Spatial Organization in Protein Kinase A Signaling Emerged at the Base of Animal Evolution

Journal of Proteome Research

Volumn 14, Issue 7, 2015, Pages 2976-2987

  Peng, Mao ^a,b,d   Aye, Thin Thin ^a,b   Snel, Berend ^c   Van Breukelen, Bas ^a,b   Scholten, Arjen ^a,b   Heck, Albert J R ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

^d MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

AKAP; evolution; PKA; proteomics; RIIa

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE CATALYTIC SUBUNIT; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT; ENZYME VARIANT; HOLOENZYME; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; CELLULAR DISTRIBUTION; COMPUTER MODEL; DIMERIZATION; ENZYME ACTIVITY; ENZYME BINDING; EUKARYOTE; EVOLUTION; LIQUID CHROMATOGRAPHY; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEOMICS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; AMINO ACID SEQUENCE; ANIMAL; CELL FRACTIONATION; ENZYME ACTIVE SITE; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL EVOLUTION; CATALYTIC DOMAIN; CONSERVED SEQUENCE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEOMICS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS;

EID: 84940068373     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00370     Document Type: Article

References (78)

1. Scott, J. D.; Pawson, T. Cell signaling in space and time: where proteins come together and when theyre apart Science 2009, 326, 1220-4
2. Wong, W.; Scott, J. D. AKAP signalling complexes: focal points in space and time Nat. Rev. Mol. Cell Biol. 2004, 5, 959-70
3. Good, M. C.; Zalatan, J. G.; Lim, W. A. Scaffold proteins: hubs for controlling the flow of cellular information Science 2011, 332, 680-6
4. Lim, W. A.; Pawson, T. Phosphotyrosine signaling: evolving a new cellular communication system Cell 2010, 142, 661-7
5. Muller, J.; Ory, S.; Copeland, T.; Piwnica-Worms, H.; Morrison, D. K. C-TAK1 regulates Ras signaling by phosphorylating the MAPK scaffold, KSR1 Mol. Cell 2001, 8, 983-93
6. Sutherland, E. W.; Rall, T. W. Fractionation and characterization of a cyclic adenine ribonucleotide formed by tissue particles J. Biol. Chem. 1958, 232, 1077-91
7. Taylor, S. S.; Ilouz, R.; Zhang, P.; Kornev, A. P. Assembly of allosteric macromolecular switches: lessons from PKA Nat. Rev. Mol. Cell Biol. 2012, 13, 646-58
8. Corbin, J. D.; Soderling, T. R.; Park, C. R. Regulation of adenosine 3′,5′-monophosphate-dependent protein kinase. I. Preliminary characterization of the adipose tissue enzyme in crude extracts J. Biol. Chem. 1973, 248, 1813-21
9. Scholten, A.; Aye, T. T.; Heck, A. J. A multi-angular mass spectrometric view at cyclic nucleotide dependent protein kinases: in vivo characterization and structure/function relationships Mass Spectrom. Rev. 2008, 27, 331-53
10. Canaves, J. M.; Taylor, S. S. Classification and phylogenetic analysis of the cAMP-dependent protein kinase regulatory subunit family J. Mol. Evol. 2002, 54, 17-29
11. Vleugel, M.; Hoogendoorn, E.; Snel, B.; Kops, G. J. Evolution and function of the mitotic checkpoint Dev. Cell 2012, 23, 239-50
12. Altschul, S. F.; Gish, W.; Miller, W.; Myers, E. W.; Lipman, D. J. Basic local alignment search tool J. Mol. Biol. 1990, 215, 403-10
13. Katoh, K.; Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability Mol. Biol. Evol. 2013, 30, 772-80
14. Stamatakis, A.; Ludwig, T.; Meier, H. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees Bioinformatics 2005, 21, 456-63
15. Eddy, S. R. Accelerated profile HMM searches PLoS Comput. Biol. 2011, 7, e1002195
