Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Influence of Oxidative Stress on Catalytic and Non-glycolytic Functions of Glyceraldehyde-3-phosphate Dehydrogenase

Author(s): Vladimir I. Muronetz*, Aleksandra K. Melnikova, ">Luciano Saso and Elena V. Schmalhausen

Volume 27, Issue 13, 2020

Page: [2040 - 2058] Pages: 19

DOI: 10.2174/0929867325666180530101057

Price: $65

Abstract

Background: Glyceraldehyde-3-phosphate Dehydrogenase (GAPDH) is a unique enzyme that, besides its main function in glycolysis (catalysis of glyceraldehyde-3-phosphate oxidation), possesses a number of non-glycolytic activities. The present review summarizes information on the role of oxidative stress in the regulation of the enzymatic activity as well as non-glycolytic functions of GAPDH.

Methods: Based on the analysis of literature data and the results obtained in our research group, mechanisms of the regulation of GAPDH functions through the oxidation of the sulfhydryl groups in the active site of the enzyme have been suggested.

Results: Mechanism of GAPDH oxidation includes consecutive oxidation of the catalytic Cysteine (Cys150) into sulfenic, sulfinic, and sulfonic acid derivatives, resulting in the complete inactivation of the enzyme. The cysteine sulfenic acid reacts with reduced glutathione (GSH) to form a mixed disulfide (S-glutathionylated GAPDH) that further reacts with Cys154 yielding the disulfide bond in the active site of the enzyme. In contrast to the sulfinic and sulfonic acids, the mixed disulfide and the intramolecular disulfide bond are reversible oxidation products that can be reduced in the presence of GSH or thioredoxin.

Conclusion: Oxidation of sulfhydryl groups in the active site of GAPDH is unavoidable due to the enhanced reactivity of Cys150. The irreversible oxidation of Cys150 is prevented by Sglutathionylation and disulfide bonding with Cys154. The oxidation/reduction of the sulfhydryl groups in the active site of GAPDH can be used for regulation of glycolysis and numerous side activities of this enzyme including the induction of apoptosis.

Keywords: Glyceraldehyde-3-phosphate dehydrogenase, sulfhydryl groups, oxidation, S-nitrosylation, S-glutathionylation, oxidative stress.

[1]
Seidler, N.W. GAPDH: biological properties and diversity in: Advances in experimental medicine and biology; Crusio, W.E.; Lambris, J.D.; Radeke, H.H.; Rezaei, N. (Eds.), Springer, 2013, Vol. 985.
[http://dx.doi.org/10.1007/978-94-007-4716-6]
[2]
Harris, J.I.; Waters, M. Glyceraldehyde 3-Phosphate Dehydrogenase in: The enzymes, 3rd edition, Oxidationreduction Part C; Boyer, P. D., Ed.; Academic Press: London, 1976, vol. XIII.
[3]
Peralta, D.; Bronowska, A.K.; Morgan, B.; Dóka, É.; Van Laer, K.; Nagy, P.; Gräter, F.; Dick, T.P. A proton relay enhances H2O2 sensitivity of GAPDH to facilitate metabolic adaptation. Nat. Chem. Biol., 2015, 11(2), 156-163.
[http://dx.doi.org/10.1038/nchembio.1720] [PMID: 25580853]
[4]
Schmalhausen, E.V.; Nagradova, N.K.; Boschi-Muller, S.; Branlant, G.; Muronetz, V.I. Mildly oxidized GAPDH: the coupling of the dehydrogenase and acyl phosphatase activities. FEBS Lett., 1999, 452(3), 219-222.
[http://dx.doi.org/10.1016/S0014-5793(99)00627-4] [PMID: 10386594]
[5]
Zaffagnini, M.; Michelet, L.; Marchand, C.; Sparla, F.; Decottignies, P.; Le Maréchal, P.; Miginiac-Maslow, M.; Noctor, G.; Trost, P.; Lemaire, S.D. The thioredoxin-independent isoform of chloroplastic glyceraldehyde-3-phosphate dehydrogenase is selectively regulated by glutathionylation. FEBS J., 2007, 274(1), 212-226.
[http://dx.doi.org/10.1111/j.1742-4658.2006.05577.x] [PMID: 17140414]
[6]
Deng, X.; Liang, H.; Ulanovskaya, O.A.; Ji, Q.; Zhou, T.; Sun, F.; Lu, Z.; Hutchison, A.L.; Lan, L.; Wu, M.; Cravatt, B.F.; He, C. Steady-state hydrogen peroxide induces glycolysis in Staphylococcus aureus and Pseudomonas aeruginosa. J. Bacteriol., 2014, 196(14), 2499-2513.
[http://dx.doi.org/10.1128/JB.01538-14] [PMID: 24769698]
[7]
Cabiscol, E.; Piulats, E.; Echave, P.; Herrero, E.; Ros, J. Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. J. Biol. Chem., 2000, 275(35), 27393-27398.
[http://dx.doi.org/10.1074/jbc.M003140200] [PMID: 10852912]
[8]
Costa, V.M.V.; Amorim, M.A.; Quintanilha, A.; Moradas-Ferreira, P. Hydrogen peroxide-induced carbonylation of key metabolic enzymes in Saccharomyces cerevisiae: the involvement of the oxidative stress response regulators Yap1 and Skn7. Free Radic. Biol. Med., 2002, 33(11), 1507-1515.
[http://dx.doi.org/10.1016/S0891-5849(02)01086-9] [PMID: 12446208]
[9]
Shenton, D.; Perrone, G.; Quinn, K.A.; Dawes, I.W.; Grant, C.M. Regulation of protein S-thiolation by glutaredoxin 5 in the yeast Saccharomyces cerevisiae. J. Biol. Chem., 2002, 277(19), 16853-16859.
