Hostname: page-component-7c8c6479df-995ml Total loading time: 0 Render date: 2024-03-29T08:20:04.747Z Has data issue: false hasContentIssue false

Characterization of a glycine-rich protein from Rhipicephalus microplus: tissue expression, gene silencing and immune recognition

Published online by Cambridge University Press:  16 November 2017

B. F. Leal
Affiliation:
Laboratório de Imunologia e Microbiologia, Pontifícia Universidade Católica do Rio Grande do Sul (PUCRS), Av. Ipiranga, 6681, 90619-900, Porto Alegre, RS, Brazil
M. F. Alzugaray
Affiliation:
Laboratório de Imunologia Aplicada à Saúde Animal, Universidade Federal do Rio Grande do Sul (UFRGS), Av. Bento Gonçalves, 9500, 91501-970, Porto Alegre, RS, Brazil Departamento de Microbiología, Universidad de la Republica, Alberto Lasplaces 1550 a 1620, 11600 Montevideo, Uruguay
A. Seixas
Affiliation:
Departamento de Farmacociências, Universidade Federal de Ciências da Saúde de Porto Alegre (UFCSPA), Rua Sarmento Leite, 245, 90050-170, Porto Alegre, RS, Brazil
I. Da Silva Vaz Jr
Affiliation:
Laboratório de Imunologia Aplicada à Saúde Animal, Universidade Federal do Rio Grande do Sul (UFRGS), Av. Bento Gonçalves, 9500, 91501-970, Porto Alegre, RS, Brazil
C. A. S. Ferreira*
Affiliation:
Laboratório de Imunologia e Microbiologia, Pontifícia Universidade Católica do Rio Grande do Sul (PUCRS), Av. Ipiranga, 6681, 90619-900, Porto Alegre, RS, Brazil
*
Author for correspondence: C. A. S. Ferreira, E-mail: cferreira@pucrs.br

Abstract

Salivary molecules, as glycine-rich proteins (GRPs), are essential to tick attachment and feeding on the host and are suggested to be involved in the host's immune system evasion, therefore representing natural candidates in the search for protective vaccine antigens. This work shows the molecular characterization of a GRP from Rhipicephalus microplus (RmGRP). The cDNA and putative amino acid sequences were analysed, as well as the transcription level in tick tissues/developmental stages, showing the highest levels of gene expression in 1-day-old larvae and salivary glands of fully engorged females. RmGRP gene silencing resulted in a lower hatching rate of larvae from treated females. In addition, recombinant RmGRP (rRmGRP) was recognized by sera from naturally and experimentally infested bovines, displaying considerable differences among the individuals tested. rRmGRP was recognized by anti-saliva and anti-salivary glands sera, while anti-rRmGRP serum recognized RmGRP in saliva and salivary glands, indicating its secretion into the host. The data collected indicate that RmGRP may present roles other than in the tick–host relationship, especially in embryo development. In addition, the high expression in adult females, antigenicity and presence of shared characteristics with other tick protective GRPs turns RmGRP a potential candidate to compose an anti-tick vaccine cocktail.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, JM, Sonenshine, DE and Valenzuela, JG (2008) Exploring the mialome of ticks: an annotated catalogue of midgut transcripts from the hard tick, Dermacentor variabilis (Acari: Ixodidae). BMC Genomics 9, 552.Google Scholar
Andersen, SO, Hojrup, P and Roepstorff, P (1995) Insect cuticular proteins. Insect Biochemistry and Molecular Biology 25, 153176.Google Scholar
Antunes, S, Merino, O, Lérias, J, Domingues, N, Mosqueda, J, de la Fuente, J and Domingos, A (2015) Artificial feeding of Rhipicephalus microplus female ticks with anti calreticulin serum do not influence tick and Babesia bigemina acquisition. Ticks and Tick-Borne Diseases 6, 4755.Google Scholar
Beckwitt, R, Arcidiacono, S and Stote, R (1998) Evolution of repetitive protein: spider silks from Nephila clavipes (Tetragnathidae) and Araneus bicentenarius (Araneidae). Insect Biochemistry and Molecular Biology 28, 121130.Google Scholar
