A complex containing SNF1-related kinase (SnRK1) and adenosine kinase in arabidopsis

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Mohannath, Gireesha ^a,d   Jackel, Jamie N ^a   Lee, Youn Hyung ^b   Buchmann, R Cody ^a   Wang, Hui ^a,c   Patil, Veena ^a,d   Adams, Allie K ^a,e   Bisaro, David M ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b Kyung Hee University   (South Korea)

^c PFIZER INC   (United States)

^d INDIANA UNIVERSITY   (United States)

^e CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE KINASE; PROTEIN KINASE; SUCROSE NONFERMENTING 1 KINASE; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; IMMUNOPRECIPITATION; NONHUMAN; PLANT CELL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TRANSGENIC PLANT; YEAST CELL;

ADENOSINE KINASE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYTOPLASM; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; PHOSPHORYLATION; PLANTS, GENETICALLY MODIFIED; PROTEIN-SERINE-THREONINE KINASES; YEASTS;

EID: 84900434071     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087592     Document Type: Article

References (64)

1. Hardie DG (2007) AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nature Rev 8: 774-785.
2. Polge C, Thomas M (2007) SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control? Trends Plant Sci 12: 20-28. (Pubitemid 46110874)
3. Halford N, Hey SJ (2009) Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. Biochem J 419: 247-259.
4. Ghillebert R, Swinnen E, Wen J, Vandesteene L, Ramon M, et al. (2011) The AMPK/SNF1/SnRK1 fuel gauge and energy regulator: structure, function and regulation. FEBS J 278: 3978-3990.
5. Robaglia C, Thomas M, Meyer C (2012) Sensing nutrient and energy status by SnRK1 and TOR kinases. Curr Opin Plant Biol 15: 301-307.
6. Sugden C, Donaghy PG, Halford N, Hardie DG (1999) Two SNF1-related protein kinases from spinach leaf phosphorylate and inactivate 3-hydroxyl-3-methylglutaryl-coenzyme A reductase, nitrate reductase, and sucrose phosphate synthase in vitro. Plant Physiol 120: 257-274. (Pubitemid 29375428)
7. Harthill JE, Meek SEM, Morrice N, Peggie MW, Borch J, et al. (2006) Phosphorylation and 14-3-3 binding of Arabidopsis trehalose-phosphate synthase 5 in response to 2-deoxyglucose. Plant J 47: 211-223. (Pubitemid 43974629)
8. Jossier M, Bouly J-P, Meimoun P, Arjmand A, Lessard P, et al. (2009) SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana. Plant J 59: 316-328.
9. Baena-Gonzalez E, Rolland F, Thevelian JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448: 938-943.
10. Baena-Gonzalez E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13: 474-482.
11. Hao L, Wang H, Sunter G, Bisaro DM (2003) Geminivirus AL2 and L2 proteins interact with and inactivate SNF1 kinase. Plant Cell 15: 1034-1048. (Pubitemid 36453298)
12. Baliji S, Sunter J, Sunter G (2007) Transcriptional analysis of complementary sense genes in Spinach curly top virus and functional role of C2 in pathogenesis. Mol Plant-Microbe Interact 20: 194-206. (Pubitemid 46146182)
13. Shen W, Hanley-Bowdoin L (2006) Geminivirus infection up-regulates the expression of two Arabidopsis protein kinases related to yeast SNF1- and mammalian AMPK activating kinases. Plant Physiol 142: 1642-1655. (Pubitemid 44956939)
14. Kudchodkar SB, Del Prete GQ, Maguire TG, Alwine JC (2007) AMPK-mediated inhibition of mTOR kinase is circumvented during immediate-early times of human cytomegalovirus infection. J Virol 81: 3649-3651. (Pubitemid 46456675)
