Abstract
The possibility of inhibition of chaperonin functional activity by amyloid proteins was studied. It was found that the ovine prion protein PrP as well as its oligomeric and fibrillar forms are capable of binding with the chaperonin GroEL. Besides, GroEL was shown to promote amyloid aggregation of the monomeric and oligomeric PrP as well as PrP fibrils. The monomeric PrP was shown to inhibit the GroEL-assisted reactivation of the glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase (GAPDH). The oligomers of PrP decelerate the GroEL-assisted reactivation of GAPDH, and PrP fibrils did not affect this process. The chaperonin GroEL is capable of interacting with GAPDH and different PrP forms simultaneously. A possible role of the inhibition of chaperonins by amyloid proteins in the misfolding of the enzymes involved in cell metabolism and in progression of neurodegenerative diseases of amyloid nature is discussed.
Similar content being viewed by others
Abbreviations
- DEAE:
-
diethylaminoethyl
- DLS:
-
dynamic light scattering
- EDTA:
-
ethylenediaminetetraacetate
- GAPDH:
-
glyceraldehyde-3-phosphate dehydrogenase
- HEPES:
-
4-(2hydroxyethyl)-1-piperazinethanesulfonic acid
- β-ME:
-
β-mercaptoethanol
- MOPS:
-
3-[N-morpholino]propanesulfonic acid
- PBST:
-
phosphate-buffered saline containing 0.05% Tween-20
- PrP:
-
prion protein
- ThT:
-
thioflavin T
References
Nussbaum-Krammer, C., Mogk, A., Nillegoda, N. B., Szlachcic, A., Guilbride, D. L., Saibil, H. R., Mayer, M. P., and Bukau, B. (2015) Human Hsp70 disaggregase reverses Parkinson’s-linked a-synuclein amyloid fibrils, Mol. Cell, 59, 781–793.
Landreh, M., Rising, A., Presto, J., Jornvall, H., and Johansson, J. (2015) Specific chaperones and regulatory domains in control of amyloid formation, J. Biol. Chem., 290, 26430–26436.
Sablon-Carrazana, M., Fernandez, I., Bencomo, A., LaraMarinez, R., Rivera-Marrero, S., Dominguez, G., PerezPerera, R., Jimenez-Garcia, L. F., AltamiranoBustamante, N. F., Diaz-Delgado, M., Vedrenne, F., Rivillas-Acevedo, L., Pasten-Hidalgo, K., De Lourdes Segura-Valdez, M., Islas-Andrade, S., Garrido-Magana, E., Perera-Pintado, A., Prats-Capote, A., RodriguezTanty, C., and Altamirano-Bustamante, M. M. (2015) Drug development in conformational diseases: a novel family of chemical chaperones that bind and stabilise several polymorphic amyloid structures, PLoS One, 10, 1–24.
Wisniewski, T., and Sadowski, M. (2008) Preventing betaamyloid fibrillization and deposition: beta-sheet breakers and pathological chaperone inhibitors, BMC Neurosci., 9 (Suppl. 2), S5.
Xi, D., Dong, X., Deng, W., and Lai, L. (2011) Dynamic behavior of small heat shock protein inhibition on amyloid fibrillization of a small peptide (SSTSAA) from RNase A, Biochem. Biophys. Res. Commun., 416, 130–134.
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.
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.
Tillement, L., Lecanu, L., and Papadopoulos, V. (2011) Alzheimer’s disease: effects of β-amyloid on mitochondria, Mitochondrion, 11, 13–21.
Mamelak, M. (2012) Sporadic Alzheimer’s disease: the starving brain, J. Alzheimer’s Dis., 31, 459–474.
Yao, J., Rettberg, J., Klosinski, L., Cadenas, E., and Brinton, R. (2011) Shift in brain metabolism in late onset Alzheimer’s disease: implications for biomarkers and therapeutic interventions, Mol. Asp. Med., 32, 247–257.
Rama Rao, K. V., and Norenberg, M. D. (2012) Brain energy metabolism and mitochondrial dysfunction in acute and chronic hepatic encephalopathy, Neurochem. Int., 60, 697–706.
Vlassenko, A. G., Vaishnavi, S. N., Couture, L., Sacco, D., Shannon, B. J., Mach, R. H., Morris, J. C., Raichle, M. E., and Mintun, M. A. (2010) Spatial correlation between brain aerobic glycolysis and amyloid-β (Aβ) deposition, Proc. Natl. Acad. Sci. USA, 107, 17763–17767.
Vaishnavi, S. N., Vlassenko, A. G., Rundle, M. M., Snyder, A. Z., Mintun, M. A., and Raichle, M. E. (2010) Regional aerobic glycolysis in the human brain, Proc. Natl. Acad. Sci. USA, 107, 17757–17762.
