Research Group Pierik

Research

Prof. Dr. Antonio Pierik

Research

Iron-sulfur proteins of prokaryotes and eukaryotes

My group discovers and characterizes novel iron-sulfur proteins through a combination of bioinformatic, protein biochemical and spectroscopic approaches. Equally of interest are non-cysteine coordinated Fe/S proteins, catalytically active (dehydratase) Fe/S enzymes and Fe/S biogenesis in the cytosol of eukaryotes. Our results are of importance for a fundamental understanding of bioinorganic cofactors in Life and for biotechnological application.

In collaborative efforts with the laboratories of Prof. Dr. Matthias Boll (Freiburg), Prof. Dr. Gunhild Layer (Leipzig), Prof. Dr. Holger Dobbek, Dr. Berta Martins (both Humboldt University), Prof. Dr. Hans Heider (Philipps University, Marburg) and others we contribute by the determination of cluster type, amount, redox state and function via application of EPR spectroscopy in a wide range of Fe/S proteins from all kingdoms.

Within the TU Kaiserslautern the Schünemann group is our key collaborator for Mössbauer spectroscopy. We enjoy the collaboration with Dr. Ed Reijerse and Prof. Dr. Wolfgang Lubitz (MPI Müllheim) on pulsed EPR spectroscopies and the collaboration with Prof. Mario Piccioli and Prof. Dr. Simone Ciofi-Baffoni (CERM, Florence, Italy) on NMR spectroscopy.

In the Biology department we have ongoing collaborations with Jun. Prof. Dr. Sabine Filker, Prof. Dr. Thorsten Stoeck and Prof. Dr. Nicole Frankenberg-Dinkel.

Mass spectrometry is carried out with the MALDI-TOF mass spectrometer of physical chemistry group in our department (Prof. Dr. Gereon Niedner-Schattenburg) or with the Centre for Mass Spectrometry Analytics (Prof. Dr. Michael Schroda) in the department of Biology.

 

Publications

1. Khelwati, H., Schäfgen, B., Bechtel, D.F., DeCuyper, A., Schüssler, A., Neuba, A., Pierik, A.J., Ernst, S., Müller, T.J.J. & Thiel, W.R. (2019) New J. Chem., in press. Phenothiazine electrophores immobilized by ion exchange on periodic mesoporous organosilicas

 

2. Willistein, M., Bechtel, D.F., Müller, C.S., Demmer, D., Heimann, L., Kayastha, K., Volker Schünemann, V., Pierik, A.J., Ullmann, G.M., Ermler, U. & Boll, M. (2019) Nat. Commun. 10, 2074. Low potential enzymatic hydride transfer via highly cooperative and inversely functionalized flavin cofactors.

 

3. Stegmaier, K., Blinn, C.M., Bechtel, D.F., Greth, C., Auerbach, H., Müller, C.S., Jakob, V., Reijerse, E.J., Netz, D.J.A., Schünemann, V. & Pierik, A.J. (2019) J. Am. Chem. Soc. 141, 5753-5765. Apd1 and Aim32 are prototypes of bishistidinyl-coordinated non-Rieske [2Fe-2S] proteins.

 

4. Weinisch, L., Kirchner, I., Grimm, M., Kühnert, S., Pierik, A.J., Rosselló-Móra, R. & Filker, S. (2019) Microbial Ecol. 77, 317-331. Glycine betaine and ectoine are the major compatible solutes used by four different halophilic heterotrophic ciliates.

 

5. Tonini, M.L., Peña-Diaz, P., Haindrich, A.C., Basu, S., Kriegová, E., Pierik, A.J., Lill, R., MacNeill, S.A., Smith, T.K., Lukeš, J. (2018) PLoS Pathog. 14, e1007326. Branched late-steps of the cytosolic iron-sulphur cluster assembly machinery of Trypanosoma brucei.

 

6. Weinisch, L., Kühner, S., Roth, R., Grimm, M., Roth, T., Netz, D.J.A., Pierik, A.J. & Filker, S. (2018) PLoS Biol. 16, e2003892. Identification of osmoadaptive strategies in the halophile, heterotrophic ciliate Schmidingerothrix salinarum.

 

7. Müller, C.S., Auerbach, H., Stegmaier, K., Wolny, J.A., Schünemann, V. & Pierik, A.J. (2017) Hyperfine Interact. 238, 102. Mössbauer spectroscopy and DFT calculations on all protonation states of the 2Fe-2S cluster of the Rieske protein.

 

8. Mergelsberg, M., Willistein, M., Meyer, H., Stärk, H.-J., Bechtel, D.F., Pierik, A.J. & Boll, M. (2017) Environm. Microbiol. 19, 3734-3744. Phthaloyl-coenzyme A decarboxylase from Thauera chlorobenzoica: the prenylated flavin-, K+- and Fe2+-dependent key enzyme of anaerobic phthalate degradation

 

9. Grandl, M., Rudolf, B., Sun, Y., Bechtel, D.F., Pierik, A.J. & Pammer, F. (2017) Organometallics 36, 2527-2535. Intramolecular N→B coordination as a stabilizing scaffold for π-conjugated radical anions with tunable redox potentials.

