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BTK operates a phospho-tyrosine switch to regulate NLRP3 inflammasome activity

Zsófia A. Bittner, Xiao Liu, Sangeetha Shankar, Ana Tapia-Abellán, Hubert Kalbacher, Liudmila Andreeva, Matthew Mangan, Peter Düwell, Marta Lovotti, Karlotta Bosch, Sabine Dickhöfer, Ana Marcu, Stefan Stevanović, Franziska Herster, Markus W. Löffler, Olaf-Oliver Wolz, Nadine A. Schilling, Jasmin Kümmerle-Deschner, Samuel Wagner, Anita Delor, Bodo Grimbacher, Hao Wu, Eicke Latz, Alexander N. R. Weber

Preprint posted on 25 June 2020 https://www.biorxiv.org/content/10.1101/864702v4.full

Article now published in Journal of Experimental Medicine at http://dx.doi.org/10.1084/jem.20201656

BTK promotes NLRP3 inflammasome activity by aiding movement from the Golgi and promoting NLRP3 oligomerisation and inflammasome complex formation.

Selected by Louise Fraser

Categories: biochemistry, cell biology, immunology, molecular biology

Background:

The NLRP3 inflammasome, a protein complex composed of NLRP3, NEK7, ASC, and caspase-1, is a critical contributor to inflammation thanks to its production of pro-inflammatory cytokines such as IL-1β and IL-18. Those same inflammatory effects have been attributed to a range of inflammatory conditions, including gout, atherosclerosis, and CAPS. It is therefore essential that NLRP3 inflammasome activity is tightly controlled. Many regulators of NLRP3 inflammasome activity have been uncovered. Here, Bittner et al identify a new player in the field of NLRP3 inflammasome regulation – Bruton’s tyrosine kinase (BTK), an activator of NLRP3. Importantly for the world of therapeutics and patient care, BTK already has FDA-approved inhibitors in the market, suggesting that BTK is a viable target for treating NLRP3-mediated inflammatory diseases.

 

Key Findings

NLRP3 and BTK interact

The first step to investigating any mechanism is to determine whether your two proteins of interest interact. Through co-immunoprecipitation studies, the authors found that endogenous NLRP3 and endogenous BTK precipitated together. This interaction was unaffected by treatment with the BTK kinase inhibitor ibrutinib and occurred whether or not nigericin (a commonly used stimulator of NLRP3 inflammasome activity) was used. As a result, BTK constitutively binds to NLRP3 through a mechanism that is independent of its kinase activity.

 

BTK phosphorylates tyrosine residues of NLRP3

With the interaction confirmed, the authors proceeded to investigate whether the kinase activity of BTK mediates NLRP3 tyrosine phosphorylation. By using the BTK inhibitors ibrutinib and acalabrutinib, and the NLRP3 inhibitor MCC950, the authors found that BTK and NLRP3 binding occurred independently of BTK kinase activity and inhibition of BTK prevented tyrosine phosphorylation of NLRP3, confirming a role for BTK kinase activity in NLRP3 phosphorylation. Inhibition of NLRP3 had no effect on either its phosphorylation state or interaction with BTK. This proved true in both HEK293T cells and BMDMs. Furthermore, generated BTK mutants, which lacked kinase activity, were able to bind to NLRP3; following this binding, however, NLRP3 did not undergo tyrosine phosphorylation. BTK is therefore responsible for the phosphorylation of NLRP3.

 

BTK destabilises the association of NLRP3 with Golgi membranes

To explore the role this phosphorylation has on NLRP3 inflammasome activity, Bittner et al used truncated and full length NLRP3 constructs to identify four tyrosine residues within the NACHT domain of NLRP3 that were targeted for phosphorylation by BTK. These tyrosine residues were located in a region thought to be important for binding of NLRP3 to the Golgi phosphatidylinositol phosphates (PtdInsPs). Through fractionation experiments, BTK-mediated typrosine phosphorylation appeared to weaken NLRP3 binding to heavy membranes associated with the Golgi and mitochondria following nigericin treatment, indicating that BTK-mediated phosphorylation is important in allowing the release and movement of NLRP3 following recognition of inflammasome activating signals. NLRP3 binding to Golgi PtdInsPs has previously been shown to be important in the NLRP3 activation process(Chen and Chen 2018); this observation therefore presents a potential effector protein in this process.

