Acquisition of exogenous haem is essential for tick reproduction

. 2016 Mar 07 ; 5 () : . [epub] 20160307

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid26949258

Haem and iron homeostasis in most eukaryotic cells is based on a balanced flux between haem biosynthesis and haem oxygenase-mediated degradation. Unlike most eukaryotes, ticks possess an incomplete haem biosynthetic pathway and, together with other (non-haematophagous) mites, lack a gene encoding haem oxygenase. We demonstrated, by membrane feeding, that ticks do not acquire bioavailable iron from haemoglobin-derived haem. However, ticks require dietary haemoglobin as an exogenous source of haem since, feeding with haemoglobin-depleted serum led to aborted embryogenesis. Supplementation of serum with haemoglobin fully restored egg fertility. Surprisingly, haemoglobin could be completely substituted by serum proteins for the provision of amino-acids in vitellogenesis. Acquired haem is distributed by haemolymph carrier protein(s) and sequestered by vitellins in the developing oocytes. This work extends, substantially, current knowledge of haem auxotrophy in ticks and underscores the importance of haem and iron metabolism as rational targets for anti-tick interventions.

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Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, Sutton GG, Wortman JR, Yandell MD, Zhang Q, Chen LX, Brandon RC, Rogers YH, Blazej RG, Champe M, Pfeiffer BD, Wan KH, Doyle C, Baxter EG, Helt G, Nelson CR, Gabor GL, Abril JF, Agbayani A, An HJ, Andrews-Pfannkoch C, Baldwin D, Ballew RM, Basu A, Baxendale J, Bayraktaroglu L, Beasley EM, Beeson KY, Benos PV, Berman BP, Bhandari D, Bolshakov S, Borkova D, Botchan MR, Bouck J, Brokstein P, Brottier P, Burtis KC, Busam DA, Butler H, Cadieu E, Center A, Chandra I, Cherry JM, Cawley S, Dahlke C, Davenport LB, Davies P, de Pablos B, Delcher A, Deng Z, Mays AD, Dew I, Dietz SM, Dodson K, Doup LE, Downes M, Dugan-Rocha S, Dunkov BC, Dunn P, Durbin KJ, Evangelista CC, Ferraz C, Ferriera S, Fleischmann W, Fosler C, Gabrielian AE, Garg NS, Gelbart WM, Glasser K, Glodek A, Gong F, Gorrell JH, Gu Z, Guan P, Harris M, Harris NL, Harvey D, Heiman TJ, Hernandez JR, Houck J, Hostin D, Houston KA, Howland TJ, Wei MH, Ibegwam C, Jalali M, Kalush F, Karpen GH, Ke Z, Kennison JA, Ketchum KA, Kimmel BE, Kodira CD, Kraft C, Kravitz S, Kulp D, Lai Z, Lasko P, Lei Y, Levitsky AA, Li J, Li Z, Liang Y, Lin X, Liu X, Mattei B, McIntosh TC, McLeod MP, McPherson D, Merkulov G, Milshina NV, Mobarry C, Morris J, Moshrefi A, Mount SM, Moy M, Murphy B, Murphy L, Muzny DM, Nelson DL, Nelson DR, Nelson KA, Nixon K, Nusskern DR, Pacleb JM, Palazzolo M, Pittman GS, Pan S, Pollard J, Puri V, Reese MG, Reinert K, Remington K, Saunders RD, Scheeler F, Shen H, Shue BC, Sidén-Kiamos I, Simpson M, Skupski MP, Smith T, Spier E, Spradling AC, Stapleton M, Strong R, Sun E, Svirskas R, Tector C, Turner R, Venter E, Wang AH, Wang X, Wang ZY, Wassarman DA, Weinstock GM, Weissenbach J, Williams SM, Woodage T, Worley KC, Wu D, Yang S, Yao QA, Ye J, Yeh RF, Zaveri JS, Zhan M, Zhang G, Zhao Q, Zheng L, Zheng XH, Zhong FN, Zhong W, Zhou X, Zhu S, Zhu X, Smith HO, Gibbs RA, Myers EW, Rubin GM, Venter JC. The genome sequence of Drosophila melanogaster. Science. 2000;287:2185–2195. doi: 10.1126/science.287.5461.2185. PubMed DOI

