Insight into the redox regulation of the phosphoglucan phosphatase SEX4 involved in starch degradation

FEBS Journal

Volumn 280, Issue 2, 2013, Pages 538-548

  Silver, Dylan M ^a   Silva, Leslie P ^b   Issakidis Bourguet, Emmanuelle ^c   Glaring, Mikkel A ^d   Schriemer, David C ^b   Moorhead, Greg B G ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^d ETH ZURICH   (Switzerland)

Author keywords

disulfide bond; dual specificity phosphatase; redox; starch degradation; thioredoxin

Indexed keywords

CYSTEINE; DITHIOTHREITOL; DUAL SPECIFICITY PHOSPHATASE; STARCH; STARCH EXCESS 4 PHOSPHATASE; THIOREDOXIN; UNCLASSIFIED DRUG;

CARBOHYDRATE METABOLISM; CATALYSIS; CHEMICAL ANALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; DISULFIDE BOND; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; ENZYME REACTIVATION; ENZYME REGULATION; ENZYME STRUCTURE; IN VIVO STUDY; MOLECULAR CLONING; MOLECULAR MECHANICS; NONHUMAN; OXIDATION REDUCTION REACTION; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CATALYTIC DOMAIN; CHROMATOGRAPHY, LIQUID; CYSTEINE; DISULFIDES; DITHIOTHREITOL; DUAL-SPECIFICITY PHOSPHATASES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME ACTIVATION; GLUCANS; HYDROGEN PEROXIDE; KINETICS; MASS SPECTROMETRY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NITROPHENOLS; ORGANOPHOSPHORUS COMPOUNDS; OXIDANTS; OXIDATION-REDUCTION; PHOSPHORYLATION; STARCH;

MAMMALIA;

EID: 84872805864     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08546.x     Document Type: Review

References (60)

