Urea ameliorates trimethylamine N-oxide-Induced aggregation of intrinsically disordered α-casein protein: the other side of the urea-methylamine counteraction

References

• Bhat, M. Y., Singh, L. R., & Dar, T. A. (2017). Trimethylamine N-oxide abolishes the chaperone activity of alpha-casein: An intrinsically disordered protein. Scientific Reports, 7(1), 1–8. https://doi.org/10.1038/s41598-017-06836-2
   PubMedGoogle Scholar
• Borwankar, T., Rothlein, C., Zhang, G., Techen, A., Dosche, C., & Ignatova, Z. (2011). Natural osmolytes remodel the aggregation pathway of mutant huntingtin exon 1. Biochemistry, 50(12), 2048–2060. https://doi.org/10.1021/bi1018368
   PubMed Web of Science ®Google Scholar
• Chen, S.-J., Kuo, C.-H., Kuo, H.-C., Chen, C.-C., Wu, W.-K., Liou, J.-M., Wu, M.-S., & Lin, C.-H. (2020). The gut metabolite trimethylamine N-oxide is associated with Parkinson's disease severity and progression. Movement Disorders: Official Journal of the Movement Disorder Society, 35(11), 2115–2116. https://doi.org/10.1002/mds.28246
   PubMed Web of Science ®Google Scholar
• Debnath, K., Shekhar, S., Kumar, V., Jana, N. R., & Jana, N. R. (2016). Efficient inhibition of protein aggregation, disintegration of aggregates, and lowering of cytotoxicity by green tea polyphenol-based self-assembled polymer nanoparticles. ACS Applied Materials & Interfaces, 8(31), 20309–20318. https://doi.org/10.1021/acsami.6b06853
   PubMed Web of Science ®Google Scholar
• Ganguly, P., Boserman, P., Van Der Vegt, N. F. A., & Shea, J.-E. (2018). Trimethylamine N-oxide counteracts urea denaturation by inhibiting protein-urea preferential interaction. Journal of the American Chemical Society, 140(1), 483–492. https://doi.org/10.1021/jacs.7b11695
   PubMed Web of Science ®Google Scholar
• Ganguly, P., Polak, J., van der Vegt, N. F. A., Heyda, J., & Shea, J.-E. (2020). Protein stability in TMAO and mixed urea-TMAO solutions. The Journal of Physical Chemistry. B, 124(29), 6181–6197. https://doi.org/10.1021/acs.jpcb.0c04357
   PubMed Web of Science ®Google Scholar
• Holthauzen, L. M. F., & Bolen, D. W. (2007). Mixed osmolytes: the degree to which one osmolyte affects the protein stabilizing ability of another. Protein Science : A Publication of the Protein Society, 16(2), 293–298.
   PubMed Web of Science ®Google Scholar
• Jahan, I., & Nayeem, S. M. (2019). Effect of osmolytes on conformational behavior of intrinsically disordered protein α-synuclein. Biophysical Journal, 117(10), 1922–1934. https://doi.org/10.1016/j.bpj.2019.09.046
   PubMed Web of Science ®Google Scholar
• Khan, S. H., Ahmad, N., Ahmad, F., & Kumar, R. (2010). Naturally occurring organic osmolytes: From cell physiology to disease prevention. IUBMB Life, 62(12), 891–895. https://doi.org/10.1002/iub.406
   PubMed Web of Science ®Google Scholar
• Lee, S., Choi, M. C., Al Adem, K., Lukman, S., & Kim, T.-Y. (2020). Aggregation and cellular toxicity of pathogenic or non-pathogenic proteins. Scientific Reports, 10(1), 1–14. https://doi.org/10.1038/s41598-020-62062-3
   PubMedGoogle Scholar
• Levine, Z. A., Larini, L., LaPointe, N. E., Feinstein, S. C., & Shea, J.-E. (2015). Regulation and aggregation of intrinsically disordered peptides. Proceedings of the National Academy of Sciences of the United States of America, 112(9), 2758–2763. https://doi.org/10.1073/pnas.1418155112
   PubMed Web of Science ®Google Scholar
• Ma, J., Pazos, I. M., & Gai, F. (2014). Microscopic insights into the protein-stabilizing effect of trimethylamine N-oxide (TMAO). Proceedings of the National Academy of Sciences of the United States of America, 111(23), 8476–8481. https://doi.org/10.1073/pnas.1403224111
   PubMed Web of Science ®Google Scholar
• Meersman, F., Bowron, D., Soper, A. K., & Koch, M. H. J. (2009). Counteraction of urea by trimethylamine N-oxide is due to direct interaction. Biophysical Journal, 97(9), 2559–2566. https://doi.org/10.1016/j.bpj.2009.08.017
