Advertisement

Science China Life Sciences

, Volume 59, Issue 8, pp 792–801 | Cite as

Binding of transition metals to S100 proteins

  • Benjamin A. Gilston
  • Eric P. Skaar
  • Walter J. ChazinEmail author
Open Access
Review

Abstract

The S100 proteins are a unique class of EF-hand Ca2+ binding proteins distributed in a cell-specific, tissue-specific, and cell cycle-specific manner in humans and other vertebrates. These proteins are distinguished by their distinctive homodimeric structure, both intracellular and extracellular functions, and the ability to bind transition metals at the dimer interface. Here we summarize current knowledge of S100 protein binding of Zn2+, Cu2+ and Mn2+ ions, focusing on binding affinities, conformational changes that arise from metal binding, and the roles of transition metal binding in S100 protein function.

Keywords

S100 Proteins Zinc Manganese Copper 

References

  1. Arnesano, F., Banci, L., Bertini, I., Fantoni, A., Tenori, L., and Viezzoli, M.S. (2005). Structural interplay between calcium(II) and copper(II) binding to S100A13 protein. Angew Chem Int Ed Engl 44, 6341–6344.CrossRefPubMedGoogle Scholar
  2. Baudier, J., Glasser, N., and Gerard, D. (1986). Ions binding to s100 proteins. I. Calcium-and zinc-binding properties of bovine brain s100 alpha alpha, s100a (alpha beta), and s100b (beta beta) protein: Zn2+ regulates Ca2+ binding on s100b protein. J Biol Chem 261, 8192–8203.PubMedGoogle Scholar
  3. Baudier, J., Glasser, N., Haglid, K., and Gerard, D. (1984). Purification, characterization and ion binding properties of human brain S100b protein. Biochim Biophys Acta 790, 164–173.CrossRefPubMedGoogle Scholar
  4. Baudier, J., Holtzscherer, C., and Gerard, D. (1982). Zinc-dependent affinity chromatography of the S100b protein on phenyl-Sepharose. A rapid purification method. FEBS Lett 148, 231–234.PubMedGoogle Scholar
  5. Bhattacharya, S., Bunick, C.G., and Chazin, W.J. (2004). Target selectivity in EF-hand calcium binding proteins. Biochim Biophys Acta 1742, 69–79.CrossRefPubMedGoogle Scholar
  6. Brodersen, D.E., Nyborg, J., and Kjeldgaard, M. (1999). Zinc-binding site of an S100 protein revealed. Two crystal structures of Ca2+-bound human psoriasin (S100A7) in the Zn2+-loaded and Zn2+-free states. Biochemistry 38, 1695–1704.CrossRefPubMedGoogle Scholar
  7. Brophy, M.B., and Nolan, E.M. (2015). Manganese and microbial pathogenesis: sequestration by the Mammalian immune system and utilization by microorganisms. ACS Chem Biol 10, 641–651.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brophy, M.B., Hayden, J.A., and Nolan, E.M. (2012). Calcium ion gradients modulate the zinc affinity and antibacterial activity of human calprotectin. J Am Chem Soc 134, 18089–18100.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Brophy, M.B., Nakashige, T.G., Gaillard, A., and Nolan, E.M. (2013). 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.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bunick, C.G., Nelson, M.R., Mangahas, S., Hunter, M.J., Sheehan, J.H., Mizoue, L.S., Bunick, G.J., and Chazin, W.J. (2004). Designing sequence to control protein function in an EF-hand protein. J Am Chem Soc 126, 5990–5998.CrossRefPubMedGoogle Scholar
