Use of magnetic circular dichroism to study dinuclear metallohydrolases and the corresponding biomimetics

European Biophysics Journal

Volumn 44, Issue 6, 2015, Pages 393-415

  Larrabee, James A ^a   Schenk, Gerhard ^b   Mitić, Nataša ^c   Riley, Mark J ^b  

^a MIDDLEBURY COLLEGE   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Biomimetics; Co(II); Dinuclear metallohydrolases; Magnetic circular dichroism; Metalloenzymes; Reaction mechanism

Indexed keywords

AEROMONAS PROTEOLYTICA AMINOPEPTIDASE; ALKALINE PHOSPHATASE; AMINOPEPTIDASE; BACTERIAL ENZYME; CARBOXYLIC ACID; COBALT; DINUCLEAR METALLOHYDROLASE; GLYCEROPHOSPHODIESTERASE; HYDROLASE; HYDROXIDE; METHIONYL AMINOPEPTIDASE; PHOSPHODIESTERASE; PHOSPHOTRIESTERASE; UNCLASSIFIED DRUG; WATER; BIOMIMETIC MATERIAL; GLYCEROPHOSPHODIESTER PHOSPHODIESTERASE;

ABSORPTION SPECTROSCOPY; AGROBACTERIUM TUMEFACIENS; BINDING AFFINITY; BINDING SITE; BIOMIMETICS; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; DIPOLE; ENTEROBACTER AEROGENES; ESCHERICHIA COLI; HYDROGEN BOND; ISOTHERM; LUMINESCENCE; MAGNETIC CIRCULAR DICHROISM; MAGNETIC CIRCULAR DICHROISM SPECTROSCOPY; MAGNETIC CIRCULAR POLARISED LUMINESCENCE; MAGNETIC FIELD; MAGNETIC OPTICAL ROTATION; NONHUMAN; OPTICAL ROTATION; PRIORITY JOURNAL; REVIEW; SPECTROSCOPY; CHEMISTRY;

BIOMIMETIC MATERIALS; CIRCULAR DICHROISM; COBALT; HYDROLASES; PHOSPHORIC DIESTER HYDROLASES;

EID: 84938963541     PISSN: 01757571     EISSN: 14321017     Source Type: Journal    
DOI: 10.1007/s00249-015-1053-6     Document Type: Review

References (60)

1. Anderson RA, Vallee BL (1977) Selective cobalt oxidation as a means to differentiate metal-binding sites of cobalt alkaline phosphatase. Biochem 16:4388–4393
2. Anderson RA, Kennedy FS, Vallee BL (1976) The effect of Mg(II) on the spectral properties of Co(II) alkaline phosphatase. Biochem 15:3710–3716
3. Averill BA (2003) Dinuclear hydrolases. Comp Coord Chem II 8:641–676
4. Benning MM, Shim H, Raushel FM, Holden HM (2001) High resolution X-ray structures of different metal-substituted forms of phosphotriesterase from Pseudomonas diminuta. Biochem 40:2712–2722
5. 2O (L = N,N′,N″-trimethyl-1,4,7-triazacyclononane). J Chem Soc, Dalton Trans 1:271–278
6. Ciurli S, Benini S, Rypniewski WR, Wilson KS, Miletti S, Mangani S (1999) Structural properties of the nickel ions in urease: novel insights into the catalytic and inhibition mechanisms. Coord Chem Rev 190–192:331–355
7. Daumann LJ, Comba P, Larrabee JA, Schenk G, Stranger R, Cavigliasso G, Gahan LR (2013) Synthesis, magnetic properties, and phosphoesterase activity of dinuclear cobalt(II) complexes. Inorg Chem 52:2029–2043
8. Daumann LJ, Schenk G, Ollis DL, Gahan LR (2014) Spectroscopic and mechanistic studies of dinuclear metallohydrolases and their biomimetic complexes. Dalton Trans 43:910–928
9. Desmarais W, Bienvenue DL, Bzymek KP, Petsko GA, Ringe D, Holz RC (2006) The high-resolution structures of the neutral and the low pH crystals of aminopeptidase from Aeromonas proteolytica. J Biol Inorg Chem 11:398–408
10. D’souza VM, Bennett B, Copik AJ, Holz RC (2000) Divalent metal binding properties of the methionyl aminopeptidase from Escherichia coli. Biochem 39:3817–3826
11. Ely F, Hadler KS, Gahan LR, Guddat LW, Ollis DL, Schenk G (2010) Catalytic mechanism of the hydrolytic reaction catalyzed by an organophosphate-degrading enzyme from Agrobacterium radiobacter. Biochem J 432:565–573
12. Ely F, Hadler KS, Mitić N, Gahan LR, Ollis DL, Plugis NM, Russo MT, Larrabee JA, Schenk G (2011) Electronic and geometric structures of the organophosphate-degrading enzyme from Agrobacterium radiobacter (OpdA). J Biol Inorg Chem 16:777–787
13. Foo J-L, Jackson CJ, Carr PD, Kim H-K, Schenk G, Gahan LR, Ollis DL (2010) Mutation of outer-shell residues modulates metal ion affinity in a metalloenzyme. Biochem J 429:313–321
14. Hadler KS, Tanifum EA, Yip SH-C, Mitić N, Guddat LW, Jackson CJ, Gahan LR, Nguyen K, Carr PD, Ollis DL, Hengge AC, Larrabee JA, Schenk G (2008) Substrate-promoted formation of a catalytically competent binuclear center and regulation of reactivity in a glycerophosphodiesterase from Enterobacter aerogenes. J Am Chem Soc 130:14129–14138
15. Hadler KS, Mitić N, Ely F, Hanson GR, Gahan LR, Larrabee JA, Ollis DL, Schenk G (2009) Structural flexibility enhances the reactivity of the bioremediator glycerophosphodiesterase by fine-tuning its mechanism of hydrolysis. J Am Chem Soc 131:11900–11908
16. Hadler KS, Mitić N, Yip SH-C, Gahan LR, Ollis DL Schenk G, Larrabee JA (2010a) Electronic structure analysis of the dinuclear metal center in the bioremediator glycerophosphodiesterase (GpdQ) from Enterobacter aerogenes. Inorg Chem 49:2727–2734
17. Hadler KS, Gahan LR, Ollis DL Schenk G (2010b) The bioremediator glycerophosphodiesterase employs a non-processive mechanism for hydrolysis. J Inorg Biochem 104:211–213
18. Harding MJ, Briat B (1973) The electronic absorption and magnetic circular dichroism spectra of cobalt (II) bromate hexahydrate. Mol Phys 25:745–776
19. Holmquist B, Kaden TA, Vallee BL (1975) Magnetic circular dichroic spectra of cobalt(II) substituted metalloenzymes. Biochem 14:1454–1461
