P2X7 receptor-mediated killing of an intracellular parasite, Toxoplasma gondii, by human and murine macrophages

Journal of Immunology

Volumn 184, Issue 12, 2010, Pages 7040-7046

  Lees, Michael P ^a   Fuller, Stephen J ^b   McLeod, Rima ^d,e,f   Boulter, Nicola R ^a   Miller, Catherine M ^a   Zakrzewski, Alana M ^a   Mui, Ernest J ^d,e,f   Witola, William H ^d,e,f   Coyne, Jessica J ^d,e,f   Hargrave, Aubrey C ^d,e,f   Jamieson, Sarra E ^c   Blackwell, Jenefer M ^c   Wiley, James S ^b   Smith, Nicholas C ^a  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d UNIVERSITY OF CHICAGO   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

^f UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; PURINERGIC P2X7 RECEPTOR; NITRIC OXIDE; PURINERGIC P2 RECEPTOR;

ALLELE; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; EXTRAPULMONARY TUBERCULOSIS; HOST CELL; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; TOXOPLASMA GONDII; WILD TYPE; ANIMAL; BIOSYNTHESIS; CELL SEPARATION; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE; MOUSE MUTANT; TOXOPLASMA; TOXOPLASMOSIS;

ANIMALS; APOPTOSIS; CELL SEPARATION; FLOW CYTOMETRY; HUMANS; MACROPHAGES; MICE; MICE, KNOCKOUT; NITRIC OXIDE; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, PURINERGIC P2; TOXOPLASMA; TOXOPLASMOSIS; TOXOPLASMOSIS, ANIMAL;

EID: 77953631796     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000012     Document Type: Article

References (55)

