B-1 cells modulate the murine macrophage response to Leishmania major infection
|
摘要
AIM To investigate the modulatory effect of B-1 cells on murine peritoneal macrophages infected with Leishmania major(L. major) in vitro.METHODS Peritoneal macrophages obtained from BALB/c andBALB/c XID mice were infected with L. major and cultured in the presence or absence of B-1 cells obtained from wild-type BALB/c mice. Intracellular amastigotes were counted, and interleukin-10(IL-10) production was quantified in the cellular supernatants using an enzymelinked immunosorbent assay. The levels of the lipid mediator prostaglandin E2(PGE2) were determined using a PGE2 enzyme immunoassay kit(Cayman Chemical, Ann Arbor, MI), and the number of lipid bodies was quantified in the cytoplasm of infected macrophages in the presence and absence of B-1 cells. Culturing the cells with selective PGE2-neutralizing drugs inhibited PGE2 production and confirmed the role of this lipid mediator in IL-10 production. In contrast, we demonstrated that B-1 cells derived from IL-10 KO mice did not favor the intracellular growth of L. major.RESULTS We report that B-1 cells promote the growth of L. major amastigotes inside peritoneal murine macrophages. We demonstrated that the modulatory effect was independent of physical contact between the cells, suggesting that soluble factor(s) were released into the cultures. We demonstrated in our co-culture system that B-1 cells trigger IL-10 production by L. major-infected macrophages. Furthermore, the increased secretion of IL-10 was attributed to the presence of the lipid mediator PGE2 in supernatants of L. major-infected macrophages. The presence of B-1 cells also favors the production of lipid bodies by infected macrophages. In contrast, we failed to obtain the same effect on parasite replication inside L. major-infected macrophages when the B-1 cells were isolated from IL-10 knockout mice. CONCLUSION Our results show that elevated levels of PGE2 and IL-10 produced by B-1 cells increase L. major growth, as indicated by the number of parasites in cell cultures.
AIM To investigate the modulatory effect of B-1 cells on murine peritoneal macrophages infected with Leishmania major(L. major) in vitro.METHODS Peritoneal macrophages obtained from BALB/c andBALB/c XID mice were infected with L. major and cultured in the presence or absence of B-1 cells obtained from wild-type BALB/c mice. Intracellular amastigotes were counted, and interleukin-10(IL-10) production was quantified in the cellular supernatants using an enzymelinked immunosorbent assay. The levels of the lipid mediator prostaglandin E2(PGE2) were determined using a PGE2 enzyme immunoassay kit(Cayman Chemical, Ann Arbor, MI), and the number of lipid bodies was quantified in the cytoplasm of infected macrophages in the presence and absence of B-1 cells. Culturing the cells with selective PGE2-neutralizing drugs inhibited PGE2 production and confirmed the role of this lipid mediator in IL-10 production. In contrast, we demonstrated that B-1 cells derived from IL-10 KO mice did not favor the intracellular growth of L. major.RESULTS We report that B-1 cells promote the growth of L. major amastigotes inside peritoneal murine macrophages. We demonstrated that the modulatory effect was independent of physical contact between the cells, suggesting that soluble factor(s) were released into the cultures. We demonstrated in our co-culture system that B-1 cells trigger IL-10 production by L. major-infected macrophages. Furthermore, the increased secretion of IL-10 was attributed to the presence of the lipid mediator PGE2 in supernatants of L. major-infected macrophages. The presence of B-1 cells also favors the production of lipid bodies by infected macrophages. In contrast, we failed to obtain the same effect on parasite replication inside L. major-infected macrophages when the B-1 cells were isolated from IL-10 knockout mice. CONCLUSION Our results show that elevated levels of PGE2 and IL-10 produced by B-1 cells increase L. major growth, as indicated by the number of parasites in cell cultures.
AIM To investigate the modulatory effect of B-1 cells on murine peritoneal macrophages infected with Leishmania major(L. major) in vitro.METHODS Peritoneal macrophages obtained from BALB/c andBALB/c XID mice were infected with L. major and cultured in the presence or absence of B-1 cells obtained from wild-type BALB/c mice. Intracellular amastigotes were counted, and interleukin-10(IL-10) production was quantified in the cellular supernatants using an enzymelinked immunosorbent assay. The levels of the lipid mediator prostaglandin E2(PGE2) were determined using a PGE2 enzyme immunoassay kit(Cayman Chemical, Ann Arbor, MI), and the number of lipid bodies was quantified in the cytoplasm of infected macrophages in the presence and absence of B-1 cells. Culturing the cells with selective PGE2-neutralizing drugs inhibited PGE2 production and confirmed the role of this lipid mediator in IL-10 production. In contrast, we demonstrated that B-1 cells derived from IL-10 KO mice did not favor the intracellular growth of L. major.RESULTS We report that B-1 cells promote the growth of L. major amastigotes inside peritoneal murine macrophages. We demonstrated that the modulatory effect was independent of physical contact between the cells, suggesting that soluble factor(s) were released into the cultures. We demonstrated in our co-culture system that B-1 cells trigger IL-10 production by L. major-infected macrophages. Furthermore, the increased secretion of IL-10 was attributed to the presence of the lipid mediator PGE2 in supernatants of L. major-infected macrophages. The presence of B-1 cells also favors the production of lipid bodies by infected macrophages. In contrast, we failed to obtain the same effect on parasite replication inside L. major-infected macrophages when the B-1 cells were isolated from IL-10 knockout mice. CONCLUSION Our results show that elevated levels of PGE2 and IL-10 produced by B-1 cells increase L. major growth, as indicated by the number of parasites in cell cultures.
