Biophysical insights into the interaction of hen egg white lysozyme with therapeutic dye clofazimine: modulation of activity and SDS induced aggregation of model protein

Journal of Biomolecular Structure and Dynamics

Volumn 35, Issue 10, 2017, Pages 2197-2210

  Ajmal, Mohammad Rehan ^a   Chaturvedi, Sumit Kumar ^a   Zaidi, Nida ^a   Alam, Parvez ^a   Zaman, Masihuz ^a   Siddiqi, Mohammad Khursheed ^a   Nusrat, Saima ^a   Jamal, Mohammad Sarwar ^b   Mahmoud, Mohamed H ^c,d   Badr, Gamal ^e   Khan, Rizwan Hasan ^a  

^a ALIGARH MUSLIM UNIVERSITY   (India)

^b KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

^d NATIONAL RESEARCH CENTRE   (Egypt)

^e Assiut University   (Egypt)

Author keywords

binding; clofazimine; fluorescence; hen egg white lysozyme; Thioflavin T

Indexed keywords

CLOFAZIMINE; DODECYL SULFATE SODIUM; HEN EGG WHITE LYSOZYME; LYSOZYME; UNCLASSIFIED DRUG; AMYLOID; EGG WHITE; FLUORESCENT DYE; HEN EGG LYSOZYME; LEPROSTATIC AGENT; PROTEIN AGGREGATE; PROTEIN BINDING; THIAZOLE DERIVATIVE; THIOFLAVINE;

ARTICLE; BINDING AFFINITY; BIOPHYSICS; CONTROLLED STUDY; DRUG DETERMINATION; DRUG PROTEIN BINDING; FLUORESCENCE SPECTROSCOPY; HYDROGEN BOND; HYDROPHOBICITY; PHOTON CORRELATION SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN SECONDARY STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY; ALPHA HELIX; ANIMAL; ANTAGONISTS AND INHIBITORS; BETA SHEET; BINDING SITE; CHEMICAL PHENOMENA; CHEMISTRY; CHICKEN; MOLECULAR DOCKING; PROTEIN DOMAIN;

AMYLOID; ANIMALS; BINDING SITES; CHICKENS; CLOFAZIMINE; EGG WHITE; FLUORESCENT DYES; HYDROGEN BONDING; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LEPROSTATIC AGENTS; MOLECULAR DOCKING SIMULATION; MURAMIDASE; PROTEIN AGGREGATES; PROTEIN BINDING; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN CONFORMATION, BETA-STRAND; PROTEIN INTERACTION DOMAINS AND MOTIFS; SODIUM DODECYL SULFATE; THIAZOLES;

EID: 84982801373     PISSN: 07391102     EISSN: 15380254     Source Type: Journal    
DOI: 10.1080/07391102.2016.1211552     Document Type: Article

References (64)

1. Abdelhameed, A. S., Ajmal, M. R., Ponnusamy, K., Subbarao, N., & Khan, R. H., (2016). Interaction of the recently approved anticancer drug nintedanib with human acute phase reactant α 1-acid glycoprotein. Journal of Molecular Structure, 1115, 171–179.10.1016/j.molstruc.2016.02.048
2. Abdelhameed, A. S., Alam, P., & Khan, R. H., (2015). Binding of Janus Kinase Inhibitor Tofacitinib with Human serum Albumin:Multi-technique approach. Journal of Biomolecular Structure and Dynamics (just-accepted), 1–25. doi:10.1080/07391102.2015.1104522
3. Ahmad, E., Rabbani, G., Zaidi, N., Ahmad, B., & Khan, R. H., (2012). Pollutant-induced modulation in conformation and beta-lactamase activity of human serum albumin. PLoS One, 7, e38372.10.1371/journal.pone.0038372
4. Ahmad, E., Rabbani, G., Zaidi, N., Khan, M. A., Qadeer, A., Ishtikhar, M., … Khan, R. H., (2013). Revisiting ligand-induced conformational changes in proteins:Essence, advancements, implications and future challenges. Journal of Biomolecular Structure and Dynamics, 31, 630–648.10.1080/07391102.2012.706081
5. Ajmal, M. R., Abdelhameed, A. S., Alam, P., & Khan, R. H., (2016). Interaction of new kinase inhibitors cabozantinib and tofacitinib with human serum alpha-1 acid glycoprotein. A comprehensive spectroscopic and molecular Docking approach. Spectrochimica Acta Part A:Molecular and Biomolecular Spectroscopy, 159, 199–208.
6. Ajmal, M. R., Nusrat, S., Alam, P., Zaidi, N., Badr, G., Mahmoud, M. H., … Khan, R. H., (2016). Differential mode of interaction of ThioflavinT with native β structural motif in human α 1-acid glycoprotein and cross beta sheet of its amyloid:Biophysical and molecular docking approach. Journal of Molecular Structure, 1117, 208–217.10.1016/j.molstruc.2016.03.081
7. Ajmal, M. R., Zaidi, N., Alam, P., Nusrat, S., Siddiqi, M. K., Badr, G., … Khan, R. H., (2015). Insight into the Interaction of antitubercular and anticancer compound Clofazimine with Human Serum Albumin:Spectroscopy and molecular modelling. Journal of Biomolecular Structure and Dynamics (just-accepted), 1–42. doi:10.1080/07391102.2015.1132258
8. Alam, P., Abdelhameed, A. S., Rajpoot, R. K., & Khan, R. H., (2016). Interplay of multiple interaction forces:Binding of tyrosine kinase inhibitor nintedanib with human serum albumin. Journal of Photochemistry and Photobiology B:Biology, 157, 70–76.10.1016/j.jphotobiol.2016.02.009
9. Alam, P., Chaturvedi, S. K., Anwar, T., Siddiqi, M. K., Ajmal, M. R., Badr, G., … Khan, R. H., (2015). Biophysical and molecular docking insight into the interaction of cytosine β-D arabinofuranoside with human serum albumin. Journal of Luminescence, 164, 123–130.10.1016/j.jlumin.2015.03.011
10. Alam, P., Chaturvedi, S. K., Siddiqi, M. K., Rajpoot, R. K., Ajmal, M. R., Zaman, M., & Khan, R. H., (2016). Vitamin k3 inhibits protein aggregation:Implication in the treatment of amyloid diseases. Scientific Reports, 6, 1–11.
11. Alam, P., Naseem, F., Abdelhameed, A. S., & Khan, R. H., (2015). Effect of galactose on acid induced molten globule state of Soybean Agglutinin:Biophysical approach. Journal of Molecular Structure, 1099, 149–153.10.1016/j.molstruc.2015.05.061
12. Berne, B. J., & Pecora, R., (2000). Dynamic light scattering:With applications to chemistry, biology, and physics. New York, NY:Courier Corporation.
13. Bi, S., Ding, L., Tian, Y., Song, D., Zhou, X., Liu, X., & Zhang, H., (2004). Investigation of the interaction between flavonoids and human serum albumin. Journal of Molecular Structure, 703, 37–45.10.1016/j.molstruc.2004.05.026
14. Boasson, E. H., (1938). On the bacteriolysis by lysozyme. The Journal of Immunology, 34, 281–293.
15. Chaturvedi, S. K., Khan, J. M., Siddiqi, M. K., Alam, P., & Khan, R. H., (2016). Comparative insight into surfactants mediated amyloidogenesis of lysozyme. International Journal of Biological Macromolecules, 83, 315–325.10.1016/j.ijbiomac.2015.11.053
16. Chaturvedi, S. K., Zaidi, N., Alam, P., Khan, J. M., Qadeer, A., Siddique, I. A., … Khan, R. H., (2015). Unraveling comparative anti-amyloidogenic behavior of pyrazinamide and D-cycloserine:A mechanistic biophysical insight. PLoS One, 10, e0136528.10.1371/journal.pone.0136528
17. Chen, Y.-H., Yang, J. T., & Martinez, H. M., (1972). Determination of the secondary structures of proteins by circular dichroism and optical rotatory dispersion. Biochemistry, 11, 4120–4131.10.1021/bi00772a015
18. Cholo, M. C., Steel, H. C., Fourie, P. B., Germishuizen, W. A., & Anderson, R., (2012). Clofazimine:Current status and future prospects. Journal of Antimicrobial Chemotherapy, 67, 290–298.
19. Cohen, S. I. A., Linse, S., Luheshi, L. M., Hellstrand, E., White, D. A., Rajah, L., … Knowles, T. P. J., (2013). Proliferation of amyloid-beta 42 aggregates occurs through a secondary nucleation mechanism. Proceedings of the National Academy of Sciences, 110, 9758–9763.10.1073/pnas.1218402110
20. Derde, M., Lechevalier, V., Guérin-Dubiard, C., Cochet, M.-F., Jan, S., Baron, F., … Nau, F., (2013). Hen egg white lysozyme permeabilizes escherichia coli outer and inner membranes. Journal of Agricultural and Food Chemistry, 61, 9922–9929.10.1021/jf4029199
21. Dobson, C. M., Evans, P. A., & Radford, S. E., (1994). Understanding how proteins fold:The lysozyme story so far. Trends in Biochemical Sciences, 19, 31–37.10.1016/0968-0004(94)90171-6
22. Duman, O., Tunç, S., & Bozoğlan, B. K., (2013). Characterization of the binding of metoprolol tartrate and guaifenesin drugs to human serum albumin and human hemoglobin proteins by fluorescence and circular dichroism spectroscopy. Journal of Fluorescence, 23, 659–669.10.1007/s10895-013-1177-y
23. Fleming, A., (1922). On a remarkable bacteriolytic element found in tissues and secretions. Proceedings of the Royal Society of London B:Biological Sciences, 93, 306–317.10.1098/rspb.1922.0023
24. Förster, T., (1948). Zwischenmolekulare energiewanderung und fluoreszenz [Intermolecular energy transfer and fluorescence]. Annalen der Physik, 437, 55–75.10.1002/(ISSN)1521-3889
25. He, W., Li, Y., Xue, C., Hu, Z., Chen, X., & Sheng, F., (2005). Effect of Chinese medicine alpinetin on the structure of human serum albumin. Bioorganic & Medicinal Chemistry, 13, 1837–1845.
26. Hou, H.-N., Qi, Z.-D., OuYang, Y.-W., Liao, F.-L., Zhang, Y., & Liu, Y., (2008). Studies on interaction between Vitamin B12 and human serum albumin. Journal of Pharmaceutical and Biomedical Analysis, 47, 134–139.10.1016/j.jpba.2007.12.029
27. Ishtikhar, M., Khan, A., Chang, C.-K., Lin, L. T.-W., Wang, S. S. S., & Khan, R. H., (2015). Effect of Guanidine hydrochloride and Urea on the interaction of 6-thioguanine with human serum albumin:A spectroscopic and molecular dynamics based study. Journal of Biomolecular Structure and Dynamics (just-accepted), 1–38. doi:10.1080/07391102.2015.1054433
28. Jiang, C.-Q., & Wang, T., (2004). Study of the interactions between tetracycline analogues and lysozyme. Bioorganic & Medicinal Chemistry, 12, 2043–2047.
29. Kelly, S. M., Jess, T. J., & Price, N. C., (2005). How to study proteins by circular dichroism. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics, 1751, 119–139.10.1016/j.bbapap.2005.06.005
30. Khan, J. M., Chaturvedi, S. K., Rahman, S. K., Ishtikhar, M., Qadeer, A., Ahmad, E., & Khan, R. H., (2014). Protonation favors aggregation of lysozyme with SDS. Soft Matter, 10, 2591–2599.10.1039/c3sm52435c
31. Khan, J. M., Qadeer, A., Chaturvedi, S. K., Ahmad, E., Rehman, S. A. A., Gourinath, S., & Khan, R. H., (2012). SDS can be utilized as an amyloid inducer:A case study on diverse proteins. PLoS One, 7, e29694.10.1371/journal.pone.0029694
32. Kornhuber, J., Muehlbacher, M., Trapp, S., Pechmann, S., Friedl, A., Reichel, M., … Spitzer, G. M., (2011). Identification of novel functional inhibitors of acid sphingomyelinase. PLoS One, 6, e23852.10.1371/journal.pone.0023852
33. Lakowicz, J. R., (2013). Principles of fluorescence spectroscopy. New York, NY:Springer Science & Business Media.
34. Lakowicz, J. R., & Weber, G., (1973). Quenching of fluorescence by oxygen. Probe for structural fluctuations in macromolecules. Biochemistry, 12, 4161–4170.10.1021/bi00745a020
35. Li, D., Zhang, T., Xu, C., & Ji, B., (2011). Effect of pH on the interaction of baicalein with lysozyme by spectroscopic approaches. Journal of Photochemistry and Photobiology B:Biology, 104, 414–424.10.1016/j.jphotobiol.2011.04.009
36. Lipinski, C. A., (2004). Lead-and drug-like compounds:The rule-of-five revolution. Drug Discovery Today:Technologies, 1, 337–341.10.1016/j.ddtec.2004.11.007
37. Lipinski, C. A., Lombardo, F., Dominy, B. W., & Feeney, P. J., (2012). Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Advanced Drug Delivery Reviews, 64, 4–17.10.1016/j.addr.2012.09.019
38. Loeb, M. B., Molloy, D. W., Smieja, M., Standish, T., Goldsmith, C. H., Mahony, J., … Davidson, W., (2004). A randomized, controlled trial of doxycycline and rifampin for patients with alzheimer’s disease. Journal of the American Geriatrics Society, 52, 381–387.10.1111/jgs.2004.52.issue-3
39. Masschalck, B., & Michiels, C. W., (2003). Antimicrobial properties of lysozyme in relation to foodborne vegetative bacteria. Critical Reviews in Microbiology, 29, 191–214.10.1080/713610448
40. Merkel, R., Nassoy, P., Leung, A., Ritchie, K., & Evans, E., (1999). Energy landscapes of receptor–ligand bonds explored with dynamic force spectroscopy. Nature, 397, 50–53.10.1038/16219
41. Min, J., Meng-Xia, X., Dong, Z., Yuan, L., Xiao-Yu, L., & Xing, C., (2004). Spectroscopic studies on the interaction of cinnamic acid and its hydroxyl derivatives with human serum albumin. Journal of Molecular Structure, 692, 71–80.10.1016/j.molstruc.2004.01.003
42. Muthu, S. A., Mothi, N., Shiriskar, S. M., Pissurlenkar, R. R. S., Kumar, A., & Ahmad, B., (2016). Physical basis for the ofloxacin-induced acceleration of lysozyme aggregation and polymorphism in amyloid fibrils. Archives of Biochemistry and Biophysics, 592, 10–19.10.1016/j.abb.2016.01.005
43. Osserman, E. F., & Lawlor, D. P., (1966). Serum and urinary lysozyme (muramidase) in monocytic and monomyelocytic leukemia. Journal of Experimental Medicine, 124, 921–952.10.1084/jem.124.5.921
44. Perillie, P. E., Kaplan, S. S., Lefkowitz, E., Rogaway, W., & Finch, S. C., (1968). Studies of muramidase (lysozyme) in leukemia. JAMA, 203, 317–322.10.1001/jama.1968.03140050001001
45. Petrônio, M. S., & Ximenes, V. F., (2012). Effects of oxidation of lysozyme by hypohalous acids and haloamines on enzymatic activity and aggregation. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics, 1824, 1090–1096.10.1016/j.bbapap.2012.06.013
46. Redfield, C., & Dobson, C. M., (1990). Proton NMR studies of human lysozyme:Spectral assignment and comparison with hen lysozyme. Biochemistry, 29, 7201–7214.10.1021/bi00483a007
47. Ruberg, F. L., & Berk, J. L., (2012). Transthyretin (TTR) cardiac amyloidosis. Circulation, 126, 1286–1300.10.1161/CIRCULATIONAHA.111.078915
48. Sandhya, B., Hegde, A. H., & Seetharamappa, J., (2013). Elucidation of binding mechanism and identification of binding site for an anti HIV drug, stavudine on human blood proteins. Molecular Biology Reports, 40, 3817–3827.10.1007/s11033-012-2460-8
49. Sarkar, N., Kumar, M., & Dubey, V. K., (2011a). Effect of sodium tetrathionate on amyloid fibril:Insight into the role of disulfide bond in amyloid progression. Biochimie, 93, 962–968.10.1016/j.biochi.2011.02.006
50. Sarkar, N., Kumar, M., & Dubey, V. K., (2011b). Exploring possibility of promiscuity of amyloid inhibitor:Studies on effect of selected compounds on folding and amyloid formation of proteins. Process Biochemistry, 46, 1179–1185.10.1016/j.procbio.2011.02.010
51. Sirangelo, I., & Irace, G., (2010). Inhibition of aggregate formation as therapeutic target in protein misfolding diseases:Effect of tetracycline and trehalose. Expert Opinion on Therapeutic Targets, 14, 1311–1321.10.1517/14728222.2010.531012
52. Smolelis, A. N., & Hartsell, S. E., (1952). Factors affecting the lytic activity of lysozyme. Journal of Bacteriology, 63, 665–674.
53. Stryer, L., & Haugland, R. P., (1967). Energy transfer:A spectroscopic ruler. Proceedings of the National Academy of Sciences, 58, 719–726.10.1073/pnas.58.2.719
54. Sund, H., & Blauer, G., (1975). Protein-ligand interactions. New York, NY:Walter de Gruyter Berlin.
55. Thompson, R., (1940). Lysozyme and its relation to the antibacterial properties of various tissues and secretions. Arch. Path, 30, 1096–1134.
56. Tomiyama, T., Shoji, A., Kataoka, K.-I., Suwa, Y., Asano, S., Kaneko, H., & Endo, N., (1996). Inhibition of amyloid protein aggregation and neurotoxicity by rifampicin its possible function as a hydroxyl radical scavenger. Journal of Biological Chemistry, 271, 6839–6844.
57. Ware, W. R., (1962). Oxygen quenching of fluorescence in solution:An experimental study of the diffusion process. The Journal of Physical Chemistry, 66, 455–458.10.1021/j100809a020
58. Xie, M.-X., Long, M., Liu, Y., Qin, C., & Wang, Y.-D., (2006). Characterization of the interaction between human serum albumin and morin. Biochimica et Biophysica Acta (BBA)-General Subjects, 1760, 1184–1191.10.1016/j.bbagen.2006.03.026
59. Yan, Y., & Marriott, G., (2003). Analysis of protein interactions using fluorescence technologies. Current Opinion in Chemical Biology, 7, 635–640.10.1016/j.cbpa.2003.08.017
60. Zaidi, N., Ahmad, E., Rehan, M., Rabbani, G., Ajmal, M. R., Zaidi, Y., … Khan, R. H., (2013). Biophysical insight into furosemide binding to human serum albumin:A study to unveil its impaired albumin binding in uremia. The Journal of Physical Chemistry B, 117, 2595–2604.10.1021/jp3069877
61. Zaidi, N., Ajmal, M. R., Rabbani, G., Ahmad, E., & Khan, R. H., (2013). A comprehensive insight into binding of hippuric acid to human serum albumin:A study to uncover its impaired elimination through hemodialysis. PLoS One, 8, e71422.10.1371/journal.pone.0071422
62. Zaidi, N., Nusrat, S., Zaidi, F. K., & Khan, R. H., (2014). pH-dependent differential interacting mechanisms of sodium dodecyl sulfate with bovine serum fetuin:A biophysical insight. The Journal of Physical Chemistry B, 118, 13025–13036.10.1021/jp501515g
63. Zhang, J., Sun, H.-H., Zhang, Y.-Z., Yang, L.-Y., Dai, J., & Liu, Y., (2012). Interaction of human serum albumin with indomethacin:Spectroscopic and molecular modeling studies. Journal of Solution Chemistry, 41, 422–435.10.1007/s10953-012-9809-4
64. Zhu, J., Li, D., Jin, J., & Wu, L., (2007). Binding analysis of farrerol to lysozyme by spectroscopic methods. Spectrochimica Acta Part A:Molecular and Biomolecular Spectroscopy, 68, 354–359.10.1016/j.saa.2006.11.045