 

10. Schmid, G., Auerbach, H., Pierik, A.J., Schünemann, V. & Boll, M. (2016) Biochemistry 55, 5578-5586. ATP-dependent electron activation module of benzoyl-coenzyme A reductase from the hyperthermophilic archaeon Ferroglobus placidus.

 

11. Benz, C., Kovářová, J., Králová-Hromadová, I., Pierik, A.J. & Lukeš, J. (2016) Int. J. Parasitol. 46, 641-651. Roles of the Nfu Fe-S targeting factors in the trypanosome mitochondrion.

 

12. Netz, D.J., Genau, H.M., Weiler, B.D., Bill, E., Pierik*, A.J. & Lill*, R. (2016) Biochem. J. 473, 2073-2085. The conserved protein Dre2 uses essential [2Fe-2S] and [4Fe-4S] clusters for its function in cytosolic iron-sulfur protein assembly.

 

13. Chung, J.-Y., Schulz,C., Bauer, H., Sun, Y., Sitzmann, H., Auerbach, H., Pierik, A.J., Schünemann, V., Neuba, A., & Thiel, W.R. (2015) Organometallics 34, 5374-5382. Cyclopentadienide ligand CpC− possessing intrinsic helical chirality and its ferrocene analogues.

 

14. Paul, V.D., Mühlenhoff, U., Stümpfig, M., Seebacher, J., Kugler, K.G., Renicke, C., Taxis, C., Gavin, A.-C., Pierik, A.J. & Lill, R. (2015) eLIFE 4, e08231. The deca-GX3 proteins Yae1-Lto1 function as adaptors recruiting the ABC protein Rli1 for iron-sulfur cluster insertion.

 

15. Zhang, J., Friedrich, P., Pierik, A.J., Martins, B.M. & Buckel, W. (2015) Appl. Environm. Microbiol. 81, 1071-1084. Substrate-induced radical formation in 4-hydroxybutyryl coenzyme A dehydratase from Clostridium aminobutyricum.

 

16. Glatt, S., Zabel, R., Vonkova, I., Kumar, A., Netz, D.J., Pierik, A.J., Rybin, V., Lill, R., Gavin, A.-C., Balbach, J., Breunig, K.D. & Müller, C.W. (2015) Structure 23, 149-160. Structure of the Kti11/Kti13 heterodimer and its double role in modifications of tRNA and eukaryotic elongation factor 2.

 

17. Rietzschel, N., Pierik, A.J., Bill, E., Lill, R. & Mühlenhoff, U. (2015) The basic leucine zipper stress response regulator Yap5 senses high-iron conditions by coordination of [2Fe-2S] clusters. Mol. Cell. Biol. 34, 370-378.

 

18. Selvaraj, B., Pierik, A.J., Bill, E. & Martins, B. (2014) The ferredoxin-like domain of the activating enzyme is required for generating a lasting glycyl radical in 4-hydroxyphenylacetate decarboxylase. J. Biol. Inorg. Chem. 19, 1317-1326.

 

19. Basu, S., Netz, D.J., Haindrich, A.C., Herlerth, N., Lagny, T.J., Pierik*, A.J., Lill*, R. & Lukeš*, J. (2014) Mol. Microbiol. 93, 897-910. Cytosolic iron-sulphur protein assembly is functionally conserved and essential in procyclic and bloodstream Trypanosoma brucei.

 

20. Srinivasan, V., Pierik, A.J. & Lill, R. (2014) Science 343, 1137-1140. Crystal structures of nucleotide-free and glutathione-bound mitochondrial ABC transporter Atm1.

 

21. Vitt, S., Ma, K., Warkentin, E., Moll, J., Pierik, A.J., Shima, S. & Ermler, U. (2014) J. Mol. Biol. 426, 2813-2826. The F420-reducing [NiFe]-hydrogenase complex from Methanothermobacter marburgensis, the first X-ray structure of a group 3 family member.

 

22. Selvaraj, B., Pierik, A.J., Bill, E. & Martins, B.M. (2013) J. Biol. Inorg. Chem. 18, 633-643. 4-Hydroxyphenylacetate decarboxylase activating enzyme catalyses a classical S adenosylmethionine reductive cleavage reaction.

 

23. Stehling, O., Mascarenhas, J., Vashisht, A.A., Sheftel, A.D., Niggemeyer, B., Rösser, R., Pierik, A.J., Wohlschlegel, J.A. & Lill, R. (2013) Cell Metab. 18, 187-198. Human CIA2A-FAM96A and CIA2B-FAM96B integrate iron homeostasis and maturation of different subsets of cytosolic-nuclear iron-sulfur proteins.

 

24. Bernard, D.G., Netz, D.J.A., Lagny, T.J., Pierik*, A.J. & Balk*, J. (2013) Philos. Trans. R. Soc. Lond. B 368, 20120259. Requirements of the cytosolic iron–sulphur cluster assembly pathway in Arabidopsis.

 

25. Ringel, P., Krausze, J., van den Heuvel, J., Curth, U., Pierik, A.J., Herzog, S., Mendel, R.R. & Kruse, T. (2013) J. Biol. Chem. 288, 14657-14671. Biochemical characterization of molybdenum cofactor-free nitrate reductase from Neurospora crassa.

