Exploring Redox Modulation of Plant UDP-Glucose Pyrophosphorylase

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2023 May 27

PMID 37240260

Authors

Daniel Decker

Juliette Aubert

Malgorzata Wilczynska

Leszek A Kleczkowski

Affiliations

Soon will be listed here.

Abstract

UDP-glucose (UDPG) pyrophosphorylase (UGPase) catalyzes a reversible reaction, producing UDPG, which serves as an essential precursor for hundreds of glycosyltransferases in all organisms. In this study, activities of purified UGPases from sugarcane and barley were found to be reversibly redox modulated in vitro through oxidation by hydrogen peroxide or oxidized glutathione (GSSG) and through reduction by dithiothreitol or glutathione. Generally, while oxidative treatment decreased UGPase activity, a subsequent reduction restored the activity. The oxidized enzyme had increased values with substrates, especially pyrophosphate. The increased values were also observed, regardless of redox status, for UGPase cysteine mutants (Cys102Ser and Cys99Ser for sugarcane and barley UGPases, respectively). However, activities and substrate affinities (s) of sugarcane Cys102Ser mutant, but not barley Cys99Ser, were still prone to redox modulation. The data suggest that plant UGPase is subject to redox control primarily via changes in the redox status of a single cysteine. Other cysteines may also, to some extent, contribute to UGPase redox status, as seen for sugarcane enzymes. The results are discussed with respect to earlier reported details of redox modulation of eukaryotic UGPases and regarding the structure/function properties of these proteins.

References

Le Gall H, Philippe F, Domon J, Gillet F, Pelloux J, Rayon C . Cell Wall Metabolism in Response to Abiotic Stress. Plants (Basel). 2016; 4(1):112-66. PMC: 4844334. DOI: 10.3390/plants4010112. View

Stucki J . The thermodynamic-buffer enzymes. Eur J Biochem. 1980; 109(1):257-67. DOI: 10.1111/j.1432-1033.1980.tb04791.x. View

Iyer B, Mahalakshmi R . Hydrophobic Characteristic Is Energetically Preferred for Cysteine in a Model Membrane Protein. Biophys J. 2019; 117(1):25-35. PMC: 6626846. DOI: 10.1016/j.bpj.2019.05.024. View

Igamberdiev A, Kleczkowski L . Magnesium and cell energetics in plants under anoxia. Biochem J. 2011; 437(3):373-9. DOI: 10.1042/BJ20110213. View

Park J, Ishimizu T, Suwabe K, Sudo K, Masuko H, Hakozaki H . UDP-glucose pyrophosphorylase is rate limiting in vegetative and reproductive phases in Arabidopsis thaliana. Plant Cell Physiol. 2010; 51(6):981-96. DOI: 10.1093/pcp/pcq057. View

Decker D, Oberg C, Kleczkowski L . Identification and characterization of inhibitors of UDP-glucose and UDP-sugar pyrophosphorylases for in vivo studies. Plant J. 2017; 90(6):1093-1107. DOI: 10.1111/tpj.13531. View

Soares J, Gentile A, Scorsato V, Lima A, Kiyota E, Dos Santos M . Oligomerization, membrane association, and in vivo phosphorylation of sugarcane UDP-glucose pyrophosphorylase. J Biol Chem. 2014; 289(48):33364-77. PMC: 4246093. DOI: 10.1074/jbc.M114.590125. View

Elling L, Kula M . Purification of UDP-glucose pyrophosphorylase from germinated barley (malt). J Biotechnol. 1994; 34(2):157-63. DOI: 10.1016/0168-1656(94)90085-x. View

Meng M, Geisler M, Johansson H, Mellerowicz E, Karpinski S, Kleczkowski L . Differential tissue/organ-dependent expression of two sucrose- and cold-responsive genes for UDP-glucose pyrophosphorylase in Populus. Gene. 2007; 389(2):186-95. DOI: 10.1016/j.gene.2006.11.006. View

10.

Decker D, Kleczkowski L . Substrate Specificity and Inhibitor Sensitivity of Plant UDP-Sugar Producing Pyrophosphorylases. Front Plant Sci. 2017; 8:1610. PMC: 5609113. DOI: 10.3389/fpls.2017.01610. View

11.

Ebrecht A, Asencion Diez M, Piattoni C, Guerrero S, Iglesias A . The UDP-glucose pyrophosphorylase from Giardia lamblia is redox regulated and exhibits promiscuity to use galactose-1-phosphate. Biochim Biophys Acta. 2014; 1850(1):88-96. DOI: 10.1016/j.bbagen.2014.10.002. View

12.

Weber J, Senior A . Location and properties of pyrophosphate-binding sites in Escherichia coli F1-ATPase. J Biol Chem. 1995; 270(21):12653-8. DOI: 10.1074/jbc.270.21.12653. View

13.

McCoy J, Bitto E, Bingman C, Wesenberg G, Bannen R, Kondrashov D . Structure and dynamics of UDP-glucose pyrophosphorylase from Arabidopsis thaliana with bound UDP-glucose and UTP. J Mol Biol. 2006; 366(3):830-41. PMC: 1847403. DOI: 10.1016/j.jmb.2006.11.059. View

14.

Kim G, Weiss S, Levine R . Methionine oxidation and reduction in proteins. Biochim Biophys Acta. 2013; 1840(2):901-5. PMC: 3766491. DOI: 10.1016/j.bbagen.2013.04.038. View

15.

Yan S, Tang Z, Su W, Sun W . Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics. 2005; 5(1):235-44. DOI: 10.1002/pmic.200400853. View

16.

Kleczkowski L, Decker D . Effects of Magnesium, Pyrophosphate and Phosphonates on Pyrophosphorolytic Reaction of UDP-Glucose Pyrophosphorylase. Plants (Basel). 2022; 11(12). PMC: 9230926. DOI: 10.3390/plants11121611. View

17.

Hasanuzzaman M, Nahar K, Anee T, Fujita M . Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiol Mol Biol Plants. 2017; 23(2):249-268. PMC: 5391355. DOI: 10.1007/s12298-017-0422-2. View

18.

Carpentier S, Witters E, Laukens K, Van Onckelen H, Swennen R, Panis B . Banana (Musa spp.) as a model to study the meristem proteome: acclimation to osmotic stress. Proteomics. 2006; 7(1):92-105. DOI: 10.1002/pmic.200600533. View

19.

Ciereszko I, Johansson H, Kleczkowski L . Sucrose and light regulation of a cold-inducible UDP-glucose pyrophosphorylase gene via a hexokinase-independent and abscisic acid-insensitive pathway in Arabidopsis. Biochem J. 2001; 354(Pt 1):67-72. PMC: 1221629. DOI: 10.1042/0264-6021:3540067. View

20.

Martz F, Wilczynska M, Kleczkowski L . Oligomerization status, with the monomer as active species, defines catalytic efficiency of UDP-glucose pyrophosphorylase. Biochem J. 2002; 367(Pt 1):295-300. PMC: 1222863. DOI: 10.1042/BJ20020772. View