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A Common Binding Site for Actin-Binding Proteins on the Actin Surface

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Actin-Monomer-Binding Proteins

Part of the book series: Molecular Biology Intelligence Unit ((MBIU))

Abstract

The dynamic remodeling of the actin cytoskeleton plays an essential role in many cellular processes, including cell motility, cytokinesis, and intracellular transport. A large number of actin-binding proteins (ABPs) participate in this process, regulating the assembly of actin filaments into functional networks. ABPs are extremely diverse, both structurally and functionally, but they most seem to share a common binding area on the actin surface, consistent of the cleft between actin subdomains 1 and 3. Actin itself is thought to interact in this cleft in the filament. As a result, part of the cleft becomes buried in F-actin by inter-subunit contacts, whereas another part remains exposed and mediates the interactions of various filamentous actin-binding proteins. The convergence of actin-binding proteins into a common binding area imposes enormous constraints on their interactions and could serve a regulatory function. Because the cleft falls near the hinge for domain motions in actin, binding in this area is an effective way for ABPs to “sense” the conformation of actin, in particular conformational changes resulting from ATP hydrolysis by actin or from the G- to F-actin transition.

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References

  1. Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003; 112(4):453–465.

    Article  PubMed  CAS  Google Scholar 

  2. Paavilainen VO, Bertling E, Falck S et al. Regulation of cytoskeletal dynamics by actin-monomer-binding proteins. Trends Cell Biol 2004; 14(7):386–394.

    Article  PubMed  CAS  Google Scholar 

  3. Lambrechts A, Van Troys M, Ampe C. The actin cytoskeleton in normal and pathological cell motility. Int J Biochem Cell Biol 2004; 36(10):1890–1909.

    Article  PubMed  CAS  Google Scholar 

  4. dos Remedios CG, Chhabra D, Kekic M et al. Actin binding proteins: Regulation of cytoskeletal microfilaments. Physiol Rev 2003; 83(2):433–473.

    PubMed  Google Scholar 

  5. Paunola E, Mattila PK, Lappalainen P. WH2 domain: A small, versatile adapter for actin monomers. FEBS Lett 2002; 513(1):92–97.

    Article  PubMed  CAS  Google Scholar 

  6. Lappalainen P, Kessels MM, Cope MJ et al. The ADF homology (ADF-H) domain: A highly exploited actin-binding module. Mol Biol Cell 1998; 9(8):1951–1959.

    PubMed  CAS  Google Scholar 

  7. McGough AM, Staiger CJ, Min JK et al. The gelsolin family of actin regulatory proteins: Modular structures, versatile functions. FEBS Lett 2003; 552(2–3):75–81.

    Article  PubMed  CAS  Google Scholar 

  8. Gimona M, Djinovic-Carugo K, Kranewitter WJ et al. Functional plasticity of CH domains. FEBS Lett 2002; 513(1):98–106.

    Article  PubMed  CAS  Google Scholar 

  9. Higgs HN. Formin proteins: A domain-based approach. Trends Biochem Sci 2005; 30(6):342–353.

    Article  PubMed  CAS  Google Scholar 

  10. Sellers JR. Myosins: A diverse superfamily. Biochim Biophys Acta 2000; 1496(1):3–22.

    Article  PubMed  CAS  Google Scholar 

  11. Dominguez R. Actin-binding proteins—A unifying hypothesis. Trends Biochem Sci 2004;29(11):572–578.

    Article  PubMed  CAS  Google Scholar 

  12. Sheterline P, Clayton J, Sparrow J. Actin. 4th ed. Protein Profile 1998; 2(1):1–272.

    Google Scholar 

  13. Kabsch W, Mannherz HG, Suck D et al. Atomic structure of the actin: DNase I complex. Nature 1990; 347(6288):37–44.

    Article  PubMed  CAS  Google Scholar 

  14. Schutt CE, Myslik JC, Rozycki MD et al. The structure of crystalline profilin-beta-actin. Nature 1993; 365(6449):810–816.

    Article  PubMed  CAS  Google Scholar 

  15. McLaughlin PJ, Gooch JT, Mannherz HG et al. Structure of gelsolin segment 1-actin complex and the mechanism of filament severing. Nature 1993; 364(6439):685–692.

    Article  PubMed  CAS  Google Scholar 

  16. Irobi E, Burtnick LD, Urosev D et al. From the first to the second domain of gelsolin: A common path on the surface of actin? FEBS Lett 2003; 552(2–3):86–90.

    Article  PubMed  CAS  Google Scholar 

  17. Otterbein LR, Cosio C, Graceffa P et al. Crystal structures of the vitamin D-binding protein and its complex with actin: Structural basis of the actin-scavenger system. Proc Natl Acad Sci USA 2002; 99(12):8003–8008.

    Article  PubMed  CAS  Google Scholar 

  18. Bubb MR. Thymosin beta 4 interactions. Vitam Horm 2003; 66:297–316.

    PubMed  CAS  Google Scholar 

  19. Irobi E, Aguda AH, Larsson M et al. Structural basis of actin sequestration by thymosin-beta4: Implications for WH2 proteins. EMBO J 2004; 23(18):3599–3608.

    Article  PubMed  CAS  Google Scholar 

  20. Hertzog M, van Heijenoort C, Didry D et al. The beta-thymosin/WH2 domain; structural basis for the switch from inhibition to promotion of actin assembly. Cell 2004; 117(5):611–623.

    Article  PubMed  CAS  Google Scholar 

  21. Edwards J. Are beta-thymosins WH 2 domains? FEBS Lett 2004; 573(1–3):231–232, (author reply 233).

    Article  PubMed  CAS  Google Scholar 

  22. Chereau D, Kerff F, Graceffa P et al. Actin-bound structures of Wiskott-Aldrich syndrome protein (WASP)-homology domain 2 and the implications for filament assembly. Proc Natl Acad Sci USA 2005; 102(46):16644–16649.

    Article  PubMed  CAS  Google Scholar 

  23. Quinlan ME, Heuser JE, Kerkhoff E et al. Drosophila Spire is an actin nucleation factor. Nature 2005; 433(7024):382–388.

    Article  PubMed  CAS  Google Scholar 

  24. Otomo T, Tomchick DR, Otomo C et al. Structural basis of actin filament nucleation and processive capping by a formin homology 2 domain. Nature 2005; 433(7025):488–494.

    Article  PubMed  CAS  Google Scholar 

  25. Poupel O, Boleti H, Axisa S et al. Toxofilin, a novel actin-binding protein from Toxoplasma gondii, sequesters actin monomers and caps actin filaments. Mol Biol Cell 2000; 11(1):355–368.

    PubMed  CAS  Google Scholar 

  26. Klenchin VA, Allingham JS, King R et al. Trisoxazole macrolide toxins mimic the binding of actin-capping proteins to actin. Nat Struct Biol 2003; 10(12):1058–1063.

    Article  PubMed  CAS  Google Scholar 

  27. Domanski M, Hertzog M, Coutant J et al. Coupling of folding and binding of thymosin beta4 upon interaction with monomeric actin monitored by nuclear magnetic resonance. J Biol Chem 2004; 279(22):23637–23645.

    Article  PubMed  CAS  Google Scholar 

  28. Yarmola EG, Parikh S, Bubb MR. Formation and implications of a ternary complex of profilin, thymosin beta 4, and actin. J Biol Chem 2001; 276(49):45555–45563.

    Article  PubMed  CAS  Google Scholar 

  29. Ballweber E, Hannappel E, Huff T et al. Polymerisation of chemically cross-linked actin:thymosin beta(4) complex to filamentous actin: Alteration in helical parameters and visualisation of thymosin beta(4) binding on F-actin. J Mol Biol 2002; 315(4):613–625.

    Article  PubMed  CAS  Google Scholar 

  30. McGough A, Pope B, Chiu W et al. Cofilin changes the twist of F-actin: Implications for actin filament dynamics and cellular function. J Cell Biol 1997; 138(4):771–781.

    Article  PubMed  CAS  Google Scholar 

  31. Schuler H. ATPase activity and conformational changes in the regulation of actin. Biochim Biophys Acta 2001; 1549(2):137–147.

    PubMed  CAS  Google Scholar 

  32. Graceffa P, Dominguez R. Crystal structure of monomeric actin in the ATP state: Structural basis of nucleotide-dependent actin dynamics. J Biol Chem 2003; 278(36):34172–34180.

    Article  PubMed  CAS  Google Scholar 

  33. Holmes KC, Geeves MA. The structural basis of muscle contraction. Philos Trans R Soc Lond B Biol Sci 2000; 355(1396):419–431.

    Article  PubMed  CAS  Google Scholar 

  34. Hatanaka H, Ogura K, Moriyama K et al. Tertiary structure of destrin and structural similarity between two actin-regulating protein families. Cell 1996; 85(7):1047–1055.

    Article  PubMed  CAS  Google Scholar 

  35. Fedorov AA, Lappalainen P, Fedorov EV et al. Structure determination of yeast cofilin. Nat Struct Biol 1997; 4(5):366–369.

    Article  PubMed  CAS  Google Scholar 

  36. Leonard SA, Gittis AG, Petrella EC et al. Crystal structure of the actin-binding protein actophorin from Acanthamoeba. Nat Struct Biol 1997; 4(5):369–373.

    Article  PubMed  CAS  Google Scholar 

  37. Bowman GD, Nodelman IM, Hong Y et al. A comparative structural analysis of the ADF/cofilin family. Proteins 2000; 41(3):374–384.

    Article  PubMed  CAS  Google Scholar 

  38. Paavilainen VO, Merckel MC, Falck S et al. Structural conservation between the actin monomer-binding sites of twinfilin and actin-depolymerizing factor (ADF)/cofilin. J Biol Chem 2002; 277(45):43089–43095.

    Article  PubMed  CAS  Google Scholar 

  39. Lappalainen P, Fedorov EV, Fedorov AA et al. Essential functions and actin-binding surfaces of yeast cofilin revealed by systematic mutagenesis. EMBO J 1997; 16(18):5520–5530.

    Article  PubMed  CAS  Google Scholar 

  40. Guan JQ, Vorobiev S, Almo SC et al. Mapping the G-actin binding surface of cofilin using synchrotron protein footprinting. Biochemistry 2002; 41(18):5765–5775.

    Article  PubMed  CAS  Google Scholar 

  41. Ojala PJ, Paavilainen V, Lappalainen P. Identification of yeast cofilin residues specific for actin monomer and PIP2 binding. Biochemistry 2001; 40(51):15562–15569.

    Article  PubMed  CAS  Google Scholar 

  42. Wriggers W, Tang JX, Azuma T et al. Cofilin and gelsolin segment-1: Molecular dynamics simulation and biochemical analysis predict a similar actin binding mode. J Mol Biol 1998; 282(5):921–932.

    Article  PubMed  CAS  Google Scholar 

  43. Holmes KC, Popp D, Gebhard W et al. Atomic model of the actin filament. Nature 1990; 347(6288):44–49.

    Article  PubMed  CAS  Google Scholar 

  44. Otterbein LR, Graceffa P, Dominguez R. The crystal structure of uncomplexed actin in the ADP state. Science 2001; 293(5530):708–711.

    Article  PubMed  CAS  Google Scholar 

  45. Burtnick LD. Modification of actin with fluorescein isothiocyanate. Biochim Biophys Acta 1984; 791(1):57–62.

    PubMed  CAS  Google Scholar 

  46. Khaitlina SY, Strzelecka-Golaszewska H. Role of the DNase-I-binding loop in dynamic properties of actin filament. Biophys J 2002; 82(1 Pt 1):321–334.

    Article  PubMed  CAS  Google Scholar 

  47. Schwyter DH, Kron SJ, Toyoshima YY et al. Subtilisin cleavage of actin inhibits in vitro sliding movement of actin filaments over myosin. J Cell Biol 1990; 111(2):465–470.

    Article  PubMed  CAS  Google Scholar 

  48. Hegyi G, Mak M, Kim E et al. Intrastrand cross-linked actin between Gln-41 and Cys-374. I. Mapping of sites cross-linked in F-actin by N-(4-azido-2-nitrophenyl) putrescine. Biochemistry 1998; 37(51):17784–17792.

    Article  PubMed  CAS  Google Scholar 

  49. Kim E, Phillips M, Hegyi G et al. Intrastrand cross-linked actin between Gln-41 and Cys-374. II. Properties of cross-linked oligomers. Biochemistry 1998; 37(51):17793–17800.

    Article  PubMed  CAS  Google Scholar 

  50. Holmes KC, Angert I, Kull FJ et al. Electron cryo-microscopy shows how strong binding of to actin releases nucleotide. Nature 2003; 425(6956):423–427.

    Article  PubMed  CAS  Google Scholar 

  51. Rayment I, Holden HM, Whittaker M et al. Structure of the actin-myosin complex and its implications for muscle contraction. Science 1993; 261(5117):58–65.

    Article  PubMed  CAS  Google Scholar 

  52. McGough A, Way M, DeRosier D. Determination of the alpha-actinin-binding site on actin filaments by cryoelectron microscopy and image analysis. J Cell Biol 1994; 126(2):433–443.

    Article  PubMed  CAS  Google Scholar 

  53. Hanein D, Volkmann N, Goldsmith S et al. An atomic model of fimbrin binding to F-actin and its implications for filament crosslinking and regulation. Nat Struct Biol 1998; 5(9):787–792.

    Article  PubMed  CAS  Google Scholar 

  54. Sutherland-Smith AJ, Moores CA, Norwood FL et al. An atomic model for actin binding by the CH domains and spectrin-repeat modules of utrophin and dystrophin. J Mol Biol 2003; 329(1):15–33.

    Article  PubMed  CAS  Google Scholar 

  55. Moores CA, Keep NH, Kendrick-Jones J. Structure of the utrophin actin-binding domain bound to F-actin reveals binding by an induced fit mechanism. J Mol Biol 2000; 297(2):465–480.

    Article  PubMed  CAS  Google Scholar 

  56. Galkin VE, Orlova A, VanLoock MS et al. The utrophin actin-binding domain binds F-actin in two different modes: Implications for the spectrin superfamily of proteins. J Cell Biol 2002; 157(2):243–251.

    Article  PubMed  Google Scholar 

  57. McGough A. F-actin-binding proteins. Curr Opin Struct Biol 1998; 8(2):166–176.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Boston Biomedical Research Institute, 64 Grove Street, Watertown, Massachusetts, 02472, USA

    Roberto Dominguez

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  1. Roberto Dominguez
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© 2007 Landes Bioscience and Springer Science+Business Media

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Dominguez, R. (2007). A Common Binding Site for Actin-Binding Proteins on the Actin Surface. In: Actin-Monomer-Binding Proteins. Molecular Biology Intelligence Unit. Springer, New York, NY. https://doi.org/10.1007/978-0-387-46407-7_10

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