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Reprolysin metalloproteases from Ixodes persulcatus, Rhipicephalus sanguineus and Rhipicephalus microplus ticks

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Abstract

Metalloproteases (MPs) have been considered essential for blood feeding and other physiological functions in several hematophagous animals, including ticks. We report the characterization of MP sequences of three important ticks from Asia, Africa and America: Ixodes persulcatus (Ip-MPs), Rhipicephalus sanguineus (Rs-MPs) and R. microplus (BrRm-MPs). Amino acid sequence identity between R. microplus and R. sanguineus MPs ranged from 76 to 100 %, and identities among I. persulcatus, I. ricinus and I. scapularis MP sequences ranged from 88 to 97 %. This high sequence identity and typical functional motifs show that all sequences are MPs. The presence of a zinc binding site, a Met-turn and cysteine rich domain at the C-terminal region indicates that these proteins belong to the reproplysin family of MPs. Differences in amino acid sequences of BrRm-MP1, BrRm-MP2, BrRm-MP4 and BrRm-MP5 (from Porto Alegre strain ticks) were 6, 2, 7 and 5 %, respectively, when compared with sequences deposited in GenBank for the same genes from other R. microplus isolates. Analyses of MPs predicted that they have various highly antigenic regions. Semi-quantitative RT-PCR analysis revealed the presence of transcripts in salivary glands of partially and fully fed female ticks. None of these transcripts were observed in males (except BrRm-MP4) and eggs. These enzymes may be functional components required during tick feeding to manipulate host defenses and support tick hematophagy.

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References

  • Adamson SW, Browning RE, Chao CC, Bateman RC, Ching WM, Karim S (2013) Molecular characterization of tick salivary gland glutaminyl cyclase. Insect Biochem Mol Biol 43:781–793

    Article  CAS  PubMed  Google Scholar 

  • Aljamali M, Bowman AS, Dillwith JW, Tucker JS, Yates GW, Essenberg RC, Sauer JR (2002) Identity and synthesis of prostaglandins in the lone star tick, Amblyomma americanum (L.), as assessed by radio-immunoassay and gas chromatography/mass spectrometry. Insect Biochem Mol Biol 32:331–341

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Anisuzzaman Islam MK, Alim MA, Miyoshi T, Hatta T, Yamaji K, Matsumoto Y, Fujisaki K, Tsuji N (2011) Longistatin, a plasminogen activator, is key to the availability of blood-meals for ixodid ticks. PLoS Pathog 7(3):e1001312

    Article  Google Scholar 

  • Antuch W, Guntert P, Billeter M, Hawthorne T, Grossenbacher H, Wuthrich K (1994) Nmr solution structure of the recombinant tick anticoagulant protein (Rtap), a factor Xa inhibitor from the tick Ornithodoros-Moubata. FEBS Lett 352:251–257

    Article  CAS  PubMed  Google Scholar 

  • Barnard AC, Nijhof AM, Gaspar ARM, Neitz AWH, Jongejan F, Maritz-Olivier C (2012) Expression profiling, gene silencing and transcriptional networking of metzincin metalloproteases in the cattle tick, Rhipicephalus (Boophilus) microplus. Vet Parasitol 186:403–414

    Article  CAS  PubMed  Google Scholar 

  • Bastiani M, Hillebrand S, Horn F, Kist TBL, Guimaraes JA, Termignoni C (2002) Cattle tick Boophilus microplus salivary gland contains a thiol-activated metalloendopeptidase displaying kininase activity. Insect Biochem Mol Biol 32:1439–1446

    Article  CAS  PubMed  Google Scholar 

  • Bellgard MI, Moolhuijzen PM, Guerrero FD, Schibeci D, Rodriguez-Valle M, Peterson DG, Dowd SE, Barrero R, Hunter A, Miller RJ, Lew-Tabor AE (2012) CattleTickBase: an integrated Internet-based bioinformatics resource for Rhipicephalus (Boophilus) microplus. Int J Parasitol 42:161–169

