Interaction of two intrinsically disordered plant stress proteins (COR15A and COR15B) with lipid membranes in the dry state

Oldfield, 2005, Comparing and combining predictors of mostly disordered proteins, Biochemistry, 44, 1989, 10.1021/bi047993o Dyson, 2005, Intrinsically unstructured proteins and their functions, Nat. Rev. Mol. Cell Biol., 6, 197, 10.1038/nrm1589 Tompa, 2005, The interplay between structure and function in intrinsically unstructured proteins, FEBS Lett., 579, 3346, 10.1016/j.febslet.2005.03.072 Tompa, 2004, The role of structural disorder in the function of RNA and protein chaperones, FASEB J., 18, 1169, 10.1096/fj.04-1584rev Oldfield, 2005, Coupled folding and binding with α-helix-forming molecular recognition elements, Biochemistry, 44, 12454, 10.1021/bi050736e Wright, 2009, Linking folding and binding, Curr. Opin. Struct. Biol., 19, 31, 10.1016/j.sbi.2008.12.003 Dure, 1981, Developmental biochemistry of cottonseed embryogenesis and germination: changing messenger ribonucleic acid populations as shown by in vitro and in vivo protein synthesis, Biochemistry, 20, 4162, 10.1021/bi00517a033 Tunnacliffe, 2007, The continuing conundrum of LEA proteins, Naturwissenschaften, 94, 791, 10.1007/s00114-007-0254-y Thomashow, 1999, Plant cold acclimation: freezing tolerance genes and regulatory mechanisms, Annu. Rev. Plant Physiol. Plant Mol. Biol., 50, 571, 10.1146/annurev.arplant.50.1.571 Chinnusamy, 2007, Cold stress regulation of gene expression in plants, Trends Plant Sci., 12, 444, 10.1016/j.tplants.2007.07.002 van Buskirk, 2006, Arabidopsis transcription factors regulating cold acclimation, Physiol. Plant., 126, 72, 10.1111/j.1399-3054.2006.00625.x Vogel, 2005, Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis, Plant J., 41, 195, 10.1111/j.1365-313X.2004.02288.x Hajela, 1990, Molecular cloning and expression of cor (cold-regulated) genes in Arabidopsis thaliana, Plant Physiol., 93, 1246, 10.1104/pp.93.3.1246 Lin, 1992, DNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis gene cor15 and characterization of the COR15 polypeptide, Plant Physiol., 99, 519, 10.1104/pp.99.2.519 Nakayama, 2007, Arabidopsis Cor15am is a chloroplast stromal protein that has cryoprotective activity and forms oligomers, Plant Physiol., 144, 513, 10.1104/pp.106.094581 Wilhelm, 1993, Arabidopsis thaliana cor15b, an apparent homologue of cor15a, is strongly responsive to cold and ABA, but not drought, Plant Mol. Biol., 23, 1073, 10.1007/BF00021822 Hundertmark, 2008, LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana, BMC Genomics, 9, 118, 10.1186/1471-2164-9-118 Bray, 1993, Molecular responses to water deficit, Plant Physiol., 103, 1035, 10.1104/pp.103.4.1035 Artus, 1996, Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance, Proc. Natl Acad. Sci. USA, 93, 13404, 10.1073/pnas.93.23.13404 Steponkus, 1998, Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana, Proc. Natl Acad. Sci. USA, 95, 14570, 10.1073/pnas.95.24.14570 Gilmour, 1996, Purification and properties of Arabidopsis thaliana COR (Cold-Regulated) gene polypeptides COR15am and COR6.6 expressed in Escherichia coli, Plant Physiol., 111, 293, 10.1104/pp.111.1.293 Lin, 1992, A cold-regulated Arabidopsis gene encodes a polypeptide having potent cryoprotective activity, Biochem. Biophys. Res. Comm., 183, 1103, 10.1016/S0006-291X(05)80304-3 Nakayama, 2008, Evaluation of the protective activities of a late embryogenesis abundant (LEA) related protein, Cor15am, during various stresses in vitro, Biosci. Biotechnol. Biochem., 72, 1642, 10.1271/bbb.80214 Chakrabortee, 2007, Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function, Proc. Natl Acad. Sci. USA, 104, 18073, 10.1073/pnas.0706964104 Goyal, 2005, LEA proteins prevent protein aggregation due to water stress, Biochem. J., 388, 151, 10.1042/BJ20041931 Pouchkina-Stantcheva, 2007, Functional divergence of former alleles in an ancient asexual invertebrate, Science, 318, 268, 10.1126/science.1144363 Sakurai, 2005, RARGE: a large-scale database of RIKEN Arabidopsis resources ranging from transcriptome to phenome, Nucliec Acids Res., 33, D647, 10.1093/nar/gki014 Seki, 2002, Functional annotation of a full-length Arabidopsis cDNA collection, Science, 296, 141, 10.1126/science.1071006 Schägger, 1987, Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100kDa, Anal. Biochem., 166, 368, 10.1016/0003-2697(87)90587-2 Wetlaufer, 1962, Ultraviolet spectra of proteins and amino acids, Adv. Protein Chem., 17, 303, 10.1016/S0065-3233(08)60056-X Sreerama, 2000, Estimation of protein secondary structure from circular dichroism spectra: inclusion of denatured proteins with native proteins in the analysis, Anal. Biochem., 287, 243, 10.1006/abio.2000.4879 MacDonald, 1991, Small-volume extrusion apparatus for preparation of large, unilamellar vesicles, Biochim. Biophys. Acta, 1061, 297, 10.1016/0005-2736(91)90295-J Hincha, 2002, Specific effects of fructo- and gluco-oligosaccharides in the preservation of liposomes during drying, Glycobiology, 12, 103, 10.1093/glycob/12.2.103 Cacela, 2006, Low amounts of sucrose are sufficient to depress the phase transition temperature of dry phosphatidylcholine, but not for lyoprotection of liposomes, Biophys. J., 90, 2831, 10.1529/biophysj.105.074427 Popova, 2003, Intermolecular interactions in dry and rehydrated pure and mixed bilayers of phosphatidylcholine and digalactosyldiacylglycerol: a Fourier-transform infrared spectroscopy study, Biophys. J., 85, 1682, 10.1016/S0006-3495(03)74598-6 Crowe, 1997, Stabilization of dry membranes by mixtures of hydroxyethyl starch and glucose: the role of vitrification, Cryobiology, 35, 20, 10.1006/cryo.1997.2020 Popova, 2007, Effects of cholesterol on dry bilayers: interactions between phosphatidylcholine unsaturation and glycolopid or free sugar, Biophys. J., 93, 1204, 10.1529/biophysj.107.108886 Lassmann, 2006, Kalign, Kalignvu and Mumsa: web servers for multiple sequence alignment, Nucleic Acids Res., 34, W596, 10.1093/nar/gkl191 Waterhouse, 2009, Jalview Version 2 - a multiple sequence alignment editor and analysis workbench, Bioinformatics, 25, 1189, 10.1093/bioinformatics/btp033 Kneller, 1990, Improvements in protein secondary structure prediction by an enhanced neural network, J. Mol. Biol., 214, 171, 10.1016/0022-2836(90)90154-E Geourjon, 1995, SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments, Comput. Appl. Biosci., 11, 681 Pollastrii, 2002, Improving the prediction of protein secondary structure in three and eight classes using recurrent neural networks and profiles, Proteins, 47, 228, 10.1002/prot.10082 Cole, 2008, The Jpred 3 secondary structure prediction server, Nucleic Acids Res., 36, W197, 10.1093/nar/gkn238 Adamczak, 2005, Combining prediction of secondary structure and solvent accessibility in proteins, Proteins, 59, 467, 10.1002/prot.20441 Burgess, 1974, Analysis of conformations of amino acid residues and prediction of backbone topography in proteins, Israel J. Chem., 2, 239, 10.1002/ijch.197400022 Deleage, 1987, An algorithm for secondary structure prediction based on class prediction, Protein Eng., 1, 289, 10.1093/protein/1.4.289 King, 1996, Identification and application of the concepts important for accurate and reliable protein secondary structure prediction, Protein Sci., 5, 2298, 10.1002/pro.5560051116 Garnier, 1996, GOR method for predicting protein secondary structure from amino acid sequence, Meth. Enzymol., 266, 97 Garnier, 1978, Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins, J. Mol. Biol., 120, 97, 10.1016/0022-2836(78)90297-8 Holley, 1989, Protein secondary structure prediction with neural networks, Proc. Natl Acad. Sci. USA, 86, 152, 10.1073/pnas.86.1.152 King, 1990, Machine learning approach for the prediction of protein secondary structure, J. Mol. Biol., 216, 441, 10.1016/S0022-2836(05)80333-X Gautier, 2008, HELIQUEST: a web server to screen sequences with specific α-helical properties, Bioinformatics, 15, 2101, 10.1093/bioinformatics/btn392 Kovacs, 2008, Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins, Plant Physiol., 147, 381, 10.1104/pp.108.118208 Webb, 1996, Effects of COR6.6 and COR15am polypeptides encoded by cor (cold-regulated) genes of Arabidopsis thaliana on dehydration-induced phase transitions of phospholipid membranes, Plant Physiol., 111, 301, 10.1104/pp.111.1.301 Webb, 1991, Biochemical and biophysical properties of thylakoid acyl lipids, Biochim. Biophys. Acta, 1060, 133, 10.1016/S0005-2728(09)91002-7 Aurell Wistrom, 1989, Direct transition of dioleoylphosphatidylethanolamine from lamellar gel to inverted hexagonal phase caused by trehalose, Biochim. Biophys. Acta, 984, 238, 10.1016/0005-2736(89)90222-8 Mantsch, 1991, Phospholipid phase transitions in model and biological membranes as studied by infrared spectroscopy, Chem. Phys. Lipids, 57, 213, 10.1016/0009-3084(91)90077-O Seddon, 1990, Structure of the inverted hexagonal (HII) phase, and non-lamellar phase transitions of lipids, Biochim. Biophys. Acta, 1031, 1, 10.1016/0304-4157(90)90002-T Segrest, 1992, The amphipathic helix in the exchangeable apolipoproteins: a review of secondary structure and function, J. Lipid Res., 35, 141, 10.1016/S0022-2275(20)41536-6 Schiffer, 1967, Use of helical wheels to represent the structures of proteins and to identify segments with helical potential, Biophys. J., 7, 121, 10.1016/S0006-3495(67)86579-2 Bies-Etheve, 2008, Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana, Plant Mol. Biol., 67, 107, 10.1007/s11103-008-9304-x Mouillon, 2006, Structural investigation of disordered stress proteins. Comparison of full-length dehydrins with isolated peptides of their conserved segments, Plant Physiol., 141, 638, 10.1104/pp.106.079848 Boudet, 2006, Comparative analysis of the heat stable proteome of radicles of Medicago truncatula seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance, Plant Physiol., 140, 1418, 10.1104/pp.105.074039 Goyal, 2003, Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein, J. Biol. Chem., 278, 12977, 10.1074/jbc.M212007200 Shih, 2004, Gene cloning and characterization of a soybean (Glycine max L.) LEA protein, GmPM16, Plant Mol. Biol., 56, 689, 10.1007/s11103-004-4680-3 Tolleter, 2007, Structure and function of a mitochondrial late embryogenesis abundant protein are revealed by desiccation, Plant Cell, 19, 1580, 10.1105/tpc.107.050104 Wolkers, 2001, Isolation and characterization of a D-7 LEA protein from pollen that stabilizes glasses in vitro, Biochim. Biophys. Acta, 1544, 196, 10.1016/S0167-4838(00)00220-X Hristova, 1999, An amphipathic α-helix at a membrane interface: a structural study using a novel X-ray diffraction method, J. Mol. Biol., 290, 99, 10.1006/jmbi.1999.2840 Mishra, 1994, Interactions of synthetic peptide analogs of the class A amphipathic helix with lipids, J. Biol. Chem., 289, 7185, 10.1016/S0021-9258(17)37266-6 Segrest, 1990, Amphipathic helix motif: classes and properties, Proteins, 8, 103, 10.1002/prot.340080202 Dure, 1993, A repeating 11-mer amino acid motif and plant desiccation, Plant J., 3, 363, 10.1046/j.1365-313X.1993.t01-19-00999.x Li, 2009, Desiccation induced structural alterations in a 66-amino acid fragment of an anhydrobiotic nematode late embryogenesis abundant (LEA) protein, Biomacromolecules, 10, 1469, 10.1021/bm9002688 Hincha, 2006, Effects of sugars on the stability of lipid membranes during drying, vol. 3, 189 Oliver, 2002, Looking beyond sugars: the role of amphiphilic solutes in preventing adventitious reactions in anhydrobiotes at low water contents, Comp. Biochem. Physiol., 131A, 515, 10.1016/S1095-6433(01)00514-1 Mouillon, 2008, Mimicking the plant cell interior under water stress by macromolecular crowding: disordered dehydrin proteins are highly resistant to structural collapse, Plant Physiol., 148, 1925, 10.1104/pp.108.124099 Tompa, 2005, Structural disorder throws new light on moonlighting, Trends Biochem. Sci., 30, 484, 10.1016/j.tibs.2005.07.008 Kalign: http://www.ebi.ac.uk/Tools/kalign/index.html. NNpredict: http://www.cmpharm.ucsf.edu/nomi/nnpredict.html. SOPMA: http://npsa-pbil.ibcp.fr/cgi-bin/npsa_automat.pl?page=/NPSA/npsa_sopma.html. SSPro8: http://scratch.proteomics.ics.uci.edu/. JPred: http://www.compbio.dundee.ac.uk/www-jpred/. Sable2: http://sable.cchmc.org/. SDSC Biology Workbench: http://workbench.sdsc.edu/. Helical wheel diagrams: http://heliquest.ipmc.cnrs.fr/cgi-bin/ComputParams.py.