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Inhibition of Human Immunodeficiency Type 1 Virus (HIV-1) Life Cycle by Different Egg White Lysozymes

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Abstract

Lysozyme is a relatively small enzyme with different biological activities, which is found in tears, saliva, egg white, and human milk. In the study, the anti-HIV-1 activity of lysozymes purified from quail, Meleagris, and hen egg white has been determined. For this end, a time-of-drug-addition assay was performed to identify the target of anti-HIV-1 agents and for determination of probable anti HIV-1 mechanism of the studied lysozyme, the binding affinity of the lysozymes to the human CD4 receptor was studied by molecular docking method. To define structural differences between studied lysozymes, structural motifs of them were predicted by MEME tool. Quail, hen, and Meleagris lysozymes showed potent anti-HIV-1 activity with EC50 of 7.5, 10, and 55 nM, respectively. The time-of-drug-addition study demonstrated that the inhibitory effect of all purified lysozymes is before HIV-1 infection. The frequency and intensity of CD4 expression in PBMCs decreased in the presence of all mentioned lysozymes. Also, the expression level of C-C chemokine receptor type 5 (CCR5) and chemokine receptor type 4 (CXCR4) on CD4+ T cells was not changed in cells treated with these lysozymes. The results of in silico study confirmed that the binding energy of quail lysozyme with CD4 was more than that of other studied lysozymes. The results revealed that these lysozymes restrict HIV-1 attachment to host cell CD4.

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References

  1. Burley, R. (1989). The avian egg: chemistry and biology.

  2. Feeney, R. E., et al. (1960). The comparative biochemistry of avian egg white proteins. Journal of Biological Chemistry, 235, 2307–2311.

    Article  CAS  Google Scholar 

  3. Ting, B., et al. (2010). Fractionation of egg proteins and peptides for nutraceutical applications. Separation, extraction and concentration processes in the food, beverage and nutraceutical industries. p. 595–618.

  4. Abeyrathne, E., Lee, H., & Ahn, D. (2013). Egg white proteins and their potential use in food processing or as nutraceutical and pharmaceutical agents—a review. Poultry Science, 92(12), 3292–3299. https://doi.org/10.3382/ps.2013-03391.

    Article  CAS  Google Scholar 

  5. Stevens, L. (1991). Egg white proteins. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 100(1), 1–9. https://doi.org/10.1016/0305-0491(91)90076-P.

    Article  CAS  Google Scholar 

  6. Pellegrini, A., et al. (1997). Identification and isolation of a bactericidal domain in chicken egg white lysozyme. Journal of Applied Microbiology, 82(3), 372–378. https://doi.org/10.1046/j.1365-2672.1997.00372.x.

    Article  CAS  Google Scholar 

  7. Mine, Y., Ma, F., & Lauriau, S. (2004). Antimicrobial peptides released by enzymatic hydrolysis of hen egg white lysozyme. Journal of Agricultural and Food Chemistry, 52(5), 1088–1094. https://doi.org/10.1021/jf0345752.

    Article  CAS  Google Scholar 

  8. Lee-Huang, S., Huang, P. L., Sun, Y., Huang, P. L., Kung, H.f., Blithe, D. L., & Chen, H. C. (1999). Lysozyme and RNases as anti-HIV components in β-core preparations of human chorionic gonadotropin. Proceedings of the National Academy of Sciences, 96(6), 2678–2681. https://doi.org/10.1073/pnas.96.6.2678.

  9. Lee-Huang, S., Huang, P. L., & Huang P. (2010). Anti-HIV and anti-tumor peptides and fragments of lysozyme, Google Patents.

  10. Jin, Q., Chen, H., Wang, X., Zhao, L., Xu, Q., Wang, H., Li, G., Yang, X., Ma, H., Wu, H., & Ji, X. (2015). The effects of the recombinant CCR5 T4 lysozyme fusion protein on HIV-1 infection. PLoS One, 10(7), e0131894. https://doi.org/10.1371/journal.pone.0131894.

    Article  Google Scholar 

  11. Lin, K.-C., Wey, M. T., Kan, L. S., & Shiuan, D. (2009). Characterization of the interactions of lysozyme with DNA by surface plasmon resonance and circular dichroism spectroscopy. Applied Biochemistry and Biotechnology, 158(3), 631–641. https://doi.org/10.1007/s12010-008-8348-3.

    Article  CAS  Google Scholar 

  12. Cooke, D. G., & Blackwell, L. F. (2007). Clearing of suspensions of Micrococcus lysodeikticus catalysed by lysozymes from hen, goose, and turkey egg whites, human milk, and phage T4. Assessment of potential as signal generators for homogeneous enzyme immunoassays for urinary steroids. Journal of Immunoassay & Immunochemistry, 28(2), 67–90. https://doi.org/10.1080/15321810701209704.

    Article  CAS  Google Scholar 

  13. Ibrahimi, I. M., Prager, E. M., White, T. J., & Wilson, A. C. (1979). Amino acid sequence of California quail lysozyme. Effect of evolutionary substitutions on the antigenic structure of lysozyme. Biochemistry, 18(13), 2736–2744. https://doi.org/10.1021/bi00580a008.

    Article  CAS  Google Scholar 

  14. Prager, E. M., Arnheim, N., Mross, G. A., & Wilson, A. C. (1972). Amino acid sequence studies on bobwhite quail egg white lysozyme. Journal of Biological Chemistry, 247(9), 2905–2916.

    Article  CAS  Google Scholar 

  15. Liburdi, K., Benucci, I., & Esti, M. (2014). Lysozyme in wine: an overview of current and future applications. Comprehensive Reviews in Food Science and Food Safety, 13(5), 1062–1073. https://doi.org/10.1111/1541-4337.12102.

    Article  CAS  Google Scholar 

  16. Lucotte, G., & Kaminski, M. (1978). Increased stability of a hybrid molecule. Journal of Heredity, 69(5), 354–354. https://doi.org/10.1093/oxfordjournals.jhered.a108968.

    Article  CAS  Google Scholar 

  17. Thammasirirak, S., Preecharram, S., Ponkham, P., Daduang, S., Araki, T., & Svasti, J. (2007). New variant of quail egg white lysozyme identified by peptide mapping. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 147(2), 314–324. https://doi.org/10.1016/j.cbpb.2007.01.019.

    Article  Google Scholar 

  18. Cegielska-Radziejewska, R., Lesnierowski, G., & Kijowski, J. (2009). Antibacterial activity of hen egg white lysozyme modified by thermochemical technique. European Food Research and Technology, 228(5), 841–845. https://doi.org/10.1007/s00217-008-0997-5.

    Article  CAS  Google Scholar 

  19. Cegielska-Radziejewska, R., Lesnierowski, G., Szablewski, T., & Kijowski, J. (2010). Physico-chemical properties and antibacterial activity of modified egg white—lysozyme. European Food Research and Technology, 231(6), 959–964. https://doi.org/10.1007/s00217-010-1347-y.

    Article  CAS  Google Scholar 

  20. Cisani, G., Varaldo, P. E., Ingianni, A., Pompei, R., & Satta, G. (1984). Inhibition of herpes simplex virus-induced cytopathic effect by modified hen egg-white lysozymes. Current Microbiology, 10(1), 35–40. https://doi.org/10.1007/BF01576045.

    Article  CAS  Google Scholar 

  21. Meng, X.-Y., Zhang, H. X., Mezei, M., & Cui, M. (2011). Molecular docking: a powerful approach for structure-based drug discovery. Current Computer-Aided Drug Design, 7(2), 146–157. https://doi.org/10.2174/157340911795677602.

    Article  CAS  Google Scholar 

  22. de Ruyck, J., Brysbaert, G., Blossey, R., & Lensink, M. (2016). Molecular docking as a popular tool in drug design, an in silico travel. Advances and Applications in Bioinformatics and Chemistry: AABC, 9, 1–11. https://doi.org/10.2147/AABC.S105289.

    Article  Google Scholar 

  23. Wang, J., & Hou, T. (2011). Application of molecular dynamics simulations in molecular property prediction. 1. density and heat of vaporization. Journal of Chemical Theory and Computation, 7(7), 2151–2165. https://doi.org/10.1021/ct200142z.

    Article  CAS  Google Scholar 

  24. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227(5259), 680–685. https://doi.org/10.1038/227680a0.

    Article  CAS  Google Scholar 

  25. Shugar, D. (1952). The measurement of lysozyme activity and the ultra-violet inactivation of lysozyme. Biochimica et Biophysica Acta, 8(3), 302–309. https://doi.org/10.1016/0006-3002(52)90045-0.

    Article  CAS  Google Scholar 

  26. Morgan, D. M. (1998). Tetrazolium (MTT) assay for cellular viability and activity. Polyamine Protocols, p. 179–184.

  27. Tao, J., Hu, Q., Yang, J., Li, R., Li, X., Lu, C., Chen, C., Wang, L., Shattock, R., & Ben, K. (2007). In vitro anti-HIV and-HSV activity and safety of sodium rutin sulfate as a microbicide candidate. Antiviral Research, 75(3), 227–233. https://doi.org/10.1016/j.antiviral.2007.03.008.

    Article  CAS  Google Scholar 

  28. Sievers, F., et al. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology, 7(1), 539.

    Article  Google Scholar 

  29. Bailey, T. L., et al. (2009). MEME SUITE: tools for motif discovery and searching. Nucleic Acids Research, p. gkp335.

  30. Maehashi, K., Matano, M., Irisawa, T., Uchino, M., Kashiwagi, Y., & Watanabe, T. (2012). Molecular characterization of goose-and chicken-type lysozymes in emu (Dromaius novaehollandiae): evidence for extremely low lysozyme levels in emu egg white. Gene, 492(1), 244–249. https://doi.org/10.1016/j.gene.2011.10.021.

    Article  CAS  Google Scholar 

  31. Sakurai, N., Wu, J. H., Sashida, Y., Mimaki, Y., Nikaido, T., Koike, K., Itokawa, H., & Lee, K. H. (2004). Anti-AIDS agents. Part 57: Actein, an anti-HIV principle from the rhizome of Cimicifuga racemosa (black cohosh), and the anti-HIV activity of related saponins. Bioorganic & Medicinal Chemistry Letters, 14(5), 1329–1332. https://doi.org/10.1016/j.bmcl.2003.12.035.

    Article  CAS  Google Scholar 

  32. Buonocore, F., Randelli, E., Trisolino, P., Facchiano, A., de Pascale, D., & Scapigliati, G. (2014). Molecular characterization, gene structure and antibacterial activity of a g-type lysozyme from the European sea bass (Dicentrarchus labrax L.) Molecular Immunology, 62(1), 10–18. https://doi.org/10.1016/j.molimm.2014.05.009.

    Article  CAS  Google Scholar 

  33. Hashemi, M. M., Aminlari, M., & Moosavinasab, M. (2014). Preparation of and studies on the functional properties and bactericidal activity of the lysozyme–xanthan gum conjugate. LWT-Food Science and Technology, 57(2), 594–602. https://doi.org/10.1016/j.lwt.2014.01.040.

    Article  CAS  Google Scholar 

  34. Mateus, L., Costa, L., Silva, Y. J., Pereira, C., & Almeida, A. (2014). Effect of lysozyme addition on the activity of phages against Vibrio parahaemolyticus. Aquaculture, 432, 125–129. https://doi.org/10.1016/j.aquaculture.2014.04.037.

    Article  CAS  Google Scholar 

  35. Lambe, T., Leung, J. C. H., Bouriez-Jones, T., Silver, K., Makinen, K., Crockford, T. L., Ferry, H., Forrester, J. V., & Cornall, R. J. (2006). CD4 T cell-dependent autoimmunity against a melanocyte neoantigen induces spontaneous vitiligo and depends upon Fas-Fas ligand interactions. The Journal of Immunology, 177(5), 3055–3062. https://doi.org/10.4049/jimmunol.177.5.3055.

    Article  CAS  Google Scholar 

  36. Kaneda, M., Kato, I., Tominaga, N., Titani, K., & Narita, K. (1969). The amino acid sequence of quail lysozyme. The Journal of Biochemistry, 66(5), 747–749.

    CAS  PubMed  Google Scholar 

  37. Lee-Huang, S., Maiorov, V., Huang, P. L., Ng, A., Lee, H. C., Chang, Y. T., Kallenbach, N., Huang, P. L., & Chen, H. C. (2005). Structural and functional modeling of human lysozyme reveals a unique nonapeptide, HL9, with anti-HIV activity. Biochemistry, 44(12), 4648–4655. https://doi.org/10.1021/bi0477081.

    Article  CAS  Google Scholar 

  38. Hartono, Y. D., Lee, A. N., Lee-Huang, S., & Zhang, D. (2011). Computational study of bindings of HL9, a nonapeptide fragment of human lysozyme, to HIV-1 fusion protein gp41. Bioorganic & Medicinal Chemistry Letters, 21(6), 1607–1611. https://doi.org/10.1016/j.bmcl.2011.01.121.

    Article  CAS  Google Scholar 

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The authors would like to acknowledge the University of Isfahan for the financial support of this study.

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Correspondence to Hassan Mohabatkar.

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Behbahani, M., Nosrati, M. & Mohabatkar, H. Inhibition of Human Immunodeficiency Type 1 Virus (HIV-1) Life Cycle by Different Egg White Lysozymes. Appl Biochem Biotechnol 185, 786–798 (2018). https://doi.org/10.1007/s12010-017-2678-y

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