Manganese binding properties of human calprotectin under conditions of high and low calcium: X-ray crystallographic and advanced electron paramagnetic resonance spectroscopic analysis

Journal of the American Chemical Society

Volumn 137, Issue 8, 2015, Pages 3004-3016

  Gagnon, Derek M ^a   Brophy, Megan Brunjes ^b   Bowman, Sarah E J ^b   Stich, Troy A ^a   Drennan, Catherine L ^b   Britt, R David ^a   Nolan, Elizabeth M ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING ENERGY; BINDING SITES; CALCIUM; COORDINATION REACTIONS; CRYSTALLOGRAPHY; ELECTRON RESONANCE; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRONS; IONS; MAGNETIC MOMENTS; MAGNETIC RESONANCE; MAMMALS; MANGANESE; NITROGEN; PARAMAGNETIC RESONANCE; PARAMAGNETISM; PROTEINS; RESONANCE; SPECTROSCOPIC ANALYSIS;

ANTIMICROBIAL PROTEINS; CO-ORDINATION CHEMISTRIES; ELECTRON NUCLEAR DOUBLE RESONANCE; ELECTRON PARAMAGNETIC RESONANCE SPECTROSCOPY; ELECTRON SPIN-ECHO ENVELOPE MODULATIONS; THREE ORDERS OF MAGNITUDE; X-RAY CRYSTALLOGRAPHIC STRUCTURES; ZERO-FIELD SPLITTINGS;

X RAY CRYSTALLOGRAPHY;

CALCIUM; CALGRANULIN; HETERODIMER; HISTIDINE; IMIDAZOLE; MANGANESE; NITROGEN 15; HIS-HIS-HIS-HIS-HIS-HIS; IMIDAZOLE DERIVATIVE; OLIGOPEPTIDE; PROTEIN BINDING; PROTON;

ARTICLE; BINDING AFFINITY; BINDING COMPETITION; BINDING SITE; CHEMICAL BINDING; CHEMICAL INTERACTION; CHEMICAL STRUCTURE; CROSS COUPLING REACTION; CRYSTAL STRUCTURE; ELECTRON NUCLEAR DOUBLE RESONANCE; ELECTRON SPIN RESONANCE; HYDROGEN BOND; STOICHIOMETRY; X RAY CRYSTALLOGRAPHY; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR MODEL; MUTATION; PROTEIN SECONDARY STRUCTURE;

CALCIUM; CRYSTALLOGRAPHY, X-RAY; ELECTRON SPIN RESONANCE SPECTROSCOPY; HISTIDINE; HUMANS; IMIDAZOLES; LEUKOCYTE L1 ANTIGEN COMPLEX; MANGANESE; MODELS, MOLECULAR; MUTATION; OLIGOPEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTONS;

EID: 84924322835     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja512204s     Document Type: Article

References (71)

