Purinergic and calcium signaling in macrophage function and plasticity

Frontiers in Immunology

Volumn 5, Issue NOV, 2014, Pages

  Desai, Bimal N ^a   Leitinger, Norbert ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Calcium; Inflammasome activation; Inflammation; Macrophages; Purinergic receptors

Indexed keywords

ADENOSINE; CALCIUM CHANNEL; CATHEPSIN; CHEMOTACTIC FACTOR; CLUSTERIN; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; PURINERGIC P2Y RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1; VANILLOID RECEPTOR 2;

APOPTOSIS; ARTICLE; BACTERIAL CLEARANCE; CALCIUM SIGNALING; CELL MIGRATION; COUPLING FACTOR; DOWN REGULATION; DOWNSTREAM PROCESSING; ENTERITIS; EXTRACELLULAR SPACE; HUMAN; INFLAMMATORY DISEASE; INNATE IMMUNITY; MACROPHAGE FUNCTION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHAGOCYTOSIS; PHENOTYPIC PLASTICITY; PNEUMONIA; POTASSIUM TRANSPORT; RESPIRATORY TRACT INFLAMMATION; SEPSIS; SIGNAL TRANSDUCTION; TISSUE INJURY;

EID: 84919402274     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00580     Document Type: Article

References (80)

1. Junger WG. Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol (2011) 11(3):201-12. doi:10.1038/nri2938
2. Idzko M, Ferrari D, Eltzschig HK. Nucleotide signalling during inflammation. Nature (2014) 509(7500):310-7. doi:10.1038/nature13085
3. Coutinho-Silva R, Ojcius DM, Gorecki DC, Persechini PM, Bisaggio RC, Mendes AN, et al. Multiple P2X and P2Y receptor subtypes in mouse J774, spleen and peritoneal macrophages. Biochem Pharmacol (2005) 69(4):641-55. doi:10.1016/j.bcp.2004.11.012
4. Haynes SE, Hollopeter G, Yang G, Kurpius D, Dailey ME, Gan WB, et al. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci (2006) 9(12):1512-9. doi:10.1038/nn1805
5. Kronlage M, Song J, Sorokin L, Isfort K, Schwerdtle T, Leipziger J, et al. Autocrine purinergic receptor signaling is essential for macrophage chemotaxis. Sci Signal (2010) 3(132):ra55. doi:10.1126/scisignal.2000588
6. Falzoni S, Munerati M, Ferrari D, Spisani S, Moretti S, Di Virgilio F. The purinergic P2Z receptor of human macrophage cells. Characterization and possible physiological role. J Clin Invest (1995) 95(3):1207-16. doi:10.1172/JCI117770
7. Surprenant A, Rassendren F, Kawashima E, North RA, Buell G. The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science (1996) 272(5262):735-8. doi:10.1126/science.272.5262.735
8. Lazarowski ER. Vesicular and conductive mechanisms of nucleotide release. Purinergic Signal (2012) 8(3):359-73. doi:10.1007/s11302-012-9304-9
9. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature (2009) 461(7261):282-6. doi:10.1038/nature08296
10. Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER, et al. Pannexin 1 channels mediate 'find-me' signal release and membrane permeability during apoptosis. Nature (2010) 467(7317):863-7. doi:10.1038/nature09413
11. Piccini A, Carta S, Tassi S, Lasiglie D, Fossati G, Rubartelli A. ATP is released by monocytes stimulated with pathogen-sensing receptor ligands and induces IL-1beta and IL-18 secretion in an autocrine way. Proc Natl Acad Sci U S A (2008) 105(23):8067-72. doi:10.1073/pnas.0709684105
12. Asgari E, Le Friec G, Yamamoto H, Perucha E, Sacks SS, Kohl J, et al. C3a modulates IL-1beta secretion in human monocytes by regulating ATP efflux and subsequent NLRP3 inflammasome activation. Blood (2013) 122(20):3473-81. doi:10.1182/blood-2013-05-502229
13. Cowen DS, Lazarus HM, Shurin SB, Stoll SE, Dubyak GR. Extracellular adenosine triphosphate activates calcium mobilization in human phagocytic leukocytes and neutrophil/monocyte progenitor cells. J Clin Invest (1989) 83(5):1651-60. doi:10.1172/JCI114064
14. Honda S, Sasaki Y, Ohsawa K, Imai Y, Nakamura Y, Inoue K, et al. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci (2001) 21(6):1975-82.
15. Koizumi S, Shigemoto-Mogami Y, Nasu-Tada K, Shinozaki Y, Ohsawa K, Tsuda M, et al. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature (2007) 446(7139):1091-5. doi:10.1038/nature05704
16. Muller T, Robaye B, Vieira RP, Ferrari D, Grimm M, Jakob T, et al. The purinergic receptor P2Y2 receptor mediates chemotaxis of dendritic cells and eosinophils in allergic lung inflammation. Allergy (2010) 65(12):1545-53. doi:10.1111/j.1398-9995.2010.02426.x
17. Gudipaty L, Humphreys BD, Buell G, Dubyak GR. Regulation of P2X(7) nucleotide receptor function in human monocytes by extracellular ions and receptor density. Am J Physiol Cell Physiol (2001) 280(4):C943-53.
18. Le Feuvre RA, Brough D, Iwakura Y, Takeda K, Rothwell NJ. Priming of macrophages with lipopolysaccharide potentiates P2X7-mediated cell death via a caspase-1-dependent mechanism, independently of cytokine production. J Biol Chem (2002) 277(5):3210-8. doi:10.1074/jbc.M104388200
19. Gudipaty L, Munetz J, Verhoef PA, Dubyak GR. Essential role for Ca2+ in regulation of IL-1beta secretion by P2X7 nucleotide receptor in monocytes, macrophages, and HEK-293 cells. Am J Physiol Cell Physiol (2003) 285(2):C286-99. doi:10.1152/ajpcell.00070.2003
20. Kahlenberg JM, Dubyak GR. Mechanisms of caspase-1 activation by P2X7 receptor-mediated K+ release. Am J Physiol Cell Physiol (2004) 286(5):C1100-8. doi:10.1152/ajpcell.00494.2003
21. Kahlenberg JM, Lundberg KC, Kertesy SB, Qu Y, Dubyak GR. Potentiation of caspase-1 activation by the P2X7 receptor is dependent on TLR signals and requires NF-kappaB-driven protein synthesis. J Immunol (2005) 175(11):7611-22. doi:10.4049/jimmunol.175.11.7611
22. Qu Y, Ramachandra L, Mohr S, Franchi L, Harding CV, Nunez G, et al. P2X7 receptor-stimulated secretion of MHC class II-containing exosomes requires the ASC/NLRP3 inflammasome but is independent of caspase-1. J Immunol (2009) 182(8):5052-62. doi:10.4049/jimmunol.0802968
23. Weber FC, Esser PR, Muller T, Ganesan J, Pellegatti P, Simon MM, et al. Lack of the purinergic receptor P2X(7) results in resistance to contact hypersensitivity. J Exp Med (2010) 207(12):2609-19. doi:10.1084/jem.20092489
24. Wilhelm K, Ganesan J, Muller T, Durr C, Grimm M, Beilhack A, et al. Graft-versus-host disease is enhanced by extracellular ATP activating P2X7R. Nat Med (2010) 16(12):1434-8. doi:10.1038/nm.2242
25. Lucattelli M, Cicko S, Muller T, Lommatzsch M, De Cunto G, Cardini S, et al. P2X7 receptor signaling in the pathogenesis of smoke-induced lung inflammation and emphysema. Am J Respir Cell Mol Biol (2011) 44(3):423-9. doi:10.1165/rcmb.2010-0038OC
26. Kurashima Y, Amiya T, Nochi T, Fujisawa K, Haraguchi T, Iba H, et al. Extracellular ATP mediates mast cell-dependent intestinal inflammation through P2X7 purinoceptors. Nat Commun (2012) 3:1034. doi:10.1038/ncomms2023
27. Lopez-Castejon G, Theaker J, Pelegrin P, Clifton AD, Braddock M, Surprenant A. P2X(7) receptor-mediated release of cathepsins from macrophages is a cytokine-independent mechanism potentially involved in joint diseases. J Immunol (2010) 185(4):2611-9. doi:10.4049/jimmunol.1000436
28. Castrichini M, Lazzerini PE, Gamberucci A, Capecchi PL, Franceschini R, Natale M, et al. The purinergic P2x7 receptor is expressed on monocytes in Behcet's disease and is modulated by TNF-alpha. Eur J Immunol (2014) 44(1):227-38. doi:10.1002/eji.201343353
29. Baroja-Mazo A, Barbera-Cremades M, Pelegrin P. P2X7 receptor activation impairs exogenous MHC class I oligopeptides presentation in antigen presenting cells. PLoS One (2013) 8(8):e70577. doi:10.1371/journal.pone.0070577
30. Gavala ML, Liu YP, Lenertz LY, Zeng L, Blanchette JB, Guadarrama AG, et al. Nucleotide receptor P2RX7 stimulation enhances LPS-induced interferon-beta production in murine macrophages. J Leukoc Biol (2013) 94(4):759-68. doi:10.1189/jlb.0712351
31. Pelegrin P, Surprenant A. Dynamics of macrophage polarization reveal new mechanism to inhibit IL-1beta release through pyrophosphates. EMBO J (2009) 28(14):2114-27. doi:10.1038/emboj.2009.163
32. Randriamampita C, Trautmann A. Biphasic increase in intracellular calcium induced by platelet-activating factor in macrophages. FEBS Lett (1989) 249(2):199-206. doi:10.1016/0014-5793(89)80624-6
33. Randriamampita C, Bismuth G, Trautmann A. Ca(2+)-induced Ca2+ release amplifies the Ca2+ response elicited by inositol trisphosphate in macrophages. Cell Regul (1991) 2(7):513-22.
34. Hogan PG, Lewis RS, Rao A. Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol (2010) 28:491-533. doi:10.1146/annurev.immunol.021908.132550
35. Jin SW, Zhang L, Lian QQ, Yao SL, Wu P, Zhou XY, et al. Close functional coupling between Ca2+ release-activated Ca2+ channels and reactive oxygen species production in murine macrophages. Mediators Inflamm (2006) 2006(6):36192. doi:10.1155/MI/2006/36192
36. Gronski MA, Kinchen JM, Juncadella IJ, Franc NC, Ravichandran KS. An essential role for calcium flux in phagocytes for apoptotic cell engulfment and the anti-inflammatory response. Cell Death Differ (2009) 16(10):1323-31. doi:10.1038/cdd.2009.55
37. Nilius B, Szallasi A. Transient receptor potential channels as drug targets: from the science of basic research to the art of medicine. Pharmacol Rev (2014) 66(3):676-814. doi:10.1124/pr.113.008268
38. Yamamoto S, Shimizu S, Kiyonaka S, Takahashi N, Wajima T, Hara Y, et al. TRPM2-mediated Ca2+influx induces chemokine production in monocytes that aggravates inflammatory neutrophil infiltration. Nat Med (2008) 14(7):738-47. doi:10.1038/nm1758
39. Link TM, Park U, Vonakis BM, Raben DM, Soloski MJ, Caterina MJ. TRPV2 has a pivotal role in macrophage particle binding and phagocytosis. Nat Immunol (2010) 11(3):232-9. doi:10.1038/ni.1842
40. Di A, Nelson DJ, Bindokas V, Brown ME, Libunao F, Palfrey HC. Dynamin regulates focal exocytosis in phagocytosing macrophages. Mol Biol Cell (2003) 14(5):2016-28. doi:10.1091/mbc.E02-09-0626
41. Samie M, Wang X, Zhang X, Goschka A, Li X, Cheng X, et al. A TRP channel in the lysosome regulates large particle phagocytosis via focal exocytosis. Dev Cell (2013) 26(5):511-24. doi:10.1016/j.devcel.2013.08.003
42. Py BF, Jin M, Desai BN, Penumaka A, Zhu H, Kober M, et al. Caspase-11 controls interleukin-1beta release through degradation of TRPC1. Cell Rep (2014) 6(6):1122-8. doi:10.1016/j.celrep.2014.02.015
43. Alonso-Torre SR, Trautmann A. Calcium responses elicited by nucleotides in macrophages. Interaction between two receptor subtypes. J Biol Chem (1993) 268(25):18640-7.
44. Brough D, Le Feuvre RA, Wheeler RD, Solovyova N, Hilfiker S, Rothwell NJ, et al. Ca2+ stores and Ca2+ entry differentially contribute to the release of IL-1 beta and IL-1 alpha from murine macrophages. J Immunol (2003) 170(6):3029-36. doi:10.4049/jimmunol.170.6.3029
45. Hanley PJ, Musset B, Renigunta V, Limberg SH, Dalpke AH, Sus R, et al. Extracellular ATP induces oscillations of intracellular Ca2+ and membrane potential and promotes transcription of IL-6 in macrophages. Proc Natl Acad Sci U S A (2004) 101(25):9479-84. doi:10.1073/pnas.0400733101
46. del Rey A, Renigunta V, Dalpke AH, Leipziger J, Matos JE, Robaye B, et al. Knock-out mice reveal the contributions of P2Y and P2X receptors to nucleotide-induced Ca2+ signaling in macrophages. J Biol Chem (2006) 281(46):35147-55. doi:10.1074/jbc.M607713200
47. Zhou X, Yang W, Li J. Ca2+- and protein kinase C-dependent signaling pathway for nuclear factor-kappaB activation, inducible nitric-oxide synthase expression, and tumor necrosis factor-alpha production in lipopolysaccharide-stimulated rat peritoneal macrophages. J Biol Chem (2006) 281(42):31337-47. doi:10.1074/jbc.M602739200
48. Chun J, Prince A. Activation of Ca2+-dependent signaling by TLR2. J Immunol (2006) 177(2):1330-7. doi:10.4049/jimmunol.177.2.1330
49. Malik ZA, Thompson CR, Hashimi S, Porter B, Iyer SS, Kusner DJ. Cutting edge: Mycobacterium tuberculosis blocks Ca2+ signaling and phagosome maturation in human macrophages via specific inhibition of sphingosine kinase. J Immunol (2003) 170(6):2811-5. doi:10.4049/jimmunol.170.6.2811
50. Roy D, Liston DR, Idone VJ, Di A, Nelson DJ, Pujol C, et al. A process for controlling intracellular bacterial infections induced by membrane injury. Science (2004) 304(5676):1515-8. doi:10.1126/science.1098371
51. Czibener C, Sherer NM, Becker SM, Pypaert M, Hui E, Chapman ER, et al. Ca2+ and synaptotagmin VII-dependent delivery of lysosomal membrane to nascent phagosomes. J Cell Biol (2006) 174(7):997-1007. doi:10.1083/jcb.200605004
52. Canton J. Phagosome maturation in polarized macrophages. J Leukoc Biol (2014) 96(5):729-38. doi:10.1189/jlb.1MR0114-021R
53. Evans JH, Falke JJ. Ca2+ influx is an essential component of the positive-feedback loop that maintains leading-edge structure and activity in macrophages. Proc Natl Acad Sci U S A (2007) 104(41):16176-81. doi:10.1073/pnas.0707719104
54. Chen Y, Corriden R, Inoue Y, Yip L, Hashiguchi N, Zinkernagel A, et al. ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science (2006) 314(5806):1792-5. doi:10.1126/science.1132559
55. Idzko M, Hammad H, van Nimwegen M, Kool M, Willart MA, Muskens F, et al. Extracellular ATP triggers and maintains asthmatic airway inflammation by activating dendritic cells. Nat Med (2007) 13(8):913-9. doi:10.1038/nm1617
56. Kadl A, Meher AK, Sharma PR, Lee MY, Doran AC, Johnstone SR, et al. Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2. Circ Res (2010) 107(6):737-46. doi:10.1161/CIRCRESAHA.109.215715
57. Hogquist KA, Nett MA, Unanue ER, Chaplin DD. Interleukin 1 is processed and released during apoptosis. Proc Natl Acad Sci U S A (1991) 88(19):8485-9. doi:10.1073/pnas.88.19.8485
58. Perregaux D, Gabel CA. Interleukin-1 beta maturation and release in response to ATP and nigericin. Evidence that potassium depletion mediated by these agents is a necessary and common feature of their activity. J Biol Chem (1994) 269(21):15195-203.
59. Laliberte RE, Eggler J, Gabel CA. ATP treatment of human monocytes promotes caspase-1 maturation and externalization. J Biol Chem (1999) 274(52):36944-51. doi:10.1074/jbc.274.52.36944
60. Qu Y, Misaghi S, Newton K, Gilmour LL, Louie S, Cupp JE, et al. Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J Immunol (2011) 186(11):6553-61. doi:10.4049/jimmunol.1100478
61. Sawada K, Echigo N, Juge N, Miyaji T, Otsuka M, Omote H, et al. Identification of a vesicular nucleotide transporter. Proc Natl Acad Sci U S A (2008) 105(15):5683-6. doi:10.1073/pnas.0800141105
62. Sakaki H, Tsukimoto M, Harada H, Moriyama Y, Kojima S. Autocrine regulation of macrophage activation via exocytosis of ATP and activation of P2Y11 receptor. PLoS One (2013) 8(4):e59778. doi:10.1371/journal.pone.0059778
63. Csoka B, Selmeczy Z, Koscso B, Nemeth ZH, Pacher P, Murray PJ, et al. Adenosine promotes alternative macrophage activation via A2A and A2B receptors. FASEB J (2012) 26(1):376-86. doi:10.1096/fj.11-190934
64. Bouma MG, Stad RK, van den Wildenberg FA, Buurman WA. Differential regulatory effects of adenosine on cytokine release by activated human monocytes. J Immunol (1994) 153(9):4159-68.
65. Sajjadi FG, Takabayashi K, Foster AC, Domingo RC, Firestein GS. Inhibition of TNF-alpha expression by adenosine: role of A3 adenosine receptors. J Immunol (1996) 156(9):3435-42.
66. McWhinney CD, Dudley MW, Bowlin TL, Peet NP, Schook L, Bradshaw M, et al. Activation of adenosine A3 receptors on macrophages inhibits tumor necrosis factor-alpha. Eur J Pharmacol (1996) 310(2-3):209-16. doi:10.1016/0014-2999(96)00272-5
67. Baharav E, Bar-Yehuda S, Madi L, Silberman D, Rath-Wolfson L, Halpren M, et al. Antiinflammatory effect of A3 adenosine receptor agonists in murine autoimmune arthritis models. J Rheumatol (2005) 32(3):469-76.
68. Ohta A, Sitkovsky M. Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage. Nature (2001) 414(6866):916-20. doi:10.1038/414916a
69. Csoka B, Nemeth ZH, Virag L, Gergely P, Leibovich SJ, Pacher P, et al. A2A adenosine receptors and C/EBPbeta are crucially required for IL-10 production by macrophages exposed to Escherichia coli. Blood (2007) 110(7):2685-95. doi:10.1182/blood-2007-01-065870
70. Orr AG, Orr AL, Li XJ, Gross RE, Traynelis SF. Adenosine A(2A) receptor mediates microglial process retraction. Nat Neurosci (2009) 12(7):872-8. doi:10.1038/nn.2341
71. Schingnitz U, Hartmann K, Macmanus CF, Eckle T, Zug S, Colgan SP, et al. Signaling through the A2B adenosine receptor dampens endotoxin-induced acute lung injury. J Immunol (2010) 184(9):5271-9. doi:10.4049/jimmunol.0903035
72. Csoka B, Nemeth ZH, Rosenberger P, Eltzschig HK, Spolarics Z, Pacher P, et al. A2B adenosine receptors protect against sepsis-induced mortality by dampening excessive inflammation. J Immunol (2010) 185(1):542-50. doi:10.4049/jimmunol.0901295
73. Hasko G, Pacher P, Deitch EA, Vizi ES. Shaping of monocyte and macrophage function by adenosine receptors. Pharmacol Ther (2007) 113(2):264-75. doi:10.1016/j.pharmthera.2006.08.003
74. Ferrante CJ, Pinhal-Enfield G, Elson G, Cronstein BN, Hasko G, Outram S, et al. The adenosine-dependent angiogenic switch of macrophages to an M2-like phenotype is independent of interleukin-4 receptor alpha (IL-4Ralpha) signaling. Inflammation (2013) 36(4):921-31. doi:10.1007/s10753-013-9621-3
75. Koscso B, Csoka B, Kokai E, Nemeth ZH, Pacher P, Virag L, et al. Adenosine augments IL-10-induced STAT3 signaling in M2c macrophages. J Leukoc Biol (2013) 94(6):1309-15. doi:10.1189/jlb.0113043
76. Mediero A, Frenkel SR, Wilder T, He W, Mazumder A, Cronstein BN. Adenosine A2A receptor activation prevents wear particle-induced osteolysis. Sci Transl Med (2012) 4(135):135ra65. doi:10.1126/scitranslmed.3003393
77. Tanke T, van de Loo JW, Rhim H, Leventhal PS, Proctor RA, Bertics PJ. Bacterial lipopolysaccharide-stimulated GTPase activity in RAW 264.7 macrophage membranes. Biochem J (1991) 277(Pt 2):379-85.
78. Proctor RA, Denlinger LC, Leventhal PS, Daugherty SK, van de Loo JW, Tanke T, et al. Protection of mice from endotoxic death by 2-methylthio- ATP. Proc Natl Acad Sci U S A (1994) 91(13):6017-20. doi:10.1073/pnas.91.13.6017
79. Hu Y, Fisette PL, Denlinger LC, Guadarrama AG, Sommer JA, Proctor RA, et al. Purinergic receptor modulation of lipopolysaccharide signaling and inducible nitric-oxide synthase expression in RAW 264.7 macrophages. J Biol Chem (1998) 273(42):27170-5. doi:10.1074/jbc.273.42.27170
80. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, et al. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci (2005) 8(6):752-8. doi:10.1038/nn1472