Atamna H, Ginsburg H. Heme degradation in the presence of glutathione. A proposed mechanism to account for the high levels of non-heme iron found in the membranes of hemoglobinopathic red blood cells. Journal of Biological Chemistry. 1995;270:24876–24883. doi: 10.1074/jbc.270.42.24876. PubMed DOI

Boldbaatar D, Umemiya-Shirafuji R, Liao M, Tanaka T, Xuan X, Fujisaki K. Multiple vitellogenins from the Haemaphysalis longicornis tick are crucial for ovarian development. Journal of Insect Physiology. 2010;56:1587–1598. doi: 10.1016/j.jinsphys.2010.05.019. PubMed DOI

Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. PubMed DOI

Brayton KA, Lau AOT, Herndon DR, Hannick L, Kappmeyer LS, Berens SJ, Bidwell SL, Brown WC, Crabtree J, Fadrosh D, Feldblum T, Forberger HA, Haas BJ, Howell JM, Khouri H, Koo H, Mann DJ, Norimine J, Paulsen IT, Radune D, Ren Q, Smith RK, Suarez CE, White O, Wortman JR, Knowles DP, McElwain TF, Nene VM. Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa. PLoS Pathogens. 2007;3:1401–1413. doi: 10.1371/journal.ppat.0030148. PubMed DOI PMC

Braz GRC, Coelho HSL, Masuda H, Oliveira PL. A missing metabolic pathway in the cattle tick Boophilus microplus. Current Biology. 1999;9:703–706. doi: 10.1016/S0960-9822(99)80312-1. PubMed DOI

Chipman AD, Ferrier DE, Brena C, Qu J, Hughes DS, Schröder R, Torres-Oliva M, Znassi N, Jiang H, Almeida FC, Alonso CR, Apostolou Z, Aqrawi P, Arthur W, Barna JC, Blankenburg KP, Brites D, Capella-Gutiérrez S, Coyle M, Dearden PK, Du Pasquier L, Duncan EJ, Ebert D, Eibner C, Erikson G, Evans PD, Extavour CG, Francisco L, Gabaldón T, Gillis WJ, Goodwin-Horn EA, Green JE, Griffiths-Jones S, Grimmelikhuijzen CJ, Gubbala S, Guigó R, Han Y, Hauser F, Havlak P, Hayden L, Helbing S, Holder M, Hui JH, Hunn JP, Hunnekuhl VS, Jackson L, Javaid M, Jhangiani SN, Jiggins FM, Jones TE, Kaiser TS, Kalra D, Kenny NJ, Korchina V, Kovar CL, Kraus FB, Lapraz F, Lee SL, Lv J, Mandapat C, Manning G, Mariotti M, Mata R, Mathew T, Neumann T, Newsham I, Ngo DN, Ninova M, Okwuonu G, Ongeri F, Palmer WJ, Patil S, Patraquim P, Pham C, Pu LL, Putman NH, Rabouille C, Ramos OM, Rhodes AC, Robertson HE, Robertson HM, Ronshaugen M, Rozas J, Saada N, Sánchez-Gracia A, Scherer SE, Schurko AM, Siggens KW, Simmons D, Stief A, Stolle E, Telford MJ, Tessmar-Raible K, Thornton R, van der Zee M, von Haeseler A, Williams JM, Willis JH, Wu Y, Zou X, Lawson D, Muzny DM, Worley KC, Gibbs RA, Akam M, Richards S. The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima. PLoS Biology. 2014;12:e12318. doi: 10.1371/journal.pbio.1002005. PubMed DOI PMC

Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A, Oakley TH, Tokishita S, Aerts A, Arnold GJ, Basu MK, Bauer DJ, Caceres CE, Carmel L, Casola C, Choi J-H, Detter JC, Dong Q, Dusheyko S, Eads BD, Frohlich T, Geiler-Samerotte KA, Gerlach D, Hatcher P, Jogdeo S, Krijgsveld J, Kriventseva EV, Kultz D, Laforsch C, Lindquist E, Lopez J, Manak JR, Muller J, Pangilinan J, Patwardhan RP, Pitluck S, Pritham EJ, Rechtsteiner A, Rho M, Rogozin IB, Sakarya O, Salamov A, Schaack S, Shapiro H, Shiga Y, Skalitzky C, Smith Z, Souvorov A, Sung W, Tang Z, Tsuchiya D, Tu H, Vos H, Wang M, Wolf YI, Yamagata H, Yamada T, Ye Y, Shaw JR, Andrews J, Crease TJ, Tang H, Lucas SM, Robertson HM, Bork P, Koonin EV, Zdobnov EM, Grigoriev IV, Lynch M, Boore JL. The ecoresponsive genome of Daphnia pulex. Science. 2011;331:555–561. doi: 10.1126/science.1197761. PubMed DOI PMC

Croucher PJP, Brewer MS, Winchell CJ, Oxford GS, Gillespie RG. De novo characterization of the gene-rich transcriptomes of two color-polymorphic spiders, Theridion grallator and T. californicum (Araneae: Theridiidae), with special reference to pigment genes. BMC Genomics. 2013;14:862. doi: 10.1186/1471-2164-14-862. PubMed DOI PMC

Donohue KV, Khalil SMS, Mitchell RD, Sonenshine DE, Michael Roe R. Molecular characterization of the major hemelipoglycoprotein in ixodid ticks. Insect Molecular Biology. 2008;17:197–208. doi: 10.1111/j.1365-2583.2008.00794.x. PubMed DOI

Donohue KV, Khalil SMS, Sonenshine DE, Roe RM. Heme-binding storage proteins in the Chelicerata. Journal of Insect Physiology. 2009;55:287–296. doi: 10.1016/j.jinsphys.2009.01.002. PubMed DOI

Dunn LL, Rahmanto YS, Richardson DR. Iron uptake and metabolism in the new millennium. Trends in Cell Biology. 2007;17:93–100. doi: 10.1016/j.tcb.2006.12.003. PubMed DOI

Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV, Haddock SHD, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature. 2008;452:745–749. doi: 10.1038/nature06614. PubMed DOI

Furuyama K, Kaneko K, Vargas V. PD. Heme as a magnificent molecule with multiple missions: Heme determines its own fate and governs cellular homeostasis. The Tohoku Journal of Experimental Medicine. 2007;213:1–16. doi: 10.1620/tjem.213.1. PubMed DOI

Galay RL, Aung KM, Umemiya-Shirafuji R, Maeda H, Matsuo T, Kawaguchi H, Miyoshi N, Suzuki H, Xuan X, Mochizuki M, Fujisaki K, Tanaka T. Multiple ferritins are vital to successful blood feeding and reproduction of the hard tick Haemaphysalis longicornis. Journal of Experimental Biology. 2013;216:1905–1915. doi: 10.1242/jeb.081240. PubMed DOI

Galay RL, Umemiya-Shirafuji R, Mochizuki M, Fujisaki K, Tanaka T. Iron metabolism in hard ticks (Acari: Ixodidae): The antidote to their toxic diet. Parasitology International. 2015;64:182–189. doi: 10.1016/j.parint.2014.12.005. PubMed DOI

Garcia G, Gardinassi L, Ribeiro J, Anatriello E, Ferreira B, Moreira HN, Mafra C, Martins M, Szabó MP, de Miranda-Santos IK, Maruyama S. The sialotranscriptome of Amblyomma triste, Amblyomma parvum and Amblyomma cajennense ticks, uncovered by 454-based RNA-seq. Parasites & Vectors. 2014;7:430. doi: 10.1186/1756-3305-7-430. PubMed DOI PMC

Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, Crabtree J, Allen JE, Delcher AL, Guiliano DB, Miranda-Saavedra D, Angiuoli SV, Creasy T, Amedeo P, Haas B, El-Sayed NM, Wortman JR, Feldblyum T, Tallon L, Schatz M, Shumway M, Koo H, Salzberg SL, Schobel S, Pertea M, Pop M, White O, Barton GJ, Carlow CKS, Crawford MJ, Daub J, Dimmic MW, Estes CF, Foster JM, Ganatra M, Gregory WF, Johnson NM, Jin J, Komuniecki R, Korf I, Kumar S, Laney S, Li B-W, Li W, Lindblom TH, Lustigman S, Ma D, Maina CV, Martin DMA, McCarter JP, McReynolds L, Mitreva M, Nutman TB, Parkinson J, Peregrin-Alvarez JM, Poole C, Ren Q, Saunders L, Sluder AE, Smith K, Stanke M, Unnasch TR, Ware J, Wei AD, Weil G, Williams DJ, Zhang Y, Williams SA, Fraser-Liggett C, Slatko B, Blaxter ML, Scott AL. Draft genome of the filarial nematode parasite brugia malayi. Science. 2007;317:1756–1760. doi: 10.1126/science.1145406. PubMed DOI PMC

Gozzelino R, Soares MP. Coupling heme and iron metabolism via Ferritin H chain. Antioxidants & Redox Signaling. 2014;20:1754–1769. doi: 10.1089/ars.2013.5666. PubMed DOI PMC

Graca-Souza A, Maya-Monteiro C, Paiva-Silva GO, Braz GR, Paes MC, Sorgine MH, Oliveira MF, Oliveira P. Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochemistry and Molecular Biology. 2006;36:322–335. doi: 10.1016/j.ibmb.2006.01.009. PubMed DOI

Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, Osborne EJ, Dermauw W, Thi Ngoc PC, Ortego F, Hernández-Crespo P, Diaz I, Martinez M, Navajas M, Sucena Élio, Magalhães S, Nagy L, Pace RM, Djuranović S, Smagghe G, Iga M, Christiaens O, Veenstra JA, Ewer J, Villalobos RM, Hutter JL, Hudson SD, Velez M, Yi SV, Zeng J, Pires-daSilva A, Roch F, Cazaux M, Navarro M, Zhurov V, Acevedo G, Bjelica A, Fawcett JA, Bonnet E, Martens C, Baele G, Wissler L, Sanchez-Rodriguez A, Tirry L, Blais C, Demeestere K, Henz SR, Gregory TR, Mathieu J, Verdon L, Farinelli L, Schmutz J, Lindquist E, Feyereisen R, Van de Peer Y. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature. 2011;479:487–492. doi: 10.1038/nature10640. PubMed DOI PMC

Grunclová L, Horn M, Vancová M, Sojka D, Franta Z, Mareš M, Kopáček P. Two secreted cystatins of the soft tick Ornithodoros moubata: differential expression pattern and inhibitory specificity. Biological Chemistry. 2006;387:1635–1644. doi: 10.1515/BC.2006.204. PubMed DOI

Gulia-Nuss M, Nuss AB, Meyer JM, Sonenshine DE, Roe RM, Waterhouse RM, Sattelle DB, de la Fuente J, Ribeiro JM, Megy K, Thimmapuram J, Miller JR, Walenz BP, Koren S, Hostetler JB, Thiagarajan M, Joardar VS, Hannick LI, Bidwell S, Hammond MP, Young S, Zeng Q, Abrudan JL, Almeida FC, Ayllón N, Bhide K, Bissinger BW, Bonzon-Kulichenko E, Buckingham SD, Caffrey DR, Caimano MJ, Croset V, Driscoll T, Gilbert D, Gillespie JJ, Giraldo-Calderón GI, Grabowski JM, Jiang D, Khalil SMS, Kim D, Kocan KM, Koči J, Kuhn RJ, Kurtti TJ, Lees K, Lang EG, Kennedy RC, Kwon H, Perera R, Qi Y, Radolf JD, Sakamoto JM, Sánchez-Gracia A, Severo MS, Silverman N, Šimo L, Tojo M, Tornador C, Van Zee JP, Vázquez J, Vieira FG, Villar M, Wespiser AR, Yang Y, Zhu J, Arensburger P, Pietrantonio PV, Barker SC, Shao R, Zdobnov EM, Hauser F, Grimmelikhuijzen CJP, Park Y, Rozas J, Benton R, Pedra JHF, Nelson DR, Unger MF, Tubio JMC, Tu Z, Robertson HM, Shumway M, Sutton G, Wortman JR, Lawson D, Wikel SK, Nene VM, Fraser CM, Collins FH, Birren B, Nelson KE, Caler E, Hill CA. Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nature Communications. 2016;7:10507. doi: 10.1038/ncomms10507. PubMed DOI PMC

Hajdusek O, Sojka D, Kopacek P, Buresova V, Franta Z, Sauman I, Winzerling J, Grubhoffer L. Knockdown of proteins involved in iron metabolism limits tick reproduction and development. Proceedings of the National Academy of Sciences of the United States of America. 2009;106:1033–1038. doi: 10.1073/pnas.0807961106. PubMed DOI PMC

Hajdusek O, Sima R, Perner J, Loosova G, Harcubova A, Kopacek P. Tick iron and heme metabolism – New target for an anti-tick intervention. Ticks and Tick-Borne Diseases. 2016 doi: 10.1016/j.ttbdis.2016.01.006. PubMed DOI

Hamza I, Dailey HA. One ring to rule them all: Trafficking of heme and heme synthesis intermediates in the metazoans. Biochimica Et Biophysica Acta (BBA) - Molecular Cell Research. 2012;1823:1617–1632. doi: 10.1016/j.bbamcr.2012.04.009. PubMed DOI PMC

Hentze MW, Muckenthaler MU, Andrews NC. Balancing acts. Cell. 2004;117:285–297. doi: 10.1016/S0092-8674(04)00343-5. PubMed DOI

Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JM, Wides R, Salzberg SL, Loftus B, Yandell M, Majoros WH, Rusch DB, Lai Z, Kraft CL, Abril JF, Anthouard V, Arensburger P, Atkinson PW, Baden H, de Berardinis V, Baldwin D, Benes V, Biedler J, Blass C, Bolanos R, Boscus D, Barnstead M, Cai S, Center A, Chaturverdi K, Christophides GK, Chrystal MA, Clamp M, Cravchik A, Curwen V, Dana A, Delcher A, Dew I, Evans CA, Flanigan M, Grundschober-Freimoser A, Friedli L, Gu Z, Guan P, Guigo R, Hillenmeyer ME, Hladun SL, Hogan JR, Hong YS, Hoover J, Jaillon O, Ke Z, Kodira C, Kokoza E, Koutsos A, Letunic I, Levitsky A, Liang Y, Lin JJ, Lobo NF, Lopez JR, Malek JA, McIntosh TC, Meister S, Miller J, Mobarry C, Mongin E, Murphy SD, O'Brochta DA, Pfannkoch C, Qi R, Regier MA, Remington K, Shao H, Sharakhova MV, Sitter CD, Shetty J, Smith TJ, Strong R, Sun J, Thomasova D, Ton LQ, Topalis P, Tu Z, Unger MF, Walenz B, Wang A, Wang J, Wang M, Wang X, Woodford KJ, Wortman JR, Wu M, Yao A, Zdobnov EM, Zhang H, Zhao Q, Zhao S, Zhu SC, Zhimulev I, Coluzzi M, della Torre A, Roth CW, Louis C, Kalush F, Mural RJ, Myers EW, Adams MD, Smith HO, Broder S, Gardner MJ, Fraser CM, Birney E, Bork P, Brey PT, Venter JC, Weissenbach J, Kafatos FC, Collins FH, Hoffman SL. The Genome sequence of the malaria mosquito Anopheles gambiae. Science. 2002;298:129–149. doi: 10.1126/science.1076181. PubMed DOI

James AM, Oliver JH. Purification and partial characterization of vitellin from the black-legged tick, Ixodes scapularis. Insect Biochemistry and Molecular Biology. 1997;27:639–649. doi: 10.1016/S0965-1748(97)00038-6. PubMed DOI

Jeney V, Balla J, Yachie A, Varga Z, Vercellotti GM, Eaton JW, Balla G. Pro-oxidant and cytotoxic effects of circulating heme. Blood. 2002;100:879–887. doi: 10.1182/blood.V100.3.879. PubMed DOI

Kanehisa M, Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Research. 2000;28:27–30. doi: 10.1093/nar/28.1.27. PubMed DOI PMC

Karim S, Ribeiro JMC. 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:e12318. doi: 10.1371/journal.pone.0131292. PubMed DOI PMC

Khalil SMS, Donohue KV, Thompson DM, Jeffers LA, Ananthapadmanaban U, Sonenshine DE, Mitchell RD, Roe RM. Full-length sequence, regulation and developmental studies of a second vitellogenin gene from the American dog tick, Dermacentor variabilis. Journal of Insect Physiology. 2011;57:400–408. doi: 10.1016/j.jinsphys.2010.12.008. PubMed DOI

Khan AA, Quigley JG. Control of intracellular heme levels: Heme transporters and heme oxygenases. Biochimica Et Biophysica Acta (BBA) - Molecular Cell Research. 2011;1813:668–682. doi: 10.1016/j.bbamcr.2011.01.008. PubMed DOI PMC

Klouche K, Morena M, Canaud B, Descomps B, Beraud JJ, Cristol JP. Mechanism of in vitro heme-induced LDL oxidation: effects of antioxidants. European Journal of Clinical Investigation. 2004;34:619–625. doi: 10.1111/j.1365-2362.2004.01395.x. PubMed DOI

Kopáček P, Ždychová J, Yoshiga T, Weise C, Rudenko N, Law JH. Molecular cloning, expression and isolation of ferritins from two tick species—Ornithodoros moubata and Ixodes ricinus. Insect Biochemistry and Molecular Biology. 2003;33:103–113. doi: 10.1016/S0965-1748(02)00181-9. PubMed DOI

Kořený L, Lukeš J, Oborník M. Evolution of the haem synthetic pathway in kinetoplastid flagellates: An essential pathway that is not essential after all? International Journal for Parasitology. 2010;40:149–156. doi: 10.1016/j.ijpara.2009.11.007. PubMed DOI

Kořený L, Oborník M, Lukeš J. Make it, Take it, or Leave it: Heme Metabolism of Parasites. PLoS Pathogens. 2013;9:e12318. doi: 10.1371/journal.ppat.1003088. PubMed DOI PMC

Kotsyfakis M, Schwarz A, Erhart J, Ribeiro JMC. Tissue- and time-dependent transcription in Ixodes ricinus salivary glands and midguts when blood feeding on the vertebrate host. Scientific Reports. 2015;5:9103. doi: 10.1038/srep09103. PubMed DOI PMC

Kröber T, Guerin PM. In vitro feeding assays for hard ticks. Trends in Parasitology. 2007;23:445–449. doi: 10.1016/j.pt.2007.07.010. PubMed DOI

Lara FA, Lins U, Paiva-Silva G, Almeida IC, Braga CM, Miguens FC, Oliveira PL, Dansa-Petretski M. A new intracellular pathway of haem detoxification in the midgut of the cattle tick Boophilus microplus: aggregation inside a specialized organelle, the hemosome. Journal of Experimental Biology. 2003;206:1707–1715. doi: 10.1242/jeb.00334. PubMed DOI

Lara FA, Lins U, Bechara GH, Oliveira PL. Tracing heme in a living cell: hemoglobin degradation and heme traffic in digest cells of the cattle tick Boophilus microplus. Journal of Experimental Biology. 2005;208:3093–3101. doi: 10.1242/jeb.01749. PubMed DOI

Lara FA, Pohl PC, Gandara AC, Ferreira Jessica da Silva, Nascimento-Silva MC, Bechara GH, Sorgine MHF, Almeida IC, Vaz Itabajara da Silva, Oliveira PL. ATP binding cassette transporter mediates both heme and pesticide detoxification in tick midgut cells. PLOS ONE. 2015;10:e12318. doi: 10.1371/journal.pone.0134779. PubMed DOI PMC

Levashina EA, Moita LF, Blandin S, Vriend G, Lagueux M, Kafatos FC. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell. 2001;104:709–718. doi: 10.1016/S0092-8674(01)00267-7. PubMed DOI

Logullo C, Moraes J, Dansa-Petretski M, Vaz IS, Masuda A, Sorgine MHF, Braz GR, Masuda H, Oliveira PL. Binding and storage of heme by vitellin from the cattle tick, Boophilus microplus. Insect Biochemistry and Molecular Biology. 2002;32:1805–1811. doi: 10.1016/S0965-1748(02)00162-5. PubMed DOI

