Effect of Nitric Oxide on the Interaction Between Mitochondrial Malate Dehydrogenase and Citrate Synthase

doi:10.1016/S2095-3119(13)60736-4

Journal of Integrative Agriculture ›› 2014, Vol. 13 ›› Issue (12): 2616-2624.DOI: 10.1016/S2095-3119(13)60736-4

Effect of Nitric Oxide on the Interaction Between Mitochondrial Malate Dehydrogenase and Citrate Synthase

LIU Yu-chen, WANG Juan, SU Pei-ying, MA Chun-mei , ZHU Shu-hua

1、College of Chemistry and Material Science, Shandong Agricultural University, Tai’an 271018, P.R.China
2、Department of Horticultural and Forest Engineer, Heze University, Heze 274015, P.R.China
3、Tai’an Tumor Prevention and Treatment Hospital, Tai’an 271000, P.R.China

收稿日期:2013-11-04 出版日期:2014-12-01 发布日期:2014-12-10
通讯作者: ZHU Shu-hua, Tel: +86-538-8247790, E-mail: shuhua@sdau.edu.cn
作者简介:LIU Yu-chen, E-mail: 4660623@163.com;
基金资助:
Acknowledgements This work was supported by the National Natural Science Foundation of China (31270723, 31370686, 31470686) and the Science and Technology Development Planning of Shandong Province, China (2013CEX20109).

Effect of Nitric Oxide on the Interaction Between Mitochondrial Malate Dehydrogenase and Citrate Synthase

LIU Yu-chen, WANG Juan, SU Pei-ying, MA Chun-mei , ZHU Shu-hua

1、College of Chemistry and Material Science, Shandong Agricultural University, Tai’an 271018, P.R.China
2、Department of Horticultural and Forest Engineer, Heze University, Heze 274015, P.R.China
3、Tai’an Tumor Prevention and Treatment Hospital, Tai’an 271000, P.R.China

Received:2013-11-04 Online:2014-12-01 Published:2014-12-10
Contact: ZHU Shu-hua, Tel: +86-538-8247790, E-mail: shuhua@sdau.edu.cn
About author:LIU Yu-chen, E-mail: 4660623@163.com;
Supported by:
Acknowledgements This work was supported by the National Natural Science Foundation of China (31270723, 31370686, 31470686) and the Science and Technology Development Planning of Shandong Province, China (2013CEX20109).

摘要/Abstract

摘要： Mitochondrial malate dehydrogenase (mMDH) and citrate synthase (CS) are sequential enzymes in Krebs cycle. mMDH, CS and the complex between mMDH and CS (mMDH+CS) were treated with nitric oxide solution. The roles of notric oxide (NO) on the secondary structures and the interactions between mMDH and CS were studied using circular diehroism (CD) and Fourier transform surface plasmon resonance (FT-SPR), respectivley. The effects of NO on the activities of mMDH, CS and mMDH+CS were also studied. And the regulations by NO on mMDH and CS were simulated by PyMOL software. The results of SPR confirmed that strong interaction between mMDH and CS existed and NO could significantly regulate the interaction between the two enzymes. NO reduced the mass percents of α-helix and increased that of random in mMDH, CS and mMDH+CS. NO increased the activities of CS and mMDH+CS, and inhibited the activity of mMDH. Graphic simulation indicated that covalent bond was formed between NO and Asn242 in active site of CS. However, there was no direct bond between NO and mMDH. The increase in activity of mMDH+CS complex depended mostly on the interaction between NO and CS. All the results suggested that the regulations by NO on the activity and interaction between mMDH and CS were accord with the changes in mMDH, CS and mMDH+CS caused by NO.

关键词: Krebs cycle , nitric oxide , surface plasmon resonance , protein-protein interaction , citrate synthase , malate dehydrogenase

Abstract: Mitochondrial malate dehydrogenase (mMDH) and citrate synthase (CS) are sequential enzymes in Krebs cycle. mMDH, CS and the complex between mMDH and CS (mMDH+CS) were treated with nitric oxide solution. The roles of notric oxide (NO) on the secondary structures and the interactions between mMDH and CS were studied using circular diehroism (CD) and Fourier transform surface plasmon resonance (FT-SPR), respectivley. The effects of NO on the activities of mMDH, CS and mMDH+CS were also studied. And the regulations by NO on mMDH and CS were simulated by PyMOL software. The results of SPR confirmed that strong interaction between mMDH and CS existed and NO could significantly regulate the interaction between the two enzymes. NO reduced the mass percents of α-helix and increased that of random in mMDH, CS and mMDH+CS. NO increased the activities of CS and mMDH+CS, and inhibited the activity of mMDH. Graphic simulation indicated that covalent bond was formed between NO and Asn242 in active site of CS. However, there was no direct bond between NO and mMDH. The increase in activity of mMDH+CS complex depended mostly on the interaction between NO and CS. All the results suggested that the regulations by NO on the activity and interaction between mMDH and CS were accord with the changes in mMDH, CS and mMDH+CS caused by NO.