 

26. Soboh, B., Kuhns, M., Braussemann, M., Waclawek, M., Muhr, E., Pierik, A.J. & Sawers, R.G. (2012) Biochem Biophys. Res. Commun. 424, 158-163. Evidence for an oxygen-sensitive iron-sulfur cluster in an immature large subunit species of Escherichia coli [NiFe]-hydrogenase 2.

 

27. Stehling, O., Vashisht, A.A., Mascarenhas, J., Jonsson, Z.O., Sharma, T., Netz, D.J., Pierik, A.J., Wohlschlegel, J.A. & Lill, R. (2012) Science 337, 195-199. MMS19 assembles iron-sulfur proteins required for DNA metabolism and genomic integrity.

 

28. Netz, D. J. A., Pierik, A.J., Stümpfig, M., Bill, E., Sharma, A.K., Pallesen, L.J., Walden, W.E. & Lill, R. (2012) J. Biol. Chem. 287, 12365-12378. A bridging [4Fe-4S] cluster and nucleotide binding are essential for function of the Cfd1-Nbp35 complex as a scaffold in iron-sulfur protein maturation.

 

29. Netz, D. J. A., Stith, C. M., Stümpfig, M., Köpf, G., Vogel, D., Genau, H.M., Stodola, J.L., Lill*, R., Burgers*, P.M.J. & Pierik*, A.J. (2012) Nat. Chem. Biol. 8, 125-132. Eukaryotic DNA polymerases require an iron-sulfur cluster for formation of active complexes.

 

30. Geisselbrecht, Y., Frühwirth, S., Schröder, C., Pierik, A.J., Klug, G., Essen, L.-O. (2012) EMBO Rep. 13, 223-229. CryB from Rhodobacter sphaeroides: a unique class of cryptochromes with new cofactors.

 

31. Hilberg, M., Pierik, A.J., Bill, E., Friedrich, T., Lippert, M.-L. & Heider, J. (2012) J. Biol. Inorg. Chem. 17, 49-56. Identification of FeS clusters in the glycyl-radical enzyme benzylsuccinate synthase via EPR and Mössbauer spectroscopy.

 

32. Mühlenhoff, U., Richter, N., Pines, O., Pierik, A.J. & Lill, R. (2011) J. Biol. Chem. 286, 41205-41216. Specialized function of yeast Isa1 and Isa2 proteins in the maturation of mitochondrial [4Fe-4S] proteins.

 

33. Oberpichler, I., Pierik, A.J., Wesslowski, J., Pokorny, R., Rosen, R., Vugman, M., Zhang, F., Neubauer, O. Ron, E.Z., Batschauer, A. & Lamparter, T. (2011) PLoS ONE 6, e26775. A photolyase-like protein from Agrobacterium tumefaciens with an iron-sulfur cluster.

 

34. Parthasarathy, A., Pierik, A.J., Kahnt, J., Zelder, O. & Buckel, W. (2011) Biochemistry 50, 3540-3550. Substrate specificity of 2-hydroxyglutaryl-CoA dehydratase from Clostridium symbiosum: towards a bio-based production of adipic acid.

 

35. Miethke, M., Pierik, A.J., Peuckert, F., Seubert, A. & Marahiel, M.A. (2011) J. Biol. Chem. 286, 2245-2260. Identification and characterization of a novel-type ferric siderophore reductase from a Gram-positive extremophile.

 

36. Stolle, P., Barckhausen, O., Oehlmann, W., Knobbe, N., Vogt, C., Pierik, A.J., Cox, N., Schmidt, P., Reijerse, E., Lubitz, W. & Auling, G. (2010) Homologous expression of the nrdF gene of Corynebacterium ammoniagenes strain ATCC 6872 generates a manganese-metallo-cofactor (R2F) and a stable tyrosyl radical (Y•) involved in ribonucleotide reduction. FEBS J. 277, 4849-4862.

 

37. Netz, D.J.A., Stümpfig, M., Doré, C., Mühlenhoff, U., Pierik*, A.J. & Lill*, R. (2010) Nat. Chem. Biol. 6, 758-765. Tah18 transfers electrons to Dre2 in cytosolic iron-sulfur protein biogenesis.

 

38. Sheftel, A.D., Stehling, O., Pierik, A.J., Elsässer, H.-P., Mühlenhoff, U., Webert, H., Hobler, A., Hannemann, F., Bernhardt, R. & Lill, R. (2010) Proc. Nat. Acad. Sci. USA 107, 11775-11780. Humans possess two mitochondrial ferredoxins, Fdx1 and Fdx2, with distinct roles in steroidogenesis, heme, and Fe/S cluster biosynthesis.

 

39. Kim, J., Pierik, A.J. & Buckel, W. (2010) ChemPhysChem 11, 1307-1312. A complex of 2-hydroxyisocaproyl-coenzyme A dehydratase and its activator from Clostridium difficile stabilized by aluminium tetrafluoride-adenosine diphosphate.

 

40. Albrecht, A.G., Netz, D.J.A., Miethke, M., Pierik, A.J., Burghaus, O., Peuckert, F., Lill, R. & Marahiel, M.A. (2010) J. Bacteriol. 192, 1643-1651. SufU is an essential iron-sulfur cluster scaffold protein in Bacillus subtilis.

