Role of extracellular nucleotides in the immune response against intracellular bacteria and protozoan parasites

Microbes and Infection

Volumn 14, Issue 14, 2012, Pages 1271-1277

  Coutinho Silva, Robson ^a   Ojcius, David M ^b  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Danger signals; Extracellular ATP; Inflammasome; Inflammation; Intracellular pathogens; Purinergic receptors

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE A2B RECEPTOR; ADENOSINE TRIPHOSPHATE; BENZOYL ADENOSINE TRIPHOSPHATE; CD39 ANTIGEN; CRYOPYRIN; CYCLIC AMP; CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; NUCLEOTIDE; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PATTERN RECOGNITION RECEPTOR; PHOSPHOLIPASE D; PURINERGIC P2X RECEPTOR; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; PURINERGIC P2Y4 RECEPTOR; PURINERGIC RECEPTOR; PURINERGIC RECEPTOR STIMULATING AGENT; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIUM; CD4 CD8 RATIO; CELL MEMBRANE PERMEABILITY; CHAGAS DISEASE; CHEMOTAXIS; CHLAMYDIA; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; ENZYME INHIBITION; EXTRACELLULAR SPACE; GINGIVA; GROWTH INHIBITION; HUMAN; IMMUNE RESPONSE; IMMUNITY; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SPACE; LEISHMANIA; LEISHMANIASIS; LYMPHOCYTE PROLIFERATION; LYSOSOME; MACROPHAGE; MEDIATOR; NONHUMAN; PATHOGENESIS; PHAGOSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTOZOON; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE; THYMUS; TRYPANOSOMA CRUZI;

ADENOSINE TRIPHOSPHATE; ANIMALS; BACTERIA; BACTERIAL INFECTIONS; EXTRACELLULAR SPACE; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMASOMES; INFLAMMATION; INTRACELLULAR SPACE; MODELS, BIOLOGICAL; PARASITES; PARASITIC DISEASES;

PROTOZOA;

EID: 84870249420     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2012.05.009     Document Type: Article

References (83)

1. Aymeric L., Apetoh L., Ghiringhelli F., Tesniere A., Martins I., Kroemer G., Smyth M.J., Zitvogel L. Tumor cell death and ATP release prime dendritic cells and efficient anticancer immunity. Cancer Res. 2010, 70:855-858.
2. Burnstock G. Purinergic signalling. Br. J. Pharmacol. 2006, 147(Suppl 1):S172-S181.
3. Praetorius H.A., Leipziger J. ATP release from non-excitable cells. Purinergic Signal. 2009, 5:433-446.
4. Burnstock G. Purine and pyrimidine receptors. Cell Mol. Life Sci. 2007, 64:1471-1483.
5. Abbracchio M.P., Burnstock G., Boeynaems J.M., Barnard E.A., Boyer J.L., Kennedy C., Knight G.E., Fumagalli M., Gachet C., Jacobson K.A., Weisman G.A. International union of pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol. Rev. 2006, 58:281-341.
6. Kukulski F., Ben Y.F., Lecka J., Kauffenstein G., Levesque S.A., Martin-Satue M., Sevigny J. Extracellular ATP and P2 receptors are required for IL-8 to induce neutrophil migration. Cytokine 2009, 46:166-170.
7. Kronlage M., Song J., Sorokin L., Isfort K., Schwerdtle T., Leipziger J., Robaye B., Conley P.B., Kim H.C., Sargin S., Schon P., Schwab A., Hanley P.J. Autocrine purinergic receptor signaling is essential for macrophage chemotaxis. Sci. Signal. 2010, 3:ra55.
8. McDonald B., Pittman K., Menezes G.B., Hirota S.A., Slaba I., Waterhouse C.C., Beck P.L., Muruve D.A., Kubes P. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 2010, 330:362-366.
9. Ferrari D., Chiozzi P., Falzoni S., Dal Susino M., Melchiorri L., Baricordi O.R., Di Virgilio F. Extracellular ATP triggers IL-1 beta release by activating the purinergic P2Z receptor of human macrophages. J. Immunol. 1997, 159:1451-1458.
10. Ferrari D., Pizzirani C., Adinolfi E., Lemoli R.M., Curti A., Idzko M., Panther E., Di Virgilio F. The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 2006, 176:3877-3883.
11. la Sala A., Ferrari D., Corinti S., Cavani A., Di Virgilio F., Girolomoni G., Meyer M.P., Clarke J.D., Patel K., Townsend-Nicholson A., Burnstock G. Extracellular ATP induces a distorted maturation of dendritic cells and inhibits their capacity to initiate Th1 responses. J. Immunol. 2001, 166:1611-1617.
12. Coutinho-Silva R., Correa G., Sater A.A., Ojcius D.M. The P2X(7) receptor and intracellular pathogens: a continuing struggle. Purinergic Signal. 2009, 5:197-204.
13. Junger W.G. Immune cell regulation by autocrine purinergic signalling. Nat. Rev. Immunol. 2011, 11:201-212.
14. Elliott M.R., Chekeni F.B., Trampont P.C., Lazarowski E.R., Kadl A., Walk S.F., Park D., Woodson R.I., Ostankovich M., Sharma P., Lysiak J.J., Harden T.K., Leitinger N., Ravichandran K.S. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009, 461:282-286.
15. Chen Y., Corriden R., Inoue Y., Yip L., Hashiguchi N., Zinkernagel A., Nizet V., Insel P.A., Junger W.G. ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science 2006, 314:1792-1795.
16. Koizumi S., Shigemoto-Mogami Y., Nasu-Tada K., Shinozaki Y., Ohsawa K., Tsuda M., Joshi B.V., Jacobson K.A., Kohsaka S., Inoue K. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 2007, 446:1091-1095.
17. Marques-da-Silva C., Burnstock G., Ojcius D.M., Coutinho-Silva R. Purinergic receptor agonists modulate phagocytosis and clearance of apoptotic cells in macrophages. Immunobiology 2011, 216:1-11.
18. la Sala A., Sebastiani S., Ferrari D., Di Virgilio F., Idzko M., Norgauer J., Girolomoni G. Dendritic cells exposed to extracellular adenosine triphosphate acquire the migratory properties of mature cells and show a reduced capacity to attract type 1 T lymphocytes. Blood 2002, 99:1715-1722.
19. Fredholm B.B., Ijzerman A.P., Jacobson K.A., Klotz K.N., Linden J. International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol. Rev. 2001, 53:527-552.
20. Verzijl D., Ijzerman A.P. Functional selectivity of adenosine receptor ligands. Purinergic Signal. 2011, 7:171-192.
21. Bours M.J., Swennen E.L., Di Virgilio F., Cronstein B.N., Dagnelie P.C. Adenosine 5'-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol. Ther. 2006, 112:358-404.
22. 7 nucleotide receptor and associated phospholipase D activity by lipopolysaccharide and IFN-gamma in the human THP-1 monocytic cell line. J. Immunol. 1996, 157:5627-5637.