Key words: Krebs cycle , nitric oxide , surface plasmon resonance , protein-protein interaction , citrate synthase , malate dehydrogenase

LIU Yu-chen, WANG Juan, SU Pei-ying, MA Chun-mei , ZHU Shu-hua. Effect of Nitric Oxide on the Interaction Between Mitochondrial Malate Dehydrogenase and Citrate Synthase[J]. Journal of Integrative Agriculture, 2014, 13(12): 2616-2624.

参考文献

Brown G C, Borutaite V. 2002. Nitric oxide inhibition ofmitochondrial respiration and its role in cell death. FreeRadical Biology and Medicine, 33, 1440-1450

Buxbaum E 2011. Protein secondary structure. In: BiophysicalChemistry of Proteins. Springer, US. pp. 291-302

Centeno D C, Osorio S, Nunes-Nesi A, Bertolo A L F, CarneiroR T, Araújo W L, Steinhauser M C, Michalska J, RohrmannJ, Geigenberger P, Olivera S N, Stitta M, Carrarid F,Roseb J, Ferniea A. 2011. Malate plays a crucial role instarch metabolism, ripening, and soluble solid content oftomato fruit and affects postharvest softening. The PlantCell, 23, 162-184

Choi S E, Lee Y J, Hwang G S, Chung J H, Lee S J, Lee J H,Han S J, Kim H J, Lee K W, Kim Y. 2011. Supplementof TCA cycle intermediates protects against high glucose/palmitate-induced INS-1 beta cell death Archives ofBiochemistry and Biophysics, 505, 231-241

Chow K M, Ma Z, Cai J, Pierce W M, Hersh L B. 2005.Nardilysin facilitates complex formation betweenmitochondrial malate dehydrogenase and citrate synthase.Biochimica et Biophysica Acta, 1723, 292-301

La Cognata U, Landschutze V, Willmitzer L, Muller-RoberB. 1996. Structure and expression of mitochondrial citratesynthases from higher plants. Plant Cell Physiology, 37,1022-1029

Dai Z, Wu Z, Yang Y, Wang J, Satterfield M C, MeiningerC J, Bazer F W, Wu G. 2013. Nitric oxide and energymetabolism in mammals. BioFactors, 39, 383-391

Daidone I, Roccatano D, Hayward S. 2004. Investigating theaccessibility of the closed domain conformation of citratesynthase using essential dynamics sampling. Journal ofMolecular Biology, 339, 515-525

Deng W, Luo K, Li Z, Yang Y, Hu N, Wu Y. 2009.Overexpression of Citrus junos mitochondrial citratesynthase gene in Nicotiana benthamiana confers aluminumtolerance. Planta, 230, 355-365

Duan X, Su X, You Y, Qu H, Li Y, Jiang Y. 2007. Effect ofnitric oxide on pericarp browning of harvested longanfruit in relation to phenolic metabolism. Food Chemistry,104, 571-576

Elcock A H, McCammon J A. 1996. Evidence for electrostaticchanneling in a fusion protein of malate dehydrogenase andcitrate synthase. Biochemistry, 35, 12652-12658

Etienne A, Genard M, Lobit P, Mbeguie A M D, BugaudC. 2013. What controls fleshy fruit acidity? A review ofmalate and citrate accumulation in fruit cells. Journal ofExperimental Botany, 64, 1451-1469

Gould N, Doulias P T, Tenopoulou M, Raju K, IschiropoulosH. 2013. Regulation of protein function and signaling byreversible cysteine S-nitrosylation. Journal of BiologicalChemistry, 288, 26473-26479

Han D G, Wang Y, Zhang L, Ma L, Zhang X Z, Xu X F,Han Z H. 2012. Isolation and functional characterizationof MxCS1: a gene encoding a citrate synthase in Malusxiaojinensis. Biologia Plantarum, 56, 50-56

Iannetta P P M, Escobar N M, Ross H A, Souleyre EJ F, Hancock R D, Witte C P, Davies H V. 2004.Identification, cloning and expression analysis ofstrawberry (Fragaria×ananassa) mitochondrial citratesynthase and mitochondrial malate dehydrogenase.Physiologia Plantarum, 121, 15-26

Karplus M, Kuriyan J. 2005. Molecular dynamics and proteinfunction. Proceedings of the National Academy of Sciencesof the United States of America, 102, 6679-6685

Keighron J D, Keating C D. 2010. Enzyme: Nanoparticlebioconjugates with two sequential enzymes: Stoichiometryand activity of malate dehydrogenase and citrate synthaseon Au nanoparticles. Langmuir, 26, 18992-19000

Koyama H, Kawamura A, Kihara T, Hara T, Takita E, ShibataD. 2000. Overexpression of mitochondrial citrate synthasein Arabidopsis thaliana improved growth on a phosphoruslimitedsoil. Plant and Cell Physiology, 41, 1030-1037

Koyama H, Takita E, Kawamura A, Hara T, Shibata D.1999. Over expression of mitochondrial citrate synthasegene improves the growth of carrot cells in Al-phosphatemedium. Plant and Cell Physiology, 40, 482-488

Landschutze V, Muller-Rober B, Willmitzer L. 1995.Mitochondrial citrate synthase from potato: Predominantexpression in mature leaves and young flower buds. Planta,196, 756-764

Larson S B, Day J S, Nguyen C, Cudney R, McPherson A.2009. Structure of pig heart citrate synthase at 1.78 Aresolution. Acta Crystallographica Section F, 65, 430-434

Lindbladh C, Rault M, Hagglund C, Small W, Mosbach K,Bulow L, Evans C, Srere P. 1994. Preparation and kineticcharacterization of a fusion protein of yeast mitochondrialcitrate synthase and malate dehydrogenase. Biochemistry,33, 11692-11698

Liu J H, Chi G H, Jia C H, Zhang J B, Xu B Y, Jin Z Q. 2013.Function of a citrate synthase gene (MaGCS) duringpostharvest banana fruit ripening. Postharvest Biology andTechnology, 84, 43-50

Lu X P, Liu Y Z, Zhou G F, Wei Q J, Hu H J, Peng S A.2011. Identification of organic acid-related genes and theirexpression profiles in two pear (Pyrus pyrifolia) cultivarswith difference in predominant acid type at fruit ripeningstage. Scientia Horticulturae, 129, 680-687

Lü J, Gao X, Dong Z, Yi J, An L. 2012. Improved phosphorusacquisition by tobacco through transgenic expression ofmitochondrial malate dehydrogenase from Penicillium oxalicum. Plant Cell Reports, 31, 49-56

Ma C, Sun Z, Zhou J, Zhu S. 2011. Effects of exogenousnitric oxide on Krebs cycle-associated enzyme activitiesin Feicheng peach fruit. In: The 3rd Conference on KeyTechnology of Horticulture. Shenyang, China. LondonScience Publishing, UK. pp. 275-283

Madeira A, Vikeved E, Nilsson A, Sjögren B, Andrén P E,Svenningsson P. 2011. Identification of protein-proteininteractions by surface plasmon resonance followed bymass spectrometry. Current Protocols in Protein Science,65:19.21:19.21.1–19.21.9. http://onlinelibrary.wiley.com/doi/10.1002/0471140864.ps1921s65/full

Manjunatha G, Lokesh V, Neelwarne B. 2010. Nitric oxidein fruit ripening: Trends and opportunities. BiotechnologyAdvances, 28, 489-499

McCarthy N. 2013. Metabolism: Sensitivity to serinestarvation. Nature Reviews Cancer, 13, 77-77

Meeks J C. 2011. Closing the cycle. Science, 334, 1508-1509

van der Merwe M J, Osorio S, Moritz T, Nunes-Nesi A,Fernie A R. 2009. Decreased mitochondrial activitiesof malate dehydrogenase and fumarase in tomato leadto altered root growth and architecture via diversemechanisms. Plant Physiology, 149, 653-669

Meyer F M, Gerwig J, Hammer E, Herzberg C, CommichauF M, Völker U, Stülke J. 2011. Physical interactionsbetween tricarboxylic acid cycle enzymes in Bacillussubtilis: evidence for a metabolon. Metabolic Engineering,13, 18-27

Minarik P, Tomaskova N, Kollarova M, Antalik M. 2002.Malate dehydrogenases-structure and function. GeneralPhysiology and Biophysics, 21, 257-266

Morgunov I, Srere P A. 1998. Interaction between citratesynthase and malate dehydrogenase substrate channelingof oxaloacetate. Journal of Biological Chemistry, 273,29540-29544

