An evolutionary conserved motif is responsible for Immunoglobulin heavy chain packing in the B cell membrane(388 views) Varriale S, Merlino A, Coscia MR, Mazzarella L, Oreste U
Molecular Phylogenetics And Evolution (ISSN: 1055-7903), 2010 Dec; 57(3): 1238-1244.
Keywords: Immunoglobulin Evolution, Immunoglobulin Heavy Chain, Immunoglobulin Isotypes, Molecular Dynamics, Popc Lipid Bilayer, Purifying Selection, Transmembrane Helix, Amino Acid Sequence, Animal, Article, B Lymphocyte, Chemical Structure, Computer Simulation, Genetic Selection, Molecular Genetics, Nucleotide Sequence, Phylogeny, Protein Tertiary Structure, Sequence Analysis, Vertebrate, B-Lymphocytes, Conserved Sequence, Models, Molecular Sequence Data, Protein Structure, Chondrichthyes, Mammalia,
Affiliations: *** IBB - CNR ***
Institute of Protein Biochemistry, CNR, Via P. Castellino 111, 80131 Napoli, Italy
Department of Chemistry University of Naples 'Federico II', Via Cintia, 80126 Napoli, Italy
Institute of Biostructures and Bioimages, CNR, Via Mezzocannone 16, 80100 Napoli, Italy
References: Bagos, P.G., Liakopoulos, T.D., Hamodrakas, S.J., Algorithms for incorporating prior topological information in HMMs: application to transmembrane proteins (2006) BMC Bioinf., 7, p. 18
Berendsen, H.J.C., Postma, J.P.M., van Gusteren, W.F., Di Nola, A., Haak, J.R., Molecular dynamics with coupling to an external bath (1984) J. Chem. Phys., 81, pp. 3684-3690
Call, M.E., Wucherpfennig, K.W., Common themes in the assembly and architecture of activating immune receptors (2007) Nature, 7, pp. 841-850
Campbell, K.S., Backstrom, B.T., Tiefenthaler, G., Palmer, E., CART: a conserved antigen receptor transmembrane motif (1994) Semin. Immunol., 6, pp. 393-410
The CCP4 suite: programs for protein crystallography (1994) Acta Crystallogr. Sect. D, 50, pp. 760-763. , Collaborative Computational Project Number 4
Crooks, G.E., Hon, G., Chandonia, J.M., Brenner, S.E., WebLogo: a sequence logo generator (2004) Genome Res., 14, pp. 1188-1190
Cuthbertson, J.M., Bond, P.J., Sansom, M.S., Transmembrane helix-helix interactions: comparative simulations of the glycophorin a dimer (2006) Biochemistry, 45, pp. 14298-14310
Darden, T., York, D., Pedersen, L., Particle mesh Ewald: An N_log(N) method for Ewald sums in large systems (1993) J. Chem. Phys., 98, pp. 10089-10092
Dawson, J.P., Weinger, J.S., Engelman, D.M., Motifs of serine and threonine can drive association of transmembrane helices (2002) J. Mol. Biol., 316, pp. 799-805
Felsenstein, J., (2004) Inferring Phylogenies, , Sinauer, Sunderland, MA
Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M.R., Appel, R.D., Bairoch, A., Protein identification and analysis tools on the ExPASy server (2005) The Proteomics Protocols Handbook, pp. 571-607. , Humana Press, J.M. Walker (Ed.)