    Article  CAS  PubMed  Google Scholar 

  • Ben-Ami I, Freimann S, Armon L, Dantes A, Ron-El R, Amsterdam A (2006) Novel function of ovarian growth factors: combined studies by DNA microarray, biochemical and physiological approaches. Mol Hum Reprod 12:413–419

    Article  CAS  PubMed  Google Scholar 

  • Bjellqvist B, Hughes GJ, Pasquali C, Paquet N, Ravier F, Sanchez JC, Frutiger S, Hochstrasser D (1993) The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino-acid-sequences. Electrophoresis 14:1023–1031

    Article  CAS  PubMed  Google Scholar 

  • Bjellqvist B, Basse B, Olsen E, Celis JE (1994) Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions. Electrophoresis 15:529–539

    Article  CAS  PubMed  Google Scholar 

  • Boldt HB, Overgaard MT, Laursen LS, Weyer K, Sottrup-Jensen L, Oxvig C (2001) Mutational analysis of the proteolytic domain of pregnancy-associated plasma protein-A (PAPP-A): classification as a metzincin. Biochem J 358:359–367

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bond ND (2010) The Role of ecdysone signaling in fat-body tissue remodeling and pupal metabolism. Dissertation, University of Nevada Las Vegas

  • Bowman AS, Dillwith JW, Sauer JR (1996) Tick salivary prostaglandins: presence, origin and significance. Parasitol Today 12:388–396

    Article  CAS  PubMed  Google Scholar 

  • Brumpt E (1932) Longévité du virus de la fièvre boutonneuse (Rickettsia conorii n. sp.) chez la tique Rhipicephalus sanguineus. C R Soc Biol Fil 110:1199–1209

    Google Scholar 

  • Chang C, Werb Z (2001) The many faces of metalloproteases: cell growth, invasion, angiogenesis and metastasis. Trends Cell Biol 11:S37–S43

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chmelar J, Calvo E, Pedra JHF, Francischetti IMB, Kotsyfakis M (2012) Tick salivary secretion as a source of antihemostatics. J Proteomics 75:3842–3854

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Curry TE, Osteen KG (2003) The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev 24:428–465

    Article  CAS  PubMed  Google Scholar 

  • Dantas-Torres F (2008) The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): from taxonomy to control. Vet Parasitol 152:173–185

    Article  PubMed  Google Scholar 

  • Dantas-Torres F (2009) Ticks on domestic animals in Pernambuco. Northeast Braz Rev Bras Parasitol Vet 3:22–28

    Article  Google Scholar 

  • Dantas-Torres F, Chomel BB, Otranto D (2012) Ticks and tick-borne diseases: a one health perspective. Trends Parasitol 28:437–446

    Article  PubMed  Google Scholar 

  • Decrem Y, Beaufays J, Blasioli V, Lahaye K, Brossard M, Vanhamme L, Godfroid E (2008a) A family of putative metalloproteases in the salivary glands of the tick Ixodes ricinus. FEBS J 275:1485–1499

    Article  CAS  PubMed  Google Scholar 

  • Decrem Y, Mariller M, Lahaye K, Blasioli V, Beaufays J, Boudjeltia KZ, Vanhaeverbeek M, Cerutti M, Brossard M, Vanhamme L, Godfroid E (2008b) The impact of gene knock-down and vaccination against salivary metalloproteases on blood feeding and egg laying by Ixodes ricinus. Int J Parasitol 38:549–560

    Article  CAS  PubMed  Google Scholar 

  • Dong JY, Opresko LK, Dempsey PJ, Lauffenburger DA, Coffey RJ, Wiley HS (1999) Metalloprotease-mediated ligand release regulates autocrine signaling through the epidermal growth factor receptor. Proc Natl Acad Sci USA 96:6235–6240

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Escrevente C, Morais VA, Keller S, Soares CM, Altevogt P, Costa J (2008) Functional role of N-glycosylation from ADAM10 in processing, localization and activity of the enzyme. Biochim Biophys Acta 1780:905–913

    Article  CAS  PubMed  Google Scholar 

  • Francischetti IMB (2010) Platelet aggregation inhibitors from hematophagous animals. Toxicon 56:1130–1144

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Francischetti IMB, Mather TN, Ribeiro JMC (2003) Cloning of a salivary gland metalloprotease and characterization of gelatinase and fibrin(ogen)lytic activities in the saliva of the Lyme disease tick vector Ixodes scapularis. Biochem Biophys Res Commun 305:869–875

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Franta Z, Frantova H, Konvickova J, Horn M, Sojka D, Mares M, Kopacek P (2010) Dynamics of digestive proteolytic system during blood feeding of the hard tick Ixodes ricinus. Parasit Vectors 3:119

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • García-García JC, Gonzalez IL, Gonzalez DM, Valdes M, Mendez L, Lamberti J, D’Agostino B, Citroni D, Fragoso H, Ortiz M, Rodriguez M, De La Fuente J (1999) Sequence variations in the Boophilus microplus Bm86 locus and implications for immunoprotection in cattle vaccinated with this antigen. Exp Appl Acarol 23:883–895

    Article  PubMed  Google Scholar 

  • García-García JC, Montero C, Redondo M, Vargas M, Canales M, Boue O, Rodriguez M, Joglar M, Machado H, Gonzalez IL, Valdes M, Mendez L, De La Fuente J (2000) Control of ticks resistant to immunization with Bm86 in cattle vaccinated with the recombinant antigen Bm95 isolated from the cattle tick, Boophilus microplus. Vaccine 18:2275–2287

    Article  PubMed  Google Scholar 

  • Dagda RK, Gasanov S, OIII YDL, Rael ED, Lieb CS (2013) Genetic basis for variation of metalloproteinase-associated biochemical activity in venom of the Mojave rattlesnake (Crotalus scutulatus scutulatus). Biochem Res Int 2013: Article ID. 251474

  • Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook, 2nd edn. Humana Press, New York, pp 571–607

    Chapter  Google Scholar 

  • Ghosh S, Bansal GC, Gupta SC, Ray D, Khan MQ, Irshad H, Shahiduzzaman M, Seitzer U, Ahmed JS (2007) Status of tick distribution in Bangladesh, India and Pakistan. Parasitol Res 101:S207–S216

    Article  PubMed  Google Scholar 

  • Gomis-Rüth FX (2009) Catalytic domain architecture of metzincin metalloproteases. J Biol Chem 284:15353–15357

    Article  PubMed Central  PubMed  Google Scholar 

  • Gray J, Dantas-Torres F, Estrada-Pena A, Levin M (2013) Systematics and ecology of the brown dog tick, Rhipicephalus sanguineus. Ticks Tick Borne Dis 4:171–180

    Article  PubMed  Google Scholar 

  • Guerrero FD, Miller RJ, Rousseau ME, Sunkara S, Quackenbush J, Lee Y, Nene V (2005) BmiGI: a database of cDNAs expressed in Boophilus microplus, the tropical/southern cattle tick. Insect Biochem Mol Biol 35:585–595

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser Ser 41:95–98

    CAS  Google Scholar 

  • Harnnoi T, Sakaguchi T, Nishikawa Y, Xuan XA, Fujisaki K (2007) Molecular characterization and comparative study of 6 salivary gland metalloproteases from the hard tick, Haemaphysalis longicornis. Comp Biochem Physiol B Biochem Mol Biol 147:93–101

    Article  PubMed  Google Scholar 

  • Hayasaka D, Ivanov L, Leonova GN, Goto A, Yoshii K, Mizutani T, Kariwa H, Takashima I (2001) Distribution and characterization of tick-borne encephalitis viruses from Siberia and far-eastern Asia. J Gen Virol 82:1319–1328

    CAS  PubMed  Google Scholar 

  • Hinkle CL, Sunnarborg SW, Loiselle D, Parker CE, Stevenson M, Russell WE, Lee DC (2004) Selective roles for tumor necrosis factor alpha-converting enzyme/ADA-M17 in the shedding of the epidermal growth factor receptor ligand family—the juxtamembrane stalk determines cleavage efficiency. J Biol Chem 279:24179–24188

    Article  CAS  PubMed  Google Scholar 

  • Hirokawa T, Boon-Chieng S, Mitaku S (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378–379

    Article  CAS  PubMed  Google Scholar 

  • Hofmann K, Stoffel W (1993) TMbase—a database of membrane spanning proteins segments. Biol Chem Hoppe-Seyler 374:166

    Google Scholar 

  • Horn F, Dos-Santos PC, Termignoni C (2000) Boophilus microplus anticoagulant protein: an antithrombin inhibitor from the cattle tick saliva. Arch Biochem Biophys 384:68–73

    Article  CAS  PubMed  Google Scholar 

  • Ibelli AMG, Hermance MM, Kim TK, Gonzalez CL, Mulenga A (2013) Bioinformatics and expression analyses of the Ixodes scapularis tick cystatin family. Exp Appl Acarol 60:41–53

    Article  PubMed  Google Scholar 

  • Imamura S, Vaz Junior ID, Konnai S, Yamada S, Nakajima C, Onuma M, Ohashi K (2009) Effect of vaccination with a recombinant metalloprotease from Haemaphysalis longicornis. Exp Appl Acarol 48:345–358

    Article  CAS  PubMed  Google Scholar 

  • Jameson BA, Wolf H (1988) The antigenic index—a novel algorithm for predicting antigenic determinants. Comput Appl Biosci 4:181–186

    CAS  PubMed  Google Scholar 

  • Joh JH, Kim BG, Kong WS, Yoo YB, Kim NK, Park HR, Cho BG, Lee CS (2004) Cloning and developmental expression of a metzincin family metalloprotease cDNA from oyster mushroom Pleurotus ostreatus. FEMS Microbiol Lett 239:57–62

    Article  CAS  PubMed  Google Scholar 

  • Joubert AM, Crause JC, Gaspar ARMD, Clarke FC, Spickett AM, Neitz AWH (1995) Isolation and characterization of an anticoagulant present in the salivary-glands of the bont-legged tick, Hyalomma truncatum. Exp Appl Acarol 19:79–92

    Article  CAS  PubMed  Google Scholar 

  • Kang YB, Jang DH (1985) A description with scanning electron microscopy on the tick Ixodes persulcatus (Schulze, 1930) male and female specimens. Kisaengchunghak. Chapchi 2:305–312

    Google Scholar 

  • Kearns DB, Bonner PJ, Smith DR, Shimkets LJ (2002) An extracellular matrix-associated zinc metalloprotease is required for dilauroyl phosphatidylethanolamine chemotactic excitation in Myxococcus xanthus. J Bacteriol 184:1678–1684

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Konnai S, Saito Y, Nishikado H, Yamada S, Imamura S, Mori A, Ito T, Onuma M, Ohashi K (2008) Establishment of a laboratory colony of taiga tick Ixodes persulcatus for tick-borne pathogen transmission studies. Jpn J Vet Res 55:85–92

    PubMed  Google Scholar 

  • Konnai S, Nishikado H, Yamada S, Imamura S, Ito T, Onuma M, Murata S, Ohashi K (2011) Molecular identification and expression analysis of lipocalins from blood feeding taiga tick, Ixodes persulcatus Schulze. Exp Parasitol 127:467–474

    Article  CAS  PubMed  Google Scholar 

  • Kotsyfakis M, Sa-Nunes A, Francischetti IMB, Mather TN, Andersen JF, Ribeiro JMC (2006) Antiinflammatory and immunosuppressive activity of sialostatin L, a salivary cystatin from the tick Ixodes scapularis. J Biol Chem 281:26298–26307

    Article  CAS  PubMed  Google Scholar 

  • Kovalev SY, Mukhacheva TA (2012) Phylogeographical structure of the tick Ixodes persulcatus: a novel view. Ticks Tick Borne Dis 3:212–218

