Leukocyte Behavior in Mesenteric Microcirculation upon Experimental By Leishmania Spp. in BALB/c Mice
-
Herintha Coeto Neitzke-Abreu
,
Rhuan Carlos Souza Caetano
,
Kárin Rosi Reinhold-Castro
,
Manoel Sebastião da Costa Lima-Junior
,
Wagner José Tenório dos Santos
,
Gessilda de Alcantara Nogueira de Melo
,
Roberto Kenji Nakamura Cuman
,
Sandra Mara Alessi Aristides
,
Thais Gomes Verzignassi Silveira
,
Maria Valdrinez Campana Lonardoni
Abstract
Background: We aimed to determine the cellular recruitment (leukocyte rolling and adhesion) by which the Leishmania (Viannia) braziliensis, L. (Leishmania) amazonensis, and L. (Leishmania) major species in the mesenteric microcirculation of BALB/c mice.
Methods: Five experimental groups were considered: group 1 (L. braziliensis); group 2 (L. amazonensis); group 3 (L. major); group 4 (control group with PBS); group 5 (negative control group), analyzed 3, 6, 12, and 24 h after parasite inoculation.
Results: Infections by the different Leishmania species caused an increase in the number of rolling leukocytes: L. braziliensis a peak at 6 h; L. amazonensis and L. major a peak at 3 h. The Leishmania infections induced leukocyte adhesion: L. major and L. amazonensis showed an increase after 3 and 6 h, respectively.
Conclusion: The kinetics of cellular recruitment in Leishmania infections, leading to infection susceptibility or resistance, indicates that distinct mechanisms regulate the initial response to Leishmania infection and determine its course.
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2. Brazil, Ministry of Health. Manual de Vigilância da Leishmaniose Tegumentar. 2017. http://bvsms.saude.gov.br/bvs/publicacoes/manual_vigilancia_leishmaniose_tegumentar.pdf, Accessed date: 6 February 2020.
3. Bañuls AL, Bastien P, Pomares C, et al. Clinical pleiomorphism in human leish-maniases, with special mention of asymp-tomatic infection. Clin Microbiol Infect. 2011;17:1451-61.
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5. Müller AJ, Filipe-Santos O, Eberl G, et al. CD4+ T cells rely on a cytokine gradient to control intracellular pathogens beyond sites of antigen presentation. Immunity. 2012;37:147-57.
6. Charmoy M, Megnekou R, Allenbach C, et al. Leishmania major induces distinct neutro-phil phenotypes in mice that are resistant or susceptible to infection. J Leukoc Biol. 2007;82:288-99.
7. Teixeira CR, Teixeira MJ, Gomes RB, et al. Saliva from Lutzomyia longipalpis induces CC chemokine ligand 2/monocyte chemoat-tractant protein-1 expression and macro-phage recruitment. J Immunol. 2005;175:8346-53.
8. Baez S. A method for in-line measurement of lumen and wall of microscopic vessels in vivo. Microvasc Res. 1973;5:299-308.
9. Fortes ZB, Farsky SP, Oliveira MA, et al. Direct vital microscopic study of defective leukocyte-endothelial interaction in diabe-tes mellitus. Diabetes. 1991;40:1267-73.
10. León B, Lopez-Bravo M, Ardavin C. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania (see comment). Immunity. 2007;26:519-31.
11. Matte C, Olivier M. Leishmania - induced cellular recruitment during the early in-flammatory response: modulation of pro-inflammatory mediators. J Infect Dis. 2002;185:673-81.
12. León B, Ardavín C. Monocyte migration to inflamed skin and lymphonodes is dif-ferentially controlled by L-selectin and PSGL-1. Blood. 2008;111:3126-30.
13. Müller K, van Zandbergen G, Hansen B, et al. Chemokines, natural killer cells and granulocytes in the early course of Leishma-nia major infection in mice. Med Microbiol Immunol. 2001;190:73-6.
14. Ribeiro-Gomes FL, Roma EH, Carneiro MB. Site-dependent recruitment of in-flammatory cells determines the effective dose of Leishmania major. Infect Immun. 2014;82:2713-27.
15. Tacchini-Cottier F, Zweifel C, Belkaid Y, et al. An immunomodulatory function for neutrophilis during the induction of a CD4+ Th2 response in BALB/c mice in-fected with Leishmania major. J Immunol. 2000;165:2628-36.
16. Awasthi A, Mathur R, Saha B. Immune response to Leishmania infection. Indian J Med Res. 2004;119:238-58.
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18. Chen L, Zhang Z-H, Watanabe T, et al. The involvement of neutrophils in the re-sistance to Leishmania major infection in susceptible but not in resistant mice. Para-sitol Int. 2005;54:109-18.
19. Wakimoto DT, Gaspareto KV, Silveira TGV, et al. Cell migration induced by Leishmania (Leishmania) amazonensis, Leishma-nia (Leishmania) major and Leishmania (Vian-nia) braziliensis into the peritoneal cavity of BALB/c mice. J Venom Anim Toxins Incl Trop Dis. 2010;16:170-7.
