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Alteration in mononuclear cell subpopulations in dogs immunized with gentamicin-attenuated Leishmania infantum

Published online by Cambridge University Press:  21 August 2012

HAMID DANESHVAR ,
FARNAZ SEDGHY ,
SHAHRIAR DABIRI ,
HOSSEIN KAMIABI ,
MOHAMMAD M. MOLAEI ,
STEPHEN PHILLIPS  and
RICHARD BURCHMORE
HAMID DANESHVAR*
Affiliation:
Research Center of Tropical and Infectious Diseases, Kerman University of Medical Sciences, Kerman, Iran
FARNAZ SEDGHY
Affiliation:
Immunology Department, Kerman Medical University, Kerman, Iran
SHAHRIAR DABIRI
Affiliation:
Surgical Pathology Department, Afzalipoor Hospital, Kerman Medical University, Kerman, Iran
HOSSEIN KAMIABI
Affiliation:
Leishmaniasis Research Centre, Kerman Medical University, Kerman, Iran
MOHAMMAD M. MOLAEI
Affiliation:
Veterinary Medical School, Shahid Bahonar University of Kerman, Kerman, Iran
STEPHEN PHILLIPS
Affiliation:
Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK
RICHARD BURCHMORE
Affiliation:
Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK
*
*Corresponding author: Research Center of Tropical and Infectious Diseases, Kerman University of Medical Sciences, Kerman, Iran. Tel: 0098 9133403912. E-mail: h.daneshvar@bio.gla.ac.uk
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Summary

The impact of immunization with gentamicin-attenuated Leishmania infantum (H-line) on the immunophenotypic profile of popliteal lymph node (PLN) and peripheral blood mononuclear cells (PBMCs) of dogs was assessed by flow cytometry and immunohistochemistry. Compared with the dogs infected with L. infantum wild-type (Group WT), there was a significantly higher percentage of CD4+, CD44+ T cells and CD14+, MHC-II+ cells and a lower percentage of CD4+ CD25+ regulatory T cells in PLN of the immunized dogs with L. infantum H-line (Group H). The percentage of CD4+ and CD8+ T cells in PBMCs of immunized dogs was higher than that in dogs of Group WT. The CD4:CD8 ratio in PLN of dogs of Group H was significantly higher than that in dogs of Group WT. A significantly higher percentage of CD21+ B cells and a lower percentage of CD79b+ cells were found in PLN of the immunized dogs compared with dogs of Group WT. Immunohistochemical investigation showed no parasites in the PLN of immunized dogs whereas there were parasites in the PLN of 60% of dogs infected with L. infantum WT. In this study, the immunophenotypic profile of mononuclear cells of the immunized dogs correlates with cellular immunity.

Type
Research Article
Information
Parasitology , Volume 139 , Issue 13 , November 2012 , pp. 1689 - 1696
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Araújo, M. S. S., de Andrade, R. A., Sathler-Avelar, R., Teixeira-Carvalho, A., Andrade, M. C., Viannac, L. R., Reis, M. A. B., Malaquiase, L. C. C., Mello, M. N. and Martins-Filho, O. A. (2009). T-cell-derived cytokines, nitric oxide production by peripheral blood monocytes and seric anti-Leishmania (Leishmania) chagasi IgG subclass patterns following immunization against canine visceral leishmaniasis using Leishvaccine and Leishmune®. Vaccine 27, 1008–1017.CrossRefGoogle ScholarPubMed
Belkaid, Y. (2003). The role of CD4(+)CD25(+) regulatory T cells in Leishmania infection. Experimental Opinion Biological Therapy 3, 875–885.CrossRefGoogle ScholarPubMed
