Human calprotectin is an iron-sequestering host-defense protein

Nature Chemical Biology

Volumn 11, Issue 10, 2015, Pages 765-771

  Nakashige, Toshiki G ^a   Zhang, Bo ^b   Krebs, Carsten ^b   Nolan, Elizabeth M ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CALGRANULIN; HEXAHISTIDINE; IRON; MANGANESE; ZINC; CALCIUM; IRON CHELATING AGENT;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; BINDING AFFINITY; BINDING SITE; BIOCHEMICAL ANALYSIS; CONTROLLED STUDY; CULTURE MEDIUM; ESCHERICHIA COLI; GROWTH INHIBITION; HOST RESISTANCE; IRON CHELATION; IRON DEPLETION; IRON METABOLISM; IRON TRANSPORT; MICROBIAL GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; STAPHYLOCOCCUS AUREUS; CHEMISTRY; DRUG EFFECTS; ELECTRON SPIN RESONANCE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; HUMAN; LACTOBACILLUS PLANTARUM; METABOLISM; MICROBIAL SENSITIVITY TEST; MOSSBAUER SPECTROSCOPY; PHYSIOLOGY;

CALCIUM; ELECTRON SPIN RESONANCE SPECTROSCOPY; ESCHERICHIA COLI; HOST-PATHOGEN INTERACTIONS; HUMANS; IRON; IRON CHELATING AGENTS; LACTOBACILLUS PLANTARUM; LEUKOCYTE L1 ANTIGEN COMPLEX; MICROBIAL SENSITIVITY TESTS; SPECTROSCOPY, MOSSBAUER; STAPHYLOCOCCUS AUREUS;

EID: 84941874897     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1891     Document Type: Article

References (49)