1. Lisher, J. P.; Giedroc, D. P. Front. Cell. Infect. Microbiol. 2013, 3, 91
2. Brophy, M. B.; Nolan, E. M. ACS Chem. Biol. 2015, 10.1021/cb500792b
3. Kehl-Fie, T. E.; Skaar, E. P. Curr. Opin. Chem. Biol. 2010, 14, 218-224
4. Diaz-Ochoa, V. E.; Jellbauer, S.; Klaus, S.; Raffatellu, M. Front. Cell. Infect. Microbiol. 2014, 4, 2
5. Papp-Wallace, K. M.; Maguire, M. E. Annu. Rev. Microbiol. 2006, 60, 187-209
6. Kadioglu, A.; Weiser, J. N.; Paton, J. C.; Andrew, P. W. Nat. Rev. Microbiol. 2008, 6, 288-301
7. Liu, J. Z.; Jellbauer, S.; Poe, A. J.; Ton, V.; Pesciaroli, M.; Kehl-Fie, T. E.; Restrepo, N. A.; Hosking, M. P.; Edwards, R. A.; Battistoni, A.; Pasquali, P.; Lane, T. E.; Chazin, W. J.; Vogl, T.; Roth, J.; Skaar, E. P.; Raffatellu, M. Cell Host Microbe 2012, 11, 227-239
8. Corbin, B. D.; Seeley, E. H.; Raab, A.; Feldmann, J.; Miller, M. R.; Torres, V. J.; Anderson, K. L.; Dattilo, B. M.; Dunman, P. M.; Gerads, R.; Caprioli, R. M.; Nacken, W.; Chazin, W. J.; Skaar, E. P. Science 2008, 319, 962-965
9. Brophy, M. B.; Hayden, J. A.; Nolan, E. M. J. Am. Chem. Soc. 2012, 134, 18089-18100
10. Hayden, J. A.; Brophy, M. B.; Cunden, L. S.; Nolan, E. M. J. Am. Chem. Soc. 2013, 135, 775-787
11. Brophy, M. B.; Nakashige, T. G.; Gaillard, A.; Nolan, E. M. J. Am. Chem. Soc. 2013, 135, 17804-17817
12. Kehl-Fie, T. E.; Chitayat, S.; Hood, M. I.; Damo, S.; Restrepo, N.; Garcia, C.; Munro, K. A.; Chazin, W. J.; Skaar, E. P. Cell Host Microbe 2011, 10, 158-164
13. Damo, S. M.; Kehl-Fie, T. E.; Sugitani, N.; Holt, M. E.; Rathi, S.; Murphy, W. J.; Zhang, Y.; Betz, C.; Hench, L.; Fritz, G.; Skaar, E. P.; Chazin, W. J. Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 3841-3846
14. Donato, R. Biochim. Biophys. Acta 1999, 1450, 191-231
15. Heizmann, C. W.; Cox, J. A. Biometals 1998, 11, 383-397
16. Hunter, M. J.; Chazin, W. J. J. Biol. Chem. 1998, 273, 12427-12435
17. Leukert, N.; Vogl, T.; Strupat, K.; Reichelt, R.; Sorg, C.; Roth, J. J. Mol. Biol. 2006, 359, 961-972
18. Korndörfer, I. P.; Brueckner, F.; Skerra, A. J. Mol. Biol. 2007, 370, 887-898
19. Vogl, T.; Roth, J.; Sorg, C.; Hillenkamp, F.; Strupat, K. J. Am. Soc. Mass Spectrom. 1999, 10, 1124-1130
20. Gifford, J. L.; Walsh, M. P.; Vogel, H. J. Biochem. J. 2007, 405, 199-221
21. Persechini, A.; Moncrief, N. D.; Kretsinger, R. H. Trends Neurosci. 1989, 12, 462-467
22. Santamaria-Kisiel, L.; Rintala-Dempsey, A. C.; Shaw, G. S. Biochem. J. 2006, 396, 201-214
23. Eckert, R. L.; Broome, A.-M.; Ruse, M.; Robinson, N.; Ryan, D.; Lee, K. J. Invest. Dermatol. 2004, 123, 23-33
24. Garrett, S. C.; Hodgson, L.; Rybin, A.; Toutchkine, A.; Hahn, K. M.; Lawrence, D. S.; Bresnick, A. R. Biochemistry 2008, 47, 986-996
25. Donato, R. Cell Calcium 1986, 7, 123-145
26. Morin, A.; Eisenbraun, B.; Key, J.; Sanschagrin, P. C.; Timony, M. A.; Ottaviano, M.; Sliz, P. eLife 2013, 2, e01456
27. Otwinowski, Z.; Minor, W. Methods Enzymol. 1997, 276, 307-326
28. McCoy, A. J.; Grosse-Kunstleve, R. W.; Adams, P. D.; Winn, M. D.; Storoni, L. C.; Read, R. J. J. Appl. Crystallogr. 2007, 40, 658-674
29. 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.; McCoy, A. J.; Moriarty, N. W.; Oeffner, R.; Read, R. J.; Richardson, D. C.; Richardson, J. S.; Terwilliger, T. C.; Zwart, P. H. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 213-221
30. Emsley, P.; Lohkamp, B.; Scott, W. G.; Cowtan, K. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 486-501
31. Sienkiewicz, A.; Smith, B. G.; Veselov, A.; Scholes, C. P. Rev. Sci. Instrum. 1996, 67, 2134-2138
32. Mims, W. B. Proc. R. Soc. London 1965, 283, 452-457
33. Gemperle, C.; Aebli, G.; Schweiger, A.; Ernst, R. R. J. Magn. Reson. 1990, 88, 241-256
