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NLRs at the intersection of cell death and immunity
Abstract
Inflammation is a crucial element of the host response to cellular insult. Pathogen-induced inflammation includes a molecular pathway which proceeds through activation of the protease caspase-1 to the release of the inflammatory cytokines interleukin-1 (IL-1) and IL-18. Importantly, pathogens may also induce forms of cell death that have inherently pro-inflammatory features. Here, we review recent evidence demonstrating that NLR (nucleotide-binding domain, leucine-rich repeat containing) family proteins serve as a common component of both caspase-1-activated apoptotic pathways and caspase-independent necrotic pathways. Parallels are drawn between NLR protein function and the activity of structurally similar proteins involved in cell death: the apoptotic mediator APAF1 (apoptotic-protease-activating factor 1) and the plant disease resistance NBS-LRR (nucleotide-binding site leucine-rich repeats) proteins.
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“Polynucleotides and oligonucleotides derived from degrading DNA or RNA can act on TLR3, TLR7, TLR8, or TLR9 as well as on intracellular receptors including RIG1, MDA5, or LGP2, while ATP and its degradation products may activate or inhibit distinct classes of purinergic receptors 45,108,109.”
From Immunogenic and tolerogenic cell death (2009) · cites this paper as [108]
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“NAIP is unique among the IAPs in that it possesses a nucleotide-binding and oligomerization domain as well as leucine-rich repeats that classify this IAP along with other proteins involved in innate immunity, called the nucleotide-binding and oligomerization domain-like receptors (Kanneganti et al., 2007; Mariathasan…”
BackgroundInflammasomes in liver diseases
Szabó, G., & Csák, T. (2012) · Journal of Hepatology · doi:10.1016/j.jhep.2012.03.035 · Cited by 498
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“The later, in turn, processes pro-IL-1β to its mature form which is able to be released then (Ferrari et al., 1997, 2006; Qu et al., 2007; Ting et al., 2008; Di Virgilio et al., 2017).”
BackgroundNLR family member NLRC5 is a transcriptional regulator of MHC class I genes
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“There are 22 NLR proteins in humans, which share three characteristic functional domains: an N-terminal protein–protein interaction domain such as a caspase recruitment domain (CARD) or a PYRIN domain, a centrally located NBD (or NACHT, NAIP, CIITA, HET-E and TP1 domain), and C-terminal LRRs (11, 12).”
BackgroundInfluentialImmunomodulatory mechanisms of lactobacilli
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“There are more than 20 members of this receptor family in humans and they recognize a wide range of bacterial ligands and toxins as well as certain damageassociated molecular patterns (DAMPs) of the host cell [19,54].”
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Gasse, P., Riteau, N., Charron, S., Girre, S., Fick, L., Pétrilli, V., Tschopp, J., Lagente, V., Quesniaux, V. F. J., Ryffel, B., et al. (2009) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200808-1274oc · Cited by 410
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“Recently, HSP90 and HSC70, important players in plant (Ting et al., 2008) and animal (Shirasu, 2009) innate immunity, have been reported to fulfil a critical role in stomatal closure and modulation of physiological responses to ABA (Clément et al.”
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Fraunholz, M. J., & Sinha, B. N. M. (2012) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2012.00043 · Cited by 392
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“atrbohD (2), lsd1-2 (3), npr1-1 (4), rps2-101C (5), rpm1-3 (6), sid2-1 (7), fls2 (8), and efr (8) are described elsewhere.”
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Lambrecht, B. N., Kool, M., Willart, M. A. M., & Hammad, H. (2009) · Current Opinion in Immunology · doi:10.1016/j.coi.2009.01.004 · Cited by 354
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“Recent studies have demonstrated that NOD-dependent signaling cascades can also activate NF- B (76, 84).”
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“Plant NB-LRR immune receptors are structurally analogous to animal NLR (nucleotide-binding domain, leucine-rich repeat containing) receptors (Ting et al., 2008).”
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“…including the nucleotide-binding, leucine-rich repeat, pyrin domain containing 1 (NLRP1), the NLRP3 and the nucleotide-binding, leucine-rich repeat, CARD domain containing 4 (NLRC4) inflammasome (Tschopp et al, 2003; Agostini et al, 2004; Dinarello, 2005; Miao et al, 2006; Ting et al, 2008).”
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Caspase-1: The inflammasome and beyond
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Monocytic microparticles activate endothelial cells in an IL-1β–dependent manner
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Self-citationInnate Immune Responses to Danger Signals in Systemic Inflammatory Response Syndrome and Sepsis
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“Cells of the immune system rely on specific receptors to detect the presence of exogenous and endogenous danger signals (lipopolysacharide [LPS], bacterial toxins, viral proteins) that subsequently trigger an immediate innate proinflammatory response.(31,32) Several trans-membrane proteins are identified as pattern re…”
Interaction of staphylococci with bone
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“This complex consists of caspase-1, the adaptor protein ASC (apoptosis-associated speck-like protein containing a caspase recruitment domain (CARD)) and one of several NLR proteins, of which four are known to associate with inflammasomes (Ting et al., 2008).”
BackgroundAn Inflammasome-Independent Role for Epithelial-Expressed Nlrp3 in Renal Ischemia-Reperfusion Injury
Shigeoka, A. A., Mueller, J. L., Kambo, A., Mathison, J. C., King, A. J., Hall, W. F., Correia, J. D. S., Ulevitch, R. J., Hoffman, H. M., & McKay, D. B. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1002330 · Cited by 229
Mechanisms of uric acid crystal‐mediated autoinflammation
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“Although IPAF ⁄ NLRC4, NALP3 ⁄ NLRP3, and NALP1 ⁄NLRP1 inflammasomes define the general structure of NLR inflammasome complexes, recent observations suggest that other NLRs, such as NAIP or NOD2, may be involved in forming NLR inflammasomes or in modulating their activity (49, 59).”
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Nakhaei, P., Génin, P., Civas, A., & Hiscott, J. B. (2009) · Seminars in Immunology · doi:10.1016/j.smim.2009.05.001 · Cited by 229
Critical role for NLRP3 in necrotic death triggered by Mycobacterium tuberculosis
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“The second type, called pyronecrosis, is caspase-1independent (Ting et al., 2008).”
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Karki, R., Man, S. M., Malireddi, R. K. S., Kesavardhana, S., Zhu, Q., Burton, A. R., Sharma, B. R., Qi, X., Pelletier, S. W., Vogel, P., et al. (2016) · Nature · doi:10.1038/nature20597 · Cited by 218
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“Pathogen-mediated activation of caspase 1 and/or NLRs can induce several cell death pathways that are broadly characterized as proinflammatory because they result in the further release of inflammatory molecules (13, 14).”
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“Members of the NLR family assemble into large multiprotein complexes ( 700 kDa), termed inflammasomes, that can be activated by cellular pathogens (bacteria, fungi, viruses, and protozoa) or stress to engage innate immune defenses (23, 35).”
BackgroundGao, Z., Chung, E., Eitas, T. K., & Dangl, J. L. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104410108 · Cited by 196
“Plant NB-LRR proteins are structurally and functionally analogous to animal nucleotide-binding leucine-rich repeat receptor (NLR) innate immune receptors (3, 4).”
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Caspase-7 Activation by the Nlrc4/Ipaf Inflammasome Restricts Legionella pneumophila Infection
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“These cytosolic receptors belong to the nucleotide binding oligomerization domain-leucine rich repeat proteins (NOD-likereceptors or CATERPILLAR family of proteins) [7–12].”
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“Alternatively, RV infection and, in particular, the overexpression of the RV G protein might result in pyroptosis, a cell death pathway similar to apoptosis, which, in contrast to apoptosis, involves the activation of caspase 1 and thereby leading to necrosis [61].”
BackgroundAmelioration of sepsis by inhibiting sialidase-mediated disruption of the CD24-SiglecG interaction
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“transduction elements involved in the hypersensitive response (a pathway leading to PCD; Innes and DeYoung, 2006; Ting et al., 2008).”
BackgroundPure Hemozoin Is Inflammatory In Vivo and Activates the NALP3 Inflammasome via Release of Uric Acid
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“Two of the best studied NLR family members are IPAF and NALP3, and these have been shown to be indispensable for the production of IL-1 in response to a large number of pathogens and endogenous molecules (41).”
BackgroundInflammasome signaling at the heart of central nervous system pathology
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“APAF-1 bears close structural resemblance to NLRs with a CARD domain for recruiting caspase-9, which corroborates the idea that low intracellular K(1)activated apoptosomes evoke exclusively apoptotic cell death, while activated inflammasomes mediate inflammation along with pyroptotic cell-death (Ting et al., 2008).”
BackgroundMeixenberger, K., Pache, F. C., Eitel, J., Schmeck, B., Hippenstiel, S., Slevogt, H., N’Guessan, P. D., Witzenrath, M., Netea, M. G., Chakraborty, T., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0901346 · Cited by 186
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“Inflammasome proteins and even the functional machinery of inflammasomes have been linked to cell death in several cell types [123].”
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“Nevertheless, CTSB inhibition only partially reduced cell death, and therefore, programmed necrosis, socalled pyronecrosis [65], is not the only pathway leading to PVLmediated necrosis.”
BackgroundThe P2X7 receptor–pannexin connection to dye uptake and IL-1β release
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“[72] Purinergic Signalling (2009) 5:129–137 133”
The Pathology of Orthopedic Implant Failure Is Mediated by Innate Immune System Cytokines
Landgraeber, S., Jäger, M., Jacobs, J. J., & Hallab, N. J. (2014) · Mediators of Inflammation · doi:10.1155/2014/185150 · Cited by 167
“Effective immune system activation requires specific receptors that recognize both pathogen associated molecular patterns (PAMPs) and danger associatedmolecular patterns (DAMPs) to initiate innate proinflammatory responses, Figures 1 and 3 [61, 62].”
BackgroundMechanisms of Neutrophil Accumulation in the Lungs Against Bacteria
Balamayooran, G., Batra, S., Fessler, M. B., Happel, K. I., & Jeyaseelan, S. (2009) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2009-0047tr · Cited by 169
“NLRs are characterized by the presence of a central NOD domain, a C-terminal LRR, and an N-terminal domain, including CARD or the putative protein–protein interaction (PYRIN) domain (37).”
BackgroundInfluentialAmyloid‐β oligomers set fire to inflammasomes and induce Alzheimer's pathology
Salminen, A., Ojala, J. O., Suuronen, T., Kaarniranta, K., & Kauppinen, A. (2008) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2008.00496.x · Cited by 167
“2258 APAF-1 protein is structurally very similar to NOD-like receptors, containing a CARD motif for the recruitment of caspase-9 [34].”
BackgroundInfluentialMcElvania, E., Allen, I. C., Hulseberg, P. D., Sullivan, J. T., McCann, J. R., Sándor, M., Braunstein, M., & Ting, J. P. ‐. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012320 · Cited by 159
“In addition to these inflammatory functions, PYCARD association with NLR proteins is required for pyroptotic and pyronecrotic cell death [19,20].”
BackgroundSelf-citationShaw, P. J., Lukens, J. R., Burns, S., Chi, H., McGargill, M. A., & Kanneganti, T. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1000217 · Cited by 160
Morishige, T., Yoshioka, Y., Inakura, H., Tanabe, A., Yao, X., Narimatsu, S., Monobe, Y., Imazawa, T., Tsunoda, S., Tsutsumi, Y. M., et al. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.05.036 · Cited by 155
“Pyronecrosis is considered to elicit substantial inflammation and to affect the local environment, whereas apoptosis is widely accepted as non-inflammatory cell death without effects around the dying cells [48].”
Shigella Induces Mitochondrial Dysfunction and Cell Death in Nonmyleoid Cells
Carneiro, L. A. M., Travassos, L. H., Soares, F., Tattoli, I., Magalhaes, J. G., Bozza, M. T., Plotkowski, M. C., Sansonetti, P. J., Molkentin, J. D., Philpott, D. J., et al. (2009) · Cell Host & Microbe · doi:10.1016/j.chom.2008.12.011 · Cited by 155
“In macrophages, the NLR family members NLRC4 and NLRP3 mediate Shigella-induced pyroptosis and pyronecrosis, respectively, with activation of the caspase-1 inflammasome and subsequent IL-1b processing and release (Ting et al., 2008).”
InfluentialLi, L., Lu, Q., Chen, W., Li, J., Li, C., & Zheng, Z. J. (2018) · Journal of Diabetes Research · doi:10.1155/2018/8193523 · Cited by 164
“The NLRP3 inflammasome induces inflammation by mediating the catalytic activation of caspase-1, followed by the cleavage and release of the proinflammatory cytokines IL-1β and IL-18 [25, 26].”
BackgroundChen, G., Brown, N. K., Wu, W., Khedri, Z., Yu, H., Chen, X., van de Vlekkert, D., d’Azzo, A., Zheng, P., & Liu, Y. (2014) · eLife · doi:10.7554/elife.04066 · Cited by 153
“, 2012) and cellular injuries (Ting et al., 2008; Tschopp and Schroder, 2010).”
BackgroundEvolutionary Convergence and Divergence in NLR Function and Structure
Meunier, É., & Brož, P. (2017) · Trends in Immunology · doi:10.1016/j.it.2017.04.005 · Cited by 148
“the eighth conserved member of this group, but it differs structurally because its NBD is not strictly a NACHT domain and because it contains WD40 repeats instead of LRRs [33,36,37].”
BackgroundThe Role of Inflammasome-Dependent and Inflammasome-Independent NLRP3 in the Kidney
Kim, Y., Kim, S., Kim, K., Lee, S.-H., & Moon, J.-Y. (2019) · Cells · doi:10.3390/cells8111389 · Cited by 157
“AKI caused by IRI is attenuated in NLRP3, ASC, or caspase 1 KO kidneys [11,53].”
BackgroundPyroptosis – a cell death modality of its kind?
Kepp, O., Galluzzi, L., Zitvogel, L., & Kroemer, G. (2010) · European Journal of Immunology · doi:10.1002/eji.200940160 · Cited by 151
Control of infection by pyroptosis and autophagy: role of TLR and NLR
Bortoluci, K. R., & Medzhitov, R. M. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0335-5 · Cited by 150
“However, the idea of pyroptotic cell death as an effector mechanism of the host cell to control infections by itself is a matter of debate [9, 28, 42].”
BackgroundCD24-Siglec G/10 discriminates danger- from pathogen-associated molecular patterns
Liu, Y., Chen, G.-Y., & Zheng, P. (2009) · Trends in Immunology · doi:10.1016/j.it.2009.09.006 · Cited by 147
Sensors of the innate immune system: their mode of action
Baccalà, R., González‐Quintial, R., Lawson, B. R., Stern, M. E., Kono, D. H., Beutler, B., & Theofilopoulos, A. N. (2009) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2009.136 · Cited by 145
“NLR activation mediates inflammation and immunity not only through the induction of pyrogenic and inflammatory cytokines, but also by promoting cell death”
BackgroundModulation of obesity-induced inflammation by dietary fats: mechanisms and clinical evidence
Teng, K., Chang, C.-Y., Chang, L. F., & Nesaretnam, K. (2014) · Nutrition Journal · doi:10.1186/1475-2891-13-12 · Cited by 151
“This complex regulates the cleavage of interleukin-1β (IL-1β) from pro-IL-1β [40,41].”
BackgroundType-I-interferons in infection and cancer: Unanticipated dynamics with therapeutic implications
Musella, M., Manic, G., Maria, R. D., Vitale, I., & Sistigu, A. (2017) · OncoImmunology · doi:10.1080/2162402x.2017.1314424 · Cited by 147
“nucleotide-binding domain and a C-terminal leucinerich repeat domain.(22) Among the more than 20 NLRs identified in humans so far,(22) only the cytosolic molecular sensor NODcontaining protein 2 (NOD2) was clearly shown to recognize”
BackgroundExpression Regulation of Major Histocompatibility Complex Class I and Class II Encoding Genes
van den Elsen, P. J. (2011) · Frontiers in Immunology · doi:10.3389/fimmu.2011.00048 · Cited by 139
“CIITA belongs to the large NLR (nucleotide binding domain, leucine-rich repeat containing) family of proteins that play multiple functions in innate immune responses (Harton et al., 2002; Ting et al., 2008).”
BackgroundInnate instruction of adaptive immunity revisited: the inflammasome
Eisenbarth, S. C., & Flavell, R. A. (2009) · EMBO Molecular Medicine · doi:10.1002/emmm.200900014 · Cited by 135
“Keywords: aluminium hydroxide; caspase-1; inflammasome; nalp3; toll-like receptors DOI 10.1002/emmm.200900014”
BackgroundInfluentialInterleukin-1, inflammasomes, autoinflammation and the skin
Contassot, E., Beer, H.-D., & French, L. E. (2012) · Swiss Medical Weekly · doi:10.4414/smw.2012.13590 · Cited by 130
Welin, A., Eklund, D., Stendahl, O. I., & Lerm, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020302 · Cited by 127
“This is consistent with the morphological features observed [11,12,26], including DNA fragmentation, which is a hallmark of apoptosis, but has also been observed in a disorganized fashion during necrosis [12,48,49].”
BackgroundResultEitel, J., Meixenberger, K., Suttorp, N., & Opitz, B. (2009) · Thrombosis and Haemostasis · doi:10.1160/th09-05-0323 · Cited by 133
Nod2: A Critical Regulator of Ileal Microbiota and Crohn’s Disease
Sidiq, T., Yoshihama, S., Downs, I., & Kobayashi, K. S. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00367 · Cited by 140
“NLRs have a tripartite structure consisting of an aminoterminal effector domain, a central NBD, and a carboxy-terminal LRR (17).”
BackgroundInfluentialThe Antisocial Network: Cross Talk Between Cell Death Programs in Host Defense
Snyder, A. G., & Oberst, A. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-112019-072301 · Cited by 129
“Strikingly, the activation of APAF-1 by cytochrome c following MOMP—central to the apoptotic pathway—closely mirrors inflammasome activation (106).”
BackgroundSun, X., Hao, H., Han, Q., Song, X., Liu, J., Dong, L., Han, W., & Mu, Y. (2017) · Stem Cell Research & Therapy · doi:10.1186/s13287-017-0668-1 · Cited by 129
“The processing requires two signals: the first can be achieved by LPS stimulation to induce the IL-1β and IL-18 production from pro-IL-1β and pro-IL-18; and saturated fatty acids are the second signal to activate the inflammasome to further cause the release of procaspase-1 to caspase-1.”
InfluentialWang, S., Gu, Y., Zebell, S. G., Anderson, L. K., Wang, W., Mohan, R., & Dong, X. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2014.10.005 · Cited by 125
“In the mammalian system, activation of NLRs can trigger programmed cell death (PCD) through recruitment of caspases (Ting et al., 2008).”
BackgroundToll-Like Receptor 2 and NLRP3 Cooperate To Recognize a Functional Bacterial Amyloid, Curli
Rapsinski, G. J., Wynosky-Dolfi, M. A., Oppong, G. O., Tursi, S. A., Wilson, R. P., Brodsky, I. E., & Tükel, Ç. (2014) · Infection and Immunity · doi:10.1128/iai.02370-14 · Cited by 127
“343 Activation of inflammasomes can lead to the pyroptosis via caspase-1 activation 344 (47, 48).”
BackgroundThe NLRP3 Inflammasome as a Novel Player of the Intercellular Crosstalk in Metabolic Disorders
Benetti, E., Chiazza, F., Patel, N. S. A., & Collino, M. (2013) · Mediators of Inflammation · doi:10.1155/2013/678627 · Cited by 122
“We will provide here a perspective on the current research on NLRP3 inflammasome, which may represent an innovative therapeutic target to reverse the detrimental metabolic consequences of the metabolic inflammation.”
BackgroundYuen, B., Bayes, J. M., & Degnan, S. M. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst174 · Cited by 117
“To investigate the origin of the bona fide NLRs (as defined by the NACHT-LRR domain combination; Ting, Harton et al. 2008), a number of fungal, plant, protozoan, and metazoan genomes were also interrogated (supplementary file S2, Supplementary Material online).”
BackgroundInfluentialSweet immunity in the plant circadian regulatory network
Moghaddam, M. R. B., & den Ende, W. V. (2013) · Journal of Experimental Botany · doi:10.1093/jxb/ert046 · Cited by 118
Pannexin1 as mediator of inflammation and cell death
Yanguas, S. C., Willebrords, J., Johnstone, S. R., Maes, M., Decrock, E., Bock, M. D., Leybaert, L., Cogliati, B., & Vinken, M. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2016.10.006 · Cited by 122
“This mechanism is caspase 11 independent and mainly implies the contribution of the NLRC4 inflammasome [125].”
BackgroundInfluentialClément, M., Leonhardt, N., Droillard, M., Reiter, I. M., Montillet, J., Genty, B., Laurière, C., Nussaume, L., & Noël, L. D. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.174425 · Cited by 117
“Molecular chaperones are key components of innate immunity in mammals (Ting et al., 2008) and plants (Shirasu, 2009).”
BackgroundToxicology of Autoimmune Diseases
Pollard, K. M., Hultman, P. A., & Kono, D. H. (2010) · Chemical Research in Toxicology · doi:10.1021/tx9003787 · Cited by 119
Tumor-host interactions: the role of inflammation
Bitoux, M. L., & Stamenkovic, I. (2008) · Histochemistry and Cell Biology · doi:10.1007/s00418-008-0527-3 · Cited by 113
“Depending on the stimulus, caspase-1, also called IL-1 converting enzyme (ICE), can induce secretion of pro-inXammatory cytokines or trigger cell pyroptosis, a caspase-1-dependent cell death pathway (Ting et al. 2008).”
Cell death and autophagy in tuberculosis
Moraco, A. H., & Kornfeld, H. (2014) · Seminars in Immunology · doi:10.1016/j.smim.2014.10.001 · Cited by 111
The role of mitochondria in cellular defense against microbial infection
Arnoult, D., Carneiro, L. A. M., Tattoli, I., & Girardin, S. E. (2009) · Seminars in Immunology · doi:10.1016/j.smim.2009.05.009 · Cited by 107
mTOR: Its Critical Role in Metabolic Diseases, Cancer, and the Aging Process
Marafie, S. K., Al‐Mulla, F., & Abubaker, J. A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25116141 · Cited by 119
“NLRs are a family of cytoplasmic sensors that regulate a range of biological functions involved in immunity against infectious diseases [54] and are central regulators of intestinal homeostasis [55].”
Background
Metadata
- Authors
- Ting, J. P.-Y., Willingham, S. B., & Bergstralh, D. T.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- Corresponding author
- Ting, Jenny P.-Y.
- ORCID
- Ting, Jenny P.-Y.
- Venue
- Nature Reviews Immunology
- Published
- 2008-05
- Volume
- 8
- Issue
- 5
- Pages
- 372-379
- ISSN
- 1474-1733 (ISSN-L)
- 1474-1741
- OpenAlex
- W2050870561
- Cited by
- 371
- References
- 145
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 7 · 2023: 8 · 2022: 10 · 2021: 14 · 2020: 10 · 2019: 19 · 2018: 18 · 2017: 18 · 2016: 17 · 2015: 19 · 2014: 22 · 2013: 27 · 2012: 36
- FWCI
- 3.40
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature reviews. Immunology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- NLR proteins, cell death, pyroptosis, caspase-1, apoptosis, necrosis, inflammation, interleukin-1, IL-18, Apaf-1, NBS-LRR proteins, plant disease resistance, host-pathogen interaction
- MeSH terms
- NLR Proteins, Leucine-Rich Repeat Proteins, Animals, Communicable Diseases, Humans, Interleukin-1, Necrosis, Proteins, Tumor Necrosis Factor-alpha, Apoptosis, Caspase 1, HMGB1 Protein, Intracellular Signaling Peptides and Proteins, Adaptor Proteins, Signal Transducing, Apoptosis Regulatory Proteins, Apoptotic Protease-Activating Factor 1
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