[http://dx.doi.org/10.1074/jbc.M200559200] [PMID: 11882660]
[10]
Nakajima, H.; Amano, W.; Fujita, A.; Fukuhara, A.; Azuma, Y-T.; Hata, F.; Inui, T.; Takeuchi, T. The active site cysteine of the proapoptotic protein glyceraldehyde-3-phosphate dehydrogenase is essential in oxidative stress-induced aggregation and cell death. J. Biol. Chem., 2007, 282(36), 26562-26574.
[http://dx.doi.org/10.1074/jbc.M704199200] [PMID: 17613523]
[11]
Nakajima, H.; Amano, W.; Kubo, T.; Fukuhara, A.; Ihara, H.; Azuma, Y-T.; Tajima, H.; Inui, T.; Sawa, A.; Takeuchi, T. Glyceraldehyde-3-phosphate dehydrogenase aggregate formation participates in oxidative stress-induced cell death. J. Biol. Chem., 2009, 284(49), 34331-34341.
[http://dx.doi.org/10.1074/jbc.M109.027698] [PMID: 19837666]
[12]
Meyer-Siegler, K.; Mauro, D.J.; Seal, G.; Wurzer, J.; deRiel, J.K.; Sirover, M.A. A human nuclear uracil DNA glycosylase is the 37-kDa subunit of glyceraldehyde-3-phosphate dehydrogenase. Proc. Natl. Acad. Sci. USA, 1991, 88(19), 8460-8464.
[http://dx.doi.org/10.1073/pnas.88.19.8460] [PMID: 1924305]
[13]
Singh, R.; Green, M.R. Sequence-specific binding of transfer RNA by glyceraldehyde-3-phosphate dehydrogenase. Science, 1993, 259(5093), 365-368.
[http://dx.doi.org/10.1126/science.8420004] [PMID: 8420004]
[14]
Glaser, P.E.; Gross, R.W. Rapid plasmenylethanolamine-selective fusion of membrane bilayers catalyzed by an isoform of glyceraldehyde-3-phosphate dehydrogenase: discrimination between glycolytic and fusogenic roles of individual isoforms. Biochemistry, 1995, 34(38), 12193-12203.
[http://dx.doi.org/10.1021/bi00038a013] [PMID: 7547960]
[15]
Hara, M.R.; Agrawal, N.; Kim, S.F.; Cascio, M.B.; Fujimuro, M.; Ozeki, Y.; Takahashi, M.; Cheah, J.H.; Tankou, S.K.; Hester, L.D.; Ferris, C.D.; Hayward, S.D.; Snyder, S.H.; Sawa, A. S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat. Cell Biol., 2005, 7(7), 665-674.
[http://dx.doi.org/10.1038/ncb1268] [PMID: 15951807]
[16]
Ishitani, R.; Chuang, D.M. Glyceraldehyde-3-phosphate dehydrogenase antisense oligodeoxynucleotides protect against cytosine arabinonucleoside-induced apoptosis in cultured cerebellar neurons. Proc. Natl. Acad. Sci. USA, 1996, 93(18), 9937-9941.
[http://dx.doi.org/10.1073/pnas.93.18.9937] [PMID: 8790435]
[17]
Saunders, P.A.; Chalecka-Franaszek, E.; Chuang, D.M. Subcellular distribution of glyceraldehyde-3-phosphate dehydrogenase in cerebellar granule cells undergoing cytosine arabinoside-induced apoptosis. J. Neurochem., 1997, 69(5), 1820-1828.
[http://dx.doi.org/10.1046/j.1471-4159.1997.69051820.x] [PMID: 9349524]
[18]
Sawa, A.; Khan, A.A.; Hester, L.D.; Snyder, S.H. Glyceraldehyde-3-phosphate dehydrogenase: nuclear translocation participates in neuronal and nonneuronal cell death. Proc. Natl. Acad. Sci. USA, 1997, 94(21), 11669-11674.
[http://dx.doi.org/10.1073/pnas.94.21.11669] [PMID: 9326668]
[19]
Sirover, M.A. New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochim. Biophys. Acta, 1999, 1432(2), 159-184.
[http://dx.doi.org/10.1016/S0167-4838(99)00119-3] [PMID: 10407139]
[20]
Sirover, M.A. New nuclear functions of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in mammalian cells. J. Cell. Biochem., 2005, 95(1), 45-52.
[http://dx.doi.org/10.1002/jcb.20399] [PMID: 15770658]
[21]
Hara, M.R.; Snyder, S.H. Nitric oxide-GAPDH-Siah: a novel cell death cascade. Cell. Mol. Neurobiol., 2006, 26(4-6), 527-538.
[http://dx.doi.org/10.1007/s10571-006-9011-6] [PMID: 16633896]
[22]
Ishitani, R.; Tanaka, M.; Sunaga, K.; Katsube, N.; Chuang, D.M. Nuclear localization of overexpressed glyceraldehyde-3-phosphate dehydrogenase in cultured cerebellar neurons undergoing apoptosis. Mol. Pharmacol., 1998, 53(4), 701-707.
[http://dx.doi.org/10.1124/mol.53.4.701] [PMID: 9547361]
[23]
Arutyunova, E.I.; Domnina, L.V.; Chudinova, A.A.; Makshakova, O.N.; Arutyunov, D.Y.; Muronetz, V.I. Localization of non-native D-glyceraldehyde-3-phosphate dehydrogenase in growing and apoptotic HeLa cells. Biochemistry (Mosc.), 2013, 78(1), 91-95.
[http://dx.doi.org/10.1134/S0006297913010112] [PMID: 23379564]
[24]
Nagy, E.; Rigby, W.F. Glyceraldehyde-3-phosphate dehydrogenase selectively binds AU-rich RNA in the NAD(+)-binding region (Rossmann fold). J. Biol. Chem., 1995, 270(6), 2755-2763.
