Skip to main content
Top
Published in: BMC Infectious Diseases 1/2012

Open Access 01-12-2012 | Research article

Macrophages participate in host protection and the disease pathology associated with Leishmania braziliensisinfection

Authors: Angela Giudice, Célia Vendrame, Caroline Bezerra, Lucas P Carvalho, Thaís Delavechia, Edgar M Carvalho, Olívia Bacellar

Published in: BMC Infectious Diseases | Issue 1/2012

Login to get access

Abstract

Background

Leishmania preferentially infects macrophages, which allow the parasite to multiply but can also kill the parasite. Although the T cell response in human leishmaniasis is well-characterized, little is known about the concomitant macrophage behavior. The aim of this study was to characterize the macrophage immune response after Leishmania braziliensis infection in cells derived from cutaneous leishmaniasis (CL) or mucosal leishmaniasis (ML) patients, subclinical individuals (SC) and healthy control subjects (HS).

Methods

Peripheral blood mononuclear cell-derived macrophages from the different groups were exposed to L. braziliensis in vitro and were evaluated for susceptibility to Leishmania infection, ability to kill Leishmania and chemokine/cytokine production. Nitric Oxide (NO) and superoxide (O2 -) levels in the supernatant of infected macrophage cultures were monitored.

Results

After exposure to L. braziliensis, peripheral blood mononuclear cell-derived macrophages from SC individuals showed a lower infection rate and a smaller number of intracellular amastigotes compared to cells from CL and ML patients. Macrophages from CL and ML patients produced more chemokines and TNF-α than those from the SC group. Production of NO and O2 - were detected but did not vary significantly among the different groups.