1. Bertini, I., Gray, H.B., Stiefel, E.I. & Valentine, J.S. Biological Inorganic Chemistry: Structure and Reactivity (University Science Books, 2007).
2. Weinberg, E.D. Nutritional immunity: host's attempt to withhold iron from microbial invaders. J. Am. Med. Assoc. 231, 39-41 (1975).
3. Fischbach, M.A., Lin, H., Liu, D.R. & Walsh, C.T. How pathogenic bacteria evade mammalian sabotage in the battle for iron. Nat. Chem. Biol. 2, 132-138 (2006).
4. Hood, M.I. & Skaar, E.P. Nutritional immunity: transition metals at the pathogen-host interface. Nat. Rev. Microbiol. 10, 525-537 (2012).
5. Cassat, J.E. & Skaar, E.P. Iron in infection and immunity. Cell Host Microbe 13, 509-519 (2013).
6. Diaz-Ochoa, V.E., Jellbauer, S., Klaus, S. & Raffatellu, M. Transition metal ions at the crossroads of mucosal immunity and microbial pathogenesis. Front. Cell. Infect. Microbiol. 4, 2 (2014).
7. Sohnle, P.G., Collins-Lech, C. & Wiessner, J.H. The zinc-reversible antimicrobial activity of neutrophil lysates and abscess fluid supernatants. J. Infect. Dis. 164, 137-142 (1991).
8. Corbin, B.D. et al. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319, 962-965 (2008).
9. Kehl-Fie, T.E. et al. Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe 10, 158-164 (2011).
10. Brophy, M.B., Hayden, J.A. & Nolan, E.M. Calcium ion gradients modulate the zinc affinity and antibacterial activity of human calprotectin. J. Am. Chem. Soc. 134, 18089-18100 (2012).
11. Hayden, J.A., Brophy, M.B., Cunden, L.S. & Nolan, E.M. High-affinity manganese coordination by human calprotectin is calcium dependent and requires the histidine-rich site formed at the dimer interface. J. Am. Chem. Soc. 135, 775-787 (2013).
12. Damo, S.M. et al. Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc. Natl. Acad. Sci. USA 110, 3841-3846 (2013).
13. Brophy, M.B., Nakashige, T.G., Gaillard, A. & Nolan, E.M. Contributions of the S100A9 C-terminal tail to high-affinity Mn(II) chelation by the host-defense protein human calprotectin. J. Am. Chem. Soc. 135, 17804-17817 (2013).
14. Vogl, T., Leukert, N., Barczyk, K., Strupat, K. & Roth, J. Biophysical characterization of S100A8 and S100A9 in the absence and presence of bivalent cations. Biochim. Biophys. Acta 1763, 1298-1306 (2006).
15. Gagnon, D.M. et al. Manganese-binding properties of human calprotectin under conditions of high and low calcium: X-ray crystallographic and advanced electron paramagnetic resonance spectroscopic analysis. J. Am. Chem. Soc. 137, 3004-3016 (2015).
16. 2 heterotetramer, calprotectin, illustrates how conformational changes of interacting α-helices can determine specific association of two EF-hand proteins. J. Mol. Biol. 370, 887-898 (2007).
17. 2+ and bacterial pathogenesis. Front. Biosci. 9, 1035-1042 (2004).
18. Papp-Wallace, K.M. & Maguire, M.E. Manganese transport and the role of manganese in virulence. Annu. Rev. Microbiol. 60, 187-209 (2006).
19. Jacobsen, F.E., Kazmierczak, K.M., Lisher, J.P., Winkler, M.E. & Giedroc, D.P. Interplay between manganese and zinc homeostasis in the human pathogen Streptococcus pneumoniae. Metallomics 3, 38-41 (2011).
20. Aguirre, J.D. et al. A manganese-rich environment supports superoxide dismutase activity in a Lyme disease pathogen, Borrelia burgdorferi. J. Biol. Chem. 288, 8468-8478 (2013).
21. Lisher, J.P. & Giedroc, D.P. Manganese acquisition and homeostasis at the host-pathogen interface. Front. Cell. Infect. Microbiol. 3, 91 (2013).
22. Irving, H. & Williams, R.J.P. The stability of transition-metal complexes. J. Chem. Soc. 3192-3210 (1953).
23. Brophy, M.B. & Nolan, E.M. Manganese and microbial pathogenesis: sequestration by the mammalian immune system and utilization by microorganisms. ACS Chem. Biol. 10, 641-651 (2015).
24. Archibald, F.S. & Fridovich, I. Manganese and defenses against oxygen toxicity in Lactobacillus plantarum. J. Bacteriol. 145, 442-451 (1981).
25. Frey, P.A. & Reed, G.H. The ubiquity of iron. ACS Chem. Biol. 7, 1477-1481 (2012).
26. Münck, E. in Physical Methods in Bioinorganic Chemistry: Spectroscopy and Magnetism (ed. Que, L., Jr.) 287-319 (University Science Books, 2000).
27. Greenwood, N.N. & Gibb, T.C. Mössbauer Spectroscopy. (Springer, 1971).
28. Asch, L., Adloff, J.P., Friedt, J.M. & Danon, J. Motional effects in the Mössbauer spectra of iron(II) hexammines. Chem. Phys. Lett. 5, 105-108 (1970).
29. 4 (M = Mn, Fe, Co, Ni, Zn; X = Cl, Br; L=1,4,7-trimethyl-1,4,7-triazacyclononane). Inorg. Chem. 36, 2834-2843 (1997).
30. Cotruvo, J.A. Jr. & Stubbe, J. Metallation and mismetallation of iron and manganese proteins in vitro and in vivo: the class I ribonucleotide reductases as a case study. Metallomics 4, 1020-1036 (2012).
31. 2+. J. Am. Chem. Soc. 122, 5644-5645 (2000).
32. Gibbs, C.R. Characterization and application of ferrozine iron reagent as a ferrous iron indicator. Anal. Chem. 48, 1197-1201 (1976).
33. Stookey, L.L. Ferrozine-a new spectrophotometric reagent for iron. Anal. Chem. 42, 779-781 (1970).
34. Moroz, O.V., Blagova, E.V., Wilkinson, A.J., Wilson, K.S. & Bronstein, I.B. The crystal structures of human S100A12 in apo form and in complex with zinc: new insights into S100A12 oligomerization. J. Mol. Biol. 391, 536-551 (2009).
35. 2+-free states. Biochemistry 38, 1695-1704 (1999).
36. Ostendorp, T., Diez, J., Heizmann, C.W. & Fritz, G. The crystal structures of human S100B in the zinc- and calcium-loaded state at three pH values reveal zinc ligand swapping. Biochim. Biophys. Acta 1813, 1083-1091 (2011).
37. Liu, J.Z. et al. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11, 227-239 (2012).
38. Königsberger, L.C., Königsberger, E., May, P.M. & Hefter, G.T. Complexation of iron(III) and iron(II) by citrate. Implications for iron speciation in blood plasma. J. Inorg. Biochem. 78, 175-184 (2000).
39. Mills, S.A. & Marletta, M.A. Metal-binding characteristics and role of iron oxidation in the ferric uptake regulator from Escherichia coli. Biochemistry 44, 13553-13559 (2005).
40. Mizuno, K., Whittaker, M.M., Bächinger, H.P. & Whittaker, J.W. Calorimetric studies on the tight binding metal interactions of Escherichia coli manganese superoxide dismutase. J. Biol. Chem. 279, 27339-27344 (2004).
41. 2+ cation. Inorg. Chem. 42, 5771-5777 (2003).
42. 3)iron(II) sulfate-1H-imidazole (1/2). Acta Crystallogr. Sect. E Struct. Rep. Online 67, m1600-m1601 (2011).
43. Singh, P.K., Parsek, M.R., Greenberg, E.P. & Welsh, M.J. A component of innate immunity prevents bacterial biofilm development. Nature 417, 552-555 (2002).
44. Flo, T.H. et al. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432, 917-921 (2004).
45. Cartron, M.L., Maddocks, S., Gillingham, P., Craven, C.J. & Andrews, S.C. Feo-transport of ferrous iron into bacteria. Biometals 19, 143-157 (2006).
46. Stojiljkovic, I., Cobeljic, M. & Hantke, K. Escherichia coli K-12 ferrous iron-uptake mutants are impaired in their ability to colonize the mouse intestine. FEMS Microbiol. Lett. 108, 111-115 (1993).
47. Konings, A.F. et al. Pseudomonas aeruginosa uses multiple pathways to acquire iron during chronic infection in cystic fibrosis lungs. Infect. Immun. 81, 2697-2704 (2013).
48. Velayudhan, J. et al. Iron acquisition and virulence in Helicobacter pylori: a major role for FeoB, a high-affinity ferrous iron transporter. Mol. Microbiol. 37, 274-286 (2000).
49. Carter, P. Spectrophotometric determination of serum iron at the submicrogram level with a new reagent (ferrozine). Anal. Biochem. 40, 450-458 (1971).