrinogen oxidase activity in mitochondrial extracts of Saccharomyces. J. Biol. Chem. 250:1975;1269-1274.
2. Dailey H.A. Conversion of coproporphyrin to protoheme in higher eukaryotes: terminal three enzymes. Dailey H.A. Biosynthesis of Haem and Chlorophylls. 1990;123-161 McGraw-Hill, New York.
3. Camadro J.-M., Thome F., Brouillet N., Labbe P. Purification and properties of protoporphyrinogen oxidase from the yeast Saccharomyces cerevisiae. Mitochondrial location and evidence for a precursor form of the protein. J. Biol. Chem. 269:1994;32085-32091.
4. Klemm D.J., Barton L.L. Oxidation of protoporphyrinogen in the obligate anaerobe Desulfovibrio gigas. J. Bacteriol. 164:1985;316-320.
5. Ferreira G.C., Andrew T.A., Karr S.W., Dailey H.A. Organisation of the terminal two enzymes of the heme biosynthetic pathway. J. Biol. Chem. 263:1988;3825-3839.
6. Dailey H.A., Dailey T.A. Protoporphyrinogen oxidase of Myxococcus xanthus. Expression, purification, and characterization of the cloned enzyme. J. Biol. Chem. 271:1996;8714-8718.
7. Jones C., Jordan P.M., Akhtar M. Mechanism and stereochemistry of the porphobilinogen deaminase and protoporphyrinogen IX oxidase reaction: stereospecific manipulation of hydrogen atoms at the four methylene bridges during the biosynthesis of haem. J. Chem. Soc., Perkin Trans. 1:1984;2625-2633.
8. Akhtar M. Mechanism and stereochemistry of the enzymes involved in the conversion of uroporphyrinogen III into haem. Jordan P.M. Biosynthesis of Tetrapyrroles. 1991;67-99 Elsevier, Amsterdam.
9. Dailey T.A., Dailey H.A. Identification of an FAD superfamily containing protoporphyrinogen oxidases, monoamine oxidases, and phytoene desaturase. J. Biol. Chem. 273:1998;13658-13662.
10. Dailey H.A., Karr S.W. Purification and characterization of murine protoporphyrinogen oxidase. Biochemistry. 26:1987;2697-2701.
11. Proulx K.L., Dailey H.A. Characteristics of murine protoporphyrinogen oxidase. Protein Sci. 1:1992;801-809.
12. Siepker L.J., Ford M., de Kork R., Kramer S. Purification of bovine protoporphyrinogen oxidase: immunological cross-reactivity and structural relationship to ferrochelatase. Biochim. Biophys. Acta. 913:1987;349-358.
13. Jacobs J.M., Jacobs J.N. Oxidation of protoporphyrinogen to protoporphyrin, a step in chlorophyll and haem biosynthesis: purification and partial characterization of the enzyme from barley organelles. Biochem. J. 244:1987;219-224.
14. De Marco A., Volrath S., Bruyere T., Law M., Fonné-Pfister R. Recombinant maize protoporphyrinogen IX oxidase expressed in Escherichia coli forms complexes with GroEL and DnaK chaperones. Protein Expr. Purif. 20:2000;81-86.
15. Watanabe N., Che F., Terashima K., Takayama S., Yoshida S., Isogai A. Purification and properties of protoporphyrinogen oxidase from spinach chloroplasts. Plant Cell Physiol. 41:2000;889-892.
16. Dailey T.A., Dailey H.A. Human protoporphyrinogen oxidase: expression, purification and characterization of the cloned enzyme. Protein Sci. 5:1996;98-105.
17. Nishimura K., Taketani S., Inokuchi H. Cloning of a human cDNA for protoporphyrinogen oxidase by complementation in vivo on a hemG mutant of Escherichia coli. J. Biol. Chem. 270:1995;8076-8080.
18. Arnould S., Camadro J.-M. The domain structure of protoporphyrinogen oxidase, the molecular target of diphenyl ether-type herbicides. Proc. Natl. Acad. Sci. U. S. A. 95:1998;10553-10558.
19. Camadro J.-M., Matringe M., Scalla R., Labbe P. Kinetic studies on protoporphyrinogen oxidase inhibition by diphenyl ether herbicides. Biochem. J. 277:1991;17-21.
20. Corrigall A.V., Hift R.J., Adams P.A., Kirsch R.E. Inhibition of mammalian protoporphyrinogen oxidase by acifluorfen. Biochem. Mol. Biol. Int. 34:1994;1283-1289.
21. Jacobs J.M., Jacobs N.J., Borotz S.E., Guerinot M.L. Effects of photobleaching herbicide, acifluorfen methyl, on protoporphyrinogen oxidation in barley organelles, soybean root mitochondria, soybean root nodules, and bacteria. Arch. Biochem. Biophys. 280:1990;369-375.
