Specific metal ion binding sites in unstructured regions of proteins

Coordination Chemistry Reviews

Volumn 257, Issue 19-20, 2013, Pages 2625-2638

  Kozlowski, Henryk ^a   Potocki, Slawomir ^a   Remelli, Maurizio ^b   Rowinska Zyrek, Magdalena ^a   Valensin, Daniela ^c  

^a UNIVERSITY OF WROC AW   (Poland)

^b UNIVERSITY OF FERRARA   (Italy)

^c UNIVERSITY OF SIENA   (Italy)

Author keywords

synuclein; Cys Cys binding sites; Cysteines; Extra stability effects; Histidines; Met containing regions; Metal ion binding; Polyhistidine sequences; Prion protein; Unstructured binding sites; ZIP and Znt transporters

Indexed keywords

EID: 84882880138     PISSN: 00108545     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2013.01.024     Document Type: Review

References (131)

1. Bertoncini C.W., Jung Y.S., Fernandez C.O., Hoyer W., Griesinger C., Jovin T.M., Zweckstetter M. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:1430.
2. Kozlowski H., Luczkowski M., Remelli M., Valensin D. Coord. Chem. Rev. 2012, 256:2129-2141.
3. Faller P., Hureau C. Dalton Trans. 2009, 1080-1094.
4. Arena G., Pappalardo G., Sovago I., Rizzarelli E. Coord. Chem. Rev. 2012, 256:3-12.
5. Ginotra Y.P., Ramteke S.N., Srikanth R., Kulkarni P.P. Inorg. Chem. 2012, 51:7960-7962.
6. Hureau C. Coord. Chem. Rev. 2012, 256:2164-2174.
7. Migliorini C., Porciatti E., Luczkowski M., Valensin D. Coord. Chem. Rev. 2012, 256:352-368.
8. Sarell C.J., Syme C.D., Rigby S.E.J., Viles J.H. Biochimie 2009, 48:4388-4402.
9. Tougu V., Tiiman A., Palumaa P. Metallomics 2011, 3:250-261.
10. Shearer J., Callan P.E., Tran T., Szalai V.A. Chem. Commun. 2010, 46:9137-9139.
11. Jozsa E., Osz K., Kallay C., de Bona P., Damante C.A., Pappalardo G., Rizzarelli E., Sovago I. Dalton Trans. 2010, 39:7046-7053.
12. Damante C.A., Osz K., Nagy Z., Pappalardo G., Grasso G., Impellizzeri G., Rizzarelli E., Sovago I. Inorg. Chem. 2009, 48:10405-10415.
13. Bousejra-ElGarah F., Bijani C., Coppel Y., Faller P., Hureau C. Inorg. Chem. 2011, 50:9024-9030.
14. Viles J.H. Coord. Chem. Rev. 2012, 256:2271-2284.
15. Valensin D., Migliorini C., Valensin G., Gaggelli E., La Penna G., Kozlowski H., Gabbiani C., Messori L. Inorg. Chem. 2011, 50:6865-6867.
16. Binolfi A., Quintanar L., Bertoncini C.W., Griesinger C., Fernández C.O. Coord. Chem. Rev. 2012, 256:2188.
17. Binolfi A., Valiente-Gabioud A.A., Duran R., Zweckstetter M., Griesinger C., Fernandez C.O. J. Am. Chem. Soc. 2011, 133:194-196.
18. Prusiner S.B. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:13363-13383.
19. Kozlowski H., Luczkowski M., Remelli M. Dalton Trans. 2010, 39:6371-6385.
20. Arena G., La Mendola D., Pappalardo G., Sóvágó I., Rizzarelli E. Coord. Chem. Rev. 2012, 256:2202-2218.