引文
1 Abrah?o TB,Freymüller E,Mortara RA,Lopes JD,Mariano M.Morphological characterization of mouse B-1 cells.Immunobiology2003;208:401-411[PMID:14748513 DOI:10.1078/0171-2985-00287]
2 Lopes JD,Mariano M.B-1 cell:the precursor of a novel mononuclear phagocyte with immuno-regulatory properties.An Acad Bras Cienc 2009;81:489-496[PMID:19722018 DOI:10.1590/s0001-37652009000300013]
3 Hardy RR.B-1 B cell development.J Immunol 2006;177:2749-2754[PMID:16920907 DOI:10.4049/jimmunol.177.5.2749]
4 Hayakawa K,Hardy RR,Parks DR,Herzenberg LA.The“Ly-1B”cell subpopulation in normal immunodefective,and autoimmune mice.J Exp Med 1983;157:202-218[PMID:6600267 DOI:10.1084/jem.157.1.202]
5 Boumsell L,Bernard A,Lepage V,Degos L,Lemerle J,Dausset J.Some chronic lymphocytic leukemia cells bearing surface immunoglobulins share determinants with T cells.Eur J Immunol1978;8:900-904[PMID:83236 DOI:10.1002/eji.1830081214]
6 Casali P,Burastero SE,Nakamura M,Inghirami G,Notkins AL.Human lymphocytes making rheumatoid factor and antibody to ss DNA belong to Leu-1+B-cell subset.Science 1987;236:77-81[PMID:3105056 DOI:10.1126/science.3105056]
7 Popi AF,Motta FL,Mortara RA,Schenkman S,Lopes JD,Mariano M.Co-ordinated expression of lymphoid and myeloid specific transcription factors during B-1b cell differentiation into mononuclear phagocytes in vitro.Immunology 2009;126:114-122[PMID:18710404 DOI:10.1111/j.1365-2567.2008.02883.x]
8 Almeida SR,Aroeira LS,Frymuller E,Dias MA,Bogsan CS,Lopes JD,Mariano M.Mouse B-1 cell-derived mononuclear phagocyte,a novel cellular component of acute non-specific inflammatory exudate.Int Immunol 2001;13:1193-1201[PMID:11526100 DOI:10.1093/intimm/13.9.1193]
9 Barbeiro DF,Barbeiro HV,Faintuch J,Ariga SK,Mariano M,Popi AF,de Souza HP,Velasco IT,Soriano FG.B-1 cells temper endotoxemic inflammatory responses.Immunobiology 2011;216:302-308[PMID:20817308 DOI:10.1016/j.imbio.2010.08.002]
10 Popi AF,Osugui L,Perez KR,Longo-Maugéri IM,Mariano M.Could a B-1 cell derived phagocyte“be one”of the peritoneal macrophages during LPS-driven inflammation?PLo S One 2012;7:e34570[PMID:22479646 DOI:10.1371/journal.pone.0034570]
11 Borrello MA,Phipps RP.Fibroblast-secreted macrophage colonystimulating factor is responsible for generation of biphenotypic B/macrophage cells from a subset of mouse B lymphocytes.J Immunol1999;163:3605-3611[PMID:10490953]
12 Cunningham AC.Parasitic adaptive mechanisms in infection by leishmania.Exp Mol Pathol 2002;72:132-141[PMID:11890722DOI:10.1006/exmp.2002.2418]
13 Arcanjo AF,La Rocque-de-Freitas IF,Rocha JD,Zamith D,Costada-Silva AC,Nunes MP,Mesquita-Santos FP,Morrot A,Filardy AA,Mariano M,Bandeira-Melo C,Dos Reis GA,Decote-Ricardo D,Freire-de-Lima CG.The PGE2/IL-10 Axis Determines Susceptibility of B-1 Cell-Derived Phagocytes(B-1CDP)to Leishmania major Infection.PLo S One 2015;10:e0124888[PMID:25933287 DOI:10.1371/journal.pone.0124888]
14 Filardy AA,Pires DR,Nunes MP,Takiya CM,Freire-de-Lima CG,Ribeiro-Gomes FL,Dos Reis GA.Proinflammatory clearance of apoptotic neutrophils induces an IL-12(low)IL-10(high)regulatory phenotype in macrophages.J Immunol 2010;185:2044-2050[PMID:20660352 DOI:10.4049/jimmunol.1000017]
15 Liese J,Schleicher U,Bogdan C.The innate immune response against Leishmania parasites.Immunobiology 2008;213:377-387[PMID:18406382 DOI:10.1016/j.imbio.2008.02.001]
