Nod-like Receptors: Critical Intracellular Sensors for Host Protection and Cell Death in Microbial and Parasitic Infections
Abstract
:1. Introduction
Inflammatory Diseases | Affected Organs | Dysregulated NLRs Family | References |
---|---|---|---|
Thyroiditis | Thyroid gland | Over-expression and activation of NLRC4, NLRP1, AIM2 and NLRP3 inflammasome | [25,26,27] |
Type 1 Diabetes | Pancreas | Over-expression NLRP1, NOD1/2, CIITA and NLRP3 | [26,28,29] |
Inflammatory bowel diseases (IBD: Ulcerative colitis and Crohn’s disease) | Gastrointestinal | NOD1, NOD2, NLRP3 and NLRP1 | [26,30,31,32,33] |
Celiac diseases | Small intestine | Enhanced expression of NLRP3 and CIITA, NLRP6 | [26,29,34] |
Autoimmune hepatitis | Liver | Hyperactivation of NLRP3 and deficiency of NLRX1 | [2,26,35,36] |
Arthritis | Joints | Excessive expression of NLRP3, NLRP2, CIITA, NOD2, NLRC5 and NLRP12 (beneficial), and NLRP9 and NLRP11 | [25,26,37,38,39,40] |
Systemic Lupus Erythematous (SLE) | Multiple organs such as Kidney, Lung and CNS | Over-expression of NOD2, NLRP3, SNPs in CIITA, NLRP1 and NLRX1 | [26,41,42,43,44] |
Vitiligo | Skin | Increased expression/activation of NLRP1 and NLRP3 | [26,44,45,46] |
Psoriasis | Epidermal layer (from the limbs to eyelids) | Enhanced expression of NOD2, PYCARD, CARD6, CARD14, NLRP3, NLRP1 and IFI16 | [47,48,49,50] |
Multiple Sclerosis | CNS: brain, spinal cord and optic nerves. | Over-activation of NOD1, NOD2 and NLRP1. Mutation in CIITA, NLRP3 and regulatory role of NLRP12, NLRC3 and NLRX1 | [51,52,53,54] |
2. Structure, Function and Classification of NOD-like Receptors
- (i)
- Transcriptional trans-activators: members are CIITA and NLRC5, located at the promoter region of major histocompatibility complex (MHC) II and MHC-I, respectively [57,58]. CIITA, via its unique acidic domain (AD), is recruited to the MHC enhanceosome complex as a non-DNA binding activator to promote the transcriptional activation of MHC-II [57]. NLRC5, on the other hand, is conserved in vertebrates, with high expression in immune cells and mucosal epithelia. NLRC5 controls basal MHC I gene expression and is inducible by IFNγ stimulation to trans-activate the MHC-I gene in lymphoid and epithelial cells by reducing H3K27me3 in the MHC-I promoter [59,60,61]. The cis-regulatory elements of the promoter of the MHC-I gene interact with NLRC5 through a distinct transcriptional factor to recruit modifiers and initiate the MHC I enhanceosome transcriptional complex [60]. Nlrc5−/− mice exhibit impaired CTL responses, and NLRC5-null target cells are not efficiently cleared by CTLs, while the immunogenic melanoma was able to activate CD8+ T cells by restoring the expression of NLRC5 alongside with CD80 [56].
- (ii)
- Activators of NF-κB and MAPK pathways: The NLRs in this category are the first described NOD-like receptors; NOD1 (NLRC1) and NOD2 (NLRC2) recognize bacterial peptidoglycans components D-glutamyl-meso-diaminopimelic acid (iE-DAP) and muramyl dipeptide (MDP), respectively, to induce the production of proinflammatory cytokines (TNF, IL-6 and IL-1β) via NF-κB and MAPK pathways [9,62]. Peptidoglycans (PGN), a constituent of the bacterial cell wall, have been demonstrated to trigger NOD2 activity sufficiently [63]. A gain-of-function mutation in the NOD2 gene is associated with autoinflammatory condition Blau syndrome [64] and sarcoidosis [65], whereas its loss of function is linked to Crohn’s disease [66]. Intracellular ligands recognition through the LRR domain induced the formation of a protein complex at their CARD N-terminal with an adaptor protein RIP2 for the subsequent phosphorylation of NF-κB. Moreover, the downstream signal may also go through the activation of MAPKs, including the p38, extracellular signal-regulated protein kinase (ERK) and c-Jun N-terminal kinase (JNK) pathways [10].
- (iii)
- Inflammasome activators of the NLRs family: members of this family are involved in the inflammasome complex, i.e., an intracellular multi-protein complex that leads to the activation of caspase 1, required for the maturation of IL-1β and IL-18, as well as the amplification of NF-κB, JNK and p38 MAPK-signaling pathways [67,68]. These NLRs conduct robust secretion of proinflammatory cytokines and chemokines to the distressing site and also mediate pyroptotic cell death [57]. NLRC4 directly recruits pro-caspase 1 while intermediary cytosolic-resident adaptor apoptosis-associated speck-like protein containing a CARD (ASC) is required for PYD-carrying NLRs (such as NLRP3 and NLRP12) for the recruitment of pro-caspase 1. Aside from caspase 1, NALP1 has also been shown to participate in the activation of caspase 5 [69].
- (iv)
- Members of the NLR family are essentially involved in the negative regulation of the proinflammatory responses by limiting IL-1β secretion, NF-κB and type I IFN (IFN-I) signaling. These include NLRP2, NLRC3, NLRP4, NLRP6, NLRP7, NLRP10, NLRP12 and NLRX1 [57]. Although the majority of NLR members here exhibit both inflammasome activation and inhibitory functions under varying conditions, ASC is recruited for the exhibition of inflammasome function; meanwhile, different endogenous proteins are engaged for the inhibitory function. Information about the NOD-like receptors in this category is scant, and their therapeutic potentials are remarkable.
3. NOD1 and NOD2 in Sensing PAMP/DAMP and Inflammatory Responses
4. NLRP3 and NLRC4 Inflammasomes
5. NLRP6 and NLRP10 in Regulatory and Inflammatory Responses
6. NOD-Like Receptors in the Regulation of IFN-I and Proinflammatory Responses
- (i)
- Regulator of canonical and noncanonical NF-κB and MAPK signaling pathways: NLRP12 is a negative regulator protein that inhibits canonical and noncanonical activations of NF-κB and ERK (Figure 2A). Nlrp12–/– mice show exaggerated NF-κB activation and ERK phosphorylation in colitis-associated colorectal cancer models [193], osteoclast differentiation [194] and in bone marrow-derived macrophages treated with Mycobacterium tuberculosis [190] and Salmonella LPS but not flagellin [195]. Canonical interference of NLRP12, as demonstrated by Zaki et al., is via the suppression of hyperphosphorylation of IRAK1 to limit of IκBα and ERK phosphorylation downstream of TLR-MyD88, thus reducing nuclear translocation of NF-κB and secretion of proinflammatory cytokines in macrophage stimulated with S. typhimurium [195]. Similarly, its interaction with NF-κB-inducing kinase (NIK) and TRAF3 was through its NOD and LRR domains, leading to proteasomal degradation of NIK in noncanonical NF-κB signaling [33,57,190] in microbial and parasitic (Leishmania major) infections [196]. Therefore, the constitutive elevation of NIK, processing of p100 to p52 and reduced degradation of TRAF3, was observed in Nlrp12–/– cells [33]. These studies recapitulate NLRP12 as a potential checkpoint for NF-κB signaling in murine macrophages and human THP-1 monocytic cells by negatively regulating both TLR and TNFR pathways [33]. In fact, NLRP12 also exhibits its inhibitory role by degrading NOD2 through the ubiquitin–proteasome pathway to raise host tolerance towards bacterial muramyl dipeptide (MDP) by sequestering heat-shock protein 90 (HSP90). Sequestration of HSP90 prevents the stabilization of NOD2/RIPK2 complex in response to MDP, thus repressing NOD2 signal transduction of NF-κB and subsequent activity of the JAK/STAT signaling pathway [197]. The physiological impact of NLRP12 regulation in the immune response is still elusive, for instance, the loss of NLRP12 in BMDC induces IL-6 and TNF upon M. tuberculosis or Klebsiella pneumonia without conferring resistance against these bacteria [198]. In hepatocellular carcinoma (HCC), however, NLRP12 downregulates the JNK-dependent inflammation and proliferation of hepatocytes and NLRP12 deficient mice were highly susceptible to diethyl nitrosamine (DEN)-induced HCC with increased inflammation, hepatocyte proliferation and tumor burden. In contrast, the upregulation of NLRP12 was reported in response to Porphyromonas gingivalis LPS in RAW264.7, and its depletion in the cell line corresponds to an increase in TNF production and iNOS expression [199].
- (ii)
- A negative regulator of Type-I interferon and proinflammatory responses: This is another remarkable function of NLRP12 that was recently demonstrated by our research group; we reported an interference of NLRP12 on RIG-I-mediated IFN-I production during vesicular stomatitis virus (VSV) [200]. We found that VSV infection downregulates NLRP12 expression, and its deletion in BMDC provokes severe transcription and production of IFN-I (IFNα/β) and TNF that corresponds with reduced viral titer and relative genomic copy in Nlrp12–/– DCs upon infection. In the infected DCs, TRIM25, an E3 ligase required for Lys63-linked polyubiquitination and activation of RIG-I, mediates the downstream activation of MAVS (Figure 2C). MAVS associates with the adaptor protein TRAF3 and TRAF family member-associated NF-κB activator (TANK) to trigger the activation of TANK-binding kinase 1 (TBK1) and IκB kinase, leading to the activation of IRFs and production of IFN-I and TNF; thus, enhanced immune signaling cascades were observed in Nlrp12–/– DCs treated with VSV and 5′ppp dsRNA. However, the presence of NLRP12 relieved the binding of TRIM25 with RIG-I to suppress IFN-I production. Mechanistically, NLRP12 promotes RNF125-mediated degradation of RIG-I by associating with ubiquitin ligase TRIM25 to reduce K63-linked ubiquitination of the antiviral innate immune receptor RIG-I (Figure 2C). This will ultimately prevent RIG-I association with MAVS to checkmate the transcription and secretion of interferon and cytokine induction in response to RNA viruses. Domain mapping analysis showed that the NBD domain is presumably a critical target for TRIM25 interaction [200]. Nlrp12–/– mice are more resistant to VSV infection with lower viral loads in the brain and recover faster than WT mice with less neuronal loss in the ventral striatum and hypothalamus in in vivo study.
- (iii)
- NLRP12 inflammasome and its positive regulatory property in other inflammasomes: The foremost inflammasome functions of NLRP12 were reported in an overexpression system where NLRP12 co-expressed with ASC for caspase 1 and IL-1β production [201]. In primary cell and animal study, NLRP12 is involved in the caspase 1-mediating production of inflammatory cytokines (IL-18) and is crucial for the host defense against Yersinia pestis infection; thereby, deficiency of NLRP12 causes the susceptibility to Yersinia pestis infection as it occurred in the IL-18 deficient mice [202]. The actual ligand sensed by NLRP12 in Yersinia for its activation is not known, but it was noted that ligand generation requires a complex type III secretion system (T3SS) (Figure 2B).The inflammasome assemblage of NLRP12 was demonstrated in the dendritic cells from spleen and bone marrow treated with Plasmodium chabaudi, where NLRP12 was collaboratively required for ASC-dependent caspase 1 for the systemic production of IL-1β and pyroptosis [203]. Similarly, collaboration of NLRP12 with other inflammasomes was reported in pyroptosis mediating ganglion cell death of acute glaucoma, NLRP12 collaborates with NLRP3 and NLRC4 to elicit pyroptotic processes and IL-1β maturation through caspase 1 activation [204]. Not only that, simultaneous expression of the NLRP3, NLRP12 and IFI16 inflammasomes in cornea infection induced by virulent HSV-1 strains is ascribed to the enhanced caspase 1, IL-1β and IL18 alongside with co-expression of dense specks of the adapter molecule ASC [205]. However, a contrary report was obtained during Brucella abortus infection that portends NLRP12 as an anti-inflammatory regulator that inhibits not only NF-κB and MAPK signaling but also caspase 1 activation in BMDMs, and its absence conferred the host resistance in murine brucellosis [206]. All these indicate that the function of NLRP12 is stimuli-dependent, and its collaboration with other NLRs may be partially ascribed to dearth of specific ligands to be sensed. However, evidence-based reports have described it as a critical checkpoint in innate immunity in microbial and parasitic infections by regulating innate immune signaling cascades negatively or positively. Since its function varies with pathogens, it is pertinent to investigate the role of NLRP12 in other pathogens.
7. NOD-Like Receptors in the Regulation of Pyroptosis Cell Death
8. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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NLRs Family | Sub-Family/Domain Architectures | Gene |
---|---|---|
Acidic transcription-carrying domain (NLRA) | CIITA (NLRA) | |
BIR- carrying domain (NLRB) | NLRB (NAIP) | |
CARD—carrying domain (NLRC) | NOD1, NLRC4 NOD2 | |
PYD-carrying domain | NLRP2-NLRP9 NLRP11-NLRP14 | |
Additional domain (FIIND) | NLRP1 | |
No LRR | NLRP10 | |
Unidentified domain | NLRs without PYD nor CARD | NLRC3 NLRC5 NLRX1 |
NLR-related molecules | Apaf-1 |
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Babamale, A.O.; Chen, S.-T. Nod-like Receptors: Critical Intracellular Sensors for Host Protection and Cell Death in Microbial and Parasitic Infections. Int. J. Mol. Sci. 2021, 22, 11398. https://doi.org/10.3390/ijms222111398
Babamale AO, Chen S-T. Nod-like Receptors: Critical Intracellular Sensors for Host Protection and Cell Death in Microbial and Parasitic Infections. International Journal of Molecular Sciences. 2021; 22(21):11398. https://doi.org/10.3390/ijms222111398
Chicago/Turabian StyleBabamale, Abdulkareem Olarewaju, and Szu-Ting Chen. 2021. "Nod-like Receptors: Critical Intracellular Sensors for Host Protection and Cell Death in Microbial and Parasitic Infections" International Journal of Molecular Sciences 22, no. 21: 11398. https://doi.org/10.3390/ijms222111398
APA StyleBabamale, A. O., & Chen, S. -T. (2021). Nod-like Receptors: Critical Intracellular Sensors for Host Protection and Cell Death in Microbial and Parasitic Infections. International Journal of Molecular Sciences, 22(21), 11398. https://doi.org/10.3390/ijms222111398