 

BTK specifically promotes NLRP3 inflammasome formation and activity

Early in the paper, the authors describe that BTK-deficient BMDMs, as well as PBMCs taken from patients with X-linked Agammaglobulinaemia (XLA) had reduced IL-1β secretion. XLA is an inherited condition with a genetic depletion of BTK and therefore makes an interesting model for studying the effects of BTK loss in inflammasome activation. As confirmation of what they found in BMDMs, XLA PBMCs had reduced phospho-tyrosine phosphorylation of NLRP3, suggesting that the mechanisms studied in mice are transferable to humans.

When investigating the mechanism behind the BTK-mediated promotion of IL-1β production, the authors found that BTK-deficient BMDMs, or WT BMDMs treated with BTK inhibitors, had compromised NLRP3 oligomerisation, and reduced association with the adaptor protein ASC. ASC recruitment to NLRP3 oligomers is required for subsequent inflammasome assembly and activation – BTK-mediated phosphorylation of NLRP3 therefore plays an important role in enabling the assembly of the NLRP3 inflammasome, allowing for downstream activation and IL-1β production. Curiously, AIM2, another inflammasome pathway receptor, showed no change with BTK depletion or inhibition, suggesting that the effects mediated by BTK are NLRP3-specific.

 

Why is this important?

Considering the role NLRP3 plays, either as a benefactor in host defence or as a perpetrator in inflammatory disease, understanding the complex regulatory mechanisms at work is essential for the development of targeted therapies that can manipulate it. It is interesting here that XLA patient PBMCs were also used and were shown to confirm the results seen in the murine BTK-deficient BMDMs. This is an excellent way of demonstrating that the research conducted here is applicable for humans as well as mice.

When it comes to adding to the current knowledge available for the NLRP3 inflammasome pathways, this paper builds on work by Chen and Chen, who noted that NLRP3 binding to Golgi PtdInsPs is important for NLRP3 activation(Chen and Chen 2018). Furthermore, it is interesting to note that Mao et al have found the opposite effect of BTK in NLRP3 inflammasome regulation, whereby BTK appears to inhibit NLRP3 activation during the first of the two-step activation process for NLRP3 (Mao, Kitani et al. 2020). Further research is needed to better understand the apparent conflict here, however, this may suggest that BTK can be targeted for either up- or down-regulation of NLRP3 inflammasome activity. Either way, it is an excellent example of the complexity surrounding the NLRP3 inflammasome and highlights the continuing need for research.

Figure 1: BTK regulation of NLRP3 comes in many forms. Expanding knowledge of these pathways will allow a better understanding of the regulatory mechanisms that underpin inflammasome formation and activation and allow the development of therapeutics targeting inflammation. Figure reproduced without modification from S6 of the supplementary materials of Bittner Z. A. et al, 2020, and shown here with permission of the authors.

Questions for the authors:

  1. BTK has also been shown to inhibit inflammasome activity(Mao, Kitani et al. 2020). Do you have any explanation for the difference between your findings, or do you think that there might be a timing and/or activation state control switch that determines which way BTK goes to regulate NLRP3 inflammasome activity?
  2. Is there any evidence suggesting that an apparent decrease in NLRP3 activity might be either detrimental or beneficial to patients with XLA? Can this information be used to further focus therapies targeting the NLRP3 inflammasome?

 

References

Abbate, A., A. C. Morton, et al. (2015). “Anti-inflammatory therapies in myocardial infarction.” Lancet 385(9987): 2573-2574.