16. Letunic, I.; Bork, P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation Bioinformatics 2007, 23, 127-8
17. Letunic, I.; Doerks, T.; Bork, P. SMART 7: recent updates to the protein domain annotation resource Nucleic Acids Res. 2012, 40, D302-5
18. Punta, M.; Coggill, P. C.; Eberhardt, R. Y.; Mistry, J.; Tate, J.; Boursnell, C.; Pang, N.; Forslund, K.; Ceric, G.; Clements, J.; Heger, A.; Holm, L.; Sonnhammer, E. L.; Eddy, S. R.; Bateman, A.; Finn, R. D. The Pfam protein families database Nucleic Acids Res. 2012, 40, D290-301
19. Wilson, D.; Pethica, R.; Zhou, Y.; Talbot, C.; Vogel, C.; Madera, M.; Chothia, C.; Gough, J. SUPERFAMILY-sophisticated comparative genomics, data mining, visualization and phylogeny Nucleic Acids Res. 2009, 37, D380-6
20. Mackey, A. J.; Haystead, T. A.; Pearson, W. R. Getting more from less: algorithms for rapid protein identification with multiple short peptide sequences Mol. Cell. Proteomics 2002, 1, 139-47
21. Bailey, T. L.; Boden, M.; Buske, F. A.; Frith, M.; Grant, C. E.; Clementi, L.; Ren, J.; Li, W. W.; Noble, W. S. MEME SUITE: tools for motif discovery and searching Nucleic Acids Res. 2009, 37, W202-8
22. Kovanich, D.; van der Heyden, M. A.; Aye, T. T.; van Veen, T. A.; Heck, A. J.; Scholten, A. Sphingosine kinase interacting protein is an A-kinase anchoring protein specific for type I cAMP-dependent protein kinase ChemBioChem 2010, 11, 963-71
23. Burgers, P. P.; van der Heyden, M. A.; Kok, B.; Heck, A. J.; Scholten, A. A systematic evaluation of protein kinase A-A-kinase anchoring protein interaction motifs Biochemistry 2015, 54, 11-21
24. Hou, T.; Li, Y.; Wang, W. Prediction of peptides binding to the PKA RIIalpha subunit using a hierarchical strategy Bioinformatics 2011, 27, 1814-21
25. Savidor, A.; Donahoo, R. S.; Hurtado-Gonzales, O.; Land, M. L.; Shah, M. B.; Lamour, K. H.; McDonald, W. H. Cross-species global proteomics reveals conserved and unique processes in Phytophthora sojae and Phytophthora ramorum Mol. Cell. Proteomics 2008, 7, 1501-16
26. Aye, T. T.; Mohammed, S.; van den Toorn, H. W.; van Veen, T. A.; van der Heyden, M. A.; Scholten, A.; Heck, A. J. Selectivity in enrichment of cAMP-dependent protein kinase regulatory subunits type I and type II and their interactors using modified cAMP affinity resins Mol. Cell. Proteomics 2009, 8, 1016-28
27. Dunn, B.; Wobbe, C. R. Preparation of protein extracts from yeast. In Current Protocols in Molecular Biology; Ausubel, F. M., Ed.; J. Wiley: New York, 2001.
28. Betapudi, V.; Mason, C.; Licate, L.; Egelhoff, T. T. Identification and characterization of a novel alpha-kinase with a von Willebrand factor A-like motif localized to the contractile vacuole and Golgi complex in Dictyostelium discoideum Mol. Biol. Cell 2005, 16, 2248-62
29. Anand, G. S.; Krishnamurthy, S.; Bishnoi, T.; Kornev, A.; Taylor, S. S.; Johnson, D. A. Cyclic AMP- and (Rp)-cAMPS-induced conformational changes in a complex of the catalytic and regulatory (RI{alpha}) subunits of cyclic AMP-dependent protein kinase Mol. Cell. Proteomics 2010, 9, 2225-37
30. Benevento, M.; Di Palma, S.; Snijder, J.; Moyer, C. L.; Reddy, V. S.; Nemerow, G. R.; Heck, A. J. Adenovirus composition, proteolysis, and disassembly studied by in-depth qualitative and quantitative proteomics J. Biol. Chem. 2014, 289, 11421-30
31. Cox, J.; Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat. Biotechnol. 2008, 26, 1367-72
