Affinage

S100A1

Protein S100-A1 · UniProt P23297

Length
94 aa
Mass
10.5 kDa
Annotated
2026-06-10
100 papers in source corpus 45 papers cited in narrative 44 extracted findings
Cross-family judge vs UniProt: Affinage preferred faithfulness: 8/8 claims corpus-supported (100%)

Mechanistic narrative

Synthesis pass · prose summary of the discoveries below

S100A1 is a dimeric EF-hand Ca2+-sensor that transduces intracellular Ca2+ signals into the regulation of muscle excitation-contraction coupling, energy metabolism, and vascular tone through Ca2+-dependent engagement of diverse effector proteins (PMID:3722149, PMID:16236309). Each homodimer binds four Ca2+ via canonical and pseudo EF-hands; Ca2+ binding reorients helix 3 to expose a hydrophobic cleft formed by the hinge region, C-terminus, and helix 3 that serves as the target-binding pocket (PMID:16169012), with the C-terminal aromatic residues Phe88/Phe89/Trp90 being essential for Ca2+-dependent target engagement while a mechanistically distinct Ca2+-independent mode does not require this extension (PMID:9860858). In striated muscle this pocket binds the calmodulin-binding domain of RyR1, activating SR Ca2+ release and channel open probability and supporting voltage-sensor coupling, as confirmed by genetic knockout phenotypes (PMID:9298970, PMID:18089560, PMID:19651767), while in cardiomyocytes S100A1 selectively interacts with both RyR2 and SERCA2a to raise the gain of excitation-contraction coupling, increasing Ca2+ transients and SR Ca2+ uptake while suppressing diastolic Ca2+ sparks via its C-terminus (PMID:16236309, PMID:16919727). S100A1 also binds mitochondrial F1-ATPase to enhance ATP production (PMID:17438143) and reduces myofibrillar Ca2+ sensitivity, integrating contractile and energetic control (PMID:11717446). Restoring S100A1 by gene transfer in failing cardiomyocytes normalizes SR Ca2+ handling, reduces SR Ca2+ leak, reverses fetal gene reactivation, and rescues contractile function in vivo (PMID:15578088). Beyond muscle, endothelial S100A1 stimulates eNOS-dependent NO production to regulate vascular relaxation and postischemic angiogenesis (PMID:18292599, PMID:23048072), and extracellular S100A1 acts both as a pro-survival ligand internalized via clathrin-mediated endocytosis that activates PLC-PKC-MEK-ERK signaling (PMID:12960148) and as a released alarmin engaging TLR4 on cardiac fibroblasts (PMID:24833748). The protein additionally functions as a Ca2+-regulated chaperone within the Hsp70/Hsp90 multichaperone complex (PMID:14638689) and binds cytoskeletal and regulatory targets including GFAP, tubulin, MyoD, synapsin I, and other S100 proteins (PMID:7794894, PMID:9920729, PMID:10753920, PMID:15608682). Redox modification of Cys85 by glutathionylation or S-nitrosylation drives large structural changes and dramatically amplifies Ca2+ affinity, coupling redox state to Ca2+ sensing (PMID:15885104, PMID:15590070).

Mechanistic history

Synthesis pass · year-by-year structured walk · 14 steps
  1. 1986 High

    Established that S100A1 is a genuine Ca2+ sensor whose ligand binding drives a conformational switch, defining the biophysical basis for downstream effector regulation.

    Evidence Flow dialysis and spectroscopy of purified S100-alpha measuring 4 Ca2+ per dimer and Ca2+-induced hydrophobic exposure of Cys85

    PMID:3722149 PMID:3722150

    Open questions at the time
    • Did not identify physiological effector proteins
    • No atomic structure of the conformational change
  2. 1995 High

    Showed S100A1 can act as a Ca2+-dependent inhibitor of a transcription factor, broadening its role beyond a generic Ca2+ buffer to targeted protein regulation.

    Evidence Affinity chromatography, co-IP and in vitro PKC assays showing S100A1 binds MyoD helix I and blocks its phosphorylation and DNA binding

    PMID:7794894

    Open questions at the time
    • In vivo relevance to myogenic differentiation not established
    • Cellular context where this regulation dominates unclear
  3. 1997 High

    Identified RyR1 as a direct S100A1 target, linking S100A1 to skeletal muscle SR Ca2+ release at the channel level.

    Evidence Lipid bilayer single-channel recording, [3H]ryanodine binding and biosensor mapping of three RyR1 binding domains

    PMID:9298970

    Open questions at the time
    • Did not resolve binding stoichiometry on intact channel
    • Physiological consequence in muscle not yet tested genetically
  4. 1998 High

    Mapped the structural determinant of Ca2+-dependent target binding to C-terminal aromatic residues and revealed two distinct interaction modes.

    Evidence Site-directed mutagenesis of Phe88/Phe89/Trp90 with phenyl-Sepharose, TRTK peptide binding, and Ca2+-independent aldolase assays

    PMID:9860858

    Open questions at the time
    • Structural basis of the Ca2+-independent mode not defined
    • Which physiological targets use each mode unknown
  5. 2001 High

    Demonstrated that S100A1 enhances cardiac contractility by improving SR Ca2+ handling, establishing its functional role in the heart.

    Evidence Adenoviral overexpression in cardiomyocytes and engineered tissue with Ca2+ imaging, SR uptake assays, and cAMP-independence controls

    PMID:11717446

    Open questions at the time
    • Molecular targets mediating the effect not yet identified in this study
    • Relevance to failing myocardium not addressed
  6. 2003 High

    Revealed S100A1 functions as a Ca2+-regulated molecular chaperone, an activity distinct from its EC-coupling role.

    Evidence GST pull-down and co-IP with Hsp90/Hsp70/FKBP52/CyP40 plus in vitro client aggregation-protection assays

    PMID:14638689

    Open questions at the time
    • Physiological client proteins in vivo not defined
    • Whether chaperone role intersects with cardiac function unknown
  7. 2004 High

    Established the therapeutic principle that restoring S100A1 reverses heart failure pathophysiology at the SR Ca2+-handling level.

    Evidence Adenoviral S100A1 delivery in a post-infarction rat model with echocardiography, Ca2+ transient, SR leak/load, and metabolic measurements

    PMID:15578088

    Open questions at the time
    • Long-term durability of rescue not assessed
    • Large-animal translation not addressed in this study
  8. 2005 High

    Provided the atomic-resolution structure of Ca2+-bound S100A1, defining the target-binding pocket geometry.

    Evidence Multidimensional NMR solution structure with thousands of NOE constraints and RDCs versus apo-S100A1

    PMID:16169012

    Open questions at the time
    • Bound-complex structures with physiological targets not yet solved here
    • Dynamics of pocket opening not quantified
  9. 2005 High

    Linked redox chemistry to Ca2+ sensing by showing Cys85 glutathionylation massively increases Ca2+ affinity.

    Evidence Trp90 fluorescence Ca2+ titration with EF-hand mutants and TRTK-12 binding on glutathionylated S100A1

    PMID:15590070 PMID:15885104

    Open questions at the time
    • In vivo redox regulation of S100A1 not demonstrated
    • Reversibility kinetics under physiological conditions unclear
  10. 2007 High

    Connected S100A1 to cardiac energetics by identifying mitochondrial F1-ATPase as a direct target.

    Evidence Reciprocal pull-down, co-IP, colocalization, and ATP/F1-ATPase activity assays across gain- and loss-of-function

    PMID:17438143

    Open questions at the time
    • Mechanism of ATPase stimulation not structurally defined
    • Contribution to whole-heart energetics not quantified
  11. 2007 High

    Confirmed RyR1 as a physiological S100A1 target in skeletal muscle and resolved the binding interface structurally.

    Evidence S100A1 knockout mice with Ca2+ imaging plus NMR of S100A1 bound to the RyR1 CaM-binding peptide

    PMID:18089560 PMID:18650434

    Open questions at the time
    • Whether binding competes with CaM in situ unresolved at this stage
    • Stoichiometry on intact tetrameric channel unknown
  12. 2008 High

    Established S100A1 as a regulator of endothelial NO production and vascular tone, extending its role beyond muscle.

    Evidence S100A1 knockout mice with vascular relaxation, EC Ca2+ imaging, NO measurement, and IP3R-dependence pharmacology

    PMID:18292599

    Open questions at the time
    • Direct S100A1-eNOS structural interaction not resolved here
    • Relative contribution versus IP3R-driven Ca2+ unclear
  13. 2011 High

    Revised the RyR regulation model, showing S100A1 and CaM can co-occupy and concurrently modulate the channel rather than strictly competing at physiological levels.

    Evidence Time-resolved FRET on native SR vesicles across RyR1 and RyR2 with S100A1 concentration-response

    PMID:27226555

    Open questions at the time
    • Structural basis of the CaM conformational shift not defined
    • Functional output of dual occupancy on Ca2+ release not fully mapped
  14. 2014 High

    Defined an extracellular alarmin function whereby released S100A1 signals through TLR4 to shape post-infarction remodeling.

    Evidence Mouse MI model with neutralizing antibody, fibroblast co-culture, TLR4/NF-kB Western blots, and patient serum ELISA

    PMID:24833748

    Open questions at the time
    • Direct S100A1-TLR4 binding not structurally shown
    • Balance between protective and adverse extracellular effects unclear

Open questions

Synthesis pass · forward-looking unresolved questions
  • How the many Ca2+-dependent S100A1 interactions are spatially and temporally prioritized within a single cell, and how redox state tunes this in vivo, remains unresolved.
  • No integrated model of target selection among competing effectors
  • In vivo redox regulation of Ca2+ affinity not demonstrated
  • Quantitative occupancy of competing targets in intact tissue unknown

Mechanism profile

Synthesis pass · controlled-vocabulary classification · explore literature graph →
Molecular activity
GO:0098772 molecular function regulator activity 4 GO:0140299 molecular sensor activity 3 GO:0008092 cytoskeletal protein binding 2 GO:0044183 protein folding chaperone 1 GO:0140110 transcription regulator activity 1
Localization
GO:0005576 extracellular region 2 GO:0005783 endoplasmic reticulum 2 GO:0005829 cytosol 2 GO:0005739 mitochondrion 1
Pathway
R-HSA-162582 Signal Transduction 3 R-HSA-397014 Muscle contraction 3 R-HSA-1430728 Metabolism 2 R-HSA-168256 Immune System 1 R-HSA-392499 Metabolism of proteins 1
Partners
ANXA6ATP2A2HSP90MYODRYR1RYR2S100A4S100B
Complex memberships
Hsp70/Hsp90 multichaperone complex

Evidence

Reading pass · 44 per-paper findings extracted from the source corpus
Year Finding Method Journal Conf PMIDs
1986 S100A1 (S100-alpha subunit) binds calcium at 4 Ca2+ per dimer with specific EF-hand sites; zinc binding increases calcium affinity of S100b but only weakly affects S100-alpha; calcium binding induces conformational changes exposing hydrophobic domains including Cys85. Flow dialysis, UV spectroscopy, fluorescence spectroscopy, sulfhydryl reactivity assays The Journal of biological chemistry High 3722149
1986 Calcium binding to S100A1 (S100a) induces a conformational change that exposes hydrophobic domains; the alpha-subunit conformation is nearly identical whether in the S100a heterodimer or S100-alpha homodimer; calcium at high protein concentrations triggers subunit dissociation and exchange. UV absorption, circular dichroism, intrinsic fluorescence, sulfhydryl reactivity, hydrophobic fluorescent probe (ANS), FPLC separation The Journal of biological chemistry High 3722150
1991 S100A1 protein in skeletal muscle co-localizes with the A-band and/or longitudinal sarcoplasmic reticulum; isolated sarcoplasmic reticulum fractions and myofibrils contain multiple S100A1-binding proteins, suggesting a role in excitation-contraction coupling. Immunohistochemistry, radioimmunoassay, Northern blot, gel overlay for binding proteins, subcellular fractionation Cell motility and the cytoskeleton Medium 1802419
1995 S100A1 (S100a, alpha-alpha homodimer) binds to the basic helix I domain of MyoD (and other myogenic bHLH transcription factors) in a calcium-dependent manner; this binding inhibits PKC-mediated phosphorylation of MyoD at Thr115 and blocks MyoD DNA-binding activity; S100A1 is more potent than calmodulin in inhibiting MyoD DNA binding. Affinity chromatography, chemical cross-linking, native gel electrophoresis, fluorescence spectroscopy with DANSYL-CaM competition, in vitro PKC phosphorylation assay, co-immunoprecipitation from H9c2 cells Biochemistry High 7794894
1996 S100A1 inhibits phosphoglucomutase activity in a calcium-dependent manner (while S100B stimulates it); both S100A1 and S100B bind phosphoglucomutase via calcium-dependent affinity chromatography, identifying phosphoglucomutase as an S100A1 target protein. Gel overlay, affinity chromatography (S100A1/B-Sepharose and phosphoglucomutase-Sepharose), enzyme activity assay Cell calcium High 8894274
1996 S100A1-S100B heterodimer (CD-GCAP) is expressed in bovine retina and stimulates rod outer segment membrane guanylate cyclase (ROS-GC) activity in a calcium-dependent manner (EC50 ~17 µM Ca2+); the kinase-like domain of ROS-GC is not involved; the interaction domain resides in the C-terminal segment (aa 731–1054) of ROS-GC. Western blot, in vitro guanylate cyclase activity assay, domain mapping with deletion constructs Biochemistry Medium 8639567
1997 S100A1 directly interacts with three distinct binding domains on the skeletal muscle ryanodine receptor (RyR1) in a calcium-dependent and calcium-independent manner; at nanomolar Ca2+, S100A1 activates [3H]ryanodine binding (~40%) and increases single-channel open probability ~6-fold in planar lipid bilayer reconstitution; S100A1 increases apparent affinity of RyR for ryanodine (Kd 383→191 nM). Equilibrium [3H]ryanodine binding, planar lipid bilayer single-channel recording, BIAcore optical biosensor, ligand overlay on RyR fusion proteins, affinity chromatography on S100A1-Sepharose Biochemistry High 9298970
1997 S100A1 activates twitchin kinase in a calcium-dependent, zinc-enhanced manner; Ca2+/S100A1 binds twitchin kinase fragments with Kd <50 nM; Zn2+ reduces the off-rate; other Ca2+-binding proteins (S100A6, calmodulin, Ca2+-dependent protein kinase CaM-domain) bind the kinase but do not activate it, indicating specificity of S100A1 for kinase activation. BIAcore biosensor binding assay, in vitro kinase activity assay with recombinant S100A1 European journal of biochemistry High 9363763
1998 The carboxyl-terminal aromatic residues Phe88, Phe89, and Trp90 of S100A1 are essential for calcium-dependent target protein binding (TRTK/CapZ peptide) and hydrophobic exposure (phenyl-Sepharose interaction); deletion of residues 85–93 or triple aromatic mutation abolishes calcium-dependent target binding; calcium-independent target activation (aldolase A) does not require the C-terminus, revealing two mechanistically distinct interaction modes. Site-directed mutagenesis, affinity chromatography (phenyl-Sepharose), fluorescence binding assay with TRTK peptide, aldolase A activity assay Biochemistry High 9860858
1999 The C-terminal extension of S100A1 (residues Phe88–Ser93) is required for binding to GFAP, tubulin, the TRTK-12 peptide (CapZ), and a p53-derived peptide; S100A1 inhibits GFAP assembly into intermediate filaments via this C-terminal region; the truncated S100A1Δ88-93 lacks these interactions. Fluorescence spectroscopy with acrylodan-labeled S100A1, chemical crosslinking, GFAP polymerization assay, competition with TRTK-12 and p53 peptide Biochemical and biophysical research communications High 9920729
1998 Annexin VI binds S100A1 (and S100B) in a calcium-dependent manner and blocks their ability to inhibit desmin and GFAP assembly into intermediate filaments; each S100A1 dimer has one annexin VI binding site (sub-µM affinity); the annexin VI binding site on S100A1 does not overlap with the C-terminal extension required for desmin/GFAP binding. In vitro intermediate filament assembly assay, affinity chromatography, fluorescence binding Cell calcium Medium 9883272
2000 S100A4 and S100A1 interact directly in vitro and in vivo; the interaction requires conserved dimerization-interface residues (site-directed mutagenesis); S100A1 reduces S100A4-mediated inhibition of nonmuscle myosin A self-association and phosphorylation in vitro, and reduces S100A4-driven cell motility and metastasis. Yeast two-hybrid, affinity chromatography, gel overlay, FRET in living cells, biosensor binding kinetics, in vitro myosin assay, soft agar growth, in vivo metastasis assay The Journal of biological chemistry High 10753920 15608682
2000 S100A1 and S100B cause calcium-dependent disassembly of cytoplasmic microtubules in situ in glioma and myoblast triton-cytoskeletons; the C-terminal extension of S100A1 is required (S100A1Δ88-93 is inactive); TRTK-12 peptide blocks the effect; no direct intermediate filament disassembly was observed under these conditions. Triton-cytoskeleton preparation from live cells, immunofluorescence microscopy, inhibitory peptide competition Neuroscience Medium 10974440
2001 S100A1 overexpression in adult cardiomyocytes and engineered heart tissue (adenoviral gene transfer) increases unloaded shortening, isometric contraction, cytosolic Ca2+ transients, and SR Ca2+ uptake; S100A1 protein decreases myofibrillar Ca2+ sensitivity and cooperativity in Triton-skinned trabeculae without changing maximal force; effects are cAMP-independent (PKA phosphorylation of phospholamban unchanged). Adenoviral gene transfer, video-edge detection, FURA-2 Ca2+ imaging, saponin-permeabilized cell SR Ca2+ uptake assay, force-Ca2+ relationship in skinned trabeculae, cAMP measurement, PKA phosphorylation assay Proceedings of the National Academy of Sciences of the United States of America High 11717446
2002 S100A1 protein increases SERCA2a activity in skinned rat cardiomyocytes; adenoviral S100A1 overexpression increases fractional shortening by 55% and systolic Ca2+ amplitudes by 62% in adult rat cardiomyocytes. Adenoviral gene transfer, video-edge detection, FURA-2 Ca2+ imaging, SERCA activity assay in skinned cell preparations Basic research in cardiology High 12479236
2003 Extracellular S100A1 is endocytosed into neonatal cardiomyocytes via calcium-dependent clathrin-mediated endocytosis; internalized S100A1 activates ERK1/2 pro-survival signaling via a PLC→PKC→MEK1→ERK1/2 cascade, protecting cardiomyocytes from apoptosis; PKA and L-type Ca2+ channel are not required. Fluorescence microscopy of rhodamine-S100A1 uptake, apoptosis assay (2-deoxyglucose/oxidative stress), pharmacological inhibitors of signaling pathway, ERK1/2 phosphorylation Western blot The Journal of biological chemistry High 12960148
2003 S100A1 is a molecular chaperone that forms stable complexes with Hsp90, Hsp70, FKBP52, and CyP40 (components of the Hsp70/Hsp90 multichaperone complex) both in vitro and in mammalian cells; S100A1 protects multiple client proteins (citrate synthase, aldolase, GAPDH, rhodanese) from heat-induced aggregation and inactivation; overexpression protects luciferase and β-galactosidase from heat-shock inactivation in COS-7 cells. GST pull-down, co-immunoprecipitation, in vitro aggregation protection assay, thermal inactivation assay, COS-7 overexpression with heat shock The Journal of biological chemistry High 14638689
2004 Adenoviral S100A1 gene delivery to failing rat cardiomyocytes (post-infarction model) normalizes S100A1 protein, restores SR Ca2+ uptake, reduces SR Ca2+ leak, restores intracellular Ca2+ transients, decreases elevated intracellular Na+, reverses fetal gene reactivation, and restores energy supply; intracoronary delivery normalizes in vivo contractile function. Adenoviral gene transfer in vivo and in vitro, echocardiography, Ca2+ transient imaging (FURA-2), SR Ca2+ load (caffeine), SR Ca2+ leak measurements, intracellular Na+ measurement, gene expression, metabolic assays The Journal of clinical investigation High 15578088
2004 S100A1 binds S100P to form a heterodimer with Kd 10–20 nM (higher affinity than S100P homodimer, Kd 40–120 nM); FRET confirms the interaction in living cells; S100A1/S100P heterodimer is stabilized by hydrophobic interactions at the dimer interface (confirmed by site-directed mutagenesis); S100A1 preincubation reduces S100P binding to nonmuscle myosin A by ~50%. Yeast two-hybrid, optical biosensor (BIAcore), FRET in mammalian cells, site-directed mutagenesis, homology modelling The Biochemical journal High 15171681
2005 The three-dimensional NMR solution structure of Ca2+-bound S100A1 was determined; calcium binding causes large reorientation of helix 3 (typical EF-hand) but not of the pseudo EF-hand, exposing a hydrophobic cleft formed by hinge region, C-terminus, and helix 3 residues that constitutes the target-binding pocket for TRTK-12 (CapZ-derived peptide). Multidimensional NMR spectroscopy (2D/3D/4D), 3354 NOE constraints, 362 residual dipolar couplings, comparison with apo-S100A1 structure Journal of molecular biology High 16169012
2005 S100A1 protein increases the gain of excitation-contraction coupling in rabbit ventricular cardiomyocytes: 0.1 µM S100A1 increases Ca2+ transient amplitude (~41%), increases SERCA2a Ca2+ uptake rate (~22%), increases RyR2 activity ([3H]-ryanodine binding at 0.1–0.3 µM Ca2+), and shifts the SR Ca2+ content–fractional release relationship leftward without changing SR Ca2+ content; co-immunoprecipitation confirms selective S100A1 interaction with SERCA2a and RyR2. Patch pipette protein delivery, voltage clamp, FURA-2 Ca2+ imaging, caffeine-induced SR Ca2+ release, NCX current measurement, [3H]-ryanodine binding, co-immunoprecipitation Journal of molecular and cellular cardiology High 16236309
2005 S100A1 affinity for Ca2+ is dramatically increased (~10,000-fold increase in N-loop affinity, ~10-fold in C-loop) upon S-glutathionylation of Cys85; glutathionylated S100A1 still binds TRTK-12 in a Ca2+-dependent manner, linking redox and Ca2+ signaling. Trp90 fluorescence Ca2+-titration, TRTK-12 binding, site-directed mutagenesis of EF-hand loops (E32Q, E73Q), 2-p-toluidinylnaphthalene-6-sulfonate hydrophobicity probe The FEBS journal High 15885104
2004 Redox modification (S-nitrosylation and S-glutathionylation) of the conserved C-terminal cysteine (Cys85) of S100A1 strongly activated by Ca2+ binding results in global structural alterations of S100A1, as demonstrated by multiple spectroscopic techniques. RP-HPLC, ESI-MS, circular dichroism, fluorescence spectroscopy Biochimica et biophysica acta Medium 15590070
2007 S100A1 interacts with mitochondrial F1-ATPase alpha- and beta-chains in a Ca2+-dependent manner; S100A1 overexpression in cardiomyocytes increases cellular ATP content and F1-ATPase activity; S100A1 knockdown decreases ATP levels; ATP synthase activity is reduced in S100A1 knockout cardiomyocytes. GST pull-down, co-immunoprecipitation, confocal colocalization, gel filtration chromatography, ATP content measurement, F1-ATPase activity assay Molecular and cellular biology High 17438143
2007 S100A1 binds to the calmodulin-binding domain (CaM/S100A1 binding domain, RyRP12, residues 3616–3627) of RyR1 in skeletal muscle; genetic knockout of S100A1 reduces global myoplasmic Ca2+ transients and SR Ca2+ release following electrical excitation; the binding site is identified by competition assays and tryptophan fluorescence, and shows low micromolar affinity; NMR reveals the peptide binds in the Ca2+-dependent hydrophobic pocket of S100A1. S100A1 knockout mice, confocal microscopy Ca2+ imaging, competition binding assays with SR vesicles, tryptophan fluorescence, NMR spectroscopy The Journal of biological chemistry High 18089560
2007 S100A1 and S100B are transcriptional targets of the SOX trio (SOX9/SOX5/SOX6) in chondrocytes; S100A1 overexpression suppresses hypertrophic chondrocyte differentiation and mineralization; S100A1/S100B knockdown stimulates terminal differentiation and reverses SOX trio-mediated inhibition; SOX-trio-responsive enhancer elements identified in the S100A1 5'-flanking region. Microarray, overexpression, siRNA knockdown, luciferase reporter assay, EMSA, chromatin immunoprecipitation EMBO reports High 17396138
2008 Ca2+-S100A1 competes with Ca2+-calmodulin for the same binding site on RyR1 (RyRP12 domain, residues 3616–3627 in human RyR1); NMR structure of Ca2+-S100A1 bound to RyRP12 reveals key hydrophobic/electrostatic interactions involving RyRP12 residues Lys3616, Trp3620, Lys3622, Leu3623, Leu3624, Lys3626 with the Ca2+-induced hydrophobic pocket of S100A1. Competition binding assays (skeletal muscle SR), NMR spectroscopy (structure determination of S100A1-RyRP12 complex) The Journal of biological chemistry High 18650434
2008 Endothelial S100A1 modulates vascular function: S100A1 knockout mice show reduced acetylcholine-induced vascular relaxation, reduced basal and agonist-induced endothelial NO release, diminished agonist-induced Ca2+ transients in ECs, and hypertension; S100A1 overexpression in ECs increases NO generation in an IP3R-dependent manner; endothelial S100A1 is downregulated in heart failure. S100A1 knockout mice, vascular ring relaxation assay, Ca2+ imaging in ECs, NO measurement, siRNA knockdown, adenoviral overexpression, IP3R blocker (2-APB) Circulation research High 18292599
2009 NMR solution structure of S100A1 bound to TRTK12 (CapZ-derived peptide) reveals that TRTK12 forms an amphipathic helix with W7, I10, and L11 making key hydrophobic contacts with the Ca2+-dependent hydrophobic binding pocket of S100A1; Ca2+ binding affinity of S100A1 is tightened >3-fold upon TRTK12 binding. Solution NMR structure determination, ITC/fluorescence Ca2+ binding measurements Journal of molecular biology High 19452629
2009 In skeletal muscle fibers, S100A1 knockout selectively suppresses the Qgamma component of intra-membrane charge movement (voltage sensor activation) while leaving Qbeta unaffected; transient intracellular S100A1 application restores Qgamma; dantrolene (RyR1 inhibitor) similarly suppresses this charge movement component, linking S100A1 to RyR1-voltage sensor coupling. S100A1 knockout mice, whole-cell patch clamp of isolated flexor digitorum brevis fibers, intracellular S100A1 application, dantrolene pharmacology The Journal of physiology High 19651767
2009 Exogenous S100A1 taken up by superior cervical ganglion neurons enhances Cav1 (L-type) Ca2+ channel currents and prolongs action potentials in a PKA-dependent manner; NMR chemical shift perturbation confirms direct Ca2+-S100A1 interaction with a peptide from the PKA regulatory subunit within S100A1's hydrophobic binding pocket. SCG neuron culture, whole-cell patch clamp, Ca2+ imaging, rhodamine-S100A1 uptake, PKA inhibitor, NMR chemical shift perturbation American journal of physiology. Cell physiology High 19657060
2011 S100A1 is released from ischemic/necrotic cardiomyocytes and acts as an alarmin; it is endocytosed by cardiac fibroblasts and activates TLR4-dependent MAP kinase and NF-κB signaling, inducing an immunomodulatory/anti-fibrotic phenotype (elevated ICAM1, decreased collagen); antibody-mediated neutralization of S100A1 worsens infarct size and LV function post-MI. Patient serum ELISA, mouse MI model, in vitro co-culture, fluorescence microscopy of S100A1 endocytosis, Western blot (TLR4, MAP kinases, NF-κB), intracardiac S100A1 injection, neutralizing antibody EMBO molecular medicine High 24833748
2012 Calmodulin and S100A1 bind to two independent but overlapping domains on the N-terminus of TRPM3 (Ala35-Lys124 and His291-Gly382); key positively charged residues in these domains are required for binding; CaM and S100A1 compete for the same binding sites on TRPM3; interactions are calcium-dependent. Biophysical binding assays, biochemical pull-down, site-directed mutagenesis of TRPM3 N-terminal domains, competition assays The Journal of biological chemistry Medium 22451665
2012 S100A1 deficiency in endothelial cells impairs postischemic angiogenesis; mechanistically, S100A1 deficiency disrupts stimulatory S100A1/eNOS interaction, causes PKC hyperactivation leading to inhibitory eNOS phosphorylation, degrades VEGFR-2 with blunted PI3K/Akt/eNOS signaling; NO supplementation rescues angiogenesis and limb salvage in SKO mice. S100A1 knockout mice, femoral artery resection, perfusion measurement, EC proliferation/migration/tube formation assays, siRNA knockdown, eNOS activity, PKC inhibitor, Western blot, in vivo NO measurement Circulation research High 23048072
2013 In the PSAPP Alzheimer's disease mouse model, genetic ablation of S100A1 reduces astrocytosis, microgliosis, and amyloid plaque load; S100A1·RyR complexes are detected in human and mouse AD brain in a Ca2+-dependent manner (co-immunoprecipitation), identifying RyR as a primary S100A1 target protein in the brain; S100A1·Akt complexes are not detected, indicating indirect modulation of Akt. S100A1 knockout in PSAPP mice, immunohistochemistry (GFAP, Iba1, plaque), co-immunoprecipitation (S100A1·RyR and S100A1·Akt), Ca2+-dependent complex formation in neuronal cells Cell calcium Medium 24931125
2013 MicroRNA-138 (miR-138) downregulates S100A1 protein in endothelial cells by targeting the 3'UTR of S100A1; hypoxia induces miR-138 via HIF1α; miR-138-mediated reduction of S100A1 impairs tube formation and NO production; S100A1 adenoviral gene transfer rescues these defects. 3'UTR luciferase reporter, miR-138 mimic/inhibitor transfection, HIF1α siRNA, IOX2 (prolyl-hydroxylase inhibitor), tube formation assay, NO measurement, adenoviral S100A1 rescue PloS one High 24244340
2016 At physiological concentrations, S100A1 does NOT compete with calmodulin for the same binding site on intact RyR1 or RyR2 (Ki for FRET-detected CaM displacement >10 µM); instead, high micromolar S100A1 alters the structural state of RyR-bound CaM (shifting to lower FRET orientation) without reducing CaM amount bound; CaM and S100A1 can concurrently bind and modulate RyR. FRET between donor-labeled FKBP12.6 and acceptor-labeled CaM on RyR in SR vesicles, time-resolved FRET, concentration-response with S100A1 The Journal of biological chemistry High 27226555
2011 NMR solution structure of human apo-S100A1 (PDB 2L0P) was determined; backbone dynamics by 15N relaxation show that human apo-S100A1 is less mobile globally than bovine apo-S100A1 modified by disulfide at Cys85; secondary structure is nearly identical between the two forms. NMR spectroscopy, 15N magnetic relaxation Journal of structural biology High 21296671
2004 S100A1 binds to synapsin I (dephosphorylated and phosphorylated forms) in nerve terminals, inhibiting synapsin-induced F-actin bundling and abolishing synapsin dimerization in a dose- and Ca2+-dependent manner, without affecting synapsin binding to F-actin, G-actin, or synaptic vesicles; S100A1 is present in the soluble fraction of isolated nerve endings and co-distributes with synapsin I in ~5–20% of nerve terminals. Subcellular fractionation, confocal microscopy, immunogold electron microscopy, in vitro F-actin bundling assay, synapsin dimerization assay Journal of neurochemistry Medium 15147519
2002 Annexin VI and S100A1 form in vivo complexes (ANXA6/S100A1) in avian skeletal muscle, as shown by immunoprecipitation; both proteins co-localize at sarcolemma, sarcoplasmic reticulum membranes, and putative transverse tubules from embryonic day 18 onward; annexin V is not recovered in S100A1 immunoprecipitates. Confocal laser scanning microscopy, immunogold cytochemistry, Western blot, co-immunoprecipitation Neuroscience Medium 11801372
2005 Extracellular S100A1 (1 µM) applied to embryonic mouse and neonatal rat ventricular cardiomyocytes rapidly translocates into cells and enhances L-type Ca2+ current density (~112%); this effect is PKA-dependent (blocked by PKA inhibitor) and associated with increased PKA activity; in vitro reconstitution assays show S100A1 enhances PKA activity; cAMP levels are unchanged. Whole-cell patch clamp, rhodamine-S100A1 fluorescence uptake, PKA activity assay, cAMP measurement, PKA inhibitor (PKI) The Journal of biological chemistry Medium 16129693
2006 S100A1 protein (0.1 µM) reduces Ca2+ spark frequency (~38%), amplitude (~14%), and duration (~18%) in resting permeabilized rabbit cardiomyocytes at diastolic Ca2+ (~150 nM) via its C-terminus (aa 75–94); the S100A1 C-terminal peptide mimics and blocks these effects, slightly increasing SR Ca2+ content; accessory RyR2 modulators (sorcin, FKBP12.6) stoichiometry is unaltered. Saponin-permeabilized cardiomyocytes, confocal Ca2+ spark imaging, S100A1-ct peptide competition, SR Ca2+ content measurement, co-immunoprecipitation Cell calcium High 16919727
2013 Loss of CaM inhibition of RyR2 at diastolic Ca2+ (via single RyR2-L3591D mutation) also eliminates S100A1 regulation at both diastolic and systolic Ca2+ in single-channel measurements; Ryr2D/D mice develop cardiac hypertrophy and altered function, confirming that the RyR2 CaM/S100A1 binding domain is functionally important in vivo. Knock-in mouse (Ryr2D/D), single-channel planar lipid bilayer recording, echocardiography, heart weight/body weight ratio, ANP mRNA, transverse aortic constriction American journal of physiology. Heart and circulatory physiology High 23666671
2002 S100A1 interaction with antiallergic drugs (olopatadine, amlexanox, cromolyn) is Ca2+-dependent; mutagenesis mapped the olopatadine-binding site to residues 76–85 of S100A1 and the amlexanox-binding site to residues 89–94; the two drug-binding sites are distinct and non-competitive; both drug sites overlap with the target protein-binding region at the S100A1 C-terminus. Affinity chromatography with drug-conjugated resin, site-directed mutagenesis, competition binding with target peptides Biochemical and biophysical research communications Medium 11944917

Source papers

Stage 0 corpus · 100 papers · ranked by NIH iCite citations
Year Title Journal Citations PMID
1987 Differential distribution of immunoreactive S100-alpha and S100-beta proteins in normal nonnervous human tissues. Laboratory investigation; a journal of technical methods and pathology 308 3316838
2002 Gastric cancers overexpress S100A calcium-binding proteins. Cancer research 211 12460893
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. The Journal of biological chemistry 193 3722149
2011 Cardiac AAV9-S100A1 gene therapy rescues post-ischemic heart failure in a preclinical large animal model. Science translational medicine 189 21775667
2004 Cardiac adenoviral S100A1 gene delivery rescues failing myocardium. The Journal of clinical investigation 165 15578088
2007 Stable myocardial-specific AAV6-S100A1 gene therapy results in chronic functional heart failure rescue. Circulation 144 17470693
1996 Altered expression of the Ca(2+)-binding protein S100A1 in human cardiomyopathy. Biochimica et biophysica acta 141 8898862
2001 S100A1: a regulator of myocardial contractility. Proceedings of the National Academy of Sciences of the United States of America 124 11717446
2006 Cardiac S100A1 protein levels determine contractile performance and propensity toward heart failure after myocardial infarction. Circulation 123 16952982
1997 Interaction of S100A1 with the Ca2+ release channel (ryanodine receptor) of skeletal muscle. Biochemistry 104 9298970
2008 S100A1 and calmodulin compete for the same binding site on ryanodine receptor. The Journal of biological chemistry 102 18650434
2007 S100A1 and S100B, transcriptional targets of SOX trio, inhibit terminal differentiation of chondrocytes. EMBO reports 94 17396138
2023 Single-cell transcriptome profiling of sepsis identifies HLA-DRlowS100Ahigh monocytes with immunosuppressive function. Military Medical Research 93 37337301
2007 S100A1 binds to the calmodulin-binding site of ryanodine receptor and modulates skeletal muscle excitation-contraction coupling. The Journal of biological chemistry 91 18089560
1992 S100 alpha, CAPL, and CACY: molecular cloning and expression analysis of three calcium-binding proteins from human heart. Biochemistry 89 1384693
2007 Ca2+ -dependent interaction of S100A1 with F1-ATPase leads to an increased ATP content in cardiomyocytes. Molecular and cellular biology 85 17438143
2013 S100A proteins as molecular targets in the ocular surface inflammatory diseases. The ocular surface 83 24439044
2005 The three-dimensional solution structure of Ca(2+)-bound S100A1 as determined by NMR spectroscopy. Journal of molecular biology 81 16169012
2014 S100A1 is released from ischemic cardiomyocytes and signals myocardial damage via Toll-like receptor 4. EMBO molecular medicine 76 24833748
2000 Effects of S100A1 and S100B on microtubule stability. An in vitro study using triton-cytoskeletons from astrocyte and myoblast cell lines. Neuroscience 76 10974440
2009 S100A1 in cardiovascular health and disease: closing the gap between basic science and clinical therapy. Journal of molecular and cellular cardiology 69 19538970
2005 S100A1 gene therapy preserves in vivo cardiac function after myocardial infarction. Molecular therapy : the journal of the American Society of Gene Therapy 69 16168714
2009 S100A1: Structure, Function, and Therapeutic Potential. Current chemical biology 68 19890475
2003 Extracellular S100A1 protein inhibits apoptosis in ventricular cardiomyocytes via activation of the extracellular signal-regulated protein kinase 1/2 (ERK1/2). The Journal of biological chemistry 68 12960148
1986 Ions binding to S100 proteins. II. Conformational studies and calcium-induced conformational changes in S100 alpha alpha protein: the effect of acidic pH and calcium incubation on subunit exchange in S100a (alpha beta) protein. The Journal of biological chemistry 67 3722150
2007 S100A1: a novel inotropic regulator of cardiac performance. Transition from molecular physiology to pathophysiological relevance. American journal of physiology. Regulatory, integrative and comparative physiology 66 17459908
2005 S100A1 increases the gain of excitation-contraction coupling in isolated rabbit ventricular cardiomyocytes. Journal of molecular and cellular cardiology 66 16236309
2000 Interaction in vivo and in vitro of the metastasis-inducing S100 protein, S100A4 (p9Ka) with S100A1. The Journal of biological chemistry 66 10753920
1996 Molecular characterization of S100A1-S100B protein in retina and its activation mechanism of bovine photoreceptor guanylate cyclase. Biochemistry 65 8639567
2011 S100A1 genetically targeted therapy reverses dysfunction of human failing cardiomyocytes. Journal of the American College of Cardiology 62 21851887
2002 Annexin V, annexin VI, S100A1 and S100B in developing and adult avian skeletal muscles. Neuroscience 62 11801372
2020 Liposomal Resveratrol and/or Carvedilol Attenuate Doxorubicin-Induced Cardiotoxicity by Modulating Inflammation, Oxidative Stress and S100A1 in Rats. Antioxidants (Basel, Switzerland) 59 32079097
2006 S100A1 decreases calcium spark frequency and alters their spatial characteristics in permeabilized adult ventricular cardiomyocytes. Cell calcium 59 16919727
1995 Interactions of myogenic bHLH transcription factors with calcium-binding calmodulin and S100a (alpha alpha) proteins. Biochemistry 57 7794894
2007 Diagnostic utility of S100A1 expression in renal cell neoplasms: an immunohistochemical and quantitative RT-PCR study. Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc 56 17483815
1997 S100A1 and S100B expression and target proteins in type I diabetes. Endocrinology 54 9389498
2017 Long non-coding RNA FOXD2-AS1 aggravates nasopharyngeal carcinoma carcinogenesis by modulating miR-363-5p/S100A1 pathway. Gene 52 29248577
2010 S100A1: a multifaceted therapeutic target in cardiovascular disease. Journal of cardiovascular translational research 51 20645037
2010 S100A1: a regulator of striated muscle sarcoplasmic reticulum Ca2+ handling, sarcomeric, and mitochondrial function. Journal of biomedicine & biotechnology 50 20368797
2000 S100A1, a new marker for acute myocardial ischemia. Biochemical and biophysical research communications 49 10924368
2001 Expression of S100a, vimentin, NSE, and melan A/MART-1 in seven canine melanoma cells lines and twenty-nine retrospective cases of canine melanoma. Veterinary pathology 48 11467477
1996 Identification of an S100A1/S100B target protein: phosphoglucomutase. Cell calcium 48 8894274
2013 MicroRNA-138 regulates hypoxia-induced endothelial cell dysfunction by targeting S100A1. PloS one 47 24244340
2012 Calmodulin and S100A1 protein interact with N terminus of TRPM3 channel. The Journal of biological chemistry 46 22451665
2004 Redox modifications of the C-terminal cysteine residue cause structural changes in S100A1 and S100B proteins. Biochimica et biophysica acta 46 15590070
2002 The small EF-hand Ca2+ binding protein S100A1 increases contractility and Ca2+ cycling in rat cardiac myocytes. Basic research in cardiology 46 12479236
1991 Isolation of a rat S100 alpha cDNA and distribution of its mRNA in rat tissues. Brain research bulletin 46 1742602
2014 Genomic analysis and differential expression of HMG and S100A family in human arthritis: upregulated expression of chemokines, IL-8 and nitric oxide by HMGB1. DNA and cell biology 45 24905701
1999 Role of the C-terminal extension in the interaction of S100A1 with GFAP, tubulin, the S100A1- and S100B-inhibitory peptide, TRTK-12, and a peptide derived from p53, and the S100A1 inhibitory effect on GFAP polymerization. Biochemical and biophysical research communications 45 9920729
2005 Mutually antagonistic actions of S100A4 and S100A1 on normal and metastatic phenotypes. Oncogene 44 15608682
2005 Affinity of S100A1 protein for calcium increases dramatically upon glutathionylation. The FEBS journal 44 15885104
2002 Induced transcriptional expression of calcium-binding protein S100A1 and S100A10 genes in human renal cell carcinoma. Cancer letters 44 11734338
2009 Solution structure of S100A1 bound to the CapZ peptide (TRTK12). Journal of molecular biology 42 19452629
2003 S100A1 is a novel molecular chaperone and a member of the Hsp70/Hsp90 multichaperone complex. The Journal of biological chemistry 42 14638689
2012 Targeting S100A1 in heart failure. Gene therapy 41 22336719
2011 S100A expression in normal corneal-limbal epithelial cells and ocular surface squamous cell carcinoma tissue. Molecular vision 41 21897749
2002 Interaction of S100 proteins with the antiallergic drugs, olopatadine, amlexanox, and cromolyn: identification of putative drug binding sites on S100A1 protein. Biochemical and biophysical research communications 41 11944917
2008 Endothelial S100A1 modulates vascular function via nitric oxide. Circulation research 40 18292599
1998 Annexin VI binds S100A1 and S100B and blocks the ability of S100A1 and S100B to inhibit desmin and GFAP assemblies into intermediate filaments. Cell calcium 40 9883272
2000 Transcriptional regulation of S100A1 and expression during mouse heart development. Biochimica et biophysica acta 39 11108964
2014 S100A1: a major player in cardiovascular performance. Physiological research 38 25157660
2018 Multiomics analyses identified epigenetic modulation of the S100A gene family in Kawasaki disease and their significant involvement in neutrophil transendothelial migration. Clinical epigenetics 37 30382880
1998 S100A1 utilizes different mechanisms for interacting with calcium-dependent and calcium-independent target proteins. Biochemistry 37 9860858
2011 S100A1 and calmodulin regulation of ryanodine receptor in striated muscle. Cell calcium 36 21784520
2010 S100A proteins in the pathogenesis of experimental corneal neovascularization. Molecular vision 35 21139687
2012 Immunohistochemical expression of Annexin A2 and S100A proteins in patients with bulky stage IB-IIA cervical cancer treated with neoadjuvant chemotherapy. Gynecologic oncology 34 22487537
1995 S100, alpha-smooth muscle actin and cytokeratin 19 immunohistochemistry in odontogenic and soft tissue myxomas. Journal of clinical pathology 34 7560205
1991 Examination of the calcium-modulated protein S100 alpha and its target proteins in adult and developing skeletal muscle. Cell motility and the cytoskeleton 34 1802419
2012 S100A1 deficiency impairs postischemic angiogenesis via compromised proangiogenic endothelial cell function and nitric oxide synthase regulation. Circulation research 32 23048072
2017 S100A1 promotes cell proliferation and migration and is associated with lymph node metastasis in ovarian cancer. Discovery medicine 31 28595036
2015 Role of S100A1 in hypoxia-induced inflammatory response in cardiomyocytes via TLR4/ROS/NF-κB pathway. The Journal of pharmacy and pharmacology 30 25880347
2013 Cardiac hypertrophy associated with impaired regulation of cardiac ryanodine receptor by calmodulin and S100A1. American journal of physiology. Heart and circulatory physiology 30 23666671
2009 The Qgamma component of intra-membrane charge movement is present in mammalian muscle fibres, but suppressed in the absence of S100A1. The Journal of physiology 30 19651767
2005 S100A1 enhances the L-type Ca2+ current in embryonic mouse and neonatal rat ventricular cardiomyocytes. The Journal of biological chemistry 30 16129693
1999 Replicating myoblasts and fused myotubes express the calcium-regulated proteins S100A1 and S100B. Cell calcium 30 10326676
2016 S100A1 Protein Does Not Compete with Calmodulin for Ryanodine Receptor Binding but Structurally Alters the Ryanodine Receptor·Calmodulin Complex. The Journal of biological chemistry 29 27226555
2004 S100A1 gene transfer: a strategy to strengthen engineered cardiac grafts. The journal of gene medicine 29 15079813
2004 Heterodimeric interaction and interfaces of S100A1 and S100P. The Biochemical journal 29 15171681
2000 S100A1 and S100B interactions with annexins. Biochimica et biophysica acta 29 11108963
1999 The calcium-modulated proteins, S100A1 and S100B, as potential regulators of the dynamics of type III intermediate filaments. Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas 29 10510252
1995 Analysis of S100A1 expression during skeletal muscle and neuronal cell differentiation. Journal of neurochemistry 29 7760053
2014 The Ca2+ sensor S100A1 modulates neuroinflammation, histopathology and Akt activity in the PSAPP Alzheimer's disease mouse model. Cell calcium 28 24931125
2010 S100A1 gene therapy for heart failure: a novel strategy on the verge of clinical trials. Journal of molecular and cellular cardiology 28 20732326
1991 Structure and chromosome assignment of human S100 alpha and beta subunit genes. Biochemical and biophysical research communications 27 1998503
2010 Immunohistochemical analysis of the S100A1, S100B, CD44 and Bcl-2 antigens and the rate of cell proliferation assessed by Ki-67 antibody in benign and malignant melanocytic tumours. Melanoma research 26 20042890
2004 S100A1 codistributes with synapsin I in discrete brain areas and inhibits the F-actin-bundling activity of synapsin I. Journal of neurochemistry 26 15147519
2020 The Zn2+ and Ca2+ -binding S100B and S100A1 proteins: beyond the myths. Biological reviews of the Cambridge Philosophical Society 25 32027773
1997 Interaction of the recombinant S100A1 protein with twitchin kinase, and comparison with other Ca2+-binding proteins. European journal of biochemistry 25 9363763
2015 HNF1β and S100A1 are useful biomarkers for distinguishing renal oncocytoma and chromophobe renal cell carcinoma in FNA and core needle biopsies. Cancer cytopathology 24 25739652
2014 S100A1 and S100B expression patterns identify differentiation status of human articular chondrocytes. Journal of cellular physiology 24 24402969
2017 S100A1 and S100B: Calcium Sensors at the Cross-Roads of Multiple Chondrogenic Pathways. Journal of cellular physiology 23 27925190
2013 S100A expression and interleukin-10 polymorphisms are associated with ulcerative colitis and diarrhea predominant irritable bowel syndrome. Digestive diseases and sciences 23 23595519
2005 Co-expression/co-location of S100 proteins (S100B, S100A1 and S100A2) and protein kinase C (PKC-beta, -eta and -zeta) in a rat model of cerebral basilar artery vasospasm. Neuropathology and applied neurobiology 23 16281914
2020 Expression of S100A Alarmins in Cord Blood Monocytes Is Highly Associated With Chorioamnionitis and Fetal Inflammation in Preterm Infants. Frontiers in immunology 21 32612607
2012 S100A proteins in propagation of a calcium signal in norm and pathology. Postepy biochemii 21 23662436
2006 S100A1-deficient male mice exhibit increased exploratory activity and reduced anxiety-related responses. Biochimica et biophysica acta 21 17045663
2017 Annexin/S100A Protein Family Regulation through p14ARF-p53 Activation: A Role in Cell Survival and Predicting Treatment Outcomes in Breast Cancer. PloS one 20 28068434
2009 Augmentation of Cav1 channel current and action potential duration after uptake of S100A1 in sympathetic ganglion neurons. American journal of physiology. Cell physiology 20 19657060
2011 Solution NMR structure and dynamics of human apo-S100A1 protein. Journal of structural biology 19 21296671
1996 Expression of the rat S100A1 gene in neurons, glia, and skeletal muscle. Brain research 19 8793102

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