Nonclassical IL-1β Secretion Stimulated by P2X7 Receptors Is Dependent on Inflammasome Activation and Correlated with Exosome Release in Murine Macrophages

Qu, Yan; Franchi, Luigi; Nunez, Gabriel; Dubyak, George R

doi:10.4049/jimmunol.179.3.1913

Cited by 564Inflammasome and immune disordersAdenosine and Purinergic SignalingImmune Response and Inflammation

Nonclassical IL-1β Secretion Stimulated by P2X7 Receptors Is Dependent on Inflammasome Activation and Correlated with Exosome Release in Murine Macrophages

Qu, Yan, Franchi, Luigi, Nunez, Gabriel, Dubyak, George R·2007·The Journal of Immunology

DOI 10.4049/jimmunol.179.3.1913

Open this paper in CoChat — free account

Abstract

Several mechanistically distinct models of nonclassical secretion, including exocytosis of secretory lysosomes, shedding of plasma membrane microvesicles, and direct efflux through plasma membrane transporters, have been proposed to explain the rapid export of caspase-1-processed IL-1β from monocytes/macrophages in response to activation of P2X7 receptors (P2X7R) by extracellular ATP. We compared the contribution of these mechanisms to P2X7R-stimulated IL-1β secretion in primary bone marrow-derived macrophages isolated from wild-type, P2X7R knockout, or apoptosis-associated speck-like protein containing a C-terminal CARD knockout mice. Our experiments revealed the following: 1) a novel correlation between IL-1β secretion and the release of the MHC-II membrane protein, which is a marker of plasma membranes, recycling endosomes, multivesicular bodies, and released exosomes; 2) a common and absolute requirement for inflammasome assembly and active caspase-1 in triggering the cotemporal export of IL-1β and MHC-II; and 3) mechanistic dissociation of IL-1β export from either secretory lysosome exocytosis or plasma membrane microvesicle shedding on the basis of different requirements for extracellular Ca2+ and differential sensitivity to pharmacological agents that block activation of caspase-1 inflammasomes. Thus, neither secretory lysosome exocytosis nor microvesicle shedding models constitute the major pathways for nonclassical IL-1β secretion from ATP-stimulated murine macrophages. Our findings suggest an alternative model of IL-1β release that may involve the P2X7R-induced formation of multivesicular bodies that contain exosomes with entrapped IL-1β, caspase-1, and other inflammasome components.

Integrity signals

Registry

Crossref · 10.4049/jimmunol.179.3.1913

Cites

74 of 74 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Exocytosis of P2X7R-positive multivesicular bodies containing exosomes plays an important role in the release of IL-1β.
“Additionally, exocytosis of P2X7R-positive multivesicular bodies containing exosomes has also been reported to play an important role in the release of this cytokine (39).”
From Macrophage Cytokines: Involvement in Immunity and Infectious Diseases (2014) · cites this paper as [39]
The P2X7 receptor is a major activator of the NLRP3 inflammasome in several cell types, including macrophages and microglial cells.
“The P2X7 receptor is a major activator of the NLRP3 inflammasome in several cell types [16], including macrophages and microglial cells [72, 74–76].”
From Hyperactivation of P2X7 receptors as a culprit of COVID-19 neuropathology (2021) · cites this paper as [75]

