Myeloid-derived miR-223 regulates intestinal inflammation via repression of the NLRP3 inflammasome

doi:10.1084/jem.20160462

. 2017 Jun 5;214(6):1737-1752.

doi: 10.1084/jem.20160462. Epub 2017 May 9.

Myeloid-derived miR-223 regulates intestinal inflammation via repression of the NLRP3 inflammasome

Viola Neudecker^{1

2}, Moritz Haneklaus³, Owen Jensen^{4

2}, Ludmila Khailova², Joanne C Masterson^{5

4}, Hazel Tye^{6

7}, Kathryn Biette^{5

4}, Paul Jedlicka⁸, Kelley S Brodsky², Mark E Gerich^{9

4}, Matthias Mack¹⁰, Avril A B Robertson¹¹, Matthew A Cooper¹¹, Glenn T Furuta^{5

4}, Charles A Dinarello^{12

13}, Luke A O'Neill³, Holger K Eltzschig^{14

2}, Seth L Masters^{6

7}, Eóin N McNamee^{15

2}

Affiliations

¹ Clinic for Anesthesiology, University Hospital of Ludwig-Maximilians-University, 80539 Munich, Germany.
² Department of Anesthesiology, School of Medicine, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045.
³ School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland.
⁴ Mucosal Inflammation Program, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045.
⁵ Gastrointestinal Eosinophilic Disease Program, Section of Pediatric Gastroenterology, Hepatology, and Nutrition, Children's Hospital Colorado, Aurora, CO 80045.
⁶ Division of Inflammation, The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC 3052, Australia.
⁷ Department of Medical Biology, The University of Melbourne, Parkville, VIC 3010, Australia.
⁸ Department of Pathology, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045.
⁹ Division of Gastroenterology and Hepatology, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045.
¹⁰ Department of Internal Medicine II, University Hospital Regensburg, 93053 Regensburg, Germany.
¹¹ Institute for Molecular Bioscience, The University of Queensland, Brisbane City, QLD 4067, Australia.
¹² Department of Medicine, Radboud University Medical Center, 6525 GA Nijmegen, Netherlands.
¹³ Department of Medicine, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045.
¹⁴ Department of Anesthesiology, University of Texas Medical School at Houston, Houston, TX 77030.
¹⁵ Mucosal Inflammation Program, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045 eoin.mcnamee@ucdenver.edu.

PMID: 28487310
PMCID: PMC5460990
DOI: 10.1084/jem.20160462

Myeloid-derived miR-223 regulates intestinal inflammation via repression of the NLRP3 inflammasome

Viola Neudecker et al. J Exp Med. 2017.

. 2017 Jun 5;214(6):1737-1752.

doi: 10.1084/jem.20160462. Epub 2017 May 9.

Authors

Affiliations

¹ Clinic for Anesthesiology, University Hospital of Ludwig-Maximilians-University, 80539 Munich, Germany.
² Department of Anesthesiology, School of Medicine, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045.
³ School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland.
⁴ Mucosal Inflammation Program, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045.
⁵ Gastrointestinal Eosinophilic Disease Program, Section of Pediatric Gastroenterology, Hepatology, and Nutrition, Children's Hospital Colorado, Aurora, CO 80045.
⁶ Division of Inflammation, The Walter and Eliza Hall Institute of Medical Research, Parkville, VIC 3052, Australia.
⁷ Department of Medical Biology, The University of Melbourne, Parkville, VIC 3010, Australia.
⁸ Department of Pathology, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045.
⁹ Division of Gastroenterology and Hepatology, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045.
¹⁰ Department of Internal Medicine II, University Hospital Regensburg, 93053 Regensburg, Germany.
¹¹ Institute for Molecular Bioscience, The University of Queensland, Brisbane City, QLD 4067, Australia.
¹² Department of Medicine, Radboud University Medical Center, 6525 GA Nijmegen, Netherlands.
¹³ Department of Medicine, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045.
¹⁴ Department of Anesthesiology, University of Texas Medical School at Houston, Houston, TX 77030.
¹⁵ Mucosal Inflammation Program, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045 eoin.mcnamee@ucdenver.edu.