[http://dx.doi.org/10.1074/jbc.270.6.2755] [PMID: 7531693]
[25]
Backlund, M.; Paukku, K.; Daviet, L.; De Boer, R.A.; Valo, E.; Hautaniemi, S.; Kalkkinen, N.; Ehsan, A.; Kontula, K.K.; Lehtonen, J.Y. Posttranscriptional regulation of angiotensin II type 1 receptor expression by glyceraldehyde 3-phosphate dehydrogenase. Nucleic Acids Res., 2009, 37(7), 2346-2358.
[http://dx.doi.org/10.1093/nar/gkp098] [PMID: 19246543]
[26]
White, M.R.; Khan, M.M.; Deredge, D.; Ross, C.R.; Quintyn, R.; Zucconi, B.E.; Wysocki, V.H.; Wintrode, P.L.; Wilson, G.M.; Garcin, E.D. A dimer interface mutation in glyceraldehyde-3-phosphate dehydrogenase regulates its binding to AU-rich RNA. J. Biol. Chem., 2015, 290(3), 1770-1785.
[http://dx.doi.org/10.1074/jbc.M114.618165] [PMID: 25451934]
[27]
Barinova, K.; Khomyakova, E.; Semenyuk, P.; Schmalhausen, E.; Muronetz, V. Binding of alpha-synuclein to partially oxidized glyceraldehyde-3-phosphate dehydrogenase induces subsequent inactivation of the enzyme. Arch. Biochem. Biophys., 2018, 642, 10-22.
[http://dx.doi.org/10.1016/j.abb.2018.02.002] [PMID: 29408361]
[28]
Guzhova, I.V.; Lazarev, V.F.; Kaznacheeva, A.V.; Ippolitova, M.V.; Muronetz, V.I.; Kinev, A.V.; Margulis, B.A. Novel mechanism of Hsp70 chaperone-mediated prevention of polyglutamine aggregates in a cellular model of huntington disease. Hum. Mol. Genet., 2011, 20(20), 3953-3963.
[http://dx.doi.org/10.1093/hmg/ddr314] [PMID: 21775503]
[29]
Naletova, I.; Schmalhausen, E.; Kharitonov, A.; Katrukha, A.; Saso, L.; Caprioli, A.; Muronetz, V. Non-native glyceraldehyde-3-phosphate dehydrogenase can be an intrinsic component of amyloid structures. Biochim. Biophys. Acta, 2008, 1784(12), 2052-2058.
[http://dx.doi.org/10.1016/j.bbapap.2008.07.013] [PMID: 18725330]
[30]
Little, C.; O’Brien, P.J. Mechanism of peroxide-inactivation of the sulphydryl enzyme glyceraldehyde-3-phosphate dehydrogenase. Eur. J. Biochem., 1969, 10(3), 533-538.
[http://dx.doi.org/10.1111/j.1432-1033.1969.tb00721.x] [PMID: 5348077]
[31]
Cremers, C.M.; Jakob, U. Oxidant sensing by reversible disulfide bond formation. J. Biol. Chem., 2013, 288(37), 26489-26496.
[http://dx.doi.org/10.1074/jbc.R113.462929] [PMID: 23861395]
[32]
Biteau, B.; Labarre, J.; Toledano, M.B. ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature, 2003, 425(6961), 980-984.
[http://dx.doi.org/10.1038/nature02075] [PMID: 14586471]
[33]
Woo, H.A.; Jeong, W.; Chang, T-S.; Park, K.J.; Park, S.J.; Yang, J.S.; Rhee, S.G. Reduction of cysteine sulfinic acid by sulfiredoxin is specific to 2-cys peroxiredoxins. J. Biol. Chem., 2005, 280(5), 3125-3128.
[http://dx.doi.org/10.1074/jbc.C400496200] [PMID: 15590625]
[34]
Chang, T-S.; Jeong, W.; Woo, H.A.; Lee, S.M.; Park, S.; Rhee, S.G. Characterization of mammalian sulfiredoxin and its reactivation of hyperoxidized peroxiredoxin through reduction of cysteine sulfinic acid in the active site to cysteine. J. Biol. Chem., 2004, 279(49), 50994-51001.
[http://dx.doi.org/10.1074/jbc.M409482200] [PMID: 15448164]
[35]
You K-S, ; Benitez, L.V.; McConachie, W.A.; Allison, W.S. The conversion of glyceraldehyde-3-phosphate dehydrogenase to an acylphosphatase by trinitroglycerin and inactivation of this activity by azide and ascorbate. Biochim. Biophys. Acta, 1975, 384(2), 317-330.
[http://dx.doi.org/10.1016/0005-2744(75)90033-9] [PMID: 235996]
[36]
Poole, L.B.; Karplus, P.A.; Claiborne, A. Protein sulfenic acids in redox signaling. Annu. Rev. Pharmacol. Toxicol., 2004, 44, 325-347.
[http://dx.doi.org/10.1146/annurev.pharmtox.44.101802.121735] [PMID: 14744249]
[37]
Barinova, K.V.; Serebryakova, M.V.; Muronetz, V.I.; Schmalhausen, E.V. S-glutathionylation of glyceraldehyde-3-phosphate dehydrogenase induces formation of C150-C154 intrasubunit disulfide bond in the active site of the enzyme. Biochim. Biophys. Acta, Gen. Subj., 2017, 1861(12), 3167-3177.
[http://dx.doi.org/10.1016/j.bbagen.2017.09.008] [PMID: 28935607]
[38]
Parker, D.J.; Allison, W.S. The mechanism of inactivation of glyceraldehyde 3-phosphate dehydrogenase by tetrathionate, o-iodosobenzoate, and iodine monochloride. J. Biol. Chem., 1969, 244(1), 180-189.
[PMID: 5773281]
[39]
Ehring, R.; Colowick, S.P. The two-step formation and inactivation of acylphosphatase by agents acting on glyceraldehyde phosphate dehydrogenase. J. Biol. Chem., 1969, 244(17), 4589-4599.
[PMID: 4309146]
[40]
Schmalhausen, E.V.; Muronetz, V.I.; Nagradova, N.K. Rabbit muscle GAPDH: non-phosphorylating dehydrogenase activity induced by hydrogen peroxide. FEBS Lett., 1997, 414(2), 247-252.
[http://dx.doi.org/10.1016/S0014-5793(97)01044-2] [PMID: 9315695]
[41]
Danshina, P.V.; Schmalhausen, E.V.; Avetisyan, A.V.; Muronetz, V.I. Mildly oxidized glyceraldehyde-3-phosphate dehydrogenase as a possible regulator of glycolysis. IUBMB Life, 2001, 51(5), 309-314.
[http://dx.doi.org/10.1080/152165401317190824] [PMID: 11699877]
[42]
Schuppe-Koistinen, I.; Moldéus, P.; Bergman, T.; Cotgreave, I.A. S-thiolation of human endothelial cell glyceraldehyde-3-phosphate dehydrogenase after hydrogen peroxide treatment. Eur. J. Biochem., 1994, 221(3), 1033-1037.
[http://dx.doi.org/10.1111/j.1432-1033.1994.tb18821.x] [PMID: 8181459]
[43]
Gao, X-H.; Bedhomme, M.; Veyel, D.; Zaffagnini, M.; Lemaire, S.D. Methods for analysis of protein glutathionylation and their application to photosynthetic organisms. Mol. Plant, 2009, 2(2), 218-235.
[http://dx.doi.org/10.1093/mp/ssn072] [PMID: 19825609]
[44]
Newman, S.F.; Sultana, R.; Perluigi, M.; Coccia, R.; Cai, J.; Pierce, W.M.; Klein, J.B.; Turner, D.M.; Butterfield, D.A. An increase in S-glutathionylated proteins in the Alzheimer’s disease inferior parietal lobule, a proteomics approach. J. Neurosci. Res., 2007, 85(7), 1506-1514.
[http://dx.doi.org/10.1002/jnr.21275] [PMID: 17387692]
[45]
Bedhomme, M.; Adamo, M.; Marchand, C.H.; Couturier, J.; Rouhier, N.; Lemaire, S.D.; Zaffagnini, M.; Trost, P. Glutathionylation of cytosolic glyceraldehyde-3-phosphate dehydrogenase from the model plant Arabidopsis thaliana is reversed by both glutaredoxins and thioredoxins in vitro. Biochem. J., 2012, 445(3), 337-347.
[http://dx.doi.org/10.1042/BJ20120505] [PMID: 22607208]
[46]
Leichert, L.I.; Gehrke, F.; Gudiseva, H.V.; Blackwell, T.; Ilbert, M.; Walker, A.K.; Strahler, J.R.; Andrews, P.C.; Jakob, U. Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc. Natl. Acad. Sci. USA, 2008, 105(24), 8197-8202.
[http://dx.doi.org/10.1073/pnas.0707723105] [PMID: 18287020]
[47]
Roos, G.; Messens, J. Protein sulfenic acid formation: from cellular damage to redox regulation. Free Radic. Biol. Med., 2011, 51(2), 314-326.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.04.031] [PMID: 21605662]
[48]
Hogg, N. The biochemistry and physiology of S-nitrosothiols. Annu. Rev. Pharmacol. Toxicol., 2002, 42, 585-600.
[http://dx.doi.org/10.1146/annurev.pharmtox.42.092501.104328] [PMID: 11807184]
[49]
Giustarini, D.; Milzani, A.; Aldini, G.; Carini, M.; Rossi, R.; Dalle-Donne, I. S-nitrosation versus S-glutathionylation of protein sulfhydryl groups by S-nitrosoglutathione. Antioxid. Redox Signal., 2005, 7(7-8), 930-939.
[http://dx.doi.org/10.1089/ars.2005.7.930] [PMID: 15998248]
[50]
Hildebrandt, T.; Knuesting, J.; Berndt, C.; Morgan, B.; Scheibe, R. Cytosolic thiol switches regulating basic cellular functions: GAPDH as an information hub? Biol. Chem., 2015, 396(5), 523-537.
[http://dx.doi.org/10.1515/hsz-2014-0295] [PMID: 25581756]
[51]
Ralser, M.; Wamelink, M.M.; Kowald, A.; Gerisch, B.; Heeren, G.; Struys, E.A.; Klipp, E.; Jakobs, C.; Breitenbach, M.; Lehrach, H.; Krobitsch, S. Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress. J. Biol., 2007, 6(4), 10.
[http://dx.doi.org/10.1186/jbiol61] [PMID: 18154684]
[52]
Sirover, M.A. On the functional diversity of glyceraldehyde-3-phosphate dehydrogenase: biochemical mechanisms and regulatory control. Biochim. Biophys. Acta, 2011, 1810(8), 741-751.
[http://dx.doi.org/10.1016/j.bbagen.2011.05.010] [PMID: 21640161]
[53]
Rodríguez-Pascual, F.; Redondo-Horcajo, M.; Magán-Marchal, N.; Lagares, D.; Martínez-Ruiz, A.; Kleinert, H.; Lamas, S. Glyceraldehyde-3-phosphate dehydrogenase regulates endothelin-1 expression by a novel, redox-sensitive mechanism involving mRNA stability. Mol. Cell. Biol., 2008, 28(23), 7139-7155.
[http://dx.doi.org/10.1128/MCB.01145-08] [PMID: 18809573]
[54]
Hara, M.R.; Cascio, M.B.; Sawa, A. GAPDH as a sensor of NO stress. Biochim. Biophys. Acta, 2006, 1762(5), 502-509.
[http://dx.doi.org/10.1016/j.bbadis.2006.01.012] [PMID: 16574384]
[55]
Nakamura, T.; Prikhodko, O.A.; Pirie, E.; Nagar, S.; Akhtar, M.W.; Oh, C-K.; McKercher, S.R.; Ambasudhan, R.; Okamoto, S.; Lipton, S.A. Aberrant protein S-nitrosylation contributes to the pathophysiology of neurodegenerative diseases. Neurobiol. Dis., 2015, 84, 99-108.
[http://dx.doi.org/10.1016/j.nbd.2015.03.017] [PMID: 25796565]
[56]
Zahid, S.; Khan, R.; Oellerich, M.; Ahmed, N.; Asif, A.R. Differential S-nitrosylation of proteins in Alzheimer’s disease. Neuroscience, 2014, 256, 126-136.
[http://dx.doi.org/10.1016/j.neuroscience.2013.10.026] [PMID: 24157928]
[57]
Yang, Y.; Loscalzo, J. S-nitrosoprotein formation and localization in endothelial cells. Proc. Natl. Acad. Sci. USA, 2005, 102(1), 117-122.
[http://dx.doi.org/10.1073/pnas.0405989102] [PMID: 15618409]
[58]
Wang, J.; Wang, Y.; Lv, Q.; Wang, L.; Du, J.; Bao, F.; He, Y-K. Nitric oxide modifies root growth by S-nitrosylation of plastidial glyceraldehyde-3-phosphate dehydrogenase. Biochem. Biophys. Res. Commun., 2017, 488(1), 88-94.
[http://dx.doi.org/10.1016/j.bbrc.2017.05.012] [PMID: 28478036]
[59]
Zaffagnini, M.; Morisse, S.; Bedhomme, M.; Marchand, C.H.; Festa, M.; Rouhier, N.; Lemaire, S.D.; Trost, P. Mechanisms of nitrosylation and denitrosylation of cytoplasmic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana. J. Biol. Chem., 2013, 288(31), 22777-22789.
[http://dx.doi.org/10.1074/jbc.M113.475467] [PMID: 23749990]
[60]
Huang, B.; Chen, C. An ascorbate-dependent artifact that interferes with the interpretation of the biotin switch assay. Free Radic. Biol. Med., 2006, 41(4), 562-567.
[http://dx.doi.org/10.1016/j.freeradbiomed.2006.03.006] [PMID: 16863989]
[61]
Reisz, J.A.; Bechtold, E.; King, S.B.; Poole, L.B.; Furdui, C.M. Thiol-blocking electrophiles interfere with labeling and detection of protein sulfenic acids. FEBS J., 2013, 280(23), 6150-6161.
[http://dx.doi.org/10.1111/febs.12535] [PMID: 24103186]
[62]
Nakamura, T.; Lipton, S.A. Protein S-nitrosylation as a therapeutic target for neurodegenerative diseases. Trends Pharmacol. Sci., 2016, 37(1), 73-84.
[http://dx.doi.org/10.1016/j.tips.2015.10.002] [PMID: 26707925]
[63]
Shen, B.; English, A.M. Mass spectrometric analysis of nitroxyl-mediated protein modification: comparison of products formed with free and protein-based cysteines. Biochemistry, 2005, 44(42), 14030-14044.
[http://dx.doi.org/10.1021/bi0507478] [PMID: 16229492]
[64]
Yap, L-P.; Garcia, J.V.; Han, D.S.; Cadenas, E. Role of nitric oxide-mediated glutathionylation in neuronal function: potential regulation of energy utilization. Biochem. J., 2010, 428(1), 85-93.
[http://dx.doi.org/10.1042/BJ20100164] [PMID: 20210787]
[65]
Tan, A.L.Y.; Forbes, J.M.; Cooper, M.E. AGE, RAGE, and ROS in diabetic nephropathy. Semin. Nephrol., 2007, 27(2), 130-143.
[http://dx.doi.org/10.1016/j.semnephrol.2007.01.006] [PMID: 17418682]
[66]
Volpe, C.M.O.; Villar-Delfino, P.H.; Dos Anjos, P.M.F.; Nogueira-Machado, J.A. Cellular death, reactive oxygen species (ROS) and diabetic complications. Cell Death Dis., 2018, 9(2), 119.
[http://dx.doi.org/10.1038/s41419-017-0135-z] [PMID: 29371661]
[67]
Chang, T.; Wu, L. Methylglyoxal, oxidative stress, and hypertension. Can. J. Physiol. Pharmacol., 2006, 84(12), 1229-1238.
[http://dx.doi.org/10.1139/y06-077] [PMID: 17487230]
[68]
Zephy, D.; Ahmad, J. Type 2 diabetes mellitus: Role of melatonin and oxidative stress. Diabetes Metab. Syndr., 2015, 9(2), 127-131.
[http://dx.doi.org/10.1016/j.dsx.2014.09.018] [PMID: 25450812]
[69]
Yan, L-J. Pathogenesis of chronic hyperglycemia: from reductive stress to oxidative stress. J. Diabetes Res., 2014, 2014137919
[http://dx.doi.org/10.1155/2014/137919] [PMID: 25019091]
[70]
Zhao, W.; Devamanoharan, P.S.; Varma, S.D. Fructose induced deactivation of antioxidant enzymes: preventive effect of pyruvate. Free Radic. Res., 2000, 33(1), 23-30.
[http://dx.doi.org/10.1080/10715760000300581] [PMID: 10826918]
[71]
Hartl, F.U.; Martin, J. Molecular chaperones in cellular protein folding. Curr. Opin. Struct. Biol., 1995, 5(1), 92-102.
[http://dx.doi.org/10.1016/0959-440X(95)80014-R] [PMID: 7773752]
[72]
Beissinger, M.; Buchner, J. How chaperones fold proteins. Biol. Chem., 1998, 379(3), 245-259.
[PMID: 9563819]
[73]
Lackie, R.E.; Maciejewski, A.; Ostapchenko, V.G.; Marques-Lopes, J.; Choy, W-Y.; Duennwald, M.L.; Prado, V.F.; Prado, M.A.M. The Hsp70/Hsp90 chaperone machinery in neurodegenerative diseases. Front. Neurosci., 2017, 11, 254.
[http://dx.doi.org/10.3389/fnins.2017.00254] [PMID: 28559789]
[74]
Stroylova, Y.Y.; Kiselev, G.G.; Schmalhausen, E.V.; Muronetz, V.I. Prions and chaperones: friends or foes? Biochemistry (Mosc.), 2014, 79(8), 761-775.
[http://dx.doi.org/10.1134/S0006297914080045] [PMID: 25365486]
[75]
Polyakova, O.V.; Roitel, O.; Asryants, R.A.; Poliakov, A.A.; Branlant, G.; Muronetz, V.I. Misfolded forms of glyceraldehyde-3-phosphate dehydrogenase interact with GroEL and inhibit chaperonin-assisted folding of the wild-type enzyme. Protein Sci., 2005, 14(4), 921-928.
[http://dx.doi.org/10.1110/ps.041211205] [PMID: 15741339]
[76]
Naletova, I.N.; Muronetz, V.I.; Schmalhausen, E.V. Unfolded, oxidized, and thermoinactivated forms of glyceraldehyde-3-phosphate dehydrogenase interact with the chaperonin GroEL in different ways. Biochim. Biophys. Acta, 2006, 1764(4), 831-838.
[http://dx.doi.org/10.1016/j.bbapap.2006.02.002] [PMID: 16551514]
[77]
Kiselev, G.G.; Naletova, I.N.; Sheval, E.V.; Stroylova, Y.Y.; Schmalhausen, E.V.; Haertlé, T.; Muronetz, V.I. Chaperonins induce an amyloid-like transformation of ovine prion protein: the fundamental difference in action between eukaryotic TRiC and bacterial GroEL. Biochim. Biophys. Acta, 2011, 1814(12), 1730-1738.
[http://dx.doi.org/10.1016/j.bbapap.2011.08.006] [PMID: 21856455]
[78]
Itakura, M.; Nakajima, H.; Kubo, T.; Semi, Y.; Kume, S.; Higashida, S.; Kaneshige, A.; Kuwamura, M.; Harada, N.; Kita, A.; Azuma, Y.T.; Yamaji, R.; Inui, T.; Takeuchi, T. Glyceraldehyde-3-phosphate dehydrogenase aggregates accelerate amyloid-β amyloidogenesis in Alzheimer disease. J. Biol. Chem., 2015, 290(43), 26072-26087.
[http://dx.doi.org/10.1074/jbc.M115.669291] [PMID: 26359500]
[79]
Cumming, R.C.; Schubert, D. Amyloid-beta induces disulfide bonding and aggregation of GAPDH in Alzheimer’s disease. FASEB J., 2005, 19(14), 2060-2062.
[http://dx.doi.org/10.1096/fj.05-4195fje] [PMID: 16186172]
[80]
Shalova, I.N.; Cechalova, K.; Rehakova, Z.; Dimitrova, P.; Ognibene, E.; Caprioli, A.; Schmalhausen, E.V.; Muronetz, V.I.; Saso, L. Decrease of dehydrogenase activity of cerebral glyceraldehyde-3-phosphate dehydrogenase in different animal models of Alzheimer’s disease. Biochim. Biophys. Acta, 2007, 1770(5), 826-832.
[http://dx.doi.org/10.1016/j.bbagen.2007.01.014] [PMID: 17324518]
[81]
Tatton, N.A. Increased caspase 3 and Bax immunoreactivity accompany nuclear GAPDH translocation and neuronal apoptosis in Parkinson’s disease. Exp. Neurol., 2000, 166(1), 29-43.
[http://dx.doi.org/10.1006/exnr.2000.7489] [PMID: 11031081]
[82]
Tsuchiya, K.; Tajima, H.; Kuwae, T.; Takeshima, T.; Nakano, T.; Tanaka, M.; Sunaga, K.; Fukuhara, Y.; Nakashima, K.; Ohama, E.; Mochizuki, H.; Mizuno, Y.; Katsube, N.; Ishitani, R. Pro-apoptotic protein glyceraldehyde-3-phosphate dehydrogenase promotes the formation of Lewy body-like inclusions. Eur. J. Neurosci., 2005, 21(2), 317-326.
[http://dx.doi.org/10.1111/j.1460-9568.2005.03870.x] [PMID: 15673432]
[83]
Lazarev, V.F.; Benken, K.A.; Semenyuk, P.I.; Sarantseva, S.V.; Bolshakova, O.I.; Mikhaylova, E.R.; Muronetz, V.I.; Guzhova, I.V.; Margulis, B.A. GAPDH binders as potential drugs for the therapy of polyglutamine diseases: design of a new screening assay. FEBS Lett., 2015, 589(5), 581-587.
[http://dx.doi.org/10.1016/j.febslet.2015.01.018] [PMID: 25625921]
[84]
Butterfield, D.A.; Hardas, S.S.; Lange, M.L.B. Oxidatively modified glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and Alzheimer’s disease: many pathways to neurodegeneration. J. Alzheimers Dis., 2010, 20(2), 369-393.
[http://dx.doi.org/10.3233/JAD-2010-1375] [PMID: 20164570]
[85]
Gómez, A.; Ferrer, I. Increased oxidation of certain glycolysis and energy metabolism enzymes in the frontal cortex in Lewy body diseases. J. Neurosci. Res., 2009, 87(4), 1002-1013.
[http://dx.doi.org/10.1002/jnr.21904] [PMID: 18855937]
[86]
Savreux-Lenglet, G.; Depauw, S.; David-Cordonnier, M.H. Protein recognition in drug-induced DNA alkylation: when the moonlight protein GAPDH meets S23906-1/DNA minor groove adducts. Int. J. Mol. Sci., 2015, 16(11), 26555-26581.
[http://dx.doi.org/10.3390/ijms161125971] [PMID: 26556350]
[87]
White, M.R.; Garcin, E.D. The sweet side of RNA regulation: glyceraldehyde-3-phosphate dehydrogenase as a noncanonical RNA-binding protein. Wiley Interdiscip. Rev. RNA, 2016, 7(1), 53-70.
[http://dx.doi.org/10.1002/wrna.1315] [PMID: 26564736]
[88]
Ronai, Z. Glycolytic enzymes as DNA binding proteins. Int. J. Biochem., 1993, 25(7), 1073-1076.
[http://dx.doi.org/10.1016/0020-711X(93)90123-V] [PMID: 8365548]
[89]
Nagy, E.; Henics, T.; Eckert, M.; Miseta, A.; Lightowlers, R.N.; Kellermayer, M. Identification of the NAD(+)-binding fold of glyceraldehyde-3-phosphate dehydrogenase as a novel RNA-binding domain. Biochem. Biophys. Res. Commun., 2000, 275(2), 253-260.
[http://dx.doi.org/10.1006/bbrc.2000.3246] [PMID: 10964654]
[90]
Ryazanov, A.G. Glyceraldehyde-3-phosphate dehydrogenase is one of the three major RNA-binding proteins of rabbit reticulocytes. FEBS Lett., 1985, 192(1), 131-134.
[http://dx.doi.org/10.1016/0014-5793(85)80058-2] [PMID: 2414129]
[91]
Ryazanov, A.G.; Ashmarina, L.I.; Muronetz, V.I. Association of glyceraldehyde-3-phosphate dehydrogenase with mono- and polyribosomes of rabbit reticulocytes. Eur. J. Biochem., 1988, 171(1-2), 301-305.
[http://dx.doi.org/10.1111/j.1432-1033.1988.tb13790.x] [PMID: 3276518]
[92]
Arutyunova, E.I.; Danshina, P.V.; Domnina, L.V.; Pleten, A.P.; Muronetz, V.I. Oxidation of glyceraldehyde-3-phosphate dehydrogenase enhances its binding to nucleic acids. Biochem. Biophys. Res. Commun., 2003, 307(3), 547-552.
[http://dx.doi.org/10.1016/S0006-291X(03)01222-1] [PMID: 12893257]
[93]
Sunaga, K.; Takahashi, H.; Chuang, D.M.; Ishitani, R. Glyceraldehyde-3-phosphate dehydrogenase is over-expressed during apoptotic death of neuronal cultures and is recognized by a monoclonal antibody against amyloid plaques from Alzheimer’s brain. Neurosci. Lett., 1995, 200(2), 133-136.
[http://dx.doi.org/10.1016/0304-3940(95)12098-O] [PMID: 8614562]
[94]
Sirover, M.A. Role of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in normal cell function and in cell pathology. J. Cell. Biochem., 1997, 66(2), 133-140.
[http://dx.doi.org/10.1002/(SICI)1097-4644(19970801)66:2<133:AID-JCB1>3.0.CO;2-R] [PMID: 9213215]
[95]
Tatton, W.G.; Chalmers-Redman, R.M.; Elstner, M.; Leesch, W.; Jagodzinski, F.B.; Stupak, D.P.; Sugrue, M.M.; Tatton, N.A. Glyceraldehyde-3-phosphate dehydrogenase in neurodegeneration and apoptosis signaling. J. Neural Transm. Suppl., 2000, (60), 77-100.
[http://dx.doi.org/10.1007/978-3-7091-6301-6_5] [PMID: 11205159]
[96]
Brown, G.C. Nitric oxide and neuronal death. Nitric Oxide, 2010, 23(3), 153-165.
[http://dx.doi.org/10.1016/j.niox.2010.06.001] [PMID: 20547235]
[97]
Bryksin, A.V.; Laktionov, P.P. Role of glyceraldehyde-3-phosphate dehydrogenase in vesicular transport from golgi apparatus to endoplasmic reticulum. Biochemistry (Mosc.), 2008, 73(6), 619-625.
[http://dx.doi.org/10.1134/S0006297908060011] [PMID: 18620527]
[98]
Sen, N.; Hara, M.R.; Kornberg, M.D.; Cascio, M.B.; Bae, B-I.; Shahani, N.; Thomas, B.; Dawson, T.M.; Dawson, V.L.; Snyder, S.H.; Sawa, A. Nitric oxide-induced nuclear GAPDH activates p300/CBP and mediates apoptosis. Nat. Cell Biol., 2008, 10(7), 866-873.
[http://dx.doi.org/10.1038/ncb1747] [PMID: 18552833]
[99]
Tristan, C.; Shahani, N.; Sedlak, T.W.; Sawa, A. The diverse functions of GAPDH: views from different subcellular compartments. Cell. Signal., 2011, 23(2), 317-323.
[http://dx.doi.org/10.1016/j.cellsig.2010.08.003] [PMID: 20727968]
[100]
Tristan, C.A.; Ramos, A.; Shahani, N.; Emiliani, F.E.; Nakajima, H.; Noeh, C.C.; Kato, Y.; Takeuchi, T.; Noguchi, T.; Kadowaki, H.; Sedlak, T.W.; Ishizuka, K.; Ichijo, H.; Sawa, A. Role of apoptosis signal-regulating kinase 1 (ASK1) as an activator of the GAPDH-Siah1 stress-signaling cascade. J. Biol. Chem., 2015, 290(1), 56-64.
[http://dx.doi.org/10.1074/jbc.M114.596205] [PMID: 25391652]
[101]
Sevostyanova, I.A.; Kulikova, K.V.; Kuravsky, M.L.; Schmalhausen, E.V.; Muronetz, V.I. Sperm-specific glyceraldehyde-3-phosphate dehydrogenase is expressed in melanoma cells. Biochem. Biophys. Res. Commun., 2012, 427(3), 649-653.
[http://dx.doi.org/10.1016/j.bbrc.2012.09.115] [PMID: 23026046]
[102]
Miki, K.; Qu, W.; Goulding, E.H.; Willis, W.D.; Bunch, D.O.; Strader, L.F.; Perreault, S.D.; Eddy, E.M.; O’Brien, D.A. Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc. Natl. Acad. Sci. USA, 2004, 101(47), 16501-16506.
[http://dx.doi.org/10.1073/pnas.0407708101] [PMID: 15546993]
[103]
Muronetz, V.I.; Kuravsky, M.L.; Barinova, K.V.; Schmalhausen, E.V. Sperm-specific glyceraldehyde-3-phosphate dehydrogenase - an evolutionary acquisition of mammals. Biochemistry (Mosc.), 2015, 80(13), 1672-1689.
[http://dx.doi.org/10.1134/S0006297915130040] [PMID: 26878573]
[104]
Kuravsky, M.L.; Aleshin, V.V.; Frishman, D.; Muronetz, V.I. Testis-specific glyceraldehyde-3-phosphate dehydrogenase: origin and evolution. BMC Evol. Biol., 2011, 11, 160.
[http://dx.doi.org/10.1186/1471-2148-11-160] [PMID: 21663662]
[105]
Elkina, Y.L.; Kuravsky, M.L.; El’darov, M.A.; Stogov, S.V.; Muronetz, V.I.; Schmalhausen, E.V. Recombinant human sperm-specific glyceraldehyde-3-phosphate dehydrogenase: structural basis for enhanced stability. Biochim. Biophys. Acta, 2010, 1804(12), 2207-2212.
[http://dx.doi.org/10.1016/j.bbapap.2010.09.002] [PMID: 20833277]
[106]
Kuravsky, M.; Barinova, K.; Marakhovskaya, A.; Eldarov, M.; Semenyuk, P.; Muronetz, V.; Schmalhausen, E. Sperm-specific glyceraldehyde-3-phosphate dehydrogenase is stabilized by additional proline residues and an interdomain salt bridge. Biochim. Biophys. Acta, 2014, 1844(10), 1820-1826.
[http://dx.doi.org/10.1016/j.bbapap.2014.07.018] [PMID: 25091199]
[107]
Kuravsky, M.L.; Barinova, K.V.; Asryants, R.A.; Schmalhausen, E.V.; Muronetz, V.I. Structural basis for the NAD binding cooperativity and catalytic characteristics of sperm-specific glyceraldehyde-3-phosphate dehydrogenase. Biochimie, 2015, 115, 28-34.
[http://dx.doi.org/10.1016/j.biochi.2015.04.016] [PMID: 25936797]
[108]
Shchutskaya, Y.Y.; Elkina, Y.L.; Kuravsky, M.L.; Bragina, E.E.; Schmalhausen, E.V. Investigation of glyceraldehyde-3-phosphate dehydrogenase from human sperms. Biochemistry (Mosc.), 2008, 73(2), 185-191.
[http://dx.doi.org/10.1134/S0006297908020107] [PMID: 18298375]
[109]
Elkina, Y.L.; Atroshchenko, M.M.; Bragina, E.E.; Muronetz, V.I.; Schmalhausen, E.V. Oxidation of glyceraldehyde-3-phosphate dehydrogenase decreases sperm motility. Biochemistry (Mosc.), 2011, 76(2), 268-272.
[http://dx.doi.org/10.1134/S0006297911020143] [PMID: 21568861]
[110]
Evdokimov, V.V.; Barinova, K.V.; Turovetskii, V.B.; Muronetz, V.I.; Schmalhausen, E.V. Low concentrations of hydrogen peroxide activate the antioxidant defense system in human sperm cells. Biochemistry (Mosc.), 2015, 80(9), 1178-1185.
[http://dx.doi.org/10.1134/S0006297915090084] [PMID: 26555470]
[111]
Kouwen, T.R.H.M.; Andréll, J.; Schrijver, R.; Dubois, J-Y.F.; Maher, M.J.; Iwata, S.; Carpenter, E.P.; van Dijl, J.M. Thioredoxin A active-site mutants form mixed disulfide dimers that resemble enzyme-substrate reaction intermediates. J. Mol. Biol., 2008, 379(3), 520-534.
[http://dx.doi.org/10.1016/j.jmb.2008.03.077] [PMID: 18455736]
[112]
Sirover, M.A. Minireview. Emerging new functions of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in mammalian cells. Life Sci., 1996, 58(25), 2271-2277.
[http://dx.doi.org/10.1016/0024-3205(96)00123-3] [PMID: 8649216]
[113]
Mazzola, J.L.; Sirover, M.A. Alteration of intracellular structure and function of glyceraldehyde-3-phosphate dehydrogenase: a common phenotype of neurodegenerative disorders? Neurotoxicology, 2002, 23(4-5), 603-609.
[http://dx.doi.org/10.1016/S0161-813X(02)00062-1] [PMID: 12428732]
[114]
Berry, M.D. Glyceraldehyde-3-phosphate dehydrogenase as a target for small-molecule disease-modifying therapies in human neurodegenerative disorders. J. Psychiatry Neurosci., 2004, 29(5), 337-345.
[PMID: 15486605]
[115]
Muronetz, V.I.; Barinova, K.V.; Stroylova, Y.Y.; Semenyuk, P.I.; Schmalhausen, E.V. Glyceraldehyde-3-phosphate dehydrogenase: Aggregation mechanisms and impact on amyloid neurodegenerative diseases. Int. J. Biol. Macromol., 2017, 100, 55-66.
[http://dx.doi.org/10.1016/j.ijbiomac.2016.05.066] [PMID: 27215901]
[116]
Muronetz, V.I.; Melnikova, A.K.; Seferbekova, Z.N.; Barinova, K.V.; Schmalhausen, E.V. Glycation, glycolysis, and neurodegenerative diseases: is there any connection? Biochemistry (Mosc.), 2017, 82(8), 874-886.
[http://dx.doi.org/10.1134/S0006297917080028] [PMID: 28941455]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy