Morphological Plasticity of Ticks’ Salivary Glands and the Meaning of Hematophagy in Hosts Immunized with Glandular Extract of Females Fed for 4 Days
Animal and Veterinary Sciences
Volume 2, Issue 6, November 2014, Pages: 194-207
Received: Nov. 11, 2014; Accepted: Nov. 28, 2014; Published: Dec. 15, 2014
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Authors
Karim Christina Scopinho Furquim, Departamento de Biologia, Instituto de Biociências, UNESP, Av. 24 A, nº 1515, Cx. Postal 199, CEP: 13506-900, Rio Claro, S.P., Brazil
Maria Izabel Camargo Mathias, Departamento de Biologia, Instituto de Biociências, UNESP, Av. 24 A, nº 1515, Cx. Postal 199, CEP: 13506-900, Rio Claro, S.P., Brazil
Gislaine Cristina Roma, Departamento de Biologia, Instituto de Biociências, UNESP, Av. 24 A, nº 1515, Cx. Postal 199, CEP: 13506-900, Rio Claro, S.P., Brazil
Letícia Maria Gráballos Ferraz Hebling, Departamento de Biologia, Instituto de Biociências, UNESP, Av. 24 A, nº 1515, Cx. Postal 199, CEP: 13506-900, Rio Claro, S.P., Brazil
Gervásio Henrique Bechara, Departamento de Patologia Veterinária, FCAV, UNESP, Via de Acesso Prof. Paulo Castellane, s/n, CEP: 14884-900, Jaboticabal, S.P., Brazil
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Abstract
A histochemical analysis was performed in this study in order to detect proteins, polysaccharides, lipids, acid phosphatase and calcium in the secretion produced by the salivary glands of Rhipicephalus sanguineus females (Latreille, 1806) (Acari, Ixodidae) fed for 2, 4 and 6 days in New Zealand White rabbits which had been previously immunized with glandular extract obtained from females fed for 4 days (SGE4). The results revealed that such glands presented alterations in their secretory cycle, which occurred: a) by the inactivity of some c1 cells (in the glands of females fed for 2 days) and c4 (in those fed for 4 days) and b) by the modification in the constitution of the secretion of females fed for 2-6 days. It was verified that, in the glands of females fed for 2 days, there was an increase in proteins and calcium; a reduction in lipids and the contents of polysaccharides and acid phosphatase remained unaltered. In those fed for 4 days there was an increase in proteins, calcium and acid phosphatase; reduction in the lipids, and the content of polysaccharides remained unaltered. In the females fed for 6 days an increase in the components was observed; however, there was a reduction in lipids and acid phosphatase. In addition, it was verified that, in a decrescent order of histochemical alterations, the most affected cells were: f; c2, c3, c5; a, d and c4, e in the glands of females fed for 2 days; c5; a, c2, c3, d and c1, e in the glands of females fed for 4 days and a, c1, c2, d and e, c3 in the glands of females fed for 6 days. The data here obtained clearly show that the most pronounced histochemical modifications were detected in the glands of females fed for 2 and 6 days; however, the modifications observed in the females fed for 4 days must also be considered, once they were significant as well. This has probably occurred because the hosts were inoculated with SGE4, obtained from the salivary glands of females fed for 4 days, intermediate stage of the glandular cycle, which contains antigens that are common to glandular tissues of females fed for 2 and 6 days.
Keywords
Rhipicephalus sanguineus, Immunization, Antigen, Salivary Gland, Secretory Cycle, Histochemistry, Immune-Inflammatory Response
To cite this article
Karim Christina Scopinho Furquim, Maria Izabel Camargo Mathias, Gislaine Cristina Roma, Letícia Maria Gráballos Ferraz Hebling, Gervásio Henrique Bechara, Morphological Plasticity of Ticks’ Salivary Glands and the Meaning of Hematophagy in Hosts Immunized with Glandular Extract of Females Fed for 4 Days, Animal and Veterinary Sciences. Vol. 2, No. 6, 2014, pp. 194-207. doi: 10.11648/j.avs.20140206.17
References
[1]
N. A. Steen, S. C. Barker, P. F. Alewood, “Proteins in the saliva of the Ixodida (ticks): Pharmacological features and biological significance”, Toxicon, vol. 47, pp. 1-20, Janery 2006.
[2]
B. J. Mans, A. W. H. Neitz, “Adaptation of ticks to a blood feeding environment: Evolution from a functional perspective”, Insect Biochem. Mol. Biol., vol. 34, pp. 1-17, Janery 2004.
[3]
K. C. Binnington, “Sequential changes in salivary gland structure during attachment and feeding of the cattle tick Boophilus microplus”, Int. J. Parasitol., vol. 8, pp. 97-115, April 1978.
[4]
A. Walker, J. D. Fletcher, H. S. Gill, “Structural and histochemical changes in the salivary glands of Rhipicephalus appendiculatus during feeding”, Int. J. Parasitol. vol. 15, pp. 81-100, February 1985.
[5]
H. S. Gill, A. R. Walker, “The salivary glands of Hyalomma anatolicum anatolicum: Nature of salivary gland components and their role in tick attachment and feeding”, Int. J. Parasitol., vol. 18, pp. 83-93, February 1988.
[6]
D. E. Sonenshine, Biology of ticks. New York: Oxford University Press, 1991.
[7]
K. C. S. Furquim, M. I. Camargo-Mathias, L. M. G. F. Hebling, G. C. Roma, G. H. Bechara, “Ticks’ response to feeding on host immunized with glandular extracts of Rhipicephalus sanguineus females fed for 2, 4, and 6 days. I. Inactivity or early degeneration of salivary glands?”, Parasitol. Res., vol. 109, pp. 147-162, July 2011.
[8]
M. I. Camargo-Matias, K. C. S. Furquim, “The histology as a tool for the understanding of the morphophysiology of the brown dog tick (Rhipicephalus sanguineus)”, in Advances in zoology research, vol. 5, O. P. Jenkins, Eds. New York: Nova Science Publishers, 2013, pp. 167-191.
[9]
M. I. Camargo-Mathias, K. C. S. Furquim, P. H. Nunes, “Immunomodulatory effects of tick saliva”, Invertebrate Surviv. J., vol. 8, pp. 231-240, December 2011.
[10]
J. M. C. Ribeiro, G. T. Makoul, J. Levine, D. K. Robinson, A. Spilman, “Antihaemostatic, antiinflammatory and immunosupressive properties of the saliva of a tick, Ixodes dammini”, J. Exp. Med., vol. 161, pp. 332-344, February 1985.
[11]
M. Brossar, S. K. Wikel, “Tick immunobiology”, Parasitology, vol. 129, pp. S161-S176, October 2004.
[12]
I. M. B. Francicchetti, T. N. Mather, J. N. C. Ribeiro, “Tick saliva is a potent inhibitor of endothelial cell proliferation and angiogenesis”, Thromb. Haemost., vol. 94, pp. 167-174, July 2005.
[13]
S. Jittapalapong, R. W. Stich, J. C. Gordon, T. E. Wittum, O. O. Barriga, “Performance of female Rhipicephalus sanguineus (Acari: Ixodidae) fed dogs exposed to multiple infestations or immunization with tick salivary gland or midgut tissues”, J. Med. Entomol., 37: 601-611, July 2000.
[14]
C. M. Wheeler, J. L. Coleman, J. L. Benach, “Salivary gland antigens of Ixodes dammini are glycoproteins that have interspecies cross-reactivity”, J. Parasitol., vol. 77, pp. 965-973, December 1991.
[15]
G. H. Bechara, M. P. J. Szabó, B. R. Ferreira, M. V. Garcia, “Rhipicephalus sanguineus tick in Brazil: feeding and reproductive aspects under laboratorial conditions”, Brazil. J. Vet. Parasitol., vol. 4, pp. 61-66, August 1995.
[16]
K. C. S. Furquim, M. I. Camargo-Mathias, L. M. G. F. Hebling, G. C. Roma, G. H. Bechara, “Alterations in the secretory behavior of salivary glands of Rhipicephalus sanguineus females (Latreille, 1806) (Acari: Ixodidae) feeding in resistant rabbit”, Air Water Borne Diseases, vol. 2, pp. 114, doi: 10.4172/2167-7719.1000114, October 2013.
[17]
A. G. E. Pearse, Histochemistry. Theoretical and applied, vol. 2: Analytic Technology, 4th ed., Edinburgh: Churchill Livingston, 1985.
[18]
J. F. A. McManus, “Histological demonstration of mucin after periodic acid”. Nature, vol. 158, pp. 202, August 1946.
[19]
L. C. U. Junqueira, L. M. M. S. Junqueira, Técnicas básicas de citologia e histologia, São Paulo: Editora Santos, 1983.
[20]
J. R. Baker, “The histochemical regogntion of lipine”. Q. J. Microsc. Sci., vol. 87, pp. 441-470, December 1946.
[21]
M. A. Hussein, I. D. Bowen, G. H. Lewis, “The histochemical localization of ATPase, cholinesterase and acid phosphatase activity in Culex pipiens (Diptera, Culicidae) larvae using a methacrylate embedding technique”, Cell Biol. Int. Rep., vol. 14, pp. 775-781, September 1990.
[22]
J. M. C. Ribeiro, “Role of saliva in blood feeding by arthropods”, Annu. Rev. Entomol., vol. 32, pp. 463-478, January 1987.
[23]
H. L. McMullen, J. R. Sauer, R. L. Burton, “Possible role in uptake of water vapour by ixodid ticks salivary glands”, J. Insect Physiol., vol. 22, pp. 1281-1285, April 1976.
[24]
D. Rudolph, W. Knülle, “Uptake of water vapour from air: process, site, and mechanism in ticks”, in Comparative Physiology: Water, Ions and Fluid Mechanics, K. Schmidt-Nielsen, L. Bolis and S. H. P. Maddrell, Eds. Cambridge: Cambridge University Press, 1978, pp.84-85.
[25]
A. Mulenga, M. Blandon, R. Khumthong, “The molecular basis of the Amblyomma americanum tick attachment phase”, Exp. Appl. Acarol., vol. 41, pp. 267-287, April 2007.
[26]
D. E. Sonenshine, Biology of Ticks, vol. 2. Oxford: Oxford University Press, 1993.
[27]
S. G. Harris, J. Padilla, L. Koumas, D. Ray, R. P. Phipps, “Prostaglandins as modulators of immunity”, Trends Immunol., vol. 23, pp. 144–150, March 2002.
[28]
J. C. Oliveira, A. Sá-Nunes, I. M. B. Francischetti, V.Carregaro, E. Anatriello, J. S. Silva, I. K. F. Miranda Santos, J. M. C. Ribeiro, B. R. Ferreira, “Deconstructing saliva. Non-protein molecules with potent immunomodulatory properties”, J. Biol. Chem., vol. 286, pp. 10960-10969, April 2011.
[29]
J. M. C. Ribeiro, G. Makoul, D. Robinson, “Ixodes dammini: Evidence for salivary prostacyclin secretion”, J. Parasitol., vol. 74, pp. 1068-1069, December 1988.
[30]
I. M. B. Francischetti, A. Sá-Nunes, B. J. Mans, I. M. Santos, J. M. C. Ribeiro, “The role of saliva in tick feeding”, Front. Biosci., vol. 14, pp. 2051-2088, January 2010.
[31]
R. Bishop, B. Lambson, C. Wells, P. Pandit, J. Osaso, C. Nkonge, S. Morzaria, A. Musoke, V. Nene, “A cement protein of the tick Rhipicephalus sanguineus, located in the secretory e cell granules of the type III salivary gland acini, induces strong antibody response in cattle”, Int J Parasitol, vol. 32, pp. 833-842, January 2002.
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