15. Kumar SH, Rangarajan A (2009) Simian virus 40 small T antigen activates AMPK and triggers autophagy to protect cancer cells from nutrient deprivation. J Virol 83: 8565-8574.
16. Zhang H-S, Wu M-R (2009) SIRT1 regulates Tat-induced HIV-1 transcription through activating AMP-activated protein kinase. Virus Res 146: 51-57.
17. Mankouri J, Tedbury PR, Gretton S, Hughes ME, Griffen SDC, et al. (2010) Enhanced hepatitis C virus genome replication and lipid accumulation mediated by inhibition of AMP-activated protein kinase. Proc Natl Acad Sci USA 107: 11549-11554.
18. Scott JW, Hawley SA, Green SA, Anis M, Stewart G, et al. (2004) CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J Clin Invest 113: 274-284. (Pubitemid 38544212)
19. Xiao B, Heath R, Saiu P, Leiper FC, Leone P, et al. (2007) structural basis for AMP binding to mammalian AMP-activated protein kinase. Nature 449: 496-500. (Pubitemid 47509548)
20. Hawley SA, Davison M, Woods A, Davies SP, Beri RK, et al. (1996) Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP activated protein kinase. J Biol Chem 271: 27879-27887. (Pubitemid 26367365)
21. Wilson WA, Hawley SA, Hardie DG (1996) The mechanism of glucose repression/derepression in yeast: SNF1 protein kinase is activated by phosphorylation under derepressing conditions, and this correlates with a high AMP:ATP ratio. Curr Biol 6: 1426-1434. (Pubitemid 27012241)
22. Sugden C, Crawford RM, Halford NG, Hardie DG (1999) Regulation of spinach SNF1-related (SnRK1) kinases by protein kinases and phosphatases is associated with phosphorylation of the T loop and is regulated by 5′-AMP. Plant J 19: 433-439.
23. Sutherland CM, Hawley SA, McCartney RR, Leech A, Stark MJR, et al. (2003) Elm1p is one of three upstream kinases for the Saccharomyces cerevisiae SNF1 complex. Curr Biol 13: 1299-1305. (Pubitemid 36953302)
24. Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LGD, et al. (2003) LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 13: 2004-2008. (Pubitemid 37425212)
25. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, et al. (2005) Calmodul-independent protein kinase kinase-b is an alternative upstream kinase for AMPactivated protein kinase. Cell Metab 2: 9-19. (Pubitemid 43239821)
26. 2+/calmodulin-dependent protein kinase kinase-b acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2: 21-33.
27. Shen W, Reyes MI, Hanley-Bowdoin L (2009) Arabidopsis protein kinases GRIK1 and GRIK2 specifically activate SnRK1 by phosphorylating its activation loop. Plant Physiol 150: 996-1005.
28. Crozet P, Jammes F, Valot B, Ambard-Bretteville F, Nessler S, et al. (2010) Cross-phosphorylation between Arabidopsis thaliana sucrose nonfermenting 1- related protein kinase 1 (AtSnRK1) and its activating kinase (AtSnAK) determines their catalytic activities. J Biol Chem 285: 12071-12077.
29. Davies SP, Helps NR, Cohen PTW, Hardie DG (1995) 59-AMP inhibits dephosphorylation, as well as promoting phosphorylation, of the AMP-activated protein kinase. Studies using bacterially expressed human protein phosphatase- 2Ca and native bovine protein phosphatase-2Ac. FEBS Lett 377: 421-425. (Pubitemid 26027159)
30. Suter M, Riek U, Tuerk R, Schlattner U, Wallimann T, et al. (2006) Dissecting the role of 59-AMP for allosteric stimulation, activation, and deactivation of AMP-activated protein kinase. J Biol Chem 281: 32207-32216. (Pubitemid 46036775)