Bennington, KC (1978) Sequential changes in salivary gland structure during attachment and feeding of the cattle tick, Boophilus microplus. International Journal for Parasitology 8, 97115.Google Scholar
Bishop, R, Lambson, B, Wells, C, Pandit, P, Osaso, J, Nikonge, C, Morzaria, S, Musoke, A and Nene, V (2002) A cement protein of the tick Rhipicephalus appendiculatus, located in the secretory e cell granules of the type III salivary gland acini, induces strong antibody responses in cattle. International Journal for Parasitology 32, 833842.Google Scholar
Blom, N, Gammeltoft, S and Brunak, S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. Journal of Molecular Biology 294, 13511362.Google Scholar
Bullard, RL, Williams, J and Karim, S (2016 a) Temporal gene expression analysis and RNA silencing of single and multiple members of gene family in the lone star tick Amblyomma americanum. PLoS ONE 11, e0147966.Google Scholar
Bullard, RL, Allen, P, Chao, CC, Douglas, J, Das, P, Morgan, SE, Ching, WM and Karim, S (2016 b) Structural characterization of tick cement cones collected from in vivo and artificial membrane blood-fed lone star ticks (Amblyomma americanum). Ticks and Tick-Borne Diseases 7, 880892.Google Scholar
Bustin, SA, Beaulieu, JF, Huggett, J, Jaggi, R, Kibenge, FSB, Olsvik, PA, Penning, LC and Toegel, S (2010) MIQE précis: practical implementation of minimum standard guidelines for fluorescence-based quantitative real-time PCR experiments. BMC Molecular Biology 11, 74.Google Scholar
Canal, CW, Maia, HM, da Silva Vaz, I Jr., Chies, JM, Farias, NAR, Masuda, A, Gonzales, JC, Ozaki, LS and Dewes, H (1995) Changing patterns of vitellin-related peptides during development of the cattle tick Boophilus microplus. Experimental & Applied Acarology 19, 325336.Google Scholar
Cruz, APR, Silva, SS, Mattos, RT, da Silva Vaz, I Jr., Masuda, A and Ferreira, CAS (2008) Comparative IgG recognition of tick extracts by sera of experimentally infested bovines. Veterinary Parasitology 158, 152158.Google Scholar
da Silva Vaz, I Jr., Ozaki, LS and Masuda, A (1994) Serum of Boophilus microplus infested cattle reacts with different tick tissues. Veterinary Parasitology 52, 7178.Google Scholar
da Silva Vaz, I Jr., Logullo, C, Sergine, M, Veloso, FF, Rosa de Lima, MF, Gonzales, JV, Masuda, H, Oliveira, PL and Masuda, A (1998) Immunization of bovines with an aspartic proteinase precursor isolated from Boophilus microplus eggs. Veterinary Immunology and Immunopathology 66, 331341.Google Scholar
de Castro, JJ and Newson, RM (1993) Host resistance in cattle tick control. Parasitology Today 9, 1317.Google Scholar
de Castro, MH, de Klerk, D, Pienaar, R, Latif, AA, Rees, DJG and Mans, BJ (2016) De novo assembly and annotation of the salivary gland transcriptome of Rhipicephalus appendiculatus male and female ticks during blood feeding. Ticks and Tick-Borne Diseases 7, 536548.Google Scholar
de la Fuente, J, Rodríguez, M, Montero, C, Redondo, M, García-García, JC, Méndez, L, Serrano, E, Valdés, M, Enríquez, A, Canales, M, Ramos, E, Boué, O, Machado, H and Lleonart, R (1999) Vaccination against ticks (Boophilus spp.): the experience with the Bm86-based vaccine gavac™. Genetic Analysis: Biomolecular Engineering 15, 143148.Google Scholar
de la Fuente, J, Almazán, C, Canales, M, de la Lastra, JMP, Kocan, KM and Willadsen, P (2007) A ten-year review of commercial vaccine performance for control of tick infestations on cattle. Animal Health Research Reviews 8, 2328.Google Scholar
de la Fuente, J, Kopácek, P, Lew-Tabor, A and Maritz-Oliver, C (2016) Strategies for new and improved vaccines against ticks and tick-borne diseases. Parasite Immunology 38, 754769.Google Scholar
