Structural comparisons of calponin homology domains: implications for actin binding.

BACKGROUND The actin-binding site of several cytoskeletal proteins is comprised of two calponin homology (CH) domains in a tandem arrangement. As a single copy, the CH domain is also found in regulatory proteins in muscle and in signal-transduction proteins. The three-dimensional structures of three CH domains are known, but they have not yet clarified the molecular details of the interaction between actin filaments and proteins harbouring CH domains. RESULTS We have compared the crystal structure of a CH domain from beta-spectrin, which has been refined to 1.1 A resolution, with the two CH domains that constitute the actin-binding region of fimbrin. This analysis has allowed the construction of a structure-based sequence alignment of CH domains that can be used in further comparisons of members of the CH domain family. The study has also improved our understanding of the factors that determine domain architecture, and has led to discussion on the functional differences that seem to exist between subfamilies of CH domains, as regards binding to F-actin. CONCLUSIONS Our analysis supports biochemical data that implicate a surface centered at the last helix of the N-terminal CH domain as the most probable actin-binding site in cytoskeletal proteins. It is not clear whether the C-terminal domains of the tandem arrangement or the single CH domains have this function alone. This may imply that although the CH domains are homologous and have a conserved structure, they may have evolved to perform different functions.

[1]  T. Takenawa,et al.  Identification of a Phosphatidylinositol 4,5-Bisphosphate-binding Site in Chicken Skeletal Muscle α-Actinin (*) , 1996, The Journal of Biological Chemistry.

[2]  A. Fedorov,et al.  The structure of an actin-crosslinking domain from human fimbrin , 1997, Nature Structural Biology.

[3]  D. Branton,et al.  Interchain binding at the tail end of the Drosophila spectrin molecule. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[4]  J. Léger,et al.  Actin-dystrophin interface. , 1993, Biochemistry.

[5]  P. Kraulis A program to produce both detailed and schematic plots of protein structures , 1991 .

[6]  A. Moir,et al.  Binding sites involved in the interaction of actin with the N‐terminal region of dystrophin , 1992, FEBS letters.

[7]  C. Herberhold,et al.  The repeating segments of the F-actin cross-linking gelation factor (ABP-120) have an immunoglobulin-like fold , 1997, Nature Structural Biology.

[8]  M. Way,et al.  Evidence for functional homology in the F-actin binding domains of gelsolin and alpha-actinin: implications for the requirements of severing and capping , 1992, The Journal of cell biology.

[9]  V. Luzzati,et al.  Traitement statistique des erreurs dans la determination des structures cristallines , 1952 .

[10]  M Nilges,et al.  Functional diversity of PH domains: an exhaustive modelling study. , 1997, Folding & design.

[11]  J. Zou,et al.  Improved methods for building protein models in electron density maps and the location of errors in these models. , 1991, Acta crystallographica. Section A, Foundations of crystallography.

[12]  D. Tronrud Conjugate-direction minimization: an improved method for the refinement of macromolecules. , 1992, Acta crystallographica. Section A, Foundations of crystallography.

[13]  R. Huber,et al.  Accurate Bond and Angle Parameters for X-ray Protein Structure Refinement , 1991 .

[14]  E. Lane,et al.  Loss of plectin causes epidermolysis bullosa with muscular dystrophy: cDNA cloning and genomic organization. , 1996, Genes & development.

[15]  D. DeRosier,et al.  Evidence for a Conformational Change in Actin Induced by Fimbrin (N375) Binding , 1997, The Journal of cell biology.

[16]  S. Colowick,et al.  Methods in Enzymology , Vol , 1966 .

[17]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[18]  Z. Otwinowski,et al.  [20] Processing of X-ray diffraction data collected in oscillation mode. , 1997, Methods in enzymology.

[19]  C. Schutt,et al.  Plugging into actin's architectonic socket , 1997, Nature Structural Biology.

[20]  M. Saraste,et al.  Does Vav bind to F‐actin through a CH domain? , 1995, FEBS letters.

[21]  A. Pastore,et al.  Molecular mechanism of the calcium‐induced conformational change in the spectrin EF‐hands. , 1995, The EMBO journal.

[22]  D. Critchley,et al.  The identification and characterisation of an actin‐binding site in α‐actinin by mutagenesis , 1992, FEBS Letters.

[23]  G. N. Ramachandran,et al.  Conformation of polypeptides and proteins. , 1968, Advances in protein chemistry.

[24]  G. Bloom,et al.  IQGAP1, a Rac- and Cdc42-binding Protein, Directly Binds and Cross-links Microfilaments , 1997, The Journal of cell biology.

[25]  Collaborative Computational,et al.  The CCP4 suite: programs for protein crystallography. , 1994, Acta crystallographica. Section D, Biological crystallography.

[26]  J. Thornton,et al.  PROCHECK: a program to check the stereochemical quality of protein structures , 1993 .

[27]  C. Schutt,et al.  Structural studies on the ribbon-to-helix transition in profilin: actin crystals. , 1995, Biophysical journal.

[28]  K. Holmes,et al.  An atomic model of the unregulated thin filament obtained by X-ray fiber diffraction on oriented actin-tropomyosin gels. , 1995, Journal of molecular biology.

[29]  M. Saraste,et al.  Crystal structure of a calponin homology domain , 1997, Nature Structural Biology.

[30]  K. Diederichs Structural superposition of proteins with unknown alignment and detection of topological similarity using a six‐dimensional search algorithm , 1995, Proteins.

[31]  D. DeRosier,et al.  Determination of the alpha-actinin-binding site on actin filaments by cryoelectron microscopy and image analysis , 1994, The Journal of cell biology.

[32]  M Nilges,et al.  Solution structure of the spectrin repeat: a left-handed antiparallel triple-helical coiled-coil. , 1997, Journal of molecular biology.

[33]  S. Almo,et al.  The modular structure of actin-regulatory proteins. , 1998, Current opinion in cell biology.

[34]  D. Bordo,et al.  ENVIRON: a software package to compare protein three-dimensional structures with homologous sequences using local structural motifs , 1993, Comput. Appl. Biosci..

[35]  T. Stradal,et al.  CH domains revisited , 1998, FEBS letters.

[36]  G. Sheldrick,et al.  SHELXL: high-resolution refinement. , 1997, Methods in enzymology.

[37]  M. Gimona,et al.  The single CH domain of calponin is neither sufficient nor necessary for F-actin binding. , 1998, Journal of cell science.

[38]  J H Hartwig,et al.  Actin-binding proteins 1: spectrin superfamily. , 1994, Protein profile.

[39]  S V Evans,et al.  SETOR: hardware-lighted three-dimensional solid model representations of macromolecules. , 1993, Journal of molecular graphics.

[40]  W. Lehman,et al.  3-D image reconstruction of reconstituted smooth muscle thin filaments containing calponin: visualization of interactions between F-actin and calponin. , 1997, Journal of molecular biology.

[41]  S. Jones,et al.  Principles of protein-protein interactions. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[42]  A. McGough F-actin-binding proteins. , 1998, Current opinion in structural biology.

[43]  A. Adams,et al.  Genetic analysis of the fimbrin-actin binding interaction in Saccharomyces cerevisiae. , 1995, Genetics.

[44]  R. Goldman,et al.  Intermediate filaments and cytoplasmic networking: new connections and more functions. , 1997, Current opinion in cell biology.

[45]  J. Chant,et al.  An IQGAP-related protein controls actin-ring formation and cytokinesis in yeast , 1997, Current Biology.

[46]  G J Barton,et al.  ALSCRIPT: a tool to format multiple sequence alignments. , 1993, Protein engineering.

[47]  J. Derancourt,et al.  Characterization of the actin binding site on smooth muscle filamin. , 1994, The Journal of biological chemistry.