PMID: 28487310
PMCID: PMC5460990
DOI: 10.1084/jem.20160462

Abstract

MicroRNA (miRNA)-mediated RNA interference regulates many immune processes, but how miRNA circuits orchestrate aberrant intestinal inflammation during inflammatory bowel disease (IBD) is poorly defined. Here, we report that miR-223 limits intestinal inflammation by constraining the nlrp3 inflammasome. miR-223 was increased in intestinal biopsies from patients with active IBD and in preclinical models of intestinal inflammation. miR-223^-/y mice presented with exacerbated myeloid-driven experimental colitis with heightened clinical, histopathological, and cytokine readouts. Mechanistically, enhanced NLRP3 inflammasome expression with elevated IL-1β was a predominant feature during the initiation of colitis with miR-223 deficiency. Depletion of CCR2⁺ inflammatory monocytes and pharmacologic blockade of IL-1β or NLRP3 abrogated this phenotype. Generation of a novel mouse line, with deletion of the miR-223 binding site in the NLRP3 3' untranslated region, phenocopied the characteristics of miR-223^-/y mice. Finally, nanoparticle-mediated overexpression of miR-223 attenuated experimental colitis, NLRP3 levels, and IL-1β release. Collectively, our data reveal a previously unappreciated role for miR-223 in regulating the innate immune response during intestinal inflammation.

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Figures

**Figure 1.**
**miR-223 regulates acute intestinal inflammation.** (A) hsa-miR-223 expression was assessed in intestinal mucosal biopsies from patients with either CD or UC. n = 4–10 patients/group; statistical significance determined by ANOVA with Bonferroni’s multiple comparison test. (B) DSS (3% wt/vol) was administered in drinking water ad libitum to B6.WT mice. Colonic mmu-miR-223 expression was determined from mice undergoing DSS-colitis (days 0, 2, 4, and 6). n = 3–5 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (C) Histopathology scores from DSS-colitis on days 0, 2, 4, and 6 of treatment (3% wt/vol). n = 5 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (D) Neutrophils were depleted with 300 µg (i.p.) anti-Ly6G (1A8) or isotype control on days 0 and 1 after DSS. Monocytes were depleted with 20 µg (i.p.) anti-CCR2 (MC21) or isotype control on days 0 and 1 after DSS. Mice were euthanized on day 2 after DSS, and miR-223 expression was analyzed in colon tissues. n = 5 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (E) Weight loss during DSS-colitis was expressed as the percentage of change from day 0. n = 9 mice/group; statistical significance determined by unpaired Student’s t test. (F) Clinical DAI was a composite of weight change (percentage of day 0), stool score, and occult blood index. n = 9 mice/group; statistical significance determined by unpaired Student’s t test. (G) Colon lengths of DSS-treated mice were assessed at the time of necropsy with representative macroscopic images. n = 9 mice/group; statistical significance determined by unpaired Student’s t test. (H) Histopathology scores from WT and *miR-223^-/y* colons after DSS-colitis. n = 9 mice/group; statistical significance determined by unpaired Student’s t test. (I) Representative micrographs of colon H&E from WT and *miR-223^-/y* mice 6 d after DSS-colitis. Data are expressed as mean ± SEM; *, P < 0.05; **, P < 0.01; ***, P < 0.001 versus the indicated counterparts from three independent experiments. Bars, 100 µm.

**Figure 2.**
**Hematopoietic-derived miR-223 constrains experimental DSS-colitis.** BM chimeric mice were generated after irradiation of WT (CD45.1) or *miR-223^-/y* (CD45.2) mice. 8 wk after irradiation, DSS was administered in drinking water ad libitum (3% wt/vol) for 6 d. (A) Clinical DAI was a composite of weight changes (percentage of day 0), stool score, and occult blood index. n = 5–10 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (B) Colon lengths were assessed at the time of necropsy, and representative macroscopic images were acquired. n = 5 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (C) Histopathology scores from WT and *miR-223^-/y* colons. n = 5–10 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (D) Representative micrographs of colon H&E from WT and *miR-223^-/y* mice 6 d after DSS-colitis. Data are expressed as mean ± SEM; *, P < 0.05; **, P < 0.01; ***, P < 0.001 versus WT counterpart from two independent experiments. Bars, 100 µm.

**Figure 3.**
**Onset of colitis in *miR-223^-/y* mice is characterized by the enhanced expression of IL-1β and influx of neutrophils and monocytes.** DSS was administered in drinking water ad libitum (3% wt/vol) to WT and *miR-223^-/y* mice for 2 d. (A–D) Flow cytometry characterized collagenase digested colons for the presence of live, CD45⁺ CD11b⁺ myeloid cells that were neutrophils (Ly6G⁺ MHCII⁻; A), monocytes (Ly6C⁺ MHCII⁻; B), intermediate monocytes (Ly6C⁺ MHCII⁺; C), macrophages (Ly6C⁻ MHCII⁺; D), and dendritic cells (MHCII⁺ CD11c⁺ CD11b⁻; E). n = 4 mice/group; statistical significance determined by two-way ANOVA with Bonferroni test. (F) Inflammatory cytokine expression was quantified in whole colon tissues from WT or *miR-223^-/y* mice after DSS by LEGENDplex bead array (see Materials and methods) or ELISA (IL-18). n = 4 mice/group; statistical significance determined by unpaired Student’s t test. (G–I) Relative gene expression of the neutrophil and monocyte chemokines CXCL1 (G), CXCL2 (H), and CCL2 (I) was measured by RT-PCR from whole colon tissue and expressed relative to 18s. n = 5 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. Data are expressed as mean ± SEM; *, P < 0.05; **, P < 0.01 versus the indicated counterpart from two independent experiments.

**Figure 4.**
**Increased NLRP3 inflammasome activity in BMDMs and colons from *miR-223^-/y* mice during DSS-colitis.** (A) Schematic of in silico miR-223 binding sequence to the 3′ UTR of the mouse NLRP3 and conservation across multiple species. (B) ELISA measurement of IL-1β in whole colon biopsies from WT and *miR-233^-/y* mice on day 6 after DSS-colitis. n = 5 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (C) Western immunoblot assessment of NLRP3, pro–IL-1β, cleaved IL-1β, ASC, and β-actin in whole colon biopsies from WT and *miR-233^-/y* mice on day 6 after DSS-colitis. Representative immunoblot from three independent mice. (D) Western immunoblot assessment of NLRP3, IL-1β, and β-actin in BMDM after 6-h treatment with media vehicle or LPS (100 ng/ml). Representative immunoblot from three independent mice. (E–J) BMDMs were cultured for 5 d and primed with LPS (100 ng/ml) for 3 h, and NLRP3 was activated with ATP (1 mM) for 3 h. Gene expression of IL-1β (E), IL-18 (F), and TNF (G) were assessed by quantitative PCR. n = 3–4 mice/group; statistical significance determined by two-way ANOVA with Bonferroni test. Secreted cytokines IL-1β (H), IL-18 (I), and TNF (J), were quantified in cell-free supernatants by ELISA. n = 3–4 mice/group; statistical significance determined by two-way ANOVA with Bonferroni test. Data are expressed as mean ± SEM; *, P < 0.05; **, P < 0.001 versus the indicated counterpart from two independent experiments.