de Vos, S, Zeinstra, L, Taoufik, O, Willadsen, P and Jongejan, F (2001) Evidence for the utility of the Bm86 antigen from Boophilus microplus in vaccination against other tick species. Experimental & Applied Acarology 25, 245261.CrossRefGoogle ScholarPubMed
Díaz-Martín, V, Manzano-Román, R, Valero, L, Oleaga, A, Encinas-Grandes, A and Pérez-Sánchez, R (2013) An insight into the proteome of the saliva of the argasid tick Ornithodoros moubata reveals important differences in saliva protein composition between the sexes. Journal of Proteomics 80, 216235.Google Scholar
Dunn, SD (1986) Effects of the modification of transfer buffer composition and the renaturation of proteins in gels on the recognition of proteins on western blots by monoclonal antibodies. Analytical Biochemistry 157, 144153.Google Scholar
Fabres, A, de Andrade, CP, Guizzo, M, Sorgine, MHF, Paiva-Silva, GD, Masuda, A, da Silva Vaz Silva, I and Logullo, C (2010) Effect of GSK-3 activity, enzymatic inhibition and gene silencing by RNAi on tick oviposition and egg hatching. Parasitology 137, 15371546.CrossRefGoogle ScholarPubMed
Fielden, LJ, Rechav, Y and Bryson, NR (1992) Acquired immunity to larvae of Amblyornma marmoreurn and A. Hebraeum by tortoises, Guinea-pigs and Guinea-fowl. Medical and Veterinary Entomology 6, 251254.Google Scholar
Fragoso, H, Rad, PH, Ortiz, M, Rodríguez, M, Redondo, M, Herrera, L and de la Fuente, J (1998) Protection against Boophilus annulatus infestations in cattle vaccinated with the B. microplus BmS6-containing vaccine Gavac. Vaccine 16, 19901992.Google Scholar
Francischetti, IMB, Meng, Z, Mans, BJ, Guderra, N, Hall, M, Veenstra, TD, Pham, VM, Kotsyfakis, M and Ribeiro, JMC (2008) An insight into the salivary transcriptome and proteome of the soft tick and vector of epizootic bovine abortion, Ornithodoros coriaceus. Journal of Proteomics 71, 493512.Google Scholar
Garcia, GR, Gardinassi, LG, Ribeiro, JM, Anatriello, E, Ferreira, BR, Moreira, HNS, Mafra, C, Martins, MM, Szabó, MPJ, de Miranda-Santos, IKF and Maruyama, SR (2014) The sialotranscriptoma of Amblyomma triste, Amblyomma parvum and Amblyomma cajennense ticks, uncovered by 454-based RNA-seq. Parasites & Vectors 7, 430.Google Scholar
Garnier, J, Gibrat, J-F and Robson, B (1996) GOR method for predicting protein secondary structure from amino acid sequence. In Doolittle, RF (ed). Methods in Enzymology, . San Diego, CA: Academic Press, pp. 540553.Google Scholar
Gasteiger, E, Hoogland, C, Gattiker, A, Duvaud, S, Wilkins, MR, Appel, RD and Bairoch, A (2005) Protein identification and analysis tools on the expasy server. In Walker, JM (ed). The Proteomics Protocols Handbook, Totowa, NJ: Humana Press, pp. 571607.CrossRefGoogle Scholar
Harnnoi, T, Sakaguchi, T, Xuan, X and Fujisaki, K (2006) Identification of genes encoding cement-like antigens expressed in the salivary glands of Haemaphysalis longicornis. Parasitology 68, 11551160.Google Scholar
Havlíková, S, Roller, L, Koči, J, Trimnell, AR, Kazimírová, M, Klempa, B and Nuttall, PA (2009) Functional role of 64P, the candidate transmission-blocking vaccine antigen from the tick, Rhipicephalus appendiculatus. International Journal for Parasitology 39, 14851494.Google Scholar
Jiang, X, Gao, J, Wang, W, Xu, M, Li, W, Qi, M, Yang, C, Ji, L, Zhang, D, Luo, J and Yin, H (2014) Molecular characterization of an alanine-, proline-, glycine-, threonine-, and serine-rich protein of the hard tick Haemaphysalis qinghaiensis and its effect as a vaccine against tick infestation in sheep. Ticks and Tick-Borne Diseases 5, 1420.Google Scholar
Jiz, M, Wu, H, Meng, R, Pond-Tor, S, Reynolds, M, Friedman, JF, Olveda, R, Acosta, L and Kurtis, JD (2008) Pilot-scale production and characterization of paramyosin, a vaccine candidate for schistosomiasis japonica. Infection and Immunity 76, 31643169.Google Scholar