1. 7 receptor: a pivotal role in inflammation and immunomodulation. Drug Dev. Res. 45: 207-213.
2. Molloy, A., P. Laochumroonvorapong, and G. Kaplan. 1994. Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular Bacillus Calmette-Guerin. J. Exp. Med. 180: 1499-1509.
3. Lammas, D. A., C. Stober, C. J. Harvey, N. Kendrick, S. Panchalingam, and D. S. Kumararatne. 1997. ATP-induced killing of mycobacteria by human macrophages ismediated by purinergic P2Z (P2X7) receptors. Immunity 7: 433-444.
4. Kusner, D. J., and J. Adams. 2000. ATP-induced killing of virulent Mycobacterium tuberculosis within human macrophages requires phospholipase D. J. Immunol. 164: 379-388.
5. Stober, C. B., D. A. Lammas, C. M. Li, D. K. Kumararatne, S. L. Lightman, and C. A. McArdle. 2001. 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. 166: 6276-6286.
6. 7- dependent process inducing bacterial death by phagosome-lysosome fusion. J. Immunol. 167: 3300-3307.
7. 7 receptor abolishes ATP-mediated killing of mycobacteria. J. Immunol. 171: 5442-5446.
8. 7 receptor on adenosine triphosphate-mediated killing of mycobacteria by human macrophages. J. Infect. Dis. 192: 149-155.
9. 7 function and impairs ATP-induced mycobacterial killing by macrophages. J. Biol. Chem. 281: 2079-2086.
10. Placido, R., G. Auricchio, S. Falzoni, L. Battistini, V. Colizzi, E. Brunetti, F. Di Virgilio, and G. Mancino. 2006. P2X7 purinergic receptors and extracellular ATP mediate apoptosis of human monocytes/macrophages infected with Mycobacterium tuberculosis reducing the intracellular bacterial viability. Cell. Immunol. 244: 10-18.
11. 7 gene increases susceptibility to extrapulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 175: 360-366.
12. 7 receptor activity in macrophages infected with Chlamydia psittaci. Am. J. Physiol. 280: C81-C89.
13. 7R-dependent phospholipase D activation. Immunity 19: 403-412.
14. 7 on Chlamydia infection in cervical epithelial cells and vaginally infected mice. J. Immunol. 179: 3707-3714.
15. 7 purinergic receptor in macrophages by Leishmania amazonensis and its role in parasite elimination. Microbes Infect. 11: 842-849.
16. 7 and NRAMP1/SLC11 A1 gene polymorphisms in Mexican mestizo subjects with pulmonary tuberculosis. Clin. Exp. Immunol. 148: 469-477.
17. McLeod, R., F. Kieffer, M. Sautter, T. Hosten, and H. Pelloux. 2009. Why prevent, diagnose and treat congenital toxoplasmosis? Mem. Inst. Oswaldo Cruz 104: 320-344.
18. McLeod, R., K. Boyer, T. Karrison, C. Swisher, N. Roizen, J. Jalbrzikowski, J. Remington, P. Heydemann, A. G. Noble, M. Mets, et al. 2006. Outcome of treatment for congenital toxoplasmosis, 1981-2004: the National Collaborative Chicago-based, Congenital Toxoplasmosis Study. Clin. Infect. Dis. 42: 1383-1394.
19. Jamieson, S. E., L.-A. de Roubaix, M. Cortina-Borja, H. K. Tan, E. J. Mui, H. J. Cordell, M. J. Kirisitis, E. N. Miller, C. S. Peacock, A. C. Hargrave, et al. 2008. Genetic and epigenetic factors at COL2A1 and ABCA4 influence clinical outcome in congenital toxoplasmosis. PLoS One 3: e2285.
20. Dobbin, C. A., N. C. Smith, and A. M. Johnson. 2002. Heat shock protein 70 is a potential virulence factor in murine Toxoplasma infection via modulation of host NF-kB and nitric oxide. J. Immunol. 169: 958-965.
21. Phinney, D. G., G. Kopen, R. L. Isaacson, and D. J. Prockop. 1999. Plastic adherent stromal cells from the bone marrow of commonly used strains of inbred mice: variations in yield, growth, and differentiation. J. Cell. Biochem. 72: 570-585.
22. Gubbels, M.-J., C. Li, and B. Striepen. 2003. High-throughput growth assay for Toxoplasma gondii using yellow fluorescent protein. Antimicrob. Agents Chemother. 47: 309-316.
23. Duke, R. C., R. Z. Witter, P. B. Nash, J. D. Young, and D. M. Ojcius. 1994. Cytolysis mediated by ionophores and pore-forming agents: role of intracellular calcium in apoptosis. FASEB J. 8: 237-246.
24. Borel, E., M. Mayencon, K. Kaiser, S. Picot, and F. Peyron. 1998. Fluorogenic detection of viable Toxoplasma gondii. Parasite 5: 371-373. (Pubitemid 128505085)
25. Abbasi, M., K. Kowalewski-Grochowska, M. A. Bahar, R. T. Kilani, B. Winkler- Lowen, and L. J. Guilbert. 2003. Infection of placental trophoblasts by Toxoplasma gondii. J. Infect. Dis. 188: 608-616.
26. Buffet, P. A., A. Sulahian, Y. J. F. Garin, N. Nassar, and F. Derouin. 1995. Culture microtitration: a sensitive method for quantifying Leishmania infantum in tissues of infected mice. Antimicrob. Agents Chemother. 39: 2167-2168.
27. Miller, C. M. D., C. Akratos, A. M. Johnson, and N. C. Smith. 2000. The production of a 70 kDa heat shock protein by Toxoplasma gondii RH strain in immunocompromised mice. Int. J. Parasitol. 30: 1467-1473.
28. Fuller, S. J., L. Stokes, K. K. Skarratt, B. J. Gu, and J. S. Wiley. 2009. Genetics of the P2X7 receptor and human disease. Purinergic Signal. 5: 257-262.
29. Adriouch, S., C. Dox, V. Welge, M. Seman, F. Koch-Noble, and F. Haag. 2002. A natural P451L mutation in the cytoplasmic domain impairs the function of the mouse P2X7 receptor. J. Immunol. 169: 4108-4112. (Pubitemid 35178179)
30. Le Stunff, H., R. Auger, J. Kanellopoulos, and M.-N. Raymond. 2004. The Pro- 451 to Leu polymorphism within the C-terminal tail of the P2X7 receptor impairs cell death but not phospholipase D activation in murine thymocytes. J. Biol. Chem. 279: 16918-16926.
31. Yip, L., T. Woehrle, R. Corriden, M. Hirsh, Y. Chen, Y. Inoue, V. Ferrari, P. A. Insel, and W. G. Junger. 2009. Autocrine regulation of T-cell activation by ATP release and P2X7 receptors. FASEB J. 23: 1685-1693.
32. Suadicani, S. O., R. Iglesias, D. C. Spray, and E. Scemes. 2009. Point mutation in the mouse P2X7 receptor affects intercellular calcium waves in astrocytes. ASN Neuro. 1. pii: e00005. DOI: 10.1042/AN20090001.
33. Aswad, F., and G. Dennert. 2006. P2X7 receptor expression levels determine lethal effects of a purine based danger signal in T lymphocytes. Cell. Immunol. 243: 58-65.
34. 7 receptor activation by extracellular nicotinamide adenine dinucleotide and ecto-ADP-ribosyltransferases in murine macrophages and T cells. J. Immunol. 183: 578-592.
35. + T cells determine cyst number in Toxoplasma gondii infection. J. Immunol. 145: 3438-3441.
36. Peng, B.-W., J. Lin, J.-Y. Lin, M.-S. Jiang, and T. Zhang. 2003. Exogenous nitric oxide induces apoptosis in Toxoplasma gondii tachyzoites via a calcium signal transduction pathway. Parasitology 126: 541-550.
37. Khakh, B. S., and R. A. North. 2006. P2X receptors as cell-surface ATP sensors in health and disease. Nature 442: 527-532.
38. Ferrari, D., S. Wesselborg, M. K. Bauer, and K. Schulze-Osthoff. 1997. Extracellular ATP activates transcription factor NF-kappaB through the P2Z purinoreceptor by selectively targeting NF-kappaBp65. J. Cell Biol. 139: 1635-1643. (Pubitemid 28079229)
39. Gargett, C. E., E. J. Cornish, and J. S. Wiley. 1996. Phospholipase D activation by P2Z purinoreceptor agonists in human lymphocytes is dependent on divalent cation influx. Biochem. J. 313: 529-535.
40. Gu, B. J., and J. S. Wiley. 2006. Rapid ATP-induced release of matrix metalloproteinase 9 is mediated by the P2X7 receptor. Blood 107: 4946-4952.
41. 7 receptor-induced IL-1β processing in human monocytes. J. Immunol. 180: 8410-8420.
42. Ferrari, D., M. Los, M. K. Bauer, P. Vandenabeele, S. Wesselborg, and K. Schulze-Osthoff. 1999. P2Z purinoreceptor ligation induces activation of caspases with distinct roles in apoptosis and necrotic alterations of cell death. FEBS Lett. 447: 71-75. (Pubitemid 29134951)
43. Sluyter, R., J. G. Dalitz, and J. S. Wiley. 2004. P2X7 receptor polymorphism impairs extracellular adenosine 5-triphosphate-induced interleukin-18 release from human monocytes. Genes Immun. 5: 588-591. (Pubitemid 39529976)
44. Sluyter, R., A. N. Shemon, and J. S. Wiley. 2004. Glu-496 Ala polymorphism in the P2X7 receptor impairs ATP-induced IL-1β release from human monocytes. J. Immunol. 172: 3399-3405.
45. Sibley, L. D., E. Weidner, and J. L. Krahenbuhl. 1985. Phagosome acidification blocked by intracellular Toxoplasma gondii. Nature 315: 416-419.
46. Sibley, L. D., J. L. Krahenbuhl, G. M. Adams, and E.Weidner. 1986. Toxoplasma modifies macrophage phagosomes by secretion of a vesicular network rich in surface proteins. J. Cell Biol. 103: 867-874.
47. Morisaki, J. H., J. E. Heuser, and L. D. Sibley. 1995. Invasion of Toxoplasma gondii occurs by active penetration of the host cell. J. Cell Sci. 108: 2457-2464.
48. 7 receptor differentially couples to distinct release pathways for IL-1β in mouse macrophages. J. Immunol. 180: 7147-7157.
49. Nash, P. B., M. B. Purner, R. P. Leon, P. Clarke, R. C. Duke, and T. J. Curiel. 1998. Toxoplasma gondii-infected cells are resistant to multiple inducers of apoptosis. J. Immunol. 160: 1824-1830.
50. Goebel, S., U. Gross, and C. G. Luder. 2001. Inhibition of host cell apoptosis by Toxoplasma gondii is accompanied by reduced activation of the caspase cascade and alterations of poly(ADP-ribose) polymerase expression. J. Cell Sci. 114: 3495-3505.
51. Payne, T. M., R. E. Molestina, and A. P. Sinai. 2003. Inhibition of caspase activation and a requirement for NF-kappaB function in the Toxoplasma gondii-mediated blockade of host apoptosis. J. Cell Sci. 116: 4345-4358.
52. Keller, P., F. Schaumburg, S. F. Fischer, G. Hacker, U. Gross, and C. G. Luder. 2006. Direct inhibition of cytochrome c-induced caspase activation in vitro by Toxoplasma gondii reveals novel mechanisms of interference with host cell apoptosis. FEMS Microbiol. Lett. 258: 312-319.
53. Vutova, P., M. Wirth, D. Hippe, U. Gross, K. Schulze-Osthoff, I. Schmitz, and C. G. Luder. 2007. Toxoplasma gondii inhibits Fas/CD95-triggered cell death by inducing aberrant processing and degradation of caspase 8. Cell. Microbiol. 9: 1556-1570.
54. Hippe, D., O. Lytocvchenko, I. Schmitz, and C. G. Luder. 2008. Fas/CD95- mediated apoptosis of type II cells is blocked by Toxoplasma gondii primarily via interference with the mitochondrial amplification loop. Infect. Immun. 76: 2905-2912.
55. Luder, C. G., R. R. Stanway, M. Chaussepied, G. Langsley, and V. T. Heussler. 2009. Intracellular survival of apicomplexan parasites and host cell modification. Int. J. Parasitol. 39: 163-173.