**Figure 5.**
**Depletion of CCR2⁺ monocytes attenuates DSS-colitis and IL-1β in *miR-223^-/y* mice.** DSS was administered in drinking water ad libitum (3% wt/vol) for 6 d to *miR-223^-/y* mice. Mice were treated on days 0–5 with anti-Ly6G (1A8; 300 µg/d, i.p.), anti-CCR2 (MC21; 20 µg/d, i.p.), or isotype vehicles and euthanized 24 h after the final treatment. (A) Representative flow cytometry analysis from *miR-223^-/y* mice subjected to DSS (3% wt/vol; day 2). (B) Neutrophils were identified as live, CD45⁺ singlets, SSC-A^high GR1^high CD11b⁺; monocytes were identified as live, CD45⁺ singlets, SSC-A^high GR1^int CD11b⁺. n = 3 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (C) Histopathology scores from *miR-223^-/y* mice after DSS-colitis. n = 5 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (D) Representative micrographs of colon H&E from *miR-223^-/y* mice after DSS-colitis. (E) IL-1β was measured by ELISA from whole colon tissue. n = 5 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (F–J) mRNA for IL-1β (F), TNF (G), IL-6 (H), CXCL1 (I), and iNOS (J) was assessed by QPCR from whole colon tissue. n = 4–5 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. Data are expressed as mean ± SEM; *, P < 0.05; **, P < 0.01; ***, P < 0.001 versus the indicated counterpart from two independent experiments. Bars, 100 µm.

**Figure 6.**
**Inhibition of NLRP3 or IL-1β attenuates DSS-colitis in *miR-223^-/y* mice**. DSS was administered in drinking water ad libitum (3% wt/vol) for 6 d to WT and *miR-223^-/y* mice. *miR-223^-/y* mice received the small molecule inhibitor of NLRP3, MCC950 (20 mg/kg/d, i.p.); the IL-1 receptor antagonist, anakinra (20 mg/kg/d, i.p.); or saline vehicle and were euthanized 24 h after the final treatment. (A) Weight loss during colitis was expressed as the percentage of change from day 0. n = 7–9 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (B) Clinical DAI was a composite of weight changes (percentage of day 0), stool score, and occult blood index. n = 7–9 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (C) Colon lengths of DSS-treated mice were assessed at the time of necropsy. n = 6–9 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (D) Representative macroscopic images of colons after treatment. (E) Histopathology scores from WT and *miR-223^-/y* colons after DSS-colitis. n = 6–9 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (F) Representative micrographs of colon H&E from WT and *miR-223^-/y* mice after treatment. (G and H) Flow cytometry–characterized collagenase digested colons for the presence of live, CD45⁺ CD11b⁺ myeloid cells that were neutrophils (Ly6G⁺ MHCII^-; G) and monocytes (Ly6C⁺ MHCII^-; H). n = 3–5 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. (I–K) Inflammatory cytokine expression was quantified in whole colon tissues from WT or *miR-223^-/y* mice after treatment by LEGENDplex bead array (see Materials and methods). n = 5–7 mice/group; statistical significance determined by ANOVA with Newman–Keuls multiple comparison test. Data are expressed as mean ± SEM; *, P < 0.05; **, P < 0.01; ***, P < 0.001 versus the indicated counterparts from two independent experiments. Bars, 100 µm.

**Figure 7.**
*Nlrp3^m223del* mice display increased NLRP3 activation in vitro and susceptibility to DSS-colitis. (A) Neutrophils were cultured ex vivo from WT (+/+) or *Nlrp3^m223del* (del/del) mice and stimulated with LPS (1 or 100 ng/ml) for 3 h, as indicated. Samples were lysed in SDS loading buffer and NLRP3, and β-actin protein expression was analyzed by Western immunoblot. Representative immunoblot from three independent mice. (B and C) Neutrophils were cultured with LPS (100 ng/ml) for 3 h, followed by 3 h with nigericin (10 mM), and supernatants were collected for IL-1β (B) or TNF (C) measurement by ELISA. n = 4 mice/group; statistical significance determined by unpaired Student’s t test. DSS was administered in drinking water ad libitum (3% wt/vol) for 6 d to WT and *Nlrp3^m223del* mice. (D) Weight loss during colitis was expressed as the percentage of change from day 0. n = 3 mice/group; statistical significance determined by unpaired Student’s t test. (E) Colon lengths were assessed at the time of necropsy from WT and *Nlrp3^m223del* mice after DSS. n = 3 mice/group; statistical significance determined by unpaired Student’s t test. (F) Histopathology scores from WT and *Nlrp3^m223del* colons after DSS. n = 3 mice/group; statistical significance determined by unpaired Student’s t test. (G) Representative micrographs of colon H&E from WT and *Nlrp3^m223del* mice after DSS-colitis. (H) The frequencies of monocytes, macrophages, and neutrophils were analyzed in WT and *Nlrp3^m223del* mice by flow cytometry as a percentage of myeloid cells (gated on CD45⁺ CD11b⁺ cells) in the colon at day 2 after DSS treatment. n = 3 mice/group; statistical significance determined by unpaired Student’s t test. Data are expressed as mean ± SEM; *, P < 0.05; **, P < 0.01 versus the indicated counterparts. Data are representative of two independent experiments with three to four mice per group. Bars, 1 mm.