20. Thalhofer CJ, Chen Y, Sudan B, et al. Leukocytes infiltrate the skin and draining lymph nodes in response to the protozo-an Leishmania infantum chagasi. Infect Immun. 2011;79:108-17.
21. Mendes-Aguiar C, Gomes-Silva A, Nunes E, et al. The skin homing receptor cutane-ous leucocyte-associated antigen (CLA) is up-regulated by Leishmania antigens in T lymphocytes during active cutaneous leishmaniasis. Clin Exp Immunol. 2009;157:377-84.
22. Sundd P, Gutierrez E, Pospieszalska MK, et al. Quantitative dynamic footprinting microscopy reveals mechanisms of neu-trophil rolling. Nat Methods. 2010;7:821-24.
23. Pereira MA, Alexandre-Pires G, Câmara M, et al. Canine neutrophils cooperate with macrophages in the early stages of Leish-mania infantum in vitro infection. Parasite Immunol. 2019;8:e12617.
24. Aga E, Katschinski DM, Zandbergen GV, et al. Inhibition of the spontaneous apop-tosis of neutrophil granulocytes by the in-tracellular parasite Leishmania major. J Im-munol. 2002;169:898-905.
25. Aebischer T, Moody SF, Handman E. Persistence of virulent Leishmania major in murine cutaneous leishmaniasis: a possible hazard for the host. Infect Immun. 1993;61:220-6.
26. Alves-Filho JC, de Freitas A, Spiller F, et al. The role of neutrophils in severe sepsis. Shock. 2008;30:3-9.
27. Charmoy M, Auderset F, Allenbach C, et al. The prominent role of neutrophils dur-ing the initial phase of infection by Leish-mania parasites. J Biomed Biotechnol. 2010;10:ID719361.
28. Hurrell BP, Regli IB, Tacchini-Cottier F. Different Leishmania species drive distinct neutrophil functions. Trends Parasitol. 2016;32:392-401.
29. Souza Carmo EV, Katz S, Barbieri CL. Neutrophils reduce the parasite burden in Leishmania (Leishmania) amazonensis-infected macrophages. PLoS One. 2010;5:e13815.
30. Novais FO, Santiago RC, Bafica A, et al. Neutrophils and macrophages cooperate in host resistance against Leishmania braziliensis infection. J Immunol. 2009;183:8088-98.
31. Terui T, Ozawa M, Tagami H. Role of neutrophils in induction of acute inflam-mation in T-cell-mediated immune derma-tosis, psoriasis: a neutrophil-associated in-flammation-boosting loop. Exp Dermatol. 2000;9:1-10.
32. Hodgkinson JW, Fibke C, Belosevic M. Recombinant IL-4/13A and IL-4/13B in-duce arginase activity and down-regulate nitric oxide response of primary goldfish (Carassius auratus L.) macrophages. Dev Comp Immunol. 2017;67:377-84.
33. Okabe Y, Medzhitov R. Tissue biology perspective on macrophages. Nat Immu-nol. 2016;17:9-17.
2. Brazil, Ministry of Health. Manual de Vigilância da Leishmaniose Tegumentar. 2017. http://bvsms.saude.gov.br/bvs/publicacoes/manual_vigilancia_leishmaniose_tegumentar.pdf, Accessed date: 6 February 2020.
3. Bañuls AL, Bastien P, Pomares C, et al. Clinical pleiomorphism in human leish-maniases, with special mention of asymp-tomatic infection. Clin Microbiol Infect. 2011;17:1451-61.
4. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140:805-20.
5. Müller AJ, Filipe-Santos O, Eberl G, et al. CD4+ T cells rely on a cytokine gradient to control intracellular pathogens beyond sites of antigen presentation. Immunity. 2012;37:147-57.
6. Charmoy M, Megnekou R, Allenbach C, et al. Leishmania major induces distinct neutro-phil phenotypes in mice that are resistant or susceptible to infection. J Leukoc Biol. 2007;82:288-99.
7. Teixeira CR, Teixeira MJ, Gomes RB, et al. Saliva from Lutzomyia longipalpis induces CC chemokine ligand 2/monocyte chemoat-tractant protein-1 expression and macro-phage recruitment. J Immunol. 2005;175:8346-53.
8. Baez S. A method for in-line measurement of lumen and wall of microscopic vessels in vivo. Microvasc Res. 1973;5:299-308.
9. Fortes ZB, Farsky SP, Oliveira MA, et al. Direct vital microscopic study of defective leukocyte-endothelial interaction in diabe-tes mellitus. Diabetes. 1991;40:1267-73.
10. León B, Lopez-Bravo M, Ardavin C. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania (see comment). Immunity. 2007;26:519-31.
11. Matte C, Olivier M. Leishmania - induced cellular recruitment during the early in-flammatory response: modulation of pro-inflammatory mediators. J Infect Dis. 2002;185:673-81.
12. León B, Ardavín C. Monocyte migration to inflamed skin and lymphonodes is dif-ferentially controlled by L-selectin and PSGL-1. Blood. 2008;111:3126-30.
13. Müller K, van Zandbergen G, Hansen B, et al. Chemokines, natural killer cells and granulocytes in the early course of Leishma-nia major infection in mice. Med Microbiol Immunol. 2001;190:73-6.
14. Ribeiro-Gomes FL, Roma EH, Carneiro MB. Site-dependent recruitment of in-flammatory cells determines the effective dose of Leishmania major. Infect Immun. 2014;82:2713-27.
15. Tacchini-Cottier F, Zweifel C, Belkaid Y, et al. An immunomodulatory function for neutrophilis during the induction of a CD4+ Th2 response in BALB/c mice in-fected with Leishmania major. J Immunol. 2000;165:2628-36.
16. Awasthi A, Mathur R, Saha B. Immune response to Leishmania infection. Indian J Med Res. 2004;119:238-58.
17. Reis LC, Brito MEF, Souza MA, et al. Mecanismos imunológicos na resposta celular e humoral na leishmaniose tegumentar americana. Rev Patol Trop. 2006;35:103-15.
18. Chen L, Zhang Z-H, Watanabe T, et al. The involvement of neutrophils in the re-sistance to Leishmania major infection in susceptible but not in resistant mice. Para-sitol Int. 2005;54:109-18.
19. Wakimoto DT, Gaspareto KV, Silveira TGV, et al. Cell migration induced by Leishmania (Leishmania) amazonensis, Leishma-nia (Leishmania) major and Leishmania (Vian-nia) braziliensis into the peritoneal cavity of BALB/c mice. J Venom Anim Toxins Incl Trop Dis. 2010;16:170-7.
20. Thalhofer CJ, Chen Y, Sudan B, et al. Leukocytes infiltrate the skin and draining lymph nodes in response to the protozo-an Leishmania infantum chagasi. Infect Immun. 2011;79:108-17.
21. Mendes-Aguiar C, Gomes-Silva A, Nunes E, et al. The skin homing receptor cutane-ous leucocyte-associated antigen (CLA) is up-regulated by Leishmania antigens in T lymphocytes during active cutaneous leishmaniasis. Clin Exp Immunol. 2009;157:377-84.
22. Sundd P, Gutierrez E, Pospieszalska MK, et al. Quantitative dynamic footprinting microscopy reveals mechanisms of neu-trophil rolling. Nat Methods. 2010;7:821-24.
23. Pereira MA, Alexandre-Pires G, Câmara M, et al. Canine neutrophils cooperate with macrophages in the early stages of Leish-mania infantum in vitro infection. Parasite Immunol. 2019;8:e12617.
24. Aga E, Katschinski DM, Zandbergen GV, et al. Inhibition of the spontaneous apop-tosis of neutrophil granulocytes by the in-tracellular parasite Leishmania major. J Im-munol. 2002;169:898-905.
25. Aebischer T, Moody SF, Handman E. Persistence of virulent Leishmania major in murine cutaneous leishmaniasis: a possible hazard for the host. Infect Immun. 1993;61:220-6.
26. Alves-Filho JC, de Freitas A, Spiller F, et al. The role of neutrophils in severe sepsis. Shock. 2008;30:3-9.
27. Charmoy M, Auderset F, Allenbach C, et al. The prominent role of neutrophils dur-ing the initial phase of infection by Leish-mania parasites. J Biomed Biotechnol. 2010;10:ID719361.
28. Hurrell BP, Regli IB, Tacchini-Cottier F. Different Leishmania species drive distinct neutrophil functions. Trends Parasitol. 2016;32:392-401.
29. Souza Carmo EV, Katz S, Barbieri CL. Neutrophils reduce the parasite burden in Leishmania (Leishmania) amazonensis-infected macrophages. PLoS One. 2010;5:e13815.
30. Novais FO, Santiago RC, Bafica A, et al. Neutrophils and macrophages cooperate in host resistance against Leishmania braziliensis infection. J Immunol. 2009;183:8088-98.
31. Terui T, Ozawa M, Tagami H. Role of neutrophils in induction of acute inflam-mation in T-cell-mediated immune derma-tosis, psoriasis: a neutrophil-associated in-flammation-boosting loop. Exp Dermatol. 2000;9:1-10.
32. Hodgkinson JW, Fibke C, Belosevic M. Recombinant IL-4/13A and IL-4/13B in-duce arginase activity and down-regulate nitric oxide response of primary goldfish (Carassius auratus L.) macrophages. Dev Comp Immunol. 2017;67:377-84.
33. Okabe Y, Medzhitov R. Tissue biology perspective on macrophages. Nat Immu-nol. 2016;17:9-17.
| Files | ||
| Issue | Vol 16 No 4 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v16i4.7869 | |
| Keywords | ||
| Leishmania Rolling Cellular adhesion Leukocyte | ||
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How to Cite
1.
Neitzke-Abreu H, Caetano R, Reinhold-Castro K, Lima-Junior MS, Santos W, de Melo G, Cuman R, Aristides S, Silveira T, Lonardoni M. Leukocyte Behavior in Mesenteric Microcirculation upon Experimental By Leishmania Spp. in BALB/c Mice. Iran J Parasitol. 2021;16(4):567-575.
