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A dimer interface mutation in glyceraldehyde-3-phosphate dehydrogenase regulates its binding to AU-rich RNA.

White MR, Khan MM, Deredge D, Ross CR, Quintyn R, Zucconi BE, Wysocki VH, Wintrode PL, Wilson GM, Garcin ED
J Biol Chem 290 1770-85 (2015)
Cited: 33 times
EuropePMC logo PMID: 25451934

Abstract

Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) is an enzyme best known for its role in glycolysis. However, extra-glycolytic functions of GAPDH have been described, including regulation of protein expression via RNA binding. GAPDH binds to numerous adenine-uridine rich elements (AREs) from various mRNA 3'-untranslated regions in vitro and in vivo despite its lack of a canonical RNA binding motif. How GAPDH binds to these AREs is still unknown. Here we discovered that GAPDH binds with high affinity to the core ARE from tumor necrosis factor-α mRNA via a two-step binding mechanism. We demonstrate that a mutation at the GAPDH dimer interface impairs formation of the second RNA-GAPDH complex and leads to changes in the RNA structure. We investigated the effect of this interfacial mutation on GAPDH oligomerization by crystallography, small-angle x-ray scattering, nano-electrospray ionization native mass spectrometry, and hydrogen-deuterium exchange mass spectrometry. We show that the mutation does not significantly affect GAPDH tetramerization as previously proposed. Instead, the mutation promotes short-range and long-range dynamic changes in regions located at the dimer and tetramer interface and in the NAD(+) binding site. These dynamic changes are localized along the P axis of the GAPDH tetramer, suggesting that this region is important for RNA binding. Based on our results, we propose a model for sequential GAPDH binding to RNA via residues located at the dimer and tetramer interfaces.

Reviews - 4wnc mentioned but not cited (3)

  1. The Writers, Readers, and Erasers in Redox Regulation of GAPDH. Tossounian MA, Zhang B, Gout I. Antioxidants (Basel) 9 E1288 (2020)
  2. The sweet side of RNA regulation: glyceraldehyde-3-phosphate dehydrogenase as a noncanonical RNA-binding protein. White MR, Garcin ED. Wiley Interdiscip Rev RNA 7 53-70 (2016)
  3. The more the merrier: how homo-oligomerization alters the interactome and function of ribonucleotide reductase. Long MJC, Van Hall-Beauvais A, Aye Y. Curr Opin Chem Biol 54 10-18 (2020)

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  2. Diverse Redoxome Reactivity Profiles of Carbon Nucleophiles. Gupta V, Yang J, Liebler DC, Carroll KS. J Am Chem Soc 139 5588-5595 (2017)
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  4. A dimer interface mutation in glyceraldehyde-3-phosphate dehydrogenase regulates its binding to AU-rich RNA. White MR, Khan MM, Deredge D, Ross CR, Quintyn R, Zucconi BE, Wysocki VH, Wintrode PL, Wilson GM, Garcin ED. J Biol Chem 290 1770-1785 (2015)
  5. Protein Footprinting via Covalent Protein Painting Reveals Structural Changes of the Proteome in Alzheimer's Disease. Bamberger C, Pankow S, Martínez-Bartolomé S, Ma M, Diedrich J, Rissman RA, Yates JR. J Proteome Res 20 2762-2771 (2021)
  6. Glyceraldehyde-3-Phosphate Dehydrogenase (GAPDH) Protein-Protein Interaction Inhibitor Reveals a Non-catalytic Role for GAPDH Oligomerization in Cell Death. Qvit N, Joshi AU, Cunningham AD, Ferreira JC, Mochly-Rosen D. J Biol Chem 291 13608-13621 (2016)
  7. Deciphering Key Residues Involved in the Virulence-promoting Interactions between Streptococcus pneumoniae and Human Plasminogen. Moreau C, Terrasse R, Thielens NM, Vernet T, Gaboriaud C, Di Guilmi AM. J Biol Chem 292 2217-2225 (2017)
  8. REST Protects Dopaminergic Neurons from Mitochondrial and α-Synuclein Oligomer Pathology in an Alpha Synuclein Overexpressing BAC-Transgenic Mouse Model. Ryan BJ, Bengoa-Vergniory N, Williamson M, Kirkiz E, Roberts R, Corda G, Sloan M, Saqlain S, Cherubini M, Poppinga J, Bogtofte H, Cioroch M, Hester S, Wade-Martins R. J Neurosci 41 3731-3746 (2021)
  9. Structures of glyceraldehyde 3-phosphate dehydrogenase in Neisseria gonorrhoeae and Chlamydia trachomatis. Barrett KF, Dranow DM, Phan IQ, Michaels SA, Shaheen S, Navaluna ED, Craig JK, Tillery LM, Choi R, Edwards TE, Conrady DG, Abendroth J, Horanyi PS, Lorimer DD, Van Voorhis WC, Zhang Z, Barrett LK, Subramanian S, Staker B, Fan E, Myler PJ, Soge OO, Hybiske K, Ojo KK. Protein Sci 29 768-778 (2020)
  10. Structural Study of Monomethyl Fumarate-Bound Human GAPDH. Park JB, Park H, Son J, Ha SJ, Cho HS. Mol Cells 42 597-603 (2019)
  11. Partial catalytic Cys oxidation of human GAPDH to Cys-sulfonic acid. Lia A, Dowle A, Taylor C, Santino A, Roversi P. Wellcome Open Res 5 114 (2020)
  12. Plausible computational insights and new atomic-level perspective of epicathechin gallate from Crataegus oxycantha extract in preventing caspase 3 activation in conditions like post-myocardial infarction. Ravindran ASK, Venkatabalasubramanian S, Manickam R, Anusuyadevi M, K Swaminathan J. J Biomol Struct Dyn 40 3400-3415 (2022)
  13. Efficient tagging of endogenous proteins in human cell lines for structural studies by single-particle cryo-EM. Choi W, Wu H, Yserentant K, Huang B, Cheng Y. Proc Natl Acad Sci U S A 120 e2302471120 (2023)
  14. Monitoring GAPDH activity and inhibition with cysteine-reactive chemical probes. Canarelli SE, Swalm BM, Larson ET, Morrison MJ, Weerapana E. RSC Chem Biol 3 972-982 (2022)


Reviews citing this publication (4)

  1. Protein Recognition in Drug-Induced DNA Alkylation: When the Moonlight Protein GAPDH Meets S23906-1/DNA Minor Groove Adducts. Savreux-Lenglet G, Depauw S, David-Cordonnier MH. Int J Mol Sci 16 26555-26581 (2015)
  2. Dithiolethiones: a privileged pharmacophore for anticancer therapy and chemoprevention. Ansari MI, Khan MM, Saquib M, Khatoon S, Hussain MK. Future Med Chem 10 1241-1260 (2018)
  3. Central Metabolism in Mammals and Plants as a Hub for Controlling Cell Fate. Selinski J, Scheibe R. Antioxid Redox Signal 34 1025-1047 (2021)
  4. The mutual interaction of glycolytic enzymes and RNA in post-transcriptional regulation. Wegener M, Dietz KJ. RNA 28 1446-1468 (2022)

Articles citing this publication (12)

  1. Malonylation of GAPDH is an inflammatory signal in macrophages. Galván-Peña S, Carroll RG, Newman C, Hinchy EC, Palsson-McDermott E, Robinson EK, Covarrubias S, Nadin A, James AM, Haneklaus M, Carpenter S, Kelly VP, Murphy MP, Modis LK, O'Neill LA. Nat Commun 10 338 (2019)
  2. GAPDH controls extracellular vesicle biogenesis and enhances the therapeutic potential of EV mediated siRNA delivery to the brain. Dar GH, Mendes CC, Kuan WL, Speciale AA, Conceição M, Görgens A, Uliyakina I, Lobo MJ, Lim WF, El Andaloussi S, Mäger I, Roberts TC, Barker RA, Goberdhan DCI, Wilson C, Wood MJA. Nat Commun 12 6666 (2021)
  3. Active site cysteine-null glyceraldehyde-3-phosphate dehydrogenase (GAPDH) rescues nitric oxide-induced cell death. Kubo T, Nakajima H, Nakatsuji M, Itakura M, Kaneshige A, Azuma YT, Inui T, Takeuchi T. Nitric Oxide 53 13-21 (2016)
  4. Protein arginine methyltransferase 3-induced metabolic reprogramming is a vulnerable target of pancreatic cancer. Hsu MC, Tsai YL, Lin CH, Pan MR, Shan YS, Cheng TY, Cheng SH, Chen LT, Hung WC. J Hematol Oncol 12 79 (2019)
  5. Imatinib binding to human c-Src is coupled to inter-domain allostery and suggests a novel kinase inhibition strategy. Tsutsui Y, Deredge D, Wintrode PL, Hays FA. Sci Rep 6 30832 (2016)
  6. Biosynthesis of the fungal glyceraldehyde-3-phosphate dehydrogenase inhibitor heptelidic acid and mechanism of self-resistance. Yan Y, Zang X, Jamieson CS, Lin HC, Houk KN, Zhou J, Tang Y. Chem Sci 11 9554-9562 (2020)
  7. A metabolic control analysis approach to introduce the study of systems in biochemistry: the glycolytic pathway in the red blood cell. Angelani CR, Carabias P, Cruz KM, Delfino JM, de Sautu M, Espelt MV, Ferreira-Gomes MS, Gómez GE, Mangialavori IC, Manzi M, Pignataro MF, Saffioti NA, Salvatierra Fréchou DM, Santos J, Schwarzbaum PJ. Biochem Mol Biol Educ 46 502-515 (2018)
  8. Roles of myeloperoxidase and GAPDH in interferon-gamma production of GM-CSF-dependent macrophages. Yamaguchi R, Yamamoto T, Sakamoto A, Ishimaru Y, Narahara S, Sugiuchi H, Yamaguchi Y. Heliyon 2 e00080 (2016)
  9. Isolation of recombinant human untagged glyceraldehyde-3-phosphate dehydrogenase from E. coli producer strain. Barinova KV, Eldarov MA, Khomyakova EV, Muronetz VI, Schmalhausen EV. Protein Expr Purif 137 1-6 (2017)
  10. Cellular Exposure to Chloroacetanilide Herbicides Induces Distinct Protein Destabilization Profiles. Quanrud GM, Lyu Z, Balamurugan SV, Canizal C, Wu HT, Genereux JC. ACS Chem Biol 18 1661-1676 (2023)
  11. Investigating the Prevalence of RNA-Binding Metabolic Enzymes in E. coli. Klein T, Funke F, Rossbach O, Lehmann G, Vockenhuber M, Medenbach J, Suess B, Meister G, Babinger P. Int J Mol Sci 24 11536 (2023)
  12. Regulation of Intersubunit Interactions in Homotetramer of Glyceraldehyde-3-Phosphate Dehydrogenases upon Its Immobilization in Protein-Kappa-Carrageenan Gels. Makshakova O, Antonova M, Bogdanova L, Faizullin D, Zuev Y. Polymers (Basel) 15 676 (2023)


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