The Inflammasome
Martinon, F., Burns, K., & Tschopp, J. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00599-3 · Cited by 6,066 · see citing works
Exosomes: composition, biogenesis and function
Théry, C., Zitvogel, L., & Amigorena, S. (2002) · Nature reviews. Immunology · doi:10.1038/nri855 · Cited by 5,355 · see citing works
Gout-associated uric acid crystals activate the NALP3 inflammasome
Martinon, F., Pétrilli, V., Mayor, A., Tardivel, A., & Tschopp, J. (2006) · Nature · doi:10.1038/nature04516 · Cited by 5,326 · see citing works
Biologic basis for interleukin-1 in disease.
Dinarello, C. (1996) · Blood · doi:10.1182/blood.v87.6.2095.bloodjournal8762095 · Cited by 3,380 · see citing works
Cryopyrin activates the inflammasome in response to toxins and ATP
Mariathasan, S., Weiss, D. S., Newton, K., McBride, J., O'Rourke, K., Roose-Girma, M., Lee, W. P., Weinrauch, Y., Monack, D. M., & Dixit, V. M. (2006) · Nature · doi:10.1038/nature04515 · Cited by 3,080 · see citing works
Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf
Mariathasan, S., Newton, K., Monack, D. M., Vucic, D., French, D. M., Lee, W. P., Roose-Girma, M., Erickson, S. L., & Dixit, V. M. (2004) · Nature · doi:10.1038/nature02664 · Cited by 1,822 · see citing works
Pannexin‐1 mediates large pore formation and interleukin‐1β release by the ATP‐gated P2X7 receptor
Pelegrı́n, P., & Surprenant, A. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601378 · Cited by 1,428 · see citing works
Mice deficient in IL-1β-converting enzyme are defective in production of mature IL-1β and resistant to endotoxic shock
Li, P., Allen, H., Banerjee, S., Franklin, S., Herzog, L., Johnston, C. G., McDowell, J., Paskind, M. P., Rodman, L., Salfeld, J. G., et al. (1995) · Cell · doi:10.1016/0092-8674(95)90490-5 · Cited by 1,408 · see citing works
Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3
Kanneganti, T., Özören, N., Body–Malapel, M., Amer, A. O., Park, J., Franchi, L., Whitfield, J. R., Barchet, W., Colonna, M., Vandenabeele, P., et al. (2006) · Nature · doi:10.1038/nature04517 · Cited by 1,149 · see citing works
Self-citation
Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1β in salmonella-infected macrophages
Franchi, L., Amer, A., Body-Malapel, M., Kanneganti, T.-D., Özören, N., Jagirdar, R., Inohara, N., Vandenabeele, P., Bertin, J., Coyle, A., et al. (2006) · Nature Immunology · doi:10.1038/ni1346 · Cited by 1,131 · see citing works
Self-citation
Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1β via Ipaf
Miao, E. A., Alpuche-Aranda, C. M., Dors, M., Clark, A. E., Bader, M. W., Miller, S. I., & Aderem, A. (2006) · Nature Immunology · doi:10.1038/ni1344 · Cited by 1,127 · see citing works
Plasma Membrane Repair Is Mediated by Ca2+-Regulated Exocytosis of Lysosomes
Reddy, A. J., Caler, E. V., & Andrews, N. W. (2001) · Cell · doi:10.1016/s0092-8674(01)00421-4 · Cited by 1,043 · see citing works
Exosomes: endosomal-derived vesicles shipping extracellular messages
Février, B., & Raposo, G. (2004) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2004.06.003 · Cited by 1,013 · see citing works
NOD-LRR PROTEINS: Role in Host-Microbial Interactions and Inflammatory Disease
Inohara, N., Chamaillard, M., McDonald, C., & Núñez, G. (2005) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.74.082803.133347 · Cited by 993 · see citing works
Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1
Sutterwala, F. S., Ogura, Y., Szczepanik, M., Lara-Tejero, M., Lichtenberger, G. S., Grant, E. P., Bertin, J., Coyle, A. J., Galán, J. E., Askenase, P. W., et al. (2006) · Immunity · doi:10.1016/j.immuni.2006.02.004 · Cited by 980 · see citing works
Altered Cytokine Production in Mice Lacking P2X7Receptors
Solle, M., Labasi, J. M., Perregaux, D. G., Stam, E. J., Petrushova, N., Koller, B. H., Griffiths, R., & Gabel, C. A. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m006781200 · Cited by 924 · see citing works
Exosomes: A Common Pathway for a Specialized Function
van Niel, G., Porto-Carreiro, I., Simoes, S., & Raposo, G. (2006) · The Journal of Biochemistry · doi:10.1093/jb/mvj128 · Cited by 922 · see citing works
Rapid Secretion of Interleukin-1β by Microvesicle Shedding
Mackenzie, A. B., Wilson, H. L., Kiss‐Toth, E., Dower, S., North, R. A., & Surprenant, A. (2001) · Immunity · doi:10.1016/s1074-7613(01)00229-1 · Cited by 862 · see citing works
Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain
Chessell, I. P., Hatcher, J. P., Bountra, C., Michel, A. D., Hughes, J. P., Green, P., Egerton, J., Murfin, M., Richardson, J. C., Peck, W. L., et al. (2005) · Pain · doi:10.1016/j.pain.2005.01.002 · Cited by 790 · see citing works
A novel secretory pathway for interleukin‐1 beta, a protein lacking a signal sequence.
Rubartelli, A., Cozzolino, F., Talio, M., & Sitia, R. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb08268.x · Cited by 780 · see citing works
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.
Perregaux, D. G., & Gabel, C. A. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)36591-2 · Cited by 760 · see citing works
NALPs: a novel protein family involved in inflammation
Tschopp, J., Martinon, F., & Burns, K. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1019 · Cited by 719 · see citing works
Critical Role for Cryopyrin/Nalp3 in Activation of Caspase-1 in Response to Viral Infection and Double-stranded RNA
Kanneganti, T., Body–Malapel, M., Amer, A. O., Park, J., Whitfield, J. R., Franchi, L., Taraporewala, Z. F., Miller, D. J., Patton, J. T., Inohara, N., et al. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m607594200 · Cited by 706 · see citing works
Self-citation
Secretory lysosomes
Blott, E. J., & Griffiths, G. M. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm732 · Cited by 686 · see citing works
Extracellular ATP triggers IL-1 beta release by activating the purinergic P2Z receptor of human macrophages
Ferrari, D., Chiozzi, P., Falzoni, S., Susino, M. D., Melchiorri, L., Baricordi, O. R., & Virgilio, F. D. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.159.3.1451 · Cited by 616 · see citing works
Astrocyte-Derived ATP Induces Vesicle Shedding and IL-1β Release from Microglia
Bianco, F., Pravettoni, E., Colombo, A., Schenk, U., Möller, T., Matteoli, M., & Verderio, C. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.11.7268 · Cited by 596 · see citing works
The PYRIN-CARD Protein ASC Is an Activating Adaptor for Caspase-1
Srinivasula, S. M., Poyet, J.-L., Razmara, M., Datta, P., Zhang, Z., & Alnemri, E. S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.c200179200 · Cited by 573 · see citing works
Lysosomes Behave as Ca2+-regulated Exocytic Vesicles in Fibroblasts and Epithelial Cells
Rodrı́guez, A., Webster, P. C., Ortego, J., & Andrews, N. W. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.137.1.93 · Cited by 532 · see citing works
Pannexin-1-Mediated Recognition of Bacterial Molecules Activates the Cryopyrin Inflammasome Independent of Toll-like Receptor Signaling
Kanneganti, T., Lamkanfi, M., Kim, Y., Chen, G., Park, J., Franchi, L., Vandenabeele, P., & Núñez, G. (2007) · Immunity · doi:10.1016/j.immuni.2007.03.008 · Cited by 526 · see citing works
Self-citation
Caspase-1 Activation of Lipid Metabolic Pathways in Response to Bacterial Pore-Forming Toxins Promotes Cell Survival
Gurcel, L., Abrami, L., Girardin, S. E., Tschopp, J., & van der Goot, F. G. (2006) · Cell · doi:10.1016/j.cell.2006.07.033 · Cited by 508 · see citing works
Absence of the P2X7 Receptor Alters Leukocyte Function and Attenuates an Inflammatory Response
Labasi, J. M., Petrushova, N., Donovan, C. B., McCurdy, S. P., Lira, P. D., Payette, M. M., Brissette, W. H., Wicks, J. R., Audoly, L., & Gabel, C. A. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.12.6436 · Cited by 490 · see citing works
The Secretory Route of the Leaderless Protein Interleukin 1β Involves Exocytosis of Endolysosome-related Vesicles
Andrei, C., Dazzi, C., Lotti, L. V., Torrisi, M. R., Chimini, G., & Rubartelli, A. (1999) · Molecular Biology of the Cell · doi:10.1091/mbc.10.5.1463 · Cited by 475 · see citing works
The Inflammasome: First Line of the Immune Response to Cell Stress
Ogura, Y., Sutterwala, F. S., & Flavell, R. A. (2006) · Cell · doi:10.1016/j.cell.2006.08.002 · Cited by 474 · see citing works
Identification of Ipaf, a Human Caspase-1-activating Protein Related to Apaf-1
Poyet, J., Srinivasula, S. M., Tnani, M., Razmara, M., Fernandes‐Alnemri, T., & Alnemri, E. S. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.c100250200 · Cited by 456 · see citing works
Regulation of Legionella Phagosome Maturation and Infection through Flagellin and Host Ipaf
Amer, A., Franchi, L., Kanneganti, T.-D., Body-Malapel, M., Özören, N., Brady, G., Meshinchi, S., Jagirdar, R., Gewirtz, A., Akira, S., et al. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m604933200 · Cited by 453 · see citing works
Self-citation
Phospholipases C and A 2 control lysosome-mediated IL-1β secretion: Implications for inflammatory processes
Andrei, C., Margiocco, P., Poggi, A. D., Lotti, L. V., Torrisi, M. R., & Rubartelli, A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308558101 · Cited by 409 · see citing works
Regulated secretion of conventional lysosomes
Andrews, N. W. (2000) · Trends in Cell Biology · doi:10.1016/s0962-8924(00)01794-3 · Cited by 354 · see citing works
Mechanisms of caspase-1 activation by P2X7 receptor-mediated K+ release
Kahlenberg, J. M., & Dubyak, G. (2004) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00494.2003 · Cited by 337 · see citing works
Self-citation
