ATP-induced P2X7-associated uptake of large molecules involves distinct mechanisms for cations and anions in macrophages

Journal of Cell Science

Volumn 121, Issue 19, 2008, Pages 3261-3270

  Schachter, Julieta ^a   Motta, Andressa Piedade ^a   Zamorano, Aliane de Souza ^a   da Silva Souza, Hercules Antônio ^a   Guimarães, Marilia Zaluar P ^a   Persechini, Pedro Muanis ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Anion; ATP; Cation; Macrophage; P2 receptor; P2X7; Permeabilization; Pore

Indexed keywords

ADENOSINE TRIPHOSPHATE; PURINERGIC P2X7 RECEPTOR; ANION; CATION; COLORING AGENT; ETHIDIUM; LISSAMINE RHODAMINE B; NERVE PROTEIN; PURINERGIC P2 RECEPTOR; RHODAMINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANION TRANSPORT; ARTICLE; CALCIUM CELL LEVEL; CATION TRANSPORT; CELL ACTIVITY; CELL PERMEABILIZATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MACROPHAGE; MOUSE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; TEMPERATURE DEPENDENCE; TEMPERATURE SENSITIVITY; ANIMAL; CALCIUM SIGNALING; CELL LINE; CHANNEL GATING; CYTOLOGY; DIFFUSION; DRUG EFFECT; EXTRACELLULAR SPACE; ION TRANSPORT; METABOLISM; RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANIONS; CALCIUM SIGNALING; CATIONS; CELL LINE; COLORING AGENTS; DIFFUSION; ETHIDIUM; EXTRACELLULAR SPACE; HUMANS; ION CHANNEL GATING; ION TRANSPORT; MACROPHAGES; MICE; NERVE TISSUE PROTEINS; RATS; RECEPTORS, PURINERGIC P2; RHODAMINES;

EID: 55649094970     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.029991     Document Type: Article

References (57)

1. Adinolfi, E., Pizzirani, C., Idzko, M., Panther, E., Norgauer, J., Di Virgilio, F. and Ferrari, D. (2005). P2X7 receptor: death or life? Purinergic Signal. 1, 219-227.
2. Albuquerque, C., Oliveira, S. M., Coutinho-Silva, R., Oliveira-Castro, G. M. and Persechini, P. M. (1993). ATP- and UTP-induced currents in macrophages and macrophage-polykaryons. Am. J. Physiol. 265, C1663-C1673.
3. Alves, L. A., Coutinho-Silva, R., Persechini, P. M., Spray, D. C., Savino, W. and Campos-de-Carvalho, A. C. (1996). Are there functional gap junctions or junctional hemichannels in macrophages? Blood 88, 328-334.
4. Bao, L., Locovei, S. and Dahl, G. (2004). Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett. 572, 65-68.
5. Barbe, M. T., Monyer, H. and Bruzzone, R. (2006). Cell-cell communication beyond connexins: the pannexin channels. Physiol. 21, 103-114.
6. Bisaggio, R. C., Nihei, O. K., Persechini, P. M., Savino, W. and Alves, L. A. (2001). Characterization of P2 receptors in thymic epithelial cells. Cell. Mol. Biol. 47, 19-31.
7. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
8. Bruzzone, R., Barbe, M. T., Jakob, N. J. and Monyer, H. (2005). Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J. Neurochem. 92, 1033-1043.
9. Chessell, I. P., Simon, J., Hibell, A. D., Michel, A. D., Barnard, E. A. and Humphrey, P. P. (1998). Cloning and functional characterisation of the mouse P2X7 receptor. FEBS Lett. 439, 26-30.
10. Coutinho-Silva, R. and Persechini, P. M. (1997). P2Z purinoceptor-associated pores induced by extracellular ATP in macrophages and J774 cells. Am. J. Physiol. 273, C1793-C1800.
11. Coutinho-Silva, R., Stahl, L., Raymond, M.-N., Jungas, T., Verbeke, P., Burnstock, G., Darville, T. and Ojcius, D. M. (2003). Inhibition of chlamydial infectious activity due to P2X7R-dependent phospholipase D activation. Immunity 19, 403-412.
12. Di Virgillo, F., Chiozzi, P., Ferrari, D., Falzoni, S., Sanz, J. M., Morelli, A., Torboli, M., Bolognesi, G. and Baricordi, O. R. (2001). Nucleotide receptors: an emerging family of regulatory molecules in blood cells. Blood 97, 587-600.
13. Duan, S., Anderson, C. M., Keung, E. C., Chen, Y., Chen, Y. and Swanson, R. A. (2003). P2X7 receptor-mediated release of excitatory amino acids from astrocytes. J. Neurosci. 23, 1320-1328.
14. Dwyer, K. M., Deaglio, S., Gao, W., Friedman, D., Strom, T. B. and Robson, S. C. (2007). CD39 and control of cellular immune responses. Purinergic Signal. 3, 171-180.
15. Egan, T. M., Samways, D. S. and Li, Z. (2006). Biophysics of P2X receptors. Pflugers Arch. 452, 501-512.
16. Elliott, G. D., Liu, X. H., Cusick, J. L., Menze, M., Vincent, J., Witt, T., Hand, S. and Toner, M. (2006). Trehalose uptake through P2X(7) purinergic channels provides dehydration protection. Cryobiology 52, 114-127.
17. Erb, L., Liao, Z., Seye, C. I. and Weisman, G. A. (2006). P2 receptors: intracellular signaling. Pflugers Arch. 452, 552-562.
18. Faria, R. X., de Farias, F. P. and Alves, L. A. (2004). Are second messengers crucial for opening the pore associated with P2X7 receptor? Am. J. Physiol., Cell Physiol. 288, C260-C271.
19. Ferrari, D., la Sala, A., Chiozzi, P., Morelli, A., Falzoni, S., Girolomoni, G., Idzko, M., Dichmann, S., Norgauer, J. and Di Virgilio, F. (2000). The P2 purinergic receptors of human dendritic cells: identification and coupling to cytokine release. FASEB J. 14, 2466-2476.
20. Ferrari, D., Pizzirani, C., Adinolfi, E., Lemoli, R. M., Curti, A., Idzko, M., Panther, E. and Di Virgilio, F. (2006). The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 176, 3877-3883.
21. Fortes, F. S. A., Pecora, I. L., Persechini, P. M., Hurtado, S., Costa, V., Coutinho-Silva, R., Melo-Braga, M. B., Silva-Filho, F. C., Bisaggio, R. C., Pires-de-Farias, F. et al. (2004). Modulation of intercellular communication in macrophages: possible interactions between GAP junctions and P2 receptors. J. Cell Sci. 117, 4717-4726.
22. Garcia-Marcos, M., Pochet, S., Marino, A. and Dehaye, J. P. (2006). P2X(7) and phospholipid signalling: the search of the "missing link" in epithelial cells. Cell Signal. 18, 2098-2104.
23. Gibbons, S. J., Washburn, K. B. and Talamo, B. R. (2001). P2X7 receptors in rat parotid acinar cells: formation of large pores. J. Auton. Pharmacol. 21, 181-190.
24. Hamill, O. P., Marty, A., Neher, E., Sakmann, B. and Sigworth, F. J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Eur. J. Physiol. 391, 85-100.
25. Hibell, A. D., Thompson, K. M., Xing, M., Humphrey, P. P. and Michel, A. D. (2001). Complexities of measuring antagonist potency at P2X(7) receptor orthologs. J. Pharmacol. Exp. Ther. 296, 947-957.
26. Humphreys, B. D., Rice, J., Kertesy, S. B. and Dubyak, G. R. (2000). Stress-activated protein kinase/JNK activation and apoptotic induction by the macrophage P2X7 nucleotide receptor. J. Biol. Chem. 275, 26792-26798.
27. Iacobas, D. A., Suadicani, S. O., Iacobas, S., Chrisman, C., Cohen, M. A., Spray, D. C. and Scemes, E. (2007). Gap junction and purinergic P2 receptor proteins as a functional unit: insights from transcriptomics. J. Membr. Biol. 217, 83-91.
28. Kim, M., Jiang, L. H., Wilson, H. L., North, R. A. and Surprenant, A. (2001). Proteomic and functional evidence for a P2X(7) receptor signalling complex. EMBO J. 20, 6347-6358.
29. Kornbluth, R. S. and Stone, G. W. (2006). Immunostimulatory combinations: designing the next generation of vaccine adjuvants. J. Leukoc. Biol. 80, 1084-1102.
30. Locovei, S., Wang, J. and Dahl, G. (2006). Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett. 580, 239-244.
31. Locovei, S., Scemes, E., Qiu, F., Spray, D. C. and Dahl, G. (2007). Pannexin1 is part of the pore forming unit of the P2X(7) receptor death complex. FEBS Lett. 581, 483-488.
32. Mackenzie, A. B., Young, M. T., Adinolfi, E. and Surprenant, A. (2005). Pseudoapoptosis induced by brief activation of ATP-gated P2X7 receptors. J. Biol. Chem. 280, 33968-33976.
33. Mariathasan, S. and Monack, D. M. (2007). Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat. Rev. Immunol. 7, 31-40.
34. Monteiro-da-Cruz, C., Ventura, A. L., Schachter, J., Costa-Junior, H. M., Silva-Souza, H. A., Gomes, F. R., Coutinho-Silva, R., Ojcius, D. M. and Persechini, P. M. (2006). Activation of ERK1/2 by extracellular nucleotides in macrophages is mediated by multiple P2 receptors independently of P2X7-associated pore or channel formation. Br. J. Pharmacol. 147, 324-334.
35. Monteiro-da-Cruz, C., Rinna, A., Forman, H. J., Ventura, A. L., Persechini, P. M. and Ojcius, D. M. (2007). ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. J. Biol. Chem. 282, 2871-2879.
36. Munkonge, F., Alton, E. W., Andersson, C., Davidson, H., Dragomir, A., Edelman, A., Farley, R., Hjelte, L., McLachlan, G., Stern, M. et al. (2004). Measurement of halide efflux from cultured and primary airway epithelial cells using fluorescence indicators. J. Cyst. Fibros. 3, Suppl. 2, 171-176.
37. Murgia, M., Hanau, S., Pizzo, P., Rippa, M. and Di Virgilio, F. (1993). Oxidized ATP an irreversible inhibitor of macrophage purinergic P2Z receptor. J. Biol. Chem. 268, 8199-8203.
38. North, R. A. (2002). Molecular physiology of P2X receptors. Physiol. Rev. 82, 1013-1067.
39. Nuttle, L. C. and Dubyak, G. R. (1994). Differential activation of cation channels and non-selective pores by macrophage P-2Z purinergic receptors expressed in Xenopus oocytes. J. Biol. Chem. 269, 13988-13996.
40. Paukert, M., Hidayat, S. and Grunder, S. (2002). The P2X(7) receptor from Xenopus laevis: formation of a large pore in Xenopus oocytes. FEBS Lett. 513, 253-258.
41. Pelegrin, P. and Surprenant, A. (2006). Pannexin-1 mediates large pore formation and interleukin-1 beta release by the ATP-gated P2X(7) receptor. EMBO J. 25, 5071-5082.
42. Persechini, P. M., Bisaggio, R. C., Alves-Neto, J. L. and Coutinho-Silva, R. (1998). Extracellular ATP in the lymphohematopoietic system: P2Z purinoceptors and membrane permeabilization. Braz. J. Med. Biol. Res. 31, 25-34.
43. Pfeiffer, Z. A., Guerra, A. N., Hill, L. M., Gavala, M. L., Prabhu, U., Aga, M., Hall, D. J. and Bertics, P. J. (2007). Nucleotide receptor signaling in marine macrophages is linked to reactive oxygen species generation. Free Radic. Biol. Med. 42, 1506-1516.
44. Ralevic, V. and Burnstock, G. (1998). Receptors for purines and pyrimidines. Pharmacol. Rev. 50, 413-492.
45. Rassendren, F., Buell, G. N., Virginio, C., Collo, G., North, R. A. and Surprenant, A. (1997). The permeabilizing ATP receptor, P2X7. Cloning and expression of a human cDNA. J. Biol. Chem. 272, 5482-5486.
46. Riedel, T., Lozinsky, I., Schmalzing, G. and Markwardt, F. (2006). Kinetics of P2X7 receptor-operated single channels currents. Biophys. J. 92, 2377-2391.
47. Saez, J. C., Retamal, M. A., Basilio, D., Bukauskas, F. F. and Bennett, M. V. (2005). Connexin-based gap junction hemichannels: gating mechanisms. Biochim. Biophys. Acta 1711, 215-224.
48. Shestopalov, V. I. and Panchin, Y. (2009). Pannexins and gap junction protein diversity. Cell Mol. Life Sci. 65, 376-394.
49. 4permeabilizes the plasma membrane of mouse macrophages to fluorescent dyes. J. Biol. Chem. 262, 8884-8888.
50. Steinberg, T. H., Newman, A. S., Swanson, J. A. and Silverstein, S. C. (1987b). Macrophages possess probenecid-inhibitable organic anion transporters that remove fluorescent dyes from the cytoplasmic matrix. J. Cell Biol. 105, 2695-2702.
51. 2+ signaling. J. Neurosci. 26, 1378-1385.
52. Sub, B. C., Kim. J. S., Namgung, U., Ha, H. and Kim, K. T. (2001). P2X7 nucleotide receptor mediation of membrane pore formation and superoxide generation in human promyelocytes and neutrophils. J. Immunol. 166, 6754-6763.
53. 7). Science 272, 735-738.
54. Virginio, C., Church, D., North, R. A. and Surprenant, A. (1997). Effects of divalent cations, protons and calmidazolium at the rat P2X7 receptor. Neuropharmacology 36, 1285-1294.
55. Virginio, C., MacKenzie, A., North, R. A. and Surprenant, A. (1999). Kinetics of cell lysis, dye uptake and permeability changes in cells expressing the rat P2X7 receptor. J. Physiol. (Lond.) 519, 335-346.
56. Wang, J., Ma, M., Locovei, S., Keane, R. W. and Dahl, G. (2007). Modulation of membrane channel currents by gap junction protein mimetic peptides: size matters. Am. J. Physiol. Cell Physiol. 293, C1112-C1119.
57. +uptake-inhibition of fluxes by suramin. Arch. Biochem. Biophys. 305, 54-60.