Conclusions

Our data indicate that macrophages play a pivotal role in controlling L. braziliensis infection and in leishmaniasis pathology by secreting pro-inflammatory chemokines/cytokines that activate and recruit T cells, overwhelming the inflammatory response.
Appendix
Available only for authorised users
Literature
1.
go back to reference Bittencourt AL, Barral A: Evaluation of the histopathological classifications of American cutaneous and mucocutaneous leishmaniasis. Mem Inst Oswaldo Cruz. 1991, 86 (1): 51-56. 10.1590/S0074-02761991000100009.CrossRefPubMed Bittencourt AL, Barral A: Evaluation of the histopathological classifications of American cutaneous and mucocutaneous leishmaniasis. Mem Inst Oswaldo Cruz. 1991, 86 (1): 51-56. 10.1590/S0074-02761991000100009.CrossRefPubMed
2.
go back to reference Marsden PD, Jones TC: Clinical manifestations, diagnosis and treatment of leishmaniasis. 1985, Amsterdam: Elsevier Science Publisher Marsden PD, Jones TC: Clinical manifestations, diagnosis and treatment of leishmaniasis. 1985, Amsterdam: Elsevier Science Publisher
3.
go back to reference Ben Salah A, Louzir H, Chlif S, Mokni M, Zaatour A, Raouene M, Ismail RB, Dellagi K: The predictive validity of naturally acquired delayed-type hypersensitivity to leishmanin in resistance to Leishmania major-associated cutaneous leishmaniasis. J Infect Dis. 2005, 192 (11): 1981-1987. 10.1086/498042.CrossRefPubMed Ben Salah A, Louzir H, Chlif S, Mokni M, Zaatour A, Raouene M, Ismail RB, Dellagi K: The predictive validity of naturally acquired delayed-type hypersensitivity to leishmanin in resistance to Leishmania major-associated cutaneous leishmaniasis. J Infect Dis. 2005, 192 (11): 1981-1987. 10.1086/498042.CrossRefPubMed
4.
go back to reference Bittar RC, Nogueira RS, Vieira-Goncalves R, Pinho-Ribeiro V, Mattos MS, Oliveira-Neto MP, Coutinho SG, Da-Cruz AM: T-cell responses associated with resistance to Leishmania infection in individuals from endemic areas for Leishmania (Viannia) braziliensis. Mem Inst Oswaldo Cruz. 2007, 102 (5): 625-630. 10.1590/S0074-02762007005000069.CrossRefPubMed Bittar RC, Nogueira RS, Vieira-Goncalves R, Pinho-Ribeiro V, Mattos MS, Oliveira-Neto MP, Coutinho SG, Da-Cruz AM: T-cell responses associated with resistance to Leishmania infection in individuals from endemic areas for Leishmania (Viannia) braziliensis. Mem Inst Oswaldo Cruz. 2007, 102 (5): 625-630. 10.1590/S0074-02762007005000069.CrossRefPubMed
5.
go back to reference Follador I, Araujo C, Orge G, Cheng LH, de Carvalho LP, Bacellar O, Almeida RP, Carvalho EM: Immune responses to an inactive vaccine against American cutaneous leishmaniasis together with granulocyte-macrophage colony-stimulating factor. Vaccine. 2002, 20 (9-10): 1365-1368. 10.1016/S0264-410X(01)00469-8.CrossRefPubMed Follador I, Araujo C, Orge G, Cheng LH, de Carvalho LP, Bacellar O, Almeida RP, Carvalho EM: Immune responses to an inactive vaccine against American cutaneous leishmaniasis together with granulocyte-macrophage colony-stimulating factor. Vaccine. 2002, 20 (9-10): 1365-1368. 10.1016/S0264-410X(01)00469-8.CrossRefPubMed
6.
go back to reference Trujillo CM, Robledo SM, Franco JL, Velez ID, Erb KJ, Patino PJ: Endemically exposed asymptomatic individuals show no increase in the specific Leishmania (Viannia) panamensis-Th1 immune response in comparison to patients with localized cutaneous leishmaniasis. Parasite Immunol. 2002, 24 (9-10): 455-462. 10.1046/j.1365-3024.2002.00488.x.CrossRefPubMed Trujillo CM, Robledo SM, Franco JL, Velez ID, Erb KJ, Patino PJ: Endemically exposed asymptomatic individuals show no increase in the specific Leishmania (Viannia) panamensis-Th1 immune response in comparison to patients with localized cutaneous leishmaniasis. Parasite Immunol. 2002, 24 (9-10): 455-462. 10.1046/j.1365-3024.2002.00488.x.CrossRefPubMed