Pannexin-1 Couples to Maitotoxin- and Nigericin-induced Interleukin-1β Release through a Dye Uptake-independent Pathway
Pelegrı́n, P., & Surprenant, A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m610351200 · Cited by 301 · see citing works
Stimulation of P2 receptors causes release of IL-1β–loaded microvesicles from human dendritic cells
Pizzirani, C., Ferrari, D., Chiozzi, P., Adinolfi, E., Sandonà, D., Savaglio, E., & Virgilio, F. D. (2006) · Blood · doi:10.1182/blood-2005-06-031377 · Cited by 280 · see citing works
Potassium‐inhibited processing of IL‐1 beta in human monocytes.
Walev, I., Reske, K., Palmer, M., Valeva, A., & Bhakdi, S. C. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb07149.x · Cited by 278 · see citing works
Caspase-1-dependent processing of pro-interleukin-1β is cytosolic and precedes cell death
Brough, D., & Rothwell, N. J. (2007) · Journal of Cell Science · doi:10.1242/jcs.03377 · Cited by 265 · see citing works
Interleukin-1β Secretion Is Impaired by Inhibitors of the Atp Binding Cassette Transporter, ABC1
Hamon, Y., Luciani, M., Becq, F., Verrier, B., Rubartelli, A., & Chimini, G. (1997) · Blood · doi:10.1182/blood.v90.8.2911 · Cited by 224 · see citing works
Potentiation of Caspase-1 Activation by the P2X7 Receptor Is Dependent on TLR Signals and Requires NF-κB-Driven Protein Synthesis
Kahlenberg, J. M., Lundberg, K. C., Kertesy, S. B., Qu, Y., & Dubyak, G. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.11.7611 · Cited by 211 · see citing works
Self-citation
Activation of the Native 45-kDa Precursor Form of Interleukin-1-converting Enzyme
Yamin, T.-T., Ayala, J. M., & Miller, D. K. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.22.13273 · Cited by 198 · see citing works
Isolation and Culture of Murine Macrophages
Davies, J. Q., & Gordon, S. (2004) · Humana Press eBooks · doi:10.1385/1-59259-838-2:091 · Cited by 192 · see citing works
Priming of Macrophages with Lipopolysaccharide Potentiates P2X7-mediated Cell Death via a Caspase-1-dependent Mechanism, Independently of Cytokine Production
Feuvre, R. A. L., Brough, D., Iwakura, Y., Takeda, K., & Rothwell, N. J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m104388200 · Cited by 192 · see citing works
Epithelial Membrane Proteins Induce Membrane Blebbing and Interact with the P2X7 Receptor C Terminus
Wilson, H. L., Wilson, S. A., Surprenant, A., & North, R. A. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205120200 · Cited by 181 · see citing works
Pseudoapoptosis Induced by Brief Activation of ATP-gated P2X7 Receptors
Mackenzie, A. B., Young, M. T., Adinolfi, E., & Surprenant, A. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m502705200 · Cited by 174 · see citing works
P2X7 Receptor-Dependent Blebbing and the Activation of Rho-Effector Kinases, Caspases, and IL-1β Release
Verhoef, P. A., Estación, M., Schilling, W. P., & Dubyak, G. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.11.5728 · Cited by 173 · see citing works
Self-citation
Spontaneous Cell Fusion in Macrophage Cultures Expressing High Levels of the P2Z/P2X7 Receptor
Chiozzi, P., Sanz, J. M., Ferrari, D., Falzoni, S., Aleotti, A., Buell, G. N., Collo, G., & Virgilio, F. D. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.138.3.697 · Cited by 172 · see citing works
Ca2+ Stores and Ca2+ Entry Differentially Contribute to the Release of IL-1β and IL-1α from Murine Macrophages
Brough, D., Feuvre, R. A. L., Wheeler, R. D., Solovyova, N. A., Hilfiker, S., Rothwell, N. J., & Verkhratsky, A. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.6.3029 · Cited by 168 · see citing works
The nucleotide receptor P2X7 mediates actin reorganization and membrane blebbing in RAW 264.7 macrophages via p38 MAP kinase and Rho
Pfeiffer, Z. A., Aga, M., Prabhu, U., Watters, J. J., Hall, D. J., & Bertics, P. J. (2004) · Journal of Leukocyte Biology · doi:10.1189/jlb.1203648 · Cited by 159 · see citing works
Peripheral inflammation selectively increases TRPV1 function in IB4-positive sensory neurons from adult mouse
Breese, N. M., George, A., Pauers, L. E., & Stucky, C. L. (2005) · Pain · doi:10.1016/j.pain.2005.02.010 · Cited by 158 · see citing works
ATP-Induced Killing of Virulent Mycobacterium tuberculosis Within Human Macrophages Requires Phospholipase D
Kusner, D. J., & Adams, J. A. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.1.379 · Cited by 157 · see citing works
Histone deacetylase inhibitors prevent exocytosis of interleukin-1β-containing secretory lysosomes: role of microtubules
Carta, S., Tassi, S., Semino, C., Fossati, G., Mascagni, P., Dinarello, C. A., & Rubartelli, A. (2006) · Blood · doi:10.1182/blood-2006-03-014126 · Cited by 151 · see citing works
Exocytosis of active cathepsin B
Linebaugh, B. E., Sameni, M., Day, N. A., Sloane, B. F., & Keppler, D. (1999) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.1999.00582.x · Cited by 148 · see citing works
The immunogenicity of dendritic cell-derived exosomes
Quah, B., & O'Neill, H. C. (2005) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2005.05.002 · Cited by 147 · see citing works
ATP Treatment of Human Monocytes Promotes Caspase-1 Maturation and Externalization
Laliberte, R. E., Eggler, J. F., & Gabel, C. A. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.52.36944 · Cited by 138 · see citing works
IL-1 beta maturation: evidence that mature cytokine formation can be induced specifically by nigericin
Perregaux, D. G., Barberia, J. T., Lanzetti, A. J., Geoghegan, K. F., Carty, T. J., & Gabel, C. A. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.149.4.1294 · Cited by 135 · see citing works
Control of inflammatory pain by chemokine-mediated recruitment of opioid-containing polymorphonuclear cells
Brack, A., Rittner, H. L., Machelska, H., Leder, K., Mousa, S. A., Schäfer, M., & Stein, C. (2004) · Pain · doi:10.1016/j.pain.2004.08.029 · Cited by 126 · see citing works
Essential role for Ca2+ in regulation of IL-1β secretion by P2X7 nucleotide receptor in monocytes, macrophages, and HEK-293 cells
Gudipaty, L., Munetz, J., Verhoef, P. A., & Dubyak, G. (2003) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00070.2003 · Cited by 126 · see citing works
Self-citation
Inhibitory Effects of Chloride on the Activation of Caspase-1, IL-1β Secretion, and Cytolysis by the P2X7 Receptor
Verhoef, P. A., Kertesy, S. B., Lundberg, K. C., Kahlenberg, J. M., & Dubyak, G. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.11.7623 · Cited by 124 · see citing works
Self-citation
P2X7 Nucleotide Receptors Mediate Blebbing in Osteoblasts through a Pathway Involving Lysophosphatidic Acid
Panupinthu, N., Zhao, L., Possmayer, F., Ke, H. Z., Sims, S. M., & Dixon, S. J. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m605620200 · Cited by 123 · see citing works
Purification and characterization of active human interleukin-1 beta-converting enzyme from THP.1 monocytic cells.
Miller, D. K., Ayala, J. M., Egger, L. A., Raju, S. M., Yamin, T.-T., DING, G. J.-F., Gaffney, E. P., Howard, A. D., Palyha, O. C., & Rolando, A. M. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)46811-6 · Cited by 113 · see citing works
Potassium Regulates IL-1β Processing Via Calcium-Independent Phospholipase A2
Walev, I., Klein, J., Husmann, M., Valeva, A., Strauch, S., Wirtz, H., Weichel, O., & Bhakdi, S. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.10.5120 · Cited by 94 · see citing works
Interleukin Iβ and thioredoxin are secreted through a novel pathway of secretion
Rubartelli, A., & Sitia, R. (1991) · Biochemical Society Transactions · doi:10.1042/bst0190255 · Cited by 80 · see citing works
Involvement of the Purinergic P2X7 Receptor in the Formation of Multinucleated Giant Cells
Lemaire, I. B., Falzoni, S., Leduc, N., Zhang, B., Pellegatti, P., Adinolfi, E., Chiozzi, P., & Virgilio, F. D. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.10.7257 · Cited by 71 · see citing works
Human monocyte stimulus-coupled IL-1β posttranslational processing: modulation via monovalent cations
Perregaux, D. G., & Gabel, C. A. (1998) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1998.275.6.c1538 · Cited by 63 · see citing works
IL-1β: An endosomal exit
Wewers, M. D. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403971101 · Cited by 49 · see citing works
Knock-out Mice Reveal the Contributions of P2Y and P2X Receptors to Nucleotide-induced Ca2+ Signaling in Macrophages
del Rey, A., Renigunta, V., Dalpke, A. H., Leipziger, J., Matos, J., Robaye, B., Zuzarte, M., Kavelaars, A., & Hanley, P. J. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m607713200 · Cited by 48 · see citing works
Maitotoxin Induces Biphasic Interleukin-1β Secretion and Membrane Blebbing in Murine Macrophages
Verhoef, P. A., Kertesy, S. B., Estación, M., Schilling, W. P., & Dubyak, G. (2004) · Molecular Pharmacology · doi:10.1124/mol.66.4.909 · Cited by 47 · see citing works
Self-citation
Activation of ERK1/2 by extracellular nucleotides in macrophages is mediated by multiple P2 receptors independently of P2X7‐associated pore or channel formation
da Cruz, C. M., Ventura, A. L. M., Schachter, J., Costa‐Junior, H. M., Souza, H. A. D. S., Gomes, F. R., Coutinho‐Silva, R., Ojcius, D. M., & Persechini, P. M. (2005) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0706559 · Cited by 38 · see citing works
Identification of cytoskeletal [14C]carboplatin-binding proteins reveals reduced expression and disorganization of actin and filamin in cisplatin-resistant cell lines.
Shen, D., Liang, X., Gawinowicz, M. A., & Gottesman, M. M. (2004) · PubMed · doi:10.1124/mol.66.4 · Cited by 31 · see citing works
Self-citation