 

41. Schwenkert, S., Netz, D.J.A., Frazzon, J., Pierik, A.J., Bill, E., Gross, J., Lill, R. & Meurer, J. (2010) Biochem. J. 425, 207-214. Chloroplast HCF101 is a scaffold protein for [4Fe-4S] cluster assembly.

 

42. Sheftel, A.D., Stehling, O., Pierik, A.J., Netz, D.J.A., Kerscher, S., Elsässer, H.-P., Wittig, I., Balk, J., Brandt, U. & Lill, R. (2009) Mol. Cell. Biol. 29, 6059-6073. Human Ind1, an iron-sulfur cluster assembly factor for respiratory complex I.

 

43. Abbouni, B., Oehlmann, W., Stolle, P., Pierik, A.J. & Auling, G. (2009) Free Rad. Res. 43, 943-950. Electron paramagnetic resonance (EPR) spectroscopy of the stable-free radical in the native metallo-cofactor of the manganese-ribonucleotide reductase (Mn-RNR) of Corynebacterium glutamicum.

 

44. Wagener, N., Pierik, A.J., Ibdah, A., Hille, R. & Dobbek, H. (2009) Proc. Nat. Acad. Sci. USA 106, 11055-11060. The Mo-Se active site of nicotinate dehydrogenase.

 

45. Velarde, M., Macieira, S., Hilberg, M., Bröker,G., Tu, S.-M., Golding, B.T., Pierik, A.J., Buckel, W. & Messerschmidt, A. (2009) J. Mol. Biol. 391, 609–620. Crystal structure and putative mechanism of methylitaconate-Δ-isomerase from Eubacterium barkeri.

 

46. Pierik, A.J., Netz, D.J.A. & Lill, R. (2009) Nat. Protoc. 4, 753-766. Analysis of iron-sulfur protein maturation in eukaryotes.

 

47. Urzica, U., Pierik, A.J., Mühlenhoff, U. & Lill, R. (2009) Biochemistry 48, 4946-4958. Crucial role of conserved cysteine residues in the assembly of two iron-sulfur clusters on the CIA protein Nar1.

 

48. Schilhabel, A., Studenik, S., Vödisch, M., Kreher, S., Schlott, B., Pierik, A.J. & Diekert, G. (2009) J. Bact. 191, 588-599. The ether-cleaving methyltransferase system of the strict anaerobe Acetobacterium dehalogenans: Analysis and expression of the encoding genes.

 

49. Bych, K., Netz, D.J.A., Vigani, G., Bill, E., Lill, R., Pierik, A.J. & Balk, J. (2008) J. Biol. Chem. 284, 35797-35804. The essential cytosolic iron-sulfur protein Nbp35 acts without Cfd1 partner in the green lineage.

 

50. Kreß, D., Alhapel, A., Pierik*, A.J. & Essen*, L.-O. (2008) J. Mol. Biol. 384, 837-847. The crystal structure of enamidase: a bifunctional enzyme of the nicotinate catabolism.

 

51. Bursy, J., Kuhlmann, A.U., Pittelkow, M., Hartmann, H., Jebbar, M., Pierik, A.J. & Bremer, E. (2008) Appl. Environm. Microbiol. 74, 7286-7296. Synthesis and uptake of the compatible solutes ectoine and 5-hydroxyectoine by Streptomyces coelicolor A3(2) in response to salt and heat stress.

 

52. Pierik, A.J., Graf, T., Pemberton, L., Golding, B.T. & Rétey, J. (2008) ChemBioChem 9, 2268-2275. But-3-ene-1,2-diol: a mechanism-based active site inhibitor for coenzyme B12-dependent glycerol dehydratase.

 

53. Reitz, S., Alhapel, A., Essen*, L.-O. & Pierik*, A.J. (2008) J. Mol. Biol. 382, 802-811. Structural and kinetic properties of a β-hydroxyacid dehydrogenase involved in nicotinate fermentation.

 

54. Boyd, J.M., Pierik, A.J., Netz, D.J.A., Lill, R. & Downs, D.M. (2008) Biochemistry 47, 8195–8202. Bacterial ApbC can bind and effectively transfer iron−sulfur clusters.

 

55. Stehling, O., Netz, D.J.A., Niggemeyer, B., Rösser, R., Eisenstein, R.S., Puccio, H., Pierik, A.J. & Lill, R. (2008) Mol. Cell. Biol. 28, 5517-5528. Human Nbp35 is essential for both cytosolic iron-sulfur protein assembly and iron homeostasis.

 

56. Bych, K., Kerscher, S., Netz, D.J.A., Pierik, A.J., Zwicker, K., Huynen, M.A., Lill, R., Brandt, U. & Balk, J. (2008) EMBO J. 27, 1736–1746. The iron-sulphur protein Ind1 is required for effective complex I assembly.

 

57. Kim, J., Darley, D.J., Buckel, W. & Pierik*, A.J. (2008) Nature 452, 239-242. An allylic ketyl radical intermediate in clostridial amino-acid fermentation.

 

58. Srinivasan, V., Netz, D.J.A., Webert, H., Mascarenhas, J., Pierik, A.J., Michel, H. & Lill, R. (2007) Structure 15, 1246-1257. Structure of the yeast WD40 domain protein Cia1, a component acting late in iron-sulfur protein biogenesis.

