Circles within circles: Crosstalk between protein Ser/Thr/Tyr-phosphorylation and Met oxidation

BMC Bioinformatics

Volumn 14, Issue SUPPL.14, 2013, Pages

  Rao, R S P ^a,b   Xu, Dong ^b,c   Thelen, Jay J ^a,b   Miernyk, Ján A ^a,b  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c University of Missouri   (United States)

Author keywords

Methionine; methionine sulfoxide; oxidation; protein phosphorylation; regulation; reversible posttranslational modifications; signalling

Indexed keywords

METHIONINE; METHIONINE SULFOXIDE; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN PHOSPHORYLATION; REGULATION;

AMINO ACIDS; CROSSTALK; OXIDATION; PROTEINS; SIGNALING;

PHOSPHORYLATION;

AMINO ACID; PROTEIN KINASE; PROTEOME;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; METABOLISM; OXIDATION REDUCTION REACTION; PHOSPHORYLATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; AMINO ACIDS; ANIMALS; OXIDATION-REDUCTION; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; SIGNAL TRANSDUCTION;

EID: 84885339230     PISSN: None     EISSN: 14712105     Source Type: Journal    
DOI: 10.1186/1471-2105-14-S14-S14     Document Type: Article

References (84)

1. Prabakaran S, Lippens G, Steen H, Gunawardena J. Post-translational modification: nature's escape from genetic imprisonment and the basis for dynamic information encoding. Wiley Interdiscip Rev Syst Biol Med 2012, 4:565-583. 10.1002/wsbm.1185, 22899623.
2. Mann M, Jensen ON. Proteomic analysis of post-translational modifications. Nature Biotechnol 2003, 21:255-261.
3. Walsh CT, Garneau-Tsodikova S, Gatto GJ. Protein posttranslational modifications: The chemistry of proteome diversifications. Angew Chem Int Ed Engl 2005, 44:7342-7372. 10.1002/anie.200501023, 16267872.
4. Khoury GA, Baliban RC, Floudasa CA. Proteome-wide post-translational modification statistics: Frequency analysis and curation of the swiss-prot database. Sci Rep 2011, 1:90.
5. Minguez P, Parca L, Diella F, Mende DR, Kumar R, Helmer-Citterich M, Gavin AC, van Noort V, Bork P. Deciphering a global network of functionally associated post-translational modifications. Molec Syst Biol 2012, 8:599.
6. Hunter T. The age of crosstalk: Phosphorylation, ubiquitination and beyond. Mol Cell 2007, 28:730-738. 10.1016/j.molcel.2007.11.019, 18082598.
7. Beltrao P, Albanèse V, Kenner LR, Swaney DL, Burlingame A, Villén J, Lim WA, Fraser JS, Frydman J, Krogan NJ. Systematic functional prioritization of protein posttranslational modifications. Cell 2012, 150:413-425. 10.1016/j.cell.2012.05.036, 3404735, 22817900.
8. Deribe YL, Pawson T, Dikic I. Post-translational modifications in signal integration. Nature Struct Mol Biol 2010, 17:666-672.
9. Loroch S, Dickhut C, Zahedi RP, Sickmann A. Phosphoproteomics - More than meets the eye. Electrophoresis 2013, doi: 10.1002/elps.201200710.
10. Havelund JF, Thelen JJ, Møller IM. Biochemistry, proteomics, and phosphoproteomics of plant mitochondria from non-photosynthetic cells. Front Plant Sci 2013, 4:51. 3595712, 23494127.
11. Mijakovic I, Macek B. Impact of phosphoproteomics on studies of bacterial physiology. FEMS Microbiol Rev 2012, 36:877-892. 10.1111/j.1574-6976.2011.00314.x, 22091997.
12. Rogne M, Taskén K. Cell signalling analyses in the functional genomics era. Nature Biotechnol 2013, 30:333-338.
