Differential Tick Salivary Protein Profiles and Human Immune Responses to Lone Star Ticks (Amblyomma americanum) From the Wild vs. a Laboratory Colony

. 2019 ; 10 () : 1996. [epub] 20190828

Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, Research Support, U.S. Gov't, Non-P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid31555263

Ticks are a growing concern to human and animal health worldwide and they are leading vectors of arthropod-borne pathogens in the United States. Ticks are pool blood feeders that can attach to the host skin for days to weeks using their saliva to counteract the host defenses. Tick saliva, as in other hematophagous arthropods, contains pharmacological and immunological active compounds, which modulate local and systemic immune responses and induce antibody production. In the present study, we explore differences in the salivary gland extract (SGE) protein content of Amblyomma americanum ticks raised in a laboratory colony (CT) vs. those collected in the field (FT). First, we measured the IgG antibody levels against SGE in healthy volunteers residing in Kansas. ELISA test showed higher IgG antibody levels when using the SGE from CT as antigen. Interestingly, antibody levels against both, CT-SGE and FT-SGE, were high in the warm months (May-June) and decreased in the cold months (September-November). Immunoblot testing revealed a set of different immunogenic bands for each group of ticks and mass spectrometry data revealed differences in at 19 proteins specifically identified in the CT-SGE group and 20 from the FT-SGE group. Our results suggest that differences in the salivary proteins between CT-SGE and FT-SGE may explain the differential immune responses observed in this study.

Zobrazit více v PubMed

Brites-Neto J, Duarte KM, Martins TF. Tick-borne infections in human and animal population worldwide. Vet World. (2015) 8:301–15. 10.14202/vetworld.2015.301-315 PubMed DOI PMC

Simo L, Kazimirova M, Richardson J, Bonnet SI. The essential role of tick salivary glands and saliva in tick feeding and pathogen transmission. Front Cell Infect Microbiol. (2017) 7:281. 10.3389/fcimb.2017.00281 PubMed DOI PMC

Nuttall PA. Wonders of tick saliva. Ticks Tick Borne Dis. (2019) 10:470–81. 10.1016/j.ttbdis.2018.11.005 PubMed DOI

Titus RG, Bishop JV, Mejia JS. The immunomodulatory factors of arthropod saliva and the potential for these factors to serve as vaccine targets to prevent pathogen transmission. Parasite Immunol. (2006) 28:131–41. 10.1111/j.1365-3024.2006.00807.x PubMed DOI

Kotal J, Langhansova H, Lieskovska J, Andersen JF, Francischetti IM, Chavakis T, et al. . Modulation of host immunity by tick saliva. J Proteomics. (2015) 128:58–68. 10.1016/j.jprot.2015.07.005 PubMed DOI PMC

Perner J, Kropackova S, Kopacek P, Ribeiro JMC. Sialome diversity of ticks revealed by RNAseq of single tick salivary glands. PLoS Negl Trop Dis. (2018) 12:e0006410. 10.1371/journal.pntd.0006410 PubMed DOI PMC

Kazimirova M, Thangamani S, Bartikova P, Hermance M, Holikova V, Stibraniova I, et al. . Tick-borne viruses and biological processes at the tick-host-virus interface. Front Cell Infect Microbiol. (2017) 7:339. 10.3389/fcimb.2017.00339 PubMed DOI PMC

Hermance ME, Thangamani S. Tick saliva enhances powassan virus transmission to the host, influencing its dissemination and the course of disease. J Virol. (2015) 89:7852–60. 10.1128/JVI.01056-15 PubMed DOI PMC

Nuttall PA. Tick saliva and its role in pathogen transmission. Wien Klin Wochenschr. (2019) 10:1–12. 10.1007/s00508-019-1500-y PubMed DOI PMC

Schuijt TJ, Hovius JW, van Burgel ND, Ramamoorthi N, Fikrig E, van Dam AP. The tick salivary protein Salp15 inhibits the killing of serum-sensitive Borrelia burgdorferi sensu lato isolates. Infect Immun. (2008) 76:2888–94. 10.1128/IAI.00232-08 PubMed DOI PMC