Karim, S and Ribeiro, JMC (2015) An insight into the sialome of the lone star tick, Amblyomma americanum, with a glimpse on its time dependent gene expression. PLoS ONE 10, e0131292.Google Scholar
Katoh-Fukui, Y, Noce, T, Ueda, T, Fujiwara, Y, Hashimoto, N, Higashinakagawa, T, Killian, CE, Livingston, BT, Wilt, FH, Benson, SC, Sucov, HM and Davidson, EH (1991) The corrected structure of the SM50 spicule matrix protein of Strongylocentrotus purpuratus. Developmental Biology 145, 201201.Google Scholar
Katoh-Fukui, Y, Noce, T, Ueda, T, Fujiwara, Y, Hashimoto, N, Tanaka, S and Higashinakagawa, T (1992) Isolation and characterization of cDNA encoding a spicule matrix protein in Hemicentrotus pulcherrimus micromeres. The International Journal of Developmental Biology 36, 353361.Google Scholar
Kemp, DH, Stone, BF and Binnington, KC (1982) Tick attachment and feeding: role of the mouthparts, feeding apparatus, salivary gland secretions and host response. In Obenchain, FD, Galun, R (eds). Physiology of Ticks. Oxford, UK: Pergamon Press, pp. 119168.Google Scholar
Killian, CE, Croker, L and Wilt, FH (2010) SpSM30 gene family expression patterns in embryonic and adult biomineralized tissues of the sea urchin, Strongylocentrotus purpuratus. Gene Expression Patterns 10, 135139.Google Scholar
Kim, TK, Tirloni, L, Pinto, AFM, Moresco, J, Yates, JR, da Silva Vaz, I and Mulenga, A (2016) Ixodes scapularis tick saliva proteins sequentially secreted every 24 h during blood feeding. PLoS Neglected Tropical Diseases 10, e0004323.Google Scholar
Kotál, J, Langhansová, H, Lieskovská, J, Andersen, JF, Francischetti, IMB, Chavakis, T, Kopecký, J, Pedra, JHF, Kotsyfakis, M and Chmelař, J (2015) Modulation of host immunity by tick saliva. Journal of Proteomics 128, 5868.Google Scholar
Lara, FA, Pohl, PC, Gandara, AC, Ferreira, JS, Nascimento-Silva, MC, Bechara, GH, Sorgine, MH, Almeida, IC, da Silva Vaz, I Jr. and Oliveira, PL (2015) ATP binding cassette transporter mediates both heme and pesticide detoxification in tick midgut cells. PLoS ONE 10, e0134779.Google Scholar
Leal, AT, Pohl, PC, Ferreira, CAS, Nascimento-Silva, MC, Sorgine, MH, Logullo, C, Oliveira, PL, Farias, SE, da Silva Vaz, I Jr. and Masuda, A (2006) Purification and antigenicity of two recombinant forms of Boophilus microplus yolk pro-cathepsin expressed in inclusion bodies. Protein Expression and Purification 45, 107114.Google Scholar
Leal, BF, Seixas, A, Mattos, RT, Coutinho, ML, Masuda, A, da Silva Vaz, I Jr. and Ferreira, CAS (2013) Tissue expression and the host's immunological recognition of a Rhipicephalus microplus paramyosin. Veterinary Parasitology 197, 304311.Google Scholar
Lew-Tabor, AE, Moolhuijzen, PM, Vance, ME, Kurscheid, S, Rodriguez Valle, M, Jarrett, S, Minchin, CM, Jackson, LA, Jonsson, NN, Bellgard, MI and Guerrero, FD (2010) Suppressive subtractive hybridization analysis of Rhipicephalus (Boophilus) microplus larval and adult transcript expression during attachment and feeding. Veterinary Parasitology 167, 304320.Google Scholar
Livingston, BT, Shaw, R, Bailey, A and Wilt, F (1991) Characterization of a cDNA encoding a protein involved in formation of the skeleton during development of the sea urchin Lytechinus pictus. Developmental Biology 148, 473480.Google Scholar
Lovis, L, Reggi, J, Berggoetz, M, Betschart, B and Sager, H. (2013) Determination of acaricide resistance in Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) field populations of Argentina, South Africa, and Australia with the larval tarsal test. Journal of Medical Entomology 50, 326335.Google Scholar
Mangeon, A, Junqueira, RM and Sachetto-Martins, G (2010) Functional diversity of the plant glycine-rich proteins superfamily. Plant Signaling Behavior 5, 99104.Google Scholar
Maruyama, SR, Anatriello, E, Anderson, JM, Ribeiro, JM, Brandão, LG, Valenzuela, JG, Ferreira, BR, Garcia, GR, Szabó, MPJ, Patel, S, Bishop, R and de Miranda-Santos, IKF (2010) The expression of genes coding for distinct types of glycine-rich proteins varies according to the biology of three metastriate ticks, Rhipicephalus (Boophilus) microplus, Rhipicephalus sanguineus and Amblyomma cajennense. BMC Genomics 11, 363.Google Scholar
Maruyama, SR, Garcia, G. R., Teixeira, FR, Brandão, LG, Anderson, JM, Ribeiro, JMC, Valenzuela, JG, Horackova, J, Veríssimo, CJ, Katiki, LM, Banin, TM, Zangirolamo, AF, Gardinasse, LG, Ferreira, BR and de Miranda-Santos, IKF (2017) Mining a differential sialotranscriptome of Rhipicephalus microplus guides antigen discovery to formulate a vaccine that reduces tick infestations. Parasites & Vectors 10, 206.Google Scholar
Mendes, EC, Mendes, MC and Sato, ME (2013) Diagnosis of amitraz resistance in Brazilian populations of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) with larval immersion test. Experimental & Applied Acarology 61, 357369.Google Scholar
Mortazavi, A, Williams, BA, McCue, K, Schaeffer, L and Wold, B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5, 621628.Google Scholar
Mulenga, A, Sugimoto, C, Ingram, G, Ohashi, K and Onuma, M (1999) Molecular cloning of two Haemaphysalis Longicornis Cathepsin L-like cysteine proteinase genes. The Journal of Veterinary Medical Science 61, 497502.Google Scholar
Mulenga, A, Sugimoto, C and Onuma, M (2000) Issues in tick vaccine development: identification and characterization of potential candidate vaccine antigens. Microbes and Infection 2, 13531361.CrossRefGoogle ScholarPubMed
Nunes, ET, Mathias, MIC and Bechara, GH (2006) Structural and cytochemical changes in the salivary glands of the Rhipicephalus (Boophilus) microplus (CANESTRINI, 1887) (Acari: Ixodidae) tick female during feeding. Veterinary Parasitology 140, 114123.Google Scholar
Nuttall, PA, Trimnell, AR, Kazimirova, M and Labuda, M (2006) Exposed and concealed antigens as vaccine targets for controlling ticks and tick-borne diseases. Parasite Immunology 28, 155163.Google Scholar
Ogden, NH, Casey, ANJ, French, NP, Adams, JDW and Woldehiwet, Z (2002) Field evidence for density-dependent facilitation amongst Ixodes ricinus ticks feeding on sheep. Parasitology 124, 117125.Google Scholar
Perner, J, Provazník, J, Schrenková, J, Urbanová, V, Ribeiro, JMC and Kopáček, P (2016) RNA-seq analyses of the midgut from blood- and serum-fed Ixodes ricinus ticks. Scientific Reports 6, 36695.Google Scholar
Petersen, TN, Brunak, S, Heijne, GV and Nielsen, H (2011) Signalp 4·0: discriminating signal peptides from transmembrane regions. Nature Methods 8, 785786.Google Scholar
Pfaffl, MW, Horgan, GW and Dempfle, L (2002) Relative expression software tool (REST ©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 30, e36.Google Scholar
Piper, EK, Jonsson, NN, Gondro, C, Vance, ME, Lew-Tabor, AE and Jackson, LA (2016) Peripheral cellular and humoral responses to infestation with the cattle tick Rhipicephalus microplus in Santa-gertrudis cattle. International Journal for Parasitology 39, e12402.Google Scholar
Pohl, PC, Sorgine, MHF, Leal, AT, Logullo, C, Oliveira, PL, da Silva Vaz, I Jr. and Masuda, A (2008) An extraovarian aspartic protease accumulated in tick oocytes with vitellin-degradation activity. Comparative Biochemistry and Physiology, Part B 151, 392399.Google Scholar
Pohl, PC, Klafke, GM, Carvalho, DD, Martins, JR, Daffre, S, da Silva Vaz, I Jr., and Masuda, A (2011) ABC transporter efflux pumps: a defense mechanism against ivermectin in Rhipicephalus (Boophilus) microplus. International Journal For Parasitology 41, 13231333.CrossRefGoogle ScholarPubMed
Radulović, ŽM, Kim, TK, Porter, LM, Sze, S-H, Lewis, L and Mulenga, A (2014) A 24-48 h fed Amblyomma americanum tick saliva immuno-proteome. BMC Genomics 15, 518.Google Scholar
Reck, J Jr., Berger, M, Marks, FS, Zingali, RB, Canal, CW, Ferreira, CAS, Guimarães, JA and Termignoni, C (2009) Pharmacological action of tick saliva upon haemostasis and the neutralization ability of sera from repeatedly infested hosts. Parasitology 136, 13391349.Google Scholar
Reck, J, Klafke, GM, Webster, A, Dall'Agnol, B, Scheffer, R, Souza, UA, Corassini, VB, Vargas, R, dos Santos, JS and Martins, JR (2014) First report of fluazuron resistance in Rhipicephalus microplus: a field tick population resistant to six classes of acaricides. Veterinary Parasitology 201, 128136.Google Scholar
Renard, G, Garcia, JF, Cardoso, FC, Richter, MF, Sanakari, JA, Ozaki, LS, Termignoni, C and Masuda, A (2000) Cloning and functional expression of a Boophilus microplus cathepsin L-like enzyme. Insect Biochemistry and Molecular Biology 30, 10171026.Google Scholar
Ribeiro, JMC (1987) Role of saliva in blood feeding by arthropods. Annual Reviews of Entomology 32, 463478.Google Scholar
Ribeiro, JMC, Alarcon-Chaidez, F, Francischetti, IMB, Mans, BJ, Mather, TN, Valenzuela, JG and Wikel, SK (2006) An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochemistry and Molecular Biology 36, 111129.CrossRefGoogle ScholarPubMed
Roberts, AJA (1968) Resistance of cattle to the tick Boophilus microplus (Canestrini). I. Development of ticks on Bos Taurus. The Jornal of Parasitology 54, 663666.Google Scholar
Rodriguez-Valle, M, Lew-Tabor, A, Gondro, C, Moolhuijzen, P, Vance, M, Guerrero, FD, Bellgard, M and Jorgensen, W (2010) Comparative microarray analysis of Rhipicephalus (Boophilus) microplus expression profiles of larvae pre-attachment and feeding adult female stages on Bos indicus and Bos Taurus cattle. BMC Genomics 11, 437.Google Scholar
Rott, MB, Fernández, V, Farias, S, Ceni, J, Ferreira, HB, Haag, KL and Zaha, A (2000) Comparative analysis of two different subunits of antigen B from Echinococcus granulosus: gene sequences, expression in Escherichia coli and serological evaluation. Acta Troprica 75, 331340.Google Scholar
Sachetto-Martins, G, Franco, LO and de Oliveira, DE (2000) Plant glycine-rich proteins: a family or just proteins with a common motif? Biochimica et Biophysica Acta 1492, 114.Google Scholar
Sambrook, J, Fritsch, EF and Maniatis, T (1989) Molecular Cloning. A Laboratory Manual, 2nd edn., New York, USA: Cold Spring Harbor Laboratory Press.Google Scholar
Shahein, YE, Abouelella, AM, Hussein, NA, Hamed, RR, El-Hakim, AE, Abdel-Shafy, S and Tork, SE (2013) Identification of four novel Rhipicephalus annulatus upregulated salivary gland proteins as candidate vaccines. The Protein Journal 32, 392398.Google Scholar
Shapiro, SZ, Voigt, WP and Ellis, JA (1989) Acquired resistance to ixodid ticks induced by tick cement antigen. Experimental & Applied Acarology 7, 3341.Google Scholar
Steentoft, C, Vakhrushev, SY, Joshi, HJ, Kong, Y, Vester-Christensen, MB, Schjoldager, KT, Lavrsen, K, Dabelsteen, S, Pedersen, NB, Marcos-Silva, L, Gupta, R, Bennett, EP, Mandel, U, Brunak, S, Wandall, HH, Levery, SB and Clausen, H (2013) Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. The EMBO Journal 32, 14781488.Google Scholar
Sudo, S, Fujikawa, T, Nagakura, T, Ohkubo, T, Sakaguchi, K, Tanaka, M, Nakashima, K and Takahashi, T (1997) Structures of mollusc shell framework proteins. Nature 387, 563564.Google Scholar
Tan, AWL, Francischetti, IMB, Slovak, M, Kini, RM and Ribeiro, JMC (2015) Sexual differences in the sialomes of the zebra tick, Rhipicephalus pulchellus. Journal of Proteomics 117, 120144.Google Scholar
Thompson, JD, Higgins, DG and Gibson, TJ (1994) CLUSTAL w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.Google Scholar
Tirloni, L, Reck, J, Terra, RMS, Martins, JR, Mulenga, A, Sherman, NE, Fox, JW, Yates, JR, Termignoni, C, Pinto, AFM and da Silva Vaz, I Jr. (2014) Proteomic analysis of cattle tick Rhipicephalus (Boophilus) microplus saliva: a comparison between partially and fully engorged females. PLoS ONE 9, e94831.Google Scholar
Trager, W (1939) Acquired immunity to ticks. The Journal of Parasitology 25, 5781.Google Scholar
Trimnell, AR, Hails, RS and Nuttall, PA (2002) Dual action ectoparasite vaccine targeting ‘exposed’ and ‘concealed’ antigens. Vaccine 20, 35603568.Google Scholar
Trimnell, AR, Davies, GM, Lissina, O, Hails, RS and Nuttall, PA (2005) A cross-reactive tick cement antigen is a candidate broad-spectrum tick vaccine. Vaccine 23, 43294341.Google Scholar
Tsitilout, SG, Rodakis, GC, Alexopoulou, M, Kafatos, FC, Ito, K and Iatroul, K (1983) Structural features of B family chorion sequences in the silkmoth Bombyx mori, and their evolutionary implications. The EMBO Journal 2, 18451852.Google Scholar
Untalan, PM, Guerrero, FD, Haines, LR and Pearson, TW (2005) Proteome analysis of abundantly expressed proteins from unfed larvae of the cattle tick, Boophilus microplus. Insect Biochemistry and Molecular Biology 35, 141151.Google Scholar
Wang, H, Paesen, GC, Nuttall, PA and Barbour, AG (1998) Male ticks help their mates to feed. Nature 391, 753754.Google Scholar
Willadsen, P (2004) Anti-tick vaccines. Parasitology 129, S367S387.Google Scholar
Willadsen, P (2006) Vaccination against ectoparasites. Parasitology 133, 925.Google Scholar
Willadsen, P and Kemp, DH (1988) Vaccination with ‘concealed’ antigens for tick control. Parasitology Today 4, 196198.Google Scholar
Xu, XL, Cheng, TY, Yang, H and Liao, ZH (2016) De novo assembly and analysis of midgut transcriptome of Haemaphysalis flava and identification of genes involved in blood digestion, feeding and defending from pathogens. Infection, Genetics and Evolution 38, 6272.Google Scholar
Yamaguchi, E, Yamauchi, K, Gullion, T and Asakura, T (2009) Structural analysis of the Gly-rich region in spider dragline silk using stable-isotope labeled sequential model peptides and solid-state NMR. Chemical Communications 28, 41764178.Google Scholar
Yazawa, K, Yamaguchi, E, Knight, D and Asakura, T (2011) 13C solid-state NMR study of the 13C-labeled peptide, (E)8GGLGGQGAG(A)6GGAGQGGYGG as a model for the local structure of Nephila clavipes dragline silk (MaSp1) before and after spinning. Biopolymers 97, 347354.Google Scholar
Zhang, J, Goyer, C and Pelletier, Y (2008) Environmental stresses induce the expression of putative glycine-rich insect cuticular protein genes in adult Leptinotarsa decemlineata (Say). Insect Molecular Biology 17, 209216.CrossRefGoogle ScholarPubMed
Zhong, YS, Mita, K, Shimada, T and Kawasaki, H (2006) Glycine-rich protein genes, which encode a major component of the cuticle, have different developmental profiles from other cuticle protein genes in Bombyx mori. Insect Biochemistry and Molecular Biology 36, 99110.Google Scholar
Zhou, J, Gong, H, Zhou, Y, Xuan, X and Fujisaki, K (2006) Identification of a glycine-rich protein from the tick Rhipicephalus haemaphysaloides and evaluation of its vaccine potential against tick feeding. Parasitology Research 100, 7784.Google Scholar
Supplementary material: File

Leal et al supplementary material

Leal et al supplementary material 1

Download Leal et al supplementary material(File)
File 2.2 MB
Supplementary material: File

Leal et al supplementary material

Leal et al supplementary material 2

Download Leal et al supplementary material(File)
File 20.1 KB