**Figure 8.**
**Nanoparticle delivery of an miR-223 mimetic attenuates experimental DSS-colitis.** DSS was administered in drinking water ad libitum (3% wt/vol) for 6 d to WT mice. Mice were treated with 50 µg (via retro-orbital injection) of either control (Cel-miR239b) or miR-223 mimetic in a nanoparticle solution on days 1 and 3 after DSS administration. (A) miR-223 expression was measured in whole colon tissue by QPCR on day 4 after DSS. (B) Weight loss during treatment was expressed as the percentage of change from day 0. n = 9 mice/group; statistical significance determined by unpaired Student’s t test. (C) Clinical DAI was a composite of weight changes (percentage of day 0), stool score, and bleeding index. n = 9 mice/group; statistical significance determined by unpaired Student’s t test. (D) Colonic histopathology scores after treatment. n = 9 mice/group; statistical significance determined by unpaired Student’s t test. (E) Representative micrographs of colon H&E from treated mice after DSS-colitis. (F) Western immunoblot assessment of NLRP3, ASC, and β-actin in whole colon biopsies. Representative immunoblots from three independent mice. (G) Relative mRNA was assessed by quantitative PCR for NLRP3. n = 3–5 mice/group; statistical significance determined by unpaired Student’s t test. (H) ELISA measurement of IL-1β whole colon biopsies. n = 3–5 mice/group; statistical significance determined by unpaired Student’s t test. (I) Relative mRNA was assessed by QPCR for IL-1, TNF, IL-6, and CXCL1 in whole colon tissues. n = 3–5 mice/group; statistical significance determined by unpaired Student’s t test. Data are expressed as mean ± SEM; *, P < 0.05; **, P < 0.01 versus the indicated counterpart from two independent experiments. Bars, 100 µm.

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References

1. Allen I.C., TeKippe E.M., Woodford R.M., Uronis J.M., Holl E.K., Rogers A.B., Herfarth H.H., Jobin C., and Ting J.P.. 2010. The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer. J. Exp. Med. 207:1045–1056. 10.1084/jem.20100050 - DOI - PMC - PubMed
1. Andres P.G., Beck P.L., Mizoguchi E., Mizoguchi A., Bhan A.K., Dawson T., Kuziel W.A., Maeda N., MacDermott R.P., Podolsky D.K., and Reinecker H.C.. 2000. Mice with a selective deletion of the CC chemokine receptors 5 or 2 are protected from dextran sodium sulfate-mediated colitis: Lack of CC chemokine receptor 5 expression results in a NK1.1+ lymphocyte-associated Th2-type immune response in the intestine. J. Immunol. 164:6303–6312. 10.4049/jimmunol.164.12.6303 - DOI - PubMed
1. Baek D., Villén J., Shin C., Camargo F.D., Gygi S.P., and Bartel D.P.. 2008. The impact of microRNAs on protein output. Nature. 455:64–71. 10.1038/nature07242 - DOI - PMC - PubMed
1. Bamias G., Corridoni D., Pizarro T.T., and Cominelli F.. 2012. New insights into the dichotomous role of innate cytokines in gut homeostasis and inflammation. Cytokine. 59:451–459. 10.1016/j.cyto.2012.06.014 - DOI - PMC - PubMed
1. Bauer C., Duewell P., Mayer C., Lehr H.A., Fitzgerald K.A., Dauer M., Tschopp J., Endres S., Latz E., and Schnurr M.. 2010. Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome. Gut. 59:1192–1199. 10.1136/gut.2009.197822 - DOI - PubMed