16 Graf BA,Nazarenko DA,Borrello MA,Roberts LJ,Morrow JD,Palis J,Phipps RP.Biphenotypic B/macrophage cells express COX-1and up-regulate COX-2 expression and prostaglandin E(2)production in response to pro-inflammatory signals.Eur J Immunol 1999;29:3793-3803[PMID:10556836 DOI:10.1002/(SICI)1521-4141(199911)29:11<3793::AID-IMMU3793>3.0.CO;2-3]
17 Pinheiro RO,Nunes MP,Pinheiro CS,D’Avila H,Bozza PT,Takiya CM,C?rte-Real S,Freire-de-Lima CG,Dos Reis GA.Induction of autophagy correlates with increased parasite load of Leishmania amazonensis in BALB/c but not C57BL/6 macrophages.Microbes Infect 2009;11:181-190[PMID:19070676 DOI:10.1016/j.micinf.2008.11.006]
18 Ribeiro-Gomes FL,Otero AC,Gomes NA,Moniz-De-Souza MC,Cysne-Finkelstein L,Arnholdt AC,Calich VL,Coutinho SG,Lopes MF,Dos Reis GA.Macrophage interactions with neutrophils regulate Leishmania major infection.J Immunol 2004;172:4454-4462[PMID:15034061 DOI:10.4049/jimmunol.172.7.4454]
19 Freire-de-Lima CG,Nascimento DO,Soares MB,Bozza PT,CastroFaria-Neto HC,de Mello FG,Dos Reis GA,Lopes MF.Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages.Nature 2000;403:199-203[PMID:10646605 DOI:10.1038/35003208]
20 Luna-Gomes T,Filardy AA,Rocha JD,Decote-Ricardo D,La Rocque-de-Freitas IF,Morrot A,Bozza PT,Castro-Faria-Neto HC,Dos Reis GA,Nunes MP,Freire-de-Lima CG.Neutrophils increase or reduce parasite burden in Trypanosoma cruzi-infected macrophages,depending on host strain:role of neutrophil elastase.PLo S One 2014;9:e90582[PMID:24599360 DOI:10.1371/journal.pone.0090582]
21 Lopes MF,Freire-de-Lima CG,Dos Reis GA.The macrophage haunted by cell ghosts:a pathogen grows.Immunol Today 2000;21:489-494[PMID:11071527 DOI:10.1016/S0167-5699(00)01713-8]
22 Popi AF,Lopes JD,Mariano M.Interleukin-10 secreted by B-1 cells modulates the phagocytic activity of murine macrophages in vitro.Immunology 2004;113:348-354[PMID:15500621 DOI:10.1111/j.1365-2567.2004.01969.x]
23 Geraldo MM,Costa CR,Barbosa FM,Vivanco BC,Gonzaga WF,Novaes E Brito RR,Popi AF,Lopes JD,Xander P.In vivo and in vitro phagocytosis of Leishmania(Leishmania)amazonensis promastigotes by B-1 cells.Parasite Immunol 2016;38:365-376[PMID:27084328DOI:10.1111/pim.12324]
24 Bozza PT,Bakker-Abreu I,Navarro-Xavier RA,Bandeira-Melo C.Lipid body function in eicosanoid synthesis:an update.Prostaglandins Leukot Essent Fatty Acids 2011;85:205-213[PMID:21565480 DOI:10.1016/j.plefa.2011.04.020]
25 Toledo DA,Roque NR,Teixeira L,Milán-Garcés EA,Carneiro AB,Almeida MR,Andrade GF,Martins JS,Pinho RR,Freire-de-Lima CG,Bozza PT,D’Avila H,Melo RC.Lipid Body Organelles within the Parasite Trypanosoma cruzi:A Role for Intracellular Arachidonic Acid Metabolism.PLo S One 2016;11:e0160433[PMID:27490663DOI:10.1371/journal.pone.0160433]
26 D’Avila H,Freire-de-Lima CG,Roque NR,Teixeira L,Barja-Fidalgo C,Silva AR,Melo RC,Dosreis GA,Castro-Faria-Neto HC,Bozza PT.Host cell lipid bodies triggered by Trypanosoma cruzi infection and enhanced by the uptake of apoptotic cells are associated with prostaglandin E?generation and increased parasite growth.J Infect Dis 2011;204:951-961[PMID:21849292 DOI:10.1093/infdis/jir432]
27 Araújo-Santos T,Prates DB,Andrade BB,Nascimento DO,Clarêncio J,Entringer PF,Carneiro AB,Silva-Neto MA,Miranda JC,Brodskyn CI,Barral A,Bozza PT,Borges VM.Lutzomyia longipalpis saliva triggers lipid body formation and prostaglandin E?production in murine macrophages.PLo S Negl Trop Dis 2010;4:e873[PMID:21072234 DOI:10.1371/journal.pntd.0000873]
