Anaplasma phagocytophilum MSP4 and HSP70 Proteins Are Involved in Interactions with Host Cells during Pathogen Infection

. 2017 ; 7 () : 307. [epub] 20170705

Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid28725639

Anaplasma phagocytophilum transmembrane and surface proteins play a role during infection and multiplication in host neutrophils and tick vector cells. Recently, A. phagocytophilum Major surface protein 4 (MSP4) and Heat shock protein 70 (HSP70) were shown to be localized on the bacterial membrane, with a possible role during pathogen infection in ticks. In this study, we hypothesized that A. phagocytophilum MSP4 and HSP70 have similar functions in tick-pathogen and host-pathogen interactions. To address this hypothesis, herein we characterized the role of these bacterial proteins in interaction and infection of vertebrate host cells. The results showed that A. phagocytophilum MSP4 and HSP70 are involved in host-pathogen interactions, with a role for HSP70 during pathogen infection. The analysis of the potential protective capacity of MSP4 and MSP4-HSP70 antigens in immunized sheep showed that MSP4-HSP70 was only partially protective against pathogen infection. This limited protection may be associated with several factors, including the recognition of non-protective epitopes by IgG in immunized lambs. Nevertheless, these antigens may be combined with other candidate protective antigens for the development of vaccines for the control of human and animal granulocytic anaplasmosis. Focusing on the characterization of host protective immune mechanisms and protein-protein interactions at the host-pathogen interface may lead to the discovery and design of new effective protective antigens.

Zobrazit více v PubMed

Abraham N. M., Liu L., Jutras B. L., Yadav A. K., Narasimhan S., Gopalakrishnan V., et al. (2017). Pathogen-mediated manipulation of arthropod microbiota to promote infection. Proc. Natl. Acad. Sci. U.S.A. 14, E781–E790. 10.1073/pnas.1613422114 PubMed DOI PMC

Alberdi P., Ayllón N., Cabezas-Cruz A., Bell-Sakyi L., Zweygarth E., Stuen S., et al. . (2015). Infection of Ixodes spp. tick cells with different Anaplasma phagocytophilum isolates induces the inhibition of apoptotic cell death. Ticks Tick Borne Dis. 6, 758–767. 10.1016/j.ttbdis.2015.07.001 PubMed DOI

Asanovich K. M., Bakken J. S., Madigan J. E., Aguero-Rosenfeld M., Wormser G. P., Dumler J. S., et al. . (1997). Antigenic diversity of granulocytic Ehrlichia isolates from humans in Wisconsin and New York and a horse in California. J. Infect. Dis. 176, 1029–1034. 10.1086/516529 PubMed DOI

Ayllón N., Villar M., Busby A. T., Kocan K. M., Blouin E. F., Bonzón-Kulichenko E., et al. . (2013). Anaplasma phagocytophilum inhibits apoptosis and promotes cytoskeleton rearrangement for infection of tick cells. Infect. Immun. 81, 2415–2425. 10.1128/IAI.00194-13 PubMed DOI PMC

Ayllón N., Villar M., Galindo R. C., Kocan K. M., Šíma R., López J. A., et al. . (2015). Systems biology of tissue-specific response to Anaplasma phagocytophilum reveals differentiated apoptosis in the tick vector Ixodes scapularis. PLoS Genet. 11:e1005120. 10.1371/journal.pgen.1005120 PubMed DOI PMC

Bakken J. S., Dumler J. S. (2015). Human granulocytic anaplasmosis. Infect. Dis. Clin. North Am. 29, 341–355. 10.1016/j.idc.2015.02.007 PubMed DOI PMC

Bowers K. J., Chow E., Huageng X., Dror R. O., Eastwood M. P., Gregersen B. A., et al. (2006). Scalable algorithms for molecular dynamics simulations on commodity clusters, in Proceedings of the ACM/IEEE Conference on Supercomputing (SC06) (Tampa, FL: ), 43–56.

Cabezas-Cruz A., Alberdi P., Ayllón N., Valdés J. J., Pierce R., Villar M., et al. . (2016). Anaplasma phagocytophilum increases the levels of histone modifying enzymes to inhibit cell apoptosis and facilitate pathogen infection in the tick vector, Ixodes scapularis. Epigenetics 11, 303–319. 10.1080/15592294.2016.1163460 PubMed DOI PMC

Cabezas-Cruz A., Alberdi P., Valdés J. J., Villar M., de la Fuente J. (2017). Anaplasma phagocytophilum infection subverts carbohydrate metabolic pathways in the tick vector, Ixodes scapularis. Front. Cell. Infect. Microbiol. 7:23. 10.3389/fcimb.2017.00023 PubMed DOI PMC

de la Fuente J., Contreras M. (2015). Tick vaccines: current status and future directions. Expert Rev. Vaccines 14, 1367–1376. 10.1586/14760584.2015.1076339 PubMed DOI

de la Fuente J., Antunes S., Bonnet S., Cabezas-Cruz A., Domingos A., Estrada-Pe-a A., et al. . (2017). Tick-pathogen interactions and vector competence: identification of molecular drivers for tick-borne diseases. Front. Cell. Infect. Microbiol. 7:114. 10.3389/fcimb.2017.00114 PubMed DOI PMC

de la Fuente J., Ayoubi P., Blouin E. F., Almazán C., Naranjo V., Kocan K. M. (2005). Gene expression profiling of human promyelocytic cells in response to infection with Anaplasma phagocytophilum. Cell. Microbiol. 7, 549–559. 10.1111/j.1462-5822.2004.00485.x PubMed DOI

de la Fuente J., Estrada-Pe-a A., Cabezas-Cruz A., Kocan K. M. (2016a). Anaplasma phagocytophilum uses common strategies for infection of ticks and vertebrate hosts. Trends Microbiol. 24, 173–180. 10.1016/j.tim.2015.12.001 PubMed DOI

de la Fuente J., García-García J. C., Blouin E. F., Kocan K. M. (2001). Differential adhesion of major surface proteins 1a and 1b of the ehrlichial cattle pathogen Anaplasma marginale to bovine erythrocytes and tick cells. Int. J. Parasitol. 31, 145–153. 10.1016/S0020-7519(00)00162-4 PubMed DOI

de la Fuente J., Kocan K. M., Blouin E. F., Zivkovic Z., Naranjo V., Almazán C., et al. . (2010). Functional genomics and evolution of tick-Anaplasma interactions and vaccine development. Vet. Parasitol. 167, 175–186. 10.1016/j.vetpar.2009.09.019 PubMed DOI

de la Fuente J., Kocan K. M., Garcia-Garcia J. C., Blouin E. F., Halbur T., Onet V. (2003). Immunization against Anaplasma marginale major surface protein 1a reduces infectivity for ticks. J. Appl. Res. Vet. Med. 1, 285–292.

de la Fuente J., Kopáček P., Lew-Tabor A., Maritz-Olivier C. (2016b). Strategies for new and improved vaccines against ticks and tick-borne diseases. Parasite Immunol. 38, 754–769. 10.1111/pim.12339 PubMed DOI

de la Fuente J., Villar M., Cabezas-Cruz A., Estrada-Pe-a A., Ayllón N., Alberdi P. (2016c). Tick-host-pathogen interactions: conflict and cooperation. PLoS Pathog. 12:e1005488. 10.1371/journal.ppat.1005488 PubMed DOI PMC

de la Fuente J., Waterhouse R. M., Sonenshine D. E., Michael Roe R., Ribeiro J. M., Sattelle D. B., et al. . (2016d). Tick genome assembled: new opportunities for research on tick-host-pathogen interactions. Front. Cell. Infect. Microbiol. 6:103. 10.3389/fcimb.2016.00103 PubMed DOI PMC

Dugat T., Lagrée A. C., Maillard R., Boulouis H. J., Haddad N. (2015). Opening the black box of Anaplasma phagocytophilum diversity: current situation and future perspectives. Front. Cell. Infect. Microbiol. 5:61. 10.3389/fcimb.2015.00061 PubMed DOI PMC

Dumler J. S., Barbet A. C., Bekker C. P. J., Dasch G. A., Palmer G. H., Ray S. C., et al. . (2001). Reorganization of the genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions subjective synonyms of Ehrlichia phagocytophila. Int. J. Syst. Evol. Microbiol. 51, 2145–2165. 10.1099/00207713-51-6-2145 PubMed DOI

Eberts M. D., Vissotto de Paiva Diniz P. P., Beall M. J., Stillman B. A., Chandrashekar R., Breitschwerdt E. B. (2011). Typical and atypical manifestations of Anaplasma phagocytophilum infection in dogs. J. Am. Anim. Hosp. Assoc. 47, e86–e94. 10.5326/JAAHA-MS-5578 PubMed DOI

Foggie A. (1951). Studies on the infectious agent of tick-borne fever in sheep. J. Path. Bact. 63, 1–15. 10.1002/path.1700630103 PubMed DOI

Garcia-Garcia J. C., de la Fuente J., Blouin E. F., Halbur T., Onet V. C., Saliki J. T., et al. . (2004). Differential expression of the msp1α gene of Anaplasma marginale occurs in bovine erythrocytes and tick cells. Vet. Microbiol. 98, 261–272. 10.1016/j.vetmic.2003.10.021 PubMed DOI

Ge Y., Rikihisa Y. (2006). Anaplasma phagocytophilum delays spontaneous human neutrophil apoptosis by modulation of multiple apoptotic pathways. Cell. Microbiol. 8, 1406–1416. 10.1111/j.1462-5822.2006.00720.x PubMed DOI

Ge Y., Rikihisa Y. (2007). Identification of novel surface proteins of Anaplasma phagocytophilum by affinity purification and proteomics. J. Bacteriol. 189, 7819–7828. 10.1128/JB.00866-07 PubMed DOI PMC

Gomes-Solecki M. (2014). Blocking pathogen transmission at the source: reservoir targeted OspA-based vaccines against Borrelia burgdorferi. Front. Cell. Infect. Microbiol. 4:136. 10.3389/fcimb.2014.00136 PubMed DOI PMC

Gordon W. S., Brownlee A., Wilson D. R., MacLeod J. (1932). Tick-borne fever. J. Comp. Path. 45, 301–302. 10.1016/S0368-1742(32)80025-1 DOI

Grøva L., Olesen I., Steinshamn H., Stuen S. (2011). Prevalence of Anaplasma phagocytophilum infection and effect on lamb growth. Acta Vet. Scand. 53:30. 10.1186/1751-0147-53-30 PubMed DOI PMC

Gulia-Nuss M., Nuss A. B., Meyer J. M., Sonenshine D. E., Roe R. M., Waterhouse R. M., et al. . (2016). Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nat. Commun. 7:10507. 10.1038/ncomms10507 PubMed DOI PMC

Gunti S., Notkins A. L. (2015). Polyreactive antibodies: function and quantification. J. Infect. Dis. 212(Suppl. 1), S42–S46. 10.1093/infdis/jiu512 PubMed DOI PMC

Hajdušek O., Šíma R., Ayllón N., Jalovecká M., Perner J., de la Fuente J., et al. . (2013). Interaction of the tick immune system with transmitted pathogens. Front. Cell. Infect. Microbiol. 3:26. 10.3389/fcimb.2013.00026 PubMed DOI PMC

Haste Andersen P., Nielsen M., Lund O. (2006). Prediction of residues in discontinuous B-cell epitopes using protein 3D structures. Protein Sci. 15, 2558–2567. 10.1110/ps.062405906 PubMed DOI PMC

Hebert K. S., Seidman D., Oki A. T., Izac J., Emani S., Oliver L. D., Jr., et al. . (2017). Anaplasma marginale outer membrane protein A is an adhesin that recognizes sialylated and fucosylated glycans and functionally depends on an essential binding domain. Infect. Immun. 85:e00968–16. 10.1128/IAI.00968-16 PubMed DOI PMC

Heyman P., Cochez C., Hofhuis A., van der Giessen J., Sprong H., Porter S. R., et al. . (2010). A clear and present danger: tick-borne diseases in Europe. Expert Rev. Anti Infect. Ther. 8, 33–50. 10.1586/eri.09.118 PubMed DOI

Huang B., Troese M. J., Ye S., Sims J. T., Galloway N. L., Borjesson D. L., et al. . (2010). Anaplasma phagocytophilum APH_1387 is expressed throughout bacterial intracellular development and localizes to the pathogen-occupied vacuolar membrane. Infect. Immun. 78, 1864–1873. 10.1128/IAI.01418-09 PubMed DOI PMC

Humphrey W., Dalke A., Schulten K. (1996). VMD - Visual Molecular Dynamics. J. Mol. Graph. 14, 33–38. 10.1016/0263-7855(96)00018-5 PubMed DOI

Hurtado A., Barandika J. F., Oporto B., Minguijón E., Povedano I., García-Pérez A. L. (2015). Risks of suffering tick-borne diseases in sheep translocated to a tick infested area: a laboratory approach for the investigation of an outbreak. Ticks Tick Borne Dis. 6, 31–37. 10.1016/j.ttbdis.2014.09.001 PubMed DOI

Johnson J. L. (2012). Evolution and function of diverse Hsp90 homologs and cochaperone proteins. Biochim. Biophys. Acta. 1823, 607–613. 10.1016/j.bbamcr.2011.09.020 PubMed DOI

Kahlon A., Ojogun N., Ragland S. A., Seidman D., Troese M. J., Ottens A. K., et al. . (2013). Anaplasma phagocytophilum Asp14 is an invasin that interacts with mammalian host cells via its C terminus to facilitate infection. Infect. Immun. 81, 65–79. 10.1128/IAI.00932-12 PubMed DOI PMC

Katoh K., Standley D. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780. 10.1093/molbev/mst010 PubMed DOI PMC

Kaylor P. S., Crawford T. B., McElwain T. F., Palmer G. H. (1991). Passive transfer of antibody to Ehrlichia risticii protects mice from ehrlichiosis. Infect. Immun. 59, 2058–2062. PubMed PMC

Kim D. E., Chivian D., Baker D. (2004). Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res. 32, W526–W531. 10.1093/nar/gkh468 PubMed DOI PMC

Larsen J. E., Lund O., Nielsen M. (2006). Improved method for predicting linear B-cell epitopes. Immunome Res. 2:2. 10.1186/1745-7580-2-2 PubMed DOI PMC

Li X., Jacobson M. P., Zhu K., Zhao S., Friesner R. A. (2007). Assignment of polar states for protein amino acid residues using an interaction cluster decomposition algorithm and its application to high resolution protein structure modeling. Proteins 66, 824–837. 10.1002/prot.21125 PubMed DOI

Lin M., den Dulk-Ras A., Hooykaas P. J., Rikihisa Y. (2007). Anaplasma phagocytophilum AnkA secreted by type IV secretion system is tyrosine phosphorylated by Abl-1 to facilitate infection. Cell. Microbiol. 9, 2644–2657. 10.1111/j.1462-5822.2007.00985.x PubMed DOI

Lin M., Kikuchi T., Brewer H. M., Norbeck A. D., Rikihisa Y. (2011). Global proteomic analysis of two tick-borne emerging zoonotic agents: Anaplasma phagocytophilum and Ehrlichia chaffeensis. Front. Microbiol. 2:24. 10.3389/fmicb.2011.00024 PubMed DOI PMC

Lis K., Najm N., de la Fuente J., Fernández de Mera I., Zweygarth E., Pfister K., et al. . (2014). Use of Percoll gradients to purify Anaplasma marginale (Rickettsiales: Anaplasmataceae) from tick cell cultures. Ticks Tick Borne Dis. 5, 511–515. 10.1016/j.ttbdis.2014.03.006 PubMed DOI

Livak K. J., Schmittgen T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(−ΔΔCT) method. Methods 25, 402–408. 10.1006/meth.2001.1262 PubMed DOI

Lomize M. A., Lomize A. L., Pogozheva I. D., Mosberg H. I. (2006). OPM: orientations of proteins in membranes database. Bioinformatics 22, 623–625. 10.1093/bioinformatics/btk023 PubMed DOI

Mansfield K. L., Cook C., Ellis R., Bell-Sakyi L., Johnson N., Alberdi P., et al. . (2017). Tick-borne pathogens induce differential expression of genes promoting cell survival and host resistence in Ixodes ricinus cells. Parasit. Vectors 10, 81. 10.1186/s13071-017-2011-1 PubMed DOI PMC

Mastronunzio J. E., Kurscheid S., Fikrig E. (2012). Postgenomic analyses reveal development of infectious Anaplasma phagocytophilum during transmission from ticks to mice. J. Bacteriol. 194, 2238–2247. 10.1128/JB.06791-11 PubMed DOI PMC

Merino M., Antunes S., Mosqueda J., Moreno-Cid J. A., Pérez de la Lastra J. M., Rosario-Cruz R., et al. . (2013). Vaccination with proteins involved in tick-pathogen interactions reduces vector infestations and pathogen infection. Vaccine 31, 5889–5896. 10.1016/j.vaccine.2013.09.037 PubMed DOI

Merino O., Almazán C., Canales M., Villar M., Moreno-Cid J. A., Estrada-Pe-a A., et al. . (2011). Control of Rhipicephalus (Boophilus) microplus infestations by the combination of subolesin vaccination and tick autocidal control after subolesin gene knockdown in ticks fed on cattle. Vaccine 29, 2248–2254. 10.1016/j.vaccine.2011.01.050 PubMed DOI

Messick J. B., Rikihisa Y. (1994). Inhibition of binding, entry, or intracellular proliferation of Ehrlichia risticii in P388D1 cells by anti-E. risticii serum, immunoglobulin G, or Fab fragment. Infect. Immun. 62, 3156–3161. PubMed PMC

Multhoff G. (2007). Heat shock protein 70 (Hsp70): membrane location, export and immunological relevance. Methods 43, 229–237. 10.1016/j.ymeth.2007.06.006 PubMed DOI

Neelakanta G., Sultana H., Fish D., Anderson J. F., Fikrig E. (2010). Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold. J. Clin. Invest. 120, 3179–3190. 10.1172/JCI42868 PubMed DOI PMC

Niu H., Rikihisa Y., Yamaguchi M., Ohashi N. (2006). Differential expression of VirB9 and VirB6 during the life cycle of Anaplasma phagocytophilum in human leucocytes is associated with differential binding and avoidance of lysosome pathway. Cell. Microbiol. 8, 523–534. 10.1111/j.1462-5822.2005.00643.x PubMed DOI

Ojogun N., Kahlon A., Ragland S. A., Troese M. J., Mastronunzio J. E., Walker N. J., et al. . (2012). Anaplasma phagocytophilum outer membrane protein A interacts with sialylated glycoproteins to promote infection of mammalian host cells. Infect. Immun. 80, 3748–3760. 10.1128/IAI.00654-12 PubMed DOI PMC

Oliva Chávez A. S., Fairman J. W., Felsheim R. F., Nelson C. M., Herron M. J., Higgins L., et al. . (2015). An O-Methyltransferase is required for infection of tick cells by Anaplasma phagocytophilum. PLoS Pathog. 11:e1005248. 10.1371/journal.ppat.1005248 PubMed DOI PMC

Palmer G. H., Rurangirwa F. R., Kocan K. M., Brown W. C. (1999). Molecular basis for vaccine development against the ehrlichial pathogen Anaplasma marginale. Parasitol. Today 15, 281–286. 10.1016/S0169-4758(99)01469-6 PubMed DOI

Ponomarenko J. V., Bourne P. E. (2007). Antibody-protein interactions: benchmark datasets and prediction tools evaluation. BMC Struct. Biol. 7:64. 10.1186/1472-6807-7-64 PubMed DOI PMC

Rikihisa Y. (2011). Mechanisms of obligatory intracellular infection with Anaplasma phagocytophilum. Curr. Microbiol. Rev. 24, 469–489. 10.1128/CMR.00064-10 PubMed DOI PMC

Ririe K. M., Rasmussen R. P., Wittwer C. T. (1997). Product differentiation by analysis of DNA melting curves during the polymerase chain reaction. Anal. Biochem. 245, 154–160. 10.1006/abio.1996.9916 PubMed DOI

Scopio A., Johnson P., Laquerre A., Nelson D. R. (1994). Subcellular localization and chaperone activities of Borrelia burgdorferi Hsp60 and Hsp70. J. Bacteriol. 176, 6449–6456. 10.1128/jb.176.21.6449-6456.1994 PubMed DOI PMC

Seidman D., Hebert K. S., Truchan H. K., Miller D. P., Tegels B. K., Marconi R. T., et al. . (2015). Essential domains of Anaplasma phagocytophilum invasins utilized to infect mammalian host cells. PLoS Pathog. 11:e1004669. 10.1371/journal.ppat.1004669 PubMed DOI PMC

Severo M. S., Pedra J. H. F., Ayllón N., Kocan K. M., de la Fuente J. (2013). Anaplasma, in Molecular Medical Microbiology, 2nd Edn, eds Yi-Wei T., Dongyou L., Ian P. R., Schwartzman J. D., Sussman M. (Cambridge, MA: Academic Press, Elsevier; ).

Severo M. S., Stephens K. D., Kotsyfakis M., Pedra J. H. (2012). Anaplasma phagocytophilum: deceptively simple or simply deceptive? Fut. Microbiol. 7, 719–731. 10.2217/fmb.12.45 PubMed DOI PMC

Seydlová G., Halada P., Fišer R., Toman O., Ulrych A., Svobodová J. (2012). DnaK and GroEL chaperones are recruited to the Bacillus subtilis membrane after short-term ethanol stress. J. Appl. Microbiol. 112, 765–774. 10.1111/j.1365-2672.2012.05238.x PubMed DOI

Shaw D. K., Wang X., Brown L. J., Oliva Chávez A. S., Reif K. E., Smith A. A., et al. . (2017). Infection-derived lipids elicit an immune deficiency circuit in arthropods. Nat. Commun. 8:14401. 10.1038/ncomms14401 PubMed DOI PMC

Sievers F., Wilm A., Dineen D., Gibson T. J., Karplus K., Li W., et al. . (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539. 10.1038/msb.2011.75 PubMed DOI PMC

Stuen S., Granquist E. G., Silaghi C. (2013). Anaplasma phagocytophilum–a widespread multi-host pathogen with highly adaptive strategies. Front. Cell. Infect. Microbiol. 3:31. 10.3389/fcimb.2013.00031 PubMed DOI PMC

Stuen S., Grøva L., Granquist E. G., Sandstedt K., Olesen I., Steinshamn H. (2011). A comparative study of clinical manifestations, haematological and serological responses after experimental infection with Anaplasma phagocytophilum in two Norwegian sheep breeds. Acta Vet. Scand. 53:8. 10.1186/1751-0147-53-8 PubMed DOI PMC

Stuen S., Okstad W., Artursson K., Al-Khedery B., Barbet A., Granquist E. G. (2015). Lambs immunized with an inactivated variant of Anaplasma phagocytophilum. Acta Vet. Scand. 57, 40. 10.1186/s13028-015-0131-1 PubMed DOI PMC

Sukumaran B., Narasimham S., Anderson J. F., DePonte K., Marcantonio K., Krishnan M. N., et al. (2006). An Ixodes scapularis protein required for survival of Anaplasma phagocytophilum in tick salivary glands. J. Exp. Med. 6, 1507–1517. 10.1084/jem.20060208 PubMed DOI PMC

Sun W., Ijdo J. W., Telford S. R., III., Hodzic E., Zhang Y., Barthold S. W., et al. . (1997). Immunization against the agent of human granulocytic ehrlichiosis in a murine model. J. Clin. Invest. 100, 3014–3018. 10.1172/JCI119855 PubMed DOI PMC

Susin M. F., Baldini R. L., Gueiros-Filho F., Gomes S. L. (2006). GroES/GroEL and DnaK/DnaJ have distinct roles in stress responses and during cell cycle progression in Caulobacter crescentus. J. Bacteriol. 188, 8044–8053. 10.1128/JB.00824-06 PubMed DOI PMC

Terajima M., Babon J. A., Co M. D., Ennis F. A. (2013). Cross-reactive human B cell and T cell epitopes between influenza A and B viruses. Virol. J. 10:244. 10.1186/1743-422X-10-244 PubMed DOI PMC

Torchala M., Moal I. H., Chaleil R. A. G., Fernandez-Recio J., Bates P. A. (2013). SwarmDock: a server for flexible protein-protein docking. Bioinformatics 29, 807–809. 10.1093/bioinformatics/btt038 PubMed DOI

Troese M. J., Kahlon A., Ragland S. A., Ottens A. K., Ojogun N., Nelson K. T., et al. . (2011). Proteomic analysis of Anaplasma phagocytophilum during infection of human myeloid cells identifies a protein that is pronouncedly upregulated on the infectious dense-cored cell. Infect. Immun. 79, 4696–4707. 10.1128/IAI.05658-11 PubMed DOI PMC

Truchan H. K., Cockburn C. L., Hebert K. S., Magunda F., Noh S. M., Carlyon J. A. (2016). The pathogen-occupied vacuoles of Anaplasma phagocytophilum and Anaplasma marginale Interact with the Endoplasmic Reticulum. Front. Cell. Infect. Microbiol. 6:22. 10.3389/fcimb.2016.00022 PubMed DOI PMC

Villar M., Ayllón N., Alberdi P., Moreno A., Moreno M., Tobes R., et al. . (2015a). Integrated metabolomics, transcriptomics and proteomics identifies metabolic pathways affected by Anaplasma phagocytophilum infection in tick cells. Mol. Cell. Proteomics 14, 3154–3172. 10.1074/mcp.M115.051938 PubMed DOI PMC

Villar M., Ayllón N., Kocan K. M., Bonzón-Kulichenko E., Alberdi P., Blouin E. F., et al. . (2015b). Identification and characterization of Anaplasma phagocytophilum proteins involved in infection of the tick vector, Ixodes scapularis. PLoS ONE 10:e0137237. 10.1371/journal.pone.0137237 PubMed DOI PMC

Whist S. K., Storset A. K., Johansen G. M., Larsen H. J. (2003). Modulation of leukocyte populations and immune responses in sheep experimentally infected with Anaplasma (formerly Ehrlichia) phagocytophilum. Vet. Immunol. Immunopathol. 94, 163–175. 10.1016/S0165-2427(03)00101-6 PubMed DOI

Woldehiwet Z. (2006). Anaplasma phagocytophilum in ruminants in Europe. Ann. N.Y. Acad. Sci. 1078, 446–460. 10.1196/annals.1374.084 PubMed DOI

Zhang Y. (2008). I-TASSER server for protein 3D structure prediction. BMC Bioinform. 9:40. 10.1186/1471-2105-9-40 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace