Secreted heme peroxidase from Dictyostelium discoideum: Insights into catalysis, structure, and biological role

Journal of Biological Chemistry

Volumn 293, Issue 4, 2018, Pages 1330-1345

  Nicolussi, Andrea ^a   Dunn, Joe Dan ^b   Mlynek, Georg ^c   Bellei, Marzia ^d   Zamocky, Marcel ^a,e   Battistuzzi, Gianantonio ^d   Djinovic Carugo, Kristina ^c,f   Furtmüller, Paul G ^a   Soldati, Thierry ^b   Obinger, Christian ^a  

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

^b UNIVERSITY OF GENEVA   (Switzerland)

^c UNIVERSITY OF VIENNA   (Austria)

^d UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^e INSTITUTE OF CHEMISTRY   (Slovakia)

^f UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN-ANTIBODY REACTIONS; MAMMALS; NETWORK SECURITY; PORPHYRINS;

ANTIBACTERIAL DEFENSE; BACTERIAL CONTAMINATION; DICTYOSTELIUM DISCOIDEUM; FRUITING BODIES; INNATE IMMUNE SYSTEMS; MAMMALIAN PEROXIDASE; MULTICELLULAR DEVELOPMENT; NUTRIENT ACQUISITION;

CRYSTAL STRUCTURE;

BROMIDE; DDPOXA PROTEIN; GLUTAMIC ACID; HEME; IODIDE; METALLOPROTEIN; PEROXIDASE; THIOCYANATE; UNCLASSIFIED DRUG; HEME OXYGENASE; PROTOZOAL PROTEIN;

ARTICLE; COVALENT BOND; CRYSTAL STRUCTURE; DEVELOPMENT; DICTYOSTELIUM DISCOIDEUM; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME MODIFICATION; ENZYME REGULATION; ENZYME RELEASE; ENZYME STRUCTURE; HALOGENATION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA TRANSLATION; SEQUENCE HOMOLOGY; UPREGULATION; CATALYSIS; CHEMISTRY; DICTYOSTELIUM; ENZYMOLOGY; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION; STRUCTURE ACTIVITY RELATION;

CATALYSIS; DICTYOSTELIUM; HEME OXYGENASE (DECYCLIZING); OXIDATION-REDUCTION; PROTOZOAN PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 85041184397     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.RA117.000463     Document Type: Article

References (68)

1. Annesley, S. J., and Fisher, P. R. (2009) Dictyostelium discoideum-a model for many reasons. Mol. Cell. Biochem. 329, 73-91 CrossRef Medline
2. Cosson, P., and Soldati, T. (2008) Eat, kill or die: when amoeba meets bacteria. Curr. Opin. Microbiol. 11, 271-276 CrossRef Medline
3. Romeralo, M., Escalante, R., and Baldauf, S. L. (2012) Evolution and diversity of dictyostelid social amoebae. Protist 163, 327-343 CrossRef Medline
4. Li, S. I., and Purugganan, M. D. (2011) The cooperative amoeba: Dictyostelium as a model for social evolution. Trends Genet. 27, 48-54 CrossRef Medline
5. Williams, J. G. (2010) Dictyostelium finds new roles to model. Genetics 185, 717-726 CrossRef Medline
6. Eichinger, L., Pachebat, J. A., Glöckner, G., Rajandream, M. A., Sucgang, R., Berriman, M., Song, J., Olsen, R., Szafranski, K., Xu, Q., Tunggal, B., Kummerfeld, S., Madera, M., Konfortov, B. A., Rivero, F., et al. (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435, 43-57 CrossRef Medline
7. Zamocký, 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 CrossRef Medline
8. Hofbauer, S., Schaffner, I., Furtmüller, P. G., and Obinger, C. (2014) Chlorite dismutases-a heme enzyme family for use in bioremediation and generation of molecular oxygen. Biotechnol. J. 9, 461-473 CrossRef Medline
9. 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 71, 589-605Medline
10. Klebanoff, S. J., Kettle, A. J., Rosen, H., Winterbourn, C. C., and Nauseef, W. M. (2013) Myeloperoxidase: A front-line defender against phagocytosed microorganisms. J. Leukocyte Biol. 93, 185-198 CrossRef Medline
11. Bafort, F., Parisi, O., Perraudin, J. P., and Jijakli, M. H. (2014) Mode of action of lactoperoxidase as related to its antimicrobial activity: A review. Enzyme Res. 2014, 517164 Medline
12. Nauseef, W. M. (2014) Myeloperoxidase in human neutrophil host defence. Cell. Microbiol. 16, 1146-1155 CrossRef Medline
13. Ihalin, R., Loimaranta, V., and Tenovuo, J. (2006) Origin, structure, and biological activities of peroxidases in human saliva. Arch. Biochem. Biophys. 445, 261-268 CrossRef Medline
14. 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 CrossRef Medline
15. Desjardins, M., Houde, M., and Gagnon, E. (2005) Phagocytosis: The convoluted way from nutrition to adaptive immunity. Immunol. Rev. 207, 158-165 CrossRef Medline
16. Cosson, P., and Lima, W. C. (2014) Intracellular killing of bacteria: Is Dictyostelium a model macrophage or an alien? Cell. Microbiol. 16, 816-823 CrossRef Medline
17. 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 CrossRef Medline
18. 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 CrossRef Medline
19. Lin, Y. W. (2015) The broad diversity of heme-protein cross-links: An overview. Biochim. Biophys. Acta 1854, 844-859 CrossRef Medline
20. Zhang, M., Gaschen, B., Blay, W., Foley, B., Haigwood, N., Kuiken, C., and Korber, B. (2004) Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology 14, 1229-1246 CrossRef Medline
21. Monnat, J., Hacker, U., Geissler, H., Rauchenberger, R., Neuhaus, E. M., Maniak, M., and Soldati, T. (1997) Dictyostelium discoideum protein disulfide isomerase, an endoplasmic reticulum resident enzyme lacking a KDEL-type retrieval signal. FEBS Lett. 418, 357-362 CrossRef Medline
22. 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 Å resolution. J. Mol. Biol. 376, 1060-1075 CrossRef Medline
23. 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 CrossRef Medline
24. Ortiz de Montellano, P. R. (2016) in 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, UK
25. Auer, M., Gruber, C., Bellei, M., Pirker, K. F., Zamocky, M., Kroiss, D., Teufer, S. A., 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 CrossRef Medline
26. 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 CrossRef Medline
27. Nicolussi, A., Auer, M., Weissensteiner, J., Schütz, G., Katz, S., Maresch, D., Hofbauer, S., Bellei, M., Battistuzzi, G., Furtmüller, P. G., and Obinger, C. (2017) Posttranslational modification of heme b in a bacterial peroxidase: The role of heme to protein bonds in ligand binding and catalysis. Biochemistry 56, 4525-4538 CrossRef Medline
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) Pre-steady-state kinetics reveal the substrate specificity and mechanism of halide oxidation of truncated human peroxidasin 1. J. Biol. Chem. 292, 4583-4592 CrossRef Medline
29. Long, F., Vagin, A. A., Young, P., and Murshudov, G. N. (2008) BALBES: A molecular-replacement pipeline. Acta Crystallogr. D Biol. Crystallogr. 64, 125-132 CrossRef Medline
30. Furtmüller, P. G., Janschko, W., Zederbauer, M., Jakopitsch, C., Arnhold, J., and Obinger, C. (2004) Kinetics of interconversion of redox intermediates of lactoperoxidase, eosinophil peroxidase and myeloperoxidase. Jpn. J. Infect. Dis. 57, 30-31Medline
31. Banerjee, S., Furtmüller, P. G., and Obinger, C. (2011) Bovine lactoperoxidase-a versatile one- and two-electron catalyst of high structural and thermal stability. Biotechnol. J. 6, 231-243 CrossRef Medline
32. Sharma, S., Singh, A. K., Kaushik, S., Sinha, M., Singh, R. P., Sharma, P., Sirohi, H., Kaur, P., and Singh, T. P. (2013) Lactoperoxidase: Structural insights into the function, ligand binding and inhibition. Int. J. Biochem. Mol. Biol. 4, 108-128 Medline
33. Stajdohar, M., Rosengarten, R. D., Kokosar, J., Jeran, L., Blenkus, D., Shaulsky, G., and Zupan, B. (2017) dictyExpress: A web-based platform for sequence data management and analytics in Dictyostelium and beyond. BMC Bioinform. 18, 291 CrossRef Medline
34. Parikh, A., Miranda, E. R., Katoh-Kurasawa, M., Fuller, D., Rot, G., Zagar, L., Curk, T., Sucgang, R., Chen, R., Zupan, B., Loomis, W. F., Kuspa, A., and Shaulsky, G. (2010) Conserved developmental transcriptomes in evolutionary divergent species. Genome Biol. 11, R35 CrossRef Medline
35. Leiba, J., Sabra, A., Bodinier, R., Marchetti, A., Lima, W. C., Melotti, A., Perrin, J., Burdet, F., Pagni, M., Soldati, T., Lelong, E., and Cosson, P. (2017) Vps13F links bacterial recognition and intracellular killing in Dictyostelium. Cell. Microbiol. 19, e12722 CrossRef Medline
36. Buckley, C. M., Gopaldass, N., Bosmani, C., Johnston, S. A., Soldati, T., Insall, R. H., and King, J. S. (2016) WASH drives early recycling from macropinosomes and phagosomes to maintain surface phagocytic receptors. Proc. Natl. Acad. Sci. U.S.A. 113, E5902-E5915Medline
37. Aguirre, J., and Lambeth, J. D. (2010) Nox enzymes from fungus to fly to fish and what they tell us about Nox function in mammals. Free Radic. Biol. Med. 49, 1342-1353 CrossRef Medline
38. Zhang, X., Zhuchenko, O., Kuspa, A., and Soldati, T. (2016) Social amoebae trap and kill bacteria by casting DNA nets. Nat. Commun. 7, 10938 CrossRef Medline
39. Zhang, X., and Soldati, T. (2016) Of amoeba and Men: Extracellular DNA traps as an ancient cell-intrinsic defense mechanism. Front. Immunol. 7, 269 Medline
40. Grishkovskaya, I., Paumann-Page, M., Tscheliessnig, R., Stampler, J., Hofbauer, S., 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 in processing and maturation. J. Biol. Chem. 292, 8244-8261 CrossRef Medline
41. Banerjee, S., Stampler, J., Furtmüller, P. G., and Obinger, C. (2011) Conformational and thermal stability of mature dimeric human myeloperoxidase and a recombinant monomeric form from CHO cells. Biochim. Biophys. Acta 1814, 375-387 CrossRef Medline
42. 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 CrossRef Medline
43. 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 CrossRef Medline
44. Battistuzzi, G., Bellei, M., Bortolotti, C. A., and Sola, M. (2010) Redox properties of heme peroxidases. Arch. Biochem. Biophys. 500, 21-36 CrossRef Medline
45. 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 CrossRef Medline
46. 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 CrossRef
47. Furtmüller, P. G., Burner, U., and Obinger, C. (1998) Reaction of myeloperoxidase compound I with chloride, bromide, iodide, and thiocyanate. Biochemistry 37, 17923-17930 CrossRef Medline
48. 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 reactions with halides and thiocyanate. Biochemistry 39, 15578-15584 CrossRef Medline
49. Klebanoff, S. J. (1967) Iodination of bacteria: A bactericidal mechanism. J. Exp. Med. 126, 1063-1078 CrossRef Medline
50. Chandler, J. D., and Day, B. J. (2015) Biochemical mechanisms and therapeutic potential of pseudohalide thiocyanate in human health. Free Radic. Res. 49, 695-710 CrossRef Medline
51. Skaff, O., Pattison, D. I., and Davies, M. J. (2009) Hypothiocyanous acid reactivity with low-molecular mass and protein thiols: Absolute rate constants and assessment of biological relevance. Biochem. J. 422, 111-117 CrossRef Medline
52. Betts, P. M., Rinder, D. F., and Fleeker, J. R. (1979) Thiocyanate utilization by an Arthrobacter. Can. J. Mircobiol. 25, 1277-1282
53. Shetaya, W. H., Young, S. D., Watts, M. J., Ander, E. L., and Bailey, E. H. (2012) Iodine dynamics in soils. Geochim. Cosmochim. Acta 77, 457-473 CrossRef
54. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786 CrossRef Medline
55. Bradford, M. M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of proteindye binding. Anal. Biochem. 72, 248-254 CrossRef Medline
56. de Sanctis, D., Beteva, A., Caserotto, H., Dobias, F., Gabadinho, J., Giraud, T., Gobbo, A., Guijarro, M., Lentini, M., Lavault, B., Mairs, T., Mc-Sweeney, S., Petitdemange, S., Rey-Bakaikoa, V., Surr, J., et al. (2012) ID29: A high-intensity highly automated ESRF beamline for macromolecular crystallography experiments exploiting anomalous scattering. J. Synchrotron Radiat. 19, 455-461 CrossRef Medline
57. Kabsch, W. (2010) XDS. Acta Crystallogr D. Crystallogr. Biol. 66, 125-132 CrossRefMedline
58. Karplus, P. A., and Diederichs, K. (2012) Linking crystallographic model and data quality. Science 336, 1030-1033 CrossRef Medline
59. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D. Biol. Crystallogr. 66, 486-501 CrossRef Medline
60. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 CrossRef Medline
61. French, S., and Wilson, K. (1978) On the treatment of negative intensity observations. Acta Crystallogr. A 34, 517-525
62. Joosten, R. P., Salzemann, J., Bloch, V., Stockinger, H., Berglund, A. C., Blanchet, C., Bongcam-Rudloff, E., Combet, C., Da Costa, A. L., Deleage, G., Diarena, M., Fabbretti, R., Fettahi, G., Flegel, V., Gisel, A., et al. (2009) PDB-REDO: Automated re-refinement of X-ray structure models in the PDB. J. Appl. Crystallogr. 42, 376-384 CrossRef Medline
63. Davis, I. W., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2004) MOLPROBITY: Structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res. 32, W615-W619 CrossRef Medline
64. Krissinel, E., and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Cryst. D Biol. Crystallogr. 60, 2256-2268 CrossRefMedline
65. Chovancova, E., Pavelka, A., Benes, P., Strnad, O., Brezovsky, J., Kozlikova, B., Gora, A., Sustr, V., Klvana, M., Medek, P., Biedermannova, L., Sochor, J., and Damborsky, J. (2012) CAVER 3.0: A tool for the analysis of transport pathways in dynamic protein structures. PLoS Comput. Biol. 8, e1002708 CrossRef Medline
66. Fey, P., Kowal, A. S., Gaudet, P., Pilcher, K. E., and Chisholm, R. L. (2007) Protocols for growth and development of Dictyostelium discoideum. Nat. Protoc. 2, 1307-1316 CrossRef Medline
67. Veltman, D. M., Akar, G., Bosgraaf, L., and Van Haastert, P. J. (2009) A new set of small, extrachromosomal expression vectors for Dictyostelium discoideum. Plasmid 61, 110-118 CrossRef Medline
68. Hagedorn, M., Neuhaus, E. M., and Soldati, T. (2006) Optimized fixation and immunofluorescence staining methods for Dictyostelium cells. Methods Mol. Biol. 346, 327-338 Medline