28 Oliveira HC,Popi AF,Bachi AL,Nonogaki S,Lopes JD,Mariano M.B-1 cells modulate the kinetics of wound-healing process in mice.Immunobiology 2010;215:215-222[PMID:19457571 DOI:10.1016/j.imbio.2009.03.009]
29 Russo RT,Mariano M.B-1 cell protective role in murine primary Mycobacterium bovis bacillus Calmette-Guerin infection.Immunobiology 2010;215:1005-1014[PMID:20188435 DOI:10.1016/j.imbio.2010.01.003]
30 Noal V,Santos S,Ferreira KS,Almeida SR.Infection with Paracoccidioides brasiliensis induces B-1 cell migration and activation of regulatory T cells.Microbes Infect 2016;18:798-803[PMID:27521490 DOI:10.1016/j.micinf.2016.08.001]
31 Gambero M,Teixeira D,Butin L,Ishimura ME,Mariano M,Popi AF,Longo-Maugéri IM.Propionibacterium acnes induces an adjuvant effect in B-1 cells and affects their phagocyte differentiation via a TLR2-mediated mechanism.Immunobiology 2016;221:1001-1011[PMID:27233619 DOI:10.1016/j.imbio.2016.03.003]
32 Popi AF,Longo-Maugéri IM,Mariano M.An Overview of B-1 Cells as Antigen-Presenting Cells.Front Immunol 2016;7:138[PMID:27148259 DOI:10.3389/fimmu.2016.00138]
33 De-Gennaro LA,Popi AF,Almeida SR,Lopes JD,Mariano M.B-1cells modulate oral tolerance in mice.Immunol Lett 2009;124:63-69[PMID:19389426 DOI:10.1016/j.imlet.2009.04.003]
34 Moore KW,de Waal Malefyt R,Coffman RL,O’Garra A.Interleukin-10and the interleukin-10 receptor.Annu Rev Immunol 2001;19:683-765[PMID:11244051 DOI:10.1146/annurev.immunol.19.1.683]
35 Kamanaka M,Kim ST,Wan YY,Sutterwala FS,Lara-Tejero M,Galán JE,Harhaj E,Flavell RA.Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse.Immunity 2006;25:941-952[PMID:17137799 DOI:10.1016/j.immuni.2006.09.013]
36 Joss A,Akdis M,Faith A,Blaser K,Akdis CA.IL-10 directly acts on T cells by specifically altering the CD28 co-stimulation pathway.Eur J Immunol 2000;30:1683-1690[PMID:10898505 DOI:10.1002/1521-4141(200006)30:6<1683::AID-IMMU1683>3.0.CO;2-A]
37 Padigel UM,Alexander J,Farrell JP.The role of interleukin-10 in susceptibility of BALB/c mice to infection with Leishmania mexicana and Leishmania amazonensis.J Immunol 2003;171:3705-3710[PMID:14500669 DOI:10.4049/jimmunol.171.7.3705]
38 Bronte V,Zanovello P.Regulation of immune responses by L-arginine metabolism.Nat Rev Immunol 2005;5:641-654[PMID:16056256DOI:10.1038/nri1668]
39 Raber P,Ochoa AC,Rodríguez PC.Metabolism of L-arginine by myeloid-derived suppressor cells in cancer:mechanisms of T cell suppression and therapeutic perspectives.Immunol Invest 2012;41:614-634[PMID:23017138 DOI:10.1111/j.1600-065X.2008.00608.x]
40 Munder M,Choi BS,Rogers M,Kropf P.L-arginine deprivation impairs Leishmania major-specific T-cell responses.Eur J Immunol2009;39:2161-2172[PMID:19637195 DOI:10.1002/eji.200839041]
41 Chowdhury BP,Das S,Majumder S,Halder K,Ghosh S,Biswas S,Bandyopadhyay S,Majumdar S.Immunomodulation of hostprotective immune response by regulating Foxp3 expression and Treg function in Leishmania-infected BALB/c mice:critical role of IRF1.Pathog Dis 2015;73:ftv063[PMID:26297915 DOI:10.1093/femspd/ftv063]
42 Clemente AM,Severini C,Castronovo G,Tanturli M,Perissi E,Cozzolino F,Torcia MG.Effects of soluble extracts from Leishmania infantum promastigotes,Toxoplasma gondii tachyzoites on TGF-βmediated pathways in activated CD4+T lymphocytes.Microbes Infect 2014;16:778-787[PMID:25130316 DOI:10.1016/j.micinf.2014.08.002]