Boggiatto, P. M., Ramer-Tait, A. E., Metz, K., Kramer, E. F., Gibson-Corley, K., Mullin, K., Hostetter, J. M., Gallup, J. M., Jones, D. E., and Petersen, C. A. (2010). Immunologic indicators of clinical progression during canine Leishmania infantum infection. Clinical Vaccine Immunology 17, 267–273.CrossRefGoogle ScholarPubMed
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dry binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle Scholar
Cabral, S. M., Silvestre, R. L., Santarem, N. M., Tavares, J. C., Silva, A. F. and Cordeiro-da-Silva, A. (2008). A Leishmania infantum cytosolic tryparedoxin activates B cells to secrete interleukin-10 and specific immunoglobulin. Immunology 123, 555–565.CrossRefGoogle ScholarPubMed
Chambers, H. F. (2001). Antimicrobial agents continued the aminoglycosides. In Goodman and Gilman's Pharmacological Basis of Therapeutics. 10th Edn. (ed. Hardman, J. G., Limbird, L. E.), pp. 1219–1238. McGraw-Hill, New York, NY, USA.Google Scholar
Chu, P. G. and Arber, D. A. (2001). CD79: a review. Applied Immunohistochemstry & Molecular Morphology 9, 97–106.CrossRefGoogle ScholarPubMed
Daneshvar, H., Coombs, G. H., Hagan, P. and Phillips, R. S. (2003). Leishmania mexicana and Leishmania major: attenuation of wild type parasites and vaccination with attenuated lines. Journal of Infectious Diseases 187, 1662–1668.CrossRefGoogle ScholarPubMed
Daneshvar, H., Molaei, M. M., Afshar, R. M., Kamiabi, H., Burchmore, R., Hagan, P. and Phillips, R. S. (2009). Gentamicin-attenuated Leishmania infantum: a clinicalpathological study in dogs. Veterinary Immunology and Immunopathology 129, 28–35.CrossRefGoogle Scholar
Daneshvar, H., Molaei, M. M., Kamiabi, H., Burchmore, R., Hagan, P. and Phillips, R. S. (2010). Gentamicin-attenuated Leishmania infantum: cellular immunity production and protection of dogs against experimental canine leishmaniasis. Parasite Immunology 32, 722–730.CrossRefGoogle ScholarPubMed
Daneshvar, H., Wyllie, S., Phillips, S. R., Hagan, P. and Burchmore, R. (2012). Comparative proteomics profiling of a gentamicin-attenuated Leishmania infantum cell line identifies key changes in parasite thiol-redox metabolism. Journal of Proteomics 75, 1463–1471.CrossRefGoogle ScholarPubMed
Day, M. J. (2008). Basic Immunology. In Clinical Immunology of the Dog and Cat, 2nd Edn. (ed. Day, M. J.), pp. 11–59. Manson Publishing Ltd, London, UK.CrossRefGoogle Scholar
Dumas, C., Ouellette, M., Tovar, J., Cunningham, M. L., Fairlamb, A. H., Tamar, S., Olivier, M. and Papadopoulou, B. (1997). Disruption of the trypanothione reductase gene of Leishmania decreases its ability to survive oxidative stress in macrophages. EMBO Journal 16, 2590–2598.CrossRefGoogle ScholarPubMed
Edson, R. S. and Terrell, C. L. (1999). The aminoglycosides. Mayo Clinic Proceedings 74, 519–528.CrossRefGoogle ScholarPubMed
Ensinger, E. M., Boekhoff, T. M. A., Carison, R., Beineke, A., Rohn, K., Tipoid, A. and Stein, V. M. (2010). Regional topographical differences of canine microglial immunophenotype and function in the healthy spinal cord. Journal of Neuroimmunology 227, 144–152.CrossRefGoogle ScholarPubMed
