Posttranslational Modification of Heme b in a Bacterial Peroxidase: The Role of Heme to Protein Ester Bonds in Ligand Binding and Catalysis

Biochemistry

Volumn 56, Issue 34, 2017, Pages 4525-4538

  Nicolussi, Andrea ^a   Auer, Markus ^a   Weissensteiner, Julia ^a   Schütz, Georg ^a   Katz, Sonja ^a   Maresch, Daniel ^a   Hofbauer, Stefan ^a   Bellei, Marzia ^b   Battistuzzi, Gianantonio ^b   Furtmüller, Paul G ^a   Obinger, Christian ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; ESCHERICHIA COLI; ESTERS; MAMMALS; PROTEINS;

BIOCHEMICAL PROPERTIES; CATALYTIC PROPERTIES; FUNCTIONAL DATAS; MAMMALIAN PEROXIDASE; POST-TRANSLATIONAL MODIFICATIONS; STRUCTURAL FEATURE; STRUCTURAL REARRANGEMENT; TWO-ELECTRON REDUCTION;

PORPHYRINS;

APOPROTEIN; BACTERIAL ENZYME; BROMIDE; ESTER; HEME B PROTEIN; HEMOPROTEIN; HYDROGEN PEROXIDE; IODIDE; PEROXIDASE; THIOCYANATE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; HEME; LIGAND;

ARTICLE; CATALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; ELECTRON; ESCHERICHIA COLI; LIGAND BINDING; LYNGBYA; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN STRUCTURE; WILD TYPE; CHEMISTRY; CYANOBACTERIUM; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY;

BACTERIAL PROTEINS; CATALYSIS; CYANOBACTERIA; HEME; LIGANDS; PEROXIDASE; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 85028565577     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.7b00632     Document Type: Article

References (42)

