Login Register Cart 0
Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Heat-Shock Triggers Inverted Induction of Hypo-S-Nitrosylation and Hyper-O-GlcNAcylation

Author(s): Min-Jae Kim, In-Hyun Ryu and Su-Il Do*

Volume 29, Issue 9, 2022

Published on: 05 September, 2022

Page: [769 - 774] Pages: 6

DOI: 10.2174/0929866529666220805151725

Price: $65

Abstract

Introduction: Protein S-nitrosylation (SNO) and O-GlcNAcylation are important posttranslational modifications. The biological connection between SNO and O-GlcNAcylation is not clear.

Objective: We aim to identify the crosstalk between SNO and O-GlcNAcylation during heat-shock.

Methods: Ex vivo heat-shock on mouse tissues together with in vitro heat-shock on culture cells was performed and global levels of SNO and O-GlcNAcylation were analyzed with Biotin-switch assay (BSA) and RL2 immunoblots.

Results: Heat-shock induces hypo-SNO in parallel with hyper-O-GlcNAcylation. Inverted induction of hypo-SNO and hyper-O-GlcNAcylation is globally progressed in a time-dependent manner.

Discussion: Moreover, heat-shock ubiquitously facilitates S-denitrosylation (SdeNO) of endogenous SNO-proteins including SNO-OGT, SNO-Hsp70, SNO-Hsp90, SNO-Akt, and SNOactin. Particularly, SdeNO of SNO-OGT leads to enhanced OGT activity.

Conclusion: These findings provide mechanistic evidence that heat-shock triggers SdeNO of SNOOGT by which OGT activity is up-regulated, resulting in hyper-O-GlcNAcylation.

Keywords: S-nitrosylation, O-GlcNAcylation, N-acetylglucosaminyltransferase, S-denitrosylation, ex vivo heat-shock, in vitro heat-shock.