  11. Cavalier, M.C., Pierce, A.D., Wilder, P.T., Alasady, M.J., Hartman, K.G., Neau, D.B., Foley, T.L., Jadhav, A., Maloney, D.J., Simeonov, A., Toth, E.A., and Weber, D.J. (2014). Covalent small molecule inhibitors of Ca2+-bound S100B. Biochemistry 53, 6628–6640.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Charpentier, T.H., Wilder, P.T., Liriano, M.A., Varney, K.M., Pozharski, E., MacKerell, A.D., Jr., Coop, A., Toth, E.A., and Weber, D.J. (2008). Divalent metal ion complexes of S100B in the absence and presence of pentamidine. J Mol Biol 382, 56–73.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Charpentier, T.H., Wilder, P.T., Liriano, M.A., Varney, K.M., Zhong, S., Coop, A., Pozharski, E., MacKerell, A.D., Toth, E.A., and Weber, D.J. (2009). Small molecules bound to unique sites in the target protein binding cleft of calcium-bound S100B as characterized by nuclear magnetic resonance and X-ray crystallography. Biochemistry 48, 6202–6212.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chazin, W.J. (2007). The impact of X-ray crystallography and NMR on intracellular calcium signal transduction by EF-hand proteins: crossing the threshold from structure to biology and medicine. Sci STKE 2007, pe27.CrossRefPubMedGoogle Scholar
  15. Clark, H.L., Jhingran, A., Sun, Y., Vareechon, C., de Jesus Carrion, S., Skaar, E.P., Chazin, W.J., Calera, J.A., Hohl, T.M., and Pearlman, E. (2016). Zinc and manganese chelation by neutrophil S100A8/A9 (Calprotectin) limits extracellular Aspergillus fumigatus hyphal growth and corneal infection. J Immunol 196, 336–344.CrossRefPubMedGoogle Scholar
  16. 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., and Skaar, E.P. (2008). Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319, 962–965.CrossRefPubMedGoogle Scholar
  17. 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., and Chazin, W.J. (2013). 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.CrossRefPubMedPubMedCentralGoogle Scholar
  18. DeLano, W.L. (2002). The PyMOL molecular graphics system (Palo Alto: DeLano Scientific).Google Scholar
  19. Dell’Angelica, E.C., Schleicher, C.H., and Santome, J.A. (1994). Primary structure and binding properties of calgranulin C, a novel S100-like calcium-binding protein from pig granulocytes. J Biol Chem 269, 28929–28936.PubMedGoogle Scholar
  20. Donato, R. (2003). Intracellular and extracellular roles of S100 proteins. Microsc Res Tech 60, 540–551.CrossRefPubMedGoogle Scholar
  21. Donato, R., Cannon, B.R., Sorci, G., Riuzzi, F., Hsu, K., Weber, D.J., and Geczy, C.L. (2013). Functions of S100 proteins. Curr Mol Med 13, 24–57.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fritz, G., Heizmann, C.W., and Kroneck, P.M. (1998). Probing the structure of the human Ca2+-and Zn2+-binding protein S100A3: spectroscopic investigations of its transition metal ion complexes, and three-dimensional structural model. Biochim Biophys Acta 1448, 264–276.CrossRefPubMedGoogle Scholar
  23. Fritz, G., Mittl, P.R., Vasak, M., Grutter, M.G., and Heizmann, C.W. (2002) The crystal structure of metal-free human EF-hand protein S100A3 at 1.7-A resolution. J Biol Chem 277, 33092–33098.Google Scholar
  24. Günter, F., and Heizmann, C.W. (2006). 3D Structures of the Calcium and Zinc Binding S100 Proteins. In Handbook of Metallproteins.Google Scholar
  25. Gaddy, J.A., Radin, J.N., Loh, J.T., Piazuelo, M.B., Kehl-Fie, T.E., Delgado, A.G., Ilca, F.T., Peek, R.M., Cover, T.L., Chazin, W.J., Skaar, E.P., and Scott Algood, H.M. (2014). The host protein calprotectin modulates the Helicobacter pylori cag type IV secretion system via zinc sequestration. PLoS Pathog 10, e1004450.CrossRefGoogle Scholar
  26. Gagnon, D.M., Brophy, M.B., Bowman, S.E., Stich, T.A., Drennan, C.L., Britt, R.D., and Nolan, E.M. (2015). 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.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gribenko, A.V., and Makhatadze, G.I. (1998). Oligomerization and divalent ion binding properties of the S100P protein: a Ca2+/Mg2+-switch model. J Mol Biol 283, 679–694.CrossRefPubMedGoogle Scholar
  28. Haase-Kohn, C., Wolf, S., Lenk, J., and Pietzsch, J. (2011). Copper-mediated cross-linking of S100A4, but not of S100A2, results in proinflammatory effects in melanoma cells. Biochem Biophys Res Commun 413, 494–498.CrossRefPubMedGoogle Scholar
  29. Haley, K.P., Delgado, A.G., Piazuelo, M.B., Mortensen, B.L., Correa, P., Damo, S.M., Chazin, W.J., Skaar, E.P., and Gaddy, J.A. (2015). The human antimicrobial protein calgranulin C participates in control of Helicobacter pylori growth and regulation of virulence. Infect Immun 83, 2944–2956.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hayden, J.A., Brophy, M.B., Cunden, L.S., and Nolan, E.M. (2013). 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.CrossRefPubMedGoogle Scholar
  31. Heizmann, C.W., and Cox, J.A. (1998). New perspectives on S100 proteins: a multi-functional Ca2+-, Zn2+-and Cu2+-binding protein family. Biometals 11, 383–397.CrossRefPubMedGoogle Scholar
  32. Heizmann, C.W., Fritz, G., and Schäfer, B.W. (2002). S100 proteins: structure, functions and pathology. Front Biosci 7, d1356–1368.PubMedGoogle Scholar
  33. Hood, M.I., Mortensen, B.L., Moore, J.L., Zhang, Y., Kehl-Fie, T.E., Sugitani, N., Chazin, W.J., Caprioli, R.M., and Skaar, E.P. (2012). Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration. PLoS Pathog 8, e1003068.CrossRefGoogle Scholar
  34. Ikura, M. (1996). Calcium binding and conformational response in EF-hand proteins. Trends Biochem Sci 21, 14–17.CrossRefPubMedGoogle Scholar
  35. Kehl-Fie, T.E., Chitayat, S., Hood, M.I., Damo, S., Restrepo, N., Garcia, C., Munro, K.A., Chazin, W.J., and Skaar, E.P. (2011). Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe 10, 158–164.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kehl-Fie, T.E., Zhang, Y., Moore, J.L., Farrand, A.J., Hood, M.I., Rathi, S., Chazin, W.J., Caprioli, R.M., and Skaar, E.P. (2013). MntABC and MntH contribute to systemic Staphylococcus aureus infection by competing with calprotectin for nutrient manganese. Infect Immun 81, 3395–3405.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kizawa, K., Jinbo, Y., Inoue, T., Takahara, H., Unno, M., Heizmann, C.W., and Izumi, Y. (2013a). Human S100A3 tetramerization propagates Ca2+/Zn2+ binding states. Biochim Biophys Acta 1833, 1712–1719.CrossRefPubMedGoogle Scholar
  38. Kizawa, K., Unno, M., Takahara, H., and Heizmann, C.W. (2013b). Purification and characterization of the human cysteine-rich S100A3 protein and its pseudo citrullinated forms expressed in insect cells. Methods Mol Biol 963, 73–86.CrossRefPubMedGoogle Scholar
  39. Koch, M., Bhattacharya, S., Kehl, T., Gimona, M., Vasak, M., Chazin, W., Heizmann, C.W., Kroneck, P.M., and Fritz, G. (2007). Implications on zinc binding to S100A2. Biochim Biophys Acta 1773, 457–470.CrossRefPubMedGoogle Scholar
  40. Kordowska, J., Stafford, W.F., and Wang, C.L. (1998). Ca2+ and Zn2+ bind to different sites and induce different conformational changes in human calcyclin. Euro J Biochem 253, 57–66.CrossRefGoogle Scholar