34. Van Doorslaer, S.; Sierra, G. A.; Schweiger, A. J. Magn. Reson. 1999, 136, 152-158
35. Stoll, S.; Schweiger, A. J. Magn. Reson. 2006, 178, 42-55
36. Hoogstraten, C. G.; Britt, R. D. RNA 2002, 8, 252-260
37. Hoogstraten, C. G.; Grant, C. V.; Horton, T. E.; DeRose, V. J.; Britt, R. D. J. Am. Chem. Soc. 2002, 124, 834-842
38. Mims, W. B.; Peisach, J. Biological Magnetic Resonance; Springer: Boston, MA, 1981; Vol. 3, pp 213-263.
39. Dikanov, S. A.; Shubin, A. A.; Parmon, V. N. J. Magn. Reson. 1981, 42, 474-487
40. Dong, G.-Y.; Liu, T.-F.; He, C.-H.; Deng, X.-C.; Shi, X.-G. Acta Crystallogr., Sect. E: Struct. Rep. Online 2011, 67, m960
41. Niu, S.-Y.; Zhang, S.-S.; Li, X.-M.; Wen, Y.-H.; Jiao, K. Acta Crystallogr., Sect. E: Struct. Rep. Online 2004, 60, m209-m211
42. Durot, S.; Policar, C.; Cisnetti, F.; Lambert, F.; Renault, J.-P.; Pelosi, G.; Blain, G.; Korri-Youssoufi, H.; Mahy, J.-P. Eur. J. Inorg. Chem. 2005, 2005, 3513-3523
43. Lemoine, P.; Viossat, V.; Dayan, E.; Dung, N.-H.; Viossat, B. Inorg. Chim. Acta 2006, 359, 4274-4280
44. Dev, S.; Ramli, E.; Rauchfuss, T. B.; Wilson, S. R. Inorg. Chem. 1991, 30, 2514-2519
45. Garrett, T. P. J.; Guss, J. M.; Freeman, H. C. Acta Crystallogr., Sect. C: Cryst. Struct. Commun. 1983, 39, 1027-1031
46. García-Rubio, I.; Angerhofer, A.; Schweiger, A. J. Magn. Reson. 2007, 184, 130-142
47. Angerhofer, A.; Moomaw, E. W.; García-Rubio, I.; Ozarowski, A.; Krzystek, J.; Weber, R. T.; Richards, N. G. J. J. Phys. Chem. B 2007, 111, 5043-5046
48. Meirovitch, E.; Luz, Z.; Kalb, A. J. J. Am. Chem. Soc. 1974, 96, 7542-7546
49. Reed, G. H.; Markham, G. D. Biol. Magn. Reson. 1984, 6, 73-142
50. Walsby, C. J.; Telser, J.; Rigsby, R. E.; Armstrong, R. N.; Hoffman, B. M. J. Am. Chem. Soc. 2005, 127, 8310-8319
51. Duboc, C.; Phoeung, T.; Zein, S.; Pécaut, J.; Collomb, M.-N.; Neese, F. Inorg. Chem. 2007, 46, 4905-4916
52. Duboc, C.; Collomb, M.-N.; Neese, F. Appl. Magn. Reson. 2010, 37, 229-245
53. Un, S. Inorg. Chem. 2013, 52, 3803-3813
54. Campomanes, P.; Kellett, W. F.; Easthon, L. M.; Ozarowski, A.; Allen, K. N.; Angerhofer, A.; Rothlisberger, U.; Richards, N. G. J. J. Am. Chem. Soc. 2014, 136, 2313-2323
55. Espe, M. P.; Hosler, J. P.; Ferguson-Miller, S.; Babcock, G. T.; McCracken, J. Biochemistry 1995, 34, 7593-7602
56. Bleaney, B.; Rubins, R. S. Proc. Phys. Soc. 1961, 77, 103-112
57. Mims, W. B.; Peisach, J. J. Chem. Phys. 1978, 69, 4921-4930
58. Zweier, J.; Aisen, P.; Peisach, J.; Mims, W. B. J. Biol. Chem. 1979, 254, 3512-3515
59. Deligiannakis, Y.; Louloudi, M.; Hadjiliadis, N. Coord. Chem. Rev. 2000, 204, 1-112
60. Matar, K.; Goldfarb, D. J. Magn. Reson. Ser. A 1994, 111, 50-61
61. Vogt, M.; Lahiri, S.; Hoogstraten, C. G.; Britt, R. D.; DeRose, V. J. J. Am. Chem. Soc. 2006, 128, 16764-16770
62. Geue, R. J.; Hambley, T. W.; Harrowfield, J. M.; Sargeson, A. M.; Snow, M. R. J. Am. Chem. Soc. 1984, 106, 5478-5488
63. Martin, L. L.; Martin, R. L.; Murray, K. S.; Sargeson, A. M. S. Inorg. Chem. 1990, 29, 1387-1394
64. Horton, T. E.; Clardy, D. R.; DeRose, V. J. Biochemistry 1998, 37, 18094-18101
65. Cohn, M.; Townsend, J. Nature 1954, 173, 1090-1091
66. Whittaker, J. W.; Whittaker, M. M. J. Am. Chem. Soc. 1991, 113, 5528-5540
67. Smoukov, S. K.; Telser, J.; Bernat, B. A.; Rife, C. L.; Armstrong, R. N.; Hoffman, B. M. J. Am. Chem. Soc. 2002, 124, 2318-2326
68. Berliner, L. J.; Ellis, P. D.; Murakami, K. Biochemistry 1983, 22, 5061-5063
69. Senguen, F. T.; Grabarek, Z. Biochemistry 2012, 51, 6182-6194
70. Moroz, O. V.; Blagova, E. V.; Wilkinson, A. J.; Wilson, K. S.; Bronstein, I. B. J. Mol. Biol. 2009, 391, 536-551
71. Koch, M.; Diez, J.; Fritz, G. J. Mol. Biol. 2008, 378, 933-942