Gazit, E., A possible role for pi-stacking in the self-assembly of amyloid fibrils (2002) FASEB J., 16, pp. 77-83
Gratkowski, H., Lear, J.D., DeGrado, W.F., Polar side chains drive the association of model transmembrane peptides (2001) Proc. Natl Acad. Sci. USA, 98, pp. 880-885
Guindon, S., Gascuel, O.A., A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood (2003) Syst. Biol., 52, pp. 696-704
Harrington, S.E., Ben-Tal, N., Structural determinants of transmembrane helical proteins (2009) Structure, 17, pp. 1092-1103
Henin, J., Pohorille, A., Chipot, C., Insights into the recognition and association of transmembrane alpha-helices. The free energy of alpha-helix dimerization in glycophorin A (2005) J. Am. Chem. Soc., 127, pp. 8478-8484
Hess, B., Bekker, H., Berendsen, H.J.C., Fraaije, J.G.E.M., LINCS: A linear constraint solver for molecular simulations (1997) J. Comp. Chem., 18, pp. 1463-1472
Hofmann, K., Stoffel, W., TMbase-A database of membrane spanning proteins segments (1993) Biol. Chem. Hoppe-Seyler, 374, p. 166
Jiang, S., Vakser, I.A., Shorter side chains optimize helix-helix packing (2004) Protein Sci., 13, pp. 1426-1429
Kabsch, W., Sander, C., Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features (1983) Biopolymers, 22, pp. 2577-2637
Kleiger, G., Grothe, R., Mallick, P., Eisenberg, D., GXXXG and AXXXA: common alphahelical interaction motifs in proteins, particularly in extremophiles (2002) Biochemistry, 41, pp. 5990-5997
Kosakovsky Pond, S.L., Frost, S.D., Not so different after all: a comparison of methods for detecting amino acid sites under selection (2005) Mol. Biol. Evol., 22, pp. 1208-1222
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Higgins, D.G., ClustalW and ClustalX version 2 (2007) Bioinformatics, 23 (21), pp. 2947-2948
Laskowski, R.A., MacArthur, M.W., Moss, M.D., Thornton, J.M., PROCHECK: a program to check the stereochemical quality of protein structures (1993) J. Appl. Cryst., 26, pp. 283-291
Lawrence, M.C., Colman, P.M., Shape complementarity at protein/protein interfaces (1993) J. Mol. Biol., 234, pp. 946-950
Le, S.Q., Gascuel, O., An improved general amino acid replacement matrix (2008) Mol. Biol. Evol., 25, pp. 1307-1320
Lemmon, M.A., Flanagan, J.M., Hunt, J.F., Adair, B.D., Bormann, B.J., Dempsey, C.E., Engelman, D.M., Glycophorin A dimerization is driven by specific interactions between transmembrane alpha-helices (1992) J. Biol. Chem., 267, pp. 7683-7689
MacKenzie, K.R., Prestegard, J.H., Engelman, D.M., A transmembrane helix dimer: structure and implications (1997) Science, 276, pp. 131-133
McGaughey, G.B., Gagné, M., Rappé, A.K., Pi-Stacking interactions. Alive and well in proteins (1998) J. Biol. Chem., 273, pp. 15458-15463
Merlino, A., Mazzarella, L., Di Fiore, A., Carannante, A., Notomista, E., Di Donato, A., Sica, F., The importance of dynamic effects on the enzyme activity: X-ray structure and molecular dynamics of onconase (2005) J. Biol. Chem., 280, pp. 17953-17960
Merlino, A., Esposito, L., Vitagliano, L., Polyglutamine repeats and beta-helix structure: molecular dynamics study (2006) Proteins, 63, pp. 918-927
Merlino, A., Variale, S., Coscia, M.R., Mazzarella, L., Oreste, U., Structure and dimerization of the teleost transmembrane immunoglobulin region (2008) J. Mol. Graph. Model., 27, pp. 401-407
Mottamal, M., Zhang, J., Lazaridis, T., Energetics of the native and non-native states of the glycophorin transmembrane helix dimer (2006) Proteins, 62, pp. 996-1009
Okada, T., Le Trong, I., Fox, B.A., Behnke, C.A., Stenkamp, R.E., Palczewski, K., X-Ray diffraction analysis of three-dimensional crystals of bovine rhodopsin obtained from mixed micelles (2000) J. Struct. Biol., 130, pp. 73-80
Pancer, Z., Saha, N.R., Kasamatsu, J., Suzuki, T., Amemiya, C.T., Kasahara, M., Cooper, M.D., Variable lymphocyte receptors in hagfish (2005) Proc. Natl Acad. Sci. USA, 102, pp. 9224-9229
Patel, A.B., Crocker, E., Reeves, P.J., Getmanova, E.V., Eilers, M., Khorana, H.G., Smith, S.O., Changes in interhelical hydrogen bonding upon rhodopsin activation (2005) J. Mol. Biol., 347, pp. 803-812
Prilusky, J., Eitan, B., Studying membrane proteins through the eyes of the genetic code revealed a strong uracil bias in their coding mRNAs (2009) Proc. Natl Acad. Sci. USA, 106, pp. 6662-6666
Rumfelt, L.L., Diaz, M., Lohr, R.L., Mochon, E., Flajnik, M.F., Unprecedented multiplicity of Ig transmembrane and secretory mRNA forms in the cartilaginous fish (2004) J. Immunol., 173, pp. 1129-1139
Schneider, D., Engelman, D.M., Motifs of two small residues can assist but are not sufficient to mediate transmembrane helix interactions (2004) J. Mol. Biol., 343, pp. 799-804
Schneider, T.D., Stephens, R.M., Sequence logos: a new way to display consensus sequences (1990) Nucleic Acids Res., 18, pp. 6097-6100
Senes, A., Gerstein, M., Engelman, D.M., Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with beta-branched residues at neighboring positions (2000) J. Mol. Biol., 296, pp. 921-936
Stewart, J.J., Lee, C.Y., Ibrahim, S., Watts, P., Shlomchik, M., Weigert, M., Litwin, S., Entropy analysis of immunoglobulin and T cell receptor (1997) Mol. Immunol., 34, pp. 1067-1082
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G., The CLUSTAL_X windows interface. Flexible strategies for multiple sequence alignment aided by quality analysis tools (1997) Nucleic Acids Res., 25, pp. 4876-4882
Vaccaro, L., Cross, K.J., Kleinjung, J., Straus, S.K., Thomas, D.J., Wharton, S.A., Skehel, J.J., Fraternali, F., Plasticity of influenza haemagglutinin fusion peptides and their interaction with lipid bilayers (2005) Biophys. J., 88, pp. 25-36
Vereshaga, Y.A., Volynsky, P.E., Pustovalova, J.E., Nolde, D.E., Arseniev, A.S., Efremov, R.G., Specificity of helix packing in transmembrane dimer of the cell death factor BNIP3: a molecular modeling study (2007) Proteins, 69, pp. 309-325
Walters, R.F., DeGrado, W.F., Helix-packing motifs in membrane proteins (2006) Proc. Natl Acad. Sci. USA, 103, pp. 13658-13663
Bagos, P. G., Liakopoulos, T. D., Hamodrakas, S. J., Algorithms for incorporating prior topological information in HMMs: application to transmembrane proteins (2006) BMC Bioinf., 7, p. 18
Berendsen, H. J. C., Postma, J. P. M., van Gusteren, W. F., Di Nola, A., Haak, J. R., Molecular dynamics with coupling to an external bath (1984) J. Chem. Phys., 81, pp. 3684-3690
Call, M. E., Wucherpfennig, K. W., Common themes in the assembly and architecture of activating immune receptors (2007) Nature, 7, pp. 841-850
Campbell, K. S., Backstrom, B. T., Tiefenthaler, G., Palmer, E., CART: a conserved antigen receptor transmembrane motif (1994) Semin. Immunol., 6, pp. 393-410
Crooks, G. E., Hon, G., Chandonia, J. M., Brenner, S. E., WebLogo: a sequence logo generator (2004) Genome Res., 14, pp. 1188-1190
Cuthbertson, J. M., Bond, P. J., Sansom, M. S., Transmembrane helix-helix interactions: comparative simulations of the glycophorin a dimer (2006) Biochemistry, 45, pp. 14298-14310
Dawson, J. P., Weinger, J. S., Engelman, D. M., Motifs of serine and threonine can drive association of transmembrane helices (2002) J. Mol. Biol., 316, pp. 799-805
Harrington, S. E., Ben-Tal, N., Structural determinants of transmembrane helical proteins (2009) Structure, 17, pp. 1092-1103
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Higgins, D. G., ClustalW and ClustalX version 2 (2007) Bioinformatics, 23 (21), pp. 2947-2948
Laskowski, R. A., MacArthur, M. W., Moss, M. D., Thornton, J. M., PROCHECK: a program to check the stereochemical quality of protein structures (1993) J. Appl. Cryst., 26, pp. 283-291
Lawrence, M. C., Colman, P. M., Shape complementarity at protein/protein interfaces (1993) J. Mol. Biol., 234, pp. 946-950
Le, S. Q., Gascuel, O., An improved general amino acid replacement matrix (2008) Mol. Biol. Evol., 25, pp. 1307-1320
Lemmon, M. A., Flanagan, J. M., Hunt, J. F., Adair, B. D., Bormann, B. J., Dempsey, C. E., Engelman, D. M., Glycophorin A dimerization is driven by specific interactions between transmembrane alpha-helices (1992) J. Biol. Chem., 267, pp. 7683-7689
MacKenzie, K. R., Prestegard, J. H., Engelman, D. M., A transmembrane helix dimer: structure and implications (1997) Science, 276, pp. 131-133
McGaughey, G. B., Gagn, M., Rapp, A. K., Pi-Stacking interactions. Alive and well in proteins (1998) J. Biol. Chem., 273, pp. 15458-15463
Patel, A. B., Crocker, E., Reeves, P. J., Getmanova, E. V., Eilers, M., Khorana, H. G., Smith, S. O., Changes in interhelical hydrogen bonding upon rhodopsin activation (2005) J. Mol. Biol., 347, pp. 803-812
Rumfelt, L. L., Diaz, M., Lohr, R. L., Mochon, E., Flajnik, M. F., Unprecedented multiplicity of Ig transmembrane and secretory mRNA forms in the cartilaginous fish (2004) J. Immunol., 173, pp. 1129-1139
Schneider, T. D., Stephens, R. M., Sequence logos: a new way to display consensus sequences (1990) Nucleic Acids Res., 18, pp. 6097-6100
Stewart, J. J., Lee, C. Y., Ibrahim, S., Watts, P., Shlomchik, M., Weigert, M., Litwin, S., Entropy analysis of immunoglobulin and T cell receptor (1997) Mol. Immunol., 34, pp. 1067-1082
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., Higgins, D. G., The CLUSTAL_X windows interface. Flexible strategies for multiple sequence alignment aided by quality analysis tools (1997) Nucleic Acids Res., 25, pp. 4876-4882
Vereshaga, Y. A., Volynsky, P. E., Pustovalova, J. E., Nolde, D. E., Arseniev, A. S., Efremov, R. G., Specificity of helix packing in transmembrane dimer of the cell death factor BNIP3: a molecular modeling study (2007) Proteins, 69, pp. 309-325
Walters, R. F., DeGrado, W. F., Helix-packing motifs in membrane proteins (2006) Proc. Natl Acad. Sci. USA, 103, pp. 13658-13663
Zhou, F. X., Cocco, M. J., Russ, W. P., Brunger, A. T., Engelman, D. M., Interhelical hydrogen bonding drives strong interactions in membrane proteins (2000) Nat. Struct. Biol., 7, pp. 154-160
An evolutionary conserved motif is responsible for Immunoglobulin heavy chain packing in the B cell membrane
All species of vertebrates synthesize immunoglobulin molecules, which differ in an number of aspects but also share a few common features responsible for their function, such as the presence of a transmembrane domain in the membrane bound form of the immunoglobulin heavy chain (IgTMD) that ensures communication with the signal transducing Ig alpha-Ig beta peptides. We have analyzed the gene sequence encoding the IgTMD of different heavy chain isotypes of very distant species, from shark to mammals. The IgTMD sequences show a high degree of sequence identity and their encoding nucleotide sequences were shown to be subject to purifying selection at most sites. We have built molecular models of seven IgTMDs from different vertebrate species and have investigated the formation of homodimer in a palmitoyl oleoyl phosphatidylcholine (POPC) lipid bilayer by molecular dynamics simulations. We found that the conserved FXXXFXXS/TXXXS motif, never observed to date in protein transmembrane chains, is responsible for the two heavy chains association through two pairs of Phe-Phe hydrophobic interactions and two pairs of Ser/Thr-Ser/Ser hydrogen bonds. This interaction pattern, which stabilizes the dimer conformation in the lipid bilayer, was unique, being different from any other pattern identified in transmembrane helices to date. (C) 2010 Elsevier Inc. All rights reserved.
An evolutionary conserved motif is responsible for Immunoglobulin heavy chain packing in the B cell membrane