Andrade BB, Teixeira CR, Barral A, Barral-Netto M. Haematophagous arthropod saliva and host defense system: a tale of tear and blood. An Acad Bras Cienc. (2005) 77:665–93. 10.1590/S0001-37652005000400008 PubMed DOI

Scholl DC, Embers ME, Caskey JR, Kaushal D, Mather TN, Buck WR, et al. . Immunomodulatory effects of tick saliva on dermal cells exposed to Borrelia burgdorferi, the agent of Lyme disease. Parasit Vectors. (2016) 9:394. 10.1186/s13071-016-1638-7 PubMed DOI PMC

Wikel S. Ticks and tick-borne pathogens at the cutaneous interface: host defenses, tick countermeasures, a suitable environment for pathogen establishment. Front Microbiol. (2013) 4:337. 10.3389/fmicb.2013.00337 PubMed DOI PMC

Londono-Renteria B, Cardenas JC, Giovanni JE, Cardenas L, Villamizar P, Rolon J, et al. . Aedes aegypti anti-salivary gland antibody concentration and dengue virus exposure history in healthy individuals living in an endemic area in Colombia. Biomedica. (2015) 35:572–81. 10.7705/biomedica.v35i4.2530 PubMed DOI

Londono-Renteria B, Patel JC, Vaughn M, Funkhauser S, Ponnusamy L, Grippin C, et al. . Long-lasting permethrin-impregnated clothing protects against mosquito bites in outdoor workers. Am J Trop Med Hyg. (2015) 93:869–74. 10.4269/ajtmh.15-0130 PubMed DOI PMC

Lane RS, Moss RB, Hsu YP, Wei T, Mesirow ML, Kuo MM. Anti-arthropod saliva antibodies among residents of a community at high risk for Lyme disease in California. Am J Trop Med Hyg. (1999) 61:850–9. 10.4269/ajtmh.1999.61.850 PubMed DOI

Huang YS, Higgs S, Vanlandingham DL. Arbovirus-mosquito vector-host interactions and the impact on transmission and disease pathogenesis of arboviruses. Front Microbiol. (2019) 10:22. 10.3389/fmicb.2019.00022 PubMed DOI PMC

Nuttall PA, Labuda M. Tick-host interactions: saliva-activated transmission. Parasitology. (2004) 129 (Suppl. 1):S177–89. 10.1017/S0031182004005633 PubMed DOI

Ferreira BR, Szabo MJ, Cavassani KA, Bechara GH, Silva JS. Antigens from Rhipicephalus sanguineus ticks elicit potent cell-mediated immune responses in resistant but not in susceptible animals. Vet Parasitol. (2003) 115:35–48. 10.1016/S0304-4017(03)00190-0 PubMed DOI

Radulovic ZM, Kim TK, Porter LM, Sze SH, Lewis L, Mulenga A. A 24–48 h fed Amblyomma americanum tick saliva immuno-proteome. BMC Genomics. (2014) 15:518. 10.1186/1471-2164-15-518 PubMed DOI PMC

Ribeiro JM. How ticks make a living. Parasitol Today. (1995) 11:91–3. 10.1016/0169-4758(95)80162-6 PubMed DOI

Sprong H, Trentelman J, Seemann I, Grubhoffer L, Rego RO, Hajdusek O, et al. . ANTIDotE: anti-tick vaccines to prevent tick-borne diseases in Europe. Parasit Vectors. (2014) 7:77. 10.1186/1756-3305-7-77 PubMed DOI PMC

Childs JE, Paddock CD. The ascendancy of Amblyomma americanum as a vector of pathogens affecting humans in the United States. Annu Rev Entomol. (2003) 48:307–37. 10.1146/annurev.ento.48.091801.112728 PubMed DOI

Barrett AW, Noden BH, Gruntmeir JM, Holland T, Mitcham JR, Martin JE, et al. . County scale distribution of Amblyomma americanum (Ixodida: Ixodidae) in Oklahoma: addressing local deficits in tick maps based on passive reporting. J Med Entomol. (2015) 52:269–73. 10.1093/jme/tju026 PubMed DOI