43 Fran?a-Costa J,Van Weyenbergh J,Boaventura VS,Luz NF,MaltaSantos H,Oliveira MC,Santos de Campos DC,Saldanha AC,dosSantos WL,Bozza PT,Barral-Netto M,Barral A,Costa JM,Borges VM.Arginase I,polyamine,and prostaglandin E2 pathways suppress the inflammatory response and contribute to diffuse cutaneous leishmaniasis.J Infect Dis 2015;211:426-435[PMID:25124926DOI:10.1093/infdis/jiu455]
44 Barral A,Teixeira M,Reis P,Vinhas V,Costa J,Lessa H,Bittencourt AL,Reed S,Carvalho EM,Barral-Netto M.Transforming growth factor-beta in human cutaneous leishmaniasis.Am J Pathol 1995;147:947-954[PMID:7573370]
45 Li L,Zhang H,Wang W,Hong Y,Wang J,Zhang S,Xu S,Shu Q,Li J,Yang F,Zheng M,Qian Z,Liu P.Comparative proteomics reveals abnormal binding of ATGL and dysferlin on lipid droplets from pressure overload-induced dysfunctional rat hearts.Sci Rep 2016;6:19782[PMID:26795240 DOI:10.1038/srep19782]
46 Shapiro H,Pecht T,Shaco-Levy R,Harman-Boehm I,Kirshtein B,Kuperman Y,Chen A,Blüher M,Shai I,Rudich A.Adipose tissue foam cells are present in human obesity.J Clin Endocrinol Metab2013;98:1173-1181[PMID:23372170 DOI:10.1210/jc.2012-2745]
47 Bozza PT,Payne JL,Morham SG,Langenbach R,Smithies O,Weller PF.Leukocyte lipid body formation and eicosanoid generation:cyclooxygenase-independent inhibition by aspirin.Proc Natl Acad Sci USA 1996;93:11091-11096[PMID:8855314 DOI:10.1073/pnas.93.20.11091]
48 Freire-de-Lima CG,Xiao YQ,Gardai SJ,Bratton DL,Schiemann WP,Henson PM.Apoptotic cells,through transforming growth factor-beta,coordinately induce anti-inflammatory and suppress proinflammatory eicosanoid and NO synthesis in murine macrophages.JBiol Chem 2006;281:38376-38384[PMID:17056601 DOI:10.1074/jbc.M605146200]
2 Lopes JD,Mariano M.B-1 cell:the precursor of a novel mononuclear phagocyte with immuno-regulatory properties.An Acad Bras Cienc 2009;81:489-496[PMID:19722018 DOI:10.1590/s0001-37652009000300013]
3 Hardy RR.B-1 B cell development.J Immunol 2006;177:2749-2754[PMID:16920907 DOI:10.4049/jimmunol.177.5.2749]
4 Hayakawa K,Hardy RR,Parks DR,Herzenberg LA.The“Ly-1B”cell subpopulation in normal immunodefective,and autoimmune mice.J Exp Med 1983;157:202-218[PMID:6600267 DOI:10.1084/jem.157.1.202]
5 Boumsell L,Bernard A,Lepage V,Degos L,Lemerle J,Dausset J.Some chronic lymphocytic leukemia cells bearing surface immunoglobulins share determinants with T cells.Eur J Immunol1978;8:900-904[PMID:83236 DOI:10.1002/eji.1830081214]
6 Casali P,Burastero SE,Nakamura M,Inghirami G,Notkins AL.Human lymphocytes making rheumatoid factor and antibody to ss DNA belong to Leu-1+B-cell subset.Science 1987;236:77-81[PMID:3105056 DOI:10.1126/science.3105056]
7 Popi AF,Motta FL,Mortara RA,Schenkman S,Lopes JD,Mariano M.Co-ordinated expression of lymphoid and myeloid specific transcription factors during B-1b cell differentiation into mononuclear phagocytes in vitro.Immunology 2009;126:114-122[PMID:18710404 DOI:10.1111/j.1365-2567.2008.02883.x]
8 Almeida SR,Aroeira LS,Frymuller E,Dias MA,Bogsan CS,Lopes JD,Mariano M.Mouse B-1 cell-derived mononuclear phagocyte,a novel cellular component of acute non-specific inflammatory exudate.Int Immunol 2001;13:1193-1201[PMID:11526100 DOI:10.1093/intimm/13.9.1193]
