Advertisement

Experimental and Applied Acarology

, Volume 76, Issue 2, pp 229–241 | Cite as

Differential expression analysis for subolesin in Rhipicephalus microplus infected with Anaplasma marginale

  • Verónica Carvajal-de la Fuente
  • Octavio Merino-Charrez
  • Erick Tovar-Carman
  • Sergio D. Rodríguez-Camarillo
  • Rodolfo E. Lagunes-Quintanilla
  • Fernando A. Muñoz-Tenería
  • Marinela Contreras
  • José de la Fuente
Article
  • 87 Downloads

Abstract

Rhipicephalus microplus (formerly Boophilus microplus) ticks are potential vectors of several pathogens of livestock especially in tropical and subtropical regions where may have substantial effects on economic development. Among tick-borne pathogens, Anaplasma marginale is considered one of the most important in domestic and wild ruminants worldwide. Different molecular mechanisms have been employed by both ticks and these intracellular pathogens, in order to be able to adapt and survive. Subolesin, originally called 4D8, is an evolutionarily well-preserved protein among ixodid tick species. This new antigen was found to be protective against tick infestations when used as a vaccine, as it has an essential role in tick blood digestion, development and infection of host cells by A. marginale. Recent studies have demonstrated that infection of both tick and vertebrate host cells with this microorganism changed gene expression. Therefore, the main objective of this study was to investigate subolesin expression in uninfected and A. marginale-infected R. microplus salivary glands by real-time reverse transcriptase (RT)-PCR. To analyze the differential expression of the recombinant protein subolesin, the gene was previously expressed from ticks infected with A. marginale. Results from this study revealed that, the expression of subolesin was significantly higher in salivary glands of infected R. microplus in comparison to uninfected ones.

Keywords

Rhipicephalus microplus Subolesin Salivary gland Gene expression Anaplasma marginale 

Notes

Acknowledgments

This work was supported by the Project CB-2015-01-255205: “Caracterización proteómica de Rhipicephalus microplus, R. annulatus y Amblyomma cajenennse para el control de infestaciones en bovinos”. Authorization DICB/C1000/3284/2016 funded by SEP-CONACYT.

Authors' contribution

All authors have seen and approved the manuscript and have contributed significantly to the work.

Compliance with ethical standards

Conflict of interest

All authors declare that there are no financial or other relationships that might lead to a conflict of interest.

References

  1. Almazán C, Kocan KM, Bergman DK, Garcia-Garcia JC, Blouin EF, De La Fuente J (2003) Identification of protective antigens for the control of Ixodes scapularis infestations using cDNA expression library immunization. Vaccine 21:1492–1501.  https://doi.org/10.1016/S0264-410X(02)00683-7 CrossRefPubMedGoogle Scholar
  2. Almazán C, Kocan KM, Blouin EF, De La Fuente J (2005) Vaccination with recombinant tick antigens for the control of Ixodes scapularis adult infestations. Vaccine 23:5294–5298.  https://doi.org/10.1016/j.vaccine.2005.08.004 CrossRefPubMedGoogle Scholar
  3. Antunes S, Merino O, Mosqueda J, Moreno-Cid JA, Bell-Sakyi L, Fragkoudis R, Weisheit S, Pérez De La Lastra JM, Alberdi P, Domingos A, De La Fuente J (2014) Tick capillary feeding for the study of proteins involved in tick-pathogen interactions as potential antigens for the control of tick infestation and pathogen infection. Parasites Vectors 7:42.  https://doi.org/10.1186/1756-3305-7-42 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Contreras M, Alberdi P, Mateos-Hernández L, Fernández de Mera IG, García-Pérez AL, Vancová M, Villar M, Ayllón N, Cabezas-Cruz A, Valdés JJ, Stuen S, Gortazar C, de la Fuente J (2017) Anaplasma phagocytophilum MSP4 and HSP70 proteins are involved in interactions with host cells during pathogen infection. Front Cell Infect Microbiol.  https://doi.org/10.3389/fcimb.2017.00307 CrossRefPubMedPubMedCentralGoogle Scholar
  5. de la Fuente J, Merino O (2013) Vaccinomics, the new road to tick vaccines. Vaccine 31:5923–5929.  https://doi.org/10.1016/j.vaccine.2013.10.049 CrossRefPubMedGoogle Scholar
  6. 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, Lleonart R (1999) Vaccination against ticks (Boophilus spp.): the experience with the Bm86-based vaccine Gavac. Genet Anal 3–5:143–148CrossRefGoogle Scholar
  7. de la Fuente J, Van Den Bussche RA, Kocan KM (2001) Molecular phylogeny and biogeography of North American isolates of Anaplasma marginale (Rickettsiaceae: Ehrlichieae). Vet Parasitol 97:65–76.  https://doi.org/10.1016/S0304-4017(01)00378-8 CrossRefPubMedGoogle Scholar
  8. de la Fuente J, Lew A, Lutz H, Meli ML, Hofmann-Lehmann R, Shkap V, Molad T, Mangold AJ, Almazán C, Naranjo V, Gortázar C, Torina A, Caracappa S, García-Pérez AL, Barral M, Oporto B, Ceci L, Carelli G, Blouin EF, Kocan KM (2005) Genetic diversity of Anaplasma species major surface proteins and implications for anaplasmosis serodiagnosis and vaccine development. Anim Health Res Rev 6:75–89.  https://doi.org/10.1079/AHR2005104 CrossRefPubMedGoogle Scholar
  9. de la Fuente J, Almazán C, Blas-Machado U, Naranjo V, Mangold AJ, Blouin EF, Gortazar C, Kocan KM (2006a) The tick protective antigen, 4D8, is a conserved protein involved in modulation of tick blood ingestion and reproduction. Vaccine 24:4082–4095.  https://doi.org/10.1016/j.vaccine.2006.02.046 CrossRefPubMedGoogle Scholar
  10. de La Fuente J, Almazán C, Blouin EF, Naranjo V, Kocan KM (2006b) Reduction of tick infections with Anaplasma marginale and A. phagocytophilum by targeting the tick protective antigen subolesin. Parasitol Res 100:85–91.  https://doi.org/10.1007/s00436-006-0244-6 CrossRefPubMedGoogle Scholar
  11. de La Fuente J, Blouin EF, Manzano-Roman R, Naranjo V, Almazán C, De La Lastra JMP, Zivkovic Z, Massung RF, Jongejan F, Kocan KM (2008a) Differential expression of the tick protective antigen subolesin in Anaplasma marginale and A. phagocytophilum-infected host cells. Ann N Y Acad Sci 1149:27–35CrossRefGoogle Scholar
  12. de la Fuente J, Maritz-Olivier C, Naranjo V, Ayoubi P, Nijhof AM, Almazán C, Canales M, de la Lastra JMP, Galindo RC, Blouin EF, Gortazar C, Jongejan F, Kocan KM (2008b) Evidence of the role of tick subolesin in gene expression. BMC Genom.  https://doi.org/10.1186/1471-2164-9-372 CrossRefGoogle Scholar
  13. de la Fuente J, Moreno-Cid JA, Canales M, Villar M, de la Lastra JMP, Kocan KM, Galindo RC, Almazán C, Blouin EF (2011) Targeting arthropod subolesin/akirin for the development of a universal vaccine for control of vector infestations and pathogen transmission. Vet Parasitol 181:17–22.  https://doi.org/10.1016/j.vetpar.2011.04.018 CrossRefPubMedGoogle Scholar
  14. Estrada-Peña SM (2013) Current limitations in the control and spread of ticks that affect livestock: a review. Agriculture 3(2):221–235CrossRefGoogle Scholar
  15. García-García JC, Montero C, Redondo M, Vargas M, Canales M, Boue O, Rodríguez M, Joglar M, MacHado H, González IL, Valdés M, Méndez 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.  https://doi.org/10.1016/S0264-410X(99)00548-4 CrossRefPubMedGoogle Scholar
  16. Ghosh S, Azhahianambi P, Yadav MP (2007) Upcoming and future strategies of tick control: a review. J Vector Borne Dis 44(2):79–89PubMedGoogle Scholar
  17. Khumalo ZTH, Catanese HN, Liesching N, Hove P, Collins NE, Chaisi ME, Gebremedhin AH, Oosthuizen MC, Brayton KA (2016) Characterization of Anaplasma marginale subsp. centrale strains by use of msp1aS genotyping reveals a wildlife reservoir. J Clin Microbiol 54(10):2503–2512CrossRefGoogle Scholar
  18. Kocan KM, De La Fuente J, Blouin EF, Garcia-Garcia JC (2004) Anaplasma marginale (Rickettsiales: Anaplasmataceae): recent advances in defining host-pathogen adaptations of a tick-borne rickettsia. Parasitology 129:285–300.  https://doi.org/10.1017/S0031182003004700 CrossRefGoogle Scholar
  19. Kocan KM, de la Fuente J, Blouin EF (2008) Advances toward understanding the molecular biology of the Anaplasma-tick interface. Front Biosci 13:7032–7045CrossRefGoogle Scholar
  20. Kocan KM, Zivkovic Z, Blouin EF, Naranjo V, Almazan C, Mitra R, de la Fuente J (2009) Silencing of genes involved in Anaplasma marginale-tick interactions affects the pathogen developmental cycle in Dermacentor variabilis. BMC Dev Biol 9(1):42CrossRefGoogle Scholar
  21. Kröber T, Guerin PM (2007) An in vitro feeding assay to test acaricides for control of hard ticks. Pest Manag Sci 63:17–22.  https://doi.org/10.1002/ps.1293 CrossRefPubMedGoogle Scholar
  22. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods (San Diego, Calif.) 25:402–408.  https://doi.org/10.1006/meth.2001.1262 CrossRefGoogle Scholar
  23. Merino O, Almazán C, Canales M, Villar M, Moreno-Cid JA, Galindo RC, de la Fuente J (2011) Targeting the tick protective antigen subolesin reduces vector infestations and pathogen infection by Anaplasma marginale and Babesia bigemina. Vaccine 29:8575–8579.  https://doi.org/10.1016/j.vaccine.2011.09.023 CrossRefPubMedGoogle Scholar
  24. Merino O, Antunes S, Mosqueda J, Moreno-Cid JA, Pérez de la Lastra JM, Rosario-Cruz R, Rodríguez S, Domingos A, de la Fuente J (2013) Vaccination with proteins involved in tick-pathogen interactions reduces vector infestations and pathogen infection. Vaccine 31:5889–5896.  https://doi.org/10.1016/j.vaccine.2013.09.037 CrossRefPubMedGoogle Scholar
  25. Moreno-Cid JA, Pérez de la Lastra JM, Villar M, Jiménez M, Pinal R, Estrada-Peña A, Molina R, Lucientes J, Gortázar C, de la Fuente J, Alarcón-Elbal PM, Delacour S, Oropeza V, Ruiz I, Prudencio CR, Galindo RC, Almazán C, Nijhof AM, Mangold AJ (2013) Control of multiple arthropod vector infestations with subolesin/akirin vaccines. Vaccine 31:1187–1196.  https://doi.org/10.1016/j.vaccine.2012.12.073 CrossRefPubMedGoogle Scholar
  26. Naranjo V, Ayllón N, Pérez de la Lastra JM, Galindo RC, Kocan KM, Blouin EF, Mitra R, Alberdi P, Villar M, de la Fuente J (2013) Reciprocal regulation of NF-kB (Relish) and subolesin in the tick vector, Ixodes scapularis. PLoS ONE.  https://doi.org/10.1371/journal.pone.0065915 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Ocampo RJ, Camarillo SDR, Cruz RR, Vega LEO, de la Fuente J (2012) Anaplasma marginale: análisis de las secuencias del fragmento variable del gen msp1 alpha y del gen msp4 de cuatro nuevas cepas mexicanas. Revista Mexicana de Ciencias Pecuarias 46(1):69–78Google Scholar
  28. Patton TG, Dietrich G, Brandt K, Dolan MC, Piesman J, Gilmore RD (2012) Saliva, salivary gland, and hemolymph collection from Ixodes scapularis ticks. J Vis Exp 60:3894.  https://doi.org/10.3791/3894 CrossRefGoogle Scholar
  29. Pipano E, Alekceev E, Galker F, Fish L, Samish M, Shkap V (2003) Immunity against Boophilus annulatus induced by the Bm86 (Tick-GARD) vaccine. Exp Appl Acarol 29:141–149.  https://doi.org/10.1023/A:1024246903197 CrossRefPubMedGoogle Scholar
  30. Sossai S, Peconick AP, Sales PA, 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.  https://doi.org/10.1007/s10493-005-3262-7 CrossRefPubMedGoogle Scholar
  31. Villar M, Marina A, de la Fuente J (2017) Applying proteomics to tick vaccine development: Where are we? Expert Rev Proteom 14(3):211–221.  https://doi.org/10.1080/14789450.2017.1284590 CrossRefGoogle Scholar
  32. Zivkovic Z, Torina A, Mitra R, Alongi A, Scimeca S, Kocan KM, Galindo RC, Almazán C, Blouin EF, Villar M, Nijhof AM, Mani R, La Barbera G, Caracappa S, Jongejan F, de la Fuente J (2010) Subolesin expression in response to pathogen infection in ticks. BMC Immunol 11:7.  https://doi.org/10.1186/1471-2172-11-7 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Verónica Carvajal-de la Fuente
    • 1
    • 2
  • Octavio Merino-Charrez
    • 2
  • Erick Tovar-Carman
    • 2
  • Sergio D. Rodríguez-Camarillo
    • 3
  • Rodolfo E. Lagunes-Quintanilla
    • 3
  • Fernando A. Muñoz-Tenería
    • 1
  • Marinela Contreras
    • 4
  • José de la Fuente
    • 4
    • 5
  1. 1.Facultad de Agronomía y VeterinariaUniversidad Autónoma de San Luis PotosíSoledad de Graciano SánchezMexico
  2. 2.Facultad de Medicina Veterinaria y ZootecniaUniversidad Autónoma de TamaulipasCiudad VictoriaMexico
  3. 3.Instituto Nacional de Investigaciones Forestales Agrícolas y PecuariasCd. de MéxicoMéxico
  4. 4.SaBioInstituto de Investigación en Recursos Cinegéticos IREC-CSIC-UCLM-JCCMCiudad RealSpain
  5. 5.Department of Veterinary Pathobiology, Center for Veterinary Health SciencesOklahoma State UniversityStillwaterUSA

Personalised recommendations