31. Sanders MJ, Grondin PO, Hegarty BD, Snowden MA, Carling D (2007) Investigating the mechanism for AMP activation of the AMP-activated protein kinase cascade. Biochem J 403: 139-148. (Pubitemid 46569875)
32. Halford NG, Hey S, Jhurreea D, Laurie S, McKibbin RS, et al. (2003) Metabiolic signalling and carbon partitioning: role of Snf1-related(SnRK1) protein kinase. J Exp Botany 54: 467-475. (Pubitemid 36122042)
33. Moffatt BA, Wang L, Allen MS, Stevens YY, Qin W, et al. (2000) Adenosine kinase of Arabidopsis. Kinetic properties and gene expression. Plant Physiol 124: 1775-1785. (Pubitemid 32053508)
34. von Schwartzenberg K, Kruse S, Reski R, Moffatt B, Laloue M (1998) Cloning and characterization of an adenosine kinase from Physcomitrella involved in cytokinin metabolism. Plant J 13: 249-257. (Pubitemid 28073330)
35. Lecoq K, Belloc I, Desgranges C, Daignan-Fornier B (2001) Role of adenosine kinase in Saccharomyces cerevisiae: identification of the ADO1 gene and study of the mutant phenotypes. Yeast 18: 335-342. (Pubitemid 32218901)
36. Moffatt BA, Stevens YY, Allen MS, Snider JD, Periera LA, et al. (2002) Adenosine kinase deficiency is associated with developmental abnormalities and reduced transmethylation. Plant Physiol 128: 812-821. (Pubitemid 34243819)
37. Wang H, Hao L, Shung C-Y, Sunter G, Bisaro DM (2003) Adenosine kinase is inactivated by geminivirus AL2 and L2 proteins. Plant Cell 15: 3020-3032. (Pubitemid 37546268)
38. Wang H, Buckley KJ, Yang X, Buchmann RC, Bisaro DM (2005) Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J Virol 79: 7410-7418. (Pubitemid 40756778)
39. Raja P, Sanville BC, Buchmann RC, Bisaro DM (2008) Viral genome methylation as an epigenetic defense against geminiviruses. J Virol 82: 8997-9007.
40. Buchmann RC, Asad S, Wolf JN, Mohannath G, Bisaro DM (2009) Geminivirus AL2 and L2 proteins suppress transcriptional gene silencing and cause genome-wide reductions in cytosine methylation. J Virol 83: 5005-5013.
41. Baliji S, Lacatus G, Sunter G (2010) The interaction between geminivirus pathogenicity proteins and adenosine kinase leads to increased expression of primary cytokinin-responsive genes. Virology 402: 238-247.
42. Raja P, Wolf JN, Bisaro DM (2010) RNA silencing directed against geminiviruses: post-transcriptional and epigenetic components. Biochim Biophys Acta 1799: 337-351.
43. Davies SP, Carling D, Hardie DG (1989) Tissue distribution of AMP-activated protein kinase, and lack of activation by cyclic AMP-dependent protein kinase, studied using a specific and sensitive peptide assay. Eur J Biochem 186: 123-128. (Pubitemid 20015134)
44. Kishimoto A, Ogura T, Esumi H (2006) A pull-down assay for 59AMP-activated protein kinase activity using the GST-fused protein. Mol Biotechnol 32: 17-21. (Pubitemid 43022764)
45. Lindbo JA (2007) TRBO: A high-efficiency Tobacco mosiac virus RNA-based overexpression vector. Plant Physiol 145: 1232-1240.
46. Lindbo JA (2007) High-efficiency protein expression in plants from agroinfection-compatible Tobacco mosaic virus expression vectors. BMC Biotechnol 7: 52.
47. Durfee T, Becherer K, Chen P-L, Yeh S-H, Yang Y, et al. (1993) The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev 7: 555-569. (Pubitemid 23125257)
48. Hu C-D, Chinenov Y, Kerppola TK (2002) Visualization of interactions among bZIP and Rel family proteins using bimolecular fluorescence complementation. Mol Cell 9: 789-798. (Pubitemid 34454889)