23. Perregaux D., Gabel C.A. Interleukin-1β maturation and release in response to ATP and nigericin. J. Biol. Chem. 1994, 269:15195-15203.
24. Perregaux D.G., McNiff P., Laliberte R., Conklyn M., Gabel C.A. ATP acts as an agonist to promote stimulus-induced secretion of IL-1 beta and IL-18 in human blood. J. Immunol. 2000, 165:4615-4623.
25. Lammas D.A., Stober C., Harvey C.J., Kendrick N., Panchalingam S., Kumararatne D.S. ATP-induced killing of mycobacteria by human macrophages is mediated by purinergic P2Z(P2X7) receptors. Immunity 1997, 7:433-444.
26. Stober C.B., Lammas D.A., Li C.M., Kumararatne D.S., Lightman S.L., McArdle C.A. ATP-mediated killing of Mycobacterium bovis Bacille calmette-guerin within human macrophages is calcium dependent and associated with the acidification of mycobacteria-containing phagosomes. J. Immunol. 2001, 166:6276-6286.
27. Fairbairn I.P., Stober C.B., Kumararatne D.S., Lammas D.A. ATP-mediated killing of intracellular mycobacteria by macrophages is a P2X(7)-dependent process inducing bacterial death by phagosome-lysosome fusion. J. Immunol. 2001, 167:3300-3307.
28. Kusner D.J., Adams J. ATP-induced killing of virulent Mycobacterium tuberculosis within human macrophages requires phospholipase D. J. Immunol. 2000, 164:379-388.
29. Kusner D.J., Barton J.A. ATP stimulates human macrophages to kill intracellular virulent Mycobacterium tuberculosis via calcium-dependent phagosome-lysosome fusion. J. Immunol. 2001, 167:3308-3315.
30. Fuller S.J., Stokes L., Skarratt K.K., Gu B.J., Wiley J.S. Genetics of the P2X7 receptor and human disease. Purinergic Signal. 2009, 5:257-262.
31. Singla N., Gupta D., Joshi A., Batra N., Singh J. Genetic polymorphisms in the P2X7 gene and its association with susceptibility to tuberculosis. Int. J. Tuberc. Lung Dis. 2011.
32. Miller C.M., Boulter N.R., Fuller S.J., Zakrzewski A.M., Lees M.P., Saunders B.M., Wiley J.S., Smith N.C. The role of the P2X(7) receptor in infectious diseases. PLoS. Pathog. 2011, 7:e1002212.
33. Scott C.C., Botelho R.J., Grinstein S. Phagosome maturation: a few bugs in the system. J. Membr. Biol. 2003, 193:137-152.
34. Wyrick P.B. Intracellular survival by Chlamydia. Cell. Microbiol. 2000, 2:275-282.
35. Coutinho-Silva R., Perfettini J.-L., Persechini P.M., Dautry-Varsat A., Ojcius D.M. Modulation of P2Z/P2X7 receptor activity in macrophages infected with Chlamydia psittaci. Am. J. Physiol. 2001, 280:C81-C89.
36. Coutinho-Silva R., Stahl L., Raymond M.-N., Jungas T., Verbeke P., Burnstock G., Darville T., Ojcius D.M. Inhibition of chlamydial infectious activity due to P2X7R-dependent phospholipase D activation. Immunity 2003, 19:403-412.
37. Coutinho-Silva R., da Cruz C.M., Persechini P.M., Ojcius D.M. The role of P2 receptors in controlling infections by intracellular pathogens. Purinergic Signal. 2007, 3:83-90.
38. Darville T., Welter-Stahl L., Cruz C., Sater A.A., Andrews C.W., Ojcius D.M. Effect of the purinergic receptor P2X7 on Chlamydia infection in cervical epithelial cells and vaginally infected mice. J. Immunol. 2007, 179:3707-3714.
39. Solle M., Labasi J., Perregaux D.G., Stam E., Petrushova N., Koller B.H., Griffiths R.J., Gabel C.A. Altered cytokine production in mice Lacking P2X7 receptors. J. Biol. Chem. 2001, 276:125-132.
40. Said-Sadier N., Ojcius D.M. Alarmins. Inflammasomes Immun. 2012.
41. Abdul-Sater A.A., Said-Sadier N., Padilla E.V., Ojcius D.M. Chlamydial infection of monocytes stimulates IL-1beta secretion through activation of the NLRP3 inflammasome. Microbes Infect. 2010, 12:652-661.
42. Nagarajan U.M., Sikes J.D., Yeruva L., Prantner D. Significant role of IL-1 signaling, but Limited role of inflammasome activation, in oviduct Pathology during Chlamydia muridarum genital infection. J. Immunol. 2012, 188:2866-2875.
43. Shimada K., Crother T.R., Karlin J., Chen S., Chiba N., Ramanujan V.K., Vergnes L., Ojcius D.M., Arditi M. Caspase-1 dependent IL-1beta secretion is critical for host defense in a mouse model of Chlamydia pneumoniae lung infection. PLoS One 2011, 6:e21477.
44. He X., Mekasha S., Mavrogiorgos N., Fitzgerald K.A., Lien E., Ingalls R.R. Inflammation and fibrosis during Chlamydia pneumoniae infection is regulated by IL-1 and the NLRP3/ASC inflammasome. J. Immunol. 2010, 184:5743-5754.
45. Yilmaz O., Yao L., Maeda K., Rose T.M., Lewis E.L., Duman M., Lamont R.J., Ojcius D.M. ATP scavenging by the intracellular pathogen Porphyromonas gingivalis inhibits P2X7-mediated host-cell apoptosis. Cell. Microbiol. 2008, 10:863-875.
46. Spooner R., Yilmaz O. Nucleoside-diphosphate-kinase: a pleiotropic effector in microbial colonization under interdisciplinary characterization. Microbes Infect. 2012, 14:228-237.
47. Dar H.H., Prasad D., Varshney G.C., Chakraborti P.K. Secretory nucleoside diphosphate kinases from both intra- and extracellular pathogenic bacteria are functionally indistinguishable. Microbiology 2011, 157:3024-3035.
48. Yilmaz O., Sater A.A., Yao L., Koutouzis T., Pettengill M., Ojcius D.M. ATP-dependent activation of an inflammasome in primary gingival epithelial cells infected by Porphyromonas gingivalis. Cell. Microbiol. 2010, 12:188-198.
49. Darveau R.P. Periodontitis: a polymicrobial disruption of host homeostasis. Nat. Rev. Microbiol. 2010, 8:481-490.
50. Kelk P., Abd H., Claesson R., Sandstrom G., Sjostedt A., Johansson A. Cellular and molecular response of human macrophages exposed to Aggregatibacter actinomycetemcomitans leukotoxin. Cell Death. Dis. 2011, 2:e126.
51. + double-positive thymocytes in mice infected with Trypanosoma cruzi. Microbes Infect. 2003, 5:1363-1371.
52. Cascabulho C.M., Menna-Barreto R.F., Coutinho-Silva R., Persechini P.M., Henriques-Pons A. P2X7 modulatory web in Trypanosoma cruzi infection. Parasitol. Res. 2008, 103:829-838.
53. Meuser-Batista M., Correa J.R., Carvalho V.F., de Carvalho Britto C.F., da Cruz M.O., Batista M.M., Soares M.J., Filho F.A., Lannes-Vieira J., Coutinho-Silva R., Henriques-Pons A. Mast cell function and death in Trypanosoma cruzi infection. Am. J. Pathol. 2011, 179:1894-1904.
54. Moncao-Ribeiro L.C., Cagido V.R., Lima-Murad G., Santana P.T., Riva D.R., Borojevic R., Zin W.A., Cavalcante M.C., Rica I., Brando-Lima A.C., Takiya C.M., Faffe D.S., Coutinho-Silva R. Lipopolysaccharide-induced lung injury: role of P2X7 receptor. Respir. Physiol. Neurobiol. 2011.
55. Chaves S.P., Torres-Santos E.C., Marques C., Figliuolo V.R., Persechini P.M., Coutinho-Silva R., Rossi-Bergmann B. Modulation of P2X(7) purinergic receptor in macrophages by Leishmania amazonensis and its role in parasite elimination. Microbes Infect. 2009, 11:842-849.
56. Torres-Santos E.C., Mantuano M.B., Persechini P.M., Coutinho-Silva R., Rossi-Bergmann B. Enhanced macrophage permeabilization by ATP upon Leishmania infection. Drug Dev. Res. 2000, 50(1):61.
57. Marques-da-Silva C., Chaves M.M., Rodrigues J.C., Corte-Real S., Coutinho-Silva R., Persechini P.M. Differential modulation of ATP-Induced P2X7-Associated Permeabilities to cations and Anions of macrophages by infection with Leishmania amazonensis. PLoS One 2011, 6:e25356.
58. Kanneganti T.D., Lamkanfi M., Kim Y.G., Chen G., Park J.H., Franchi L., Vandenabeele P., Nunez G. Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling. Immunity 2007, 26:433-443.
59. Pelegrin P., Surprenant A. The P2X(7) receptor-pannexin connection to dye uptake and IL-1beta release. Purinergic Signal. 2009, 5:129-137.
60. Schroder K., Tschopp J. The inflammasomes. Cell 2010, 19(140):821-832.
61. Marques-da-Silva C., Chaves M.M., Chaves S.P., Figliuolo V.R., Meyer-Fernandes J.R., Corte-Real S., Lameu C., Ulrich H., Ojcius D.M., Rossi-Bergmann B., Coutinho-Silva R. Infection with Leishmania amazonensis upregulates purinergic receptor expression and induces host-cell susceptibility to UTP-mediated apoptosis. Cell. Microbiol. 2011, 13:1410-1428.
62. Almeida Marques-da-Silva E.de, de Oliveira J.C., Figueiredo A.B., de Souza Lima J.D., Carneiro C.M., Rangel Fietto J.L., Crocco Afonso L.C. Extracellular nucleotide metabolism in Leishmania: influence of adenosine in the establishment of infection. Microbes Infect. 2008, 10:850-857.
63. Figueiredo A.B., Serafim T.D., Marques-da-Silva E.A., Meyer-Fernandes J.R., Afonso L.C. Leishmania amazonensis impairs DC function by inhibiting CD40 expression via A(2B) adenosine receptor activation. Eur. J. Immunol. 2012, 42(5):1203-1215.
64. Mukbel R.M., Patten C., Gibson K., Ghosh M., Petersen C., Jones D.E. Macrophage killing of Leishmania amazonensis amastigotes requires both nitric oxide and superoxide. Am. J. Trop. Med. Hyg. 2007, 76:669-675.
65. Correa G., Marques da S.C., de Abreu Moreira-Souza A.C., Vommaro R.C., Coutinho-Silva R. Activation of the P2X(7) receptor triggers the elimination of Toxoplasma gondii tachyzoites from infected macrophages. Microbes Infect. 2010, 12:497-504.
66. Lees M.P., Fuller S.J., McLeod R., Boulter N.R., Miller C.M., Zakrzewski A.M., Mui E.J., Witola W.H., Coyne J.J., Hargrave A.C., Jamieson S.E., Blackwell J.M., Wiley J.S., Smith N.C. P2X7 receptor-mediated killing of an intracellular parasite, Toxoplasma gondii, by human and murine macrophages. J. Immunol. 2010, 184:7040-7046.
67. Jamieson S.E., Peixoto-Rangel A.L., Hargrave A.C., Roubaix L.A., Mui E.J., Boulter N.R., Miller E.N., Fuller S.J., Wiley J.S., Castellucci L., Boyer K., Peixe R.G., Kirisits M.J., Elias L.S., Coyne J.J., Correa-Oliveira R., Sautter M., Smith N.C., Lees M.P., Swisher C.N., Bahia-Oliveira L.M., McLeod R., Blackwell J.M. Evidence for associations between the purinergic receptor P2X(7) (P2RX7) and toxoplasmosis. Genes Immun. 2010, 11:374-383.
68. Spooner R., Yilmaz O. The role of reactive-oxygen-species in microbial persistence and inflammation. Int. J. Mol. Sci. 2011, 12:334-352.
69. Abdul-Sater A.A., Said-Sadier N., Ojcius D.M., Yilmaz O., Kelly K.A. Inflammasomes bridge signaling between pathogen identification and the immune response. Drugs Today (Barc.) 2009, 45(Suppl B):105-112.
70. Denis M., Ghadirian E. Interleukin-1 is involved in mouse resistance to Mycobacterium avium. Infect. Immun. 1994, 62:457-461.
71. Brown C.R., Hunter C.A., Estes R.G., Beckmann E., Forman J., David C., Remington J.S., McLeod R. Definitive identification of a gene that confers resistance against Toxoplasma cyst burden and encephalitis. Immunology 1995, 85:419-428.
72. Prantner D., Darville T., Sikes J.D., Andrews C.W., Brade H., Rank R.G., Nagarajan U.M. Critical role for interleukin-1beta (IL-1beta) during Chlamydia muridarum genital infection and bacterial replication-independent secretion of IL-1beta in mouse macrophages. Infect. Immun. 2009, 77:5334-5346.
73. Burnstock G., Verkhratsky A. Evolutionary origins of the purinergic signalling system. Acta Physiol. (Oxf) 2009, 195:415-447.
74. McCloskey M.A., Fan Y., Luther S. Chemotaxis of rat mast cells toward adenine nucleotides. J. Immunol. 1999, 163:970-977.
75. Moayeri M., Wickliffe K.E., Wiggins J.F., Leppla S.H. Oxidized ATP protection against anthrax lethal toxin. Infect. Immun. 2006, 74:3707-3714.
76. Ali S.R., Timmer A.M., Bilgrami S., Park E.J., Eckmann L., Nizet V., Karin M. Anthrax toxin induces macrophage death by p38 MAPK inhibition but leads to inflammasome activation via ATP leakage. Immunity 2011, 35:34-44.
77. Skals M., Jorgensen N.R., Leipziger J., Praetorius H.A. Alpha-hemolysin from Escherichia coli uses endogenous amplification through P2X receptor activation to induce hemolysis. Proc. Natl. Acad. Sci. U.S.A 2009, 106:4030-4035.
78. Skals M., Leipziger J., Praetorius H.A. Haemolysis induced by alpha-toxin from Staphylococcus aureus requires P2X receptor activation. Pflugers Arch. 2011, 462:669-679.
79. Kolli B.K., Kostal J., Zaborina O., Chakrabarty A.M., Chang K.P. Leishmania-released nucleoside diphosphate kinase prevents ATP-mediated cytolysis of macrophages. Mol. Biochem. Parasitol. 2008, 158:163-175.
80. Zaborina O., Li X., Cheng G., Kapatral V., Chakrabarty A.M. Secretion of ATP-utilizing enzymes, nucleoside diphosphate kinase and ATPase, by Mycobacterium bovis BCG: sequestration of ATP from macrophage P2Z receptors?. Mol. Microbiol. 1999, 31:1333-1343.
81. Nakaar V., Beckers C.J., Polotsky V., Joiner K.A. Basis for substrate specificity of the Toxoplasma gondii nucleoside triphosphate hydrolase. Mol. Biochem. Parasitol. 1998, 97:209-220.
82. Gan H., He X., Duan L., Mirabile-Levens E., Kornfeld H., Remold H.G. Enhancement of antimycobacterial activity of macrophages by stabilization of inner mitochondrial membrane potential. J. Infect. Dis. 2005, 191:1292-1300.
83. Pettengill M.A., Lam V.W., Ojcius D.M. The danger signal adenosine induces persistence of chlamydial infection through stimulation of A2b receptors. PLoS One 2009, 4:e8299.