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Solution structures of the C-terminal headpiece subdomains of human villin and advillin, evaluation of headpiece F-actin-binding requirements.

Vermeulen W, Vanhaesebrouck P, Van Troys M, Verschueren M, Fant F, Goethals M, Ampe C, Martins JC, Borremans FA
Protein Sci 13 1276-87 (2004)
Cited: 33 times
EuropePMC logo PMID: 15096633

Abstract

Headpiece (HP) is a 76-residue F-actin-binding module at the C terminus of many cytoskeletal proteins. Its 35-residue C-terminal subdomain is one of the smallest known motifs capable of autonomously adopting a stable, folded structure in the absence of any disulfide bridges, metal ligands, or unnatural amino acids. We report the three-dimensional solution structures of the C-terminal headpiece subdomains of human villin (HVcHP) and human advillin (HAcHP), determined by two-dimensional 1H-NMR. They represent the second and third structures of such C-terminal headpiece subdomains to be elucidated so far. A comparison with the structure of the chicken villin C-terminal subdomain reveals a high structural conservation. Both C-terminal subdomains bind specifically to F-actin. Mutagenesis is used to demonstrate the involvement of Trp 64 in the F-actin-binding surface. The latter residue is part of a conserved structural feature, in which the surface-exposed indole ring is stacked on the proline and lysine side chain embedded in a PXWK sequence motif. On the basis of the structural and mutational data concerning Trp 64 reported here, the results of a cysteine-scanning mutagenesis study of full headpiece, and a phage display mutational study of the 69-74 fragment, we propose a modification of the model, elaborated by Vardar and coworkers, for the binding of headpiece to F-actin.

Articles - 1unc mentioned but not cited (3)

  1. Solution structures of the C-terminal headpiece subdomains of human villin and advillin, evaluation of headpiece F-actin-binding requirements. Vermeulen W, Vanhaesebrouck P, Van Troys M, Verschueren M, Fant F, Goethals M, Ampe C, Martins JC, Borremans FA. Protein Sci. 13 1276-1287 (2004)
  2. Low folding cooperativity of HP35 revealed by single-molecule force spectroscopy and molecular dynamics simulation. Lv C, Tan C, Qin M, Zou D, Cao Y, Wang W. Biophys. J. 102 1944-1951 (2012)
  3. 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 (3)

  1. Nuclear actin and actin-binding proteins in the regulation of transcription and gene expression. Zheng B, Han M, Bernier M, Wen JK. FEBS J. 276 2669-2685 (2009)
  2. Regulation of cell structure and function by actin-binding proteins: villin's perspective. Khurana S, George SP. FEBS Lett. 582 2128-2139 (2008)
  3. Targeting AVIL, a New Cytoskeleton Regulator in Glioblastoma. Cornelison R, Marrah L, Horter D, Lynch S, Li H. Int J Mol Sci 22 13635 (2021)

Articles citing this publication (27)

