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The crystal structures of human S100A12 in apo form and in complex with zinc: new insights into S100A12 oligomerisation.

Moroz OV, Blagova EV, Wilkinson AJ, Wilson KS, Bronstein IB
J Mol Biol 391 536-51 (2009)
Related entries: 1e8a, 1gqm, 1odb, 2wc8, 2wce, 2wcf

Cited: 64 times
EuropePMC logo PMID: 19501594

Abstract

The functions of the members of the S100 family of EF-hand proteins are modulated by calcium and, in a number of cases, by zinc or copper. One such protein is S100A12, which is implicated in inflammation and host-parasite responses. Previously, we reported the structures of human S100A12 in both low (dimeric) and high (hexameric) calcium forms and, in addition, that of a complex with copper and calcium. Here we report the crystal structures of the metal-free apo form of human S100A12 at 1.77 A resolution and of the zinc complex in two crystal forms (P2(1)2(1)2(1) and F222) to 1.88 A and 1.73 A resolution, respectively. These are the first structures of a zinc-only complex of an S100 protein to be determined. The zinc complex structure shows significant differences from those of both calcium-loaded and apo-S100A12 structures, and comparisons suggest an explanation for the zinc-induced 1500-fold increase in calcium affinity. In addition, the new structures provide insight into the role of zinc-calcium interplay in the transition of S100A12 from a dimer through a tetramer to a hexamer. The role of both zinc and calcium in target binding by S100A12 during host-parasite responses is confirmed by experiments with paramyosin from the tropical parasites Onchocerca volvulus and Brugia malayi.

Articles - 2wcb mentioned but not cited (7)

  1. Calcium Ions Tune the Zinc-Sequestering Properties and Antimicrobial Activity of Human S100A12. Cunden LS, Gaillard A, Nolan EM. Chem Sci 7 1338-1348 (2016)
  2. Conservation of Specificity in Two Low-Specificity Proteins. Wheeler LC, Anderson JA, Morrison AJ, Wong CE, Harms MJ. Biochemistry 57 684-695 (2018)
  3. 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)
  4. Characterization and engineering of S100A12-heparan sulfate interactions. Zhang X, Ong C, Su G, Liu J, Xu D. Glycobiology 30 463-473 (2020)
  5. Influence of nonenzymatic posttranslational modifications on constitution, oligomerization and receptor binding of S100A12. Augner K, Eichler J, Utz W, Pischetsrieder M. PLoS One 9 e113418 (2014)
  6. Calcium Regulates S100A12 Zinc Sequestration by Limiting Structural Variations. Wang Q, Aleshintsev A, Jose AN, Aramini JM, Gupta R. Chembiochem 21 1372-1382 (2020)
  7. Bioinformatics-based investigation on the genetic influence between SARS-CoV-2 infections and idiopathic pulmonary fibrosis (IPF) diseases, and drug repurposing. Islam MA, Kibria MK, Hossen MB, Reza MS, Tasmia SA, Tuly KF, Mosharof MP, Kabir SR, Kabir MH, Mollah MNH. Sci Rep 13 4685 (2023)


Reviews citing this publication (17)

  1. Functions of S100 proteins. Donato R, Cannon BR, Sorci G, Riuzzi F, Hsu K, Weber DJ, Geczy CL. Curr Mol Med 13 24-57 (2013)
  2. Nutritional Immunity: S100 Proteins at the Host-Pathogen Interface. Zackular JP, Chazin WJ, Skaar EP. J Biol Chem 290 18991-18998 (2015)
  3. S100 Calgranulins in inflammatory arthritis. Perera C, McNeil HP, Geczy CL. Immunol Cell Biol 88 41-49 (2010)
  4. Phagocyte-derived S100 proteins in autoinflammation: putative role in pathogenesis and usefulness as biomarkers. Kessel C, Holzinger D, Foell D. Clin Immunol 147 229-241 (2013)
  5. Transition Metal Sequestration by the Host-Defense Protein Calprotectin. Zygiel EM, Nolan EM. Annu Rev Biochem 87 621-643 (2018)
  6. Insights into modulation of calcium signaling by magnesium in calmodulin, troponin C and related EF-hand proteins. Grabarek Z. Biochim Biophys Acta 1813 913-921 (2011)
  7. Natural and amyloid self-assembly of S100 proteins: structural basis of functional diversity. Fritz G, Botelho HM, Morozova-Roche LA, Gomes CM. FEBS J 277 4578-4590 (2010)
  8. S100 proteins in cartilage: role in arthritis. Yammani RR. Biochim Biophys Acta 1822 600-606 (2012)
  9. Binding of transition metals to S100 proteins. Gilston BA, Skaar EP, Chazin WJ. Sci China Life Sci 59 792-801 (2016)
  10. The role of zinc in the S100 proteins: insights from the X-ray structures. Moroz OV, Wilson KS, Bronstein IB. Amino Acids 41 761-772 (2011)
  11. The impact of metal availability on immune function during infection. Monteith AJ, Skaar EP. Trends Endocrinol Metab 32 916-928 (2021)
  12. S100A12 in Digestive Diseases and Health: A Scoping Review. Carvalho A, Lu J, Francis JD, Moore RE, Haley KP, Doster RS, Townsend SD, Johnson JG, Damo SM, Gaddy JA. Gastroenterol Res Pract 2020 2868373 (2020)
  13. Host-imposed manganese starvation of invading pathogens: two routes to the same destination. Morey JR, McDevitt CA, Kehl-Fie TE. Biometals 28 509-519 (2015)
  14. Metal sequestration by S100 proteins in chemically diverse environments. Rosen T, Wang KA, Nolan EM. Trends Microbiol 30 654-664 (2022)
  15. Discerning the promising binding sites of S100/calgranulins and their therapeutic potential in atherosclerosis. Singh H, Rai V, Agrawal DK. Expert Opin Ther Pat 31 1045-1057 (2021)
  16. Introduction to molecular replacement: a time perspective. Dodson E. Acta Crystallogr D Struct Biol 77 867-879 (2021)
  17. Pathogenic role of S100 proteins in psoriasis. Liang H, Li J, Zhang K. Front Immunol 14 1191645 (2023)