Raghavan RK, Peterson AT, Cobos ME, Ganta R, Foley D. Current and future distribution of the Lone Star Tick, Amblyomma americanum (L.) (Acari: Ixodidae) in North America. PLoS ONE. (2019) 14:e0209082. 10.1371/journal.pone.0209082 PubMed DOI PMC

Mani RJ, Metcalf JA, Clinkenbeard KD. Amblyomma americanum as a bridging vector for human infection with Francisella tularensis. PLoS ONE. (2015) 10:e0130513. 10.1371/journal.pone.0130513 PubMed DOI PMC

Crispell G, Commins SP, Archer-Hartman SA, Choudhary S, Dharmarajan G, Azadi P, et al. . Discovery of alpha-gal-containing antigens in north american tick species believed to induce red meat allergy. Front Immunol. (2019) 10:1056. 10.3389/fimmu.2019.01056 PubMed DOI PMC

Monzon JD, Atkinson EG, Henn BM, Benach JL. Population and evolutionary genomics of Amblyomma americanum, an expanding arthropod disease vector. Genome Biol Evol. (2016) 8:1351–60. 10.1093/gbe/evw080 PubMed DOI PMC

Centers for Disease Control and Prevention . Tickborne diseases of the United States. (2019). Available online at: https://www.cdc.gov/ticks/tickbornediseases/tickID.html

Sonenshine DE, Nicholson WL. Ticks (Ixodida). In: Mullen GR, Durden LA, editors. Medical and Veterinary Entomology. Statesboro, GA: Academic Press; (2002). p. 517–58.

Londono-Renteria BL, Eisele TP, Keating J, James MA, Wesson DM. Antibody response against Anopheles albimanus (Diptera: Culicidae) salivary protein as a measure of mosquito bite exposure in Haiti. J Med Entomol. (2010) 47:1156–63. 10.1603/ME09240 PubMed DOI

Londono-Renteria B, Drame PM, Weitzel T, Rosas R, Gripping C, Cardenas JC, et al. . An. gambiae gSG6-P1 evaluation as a proxy for human-vector contact in the Americas: a pilot study. Parasit Vectors. (2015) 8:533. 10.1186/s13071-015-1160-3 PubMed DOI PMC

Conway MJ, Londono-Renteria B, Troupin A, Watson AM, Klimstra WB, Fikrig E, et al. . Aedes aegypti D7 saliva protein inhibits dengue virus infection. PLoS Negl Trop Dis. (2016) 10:e0004941. 10.1371/journal.pntd.0004941 PubMed DOI PMC

Vogt MB, Lahon A, Arya RP, Kneubehl AR, Spencer Clinton JL, Paust S, et al. . Mosquito saliva alone has profound effects on the human immune system. PLoS Negl Trop Dis. (2018) 12:e0006439. 10.1371/journal.pntd.0006439 PubMed DOI PMC

T.Nascimento GD, Vieira PS, Cogo SC, Dias-Netipanyj MF, Franca Junior N, Camara DAD, et al. Antitumoral effects of Amblyomma sculptum Berlese saliva in neuroblastoma cell lines involve cytoskeletal deconstruction and cell cycle arrest. Rev Bras Parasitol Vet. (2019) 28:126–33. 10.1590/s1984-296120180098 PubMed DOI

Shipley MM, Mangold CA, Kuny CV, Szpara ML. Differentiated human SH-SY5Y cells provide a reductionist model of herpes simplex virus 1 neurotropism. J Virol. (2017) 91:e00958-17. 10.1128/JVI.00958-17 PubMed DOI PMC

Gokyu M, Kobayashi H, Nanbara H, Sudo T, Ikeda Y, Suda T, et al. . Thrombospondin-1 production is enhanced by Porphyromonas gingivalis lipopolysaccharide in THP-1 cells. PLoS ONE. (2014) 9:e115107. 10.1371/journal.pone.0115107 PubMed DOI PMC

Tabata S, Ikeda R, Yamamoto M, Shimaoka S, Mukaida N, Takeda Y, et al. . Thymidine phosphorylase activates NFkappaB and stimulates the expression of angiogenic and metastatic factors in human cancer cells. Oncotarget. (2014) 5:10473–85. 10.18632/oncotarget.2242 PubMed DOI PMC

Pimentel-Nunes P, Goncalves N, Boal-Carvalho I, Afonso L, Lopes P, Roncon-Albuquerque R, Jr, et al. . Decreased Toll-interacting protein and peroxisome proliferator-activated receptor gamma are associated with increased expression of Toll-like receptors in colon carcinogenesis. J Clin Pathol. (2012) 65:302–8. 10.1136/jclinpath-2011-200567 PubMed DOI

Gu H, Jiao Y, Yu X, Li X, Wang W, Ding L, et al. . Resveratrol inhibits the IL-1beta-induced expression of MMP-13 and IL-6 in human articular chondrocytes via TLR4/MyD88-dependent and -independent signaling cascades. Int J Mol Med. (2017) 39:734–40. 10.3892/ijmm.2017.2885 PubMed DOI

Du M, Wang X, Tan X, Li X, Huang D, Huang K, et al. . Nkx2-5 is expressed in atherosclerotic plaques and attenuates development of atherosclerosis in apolipoprotein E-deficient mice. J Am Heart Assoc. (2016) 5:e004440. 10.1161/JAHA.116.004440 PubMed DOI PMC

Li Y, Chen R, Bowden M, Mo F, Lin YY, Gleave M, et al. . Establishment of a neuroendocrine prostate cancer model driven by the RNA splicing factor SRRM4. Oncotarget. (2017) 8:66878–88. 10.18632/oncotarget.19916 PubMed DOI PMC

Feng M, Kang M, He F, Xiao Z, Liu Z, Yao H, et al. . Plasma interleukin-37 is increased and inhibits the production of inflammatory cytokines in peripheral blood mononuclear cells in systemic juvenile idiopathic arthritis patients. J Transl Med. (2018) 16:277. 10.1186/s12967-018-1655-8 PubMed DOI PMC

Wang B, Wei G, Liu B, Zhou X, Xiao H, Dong N, et al. . The role of high mobility group box 1 protein in interleukin-18-induced myofibroblastic transition of valvular interstitial cells. Cardiology. (2016) 135:168–78. 10.1159/000447483 PubMed DOI

Kawka E, Witowski J, Fouqet N, Tayama H, Bender TO, Catar R, et al. . Regulation of chemokine CCL5 synthesis in human peritoneal fibroblasts: a key role of IFN-gamma. Mediators Inflamm. (2014) 2014:590654. 10.1155/2014/590654 PubMed DOI PMC

Plotnikova MA, Klotchenko SA, Vasin AV. Development of a multiplex quantitative PCR assay for the analysis of human cytokine gene expression in influenza A virus-infected cells. J Immunol Methods. (2016) 430:51–5. 10.1016/j.jim.2016.01.005 PubMed DOI

Kim S, Kim YK, Lee H, Cho JE, Kim HY, Uh Y, et al. . Interferon gamma mRNA quantitative real-time polymerase chain reaction for the diagnosis of latent tuberculosis: a novel interferon gamma release assay. Diagn Microbiol Infect Dis. (2013) 75:68–72. 10.1016/j.diagmicrobio.2012.09.015 PubMed DOI

Sanchez D, Ganfornina MD, Gutierrez G, Marin A. Exon-intron structure and evolution of the Lipocalin gene family. Mol Biol Evol. (2003) 20:775–83. 10.1093/molbev/msg079 PubMed DOI

Paesen GC, Adams PL, Nuttall PA, Stuart DL. Tick histamine-binding proteins: lipocalins with a second binding cavity. Biochim Biophys Acta. (2000) 1482:92–101. 10.1016/S0167-4838(00)00168-0 PubMed DOI

Wolk K, Wenzel J, Tsaousi A, Witte-Handel E, Babel N, Zelenak C, et al. . Lipocalin-2 is expressed by activated granulocytes and keratinocytes in affected skin and reflects disease activity in acne inversa/hidradenitis suppurativa. Br J Dermatol. (2017) 177:1385–93. 10.1111/bjd.15424 PubMed DOI

Fontaine A, Diouf I, Bakkali N, Misse D, Pages F, Fusai T, et al. . Implication of haematophagous arthropod salivary proteins in host-vector interactions. Parasit Vectors. (2011) 4:187. 10.1186/1756-3305-4-187 PubMed DOI PMC

Londono-Renteria B, Cardenas JC, Cardenas LD, Christofferson RC, Chisenhall DM, Wesson DM, et al. . Use of anti-Aedes aegypti salivary extract antibody concentration to correlate risk of vector exposure and dengue transmission risk in Colombia. PLoS ONE. (2013) 8:e81211. 10.1371/journal.pone.0081211 PubMed DOI PMC

Fontaine A, Pascual A, Orlandi-Pradines E, Diouf I, Remoue F, Pages F, et al. . Relationship between exposure to vector bites and antibody responses to mosquito salivary gland extracts. PLoS ONE. (2011) 6:e29107. 10.1371/journal.pone.0029107 PubMed DOI PMC

Rego ROM, Trentelman JJA, Anguita J, Nijhof AM, Sprong H, Klempa B, et al. . Counterattacking the tick bite: towards a rational design of anti-tick vaccines targeting pathogen transmission. Parasit Vectors. (2019) 12:229. 10.1186/s13071-019-3468-x PubMed DOI PMC

Karim S, Ribeiro JM. An insight into the sialome of the lone star tick, Amblyomma americanum, with a glimpse on its time dependent gene expression. PLoS ONE. (2015) 10:e0131292. 10.1371/journal.pone.0131292 PubMed DOI PMC

Sugino M, Imamura S, Mulenga A, Nakajima M, Tsuda A, Ohashi K, et al. . 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. (2003) 21:2844–51. 10.1016/S0264-410X(03)00167-1 PubMed DOI

Liu L, Cheng TY, He XM. Proteomic profiling of the midgut contents of Haemaphysalis flava. Ticks Tick Borne Dis. (2018) 9:490–5. 10.1016/j.ttbdis.2018.01.008 PubMed DOI

Tirloni L, Reck J, Terra RM, Martins JR, Mulenga A, Sherman NE, et al. . Proteomic analysis of cattle tick Rhipicephalus (Boophilus) microplus saliva: a comparison between partially and fully engorged females. PLoS ONE. (2014) 9:e94831. 10.1371/journal.pone.0094831 PubMed DOI PMC

Lewis LA, Radulovic ZM, Kim TK, Porter LM, Mulenga A. Identification of 24h ixodes scapularis immunogenic tick saliva proteins. Ticks Tick Borne Dis. (2015) 6:424–34. 10.1016/j.ttbdis.2015.03.012 PubMed DOI PMC

Sottrup-Jensen L, Stepanik TM, Kristensen T, Lonblad PB, Jones CM, Wierzbicki DM, et al. . Common evolutionary origin of alpha 2-macroglobulin and complement components C3 and C4. Proc Natl Acad Sci USA. (1985) 82:9–13. 10.1073/pnas.82.1.9 PubMed DOI PMC

Londono-Renteria B, Grippin C, Cardenas JC, Troupin A, Colpitts TM. Human C5a protein participates in the mosquito immune response against dengue virus. J Med Entomol. (2016) 53:505–12. 10.1093/jme/tjw003 PubMed DOI PMC

Maya-Monteiro CM, Daffre S, Logullo C, Lara FA, Alves EW, Capurro ML, et al. . HeLp, a heme lipoprotein from the hemolymph of the cattle tick, Boophilus microplus. J Biol Chem. (2000) 275:36584–9. 10.1074/jbc.M007344200 PubMed DOI

Tian Y, Chen W, Mo G, Chen R, Fang M, Yedid G, et al. . An immunosuppressant peptide from the hard tick Amblyomma variegatum. Toxins. (2016) 8:E133. 10.3390/toxins8050133 PubMed DOI PMC

Ramachandra RN, Wikel SK. Modulation of host-immune responses by ticks (Acari: Ixodidae): effect of salivary gland extracts on host macrophages and lymphocyte cytokine production. J Med Entomol. (1992) 29:818–26. 10.1093/jmedent/29.5.818 PubMed DOI

Beaufays J, Adam B, Decrem Y, Prevot PP, Santini S, Brasseur R, et al. . Ixodes ricinus tick lipocalins: identification, cloning, phylogenetic analysis and biochemical characterization. PLoS ONE. (2008) 3:e3941. 10.1371/journal.pone.0003941 PubMed DOI PMC

Mans BJ, Louw AI, Neitz AW. The major tick salivary gland proteins and toxins from the soft tick, Ornithodoros savignyi, are part of the tick Lipocalin family: implications for the origins of tick toxicoses. Mol Biol Evol. (2003) 20:1158–67. 10.1093/molbev/msg126 PubMed DOI

Frasca D, Romero M, Diaz A, Alter-Wolf S, Ratliff M, Landin AM, et al. . A molecular mechanism for TNF-alpha-mediated downregulation of B cell responses. J Immunol. (2012) 188:279–86. 10.4049/jimmunol.1003964 PubMed DOI PMC

Rieckmann P, Tuscano JM, Kehrl JH. Tumor necrosis factor-alpha (TNF-alpha) and interleukin-6 (IL-6) in B-lymphocyte function. Methods. (1997) 11:128–32. 10.1006/meth.1996.0396 PubMed DOI

Liu XJ, Liu T, Chen G, Wang B, Yu XL, Yin C, et al. . TLR signaling adaptor protein MyD88 in primary sensory neurons contributes to persistent inflammatory and neuropathic pain and neuroinflammation. Sci Rep. (2016) 6:28188. 10.1038/srep28188 PubMed DOI PMC

Li M, Feng B, Wang L, Guo S, Zhang P, Gong J, et al. . Tollip is a critical mediator of cerebral ischaemia-reperfusion injury. J Pathol. (2015) 237:249–62. 10.1002/path.4565 PubMed DOI

Haque A, Ray SK, Cox A, Banik NL. Neuron specific enolase: a promising therapeutic target in acute spinal cord injury. Metab Brain Dis. (2016) 31:487–95. 10.1007/s11011-016-9801-6 PubMed DOI PMC

Borawski K, Pancewicz S, Czupryna P, Zajkowska J, Moniuszko-Malinowska A. Tick paralysis. Przegl Epidemiol. (2018) 72:17–24. PubMed

Pienaar R, Neitz AWH, Mans BJ. Tick paralysis: solving an enigma. Vet Sci. (2018) 5:E53. 10.3390/vetsci5020053 PubMed DOI PMC

Shipley MM, Mangold CA, Szpara ML. Differentiation of the SH-SY5Y human neuroblastoma cell line. J Vis Exp. (2016) 53193. 10.3791/53193 PubMed DOI PMC

Trout RT, Steelman CD, Szalanski AL. Population genetics of Amblyomma americanum (Acari: Ixodidae) collected from Arkansas. J Med Entomol. (2010) 47:152–61. 10.1093/jmedent/47.2.152 PubMed DOI

Barrett LG, Thrall PH, Burdon JJ, Linde CC. Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends Ecol Evol. (2008) 23:678–85. 10.1016/j.tree.2008.06.017 PubMed DOI PMC

Cardenas JC, Drame PM, Luque-Burgos KA, Berrio JD, Entrena-Mutis E, Gonzalez MU, et al. . IgG1 and IgG4 antibodies against Aedes aegypti salivary proteins and risk for dengue infections. PLoS ONE. (2019) 14:e0208455. 10.1371/journal.pone.0208455 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...