13. Furuya E, Yokoyama M, Uyeda K. Regulation of fructose-6-phosphate 2-kinase by phosphorylation and dephosphorylation: possible mechanism for coordinated control of glycolysis and glycogenolysis. Proc Natl Acad Sci USA 1982, 79:325-329. 10.1073/pnas.79.2.325, 345719, 6281764.
14. Dexter JP, Gunawardena J. Dimerization and bifunctionality confer robustness to the isocitrate dehydrogenase regulatory system in Escherichia coli. J Biol Chem 2013, 288:5770-5778. 10.1074/jbc.M112.339226, 23192354.
15. Oliveira AP, Ludwig C, Picotti P, Kogadeeva M, Aebersold R, Sauer U. Regulation of yeast central metabolism by enzyme phosphorylation. Mol Syst Biol 2012, 8:623. 3531909, 23149688.
16. Just S, Illing S, Trester-Zedlitz M, Lau EK, Kotowski SJ, Miess E, Mann A, Doll C, Trinidad JC, Burlingame AL, von Zastrow M, Schulz S. Differentiation of opioid drug effects by hierarchical multi-site phosphorylation. Mol Pharmacol 2013, 83:633-639. 10.1124/mol.112.082875, 23239825.
17. Ahsan N, Huang Y, Tovar-Mendez A, Swatek KN, Zhang J, Miernyk JA, Xu D, Thelen JJ. A versatile mass spectrometry-based method to both identify kinase client-relationships and characterize signaling network topology. J Proteome Res 2013, 12:937-948. 10.1021/pr3009995, 23270405.
18. Moorhead GBG, De Wever V, Templeton G, Kerk D. Evolution of protein phosphatases in plants and animals. Biochem J 2002, 417:401-409.
19. Niedner RH, Buzko OV, Haste NM, Taylor A, Gribskov M, Taylor SS. Protein kinase resource: an integrated environment for phosphorylation research. Proteins 2006, (63):78-86.
20. Kerk D, Bulgrien J, Smith DW, Barsam B, Veretnik S, Gribskov M. The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis. Plant Physiol 2002, 129:908-925. 10.1104/pp.004002, 161711, 12068129.
21. Aivaliotis M, Macek B, Gnad F, Reichelt P, Mann M, Oesterhelt D. Ser/Thr/Tyr protein phosphorylation in the archaeon Halobacterium salinarum - A representative of the third domain of life. PLoS ONE 2009, 4:e4777. 10.1371/journal.pone.0004777, 2652253, 19274099.
22. Hatanaka E, Dermargos A, Hirata AE, Vinolo MA, Carpinelli AR, Newsholme P, Armelin HA, Curi R. Oleic, linoleic and linolenic acids increase ROS production by fibroblasts via NADPH oxidase activation. PLoS One 2013, 8:e58626. 10.1371/journal.pone.0058626, 3620266, 23579616.
23. Grivennikova VG, Vinogradov AD. Partitioning of superoxide and hydrogen peroxide production by mitochondrial respiratory complex I. Biochim Biophys Acta 2013, 1827:446-454. 10.1016/j.bbabio.2013.01.002, 23313413.
24. Panieri E, Gogvadze V, Norberg E, Venkatesh R, Orrenius S, Zhivotovsky B. Reactive oxygen species generated in different compartments induce cell death, survival, or senescence. Free Radic Biol Med 2013, 57:176-187.
25. Møller IM, Jensen PE, Hansson A. Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 2007, 58:459-481. 10.1146/annurev.arplant.58.032806.103946, 17288534.
26. Höhn A, König J, Grune T. Protein oxidation in aging and the removal of oxidized proteins. J Proteomics 2013, doi:pii: S1874-3919(13)00021-3.
27. Møller IM, Sweetlove LJ. ROS signalling--specificity is required. Trends Plant Sci 2010, 15:370-374. 10.1016/j.tplants.2010.04.008, 20605736.
28. Aiken CT, Kaake RM, Wang X, Huang L. Oxidative stress-mediated regulation of proteasome complexes. Mol Cell Proteomics 2011, 10:R110-006924. 3098605, 21543789.
29. Wang P, Du Y, Zhao X, Miao Y, Song CP. The MPK6-ERF6-ROS-responsive cis-acting Element7/GCC box complex modulates oxidative gene transcription and the oxidative response in Arabidopsis. Plant Physiol 2013, 161:1392-1408. 10.1104/pp.112.210724, 3585604, 23300166.
30. Boschi-Muller S, Olry A, Antoine M, Branlant G. The enzymology and biochemistry of methionine sulfoxide reductases. Biochim Biophys Acta 2005, 1703:231-238. 10.1016/j.bbapap.2004.09.016, 15680231.
31. Boschi-Muller S, Gand A, Branlant G. The methionine sulfoxide reductases: Catalysis and substrate specificities. Arch Biochem Biophys 2008, 474:266-273. 10.1016/j.abb.2008.02.007, 18302927.
32. Stadtman ER, Moskovitz J, Levine RL. Oxidation of methionine residues of proteins: biological consequences. Antioxid Redox Signal 2003, 5:577-582. 10.1089/152308603770310239, 14580313.
33. Carruthers NJ, Stemmer PM. Methionine oxidation in the calmodulin-binding domain of calcineurin disrupts calmodulin binding and calcineurin activation. Biochemistry 2008, 47:3085-3095. 10.1021/bi702044x, 18275158.
34. Bigelow DJ, Squier TC. Thioredoxin-dependent redox regulation of cellular signaling and stress response through reversible oxidation of methionines. Mol Biosyst 2011, 7:2101-2109. 10.1039/c1mb05081h, 21594273.
35. Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, Bartlett RK, et al. A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 2008, 133:462-474. 10.1016/j.cell.2008.02.048, 2435269, 18455987.
36. Bigelow DJ, Squier TC. Redox modulation of cellular signaling and metabolism through reversible oxidation of methionine sensors in calcium regulatory proteins. Biochim Biophys Acta 2005, 1703:121-134. 10.1016/j.bbapap.2004.09.012, 15680220.
37. Zauner G, Kozak RP, Gardner RA, Fernandes DL, Deelder AM, Wuhrer M. Protein O-glycosylation analysis. Biol Chem 2012, 393:687-708.
38. Erce MA, Pang CN, Hart-Smith G, Wilkins MR. The methylproteome and the intracellular methylation network. Proteomics 2012, 12:564-586. 10.1002/pmic.201100397, 22246820.
39. Zhang K, Tian S, Fan E. Protein lysine acetylation analysis: current MS-based proteomic technologies. Analyst 2013, 138:1628-1636. 10.1039/c3an36837h, 23361263.
40. Theillet FX, Smet-Nocca C, Liokatis S, Thongwichian R, Kosten J, Yoon MK, Kriwacki RW, et al. Cell signaling, post-translational protein modifications and NMR spectroscopy. J Biomol NMR 2012, 54:217-236. 10.1007/s10858-012-9674-x, 23011410.
41. Shi SP, Qiu JD, Sun XY, Suo SB, Huang SY, Liang RP. PMeS: prediction of methylation sites based on enhanced feature encoding scheme. PLoS One 2012, 7:e38772. 10.1371/journal.pone.0038772, 3376144, 22719939.
42. Donlin LT, Andresen C, Just S, Rudensky E, Pappas CT, Kruger M, Jacobs EY, et al. Smyd2 controls cytoplasmic lysine methylation of Hsp90 and myofilament organization. Genes Dev 2012, 26:114-119. 10.1101/gad.177758.111, 3273835, 22241783.
43. Gill DJ, Clausen H, Bard F. Location, location, location: new insights into O-GalNAc protein glycosylation. Trends Cell Biol 2011, 21:149-158. 10.1016/j.tcb.2010.11.004, 21145746.
44. Young NL, Plazas-Mayorca MD, Garcia BA. Systems-wide proteomic characterization of combinatorial post-translational modification patterns. Expert Rev Proteomics 2010, 7:79-92. 10.1586/epr.09.100, 20121478.
45. Hart GW, Slawson C, Ramirez-Correa G, Lagerlof O. Cross talk between O-GlcNAcylation and phosphorylation: Roles in signaling, transcription, and chronic disease. Annu Rev Biochem 2011, 80:825-858. 10.1146/annurev-biochem-060608-102511, 3294376, 21391816.
46. Hart GW, Housley MP, Slawson C. Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 2007, 446:1017-1022. 10.1038/nature05815, 17460662.
47. Lu Z, Cheng Z, Zhao Y, Volchenboum SL. Bioinformatic analysis and post-translational modification crosstalk prediction of lysine acetylation. PLoS One 2011, 6:e28228. 10.1371/journal.pone.0028228, 3229533, 22164248.
48. van Noort V, Seebacher J, Bader S, Mohammed S, Vonkova I, Betts MJ, Kühner S, et al. Cross-talk between phosphorylation and lysine acetylation in a genome-reduced bacterium. Mol Syst Biol 2012, 8:571. 3293634, 22373819.
49. Sharfi H, Eldar-Finkelman H. Sequential phosphorylation of insulin receptor substrate-2 by glycogen synthase kinase-3 and c-Jun NH2-terminal kinase plays a role in hepatic insulin signaling. Am J Physiol Endocrinol Metab 2008, 294:E307-315.
50. Hardin SC, Larue CT, Oh MH, Jain V, Huber SC. Coupling oxidative signals to protein phosphorylation via methionine oxidation in Arabidopsis. Biochem J 2009, 422:305-312. 10.1042/BJ20090764, 2782308, 19527223.
51. Miernyk JA, Johnston ML, Huber SC, Tovar-Méndez A, Hoyos E, Randall DD. Oxidation of an adjacent methionine residue inhibits regulatory seryl-phosphorylation of pyruvate dehydrogenase. Proteomics Insights 2009, 2:15-22.
52. Emes MJ. Oxidation of methionine residues: the missing link between stress and signalling responses in plants. Biochem J 2009, 422:e1-2. 10.1042/BJ20091063, 19663808.
53. Zhang X-H. Regulation of protein function by residue oxidation. Proteomics Insights 2010, 3:17-24.
54. Uniprot. , http://www.uniprot.org/
55. NCBI. , http://www.ncbi.nlm.nih.gov/
56. TAIR. , http://www.arabidopsis.org/
57. Rao RSP, Møller IM. Large-scale analysis of phosphorylation site occupancy in eukaryotic proteins. Biochim Biophys Acta 2012, 1824:405-412. 10.1016/j.bbapap.2011.12.001, 22178296.
58. P3DB. , http://www.p3db.org/
59. Gao J, Thelen JJ, Dunker AK, Xu D. Musite, a tool for global prediction of general and kinase-specific phosphorylation sites. Mol Cell Proteomics 2010, 9:2586-2600. 10.1074/mcp.M110.001388, 3101956, 20702892.
60. Miller ML, Soufi B, Jers C, Blom N, Macek B, Mijakovic I. NetPhosBac - A predictor for Ser/Thr phosphorylation sites in bacterial proteins. Proteomics 2009, 9:116-125. 10.1002/pmic.200800285, 19053140.
61. Iakoucheva LM, Radivojac P, Brown CJ, O'Connor TR, Sikes JG, Obradovic Z, Dunker AK. The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res 2004, 32:1037-1049. 10.1093/nar/gkh253, 373391, 14960716.
62. Beausoleil SA, Jedrychowski M, Schwartz D, Elias JE, Villén J, Li J, Cohn MA, Cantley LC, Gygi SP. Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc Natl Acad Sci USA 2004, 101:12130-12135. 10.1073/pnas.0404720101, 514446, 15302935.
63. Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein. J Mol Biol 1982, 157:105-132. 10.1016/0022-2836(82)90515-0, 7108955.
64. Du Z, Zhou X, Ling Y, Zhang Z, Su Z. AgriGO: A GO analysis toolkit for the agricultural community. Nucleic Acids Res 2010, 38:W64-70. 10.1093/nar/gkq310, 2896167, 20435677.
65. Reimand J, Kull M, Peterson H, Hansen J, Vilo J. g:Profiler - a web-based toolset for functional profiling of gene lists from large-scale experiments. Nucleic Acids Res 2007, 35:W193-200. 10.1093/nar/gkm226, 1933153, 17478515.
66. Mijakovic I. Protein phosphorylation in bacteria. Microbe 5:21-25.
67. Mok J, Kim PM, Lam HYK, Piccirillo S, Zhou X, Jeschke GR, Sheridan DL, et al. Deciphering protein kinase specificity through large-scale analysis of yeast phosphorylation site motifs. Science Signaling 2010, 3:ra12. 10.1126/scisignal.2000482, 2846625, 20159853.
68. Grantham R. Amino acid difference formula to help explain protein evolution. Science 1974, 185:862-864. 10.1126/science.185.4154.862, 4843792.
69. Akashi H, Gojobori T. Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci USA 2002, 99:3695-3700. 10.1073/pnas.062526999, 122586, 11904428.
70. Siltberg-Liberles J, Grahnen JA, Liberles DA. The evolution of protein structures and structural ensembles under functional constraint. Genes 2011, 2:748-762.
71. Raiford DW, Heizer EM, Miller RV, Akashi H, Raymer ML, Krane DE. Do amino acid biosynthetic costs constrain protein evolution in Saccharomyces cerevisiae?. J Mol Evol 2008, 67:621-630. 10.1007/s00239-008-9162-9, 18937004.
72. Jha AN, Vishveshwara S, Banavar JR. Amino acid interaction preferences in proteins. Protein Sci 2010, 19:603-616. 10.1002/pro.339, 2866284, 20073083.
73. Barton MD, Delneri D, Oliver SG, Rattray M, Bergman CM. Evolutionary systems biology of amino acid biosynthetic cost in yeast. PLoS ONE 2010, 5:e11935. 10.1371/journal.pone.0011935, 2923148, 20808905.
74. Tan CS, Pasculescu A, Lim WA, Pawson T, Bader GD, Linding R. Positive selection of tyrosine loss in metazoan evolution. Science 2009, 325:1686-1688. 10.1126/science.1174301, 3066034, 19589966.
75. Møller IM, Rogowska-Wrzesinska A, Rao RS. Protein carbonylation and metal-catalyzed protein oxidation in a cellular perspective. J Proteomics 2011, 74:2228-2242. 10.1016/j.jprot.2011.05.004, 21601020.
76. Xu K, Uversky VN, Xue B. Local flexibility facilitates oxidization of buried methionine residues. Protein Pept Lett 2012, 19:688-697. 10.2174/092986612800494084, 22519542.
77. Woodsmith J, Kamburov A, Stelzl U. Dual coordination of post translational modifications in human protein networks. PLoS Comput Biol 2013, 9:e1002933. 10.1371/journal.pcbi.1002933, 3591266, 23505349.
78. Wellen KE, Thompson CB. A two-way street: Reciprocal regulation of metabolism and signalling. Nature Rev Mol Cell Biol 2012, 13:270-276.
79. Yang X-J, Seto E. Lysine acetylation: Codified crosstalk with other posttranslational modifications. Mol Cell 2008, 31:449-461. 10.1016/j.molcel.2008.07.002, 2551738, 18722172.
80. Oien DB, Carrasco GA, Moskovitz J. Decreased phosphorylation and increased methionine oxidation of α-synuclein in the methionine sulfoxide reductase A knockout mouse. J Amino Acids 2011, 2011:721094. 3275937, 22332004.
81. Oien DB, Shinogle HE, Moore DS, Moskovitz J. Clearance and phosphorylation of alpha-synuclein are inhibited in methionine sulfoxide reductase A null yeast cells. J Mol Neurosci 2009, 39:323-332. 10.1007/s12031-009-9274-8, 3708264, 19653131.
82. Snijder J, Rose RJ, Raijmakers R, Heck AJ. Site-specific methionine oxidation in calmodulin affects structural integrity and interaction with Ca2+/calmodulin-dependent protein kinase II. J Struct Biol 174:187-195.
83. Xu S, Ding H, Su F, Zhang A, Jiang M, Ostman A, Frijhoff J, et al. Regulation of protein tyrosine phosphatases by reversible oxidation. J Biochem 2011, 150:345-356. 10.1093/jb/mvr104, 21856739.
84. Marondedze C, Turek I, Parrott B, Thomas L, Jankovic B, Lilley KS, Gehring C. Structural and functional characteristics of cGMP-dependent methionine oxidation in Arabidopsis thaliana proteins. Cell Commun Signal 2013, 11:1. 10.1186/1478-811X-11-1, 3544604, 23289948.