9 Barbeiro DF,Barbeiro HV,Faintuch J,Ariga SK,Mariano M,Popi AF,de Souza HP,Velasco IT,Soriano FG.B-1 cells temper endotoxemic inflammatory responses.Immunobiology 2011;216:302-308[PMID:20817308 DOI:10.1016/j.imbio.2010.08.002]
10 Popi AF,Osugui L,Perez KR,Longo-Maugéri IM,Mariano M.Could a B-1 cell derived phagocyte“be one”of the peritoneal macrophages during LPS-driven inflammation?PLo S One 2012;7:e34570[PMID:22479646 DOI:10.1371/journal.pone.0034570]
11 Borrello MA,Phipps RP.Fibroblast-secreted macrophage colonystimulating factor is responsible for generation of biphenotypic B/macrophage cells from a subset of mouse B lymphocytes.J Immunol1999;163:3605-3611[PMID:10490953]
12 Cunningham AC.Parasitic adaptive mechanisms in infection by leishmania.Exp Mol Pathol 2002;72:132-141[PMID:11890722DOI:10.1006/exmp.2002.2418]
13 Arcanjo AF,La Rocque-de-Freitas IF,Rocha JD,Zamith D,Costada-Silva AC,Nunes MP,Mesquita-Santos FP,Morrot A,Filardy AA,Mariano M,Bandeira-Melo C,Dos Reis GA,Decote-Ricardo D,Freire-de-Lima CG.The PGE2/IL-10 Axis Determines Susceptibility of B-1 Cell-Derived Phagocytes(B-1CDP)to Leishmania major Infection.PLo S One 2015;10:e0124888[PMID:25933287 DOI:10.1371/journal.pone.0124888]
14 Filardy AA,Pires DR,Nunes MP,Takiya CM,Freire-de-Lima CG,Ribeiro-Gomes FL,Dos Reis GA.Proinflammatory clearance of apoptotic neutrophils induces an IL-12(low)IL-10(high)regulatory phenotype in macrophages.J Immunol 2010;185:2044-2050[PMID:20660352 DOI:10.4049/jimmunol.1000017]
15 Liese J,Schleicher U,Bogdan C.The innate immune response against Leishmania parasites.Immunobiology 2008;213:377-387[PMID:18406382 DOI:10.1016/j.imbio.2008.02.001]
16 Graf BA,Nazarenko DA,Borrello MA,Roberts LJ,Morrow JD,Palis J,Phipps RP.Biphenotypic B/macrophage cells express COX-1and up-regulate COX-2 expression and prostaglandin E(2)production in response to pro-inflammatory signals.Eur J Immunol 1999;29:3793-3803[PMID:10556836 DOI:10.1002/(SICI)1521-4141(199911)29:11<3793::AID-IMMU3793>3.0.CO;2-3]
17 Pinheiro RO,Nunes MP,Pinheiro CS,D’Avila H,Bozza PT,Takiya CM,C?rte-Real S,Freire-de-Lima CG,Dos Reis GA.Induction of autophagy correlates with increased parasite load of Leishmania amazonensis in BALB/c but not C57BL/6 macrophages.Microbes Infect 2009;11:181-190[PMID:19070676 DOI:10.1016/j.micinf.2008.11.006]
18 Ribeiro-Gomes FL,Otero AC,Gomes NA,Moniz-De-Souza MC,Cysne-Finkelstein L,Arnholdt AC,Calich VL,Coutinho SG,Lopes MF,Dos Reis GA.Macrophage interactions with neutrophils regulate Leishmania major infection.J Immunol 2004;172:4454-4462[PMID:15034061 DOI:10.4049/jimmunol.172.7.4454]
19 Freire-de-Lima CG,Nascimento DO,Soares MB,Bozza PT,CastroFaria-Neto HC,de Mello FG,Dos Reis GA,Lopes MF.Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages.Nature 2000;403:199-203[PMID:10646605 DOI:10.1038/35003208]
20 Luna-Gomes T,Filardy AA,Rocha JD,Decote-Ricardo D,La Rocque-de-Freitas IF,Morrot A,Bozza PT,Castro-Faria-Neto HC,Dos Reis GA,Nunes MP,Freire-de-Lima CG.Neutrophils increase or reduce parasite burden in Trypanosoma cruzi-infected macrophages,depending on host strain:role of neutrophil elastase.PLo S One 2014;9:e90582[PMID:24599360 DOI:10.1371/journal.pone.0090582]
21 Lopes MF,Freire-de-Lima CG,Dos Reis GA.The macrophage haunted by cell ghosts:a pathogen grows.Immunol Today 2000;21:489-494[PMID:11071527 DOI:10.1016/S0167-5699(00)01713-8]
