The PKA regulatory subunit from yeast forms a homotetramer: Low-resolution structure of the N-terminal oligomerization domain

Angelo, 1998, Molecular characterization of an anchor protein (AKAPCE) that binds the RI subunit (RCE) of type I protein kinase A from Caenorhabditis elegans, J. Biol. Chem., 273, 14633, 10.1074/jbc.273.23.14633 Banky, 1998, Dimerization/docking domain of the type Ialpha regulatory subunit of cAMP-dependent protein kinase. Requirements for dimerization and docking are distinct but overlapping, J. Biol. Chem., 273, 35048, 10.1074/jbc.273.52.35048 Banky, 2003, Related protein-protein interaction modules present drastically different surface topographies despite a conserved helical platform, J. Mol. Biol., 330, 1117, 10.1016/S0022-2836(03)00552-7 Benkert, 2009, QMEAN server for protein model quality estimation, Nucleic Acids Res., 37, W510, 10.1093/nar/gkp322 Boettcher, 2011, Realizing the allosteric potential of the tetrameric protein kinase A RIalpha holoenzyme, Structure, 19, 265, 10.1016/j.str.2010.12.005 Burgers, 2012, A small novel A-kinase anchoring protein (AKAP) that localizes specifically protein kinase A-regulatory subunit I (PKA-RI) to the plasma membrane, J. Biol. Chem., 287, 43789, 10.1074/jbc.M112.395970 Canaves, 2002, Classification and phylogenetic analysis of the cAMP-dependent protein kinase regulatory subunit family, J. Mol. Evol., 54, 17, 10.1007/s00239-001-0013-1 Carlson, 1996, The 44-kDa regulatory subunit of the Paramecium cAMP-dependent protein kinase lacks a dimerization domain and may have a unique autophosphorylation site sequence, J. Eukaryot. Microbiol., 43, 347, 10.1111/j.1550-7408.1996.tb03999.x Cheng, 2005, SCRATCH: a protein structure and structural feature prediction server, Nucleic Acids Res., 33, W72, 10.1093/nar/gki396 Cole, 2008, The Jpred 3 secondary structure prediction server, Nucleic Acids Res., 36, W197, 10.1093/nar/gkn238 Comeau, 2004, ClusPro: a fully automated algorithm for protein-protein docking, Nucleic Acids Res., 32, W96, 10.1093/nar/gkh354 Conrad, 2014, Nutrient sensing and signaling in the yeast Saccharomyces cerevisiae, FEMS Microbiol. Rev., 38, 254, 10.1111/1574-6976.12065 de Beer, 2014, PDBsum additions, Nucleic Acids Res., 42, D292, 10.1093/nar/gkt940 de Gunzburg, 1982, A cAMP-dependent protein kinase is present in differentiating Dictyostelium discoideum cells, EMBO J., 1, 1063, 10.1002/j.1460-2075.1982.tb01297.x Erickson, 2009, Size and shape of protein molecules at the nanometer level determined by sedimentation, gel filtration, and electron microscopy, Biol. Proced. Online, 11, 32, 10.1007/s12575-009-9008-x Eswar, N., Webb, B., Marti-Renom, M.A., Madhusudhan, M.S., Eramian, D., Shen, M.Y., Pieper, U., Sali, A., 2006. Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinform. (Chapter 5, Unit 5 6). Franke, 2009, DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering, J. Appl. Crystallogr., 42, 342, 10.1107/S0021889809000338 Galello, 2014, Interacting proteins of protein kinase A regulatory subunit in Saccharomyces cerevisiae, J. Proteomics, 109C, 261, 10.1016/j.jprot.2014.07.008 Gancedo, 2013, Biological roles of cAMP: variations on a theme in the different kingdoms of life, Biol. Rev. Camb. Philos. Soc., 88, 645, 10.1111/brv.12020 Garcia De La Torre, 2000, Calculation of hydrodynamic properties of globular proteins from their atomic-level structure, Biophys. J., 78, 719, 10.1016/S0006-3495(00)76630-6 Griffioen, 2000, Nutritional control of nucleocytoplasmic localization of cAMP-dependent protein kinase