Flagged first, then by citations

1 of the 75 references couldn’t be matched to a known paper.

Sorted by citations

Biological properties of extracellular vesicles and their physiological functions
Yáñez‐Mó, M., Siljander, P. R. ‐., Andreu, Z., Bedina Zavec, A., Borràs, F. E., Buzas, E. I., Buzas, K., Casal, E., Cappello, F., Carvalho, J., et al. (2015) · Journal of Extracellular Vesicles · doi:10.3402/jev.v4.27066 · Cited by 5,926 · see citing works
Immunological and inflammatory functions of the interleukin-1 family
Dinarello, C. A. (2009) · Annual Review of Immunology · doi:10.1146/annurev.immunol.021908.132612 · Cited by 3,466 · see citing works
Pyroptosis: host cell death and inflammation
Bergsbaken, T., Fink, S. L., & Cookson, B. T. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2070 · Cited by 3,185 · see citing works
Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome
Nakahira, K., Haspel, J. A., Rathinam, V. A. K., Lee, S.-J., Dolinay, T., Lam, H. C., Englert, J. A., Rabinovitch, M., Cernadas, M., Kim, H. P., et al. (2011) · Nature Immunology · doi:10.1038/ni.1980 · Cited by 3,049 · see citing works
Macrophage Cytokines: Involvement in Immunity and Infectious Diseases
Arango Duque, G., & Descoteaux, A. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00491 · Cited by 2,708 · see citing works
Regulation of immune responses by extracellular vesicles
Robbins, P. D., & Morelli, A. E. (2014) · Nature Reviews Immunology · doi:10.1038/nri3622 · Cited by 2,260 · see citing works
Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles
György, B., Szabó, T. G., Pásztói, M., Pál, Z., Misják, P., Aradi, B., László, V., Pállinger, É., Pap, E., Kittel, Á., et al. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0689-3 · Cited by 2,075 · see citing works
Cytokines in Inflammatory Disease
Kany, S., Vollrath, J. T., & Relja, B. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20236008 · Cited by 2,027 · see citing works
Overview of the <scp>IL</scp> ‐1 family in innate inflammation and acquired immunity
Dinarello, C. A. (2018) · Immunological Reviews · doi:10.1111/imr.12621 · Cited by 1,866 · see citing works
Classification, Functions, and Clinical Relevance of Extracellular Vesicles
van der Pol, E., Böing, A. N., Harrison, P., Sturk, A., & Nieuwland, R. (2012) · Pharmacological Reviews · doi:10.1124/pr.112.005983 · Cited by 1,756 · see citing works
Depletion of microglia and inhibition of exosome synthesis halt tau propagation
Asai, H., Ikezu, S., Tsunoda, S., Medalla, M., Luebke, J., Haydar, T., Wolozin, B., Butovsky, O., Kügler, S., & Ikezu, T. (2015) · Nature Neuroscience · doi:10.1038/nn.4132 · Cited by 1,591 · see citing works
Understanding the mechanism of IL-1β secretion
Lopez-Castejon, G., & Brough, D. (2011) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2011.10.001 · Cited by 1,519 · see citing works
Innate Immune Pattern Recognition: A Cell Biological Perspective
Brubaker, S. W., Bonham, K. S., Zanoni, I., & Kagan, J. C. (2015) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032414-112240 · Cited by 1,475 · see citing works
The P2X7 Receptor in Infection and Inflammation
Di Virgilio, F., Dal Ben, D., Sarti, A. C., Giuliani, A. L., & Falzoni, S. (2017) · Immunity · doi:10.1016/j.immuni.2017.06.020 · Cited by 1,267 · see citing works
Anti-inflammatory Agents: Present and Future
Dinarello, C. A. (2010) · Cell · doi:10.1016/j.cell.2010.02.043 · Cited by 1,095 · see citing works
Innate immunity in the central nervous system
Ransohoff, R. M., & Brown, M. A. (2012) · Journal of Clinical Investigation · doi:10.1172/jci58644 · Cited by 1,034 · see citing works
IL‐1, IL‐18, and IL‐33 families of cytokines
Arend, W. P., Palmer, G., & Gabay, C. (2008) · Immunological Reviews · doi:10.1111/j.1600-065x.2008.00624.x · Cited by 912 · see citing works
Exosome-Mediated Transfer of miR-133b from Multipotent Mesenchymal Stromal Cells to Neural Cells Contributes to Neurite Outgrowth
Xin, H., Li, Y., Buller, B., Katakowski, M., Zhang, Y., Wang, X., Shang, X., Zhang, Z. G., & Chopp, M. (2012) · Stem Cells · doi:10.1002/stem.1129 · Cited by 897 · see citing works
Active Caspase-1 Is a Regulator of Unconventional Protein Secretion
Keller, M., Rüegg, A., Werner, S., & Beer, H. (2008) · Cell · doi:10.1016/j.cell.2007.12.040 · Cited by 851 · see citing works
The inflammasome: an integrated view
Gross, O., Thomas, C. J., Guarda, G., & Tschopp, J. (2011) · Immunological Reviews · doi:10.1111/j.1600-065x.2011.01046.x · Cited by 778 · see citing works
Exosomes and other extracellular vesicles in host–pathogen interactions
Schorey, J. S., Cheng, Y., Singh, P., & Smith, V. L. (2014) · EMBO Reports · doi:10.15252/embr.201439363 · Cited by 720 · see citing works
Mechanisms of regulated unconventional protein secretion
Nickel, W., & Rabouille, C. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2617 · Cited by 703 · see citing works
Emerging Roles of Exosomes in Normal and Pathological Conditions: New Insights for Diagnosis and Therapeutic Applications
Toro, J. D., Herschlik, L., Waldner, C., & Mongini, C. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00203 · Cited by 616 · see citing works
Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity
Lachenal, G. M., Pernet‐Gallay, K., Chivet, M., Hemming, F. J., Belly, A., Bodon, G., Blot, B., Haase, G., Goldberg, Y., & Sadoul, R. (2010) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2010.11.004 · Cited by 595 · see citing works
Acid sphingomyelinase activity triggers microparticle release from glial cells
Bianco, F., Perrotta, C., Novellino, L., Francolini, M., Riganti, L., Menna, E., Saglietti, L., Schuchman, E. H., Furlan, R., Clementi, E., et al. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.45 · Cited by 550 · see citing works
Microglial exosomes facilitate α-synuclein transmission in Parkinson’s disease
Guo, M., Wang, J., Zhao, Y., Feng, Y., Han, S., Dong, Q., Cui, M., & Tieu, K. (2020) · Brain · doi:10.1093/brain/awaa090 · Cited by 522 · see citing works
Exosomes: Small vesicles participating in intercellular communication
Ludwig, A., & Giebel, B. (2011) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2011.10.005 · Cited by 539 · see citing works
Therapeutic Applications of Extracellular Vesicles: Clinical Promise and Open Questions
György, B., Hung, M. E., Breakefield, X. O., & Leonard, J. N. (2014) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010814-124630 · Cited by 512 · see citing works
The multifaceted exosome: Biogenesis, role in normal and aberrant cellular function, and frontiers for pharmacological and biomarker opportunities
Pant, S., Hilton, H., & Burczynski, M. E. (2011) · Biochemical Pharmacology · doi:10.1016/j.bcp.2011.12.037 · Cited by 470 · see citing works
Exosomes: Looking back three decades and into the future
Harding, C. V., Heuser, J. E., & Stahl, P. D. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201212113 · Cited by 464 · see citing works
Neutrophil P2X7 receptors mediate NLRP3 inflammasome-dependent IL-1β secretion in response to ATP
Karmakar, M., Katsnelson, M. A., Dubyak, G. R., & Pearlman, E. (2016) · Nature Communications · doi:10.1038/ncomms10555 · Cited by 450 · see citing works
Self-citation
The Nlrp3 inflammasome is critical for aluminium hydroxide‐mediated IL‐1β secretion but dispensable for adjuvant activity
Franchi, L., & Núñez, G. (2008) · European Journal of Immunology · doi:10.1002/eji.200838549 · Cited by 452 · see citing works
Self-citation
Cold-inducible RNA-binding protein (CIRP) triggers inflammatory responses in hemorrhagic shock and sepsis
Qiang, X., Yang, W.-L., Wu, R., Zhou, M., Jacob, A., Dong, W., Kuncewitch, M., Ji, Y., Yang, H., Wang, H., et al. (2013) · Nature Medicine · doi:10.1038/nm.3368 · Cited by 441 · see citing works
Exosomes and Autophagy: Coordinated Mechanisms for the Maintenance of Cellular Fitness
Baixauli, F., López-Otı́n, C., & Mittelbrunn, M. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00403 · Cited by 443 · see citing works
The P2X7 Receptor in Inflammatory Diseases: Angel or Demon?
Savio, L. E. B., de Andrade Mello, P., da Silva, C. G., & Coutinho-Silva, R. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00052 · Cited by 437 · see citing works
The ins-and-outs of exosome biogenesis, secretion, and internalization
Arya, S. B., Collie, S. P., & Parent, C. A. (2023) · Trends in Cell Biology · doi:10.1016/j.tcb.2023.06.006 · Cited by 423 · see citing works
P2X7 Receptor Differentially Couples to Distinct Release Pathways for IL-1β in Mouse Macrophage
Pelegrı́n, P., Barroso-Gutierrez, C., & Surprenant, A. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.11.7147 · Cited by 413 · see citing works
Astrocytes as secretory cells of the central nervous system: idiosyncrasies of vesicular secretion
Verkhratsky, A., Matteoli, M., Parpura, V., Mothet, J., & Zorec, R. (2016) · The EMBO Journal · doi:10.15252/embj.201592705 · Cited by 397 · see citing works
Role of the inflammasome in acetaminophen-induced liver injury and acute liver failure
Woolbright, B. L., & Jaeschke, H. (2016) · Journal of Hepatology · doi:10.1016/j.jhep.2016.11.017 · Cited by 393 · see citing works
Translocation of interleukin-1β into a vesicle intermediate in autophagy-mediated secretion
Zhang, M., Kenny, S. J., Ge, L., Xu, K., & Schekman, R. W. (2015) · eLife · doi:10.7554/elife.11205 · Cited by 377 · see citing works
The IL-1 family of cytokines and receptors in rheumatic diseases
Dinarello, C. A. (2019) · Nature Reviews Rheumatology · doi:10.1038/s41584-019-0277-8 · Cited by 375 · see citing works
Malarial Hemozoin Activates the NLRP3 Inflammasome through Lyn and Syk Kinases
Shio, M. T., Eisenbarth, S. C., Savaria, M., Vinet, A. F., Bellemare, M.-J., Harder, K. W., Sutterwala, F. S., Bohle, D. S., Descoteaux, A., Flavell, R. A., et al. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000559 · Cited by 361 · see citing works
Pannexin-1 Is Required for ATP Release during Apoptosis but Not for Inflammasome Activation
Qu, Y., Misaghi, S., Newton, K., Gilmour, L. L., Louie, S., Cupp, J. E., Dubyak, G., Hackos, D. H., & Dixit, V. M. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1100478 · Cited by 365 · see citing works
Self-citation
Inflammasomes: current understanding and open questions
Bauernfeind, F. G., Ablasser, A., Bartok, E., Kim-Hellmuth, S., Schmid-Burgk, J. L., Cavlar, T., & Hornung, V. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0567-4 · Cited by 356 · see citing works
Extracellular vesicles in diagnostics and therapy of the ischaemic heart: Position Paper from the Working Group on Cellular Biology of the Heart of the European Society of Cardiology
Sluijter, J. P. G., Davidson, S. M., Boulanger, C. M., Buzás, E. I., de Kleijn, D. P. V., Engel, F. B., Giricz, Z., Hausenloy, D. J., Kishore, R., Lecour, S., et al. (2017) · Cardiovascular Research · doi:10.1093/cvr/cvx211 · Cited by 358 · see citing works
Mycobacterium tuberculosis protein ESAT-6 is a potent activator of the NLRP3/ASC inflammasome
Mishra, B. B., Moura‐Alves, P., Sonawane, A., Hacohen, N., Griffiths, G. W., Moita, L. F., & Anes, E. (2010) · Cellular Microbiology · doi:10.1111/j.1462-5822.2010.01450.x · Cited by 353 · see citing works
Inflammasomes: too big to miss
Stutz, A., Golenbock, D. T., & Latz, E. (2009) · Journal of Clinical Investigation · doi:10.1172/jci40599 · Cited by 345 · see citing works
Interleukin-1β and Cancer
Rébé, C., & Ghiringhelli, F. (2020) · Cancers · doi:10.3390/cancers12071791 · Cited by 342 · see citing works
IL-1F5, -F6, -F8, and -F9: A Novel IL-1 Family Signaling System That Is Active in Psoriasis and Promotes Keratinocyte Antimicrobial Peptide Expression
Johnston, A., Xing, X., Guzman, A. M., Riblett, M., Loyd, C. M., Ward, N. L., Wohn, C., Prens, E. P., Wang, F., Maier, L. E., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003162 · Cited by 319 · see citing works
Purinergic signalling and immune cells
Burnstock, G., & Boeynaems, J. M. (2014) · Purinergic Signalling · doi:10.1007/s11302-014-9427-2 · Cited by 310 · see citing works
Interleukin-33 – cytokine of dual function or novel alarmin?
Haraldsen, G., Balogh, J., Pollheimer, J., Sponheim, J., & Küchler, A. M. (2009) · Trends in Immunology · doi:10.1016/j.it.2009.03.003 · Cited by 309 · see citing works
Mechanisms of interleukin-1β release
Eder, C. (2009) · Immunobiology · doi:10.1016/j.imbio.2008.11.007 · Cited by 307 · see citing works
The IL-1 cytokine family and its role in inflammation and fibrosis in the lung
Borthwick, L. A. (2016) · Seminars in Immunopathology · doi:10.1007/s00281-016-0559-z · Cited by 294 · see citing works
Serum Amyloid A Activates the NLRP3 Inflammasome via P2X7 Receptor and a Cathepsin B-Sensitive Pathway
Niemi, K., Teirilä, L., Lappalainen, J., Rajamäki, K., Baumann, M. H., Öörni, K., Wolff, H., Kovanen, P. T., Matikainen, S., & Eklund, K. K. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1002843 · Cited by 298 · see citing works
Contributions of central and systemic inflammation to the pathophysiology of Parkinson's disease
Collins, L. M., Toulouse, A., Connor, T. J., & Nolan, Y. M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.01.028 · Cited by 275 · see citing works
A Translocation Pathway for Vesicle-Mediated Unconventional Protein Secretion
Zhang, M., Liu, L., Lin, X., Wang, Y., Li, Y., Guo, Q., Li, S., Sun, Y., Tao, X., Zhang, D., et al. (2020) · Cell · doi:10.1016/j.cell.2020.03.031 · Cited by 295 · see citing works
NLRP3/Cryopyrin Is Necessary for Interleukin-1β (IL-1β) Release in Response to Hyaluronan, an Endogenous Trigger of Inflammation in Response to Injury
Yamasaki, K., Muto, J., Taylor, K. R., Cogen, A. L., Audish, D., Bertin, J., Grant, E. P., Coyle, A. J., Misaghi, A., Hoffman, H. M., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m806084200 · Cited by 288 · see citing works
Inflammasome-dependent IL-1β release depends upon membrane permeabilisation
Martín‐Sánchez, F., Diamond, C. E., Zeitler, M., Gomez, A. I., Baroja‐Mazo, A., Bagnall, J., Spiller, D. G., White, M. H., Daniels, M. J. D., Mortellaro, A., et al. (2016) · Cell Death and Differentiation · doi:10.1038/cdd.2015.176 · Cited by 279 · see citing works
Diversity in unconventional protein secretion
Rabouille, C., Malhotra, V., & Nickel, W. (2012) · Journal of Cell Science · doi:10.1242/jcs.103630 · Cited by 278 · see citing works
K+ Efflux Agonists Induce NLRP3 Inflammasome Activation Independently of Ca2+ Signaling
Katsnelson, M. J., Rucker, L. G., Russo, H. M., & Dubyak, G. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402658 · Cited by 278 · see citing works
Self-citation
Focus on Extracellular Vesicles: Physiological Role and Signalling Properties of Extracellular Membrane Vesicles
Iraci, N., Leonardi, T., Gessler, F., Vega, B., & Pluchino, S. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17020171 · Cited by 301 · see citing works
Role of mitochondria ROS generation in ethanol-induced NLRP3 inflammasome activation and cell death in astroglial cells
Alfonso-Loeches, S., UreÃ±a-Peralta, J. R., Morillo-Bargues, M. J., Oliver-De La Cruz, J., & Guerri, C. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00216 · Cited by 265 · see citing works
Unconventional Mechanisms of Protein Transport to the Cell Surface of Eukaryotic Cells
Nickel, W., & Seedorf, M. (2008) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.24.110707.175320 · Cited by 259 · see citing works
Inflammasomes in Tissue Damages and Immune Disorders After Trauma
Bortolotti, P., Faure, E., & Kipnis, É. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01900 · Cited by 259 · see citing works
Potential Use of Exosomes as Diagnostic Biomarkers and in Targeted Drug Delivery: Progress in Clinical and Preclinical Applications
Huda, M. N., Nafiujjaman, M., Deaguero, I. G., Okonkwo, J., Hill, M. L., Kim, T. H., & Nurunnabi, M. (2021) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.1c00217 · Cited by 262 · see citing works
Host Matrix Modulation by Tumor Exosomes Promotes Motility and Invasiveness
Mu, W., Rana, S., & Zöller, M. (2013) · Neoplasia · doi:10.1593/neo.13786 · Cited by 248 · see citing works
TLR2/MyD88/NF-κB Pathway, Reactive Oxygen Species, Potassium Efflux Activates NLRP3/ASC Inflammasome during Respiratory Syncytial Virus Infection
Segovia, J. A., Sabbah, A., Mgbemena, V. E., Tsai, S.-Y., Chang, T.-H., Berton, M. T., Morris, I. R., Allen, I. C., Ting, J. P. ‐., & Bose, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029695 · Cited by 247 · see citing works
The Role of Reactive-Oxygen-Species in Microbial Persistence and Inflammation
Spooner, R., & Yilmaz, Ö. (2011) · International Journal of Molecular Sciences · doi:10.3390/ijms12010334 · Cited by 246 · see citing works
Exosome‐mediated inflammasome signaling after central nervous system injury
de Rivero Vaccari, J. P., Brand, F., Adamczak, S., Lee, S. W., Perez‐Barcena, J., Wang, M. Y., Bullock, M. R., Dietrich, W. D., & Keane, R. W. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13036 · Cited by 240 · see citing works
The NLRP3 and Pyrin Inflammasomes: Implications in the Pathophysiology of Autoinflammatory Diseases
de Torre‐Minguela, C., Mesa-del-Castillo, P., & Pelegrı́n, P. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00043 · Cited by 239 · see citing works
Diverse Activators of the NLRP3 Inflammasome Promote IL-1β Secretion by Triggering Necrosis
Cullen, S. P., Kearney, C. J., Clancy, D. M., & Martin, S. J. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.05.003 · Cited by 234 · see citing works
Microglia-neuron crosstalk: Signaling mechanism and control of synaptic transmission
Marinelli, S., Basilico, B., Marrone, M. C., & Ragozzino, D. (2019) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2019.05.017 · Cited by 233 · see citing works
Purinergic signaling in inflammatory cells: P2 receptor expression, functional effects, and modulation of inflammatory responses
Jacob, F., Perez-Novo, C. A., Bachert, C., & Crombruggen, K. V. (2013) · Purinergic Signalling · doi:10.1007/s11302-013-9357-4 · Cited by 232 · see citing works
Extracellular annexin A5: Functions of phosphatidylserine-binding and two-dimensional crystallization
van Genderen, H., Kenis, H., Hofstra, L., Narula, J., & Reutelingsperger, C. P. M. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2008.01.030 · Cited by 229 · see citing works
The Extracellular Vesicles of the Helminth Pathogen, Fasciola hepatica: Biogenesis Pathways and Cargo Molecules Involved in Parasite Pathogenesis*
Cwiklinski, K., de la Torre-Escudero, E., Trelis, M., Bernal, D., Dufresne, P. J., Brennan, G. P., O’Neill, S. M., Tort, J. F., Paterson, S., Marcilla, A., et al. (2015) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m115.053934 · Cited by 229 · see citing works
Nucleoside reverse transcriptase inhibitors possess intrinsic anti-inflammatory activity
Fowler, B. J., Gelfand, B. D., Kim, Y., Kerur, N., Tarallo, V., Hirano, Y., Amarnath, S., Fowler, D. H., Radwan, M., Young, M. T., et al. (2014) · Science · doi:10.1126/science.1261754 · Cited by 225 · see citing works
Inflammation and Immune Response in COPD: Where Do We Stand?
Rovina, N., Koutsoukou, A., & Koulouris, N. G. (2013) · Mediators of Inflammation · doi:10.1155/2013/413735 · Cited by 226 · see citing works
Alveolar macrophage-derived microvesicles mediate acute lung injury
Soni, S., Wilson, M. R., O'Dea, K. P., Yoshida, M., Katbeh, U., Woods, S. J., & Takata, M. (2016) · Thorax · doi:10.1136/thoraxjnl-2015-208032 · Cited by 209 · see citing works
Cytokine secretion in macrophages and other cells: Pathways and mediators
Stow, J. L., Low, P. C., Offenhäuser, C., & Sangermani, D. (2009) · Immunobiology · doi:10.1016/j.imbio.2008.11.005 · Cited by 205 · see citing works
Neutrophil pyroptosis: new perspectives on sepsis
Liu, L., & Sun, B. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03060-1 · Cited by 197 · see citing works
Lung inflammation caused by inhaled toxicants: A review
Wong, J., Magun, B., & Wood, L. (2016) · International Journal of Chronic Obstructive Pulmonary Disease · doi:10.2147/copd.s106009 · Cited by 193 · see citing works
P2X7 receptor regulation of non-classical secretion from immune effector cells
Dubyak, G. (2012) · Cellular Microbiology · doi:10.1111/cmi.12001 · Cited by 189 · see citing works
Self-citation
Colorectal cancer liver metastatic growth depends on PAD4-driven citrullination of the extracellular matrix
Yuzhalin, A. E., Gordon-Weeks, A. N., Tognoli, M. L., Jones, K. I., Markelc, B., Konietzny, R., Fischer, R., Muth, A., O’Neill, E. E., Thompson, P. R., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07306-7 · Cited by 189 · see citing works
A Novel Role for the NLRC4 Inflammasome in Mucosal Defenses against the Fungal Pathogen Candida albicans
Tomalka, J. A., Ganesan, S., Azodi, E., Patel, K., Majmudar, P. R., Hall, B. A., Fitzgerald, K. A., & Hise, A. G. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002379 · Cited by 184 · see citing works
Reverse of Age-Dependent Memory Impairment and Mitochondrial DNA Damage in Microglia by an Overexpression of Human Mitochondrial Transcription Factor A in Mice
Hayashi, Y., Yoshida, M., Yamato, M., Ide, T., Wu, Z., Ochi-Shindou, M., Kanki, T., Kang, D., Sunagawa, K., Tsutsui, H., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1957-08.2008 · Cited by 180 · see citing works
GSDMD is critical for autoinflammatory pathology in a mouse model of Familial Mediterranean Fever
Kanneganti, A., Malireddi, R. K. S., Saavedra, P. H. V., Walle, L. V., Gorp, H. V., Kambara, H., Sheppard, H., Vogel, P., Luo, H. R., Xavier, R. J., et al. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20172060 · Cited by 180 · see citing works
Unconventional Secretion, Unconventional Solutions
Zhang, M., & Schekman, R. W. (2013) · Science · doi:10.1126/science.1234740 · Cited by 179 · see citing works
Pathways of unconventional protein secretion
Nickel, W. (2010) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2010.06.004 · Cited by 177 · see citing works
Unconventional protein secretion
Ding, Y., Wang, J., Wang, J., Stierhof, Y., Robinson, D. G., & Jiang, L. (2012) · Trends in Plant Science · doi:10.1016/j.tplants.2012.06.004 · Cited by 176 · see citing works
Modulation of P2X4/P2X7/Pannexin-1 sensitivity to extracellular ATP via Ivermectin induces a non-apoptotic and inflammatory form of cancer cell death
Draganov, D., Gopalakrishna-Pillai, S., Chen, Y.-R., Zuckerman, N. S., Moeller, S., Wang, C., Ann, D. K., & Lee, P. P. (2015) · Scientific Reports · doi:10.1038/srep16222 · Cited by 175 · see citing works
Two haplotypes of the P2X 7 receptor containing the Ala‐348 to Thr polymorphism exhibit a gain‐of‐function effect and enhanced interleukin‐1β secretion
Stokes, L., Fuller, S. J., Sluyter, R., Skarratt, K. K., Gu, B. J., & Wiley, J. S. (2010) · The FASEB Journal · doi:10.1096/fj.09-150862 · Cited by 174 · see citing works
Microglial microvesicle secretion and intercellular signaling
Turola, E. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00149 · Cited by 168 · see citing works
NLRP3 Inflammasome: A Starring Role in Amyloid-β- and Tau-Driven Pathological Events in Alzheimer’s Disease
Zeller, M. V., Dias, D., Sebastião, A. M., & Valente, C. A. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-210268 · Cited by 173 · see citing works
The P2X7 receptor–pannexin connection to dye uptake and IL-1β release
Pelegrı́n, P., & Surprenant, A. (2009) · Purinergic Signalling · doi:10.1007/s11302-009-9141-7 · Cited by 169 · see citing works
P2X7 receptor signaling contributes to tissue factor–dependent thrombosis in mice
Furlan-Freguia, C., Marchese, P., Gruber, A., Ruggeri, Z. M., & Ruf, W. (2011) · Journal of Clinical Investigation · doi:10.1172/jci46129 · Cited by 169 · see citing works
P2X7 in Cancer: From Molecular Mechanisms to Therapeutics
Lara, R., Adinolfi, E., Harwood, C. A., Philpott, M. P., Barden, J. A., Virgilio, F. D., & McNulty, S. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.00793 · Cited by 165 · see citing works
Monocyte Derived Microvesicles Deliver a Cell Death Message via Encapsulated Caspase-1
Sarkar, A., Mitra, S., Mehta, S., Raices, R. M., & Wewers, M. D. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007140 · Cited by 168 · see citing works
The P2X7 Receptor-Interleukin-1 Liaison
Giuliani, A. L., Sarti, A. C., Falzoni, S., & Di Virgilio, F. (2017) · Frontiers in Pharmacology · doi:10.3389/fphar.2017.00123 · Cited by 166 · see citing works
Inflammasome proteins in cerebrospinal fluid of brain-injured patients as biomarkers of functional outcome
Adamczak, S. E., Dale, G. A., Vaccari, J. P. D. R., Bullock, M. R., Dietrich, W. D., & Keane, R. W. (2012) · Journal of neurosurgery · doi:10.3171/2012.9.jns12815 · Cited by 166 · see citing works
P2RX7 inhibitor suppresses exosome secretion and disease phenotype in P301S tau transgenic mice
Ruan, Z., Delpech, J.-C., Venkatesan Kalavai, S., Van Enoo, A. A., Hu, J., Ikezu, S., & Ikezu, T. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00396-2 · Cited by 150 · see citing works

P2X7 Receptor-Stimulated Secretion of MHC Class II-Containing Exosomes Requires the ASC/NLRP3 Inflammasome but Is Independent of Caspase-1
Qu, Y., Ramachandra, L., Mohr, S., Franchi, L., Harding, C. V., Núñez, G., & Dubyak, G. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0802968 · Cited by 157 · see citing works
Self-citation
P2X7 receptor regulation of non-classical secretion from immune effector cells
Dubyak, G. (2012) · Cellular Microbiology · doi:10.1111/cmi.12001 · Cited by 189 · see citing works
Self-citation
Ca2+ Stores and Ca2+ Entry Differentially Contribute to the Release of IL-1β and IL-1α from Murine Macrophages
Brough, D., Feuvre, R. A. L., Wheeler, R. D., Solovyova, N. A., Hilfiker, S., Rothwell, N. J., & Verkhratsky, A. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.6.3029 · Cited by 168 · see citing works
P2X7 Receptor Differentially Couples to Distinct Release Pathways for IL-1β in Mouse Macrophage
Pelegrı́n, P., Barroso-Gutierrez, C., & Surprenant, A. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.11.7147 · Cited by 413 · see citing works
Mechanisms of interleukin-1β release
Eder, C. (2009) · Immunobiology · doi:10.1016/j.imbio.2008.11.007 · Cited by 307 · see citing works

Authors: Qu, Y., Franchi, L., Nunez, G., & Dubyak, G. R.
Affiliations: Case Western Reserve University (US)
University of Michigan (US)
Department of Pathology, University of Michigan , Ann Arbor, MI 48109
ORCID: Qu, Yan
Dubyak, George R
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2007-08-01
Volume: 179
Issue: 3
Pages: 1913-1925
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.179.3.1913
OpenAlex: W2100358971
Cited by: 563
References: 75
Citations by year: 2026: 16 · 2025: 21 · 2024: 21 · 2023: 26 · 2022: 24 · 2021: 27 · 2020: 36 · 2019: 28 · 2018: 36 · 2017: 30 · 2016: 30 · 2015: 43 · 2014: 37 · 2013: 36 · 2012: 38
FWCI: 9.93
Type: journal article
Language: en
Open access: closed
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of General Medical Sciences (GM-36387, R01GM036387)
National Institute of Allergy and Infectious Diseases (AI 064748, AI063331, R01AI064748)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Adenosine and Purinergic Signaling
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords: P2X7 receptor, inflammasome, caspase-1, exosomes, macrophages, extracellular ATP, multivesicular bodies, extracellular calcium
MeSH terms: Adenosine Triphosphate, Animals, Cathepsin B, Cells, Cultured, Enzyme Activation, Exocytosis, Inflammation, Lysosomes, Macrophages, Mice, Inbred BALB C, Mice, Inbred C57BL, Endosomes, Signal Transduction, Receptors, Purinergic P2, Mice, Knockout, Models, Immunological, Caspase 1, Multiprotein Complexes, Mice, Interleukin-1beta, Receptors, Purinergic P2X7

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Nonclassical IL-1β Secretion Stimulated by P2X7 Receptors Is Dependent on Inflammasome Activation and Correlated with Exosome Release in Murine Macrophages

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks