Inhibitors of the 5-lipoxygenase arachidonic acid pathway induce ATP release and ATP-dependent organic cation transport in macrophages

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 7, 2014, Pages 1967-1977

  Da Silva Souza, Hercules Antônio ^a,b   Lira, Maria Nathalia De ^a,b   Costa Junior, Helio Miranda ^a   Da Cruz, Cristiane Monteiro ^a   Vasconcellos, Jorge Silvio Silva ^a   Mendes, Anderson Nogueira ^a   Pimenta Reis, Gabriela ^a,b   Alvarez, Cora Lilia ^a,b   Faccioli, Lucia Helena ^c   Serezani, Carlos Henrique ^d   Schachter, Julieta ^a,b   Persechini, Pedro Muanis ^a,b  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b Inst Nac de Ciencia e Tecnologia de Pesquisa Translacional em Saude e Ambiente da Regiao Amazonica INPeTAm   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

5 lipoxygenase inhibitors; ATP; Cation transporters; Macrophage; P2X7 receptor

Indexed keywords

3 [3 TERT BUTYLTHIO 1 (4 CHLOROBENZYL) 5 ISOPROPYL 2 INDOLYL] 2,2 DIMETHYLPROPIONIC ACID; ADENOSINE TRIPHOSPHATE; CALCIUM ION; ETHIDIUM; FLUORESCENT DYE; NORDIHYDROGUAIARETIC ACID; PURINERGIC P2X7 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CATION TRANSPORT; CONTROLLED STUDY; INTRACELLULAR SIGNALING; MACROPHAGE; MALE; MOUSE; NONHUMAN; P2X7 GENE; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL;

MUS;

5-LIPOXYGENASE INHIBITORS; ATP; CATION TRANSPORTERS; MACROPHAGE; P2X7 RECEPTOR;

ADENOSINE TRIPHOSPHATE; ANIMALS; ARACHIDONATE 5-LIPOXYGENASE; CALCIUM; CATIONS; ION TRANSPORT; LIPOXYGENASE INHIBITORS; MACROPHAGES; MICE; MICE, INBRED C57BL; PHOSPHOLIPASES A2; RECEPTORS, PURINERGIC P2X7;

EID: 84898760642     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.04.006     Document Type: Article

References (87)

1. F. Anselmi, V.H. Hernandez, G. Crispino, A. Seydel, S. Ortolano, S.D. Roper, N. Kessaris, W. Richardson, G. Rickheit, M.A. Filippov, H. Monyer, and F. Mammano ATP release through connexin hemichannels and gap junction transfer of second messengers propagate Ca2 + signals across the inner ear Proc. Natl. Acad. Sci. U. S. A. 105 2008 18770 18775
2. L. Antonioli, P. Pacher, E.S. Vizi, and G. Hasko CD39 and CD73 in immunity and inflammation Trends Mol. Med. 19 2013 355 367
3. S. Apasov, M. Koshiba, F. Redegeld, and M.V. Sitkovsky Role of extracellular ATP and P1 and P2 classes of purinergic receptors in T-cell development and cytotoxic T lymphocyte effector functions Immunol. Rev. 146 1995 5 19
4. M.A. Balboa, J. Balsinde, C.A. Johnson, and E.A. Dennis Regulation of arachidonic acid mobilization in lipopolysaccharide-activated P388D(1) macrophages by adenosine triphosphate J. Biol. Chem. 274 1999 36764 36768
5. N. Ballatori, and W. Wang Nordihydroguaiaretic acid depletes ATP and inhibits a swelling-activated, ATP-sensitive taurine channel Am. J. Physiol. 272 1997 C1429 C1436
6. A. Baroja-Mazo, M. Barbera-Cremades, and P. Pelegrin The participation of plasma membrane hemichannels to purinergic signaling Biochim. Biophys. Acta 1828 2012 79 93
7. C. Bhuvaneswaran, and K. Dakshinamurti Inhibition of electron and energy transfer in rat liver mitochondria by nordihydroguaiaretic acid Biochemistry 11 1972 85 91
8. K. Bishayee, and A.R. Khuda-Bukhsh 5-lipoxygenase antagonist therapy: a new approach towards targeted cancer chemotherapy Acta Biochim. Biophys. Sin. (Shanghai) 45 2013 709 719
9. G. Burnstock Discovery of purinergic signalling, the initial resistance and current explosion of interest Br. J. Pharmacol. 167 2012 238 255
10. G. Burnstock, T. Cocks, and R. Crowe Evidence for purinergic innervation of the anococcygeus muscle Br. J. Pharmacol. 64 1978 13 20 (Pubitemid 9021904)
11. S. Cankurtaran-Sayar, K. Sayar, and M. Ugur P2X7 receptor activates multiple selective dye-permeation pathways in RAW 264.7 and human embryonic kidney 293 cells Mol. Pharmacol. 76 2009 1323 1332
12. H.C. Chen, J. Xie, Z. Zhang, L.T. Su, L. Yue, and L.W. Runnels Blockade of TRPM7 channel activity and cell death by inhibitors of 5-lipoxygenase PLoS ONE 5 2010 e11161
13. J.S. Cheng, and C.R. Jan Effect of nordihydroguaiaretic acid on intracellular Ca(2 +) concentrations in hepatocytes Toxicol. In Vitro 16 2002 485 490
14. 2 and 5-lipoxygenase in macrophages Prostaglandins Other Lipid Mediat. 88 2009 51 61
15. H.M. Costa-Junior, F.S. Vieira, and R. Coutinho-Silva C terminus of the P2X7 receptor: treasure hunting Purinergic Signal 7 2011 7 19
16. R. Coutinho-Silva, and D.M. Ojcius Role of extracellular nucleotides in the immune response against intracellular bacteria and protozoan parasites Microbes Infect. 14 2012 1271 1277
17. R. Coutinho-Silva, J.-L. Perfettini, P.M. Persechini, A. Dautry-Varsat, and D.M. Ojcius Modulation of P2Z/P2X7 receptor activity in macrophages infected with Chlamydia psittaci Am. J. Physiol. Cell Physiol. 280 2001 C81 C89
18. R. Coutinho-Silva, and P.M. Persechini P2Z purinoceptor-associated pores induced by extracellular ATP in macrophages and J774 cells Am. J. Physiol. 273 1997 C1793 C1800
19. G.A. Czapski, K. Czubowicz, and R.P. Strosznajder Evaluation of the antioxidative properties of lipoxygenase inhibitors Pharmacol. Rep. 64 2012 1179 1188
20. M. Divangahi, D. Desjardins, C. Nunes-Alves, H.G. Remold, and S.M. Behar Eicosanoid pathways regulate adaptive immunity to Mycobacterium tuberculosis Nat. Immunol. 11 2010 751 758
21. G.R. Dubyak Both sides now: multiple interactions of ATP with pannexin-1 hemichannels. Focus on "A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP" Am. J. Physiol. Cell Physiol. 296 2009 C235 C241
22. G.R. Dubyak P2X7 receptor regulation of non-classical secretion from immune effector cells Cell. Microbiol. 14 2012 1697 1706
23. G.R. Dubyak, and C. El-Moatassim Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides Am. J. Physiol. 265 1993 C577 C606
24. C. Eder Mechanisms of interleukin-1beta release Immunobiology 214 2009 543 553
25. C. Eder Ion channels in monocytes and microglia/brain macrophages: promising therapeutic targets for neurological diseases J. Neuroimmunol. 224 2010 51 55
26. T.M. Egan, D.S. Samways, and Z. Li Biophysics of P2X receptors Pflugers Arch. 452 2006 501 512 (Pubitemid 44015087)
27. D. Ferrari, C. Pizzirani, E. Adinolfi, R.M. Lemoli, A. Curti, M. Idzko, E. Panther, and F. Di Virgilio The P2X7 receptor: a key player in IL-1 processing and release J. Immunol. 176 2006 3877 3883 (Pubitemid 44264361)
28. J. Fried, A.G. Perez, and B.D. Clarkson Rapid hypotonic method for flow cytofluorometry of monolayer cell cultures. Some pitfalls in staining and data analysis J. Histochem. Cytochem. 26 1978 921 933 (Pubitemid 9115928)
29. T. Fujiwara, N. Takami, Y. Misumi, and Y. Ikehara Nordihydroguaiaretic acid blocks protein transport in the secretory pathway causing redistribution of Golgi proteins into the endoplasmic reticulum J. Biol. Chem. 273 1998 3068 3075 (Pubitemid 28133962)
30. C.A. Gabel P2 purinergic receptor modulation of cytokine production Purinergic Signal 3 2007 27 38
31. A. Gombault, L. Baron, and I. Couillin ATP release and purinergic signaling in NLRP3 inflammasome activation Front. Immunol. 3 2012 414
32. R.J. Griffiths, E.J. Stam, J.T. Downs, and I.G. Otterness ATP induces the release of IL-1 from LPS-primed cells in vivo J. Immunol. 154 1995 2821 2828
33. A.N. Guerra, M.L. Gavala, H.S. Chung, and P.J. Bertics Nucleotide receptor signalling and the generation of reactive oxygen species Purinergic Signal 3 2007 39 51
34. A. Gugliucci, L. Ranzato, L. Scorrano, R. Colonna, V. Petronilli, C. Cusan, M. Prato, M. Mancini, F. Pagano, and P. Bernardi Mitochondria are direct targets of the lipoxygenase inhibitor MK886. A strategy for cell killing by combined treatment with MK886 and cyclooxygenase inhibitors J. Biol. Chem. 277 2002 31789 31795 (Pubitemid 34968984)
35. P.J. Hanley, M. Kronlage, C. Kirschning, R.A. Del, F. Di Virgilio, J. Leipziger, I.P. Chessell, S. Sargin, M.A. Filippov, O. Lindemann, S. Mohr, V. Koenigs, H. Schillers, M. Baehler, and A. Schwab Transient P2X7 receptor activation triggers macrophage death independent of TLR2/4, CASP1 AND PANX1 J. Biol. Chem. 287 2012 10650 10663
36. D.B. Hardy, L.E. Pereria, and K. Yang Prostaglandins and leukotriene B4 are potent inhibitors of 11beta-hydroxysteroid dehydrogenase type 2 activity in human choriocarcinoma JEG-3 cells Biol. Reprod. 61 1999 40 45 (Pubitemid 29295965)
37. K.A. Hogquist, M.A. Nett, E.R. Unanue, and D.D. Chaplin Interleukin 1 is processed and released during apoptosis Proc. Natl. Acad. Sci. U. S. A. 88 1991 8485 8489 (Pubitemid 21915381)
38. D.A. Hume Macrophages as APC and the dendritic cell myth J. Immunol. 181 2008 5829 5835
39. D.A. Hume, N. Mabbott, S. Raza, and T.C. Freeman Can DCs be distinguished from macrophages by molecular signatures? Nat. Immunol. 14 2013 187 189
40. W.G. Junger Immune cell regulation by autocrine purinergic signalling Nat. Rev. Immunol. 11 2011 201 212
41. A. Kawano, M. Tsukimoto, T. Noguchi, N. Hotta, H. Harada, T. Takenouchi, H. Kitani, and S. Kojima Involvement of P2X4 receptor in P2X7 receptor-dependent cell death of mouse macrophages Biochem. Biophys. Res. Commun. 419 2012 374 380
42. O. Leavy Innate immunity: Linking lipids and inflammasomes Nat. Rev. Immunol. 11 2011 368 369
43. Y. Ma, S. Adjemian, H. Yang, J.P. Catani, D. Hannani, I. Martins, M. Michaud, O. Kepp, A.Q. Sukkurwala, E. Vacchelli, L. Galluzzi, L. Zitvogel, and G. Kroemer ATP-dependent recruitment, survival and differentiation of dendritic cell precursors in the tumor bed after anticancer chemotherapy OncoImmunology 2 2013 e24568
44. A.B. Mackenzie, A. Surprenant, and R.A. North Functional and molecular diversity of purinergic ion channel receptors Ann. N. Y. Acad. Sci. 868 1999 716 729 (Pubitemid 29281190)
45. A. Mantovani, S.K. Biswas, M.R. Galdiero, A. Sica, and M. Locati Macrophage plasticity and polarization in tissue repair and remodelling J. Pathol. 229 2013 176 185
46. F. Marceau, M.T. Bawolak, R. Lodge, J. Bouthillier, A. Gagne-Henley, R.C. Gaudreault, and G. Morissette Cation trapping by cellular acidic compartments: beyond the concept of lysosomotropic drugs Toxicol. Appl. Pharmacol. 259 2012 1 12
47. C. Marques-da-Silva, M.M. Chaves, J.C. Rodrigues, S. Corte-Real, R. Coutinho-Silva, and P.M. Persechini Differential modulation of ATP-induced P2X7-associated permeabilities to cations and anions of macrophages by infection with Leishmania amazonensis PLoS ONE 6 2011 e25356
48. A. Molloy, P. Laochumroonvorapong, and G. Kaplan Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guerin J. Exp. Med. 180 1994 1499 1509
49. M. Murgia, P. Pizzo, T.H. Steinberg, and F. Di Virgilio Characterization of the cytotoxic effect of extracellular ATP in J774-mouse macrophages Biochem. J. 288 1992 897 901 (Pubitemid 23031772)
50. C. Nathan Secretory products of macrophages: twenty-five years on J. Clin. Invest. 122 2012 1189 1190
51. M. Nishikawa, T. Tanaka, and H. Hidaka Ca++-calmodulin-dependent phosphorylation and platelet secretion Nature 287 1980 863 865
52. P.C. Norris, and E.A. Dennis Omega-3 fatty acids cause dramatic changes in TLR4 and purinergic eicosanoid signaling Proc. Natl. Acad. Sci. U. S. A. 109 2012 8517 8522
53. R.A. North, and M.F. Jarvis P2X receptors as drug targets Mol. Pharmacol. 83 2012 759 769
54. A. O'Garra, and K.M. Murphy From IL-10 to IL-12: how pathogens and their products stimulate APCs to induce T(H)1 development Nat. Immunol. 10 2009 929 932
55. T. Ohtsuki, H. Tsuda, and C. Morimoto Good or evil: CD26 and HIV infection J. Dermatol. Sci. 22 2000 152 160 (Pubitemid 30068660)
56. D.E. Pafundo, O. Chara, M.P. Faillace, G. Krumschnabel, and P.J. Schwarzbaum Kinetics of ATP release and cell volume regulation of hyposmotically challenged goldfish hepatocytes Am. J. Physiol. Regul. Integr. Comp. Physiol. 294 2008 R220 R233
57. N.R. Patel, K. Swan, X. Li, S.D. Tachado, and H. Koziel Impaired M. tuberculosis-mediated apoptosis in alveolar macrophages from HIV + persons: potential role of IL-10 and BCL-3 J. Leukoc. Biol. 86 2009 53 60
58. P. Pelegrin Targeting interleukin-1 signaling in chronic inflammation: focus on P2X(7) receptor and Pannexin-1 Drug News Perspect. 21 2008 424 433
59. C. Pergola, and O. Werz 5-Lipoxygenase inhibitors: a review of recent developments and patents Expert. Opin. Ther. Pat. 20 2010 355 375
60. P.M. Persechini, R.C. Bisaggio, J.L. Alves-Neto, and R. Coutinho-Silva Extracellular ATP in the lymphohematopoietic system: P2Z purinoceptors and membrane permeabilization Braz. J. Med. Biol. Res. 31 1998 25 34 (Pubitemid 128524608)
61. M. Peters-Golden, and T.G. Brock 5-lipoxygenase and FLAP Prostaglandins Leukot. Essent. Fatty Acids 69 2003 99 109 (Pubitemid 36976166)
62. M. Peters-Golden, and W.R. Henderson Jr. Leukotrienes N. Engl. J. Med. 357 2007 1841 1854
63. R. Ramoner, C. Rieser, G. Bartsch, and M. Thurnher Nordihydroguaiaretic acid blocks secretory and endocytic pathways in human dendritic cells J. Leukoc. Biol. 64 1998 747 752 (Pubitemid 28555387)
64. A. Rayah, J.M. Kanellopoulos, and F. Di Virgilio P2 receptors and immunity Microbes Infect. 14 2012 1254 1262
65. S. Redpath, P. Ghazal, and N.R. Gascoigne Hijacking and exploitation of IL-10 by intracellular pathogens Trends Microbiol. 9 2001 86 92 (Pubitemid 32155327)
66. W.H. Reeves, P.Y. Lee, J.S. Weinstein, M. Satoh, and L. Lu Induction of autoimmunity by pristane and other naturally occurring hydrocarbons Trends Immunol. 30 2009 455 464