1. Kötting O, Santelia D, Edner C, Eicke S, Marthaler T, Gentry MS, Comparot-Moss S, Chen J, Smith AM, Steup M, et al. (2009) STARCH-EXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 21, 334-346.
2. Hejazi M, Fettke J, Kotting O, Zeeman SC, &, Steup M, (2010) The laforin-like dual-specificity phosphatase SEX4 from Arabidopsis hydrolyzes both C6- and C3-phosphate esters introduced by starch-related dikinases and thereby affects phase transition of α-glucans. Plant Physiol 152, 711-722.
3. Zeeman SC, Kossmann J, &, Smith AM, (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61, 209-234.
4. Lorberth R, Ritte G, Willmitzer L, &, Kossmann J, (1998) Inhibition of a starch-granule-bound protein leads to modified starch and repression of cold sweetening. Nat Biotechnol 16, 473-477.
5. Yu TS, Kofler H, Hausler RE, Hille D, Flugge UI, Zeeman SC, Smith AM, Kossmann J, Lloyd J, Ritte G, et al. (2001) The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell 13, 1907-1918.
6. Baunsgaard L, Lutken H, Mikkelsen R, Glaring MA, Pham TT, &, Blennow A, (2005) A novel isoform of glucan,water dikinase phosphorylates pre-phosphorylated α-glucans and is involved in starch degradation in Arabidopsis. Plant J 41, 595-605.
7. Ritte G, Lloyd JR, Eckermann N, Rottmann A, Kossmann J, &, Steup M, (2002) The starch-related R1 protein is an α-glucan,water dikinase. Proc Natl Acad Sci USA 99, 7166-7171.
8. Ritte G, Heydenreich M, Mahlow S, Haebel S, Kötting O, &, Steup M, (2006) Phosphorylation of C6- and C3-positions of glucosyl residues in starch is catalysed by distinct dikinases. FEBS Lett 580, 4872-4876.
9. Hansen PI, Spraul M, Dvortsak P, Larsen FH, Blennow A, Motawia MS, &, Engelsen SB, (2009) Starch phosphorylation-maltosidic restraints upon 3′- and 6′-phosphorylation investigated by chemical synthesis, molecular dynamics and NMR spectroscopy. Biopolymers 91, 179-193.
10. Hejazi M, Fettke J, Haebel S, Edner C, Paris O, Frohberg C, Steup M, &, Ritte G, (2008) Glucan, water dikinase phosphorylates crystalline maltodextrins and thereby initiates solubilization. Plant J 55, 323-334.
11. Fulton DC, Stettler M, Mettler T, Vaughan CK, Li J, Francisco P, Gil M, Reinhold H, Eicke S, Messerli G, et al. (2008) β-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active β-amylases in Arabidopsis chloroplasts. Plant Cell 20, 1040-1058.
12. Edner C, Li J, Albrecht T, Mahlow S, Hejazi M, Hussain H, Kaplan F, Guy C, Smith SM, Steup M, et al. (2007) Glucan,water dikinase activity stimulates breakdown of starch granules by plastidial β-amylases. Plant Physiol 145, 17-28.
13. Delatte T, Trevisan M, Parker ML, &, Zeeman SC, (2005) Arabidopsis mutants Atisa1 and Atisa2 have identical phenotypes and lack the same multimeric isoamylase, which influences the branch point distribution of amylopectin during starch synthesis. Plant J 41, 815-830.
14. Zeeman SC, Northrop F, Smith AM, &, Rees T, (1998) A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. Plant J 15, 357-365.
15. Zeeman SC, &, ap Rees T, (1999) Changes in carbohydrate metabolism and assimilate export in starch-excess mutants of Arabidopsis. Plant, Cell Environ 22, 1445-1453.
16. Niittylä T, Comparot-Moss S, Lue WL, Messerli G, Trevisan M, Seymour MD, Gatehouse JA, Villadsen D, Smith SM, Chen J, et al. (2006) Similar protein phosphatases control starch metabolism in plants and glycogen metabolism in mammals. J Biol Chem 281, 11815-11818.
17. Tagliabracci VS, Turnbull J, Wang W, Girard JM, Zhao X, Skurat AV, Delgado-Escueta AV, Minassian BA, Depaoli-Roach AA, &, Roach PJ, (2007) Laforin is a glycogen phosphatase, deficiency of which leads to elevated phosphorylation of glycogen in vivo. Proc Natl Acad Sci USA 104, 19262-19266.
18. Sakai M, Austin J, Witmer F, &, Trueb L, (1970) Studies in myoclonus epilepsy (Lafora body form). II. Polyglucosans in the systemic deposits of myoclonus epilepsy and in corpora amylacea. Neurology 20, 160-176.
19. Gentry MS, Dowen RHR, Worby CA, Mattoo S, Ecker JR, &, Dixon JE, (2007) The phosphatase laforin crosses evolutionary boundaries and links carbohydrate metabolism to neuronal disease. J Cell Biol 178, 477-488.
20. Gentry MS, &, Pace RM, (2009) Conservation of the glucan phosphatase laforin is linked to rates of molecular evolution and the glucan metabolism of the organism. BMC Evol Biol 9, 138.
21. Kerk D, Templeton G, &, Moorhead GB, (2008) Evolutionary radiation pattern of novel protein phosphatases revealed by analysis of protein data from the completely sequenced genomes of humans, green algae, and higher plants. Plant Physiol 146, 351-367.
22. Comparot-Moss S, Kotting O, Stettler M, Edner C, Graf A, Weise SE, Streb S, Lue WL, MacLean D, Mahlow S, et al. (2010) A putative phosphatase, LSF1, is required for normal starch turnover in Arabidopsis leaves. Plant Physiol 152, 685-697.
23. Santelia D, Kotting O, Seung D, Schubert M, Thalmann M, Bischof S, Meekins DA, Lutz A, Patron N, Gentry MS, et al. (2011) The phosphoglucan phosphatase Like Sex Four2 dephosphorylates starch at the C3-position in Arabidopsis. Plant Cell 23, 4096-4111.
24. Kerk D, Conley TR, Rodriguez FA, Tran HT, Nimick M, Muench DG, &, Moorhead GB, (2006) A chloroplast-localized dual-specificity protein phosphatase in Arabidopsis contains a phylogenetically dispersed and ancient carbohydrate-binding domain, which binds the polysaccharide starch. Plant J 46, 400-413.
25. Vander Kooi CW, Taylor AO, Pace RM, Meekins DA, Guo HF, Kim Y, &, Gentry MS, (2010) Structural basis for the glucan phosphatase activity of Starch Excess4. Proc Natl Acad Sci USA 107, 15379-15384.
26. Hsu S, Kim Y, Li S, Durrant ES, Pace RM, Woods VLJ, &, Gentry MS, (2009) Structural insights into glucan phosphatase dynamics using amide hydrogen-deuterium exchange mass spectrometry. Biochemistry 48, 9891-9902.
27. Pannifer AD, Flint AJ, Tonks NK, &, Barford D, (1998) Visualization of the cysteinyl-phosphate intermediate of a protein-tyrosine phosphatase by X-ray crystallography. J Biol Chem 273, 10454-10462.
28. Denu JM, Lohse DL, Vijayalakshmi J, Saper MA, &, Dixon JE, (1996) Visualization of intermediate and transition-state structures in protein-tyrosine phosphatase catalysis. Proc Natl Acad Sci USA 93, 2493-2498.
29. Peters GH, Frimurer TM, &, Olsen OH, (1998) Electrostatic evaluation of the signature motif (H/V)CX5R(S/T) in protein-tyrosine phosphatases. Biochemistry 37, 5383-5393.
30. Denu JM, &, Dixon JE, (1998) Protein tyrosine phosphatases: mechanisms of catalysis and regulation. Curr Opin Chem Biol 2, 633-641.
31. Denu JM, &, Tanner KG, (1998) Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry 37, 5633-5642.
32. Salmeen A, &, Barford D, (2005) Functions and mechanisms of redox regulation of cysteine-based phosphatases. Antioxid Redox Signal 7, 560-577.
33. Salmeen A, Andersen JN, Myers MP, Meng TC, Hinks JA, Tonks NK, &, Barford D, (2003) Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423, 769-773.
34. Meng TC, Fukada T, &, Tonks NK, (2002) Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell 9, 387-399.
35. 2. J Biol Chem 277, 20336-20342.
36. Gupta R, &, Luan S, (2003) Redox control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants. Plant Physiol 132, 1149-1152.
37. Xu Q, Fu HH, Gupta R, &, Luan S, (1998) Molecular characterization of a tyrosine-specific protein phosphatase encoded by a stress-responsive gene in Arabidopsis. Plant Cell 10, 849-857.
38. Sokolov LN, Dominguez-Solis JR, Allary AL, Buchanan BB, &, Luan S, (2006) A redox-regulated chloroplast protein phosphatase binds to starch diurnally and functions in its accumulation. Proc Natl Acad Sci USA 103, 9732-9737.
39. Schurmann P, &, Jacquot JP, (2000) Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Mol Biol 51, 371-400.
40. Lemaire SD, Michelet L, Zaffagnini M, Massot V, &, Issakidis-Bourguet E, (2007) Thioredoxins in chloroplasts. Curr Genet 51, 343-365.
41. Collin V, Issakidis-Bourguet E, Marchand C, Hirasawa M, Lancelin JM, Knaff DB, &, Miginiac-Maslow M, (2003) The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. J Biol Chem 278, 23747-23752.
42. Collin V, Lamkemeyer P, Miginiac-Maslow M, Hirasawa M, Knaff DB, Dietz KJ, &, Issakidis-Bourguet E, (2004) Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type. Plant Physiol 136, 4088-4095.
43. Tanner JJ, Parsons ZD, Cummings AH, Zhou H, &, Gates KS, (2011) Redox regulation of protein tyrosine phosphatases: structural and chemical aspects. Antioxid Redox Signal 15, 77-97.
44. Heazlewood JL, Durek P, Hummel J, Selbig J, Weckwerth W, Walther D, &, Schulze WX, (2008) PhosPhAt: a database of phosphorylation sites in Arabidopsis thaliana and a plant-specific phosphorylation site predictor. Nucleic Acids Res 36, D1015-D1021.
45. Durek P, Schmidt R, Heazlewood JL, Jones A, MacLean D, Nagel A, Kersten B, &, Schulze WX, (2010) PhosPhAt: the Arabidopsis thaliana phosphorylation site database. An update. Nucleic Acids Res 38, D828-D834.
46. Seth D, &, Rudolph J, (2006) Redox regulation of MAP kinase phosphatase 3. Biochemistry 45, 8476-8487.
47. Kötting O, Kossmann J, Zeeman SC, &, Lloyd JR, (2010) Regulation of starch metabolism: the age of enlightenment? Curr Opin Plant Biol 13, 321-329.
48. Tiessen A, Hendriks JH, Stitt M, Branscheid A, Gibon Y, Farre EM, &, Geigenberger P, (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14, 2191-2213.
49. Hendriks JH, Kolbe A, Gibon Y, Stitt M, &, Geigenberger P, (2003) ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol 133, 838-849.
50. Mikkelsen R, Mutenda KE, Mant A, Schurmann P, &, Blennow A, (2005) α-Glucan,water dikinase (GWD): a plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proc Natl Acad Sci USA 102, 1785-1790.
51. Sparla F, Costa A, Lo Schiavo F, Pupillo P, &, Trost P, (2006) Redox regulation of a novel plastid-targeted β-amylase of Arabidopsis. Plant Physiol 141, 840-850.
52. Valerio C, Costa A, Marri L, Issakidis-Bourguet E, Pupillo P, Trost P, &, Sparla F, (2010) Thioredoxin-regulated β-amylase (BAM1) triggers diurnal starch degradation in guard cells, and in mesophyll cells under osmotic stress. J Exp Bot 62, 545-555.
53. Ferrar T, Chamousset D, Nimick M, De Wever V, Andersen J, Trinkle-Mulcahy L, &, Moorhead GBG, (2012) Taperin (c9orf75), a mutated gene in nonsyndromic deafness, encodes a vertebrate specific, nuclear localized protein phosphatase one alpha (PP1α) docking protein. Biology Open 1, 128-139.
54. Montrichard F, Alkhalfioui F, Yano H, Vensel WH, Hurkman WJ, &, Buchanan BB, (2009) Thioredoxin targets in plants: the first 30 years. J Proteomics 72, 452-474.
55. Worby CA, Gentry MS, &, Dixon JE, (2006) Laforin, a dual specificity phosphatase that dephosphorylates complex carbohydrates. J Biol Chem 281, 30412-30418.
56. Schurmann P, (1995) Ferredoxin:thioredoxin system. Methods Enzymol 252, 274-283.
57. Perkins DN, Pappin DJ, Creasy DM, &, Cottrell JS, (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567.
58. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, &, Bourne PE, (2000) The Protein Data Bank. Nucleic Acids Res 28, 235-242.
59. Song H, Hanlon N, Brown NR, Noble ME, Johnson LN, &, Barford D, (2001) Phosphoprotein-protein interactions revealed by the crystal structure of kinase-associated phosphatase in complex with phosphoCDK2. Mol Cell 7, 615-626.
60. Lee JO, Yang H, Georgescu MM, Di Cristofano A, Maehama T, Shi Y, Dixon JE, Pandolfi P, &, Pavletich NP, (1999) Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell 99, 323-334.