7.
go back to reference Bacellar O, Lessa H, Schriefer A, Machado P, Ribeiro De Jesus A, Dutra WO, Gollob KJ, Carvalho EM: Up-regulation of Th1-type responses in mucosal leishmaniasis patients. Infect Immun. 2002, 70 (12): 6734-6740. 10.1128/IAI.70.12.6734-6740.2002.CrossRefPubMedPubMedCentral Bacellar O, Lessa H, Schriefer A, Machado P, Ribeiro De Jesus A, Dutra WO, Gollob KJ, Carvalho EM: Up-regulation of Th1-type responses in mucosal leishmaniasis patients. Infect Immun. 2002, 70 (12): 6734-6740. 10.1128/IAI.70.12.6734-6740.2002.CrossRefPubMedPubMedCentral
8.
go back to reference Carvalho LP, Passos S, Bacellar O, Lessa M, Almeida RP, Magalhaes A, Dutra WO, Gollob KJ, Machado P, de Jesus AR: Differential immune regulation of activated T cells between cutaneous and mucosal leishmaniasis as a model for pathogenesis. Parasite Immunol. 2007, 29 (5): 251-258. 10.1111/j.1365-3024.2007.00940.x.CrossRefPubMedPubMedCentral Carvalho LP, Passos S, Bacellar O, Lessa M, Almeida RP, Magalhaes A, Dutra WO, Gollob KJ, Machado P, de Jesus AR: Differential immune regulation of activated T cells between cutaneous and mucosal leishmaniasis as a model for pathogenesis. Parasite Immunol. 2007, 29 (5): 251-258. 10.1111/j.1365-3024.2007.00940.x.CrossRefPubMedPubMedCentral
9.
go back to reference Carvalho EM, Johnson WD, Barreto E, Marsden PD, Costa JL, Reed S, Rocha H: Cell mediated immunity in American cutaneous and mucosal leishmaniasis. J Immunol. 1985, 135 (6): 4144-4148.PubMed Carvalho EM, Johnson WD, Barreto E, Marsden PD, Costa JL, Reed S, Rocha H: Cell mediated immunity in American cutaneous and mucosal leishmaniasis. J Immunol. 1985, 135 (6): 4144-4148.PubMed
10.
go back to reference Follador I, Araujo C, Bacellar O, Araujo CB, Carvalho LP, Almeida RP, Carvalho EM: Epidemiologic and immunologic findings for the subclinical form of Leishmania braziliensis infection. Clin Infect Dis. 2002, 34 (11): E54-E58. 10.1086/340261.CrossRefPubMed Follador I, Araujo C, Bacellar O, Araujo CB, Carvalho LP, Almeida RP, Carvalho EM: Epidemiologic and immunologic findings for the subclinical form of Leishmania braziliensis infection. Clin Infect Dis. 2002, 34 (11): E54-E58. 10.1086/340261.CrossRefPubMed
11.
go back to reference Ritter U, Korner H: Divergent expression of inflammatory dermal chemokines in cutaneous leishmaniasis. Parasite Immunol. 2002, 24 (6): 295-301. 10.1046/j.1365-3024.2002.00467.x.CrossRefPubMed Ritter U, Korner H: Divergent expression of inflammatory dermal chemokines in cutaneous leishmaniasis. Parasite Immunol. 2002, 24 (6): 295-301. 10.1046/j.1365-3024.2002.00467.x.CrossRefPubMed
12.
go back to reference Brandonisio O, Panaro MA, Fumarola I, Sisto M, Leogrande D, Acquafredda A, Spinelli R, Mitolo V: Macrophage chemotactic protein-1 and macrophage inflammatory protein-1 alpha induce nitric oxide release and enhance parasite killing in Leishmania infantum-infected human macrophages. Clin Exp Med. 2002, 2 (3): 125-129. 10.1007/s102380200017.CrossRefPubMed Brandonisio O, Panaro MA, Fumarola I, Sisto M, Leogrande D, Acquafredda A, Spinelli R, Mitolo V: Macrophage chemotactic protein-1 and macrophage inflammatory protein-1 alpha induce nitric oxide release and enhance parasite killing in Leishmania infantum-infected human macrophages. Clin Exp Med. 2002, 2 (3): 125-129. 10.1007/s102380200017.CrossRefPubMed
13.
go back to reference Faria DR, Gollob KJ, Barbosa J, Schriefer A, Machado PR, Lessa H, Carvalho LP, Romano-Silva MA, de Jesus AR, Carvalho EM, et al: Decreased in situ expression of interleukin-10 receptor is correlated with the exacerbated inflammatory and cytotoxic responses observed in mucosal leishmaniasis. Infect Immun. 2005, 73 (12): 7853-7859. 10.1128/IAI.73.12.7853-7859.2005.CrossRefPubMedPubMedCentral Faria DR, Gollob KJ, Barbosa J, Schriefer A, Machado PR, Lessa H, Carvalho LP, Romano-Silva MA, de Jesus AR, Carvalho EM, et al: Decreased in situ expression of interleukin-10 receptor is correlated with the exacerbated inflammatory and cytotoxic responses observed in mucosal leishmaniasis. Infect Immun. 2005, 73 (12): 7853-7859. 10.1128/IAI.73.12.7853-7859.2005.CrossRefPubMedPubMedCentral