  41. Korndorfer, I.P., Brueckner, F., and Skerra, A. (2007). The crystal structure of the human (S100A8/S100A9)2 heterotetramer, calprotectin, illustrates how conformational changes of interacting alpha-helices can determine specific association of two EF-hand proteins. J Mol Biol 370, 887–898.CrossRefPubMedGoogle Scholar
  42. Leon, R., Murray, J.I., Cragg, G., Farnell, B., West, N.R., Pace, T.C., Watson, P.H., Bohne, C., Boulanger, M.J., and Hof, F. (2009). Identification and characterization of binding sites on S100A7, a participant in cancer and inflammation pathways. Biochemistry 48, 10591–10600.CrossRefPubMedGoogle Scholar
  43. Lin, J., Yang, Q., Yan, Z., Markowitz, J., Wilder, P.T., Carrier, F., and Weber, D.J. (2004). Inhibiting S100B restores p53 levels in primary malignant melanoma cancer cells. J Biol Chem 279, 34071–34077.CrossRefPubMedGoogle Scholar
  44. Linse, S., and Chazin, W.J. (1995). Quantitative measurements of the cooperativity in an EF-hand protein with sequential calcium binding. Protein Sci 4, 1038–1044.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Malashkevich, V.N., Dulyaninova, N.G., Ramagopal, U.A., Liriano, M.A., Varney, K.M., Knight, D., Brenowitz, M., Weber, D.J., Almo, S.C., and Bresnick, A.R. (2010). Phenothiazines inhibit S100A4 function by inducing protein oligomerization. Proc Natl Acad Sci USA 107, 8605–8610.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Maler, L., Sastry, M., and Chazin, W.J. (2002). A structural basis for S100 protein specificity derived from comparative analysis of apo and Ca2+-calcyclin. J mol biol 317, 279–290.CrossRefPubMedGoogle Scholar
  47. Moore, B.W. (1965). A soluble protein characteristic of the nervous system. Biochem Biophys Res Commun 19, 739–744.CrossRefPubMedGoogle Scholar
  48. Moroz, O.V., Antson, A.A., Dodson, E.J., Burrell, H.J., Grist, S.J., Lloyd, R.M., Maitland, N.J., Dodson, G.G., Wilson, K.S., Lukanidin, E., and Bronstein, I.B. (2002). The structure of S100A12 in a hexameric form and its proposed role in receptor signalling. Acta Crystallogr D Biol Crystallogr 58, 407–413.CrossRefPubMedGoogle Scholar
  49. Moroz, O.V., Antson, A.A., Grist, S.J., Maitland, N.J., Dodson, G.G., Wilson, K.S., Lukanidin, E., and Bronstein, I.B. (2003). Structure of the human S100A12-copper complex: implications for host-parasite defence. Acta Crystallogr D Biol Crystallogr 59, 859–867.CrossRefPubMedGoogle Scholar
  50. Moroz, O.V., Blagova, E.V., Wilkinson, A.J., Wilson, K.S., and Bronstein, I.B. (2009a). The crystal structures of human S100A12 in apo form and in complex with zinc: new insights into S100A12 oligomerisation. J Mol Biol 391, 536–551.CrossRefPubMedGoogle Scholar
  51. Moroz, O.V., Burkitt, W., Wittkowski, H., He, W., Ianoul, A., Novitskaya, V., Xie, J., Polyakova, O., Lednev, I.K., Shekhtman, A., Derrick, P.J., Bjoerk, P., Foell, D., and Bronstein, I.B. (2009b). Both Ca2+ and Zn2+ are essential for S100A12 protein oligomerization and function. BMC Biochem 10, 11.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Moroz, O.V., Burkitt, W., Wittkowski, H., He, W., Ianoul, A., Novitskaya, V., Xie, J., Polyakova, O., Lednev, I.K., Shekhtman, A., Derrick, P.J., Bjoerk, P., Foell, D., and Bronstein, I.B. (2009). Both Ca2+ and Zn2+ are essential for s100a12 protein oligomerization and function. BMC Biochem 10, 11.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Moroz, O.V., Wilson, K.S., and Bronstein, I.B. (2011). The role of zinc in the S100 proteins: insights from the X-ray structures. Amino Acids 41, 761–772.CrossRefPubMedGoogle Scholar
  54. Murray, J.I., Tonkin, M.L., Whiting, A.L., Peng, F., Farnell, B., Cullen, J.T., Hof, F., and Boulanger, M.J. (2012). Structural characterization of S100A15 reveals a novel zinc coordination site among S100 proteins and altered surface chemistry with functional implications for receptor binding. BMC Struct Biol 12, 16.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Nakashige, T.G., Zhang, B., Krebs, C., and Nolan, E.M. (2015). Human calprotectin is an iron-sequestering host-defense protein. Nat Chem Biol 11, 765–771.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Nelson, M.R., and Chazin, W.J. (1998). Structures of EF-hand Ca2+-binding proteins: diversity in the organization, packing and response to Ca2+ binding. Biometals 11, 297–318.CrossRefPubMedGoogle Scholar
  57. Nelson, M.R., Thulin, E., Fagan, P.A., Forsen, S., and Chazin, W.J. (2002). The EF-hand domain: a globally cooperative structural unit. Protein Sci 11, 198–205.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Nishikawa, T., Lee, I.S., Shiraishi, N., Ishikawa, T., Ohta, Y., and Nishikimi, M. (1997). Identification of S100b protein as copper-binding protein and its suppression of copper-induced cell damage. J Biol Chem 272, 23037–23041.CrossRefPubMedGoogle Scholar
  59. Ostendorp, T., Diez, J., Heizmann, C.W., and Fritz, G. (2011). 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.CrossRefPubMedGoogle Scholar
  60. Ostendorp, T., Leclerc, E., Galichet, A., Koch, M., Demling, N., Weigle, B., Heizmann, C.W., Kroneck, P.M., and Fritz, G. (2007). Structural and functional insights into RAGE activation by multimeric S100B. EMBO J 26, 3868–3878.CrossRefPubMedPubMedCentralGoogle Scholar
  61. Pei, J., Kim, B.H., and Grishin, N.V. (2008). PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucleic Acids Res 36, 2295–2300.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Potts, B.C., Carlstrom, G., Okazaki, K., Hidaka, H., and Chazin, W.J. (1996). 1H NMR assignments of apo calcyclin and comparative structural analysis with calbindin D9k and S100 beta. Protein Sci 5, 2162–2174.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Potts, B.C., Smith, J., Akke, M., Macke, T.J., Okazaki, K., Hidaka, H., Case, D.A., and Chazin, W.J. (1995). The structure of calcyclin reveals a novel homodimeric fold for S100 Ca2+-binding proteins. Nat Struct Biol 2, 790–796.CrossRefPubMedGoogle Scholar
  64. Rustandi, R.R., Baldisseri, D.M., Drohat, A.C., and Weber, D.J. (1998). The Ca2+-dependent interaction of s100b(beta beta) with a peptide derived from p53. Biochemistry 37, 1951–1960.CrossRefPubMedGoogle Scholar
  65. Schäfer, B.W., and Heizmann, C.W. (1996). The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem Sci 21, 134–140.CrossRefPubMedGoogle Scholar
  66. Schäfer, B.W., Fritschy, J.M., Murmann, P., Troxler, H., Durussel, I., Heizmann, C.W., and Cox, J.A. (2000). Brain S100A5 is a novel calcium-, zinc-, and copper ion-binding protein of the EF-hand superfamily. J Biol Chem 275, 30623–30630.CrossRefPubMedGoogle Scholar
  67. Schaub, M.C., and Heizmann, C.W. (2008). Calcium, troponin, calmodulin, S100 proteins: from myocardial basics to new therapeutic strategies. Biochem Biophys Res Commun 369, 247–264.CrossRefPubMedGoogle Scholar
  68. Sigel, A., and Sigel, H. (2000). Manganese and its role in biological processes (New York: Marcel Dekker).Google Scholar
  69. Sivaraja, V., Kumar, T.K., Rajalingam, D., Graziani, I., Prudovsky, I., and Yu, C. (2006). Copper binding affinity of S100A13, a key component of the FGF-1 nonclassical copper-dependent release complex. Biophys J 91, 1832–1843.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Striz, I., and Trebichavsky, I. (2004). Calprotectin-a pleiotropic molecule in acute and chronic inflammation. Physiol Res 53, 245–253.PubMedGoogle Scholar
  71. Sturchler, E., Cox, J.A., Durussel, I., Weibel, M., Heizmann, C.W. (2006). S100A16, a novel calcium-binding protein of the EF-hand superfamily. J Biol Chem 281, 38905–38917.CrossRefPubMedGoogle Scholar
  72. Unno, M., Kawasaki, T., Takahara, H., Heizmann, C.W., and Kizawa, K. (2011). Refined crystal structures of human Ca2+/Zn2+-binding S100A3 protein characterized by two disulfide bridges. J Mol Biol 408, 477–490.CrossRefPubMedGoogle Scholar
  73. van Dieck, J., Teufel, D.P., Jaulent, A.M., Fernandez-Fernandez, M.R., Rutherford, T.J., Wyslouch-Cieszynska, A., and Fersht, A.R. (2009). Posttranslational modifications affect the interaction of S100 proteins with tumor suppressor p53. J Mol Biol 394, 922–930.CrossRefPubMedGoogle Scholar
  74. Vogl, T., Leukert, N., Barczyk, K., Strupat, K., and Roth, J. (2006). Biophysical characterization of S100A8 and S100A9 in the absence and presence of bivalent cations. Biochim Biophys Acta 1763, 1298–1306.CrossRefPubMedGoogle Scholar
  75. Vorum, H., Madsen, P., Rasmussen, H.H., Etzerodt, M., Svendsen, I., Celis, J.E., and Honoré, B. (1996). Expression and divalent cation binding properties of the novel chemotactic inflammatory protein psoriasin. Electrophoresis 17, 1787–1796.CrossRefPubMedGoogle Scholar
  76. Wilder, P.T., Baldisseri, D.M., Udan, R., Vallely, K.M., and Weber, D.J. (2003). Location of the Zn2+-binding site on S100B as determined by NMR spectroscopy and site-directed mutagenesis. Biochemistry 42, 13410–13421.CrossRefPubMedGoogle Scholar
  77. Wilder, P.T., Varney, K.M., Weiss, M.B., Gitti, R.K., and Weber, D.J. (2005). Solution structure of zinc-and calcium-bound rat S100B as determined by nuclear magnetic resonance spectroscopy. Biochemistry 44, 5690–5702.CrossRefPubMedGoogle Scholar
  78. Wolf, R., Howard, O.M., Dong, H.F., Voscopoulos, C., Boeshans, K., Winston, J., Divi, R., Gunsior, M., Goldsmith, P., Ahvazi, B., Chavakis, T., Oppenheim, J.J., and Yuspa, S.H. (2008). Chemotactic activity of S100A7 (Psoriasin) is mediated by the receptor for advanced glycation end products and potentiates inflammation with highly homologous but functionally distinct S100A15. J Immunol 181, 1499–1506.CrossRefPubMedPubMedCentralGoogle Scholar
  79. Zackular, J.P., Chazin, W.J., and Skaar, E.P. (2015). Nutritional immunity: S100 proteins at the host-pathogen interface. J Biol Chem 290, 18991–18998.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Author(s) 2016

Authors and Affiliations

  • Benjamin A. Gilston
    • 1
  • Eric P. Skaar
    • 2
  • Walter J. Chazin
    • 1
    Email author
  1. 1.Departments of Biochemistry and Chemistry, and Center for Structural BiologyVanderbilt UniversityNashvilleUSA
  2. 2.Department of Pathology, Microbiology and ImmunologyVanderbilt University Medical CenterNashvilleUSA

Personalised recommendations