2,203
Views
11
CrossRef citations to date
0
Altmetric
Original Research

Evidence for interaction of the NLRP3 inflammasome and Bruton’s tyrosine kinase in tumor-associated macrophages: implications for myeloid cell production of interleukin-1beta

, , , , , , , & ORCID Icon show all
Article: 1659704 | Received 26 Apr 2019, Accepted 21 Aug 2019, Published online: 05 Sep 2019

References

  • Yang L, Zhang Y. Tumor-associated macrophages: from basic research to clinical application. J Hematol Oncol. 2017;10:1. doi:10.1186/s13045-017-0430-2.
  • Benner B, Scarberry L, Suarez-Kelly LP, Duggan MC, Campbell AR, Smith E, Lapurga G, Jiang K, Butchar JP, Tridandapani S, et al. Generation of monocyte-derived tumor-associated macrophages using tumor-conditioned media provides a novel method to study tumor-associated macrophages in vitro. J ImmunoTher Cancer. 2019;7:140. doi:10.1186/s40425-019-0622-0.
  • Lee J, Wan J, Lee L, Peng C, Xie H, Lee C. Study of the NLRP3 inflammasome component genes and downstream cytokines in patients with type 2 diabetes mellitus with carotid atherosclerosis. Lipids Health Dis. 2017;16:217. doi:10.1186/s12944-017-0595-2.
  • Ghonime MG, Shamaa OR, Das S, Eldomany RA, Fernandes-Alnemri T, Alnemri ES, Gavrilin MA, Wewers MD. Inflammasome priming by lipopolysaccharide is dependent upon ERK signaling and proteasome function. J Immunol. 2014;192:3881–13. doi:10.4049/jimmunol.1301974.
  • Mariathasan S, Weiss DS, Newton K, McBride J, O’Rourke K, Roose-Girma M, Lee WP, Weinrauch Y, Monack DM, Dixit VM. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature. 2006;440:228–232. doi:10.1038/nature04515.
  • Perregaux D, Gabel CA. Interleukin-1 beta maturation and release in response to ATP and nigericin. Evidence that potassium depletion mediated by these agents is a necessary and common feature of their activity. J Biol Chem. 1994;269:15195–15203.
  • Heid ME, Keyel PA, Kamga C, Shiva S, Watkins SC, Salter RD. Mitochondrial reactive oxygen species induces NLRP3-dependent lysosomal damage and inflammasome activation. J Immunol. 2013;191:5230–5238. doi:10.4049/jimmunol.1301490.
  • Sha W, Mitoma H, Hanabuchi S, Bao M, Weng L, Sugimoto N, Liu Y, Zhang Z, Zhong J, Sun B, et al. Human NLRP3 inflammasome senses multiple types of bacterial RNAs. Proc Natl Acad Sci U S A. 2014;111:16059–16064. doi:10.1073/pnas.1412487111.
  • Broz P, Monack DM. Molecular mechanisms of inflammasome activation during microbial infections. Immunol Rev. 2011;243:174–190. doi:10.1111/j.1600-065X.2011.01041.x.
  • Dubois H, Wullaert A, Lamkanfi M. General strategies in inflammasome biology. In: Inflammasome signaling and bacterial infections. Cham: Springer; 2016. p. 1–22. doi: 10.1007/978-3-319-41171-2_1
  • Ito M, Shichita T, Okada M, Komine R, Noguchi Y, Yoshimura A, Morita R. Bruton’s tyrosine kinase is essential for NLRP3 inflammasome activation and contributes to ischaemic brain injury. Nat Commun. 2015;6:7360. doi:10.1038/ncomms8360.
  • Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun. 2005;73:1907–1916. doi:10.1128/IAI.73.4.1907-1916.2005.
  • Elkabets M, Ribeiro VSG, Dinarello CA, Ostrand‐Rosenberg S, Di Santo JP, Apte RN, Vosshenrich CA.IL-1β regulates a novel myeloid-derived suppressor cell subset that impairs NK cell development and function. Eur J Immunol. 2010;40:3347–3357. doi:10.1002/eji.201041037.
  • Rip J, de Bruijn MJW, Appelman MK, Pal Singh S, Hendriks RW, Corneth OB.Toll-like receptor signaling drives btk-mediated autoimmune disease. Front Immunol. 2019;10:95. doi:10.3389/fimmu.2019.00095.