14.
go back to reference Assreuy J, Cunha FQ, Epperlein M, Noronha-Dutra A, O'Donnell CA, Liew FY, Moncada S: Production of nitric oxide and superoxide by activated macrophages and killing of Leishmania major. Eur J Immunol. 1994, 24 (3): 672-676. 10.1002/eji.1830240328.CrossRefPubMed Assreuy J, Cunha FQ, Epperlein M, Noronha-Dutra A, O'Donnell CA, Liew FY, Moncada S: Production of nitric oxide and superoxide by activated macrophages and killing of Leishmania major. Eur J Immunol. 1994, 24 (3): 672-676. 10.1002/eji.1830240328.CrossRefPubMed
15.
go back to reference Evans TG, Thai L, Granger DL, Hibbs JB: Effect of in vivo inhibition of nitric oxide production in murine leishmaniasis. J Immunol. 1993, 151 (2): 907-915.PubMed Evans TG, Thai L, Granger DL, Hibbs JB: Effect of in vivo inhibition of nitric oxide production in murine leishmaniasis. J Immunol. 1993, 151 (2): 907-915.PubMed
16.
go back to reference Murray HW, Teitelbaum RF: L-arginine-dependent reactive nitrogen intermediates and the antimicrobial effect of activated human mononuclear phagocytes. J Infect Dis. 1992, 165 (3): 513-517. 10.1093/infdis/165.3.513.CrossRefPubMed Murray HW, Teitelbaum RF: L-arginine-dependent reactive nitrogen intermediates and the antimicrobial effect of activated human mononuclear phagocytes. J Infect Dis. 1992, 165 (3): 513-517. 10.1093/infdis/165.3.513.CrossRefPubMed
17.
go back to reference Cupolillo E, Grimaldi G, Momen H: A general classification of New World Leishmania using numerical zymotaxonomy. Am J Trop Med Hyg. 1994, 50 (3): 296-311.PubMed Cupolillo E, Grimaldi G, Momen H: A general classification of New World Leishmania using numerical zymotaxonomy. Am J Trop Med Hyg. 1994, 50 (3): 296-311.PubMed
18.
go back to reference Reed SG, Badaro R, Masur H, Carvalho EM, Lorenco R, Lisboa A, Teixeira R, Johnson WD, Jones TC: Selection of a skin test antigen for American visceral leishmaniasis. Am J Trop Med Hyg. 1986, 35 (1): 79-85.PubMed Reed SG, Badaro R, Masur H, Carvalho EM, Lorenco R, Lisboa A, Teixeira R, Johnson WD, Jones TC: Selection of a skin test antigen for American visceral leishmaniasis. Am J Trop Med Hyg. 1986, 35 (1): 79-85.PubMed
19.
go back to reference Ding AH, Nathan CF: The measurement of cytochrome b559 in polymorphonuclear leukocytes and macrophages in the presence of hemoglobin or mitochondrial cytochromes. Anal Biochem. 1988, 175 (1): 22-29. 10.1016/0003-2697(88)90355-7.CrossRefPubMed Ding AH, Nathan CF: The measurement of cytochrome b559 in polymorphonuclear leukocytes and macrophages in the presence of hemoglobin or mitochondrial cytochromes. Anal Biochem. 1988, 175 (1): 22-29. 10.1016/0003-2697(88)90355-7.CrossRefPubMed
20.
go back to reference Elstner EF, Heupel A: Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem. 1976, 70 (2): 616-620. 10.1016/0003-2697(76)90488-7.CrossRefPubMed Elstner EF, Heupel A: Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem. 1976, 70 (2): 616-620. 10.1016/0003-2697(76)90488-7.CrossRefPubMed
21.
go back to reference Khouri R, Bafica A, Silva Mda P, Noronha A, Kolb JP, Wietzerbin J, Barral A, Barral-Netto M, Van Weyenbergh J: IFN-beta impairs superoxide-dependent parasite killing in human macrophages: evidence for a deleterious role of SOD1 in cutaneous leishmaniasis. J Immunol. 2009, 182 (4): 2525-2531. 10.4049/jimmunol.0802860.CrossRefPubMed Khouri R, Bafica A, Silva Mda P, Noronha A, Kolb JP, Wietzerbin J, Barral A, Barral-Netto M, Van Weyenbergh J: IFN-beta impairs superoxide-dependent parasite killing in human macrophages: evidence for a deleterious role of SOD1 in cutaneous leishmaniasis. J Immunol. 2009, 182 (4): 2525-2531. 10.4049/jimmunol.0802860.CrossRefPubMed