catalytic and regulatory subunits in Saccharomyces cerevisiae, J. Biol. Chem., 275, 1449, 10.1074/jbc.275.2.1449 Griffioen, 2001, Nucleocytoplasmic distribution of budding yeast protein kinase A regulatory subunit Bcy1 requires Zds1 and is regulated by Yak1-dependent phosphorylation of its targeting domain, Mol. Cell Biol., 21, 511, 10.1128/MCB.21.2.511-523.2001 Hadad, 2011, Drosophila spoonbill encodes a dual-specificity A-kinase anchor protein essential for oogenesis, Mech. Dev., 128, 471, 10.1016/j.mod.2011.09.002 Hausken, 1994, Type II regulatory subunit (RII) of the cAMP-dependent protein kinase interaction with A-kinase anchor proteins requires isoleucines 3 and 5, J. Biol. Chem., 269, 24245, 10.1016/S0021-9258(19)51074-2 Hixson, 1980, Characterization of a cyclic AMP-binding protein from bakers’ yeast. Identification as a regulatory subunit of cyclic AMP-dependent protein kinase, J. Biol. Chem., 255, 2137, 10.1016/S0021-9258(19)86004-0 Humphrey, 1996, VMD: visual molecular dynamics, J. Mol. Graph., 14, 27 Johnson, 1987, Expression in Escherichia coli of BCY1, the regulatory subunit of cyclic AMP-dependent protein kinase from Saccharomyces cerevisiae, Purification and characterization. J. Biol. Chem., 262, 8636 Johnson, 2001, Dynamics of cAMP-dependent protein kinase, Chem. Rev., 101, 2243, 10.1021/cr000226k Jones, 2012, Computational and structural characterisation of protein associations, Adv. Exp. Med. Biol., 747, 42, 10.1007/978-1-4614-3229-6_3 Kelley, 2009, Protein structure prediction on the Web: a case study using the Phyre server, Nat. Protocol, 4, 363, 10.1038/nprot.2009.2 Kinderman, 2006, A dynamic mechanism for AKAP binding to RII isoforms of cAMP-dependent protein kinase, Mol. Cell, 24, 397, 10.1016/j.molcel.2006.09.015 Kozin, 2001, Automated matching of high- and low-resolution structural models, J. Appl. Crystallogr., 34, 33, 10.1107/S0021889800014126 Kronberg, 2011, Characterization of the regulatory subunit of Yarrowia lipolytica cAMP-dependent protein kinase. Evidences of a monomeric protein, Arch. Biochem. Biophys., 509, 66, 10.1016/j.abb.2011.03.001 Li, 1995, Mutagenesis of the regulatory subunit (RII beta) of cAMP-dependent protein kinase II beta reveals hydrophobic amino acids that are essential for RII beta dimerization and/or anchoring RII beta to the cytoskeleton, J. Biol. Chem., 270, 1935, 10.1074/jbc.270.4.1935 Matthews, 2012, Dimers, oligomers, everywhere, Adv. Exp. Med. Biol., 747, 1, 10.1007/978-1-4614-3229-6_1 McGuffin, 2000, The PSIPRED protein structure prediction server, Bioinformatics, 16, 404, 10.1093/bioinformatics/16.4.404 McWilliam, 2013, Analysis Tool Web Services from the EMBL-EBI, Nucleic Acids Res., 41, W597, 10.1093/nar/gkt376 Mertens, 2010, Structural characterization of proteins and complexes using small-angle X-ray solution scattering, J. Struct. Biol., 172, 128, 10.1016/j.jsb.2010.06.012 Mutzel, 1987, Cloning and cDNA sequence of the regulatory subunit of cAMP-dependent protein kinase from Dictyostelium discoideum, Proc. Natl. Acad. Sci. USA, 84, 6, 10.1073/pnas.84.1.6 Mylonas, 2007, Accuracy of molecular mass determination of proteins in solution by small-angle X-ray scattering, J. Appl. Crystallogr., 40, 245, 10.1107/S002188980700252X Newlon, 1999, The molecular basis for protein kinase A anchoring revealed by solution NMR, Nat. Struct. Biol., 6, 222, 10.1038/6663 Paveto, 1989, Two different intrachain cAMP sites in the cAMP-dependent protein kinase of the dimorphic fungus Mucor rouxii, Eur. J. Biochem., 179, 429, 10.1111/j.1432-1033.1989.tb14571.x Peng, 2015, Spatial Organization in Protein Kinase A Signaling Emerged at the Base of Animal Evolution, J. Proteome Res., 14, 2976, 10.1021/acs.jproteome.5b00370 Pidoux, 2010, Specificity and spatial dynamics of protein kinase A signaling organized by A-kinase-anchoring proteins, J. Mol. Endocrinol., 44, 271, 10.1677/JME-10-0010 Portela, 2001, Evaluation of in vivo activation of protein kinase A under non-dissociable conditions through the overexpression of wild-type and mutant regulatory subunits in Saccharomyces cerevisiae, Microbiology, 147, 1149, 10.1099/00221287-147-5-1149 Receveur-Brechot, 2012, How random are intrinsically disordered proteins? A small angle scattering perspective, Curr. Protein Pept. Sci., 13, 55, 10.2174/138920312799277901 Rinaldi, 2010, Structure of yeast regulatory subunit: a glimpse into the evolution of PKA signaling, Structure, 18, 1471, 10.1016/j.str.2010.08.013 Rodrigues, 2012, KoBaMIN: a knowledge-based minimization web server for protein structure refinement, Nucleic Acids Res., 40, W323, 10.1093/nar/gks376 Sarma, 2010, Structure of D-AKAP2:PKA RI complex: insights into AKAP specificity and selectivity, Structure, 18, 155, 10.1016/j.str.2009.12.012 Schneidman-Duhovny, 2010, FoXS: a web server for rapid computation and fitting of SAXS profiles, Nucleic Acids Res., 38, W540, 10.1093/nar/gkq461 Schneidman-Duhovny, 2012, Integrative structural modeling with small angle X-ray scattering profiles, BMC Struct. Biol., 12, 17, 10.1186/1472-6807-12-17 Sherman, 1986 Siegel, 1966, Determination of molecular weights and frictional ratios of proteins in impure systems by use of gel filtration and density gradient centrifugation. Application to crude preparations of sulfite and hydroxylamine reductases, Biochim. Biophys. Acta, 112, 346, 10.1016/0926-6585(66)90333-5 Su, 1995, Regulatory subunit of protein kinase A: structure of deletion mutant with cAMP binding domains, Science, 269, 807, 10.1126/science.7638597 Svergun, 1992, Determination of the regularization parameter in indirect-transform methods using perceptual criteria, J. Appl. Crystallogr., 25, 495, 10.1107/S0021889892001663 Tasken, 2004, Localized effects of cAMP mediated by distinct routes of protein kinase A, Physiol. Rev., 84, 137, 10.1152/physrev.00021.2003 Taylor, 2005, Dynamics of signaling by PKA, Biochim. Biophys. Acta, 1754, 25, 10.1016/j.bbapap.2005.08.024 Toda, 1987, Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae, Mol. Cell Biol., 7, 1371, 10.1128/MCB.7.4.1371 Trevillyan, 1982, Isolation and properties of a cyclic AMP-binding protein from Neurospora. Evidence for its role as the regulatory subunit of cyclic AMP-dependent protein kinase, J. Biol. Chem., 257, 3978, 10.1016/S0021-9258(18)34879-8 Vigil, 2004, Differential effects of substrate on type I and type II PKA holoenzyme dissociation, Biochemistry, 43, 5629, 10.1021/bi0499157 Vigil, 2004, Conformational differences among solution structures of the type Ialpha, IIalpha and IIbeta protein kinase A regulatory subunit homodimers: role of the linker regions, J. Mol. Biol., 337, 1183, 10.1016/j.jmb.2004.02.028 Volkov, 2003, Uniqueness of ab initio shape determination in small-angle scattering, J. Appl. Crystallogr., 36, 860, 10.1107/S0021889803000268 Welch, 2010, Networking with AKAPs: context-dependent regulation of anchored enzymes, Mol. Interv., 10, 86, 10.1124/mi.10.2.6 Yachdav, 2014, PredictProtein–an open resource for online prediction of protein structural and functional features, Nucleic Acids Res., 42, W337, 10.1093/nar/gku366