Oxidation of an exposed methionine instigates the aggregation of glyceraldehyde-3-phosphate dehydrogenase

Journal of Biological Chemistry

Volumn 289, Issue 39, 2014, Pages 26922-26936

  Samson, Andre L ^a,b   Knaupp, Anja S ^b,c   Kass, Itamar ^a,b   Kleifeld, Oded ^b   Marijanovic, Emilia M ^b   Hughes, Victoria A ^b   Lupton, Chris J ^b   Buckle, Ashley M ^b   Bottomley, Stephen P ^b   Medcalf, Robert L ^a  

^a MONASH UNIVERSITY   (Australia)

^b Department of Biochemistry and Molecular Biology ^*  (Australia)

^c Australian Regenerative Medicine Institute and Department of Anatomy and Developmental Biology   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; FREE RADICALS;

GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE; GLYCOLYTIC ENZYME; IN-VIVO; METHIONINE OXIDATION;

OXIDATION;

GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; LEUCINE; METHIONINE; METHIONINE 46; UNCLASSIFIED DRUG;

ARTICLE; BLOOD CLOTTING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MODIFICATION; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; NUCLEOCYTOPLASMIC COAGULATION; OXIDATION; PROTEIN AGGREGATION; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FOLDING; SIGNAL TRANSDUCTION; SIMULATION; SITE DIRECTED MUTAGENESIS; AMINO ACID SUBSTITUTION; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MISSENSE MUTATION; OXIDATION REDUCTION REACTION; PROTEIN PROCESSING; PROTEINOSIS;

AMINO ACID SUBSTITUTION; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HUMANS; METHIONINE; MODELS, MOLECULAR; MUTATION, MISSENSE; OXIDATION-REDUCTION; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84907454948     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.570275     Document Type: Article

References (56)

1. Seidler, N. W. (2013) GAPDH: Biological Properties and Diversity. Adv. Exp. Med. Biol. 958, 1-291
2. Durrieu, C., Bernier-Valentin, F., and Rousset, B. (1987) Binding of glyceraldehyde 3-phosphate dehydrogenase to microtubules. Mol. Cell. Biochem. 74, 55-65
3. 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., and Sawa, A. (2005) S-Nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat. Cell Biol. 7, 665-674
4. Sen, N., Hara, M. R., Ahmad, A. S., Cascio, M. B., Kamiya, A., Ehmsen, J. T., Agrawal, N., Hester, L., Doré, S., Snyder, S. H., and Sawa, A. (2009) GOSPEL: a neuroprotective protein that binds to GAPDH upon S-nitrosylation. Neuron 63, 81-91
5. Colell, A., Ricci, J. E., Tait, S., Milasta, S., Maurer, U., Bouchier-Hayes, L., Fitzgerald, P., Guio-Carrion, A., Waterhouse, N. J., Li, C. W., Mari, B., Barbry, P., Newmeyer, D. D., Beere, H. M., and Green, D. R. (2007) GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation. Cell 129, 983-997
6. Zheng, L., Roeder, R. G., and Luo, Y. (2003) S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell 114, 255-266
7. Rodríguez-Pascual, F., Redondo-Horcajo, M., Magán-Marchal, N., Lagares, D., Martínez-Ruiz, A., Kleinert, H., and Lamas, S. (2008) Glyceraldehyde-3-phosphate dehydrogenase regulates endothelin-1 expression by a novel, redox-sensitive mechanism involving mRNA stability. Mol. Cell. Biol. 28, 7139-7155
8. Jenkins, J. L., and Tanner, J. J. (2006) High-resolution structure of human D-glyceraldehyde-3-phosphate dehydrogenase. Acta Crystallogr. D Biol. Crystallogr. 62, 290-301
9. Saunders, P. A., Chen, R. W., and Chuang, D. M. (1999) Nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase isoforms during neuronal apoptosis. J. Neurochem. 72, 925-932
10. Huang, J., Hao, L., Xiong, N., Cao, X., Liang, Z., Sun, S., and Wang, T. (2009) Involvement of glyceraldehyde-3-phosphate dehydrogenase in rotenone-induced cell apoptosis: relevance to protein misfolding and aggregation. Brain Res. 1279, 1-8
11. Nakajima, H., Amano, W., Kubo, T., Fukuhara, A., Ihara, H., Azuma, Y. T., Tajima, H., Inui, T., Sawa, A., and Takeuchi, T. (2009) Glyceraldehyde-3-phosphate dehydrogenase aggregate formation participates in oxidative stress-induced cell death. J. Biol. Chem. 284, 34331-34341
12. Snider, N. T., Weerasinghe, S. V., Singla, A., Leonard, J. M., Hanada, S., Andrews, P. C., Lok, A. S., and Omary, M. B. (2011) Energy determinants GAPDH and NDPK act as genetic modifiers for hepatocyte inclusion formation. J. Cell Biol. 195, 217-229
13. Cumming, R. C., and Schubert, D. (2005) Amyloid-β induces disulfide bonding and aggregation of GAPDH in Alzheimer's disease. FASEB J. 19, 2060-2062
14. 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., and Ishitani, R. (2005) Pro-apoptotic protein glyceraldehyde-3-phosphate dehydrogenase promotes the formation of Lewy body-like inclusions. Eur. J. Neurosci. 21, 317-326
15. Guzhova, I. V., Lazarev, V. F., Kaznacheeva, A. V., Ippolitova, M. V., Muronetz, V. I., Kinev, A. V., and Margulis, B. A. (2011) Novel mechanism of Hsp70 chaperone-mediated prevention of polyglutamine aggregates in a cellular model of Huntington disease. Hum. Mol. Genet. 20, 3953-3963
16. Burke, J. R., Enghild, J. J., Martin, M. E., Jou, Y. S., Myers, R. M., Roses, A. D., Vance, J. M., and Strittmatter, W. J. (1996) Huntingtin and DRPLA proteins selectively interact with the enzyme GAPDH. Nat. Med. 2, 347-350
17. Basso, M., Samengo, G., Nardo, G., Massignan, T., D'Alessandro, G., Tartari, S., Cantoni, L., Marino, M., Cheroni, C., De Biasi, S., Giordana, M. T., Strong, M. J., Estevez, A. G., Salmona, M., Bendotti, C., and Bonetto, V. (2009) Characterization of detergent-insoluble proteins in ALS indicates a causal link between nitrative stress and aggregation in pathogenesis. PLoS One 4, e8130
18. Samson, A. L., Knaupp, A. S., Sashindranath, M., Borg, R. J., Au, A. E., Cops, E. J., Saunders, H. M., Cody, S. H., McLean, C. A., Nowell, C. J., Hughes, V. A., Bottomley, S. P., and Medcalf, R. L. (2012) Nucleocytoplasmic coagulation: an injury-induced aggregation event that disulfide crosslinks proteins and facilitates their removal by plasmin. Cell Rep. 2, 889-901
19. Wang, Q., Woltjer, R. L., Cimino, P. J., Pan, C., Montine, K. S., Zhang, J., and Montine, T. J. (2005) Proteomic analysis of neurofibrillary tangles in Alzheimer disease identifies GAPDH as a detergent-insoluble paired helical filament tau binding protein. FASEB J. 19, 869-871
20. Yan, H., Lou, M. F., Fernando, M. R., and Harding, J. J. (2006) Thioredoxin, thioredoxin reductase, and-crystallin revive inactivated glyceraldehyde 3-phosphate dehydrogenase in human aged and cataract lens extracts. Mol. Vis. 12, 1153-1159
21. Allen, M., Cox, C., Belbin, O., Ma, L., Bisceglio, G. D., Wilcox, S. L., Howell, C. C., Hunter, T. A., Culley, O., Walker, L. P., Carrasquillo, M. M., Dickson, D. W., Petersen, R. C., Graff-Radford, N. R., Younkin, S. G., and Ertekin-Taner, N. (2012) Association and heterogeneity at the GAPDH locus in Alzheimer's disease. Neurobiol. Aging 33, 203.e25-e33
22. Nakajima, H., Amano, W., Fujita, A., Fukuhara, A., Azuma, Y. T., Hata, F., Inui, T., and Takeuchi, T. (2007) 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. 282, 26562-26574
23. Nakajima, H., Amano, W., Fukuhara, A., Kubo, T., Misaki, S., Azuma, Y. T., Inui, T., and Takeuchi, T. (2009) An aggregate-prone mutant of human glyceraldehyde-3-phosphate dehydrogenase augments oxidative stress-induced cell death in SH-SY5Y cells. Biochem. Biophys. Res. Commun. 390, 1066-1071
24. Tsolis, A. C., Papandreou, N. C., Iconomidou, V. A., and Hamodrakas, S. J. (2013) A consensus method for the prediction of 'aggregation-prone' peptides in globular proteins. PLoS One 8, e54175
25. Deutsch, E. W., Mendoza, L., Shteynberg, D., Farrah, T., Lam, H., Tasman, N., Sun, Z., Nilsson, E., Pratt, B., Prazen, B., Eng, J. K., Martin, D. B., Nesvizhskii, A. I., and Aebersold, R. (2010) A guided tour of the Trans-Proteomic Pipeline. Proteomics 10, 1150-1159
26. Han, X., He, L., Xin, L., Shan, B., and Ma, B. (2011) Peaks PTM: mass spectrometry-based identification of peptides with unspecified modifications. J. Proteome Res. 10, 2930-2936
27. Tornvall, U. (2010) Pinpointing oxidative modifications in proteinsrecent advances in analytical methods. Anal. Methods 2, 1638-1650
28. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435-447
29. Miller, S., Janin, J., Lesk, A. M., and Chothia, C. (1987) Interior and surface of monomeric proteins. J. Mol. Biol. 196, 641-656
30. Schymkowitz, J., Borg, J., Stricher, F., Nys, R., Rousseau, F., and Serrano, L. (2005) The FoldX web server: an online force field. Nucleic Acids Res. 33, W382-W388
31. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalé, L., and Schulten, K. (2005) Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802
32. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., and Simmerling, C. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712-725
33. Wickstrom, L., Okur, A., and Simmerling, C. (2009) Evaluating the performance of the ff99SB force field based on NMR scalar coupling data. Biophys. J. 97, 853-856
34. Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., and Case, D. A. (2004) Development and testing of a general amber force field. J. Comput. Chem. 25, 1157-1174
35. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935
36. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald: an Nβlog(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092
37. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38, 27-28
38. Cortez, L. M., Avila, C. L., Bugeau, C. M., Farías, R. N., Morero, R. D., and Chehín, R. N. (2010) Glyceraldehyde-3-phosphate dehydrogenase tetramer dissociation and amyloid fibril formation induced by negatively charged membranes. FEBS Lett. 584, 625-630
39. Wolfe, L. S., Calabrese, M. F., Nath, A., Blaho, D. V., Miranker, A. D., and Xiong, Y. (2010) Protein-induced photophysical changes to the amyloid indicator dye thioflavin T. Proc. Natl. Acad. Sci. U.S.A. 107, 16863-16868
40. Haigis, M. C., and Yankner, B. A. (2010) The aging stress response. Mol. Cell 40, 333-344
41. Keller, A., Eng, J., Zhang, N., Li, X. J., and Aebersold, R. (2005) A uniform proteomics MS/MS analysis platform utilizing open XML file formats. Mol. Syst. Biol. 1, 2005.0017
42. Xu, G., and Chance, M. R. (2007) Hydroxyl radical-mediated modification of proteins as probes for structural proteomics. Chem. Rev. 107, 3514-3543
43. Markossian, K. A., Khanova, H. A., Kleimenov, S. Y., Levitsky, D. I., Chebotareva, N. A., Asryants, R. A., Muronetz, V. I., Saso, L., Yudin, I. K., and Kurganov, B. I. (2006) Mechanism of thermal aggregation of rabbit muscle glyceraldehyde-3-phosphate dehydrogenase. Biochemistry 45, 13375-13384
44. Durchschlag, H., Puchwein, G., Kratky, O., Schuster, I., and Kirschner, K. (1971) X-ray small-angle scattering of yeast glyceraldehyde-3-phosphate dehydrogenase as a function of saturation with nicotinamide-adeninedinucleotide. Eur. J. Biochem. 19, 9-22
45. Ferns, J. E., Theisen, C. S., Fibuch, E. E., and Seidler, N. W. (2012) Protection against protein aggregation by-crystallin as a mechanism of preconditioning. Neurochem. Res. 37, 244-252
46. Naletova, I. N., Muronetz, V. I., and Schmalhausen, E. V. (2006) Unfolded, oxidized, and thermoinactivated forms of glyceraldehyde-3-phosphate dehydrogenase interact with the chaperonin GroEL in different ways. Biochim. Biophys. Acta 1764, 831-838
47. Polyakova, O. V., Roitel, O., Asryants, R. A., Poliakov, A. A., Branlant, G., and Muronetz, V. I. (2005) Misfolded forms of glyceraldehyde-3-phosphate dehydrogenase interact with GroEL and inhibit chaperonin-assisted folding of the wild-type enzyme. Protein Sci. 14, 921-928
48. Tanaka, N., Morimoto, Y., Noguchi, Y., Tada, T., Waku, T., Kunugi, S., Morii, T., Lee, Y. F., Konno, T., and Takahashi, N. (2011) The mechanism of fibril formation of a non-inhibitory serpin ovalbumin revealed by the identification of amyloidogenic core regions. J. Biol. Chem. 286, 5884-5894
49. Mulinacci, F., Poirier, E., Capelle, M. A., Gurny, R., and Arvinte, T. (2013) Influence of methionine oxidation on the aggregation of recombinant human growth hormone. Eur. J. Pharm. Biopharm. 85, 42-52
50. Zhao, L., Buxbaum, J. N., and Reixach, N. (2013) Age-related oxidative modifications of transthyretin modulate its amyloidogenicity. Biochemistry 52, 1913-1926
51. Herrero, R., Kajikawa, O., Matute-Bello, G., Wang, Y., Hagimoto, N., Mongovin, S., Wong, V., Park, D. R., Brot, N., Heinecke, J. W., Rosen, H., Goodman, R. B., Fu, X., and Martin, T. R. (2011) The biological activity of FasL in human and mouse lungs is determined by the structure of its stalk region. J. Clin. Investig. 121, 1174-1190
52. Wong, Y. Q., Binger, K. J., Howlett, G. J., and Griffin, M. D. (2010) Methionine oxidation induces amyloid fibril formation by full-length apolipoprotein A-I. Proc. Natl. Acad. Sci. U.S.A. 107, 1977-1982
53. Torosantucci, R., Sharov, V. S., van Beers, M., Brinks, V., Schöneich, C., and Jiskoot, W. (2013) Identification of oxidation sites and covalent cross-links in metal catalyzed oxidized interferon β-1a: potential implications for protein aggregation and immunogenicity. Mol. Pharm. 10, 2311-2322
54. Mitomi, Y., Nomura, T., Kurosawa, M., Nukina, N., and Furukawa, Y. (2012) Post-aggregation oxidation of mutant huntingtin controls the interactions between aggregates. J. Biol. Chem. 287, 34764-34775
55. Koudelka, T., Dehle, F. C., Musgrave, I. F., Hoffmann, P., and Carver, J. A. (2012) Methionine oxidation enhances β-casein amyloid fibril formation. J. Agric. Food Chem. 60, 4144-4155
56. Surgucheva, I., Sharov, V. S., and Surguchov, A. (2012) β-Synuclein: seeding of-synuclein aggregation and transmission between cells. Biochemistry 51, 4743-4754.