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Atomic structures of two novel immunoglobulin-like domain pairs in the actin cross-linking protein filamin.

Heikkinen OK, Ruskamo S, Konarev PV, Svergun DI, Iivanainen T, Heikkinen SM, Permi P, Koskela H, Kilpeläinen I, Ylänne J
J Biol Chem 284 25450-8 (2009)
Cited: 39 times
EuropePMC logo PMID: 19622754

Abstract

Filamins are actin filament cross-linking proteins composed of an N-terminal actin-binding domain and 24 immunoglobulin-like domains (IgFLNs). Filamins interact with numerous proteins, including the cytoplasmic domains of plasma membrane signaling and cell adhesion receptors. Thereby filamins mechanically and functionally link the cell membrane to the cytoskeleton. Most of the interactions have been mapped to the C-terminal IgFLNs 16-24. Similarly, as with the previously known compact domain pair of IgFLNa20-21, the two-domain fragments IgFLNa16-17 and IgFLNa18-19 were more compact in small angle x-ray scattering analysis than would be expected for two independent domains. Solution state NMR structures revealed that the domain packing in IgFLNa18-19 resembles the structure of IgFLNa20-21. In both domain pairs the integrin-binding site is masked, although the details of the domain-domain interaction are partly distinct. The structure of IgFLNa16-17 revealed a new domain packing mode where the adhesion receptor binding site of domain 17 is not masked. Sequence comparison suggests that similar packing of three tandem filamin domain pairs is present throughout the animal kingdom, and we propose that this packing is involved in the regulation of filamin interactions through a mechanosensor mechanism.

Reviews - 2k7q mentioned but not cited (2)

  1. The filamins: organizers of cell structure and function. Nakamura F, Stossel TP, Hartwig JH. Cell Adh Migr 5 160-169 (2011)
  2. The Role of Mechanotransduction in Contact Inhibition of Locomotion and Proliferation. Nakamura F. Int J Mol Sci 25 2135 (2024)

Articles - 2k7q mentioned but not cited (6)

  1. Atomic structures of two novel immunoglobulin-like domain pairs in the actin cross-linking protein filamin. Heikkinen OK, Ruskamo S, Konarev PV, Svergun DI, Iivanainen T, Heikkinen SM, Permi P, Koskela H, Kilpeläinen I, Ylänne J. J Biol Chem 284 25450-25458 (2009)
  2. Biochemical basis of the interaction between cystic fibrosis transmembrane conductance regulator and immunoglobulin-like repeats of filamin. Smith L, Page RC, Xu Z, Kohli E, Litman P, Nix JC, Ithychanda SS, Liu J, Qin J, Misra S, Liedtke CM. J Biol Chem 285 17166-17176 (2010)
  3. Flexible Structure of Peptide-Bound Filamin A Mechanosensor Domain Pair 20-21. Seppälä J, Tossavainen H, Rodic N, Permi P, Pentikäinen U, Ylänne J. PLoS One 10 e0136969 (2015)
  4. Structural and functional evaluation of C. elegans filamins FLN-1 and FLN-2. DeMaso CR, Kovacevic I, Uzun A, Cram EJ. PLoS One 6 e22428 (2011)
  5. Assembly of a filamin four-domain fragment and the influence of splicing variant-1 on the structure. Pentikäinen U, Jiang P, Takala H, Ruskamo S, Campbell ID, Ylänne J. J Biol Chem 286 26921-26930 (2011)
  6. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)


Reviews citing this publication (5)

  1. Structural characterization of proteins and complexes using small-angle X-ray solution scattering. Mertens HD, Svergun DI. J Struct Biol 172 128-141 (2010)
  2. Small-angle scattering for structural biology--expanding the frontier while avoiding the pitfalls. Jacques DA, Trewhella J. Protein Sci 19 642-657 (2010)
  3. Filamins in mechanosensing and signaling. Razinia Z, Mäkelä T, Ylänne J, Calderwood DA. Annu Rev Biophys 41 227-246 (2012)
  4. New insights into the versatile roles of platelet FlnA. Falet H. Platelets 24 1-5 (2013)
  5. Molecular Tuning of Filamin A Activities in the Context of Adhesion and Migration. Lamsoul I, Dupré L, Lutz PG. Front Cell Dev Biol 8 591323 (2020)

Articles citing this publication (26)