Chen, J. and Z. J. Chen (2018). “PtdIns4P on dispersed trans-Golgi network mediates NLRP3 inflammasome activation.” Nature 564(7734): 71-76.

Copeland, S., H. S. Warren, et al. (2005). “Acute inflammatory response to endotoxin in mice and humans.” Clin Diagn Lab Immunol 12(1): 60-67.

Ito, M., T. Shichita, et al. (2015). “Bruton’s tyrosine kinase is essential for NLRP3 inflammasome activation and contributes to ischaemic brain injury.” Nature communications 6: 7360.

Khan, W. N. (2012). “Colonel Bruton’s kinase defined the molecular basis of X-linked agammaglobulinemia, the first primary immunodeficiency.” J Immunol 188(7): 2933-2935.

Kondo, K., H. Shaim, et al. (2018). “Ibrutinib modulates the immunosuppressive CLL microenvironment through STAT3-mediated suppression of regulatory B-cell function and inhibition of the PD-1/PD-L1 pathway.” Leukemia 32(4): 960-970.

Liu, X., T. Pichulik, et al. (2017). “Human NACHT, LRR, and PYD domain-containing protein 3 (NLRP3) inflammasome activity is regulated by and potentially targetable through Bruton tyrosine kinase.” J Allergy Clin Immunol.

Mao, L., A. Kitani, et al. (2020). “Bruton tyrosine kinase deficiency augments NLRP3 inflammasome activation and causes IL-1beta-mediated colitis.” J Clin Invest.

Mao, L., A. Kitani, et al. (2020). “Bruton tyrosine kinase deficiency augments NLRP3 inflammasome activation and causes IL-1β–mediated colitis.” The Journal of Clinical Investigation 130(4): 1793-1807.

McNally, G. A., J. M. Long, et al. (2015). “Ibrutinib: Implications for Use in the Treatment of Mantle Cell Lymphoma and Chronic Lymphocytic Leukemia.” J Adv Pract Oncol 6(5): 420-431.

Mishima, Y., A. Oka, et al. (2019). “Microbiota maintain colonic homeostasis by activating TLR2/MyD88/PI3K signaling in IL-10-producing regulatory B cells.” J Clin Invest 130: 3702-3716.

Opal, S. M., P. J. Scannon, et al. (1999). “Relationship between plasma levels of lipopolysaccharide (LPS) and LPS-binding protein in patients with severe sepsis and septic shock.” J Infect Dis 180(5): 1584-1589.

Roschewski, M., M. S. Lionakis, et al. (2020). “Inhibition of Bruton tyrosine kinase in patients with severe COVID-19.” Sci Immunol 5(48).

Sattler, S., G. S. Ling, et al. (2014). “IL-10-producing regulatory B cells induced by IL-33 (Breg(IL-33)) effectively attenuate mucosal inflammatory responses in the gut.” J Autoimmun 50: 107-122.

Schmidt, E. G., H. L. Larsen, et al. (2012). “B cells exposed to enterobacterial components suppress development of experimental colitis.” Inflamm Bowel Dis 18(2): 284-293.

Wang, L., A. Ray, et al. (2015). “T regulatory cells and B cells cooperate to form a regulatory loop that maintains gut homeostasis and suppresses dextran sulfate sodium-induced colitis.” Mucosal Immunol 8(6): 1297-1312.

Yanaba, K., A. Yoshizaki, et al. (2011). “IL-10-producing regulatory B10 cells inhibit intestinal injury in a mouse model.” Am J Pathol 178(2): 735-743.

Zweigner, J., H. J. Gramm, et al. (2001). “High concentrations of lipopolysaccharide-binding protein in serum of patients with severe sepsis or septic shock inhibit the lipopolysaccharide response in human monocytes.” Blood 98(13): 3800-3808.

 

 

 

Tags: btk, golgi, inflammasome, kinase, nlrp3, regulation

Posted on: 14 July 2020

doi: https://doi.org/10.1242/prelights.23060

Read preprint (1 votes)

Author's response

Alexander N. R. Weber shared

Q1: BTK has also been shown to inhibit inflammasome activity(Mao, Kitani et al. 2020). Do you have any explanation for the difference between your findings, or do you think that there might be a timing and/or activation state control switch that determines which way BTK goes to regulate NLRP3 inflammasome activity?

A1: The first thing to note is that Mao et al. (Mao, Kitani et al. 2020) completely reproduce our data in that at physiological LPS concentrations in the low ng/ml range, (Opal, Scannon et al. 1999; Zweigner, Gramm et al. 2001; Copeland, Warren et al. 2005), BTK loss in murine BMDM and human XLA cells leads to a drop in IL-1b secretion.

We now favour the idea that under physiological LPS conditions, BTK becomes active at the dTGN to phosphorylate NLRP3 that has reached the Golgi and has formed nuclei (Chen and Chen 2018), to promote its release towards the cytosol. Our work suggests that this phospho-event cancels charge attraction to trans-Golgi network (TGN) phosphatidylinositols, releasing NLRP3 from the TGN. However, unphysiologically high LPS may cause a more dramatic BTK activation that is not confined to the TGN anymore. Consequently, BTK would phosphorylate incoming monomeric NLRP, preventing its association onto TGN membranes. As a consequence, nucleation assisted by aggregation on TGN versicles is precluded, leading to lower inflammasome seeding and consequently a drop in IL-1b levels in the presence of BTK, whereas its absence my re-instate NLRP3 localization to the Golgi. In any case, Mao et al. provide the important point that BTK may be a rheostat for NLRP3 activation, boosting IL-1b release under normal conditions but possibly restricting it under very high LPS conditions as could be expected in fulminant sepsis. What more could you ask for than a self-regulating inflammasome ‘tuning device’, BTK?

Q2: Is there any evidence suggesting that an apparent decrease in NLRP3 activity might be either detrimental or beneficial to patients with XLA? Can this information be used to further focus therapies targeting the NLRP3 inflammasome?

A2: Our previous work on XLA patients and patients treated with ibrutinib in vivo indicates that under typical LPS or ibrutinib dosage levels, targeting BTK would restrict IL-1b release (Liu, Pichulik et al. 2017). Mao et al. observe the same (Mao, Kitani et al. 2020). For XLA patients this may be a problem: they do not only lack functional B cells and hence antibodies (Khan 2012), but a concomitant impairment of their IL-1b axis may also limit the capability of their innate immune defences as well. The gastrointestinal inflammatory phenotype noted by Mao et al. for XLA patients and the observations from their DSS colitis in vivo model might be taken as a rationale for targeting must be interpreted with caution as lack/inhibition of BTK in both models is known to cause the loss of regulatory B cells which restrict intestinal inflammation in mice and patients (Yanaba, Yoshizaki et al. 2011; Schmidt, Larsen et al. 2012; Sattler, Ling et al. 2014; Wang, Ray et al. 2015; Mishima, Oka et al. 2019)(McNally, Long et al. 2015; Kondo, Shaim et al. 2018). Although limiting IL-1b (produced possibly via NLRC4 or NLRP6 rather than NLRP3) by anti-IL-1 strategies in the DSS in vivo model is beneficial, we could caution against systemically targeting the NLRP3-IL-1 axis in already immunocompromised XLA patients. We think BTK or NLRP3 inhibition may rather be suitable for treating short term inflammation, e.g. in the wake of stroke (Ito, Shichita et al. 2015), heart attack (Abbate, Morton et al. 2015) or – as recently studied – in COVID-19-related lung inflammation (Roschewski, Lionakis et al. 2020). Here a recent report observed macrophage BTK activation and a beneficial effect of ibrutinib that is probably attributable to blocking the NLRP3 inflammasome (Roschewski, Lionakis et al. 2020). Further pre-clinical and clinical studies of BTK and NLRP3 inhibitors may address this question more precisely in future.

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