Comprehensive analysis of all triple helical repeats in beta-spectrins reveals patterns of selective evolutionary conservation

• Autorzy: Baines A J
• Języki publikacji: EN

Abstrakty

EN

The spectrin superfamily (spectrin, α-actinin, utrophin and dystrophin) has in common a triple helical repeating unit of ~106 amino acid residues. In spectrin, α and β chains contain multiple copies of this repeat. β-spectrin chains contain the majority of binding activities in spectrin and are essential for animal life. Canonical β-spectrins have 17 repeats; β-heavy spectrins have 30. Here, the repeats of five human β-spectrins, plus β-spectrins from several other vertebrates and invertebrates, have been analysed. Repeats 1, 2, 14 and 17 in canonical β are highly conserved between invertebrates and vertebrates, and repeat 8 in some isoforms. This is consistent with conservation of critical functions, since repeats 1, 2 and 17 bind α-spectrin. Repeats 1 of β-spectrins are not always detected by SMART or Pfam tools. A profile hidden Markov model of β-spectrin repeat 1 detects α-actinins, but not utrophin or dystrophin. Novel examples of repeat 1 were detected in the spectraplakins MACF1, BPAG1 and plectin close to the actin-binding domain. Ankyrin binds to the C-terminal portion of repeat 14; the high conservation of this entire repeat may point to additional, undiscovered ligand-binding activities. This analysis indicates that the basic triple helical repeat pattern was adapted early in the evolution of the spectrin superfamily to encompass essential binding activities, which characterise individual repeats in proteins extant today.

Słowa kluczowe

EN

domain; beta-spectrin chain; alpha-actinin; spectrin; molecular evolution; cytoskeleton; dystrophin; utrophin; cellular function; amino acid

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2003
• Tom: 08
• Numer: 1
• Opis fizyczny: p.195-214,fig.

Twórcy

autor

Baines A J

• University of Kent, Canterbury, CT2 7NJ, U.K.

Bibliografia

• 1.Viel, A. Alpha-actinin and spectrin structures: an unfolding family story. FEBS Lett. 460 (1999) 391-394.
• 2.Thomas, G.H., Newbern, E.C., Korte, C.C., Bales, M.A., Muse, S.V., Clark, A.G. and Kiehart, D.P. Intragenic duplication and divergence in the spectrin superfamily of proteins. Mol. Biol. Evol. J. 14 (1997) 1285-1295.
• 3.Pascual, J., Castresana, J. and Saraste, M. Evolution of the spectrin repeat. Bioessays 19 (1997) 811-817.
• 4.Bennett, V. and Baines, AJ. Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 81 (2001) 1353-1392.
• 5.Roper, K., Gregory, S.L. and Brown, N.H. The 'Spectraplakins': cytoskeletal giants with characteristics of both spectrin and plakin families. J. Cell Sci. 115(2002) 4215-4225.
• 6.Djinovic-Carugo, K., Gautel, M., Ylanne, J. and Young, P. The spectrin repeat: a structural platform for cytoskeletal protein assemblies. FEBS Lett. 513 (2002)119-123.
• 7.Schultz, J., Milpetz, F., Bork, P. and Ponting, C.P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. USA 95 (1998) 5857-5864.
• 8.Bateman, A., Birney, E., Cerruti, L., Durbin, R., Etwiller, L., Eddy, S.R., Griffiths-Jones, S., Howe, K.L., Marshall, M. and Sonnhammer, E.L. The Pfam protein families database. Nucleic Acids Res. 30 (2002) 276-280.
• 9.Speicher, D.W. and Marchesi, V.T. Erythrocyte spectrin is comprised of many homologous triple helical segments. Nature 311 (1984) 177-180.
• 10.Ylanne, J., Scheffzek, K., Young, P. and Saraste, M. Crystal structure of the alpha-actinin rod reveals an extensive torsional twist. Structure (Camb) 9 (2001) 597-604.
• 11.Kennedy, S.P., Warren, S.L., Forget, B.G. and Morrow, J.S. Ankyrin binds to the 15th repetitive unit of erythroid and nonerythroid beta-spectrin. J. Cell Biol. 115 (1991) 267-277.
• 12.Neill, G.W. and Crompton, M.R. Binding of the merlin-I product of the neurofibromatosis type 2 tumour suppressor gene to a novel site in beta-fodrin is regulated by association between merlin domains. Biochem. J. 358 (2001) 727-735.
• 13.Scoles, D.R., Huynh, D.P., Morcos, P.A., Coulsell, E.R., Robinson, N.G., Tamanoi, F. and Pulst, S.M. Neurofibromatosis 2 tumour suppressor schwannomin interacts with betaII- spectrin. Nat. Genet. 18 (1998) 354- 349.
• 14.Sakaguchi, G., Orita, S., Naito, A., Maeda, M., Igarashi, H., Sasaki, T. and Takai, Y. A novel brain-specific isoform of beta spectrin: isolation and its interaction with Munc 13. Biochem. Biophys. Res. Commun. 248 (1998) 846-851.
• 15.Li, X. and Bennett, V. Identification of the spectrin subunit and domains required for formation of spectrin/adducin/actin complexes. J. Biol. Chem. 271 (1996) 15695-15702.
• 16.Harper, S.Q., Crawford, R.W., DelloRusso, C. and Chamberlain, J.S. Spectrin-like repeats from dystrophin and alpha-actinin-2 are not functionally interchangeable. Hum. Mol. Genet. 11 (2002) 1807-1815.
• 17.Harper, S.L., Begg, G.E. and Speicher, D.W. Role of terminal nonhomologous domains in initiation of human red cell spectrin dimerization. Biochemistry 40 (2001) 9935-9943.
• 18.Begg, G.E., Harper, S.L., Morris, M.B. and Speicher, D.W. Initiation of spectrin dimerization involves complementary electrostatic interactions
• between paired triple-helical bundles. J. Biol. Chem. 275 (2000) 3279- 3287.
• 19. Speicher, D.W., DeSilva, T.M., Speicher, K.D., Ursitti, J.A.,Hembach, P. and Weglarz, M. Location of the human red cell spectrin tetramer binding site and detection of a related "closed" hairpin loop dimer using proteolytic footprinting. J. Biol. Chem. 268 (1993) 4227-4235.
• 20. Nicolas, G., Pedroni, S., Fournier, C., Gautero, H., Craescu, C., Dhermy, D. and Lecomte, M.C. Spectrin self-association site: characterization and study of
• beta-spectrin mutations associated with hereditary elliptocytosis. Biochem. J. 332 (1998) 81-89.
• 21. Bignone, P. and Baines, A.J. Spectrin alpha-II and beta-II isoforms interact with high affinity at the tetramerization site. Biochemistry (2003) in press.
