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Structure of an asymmetric ternary protein complex provides insight for membrane interaction.

Dempsey BR, Rezvanpour A, Lee TW, Barber KR, Junop MS, Shaw GS
Structure 20 1737-45 (2012)
Cited: 26 times
EuropePMC logo PMID: 22940583

Abstract

Plasma membrane repair involves the coordinated effort of proteins and the inner phospholipid surface to mend the rupture and return the cell back to homeostasis. Here, we present the three-dimensional structure of a multiprotein complex that includes S100A10, annexin A2, and AHNAK, which along with dysferlin, functions in muscle and cardiac tissue repair. The 3.5 Å resolution X-ray structure shows that a single region from the AHNAK C terminus is recruited by an S100A10-annexin A2 heterotetramer, forming an asymmetric ternary complex. The AHNAK peptide adopts a coil conformation that arches across the heterotetramer contacting both annexin A2 and S100A10 protomers with tight affinity (∼30 nM) and establishing a structural rationale whereby both S100A10 and annexin proteins are needed in AHNAK recruitment. The structure evokes a model whereby AHNAK is targeted to the membrane surface through sandwiching of the binding region between the S100A10/annexin A2 complex and the phospholipid membrane.

Reviews citing this publication (9)

  1. AHNAK: the giant jack of all trades. Davis TA, Loos B, Engelbrecht AM. Cell Signal 26 2683-2693 (2014)
  2. Plasma Membrane Repair: A Central Process for Maintaining Cellular Homeostasis. Blazek AD, Paleo BJ, Weisleder N. Physiology (Bethesda) 30 438-448 (2015)
  3. S100 proteins as therapeutic targets. Bresnick AR. Biophys Rev 10 1617-1629 (2018)
  4. Formins and membranes: anchoring cortical actin to the cell wall and beyond. Cvrčková F. Front Plant Sci 4 436 (2013)
  5. Flexible Players within the Sheaths: The Intrinsically Disordered Proteins of Myelin in Health and Disease. Raasakka A, Kursula P. Cells 9 E470 (2020)
  6. The Annexin A2/S100A10 Complex: The Mutualistic Symbiosis of Two Distinct Proteins. Bharadwaj A, Kempster E, Waisman DM. Biomolecules 11 1849 (2021)
  7. The S100B Protein and Partners in Adipocyte Response to Cold Stress and Adaptive Thermogenesis: Facts, Hypotheses, and Perspectives. Baudier J, Gentil BJ. Biomolecules 10 E843 (2020)
  8. Actin Cytoskeletal Dynamics in Single-Cell Wound Repair. Ebstrup ML, Dias C, Heitmann ASB, Sønder SL, Nylandsted J. Int J Mol Sci 22 10886 (2021)
  9. Role of calcium-sensor proteins in cell membrane repair. Li Z, Shaw GS. Biosci Rep 43 BSR20220765 (2023)

Articles citing this publication (17)

  1. Annexin-phospholipid interactions. Functional implications. Lizarbe MA, Barrasa JI, Olmo N, Gavilanes F, Turnay J. Int J Mol Sci 14 2652-2683 (2013)
  2. Molecular codes for cell type specification in Brn3 retinal ganglion cells. Sajgo S, Ghinia MG, Brooks M, Kretschmer F, Chuang K, Hiriyanna S, Wu Z, Popescu O, Badea TC. Proc Natl Acad Sci U S A 114 E3974-E3983 (2017)
  3. AHNAK suppresses tumour proliferation and invasion by targeting multiple pathways in triple-negative breast cancer. Chen B, Wang J, Dai D, Zhou Q, Guo X, Tian Z, Huang X, Yang L, Tang H, Xie X. J Exp Clin Cancer Res 36 65 (2017)
  4. The Annexin A2/p11 complex is required for efficient invasion of Salmonella Typhimurium in epithelial cells. Jolly C, Winfree S, Hansen B, Steele-Mortimer O. Cell Microbiol 16 64-77 (2014)
  5. Fluorescence-Reported Allelic Exchange Mutagenesis Reveals a Role for Chlamydia trachomatis TmeA in Invasion That Is Independent of Host AHNAK. McKuen MJ, Mueller KE, Bae YS, Fields KA. Infect Immun 85 e00640-17 (2017)
  6. Proteomic investigation of the interactome of FMNL1 in hematopoietic cells unveils a role in calcium-dependent membrane plasticity. Han Y, Yu G, Sarioglu H, Caballero-Martinez A, Schlott F, Ueffing M, Haase H, Peschel C, Krackhardt AM. J Proteomics 78 72-82 (2013)
  7. Regulation of the Equilibrium between Closed and Open Conformations of Annexin A2 by N-Terminal Phosphorylation and S100A4-Binding. Ecsédi P, Kiss B, Gógl G, Radnai L, Buday L, Koprivanacz K, Liliom K, Leveles I, Vértessy B, Jeszenői N, Hetényi C, Schlosser G, Katona G, Nyitray L. Structure 25 1195-1207.e5 (2017)
  8. AHNAK is downregulated in melanoma, predicts poor outcome, and may be required for the expression of functional cadherin-1. Sheppard HM, Feisst V, Chen J, Print C, Dunbar PR. Melanoma Res 26 108-116 (2016)
  9. AHNAK controls 53BP1-mediated p53 response by restraining 53BP1 oligomerization and phase separation. Ghodke I, Remisova M, Furst A, Kilic S, Reina-San-Martin B, Poetsch AR, Altmeyer M, Soutoglou E. Mol Cell 81 2596-2610.e7 (2021)
  10. Structure of the S100A4/myosin-IIA complex. Ramagopal UA, Dulyaninova NG, Varney KM, Wilder PT, Nallamsetty S, Brenowitz M, Weber DJ, Almo SC, Bresnick AR. BMC Struct Biol 13 31 (2013)
  11. The native structure of annexin A2 peptides in hydrophilic environment determines their anti-angiogenic effects. Raddum AM, Hollås H, Shumilin IA, Henklein P, Kretsinger R, Fossen T, Vedeler A. Biochem Pharmacol 95 1-15 (2015)
  12. Giant scaffolding protein AHNAK1 interacts with β-dystroglycan and controls motility and mechanical properties of Schwann cells. von Boxberg Y, Soares S, Féréol S, Fodil R, Bartolami S, Taxi J, Tricaud N, Nothias F. Glia 62 1392-1406 (2014)
  13. A subset of calcium-binding S100 proteins show preferential heterodimerization. Spratt DE, Barber KR, Marlatt NM, Ngo V, Macklin JA, Xiao Y, Konermann L, Duennwald ML, Shaw GS. FEBS J 286 1859-1876 (2019)
  14. An alternative N-terminal fold of the intestine-specific annexin A13a induces dimerization and regulates membrane-binding. McCulloch KM, Yamakawa I, Shifrin DA, McConnell RE, Foegeding NJ, Singh PK, Mao S, Tyska MJ, Iverson TM. J Biol Chem 294 3454-3463 (2019)
  15. Protective Function of Ahnak1 in Vascular Healing after Wire Injury. Haase N, Rüder C, Haase H, Kamann S, Kouno M, Morano I, Dechend R, Zohlnhöfer D, Haase T. J Vasc Res 54 131-142 (2017)
  16. Structural characterization of a dimeric complex between the short cytoplasmic domain of CEACAM1 and the pseudo tetramer of S100A10-Annexin A2 using NMR and molecular dynamics. Hu W, Bhattacharya S, Hong T, Wong P, Li L, Vaidehi N, Kalkum M, Shively JE. Biochim Biophys Acta Biomembr 1863 183451 (2021)
  17. research-article Ahnak depletion accelerates liver regeneration by modulating the TGF-β/Smad signaling pathway. Yang I, Son Y, Shin JH, Kim IY, Seong JK. BMB Rep 55 401-406 (2022)


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