Jayasena, T., Poljak, A., Braidy, N., Smythe, G., Raftery, M., Hill, M., Brodaty, H., Trollor, J., Kochan, N., and Sachdev, P. (2015) Upregulation of glycolytic enzymes, mitochondrial dysfunction and increased cytotoxicity in glial cells treated with Alzheimer’s disease plasma, PLoS One, 10, e0116092.
Rodacka, A. (2013) Properties and functional diversity of glyceraldehyde-3-phosphate dehydrogenase, Postepy Hig. Med. Doswiadczalnej, 67, 775–789.
Seidler, N. W. (2013) Basic biology of GAPDH, Adv. Exp. Med. Biol., 985, 1–36.
Naletova, I. N., Popova, K. M., Eldarov, M. A., Kuravsky, M. L., Schmalhausen, E. V., Sevostyanova, I. A., and Muronetz, V. I. (2011) Chaperonin TRiC assists the refolding of sperm-specific glyceraldehyde-3-phosphate dehydrogenase, Arch. Biochem. Biophys., 516, 75–83.
Bulatnikov, I. G., Polyakova, O. V., Asryants, R. A., Nagradova, N. K., and Muronetz, V. I. (1999) Participation of chaperonin GroEL in the folding of D-glyceraldehyde3-phosphate dehydrogenase. An approach based on the use of different oligomeric forms of the enzyme immobilized on sepharose, J. Protein Chem., 18, 79–87.
Li, X. L., Lei, X. D., Cai, H., Li, J., Yang, S. L., Wang, C. C., and Tsou, C. L. (1998) Binding of a burst-phase intermediate formed in the folding of denatured D-glyceraldehyde-3-phosphate dehydrogenase by chaperonin 60 and 8anilino-1-naphthalenesulphonic acid, Biochem. J., 331 (Pt. 2), 505–511.
Viet, M. H., Ngo, S. T., Lam, N. S., and Li, M. S. (2011) Inhibition of aggregation of amyloid peptides by beta-sheet breaker peptides and their binding affinity, J. Phys. Chem. B, 115, 7433–7446.
Markossian, K. A., Golub, N. V., Chebotareva, N. A., Asryants, R. A., Naletov, I. N., Muronetz, V. I., Muranov, K. O., and Kurganov, B. I. (2010) Comparative analysis of the effects of alpha-crystallin and GroEL on the kinetics of thermal aggregation of rabbit muscle glyceraldehyde-3phosphate dehydrogenase, Protein J., 29, 11–25.
Kiselev, G. G., Naletova, I. N., Sheval, E. V., Stroylova, Y. Y., Schmalhausen, E. V., Haertle, T., and Muronetz, V. I. (2011) Chaperonins induce an amyloid-like transformation of ovine prion protein: the fundamental difference in action between eukaryotic TRiC and bacterial GroEL, Biochim. Biophys. Acta, 1814, 1730–1738.
Ricci, C., Ortore, M. G., Vilasi, S., Carrotta, R., Mangione, M. R., Bulone, D., Librizzi, R., Spinozzi, F., Burgio, G., Amenitsch, H., and San Biagio, P. L. (2016) Stability and disassembly properties of human naiive Hsp60 and bacterial GroEL chaperonins, Biophys. Chem., 208, 68–75.
Scopes, R. K., and Stoter, A. (1982) Purification of all glycolytic enzymes from one muscle extract, Methods Enzymol., 90 (Pt. E), 479–490.
Rezaei, H., Marc, D., Choiset, Y., Takahashi, M., Hui Bon Hoa, G., Haertle, T., Grosclaude, J., and Debey, P. (2000) High yield purification and physico-chemical properties of full-length recombinant allelic variants of sheep prion protein linked to scrapie susceptibility, Eur. J. Biochem., 267, 2833–2839.
Breydo, L., Makarava, N., and Baskakov, I. V. (2008) Methods for conversion of prion protein into amyloid fibrils, Methods Mol. Biol., 459, 105–115.
Ban, T., Hamada, D., Hasegawa, K., Naiki, H., and Goto, Y. (2003) Direct observation of amyloid fibril growth monitored by thioflavin T fluorescence, J. Biol. Chem., 278, 16462–16465.
Voropai, E. S., Samtsov, M. P., Kaplevskii, K. N., Maskevich, A. A., Stepuro, V. I., Povarova, O. I., Kuznetsova, I. M., Turoverov, K. K., Fink, A. L., and Uverskii, V. N. (2003) Spectral properties of thioflavin T and its complexes with amyloid fibrils, Appl. Spectrosc., 70, 868–874.
Author information
Authors and Affiliations
Corresponding author
Additional information
Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM16-235, September 12, 2016.
Rights and permissions
About this article
Cite this article
Kudryavtseva, S.S., Stroylova, Y.Y., Zanyatkin, I.A. et al. Inhibition of chaperonin GroEL by a monomer of ovine prion protein and its oligomeric forms. Biochemistry Moscow 81, 1213–1220 (2016). https://doi.org/10.1134/S0006297916100199
Received:
Revised:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0006297916100199