20. Holz RC (2002) The aminopeptidase from Aeromonas proteolytica: structure and mechanism of co-catalytic metal centers involved in peptide hydrolysis. Coord Chem Rev 232:5–26
21. Jackson CJ, Kim H-K, Carr PD, Liu J-W, Ollis DL (2005) The structure of an enzyme-product complex reveals the critical role of a terminal hydroxide nucleophile in the bacterial phosphotriesterase mechanism. Biochim Biphys Acta 1752:56–64
22. Jackson CJ, Carr PD, Liu J-W, Watt SJ, Beck JL, Ollis DL (2007) The structure and function of a novel glycerophosphodiesterase from Enterobacter aerogenes. J Mol Biol 367:1047–1062
23. Jackson CJ, Foo J-L, Kim H-K, Carr PD, Liu J-W, Salem G, Ollis DL (2008) In crystallo capture of a Michaelis complex and product-binding modes of a bacterial phosphotriesterase. J Mol Biol 375:1189–1196
24. Johansson FB, Bond AD, Nielsen UG, Moubaraki B, Murray KS, Berry KJ, Larrabee JA, McKenzie CJ (2008) Dicobalt II–II, II–III, and III–III complexes as spectroscopic models for dicobalt enzyme active sites. Inorg Chem 47:5079–5092
25. Johnson MK (2000) Magnetic circular dichroism spectroscopy. In: Que L (ed) Physical methods in bioinorganic chemistry. University Science Books, Sausalito, pp 233–285
26. Kaden TA, Holmquist B, Vallee BL (1974) Magnetic circular dichroism of Cobalt(II) complexes. Inorg Chem 13:2585–2590
27. Kimura E (2000) Dimetallic hydrolases and their models. Curr Opin Chem Biol 4:207–213
28. Kirk ML, Peariso K (2003) Recent applications of MCD spectroscopy to metalloenzymes. Curr Opin Chem Biol 7:220–227
29. Krzystek J, Zvyagin SA, Ozarowski A, Fiedler AT, Brunold TC, Telser J (2004) Definitive spectroscopic determination of zero-field splitting in high-spin cobalt(II). J Am Chem Soc 126:2148–2155
30. Larrabee JA, Alessi CM, Asiedu ET, Cook JO, Hoerning KR, Klingler LJ, Okin GS, Santee SG, Volkert TL (1997) Magnetic circular dichroism spectroscopy as a probe of geometric and electronic structure of cobalt(II)-substituted proteins: ground-state zero-field splitting as a coordination number indicator. J Am Chem Soc 119:4182–4196
31. Larrabee JA, Leung C-H, Moore RL, Thamrong-nawasawat T, Wessler BSH (2004) Magnetic circular diochroism and Co(II) binding studies of Escherichia coli methionyl aminopeptidase. J Am Chem Soc 126:12316–12324
32. Larrabee JA, Chyun S-A, Volwiler AS (2008) Magnetic circular dichroism study of a dicobalt(II) methionine aminopeptidase/fumagillin complex and dicobalt II-II and II-III model complexes. Inorg Chem 47:10499–10508
33. Larrabee JA, Johnson WR, Volwiler AS (2009) Magnetic circular dichroism study of a dicobalt(II) complex with mixed 5- and 6-coordination: a spectroscopic model for dicobalt(II) hydrolases. Inorg Chem 48:8822–8829
34. Liu S, Widom J, Kemp CW, Crews CM, Clardy J (1998) Structure of human methionine aminopeptidase-2 complexed with fumagillin. Science 282:1324–1327
35. Lowther WT, Matthews BW (2002) Metalloaminopeptidases: common functional themes in disparate structural surroundings. Chem Rev 102:4581–4607
36. Mason WR (2007) A practical guide to magnetic circular dichroism spectroscopy. Wiley, Hoboken
37. McCaffery AJ, Stephens PJ, Schatz PN (1967) The magnetic optical activity of d-d transitions. Octahedral chromium(III), cobalt(III), cobalt(II), nickel(II), and manganese(II) complexes. Inorg Chem 6:1614–1625
38. Mitić N, Smith SJ, Neves A, Guddat LW, Gahan LR, Schenk G (2006) The catalytic mechanisms of binuclear metallohydrolases. Chem Rev 106:3338–3363
39. Mitić N, Miraula M, Selleck C, Hadler KS, Uribe E, Pedroso MM, Schenk G (2014) Catalytic mechanisms of metallohydrolases containing two metal ions. In: Christov CZ (ed) Advances in protein chemistry and structural biology: metal-containing enzymes. Elsevier, Oxford, pp 49–81