   PubMed Web of Science ®Google Scholar
• Mello, C. C., & Barrick, D. (2003). Measuring the stability of partly folded proteins using TMAO. Protein Science: A Publication of the Protein Society, 12(7), 1522–1529. https://doi.org/10.1110/ps.0372903
   PubMed Web of Science ®Google Scholar
• Mukherjee, A., Santra, M. K., Beuria, T. K., & Panda, D. (2005). A natural osmolyte trimethylamine N-oxide promotes assembly and bundling of the bacterial cell division protein, FtsZ and counteracts the denaturing effects of urea. The FEBS Journal, 272(11), 2760–2772. https://doi.org/10.1111/j.1742-4658.2005.04696.x
   PubMed Web of Science ®Google Scholar
• Mukherjee, M., & Mondal, J. (2020). Unifying the contrasting mechanisms of protein-stabilizing osmolytes. The Journal of Physical Chemistry. B, 124(30), 6565–6574. https://doi.org/10.1021/acs.jpcb.0c04757
   PubMed Web of Science ®Google Scholar
• Oprzeska-Zingrebe, E. A., & Smiatek, J. (2019). Aqueous mixtures of urea and trimethylamine-N-oxide: Evidence for kosmotropic or chaotropic behavior? The Journal of Physical Chemistry. B, 123(20), 4415–4424. https://doi.org/10.1021/acs.jpcb.9b02598
   PubMed Web of Science ®Google Scholar
• Rahman, S., Warepam, M., Singh, L. R., & Dar, T. A. (2015). A current perspective on the compensatory effects of urea and methylamine on protein stability and function. Progress in Biophysics and Molecular Biology, 119(2), 129–136. https://doi.org/10.1016/j.pbiomolbio.2015.06.002
   PubMed Web of Science ®Google Scholar
• Saha, I., Singh, V., Burra, G., & Thakur, A. K. (2018). Osmolytes modulate polyglutamine aggregation in a sequence dependent manner. Journal of Peptide Science : An Official Publication of the European Peptide Society, 24(8-9), e3115. https://doi.org/10.1002/psc.3115
   PubMed Web of Science ®Google Scholar
• Sarma, R., & Paul, S. (2013). Crucial importance of water structure modification on trimethylamine N-oxide counteracting effect at high pressure. The Journal of Physical Chemistry. B, 117(2), 677–689. https://doi.org/10.1021/jp311102v
   PubMed Web of Science ®Google Scholar
• Scaramozzino, F., Peterson, D. W., Farmer, P., Gerig, J., Graves, D. J., & Lew, J. (2006). TMAO promotes fibrillization and microtubule assembly activity in the C-terminal repeat region of tau. Biochemistry, 45(11), 3684–3691. https://doi.org/10.1021/bi052167g
   PubMed Web of Science ®Google Scholar
• Singh, L. R., Dar, T. A., Haque, I., Anjum, F., Moosavi-Movahedi, A. A., & Ahmad, F. (2007). Testing the paradigm that the denaturing effect of urea on protein stability is offset by methylamines at the physiological concentration ratio of 2: 1 (urea: methylamines). Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, 1774(12), 1555–1562. https://doi.org/10.1016/j.bbapap.2007.09.006
   PubMed Web of Science ®Google Scholar
• Stubbs, J., House, J., Ocque, J., Zhang, S., Johnson, C., Kimber, C., Schmidt, K., Gupta, A., Wetmore, J., Nolin, T., Spertus, J., & Yu, A. (2016). Serum trimethylamine-N-oxide is elevated in CKD and correlates with coronary atherosclerosis burden. Journal of the American Society of Nephrology, 27(1), 305–313. https://doi.org/10.1681/ASN.2014111063
   PubMed Web of Science ®Google Scholar
• Su, Z., & Dias, C. L. (2019). Individual and combined effects of urea and trimethylamine N-oxide (TMAO) on protein structures. Journal of Molecular Liquids, 293, 111443. https://doi.org/10.1016/j.molliq.2019.111443
   Web of Science ®Google Scholar
• Timasheff, S. N. (2002). Protein hydration, thermodynamic binding, and preferential hydration. Biochemistry, 41(46), 13473–13482. https://doi.org/10.1021/bi020316e
   PubMed Web of Science ®Google Scholar
• Timasheff, S. N. (2002). Protein-solvent preferential interactions, protein hydration, and the modulation of biochemical reactions by solvent components. Proceedings of the National Academy of Sciences of the United States of America, 99(15), 9721–9726. https://doi.org/10.1073/pnas.122225399
   PubMed Web of Science ®Google Scholar
• Tomlinson, J. A. P., & Wheeler, D. C. (2017). The role of trimethylamine N-oxide as a mediator of cardiovascular complications in chronic kidney disease. Kidney International, 92(4), 809–815. https://doi.org/10.1016/j.kint.2017.03.053
   PubMed Web of Science ®Google Scholar
• Uversky, V. N., Li, J., & Fink, A. L. (2001). Trimethylamine-N-oxide-induced folding of alpha-synuclein . FEBS Letters, 509(1), 31–35. https://doi.org/10.1016/s0014-5793(01)03121-0
   PubMed Web of Science ®Google Scholar
• Voloshin, V., Smolin, N., Geiger, A., Winter, R., & Medvedev, N. N. (2019). Dynamics of TMAO and urea in the hydration shell of the protein SNase. Physical Chemistry Chemical Physics : PCCP, 21(35), 19469–19479. https://doi.org/10.1039/c9cp03184g
   PubMed Web of Science ®Google Scholar
• Wang, A., & Bolen, D. (1997). A naturally occurring protective system in urea-rich cells: Mechanism of osmolyte protection of proteins against urea denaturation. Biochemistry, 36(30), 9101–9108. https://doi.org/10.1021/bi970247h
   PubMed Web of Science ®Google Scholar
• Withers, P., Hefter, G., & Pang, T. S. (1994). Role of urea and methylamines in buoyancy of elasmobranchs. The Journal of Experimental Biology, 188(1), 175–189. https://doi.org/10.1242/jeb.188.1.175
   PubMedGoogle Scholar
• Yancey, P. H. (2005). Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. The Journal of Experimental Biology, 208(Pt 15), 2819–2830. https://doi.org/10.1242/jeb.01730
   PubMed Web of Science ®Google Scholar
• Yancey, P. H., & Somero, G. N. (1979). Counteraction of urea destabilization of protein structure by methylamine osmoregulatory compounds of elasmobranch fishes. The Biochemical Journal, 183(2), 317–323. https://doi.org/10.1042/bj1830317
   PubMed Web of Science ®Google Scholar
• Yancey, P. H., & Somero, G. N. (1980). Methylamine osmoregulatory solutes of elasmobranch fishes counteract urea inhibition of enzymes. Journal of Experimental Zoology, 212(2), 205–213. https://doi.org/10.1002/jez.1402120207
   Google Scholar
• Yancey, P. H., Clark, M. E., Hand, S. C., Bowlus, R. D., & Somero, G. N. (1982). Living with water stress: Evolution of osmolyte systems. Science (New York, N.Y.), 217(4566), 1214–1222. https://doi.org/10.1126/science.7112124
   PubMed Web of Science ®Google Scholar
• Yang, D.-S., Yip, C. M., Huang, T. J., Chakrabartty, A., & Fraser, P. E. (1999). Manipulating the amyloid-beta aggregation pathway with chemical chaperones. The Journal of Biological Chemistry, 274(46), 32970–32974. https://doi.org/10.1074/jbc.274.46.32970
   PubMed Web of Science ®Google Scholar
• Zeisel, S. H., & Warrier, M. (2017). Trimethylamine N-oxide, the microbiome, and heart and kidney disease. Annual Review of Nutrition, 37, 157–181. https://doi.org/10.1146/annurev-nutr-071816-064732
   PubMed Web of Science ®Google Scholar
• Zetterholm, S., Verville, G., Boutwell, L., Boland, C., Prather, J., Bethea, J., Cauley, J., Warren, K., Smith, S., Magers, D., & Hammer, N. (2018). Noncovalent interactions between trimethylamine N-Oxide (TMAO), urea, and water. The Journal of Physical Chemistry. B, 122(38), 8805–8811. https://doi.org/10.1021/acs.jpcb.8b04388
   PubMed Web of Science ®Google Scholar
• Zhou, R., & Xu, B. (2014). Insight of the cytotoxicity of the aggregates of peptides or aberrant proteins: A meta-analysis. PloS One, 9(4), e95759. https://doi.org/10.1371/journal.pone.0095759
   PubMed Web of Science ®Google Scholar
• Zou, Q., Bennion, B. J., Daggett, V., & Murphy, K. P. (2002). The molecular mechanism of stabilization of proteins by TMAO and its ability to counteract the effects of urea. Journal of the American Chemical Society, 124(7), 1192–1202. https://doi.org/10.1021/ja004206b
   PubMed Web of Science ®Google Scholar