« Previous Next »
Graphical Abstract

[1]
Stomberski, C.T.; Hess, D.T.; Stamler, J.S. Protein S-nitrosylation: Determinants of specificity and enzymatic regulation of S-nitrosothiol-based signaling. Antioxid. Redox Signal., 2019, 30(10), 1331-1351.
[http://dx.doi.org/10.1089/ars.2017.7403] [PMID: 29130312]
[2]
Hess, D.T.; Matsumoto, A.; Kim, S-O.; Marshall, H.E.; Stamler, J.S. Protein S-nitrosylation: Purview and parameters. Nat. Rev. Mol. Cell Biol., 2005, 6(2), 150-166.
[http://dx.doi.org/10.1038/nrm1569] [PMID: 15688001]
[3]
Alderton, W.K.; Cooper, C.E.; Knowles, R.G. Nitric oxide synthases: Structure, function and inhibition. Biochem. J., 2001, 357(Pt 3), 593-615.
[http://dx.doi.org/10.1042/bj3570593] [PMID: 11463332]
[4]
Nakamura, T.; Lipton, S.A. Emerging role of protein-protein transnitrosylation in cell signaling pathways. Antioxid. Redox Signal., 2013, 18(3), 239-249.
[http://dx.doi.org/10.1089/ars.2012.4703] [PMID: 22657837]
[5]
Jia, J.; Arif, A.; Terenzi, F.; Willard, B.; Plow, E.F.; Hazen, S.L.; Fox, P.L. Target-selective protein S-nitrosylation by sequence motif recognition. Cell, 2014, 159(3), 623-634.
[http://dx.doi.org/10.1016/j.cell.2014.09.032] [PMID: 25417112]
[6]
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]
[7]
Jia, L.; Bonaventura, C.; Bonaventura, J.; Stamler, J.S. S-nitrosohaemoglobin: A dynamic activity of blood involved in vascular control. Nature, 1996, 380(6571), 221-226.
[http://dx.doi.org/10.1038/380221a0] [PMID: 8637569]
[8]
Stamler, J.S.; Toone, E.J.; Lipton, S.A.; Sucher, N.J. (S)NO signals: Translocation, regulation, and a consensus motif. Neuron, 1997, 18(5), 691-696.
[http://dx.doi.org/10.1016/S0896-6273(00)80310-4] [PMID: 9182795]
[9]
Furuta, S. Basal S-nitrosylation is the guardian of tissue homeostasis. Trends Cancer, 2017, 3(11), 744-748.
[http://dx.doi.org/10.1016/j.trecan.2017.09.003] [PMID: 29120749]
[10]
Marino, S.M.; Gladyshev, V.N. Structural analysis of cysteine S-nitrosylation: A modified acid-based motif and the emerging role of trans-nitrosylation. J. Mol. Biol., 2010, 395(4), 844-859.
[http://dx.doi.org/10.1016/j.jmb.2009.10.042] [PMID: 19854201]
[11]
Doulias, P-T.; Greene, J.L.; Greco, T.M.; Tenopoulou, M.; Seeholzer, S.H.; Dunbrack, R.L.; Ischiropoulos, H. Structural profiling of endogenous S-nitrosocysteine residues reveals unique features that accommodate diverse mechanisms for protein S-nitrosylation. Proc. Natl. Acad. Sci. USA, 2010, 107(39), 16958-16963.
[http://dx.doi.org/10.1073/pnas.1008036107] [PMID: 20837516]
[12]
Benhar, M.; Forrester, M.T.; Stamler, J.S. Protein denitrosylation: Enzymatic mechanisms and cellular functions. Nat. Rev. Mol. Cell Biol., 2009, 10(10), 721-732.
[http://dx.doi.org/10.1038/nrm2764] [PMID: 19738628]
[13]
Choudhari, S.K.; Chaudhary, M.; Bagde, S.; Gadbail, A.R.; Joshi, V. Nitric oxide and cancer: A review. World J. Surg. Oncol., 2013, 11(1), 118.
[http://dx.doi.org/10.1186/1477-7819-11-118] [PMID: 23718886]
[14]
Rizza, S.; Filomeni, G. Exploiting S-nitrosylation for cancer therapy: Facts and perspectives. Biochem. J., 2020, 477(19), 3649-3672.
[http://dx.doi.org/10.1042/BCJ20200064] [PMID: 33017470]
[15]
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]
[16]
Picón-Pagès, P.; Garcia-Buendia, J.; Muñoz, F.J. Functions and dysfunctions of nitric oxide in brain. Biochim. Biophys. Acta Mol. Basis Dis., 2019, 1865(8), 1949-1967.
[http://dx.doi.org/10.1016/j.bbadis.2018.11.007] [PMID: 30500433]
[17]
Akan, I.; Olivier-Van Stichelen, S.; Bond, M.R.; Hanover, J.A. Nutrient-driven O-GlcNAc in proteostasis and neurodegeneration. J. Neurochem., 2018, 144(1), 7-34.
[http://dx.doi.org/10.1111/jnc.14242] [PMID: 29049853]
[18]
Ma, J.; Wu, C.; Hart, G.W. Analytical and biochemical perspectives of protein O-GlcNAcylation. Chem. Rev., 2021, 121(3), 1513-1581.
[http://dx.doi.org/10.1021/acs.chemrev.0c00884] [PMID: 33416322]
[19]
Shafi, R.; Iyer, S.P.; Ellies, L.G.; O’Donnell, N.; Marek, K.W.; Chui, D.; Hart, G.W.; Marth, J.D. The O-GlcNAc transferase gene resides on the X chromosome and is essential for embryonic stem cell viability and mouse ontogeny. Proc. Natl. Acad. Sci. USA, 2000, 97(11), 5735-5739.
[http://dx.doi.org/10.1073/pnas.100471497] [PMID: 10801981]
[20]
Sohn, K-C.; Lee, K-Y.; Park, J-E.; Do, S-I. OGT functions as a catalytic chaperone under heat stress response: A unique defense role of OGT in hyperthermia. Biochem. Biophys. Res. Commun., 2004, 322(3), 1045-1051.
[http://dx.doi.org/10.1016/j.bbrc.2004.08.023] [PMID: 15336570]
[21]