• 22. Hayes, N.V., Scott, C., Heerkens, E., Ohanian, V., Maggs, A.M., Pinder, J.C., Kordeli, E. and Baines, A.J. Identification of a novel C-terminal variant of beta II spectrin: two isoforms of beta II spectrin have distinct intracellular locations and activities. J. Cell Sci. 113 (2000) 2023-2034.
• 23. Hayes, N.V., Phillips, G.W., Carden, MJ. and Baines, A.J. Definition of a sequence unique in beta II spectrin required for its axon-specific interaction with fodaxin (A60). J. Neurochem. 68 (1997) 1686-1695.
• 24. Muse, S.V., Clark, A.G. and Thomas, G.H. Comparisons of the nucleotide substitution process among repetitive segments of the alpha- and beta- spectrin genes. J. Mol. Evol. 44 (1997) 492-500.
• 25. Thomas, G. Molecular evolution of spectrin repeats. Bioessays 20 (1998) 600.
• 26. McKeown, C., Praitis, V. and Austin, J. sma-1 encodes a betaH-spectrin homolog required for Caenorhabditis elegans morphogenesis. Development 125 (1998) 2087-2098.
• 27. Stabach, P.R. and Morrow, J.S. Identification and characterization of beta V spectrin, a mammalian ortholog of Drosophila beta H spectrin. J. Biol. Chem. 275 (2000) 21385-21395.
• 28. Rice, P., Longden, I. and Bleasby, A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16 (2000) 276-277.
• 29. Genetics Computer Group, Program Manual for the Wisconsin Package, Version 8. 1994, 575 Science Drive, Madison, Wisconsin, USA 53711.
• 30. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410.
• 31. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882.
• 32. Altschul, S.F., Madden, T.L.,Schaffer, A.A, Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389- 3402.
• 33.Eddy, S.R. HMMER: Profile hidden Markov models for biological sequence analysis (http://hmmer.wustl.edu/). (2001).
• 34.McGuffin, L.J., Bryson, K. and Jones, D.T. The PSIPRED protein structure prediction server. Bioinformatics 16 (2000) 404-405.
• 35.Kelley, L.A., MacCallum, R.M. and Sternberg, M.J. Enhanced genome annotation using structural profiles in the program 3D- PSSM. J. Mol. Biol. 299 (2000) 499-520.
• 36.Kraulis, P.J. Molscript - a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24 (1991) 946-950.
• 37.Grum, V.L., Li, D., MacDonald, R.I. and Mondragon, A. Structures of two repeats of spectrin suggest models of flexibility. Cell 98 (1999) 523-535.
• 38.Cuff, J.A. and Barton, G.J. Application of multiple sequence alignment profiles to improve protein secondary structure prediction. Proteins 40 (2000) 502-511.
• 39.Gimona, M., Djinovic-Carago, K., Kranewitter, W.J. and Winder, S.J. Functional plasticity of CH domains. FEBS Lett. 513 (2002) 98-106.
• 40.Kordeli, E., Ludosky, M.A., Deprette, C., Frappier, T. and Cartaud, J. AnkyrinG is associated with the postsynaptic membrane and the sarcoplasmic reticulum in the skeletal muscle fiber. J. Cell Sci. 111 (1998) 2197-2207.
• 41.Moores, C.A. and Kendrick-Jones, J. Biochemical characterisation of the actin-binding properties of utrophin. Cell Motil. Cytoskeleton 46 (2000) 116-128.
• 42.Moores, C.A., Keep, N.H. and Kendrick-Jones, J. Structure of the utrophin actin-binding domain bound to F-actin reveals binding by an induced fit mechanism. J. Mol. Biol. 297 (2000) 465-480.
• 43.Gong, T.W., Besirli, C.G. and Lomax, M.I. MACF1 gene structure: a hybrid of plectin and dystrophin. Mamm. Genome 12 (2001) 852-861.
• 44.Leung, C.L., Green, K.J. and Liem, R.K. Plakins: a family of versatile cytolinker proteins. Trends Cell. Biol. 12 (2002) 37-45.
• 45.Tang, H.Y., Chaffotte, A.F. and Thacher, S.M. Structural analysis of the predicted coiled-coil rod domain of the cytoplasmic bullous pemphigoid antigen (BPAG1). Empirical localization of the N-terminal globular domain-rod boundary. J. Biol. Chem. 271 (1996) 9716-9722.
• 46.Viel, A. and Branton, D. Interchain binding at the tail end of the Drosophila spectrin molecule. Proc. Natl. Acad. Sci. USA 91 (1994) 10839-10843.
• 47.Sihag, R.K. Brain beta-spectrin phosphorylation: phosphate analysis and identification of threonine-347 as a heparin-sensitive protein kinase phosphorylation site. J. Neurochem. 71 (1998) 2220-2228.