Abstract
Hydrogen peroxide (H2O2) and hydroxyl radicals (HO·) are generated through partial reduction of oxygen. The HO· are the most reactive and have a shorter half-life than H2O2, they are produced from comparatively stable H2O2 through Fenton reaction. Although controlling HO· is important and biologically advantageous for organisms, it may be difficult. Ticks are obligate hematophagous arthropods that need blood feeding for development. Ticks feed on vertebrate blood containing high levels of iron. Ticks also concentrate iron-containing host blood, leading to high levels of iron in ticks. Host-derived iron may react with oxygen in the tick body, resulting in high concentrations of H2O2. On the other hand, ticks have antioxidant enzymes, such as peroxiredoxins (Prxs), to scavenge H2O2. Gene silencing of Prxs in ticks affects their blood feeding, oviposition, and H2O2 concentration. Therefore, Prxs could play important roles in ticks’ blood feeding and oviposition through the regulation of the H2O2 concentration. This review discusses the current knowledge of Prxs in hard ticks. Tick Prxs are also multifunctional molecules related to antioxidants and immunity like other organisms. In addition, tick Prxs play a role in regulating the host immune response for ticks’ survival in the host body. Tick Prx also can induce Th2 immune response in the host. Thus, this review would contribute to the further understanding of the tick’s antioxidant responses during blood feeding and the search for a candidate target for tick control.
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References
Adamson S, Browning R, Nobles S, Villarreal A, Karim S (2014) Transcriptional activation of antioxidants may compensate for selenoprotein deficiencies in Amblyomma maculatum (Acari: Ixodidae) injected with selK- or selM-dsRNA. Insect Mol Biol 23:497–510. https://doi.org/10.1111/imb.12098
Ahn HM, Lee KS, Lee DS, Yu K (2012) JNK/FOXO mediated PeroxiredoxinV expression regulates redox homeostasis during Drosophila melanogaster gut infection. Dev Comp Immunol 38:466–473. https://doi.org/10.1016/j.dci.2012.07.002
Avarre JC, Lubzens E, Babin PJ (2007) Apolipocrustacein, formerly vitellogenin, is the major egg yolk precursor protein in decapod crustaceans and is homologous to insect apolipophorin II/I and vertebrate apolipoprotein B. BMC Evol Biol 7:3. https://doi.org/10.1186/1471-2148-7-3
Boldbaatar D, Umemiya-Shirafuji R, Liao M, Tanaka T, Xuan X, Fujisaki K (2010) Multiple vitellogenins from the Haemaphysalis longicornis tick are crucial for ovarian development. J Insect Physiol 56:1587–1598. https://doi.org/10.1016/j.jinsphys.2010.05.019
Braz GR, Coelho HS, Masuda H, Oliveira PL (1999) A missing metabolic pathway in the cattle tick Boophilus microplus. Curr Biol 9:703–706
Budachetri K, Crispell G, Karim S (2017a) Amblyomma maculatum SECIS binding protein 2 and putative selenoprotein P are indispensable for pathogen replication and tick fecundity. Insect Biochem Mol Biol 88:37–47. https://doi.org/10.1016/j.ibmb.2017.07.006
Budachetri K, Kumar D, Karim S (2017b) Catalase is a determinant of the colonization and transovarial transmission of Rickettsia parkeri in the Gulf Coast tick Amblyomma maculatum. Insect Mol Biol 26:414–419. https://doi.org/10.1111/imb.12304
Choi HJ, Kang SW, Yang CH, Rhee SG, Ryu SE (1998) Crystal structure of a novel human peroxidase enzyme at 2.0 A resolution. Nat Struct Biol 5:400–406
Citelli M, Lara FA, da Silva Vaz I, Oliveira PL (2007) Oxidative stress impairs heme detoxification in the midgut of the cattle tick, Rhipicephalus (Boophilus) microplus. Mol Biochem Parasitol 151:81–88. https://doi.org/10.1016/j.molbiopara.2006.10.008
Connat JL (1991) Demonstration of regurgitation of gut content during blood meals of the tick Ornithodoros moubata. Possible role in the transmission of pathogenic agents. Parasitol Res 77:452–454
