Nucleotide receptor P2RX7 stimulation enhances LPS-induced interferon-β production in murine macrophages

Journal of Leukocyte Biology

Volumn 94, Issue 4, 2013, Pages 759-768

  Gavala, M L ^a   Liu, Y P ^a   Lenertz, L Y ^a   Zeng, L ^a   Blanchette, J B ^a   Guadarrama, A G ^a   Denlinger, L C ^a   Bertics, P J ^a   Smith, J A ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Endotoxin; Enhanceosome; Extracellular ATP; IRF 3; Type I IFN

Indexed keywords

ADENOSINE TRIPHOSPHATE; BETA INTERFERON; INTERFERON REGULATORY FACTOR 3; LIPOPOLYSACCHARIDE; PURINERGIC P2X7 RECEPTOR; PURINERGIC RECEPTOR; 3'-O-(4-BENZOYL)BENZOYLADENOSINE 5'-TRIPHOSPHATE; FOSB PROTEIN, MOUSE; IRF3 PROTEIN, MOUSE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NUCLEOTIDE; PROTEIN C FOS; PURINERGIC P2X RECEPTOR AGONIST; 3' O (4 BENZOYL)BENZOYLADENOSINE 5' TRIPHOSPHATE; DRUG DERIVATIVE; ENDOTOXIN; ENHANCEOSOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; INFLAMMATION; INTERFERON PRODUCTION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION REGULATION; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL LINE; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; PROMOTER REGION; SIGNAL TRANSDUCTION; DRUG EFFECT; EXTRACELLULAR ATP; IRF-3; TYPE I IFN;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL LINE; GENE EXPRESSION REGULATION; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; LIPOPOLYSACCHARIDES; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NUCLEOTIDES; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-FOS; PURINERGIC P2X RECEPTOR AGONISTS; RECEPTORS, PURINERGIC P2X7; RNA, MESSENGER;

ENDOTOXIN; ENHANCEOSOME; EXTRACELLULAR ATP; IRF-3; TYPE I IFN;

EID: 84884897686     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0712351     Document Type: Article

References (71)

1. Burnstock, G. (2006) Pathophysiology and therapeutic potential of purinergic signaling. Pharmacol. Rev. 58, 58-86.
2. Di Virgilio, F. (2007) Purinergic signalling in the immune system. A brief update. Purinergic Signal. 3, 1-3.
3. Khakh, B. S., North, R. A. (2006) P2X receptors as cell-surface ATP sensors in health and disease. Nature 442, 527-532.
4. Di Virgilio, F. (2005) Purinergic mechanism in the immune system: a signal of danger for dendritic cells. Purinergic Signal. 1, 205-209.
5. Lister, M. F., Sharkey, J., Sawatzky, D. A., Hodgkiss, J. P., Davidson, D. J., Rossi, A. G., Finlayson, K. (2007) The role of the purinergic P2X7 receptor in inflammation. J. Inflamm. (Lond.) 4, 5.
6. Sluyter, R., Stokes, L. (2011) Significance of P2X7 receptor variants to human health and disease. Recent Pat. DNA Gene Seq. 5, 41-54.
7. Labasi, J. M., Petrushova, N., Donovan, C., McCurdy, S., Lira, P., Payette, M. M., Brissette, W., Wicks, J. R., Audoly, L., Gabel, C. A. (2002) Absence of the P2X7 receptor alters leukocyte function and attenuates an inflammatory response. J. Immunol. 168, 6436-6445.
8. Dell'Antonio, G., Quattrini, A., Cin, E. D., Fulgenzi, A., Ferrero, M. E. (2002) Relief of inflammatory pain in rats by local use of the selective P2X7 ATP receptor inhibitor, oxidized ATP. Arthritis Rheum. 46, 3378-3385.
9. Dell'Antonio, G., Quattrini, A., Dal Cin, E., Fulgenzi, A., Ferrero, M. E. (2002) Antinociceptive effect of a new P(2Z)/P2X7 antagonist, oxidized ATP, in arthritic rats. Neurosci. Lett. 327, 87-90.
10. Peng, W., Cotrina, M. L., Han, X., Yu, H., Bekar, L., Blum, L., Takano, T., Tian, G. F., Goldman, S. A., Nedergaard, M. (2009) Systemic administration of an antagonist of the ATP-sensitive receptor P2X7 improves recovery after spinal cord injury. Proc. Natl. Acad. Sci. USA 106, 12489-12493.
11. Wang, L., Jacobsen, S. E., Bengtsson, A., Erlinge, D. (2004) P2 receptor mRNA expression profiles in human lymphocytes, monocytes and CD34+ stem and progenitor cells. BMC Immunol. 5, 16.
12. Portales-Cervantes, L., Nino-Moreno, P., Doniz-Padilla, L., Baranda-Candido, L., Garcia-Hernandez, M., Salgado-Bustamante, M., Gonzalez-Amaro, R., Portales-Perez, D. (2010) Expression and function of the P2X(7) purinergic receptor in patients with systemic lupus erythematosus and rheumatoid arthritis. Hum. Immunol. 71, 818-825.
13. Aga, M., Watters, J. J., Pfeiffer, Z. A., Wiepz, G. J., Sommer, J. A., Bertics, P. J. (2004) Evidence for nucleotide receptor modulation of cross talk between MAP kinase and NF-κ B signaling pathways in murine RAW 264.7 macrophages. Am. J. Physiol. Cell. Physiol. 286, C923-C930.
14. Guerra, A. N., Gavala, M. L., Chung, H. S., Bertics, P. J. (2007) Nucleotide receptor signalling and the generation of reactive oxygen species. Purinergic Signal. 3, 39-51.
15. Pfeiffer, Z. A., Guerra, A. N., Hill, L. M., Gavala, M. L., Prabhu, U., Aga, M., Hall, D. J., Bertics, P. J. (2007) Nucleotide receptor signaling in murine macrophages is linked to reactive oxygen species generation. Free Radic. Biol. Med. 42, 1506-1516.
16. Solle, M., Labasi, J., Perregaux, D. G., Stam, E., Petrushova, N., Koller, B. H., Griffiths, R. J., Gabel, C. A. (2001) Altered cytokine production in mice lacking P2X(7) receptors. J. Biol. Chem. 276, 125-132.
17. Watters, J., Sommer, J., Fisette, P., Pfeiffer, Z., Aga, M., Prabhu, U., Guerra, A., Denlinger, L., Bertics, P. (2001) P2X7 nucleotide receptor: modulation of LPS-induced macrophage signaling and mediator production. Drug Dev. Res. 53, 91-104.
18. Proctor, R. A., Denlinger, L. C., Leventhal, P. S., Daugherty, S. K., van de Loo, J. W., Tanke, T., Firestein, G. S., Bertics, P. J. (1994) Protection of mice from endotoxic death by 2-methylthio-ATP. Proc. Natl. Acad. Sci. USA 91, 6017-6020.
19. Hu, Y., Fisette, P. L., Denlinger, L. C., Guadarrama, A. G., Sommer, J. A., Proctor, R. A., Bertics, P. J. (1998) Purinergic receptor modulation of lipopolysaccharide signaling and inducible nitric-oxide synthase expression in RAW 264.7 macrophages. J. Biol. Chem. 273, 27170-27175.
20. Lenertz, L. Y., Gavala, M. L., Hill, L. M., Bertics, P. J. (2009) Cell signaling via the P2X(7) nucleotide receptor: linkage to ROS production, gene transcription, and receptor trafficking. Purinergic Signal. 5, 175-187.
21. Tonetti, M., Sturla, L., Giovine, M., Benatti, U., De Flora, A. (1995) Extracellular ATP enhances mRNA levels of nitric oxide synthase and TNF-α in lipopolysaccharide-treated RAW 264.7 murine macrophages. Biochem. Biophys. Res. Commun. 214, 125-130.
22. Ferrari, D., Pizzirani, C., Adinolfi, E., Lemoli, R. M., Curti, A., Idzko, M., Panther, E., Di Virgilio, F. (2006) The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 176, 3877-3883.
23. Denlinger, L. C., Angelini, G., Schell, K., Green, D. N., Guadarrama, A. G., Prabhu, U., Coursin, D. B., Bertics, P. J., Hogan, K. (2005) Detection of human P2X7 nucleotide receptor polymorphisms by a novel monocyte pore assay predictive of alterations in lipopolysaccharide-induced cytokine production. J. Immunol. 174, 4424-4431.
24. Andrei, C., Margiocco, P., Poggi, A., Lotti, L. V., Torrisi, M. R., Rubartelli, A. (2004) Phospholipases C and A2 control lysosome-mediated IL-1 β secretion: implications for inflammatory processes. Proc. Natl. Acad. Sci. USA 101, 9745-9750.
25. MacKenzie, A., Wilson, H. L., Kiss-Toth, E., Dower, S. K., North, R. A., Surprenant, A. (2001) Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity 15, 825-835.
26. Guerra, A. N., Fisette, P. L., Pfeiffer, Z. A., Quinchia-Rios, B. H., Prabhu, U., Aga, M., Denlinger, L. C., Guadarrama, A. G., Abozeid, S., Sommer, J. A., Proctor, R. A., Bertics, P. J. (2003) Purinergic receptor regulation of LPS-induced signaling and pathophysiology. J. Endotoxin Res. 9, 256-263.
27. Armstrong, S., Korcok, J., Sims, S. M., Dixon, S. J. (2007) Activation of transcription factors by extracellular nucleotides in immune and related cell types. Purinergic Signal. 3, 59-69.
28. Lenertz, L. Y., Gavala, M. L., Zhu, Y., Bertics, P. J. (2011) Transcriptional control mechanisms associated with the nucleotide receptor P2X7, a critical regulator of immunologic, osteogenic, and neurologic functions. Immunol. Res. 50, 22-38.
29. Bogdan, C. (2000) The function of type I interferons in antimicrobial immunity. Curr. Opin. Immunol. 12, 419-424.
30. Barton, G. M., Medzhitov, R. (2003) Linking Toll-like receptors to IFN-α/β expression. Nat. Immunol. 4, 432-433.
31. Gessani, S., Belardelli, F., Pecorelli, A., Puddu, P., Baglioni, C. (1989) Bacterial lipopolysaccharide and γ interferon induce transcription of β interferon mRNA and interferon secretion in murine macrophages. J. Virol. 63, 2785-2789.
32. Seong, S. Y., Matzinger, P. (2004) Hydrophobicity: an ancient damageassociated molecular pattern that initiates innate immune responses. Nat. Rev. Immunol. 4, 469-478.
33. Mancuso, G., Midiri, A., Biondo, C., Beninati, C., Zummo, S., Galbo, R., Tomasello, F., Gambuzza, M., Macri, G., Ruggeri, A., Leanderson, T., Teti, G. (2007) Type I IFN signaling is crucial for host resistance against different species of pathogenic bacteria. J. Immunol. 178, 3126-3133.
34. Karaghiosoff, M., Steinborn, R., Kovarik, P., Kriegshauser, G., Baccarini, M., Donabauer, B., Reichart, U., Kolbe, T., Bogdan, C., Leanderson, T., Levy, D., Decker, T., Muller, M. (2003) Central role for type I interferons and Tyk2 in lipopolysaccharide-induced endotoxin shock. Nat. Immunol. 4, 471-477.
35. Kim, J. H., Kim, S. J., Lee, I. S., Lee, M. S., Uematsu, S., Akira, S., Oh, K. I. (2009) Bacterial endotoxin induces the release of high mobility group box 1 via the IFN-β signaling pathway. J. Immunol. 182, 2458-2466.
36. Doyle, S., Vaidya, S., O'Connell, R., Dadgostar, H., Dempsey, P., Wu, T., Rao, G., Sun, R., Haberland, M., Modlin, R., Cheng, G. (2002) IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 17, 251-263.
37. Gavala, M. L., Pfeiffer, Z. A., Bertics, P. J. (2008) The nucleotide receptor P2RX7 mediates ATP-induced CREB activation in human and murine monocytic cells. J. Leukoc. Biol. 84, 1159-1171.
38. Takeshita, S., Kaji, K., Kudo, A. (2000) Identification and characterization of the new osteoclast progenitor with macrophage phenotypes being able to differentiate into mature osteoclasts. J. Bone Miner. Res. 15, 1477-1488.
39. Liu, Y. P., Zeng, L., Tian, A., Bomkamp, A., Rivera, D., Gutman, D., Barber, G. N., Olson, J. K., Smith, J. A. (2012) Endoplasmic reticulum stress regulates the innate immunity critical transcription factor IRF3. J. Immunol. 189, 4630-4639.
40. Zhao, W., Wang, L., Zhang, M., Wang, P., Zhang, L., Yuan, C., Qi, J., Qiao, Y., Kuo, P. C., Gao, C. (2011) Peroxisome proliferator-activated receptor γ negatively regulates IFN-β production in Toll-like receptor (TLR) 3-and TLR4-stimulated macrophages by preventing interferon regulatory factor 3 binding to the IFN-β promoter. J. Biol. Chem. 286, 5519-5528.
41. Di Virgilio, F., Baricordi, O. R., Romagnoli, R., Baraldi, P. G. (2005) Leukocyte P2 receptors: a novel target for anti-inflammatory and antitumor therapy. Curr. Drug Targets Cardiovasc. Haematol. Disord. 5, 85-99.
42. Denlinger, L. C., Sommer, J. A., Parker, K., Gudipaty, L., Fisette, P. L., Watters, J. W., Proctor, R. A., Dubyak, G. R., Bertics, P. J. (2003) Mutation of a dibasic amino acid motif within the C terminus of the P2X7 nucleotide receptor results in trafficking defects and impaired function. J. Immunol. 171, 1304-1311.
43. Gavala, M. L., Hill, L. M., Lenertz, L. Y., Karta, M. R., Bertics, P. J. (2010) Activation of the transcription factor FosB/activating protein-1 (AP-1) is a prominent downstream signal of the extracellular nucleotide receptor P2RX7 in monocytic and osteoblastic cells. J. Biol. Chem. 285, 34288-34298.
44. Yamamoto, M., Sato, S., Mori, K., Hoshino, K., Takeuchi, O., Takeda, K., Akira, S. (2002) Cutting edge: a novel Toll/IL-1 receptor domaincontaining adapter that preferentially activates the IFN-β promoter in the Toll-like receptor signaling. J. Immunol. 169, 6668-6672.
45. Fitzgerald, K. A., Rowe, D. C., Barnes, B. J., Caffrey, D. R., Visintin, A., Latz, E., Monks, B., Pitha, P. M., Golenbock, D. T. (2003) LPS-TLR4 signaling to IRF-3/7 and NF-κB involves the Toll adapters TRAM and TRIF. J. Exp. Med. 198, 1043-1055.
46. Clark, K., Peggie, M., Plater, L., Sorcek, R. J., Young, E. R., Madwed, J. B., Hough, J., McIver, E. G., Cohen, P. (2011) Novel cross-talk within the IKK family controls innate immunity. Biocheml. J. 434, 93-104.
47. Reimer, T., Schweizer, M., Jungi, T. W. (2007) Stimulation-specific contribution of p38 and JNK to IFN-β gene expression in human macrophages. J. Interferon Cytokine Res. 27, 751-755.
48. Wang, F., Ma, Y., Barrett, J. W., Gao, X., Loh, J., Barton, E., Virgin, H. W., McFadden, G. (2004) Disruption of Erk-dependent type I interferon induction breaks the myxoma virus species barrier. Nat. Immunol. 5, 1266-1274.
49. Kaiser, F., Cook, D., Papoutsopoulou, S., Rajsbaum, R., Wu, X., Yang, H. T., Grant, S., Ricciardi-Castagnoli, P., Tsichlis, P. N., Ley, S. C., O'Garra, A. (2009) TPL-2 negatively regulates interferon-β production in macrophages and myeloid dendritic cells. J. Exp. Med. 206, 1863-1871.
50. Yang, H. T., Wang, Y., Zhao, X., Demissie, E., Papoutsopoulou, S., Mambole, A., O'Garra, A., Tomczak, M. F., Erdman, S. E., Fox, J. G., Ley, S. C., Horwitz, B. H. (2011) NF-κB1 inhibits TLR-induced IFN-β production in macrophages through TPL-2-dependent ERK activation. J. Immunol. 186, 1989-1996.
51. Servant, M. J., Tenoever, B., Lin, R. (2002) Overlapping and distinct mechanisms regulating IRF-3 and IRF-7 function. J. Interferon Cytokine Res. 22, 49-58.
52. Solis, M., Romieu-Mourez, R., Goubau, D., Grandvaux, N., Mesplede, T., Julkunen, I., Nardin, A., Salcedo, M., Hiscott, J. (2007) Involvement of TBK1 and IKK∈ in lipopolysaccharide-induced activation of the interferon response in primary human macrophages. Eur. J. Immunol. 37, 528-539.
53. Reimer, T., Brcic, M., Schweizer, M., Jungi, T. W. (2008) Poly(I: C) and LPS induce distinct IRF3 and NF-κB signaling during type-I IFN and TNF responses in human macrophages. J. Leukoc. Biol. 83, 1249-1257.
54. Taniguchi, T., Takaoka, A. (2001) A weak signal for strong responses: interferon-α/β revisited. Nat. Rev. Mol. Cell Biol. 2, 378-386.
55. Chang, E. Y., Guo, B., Doyle, S. E., Cheng, G. (2007) Cutting edge: involvement of the type I IFN production and signaling pathway in lipopolysaccharide-induced IL-10 production. J. Immunol. 178, 6705-6709.
56. Watts III, B. A., George, T., Sherwood, E. R., Good, D. W. (2011) Basolateral LPS inhibits NHE3 and HCOFormula absorption through TLR4/ MyD88-dependent ERK activation in medullary thick ascending limb. Am. J. Physiol. Cell. Physiol. 301, C1296-C1306.
57. Koide, N., Ito, H., Mu, M. M., Sugiyama, T., Hassan, F., Islam, S., Mori, I., Yoshida, T., Yokochi, T. (2005) Inhibition of extracellular signal-regulated kinase 1/2 augments nitric oxide production in lipopolysaccharide-stimulated RAW264.7 macrophage cells. FEMS Immunol. Med. Microbiol. 45, 213-219.
58. Ferrari, D., Chiozzi, P., Falzoni, S., Dal Susino, M., Collo, G., Buell, G., Di Virgilio, F. (1997) ATP-mediated cytotoxicity in microglial cells. Neuropharmacology 36, 1295-1301.
59. Edwards, M. R., Slater, L., Johnston, S. L. (2007) Signalling pathways mediating type I interferon gene expression. Microbes Infect. 9, 1245-1251.
60. Cheng, C. S., Feldman, K. E., Lee, J., Verma, S., Huang, D. B., Huynh, K., Chang, M., Ponomarenko, J. V., Sun, S. C., Benedict, C. A., Ghosh, G., Hoffmann, A. (2011) The specificity of innate immune responses is enforced by repression of interferon response elements by NF-κB p50. Sci. Signl. 4, ra11.
61. Zhao, X., Ross, E. J., Wang, Y., Horwitz, B. H. (2012) Nfkb1 inhibits LPS-induced IFN-β and IL-12 p40 production in macrophages by distinct mechanisms. PloS One 7, e32811.
62. Takahasi, K., Horiuchi, M., Fujii, K., Nakamura, S., Noda, N. N., Yoneyama, M., Fujita, T., Inagaki, F. (2010) Ser386 phosphorylation of transcription factor IRF-3 induces dimerization and association with CBP/p300 without overall conformational change. Genes Cells 15, 901-910.
63. Chen, W., Srinath, H., Lam, S. S., Schiffer, C. A., Royer W. E., Jr., Lin, K. (2008) Contribution of Ser386 and Ser396 to activation of interferon regulatory factor 3. J. Mol. Biol. 379, 251-260.
64. Mori, M., Yoneyama, M., Ito, T., Takahashi, K., Inagaki, F., Fujita, T. (2004) Identification of Ser-386 of interferon regulatory factor 3 as critical target for inducible phosphorylation that determines activation. J. Biol. Chem. 279, 9698-9702.
65. Servant, M. J., Grandvaux, N., tenOever, B. R., Duguay, D., Lin, R., Hiscott, J. (2003) Identification of the minimal phosphoacceptor site required for in vivo activation of interferon regulatory factor 3 in response to virus and double-stranded RNA. J. Biol. Chem. 278, 9441-9447.
66. Sakaguchi, S., Negishi, H., Asagiri, M., Nakajima, C., Mizutani, T., Takaoka, A., Honda, K., Taniguchi, T. (2003) Essential role of IRF-3 in lipopolysaccharide-induced interferon-β gene expression and endotoxin shock. Biochem. Biophys. Res. Commun. 306, 860-866.
67. Shi, L., Manthei, D. M., Guadarrama, A. G., Lenertz, L. Y., Denlinger, L. C. (2012) Rhinovirus-induced IL-1β release from bronchial epithelial cells is independent of functional P2X7. Am. J. Respir. Cell Mol. Biol. 47, 363-371.
68. Denlinger, L. C., Shi, L., Guadarrama, A., Schell, K., Green, D., Morrin, A., Hogan, K., Sorkness, R. L., Busse, W. W., Gern, J. E. (2009) Attenuated P2X7 pore function as a risk factor for virus-induced loss of asthma control. Am. J. Respir. Crit. Care Med. 179, 265-270.
69. Deonarain, R., Alcami, A., Alexiou, M., Dallman, M. J., Gewert, D. R., Porter, A. C. (2000) Impaired antiviral response and α/β interferon induction in mice lacking β interferon. J. Virol. 74, 3404-3409.
70. Guile, S. D., Alcaraz, L., Birkinshaw, T. N., Bowers, K. C., Ebden, M. R., Furber, M., Stocks, M. J. (2009) Antagonists of the P2X(7) receptor. From lead identification to drug development. J. Med. Chem. 52, 3123-3141.
71. Van Holten, J., Smeets, T. J., Blankert, P., Tak, P. P. (2005) Expression of interferon β in synovial tissue from patients with rheumatoid arthritis: comparison with patients with osteoarthritis and reactive arthritis. Ann. Rheum. Dis. 64, 1780-1782.