  • Marron TU. The role of BTK in TLR signaling. J Allergy Clin Immunol. 2009;123:S92–S92. doi:10.1016/j.jaci.2008.12.329.
  • Levy O. Bruton tyrosine kinase (Btk): key for signaling via toll-like receptor 8. Blood. 2007;109:2273–2274. doi:10.1182/blood-2006-12-064642.
  • Burger JA, Wiestner A. Targeting B cell receptor signalling in cancer: preclinical and clinical advances. Nat Rev Cancer. 2018;18:148–167. doi:10.1038/nrc.2017.121.
  • Seda V, Mraz M. B-cell receptor signalling and its crosstalk with other pathways in normal and malignant cells. Eur J Haematol. 2015;94:193–205. doi:10.1111/ejh.12427.
  • Xia B, Qu F, Yuan T, Zhang Y. Targeting Bruton’s tyrosine kinase signaling as an emerging therapeutic agent of B-cell malignancies. Oncol Lett. 2015;10:3339. doi:10.3892/OL.2015.3802.
  • Woyach JA, Johnson AJ, Byrd JC. The B-cell receptor signaling pathway as a therapeutic target in CLL. Blood. 2012;120:1175–1184. doi:10.1182/blood-2012-02-362624.
  • Stiff A, Trikha P, Wesolowski R, et al. Myeloid-derived suppressor cells express bruton’s tyrosine kinase and can be depleted in tumor-bearing hosts by ibrutinib treatment. Cancer Res. 2016;76:2125–2136. doi:10.1158/0008-5472.CAN-15-1490.
  • Fiedler K, Sindrilaru A, Terszowski G, Kokai E, Feyerabend TB, Bullinger L, Rodewald H-R, Brunner C. Neutrophil development and function critically depend on Bruton tyrosine kinase in a mouse model of X-linked agammaglobulinemia. Blood. 2011;117:1329–1339. doi:10.1182/blood-2010-04-281170.
  • Mueller H, Stadtmann A, Van Aken H, Hirsch E, Wang D, Ley K, Zarbock A. Tyrosine kinase Btk regulates E-selectin-mediated integrin activation and neutrophil recruitment by controlling phospholipase C (PLC) 2 and PI3K pathways. Blood. 2010;115:3118–3127. doi:10.1182/blood-2009-11-254185.
  • Honda F, Kano H, Kanegane H, Nonoyama S, Kim E-S, Lee S-K, Takagi M, Mizutani S, Morio T. The kinase Btk negatively regulates the production of reactive oxygen species and stimulation-induced apoptosis in human neutrophils. Nat Immunol. 2012;13:369–378. doi:10.1038/ni.2234.
  • Chang BY, Huang MM, Francesco M, Chen J, Sokolove J, Magadala P, Robinson WH, Buggy JJ. The Bruton tyrosine kinase inhibitor PCI-32765 ameliorates autoimmune arthritis by inhibition of multiple effector cells. Arthritis Res Ther. 2011;13:R115. doi:10.1186/ar3400.
  • Dubovsky JA, Beckwith KA, Natarajan G, et al. Ibrutinib is an irreversible molecular inhibitor of ITK driving a Th1-selective pressure in T lymphocytes. Blood. 2013;122:2539–2549. doi:10.1182/blood-2013-06-507947.
  • Janda E, Palmieri C, Pisano A, Pontoriero M, Iaccino E, Falcone C, Fiume G, Gaspari M, Nevolo M, Di Salle E, et al. Btk regulation in human and mouse B cells via protein kinase C phosphorylation of IBtkγ. Blood. 2011;117:6520–6531. doi:10.1182/blood-2010-09-308080.
  • Fridman WH, Pagès F, Sautès-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer. 2012;12:298–306. doi:10.1038/nrc3245.
  • Duggan MC, Regan-Fendt K, Olaverria GN, Howard JH, Stiff AR, Sabella J, Latchana N, Markowitz J, Gru A, Tridandapani S, et al. Neuroblastoma RAS viral oncogene homolog mRNA is differentially spliced to give five distinct isoforms: implications for melanoma therapy. Melanoma Res. 2019:1. doi:10.1097/CMR.0000000000000623.
  • Stiff A, Trikha P, Mundy-Bosse B, McMichael E, Mace TA, Benner B, Kendra K, Campbell A, Gautam S, Abood D, et al. Nitric oxide production by myeloid-derived suppressor cells plays a role in impairing Fc receptor–mediated natural killer cell function. Clin Cancer Res. 2018;24:1891–1904. doi:10.1158/1078-0432.CCR-17-0691.