1. Zamocky, M., Hofbauer, S., Schaffner, I., Gasselhuber, B., Nicolussi, A., Soudi, M., Pirker, K. F., Furtmüller, P. G., and Obinger, C. (2015) Independent evolution of four heme peroxidase superfamilies Arch. Biochem. Biophys. 574, 108-119 10.1016/j.abb.2014.12.025
2. Zamocky, M., Jakopitsch, C., Furtmüller, P. G., Dunand, C., and Obinger, C. (2008) The peroxidase-cyclooxygenase superfamily. Reconstructed evolution of critical enzymes of the innate immune system Proteins: Struct., Funct., Genet. 72, 589-605 10.1002/prot.21950
3. Zederbauer, M., Furtmüller, P. G., Brogioni, S., Jakopitsch, C., Smulevich, G., and Obinger, C. (2007) Heme to protein linkages in mammalian peroxidases: impact on spectroscopic, redox and catalytic properties Nat. Prod. Rep. 24, 571-584 10.1039/B604178G
4. Carpena, X., Vidossich, P., Schroettner, K., Calisto, B. M., Banerjee, S., Stampler, J., Soudi, M., Furtmüller, P. G., Rovira, C., Fita, I., and Obinger, C. (2009) Essential role of proximal histidine-asparagine interaction in mammalian peroxidases J. Biol. Chem. 284, 25929-25937 10.1074/jbc.M109.002154
5. Nauseef, W. M. (2014) Myeloperoxidase in human neutrophil host defence Cell. Microbiol. 16, 1146-1155 10.1111/cmi.12312
6. Ihalin, R., Loimaranta, V., and Tenovuo, J. (2006) Origin, structure, and biological activities of peroxidases in human saliva Arch. Biochem. Biophys. 445, 261-268 10.1016/j.abb.2005.07.004
7. Malik, A. and Batra, J. K. (2012) Antimicrobial activity of human eosinophil granule proteins: involvement in host defence against pathogens Crit. Rev. Microbiol. 38, 168-181 10.3109/1040841X.2011.645519
8. Ruf, J. and Carayon, P. (2006) Structural and functional aspects of thyroid peroxidase Arch. Biochem. Biophys. 445, 269-277 10.1016/j.abb.2005.06.023
9. Ortiz de Montellano, P. R. (2016) Heme peroxidases: self-processing of peroxidases (Raven, E. and Dunford, B., Eds) RSC Metallobiology Series No. 4, pp 3-30, The Royal Society of Chemistry, Cambridge, U.K.
10. Zbylut, S. D. and Kincaid, J. R. (2002) Resonance Raman evidence for protein-induced out-of-plane distortion of the heme prosthetic group of mammalian lactoperoxidase J. Am. Chem. Soc. 124, 6751-6758 10.1021/ja012578u
11. Brogioni, S., Feis, A., Marzocchi, M. P., Zederbauer, M., Furtmüller, P. G., Obinger, C., and Smulevich, G. (2006) Resonance assignment of myeloperoxidase and the selected mutants Asp94Val, and Met242Thr. Effect of heme distortion J. Raman Spectrosc. 37, 263-276 10.1002/jrs.1442
12. Singh, A. K., Singh, N., Sharma, S., Singh, S. B., Kaur, P., Bhushan, A., Srinivasan, A., and Singh, T. P. (2008) Crystal structure of lactoperoxidase at 2.4 A resolution J. Mol. Biol. 376, 1060-1075 10.1016/j.jmb.2007.12.012
13. Battistuzzi, G., Bellei, M., Bortolotti, C. A., and Sola, M. (2010) Redox properties of heme peroxidases Arch. Biochem. Biophys. 500, 21-36 10.1016/j.abb.2010.03.002
14. Battistuzzi, G., Stampler, J., Bellei, M., Vlasits, J., Soudi, M., Furtmüller, P. G., and Obinger, C. (2011) Influence of the covalent heme-protein bonds on the redox thermodynamics of human myeloperoxidase Biochemistry 50, 7987-7994 10.1021/bi2008432
15. Burner, U., Jantschko, W., and Obinger, C. (1999) Kinetics of oxidation of aliphatic and aromatic thiols by myeloperoxidase compounds I and II FEBS Lett. 443, 290-296 10.1016/S0014-5793(98)01727-X
16. Burner, U., Furtmüller, P. G., Kettle, A. J., Koppenol, W., and Obinger, C. (2000) Mechanism of reaction of myeloperoxidase with nitrite J. Biol. Chem. 275, 20597-20601 10.1074/jbc.M000181200
17. Jantschko, W., Furtmüller, W., Allegra, M., Livrea, M. A., Jakopitsch, C., Regelsberger, G., and Obinger, C. (2002) Redox intermediates of plant and mammalian peroxidases: a comparative transient-kinetic study of their reactivity toward indole derivatives Arch. Biochem. Biophys. 398, 12-22 10.1006/abbi.2001.2674
18. Furtmüller, P. G., Zederbauer, M., Jantschko, W., Helm, J., Bogner, M., Jakopitsch, C., and Obinger, C. (2006) Active site structure and catalytic mechanisms of human peroxidases Arch. Biochem. Biophys. 445, 199-213 10.1016/j.abb.2005.09.017
19. Arnhold, J., Monzani, E., Furtmüller, P. G., Zederbauer, M., Casella, L., and Obinger, C. (2006) Kinetics and thermodynamics of halide and nitrite oxidation by heme peroxidases Eur. J. Inorg. Chem. 2006, 3801-3811 10.1002/ejic.200600436
20. Auer, M., Gruber, C., Bellei, M., Pirker, K., Zamocky, M., Kroiß, D., Teufer, A. S., Hofbauer, S., Soudi, M., Battistuzzi, G., Furtmüller, P. G., and Obinger, C. (2013) A stable bacterial peroxidase with novel halogenating activity and an autocatalytically linked heme prosthetic group J. Biol. Chem. 288, 27181-27199 10.1074/jbc.M113.477067
21. Auer, M., Nicolussi, A., Schütz, G., Furtmüller, P. G., and Obinger, C. (2014) How covalent heme to protein bonds influence the formation and reactivity of redox intermediates of a bacterial peroxidase J. Biol. Chem. 289, 31480-31491 10.1074/jbc.M114.595157
22. Banerjee, S., Furtmüller, P. G., and Obinger, C. (2011) Bovine lactoperoxidase-a versatile one- and two-electon catalyst of high structural and thermal stability Biotechnol. J. 6, 231-243 10.1002/biot.201000375
23. Sharma, S., Singh, A. K., Kaushik, S., Sinah, M., Singh, R. P., Sharma, P., Sirohi, H., Kaur, P., and Singh, T. P. (2013) Lactoperoxidase: structural insights into the function, ligand binding and inhibiton Int. J. Biochem. Mol. Biol. 4, 108-128