22 Popi AF,Lopes JD,Mariano M.Interleukin-10 secreted by B-1 cells modulates the phagocytic activity of murine macrophages in vitro.Immunology 2004;113:348-354[PMID:15500621 DOI:10.1111/j.1365-2567.2004.01969.x]
23 Geraldo MM,Costa CR,Barbosa FM,Vivanco BC,Gonzaga WF,Novaes E Brito RR,Popi AF,Lopes JD,Xander P.In vivo and in vitro phagocytosis of Leishmania(Leishmania)amazonensis promastigotes by B-1 cells.Parasite Immunol 2016;38:365-376[PMID:27084328DOI:10.1111/pim.12324]
24 Bozza PT,Bakker-Abreu I,Navarro-Xavier RA,Bandeira-Melo C.Lipid body function in eicosanoid synthesis:an update.Prostaglandins Leukot Essent Fatty Acids 2011;85:205-213[PMID:21565480 DOI:10.1016/j.plefa.2011.04.020]
25 Toledo DA,Roque NR,Teixeira L,Milán-Garcés EA,Carneiro AB,Almeida MR,Andrade GF,Martins JS,Pinho RR,Freire-de-Lima CG,Bozza PT,D’Avila H,Melo RC.Lipid Body Organelles within the Parasite Trypanosoma cruzi:A Role for Intracellular Arachidonic Acid Metabolism.PLo S One 2016;11:e0160433[PMID:27490663DOI:10.1371/journal.pone.0160433]
26 D’Avila H,Freire-de-Lima CG,Roque NR,Teixeira L,Barja-Fidalgo C,Silva AR,Melo RC,Dosreis GA,Castro-Faria-Neto HC,Bozza PT.Host cell lipid bodies triggered by Trypanosoma cruzi infection and enhanced by the uptake of apoptotic cells are associated with prostaglandin E?generation and increased parasite growth.J Infect Dis 2011;204:951-961[PMID:21849292 DOI:10.1093/infdis/jir432]
27 Araújo-Santos T,Prates DB,Andrade BB,Nascimento DO,Clarêncio J,Entringer PF,Carneiro AB,Silva-Neto MA,Miranda JC,Brodskyn CI,Barral A,Bozza PT,Borges VM.Lutzomyia longipalpis saliva triggers lipid body formation and prostaglandin E?production in murine macrophages.PLo S Negl Trop Dis 2010;4:e873[PMID:21072234 DOI:10.1371/journal.pntd.0000873]
28 Oliveira HC,Popi AF,Bachi AL,Nonogaki S,Lopes JD,Mariano M.B-1 cells modulate the kinetics of wound-healing process in mice.Immunobiology 2010;215:215-222[PMID:19457571 DOI:10.1016/j.imbio.2009.03.009]
29 Russo RT,Mariano M.B-1 cell protective role in murine primary Mycobacterium bovis bacillus Calmette-Guerin infection.Immunobiology 2010;215:1005-1014[PMID:20188435 DOI:10.1016/j.imbio.2010.01.003]
30 Noal V,Santos S,Ferreira KS,Almeida SR.Infection with Paracoccidioides brasiliensis induces B-1 cell migration and activation of regulatory T cells.Microbes Infect 2016;18:798-803[PMID:27521490 DOI:10.1016/j.micinf.2016.08.001]
31 Gambero M,Teixeira D,Butin L,Ishimura ME,Mariano M,Popi AF,Longo-Maugéri IM.Propionibacterium acnes induces an adjuvant effect in B-1 cells and affects their phagocyte differentiation via a TLR2-mediated mechanism.Immunobiology 2016;221:1001-1011[PMID:27233619 DOI:10.1016/j.imbio.2016.03.003]
32 Popi AF,Longo-Maugéri IM,Mariano M.An Overview of B-1 Cells as Antigen-Presenting Cells.Front Immunol 2016;7:138[PMID:27148259 DOI:10.3389/fimmu.2016.00138]
33 De-Gennaro LA,Popi AF,Almeida SR,Lopes JD,Mariano M.B-1cells modulate oral tolerance in mice.Immunol Lett 2009;124:63-69[PMID:19389426 DOI:10.1016/j.imlet.2009.04.003]
34 Moore KW,de Waal Malefyt R,Coffman RL,O’Garra A.Interleukin-10and the interleukin-10 receptor.Annu Rev Immunol 2001;19:683-765[PMID:11244051 DOI:10.1146/annurev.immunol.19.1.683]
35 Kamanaka M,Kim ST,Wan YY,Sutterwala FS,Lara-Tejero M,Galán JE,Harhaj E,Flavell RA.Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse.Immunity 2006;25:941-952[PMID:17137799 DOI:10.1016/j.immuni.2006.09.013]