22. Dailey T.A., Meissner P.N., Dailey H.A. Expression of a cloned protoporphyrinogen oxidase. J. Biol. Chem. 269:1994;813-815.
23. Corrigall A.V., Siziba K.B., Maneli M.H., Shephard E.G., Ziman M., Dailey T.A., Dailey H.A., Kirsch R.E., Meissner P.N. Purification of and kinetic studies on a cloned protoporphyrinogen oxidase from aerobic bacterium Bacillus subtilis. Arch. Biochem. Biophys. 358:1998;251-256.
24. Watanabe N., Che F., Iwano M., Takayama S., Nakano T., Yoshida S., Isogai A. Molecular characterization of photomixotrophic tobacco cells resistant to protoporphyrinogen oxidase-inhibiting herbicides. Plant Physiol. 118:1998;751-758.
25. Lermontova I., Grimm B. Overexpression of plastidic protoporphyrinogen IX oxidase leads to resistance to diphenyl-ether herbicide acifluorfen. Plant Physiol. 122:2000;75-83.
26. Ferreira G.C., Dailey H.A. Mouse protoporphyrinogen oxidase. Kinetic parameters and demonstration of inhibition by bilirubin. Biochem. J. 250:1988;597-603.
27. Brenner D.A., Bloomer J.R. The enzymatic defect in variegate porphyria. N. Engl. J. Med. 302:1980;765-769.
28. Deybach J.Ch. , de Verneuil H., Nordmann Y. The inherited defect in porphyria variegata. Hum. Genet. 58:1981;425-428.
29. Meissner P.N., Day R.S., Moore M.R., Disler P.B., Harley E. Protoporphyrinogen oxidase and porphobilinogen deaminase in variegate porphyria. Eur. J. Clin. Investig. 16:1986;257-261.
30. Day R.S. Variegate porphyria. Semin. Dermatol. 5:1986;138-154.
31. Meissner P.N., Dailey T.A., Hift R.J., Ziman M., Corrigall A.V., Roberts A.G., Meissner D.M., Kirsch R.E., Dailey H.A. A R59W mutation in human protoporphyrinogen oxidase results in decreased enzyme activity and is prevalent in South Africans with variegate porphyria. Nat. Genet. 13:1996;95-97.
32. Warnich L., Kotze M.J., Groenewald I.M., Groenewald J.Z., van Brakel M.G., van Heerden C.J., de Villiers J.N.P., van de Ven W.J.M., Shoenmakers E.F.P.M., Taketani S., Retief A.E. Identification of the three mutations and associated haplotypes in the protoporphyrinogen oxidase gene in South African families with variegate porphyria. Hum. Mol. Genet. 5:1996;981-984.
33. Corrigall A.V., Hift R.J., Hancock V., Meissner D., Davids L., Kirsch R.E., Meissner P.N. Identification and characterisation of a deletion (537delAT) in the protoporphyrinogen oxidase gene in a South African variegate porphyria family. Human Mutat. 12:1998;403-407.
34. Corrigall A.V., Hift R.J., Davids L.M., Hancock V., Meissner D., Kirsch R.E., Meissner P.N. Homozygous variegate porphyria in South Africa: genotypic analysis in two cases. Mol. Genet. Metab. 69:2000;323-330.
35. Corrigall A.V., Hift R.J., Davids L.M., Hancock V., Meissner D., Kirsch R.E., Meissner P.N. Identification of the first variegate porphyria mutation in an indigenous black South African and further evidence for heterogeneity in variegate porphyria. Mol. Genet. Metab. 73:2001;91-96.
36. Whatley S.D., Puy H., Morgan R.R., Robreauw A.M., Roberts A.G., Nordmann Y., Elder G.H., Deybach J.-C. Variegate porphyria in Western Europe: identification of PPOX gene mutation in 104 families, extent of allelic heterogeneity, and absence of correlation between phenotype and type of mutation. Am. J. Hum. Genet. 65:1999;984-994.
37. Maeda N., Horie Y., Sasaki Y., Adachi K., Nanba E., Nishida K., Saigo R., Nakagawa M. Three novel mutations in the protoporphyrinogen oxidase gene in Japanese patients with variegate porphyria. Clin. Biochem. 33:2000;495-500.
38. von und zu Fraundberg M., Tenhunen R., Kauppinen R. Expression and characterization of six mutations in the protoporphyrinogen oxidase gene among Finnish variegate porphyria patients. Mol. Med. 7:2001;320-328.
39. Frank J., Jugert F.K., Merk H.K., Kalka K., Goerz G., Anderson K., Bickers D.R., Poh-Fitzpatrick M.B., Christiano A.M. A spectrum of novel mutations in the protoporphyrinogen oxidase gene in 13 families with variegate porphyria. J. Invest. Dermatol. 116:2001;821-823.