  1. Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A. Ehrlicher AJ, Nakamura F, Hartwig JH, Weitz DA, Stossel TP. Nature 478 260-263 (2011)
  2. Dynamic force sensing of filamin revealed in single-molecule experiments. Rognoni L, Stigler J, Pelz B, Ylänne J, Rief M. Proc Natl Acad Sci U S A 109 19679-19684 (2012)
  3. The regulation mechanism for the auto-inhibition of binding of human filamin A to integrin. Pentikäinen U, Ylänne J. J Mol Biol 393 644-657 (2009)
  4. FlnA binding to PACSIN2 F-BAR domain regulates membrane tubulation in megakaryocytes and platelets. Begonja AJ, Pluthero FG, Suphamungmee W, Giannini S, Christensen H, Leung R, Lo RW, Nakamura F, Lehman W, Plomann M, Hoffmeister KM, Kahr WH, Hartwig JH, Falet H. Blood 126 80-88 (2015)
  5. Differential mechanical stability of filamin A rod segments. Chen H, Zhu X, Cong P, Sheetz MP, Nakamura F, Yan J. Biophys J 101 1231-1237 (2011)
  6. Mechanical perturbation of filamin A immunoglobulin repeats 20-21 reveals potential non-equilibrium mechanochemical partner binding function. Chen H, Chandrasekar S, Sheetz MP, Stossel TP, Nakamura F, Yan J. Sci Rep 3 1642 (2013)
  7. The C-terminal rod 2 fragment of filamin A forms a compact structure that can be extended. Ruskamo S, Gilbert R, Hofmann G, Jiang P, Campbell ID, Ylänne J, Pentikäinen U. Biochem J 446 261-269 (2012)
  8. Binding of Myomesin to Obscurin-Like-1 at the Muscle M-Band Provides a Strategy for Isoform-Specific Mechanical Protection. Pernigo S, Fukuzawa A, Beedle AEM, Holt M, Round A, Pandini A, Garcia-Manyes S, Gautel M, Steiner RA. Structure 25 107-120 (2017)
  9. Documentation and localization of force-mediated filamin A domain perturbations in moving cells. Nakamura F, Song M, Hartwig JH, Stossel TP. Nat Commun 5 4656 (2014)
  10. Evidence for the mechanosensor function of filamin in tissue development. Huelsmann S, Rintanen N, Sethi R, Brown NH, Ylänne J. Sci Rep 6 32798 (2016)
  11. Evidence for multisite ligand binding and stretching of filamin by integrin and migfilin. Ithychanda SS, Qin J. Biochemistry 50 4229-4231 (2011)
  12. Molecular basis of the head-to-tail assembly of giant muscle proteins obscurin-like 1 and titin. Sauer F, Vahokoski J, Song YH, Wilmanns M. EMBO Rep 11 534-540 (2010)
  13. A novel structural unit in the N-terminal region of filamins. Sethi R, Seppälä J, Tossavainen H, Ylilauri M, Ruskamo S, Pentikäinen OT, Pentikäinen U, Permi P, Ylänne J. J Biol Chem 289 8588-8598 (2014)
  14. MVP-Associated Filamin A Mutations Affect FlnA-PTPN12 (PTP-PEST) Interactions. Duval D, Labbé P, Bureau L, Le Tourneau T, Norris RA, Markwald RR, Levine R, Schott JJ, Mérot J. J Cardiovasc Dev Dis 2 233-247 (2015)
  15. The Fc receptor-cytoskeleton complex from human neutrophils. Florentinus AK, Jankowski A, Petrenko V, Bowden P, Marshall JG. J Proteomics 75 450-468 (2011)
  16. Skeletal Dysplasia Mutations Effect on Human Filamins' Structure and Mechanosensing. Seppälä J, Bernardi RC, Haataja TJK, Hellman M, Pentikäinen OT, Schulten K, Permi P, Ylänne J, Pentikäinen U. Sci Rep 7 4218 (2017)
  17. A mechanism of global shape-dependent recognition and phosphorylation of filamin by protein kinase A. Ithychanda SS, Fang X, Mohan ML, Zhu L, Tirupula KC, Naga Prasad SV, Wang YX, Karnik SS, Qin J. J Biol Chem 290 8527-8538 (2015)
  18. Homozygous expression of the myofibrillar myopathy-associated p.W2710X filamin C variant reveals major pathomechanisms of sarcomeric lesion formation. Schuld J, Orfanos Z, Chevessier F, Eggers B, Heil L, Uszkoreit J, Unger A, Kirfel G, van der Ven PFM, Marcus K, Linke WA, Clemen CS, Schröder R, Fürst DO. Acta Neuropathol Commun 8 154 (2020)
  19. Small-angle X-ray scattering reveals compact domain-domain interactions in the N-terminal region of filamin C. Sethi R, Ylänne J. PLoS One 9 e107457 (2014)
  20. Conformational plasticity and evolutionary analysis of the myotilin tandem Ig domains. Puž V, Pavšič M, Lenarčič B, Djinović-Carugo K. Sci Rep 7 3993 (2017)
  21. Crystal structure of the filamin N-terminal region reveals a hinge between the actin binding and first repeat domains. Sawyer GM, Sutherland-Smith AJ. J Mol Biol 424 240-247 (2012)
  22. Domain-domain interactions in filamin A (16-23) impose a hierarchy of unfolding forces. Xu T, Lannon H, Wolf S, Nakamura F, Brujic J. Biophys J 104 2022-2030 (2013)
  23. MQ-HNCO-TROSY for the measurement of scalar and residual dipolar couplings in larger proteins: application to a 557-residue IgFLNa16-21. Mäntylahti S, Koskela O, Jiang P, Permi P. J Biomol NMR 47 183-194 (2010)
  24. A comprehensive analysis of the allergenicity and IgE epitopes of myosinogen allergens in Scylla paramamosain. Yang Y, Hu MJ, Jin TC, Zhang YX, Liu GY, Li YB, Zhang ML, Cao MJ, Su WJ, Liu GM. Clin Exp Allergy 49 108-119 (2019)
  25. H(N), N(H), C (α), C (β), and methyl group assignments of filamin multidomain fragments IgFLNc4-5 and IgFLNa3-5. Tossavainen H, Seppälä J, Sethi R, Pihlajamaa T, Permi P. Biomol NMR Assign 9 47-50 (2015)
  26. PACSIN2 regulates platelet integrin β1 hemostatic function. Biswas R, Boyd EK, Eaton N, Steenackers A, Schulte ML, Reusswig F, Yu H, Drew C, Kahr WHA, Shi Q, Plomann M, Hoffmeister KM, Falet H. J Thromb Haemost 21 3619-3632 (2023)


Related citations provided by authors (1)

  1. 1H,13C,15N chemical shift assignments for filamin A Ig-like domain pairs 16-17 and 18-19. Heikkinen O, Koskela H, Permi P, Heikkinen S, Kilpelainen I, Ylanne J To be published -

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