    Article  PubMed  Google Scholar 

  • Lima CA, Torquato RJS, Sasaki SD, Justo GZ, Tanaka AS (2010) Biochemical characterization of a Kunitz type inhibitor similar to dendrotoxins produced by Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) hemocytes. Vet Parasitol 167:279–287

    Article  CAS  PubMed  Google Scholar 

  • Liu K, Olofsson JI, Wahlberg P, Ny T (1999) Distinct expression of gelatinase A [matrix metalloprotein- ase (MMP)-2], collagenase-3 (MMP-13), membrane type MMP 1 (MMP-14), and tissue inhibitor of MMPs type 1 mediated by physiological signals during formation and regression of the rat corpus luteum. Endocrinology 140:5330–5338

    CAS  PubMed  Google Scholar 

  • Locke M (1984) The structure and development of the vacuolar system in the fat body of insects. In: King RC, Akai H (eds) Insect ultrastructure, vol 2, 1st edn. Plenum Press, New York, pp 151–197

    Chapter  Google Scholar 

  • Mahlaku M (2002) Biochemical investigations into the proteolytic activities in salivary glands of the tick, Ornithodoros savignyi. Dissertation, University of Pretoria

  • Mans BJ, Gaspar ARMD, Louw AI, Neitz AWH (1998) Apyrase activity and platelet aggregation inhibitors in the tick Ornithodoros savignyi (Acari: Argasidae). Exp Appl Acarol 22:353–366

    Article  CAS  PubMed  Google Scholar 

  • Maritz-Olivier C, Stutzer C, Jongejan F, Neitz AW, Gaspar AR (2007) Tick anti-hemostatics: targets for future vaccines and therapeutics. Trends Parasitol 9:397–407

    Article  Google Scholar 

  • Mazzi MV, Marcussi S, Carlos GB, Stabeli RG, Franco JJ, Ticli FK, Cintra ACO, Franca SC, Soares AM, Sampaio SV (2004) A new hemorrhagic metalloprotease from Bothrops jararacussu snake venom: isolation and biochemical characterization. Toxicon 44:215–223

    Article  CAS  PubMed  Google Scholar 

  • Mitaku S, Hirokawa T (1999) Physicochemical factors for discriminating between soluble and membrane proteins: hydrophobicity of helical segments and protein length. Protein Eng 12:953–957

    Article  CAS  PubMed  Google Scholar 

  • Mitaku S, Hirokawa T, Tsuji T (2002) Amphiphilicity index of polar amino acids as an aid in the characterization of amino acid preference at membrane–water interfaces. Bioinformatics 18:608–616

    Article  CAS  PubMed  Google Scholar 

  • Mohamed TM (2006) Adenosine deaminase from camel tick Hyalomma dromedarii: purification and characterization. Exp Appl Acarol 40:101–111

    Article  CAS  PubMed  Google Scholar 

  • Moraes-Filho J, Pinter A, Pacheco RC, Gutmann TB, Barbosa SO, Gonzáles MA, Muraro MA, Cecílio SR, Labruna MB (2009) New epidemiological data on Brazilian spotted fever in an endemic area of the state of São Paulo, Brazil. Vector Borne Zoonotic Dis 9:73–78

    Article  PubMed  Google Scholar 

  • Mulenga A, Blandon M, Khumthong R (2007) The molecular basis of the Amblyomma americanum tick attachment phase. Exp Appl Acarol 41:267–287

    Article  CAS  PubMed  Google Scholar 

  • Nicholas KB, Nicholas-Jr HB, Deerfield-II DW (1997) GeneDoc: analysis and visualization of genetic variation. EMBNEW NEWS 4:14

  • Nienaber J, Gaspar AR, Neitz AWH (1999) Savignin, a potent thrombin inhibitor isolated from the salivary glands of the tick Ornithodoros savignyi (Acari: Argasidae). Exp Parasitol 93:82–91

    Article  CAS  PubMed  Google Scholar 

  • Ohnishi J, Ohnishi E, Jin M, Hirano W, Nakane D, Matsui H, Kimura A, Sawa H, Nakayama K, Shibuya H, Nagashima K, Takahashi T (2001) Cloning and characterization of a rat ortholog of MMP-23 (matrix metalloproteinase-23), a unique type of membrane-anchored matrix metalloproteinase and conditioned switching of its expression during the ovarian follicular development. Mol Endocrinol 15:747–764

    Article  CAS  PubMed  Google Scholar 

  • Parizi LF, Githaka NW, Logullo C, Konnai S, Masuda A, Ohashi K, Vaz Junior ID (2012) The quest for a universal vaccine against ticks: cross-immunity insights. Vet J 194:158–165

    Article  PubMed  Google Scholar 

  • Parizi LF, Githaka NW, Acevedo C, Benavides U, Seixas A, Logullo C, Konnai S, Ohashi K, Masuda A, Vaz Junior ID (2013) Sequence characterization and immunogenicity of cystatins from the cattle tick Rhipicephalus (Boophilus) microplus. Ticks Tick Borne Dis 4:492–499

    Article  PubMed  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    Article  CAS  PubMed  Google Scholar 

  • Preston SG, Majtan J, Kouremenou C, Rysnik O, Burger LF, Cruz AC, Guzman MC, Nunn MA, Paesen GC, Nuttall PA, Austyn JM (2013) Novel immuno-modulators from hard ticks selectively reprogramme human dendritic cell responses. PLoS Pathog 9(6):e1003450

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ribeiro JMC, Francischetti IMB (2003) Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annu Rev Entomol 48:73–88

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro JMC, Mather TN (1998) Ixodes scapularis: salivary kininase activity is a metallo dipeptidyl carboxypeptidase. Exp Parasitol 89:213–221

    Article  CAS  PubMed  Google Scholar 

  • Roselldavis R, Coons LB (1989) Relationship between feeding, mating, vitellogenin production and vitellogenesis in the tick Dermacentor variabilis. Exp Appl Acarol 7:95–105

    Article  CAS  Google Scholar 

  • Saldivar L, Guerrero FD, Miller RJ, Bendele KG, Gondro C, Brayton KA (2008) Microarray analysis of acaricide-inducible gene expression in the southern cattle tick, Rhipicephalus (Boophilus) microplus. Insect Mol Biol 17:597–606

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Shpynov SN, Rudakov NV, Iastrebov VK, Leonova GN, Khazova TG, Egorova NV, Borisova ON, Preĭder VP, Bezrukov GV, Fedorov EG, Fedianin AP, Sherstneva MB, Turyshev AG, Gavrilov AP, Tankibaev MA, Fournier PE, Raoult D (2004) New evidence for the detection of ehrlichia and anaplasma in ixodes ticks in Russia and Kazakhstan. Med Parazitol (Mosk) 2:10–14

    Google Scholar 

  • Sigrist CJA, Cerutti L, de Castro E, Langendijk-Genevaux PS, Bulliard V, Bairoch A, Hulo N (2010) PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res 38:D161–D166

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sossai S, Peconick AP, Sales-Junior A, Marcelino FC, Vargas MI, Neves ES, Patarroyo JH (2005) Polymorphism of the bm86 gene in South American strains of the cattle tick Boophilus microplus. Exp Appl Acarol 37:199–214

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tikki N, Rhalem A, Sadak A, Sahibi H (1999) Female tick Hyalomma marginatum marginatum salivary glands: preliminary study on protein changes during feeding process and antigens recognized by repeatedly infested cattle. Parasite 6:303–309

    CAS  PubMed  Google Scholar 

  • Tusnády GE, Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17:849–850

    Article  PubMed  Google Scholar 

  • Umemiya-Shirafuji R, Boldbaatar D, Liao M, Battur B, Rahman MM, Kuboki T, Galay RL, Tanaka T, Fujisaki K (2012) Target of rapamycin (TOR) controls vitellogenesis via activation of the S6 kinase in the fat body of the tick, Haemaphysalis longicornis. Int J Parasitol 42:991–998

    Article  CAS  PubMed  Google Scholar 

  • van de Locht A, Stubbs MT, Bode W, Friedrich T, Bollschweiler C, Höffken W, Huber R (1996) The ornithodorin–thrombin crystal structure, a key to the TAP enigma? EMBO J 15:6011–6017

    PubMed Central  PubMed  Google Scholar 

  • Vaz Junior ID, Imamura S, Nakajima C, de Cardoso FC, Ferreira CAS, Renard G, Masuda A, Ohashi K, Onuma N (2005) Molecular cloning and sequence analysis of cDNAs encoding for Boophilus microplus, Haemaphysalis longicornis and Rhipicephalus appendiculatus actins. Vet Parasitol 127:147–155

    Article  Google Scholar 

  • Wang MH, Guerrero FD, Pertea G, Nene VM (2007) Global comparative analysis of ESTs from the southern cattle tick, Rhipicephalus (Boophilus) microplus. BMC Genomics 8:368

    Article  PubMed Central  PubMed  Google Scholar 

  • Wuritu, Ozawa Y, Gaowa, Kawamori F, Masuda T, Masuzawa T, Fujita H, Ohashi N (2009) Structural analysis of ap44/msp2 expression site of Anaplasma phagocytophilum in naturally infected ticks in Japan. J Med Microbiol 58:1638–1644

    Google Scholar 

  • Zhu K, Bowman AS, Brigham DL, Essenberg RC, Dillwith JW, Sauer JR (1997) Isolation and characterization of americanin, a specific inhibitor of thrombin, from the salivary glands of the lone star tick Amblyomma americanum (L.). Exp Parasitol 87:30–38

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors gratefully acknowledge the financial support from The World Academy of Sciences (TWAS), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS) and Instituto Nacional de Ciencia e Tecnologia em Entomologia Molecular, (INCT-EM). Abid Ali is a beneficiary of the TWAS/CNPq doctoral fellowship program.

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Authors and Affiliations

  1. Centro de Biotecnologia, Universidade Federal do Rio Grande do Sul, Avenida Bento Gonçalves, 9500, Prédio 43421, C.P. 15005, Porto Alegre, RS, 91501-970, Brazil

    Abid Ali, Lucas Tirloni, Adriana Seixas, Itabajara da Silva Vaz Junior & Carlos Termignoni

  2. Departamento de Bioquímica, Universidade Federal do Rio Grande do Sul, Rua Ramiro Barcelos, 2600, Porto Alegre, RS, 90035-000, Brazil

    Abid Ali & Carlos Termignoni

  3. Institute of Biotechnology Genetic Engineering, The University of Agriculture, Peshawar, 25130, Khyber Pakhtunkhwa, Pakistan

    Abid Ali

  4. Laboratory of Infectious Diseases, Department of Disease Control, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Hokkaido, 060-0818, Japan

    Masayoshi Isezaki, Satoru Konnai & Kazuhiko Ohashi

  5. Departamento de Ciências Básicas da Saúde, Universidade Federal de Ciências da Saúde de Porto Alegre, Rua Sarmento Leite 245, Porto Alegre, RS, 90050-170, Brazil

    Adriana Seixas

  6. Faculdade de Veterinária, Universidade Federal do Rio Grande do Sul, Avenida Bento Gonçalves, 9090, Porto Alegre, RS, 91540-000, Brazil

    Itabajara da Silva Vaz Junior

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  1. Abid Ali
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  8. Carlos Termignoni
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Correspondence to Carlos Termignoni.

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Ali, A., Tirloni, L., Isezaki, M. et al. Reprolysin metalloproteases from Ixodes persulcatus, Rhipicephalus sanguineus and Rhipicephalus microplus ticks. Exp Appl Acarol 63, 559–578 (2014). https://doi.org/10.1007/s10493-014-9796-9

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