Deciphering the Interactions of Crystallins with Metal Ions/ ATP and its Applications: A Novel Study

Aparajita Chakraborty
Department of Biotechnology, St. Xavier’s College (Autonomous), Kolkata–700016, India

Dimensions

Plum Analytics

Abstract

Crystallins are the predominant proteins of the eye lens which prevent the heat and oxidative-induced stress-induced aggregation of other proteins. They may be classified into two superfamilies, the α- and βγ- crystallins. The βγ- crystallins are long-lived structural proteins which refract light onto the retina. The microbial crystallins can not only bind to calcium ions, but even able to coordinate other ions such as Mg2+, Sr2+, Co2+, Mn2+, Ni2+, Zn2+ etc. Such metal ions may influence the stability and aggregation propensity of human γS- crystallin as well. Previous studies had even revealed the binding of αA- and αB- crystallins with Cu2+ ions and suppressed the formation of Cu2+ mediated oxygen species and thus protected ascorbic acid from oxidation by copper ions. The residues 71-88 present in mini αA- crystallin, a peptide of αA- crystallin were found to be responsible for the prevention of oxidation. The binding of metal ions to crystallins may influence the formation of protein aggregates, and thus cataract or other disorders but there are some ions which may even help to improve the chaperone activity of α crystallins. Adenosine triphosphate (ATP), the energy currency of the cell improves the chaperone activity of α-crystallins by regulating the chaperone-target substrate interactions. This minireview explores various insights of the interactions of crystallins with metal ions and ATP which may help in the search for more therapeutic molecules in near future.

Keywords

  • Crystallins,
  • Chaperone Activity,
  • Interactions,
  • Metal Ions,
  • Protein Aggregates,
  • Disorders,
  • ATP,
  • Therapeutic Molecules
  • ...More
    Less

References

  1. S. Ramkumar, X. Fan, B. Wang, S. Yang, V.M. Monnier, Reactive cysteine residues in the oxidative dimerization and Cu2+ induced aggregation of human γD-crystallin: Implications for age-related cataract, Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, 1864 (11) (2018) 3595-3604.
  2. K.K. Sharma, P. Santhoshkumar, Lens aging: effects of crystallins, Biochimica et Biophysica Acta (BBA) - General Subjects, 1790 (10) (2009) 1095-1108.
  3. O. Cekic, Effect of cigarette smoking on copper, lead, and cadmium accumulation in human lens, British Journal of Ophthalmology, 82 (2) (1998) 186-188.
  4. V.K. Srivastava, N. Varshney, D.C. Pandey, Role of trace elements in senile cataract, Acta Ophthalmologica, 70 (6) (1992) 839-841.
  5. A. Pande, D. Gillot, J. Pande, The cataract-associated R14C mutant of human gamma D-crystallin shows a variety of intermolecular disulfide cross-links: a Raman spectroscopic study, Biochemistry, 48 (22) (2009) 4937-4945.
  6. K.W. Roskamp, N. Kozlyuk, S. Sengupta, J.C. Bierma, R.W. Martin, Divalent Cations and the Divergence of βγ-Crystallin Function, Biochemistry, 58 (45) (2019) 4505-4518.
  7. K.S. Ghosh, A. Pande, J. Pande, Binding of γ-crystallin substrate prevents the binding of copper and zinc ions to the molecular chaperone α-crystallin, Biochemistry, 50 (16) (2011) 3279-3281.
  8. P. Aravind, A. Mishra, S.K. Suman, M.K. Jobby, R. Sankaranarayanan, Y. Sharma, The βγ-Crystallin Superfamily Contains a Universal Motif for Binding Calcium, Biochemistry, 48 (51) (2009) 12180-12190.
  9. S.S. Srivastava, A. Mishra, B. Krishnan, Y. Sharma, Ca2+-binding Motif of βγ-Crystallins, Journal of Biological Chemistry, 289 (16) (2014) 10958-10966.
  10. M. Raju, P. Santhoshkumar, T.M. Henzl, K. K. Sharma, Identification and characterization of a copper-binding site in αA-crystallin, Free Radical Biology and Medicine, 50 (10) (2011) 1429-1436.
  11. J. Horwitz, Alpha-crystallin, Experimental Eye Research, 76 (2) (2003) 145-153.
  12. B.J. Ortwerth, H.L. James, Lens proteins block the copper-mediated formation of reactive oxygen species during glycation reactions in vitro, Biochemical and Biophysical Research Communications, 259 (3) (1999) 706-710.
  13. C.D. Eckhert, Elemental concentrations in ocular tissues of various species, Experimental Eye Research, 37 (6) (1983) 639-647.
  14. R.P. Barnwal, M.K. Jobby, Y. Sharma, K.V. Chary, NMR assignment of M-crystallin: a novel Ca2+ binding protein of the betagamma-crystallin superfamily from Methanosarcina acetivorans, Journal of Biomolecular NMR, 36 (Suppl 1) (2006) 32.
  15. L. Quintanar, J.A. Domínguez-Calva, E. Serebryany, L. Rivillas-Acevedo, C. Haase-Pettingell, C. Amero, J.A. King, Copper and Zinc Ions Specifically Promote Nonamyloid Aggregation of the Highly Stable Human γ-D Crystallin, ACS Chemical Biology, 11 (1) (2016) 263-272.
  16. J.A. Domínguez-Calva, M.L. Pérez-Vázquez, E. Serebryany, J.A. King, L. Quintanar, Mercury-induced aggregation of human lens γ-crystallins reveals a potential role in cataract disease, JBIC Journal of Biological Inorganic Chemistry, 23 (7) (2018) 1105-1118.
  17. M.S. Kosinski-Collins, S.L. Flaugh, J. King, Probing folding and fluorescence quenching in human γD crystallin Greek key domains using triple tryptophan mutant proteins, Protein Science, 13 (8) (2004) 2223-2235.
  18. S.L. Flaugh, M.S. Kosinski-Collins, J. King, Contributions of hydrophobic domain interface interactions to the folding and stability of human γD-crystallin, Protein Science, 14 (3) (2005) 569-581.
  19. N. Kozlyuk, S. Sengupta, J.C. Bierma, R.W. Martin, Calcium Binding Dramatically Stabilizes an Ancestral Crystallin Fold in Tunicate βγ-Crystallin, Biochemistry, 55 (50) (2016) 6961-6968.
  20. M. Schmeling, B.I. Gaynes, S.T. Kebritchi, Heavy metal analysis in lens and aqueous humor of cataract patients by total reflection X-ray fluorescence spectrometry, Powder Diffraction, 29 (2) (2014) 155-158.
  21. M.W. Brazier, P. Davies, E. Player, F. Marken, J.H. Viles, D.R. Brown, Manganese Binding to the Prion Protein, Journal of Biological Chemistry, 283 (19) (2008) 12831-12839.
  22. J. Dawczynski, M. Blum, K. Winnefeld, J. Strobel, Increased content of zinc and iron in human cataractous lenses, Biological Trace Element Research, 90 (1-3) (2002) 15-23.
  23. M.F. Ahmad, D. Singh, A. Taiyab, T. Ramakrishna, B. Raman, M. Rao Ch, Selective Cu2+ Binding, Redox Silencing, and Cytoprotective Effects of the Small Heat Shock Proteins αA- and αB-Crystallin, Journal of Molecular Biology, 382 (3) (2008) 812-824.
  24. T. Kowalik-Jankowska, M. Ruta-Dolejsz, K. Wiśniewska, L. Lankiewicz, Cu (II) interaction with N-terminal fragments of human and mouse beta-amyloid peptide, Journal of Inorganic Biochemistry, 86 (2-3) (2001) 535-545.
  25. A. Laganowsky, J.L. Benesch, M. Landau, L. Ding, M.R. Sawaya, D. Cascio, Q. Huang, C.V. Robinson, J. Horwitz, D. Eisenberg, Crystal structures of truncated alphaA and alphaB crystallins reveal structural mechanisms of polydispersity important for eye lens function, Protein Science, 19(5) (2010) 1031-1043.
  26. S.K. Nandi, A.K. Panda, A. Chakraborty, S. Rathee, I. Roy, S. Barik, S.S. Mohapatra, A. Biswas, Role of ATP-Small Heat Shock Protein Interaction in Human Diseases, Frontiers in Molecular Biosciences, 9 (2022) 844826.
  27. E. Basha, H. O'Neill, E. Vierling, Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions, Trends in Biochemical Science, 37 (3) (2012) 106-117.
  28. K.K. Sharma, P. Santhoshkumar, Lens aging: effects of crystallins, Biochimica et Biophysica Acta (BBA) - General Subjects, 1790 (10) (2009) 1095-1108.
  29. A.K. Panda, S.K. Nandi, A. Chakraborty, R.H. Nagaraj, A. Biswas, Differential role of arginine mutations on the structure and functions of α-crystallin, Biochimica et Biophysica Acta (BBA) - General Subjects, 1860 (1) (2016) 199-210.
  30. M. Hafizi, N.A. Chebotareva, M. Ghahramani, F. Moosavi-Movahedi, S.H. Khaleghinejad, B.I. Kurganov, A.A. Moosavi-Movahedi, R. Yousefi, Structural and functional studies of D109A human αB-crystallin contributing to the development of cataract and cardiomyopathy diseases, Plos one, 16 (11) (2021) e0260306.
  31. K. Khoshaman, M. Ghahramani, M.B. Shahsavani, A.A. Moosavi-Movahedi, B.I. Kurganov, R. Yousefi, Myopathy-associated G154S mutation causes important changes in the conformational stability, amyloidogenic properties, and chaperone-like activity of human αB-crystallin, Biophysical Chemistry, 282 (2022) 106744.
  32. J.G. Ghosh, S.A. Houck, C.E. Doneanu, J.I. Clark, The β4-β8 groove is an ATP-interactive site in the α crystallin core domain of the small heat shock protein, human αB crystallin, Journal of molecular biology, 364 (3) (2006) 364-75.
  33. A. Biswas, K.P. Das, Role of ATP on the Interaction of α-Crystallin with Its Substrates and Its Implications for the Molecular Chaperone Function, Journal of Biological Chemistry, 279 (41) (2004) 42648-57.
  34. S.K. Nandi, R.B. Nahomi, J. Rankenberg, M.A. Glomb, R.H. Nagaraj, Glycation-mediated inter-protein cross-linking is promoted by chaperone–client complexes of α-crystallin: Implications for lens aging and presbyopia, Journal of Biological Chemistry, 295 (17) (2020) 5701-5716.

Downloads

PDF

Article Details

Volume 4, Issue 2, Year 2022

Published 2022-09-07

Downloads

Download data is not yet available.