67. G.P. Rizzardi, L. Brown, B.E. Souberbielle, and A.G. Dalgleish An alternative to Cr-51 release assay for measurement of natural killer activity in HIV-infected patients AIDS 10 1996 676 678 (Pubitemid 26162998)
68. A. Rossi, C. Pergola, A. Koeberle, M. Hoffmann, F. Dehm, P. Bramanti, S. Cuzzocrea, O. Werz, and L. Sautebin The 5-lipoxygenase inhibitor, zileuton, suppresses prostaglandin biosynthesis by inhibition of arachidonic acid release in macrophages Br. J. Pharmacol. 161 2010 555 570
69. C.A. Rouzer, A.W. Ford-Hutchinson, H.E. Morton, and J.W. Gillard MK886 a potent and specific leukotriene biosynthesis inhibitor blocks and reverses the membrane association of 5-lipoxygenase in ionophore-challenged leukocytes J. Biol. Chem. 265 1990 1436 1442
70. D. Rudnicka, and O. Schwartz Intrusive HIV-1-infected cells Nat. Immunol. 10 2009 933 934
71. J. Schachter, A.P. Motta, A.S. Zamorano, H.A. Silva-Souza, M.Z.P. Guimaraes, and P.M. Persechini ATP-induced P2X7-associated uptake of large molecules involves distinct mechanisms for cations and anions in macrophages J. Cell Sci. 121 2008 3261 3270
72. C.N. Serhan, N. Chiang, and T.E. Van Dyke Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators Nat. Rev. Immunol. 8 2008 349 361 (Pubitemid 351595216)
73. M. Solle, J. Labasi, D.G. Perregaux, E. Stam, N. Petrushova, B.H. Koller, R.J. Griffiths, and C.A. Gabel Altered cytokine production in mice lacking P2X7 receptors J. Biol. Chem. 276 2001 125 132 (Pubitemid 32050297)
74. T.H. Steinberg, H.P. Buisman, S. Greenberg, F. Di Virgilio, and S.C. Silverstein Effects of extracellular ATP on mononuclear phagocytes Ann. N. Y. Acad. Sci. 603 1990 120 129
75. 4 - permeabilizes the plasma membrane of mouse macrophages to fluorescent dyes J. Biol. Chem. 262 1987 8884 8888
76. B.L. Strehler Bioluminescence assay: principles and practice Methods Biochem. Anal. 16 1968 99 181
77. 7) Science 272 1996 735 738
78. F.S. Sutterwala, Y. Ogura, and R.A. Flavell The inflammasome in pathogen recognition and inflammation J. Leukoc. Biol. 82 2007 259 264 (Pubitemid 47230635)
79. M. Tagaya, N. Henomatsu, T. Yoshimori, A. Yamamoto, Y. Tashiro, and S. Mizushima Inhibition of vesicle-mediated protein transport by nordihydroguaiaretic acid J. Biochem. 119 1996 863 869 (Pubitemid 26182367)
80. O. Thastrup, P.J. Cullen, B.K. Drobak, M.R. Hanley, and A.P. Dawson Thapsigargin, a tumor promoter, discharges intracellular Ca2 + stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase Proc. Natl. Acad. Sci. U. S. A. 87 1990 2466 2470
81. J. Tschopp, and K. Schroder NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production? Nat. Rev. Immunol. 10 2010 210 215
82. L. Ulmann, H. Hirbec, and F. Rassendren P2X4 receptors mediate PGE2 release by tissue-resident macrophages and initiate inflammatory pain EMBO J. 29 2010 2290 2300
83. J.L. Wang, H.J. Chang, L.L. Tseng, C.P. Liu, K.C. Lee, K.J. Chou, J.S. Cheng, Y.K. Lo, W. Su, Y.P. Law, W.C. Chen, R.C. Chan, and C.R. Jan Nordihydroguaiaretic acid elevates osteoblastic intracellular Ca2 + Pharmacol. Toxicol. 89 2001 301 305
84. C. Watts The endosome-lysosome pathway and information generation in the immune system Biochim. Biophys. Acta 1824 2011 14 21
85. T.A. Wynn, A. Chawla, and J.W. Pollard Macrophage biology in development, homeostasis and disease Nature 496 2013 445 455
86. W. Xu, P.A. Santini, J.S. Sullivan, B. He, M. Shan, S.C. Ball, W.B. Dyer, T.J. Ketas, A. Chadburn, L. Cohen-Gould, D.M. Knowles, A. Chiu, R.W. Sanders, K. Chen, and A. Cerutti HIV-1 evades virus-specific IgG2 and IgA responses by targeting systemic and intestinal B cells via long-range intercellular conduits Nat. Immunol. 10 2009 1008 1017
87. N. Zhang, D. Yang, H. Dong, Q. Chen, D.I. Dimitrova, T.J. Rogers, M. Sitkovsky, and J.J. Oppenheim Adenosine A2a receptors induce heterologous desensitization of chemokine receptors Blood 108 2006 38 44 (Pubitemid 43990610)