22.
go back to reference Ribeiro-de-Jesus A, Almeida RP, Lessa H, Bacellar O, Carvalho EM: Cytokine profile and pathology in human leishmaniasis. Braz J Med Biol Res. 1998, 31 (1): 143-148. 10.1590/S0100-879X1998000100020.CrossRefPubMed Ribeiro-de-Jesus A, Almeida RP, Lessa H, Bacellar O, Carvalho EM: Cytokine profile and pathology in human leishmaniasis. Braz J Med Biol Res. 1998, 31 (1): 143-148. 10.1590/S0100-879X1998000100020.CrossRefPubMed
23.
go back to reference Bosque F, Saravia NG, Valderrama L, Milon G: Distinct innate and acquired immune responses to Leishmania in putative susceptible and resistant human populations endemically exposed to L. (Viannia) panamensis infection. Scand J Immunol. 2000, 51 (5): 533-541. 10.1046/j.1365-3083.2000.00724.x.CrossRefPubMed Bosque F, Saravia NG, Valderrama L, Milon G: Distinct innate and acquired immune responses to Leishmania in putative susceptible and resistant human populations endemically exposed to L. (Viannia) panamensis infection. Scand J Immunol. 2000, 51 (5): 533-541. 10.1046/j.1365-3083.2000.00724.x.CrossRefPubMed
24.
go back to reference Liew FY, Cox FE: Nonspecific defence mechanism: the role of nitric oxide. Immunol Today. 1991, 12 (3): A17-A21. 10.1016/S0167-5699(05)80006-4.CrossRefPubMed Liew FY, Cox FE: Nonspecific defence mechanism: the role of nitric oxide. Immunol Today. 1991, 12 (3): A17-A21. 10.1016/S0167-5699(05)80006-4.CrossRefPubMed
25.
go back to reference Novais FO, Santiago RC, Bafica A, Khouri R, Afonso L, Borges VM, Brodskyn C, Barral-Netto M, Barral A, de Oliveira CI: Neutrophils and macrophages cooperate in host resistance against Leishmania braziliensis infection. J Immunol. 2009, 183 (12): 8088-8098. 10.4049/jimmunol.0803720.CrossRefPubMed Novais FO, Santiago RC, Bafica A, Khouri R, Afonso L, Borges VM, Brodskyn C, Barral-Netto M, Barral A, de Oliveira CI: Neutrophils and macrophages cooperate in host resistance against Leishmania braziliensis infection. J Immunol. 2009, 183 (12): 8088-8098. 10.4049/jimmunol.0803720.CrossRefPubMed
26.
go back to reference Giudice A, Camada I, Leopoldo PT, Pereira JM, Riley LW, Wilson ME, Ho JL, de Jesus AR, Carvalho EM, Almeida RP: Resistance of Leishmania (Leishmania) amazonensis and Leishmania (Viannia) braziliensis to nitric oxide correlates with disease severity in Tegumentary Leishmaniasis. BMC Infect Dis. 2007, 7: 7-10.1186/1471-2334-7-7.CrossRefPubMedPubMedCentral Giudice A, Camada I, Leopoldo PT, Pereira JM, Riley LW, Wilson ME, Ho JL, de Jesus AR, Carvalho EM, Almeida RP: Resistance of Leishmania (Leishmania) amazonensis and Leishmania (Viannia) braziliensis to nitric oxide correlates with disease severity in Tegumentary Leishmaniasis. BMC Infect Dis. 2007, 7: 7-10.1186/1471-2334-7-7.CrossRefPubMedPubMedCentral
27.
go back to reference Linares E, Augusto O, Barao SC, Giorgio S: Leishmania amazonensis infection does not inhibit systemic nitric oxide levels elicited by lipopolysaccharide in vivo. J Parasitol. 2000, 86 (1): 78-82.CrossRefPubMed Linares E, Augusto O, Barao SC, Giorgio S: Leishmania amazonensis infection does not inhibit systemic nitric oxide levels elicited by lipopolysaccharide in vivo. J Parasitol. 2000, 86 (1): 78-82.CrossRefPubMed
28.
go back to reference Van Assche T, Deschacht M, da Luz RA, Maes L, Cos P: Leishmania-macrophage interactions: insights into the redox biology. Free Radic Biol Med. 2011, 51 (2): 337-351. 10.1016/j.freeradbiomed.2011.05.011.CrossRefPubMed Van Assche T, Deschacht M, da Luz RA, Maes L, Cos P: Leishmania-macrophage interactions: insights into the redox biology. Free Radic Biol Med. 2011, 51 (2): 337-351. 10.1016/j.freeradbiomed.2011.05.011.CrossRefPubMed
29.
go back to reference Afonso L, Borges VM, Cruz H, Ribeiro-Gomes FL, DosReis GA, Dutra AN, Clarencio J, de Oliveira CI, Barral A, Barral-Netto M, et al: Interactions with apoptotic but not with necrotic neutrophils increase parasite burden in human macrophages infected with Leishmania amazonensis. J Leukoc Biol. 2008, 84 (2): 389-396. 10.1189/jlb.0108018.CrossRefPubMed Afonso L, Borges VM, Cruz H, Ribeiro-Gomes FL, DosReis GA, Dutra AN, Clarencio J, de Oliveira CI, Barral A, Barral-Netto M, et al: Interactions with apoptotic but not with necrotic neutrophils increase parasite burden in human macrophages infected with Leishmania amazonensis. J Leukoc Biol. 2008, 84 (2): 389-396. 10.1189/jlb.0108018.CrossRefPubMed
30.
go back to reference Campanelli AP, Brodskyn CI, Boaventura V, Silva C, Roselino AM, Costa J, Saldanha AC, de Freitas LA, de Oliveira CI, Barral-Netto M, et al: Chemokines and chemokine receptors coordinate the inflammatory immune response in human cutaneous leishmaniasis. Hum Immunol. 2010, 71 (12): 1220-1227. 10.1016/j.humimm.2010.09.002.CrossRefPubMed Campanelli AP, Brodskyn CI, Boaventura V, Silva C, Roselino AM, Costa J, Saldanha AC, de Freitas LA, de Oliveira CI, Barral-Netto M, et al: Chemokines and chemokine receptors coordinate the inflammatory immune response in human cutaneous leishmaniasis. Hum Immunol. 2010, 71 (12): 1220-1227. 10.1016/j.humimm.2010.09.002.CrossRefPubMed
31.
go back to reference Guerreiro JB, Santos SB, Morgan DJ, Porto AF, Muniz AL, Ho JL, Teixeira AL, Teixeira MM, Carvalho EM: Levels of serum chemokines discriminate clinical myelopathy associated with human T lymphotropic virus type 1 (HTLV-1)/tropical spastic paraparesis (HAM/TSP) disease from HTLV-1 carrier state. Clin Exp Immunol. 2006, 145 (2): 296-301. 10.1111/j.1365-2249.2006.03150.x.CrossRefPubMedPubMedCentral Guerreiro JB, Santos SB, Morgan DJ, Porto AF, Muniz AL, Ho JL, Teixeira AL, Teixeira MM, Carvalho EM: Levels of serum chemokines discriminate clinical myelopathy associated with human T lymphotropic virus type 1 (HTLV-1)/tropical spastic paraparesis (HAM/TSP) disease from HTLV-1 carrier state. Clin Exp Immunol. 2006, 145 (2): 296-301. 10.1111/j.1365-2249.2006.03150.x.CrossRefPubMedPubMedCentral
32.
go back to reference Trebst C, Ransohoff RM: Investigating chemokines and chemokine receptors in patients with multiple sclerosis: opportunities and challenges. Arch Neurol. 2001, 58 (12): 1975-1980. 10.1001/archneur.58.12.1975.CrossRefPubMed Trebst C, Ransohoff RM: Investigating chemokines and chemokine receptors in patients with multiple sclerosis: opportunities and challenges. Arch Neurol. 2001, 58 (12): 1975-1980. 10.1001/archneur.58.12.1975.CrossRefPubMed
33.
go back to reference Kanaly ST, Nashleanas M, Hondowicz B, Scott P: TNF receptor p55 is required for elimination of inflammatory cells following control of intracellular pathogens. J Immunol. 1999, 163 (7): 3883-3889.PubMed Kanaly ST, Nashleanas M, Hondowicz B, Scott P: TNF receptor p55 is required for elimination of inflammatory cells following control of intracellular pathogens. J Immunol. 1999, 163 (7): 3883-3889.PubMed
34.
go back to reference Pizzorni C, Secchi ME, Cutolo M: Leishmaniasis in rheumatoid arthritis. Reumatismo. 2007, 59 (3): 235-239.PubMed Pizzorni C, Secchi ME, Cutolo M: Leishmaniasis in rheumatoid arthritis. Reumatismo. 2007, 59 (3): 235-239.PubMed
35.
go back to reference Antonelli LR, Dutra WO, Almeida RP, Bacellar O, Carvalho EM, Gollob KJ: Activated inflammatory T cells correlate with lesion size in human cutaneous leishmaniasis. Immunol Lett. 2005, 101 (2): 226-230. 10.1016/j.imlet.2005.06.004.CrossRefPubMed Antonelli LR, Dutra WO, Almeida RP, Bacellar O, Carvalho EM, Gollob KJ: Activated inflammatory T cells correlate with lesion size in human cutaneous leishmaniasis. Immunol Lett. 2005, 101 (2): 226-230. 10.1016/j.imlet.2005.06.004.CrossRefPubMed
36.
go back to reference Da-Cruz AM, de Oliveira MP, De Luca PM, Mendonca SC, Coutinho SG: Tumor necrosis factor-alpha in human american tegumentary leishmaniasis. Mem Inst Oswaldo Cruz. 1996, 91 (2): 225-229. 10.1590/S0074-02761996000200019.CrossRefPubMed Da-Cruz AM, de Oliveira MP, De Luca PM, Mendonca SC, Coutinho SG: Tumor necrosis factor-alpha in human american tegumentary leishmaniasis. Mem Inst Oswaldo Cruz. 1996, 91 (2): 225-229. 10.1590/S0074-02761996000200019.CrossRefPubMed
37.
go back to reference Bafica A, Oliveira F, Freitas LA, Nascimento EG, Barral A: American cutaneous leishmaniasis unresponsive to antimonial drugs: successful treatment using combination of N-methilglucamine antimoniate plus pentoxifylline. Int J Dermatol. 2003, 42 (3): 203-207. 10.1046/j.1365-4362.2003.01868.x.CrossRefPubMed Bafica A, Oliveira F, Freitas LA, Nascimento EG, Barral A: American cutaneous leishmaniasis unresponsive to antimonial drugs: successful treatment using combination of N-methilglucamine antimoniate plus pentoxifylline. Int J Dermatol. 2003, 42 (3): 203-207. 10.1046/j.1365-4362.2003.01868.x.CrossRefPubMed
38.
go back to reference Machado PR, Lessa H, Lessa M, Guimaraes LH, Bang H, Ho JL, Carvalho EM: Oral pentoxifylline combined with pentavalent antimony: a randomized trial for mucosal leishmaniasis. Clin Infect Dis. 2007, 44 (6): 788-793. 10.1086/511643.CrossRefPubMed Machado PR, Lessa H, Lessa M, Guimaraes LH, Bang H, Ho JL, Carvalho EM: Oral pentoxifylline combined with pentavalent antimony: a randomized trial for mucosal leishmaniasis. Clin Infect Dis. 2007, 44 (6): 788-793. 10.1086/511643.CrossRefPubMed
39.
go back to reference Sadeghian G, Nilforoushzadeh MA: Effect of combination therapy with systemic glucantime and pentoxifylline in the treatment of cutaneous leishmaniasis. Int J Dermatol. 2006, 45 (7): 819-821. 10.1111/j.1365-4632.2006.02867.x.CrossRefPubMed Sadeghian G, Nilforoushzadeh MA: Effect of combination therapy with systemic glucantime and pentoxifylline in the treatment of cutaneous leishmaniasis. Int J Dermatol. 2006, 45 (7): 819-821. 10.1111/j.1365-4632.2006.02867.x.CrossRefPubMed
40.
go back to reference Ives A, Ronet C, Prevel F, Ruzzante G, Fuertes-Marraco S, Schutz F, Zangger H, Revaz-Breton M, Lye LF, Hickerson SM, et al: Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science. 2011, 331 (6018): 775-778. 10.1126/science.1199326.CrossRefPubMedPubMedCentral Ives A, Ronet C, Prevel F, Ruzzante G, Fuertes-Marraco S, Schutz F, Zangger H, Revaz-Breton M, Lye LF, Hickerson SM, et al: Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science. 2011, 331 (6018): 775-778. 10.1126/science.1199326.CrossRefPubMedPubMedCentral
41.
go back to reference Pirmez C, Yamamura M, Uyemura K, Paes-Oliveira M, Conceicao-Silva F, Modlin RL: Cytokine patterns in the pathogenesis of human leishmaniasis. J Clin Invest. 1993, 91 (4): 1390-1395. 10.1172/JCI116341.CrossRefPubMedPubMedCentral Pirmez C, Yamamura M, Uyemura K, Paes-Oliveira M, Conceicao-Silva F, Modlin RL: Cytokine patterns in the pathogenesis of human leishmaniasis. J Clin Invest. 1993, 91 (4): 1390-1395. 10.1172/JCI116341.CrossRefPubMedPubMedCentral
Metadata
Title
Macrophages participate in host protection and the disease pathology associated with Leishmania braziliensisinfection
Authors
Angela Giudice
Célia Vendrame
Caroline Bezerra
Lucas P Carvalho
Thaís Delavechia
Edgar M Carvalho
Olívia Bacellar
Publication date
01-12-2012
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2012
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-12-75

Other articles of this Issue 1/2012

BMC Infectious Diseases 1/2012 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.