Daifalla NS, Bayih AG, Gedamu L (2011) Immunogenicity of Leishmania donovani iron superoxide dismutase B1 and peroxidoxin 4 in BALB/c mice: the contribution of Toll-like receptor agonists as adjuvant. Exp Parasitol 129:292–298. https://doi.org/10.1016/j.exppara.2011.07.001
Dalton JP, Robinson MW, Mulcahy G, O’Neill SM, Donnelly S (2013) Immunomodulatory molecules of Fasciola hepatica: candidates for both vaccine and immunotherapeutic development. Vet Parasitol 195:272–285. https://doi.org/10.1016/j.vetpar.2013.04.008
Donnelly S, Stack CM, O’Neill SM, Sayed AA, Williams DL, Dalton JP (2008) Helminth 2-Cys peroxiredoxin drives Th2 responses through a mechanism involving alternatively activated macrophages. FASEB J 22:4022–4032. https://doi.org/10.1096/fj.08-106278
Franta Z, Frantová H, Konvičková J, Horn M, Sojka D, Mareš M, Kopáček P (2010) Dynamics of digestive proteolytic system during blood feeding of the hard tick Ixodes ricinus. Parasit Vectors 3:119. https://doi.org/10.1186/1756-3305-3-119
Galay RL, Umemiya-Shirafuji R, Bacolod ET, Maeda H, Kusakisako K, Koyama J, Tsuji N, Mochizuki M, Fujisaki K, Tanaka T (2014) Two kinds of ferritin protect ixodid ticks from iron overload and consequent oxidative stress. PLoS ONE 9:e90661. https://doi.org/10.1371/journal.pone.0090661
Grandjean O (1983) Blood digestion in Ornithodorus moubata Murray sensu stricto Walton females (Ixodoidea: Argasidae) II. Modifications of midgut cells related to the digestive cycle and to the triggering action of mating. Ann Parasitol Hum Comp 58:493–514
Gretes MC, Poole LB, Karplus PA (2012) Peroxiredoxins in parasites. Antioxid Redox Signal 17:608–633. https://doi.org/10.1089/ars.2011.4404
Hall A, Karplus PA, Poole LB (2009) Typical 2-Cys peroxiredoxins–structures, mechanisms and functions. FEBS J 276:2469–2477. https://doi.org/10.1111/j.1742-4658.2009.06985.x
Hall A, Nelson K, Poole LB, Karplus PA (2011) Structure-based insights into the catalytic power and conformational dexterity of peroxiredoxins. Antioxid Redox Signal 15:795–815. https://doi.org/10.1089/ars.2010.3624
Halliwell B, Gutteridge JM (1986) Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts. Arch Biochem Biophys 246:501–514
Heekin AM, Guerrero FD, Bendele KG, Saldivar L, Scoles GA, Dowd SE, Gondro C, Nene V, Djikeng A, Brayton KA (2013a) Gut transcriptome of replete adult female cattle ticks, Rhipicephalus (Boophilus) microplus, feeding upon a Babesia bovis-infected bovine host. Parasitol Res 112:3075–3090. https://doi.org/10.1007/s00436-013-3482-4
Heekin AM, Guerrero FD, Bendele KG, Saldivar L, Scoles GA, Dowd SE, Gondro C, Nene V, Djikeng A, Brayton KA (2013b) The ovarian transcriptome of the cattle tick, Rhipicephalus (Boophilus) microplus, feeding upon a bovine host infected with Babesia bovis. Parasit Vectors 6:276. https://doi.org/10.1186/1756-3305-6-276
Hofmann B, Hecht H-J, Flohé L (2002) Peroxiredoxins. Biol Chem 383:347–364. https://doi.org/10.1515/BC.2002.040
Hoogstraal H (1985) Argasid and nuttalliellid ticks as parasites and vectors. Adv Parasitol 24:135–238
Kawazu S, Komaki-Yasuda K, Oku H, Kano S (2008) Peroxiredoxins in malaria parasites: parasitologic aspects. Parasitol Int 57:1–7. https://doi.org/10.1016/j.parint.2007.08.001
Kelley LA, Sternberg MJE (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363–371. https://doi.org/10.1038/nprot.2009.2
Kim TK, Tirloni L, Pinto AF, Moresco J, Yates JR 3rd, da Silva Vaz I Jr, Mulenga A (2016) Ixodes scapularis tick saliva proteins sequentially secreted every 24 h during blood feeding. PLoS Negl Trop Dis 10:e0004323. https://doi.org/10.1371/journal.pntd.0004323
Kitaoka S (1961) Physiological and ecological studies on some ticks. VII. Parthenogeneticand bisexual races of Haemaphysalis bispinosa in Japan and experimental crossing between them. Natl Inst Anim Health Q (Tokyo) 1:142–149