40. Munih P, Moulin A, Stamper CC, Bennett B, Ringe D, Petsko GA, Holz RC (2007) X-ray crystallographic characterization of the Co(II)-substituted tris-bound form of the aminopeptidase from Aeromonas proteolytica. J Inorg Biochem 101:1099–1107
41. Neese F, Solomon EI (1999) MCD C-term signs, saturation behavior, and determination of band polarizations in randomly oriented systems with spin ≥1/2. Applications to S = 1/2 and S = 5/2. Inorg Chem 38:1847–1865
42. Ostrovsky SM, Falk K, Pelikan J, Brown DA, Tomkowicz Z, Haase W (2006) Orbital angular momentum contribution to the magneto-optical behavior of a binuclear cobalt(II) complex. Inorg Chem 45:688–694
43. Ostrovsky S, Tomkowicz Z, Haase W (2009) High-spin Co(II) in monomeric and exchanged coupled oligomeric structures: magnetic and magnetic circular dichroism investigations. Coord Chem Rev 253:2363–2375
44. Pedroso MM, Ely F, Mitić N, Carpenter MC, Gahan LR, Wilcox DE, Larrabee JL, Ollis DL, Schenk G (2014) Comparative investigation of the reaction mechanisms of organophosphate-degrading phosphotriesterases from Agrobacterium radobacter (OpdA) and Pseudomonas diminuta (OPH). J Biol Inorg Chem 198:1263–1275
45. Piligkos S, Slep LD, Weyhermuller T, Chaudhuri P, Bill E, Neese F (2009) Magnetic circular dichroism spectroscopy of weakly exchanged coupled transition metal dimers: a model study. Coord Chem Rev 253:2352–2362
46. Prescott JM, Wagner FW, Holmquist B, Vallee BL (1985) Spectral and kinetic studies of metal-substituted Aeromonas aminopeptidase: nonidentical, interacting metal-binding sites. Biochem 24:5350–5356
47. 2−. J Chem Phys 45:722–734
48. Schenk G, Mitić N, Gahan LR, Ollis DL, McGeary RP, Guddat LW (2012) Binuclear metallohydrolases: complex mechanistic strategies for a simple chemical reaction. Acc Chem Res 45:1593–1603
49. Schenk G, Mitić N, Hanson GR, Comba P (2013) Purple Aacid phosphatase: a journey into the function and mechanism of a colorful enzyme. Coord Chem Rev 257:473–482
50. Schultz BE, Ye BH, Li XY, Chan SI (1997) Electronic paramagnetic resonance and magnetic properties of model complexes for binuclear active sites in hydrolase enzymes. Inorg Chem 36:2617–2622
51. Solomon EI, Pavel EG, Loeb KE, Campochiaro C (1995) Magnetic circular dichroism spectroscopy as a probe of the geometric and electronic structure of non-heme ferrous enzymes. Coord Chem Rev 144:369–460
52. Solomon EI, Brunold TC, Davis MI, Kemsley JN, Sang-Kyu L, Lehnert N, Neese F, Skulan AJ, Yi-Shan Y, Zhou J (2000) Geometric and electronic structure/function correlations in non-heme iron enzymes. Chem Rev 100:235–349
53. Solomon EI, Neidig ML, Schenk G (2003) Magnetic circular dichroism of paramagnetic species. Comp Coord Chem II 2:339–349
54. Stec B, Holtz KM, Kantrowitz EV (2000) A revised mechanism for the alkaline phosphatase reaction involving three metal ions. J Mol Biol 299:1303–1311
55. Stephens PJ (1976) Magnetic circular dichroism. Adv Chem Phys 25:197–264
56. Taylor JS, Lau CY, Applebury ML, Coleman JE (1973) Escherichia coli Co(II) alkaline phosphatase. J Biol Chem 248:6216–6220
57. Wang WL, Chai SC, Huang M, He HZ, Hurley TD, Ye QZ (2008) Discovery of inhibitors of Escherichia coli methionine aminopeptidase with the Fe(II)-form selectivity and antibacterial activity. J Med Chem 51:6110–6120
58. Weston J (2005) Mode of action of bi- and trinuclear zinc hydrolases and their synthetic analogs. Chem Rev 105:2151–2174
59. Wilcox DE (1996) Binuclear metallohydrolases. Chem Rev 96:2435–2458
60. II complexes as chemical hydrolases: biomimetic models for purple acid phosphatases (PAPs). Inorg Chem 48:7905–7921