Structural basis of the Ca2+-dependent association between S100C (S100A11) and its target, the N-terminal part of annexin I

Stéphane Réty, Dirk Osterloh, Jean Philippe Arié, Sébastien Tabaries, Joachim Seeman, Françoise Russo-Marie, Volker Gerke, Anita Lewit-Bentley

Research output: Contribution to journalArticle

141 Citations (Scopus)

Abstract

Background: S100C (S100A11) is a member of the S100 calcium-binding protein family, the function of which is not yet entirely clear, but may include cytoskeleton assembly and dynamics. S100 proteins consist of two EF- hand calcium-binding motifs, connected by a flexible loop. Like several other members of the family, S100C forms a homodimer. A number of S100 proteins form complexes with annexins, another family of calcium-binding proteins that also bind to phospholipids. Structural studies have been undertaken to understand the basis of these interactions. Results: We have solved the crystal structure of a complex of calcium-loaded S100C with a synthetic peptide that corresponds to the first 14 residues of the annexin I N terminus at 2.3 Å resolution. We find a stoichiometry of one peptide per S100C monomer, the entire complex structure consisting of two peptides per S100C dimer. Each peptide, however, interacts with both monomers of the S100C dimer. The two S100C molecules of the dimer are linked by a disulphide bridge. The structure is surprisingly close to that of the p11-annexin II N- terminal peptide complex solved previously. We have performed competition experiments to try to understand the specificity of the S100-annexin interaction. Conclusions: By solving the structure of a second annexin N terminus-S100 protein complex, we confirmed a novel mode of interaction of S100 proteins with their target peptides; there is a one-to-one stoichiometry, where the dimeric structure of the S100 protein is, nevertheless, essential for complex formation. Our structure can provide a model for a Ca2+-regulated annexin I-S100C heterotetramer, possibly involved in crosslinking membrane surfaces or organising membranes during certain fusion events.

Original languageEnglish (US)
Pages (from-to)175-184
Number of pages10
JournalStructure
Volume8
Issue number2
DOIs
StatePublished - Feb 1 2000

Fingerprint

Annexin A1
S100 Proteins
Annexins
Peptides
Calcium-Binding Proteins
Annexin A2
Calcium
EF Hand Motifs
Membranes
Cytoskeleton
Disulfides
Phospholipids

Keywords

  • Calcium-binding protein
  • Crystal structure
  • Disulphide-linked dimer
  • Protein-peptide complex
  • Protein-protein recognition

ASJC Scopus subject areas

  • Molecular Biology
  • Structural Biology

Cite this

Structural basis of the Ca2+-dependent association between S100C (S100A11) and its target, the N-terminal part of annexin I. / Réty, Stéphane; Osterloh, Dirk; Arié, Jean Philippe; Tabaries, Sébastien; Seeman, Joachim; Russo-Marie, Françoise; Gerke, Volker; Lewit-Bentley, Anita.

In: Structure, Vol. 8, No. 2, 01.02.2000, p. 175-184.

Research output: Contribution to journalArticle

Réty, S, Osterloh, D, Arié, JP, Tabaries, S, Seeman, J, Russo-Marie, F, Gerke, V & Lewit-Bentley, A 2000, 'Structural basis of the Ca2+-dependent association between S100C (S100A11) and its target, the N-terminal part of annexin I', Structure, vol. 8, no. 2, pp. 175-184. https://doi.org/10.1016/S0969-2126(00)00093-9
Réty, Stéphane ; Osterloh, Dirk ; Arié, Jean Philippe ; Tabaries, Sébastien ; Seeman, Joachim ; Russo-Marie, Françoise ; Gerke, Volker ; Lewit-Bentley, Anita. / Structural basis of the Ca2+-dependent association between S100C (S100A11) and its target, the N-terminal part of annexin I. In: Structure. 2000 ; Vol. 8, No. 2. pp. 175-184.
@article{d51ca98898dc49cbbb05c44625dd0fa6,
title = "Structural basis of the Ca2+-dependent association between S100C (S100A11) and its target, the N-terminal part of annexin I",
abstract = "Background: S100C (S100A11) is a member of the S100 calcium-binding protein family, the function of which is not yet entirely clear, but may include cytoskeleton assembly and dynamics. S100 proteins consist of two EF- hand calcium-binding motifs, connected by a flexible loop. Like several other members of the family, S100C forms a homodimer. A number of S100 proteins form complexes with annexins, another family of calcium-binding proteins that also bind to phospholipids. Structural studies have been undertaken to understand the basis of these interactions. Results: We have solved the crystal structure of a complex of calcium-loaded S100C with a synthetic peptide that corresponds to the first 14 residues of the annexin I N terminus at 2.3 {\AA} resolution. We find a stoichiometry of one peptide per S100C monomer, the entire complex structure consisting of two peptides per S100C dimer. Each peptide, however, interacts with both monomers of the S100C dimer. The two S100C molecules of the dimer are linked by a disulphide bridge. The structure is surprisingly close to that of the p11-annexin II N- terminal peptide complex solved previously. We have performed competition experiments to try to understand the specificity of the S100-annexin interaction. Conclusions: By solving the structure of a second annexin N terminus-S100 protein complex, we confirmed a novel mode of interaction of S100 proteins with their target peptides; there is a one-to-one stoichiometry, where the dimeric structure of the S100 protein is, nevertheless, essential for complex formation. Our structure can provide a model for a Ca2+-regulated annexin I-S100C heterotetramer, possibly involved in crosslinking membrane surfaces or organising membranes during certain fusion events.",
keywords = "Calcium-binding protein, Crystal structure, Disulphide-linked dimer, Protein-peptide complex, Protein-protein recognition",
author = "St{\'e}phane R{\'e}ty and Dirk Osterloh and Ari{\'e}, {Jean Philippe} and S{\'e}bastien Tabaries and Joachim Seeman and Fran{\cc}oise Russo-Marie and Volker Gerke and Anita Lewit-Bentley",
year = "2000",
month = "2",
day = "1",
doi = "10.1016/S0969-2126(00)00093-9",
language = "English (US)",
volume = "8",
pages = "175--184",
journal = "Structure with Folding & design",
issn = "0969-2126",
publisher = "Cell Press",
number = "2",

}

TY - JOUR

T1 - Structural basis of the Ca2+-dependent association between S100C (S100A11) and its target, the N-terminal part of annexin I

AU - Réty, Stéphane

AU - Osterloh, Dirk

AU - Arié, Jean Philippe

AU - Tabaries, Sébastien

AU - Seeman, Joachim

AU - Russo-Marie, Françoise

AU - Gerke, Volker

AU - Lewit-Bentley, Anita

PY - 2000/2/1

Y1 - 2000/2/1

N2 - Background: S100C (S100A11) is a member of the S100 calcium-binding protein family, the function of which is not yet entirely clear, but may include cytoskeleton assembly and dynamics. S100 proteins consist of two EF- hand calcium-binding motifs, connected by a flexible loop. Like several other members of the family, S100C forms a homodimer. A number of S100 proteins form complexes with annexins, another family of calcium-binding proteins that also bind to phospholipids. Structural studies have been undertaken to understand the basis of these interactions. Results: We have solved the crystal structure of a complex of calcium-loaded S100C with a synthetic peptide that corresponds to the first 14 residues of the annexin I N terminus at 2.3 Å resolution. We find a stoichiometry of one peptide per S100C monomer, the entire complex structure consisting of two peptides per S100C dimer. Each peptide, however, interacts with both monomers of the S100C dimer. The two S100C molecules of the dimer are linked by a disulphide bridge. The structure is surprisingly close to that of the p11-annexin II N- terminal peptide complex solved previously. We have performed competition experiments to try to understand the specificity of the S100-annexin interaction. Conclusions: By solving the structure of a second annexin N terminus-S100 protein complex, we confirmed a novel mode of interaction of S100 proteins with their target peptides; there is a one-to-one stoichiometry, where the dimeric structure of the S100 protein is, nevertheless, essential for complex formation. Our structure can provide a model for a Ca2+-regulated annexin I-S100C heterotetramer, possibly involved in crosslinking membrane surfaces or organising membranes during certain fusion events.

AB - Background: S100C (S100A11) is a member of the S100 calcium-binding protein family, the function of which is not yet entirely clear, but may include cytoskeleton assembly and dynamics. S100 proteins consist of two EF- hand calcium-binding motifs, connected by a flexible loop. Like several other members of the family, S100C forms a homodimer. A number of S100 proteins form complexes with annexins, another family of calcium-binding proteins that also bind to phospholipids. Structural studies have been undertaken to understand the basis of these interactions. Results: We have solved the crystal structure of a complex of calcium-loaded S100C with a synthetic peptide that corresponds to the first 14 residues of the annexin I N terminus at 2.3 Å resolution. We find a stoichiometry of one peptide per S100C monomer, the entire complex structure consisting of two peptides per S100C dimer. Each peptide, however, interacts with both monomers of the S100C dimer. The two S100C molecules of the dimer are linked by a disulphide bridge. The structure is surprisingly close to that of the p11-annexin II N- terminal peptide complex solved previously. We have performed competition experiments to try to understand the specificity of the S100-annexin interaction. Conclusions: By solving the structure of a second annexin N terminus-S100 protein complex, we confirmed a novel mode of interaction of S100 proteins with their target peptides; there is a one-to-one stoichiometry, where the dimeric structure of the S100 protein is, nevertheless, essential for complex formation. Our structure can provide a model for a Ca2+-regulated annexin I-S100C heterotetramer, possibly involved in crosslinking membrane surfaces or organising membranes during certain fusion events.

KW - Calcium-binding protein

KW - Crystal structure

KW - Disulphide-linked dimer

KW - Protein-peptide complex

KW - Protein-protein recognition

UR - http://www.scopus.com/inward/record.url?scp=0038734222&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0038734222&partnerID=8YFLogxK

U2 - 10.1016/S0969-2126(00)00093-9

DO - 10.1016/S0969-2126(00)00093-9

M3 - Article

C2 - 10673436

AN - SCOPUS:0038734222

VL - 8

SP - 175

EP - 184

JO - Structure with Folding & design

JF - Structure with Folding & design

SN - 0969-2126

IS - 2

ER -