Leishmania infantum parasites subvert the host inflammatory response through the adenosine A2A receptor to promote the establishment of infection

Frontiers in Immunology

Volumn 8, Issue JUL, 2017, Pages

  Lima, Mikhael H F ^a   Sacramento, Lais A ^a   Quirino, Gustavo F S ^a   Ferreira, Marcela D ^a   Benevides, Luciana ^a   Santana, Alynne K M ^b   Cunha, Fernando Q ^a   Almeida, Roque P ^b   Silva, João S ^a   Carregaro, Vanessa ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF SERGIPE   (Brazil)

Author keywords

A2AR signaling; Adenosine; Immunoregulation; Inflammation; Visceral leishmaniasis

Indexed keywords

ADENOSINE A2A RECEPTOR; CD11B ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD69 ANTIGEN; CHEMOKINE RECEPTOR CXCR2; CXCL1 CHEMOKINE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 17; MESSENGER RNA; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CONTROLLED STUDY; FEMALE; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LEISHMANIA INFANTUM; LEISHMANIASIS; MOUSE; NEUTRON ACTIVATION ANALYSIS; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOGEN LOAD; POLYMERASE CHAIN REACTION; PROTEIN DEPLETION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPLEEN CELL; TH1 CELL;

EID: 85025682096     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.00815     Document Type: Article

References (77)