  • Mace TA, Shakya R, Pitarresi JR, Swanson B, McQuinn CW, Loftus S, Nordquist E, Cruz-Monserrate Z, Yu L, Young G, et al. IL-6 and PD-L1 antibody blockade combination therapy reduces tumour progression in murine models of pancreatic cancer. Gut. 2018;67:320–332. doi:10.1136/gutjnl-2016-311585.
  • Chalons P, Amor S, Courtaut F, Cantos-Villar E, Richard T, Auger C, Chabert P, Schni-Kerth V, Aires V, Delmas D. Study of potential anti-inflammatory effects of red wine extract and resveratrol through a modulation of interleukin-1-beta in macrophages. Nutrients. 2018:10. doi:10.3390/nu10121856.
  • Edlund H, Lee SK, Andrew MA, Slatter JG, Aksenov S, Al-Huniti N. Population pharmacokinetics of the BTK inhibitor acalabrutinib and its active metabolite in healthy volunteers and patients with B-cell malignancies. Clin Pharmacokinet. 2018. doi:10.1007/s40262-018-0725-7.
  • Liu X, Pichulik T, Wolz -O-O, Dang T-M, Stutz A, Dillen C, Delmiro Garcia M, Kraus H, Dickhöfer S, Daiber E, et al. 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. 2017;140:1054–1067.e10. doi:10.1016/j.jaci.2017.01.017.
  • Horwood NJ, Page TH, McDaid JP, Palmer CD, Campbell J, Mahon T, Brennan FM, Webster D, Foxwell BMJ. Bruton’s tyrosine kinase is required for TLR2 and TLR4-induced TNF, but not IL-6, production. J Immunol. 2006;176:3635–3641. doi:10.4049/jimmunol.176.6.3635.
  • Kakoschky B, Pleli T, Schmithals C, Zeuzem S, Brüne B, Vogl TJ, Korf H-W, Weigert A, Piiper A, Mondelli MU. Selective targeting of tumor associated macrophages in different tumor models. PLoS One. 2018;13:e0193015. doi:10.1371/journal.pone.0193015.
  • Eriksson U, Kurrer MO, Sonderegger I, et al. Activation of dendritic cells through the interleukin 1 receptor 1 is critical for the induction of autoimmune myocarditis. J Exp Med. 2003;197:323–331. doi:10.1084/jem.20021788.
  • Bent R, Moll L, Grabbe S, Bros M. Interleukin-1 beta-A friend or foe in malignancies? Int J Mol Sci. 2018:19. doi:10.3390/ijms19082155.
  • Guo B, Fu S, Zhang J, Liu B, Li Z. Targeting inflammasome/IL-1 pathways for cancer immunotherapy. Sci Rep. 2016;6:36107. doi:10.1038/srep36107.
  • Georgoudaki A-M, Prokopec KE, Boura VF, Hellqvist E, Sohn S, Östling J, Dahan R, Harris R, Rantalainen M, Klevebring D, et al. Reprogramming tumor-associated macrophages by antibody targeting inhibits cancer progression and metastasis. Cell Rep. 2016;15:2000–2011. doi:10.1016/j.celrep.2016.04.084.
  • Luo Y, Zhou H, Krueger J, et al. Targeting tumor-associated macrophages as a novel strategy against breast cancer. J Clin Invest. 2006;116:2132–2141. doi:10.1172/JCI27648.
  • Duan X, He K, Li J, Cheng M, Song H, Liu J, Liu P. Tumor associated macrophages deliver iron to tumor cells via Lcn2. Int J Physiol Pathophysiol Pharmacol. 2018;10:105.
  • Makela AV, Gaudet JM, Foster PJ. Quantifying tumor associated macrophages in breast cancer: a comparison of iron and fluorine-based MRI cell tracking. Sci Rep. 2017;7:42109. doi:10.1038/srep42109.
  • Moossavi M, Parsamanesh N, Bahrami A, Atkin SL, Sahebkar A. Role of the NLRP3 inflammasome in cancer. Mol Cancer. 2018;17:158. doi:10.1186/s12943-018-0900-3.
  • Kolb R, Liu G-H, Janowski AM, Sutterwala FS, Zhang W. Inflammasomes in cancer: a double-edged sword. Protein Cell. 2014;5:12–20. doi:10.1007/s13238-013-0001-4.