36 Joss A,Akdis M,Faith A,Blaser K,Akdis CA.IL-10 directly acts on T cells by specifically altering the CD28 co-stimulation pathway.Eur J Immunol 2000;30:1683-1690[PMID:10898505 DOI:10.1002/1521-4141(200006)30:6<1683::AID-IMMU1683>3.0.CO;2-A]
37 Padigel UM,Alexander J,Farrell JP.The role of interleukin-10 in susceptibility of BALB/c mice to infection with Leishmania mexicana and Leishmania amazonensis.J Immunol 2003;171:3705-3710[PMID:14500669 DOI:10.4049/jimmunol.171.7.3705]
38 Bronte V,Zanovello P.Regulation of immune responses by L-arginine metabolism.Nat Rev Immunol 2005;5:641-654[PMID:16056256DOI:10.1038/nri1668]
39 Raber P,Ochoa AC,Rodríguez PC.Metabolism of L-arginine by myeloid-derived suppressor cells in cancer:mechanisms of T cell suppression and therapeutic perspectives.Immunol Invest 2012;41:614-634[PMID:23017138 DOI:10.1111/j.1600-065X.2008.00608.x]
40 Munder M,Choi BS,Rogers M,Kropf P.L-arginine deprivation impairs Leishmania major-specific T-cell responses.Eur J Immunol2009;39:2161-2172[PMID:19637195 DOI:10.1002/eji.200839041]
41 Chowdhury BP,Das S,Majumder S,Halder K,Ghosh S,Biswas S,Bandyopadhyay S,Majumdar S.Immunomodulation of hostprotective immune response by regulating Foxp3 expression and Treg function in Leishmania-infected BALB/c mice:critical role of IRF1.Pathog Dis 2015;73:ftv063[PMID:26297915 DOI:10.1093/femspd/ftv063]
42 Clemente AM,Severini C,Castronovo G,Tanturli M,Perissi E,Cozzolino F,Torcia MG.Effects of soluble extracts from Leishmania infantum promastigotes,Toxoplasma gondii tachyzoites on TGF-βmediated pathways in activated CD4+T lymphocytes.Microbes Infect 2014;16:778-787[PMID:25130316 DOI:10.1016/j.micinf.2014.08.002]
43 Fran?a-Costa J,Van Weyenbergh J,Boaventura VS,Luz NF,MaltaSantos H,Oliveira MC,Santos de Campos DC,Saldanha AC,dosSantos WL,Bozza PT,Barral-Netto M,Barral A,Costa JM,Borges VM.Arginase I,polyamine,and prostaglandin E2 pathways suppress the inflammatory response and contribute to diffuse cutaneous leishmaniasis.J Infect Dis 2015;211:426-435[PMID:25124926DOI:10.1093/infdis/jiu455]
44 Barral A,Teixeira M,Reis P,Vinhas V,Costa J,Lessa H,Bittencourt AL,Reed S,Carvalho EM,Barral-Netto M.Transforming growth factor-beta in human cutaneous leishmaniasis.Am J Pathol 1995;147:947-954[PMID:7573370]
45 Li L,Zhang H,Wang W,Hong Y,Wang J,Zhang S,Xu S,Shu Q,Li J,Yang F,Zheng M,Qian Z,Liu P.Comparative proteomics reveals abnormal binding of ATGL and dysferlin on lipid droplets from pressure overload-induced dysfunctional rat hearts.Sci Rep 2016;6:19782[PMID:26795240 DOI:10.1038/srep19782]
46 Shapiro H,Pecht T,Shaco-Levy R,Harman-Boehm I,Kirshtein B,Kuperman Y,Chen A,Blüher M,Shai I,Rudich A.Adipose tissue foam cells are present in human obesity.J Clin Endocrinol Metab2013;98:1173-1181[PMID:23372170 DOI:10.1210/jc.2012-2745]
47 Bozza PT,Payne JL,Morham SG,Langenbach R,Smithies O,Weller PF.Leukocyte lipid body formation and eicosanoid generation:cyclooxygenase-independent inhibition by aspirin.Proc Natl Acad Sci USA 1996;93:11091-11096[PMID:8855314 DOI:10.1073/pnas.93.20.11091]
48 Freire-de-Lima CG,Xiao YQ,Gardai SJ,Bratton DL,Schiemann WP,Henson PM.Apoptotic cells,through transforming growth factor-beta,coordinately induce anti-inflammatory and suppress proinflammatory eicosanoid and NO synthesis in murine macrophages.JBiol Chem 2006;281:38376-38384[PMID:17056601 DOI:10.1074/jbc.M605146200]