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Research Articles

Dynamic and structural insights into tick serpin from Ixodes ricinus

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Pages 2296-2303 | Received 01 Mar 2019, Accepted 04 Jun 2019, Published online: 19 Jun 2019

References

  • Andersen, O. J., Risør, M. W., Poulsen, E. C., Nielsen, N. C., Miao, Y., Enghild, J. J., & Schiøtt, B. (2017). Reactive center loop insertion in alpha-1-antitrypsin captured by accelerated molecular dynamics simulation. Biochemistry, 56(4), 634–646. doi:10.1021/acs.biochem.6b00839
  • Awang, T., Wiriyatanakorn, N., Saparpakorn, P., Japrung, D., & Pongprayoon, P. (2017). Understanding the effects of two bound glucose in Sudlow site I on structure and function of human serum albumin: Theoretical studies. Journal of Biomolecular Structure and Dynamics, 35(4), 781–790. doi:10.1080/07391102.2016.1160841
  • Baicharoen, A., Vijayan, R., & Pongprayoon, P. (2018). Structural insights into betaine aldehyde dehydrogenase (BADH2) from Oryza sativa explored by modeling and simulations. Scientific Report, 8(1), 12892. doi:10.1038/s41598-018-31204-z
  • Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. Journal of Chemical Physics, 81(8), 3684–3690. doi:10.1063/1.448118
  • Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., … Schwede, T. (2014). SWISS-MODEL: Modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research, 42(W1), W252–W258. doi:10.1093/nar/gku340
  • Bottomley, S. P., Hopkins, P. C., & Whisstock, J. C. (1998). Alpha 1-antitrypsin polymerisation can occur by both loop A and C sheet mechanisms. Biochemical and Biophysical Research Communications, 251(1), 1–5. doi:10.1006/bbrc.1998.9254
  • Cazzolli, G., Wang, F., Beccara, S. A., Gershenson, A., Faccioli, P., & Wintrode, P. L. (2014). Serpin latency transition at atomic resolution. Proceedings of the National Academy of Sciences of the United States of America, 111(43), 15414–15419. doi:10.1073/pnas.1407528111
  • Chmelar, J., Kotal, J., Langhansova, H., & Kotsyfakis, M. (2017). Protease inhibitors in tick saliva: The role of serpins and cystatins in tick–host–pathogen interaction. Frontiers in Cellular and Infection Microbiology, 7, 216. doi:10.3389/fcimb.2017.00216
  • Chmelar, J., Oliveira, C. J., Rezacova, P., Francischetti, I. M. B., Kovarova, Z., Pejler, G., … Kotsyfakis, M. (2011). A tick salivary protein targets cathepsin G and chymase and inhibits host inflammation and platelet aggregation. Blood, 117(2), 736–744. doi:10.1182/blood-2010-06-293241
  • Crowther, D. C., Serpell, L. C., Dafforn, T. R., Gooptu, B., & Lomas, D. A. (2003). Nucleation of alpha 1-antichymotrypsin polymerization. Biochemistry, 42(8), 2355–2363. doi:10.1021/bi0259305
  • Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems. Journal of Chemical Physics, 98(12), 10089–10092. doi:10.1063/1.464397
  • de la Fuente, J., Rodrı́guez, M., Montero, C., Redondo, M., Garcı́a-Garcı́a, J. C., Méndez, L., … Lleonart, R., (1999). Vaccination against ticks (Boophilus spp.): The experience with the Bm86-based vaccine Gavac. Genetic Analysis, 15(3-5), 143–148. doi:10.1016/S1050-3862(99)00018-2
  • De Meneghi, D., Stachurski, F., & Adakal, H. (2016). Experiences in tick control by acaricide in the traditional cattle sector in Zambia and Burkina Faso: Possible environmental and public health implications. Frontiers in Public Health, 4, 239. doi:10.3389/fpubh.2016.00239
  • Eisen, R. J., Kugeler, K. J., Eisen, L., Beard, C. B., & Paddock, C. D. (2017). Tick-borne zoonoses in the United States: Persistent and emerging threats to human health. ILAR Journal, 58(3), 319–335. doi:10.1093/ilar/ilx005
  • Ellisdon, A. M., Zhang, Q., Henstridge, M. A., Johnson, T. K., Warr, C. G., Law, R. H., & Whisstock, J. C. (2014). High resolution structure of cleaved serpin 42 Da from Drosophila melanogaster. BMC Structural Biology, 14(1), 14. doi:10.1186/1472-6807-14-14
  • Eswar, N., Webb, B., Marti-Renom, M. A., Madhusudhan, M. S., Eramian, D., Shen, M. Y., … Sali, A. (2006). Comparative protein structure modeling using Modeller. Current Protocols in Bioinformatics, 15, 5–6. doi:10.1002/0471250953.bi0506s15
  • Eyes, T. J., Austerberry, J. I., Dearman, R. J., Johannissen, L. O., Kimber, I., Smith, N., … Derrick, J. P. (2019). Identification of B cell epitopes enhanced by protein unfolding and aggregation. Molecular Immunology, 105, 181–189. doi:10.1016/j.molimm.2018.11.020
  • Gerbod-Giannone, M. C., Del Castillo-Olivares, A., Janciauskiene, S., Gil, G., & Hylemon, P. B. (2002). Suppression of cholesterol 7alpha-hydroxylase transcription and bile acid synthesis by an alpha1-antitrypsin peptide via interaction with alpha1-fetoprotein transcription factor. Journal of Biological Chemistry, 277(45), 42973–42980. doi:10.1074/jbc.M205089200
  • Gettins, P. G. W. (2002). Serpin structure, mechanism, and function. Chemical Reviews, 102(12), 4751–4803. doi:10.1021/cr010170 + 
  • Gooptu, B., & Lomas, D. A. (2009). Conformational pathology of the serpins: Themes, variations, and therapeutic strategies. Annual Review of Biochemistry, 78(1), 147–176. doi:10.1146/annurev.biochem.78.082107.133320
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD – Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. doi:10.1016/0263-7855(96)00018-5
  • Ibelli, A. M. G., Kim, T. K., Hill, C. C., Lewis, L. A., Bakshi, M., Miller, S., … Mulenga, A. (2014). A blood meal-induced Ixodes scapularis tick saliva serpin inhibits trypsin and thrombin, and interferes with platelet aggregation and blood clotting. International Journal of Parasitology, 44(6), 369–379. doi:10.1016/j.ijpara.2014.01.010
  • James, E. L., & Bottomley, S. P. (1998). The mechanism of alpha 1-antitrypsin polymerization probed by fluorescence spectroscopy. Archives of Biochemistry and Biophysics, 356(2), 296–300. doi:10.1006/abbi.1998.0751
  • Janciauskiene, S., Moraga, F., & Lindgren, S. (2001). C-terminal fragment of alpha1-antitrypsin activates human monocytes to a pro-inflammatory state through interactions with the CD36 scavenger receptor and LDL receptor. Atherosclerosis, 158(1), 41–51. doi:10.1016/S0021-9150(00)00767-X
  • Janciauskiene, S., & Welte, T. (2016). Well-known and less well-known functions of alpha-1 antitrypsin. Its role in chronic obstructive pulmonary disease and other disease developments. Annals of the American Thoracic Society, 13(Suppl_4), S280–S288. doi:10.1513/AnnalsATS.201507-468KV
  • Jiang, H., Mulnix, A. B., & Kanost, M. R. (1995). Expression and characterization of recombinant Manduca sexta serpin-1B and site-directed mutants that change its inhibitory selectivity. Insect Biochemistry and Molecular Biology, 25(10), 1093–1100. doi:10.1016/0965-1748(95)00042-9
  • Jittapalapong, S., Jansawan, W., Barriga, O. O., & Stich, R. W. (2004). Reduced incidence of Babesia bigemina infection in cattle immunized against the cattle tick, Boophilus microplus. Annals of the New York Academy of Sciences, 1026, 312–318. doi:10.1196/annals.1307.048
  • Jittapalapong, S., Jansawan, W., Gingkaew, A., Barriga, O. O., & Stich, R. W. (2004). Protection of dairy cows immunized with tick tissues against natural Boophilus microplus infestations in Thailand. Annals of the New York Academy of Sciences, 1026, 289–297. doi:10.1196/annals.1307.045
  • Jittapalapong, S., Kaewhom, P., Kengradomkij, C., Saratapan, N., Canales, M., de la Fuente, J., & Stich, R. W. (2010). Humoral immune response of dairy cattle immunized with rBm95 (KU-VAC1) derived from Thai Rhipicephalus microplus. Transboundary and Emerging Diseases, 57(1-2), 91–95. doi:10.1111/j.1865-1682.2010.01106.x
  • Jittapalapong, S., Kaewhom, P., Pumhom, P., Canales, M., de la Fuente, J., & Stich, R. W. (2010). Immunization of rabbits with recombinant serine protease inhibitor reduces the performance of adult female Rhipicephalus microplus. Transboundary and Emerging Diseases, 57(1–2), 103–106. doi:10.1111/j.1865-1682.2010.01108.x
  • Jittapalapong, S., Phichitrasilp, T., Chanphao, H., Rerkamnuychoke, W., & Stich, R. W. (2008). Immunization with tick salivary gland extracts impact on salivary gland ultrastructure in Rhipicephalus (Boophilus) microplus collected from immunized naturally infested cattle. Animal Biodiversity and Emerging Diseases: Prediction and Prevention, 1149, 200–204. [Mismatch] doi:10.1196/annals.1428.083
  • Jongejan, F., & Uilenberg, G. (2004). The global importance of ticks. Parasitology, 129 Suppl(Suppl), S3–S14.
  • Kaewhom, P., Sirinarumitr, T., Chantakru, S., & Jittapalapong, S. (2009). Humoral antibody responses of rabbits immunized with anti-tick vaccine using SERPIN recombinant protein. Kasetsart Journal, 43, 69–76.
  • Kaewhom, P., Sirinarumitr, T., Jantakru, S., & Jittapalapong, S. (2007). Molecular cloning of serine proteinase inhibitors (SERPINS) gene from salivary gland of cattle tick (Boophilus microplus) in Thailand. Kasetsart Journal, 41, 74–80.
  • Kaewhom, P., Sirinarumitr, T., Stich, R. W., & Jittapalapong, S. (2008). Molecular cloning and sequencing analysis of Bm91 (angiotensin converting enzymes) cDNA from salivary glands of Thai Cattle ticks, Boophilus microplus. Infection Genetics and Evolution, 8(4), S31–S32.
  • Kaewhom, P., Stich, R. W., Needham, G. R., & Jittapalapong, S. (2008). Molecular analysis of calreticulin expressed in salivary glands of Rhipicephalus (Boophilus) microplus indigenous to Thailand. Annals of the New York Academy of Sciences, 1149, 53–57. doi:10.1196/annals.1428.033
  • Kanost, M. R. (1999). Serine proteinase inhibitors in arthropod immunity. Developmental & Comparative Immunology, 23(4-5), 291–301. doi:10.1016/S0145-305X(99)00012-9
  • Kay, B. H., & Kemp, D. H. (1994). Vaccines against arthropods. The American Journal of Tropical Medicine and Hygiene, 50(6 Suppl), 87–96. doi:10.4269/ajtmh.1994.50.87
  • Lindahl, E., Hess, B., & van der Spoel, D. (2001). GROMACS 3.0: A package for molecular simulation and trajectory analysis. Journal of Molecular Modeling, 7(8), 306–317. doi:10.1007/s008940100045
  • Marszal, E., Danino, D., & Shrake, A. (2003). A novel mode of polymerization of alpha(1)-proteinase inhibitor. Journal of Biological Chemistry, 278(22), 19611–19618. doi:10.1074/jbc.M210720200
  • Meekins, D. A., Kanost, M. R., & Michel, K. (2017). Serpins in arthropod biology. Seminars in Cell and Developmental Biology, 62, 105–119. doi:10.1016/j.semcdb.2016.09.001
  • Mulenga, A., Khumthong, R., & Chalaire, K. C. (2009). Ixodes scapularis tick serine proteinase inhibitor (serpin) gene family; annotation and transcriptional analysis. BMC Genomics, 10, 217. doi:10.1186/1471-2164-10-217
  • Noto, R., Randazzo, L., Raccosta, S., Caccia, S., Moriconi, C., Miranda, E., … Manno, M. (2015). The stability and activity of human neuroserpin are modulated by a salt bridge that stabilises the reactive centre loop. Scientific Reports, 5,13666. ARTN 13666 doi:10.1038/srep13666
  • Noto, R., Santangelo, M. G., Levantino, M., Cupane, A., Mangione, M. R., Parisi, D., … Martorana, V. (2015). Functional and dysfunctional conformers of human neuroserpin characterized by optical spectroscopies and molecular dynamics. Biochimica et Biophysica Acta, 1854(2), 110–117. doi:10.1016/j.bbapap.2014.10.002
  • Opdebeeck, J. P. (1994). Vaccines against blood-sucking arthropods. Veterinary Parasitology, 54(1–3), 205–222.
  • Petersen, M., Madsen, J. B., Jorgensen, T. J. D., & Trelle, M. B. (2017). Conformational preludes to the latency transition in PAI-1 as determined by atomistic computer simulations and hydrogen/deuterium-exchange mass spectrometry. Scientific Reports, 7, 6636. ARTN 6636 doi:10.1038/s41598-017-06290-0
  • Potempa, J., Korzus, E., & Travis, J. (1994). The serpin superfamily of proteinase inhibitors: Structure, function, and regulation. Journal of Biological Chemistry, 269(23), 15957–15960.
  • Rodriguez-Valle, M., Xu, T., Kurscheid, S., & Lew-Tabor, A. E. (2015). Rhipicephalus microplus serine protease inhibitor family: Annotation, expression and functional characterisation assessment. Parasites & Vectors, 8, 7. ARTN 7 doi:10.1186/s13071-014-0605-4
  • Rosario-Cruz, R., Almazan, C., Miller, R. J., Dominguez-Garcia, D. I., Hernandez-Ortiz, R., & de la Fuente, J. (2009). Genetic basis and impact of tick acaricide resistance. Frontiers in Bioscience (Landmark Ed), 14, 2657–2665.
  • Ryu, S. E., Choi, H. J., Kwon, K. S., Lee, K. N., & Yu, M. H. (1996). The native strains in the hydrophobic core and flexible reactive loop of a serine protease inhibitor: Crystal structure of an uncleaved alpha1-antitrypsin at 2.7 A. Structure, 4(10), 1181–1192. doi:10.1016/S0969-2126(96)00126-8
  • Samykannu, G., Vijayababu, P., Antonyraj, C. B., Perumal, P., Narayanan, S., Basheer Ahamed, S. I., & Natarajan, J. (2019). In silico characterization of B cell and T cell epitopes for subunit vaccine design of Salmonella typhi PgtE: A molecular dynamics simulation approach. Journal of Computational Biology, 26(2), 105–116. doi:10.1089/cmb.2018.0010
  • Sprong, H., Azagi, T., Hoornstra, D., Nijhof, A. M., Knorr, S., Baarsma, M. E., & Hovius, J. W. (2018). Control of Lyme borreliosis and other Ixodes ricinus-borne diseases. Parasites & Vectors, 11(1), 145. doi:10.1186/s13071-018-2744-5
  • Subramaniyam, D., Glader, P., von Wachenfeldt, K., Burneckiene, J., Stevens, T., & Janciauskiene, S. (2006). C-36 peptide, a degradation product of alpha1-antitrypsin, modulates human monocyte activation through LPS signaling pathways. The International Journal of Biochemistry & Cell Biology, 38(4), 563–575. doi:10.1016/j.biocel.2005.09.021
  • Sugino, M., Imamura, S., Mulenga, A., Nakajima, M., Tsuda, A., Ohashi, K., & Onuma, M. (2003). A serine proteinase inhibitor (serpin) from Ixodid tick Haemaphysalis longicornis; cloning and preliminary assessment of its suitability as a candidate for a tick vaccine. Vaccine, 21(21–22), 2844–2851. doi:10.1016/S0264-410X(03)00167-1
  • Tirloni, L., Seixas, A., Mulenga, A., da Silva Vaz, I., & Termignoni, C. (2014). A family of serine protease inhibitors (serpins) in the cattle tick Rhipicephalus (Boophilus) microplus. Experimental Parasitology, 137, 25–34. doi:10.1016/j.exppara.2013.12.001
  • van Gent, D., Sharp, P., Morgan, K., & Kalsheker, N. (2003). Serpins: Structure, function and molecular evolution. The International Journal of Biochemistry & Cell Biology, 35(11), 1536–1547. doi:10.1016/S1357-2725(03)00134-1
  • Wang, F., Orioli, S., Ianeselli, A., Spagnolli, G., A Beccara, S., Gershenson, A., … Wintrode, P. L. (2018). All-atom simulations reveal how single-point mutations promote serpin misfolding. Biophysical Journal, 114(9), 2083–2094. doi:10.1016/j.bpj.2018.03.027
  • Wardell, M. R., Abrahams, J. P., Bruce, D., Skinner, R., & Leslie, A. G. (1993). Crystallization and preliminary X-ray diffraction analysis of two conformations of intact human antithrombin. Journal of Molecular Biology, 234(4), 1253–1258. doi:10.1006/jmbi.1993.1676
  • Xu, G., Fang, Q. Q., Keirans, J. E., & Durden, L. A. (2003). Molecular phylogenetic analyses indicate that the Ixodes ricinus complex is a paraphyletic group. Journal of Parasitology, 89(3), 452–457. doi:10.1645/0022-3395(2003)089
  • Yamasaki, M., Sendall, T. J., Harris, L. E., Lewis, G. M. W., & Huntington, J. A. (2010). Loop-sheet mechanism of serpin polymerization tested by reactive center loop mutations. Journal of Biological Chemistry, 285(40), 30752–30758. doi:10.1074/jbc.M110.156042
  • Ziegler, M. E., Chen, T., LeBlanc, J. F., Wei, X., Gjertson, D. W., Li, K.-C., … Reed, E. F. (2011). Apolipoprotein A1 and C-terminal fragment of alpha-1 antichymotrypsin are candidate plasma biomarkers associated with acute renal allograft rejection. Transplantation, 92(4), 388–395. doi:10.1097/TP.0b013e318225db6a

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