1jwd Citations

A structural basis for S100 protein specificity derived from comparative analysis of apo and Ca(2+)-calcyclin.

J Mol Biol 317 279-90 (2002)
Cited: 34 times
EuropePMC logo PMID: 11902843

Abstract

Calcyclin is a homodimeric protein belonging to the S100 subfamily of EF-hand Ca(2+)-binding proteins, which function in Ca(2+) signal transduction processes. A refined high-resolution solution structure of Ca(2+)-bound rabbit calcyclin has been determined by heteronuclear solution NMR. In order to understand the Ca(2+)-induced structural changes in S100 proteins, in-depth comparative structural analyses were used to compare the apo and Ca(2+)-bound states of calcyclin, the closely related S100B, and the prototypical Ca(2+)-sensor protein calmodulin. Upon Ca(2+) binding, the position and orientation of helix III in the second EF-hand is altered, whereas the rest of the protein, including the dimer interface, remains virtually unchanged. This Ca(2+)-induced structural change is much less drastic than the "opening" of the globular EF-hand domains that occurs in classical Ca(2+) sensors, such as calmodulin. Using homology models of calcyclin based on S100B, a binding site in calcyclin has been proposed for the N-terminal domain of annexin XI and the C-terminal domain of the neuronal calcyclin-binding protein. The structural basis for the specificity of S100 proteins is discussed in terms of the variation in sequence of critical contact residues in the common S100 target-binding site.

Articles - 1jwd mentioned but not cited (2)

  1. Structure of Ca2+-bound S100A4 and its interaction with peptides derived from nonmuscle myosin-IIA. Malashkevich VN, Varney KM, Garrett SC, Wilder PT, Knight D, Charpentier TH, Ramagopal UA, Almo SC, Weber DJ, Bresnick AR. Biochemistry 47 5111-5126 (2008)
  2. 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 (8)

  1. Calcium-dependent and -independent interactions of the S100 protein family. Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS. Biochem J 396 201-214 (2006)
  2. Structural basis for diversity of the EF-hand calcium-binding proteins. Grabarek Z. J Mol Biol 359 509-525 (2006)
  3. Target selectivity in EF-hand calcium binding proteins. Bhattacharya S, Bunick CG, Chazin WJ. Biochim Biophys Acta 1742 69-79 (2004)
  4. Molecular mechanisms of S100-target protein interactions. Zimmer DB, Wright Sadosky P, Weber DJ. Microsc Res Tech 60 552-559 (2003)
  5. S100-annexin complexes--structural insights. Rintala-Dempsey AC, Rezvanpour A, Shaw GS. FEBS J 275 4956-4966 (2008)
  6. Binding of transition metals to S100 proteins. Gilston BA, Skaar EP, Chazin WJ. Sci China Life Sci 59 792-801 (2016)
  7. 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)
  8. Recent Advances in Molecular and Cellular Functions of S100A10. Okura GC, Bharadwaj AG, Waisman DM. Biomolecules 13 1450 (2023)

Articles citing this publication (24)

  1. The extracellular region of the receptor for advanced glycation end products is composed of two independent structural units. Dattilo BM, Fritz G, Leclerc E, Kooi CW, Heizmann CW, Chazin WJ. Biochemistry 46 6957-6970 (2007)
  2. S100 protein translocation in response to extracellular S100 is mediated by receptor for advanced glycation endproducts in human endothelial cells. Hsieh HL, Schäfer BW, Weigle B, Heizmann CW. Biochem Biophys Res Commun 316 949-959 (2004)
  3. Relating form and function of EF-hand calcium binding proteins. Chazin WJ. Acc Chem Res 44 171-179 (2011)
  4. 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 391 536-551 (2009)
  5. Solution NMR structure of the C-terminal EF-hand domain of human cardiac sodium channel NaV1.5. Chagot B, Potet F, Balser JR, Chazin WJ. J Biol Chem 284 6436-6445 (2009)
  6. Structure of the S100A6 complex with a fragment from the C-terminal domain of Siah-1 interacting protein: a novel mode for S100 protein target recognition. Lee YT, Dimitrova YN, Schneider G, Ridenour WB, Bhattacharya S, Soss SE, Caprioli RM, Filipek A, Chazin WJ. Biochemistry 47 10921-10932 (2008)
  7. Unmasking the annexin I interaction from the structure of Apo-S100A11. Dempsey AC, Walsh MP, Shaw GS. Structure 11 887-897 (2003)
  8. The Calcium-Dependent Interaction of S100B with Its Protein Targets. Zimmer DB, Weber DJ. Cardiovasc Psychiatry Neurol 2010 728052 (2010)
  9. The crystal structure of metal-free human EF-hand protein S100A3 at 1.7-A resolution. Fritz G, Mittl PR, Vasak M, Grutter MG, Heizmann CW. J Biol Chem 277 33092-33098 (2002)
  10. 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)
  11. Structural and functional characterization of recombinant mouse annexin A11: influence of calcium binding. Lecona E, Turnay J, Olmo N, Guzmán-Aránguez A, Morgan RO, Fernandez MP, Lizarbe MA. Biochem J 373 437-449 (2003)
  12. Letter NMR structure of the Apo-S100P protein. Lee YC, Volk DE, Thiviyanathan V, Kleerekoper Q, Gribenko AV, Zhang S, Gorenstein DG, Makhatadze GI, Luxon BA. J Biomol NMR 29 399-402 (2004)
  13. Refinement of the solution structure and dynamic properties of Ca(2+)-bound rat S100B. Wright NT, Inman KG, Levine JA, Cannon BR, Varney KM, Weber DJ. J Biomol NMR 42 279-286 (2008)
  14. Analysis of the structure of human apo-S100B at low temperature indicates a unimodal conformational distribution is adopted by calcium-free S100 proteins. Malik S, Revington M, Smith SP, Shaw GS. Proteins 73 28-42 (2008)
  15. Solution structure and dynamics of S100A5 in the apo and Ca2+-bound states. Bertini I, Das Gupta S, Hu X, Karavelas T, Luchinat C, Parigi G, Yuan J. J Biol Inorg Chem 14 1097-1107 (2009)
  16. Solution structure and dynamics of human S100A14. Bertini I, Borsi V, Cerofolini L, Das Gupta S, Fragai M, Luchinat C. J Biol Inorg Chem 18 183-194 (2013)
  17. 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)
  18. Three-dimensional solution structure of a unique S100 protein. Sivaraja V, Kumar TK, Prudovsky I, Yu C. Biochem Biophys Res Commun 335 1140-1148 (2005)
  19. Characterization of the tissue-specific expression of the s100P gene which encodes an EF-hand Ca2+-binding protein. Jin G, Wang S, Hu X, Jing Z, Chen J, Ying K, Xie Y, Mao Y. Mol Biol Rep 30 243-248 (2003)
  20. Interaction between chromaffin and sustentacular cells in adrenal medulla of viscacha (Lagostomus maximus maximus). Rodriguez H, Filippa V, Mohamed F, Dominguez S, Scardapane L. Anat Histol Embryol 36 182-185 (2007)
  21. Theoretical study on binding of S100B protein. Gieldon A, Mori M, Del Conte R. J Mol Model 13 1123-1131 (2007)
  22. S100A4 inhibits cell proliferation by interfering with the S100A1-RAGE V domain. Khan MI, Yuan T, Chou RH, Yu C. PLoS One 14 e0212299 (2019)
  23. Probing the interaction of distamycin A with S100β: the "unexpected" ability of S100β to bind to DNA-binding ligands. Cerofolini L, Amato J, Borsi V, Pagano B, Randazzo A, Fragai M. J Mol Recognit 28 376-384 (2015)
  24. Comparative analysis of the physical properties of murine and human S100A7: Insight into why zinc piracy is mediated by human but not murine S100A7. Harrison SA, Naretto A, Balakrishnan S, Perera YR, Chazin WJ. J Biol Chem 299 105292 (2023)


Related citations provided by authors (3)

  1. High Resolution Solution Structure of Apo Calcyclin and Structural Variations in the S100 Family of Calcium-binding Proteins.. Maler L, Potts BCM, Chazin WJ J. Biomol. NMR 13 233-247 (1999)
  2. The Three-dimenisonal Structure of Ca(2+)-bound Calcyclin: Implications for Ca(2+)-signal Transduction by S100 Proteins.. Sastry M, Ketchem RR, Crescenzi O, Weber C, Lubienski MJ, Hidaka H, Chazin WJ Structure 6 223-231 (1998)
  3. The Structure of Calcyclin Reveals a Novel Homodimeric Fold for S100 Ca(2+)-binding Proteins.. Potts BC, Smith J, Akke M, Macke TJ, Okazaki K, Hidaka H, Chase DA, Chazin WJ Nat. Struct. Biol. 2 790-796 (1995)