21. Remelli M., Valensin D., Toso L., Gralka E., Guerrini R., Marzola E., Kozlowski H. Metallomics 2012, 4:794-806.
22. Millhauser G.L. Acc. Chem. Res. 2004, 37:79-85.
23. Millhauser G.L. Annu. Rev. Phys. Chem. 2007, 58:299-320.
24. Brown D.R., Qin K., Herms J.W., Madlung A., Manson J., Strome R., Fraser P.E., Kruck T., vonBohlen A., SchulzSchaeffer W., Giese A., Westaway D., Kretzschmar H. Nature 1997, 390:684-687.
25. Gaggelli E., Bernardi F., Molteni E., Pogni R., Valensin D., Valensin G., Remelli M., Luczkowski M., Kozlowski H. J. Am. Chem. Soc. 2005, 127:996-1006.
26. Remelli M., Donatoni M., Guerrini R., Janicka A., Pretegiani P., Kozlowski H. Dalton Trans. 2005, 2876-2885.
27. Berti F., Gaggelli E., Guerrini R., Janicka A., Kozlowski H., Legowska A., Miecznikowska H., Migliorini C., Pogni R., Remelli M., Rolka K., Valensin D., Valensin G. Chem. Eur. J. 2007, 13:1991-2001.
28. Gralka E., Valensin D., Porciatti E., Gajda C., Gaggelli E., Valensin G., Kamysz W., Nadolny R., Guerrini R., Bacco D., Remelli M., Kozlowski H. Dalton Trans. 2008, 5207-5219.
29. Remelli M., Valensin D., Bacco D., Gralka E., Guerrini R., Migliorini C., Kozlowski H. New J. Chem. 2009, 33:2300-2310.
30. Turi I., Kallay C., Szikszai D., Pappalardo G., Di Natale G., De Bona P., Rizzarelli E., Sovago I. J. Inorg. Biochem. 2010, 104:885-891.
31. Joszai V., Turi I., Kallay C., Pappalardo G., Di Natale G., Rizzarelli E., Sovago I. J. Inorg. Biochem. 2012, 112:17-24.
32. Brown D.R. Metallomics 2011, 3:229-238.
33. Kambe T. Biosci. Biotechnol. Biochem. 2011, 75:1036-1043.
34. Nishida S., Mizuno T., Obata H. Plant Physiol. Biochem. 2008, 46:601-606.
35. Colangelo E.P., Guerinot M.L. Plant Biol. 2006, 9:322-330.
36. Eide D.J. Biochim. Biophys. Acta 2006, 1763:711-722.
37. Guerinot M.L. Biochim. Biophys. Acta 2000, 1465:190-198.
38. Taylor K.M., Nicholson R.I. Biochim. Biophys. Acta 2003, 1611:16-30.
39. Gitan R.S., Eide D.J. Biochem. J. 2000, 346:329-336.
40. Manning D.L., McClelland R.A., Knowlden J.M., Bryant S., Gee J.M.W., Green C.D., Robertson J.F., Blamey R.W., Sutherland R.L., Ormandy C.J., Nicholson R.I. Acta Oncol. 1995, 34:641-646.
41. Gaither L.A., Eide D.J. Biometals 2001, 14:251-270.
42. Schmitt-Ulms G., Ehsani S., Watts J.C., Westaway D., Wille H. PLoS ONE 2009, 4:7208.
43. Ingle R.A., Mugford S.T., Rees J.D., Campbell M.M., Smith J.A.C. Plant Cell 2005, 17:2089-2106.
44. Kerkeb L., Krämer U. Plant Physiol. 2003, 131:716-724.
45. Mizuno T., Usui K., Nishida S., Unno T., Obata H. Plant Physiol. Biochem. 2007, 45:371-378.
46. Milon B., Wu Q., Zou J., Costello L.C., Franklin R.B. Biochim. Biophys. Acta 2006, 1758:1696-1701.