Machado EA, Oliveira PL, Moreira MF, de Souza W, Masuda H. Uptake ofRhodnius heme-binding protein (RHBP) by the ovary ofRhodnius prolixus. Archives of Insect Biochemistry and Physiology. 1998;39:133–143. doi: 10.1002/(SICI)1520-6327(1998)39:4<133::AID-ARCH1>3.0.CO;2-D. PubMed DOI

Maya-Monteiro CM, Daffre S, Logullo C, Lara FA, Alves EW, Capurro ML, Zingali R, Almeida IC, Oliveira PL. HeLp, a Heme Lipoprotein from the Hemolymph of the Cattle Tick, Boophilus microplus. Journal of Biological Chemistry. 2000;275:36584–36589. doi: 10.1074/jbc.M007344200. PubMed DOI

McDonnel A, Staehelin LA. Detection of cytochrome f, a c-Class cytochrome, with diaminobenzidine in polyacrylamide gels. Analytical Biochemistry. 1981;117:40–44. doi: 10.1016/0003-2697(81)90688-6. PubMed DOI

Mori H, Galay RL, Maeda H, Matsuo T, Umemiya-Shirafuji R, Mochizuki M, Fujisaki K, Tanaka T. Host-derived transferrin is maintained and transferred from midgut to ovary in Haemaphysalis longicornis ticks. Ticks and Tick-Borne Diseases. 2014;5:121–126. doi: 10.1016/j.ttbdis.2013.09.004. PubMed DOI

Nijhof AM, Balk JA, Postigo M, Jongejan F. Selection of reference genes for quantitative RT-PCR studies in Rhipicephalus (Boophilus) microplus and Rhipicephalus appendiculatus ticks and determination of the expression profile of Bm86. BMC Molecular Biology. 2009;10:112. doi: 10.1186/1471-2199-10-112. PubMed DOI PMC

Oliveira MF, d'Avila JCP, Torres CR, Oliveira PL, Tempone AJ, Rumjanek FD, Braga CMS, Silva JR, Dansa-Petretski Marílvia, Oliveira MA, de Souza W, Ferreira ST. Haemozoin in Schistosoma mansoni. Molecular and Biochemical Parasitology. 2000;111:217–221. doi: 10.1016/S0166-6851(00)00299-1. PubMed DOI

Pagola S, Stephens PW, Bohle DS, Kosar AD, Madsen SK. The structure of malaria pigment beta-haematin. Nature. 2000;404:307–310. doi: 10.1038/35005132. PubMed DOI

Paiva-Silva GO, Cruz-Oliveira C, Nakayasu ES, Maya-Monteiro CM, Dunkov BC, Masuda H, Almeida IC, Oliveira PL. A heme-degradation pathway in a blood-sucking insect. Proceedings of the National Academy of Sciences of the United States of America. 2006;103:8030–8035. doi: 10.1073/pnas.0602224103. PubMed DOI PMC

Pereira LO, Oliveira PL, Almeida IC, Paiva-Silva GO. Biglutaminyl-Biliverdin IX Alpha as a Heme Degradation Product in the Dengue Fever Insect-Vector Aedes aegypti . Biochemistry. 2007;46:6822–6829. doi: 10.1021/bi700011d. PubMed DOI PMC

Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research. 2001;29:45e–45. doi: 10.1093/nar/29.9.e45. PubMed DOI PMC

Rao AU, Carta LK, Lesuisse E, Hamza I. Lack of heme synthesis in a free-living eukaryote. Proceedings of the National Academy of Sciences of the United States of America. 2005;102:4270–4275. doi: 10.1073/pnas.0500877102. PubMed DOI PMC

Ryter SW, Tyrrell RM. The heme synthesis and degradation pathways: role in oxidant sensitivity. Free Radical Biology and Medicine. 2000;28:289–309. doi: 10.1016/S0891-5849(99)00223-3. PubMed DOI