1. Mansueto P, Seidita A, Vitale G, Cascio A. Leishmaniasis in travelers: a literature review. Travel Med Infect Dis (2014) 12(6 Pt A):563-81. doi:10.1016/j.tmaid.2014.09.007
2. Murray HW. Tissue granuloma structure-function in experimental visceral leishmaniasis. Int J Exp Pathol (2001) 82(5):249-67. doi:10.1046/j.1365-2613.2001.00199.x
3. Murray HW, Berman JD, Davies CR, Saravia NG. Advances in leishmaniasis. Lancet (2005) 366(9496):1561-77. doi:10.1016/S0140-6736(05)67629-5
4. Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, et al. Leishmaniasis worldwide and global estimates of its incidence. PLoS One (2012) 7(5):e35671. doi:10.1371/journal.pone.0035671
5. Liew FY, Millott S, Parkinson C, Palmer RM, Moncada S. Macrophage killing of Leishmania parasite in vivo is mediated by nitric oxide from l-arginine. J Immunol (1990) 144(12):4794-7
6. Liew FY, Wei XQ, Proudfoot L. Cytokines and nitric oxide as effector molecules against parasitic infections. Philos Trans R Soc Lond B Biol Sci (1997) 352(1359):1311-5. doi:10.1098/rstb.1997.0115
7. Nascimento MS, Carregaro V, Lima-Júnior DS, Costa DL, Ryffel B, Duthie MS, et al. Interleukin 17A acts synergistically with interferon ? to promote protection against Leishmania infantum infection. J Infect Dis (2015) 211(6):1015-26. doi:10.1093/infdis/jiu531
8. Nylen S, Sacks D. Interleukin-10 and the pathogenesis of human visceral leishmaniasis. Trends Immunol (2007) 28(9):378-84. doi:10.1016/j.it.2007.07.004
9. Carregaro V, Napimoga MH, Peres RS, Benevides L, Sacramento LA, Pinto LG, et al. Therapeutic treatment of arthritic mice with 15-deoxy Delta12, 14-prostaglandin J2 (15d-PGJ2) ameliorates disease through the suppression of Th17 cells and the induction of CD4+CD25-FOXP3+ cells. Mediators Inflamm (2016) 2016:9626427. doi:10.1155/2016/9626427
10. Chaves MM, Canetti C, Coutinho-Silva R. Crosstalk between purinergic receptors and lipid mediators in leishmaniasis. Parasit Vectors (2016) 9(1):489. doi:10.1186/s13071-016-1781-1
11. Haskó G, Linden J, Cronstein B, Pacher P. Adenosine receptors: therapeutic aspects for inflammatory and immune diseases. Nat Rev Drug Discov (2008) 7(9):759-70. doi:10.1038/nrd2638
12. Haskó G, Cronstein BN. Adenosine: an endogenous regulator of innate immunity. Trends Immunol (2004) 25(1):33-9. doi:10.1016/j.it.2003.11.003
13. Burnstock G. Purinergic signalling. Br J Pharmacol (2006) 147(Suppl 1):S172-81. doi:10.1038/sj.bjp.0706429
14. Ralevic V, Burnstock G. Receptors for purines and pyrimidines. Pharmacol Rev (1998) 50(3):413-92
15. Fredholm BB, Arslan G, Halldner L, Kull B, Schulte G, Wasserman W. Structure and function of adenosine receptors and their genes. Naunyn Schmiedebergs Arch Pharmacol (2000) 362(4-5):364-74. doi:10.1007/s002100000313
16. Ohta A, Sitkovsky M. Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage. Nature (2001) 414(6866):916-20. doi:10.1038/414916a
17. Naganuma M, Wiznerowicz EB, Lappas CM, Linden J, Worthington MT, Ernst PB. Cutting edge: critical role for A2A adenosine receptors in the T cell-mediated regulation of colitis. J Immunol (2006) 177(5):2765-9. doi:10.4049/jimmunol.177.5.2765
18. Hasko G, Pacher P. A2A receptors in inflammation and injury: lessons learned from transgenic animals. J Leukoc Biol (2008) 83(3):447-55. doi:10.1189/jlb.0607359
19. Csóka B, Selmeczy Z, Koscsó B, Németh ZH, Pacher P, Murray PJ, et al. Adenosine promotes alternative macrophage activation via A2A and A2B receptors. FASEB J (2012) 26(1):376-86. doi:10.1096/fj.11-190934
20. Salmon JE, Cronstein BN. Fc gamma receptor-mediated functions in neutrophils are modulated by adenosine receptor occupancy. A1 receptors are stimulatory and A2 receptors are inhibitory. J Immunol (1990) 145(7):2235-40
21. Cronstein BN, Daguma L, Nichols D, Hutchison AJ, Williams M. The adenosine/neutrophil paradox resolved: human neutrophils possess both A1 and A2 receptors that promote chemotaxis and inhibit O2 generation, respectively. J Clin Invest (1990) 85(4):1150-7. doi:10.1172/JCI114547
22. Fredholm BB, Zhang Y, van der Ploeg I. Adenosine A2A receptors mediate the inhibitory effect of adenosine on formyl-Met-Leu-Phe-stimulated respiratory burst in neutrophil leucocytes. Naunyn Schmiedebergs Arch Pharmacol (1996) 354(3):262-7. doi:10.1007/BF00171056
23. Fredholm BB. Purines and neutrophil leukocytes. Gen Pharmacol (1997) 28(3):345-50. doi:10.1016/S0306-3623(96)00169-3
24. Save S, Mohlin C, Vumma R, Persson K. Activation of adenosine A2A receptors inhibits neutrophil transuroepithelial migration. Infect Immun (2011) 79(8):3431-7. doi:10.1128/IAI.05005-11
25. Lappas CM, Rieger JM, Linden J. A2A adenosine receptor induction inhibits IFN-gamma production in murine CD4+ T cells. J Immunol (2005) 174(2):1073-80. doi:10.4049/jimmunol.174.2.1073
26. Bruzzese L, Fromonot J, By Y, Durand-Gorde JM, Condo J, Kipson N, et al. NF-κB enhances hypoxia-driven T-cell immunosuppression via upregulation of adenosine A(2A) receptors. Cell Signal (2014) 26(5):1060-7. doi:10.1016/j.cellsig.2014.01.024
27. Zarek PE, Huang CT, Lutz ER, Kowalski J, Horton MR, Linden J, et al. A2A receptor signaling promotes peripheral tolerance by inducing T-cell anergy and the generation of adaptive regulatory T cells. Blood (2008) 111(1):251-9. doi:10.1182/blood-2007-03-081646
28. Ohta A, Kini R, Ohta A, Subramanian M, Madasu M, Sitkovsky M. The development and immunosuppressive functions of CD4(+) CD25(+) FoxP3(+) regulatory T cells are under influence of the adenosine-A2A adenosine receptor pathway. Front Immunol (2012) 3:190. doi:10.3389/fimmu.2012.00190
29. Carregaro V, Sa-Nunes A, Cunha TM, Grespan R, Oliveira CJ, Lima-Junior DS, et al. Nucleosides from Phlebotomus papatasi salivary gland ameliorate murine collagen-induced arthritis by impairing dendritic cell functions. J Immunol (2011) 187(8):4347-59. doi:10.4049/jimmunol.1003404
30. Tasca T, Bonan CD, De Carli GA, Sarkis JJ, Alderete JF. Heterogeneity in extracellular nucleotide hydrolysis among clinical isolates of Trichomonas vaginalis. Parasitology (2005) 131(Pt 1):71-8. doi:10.1017/S0031182005007377
31. Santos RF, Possa MA, Bastos MS, Guedes PM, Almeida MR, Demarco R, et al. Influence of ecto-nucleoside triphosphate diphosphohydrolase activity on Trypanosoma cruzi infectivity and virulence. PLoS Negl Trop Dis (2009) 3(3):e387. doi:10.1371/journal.pntd.0000387
32. de Souza MC, de Assis EA, Gomes RS, Marques da Silva Ede A, Melo MN, Fietto JL, et al. The influence of ecto-nucleotidases on Leishmania amazonensis infection and immune response in C57B/6 mice. Acta Trop (2010) 115(3):262-9. doi:10.1016/j.actatropica.2010.04.007
33. Russo-Abrahao T, Cosentino-Gomes D, Daflon-Yunes N, Meyer-Fernandes JR. Giardia duodenalis: biochemical characterization of an ecto-5'-nucleotidase activity. Exp Parasitol (2011) 127(1):66-71. doi:10.1016/j.exppara.2010.06.028
34. Paletta-Silva R, Meyer-Fernandes JR. Adenosine and immune imbalance in visceral leishmaniasis: the possible role of ectonucleotidases. J Trop Med (2012) 2012:650874. doi:10.1155/2012/650874
35. Paletta-Silva R, Vieira-Bernardo R, Cosentino-Gomes D, Meyer-Fernandes JR. Leishmania amazonensis: inhibition of 3'-nucleotidase activity by Cu2+ ions. Exp Parasitol (2012) 131(1):63-8. doi:10.1016/j.exppara.2012.03.001
36. Mahamed DA, Toussaint LE, Bynoe MS. CD73-generated adenosine is critical for immune regulation during Toxoplasma gondii infection. Infect Immun (2015) 83(2):721-9. doi:10.1128/IAI.02536-14
37. Russo-Abrahao T, Cosentino-Gomes D, Gomes MT, Alviano DS, Alviano CS, Lopes AH, et al. Biochemical properties of Candida parapsilosis ecto-5'-nucleotidase and the possible role of adenosine in macrophage interaction. FEMS Microbiol Lett (2011) 317(1):34-42. doi:10.1111/j.1574-6968.2011.02216.x
38. Sansom FM, Newton HJ, Crikis S, Cianciotto NP, Cowan PJ, d'Apice AJ, et al. A bacterial ecto-triphosphate diphosphohydrolase similar to human CD39 is essential for intracellular multiplication of Legionella pneumophila. Cell Microbiol (2007) 9(8):1922-35. doi:10.1111/j.1462-5822.2007.00924.x
39. Thammavongsa V, Kern JW, Missiakas DM, Schneewind O. Staphylococcus aureus synthesizes adenosine to escape host immune responses. J Exp Med (2009) 206(11):2417-27. doi:10.1084/jem.20090097
40. Theatre E, Frederix K, Guilmain W, Delierneux C, Lecut C, BettendorffL, et al. Overexpression of CD39 in mouse airways promotes bacteria-induced inflammation. J Immunol (2012) 189(4):1966-74. doi:10.4049/jimmunol.1102600
41. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, Cerqueira GC, et al. The genome of the blood fluke Schistosoma mansoni. Nature (2009) 460(7253):352-8. doi:10.1038/nature08160
42. Zhou YP, Wu ZD, Yang LL, Sun X, You X, Yu XB, et al. Cloning, molecular characterization of a 13-kDa antigen from Schistosoma japonicum, Sj13, a putative salivary diagnosis candidate for Schistosomiasis japonica. Parasitol Res (2009) 105(5):1435-44. doi:10.1007/s00436-009-1575-x
43. Peres-Sampaio CE, Palumbo ST, Meyer-Fernandes JR. An ecto-ATPase activity present in Leishmania tropica stimulated by dextran sulfate. Z Naturforsch C (2001) 56(9-10):820-5. doi:10.1515/znc-2001-9-1023
44. Gomes RS, de Carvalho LC, de Souza Vasconcellos R, Fietto JL, Afonso LC. E-NTPDase (ecto-nucleoside triphosphate diphosphohydrolase) of Leishmania amazonensis inhibits macrophage activation. Microbes Infect (2015) 17(4):295-303. doi:10.1016/j.micinf.2014.12.009
45. Figueiredo AB, Souza-Testasicca MC, Afonso LC. Purinergic signaling and infection by Leishmania: a new approach to evasion of the immune response. Biomed J (2016) 39(4):244-50. doi:10.1016/j.bj.2016.08.004
46. Carregaro V, Ribeiro JM, Valenzuela JG, Souza-Júnior DL, Costa DL, Oliveira CJ, et al. Nucleosides present on phlebotomine saliva induce immunossuppression and promote the infection establishment. PLoS Negl Trop Dis (2015) 9(4):e0003600. doi:10.1371/journal.pntd.0003600
47. Matte C, Olivier M. Leishmania-induced cellular recruitment during the early inflammatory response: modulation of proinflammatory mediators. J Infect Dis (2002) 185(5):673-81. doi:10.1086/339260
48. Vieira DP, Paletta-Silva R, Saraiva EM, Lopes AH, Meyer-Fernandes JR. Leishmania chagasi: an ecto-3'-nucleotidase activity modulated by inorganic phosphate and its possible involvement in parasite-macrophage interaction. Exp Parasitol (2011) 127(3):702-7. doi:10.1016/j.exppara.2010.11.003
49. Rai AK, Thakur CP, Velpandian T, Sharma SK, Ghosh B, Mitra DK. High concentration of adenosine in human visceral leishmaniasis despite increased ADA and decreased CD73. Parasite Immunol (2011) 33(11):632-6. doi:10.1111/j.1365-3024.2011.01315.x
50. Vijay M, Amit A, Kumar S, Dikhit MR, Jha PK, Singh AK, et al. Up regulation of A(2B) adenosine receptor on monocytes are crucially required for immune pathogenicity in Indian patients exposed to Leishmania donovani. Cytokine (2016) 79:38-44. doi:10.1016/j.cyto.2015.12.016
51. Titus RG, Ceredig R, Cerottini JC, Louis JA. Therapeutic effect of anti-L3T4 monoclonal antibody GK1.5 on cutaneous leishmaniasis in genetically-susceptible BALB/c mice. J Immunol (1985) 135(3):2108-14
52. Buffet PA, Sulahian A, Garin YJ, Nassar N, Derouin F. Culture microtitration: a sensitive method for quantifying Leishmania infantum in tissues of infected mice. Antimicrob Agents Chemother (1995) 39(9):2167-8. doi:10.1128/AAC.39.9.2167
53. Oghumu S, Gupta G, Snider HM, Varikuti S, Terrazas CA, Papenfuss TL, et al. STAT4 is critical for immunity but not for antileishmanial activity of antimonials in experimental visceral leishmaniasis. Eur J Immunol (2014) 44(2):450-9. doi:10.1002/eji.201343477
54. Olekhnovitch R, Bousso P. Induction, propagation, and activity of host nitric oxide: lessons from Leishmania infection. Trends Parasitol (2015) 31(12):653-64. doi:10.1016/j.pt.2015.08.001
55. Thalhofer CJ, Chen Y, Sudan B, Love-Homan L, Wilson ME. Leukocytes infiltrate the skin and draining lymph nodes in response to the protozoan Leishmania infantum chagasi. Infect Immun (2011) 79(1):108-17. doi:10.1128/IAI.00338-10
56. Sacramento LA, Cunha FQ, de Almeida RP, da Silva JS, Carregaro V. Protective role of 5-lipoxigenase during Leishmania infantum infection is associated with Th17 subset. Biomed Res Int (2014) 2014:264270. doi:10.1155/2014/264270
57. Sacramento L, Trevelin SC, Nascimento MS, Lima-Junior DS, Costa DL, Almeida RP, et al. Toll-like receptor 9 signaling in dendritic cells regulates neutrophil recruitment to inflammatory foci following Leishmania infantum infection. Infect Immun (2015) 83(12):4604-16. doi:10.1128/IAI.00975-15
58. Barletta KE, Ley K, Mehrad B. Regulation of neutrophil function by adenosine. Arterioscler Thromb Vasc Biol (2012) 32(4):856-64. doi:10.1161/ATVBAHA.111.226845
59. Chen Y, Shukla A, Namiki S, Insel PA, Junger WG. A putative osmoreceptor system that controls neutrophil function through the release of ATP, its conversion to adenosine, and activation of A2 adenosine and P2 receptors. J Leukoc Biol (2004) 76(1):245-53. doi:10.1189/jlb.0204066
60. Chen Y, Corriden R, Inoue Y, Yip L, Hashiguchi N, Zinkernagel A, et al. ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science (2006) 314(5806):1792-5. doi:10.1126/science.1132559
61. Corriden R, Chen Y, Inoue Y, Beldi G, Robson SC, Insel PA, et al. Ecto-nucleoside triphosphate diphosphohydrolase 1 (E-NTPDase1/CD39) regulates neutrophil chemotaxis by hydrolyzing released ATP to adenosine. J Biol Chem (2008) 283(42):28480-6. doi:10.1074/jbc. M800039200
62. Atzeni F, Schena M, Ongari AM, Carrabba M, Bonara P, Minonzio F, et al. Induction of CD69 activation molecule on human neutrophils by GM-CSF, IFN-gamma, and IFN-alpha. Cell Immunol (2002) 220(1):20-9. doi:10.1016/S0008-8749(03)00002-9
63. Atzeni F, Del Papa N, Sarzi-Puttini P, Bertolazzi F, Minonzio F, Capsoni F. CD69 expression on neutrophils from patients with rheumatoid arthritis. Clin Exp Rheumatol (2004) 22(3):331-4
64. Ellis TN, Beaman BL. Interferon-gamma activation of polymorphonuclear neutrophil function. Immunology (2004) 112(1):2-12. doi:10.1111/j.1365-2567.2004.01849.x
65. Wei J, Duramad O, Perng OA, Reiner SL, Liu YJ, Qin FX. Antagonistic nature of T helper 1/2 developmental programs in opposing peripheral induction of Foxp3+ regulatory T cells. Proc Natl Acad Sci U S A (2007) 104(46):18169-74. doi:10.1073/pnas.0703642104
66. Moore JW, Moyo D, Beattie L, Andrews PS, Timmis J, Kaye PM. Functional complexity of the Leishmania granuloma and the potential of in silico modeling. Front Immunol (2013) 4:35. doi:10.3389/fimmu.2013.00035
67. Sacramento L, Trevelin SC, Nascimento MS, Souza-Júnior DL, Costa DL, Almeida RP, et al. TLR9 signaling on dendritic cells regulates neutrophil recruitment to inflammatory foci following Leishmania infantum infection. Infect Immun (2015) 83(12):4604-16. doi:10.1128/IAI.00975-15
68. Fortin A, Harbour D, Fernandes M, Borgeat P, Bourgoin S. Differential expression of adenosine receptors in human neutrophils: up-regulation by specific Th1 cytokines and lipopolysaccharide. J Leukoc Biol (2006) 79(3):574-85. doi:10.1189/jlb.0505249
69. Cronstein BN. Adenosine, an endogenous anti-inflammatory agent. J Appl Physiol (1985) (1994) 76(1):5-13
70. Khadem F, Gao X, Mou Z, Jia P, Movassagh H, Onyilagha C, et al. Hepatic stellate cells regulate liver immunity to visceral leishmaniasis through P110d-dependent induction and expansion of regulatory T cells in mice. Hepatology (2016) 63(2):620-32. doi:10.1002/hep.28130
71. Deaglio S, Dwyer KM, Gao W, Friedman D, Usheva A, Erat A, et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med (2007) 204(6):1257-65. doi:10.1084/jem.20062512
72. Csóka B, Németh ZH, Virág L, Gergely P, Leibovich SJ, Pacher P, et al. A2A adenosine receptors and C/EBPbeta are crucially required for IL-10 production by macrophages exposed to Escherichia coli. Blood (2007) 110(7):2685-95. doi:10.1182/blood-2007-01-065870
73. Haskó G, Pacher P. Regulation of macrophage function by adenosine. Arterioscler Thromb Vasc Biol (2012) 32(4):865-9. doi:10.1161/ATVBAHA.111.226852
74. Burnstock G. Purinergic signalling: from discovery to current developments. Exp Physiol (2014) 99(1):16-34. doi:10.1113/expphysiol.2013.071951
75. Antonioli L, Blandizzi C, Csóka B, Pacher P, Haskó G. Adenosine signalling in diabetes mellitus-pathophysiology and therapeutic considerations. Nat Rev Endocrinol (2015) 11(4):228-41. doi:10.1038/nrendo.2015.10
76. Murray HW, Lu CM, Mauze S, Freeman S, Moreira AL, Kaplan G, et al. Interleukin-10 (IL-10) in experimental visceral leishmaniasis and IL-10 receptor blockade as immunotherapy. Infect Immun (2002) 70(11):6284-93. doi:10.1128/IAI.70.11.6284-6293.2002
77. Nascimento MS, Carregaro V, Lima-Junior DS, Costa DL, Ryffel B, Duthie MS, et al. Interleukin 17A acts synergistically with interferon gamma to promote protection against Leishmania infantum infection. J Infect Dis (2015) 211(6):1015-26. doi:10.1093/infdis/jiu531