47. Rogers E.E., Eid D.J. PNAS 2000, 97:12356-12360.
48. S. Potocki, D. Valensin, F. Camponeschi, H. Kozlowski, J. Inorg. Biochem., Submitted for publication.
49. Potocki S., Rowinska-Zyrek M., Valensin D., Krzywoszynska K., Witkowska D., Luczkowski M., Kozlowski H. Inorg. Chem. 2011, 50:6135-6145.
50. Taudte N., Grass G. Biometals 2010, 23:643-656.
51. Grossoehme N.E., Akilesh S., Guerinot M.L., Wilcox D.E. Inorg. Chem. 2006, 45:8500-8508.
52. Mao X., Kim B.E., Wang F., Eide D.J., Petris M.J. J. Biol. Chem. 2007, 282:6992-7000.
53. Hall J.L., Williams L.E. J. Exp. Bot. 2003, 54:2601-2613.
54. Williams L.E., Pittman J.K., Hall J.L. Biochim. Biophys. Acta 2000, 1465:104-126.
55. Li L., Kaplan J. J. Biol. Chem. 1997, 272:28485-28493.
56. Cherezov V., Hofer N., Szebenyi D.M.E., Kolaj O., Wall J.G., Gillilan R., Srinivasan V., Jaroniec C.P., Caffrey M. Structure 2008, 16:1378-1388.
57. Chao Y., Fu D. J. Biol. Chem. 2004, 279:12043-12050.
58. Guffanti A.A., Wei Y., Rood S.V., Krulwich T.A. Mol. Microbiol. 2002, 45:145-153.
59. Lu M., Chai J., Fu D. Nat. Struct. Mol. Biol. 2009, 16:1063-1067.
60. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. J. Comput. Chem. 2004, 25:1605-1612.
61. Wan1 Q., Ahmad M.F., Fairman J., Gorzelle B., de la Fuente M., Dealwis C., Maguire M.E. Structure 2011, 19:700-710.
62. Metallothioneins and Related Chelators. Metal Ions in Life Sciences 2009, 5. RSC Publishing, Cambridge.
63. Loebus J., Peroza E.A., Bluthgen N., Fox T., Meyer-Klaucke W., Zerbe O., Freisinger E. J. Biol. Inorg. Chem. 2011, 16:683.
64. Krezel A., Maret W. JACS 2007, 129:10911.
65. Palacios O., Atrian S., Capdevila M. J. Biol. Inorg. Chem. 2011, 16:991.
66. Koppers A.J., Reddy T., O'Bryan M.K. Asian J. Androl. 2010, 13:111.
67. Scott D., Marcus E., Weeks D., Sachs G. Gastroenterology 2002, 123:187.
68. Olson J., Maier J. Science 2002, 298:1788.
69. Mehta N., Olson J.W., Maier R.J. Bacteriol. J. 2003, 185:726.
70. Schauer K., Muller C., Carriere M., Labigne A., Cavazza C., De Reuse H. Bacteriol. J. 2010, 192:1231.
71. Suerbaum S., Thiberge J.M., Kansau I., Ferrero R.L., Labigne A. Mol. Microbiol. 1994, 14:959.
72. Zambelli B., Musiani F., Savini M., Tucker P., Ciurli S. Biochemistry 2007, 46:3171.
73. Rowinska-Zyrek M., Witkowska D., Valensin D., Kamysz W., Kozlowski H. Dalton Trans. 2010, 39:5814.
74. Rowinska-Zyrek M., Witkowska D., Bielinska S., Kamysz W., Kozlowski H. Dalton Trans. 2011, 40:5604.
75. Cun S., Li H., Ge R., Lin M.C.M., Sun H. Biol. Chem. J. 2008, 283:15142.
76. Witkowska D., Rowinska-Zyrek M., Valensin G., Kozlowski H. Coord. Chem. Rev. 2012, 256:133.
77. Krzywoszyńska K., Rowińska-Żyrek M., Witkowska D., Potocki S., Łuczkowski M., Kozlowski H. Dalton Trans. 2011, 40:10434.
78. M. Rowińska-Żyrek, S. Potocki, D. Witkowska, D. Valensin, H. Kozłowski, Dalton Trans., 2013,. doi:10.1039/C2DT32195E.
79. Block H., Maertens B. Guide to Protein Purification 2009, 439-473. Elsevier/Academic Press Inc., San Diego. second ed. R.R. Burgess, M.P. Deutscher (Eds.).
80. Hochuli E., Dobeli H., Schacheral A. J. Chromatogr. 1987, 411:177.
81. Porath J., Carlsson J., Olsson I., Belfrage G. Nature 1975, 258(5536):598.
82. Knecht S., Ricklin D., Eberle A.N., Ernst B. J. Mol. Recognit. 2009, 22(4):270.
83. Li Y., Zamble D.B. Chem. Rev. 2009, 109:4617.
84. Seshadri S., Benoit S.L., Maier R.J. Bacteriol. J. 2007, 189:4120.
85. Kaluarachchi H., Chan Chung K.C., Zamble D.B. Nat. Prod. Rep. 2010, 27:681.
86. Mulrooney S.B., Hausinger R.P. FEMS Microbiol. Rev. 2003, 27:239.
87. Rowinska-Zyrek M., Witkowska D., Potocki S., Remelli M., Kozłowski H. New J. Chem. 2013, 10.1039/C2NJ40558J.
88. Ge R., Zhang Y., Sun X., Watt R.M., He Q., Huang J.D., Wilcox D.E., Sun H. Am. Chem. Soc. J. 2006, 128:11330.
89. Maier R.J., Benoit S.L., Seshadri S. Biometals 2007, 20:655.
90. Mobeley H.L., Garner R.M., Chippendale G.R., Gilbert J.V., Kane A.V., Plaut A.G. Helicobacter 1999, 4:162.
91. Zeng Y.-B., Zhang D.-M., Li H., Sun H. J. Biol. Inorg. Chem. 2008, 14:1121-1131.
92. Panagiotou K., Panagopoulou M., Karavelas T., Dokorou V., Hagarman A., Soffer J., Schweitzer-Stenner R., Malandrinos G., Hadjiliadis N. Bioinorg. Chem. Appl. 2008, 257038.
93. Kozlowski H., Kowalik-Jankowska T., Jezowska-Bojczuk M. Coord. Chem. Rev. 2005, 249:2323.
94. Witkowska D., Bielinska S., Kamysz W., Kozlowski H. J. Inorg. Biochem. 2011, 105:208.
95. Zeng Y.B., Yang N., Sun H. Protein Chem. Eur. J. 2011, 17:5852.
96. Witkowska D., Politano R., Rowinska-Zyrek M., Guerrini R., Remelli M., Kozlowski H. Chem. Eng. J. 2012, 18:11088.
97. Arnesano F., Banci L., Bertini I., Mangani S., Thompsett A.R. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:3814-3819.
98. Koay M., Zhang L., Yang B., Maher M.J., Xiao Z., Wedd A.G. Inorg. Chem. 2005, 44:5203-5205.
99. Loftin I.R., Franke S., Blackburn N.J., McEvoy M.M. Protein Sci. 2007, 16:2287-2293.
100. Xue Y., Davis A.V., Balakrishnan G., Stasser J.P., Staehlin B.M., Focia P., Spiro T.G., Penner-Hahn J.E., O'Halloran T.V. Nat. Chem. Biol. 2008, 4:107-109.
101. Loftin I.R., Franke S., Roberts S.A., Weichsel A., Heroux A., Montfort W.R., Rensing C., McEvoy M.M. Biochemistry 2005, 44:10533-10540.
102. Lee J., Peña M.M., Nose Y., Thiele D.J. J. Biol. Chem. 2002, 277:4380-4387.
103. Zimmermann M., Udagedara S.R., Sze C.M., Ryan T.M., Howlett G.J., Xiao Z.G. J. Inorg. Biochem. 2012, 115:186-197.
104. Ash M.R., Chong L.X., Maher M.J., Hinds M.G., Xiao Z.G., Wedd A.G. Biochimie 2011, 50:9237-9247.
105. Sarret G., Favier A., Covès J., Hazemann J.-L., Mergeay M., Bersch B. J. Am. Chem. Soc. 2010, 132:3770-3777.
106. Abriata L.A., Banci L., Bertini I., Ciofi-Baffoni S., Gkazonis P., Spyroulias G.A., Vila A.J., Wang S. Nat. Chem. Biol. 2008, 4:599-601.
107. Allsop D., Mayes J., Moore S., Masad A., Tabner B.J. Biochem. Soc. Trans. 2008, 36:1293.
108. Bolognin S., Messori L., Zatta P. Neuromolecular Med. 2009, 11:223.
109. Zawisza I., Rozga M., Bal W. Coord. Chem. Rev. 2012, 256:2297-2307.
110. Hureau C., Dorlet P. Coord. Chem. Rev. 2012, 256:2175-2187.
111. Feimeng Z., Millhauser G.L. Coord. Chem. Rev. 2012, 256:2285-2286.
112. Pithadia A.S., Lim M.H. Curr. Opin. Chem. Biol. 2012, 16:67-73.
113. Uversky V.N., Oldfield C.J., Dunker A.K. Annu. Rev. Biophys. 2008, 37:215-246.
114. Sethi A., Tian J.H., Vu D.M., Gnanakaran S. Biophys. J. 2012, 103:748-757.
115. Camponeschi F., Valensin D., Tessari I., Bubacco L., Dell'Acqua S., Casella L., Monzani E., Gaggelli E., Valensin G. Inorg. Chem. 2013, 52:1358-1367.
116. Kihlken M.A., Singleton C., Le Brun N.E. J. Biol. Inorg. Chem. 2008, 13:1011-1023.
117. Wimmer R., Herrmann T., Solioz M., Wuthrich W.K. J. Biol. Chem. 1999, 274:22597-22603.
118. Chakravorty D.K., Wang B., Ucisik M.N., Merz K.M. J. Am. Chem. Soc. 2011, 133:19330-19333.
119. Shearer J., Soh P. Inorg. Chem. 2007, 46:710-719.
120. Badricka A.C., Jones C.E. J. Inorg. Biochem. 2009, 103:1169-1175.
121. D'Angelo P., Della Longa S., Arcovito A., Mancini G., Zitolo A., Chillemi G., Giachin G., Legname G.F. Benetti Biochem. 2012, 51:6068-6079.
122. Rozga M., Sokolowska M., Protas A.M., Bal W. J. Biol. Inorg. Chem. 2007, 12:913-918.
123. Glennon J.D., Sarkar B. Biochem. J. 1982, 203:15-23.
124. Sankararamakrishnan R., Verma S., Kumar S. Proteins Struct. Funct. Bioinform. 2005, 58:211-221.
125. Harford C., Sarkar B. Acc. Chem. Res. 1997, 30:123-130.
126. M. Chiera, M. Rowinska-Zyrek, R. Wieczorek, R. Guerrini, D. Witkowska, M. Remelli, K. Kozlowski, Metallomics, 2013,. doi:10.1039/C3MT20166J.
127. Albarazanji K.A., Balment R.J. J. Psychol. 1989, 418:261-271.
128. Gros C., Souque A., Schwartz J.C. Neuropeptides 1990, 17:1-5.
129. Bal W., Dyba M., Kasprzykowski F., Kozlowski H., Latajka R., Lankiewicz L., Mackiewicz Z., Pettit L.D. Inorg. Chim. Acta 1998, 283:1-11.
130. Bal W., Kozlowski H., Kupryszewski G., Mackiewicz Z., Pettit L., Robbins R. J. Inorg. Biochem. 1993, 52:79-87.
131. Janicka-Klos A., Porciatti E., Valensin D., Conato C., Remelli M., Oldziej S., Valensin G., Kozlowski H. Dalton Trans. 2013, 42:448-458.