 

59. Bursy, J., Pierik, A.J., Pica, N. & Bremer, E. (2007) J. Biol. Chem. 282, 31147-31155. Osmotically induced synthesis of the compatible solute hydroxyectoine is mediated by an evolutionarily conserved ectoine hydroxylase.

 

60. Netz, D.J., Pierik, A.J., Stümpfig, M., Mühlenhoff, U. & Lill, R. (2007) Nat. Chem. Biol. 3, 278-286. The Cfd1/Nbp35 complex acts as scaffold for iron-sulfur protein assembly in the yeast cytosol.

 

61. Zameitat, E., Pierik, A.J., Zocher, K. & Löffler, M. (2007) FEMS Yeast Res. 7, 897-904. Dihydroorotate dehydrogenase from Saccharomyces cerevisiae: spectroscopic investigations with the recombinant enzyme throw light on catalytic properties and metabolism of fumarate analogues.

 

62. Pieck, J.C., Hennecke, U., Pierik, A.J., Friedel, M.G. & Carell, T. (2006) J. Biol. Chem. 281, 36317-36326. Characterization of a new thermophilic spore photoproduct lyase from Geobacillus stearothermophilus (splG) with defined lesion containing DNA substrates.

 

63. Buckel, W., Pierik, A.J., Plett, S., Alhapel, A., Suarez, D., Tu, S.-M. & Golding, B.T. (2006) Eur. J. Inorg. Chem. 3622-3626. Mechanism-based inactivation of coenzyme B12-dependent 2-methyleneglutarate mutase by (Z)-glutaconate and buta-1,3-diene-2,3-dicarboxylate.

 

64. Alhapel, A., Darley, D.J., Wagener, N., Eckel, E., Elsner, N. & Pierik*, A.J. (2006) Proc. Nat. Acad. Sci. USA 103, 12341-12346. Molecular and functional analysis of nicotinate catabolism in Eubacterium barkeri.

 

65. Yu, L., Blaser, M., Andrei, P.I., Pierik, A.J., Selmer, T. (2006) Biochemistry 45, 9584-9592. 4-Hydroxyphenylacetate decarboxylases: properties of a novel subclass of glycyl radical enzyme systems.

 

66. Layer, G., Pierik, A.J., Trost, M., Rigby, S.E., Leech, H.K., Grage, K., Breckau, D., Astner, I., Jänsch, L., Heathcote, P., Warren, M.J., Heinz, D.W. & Jahn, D. (2006) J. Biol. Chem. 281, 15727-15734. The substrate radical of Escherichia coli oxygen-independent coproporphyrinogen III oxidase HemN. (Equal contribution)

 

67. Balk, J., Aguilar Netz, D.J., Tepper, K., Pierik, A.J. & Lill, R. (2005) Mol. Cell. Biol. 25, 10833-10841. The essential WD40 protein Cia1 is involved in a late step of cytosolic and nuclear iron-sulfur protein assembly.

 

68. Seedorf, H., Kahnt, J., Pierik, A.J. & Thauer, R.K. (2005) FEBS J. 272, 5337-5342. Si-face stereospecificity at C5 of coenzyme F420 for F420H2 oxidase from methanogenic Archaea as determined by mass spectrometry.

 

69. Pierik, A.J., Ciceri, D., Lopez, R.F., Kroll, F., Bröker, G., Beatrix, B., Buckel, W. & Golding, B.T. (2005) Biochemistry 44, 10541-10551. Searching for intermediates in the carbon skeleton rearrangement of 2-methyleneglutarate to (R)-3-methylitaconate catalyzed by coenzyme B12-dependent 2-methyleneglutarate mutase from Eubacterium barkeri.

 

70. Hausmann, A., Aguilar Netz, D.J., Balk, J., Pierik, A.J., Mühlenhoff, U. & Lill. R. (2005) Proc. Natl. Acad. Sci. USA 102, 3266-3271. The eukaryotic P loop NTPase Nbp35: an essential component of the cytosolic and nuclear iron-sulfur protein assembly machinery.

 

71. Balk, J, Pierik, A.J., Aguilar Netz, D.J., Mühlenhoff, U. & Lill, R. (2005) Biochem. Soc. Trans. 33, 86-89. Nar1p, a conserved eukaryotic protein with similarity to Fe-only hydrogenases, functions in cytosolic iron-sulphur protein biogenesis.

 

72. Näser, U., Pierik, A.J., Scott, R., Çinkaya, I., Buckel, W. & Golding, B.T. (2005) Bioorg. Chem. 33, 53-66. Synthesis of 13C-labelled γ-hydroxybutyrates for EPR studies with 4-hydroxybutyryl-CoA dehydratase.

 

73. Andrei, P., Pierik, A.J., Zauner, S., Andrei-Selmer, L.C. & Selmer, T. (2004) Eur. J. Biochem. 271, 2225-2230. Subunit composition of the glycyl radical enzyme p-hydroxyphenylacetate decarboxylase. A small subunit, HpdC, is essential for catalytic activity.

 

74. Balk, J., Pierik, A.J., Aguilar Netz, D.J., Mühlenhoff, U. & Lill, R. (2004) EMBO J. 23, 2105-2115. The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron-sulfur proteins.

 

75. Mander, G.J., Pierik, A.J., Huber, H. & Hedderich, R. (2004) Eur. J. Biochem. 271, 1106-1116. Two distinct heterodisulfide reductase-like enzymes in the sulfate-reducing archaeon Archaeoglobus profundus.

 

76. Verfürth, K., Pierik, A.J., Leutwein, C., Zorn, S. & Heider, J. (2004) Arch. Microbiol. 181, 155-162. Substrate specificities and electron paramagnetic resonance properties of benzylsuccinate synthases in anaerobic toluene and m-xylene metabolism.

 

77. Weigl, U., Heimberger, M., Pierik, A.J. & Rétey, J. (2003) Chemistry Eur. J. 9, 652-660. Synthesis of enantiomerically-pure [13C]aristeromycyl-cobalamin and its reactivity in dioldehydratase, glyceroldehydratase, ethanolamine ammonia-lyase and methylmalonyl-CoA mutase reactions.

 

78. Hetzel, M., Brock, M., Selmer, T., Pierik, A.J., Golding, B.T. & Buckel, W. (2003) Eur. J. Biochem. 270, 902-910. Acryloyl-CoA reductase from Clostridium propionicum. An enzyme complex of propionyl-CoA dehydrogenase and electron-transferring flavoprotein.

 

79. Thamer, W., Cirpus, I., Hans, M., Pierik, A.J., Selmer, T., Bill, E., Linder, D. & Buckel, W. (2003) Arch. Microbiol. 179, 197-204. A two [4Fe-4S]-cluster-containing ferredoxin as an alternative electron donor for 2-hydroxyglutaryl-CoA dehydratase from Acidaminococcus fermentans.

 

80. Pierik, A.J., Ciceri, D., Bröker, G., Edwards, C.H., McFarlane, W., Winter, J., Buckel, W. & Golding, B.T. (2002) J. Am. Chem. Soc. 124, 14039-14048. Rotation of the exo-methylene group of (R)-3-methylitaconate catalyzed by coenzyme B12-dependent 2 methyleneglutarate mutase from Eubacterium barkeri.

 

81. Aguilar Netz, D.J., Pohl, R., Beck-Sickinger, A.G., Selmer, T., Pierik, A.J., Bastos, M.C.F. & Sahl, H.-G. (2002) J. Mol. Biol. 319, 745-756. Biochemical characterisation and genetic analysis of aureocin A53, a new, atypical bacteriocin from Staphylococcus aureus.

 

82. Dickert, S., Pierik, A.J. & Buckel, W. (2002) Mol. Microbiol. 44, 49-60. Molecular characterization of phenyllactate dehydratase and its initiator from Clostridium sporogenes.

 

83. Hans, M., Bill, E., Cirpus, I., Pierik, A.J., Hetzel, M., Alber, D. & Buckel, W. (2002) Biochemistry 41, 5873-5882. Adenosine triphosphate-induced electron transfer in 2 hydroxyglutaryl-CoA dehydratase from Acidaminococcus fermentans.

 

84. Rabus, R., Wilkes, H., Behrends, A., Armstroff, A., Fischer, T., Pierik, A.J. & Widdel, F. (2001) J. Bacteriol. 183, 1707-1715. Anaerobic initial reaction of n-alkanes in a denitrifying bacterium: evidence for (1-methylpentyl)succinate as initial product and for involvement of an organic radical in n-hexane metabolism.

 

85. Dickert, S., Pierik, A.J., Linder, D. & Buckel, W. (2000) Eur. J. Biochem. 267, 3874-3884. The involvement of coenzyme A esters in the dehydration of (R)-phenyllactate to (E)-cinnamate by Clostridium sporogenes.

 

86. Ciceri, D., Pierik, A.J., Hartrampf, G., Bröker, G., Speranza, G., Buckel, W., Cornforth, J. & Golding, B.T. (2000) Helv. Chim. Acta 83, 2550-2561. Stereochemistry of the methyl group in (R)-3-methylitaconate derived by rearrangement of 2 methylideneglutarate catalysed by a coenzyme B12-dependent mutase.

 

87. Bingemann, R., Pierik, A.J. & Klein, A. (2000) Arch. Microbiol. 174, 375-378. Influence of the fusion of two subunits of the F420-non-reducing hydrogenase of Methanococcus voltae on its biochemical properties.

 

88. Pierik, A.J., Roseboom, W., Happe, R.P., Bagley, K.A. & Albracht, S.P.J. (1999) J. Biol. Chem. 274, 3331-3337. Carbon monoxide and cyanide as intrinsic ligands to iron in the active site of [NiFe]-hydrogenases. NiFe(CN)2CO, biology’s way to activate H2.

 

89. Ding, X.D., Weichsel, A., Andersen, J.F., Shokhireva, T.K., Balfour, C., Pierik, A.J., Averill, B.A., Montfort, W.R. & Walker, F.A. (1999) J. Am. Chem. Soc. 121, 128-138. Nitric oxide binding to the ferri- and ferroheme states of nitrophorin 1, a reversible NO-binding heme protein from the saliva of the blood-sucking insect, Rhodnius prolixus.

 

90. Pierik, A.J., Schmelz, M., Lenz, O., Friedrich, B. & Albracht, S.P.J. (1998) FEBS Lett. 438, 231-235. Characterization of the active site of a hydrogen sensor from Alcaligenes eutrophus.

 

91. Pierik, A.J., Hulstein, M., Hagen, W.R. & Albracht, S.P.J. (1998) Eur. J. Biochem. 258, 572-578. A low-spin iron with CN and CO as intrinsic ligands forms the core of the active site in [Fe]-hydrogenases.

 

92. Thor, J.J. van, Pierik, A.J., Nugteren-Roodzant, I., Xie, A. & Hellingwerf, K.J. (1998) Biochemistry 37, 16915-16921. Characterization of the photoconversion of green fluorescent protein with FTIR spectroscopy.

 

93. Cordfunke, R., Kort, R., Pierik, A.J., Gobets, B., Koomen, G.-J., Verhoeven, J.W. & Hellingwerf, K.J. (1998) Proc. Natl. Acad. Sci. USA 95, 7396-7401. Trans/cis (Z/E) photoisomerization of the chromophore of photoactive yellow protein is not a prerequisite for the initiation of the photocycle of this photoreceptor protein.

 

94. Kooter, I.M., Pierik, A.J., Merkx, M., Averill, B.A., Moguilevsky, N., Bollen, A. & Wever, R. (1997) J. Am. Chem. Soc. 119, 11542-11543. Difference Fourier transform infrared evidence for ester bonds linking the heme group in myeloperoxidase, lactoperoxidase and eosinophil peroxidase.

 

95. Happe, R.P., Roseboom, W., Pierik, A.J., Albracht, S.P.J. & Bagley, K.A. (1997) Nature 385, 126. Biological activation of hydrogen.

 

96. Verhagen, M.F.J.M., Pierik, A.J., Wolbert, R.B.G., Malleé, L.F., Voorhorst, W.G.B. & Hagen, W.R. (1994) Eur. J. Biochem. 225, 311-319. Axial coordination and reduction potentials of the sixteen hemes in high-molecular-mass cytochrome c from Desulfovibrio vulgaris (Hildenborough).

 

97. Arendsen, A.F., Verhagen, M.F.J.M., Wolbert, R.B.G., Pierik, A.J., Stams, A.J.M., Jetten, M.S.M. & Hagen, W.R. (1993) Biochemistry 32, 10323-10330. The dissimilatory sulfite reductase from Desulfosarcina variabilis is a Desulforubidin containing uncoupled metalated sirohemes and S=9/2 iron-sulfur clusters.

 

98. Holliger, C., Pierik, A.J., Reijerse, E.J. & Hagen, W.R. (1993) J. Am. Chem. Soc. 115, 5651-5656. A spectroelectrochemical study of factor F430 Nickel(II/I) from methanogenic bacteria in aqueous solution.

 

99. Pierik, A.J., Wolbert, R.B.G., Portier, G.L., Verhagen, M.F.J.M. & Hagen, W.R. (1993) Eur. J. Biochem. 212, 237-245. Nigerythrin and rubrerythrin from Desulfovibrio vulgaris each contain two mononuclear iron centers and two dinuclear iron clusters.

 

100. Pierik, A.J., Wassink, H., Haaker, H. & Hagen, W.R. (1993) Eur. J. Biochem. 212, 51-61. Redox properties and EPR spectroscopy of the P clusters of the Azotobacter vinelandii MoFe protein.

 

101. Stokkermans, J.P.W.G., Houba, P.H.J., Pierik, A.J., Hagen, W.R., Van Dongen, W.M.A.M. & Veeger, C. (1992) Eur. J. Biochem. 210, 983-988. Overproduction of prismane protein in Desulfovibrio vulgaris (Hildenborough): evidence for a second S=1/2-spin system in the one-electron reduced state.

 

102. Pierik, A.J., Hagen, W.R., Redeker, J.S., Wolbert, R.B.G., Boersma, M., Verhagen, M.F.J.M., Grande, H.J., Veeger, C., Mutsaers, P.H.A., Sands, R.H. & Dunham, W.R. (1992) Eur. J. Biochem. 209, 63-72. Redox properties of the iron-sulfur clusters in activated Fe-hydrogenase from Desulfovibrio vulgaris (Hildenborough).

 

103. Link, T.A., Hagen, W.R., Pierik, A.J., Assmann, C. & Von Jagow, G. (1992) Eur. J. Biochem. 208, 685-691. Determination of the redox properties of the Rieske [2Fe-2S] cluster of bovine heart bc1 complex by direct electrochemistry of a water-soluble fragment.

 

104. Stokkermans, J.P.W.G., Pierik, A.J., Wolbert, R.B.G., Hagen, W.R., Van Dongen, W.M.A.M. & Veeger, C. (1992) Eur. J. Biochem. 208, 435-442. The primary structure of a protein containing a putative [6Fe-6S] prismane cluster from Desulfovibrio vulgaris (Hildenborough).

 

105. Pierik, A.J., Hagen, W.R., Dunham, W.R. & Sands, R.H. (1992) Eur. J. Biochem. 206, 705-719. Multi-frequency EPR and high-resolution Mössbauer spectroscopy of a putative [6Fe-6S] prismane-cluster-containing protein from Desulfovibrio vulgaris (Hildenborough). Characterization of a supercluster and superspin model protein.

 

106. Pierik, A.J., Wolbert, R.B.G., Mutsaers, P.H.A., Hagen, W.R. & Veeger, C. (1992) Eur. J. Biochem. 206, 697-704. Purification and biochemical characterization of a putative [6Fe-6S] prismane-cluster-containing protein from Desulfovibrio vulgaris (Hildenborough).

 

107. Pierik, A.J., Duyvis, M.G., Van Helvoort, J.M.L.M., Wolbert, R.B.G. & Hagen, W.R. (1992) Eur. J. Biochem. 205, 111-115. The third subunit of desulfoviridin-type dissimilatory sulfite reductases.

 

108. Jetten, M.S.M., Pierik, A.J. & Hagen, W.R. (1991) Eur. J. Biochem. 202, 1291-1297. EPR characterization of a high-spin system in carbon monoxide dehydrogenase from Methanothrix soehngenii.

 

109. Pierik, A.J. & Hagen, W.R. (1991) Eur. J. Biochem. 195, 505-516. S=9/2 EPR signals are evidence against coupling between the siroheme and the Fe/S cluster prosthetic groups in Desulfovibrio vulgaris (Hildenborough) dissimilatory sulfite reductase.

 

110. Jetten, M.S.M., Hagen, W.R., Pierik, A.J., Stams, A.J.M. & Zehnder, A.J.B. (1991) Eur. J. Biochem. 195, 385-391. Paramagnetic centers and acetyl-coenzyme A / CO exchange activity of carbon monoxide dehydrogenase from Methanothrix soehngenii.

 

111. Hagen, W.R., Pierik, A.J. & Veeger, C. (1989) J. Chem. Soc., Faraday Trans. I 85, 4083-4090. Novel electron paramagnetic resonance signals from an Fe/S protein containing six iron atoms.

 

112. Pierik, A.J., Nijssen, J.G., Aarsman, A.J. & Van den Bosch, H. (1988) Biochim. Biophys. Acta 962, 345-353. Calcium-independent phospholipase A2 in rat tissue cytosols.

 

 

Review articles

 

113. Freibert, S.-A., Weiler, B.D., Bill, E., Pierik, A.J., Mühlenhoff, U. & Lill, R. (2018) Methods Enzymol. 599, 197-226. Biochemical reconstitution and spectroscopic analysis of iron-sulfur proteins.

 

114. Merkx, M. & Pierik, A.J. (2017) Curr. Opin. Chem Biol. 37, vi-vii. Nine short stories of metals in biology.

 

115. Lill, R., Dutkiewicz, R., Freibert, S. A., Heidenreich, T., Mascarenhas, J., Netz, D.J., Paul, V.D., Pierik, A.J., Richter, N., Stümpfig, M., Srinivasan, V., Stehling, O. & Mühlenhoff, U. (2015) Eur. J. Cell Biol. 94, 280-291. The role of mitochondria and the CIA machinery in the maturation of cytosolic and nuclear iron-sulfur proteins.

 

116. Netz, D.J.A., Mascarenhas, J., Stehling, O., Pierik, A.J. & Lill, R. (2014) Trends Cell Biol. 24, 303-312. Maturation of cytosolic and nuclear iron–sulfur proteins.

 

117. Lill, R., Hoffmann, B., Molik, S., Pierik, A.J., Rietzschel, N., Stehling, O., Uzarska, M.A., Webert, H., Wilbrecht, C. & Mühlenhoff, U. (2012) Biochim. Biophys. Acta 1823, 1491-1508. The role of mitochondria in cellular iron-sulfur protein biogenesis and iron metabolism.

 

118. Lill, R., Dutkiewicz, R., Elsässer, H.-P., Hausmann, A., Netz, D.J.A., Pierik, A.J., Stehling, O., Urzica, E. & Mühlenhoff, U. (2006) Biochim. Biophys. Acta 1763, 652-667. Mechanisms of iron-sulfur protein maturation in mitochondria, cytosol and nucleus of eukaryotes.

 

119. Boiangiu, C.D., Jayamani, E., Brügel, D., Herrmann, G., Kim, J., Forzi, L., Hedderich, R., Vgenopoulou, I., Pierik, A.J., Steuber, J. & Buckel, W. (2005) J. Mol. Microbiol. Biotechnol. 10, 105-119. Sodium ion pumps and hydrogen production in glutamate fermenting anaerobic bacteria.

 

120. Selmer, T., Pierik, A.J. & Heider, J. (2005) Biol. Chem. 386, 981-988. New glycyl radical enzymes catalysing key metabolic steps in anaerobic bacteria.

 

Book chapters

 

121. Buckel, W., Bröker, G., Bothe, H., Pierik, A.J. & Golding, B.T. (1999) In: Chemistry and Biochemistry of B12 (Ed.: Banerjee, R.), Wiley, New York, pp. 757-781. Glutamate mutase and 2-methyleneglutarate mutase.

 

122. Dobbek, H. & Pierik, A.J. (2011) In: Handbook of Metalloproteins (Ed.: Messerschmidt, A.), Wiley, Chichester. Mo, Se-containing nicotinate dehydrogenase.

 

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