Porphyrin Binding and Distortion and Substrate Specificity in the Ferrochelatase Reaction: The Role of Active Site Residues

Journal of Molecular Biology

Volumn 378, Issue 5, 2008, Pages 1074-1083

  Karlberg, Tobias ^a   Hansson, Mattias D ^a   Yengo, Raymond K ^a   Johansson, Renzo ^a   Thorvaldsen, Hege O ^a   Ferreira, Gloria C ^b,c   Hansson, Mats ^a   Al Karadaghi, Salam ^a  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

catalysis; heme synthesis; iron; metallation; substrate distortion

Indexed keywords

ALANINE; CUPRIC ION; DEUTEROPORPHYRIN IX; DEUTEROPORPHYRIN IX 2,4 DISULFONIC ACID DIHYDROCHLORIDE; FERROCHELATASE; HISTONE; MESOPORPHYRIN; METAL; N METHYLMESOPORPHYRIN; PORPHYRIN; PROTEIN ANTIBODY;

ARTICLE; BACILLUS SUBTILIS; CATALYSIS; DRUG STRUCTURE; ENZYME MECHANISM; FLUORESCENCE ANALYSIS; HEME SYNTHESIS; METALLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION;

BACILLUS SUBTILIS;

EID: 42649101624     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.03.040     Document Type: Article

References (50)

1. J.J.R. Fraústo da Silva R.J.P. Williams Haem iron: coupled redox reactions The Biological Chemistry of the Elements vol. 2 2001 Oxford University Press Oxford, UK 370 399
2. H.A. Dailey T.A. Dailey Ferrochelatase K.M. Kadish K.M. Smith R. Guilard Porphyrin Handbook: The Iron and Cobalt Pigments: Biosynthesis, Structure and Degradation vol. 12 2003 Academic Press San Diego, CA 93 122
3. S. Al-Karadaghi R. Franco M. Hansson J.A. Shelnutt G. Isaya G.C. Ferreira Chelatases: distort to select? Trends Biochem. Sci. 31 2006 135 142
4. R.D. Willows M. Hansson Mechanism, structure, and regulation of magnesium chelatase K.M. Kadish K.M. Smith R. Guilard Porphyrin Handbook: Chlorophylls and Bilins: Biosynthesis, Synthesis and Degradation vol. 13 2003 Academic Press San Diego, CA 1 47
5. H.L. Schubert E. Raux K.S. Wilson M.J. Warren Common chelatase design in the branched tetrapyrrole pathways of heme and anaerobic cobalamin synthesis Biochemistry 38 1999 10660 10669
6. P. Hambright P.B. Chock Metal-porphyrin interactions. 3. A dissociative-interchange mechanism for metal ion incorporation into porphyrin molecules J. Am. Chem. Soc. 96 1974 3123 3131
7. D.K. Lavallee Porphyrin metalation reactions in biochemistry Molecular Structure and Energetics 1988 VCH Weinheim 279 314
8. T. Yoon J.A. Cowan Frataxin-mediated iron delivery to ferrochelatase in the final step of heme biosynthesis J. Biol. Chem. 279 2004 25943 25946
9. E. Lesuisse R. Santos B.F. Matzanke S.A. Knight J.M. Camadro A. Dancis Iron use for haeme synthesis is under control of the yeast frataxin homologue (Yfh1) Hum. Mol. Genet. 12 2003 879 889
10. H.A. O'Neill O. Gakh S. Park J. Cui S.M. Mooney M. Sampson Assembly of human frataxin is a mechanism for detoxifying redox-active iron Biochemistry 44 2005 537 545
11. T. Karlberg U. Schagerlof O. Gakh S. Park U. Ryde M. Lindahl The structures of frataxin oligomers reveal the mechanism for the delivery and detoxification of iron Structure 14 2006 1535 1546
12. R. Franco J.G. Ma Y. Lu G.C. Ferreira J.A. Shelnutt Porphyrin interactions with wild-type and mutant mouse ferrochelatase Biochemistry 39 2000 2517 2529
13. Y. Lu A. Sousa R. Franco A. Mangravita G.C. Ferreira I. Moura J.A. Shelnutt Binding of protoporphyrin IX and metal derivatives to the active site of wild-type mouse ferrochelatase at low porphyrin-to-protein ratios Biochemistry 41 2002 8253 8262
14. Z. Shi R. Franco R. Haddad J.A. Shelnutt G.C. Ferreira The conserved active-site loop residues of ferrochelatase induce porphyrin conformational changes necessary for catalysis Biochemistry 45 2006 2904 2912
15. M.E. Blackwood I.T.S. Rush F. Romesberg P.G. Schultz T.G. Spiro Alternative modes of substrate distortion in enzyme and antibody catalyzed ferrochelation reactions Biochemistry 37 1998 779 782
16. S. Venkateshrao J. Yin A.A. Jarzecki P.G. Schultz T.G. Spiro Porphyrin distortion during affinity maturation of a ferrochelatase antibody, monitored by resonance Raman spectroscopy J. Am. Chem. Soc. 126 2004 16361 16367
17. S. Al-Karadaghi M. Hansson S. Nikonov B. Jönsson L. Hederstedt Crystal structure of ferrochelatase: the terminal enzyme in heme biosynthesis Structure 5 1997 1501 1510
18. C.K. Wu H.A. Dailey J.P. Rose A. Burden V.M. Sellers B.C. Wang The 2.0 Å structure of human ferrochelatase, the terminal enzyme of heme biosynthesis Nature Struct. Biol. 8 2001 156 160
19. T. Karlberg D. Lecerof M. Gora G. Silvegren R. Labbe-Bois M. Hansson S. Al-Karadaghi Metal binding to Saccharomyces cerevisiae ferrochelatase Biochemistry 41 2002 13499 13506
20. D. Lecerof M. Fodje A. Hansson M. Hansson S. Al-Karadaghi Structural and mechanistic basis of porphyrin metallation by ferrochelatase J. Mol. Biol. 297 2000 221 232
21. J. Yin S.E. Andryski A.E. Beuscher R.C. Stevens P.G. Schultz Structural evidence for substrate strain in antibody catalysis Proc. Natl Acad. Sci. USA 100 2003 856 861
22. A. Medlock L. Swartz T.A. Dailey H.A. Dailey W.N. Lanzilotta Substrate interactions with human ferrochelatase Proc. Natl Acad. Sci. USA 104 2007 1789 1793
23. A.E. Medlock T.A. Dailey T.A. Ross H.A. Dailey W.N. Lanzilotta A π-helix switch selective for porphyrin deprotonation and product release in human ferrochelatase J. Mol. Biol. 373 2007 1006 1016
24. H.A. Dailey J.E. Fleming Bovine ferrochelatase. Kinetic analysis of inhibition by N -methylprotoporphyrin, manganese, and heme J. Biol. Chem. 258 1983 11453 11459
25. H.A. Dailey C.S. Jones S.W. Karr Interaction of free porphyrins and metalloporphyrins with mouse ferrochelatase. A model for the active site of ferrochelatase Biochim. Biophys. Acta 999 1989 7 11