40. Frank J., Aita V.M., Ahmad W., Lam H., Wolff C., Christiano A.M. Identification of a founder mutation in the protoporphyrinogen oxidase gene in variegate porphyria patients from Chile. Hum. Hered. 51:2001;160-168.
41. Roberts A.G., Whatley S.D., Daniels J., Holmans P., Fenton I., Owen M.J., Thompson P., Long C., Elder G.H. Partial characterization and assignment of the gene for protoporphyrinogen oxidase and variegate porphyria to human chromosome 1q23. Hum. Mol. Genet. 4:1995;2387-2390.
42. Taketani S., Inazawa J., Abe T., Furukawa T., Kohno H., Tokunaga R., Nishimura K., Inokuchi H. The human protoporphyrinogen oxidase (PPOX) gene: organisation and localisation to chromosome 1. Genomics. 29:1995;698-703.
43. Puy H., Robreau A.M., Rosipal R., Nordmann Y., Deybach J.C. Protoporphyrinogen oxidase: complete genomic sequence and polymorphisms in the human gene. Biochem. Biophys. Res. Commun. 226:1996;226-230.
44. Dailey H.A., Dailey T.A. Characteristics of human protoporphyrinogen oxidase in controls and variegate porphyria. Cell. Mol. Biol. 43:1997;67-73.
45. Roberts A.G., Puy H., Dailey T.A., Morgan R.R., Whatley S.D., Dailey H.A., Martasek P., Nordmann Y., Deybach J., Elder G.H. Molecular characterization of homozygous variegate porphyria. Hum. Mol. Genet. 7:1998;1921-1925.
46. Morgan R.R., Da Silva V., Puy H., Elder G.H. Functional studies of mutations in the human protoporphyrinogen oxidase gene in variegate porphyria. Cell. Mol. Biol. 48:2002;79-82.
47. Dailey T.A., Dailey H.A., Meissner P., Prasad A.R.K. Cloning, sequencing, and expression of mouse protoporphyrinogen oxidase. Arch. Biochem. Biophys. 324:1995;379-384.
48. Laemmli U.K. Cleavage of structural proteins during the assembly of head of bacteriophage T4. Nature (Lond.). 277:1970;680-685.
49. Bradford M. A rapid and sensitive method for quantitation of microgram quantities of protein utilising the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
50. Marky L.A., Breslauer K.J. Calculating thermadynamic data for transitions of any molecularity from equilibrium melting curves. Biopolymers. 26:1987;1601-1620.
51. Deléage G., Roux B. An algorithm for protein secondary structure prediction based on class prediction. Protein Eng. 1:1987;289-294.
52. Kane J.F., Hartley D.L. Formation of recombinant protein inclusion bodies in Escherichia coli. TIBTECH. 6:1988;95-101.
53. Dailey T.A., Dailey H.A. Expression, purification and characterization of mammalian protoporphyrinogen oxidase. Methods Enzymol. 281:1997;340-349.
54. Arnould S., Takahashi M., Camadro J.-M. Acylation stabilizes a protease-resistant conformation of protoporphyrinogen oxidase, the molecular target of diphenyl ether-type herbicides. Proc. Natl. Acad. Sci. U. S. A. 96:1999;14825-14830.
55. 1 complex. J. Biol. Chem. 273:1998;27953-27959.
56. Wierenga R.K., Terpstra P., Hol W.G.J. Prediction of the occurrence of the ADP-binding βαβ-fold in proteins, using an amino acid sequence fingerprint. J. Mol. Biol. 187:1986;101-107.
57. Vrielink A., Lloyd L.F., Blow D.M. Crystal structure of cholesterol oxidase from Brevibacterium sterolicum refined at 1.8 Å resolution. J. Mol. Biol. 219:1991;533-554.
58. Roberts D.L., Frerman F.E., Kim J.P. Three dimensional structure of human electron transfer flavoprotein to 2.1-Å resolution. Proc. Natl. Acad. Sci. 93:1996;14355-14360.
59. Nishiya Y., Imanaka T. Analysis of interaction between the Arthrobacter sarcosine oxidase and the coenzyme flavin adenine dinucleotide by site-directed mutagenesis. Appl. Environ. Microbiol. 62:1996;2405-2410.
60. Arnould S., Takahashi M., Camadro J.-M. Stability of recombinant yeast protoporphyrinogen oxidase: effect of diphenyl ether-type herbicides and diphenyleneiodonium. Biochemistry. 37:1998;12818-12828.
61. Hennessey J.P., Johnson W.C. Jr. Information content in the circular dichroism of proteins. Biochemistry. 20:1981;1085-1094.