24. DePillis, G. D., Ozaki, S., Kuo, J. M., Maltby, D. A., and Ortiz de Montellano, P. R. (1997) Autocatalytic processing of heme by lactoperoxidase produces the native protein-bound prosthetic group J. Biol. Chem. 272, 8857-8860 10.1074/jbc.272.14.8857
25. Colas, C., Kuo, J. M., and Ortiz de Montellano, P. R. (2002) Asp 225 and Glu 375 in autocatalytic attachment of the prosthetic heme group of lactoperoxidase J. Biol. Chem. 277, 7191-7200 10.1074/jbc.M109523200
26. Oxvig, C., Thomsen, A. R., Overgaard, M. T., Sorensen, E. S., Højrup, P., Bjerrum, M. J., Gleich, G. J., and Sottrup-Jensen, L. (1999) Biochemical evidence for heme linkage through esters with Asp-93 and Glu-241 in human eosinophil peroxidase. The ester with Asp-93 is only partially formed in vivo J. Biol. Chem. 274, 16953-16958 10.1074/jbc.274.24.16953
27. Soudi, M., Paumann-Page, M., Delporte, C., Pirker, K. F., Bellei, M., Edenhofer, E., Stadlmayr, G., Battistuzzi, G., Zouaoui Boudjeltia, K., Furtmüller, P. G., Van Antwerpen, P., and Obinger, C. (2015) Multidomain human peroxidasin 1 is a highly glycosylated and stable homotrimeric high-spin ferric peroxidase J. Biol. Chem. 290, 10876-10890 10.1074/jbc.M114.632273
28. Paumann-Page, M., Katz, R. S., Bellei, M., Schwartz, I., Edenhofer, E., Sevcnikar, B., Soudi, M., Hofbauer, S., Battistuzzi, G., Furtmüller, P. G., and Obinger, C. (2017) Kinetics of interconversion of redox intermediates of truncated human peroxidasin 1 mediated by hydrogen peroxide, bromide, iodide and thiocyanate J. Biol. Chem. 292, 4583-4592 10.1074/jbc.M117.775213
29. Colas, C. and Ortiz de Montellano, P. R. (2004) Horseradish peroxidase mutants that autocatalytically modify their prosthetic heme group: insights into mammalian peroxidase heme-protein covalent bonds J. Biol. Chem. 279, 24131-24140 10.1074/jbc.M401687200
30. Battistuzzi, G., Bellei, M., Zederbauer, M., Furtmüller, P. G., Sola, M., and Obinger, C. (2006) Redox thermodynamics of the Fe(III)/Fe(II) Couple of human myeloperoxidase in its high-spin and low-spin forms Biochemistry 45, 12750-12755 10.1021/bi061647k
31. Battistuzzi, G., Bellei, M., Vlasits, J., Banerjee, S., Furtmüller, P. G., Sola, M., and Obinger, C. (2010) Redox thermodynamics of lactoperoxidase and eosinophil peroxidase Arch. Biochem. Biophys. 494, 72-77 10.1016/j.abb.2009.11.021
32. Furtmüller, P. G., Arnhold, J., Jantschko, W., Zederbauer, M., Jakopitsch, C., and Obinger, C. (2005) Standard reduction potentials of all couples of the peroxidase cycle of lactoperoxidase J. Inorg. Biochem. 99, 1220-1229 10.1016/j.jinorgbio.2005.02.021
33. Huang, L. and Ortiz de Montellano, P. R. (2006) Heme-protein covalent bonds in peroxidases and resistance to heme modification during halide oxidation Arch. Biochem. Biophys. 446, 77-83 10.1016/j.abb.2005.11.011
34. Huang, L., Wojciechowski, G., and Ortiz de Montellano, P. R. (2006) Role of heme-protein covalent bonds in mammalian peroxidases. Protection of the heme by a single engineered heme-protein link in horseradish peroxidase J. Biol. Chem. 281, 18983-18988 10.1074/jbc.M602307200
35. Furtmüller, P. G., Burner, U., and Obinger, C. (1998) Reaction of human myeloperoxidase compound I with chloride, bromide, iodide, and thiocyanate Biochemistry 37, 17923-17930 10.1021/bi9818772
36. Furtmüller, P. G., Jantschko, W., Regelsberger, G., Jakopitsch, C., Arnhold, J., and Obinger, C. (2002) Reaction of lactoperoxidase compound I with halides and thiocyanate Biochemistry 41, 11895-11900 10.1021/bi026326x
37. Furtmüller, P. G., Burner, U., Regelsberger, G., and Obinger, C. (2000) Spectral and kinetic studies on the formation of eosinophil peroxidase compound I and its reaction with halides and thiocyanate Biochemistry 39, 15578-15584 10.1021/bi0020271
38. Blair-Johnson, M., Fiedler, T., and Fenna, R. (2001) Human myeloperoxidase: structure of a cyanide complex and its interaction with bromide and thiocyanate substrates at 1.9 Å resolution Biochemistry 40, 13990-13997 10.1021/bi0111808
39. Grishkovskaya, I., Paumann-Page, M., Tscheliessnig, R., Hofbauer, S., Stampler, J., Soudi, M., Sevcnikar, B., Oostenbrink, C., Furtmüller, P. G., Djinović-Carugo, K., Nauseef, W. M., and Obinger, C. (2017) Structure of human promyeloperoxidase (proMPO) and the role of the propeptide for processing and maturation J. Biol. Chem. 292, 8244-8261 10.1074/jbc.M117.775031
40. Singh, P. K., Sirohi, H. V., Iqbal, N., Tiwari, P., Kaur, P., Sharma, S., and Singh, T. P. (2017) Structure of bovine lactoperoxidase with a partially linked heme moiety at 1.98 Å resolution Biochim. Biophys. Acta, Proteins Proteomics 1865, 329-335 10.1016/j.bbapap.2016.12.006
41. Zederbauer, M., Jantschko, W., Neugschwandtner, K., Jakopitsch, C., Moguilevsky, N., Obinger, C., and Furtmüller, P. G. (2005) Role of covalent glutamic acid 242-heme linkage in the formation and reactivity of redox intermediates of human myeloperoxidase Biochemistry 44, 6482-6491 10.1021/bi0501737
42. Zederbauer, M., Furtmüller, P. G., Bellei, M., Stampler, J., Jakopitsch, C., Battistuzzi, G., Moguilevsky, N., and Obinger, C. (2007) Disruption of the aspartate to heme ester linkage in human myeloperoxidase: impact on ligand binding, redox chemistry, and interconversion of redox intermediates J. Biol. Chem. 282, 17041-17052 10.1074/jbc.M610685200