Articles citing this publication (40)

  1. 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)
  2. Restoration of anti-Aspergillus defense by neutrophil extracellular traps in human chronic granulomatous disease after gene therapy is calprotectin-dependent. Bianchi M, Niemiec MJ, Siler U, Urban CF, Reichenbach J. J Allergy Clin Immunol 127 1243-52.e7 (2011)
  3. Human calprotectin is an iron-sequestering host-defense protein. Nakashige TG, Zhang B, Krebs C, Nolan EM. Nat Chem Biol 11 765-771 (2015)
  4. 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)
  5. ANTI-INFECTIVE PROTECTIVE PROPERTIES OF S100 CALGRANULINS. Hsu K, Champaiboon C, Guenther BD, Sorenson BS, Khammanivong A, Ross KF, Geczy CL, Herzberg MC. Antiinflamm Antiallergy Agents Med Chem 8 290-305 (2009)
  6. 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)
  7. Zinc piracy as a mechanism of Neisseria meningitidis for evasion of nutritional immunity. Stork M, Grijpstra J, Bos MP, Mañas Torres C, Devos N, Poolman JT, Chazin WJ, Tommassen J. PLoS Pathog 9 e1003733 (2013)
  8. 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)
  9. Manganese binding properties of human calprotectin under conditions of high and low calcium: X-ray crystallographic and advanced electron paramagnetic resonance spectroscopic analysis. Gagnon DM, Brophy MB, Bowman SE, Stich TA, Drennan CL, Britt RD, Nolan EM. J Am Chem Soc 137 3004-3016 (2015)
  10. Phenothiazines inhibit S100A4 function by inducing protein oligomerization. Malashkevich VN, Dulyaninova NG, Ramagopal UA, Liriano MA, Varney KM, Knight D, Brenowitz M, Weber DJ, Almo SC, Bresnick AR. Proc Natl Acad Sci U S A 107 8605-8610 (2010)
  11. The Human Antimicrobial Protein Calgranulin C Participates in Control of Helicobacter pylori Growth and Regulation of Virulence. Haley KP, Delgado AG, Piazuelo MB, Mortensen BL, Correa P, Damo SM, Chazin WJ, Skaar EP, Gaddy JA. Infect Immun 83 2944-2956 (2015)
  12. X-ray structures of magnesium and manganese complexes with the N-terminal domain of calmodulin: insights into the mechanism and specificity of metal ion binding to an EF-hand. Senguen FT, Grabarek Z. Biochemistry 51 6182-6194 (2012)
  13. Carboxylated N-glycans on RAGE promote S100A12 binding and signaling. Srikrishna G, Nayak J, Weigle B, Temme A, Foell D, Hazelwood L, Olsson A, Volkmann N, Hanein D, Freeze HH. J Cell Biochem 110 645-659 (2010)
  14. 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)
  15. The calcium-dependent interaction between S100B and the mitochondrial AAA ATPase ATAD3A and the role of this complex in the cytoplasmic processing of ATAD3A. Gilquin B, Cannon BR, Hubstenberger A, Moulouel B, Falk E, Merle N, Assard N, Kieffer S, Rousseau D, Wilder PT, Weber DJ, Baudier J. Mol Cell Biol 30 2724-2736 (2010)
  16. The crystal structures of human S100B in the zinc- and calcium-loaded state at three pH values reveal zinc ligand swapping. Ostendorp T, Diez J, Heizmann CW, Fritz G. Biochim Biophys Acta 1813 1083-1091 (2011)
  17. 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)
  18. The Host Antimicrobial Protein Calgranulin C Participates in the Control of Campylobacter jejuni Growth via Zinc Sequestration. Shank JM, Kelley BR, Jackson JW, Tweedie JL, Franklin D, Damo SM, Gaddy JA, Murphy CN, Johnson JG. Infect Immun 86 e00234-18 (2018)
  19. 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)
  20. Crystal structure of human S100A8 in complex with zinc and calcium. Lin H, Andersen GR, Yatime L. BMC Struct Biol 16 8 (2016)
  21. Expression of Calgranulin Genes S100A8, S100A9 and S100A12 Is Modulated by n-3 PUFA during Inflammation in Adipose Tissue and Mononuclear Cells. Shah RD, Xue C, Zhang H, Tuteja S, Li M, Reilly MP, Ferguson JF. PLoS One 12 e0169614 (2017)