Felix De Lima, V. M., Ikeda, F. A., Rossi, C. N., Feitosa, M. M., Vasconcelos, R. O., Nunes, C. M. and Goto, H. (2010). Diminished CD4 + /CD25+ T cell and increased IFN-gamma levels occur in dogs vaccinated with Leishmune in an endemic area for visceral leishmaniasis. Veterinary Immunology and Immunopathology 135, 296–302.CrossRefGoogle Scholar
Ferrer, L., Rabanal, R., Fondevila, D., Ramos, J. A. and Domingo, M. (1988). Skin-lesions in canine leishmaniasis. Journal Small Animal Practice 29, 381–388.CrossRefGoogle Scholar
Giunchetti, R. C., Martins-Filho, O. A., Carneiro, C. M., Mayrink, W., Marques, M. J., Tafuri, W. L., Correa-Oliveira, R. and Reis, A. B. (2008 a). Histopathology, parasite density and cell phenotypes of the popliteal lymph node in canine visceral leishmaniasis. Veterinary Immunology and Immunopathology 121, 23–33.CrossRefGoogle ScholarPubMed
Giunchetti, R. C., Mayrink, W., Carneiro, C. M., Correa-Oliveira, R., Martins-Filho, O. A., Marques, M. J., Tafuri, W. L. and Reis, A. B. (2008 b). Histopathological and immunohistochemical investigations of the hepatic compartment associated with parasitism and serum biochemical changes in canine visceral leishmaniasis. Research in Veterinary Science 84, 269–277.CrossRefGoogle ScholarPubMed
Goyal, N., Roy, U. and Rastogi, A. K. (1996). Relative resistance of promastigotes of a virulent and an avirulent strain of Leishmania donovani to hydrogen peroxide. Free Radical Biology Medicine 21, 683–689.CrossRefGoogle Scholar
Guarga, J. L., Moreno, J, Lucientes, J, Gracia, M. J., Peribanez, M. A., Alvar, J, Castillo, J. A. (2000). Canine leishmaniasis transmission: higher infectivity amongst naturally infected dogs to sand flies is associated with lower proportions of T helper cells. Research Veterinary Science 69, 249–253.CrossRefGoogle ScholarPubMed
Kedzierski, L., Curtis, J. M. and Kedzierska, K. (2009). Early CD44(hi)CD4+ and CD44(hi)CD8+ T cell numbers and the absence of mannose-rich glycoconjugates determine the protective outcome of anti-leishmanial immunity. Parasitology 136, 833–840.CrossRefGoogle ScholarPubMed
Lima, W. G., Michalick, M. S. M., Melo, M. N., Tafuri, W. L. and Tafuri, Wg. L. (2004). Canine visceral leishmaniasis: a histopathological study of lymph nodes. Acta Tropica 92, 43–53.CrossRefGoogle ScholarPubMed
Mallinson, D. J. and Coombs, G. H. (1989). Biochemical characterisation of the metacyclic forms of Leishmania major and L. mexicana mexicana. Parasitology 98, 7–15.Google Scholar
Moreira, M. A. B., Luvizotto, M. C. R., Garcia, J. F., Corbett, C. E. P. and Laurenti, M. D. (2007). Comparison of parasitological, immunological and molecular methods for the diagnosis of leishmaniasis in dogs with different clinical signs. Veterinary Parasitology 145, 245–252.CrossRefGoogle ScholarPubMed
Murphy, E., Shibuya, K., Hosken, N., Openshaw, P., Maino, V., Davis, K., Murphy, K. and O'Garra, A. (1996). Reversibility of T helper 1 and 2 population is lost after-term stimulation. Journal of Experimental Medicine 183, 901–913.CrossRefGoogle Scholar
Palatnik-de-Sousa, C. B., dos Santos, W. R., Franca-Silva, J. C., da Costa, R. T., Reis, A. B., Palatnik, M., Mayrink, W. and Genaro, O. (2001). Impact of canine control on the epidemiology of canine and human visceral leishmaniasis in Brazil. American Journal of Tropical Medicne and Hygiene 65, 510–517.CrossRefGoogle ScholarPubMed
Papadogiannakis, E. I., Koutinas, A. F., Saridomichelakis, M. N., Vlemmas, J., Lekkas, S., Karameris, A. and Fytianou, A. (2005). Cellular immunophenotyping of exoliative dermatitis in canine leishmaniosis (Leishmania infantum). Veterinary Immunology and Immunpathology 104, 227–237.CrossRefGoogle ScholarPubMed
Pinelli, E. (1997). Cytokines in canine visceral leishmaniasis. In Cytokines in Veterinary Medicine (ed. Schijns, V. E. C. J. and Horzinek, M. C.), pp. 217–247. Utrecht University, Utrecht, The Netherlands.Google Scholar
Pinelli, E., Killick-Kendrick, R., Wagenaar, J., Bernadina, W., Del Real, G. and Ruitenberg, J. (1994). Cellular and humoral immune responses in dogs experimentally and naturally infected with Leishmania infantum. Infection and Immunity 62, 229–235.CrossRefGoogle ScholarPubMed
Reiner, N. E., Ng, W., Ma, T. and McMaster, W. R. (1988). Kinetics of gamma interferon binding and induction of major histocompatibility complex class II mRNA in Leishmania-infected macrophages. Proceedings of the National Academy of Sciences, USA 85, 4330–4334.CrossRefGoogle ScholarPubMed
Reis, A. B., Giunchetti, R. C., Carrillo, E., Martins-Filho, O. A. and Moreno, J. (2010). Immunity to Leishmania and the rational search for vaccines against canine leishmaniasis. Trends in Parasitology 26, 341–349.CrossRefGoogle ScholarPubMed
Reis, A. B., Martins-Filho, O. A., Teixeira-Carvalho, A., Carvalho, M. G., Mayrink, W., Franca-Silva, J. C., Giunchetti, R. C.Genaro, O. and Correa-Oliveira, R. (2006 b). Parasite density and impaired biochemical/hematological status are associated with severe clinical aspects of canine visceral leishmaniasis. Research in Veterinary Science 81, 68–75.CrossRefGoogle ScholarPubMed
Reis, A. B., Martins-Filho, O. A., Teixeira-Carvalho, A., Giunchetti, R. C., Carneiro, C. M., Mayrink, W., Tafuri, W. L. and Correa-Oliveira, R. (2009). Systemic and compartmentalized immune response in canine visceral leishmaniasis. Veterinary Immunology and Immunopathology 128, 87–95.CrossRefGoogle ScholarPubMed
Reis, A. B., Teixeira-Carvalho, A., Giunchetti, R. C., Guerra, l. L., Carvalho, M. G., Mayrink, W., Genaro, O., Correa-Oliveira, R. and Martins-Filho, O. A. (2006 a). Phenotypic features of circulating leucocytes as immunological markers for clinical status and bone marrow parasite density in dogs naturally infected by Leishmania chagasi. Clinical & Experimental Immunology 146, 303–311.CrossRefGoogle ScholarPubMed
Rodrigues, O. R., Marques, C., Soares-Clementea, M., Ferronha, M. H. and Santos-Gomes, G. M. (2009). Identification of regulatory T cells during experimental Leishmania infantum infection. Immunobiology 214, 101–111.CrossRefGoogle ScholarPubMed
Sanchez, M. A., Diaz, N. L., Zerpa, O., Negron, E., Convit, J. and Tapia, F. J. (2004). Organ-specific immunity in canine visceral leishmaniasis: analysis of symptomatic and asymptomatic dogs naturally infected with Lishmania chagasi. American Journal of Tropical Medicine and Hygiene 70, 618–624.CrossRefGoogle Scholar
Saridomichelakis, M. N. (2009). Advances in the pathogenesis of canine leishmaniosis: epidemiologic and diagnostic implications. Veterinary Dermatology 20, 471–489.CrossRefGoogle ScholarPubMed
Stern, J. J., Oca, M. J., Rubin, B. Y., Anderson, S. L. and Murray, H. W. (1988). Role of L3T4 and LyT-21 cells in experimental visceral leishmaniasis. Journal of Immunology 140, 3971–3927.CrossRefGoogle ScholarPubMed
Strauss-Ayali, D., Baneth, G., Shor, S., Okano, F. and Jaffe, C. L. (2005). Interleukin-12 augments a Th1-type immune response manifested as lymphocyte proliferation and interferon gamma production in Leishmania infantum-infected dogs. International Journal of Parasitology 35, 63–73.CrossRefGoogle ScholarPubMed
Surh, C. D. and Sprent, J. (2008). Homeostasis of naive and memory T cells. Immunity 29, 848–862.CrossRefGoogle ScholarPubMed
Tafuri, W. L., Rosa de Oliveira, M., Melo, M. N. and Tafuri, W. L. (2001). Canine visceral leishmaniosis: a remarkable histopathological picture of one case reported from Brazil. Veterinary Parasitology 96, 203–212.CrossRefGoogle ScholarPubMed
Tafuri, Wg. L., Santos, R. L., Arantes, R. M. E., Gonc-alves, R., Melo, M. N., Michalik, M. S. M. and Tafuri, W. L. (2004). An alternative immunohistochemical method for detecting Leishmania amastigotes in paraffin-embedded canine tissues. Journal of Immunological Methods 292, 17–23.CrossRefGoogle ScholarPubMed
Tekos, A., Tsagla, A., Stathopoulos, C. and Drainas, D. (2000). Inhibition of eukaryotic ribonuclease P activity by aminoglycosides: kinetic studies. FEBS Letters 485, 71–75.CrossRefGoogle ScholarPubMed
Walter, F., Vicens, Q. and Westhof, E. (1999). Aminoglycoside-RNA interactions. Current Opinion in Chemical Biology 3, 694–704.CrossRefGoogle ScholarPubMed
Weinstein, M. J., Luedemann, G. M., Oden, E. M., Wagman, G. H., Rosselet, J. P. and Marquez, J. A. (1963 a). Gentamicin, a new antibiotic complex from micromonospora. Journal of Medicinal Chemistry 6, 463–464.CrossRefGoogle ScholarPubMed
Weinstein, M. J., Luedemann, G. M., Odem, E. M. and Wagman, G. H. (1963 b). Gentamicin, a new broad-spectrum antibiotic complex. Antimicrobial Agents and Chemotherapy 161, 1–7.Google ScholarPubMed
Wilkerson, M. J., Dolce, K., Koopman, T., Shuman, W., Chun, R., Garrett, L., Barber, L. and Avery, A. (2005). Lineage differentiation of canine lymphoma/leukemias and aberrant expression of CD molecules. Veterinary Immunology and Immunopathology 106, 179–196.CrossRefGoogle ScholarPubMed
Wilson, M. E., Andersen, K. A. and Britigan, B. E. (1994). Response of Leishmania chagasi promastigotes to oxidant stress. Infection and Immunity 62, 5133–5141.CrossRefGoogle ScholarPubMed
Woodcock, J., Moazed, D., Cannon, M., Davies, J. and Noller, H. F. (1991). Interaction of antibiotics with A- and P-site-specific bases in 16S ribosomal RNA. EMBO Journal 10, 3099–3103.CrossRefGoogle ScholarPubMed
Xavier, S. C., de Andrade, H. M., Monte, S. J. H., Chiarelli, I. M., Lima, W. G., Michalick, M. S. M, Tafuri, W. L., Tafuri, Wg. L. (2006). Comparison of paraffin-embedded skin biopsies from different anatomical regions as sampling methods for detection of Leishmania infection in dogs using histological, immunohistochemical and PCR methods. BioMed Central Veterinary Research 2, 17. http://www.biomedcentral.com/1746-6148/2/17.Google ScholarPubMed
Yoshizawa, S., Fourmy, D. and Puglisi, J. D. (1998). Structural origins of gentamicin antibiotic action. EMBO Journal 17, 6437–6448.CrossRefGoogle ScholarPubMed