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[1] Allen I.C., TeKippe E.M., Woodford R.M., Uronis J.M., Holl E.K., Rogers A.B., Herfarth H.H., Jobin C., and Ting J.P.. 2010. The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer. J. Exp. Med. 207:1045–1056. 10.1084/jem.20100050 - DOI - PMC - PubMed

[2] Allen I.C., TeKippe E.M., Woodford R.M., Uronis J.M., Holl E.K., Rogers A.B., Herfarth H.H., Jobin C., and Ting J.P.. 2010. The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer. J. Exp. Med. 207:1045–1056. 10.1084/jem.20100050 - DOI - PMC - PubMed

[3] Andres P.G., Beck P.L., Mizoguchi E., Mizoguchi A., Bhan A.K., Dawson T., Kuziel W.A., Maeda N., MacDermott R.P., Podolsky D.K., and Reinecker H.C.. 2000. Mice with a selective deletion of the CC chemokine receptors 5 or 2 are protected from dextran sodium sulfate-mediated colitis: Lack of CC chemokine receptor 5 expression results in a NK1.1+ lymphocyte-associated Th2-type immune response in the intestine. J. Immunol. 164:6303–6312. 10.4049/jimmunol.164.12.6303 - DOI - PubMed

[4] Andres P.G., Beck P.L., Mizoguchi E., Mizoguchi A., Bhan A.K., Dawson T., Kuziel W.A., Maeda N., MacDermott R.P., Podolsky D.K., and Reinecker H.C.. 2000. Mice with a selective deletion of the CC chemokine receptors 5 or 2 are protected from dextran sodium sulfate-mediated colitis: Lack of CC chemokine receptor 5 expression results in a NK1.1+ lymphocyte-associated Th2-type immune response in the intestine. J. Immunol. 164:6303–6312. 10.4049/jimmunol.164.12.6303 - DOI - PubMed

[5] Baek D., Villén J., Shin C., Camargo F.D., Gygi S.P., and Bartel D.P.. 2008. The impact of microRNAs on protein output. Nature. 455:64–71. 10.1038/nature07242 - DOI - PMC - PubMed

[6] Baek D., Villén J., Shin C., Camargo F.D., Gygi S.P., and Bartel D.P.. 2008. The impact of microRNAs on protein output. Nature. 455:64–71. 10.1038/nature07242 - DOI - PMC - PubMed

[7] Bamias G., Corridoni D., Pizarro T.T., and Cominelli F.. 2012. New insights into the dichotomous role of innate cytokines in gut homeostasis and inflammation. Cytokine. 59:451–459. 10.1016/j.cyto.2012.06.014 - DOI - PMC - PubMed

[8] Bamias G., Corridoni D., Pizarro T.T., and Cominelli F.. 2012. New insights into the dichotomous role of innate cytokines in gut homeostasis and inflammation. Cytokine. 59:451–459. 10.1016/j.cyto.2012.06.014 - DOI - PMC - PubMed

[9] Bauer C., Duewell P., Mayer C., Lehr H.A., Fitzgerald K.A., Dauer M., Tschopp J., Endres S., Latz E., and Schnurr M.. 2010. Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome. Gut. 59:1192–1199. 10.1136/gut.2009.197822 - DOI - PubMed

[10] Bauer C., Duewell P., Mayer C., Lehr H.A., Fitzgerald K.A., Dauer M., Tschopp J., Endres S., Latz E., and Schnurr M.. 2010. Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome. Gut. 59:1192–1199. 10.1136/gut.2009.197822 - DOI - PubMed

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Myeloid-derived miR-223 regulates intestinal inflammation via repression of the NLRP3 inflammasome

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Myeloid-derived miR-223 regulates intestinal inflammation via repression of the NLRP3 inflammasome

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