  22. A Method for Selective Depletion of Zn(II) Ions from Complex Biological Media and Evaluation of Cellular Consequences of Zn(II) Deficiency. Richardson CER, Cunden LS, Butty VL, Nolan EM, Lippard SJ, Shoulders MD. J Am Chem Soc 140 2413-2416 (2018)
  23. Blocking the Interactions between Calcium-Bound S100A12 Protein and the V Domain of RAGE Using Tranilast. Chiou JW, Fu B, Chou RH, Yu C. PLoS One 11 e0162000 (2016)
  24. Calcium ion-induced formation of β-sheet/-turn structure leading to alteration of osteogenic activity of bone morphogenetic protein-2. Zhang W, He H, Tian Y, Gan Q, Zhang J, Yuan Y, Liu C. Sci Rep 5 12694 (2015)
  25. Intrinsically disordered and aggregation prone regions underlie β-aggregation in S100 proteins. Carvalho SB, Botelho HM, Leal SS, Cardoso I, Fritz G, Gomes CM. PLoS One 8 e76629 (2013)
  26. 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)
  27. 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)
  28. S100A12 suppresses pro-inflammatory, but not pro-thrombotic functions of serum amyloid A. Chung YM, Goyette J, Tedla N, Hsu K, Geczy CL. PLoS One 8 e62372 (2013)
  29. Avian MRP126 Restricts Microbial Growth through Ca(II)-Dependent Zn(II) Sequestration. Bozzi AT, Nolan EM. Biochemistry 59 802-817 (2020)
  30. Expression, Purification, and Antimicrobial Activity of S100A12. Jackson E, Little S, Franklin DS, Gaddy JA, Damo SM. J Vis Exp (2017)
  31. In silico assessment of S100A12 monomer and dimer structural dynamics: implications for the understanding of its metal-induced conformational changes. Reis RA, Bortot LO, Caliri A. J Biol Inorg Chem 19 1113-1120 (2014)
  32. Solution structure of human Ca(2+)-bound S100A12. Hung KW, Hsu CC, Yu C. J Biomol NMR 57 313-318 (2013)
  33. Human S100A5 binds Ca2+ and Cu2+ independently. Wheeler LC, Harms MJ. BMC Biophys 10 8 (2017)
  34. Membrane interactions of S100A12 (Calgranulin C). Garcia AF, Lopes JL, Costa-Filho AJ, Wallace BA, Araujo AP. PLoS One 8 e82555 (2013)
  35. 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)
  36. Dynamic regulation of Zn(II) sequestration by calgranulin C. Wang Q, Kuci D, Bhattacharya S, Hadden-Perilla JA, Gupta R. Protein Sci 31 e4403 (2022)
  37. Effect of monovalent ion binding on molecular dynamics of the S100-family calcium-binding protein calbindin D9k. Thapa M, Johnson E, Rance M. J Comput Chem 40 1936-1945 (2019)
  38. S100A12 promotes Mn(II) binding to pneumococcal PsaA and staphylococcal MntC by Zn(II) sequestration. Rosen T, Nolan EM. J Inorg Biochem 233 111862 (2022)
  39. Solving the crystal structure of human calcium-free S100Z: the siege and conquer of one of the last S100 family strongholds. Calderone V, Fragai M, Gallo G, Luchinat C. J Biol Inorg Chem 22 519-526 (2017)
  40. 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)


Related citations provided by authors (3)

  1. The three-dimensional structure of human S100A12.. Moroz OV, Antson AA, Murshudov GN, Maitland NJ, Dodson GG, Wilson KS, Skibshøj I, Lukanidin EM, Bronstein IB Acta Crystallogr D Biol Crystallogr 57 20-9 (2001)
  2. Structure of the human S100A12-copper complex: implications for host-parasite defence.. Moroz OV, Antson AA, Grist SJ, Maitland NJ, Dodson GG, Wilson KS, Lukanidin E, Bronstein IB Acta Crystallogr D Biol Crystallogr 59 859-67 (2003)
  3. The structure of S100A12 in a hexameric form and its proposed role in receptor signalling.. Moroz OV, Antson AA, Dodson EJ, Burrell HJ, Grist SJ, Lloyd RM, Maitland NJ, Dodson GG, Wilson KS, Lukanidin E, Bronstein IB Acta Crystallogr D Biol Crystallogr 58 407-13 (2002)

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