Abstract
We describe the intestinal changes and biological parameters of the tick species Rhipicephalus microplus exposed to the immune response of calves vaccinated with two subunits of immunogens. The first group of Bos taurus calves was immunized with a synthetic peptide (SBm7462), whereas the second group received an inoculum for synthetic control. The third group was immunized with a recombinant peptide (rSBm7462); an inoculum was injected into a fourth group of calves for recombinant control. Each formulation was administered to these calves during three times at intervals of 30 days. At 21 days after the last immunization, the calves were challenged using a total of 4500 larvae per animal. Indirect ELISA was realized to identify the kinetics of IgGs from samples of calves studied. Naturally detaching ticks were collected for analyses of biological performance and histological changes in the midgut. We dissected randomly detached ticks. The midgut of each of these ticks was removed and processed routinely for histology, stained with hematoxylin-eosin (H&E) and slow Giemsa. Slides were also subjected to immunohistochemistry. The antibody response showed significant induction of high-affinity IgGs in calves immunized with both peptides in comparison to calves of the control groups. Histological changes included damage of the intestinal epithelium in ticks fed on immunized hosts and intense immunostaining in midgut cells, using the serum of calves immunized with recombinant peptide. There were significant differences in all biological performing parameters of ticks detached from vaccinated calves in comparison with ticks of the control groups. We identified reductions of 87.7 and 93.5% in engorged ticks detached from calves immunized with a synthetic and recombinant peptides, respectively, a 28 and 8.60% lower egg mass in groups immunized with synthetic and recombinant peptides, respectively, and a 38.4% reduction of the value of nutrient index/tick in the group immunized with the recombinant peptide. Our findings show that the immune response induced by small peptides in cattle can modify the digestion and metabolism of ticks fed on vaccinated animals, resulting in changes in tick performance.
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References
Agbede RIS (1986) Scanning electron microscopy of digest cells in the midgut epithelium of Boophilus microplus. Exp Appl Acarol 2:329–335. https://doi.org/10.1007/BF01193899
Agbede RIS, Kemp DH (1985) Digestion in the cattle-tick Boophilus microplus: light microscope study of the gut cells in nymphs and females. Int J Parasitol 15:147–157. https://doi.org/10.1016/0020-7519(85)90080-3
Agbede RIS, Kemp DH (1986) Immunization of cattle against Boophilus microplus using extracts derived from adult female ticks: histopathology of ticks feeding on vaccinated cattle. Int J Parasitol 16:35–41. https://doi.org/10.1016/0020-7519(86)90062-7
Agbede RIS, Kemp DH, Hoyte HMD (1986) Babesia bovis infection of secretory cells in the gut of the vector tick Boophilus microplus. Int J Parasitol 16:109–114. https://doi.org/10.1016/0020-7519(86)90095-0
Agyei AD, Runham NW (1995) Studies on the morphological changes in the midguts of two ixodid tick species Boophilus microplus and Rhipicephalus appendiculatus during digestion of the blood meal. Int J Parasitol 25:55–62. https://doi.org/10.1016/0020-7519(94)00114-4
Akov S (1982) Blood digestion in ticks. In: Obenchain F, Galun R (eds) Physiology of ticks, 1st edn. Pergamon Press Ltd, Oxford, pp 197–211
Bennett GF (1974) Oviposition of Boophilus microplus (Canestrini) (Acarida : Ixodidae). I. Influence of tick size on egg production. Acarologia 16:52–61
Canal CW, Maia HM, Vaz Junior IS et al (1995) Changing patterns of vitellin-related peptides during development of the cattle tick Boophilus microplus. Exp Appl Acarol 19:325–336. https://doi.org/10.1007/BF00052390
De Campos PM (1998) Daily mean number of eggs laid by the southern cattle tick (Acari: Ixodidae) compared with mean egg mass weight. J Econ Entomol 91:153–158. https://doi.org/10.1093/jee/91.1.153
De Sousa Neves E (2011) Avaliação “in vivo” da eficiência de dois imunógenos recombinantes derivados do peptídeo sbm7462® para o controle do carrapato rhipicephalus (Boophilus) microplus (canestrini 1887). Dissertation, Universidade Federal de Viçosa
Franta Z, Frantová H, Konvičková J et al (2010a) Dynamics of digestive proteolytic system during blood feeding of the hard tick Ixodes ricinus. Parasite Vectors 3:119. https://doi.org/10.1186/1756-3305-3-119
Franta Z, Frantová H, Konvičková J et al (2010b) Dynamics of digestive proteolytic system during blood feeding of the hard tick Ixodes ricinus. Parasite Vectors 3:1–11. https://doi.org/10.1186/1756-3305-3-119
García-García JC, Gonzalez IL, González DM et al (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. https://doi.org/10.1023/A:1006270615158
George JE (2006) Present and future technologies for tick control. Ann N Y Acad Sci 916:583–588. https://doi.org/10.1111/j.1749-6632.2000.tb05340.x
Grisi L, Leite RC, Martins JRDS et al (2014) Reassessment of the potential economic impact of cattle parasites in Brazil. Rev Bras Parasitol Vet 23:150–156. https://doi.org/10.1590/S1984-29612014042
Horn M, Nussbaumerová M, Šanda M et al (2009) Hemoglobin digestion in blood-feeding ticks: mapping a multipeptidase pathway by functional proteomics. Chem Biol 16:1053–1063. https://doi.org/10.1016/j.chembiol.2009.09.009
Johnston LAY, Kemp DH, Pearson RD (1986) Immunization of cattle against Boophilus microplus using extracts derived from adult female ticks: effects of induced immunity on tick populations. Int J Parasitol 16:27–34. https://doi.org/10.1016/0020-7519(86)90061-5
Kiss T, Cadar D, Spînu M (2012) Tick prevention at a crossroad: new and renewed solutions. Vet Parasitol 187:357–366. https://doi.org/10.1016/j.vetpar.2012.02.010
Kongsuwan K, Josh P, Zhu Y et al (2010) Exploring the midgut proteome of partially fed female cattle tick (Rhipicephalus (Boophilus) microplus). J Insect Physiol 56:212–226. https://doi.org/10.1016/j.jinsphys.2009.10.003
Labruna MB, Leite RC, de Oliveira PR (1997) Study of the weight of eggs from six ixodid species from Brazil. Mem Inst Oswaldo Cruz 92:205–207. https://doi.org/10.1590/S0074-02761997000200012
Labruna MB, Naranjo V, Mangold AJ et al (2009) Allopatric speciation in ticks: genetic and reproductive divergence between geographic strains of Rhipicephalus (Boophilus) microplus. BMC Evol Biol 9:46. https://doi.org/10.1186/1471-2148-9-46
Lara FA (2003) A new intracellular pathway of haem detoxification in the midgut of the cattle tick Boophilus microplus: aggregation inside a specialized organelle, the hemosome. J Exp Biol 206:1707–1715. https://doi.org/10.1242/jeb.00334
Mans BJ (2014) Heme processing and the evolution of hematophagy. In: Sonenshine DE, Roe MR (eds) Biology of ticks, 2nd edn. Oxford University Press, Oxford, pp 220–239
Maritz-Olivier C, van Zyl W, Stutzer C (2012) A systematic, functional genomics, and reverse vaccinology approach to the identification of vaccine candidates in the cattle tick, Rhipicephalus microplus. Ticks Tick Borne Dis 3:179–187. https://doi.org/10.1016/j.ttbdis.2012.01.003
Maya-Monteiro CM, Daffre S, Logullo C et al (2000) HeLp, a heme lipoprotein from the hemolymph of the cattle tick, Boophilus microplus. J Biol Chem 275:36584–36589. https://doi.org/10.1074/jbc.M007344200
Mora Hernández C, Massard C, Soares C, Fonseca A (1997) Altareções histológicas do trato digestivo de Boophilus microplus pela ação de anticorpos anti-rBm86. Braz J Vet Parasitol 6(33):37
Nuttall PA, Trimnell AR, Kazimirova M, Labuda M (2006) Exposed and concealed antigens as vaccine targets for controlling ticks and tick-borne diseases. Parasite Immunol 28:155–163. https://doi.org/10.1111/j.1365-3024.2006.00806.x
Ogihara M, Taylor D (2014) Female reproductive system anatomy, physiology, and molecular biology. In: Sonenshine DE, Roe MR (eds) Biology of ticks, vol 1, 2nd edn. Oxford University Press, Oxford, pp 249–283
Patarroyo J, Portela R, De Castro R et al (2002) Immunization of cattle with synthetic peptides derived from the Boophilus microplus gut protein (Bm86). Vet Immunol Immunopathol 88:163–172. https://doi.org/10.1016/S0165-2427(02)00154-X
Patarroyo JH, Vargas MI, González CZ et al (2009) Immune response of bovines stimulated by synthetic vaccine SBm7462® against Rhipicephalus (Boophilus) microplus. Vet Parasitol 166:333–339. https://doi.org/10.1016/j.vetpar.2009.09.036
Peconick AP, Sossai S, Girão FA et al (2008) Synthetic vaccine (SBm7462) against the cattle tick Rhipicephalus (Boophilus) microplus: preservation of immunogenic determinants in different strains from South America. Exp Parasitol 119:37–43. https://doi.org/10.1016/j.exppara.2007.12.007
Rajput ZI, Hu S, Xiao C, Arijo AG (2007) Adjuvant effects of saponins on animal immune responses. J Zhejiang Univ Sci B 8:153–161. https://doi.org/10.1631/jzus.2007.B0153
Sojka D, Franta Z, Horn M et al (2013) New insights into the machinery of blood digestion by ticks. Trends Parasitol 29:276–285. https://doi.org/10.1016/j.pt.2013.04.002
Sonenshine DE, Anderson JM (2014) Mouthparts and digestive system: anatomy and molecular biology of feeding and digestion. In: Sonenshine DE, Roe MR (eds) Biology of ticks, vol 1, 2nd edn. Oxford University Press, Oxford, pp 122–164
Sorgine MHF, Logullo C, Zingali RB et al (2000) A heme-binding aspartic proteinase from the eggs of the hard tick Boophilus microplus. J Biol Chem 275:28659–28665. https://doi.org/10.1074/jbc.M005675200
Sossai S (2009) Expressâo de Quatro peptídeos recombinantes derivados do peptídeo sintético SBm7462 em Pichia pastoris e avaliação da resposta imunológica induzida em camundongos. Thesis, Universidade Federal de Viçosa
Stutzer C, van Zyl WA, Olivier NA et al (2013) Gene expression profiling of adult female tissues in feeding Rhipicephalus microplus cattle ticks. Int J Parasitol 43:541–554. https://doi.org/10.1016/j.ijpara.2013.01.009
Willadsen P, Riding GA, McKenna RV et al (1989) Immunologic control of a parasitic arthropod. Identification of a protective antigen from Boophilus microplus. J Immunol 143:1346–1351
Acknowledgements
The authors gratefully acknowledge FAPEMIG (Foundation for Research Support of the State of Minas Gerais, Brazil) (Grant No. APQ-00998-12) for providing financial support and CAPES (Coordination for The Improvement of Higher Education Personnel) for providing scholarships to graduate students.
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The ticks were collected from cattle without causing pain or distress. The calves used in this trial received handling and treatment under qualified veterinary supervision in accordance with the animal experimentation rules described in the International Guiding Principles for Biomedical Research Involving Animals. This study and the research proposal were approved by the Animal Research Ethics Committee of the EMBRAPA: CEUA-EGL 06/2013.
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Tafur-Gómez, G.A., Patarroyo Salcedo, J.H., Vargas, M.I. et al. Intestinal changes and performance parameters in ticks feeding on calves immunized with subunits of immunogens against Rhipicephalus microplus. Exp Appl Acarol 80, 91–107 (2020). https://doi.org/10.1007/s10493-019-00451-8
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DOI: https://doi.org/10.1007/s10493-019-00451-8