32. Mellacheruvu, D.; Wright, Z.; Couzens, A. L.; Lambert, J. P.; St-Denis, N. A.; Li, T.; Miteva, Y. V.; Hauri, S.; Sardiu, M. E.; Low, T. Y.; Halim, V. A.; Bagshaw, R. D.; Hubner, N. C.; Al-Hakim, A.; Bouchard, A.; Faubert, D.; Fermin, D.; Dunham, W. H.; Goudreault, M.; Lin, Z. Y.; Badillo, B. G.; Pawson, T.; Durocher, D.; Coulombe, B.; Aebersold, R.; Superti-Furga, G.; Colinge, J.; Heck, A. J.; Choi, H.; Gstaiger, M.; Mohammed, S.; Cristea, I. M.; Bennett, K. L.; Washburn, M. P.; Raught, B.; Ewing, R. M.; Gingras, A. C.; Nesvizhskii, A. I. The CRAPome: a contaminant repository for affinity purification-mass spectrometry data Nat. Methods 2013, 10, 730-6
33. Carr, D. W.; Stofko-Hahn, R. E.; Fraser, I. D.; Bishop, S. M.; Acott, T. S.; Brennan, R. G.; Scott, J. D. Interaction of the regulatory subunit (RII) of cAMP-dependent protein kinase with RII-anchoring proteins occurs through an amphipathic helix binding motif J. Biol. Chem. 1991, 266, 14188-92
34. Li, X.; Li, H. P.; Amsler, K.; Hyink, D.; Wilson, P. D.; Burrow, C. R. PRKX, a phylogenetically and functionally distinct cAMP-dependent protein kinase, activates renal epithelial cell migration and morphogenesis Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 9260-5
35. Soberg, K.; Jahnsen, T.; Rognes, T.; Skalhegg, B. S.; Laerdahl, J. K. Evolutionary paths of the cAMP-dependent protein kinase (PKA) catalytic subunits PLoS One 2013, 8, e60935
36. Bridges, D.; Fraser, M. E.; Moorhead, G. B. Cyclic nucleotide binding proteins in the Arabidopsis thaliana and Oryza sativa genomes BMC Bioinf. 2005, 6, 6
37. Hanks, S. K.; Hunter, T. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification FASEB J. 1995, 9, 576-96
38. Cheng, X.; Ma, Y.; Moore, M.; Hemmings, B. A.; Taylor, S. S. Phosphorylation and activation of cAMP-dependent protein kinase by phosphoinositide-dependent protein kinase Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 9849-54
39. Gould, C. M.; Kannan, N.; Taylor, S. S.; Newton, A. C. The chaperones Hsp90 and Cdc37 mediate the maturation and stabilization of protein kinase C through a conserved PXXP motif in the C-terminal tail J. Biol. Chem. 2009, 284, 4921-35
40. Yang, J.; Kennedy, E. J.; Wu, J.; Deal, M. S.; Pennypacker, J.; Ghosh, G.; Taylor, S. S. Contribution of non-catalytic core residues to activity and regulation in protein kinase A J. Biol. Chem. 2009, 284, 6241-8
41. Haste, N. M.; Talabani, H.; Doo, A.; Merckx, A.; Langsley, G.; Taylor, S. S. Exploring the Plasmodium falciparum cyclic-adenosine monophosphate (cAMP)-dependent protein kinase (PfPKA) as a therapeutic target Microbes Infect. 2012, 14, 838-50
42. Kannan, N.; Wu, J.; Anand, G. S.; Yooseph, S.; Neuwald, A. F.; Venter, J. C.; Taylor, S. S. Evolution of allostery in the cyclic nucleotide binding module Genome Biol. 2007, 8, R264
43. Sjoberg, T. J.; Kornev, A. P.; Taylor, S. S. Dissecting the cAMP-inducible allosteric switch in protein kinase A RIalpha Protein Sci. 2010, 19, 1213-21
44. Doskeland, S. O.; Ogreid, D. Characterization of the interchain and intrachain interactions between the binding sites of the free regulatory moiety of protein kinase I J. Biol. Chem. 1984, 259, 2291-301
45. Robinson-Steiner, A. M.; Corbin, J. D. Probable involvement of both intrachain cAMP binding sites in activation of protein kinase J. Biol. Chem. 1983, 258, 1032-40
46. Kim, C.; Xuong, N. H.; Taylor, S. S. Crystal structure of a complex between the catalytic and regulatory (RIalpha) subunits of PKA Science 2005, 307, 690-6
47. Kim, C.; Cheng, C. Y.; Saldanha, S. A.; Taylor, S. S. PKA-I holoenzyme structure reveals a mechanism for cAMP-dependent activation Cell 2007, 130, 1032-43
48. Herberg, F. W.; Zimmermann, B.; McGlone, M.; Taylor, S. S. Importance of the A-helix of the catalytic subunit of cAMP-dependent protein kinase for stability and for orienting subdomains at the cleft interface Protein Sci. 1997, 6, 569-79
49. Bastidas, A. C.; Deal, M. S.; Steichen, J. M.; Keshwani, M. M.; Guo, Y.; Taylor, S. S. Role of N-terminal myristylation in the structure and regulation of cAMP-dependent protein kinase J. Mol. Biol. 2012, 422, 215-29
50. Keshwani, M. M.; Klammt, C.; von Daake, S.; Ma, Y.; Kornev, A. P.; Choe, S.; Insel, P. A.; Taylor, S. S. Cotranslational cis-phosphorylation of the COOH-terminal tail is a key priming step in the maturation of cAMP-dependent protein kinase Proc. Natl. Acad. Sci. U.S.A. 2012, 109, E1221-9
51. Sastri, M.; Barraclough, D. M.; Carmichael, P. T.; Taylor, S. S. A-kinase-interacting protein localizes protein kinase A in the nucleus Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 349-54
52. Mutzel, R.; Lacombe, M. L.; Simon, M. N.; de Gunzburg, J.; Veron, M. Cloning and cDNA sequence of the regulatory subunit of cAMP-dependent protein kinase from Dictyostelium discoideum Proc. Natl. Acad. Sci. U.S.A. 1987, 84, 6-10
53. Taylor, S. S.; Buechler, J. A.; Yonemoto, W. cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes Annu. Rev. Biochem. 1990, 59, 971-1005
54. Newell, A. E.; Fiedler, S. E.; Ruan, J. M.; Pan, J.; Wang, P. J.; Deininger, J.; Corless, C. L.; Carr, D. W. Protein kinase A RII-like (R2D2) proteins exhibit differential localization and AKAP interaction Cell Motil. Cytoskeleton 2008, 65, 539-52
55. Sivadas, P.; Dienes, J. M.; St. Maurice, M.; Meek, W. D.; Yang, P. A flagellar A-kinase anchoring protein with two amphipathic helices forms a structural scaffold in the radial spoke complex J. Cell Biol. 2012, 199, 639-51
56. Glikin, G. C.; Judewicz, N. D.; Torres, H. N. Protein kinase activities in Neurospora crassa. Molecular properties Mol. Cell. Biochem. 1982, 46, 121-6
57. Kronberg, F.; Giacometti, R.; Ruiz-Herrera, J.; Passeron, S. Characterization of the regulatory subunit of Yarrowia lipolytica cAMP-dependent protein kinase. Evidences of a monomeric protein Arch. Biochem. Biophys. 2011, 509, 66-75
58. Galello, F.; Moreno, S.; Rossi, S. Interacting proteins of protein kinase A regulatory subunit in Saccharomyces cerevisiae J. Proteomics 2014, 109, 261-75
59. Gavin, A. C.; Aloy, P.; Grandi, P.; Krause, R.; Boesche, M.; Marzioch, M.; Rau, C.; Jensen, L. J.; Bastuck, S.; Dumpelfeld, B.; Edelmann, A.; Heurtier, M. A.; Hoffman, V.; Hoefert, C.; Klein, K.; Hudak, M.; Michon, A. M.; Schelder, M.; Schirle, M.; Remor, M.; Rudi, T.; Hooper, S.; Bauer, A.; Bouwmeester, T.; Casari, G.; Drewes, G.; Neubauer, G.; Rick, J. M.; Kuster, B.; Bork, P.; Russell, R. B.; Superti-Furga, G. Proteome survey reveals modularity of the yeast cell machinery Nature 2006, 440, 631-6
60. Breitkreutz, A.; Choi, H.; Sharom, J. R.; Boucher, L.; Neduva, V.; Larsen, B.; Lin, Z. Y.; Breitkreutz, B. J.; Stark, C.; Liu, G.; Ahn, J.; Dewar-Darch, D.; Reguly, T.; Tang, X.; Almeida, R.; Qin, Z. S.; Pawson, T.; Gingras, A. C.; Nesvizhskii, A. I.; Tyers, M. A global protein kinase and phosphatase interaction network in yeast Science 2010, 328, 1043-6
61. Scholten, A.; Poh, M. K.; van Veen, T. A.; van Breukelen, B.; Vos, M. A.; Heck, A. J. Analysis of the cGMP/cAMP interactome using a chemical proteomics approach in mammalian heart tissue validates sphingosine kinase type 1-interacting protein as a genuine and highly abundant AKAP J. Proteome Res. 2006, 5, 1435-47
62. Anand, G. S.; Krishnamurthy, S.; Bishnoi, T.; Kornev, A.; Taylor, S. S.; Johnson, D. A. Cyclic AMP- and (Rp)-cAMPS-induced conformational changes in a complex of the catalytic and regulatory (RI{alpha}) subunits of cyclic AMP-dependent protein kinase Mol. Cell. Proteomics 2010, 9, 2225-37
63. Peng, M.; Taouatas, N.; Cappadona, S.; van Breukelen, B.; Mohammed, S.; Scholten, A.; Heck, A. J. Protease bias in absolute protein quantitation Nat. Methods 2012, 9, 524-5
64. Aye, T. T.; Scholten, A.; Taouatas, N.; Varro, A.; Van Veen, T. A.; Vos, M. A.; Heck, A. J. Proteome-wide protein concentrations in the human heart Mol. BioSyst. 2010, 6, 1917-27
65. Grant, C. E.; Bailey, T. L.; Noble, W. S. FIMO: scanning for occurrences of a given motif Bioinformatics 2011, 27, 1017-8
66. Wang, Z.; Wu, T.; Shi, L.; Zhang, L.; Zheng, W.; Qu, J. Y.; Niu, R.; Qi, R. Z. Conserved motif of CDK5RAP2 mediates its localization to centrosomes and the Golgi complex J. Biol. Chem. 2010, 285, 22658-65
67. Li, Z.; Rossi, E. A.; Hoheisel, J. D.; Kalderon, D.; Rubin, C. S. Generation of a novel A kinase anchor protein and a myristoylated alanine-rich C kinase substrate-like analog from a single gene J. Biol. Chem. 1999, 274, 27191-200
68. Bachmann, V. A.; Riml, A.; Huber, R. G.; Baillie, G. S.; Liedl, K. R.; Valovka, T.; Stefan, E. Reciprocal regulation of PKA and Rac signaling Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 8531-6
69. Poppe, H.; Rybalkin, S. D.; Rehmann, H.; Hinds, T. R.; Tang, X. B.; Christensen, A. E.; Schwede, F.; Genieser, H. G.; Bos, J. L.; Doskeland, S. O.; Beavo, J. A.; Butt, E. Cyclic nucleotide analogs as probes of signaling pathways Nat. Methods 2008, 5, 277-8
70. Pelligrino, D. A.; Wang, Q. Cyclic nucleotide crosstalk and the regulation of cerebral vasodilation Prog. Neurobiol. 1998, 56, 1-18
71. Gavin, A. C.; Bösche, M.; Krause, R.; Grandi, P.; Marzioch, M.; Bauer, A.; Schultz, J.; Rick, J. M.; Michon, A. M.; Cruciat, C. M.; Remor, M.; Höfert, C.; Schelder, M.; Brajenovic, M.; Ruffner, H.; Merino, A.; Klein, K.; Hudak, M.; Dickson, D.; Rudi, T.; Gnau, V.; Bauch, A.; Bastuck, S.; Huhse, B.; Leutwein, C.; Heurtier, M. A.; Copley, R. R.; Edelmann, A.; Querfurth, E.; Rybin, V.; Drewes, G.; Raida, M.; Bouwmeester, T.; Bork, P.; Seraphin, B.; Kuster, B.; Neubauer, G.; Superti-Furga, G. Functional organization of the yeast proteome by systematic analysis of protein complexes Nature 2002, 415, 141-7
72. Angelo, R.; Rubin, C. S. 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. 1998, 273, 14633-43
73. Wang, X.; Herberg, F. W.; Laue, M. M.; Wullner, C.; Hu, B.; Petrasch-Parwez, E.; Kilimann, M. W. Neurobeachin: A protein kinase A-anchoring, beige/Chediak-higashi protein homolog implicated in neuronal membrane traffic J. Neurosci. 2000, 20, 8551-65
74. Lim, W. A.; Pawson, T. Phosphotyrosine signaling: evolving a new cellular communication system Cell 2010, 142, 661-7
75. Pincus, D.; Letunic, I.; Bork, P.; Lim, W. A. Evolution of the phospho-tyrosine signaling machinery in premetazoan lineages Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 9680-4
76. Holstein, T. W. The evolution of the Wnt pathway Cold Spring Harbor Perspect. Biol. 2012, 4, a007922
77. Rojas, A. M.; Fuentes, G.; Rausell, A.; Valencia, A. The Ras protein superfamily: evolutionary tree and role of conserved amino acids J. Cell Biol. 2012, 196, 189-201
78. Walker, G.; Dorrell, R. G.; Schlacht, A.; Dacks, J. B. Eukaryotic systematics: a users guide for cell biologists and parasitologists Parasitology 2011, 138, 1638-63