Kumar D, Budachetri K, Meyers VC, Karim S (2016) Assessment of tick antioxidant responses to exogenous oxidative stressors and insight into the role of catalase in the reproductive fitness of the Gulf Coast tick, Amblyomma maculatum. Insect Mol Biol 25:283–294. https://doi.org/10.1111/imb.12218
Kusakisako K, Galay RL, Umemiya-Shirafuji R, Hernandez EP, Maeda H, Talactac MR, Tsuji N, Mochizuki M, Fujisaki K, Tanaka T (2016a) 2-Cys peroxiredoxin is required in successful blood-feeding, reproduction, and antioxidant response in the hard tick Haemaphysalis longicornis. Parasit Vectors 9:457. https://doi.org/10.1186/s13071-016-1748-2
Kusakisako K, Masatani T, Miyata T, Galay RL, Maeda H, Talactac MR, Tsuji N, Mochizuki M, Fujisaki K, Tanaka T (2016b) Functional analysis of recombinant 2-Cys peroxiredoxin from the hard tick Haemaphysalis longicornis. Insect Mol Biol 25:16–23. https://doi.org/10.1111/imb.12193
Kusakisako K, Miyata T, Tsujio M, Galay RL, Talactac MR, Hernandez EP, Fujisaki K, Tanaka T (2018) Evaluation of vaccine potential of 2-Cys peroxiredoxin from the hard tick Haemaphysalis longicornis. Exp Appl Acarol 74:73–84. https://doi.org/10.1007/s10493-018-0209-3
Lara FA, Lins U, Paiva-Silva G, Almeida IC, Braga CM, Miguens FC, Oliveira PL, Dansa-Petretski M (2003) A new intracellular pathway of haem detoxification in the midgut of the cattle tick Boophilus microplus: aggregation inside a specialized organelle, the hemosome. J Exp Biol 206:1707–1715
Lu J, Holmgren A (2014) The thioredoxin antioxidant system. Free Radic Biol Med 66:75–87. https://doi.org/10.1016/j.freeradbiomed.2013.07.036
Mendes RE, Pérez-Ecija RA, Zafra R, Buffoni L, Martínez-Moreno A, Dalton JP, Mulcahy G, Pérez J (2010) Evaluation of hepatic changes and local and systemic immune responses in goats immunized with recombinant Peroxiredoxin (Prx) and challenged with Fasciola hepatica. Vaccine 28:2832–2840. https://doi.org/10.1016/j.vaccine.2010.01.055
Mitozo PA, de Souza LF, Loch-Neckel G, Flesch S, Maris AF, Figueiredo CP, Dos Santos AR, Farina M, Dafre AL (2011) A study of the relative importance of the peroxiredoxin-, catalase-, and glutathione-dependent systems in neural peroxide metabolism. Free Radic Biol Med 51:69–77. https://doi.org/10.1016/j.freeradbiomed.2011.03.017
Morais MA, Giuseppe PO, Souza TA, Alegria TG, Oliveira MA, Netto LE, Murakami MT (2015) How pH modulates the dimer-decamer interconversion of 2-Cys peroxiredoxins from the Prx1 subfamily. J Biol Chem 290:8582–8590. https://doi.org/10.1074/jbc.M114.619205
Mori H, Galay RL, Maeda H, Matsuo T, Umemiya-Shirafuji R, Mochizuki M, Fujisaki K, Tanaka T (2014) Host-derived transferrin is maintained and transferred from midgut to ovary in Haemaphysalis longicornis ticks. Ticks Tick Borne Dis 5:121–126. https://doi.org/10.1016/j.ttbdis.2013.09.004
Narasimhan S, Sukumaran B, Bozdogan U, Thomas V, Liang X, DePonte K, Marcantonio N, Koski RA, Anderson JF, Kantor F, Fikrig E (2007) A tick antioxidant facilitates the Lyme disease agent’s successful migration from the mammalian host to the arthropod vector. Cell Host Microbe 2:7–18. https://doi.org/10.1016/j.chom.2007.06.001
Perner J, Provazník J, Schrenková J, Urbanová V, Ribeiro JM, Kopáček P (2016a) RNA-seq analyses of the midgut from blood- and serum-fed Ixodes ricinus ticks. Sci Rep 6:36695. https://doi.org/10.1038/srep36695
Perner J, Sobotka R, Sima R, Konvickova J, Sojka D, Oliveira PL, Hajdusek O, Kopacek P (2016b) Acquisition of exogenous haem is essential for tick reproduction. elife. https://doi.org/10.7554/elife.12318
Rachinsky A, Guerrero FD, Scoles GA (2008) Proteomic profiling of Rhipicephalus (Boophilus) microplus midgut responses to infection with Babesia bovis. Vet Parasitol 152:294–313. https://doi.org/10.1016/j.vetpar.2007.12.027
Radyuk SN, Michalak K, Klichko VI, Benes J, Orr WC (2010) Peroxiredoxin 5 modulates immune response in Drosophila. Biochim Biophys Acta 1800:1153–1163. https://doi.org/10.1016/j.bbagen.2010.06.010
Raina OK, Nagar G, Vrarghese A, Prajitha G, Alex A, Maharana BR, Joshi P (2011) Lack of protective efficacy in buffaloes vaccinated with Fasciola gigantica leucine aminopeptidase and peroxiredoxin recombinant proteins. Acta Trop 118:217–222. https://doi.org/10.1016/j.actatropica.2011.02.008
Royet J, Reichhart J-M, Hoffmann JA (2005) Sensing and signaling during infection in Drosophila. Curr Opin Immunol 17:11–17. https://doi.org/10.1016/j.coi.2004.12.002
Rudenko N, Golovchenko M, Edwards MJ, Grubhoffer L (2005) Differential expression of Ixodes ricinus tick genes induced by blood feeding or Borrelia burgdorferi infection. J Med Entomol 42:36–41
Schmid-Hempel P (2005) Evolutionary ecology of insect immune defenses. Annu Rev Entomol 50:529–551. https://doi.org/10.1146/annurev.ento.50.071803.130420
Schröder E, Littlechild JA, Lebedev AA, Errington N, Vagin AA, Isupov MN (2000) Crystal structure of decameric 2-Cys peroxiredoxin from human erythrocytes at 1.7 A resolution. Structure 8:605–615
Seehuus SC, Norberg K, Gimsa U, Krekling T, Amdam GV (2006) Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc Natl Acad Sci USA 103:962–967. https://doi.org/10.1073/pnas.0502681103
Seo MS, Kang SW, Kim K, Baines IC, Lee TH, Rhee SG (2000) Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J Biol Chem 275:20346–20354. https://doi.org/10.1074/jbc.M001943200
Sies H (1991) Oxidative stress: from basic research to clinical application. Am J Med 91:31S–38S
Tirloni L, Islam MS, Kim TK, Diedrich JK, Yates JR 3rd, Pinto AF, Mulenga A, You MJ, Da Silva Vaz I Jr (2015) Saliva from nymph and adult females of Haemaphysalis longicornis: a proteomic study. Parasit Vectors 8:338. https://doi.org/10.1186/s13071-015-0918-y
Tsuji N, Kamio T, Isobe T, Fujisaki K (2001) Molecular characterization of a peroxiredoxin from the hard tick Haemaphysalis longicornis. Insect Mol Biol 10:121–129
Wada T, Ishiwata K, Koseki H, Ishikura T, Ugajin T, Ohnuma N, Obata K, Ishikawa R, Yoshikawa S, Mukai K, Kawano Y, Minegishi Y, Yokozeki H, Watanabe N, Karasuyama H (2010) Selective ablation of basophils in mice reveals their nonredundant role in acquired immunity against ticks. J Clin Invest 120:2867–2875. https://doi.org/10.1172/JCI42680
Wang X, Wang L, Wang X, Sun F, Wang CC (2012) Structural insights into the peroxidase activity and inactivation of human peroxiredoxin 4. Biochem J 441:113–118. https://doi.org/10.1042/BJ20110380
Wood ZA, Poole LB, Hantgan RR, Karplus PA (2002) Dimers to doughnuts: redox-sensitive oligomerization of 2-cysteine peroxiredoxins. Biochemistry 41:5493–5504
Wood ZA, Schröder E, Robin Harris J, Poole LB (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28:32–40. https://doi.org/10.1016/S0968-0004(02)00003-8
Yoshimoto T, Yasuda K, Tanaka H, Nakahira M, Imai Y, Fujimori Y, Nakanishi K (2009) Basophils contribute to TH2-IgE responses in vivo via IL-4 production and presentation of peptide-MHC class II complexes to CD4+ T cells. Nat Immunol 10:706–712. https://doi.org/10.1038/ni.1737
Acknowledgements
We are grateful to M.R. Talactac and E.P. Hernandez of the Laboratory of Infectious Diseases, Joint Faculty of Veterinary Medicine, Kagoshima University, for their helpful comments and suggestions regarding this manuscript. These studies were funded by the Japan Society for the Promotion of Science (JSPS) KAKENHI Grant Numbers 25252050, 25292173, 26460511, 26660229, 15H05264, 16H05028, and 16J08221; and Cooperative Research Grant (27-joint-11 and 29-joint-8) of the National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine. K. Kusakisako is supported by a Grant-in-Aid for JSPS fellows.
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Kusakisako, K., Fujisaki, K. & Tanaka, T. The multiple roles of peroxiredoxins in tick blood feeding. Exp Appl Acarol 75, 269–280 (2018). https://doi.org/10.1007/s10493-018-0273-8
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DOI: https://doi.org/10.1007/s10493-018-0273-8