49. Yang X, Baliji S, Buchmann RC, Wang H, Lindbo JA, et al. (2007) Functional modulation of the geminivirus AL2 transcription factor and silencing suppressor by self-interaction. J Virol 81: 11972-11981. (Pubitemid 47623828)
50. Nakazawa Y, Hiraguri A, Moriyama H, Fukuhara T (2007) The dsRNA-binding protein DRB4 interacts with the Dicer-like protein DCL4 in vivo and functions in the trans-acting siRNA pathway. Plant Mol Biol 63: 777-785. (Pubitemid 46399170)
51. Ananieva EA, Gillaspy GE, Ely A, Burnette RN, Erickson FL (2008) Interaction of the WD40 domain of a myoinositol phosphate 5-phosphatase links inositol, sugar, and stres signaling. Plant Physiol 148: 1868-1882. (Pubitemid 352847465)
52. Halford N, Hardie DG (1998) SNF1-related protein kinases: global regulators of carbon metabolism in plants? Plant Mol Biol 37: 735-748. (Pubitemid 28331590)
53. Budovskaya YV, Stephan JS, Deminoff SJ, Herman PK (2005) An evolutionary proteomics approach identifies substrates of the cAMP-dependent protein kinase. Proc Natl Acad Sci USA 102: 13933-13938. (Pubitemid 41377681)
54. McNellis TW, Mudgett MB, Li K, Aoyama T, Horvath D, et al. (1998) Glucocorticoid-inducible expression of bacterial avirulence gene in transgenic Arabidopsis induced hypersensitive cell death. Plant J 14: 247-257. (Pubitemid 28236015)
55. Lizcano JM, Goransson O, Toth R, Deak M, Morrice NA, et al. (2004) LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J 23: 833-843. (Pubitemid 38418750)
56. Shin R, Alvarez S, Burch AY, Jez JM, Schachtman DP (2007) Phosphoproteomic identification of targets of the Arabidopsis sucrose nonfermenting-like kinase SnRK2.8 reveals a connection to metabolic processes. Proc Natl Acad Sci, USA 104: 6460-6465. (Pubitemid 47186116)
57. Bachmann M, Huber JL, Liao P-C, Gage DA, Huber SC (1996) The inhibitor protein of phosphorylated nitrate reductase from spinach (Spinacea oleracea L.) is a 14-3-3 protein. FEBS Lett 387: 127-131. (Pubitemid 26178907)
58. Moorhead G, Douglas P, Morrice N, Scarabel M, Aitken A, et al. (1996) Phosphorylated nitrate reductase from spinach leaves is inhibited by 14-3-3 proteins and activated by fusicoccin. Curr Biol 6: 1104-1113. (Pubitemid 26368744)
59. Ikeda Y, Koizumi N, Kusano T, Sano H (2000) Specific binding of a 14-3-3 protein to autophosphorylated WPK4, an SNF1-related wheat protein kinase, and to WPK4-phosphorylated nitrate reductase. J Biol Chem 275: 31695-31700.
60. Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RAC, et al. (2009) Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol 149: 1860-1871.
61. Delatte T, Sedijani P, Kondou Y, Matsui M, de Jong GJ, et al. (2011) Growth arrest by trehalose-6-phosphate: an astonishing case of primary metabolite control over growth by way of the SnRK1 signaling pathway. Plant Physiol 157: 160-174.
62. Celenza JL, Carlson M (1989) Mutational analysis of the Saccharomyces cerevisiae SNF1 protein kinase and evidence for functional interaction with the SNF4 protein. Mol Cell Biol 9: 5034-5044. (Pubitemid 19275974)
63. Harper JW, Adami GR, Wei N, Keyomarsi K, Elledge SJ (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinase. Cell 75: 805-816. (Pubitemid 23346377)
64. Chakrabarty R, Banerjee R, Chung S-M, Farman M, Citovsky V, et al. (2007) pSITE vectors for stable integration or transient expression of autofluorescent protein fusions in plants: Probing Nicotiana benthamiana -virus interactions. Mol Plant-Microbe Interact 20: 740-750. (Pubitemid 46944968)