26. Z. Shi G.C. Ferreira Modulation of inhibition of ferrochelatase by N -methylprotoporphyrin Biochem. J. 399 2006 21 28
27. H. Kohno M. Okuda T. Furukawa R. Tokunaga S. Taketani Site-directed mutagenesis of human ferrochelatase - Identification of histidine-263 as a binding-site for metal-ions Biochim. Biophys. Acta 1209 1994 95 100
28. M. Gora E. Grzybowska J. Rytka R. Labbe-Bois Probing the active-site residues in Saccharomyces cerevisiae ferrochelatase by directed mutagenesis. In vivo and in vitro analyses J. Biol. Chem. 271 1996 11810 11816
29. V.M. Sellers C.K. Wu T.A. Dailey H.A. Dailey Human ferrochelatase: characterization of substrate-iron binding and proton-abstracting residues Biochemistry 40 2001 9821 9827
30. D. Lecerof M.N. Fodje R.A. Leon U. Olsson A. Hansson E. Sigfridsson Metal binding to Bacillus subtilis ferrochelatase and interaction between metal sites J. Biol. Inorg. Chem. 8 2003 452 458
31. S. Shipovskov T. Karlberg M. Fodje M.D. Hansson G.C. Ferreira M. Hansson Metallation of the transition-state inhibitor N -methyl mesoporphyrin by ferrochelatase: implications for the catalytic reaction mechanism J. Mol. Biol. 352 2005 1081 1090
32. M.D. Hansson T. Karlberg M.A. Rahardja S. Al-Karadaghi M. Hansson Amino acid residues His183 and Glu264 in Bacillus subtilis ferrochelatase direct and facilitate the insertion of metal ion into protoporphyrin IX Biochemistry 46 2007 87 94
33. K.M. Barkigia D.J. Nurco M.W. Renner D. Melamed K.M. Smith J. Fajer Multiconformational surfaces in porphyrins: previews into excited-state landscapes J. Phys. Chem. 102 1998 322 326
34. J.A. Shelnutt X.Z. Song J.G. Ma S.L. Jia W. Jentzen C.J. Medforth Nonplanar porphyrins and their significance in proteins Chem. Soc. Rev. 27 1998 31 41
35. A.A. Jarzecki T.G. Spiro Porphyrin distortion from resonance Raman intensities of out-of-plane modes: computation and modeling of N -methylmesoporphyrin, a ferrochelatase transition state analog J. Phys. Chem. A 109 2005 421 430
36. W. Jentzen J.G. Ma J.A. Shelnutt Conservation of the conformation of the porphyrin macrocycle in hemoproteins Biophys. J. 74 1998 753 763
37. H.A. Dailey A. Smith Differential interaction of porphyrins used in photoradiation therapy with ferrochelatase Biochem. J. 223 1984 441 445
38. P.R. Ortiz de Montellano K.L. Kunze S.P. Cole G.S. Marks Inhibition of hepatic ferrochelatase by the four isomers of N -methylprotoporphyrin IX Biochem. Biophys. Res. Commun. 97 1980 1436 1442
39. F. de Matteis A.H. Gibbs C. Harvey Studies on the inhibition of ferrochelatase by N -alkylated dicarboxylic porphyrins. Steric factors involved and evidence that the inhibition is reversible Biochem. J. 226 1985 537 544
40. S.M. Kimmett R.A. Whitney G.S. Marks Evidence for the stereoselective inhibition of chick embryo hepatic ferrochelatase by N -alkylated porphyrins. II Mol. Pharmacol. 42 1992 307 310
41. P.R. Ortiz de Montellano K.L. Kunze S.P. Cole G.S. Marks Differential inhibition of hepatic ferrochelatase by the isomers of N -ethylprotoporphyrin IX Biochem. Biophys. Res. Commun. 103 1981 581 586
42. M. Hoggins H.A. Dailey C.N. Hunter J.D. Reid Direct measurement of metal ion chelation in the active site of human ferrochelatase Biochemistry 46 2007 8121 8127
43. M.D. Hansson M. Lindstam M. Hansson Crosstalk between metal ions in Bacillus subtilis ferrochelatase J. Biol. Inorg. Chem. 11 2006 325 333
44. C.B. Mammen T. Ursby M. Thunnissen J. Als-Nielsen Bent diamond crystals and multilayer based optics at the new 5-station protein crystallography beamline ‘Cassiopeia’ at MAX-lab AIP Conf. Proc. 705 2004 808 811
45. T. Ursby C.B. Mammen Y. Cerenius C. Svensson B. Sommarin M.N. Fodje The new macromolecular crystallography stations at MAX-lab: The MAD station AIP Conf. Proc. 705 2004 1241 1246
46. W. Kabsch Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants J. Appl. Crystallogr. 26 1993 795 800
47. A. Vagin A. Teplyakov MOLREP: an automated program for molecular replacement J. Appl. Crystallogr. 30 1997 1022 1025
48. A.T. Brunger P.D. Adams G.M. Clore W.L. Delano P. Gros R.W. Grosse-Kunstleve Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. D 54 1998 905 921
49. T.A. Jones J.Y. Zou S.W. Cowan M. Kjeldgaard Improved methods for building protein models in electron-density maps and the location of errors in these models Acta Crystallogr. A 47 1991 110 119
50. P. Emsley K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D 60 2004 2126 2132