  • Umansky V, Sevko A. Tumor microenvironment and myeloid-derived suppressor cells. Cancer Microenviron. 2013;6:169–177. doi:10.1007/s12307-012-0126-7.
  • Najjar YG, Rayman P, Jia X, Pavicic PG, Rini BI, Tannenbaum C, Ko J, Haywood S, Cohen P, Hamilton T, et al. Myeloid-derived suppressor cell subset accumulation in renal cell carcinoma parenchyma is associated with intratumoral expression of IL1β, IL8, CXCL5, and Mip-1α. Clin Cancer Res. 2017;23:2346–2355. doi:10.1158/1078-0432.CCR-15-1823.
  • Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140:883–899. doi:10.1016/j.cell.2010.01.025.
  • Perwez Hussain S, Harris CC. Inflammation and cancer: an ancient link with novel potentials. Int J Cancer. 2007;121:2373–2380. doi:10.1002/ijc.23173.
  • Berraondo P, Minute L, Ajona D, Corrales L, Melero I, Pio R. Innate immune mediators in cancer: between defense and resistance. Immunol Rev. 2016;274:290–306. doi:10.1111/imr.12464.
  • Pal Singh S, Dammeijer F, Hendriks RW. Role of Bruton’s tyrosine kinase in B cells and malignancies. Mol Cancer. 2018;17:57. doi:10.1186/s12943-018-0779-z.
  • Weber ANR, Bittner Z, Liu X, Dang T-M, Radsak MP, Brunner C. Bruton’s tyrosine kinase: an emerging key player in innate immunity. Front Immunol. 2017;8:1454. doi:10.3389/fimmu.2017.01454.
  • Lust JA, Lacy MQ, Zeldenrust SR, Witzig TE, Moon-Tasson LL, Dinarello CA, Donovan KA. Reduction in C-reactive protein indicates successful targeting of the IL-1/IL-6 axis resulting in improved survival in early stage multiple myeloma. Am J Hematol. 2016;91:571–574. doi:10.1002/ajh.24352.
  • Lust JA, Lacy MQ, Zeldenrust SR, Dispenzieri A, Gertz MA, Witzig TE, Kumar S, Hayman SR, Russell SJ, Buadi FK, et al. Induction of a chronic disease state in patients with smoldering or indolent multiple myeloma by targeting interleukin 1β-induced interleukin 6 production and the myeloma proliferative component. Mayo Clin Proc. 2009;84:114–122. doi:10.4065/84.2.114.
  • Wu Z, Han X, Qin S, Zheng Q, Wang Z, Xiang D, Zhang J, Lu H, Wu M, Zhu S, et al. Interleukin 1 receptor antagonist reduces lethality and intestinal toxicity of 5-fluorouracil in a mouse mucositis model. Biomed Pharmacother. 2010;64:589–593. doi:10.1016/j.biopha.2010.06.006.
  • Wang X, Gao J, Qian L, Gao J, Zhu S, Wu M, Zhang Y, Guan W, Ye H, Yu Y, et al. Exogenous IL-1Ra attenuates intestinal mucositis induced by oxaliplatin and 5-fluorouracil through suppression of p53-dependent apoptosis. Anticancer Drugs. 2015;26:35–45. doi:10.1097/CAD.0000000000000142.
  • Sauter KAD, Wood LJ, Wong J, Iordanov M, Magun BE. Doxorubicin and daunorubicin induce processing and release of interleukin-1β through activation of the NLRP3 inflammasome. Cancer Biol Ther. 2011;11:1008–1016. doi:10.4161/cbt.11.12.15540.
  • Hickish T, Andre T, Wyrwicz L, et al. MABp1 as a novel antibody treatment for advanced colorectal cancer: a randomised, double-blind, placebo-controlled, phase 3 study. Lancet Oncol. 2017;18:192–201. doi:10.1016/S1470-2045(17)30006-2.
  • De Mooij CEM, Netea MG, Van Der Velden WJFM, Blijlevens NMA. Targeting the interleukin-1 pathway in patients with hematological disorders. Blood. 2017. doi:10.1182/blood-2016-12-754994.
  • Perera AP, Fernando R, Shinde T, Gundamaraju R, Southam B, Sohal SS, Robertson AAB, Schroder K, Kunde D, Eri R. MCC950, a specific small molecule inhibitor of NLRP3 inflammasome attenuates colonic inflammation in spontaneous colitis mice. Sci Rep. 2018;8:8618. doi:10.1038/s41598-018-26775-w.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.