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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.

Brodersen DE, Nyborg J, Kjeldgaard M
Biochemistry 38 1695-704 (1999)
Cited: 76 times
EuropePMC logo PMID: 10026247

Abstract

The crystal structure of human psoriasin (S100A7) in the native, calcium-bound form has been determined from two crystal forms of the protein crystallized with and without divalent zinc. The overall structures of the dimeric protein closely resemble the previously determined holmium-substituted structure. The structures also reveal a zinc-binding site of the protein, which is formed by three histidines and an aspartate residue. Together, these residues coordinate the zinc ion in a way similar to the pattern seen in certain metalloproteases and in particular the collagenase family of proteins. Sequence comparison suggests that this zinc site is present in a number of the remaining members of the S100 family. The structure of S100A7 crystallized in the absence of zinc further shows that loss of zinc results in a reorganization of the adjacent empty and distorted EF-hand loop, causing it to resemble a calcium-loaded EF-hand.

Articles - 3psr mentioned but not cited (4)

  1. Biochemical and Functional Evaluation of the Intramolecular Disulfide Bonds in the Zinc-Chelating Antimicrobial Protein Human S100A7 (Psoriasin). Cunden LS, Brophy MB, Rodriguez GE, Flaxman HA, Nolan EM. Biochemistry 56 5726-5738 (2017)
  2. Bioinorganic Explorations of Zn(II) Sequestration by Human S100 Host-Defense Proteins. Cunden LS, Nolan EM. Biochemistry 57 1673-1680 (2018)
  3. Multiple Evolutionary Origins of Ubiquitous Cu2+ and Zn2+ Binding in the S100 Protein Family. Wheeler LC, Donor MT, Prell JS, Harms MJ. PLoS One 11 e0164740 (2016)
  4. Conservation of Specificity in Two Low-Specificity Proteins. Wheeler LC, Anderson JA, Morrison AJ, Wong CE, Harms MJ. Biochemistry 57 684-695 (2018)


Reviews citing this publication (24)

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  12. Multiple structural states of S100A12: A key to its functional diversity. Moroz OV, Dodson GG, Wilson KS, Lukanidin E, Bronstein IB. Microsc Res Tech 60 581-592 (2003)
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  14. Monitoring of S100 homodimerization and heterodimeric interactions by the yeast two-hybrid system. Deloulme JC, Gentil BJ, Baudier J. Microsc Res Tech 60 560-568 (2003)
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Articles citing this publication (48)

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  2. Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Damo SM, Kehl-Fie TE, Sugitani N, Holt ME, Rathi S, Murphy WJ, Zhang Y, Betz C, Hench L, Fritz G, Skaar EP, Chazin WJ. Proc Natl Acad Sci U S A 110 3841-3846 (2013)
  3. 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. Korndörfer IP, Brueckner F, Skerra A. J Mol Biol 370 887-898 (2007)
  4. Myeloid cell function in MRP-14 (S100A9) null mice. Hobbs JA, May R, Tanousis K, McNeill E, Mathies M, Gebhardt C, Henderson R, Robinson MJ, Hogg N. Mol Cell Biol 23 2564-2576 (2003)
  5. Human calprotectin is an iron-sequestering host-defense protein. Nakashige TG, Zhang B, Krebs C, Nolan EM. Nat Chem Biol 11 765-771 (2015)
  6. MntABC and MntH contribute to systemic Staphylococcus aureus infection by competing with calprotectin for nutrient manganese. Kehl-Fie TE, Zhang Y, Moore JL, Farrand AJ, Hood MI, Rathi S, Chazin WJ, Caprioli RM, Skaar EP. Infect Immun 81 3395-3405 (2013)
  7. 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. Wolf R, Howard OM, Dong HF, Voscopoulos C, Boeshans K, Winston J, Divi R, Gunsior M, Goldsmith P, Ahvazi B, Chavakis T, Oppenheim JJ, Yuspa SH. J Immunol 181 1499-1506 (2008)
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  9. Calcium ion gradients modulate the zinc affinity and antibacterial activity of human calprotectin. Brophy MB, Hayden JA, Nolan EM. J Am Chem Soc 134 18089-18100 (2012)
  10. Both Ca2+ and Zn2+ are essential for S100A12 protein oligomerization and function. Moroz OV, Burkitt W, Wittkowski H, He W, Ianoul A, Novitskaya V, Xie J, Polyakova O, Lednev IK, Shekhtman A, Derrick PJ, Bjoerk P, Foell D, Bronstein IB. BMC Biochem 10 11 (2009)
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  13. Contributions of the S100A9 C-terminal tail to high-affinity Mn(II) chelation by the host-defense protein human calprotectin. Brophy MB, Nakashige TG, Gaillard A, Nolan EM. J Am Chem Soc 135 17804-17817 (2013)
  14. Disulphide-reduced psoriasin is a human apoptosis-inducing broad-spectrum fungicide. Hein KZ, Takahashi H, Tsumori T, Yasui Y, Nanjoh Y, Toga T, Wu Z, Grötzinger J, Jung S, Wehkamp J, Schroeder BO, Schroeder JM, Morita E. Proc Natl Acad Sci U S A 112 13039-13044 (2015)
  15. Divalent metal ion complexes of S100B in the absence and presence of pentamidine. Charpentier TH, Wilder PT, Liriano MA, Varney KM, Pozharski E, MacKerell AD, Coop A, Toth EA, Weber DJ. J Mol Biol 382 56-73 (2008)
  16. Implication of extracellular zinc exclusion by recombinant human calprotectin (MRP8 and MRP14) from target cells in its apoptosis-inducing activity. Yui S, Nakatani Y, Hunter MJ, Chazin WJ, Yamazaki M. Mediators Inflamm 11 165-172 (2002)
  17. The human antimicrobial protein psoriasin acts by permeabilization of bacterial membranes. Michalek M, Gelhaus C, Hecht O, Podschun R, Schröder JM, Leippe M, Grötzinger J. Dev Comp Immunol 33 740-746 (2009)
  18. Implications on zinc binding to S100A2. Koch M, Bhattacharya S, Kehl T, Gimona M, Vasák M, Chazin W, Heizmann CW, Kroneck PM, Fritz G. Biochim Biophys Acta 1773 457-470 (2007)
  19. A structural basis for S100 protein specificity derived from comparative analysis of apo and Ca(2+)-calcyclin. Mäler L, Sastry M, Chazin WJ. J Mol Biol 317 279-290 (2002)
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  25. S100 Proteins in the Innate Immune Response to Pathogens. Kozlyuk N, Monteith AJ, Garcia V, Damo SM, Skaar EP, Chazin WJ. Methods Mol Biol 1929 275-290 (2019)
  26. Detection of psoriasin/S100A7 in the sera of patients with psoriasis. Anderson KS, Wong J, Polyak K, Aronzon D, Enerbäck C. Br J Dermatol 160 325-332 (2009)
  27. NMR structure of a concatemer of the first and second ligand-binding modules of the human low-density lipoprotein receptor. Kurniawan ND, Atkins AR, Bieri S, Brown CJ, Brereton IM, Kroon PA, Smith R. Protein Sci 9 1282-1293 (2000)
  28. The Structure of the RAGE:S100A6 Complex Reveals a Unique Mode of Homodimerization for S100 Proteins. Yatime L, Betzer C, Jensen RK, Mortensen S, Jensen PH, Andersen GR. Structure 24 2043-2052 (2016)
  29. Zinc-dependent interaction between dishevelled and the Drosophila Wnt antagonist naked cuticle. Rousset R, Wharton KA, Zimmermann G, Scott MP. J Biol Chem 277 49019-49026 (2002)
  30. Structural interplay between calcium(II) and copper(II) binding to S100A13 protein. Arnesano F, Banci L, Bertini I, Fantoni A, Tenori L, Viezzoli MS. Angew Chem Int Ed Engl 44 6341-6344 (2005)
  31. Crystal structure of Ca2+ -free S100A2 at 1.6-A resolution. Koch M, Diez J, Fritz G. J Mol Biol 378 933-942 (2008)
  32. Differential role of psoriasin (S100A7) in estrogen receptor α positive and negative breast cancer cells occur through actin remodeling. Sneh A, Deol YS, Ganju A, Shilo K, Rosol TJ, Nasser MW, Ganju RK. Breast Cancer Res Treat 138 727-739 (2013)
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  35. Structural characterization of human S100A16, a low-affinity calcium binder. Babini E, Bertini I, Borsi V, Calderone V, Hu X, Luchinat C, Parigi G. J Biol Inorg Chem 16 243-256 (2011)
  36. Structural characterization of S100A15 reveals a novel zinc coordination site among S100 proteins and altered surface chemistry with functional implications for receptor binding. Murray JI, Tonkin ML, Whiting AL, Peng F, Farnell B, Cullen JT, Hof F, Boulanger MJ. BMC Struct Biol 12 16 (2012)
  37. Yersiniabactin contributes to overcoming zinc restriction during Yersinia pestis infection of mammalian and insect hosts. Price SL, Vadyvaloo V, DeMarco JK, Brady A, Gray PA, Kehl-Fie TE, Garneau-Tsodikova S, Perry RD, Lawrenz MB. Proc Natl Acad Sci U S A 118 e2104073118 (2021)
  38. Human S100A3 tetramerization propagates Ca(2+)/Zn(2+) binding states. Kizawa K, Jinbo Y, Inoue T, Takahara H, Unno M, Heizmann CW, Izumi Y. Biochim Biophys Acta 1833 1712-1719 (2013)
  39. Expression of S100 family proteins in neonatal rats with sepsis and its significance. Huang H, Tu L. Int J Clin Exp Pathol 8 1631-1639 (2015)
  40. Refined crystal structures of human Ca(2+)/Zn(2+)-binding S100A3 protein characterized by two disulfide bridges. Unno M, Kawasaki T, Takahara H, Heizmann CW, Kizawa K. J Mol Biol 408 477-490 (2011)
  41. Ca(II) and Zn(II) Cooperate To Modulate the Structure and Self-Assembly of S100A12. Wang Q, Aleshintsev A, Bolton D, Zhuang J, Brenowitz M, Gupta R. Biochemistry 58 2269-2281 (2019)
  42. An orthologue of the host-defense protein psoriasin (S100A7) is expressed in frog skin. Matthijs S, Hernalsteens JP, Roelants K. Dev Comp Immunol 67 395-403 (2017)
  43. Crystal structure study on human S100A13 at 2.0 A resolution. Li M, Zhang PF, Pan XW, Chang WR. Biochem Biophys Res Commun 356 616-621 (2007)
  44. In solution cation-induced secondary and tertiary structure alterations of human calprotectin. Imani M, Bahrami Y, Jaliani HZ, Ardestani SK. Protein J 33 465-473 (2014)
  45. Optimal Mutant Model of Human S100A3 Protein Citrullinated at Arg51 by Peptidylarginine Deiminase Type III and Its Solution Structural Properties. Ite K, Yonezawa K, Kitanishi K, Shimizu N, Unno M. ACS Omega 5 4032-4042 (2020)
  46. Spectroscopic and computational investigations of Cobalt(II) binding to the innate immune protein human calprotectin. Killian MM, Brophy MB, Nolan EM, Brunold TC. J Biol Inorg Chem (2024)
  47. Structural mechanism of human oncochannel TRPV6 inhibition by the natural phytoestrogen genistein. Neuberger A, Trofimov YA, Yelshanskaya MV, Nadezhdin KD, Krylov NA, Efremov RG, Sobolevsky AI. Nat Commun 14 2659 (2023)
  48. The S100A7 nuclear interactors in autoimmune diseases: a coevolutionary study in mammals. D'Amico F, Skarmoutsou E, Libra M. Immunogenetics 74 271-284 (2022)


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