Nunes-Nesi A, Araújo W L, Obata T, Fernie A R. 2013.Regulation of the mitochondrial tricarboxylic acid cycle.Current Opinion in Plant Biology, 16, 335-343

Nunes-Nesi A, Carrari F, Lytovchenko A, Smith A M O, EhlersLoureiro M, Ratcliffe R G, Sweetlove L J, Fernie A R.2005. Enhanced photosynthetic performance and growthas a consequence of decreasing mitochondrial malatedehydrogenase activity in transgenic tomato plants. PlantPhysiology, 137, 611-622

OrE, Baybik J, Sadka A, Saks Y. 2000. Isolation of mitochondrialmalate dehydrogenase and phosphoenolpyruvatecarboxylase cDNA clones from grape berries and analysisof their expression pattern throughout berry development.Journal of Plant Physiology, 157, 527-534

Peti-Peterdi J. 2013. Mitochondrial TCA cycle intermediatesregulate body fluid and acid-base balance. The Journal ofClinical Investigation, 123, 2788-2790

Pettersson H, Olsson P, Bülow L, Pettersson G. 2000. Kineticsof the coupled reaction catalysed by a fusion protein ofyeast mitochondrial malate dehydrogenase and citratesynthase. European Journal of Biochemistry, 267, 5041-5046

Sarti P, Arese M, Forte E, Giuffrè A, Mastronicola D.2012. Mitochondria and nitric oxide: chemistry andpathophysiology. In: Scatena R, Bottoni P, Giardina B,eds., Advances in Mitochondrial Medicine. Vol 942.Springer, Netherlands. pp. 75-92

Schrodinger, L L C. 2010. The PyMOL molecular graphicssystem. ver. 1.3rl. [2011-6-2] http://sourceforge.net/projects/pymol/files/.

Siriwardena K, MacKay N, Levandovskiy V, Blaser S,Raiman J, Kantor P F, Ackerley C, Robinson BH, SchulzeA, Cameron J M. 2013. Mitochondrial citrate synthasecrystals: Novel finding in Sengers syndrome caused byacylglycerol kinase (AGK) mutations. Molecular Geneticsand Metabolism, 108, 40-50

Sun Z, Li Y, Zhou J, Zhu S H. 2011. Effects of exogenousnitric oxide on contents of soluble sugars and relatedenzyme activities in ‘Feicheng’ peach fruit. Journal of theScience of Food and Agriculture, 91, 1795-1800

Sweetlove L J, Beard K F M, Nunes-Nesi A, Fernie A R,Ratcliffe R G. 2010. Not just a circle: Flux modes in theplant TCA cycle. Trends in Plant Science, 15, 462-470

Tomaz T, Bagard M, Pracharoenwattana I, Lindén P, LeeC P, Carroll A J, Ströher E, Smith S M, Gardeström P,Millar A H. 2010. Mitochondrial malate dehydrogenaselowers leaf respiration and alters photorespiration and plantgrowth in Arabidopsis. Plant Physiology, 154, 1143-1157

Tompa P, Batke J, Ovadi J, Welch G R, Srere P A. 1987.Quantitation of the interaction between citrate synthase andmalate dehydrogenase. Journal of Biological Chemistry,262, 6089-6092

Wang X Y, Wang B, Hou S T, Zhu G P. 2009. Structure andfunction of malate dehydrogenases. Journal of Biology,4, 69-72

Wang X, Li J, Liu J, He W, Bi Y. 2010. Nitric oxide increasesmitochondrial respiration in a cGMP-dependent mannerin the callus from Arabidopsis thaliana. Nitric Oxide, 23,242-250

Yang L T, Chen L S, Peng H Y, Guo P, Wang P, Ma C L. 2012.Organic acid metabolism in Citrus grandis leaves androots is differently affected by nitric oxide and aluminuminteractions. Scientia Horticulturae, 133, 40-46

Zhang S, Bryant D A. 2011. The tricarboxylic acid cycle incyanobacteria. Science, 334, 1551-1553

Zhu L Q, Zhou J, Zhu S H. 2010. Effect of a combinationof nitric oxide treatment and intermittent warming onprevention of chilling injury of ‘Feicheng’ peach fruitduring storage. Food Chemistry, 121, 165-170

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Effect of Nitric Oxide on the Interaction Between Mitochondrial Malate Dehydrogenase and Citrate Synthase

Effect of Nitric Oxide on the Interaction Between Mitochondrial Malate Dehydrogenase and Citrate Synthase

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