Ruan, H-B.; Ma, Y.; Torres, S.; Zhang, B.; Feriod, C.; Heck, R.M.; Qian, K.; Fu, M.; Li, X.; Nathanson, M.H.; Bennett, A.M.; Nie, Y.; Ehrlich, B.E.; Yang, X. Calcium-dependent O-GlcNAc signaling drives liver autophagy in adaptation to starvation. Genes Dev., 2017, 31(16), 1655-1665.
[http://dx.doi.org/10.1101/gad.305441.117] [PMID: 28903979]
[22]
Shi, J.; Gu, J.; Dai, C.; Gu, J.; Jin, J.; Sun, X.; Iqbal, J.; Liu, K.; Gong, F. O-GlcNAcylation regulates ischemia-induced neuronal apoptosis through AKT signaling. Sci. Rep., 2015, 5, 1-14.
[23]
Chou, T-Y.; Hart, G.W.; Dang, C.V. C-Myc is glycosylated at threonine 58, a known phosphorylation site and a mutational hot spot in lymphomas. J. Biol. Chem., 1995, 270(32), 18961-18965.
[http://dx.doi.org/10.1074/jbc.270.32.18961] [PMID: 7642555]
[24]
Marshall, S.; Nadeau, O.; Yamasaki, K. Dynamic actions of glucose and glucosamine on hexosamine biosynthesis in isolated adipocytes: Differential effects on glucosamine 6-phosphate, UDP-N-acetylglucosamine, and ATP levels. J. Biol. Chem., 2004, 279(34), 35313-35319.
[http://dx.doi.org/10.1074/jbc.M404133200] [PMID: 15199059]
[25]
Joiner, C.M.; Li, H.; Jiang, J.; Walker, S. Structural characterization of the O-GlcNAc cycling enzymes: Insights into substrate recognition and catalytic mechanisms. Curr. Opin. Struct. Biol., 2019, 56, 97-106.
[http://dx.doi.org/10.1016/j.sbi.2018.12.003] [PMID: 30708324]
[26]
Wani, W.Y.; Chatham, J.C.; Darley-Usmar, V.; McMahon, L.L.; Zhang, J. O-GlcNAcylation and neurodegeneration. Brain Res. Bull., 2017, 133, 80-87.
[http://dx.doi.org/10.1016/j.brainresbull.2016.08.002] [PMID: 27497832]
[27]
Ferrer, C.M.; Sodi, V.L.; Reginato, M.J. O-GlcNAcylation in cancer biology: Linking metabolism and signaling. J. Mol. Biol., 2016, 428(16), 3282-3294.
[http://dx.doi.org/10.1016/j.jmb.2016.05.028] [PMID: 27343361]
[28]
Erickson, J.R.; Pereira, L.; Wang, L.; Han, G.; Ferguson, A.; Dao, K.; Copeland, R.J.; Despa, F.; Hart, G.W.; Ripplinger, C.M.; Bers, D.M. Diabetic hyperglycaemia activates CaMKII and arrhythmias by O-linked glycosylation. Nature, 2013, 502(7471), 372-376.
[http://dx.doi.org/10.1038/nature12537] [PMID: 24077098]
[29]
Ryu, I-H.; Do, S-I. Denitrosylation of S-nitrosylated OGT is triggered in LPS-stimulated innate immune response. Biochem. Biophys. Res. Commun., 2011, 408(1), 52-57.
[http://dx.doi.org/10.1016/j.bbrc.2011.03.115] [PMID: 21453677]
[30]
Ryu, I-H. Lee, K-Y.; Do, S-I. Aβ-affected pathogenic induction of S-nitrosylation of OGT and identification of Cys-NO linkage triplet. Biochim. Biophys. Acta, 2016, 1864(5), 609-621.
[http://dx.doi.org/10.1016/j.bbapap.2016.02.003] [PMID: 26854602]
[31]
Jaffrey, S.R.; Snyder, S.H. The biotin switch method for the detection of S-nitrosylated proteins. Sci. STKE, 2001, 2001(86), pl1.
[http://dx.doi.org/10.1126/stke.2001.86.pl1] [PMID: 11752655]
[32]
Huang, B.; Chen, S.C.; Wang, D.L. Shear flow increases S-nitrosylation of proteins in endothelial cells. Cardiovasc. Res., 2009, 83(3), 536-546.
[http://dx.doi.org/10.1093/cvr/cvp154] [PMID: 19447776]
[33]
Martínez-Ruiz, A.; Villanueva, L.; González de Orduña, C.; López-Ferrer, D.; Higueras, M.A.; Tarín, C.; Rodríguez-Crespo, I.; Vázquez, J.; Lamas, S. S-nitrosylation of Hsp90 promotes the inhibition of its ATPase and endothelial nitric oxide synthase regulatory activities. Proc. Natl. Acad. Sci. USA, 2005, 102(24), 8525-8530.
[http://dx.doi.org/10.1073/pnas.0407294102] [PMID: 15937123]
[34]
Yasukawa, T.; Tokunaga, E.; Ota, H.; Sugita, H.; Martyn, J.A.J.; Kaneki, M. S-nitrosylation-dependent inactivation of Akt/protein kinase B in insulin resistance. J. Biol. Chem., 2005, 280(9), 7511-7518.
[http://dx.doi.org/10.1074/jbc.M411871200] [PMID: 15632167]
[35]
Dalle-Donne, I.; Milzani, A.; Giustarini, D.; Di Simplicio, P.; Colombo, R.; Rossi, R. S-NO-actin: S-nitrosylation kinetics and the effect on isolated vascular smooth muscle. J. Muscle Res. Cell Motil., 2000, 21(2), 171-181.
[http://dx.doi.org/10.1023/A:1005671319604] [PMID: 10961840]
[36]
Freeman, B.C.; Morimoto, R.I. The human cytosolic molecular chaperones hsp90, hsp70 (hsc70) and hdj-1 have distinct roles in recognition of a non-native protein and protein refolding. EMBO J., 1996, 15(12), 2969-2979.
[http://dx.doi.org/10.1002/j.1460-2075.1996.tb00660.x] [PMID: 8670798]
[37]
Manning, B.D.; Cantley, L.C. AKT/PKB signaling: Navigating downstream. Cell, 2007, 129(7), 1261-1274.
[http://dx.doi.org/10.1016/j.cell.2007.06.009] [PMID: 17604717]

Rights & Permissions Print Cite
Article Metrics
12
© 2024 Bentham Science Publishers | Privacy Policy