Sanggaard KW, Bechsgaard JS, Fang X, Duan J, Dyrlund TF, Gupta V, Jiang X, Cheng L, Fan D, Feng Y, Han L, Huang Z, Wu Z, Liao L, Settepani V, Thøgersen IB, Vanthournout B, Wang T, Zhu Y, Funch P, Enghild JJ, Schauser L, Andersen SU, Villesen P, Schierup MH, Bilde T, Wang J. Spider genomes provide insight into composition and evolution of venom and silk. Nature Communications. 2014;5:3765. doi: 10.1038/ncomms4765. PubMed DOI PMC

Santos VT, Ribeiro L, Fraga A, de Barros CM, Campos E, Moraes J, Fontenele MR, Araújo HM, Feitosa NM, Logullo C, da Fonseca RN. The embryogenesis of the Tick Rhipicephalus (Boophilus) microplus : The establishment of a new chelicerate model system. Genesis. 2013;51:803–818. doi: 10.1002/dvg.22717. PubMed DOI

Smith AD, Kaufman WR. Molecular characterization of two vitellogenin genes from the tick, Amblyomma hebraeum (Acari: Ixodidae) Ticks and Tick-Borne Diseases. 2014;5:821–833. doi: 10.1016/j.ttbdis.2014.06.001. PubMed DOI

Smolenaars MMW, Madsen O, Rodenburg KW, Van der Horst DJ. Molecular diversity and evolution of the large lipid transfer protein superfamily. The Journal of Lipid Research. 2007;48:489–502. doi: 10.1194/jlr.R600028-JLR200. PubMed DOI

Sojka D, Franta Z, Horn M, Caffrey CR, Mareš M, Kopáček P. New insights into the machinery of blood digestion by ticks. Trends in Parasitology. 2013;29:276–285. doi: 10.1016/j.pt.2013.04.002. PubMed DOI

Sonenshine DE, Roe RM. Biology of Ticks. Oxford University Press; 2014.

Talyuli OA, Bottino-Rojas V, Taracena ML, Soares AL, Oliveira JH, Oliveira PL. The use of a chemically defined artificial diet as a tool to study Aedes aegypti physiology. Journal of Insect Physiology. 2015;83:1–7. doi: 10.1016/j.jinsphys.2015.11.007. PubMed DOI

Toh S, Glanfield A, Gobert GN, Jones MK. Heme and blood-feeding parasites: friends or foes? Parasites & Vectors. 2010;3:108. doi: 10.1186/1756-3305-3-108. PubMed DOI PMC

Urbanová V, Hartmann D, Grunclová L, Šíma R, Flemming T, Hajdušek O, Kopáček P. IrFC – An Ixodes ricinus injury-responsive molecule related to Limulus Factor C. Developmental & Comparative Immunology. 2014;46:439–447. doi: 10.1016/j.dci.2014.05.016. PubMed DOI

Walter-Nuno AB, Oliveira MP, Oliveira MF, Goncalves RL, Ramos IB, Koerich LB, Oliveira PL, Paiva-Silva GO. Silencing of maternal heme-binding protein causes embryonic mitochondrial dysfunction and impairs embryogenesis in the blood sucking insect Rhodnius prolixus. Journal of Biological Chemistry. 2013;288:29323–29332. doi: 10.1074/jbc.M113.504985. PubMed DOI PMC

Wu B, Novelli J, Foster J, Vaisvila R, Conway L, Ingram J, Ganatra M, Rao AU, Hamza I, Slatko B. The heme biosynthetic pathway of the obligate wolbachia endosymbiont of brugia malayi as a potential anti-filarial drug target. PLoS Neglected Tropical Diseases. 2009;3:e12318. doi: 10.1371/journal.pntd.0000475. PubMed DOI PMC

Zhou G, Kohlhepp P, Geiser D, Frasquillo Maria del Carmen, Vazquez-Moreno L, Winzerling JJ. Fate of blood meal iron in mosquitoes. Journal of Insect Physiology. 2007;53:1169–1178. doi: 10.1016/j.jinsphys.2007.06.009. PubMed DOI PMC

Zwerschke D, Karrie S, Jahn D, Jahn M. Leishmania major possesses a unique HemG-type protoporphyrinogen IX oxidase. Bioscience Reports. 2014;34:e12318. doi: 10.1042/BSR20140081. PubMed DOI PMC

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