  1. High-resolution x-ray crystal structures of the villin headpiece subdomain, an ultrafast folding protein. Chiu TK, Kubelka J, Herbst-Irmer R, Eaton WA, Hofrichter J, Davies DR. Proc. Natl. Acad. Sci. U.S.A. 102 7517-7522 (2005)
  2. Probing the folding transition state structure of the villin headpiece subdomain via side chain and backbone mutagenesis. Bunagan MR, Gao J, Kelly JW, Gai F. J. Am. Chem. Soc. 131 7470-7476 (2009)
  3. Using an amino acid fluorescence resonance energy transfer pair to probe protein unfolding: application to the villin headpiece subdomain and the LysM domain. Glasscock JM, Zhu Y, Chowdhury P, Tang J, Gai F. Biochemistry 47 11070-11076 (2008)
  4. The 3D structure of villin as an unusual F-Actin crosslinker. Hampton CM, Liu J, Taylor DW, DeRosier DJ, Taylor KA. Structure 16 1882-1891 (2008)
  5. The unfolded state of the villin headpiece helical subdomain: computational studies of the role of locally stabilized structure. Wickstrom L, Okur A, Song K, Hornak V, Raleigh DP, Simmerling CL. J. Mol. Biol. 360 1094-1107 (2006)
  6. Predicting the effect of a point mutation on a protein fold: the villin and advillin headpieces and their Pro62Ala mutants. Piana S, Laio A, Marinelli F, Van Troys M, Bourry D, Ampe C, Martins JC. J. Mol. Biol. 375 460-470 (2008)
  7. Structural analysis of the conserved ubiquitin-binding motifs (UBMs) of the translesion polymerase iota in complex with ubiquitin. Burschowsky D, Rudolf F, Rabut G, Herrmann T, Peter M, Wider G. J. Biol. Chem. 286 1364-1373 (2011)
  8. A phosphorylation-induced conformation change in dematin headpiece. Jiang ZG, McKnight CJ. Structure 14 379-387 (2006)
  9. Hydrophobic core formation and dehydration in protein folding studied by generalized-ensemble simulations. Yoda T, Sugita Y, Okamoto Y. Biophys. J. 99 1637-1644 (2010)
  10. The expanding superfamily of gelsolin homology domain proteins. Ghoshdastider U, Popp D, Burtnick LD, Robinson RC. Cytoskeleton (Hoboken) 70 775-795 (2013)
  11. Identification of the PXW sequence as a structural gatekeeper of the headpiece C-terminal subdomain fold. Vermeulen W, Van Troys M, Bourry D, Dewitte D, Rossenu S, Goethals M, Borremans FA, Vandekerckhove J, Martins JC, Ampe C. J. Mol. Biol. 359 1277-1292 (2006)
  12. Advillin folding takes place on a hypersurface of small dimensionality. Piana S, Laio A. Phys. Rev. Lett. 101 208101 (2008)
  13. Solution structure of a small protein containing a fluorinated side chain in the core. Cornilescu G, Hadley EB, Woll MG, Markley JL, Gellman SH, Cornilescu CC. Protein Sci. 16 14-19 (2007)
  14. Gene expression patterns in a novel animal appendage: the sea urchin pluteus arm. Love AC, Andrews ME, Raff RA. Evol. Dev. 9 51-68 (2007)
  15. Implementation of pi-pi interactions in molecular dynamics simulation. Yuki H, Tanaka Y, Hata M, Ishikawa H, Neya S, Hoshino T. J Comput Chem 28 1091-1099 (2007)
  16. Crystallization of small proteins assisted by green fluorescent protein. Suzuki N, Hiraki M, Yamada Y, Matsugaki N, Igarashi N, Kato R, Dikic I, Drew D, Iwata S, Wakatsuki S, Kawasaki M. Acta Crystallogr. D Biol. Crystallogr. 66 1059-1066 (2010)
  17. The isolated sixth gelsolin repeat and headpiece domain of villin bundle F-actin in the presence of calcium and are linked by a 40-residue unstructured sequence. Smirnov SL, Isern NG, Jiang ZG, Hoyt DW, McKnight CJ. Biochemistry 46 7488-7496 (2007)
  18. Following easy slope paths on a free energy landscape: the case study of the Trp-cage folding mechanism. Marinelli F. Biophys. J. 105 1236-1247 (2013)
  19. Role of Drosophila gene dunc-115 in nervous system. Garcia MC, Abbasi M, Singh S, He Q. Invert. Neurosci. 7 119-128 (2007)
  20. Efficient high level expression of peptides and proteins as fusion proteins with the N-terminal domain of L9: application to the villin headpiece helical subdomain. Bi Y, Tang Y, Raleigh DP, Cho JH. Protein Expr. Purif. 47 234-240 (2006)
  21. Evolutionary Pareto-optimization of stably folding peptides. Gronwald W, Hohm T, Hoffmann D. BMC Bioinformatics 9 109 (2008)
  22. Advillin acts upstream of phospholipase C ϵ1 in steroid-resistant nephrotic syndrome. Rao J, Ashraf S, Tan W, van der Ven AT, Gee HY, Braun DA, Fehér K, George SP, Esmaeilniakooshkghazi A, Choi WI, Jobst-Schwan T, Schneider R, Schmidt JM, Widmeier E, Warejko JK, Hermle T, Schapiro D, Lovric S, Shril S, Daga A, Nayir A, Shenoy M, Tse Y, Bald M, Helmchen U, Mir S, Berdeli A, Kari JA, El Desoky S, Soliman NA, Bagga A, Mane S, Jairajpuri MA, Lifton RP, Khurana S, Martins JC, Hildebrandt F. J. Clin. Invest. 127 4257-4269 (2017)
  23. Competition between intradomain and interdomain interactions: a buried salt bridge is essential for villin headpiece folding and actin binding. Packer LE, Song B, Raleigh DP, McKnight CJ. Biochemistry 50 3706-3712 (2011)
  24. The F-actin-binding RapGEF GflB is required for efficient macropinocytosis in Dictyostelium. Inaba H, Yoda K, Adachi H. J. Cell. Sci. 130 3158-3172 (2017)
  25. Drosophila Dunc-115 mediates axon projection through actin binding. Roblodowski C, He Q. Invert. Neurosci. 17 2 (2017)
  26. F-actin-bundling sites are conserved in proteins with villin-type headpiece domains. George SP, Esmaeilniakooshkghazi A, Roy S, Khurana S. Mol Biol Cell 31 1857-1866 (2020)
  27. Steroidal glycoalkaloids from Solanum nigrum target cytoskeletal proteins: an in silico analysis. Ahmad R. PeerJ 7 e6012 (2019)


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