Galectin-3 plays an important pro-inflammatory role in the induction phase of acute colitis by promoting activation of NLRP3 inflammasome and production of IL-1β in macrophages

Journal of Crohn's and Colitis

Volumn 10, Issue 5, 2016, Pages 593-606

  Simovic Markovic, Bojana ^a   Nikolic, Aleksandar ^a   Gazdic, Marina ^a   Bojic, Sanja ^a   Vucicevic, Ljubica ^b   Kosic, Milica ^b   Mitrovic, Slobodanka ^c   Milosavljevic, Milos ^c   Besra, Gurdyal ^d   Trajkovic, Vladimir ^b   Arsenijevic, Nebojsa ^a   Lukic, Miodrag L ^a   Volarevic, Vladislav ^a  

^a University of Kragujevac Medical Faculty   (Serbia)

^b UNIVERSITY OF BELGRADE   (Serbia)

^c CLINICAL CENTER KRAGUJEVAC   (Serbia)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

DSS colitis; Gal 3; NLRP3

Indexed keywords

B7 ANTIGEN; BACTERIUM LIPOPOLYSACCHARIDE; CD45 ANTIGEN; CRYOPYRIN; DOCUSATE SODIUM; GALECTIN 3; GLYCOPROTEIN P 15095; INFLAMMASOME; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; RIBOZYME; TUMOR NECROSIS FACTOR ALPHA; BIOLOGICAL MARKER; CYTOKINE; DEXTRAN SULFATE; NLRP3 PROTEIN, MOUSE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CELL TRANSFER; CLINICAL ARTICLE; COLITIS; COLON; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DEXTRAN SODIUM SULFATE-INDUCED COLITIS; DISEASE COURSE; DISEASE SEVERITY; GENE DELETION; HISTOCHEMISTRY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPHENOTYPING; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE FUNCTION; LYMPHOCYTE FUNCTION; MACROPHAGE ACTIVATION; MALE; MOUSE; NATURAL KILLER T CELL; NEUTROPHIL; NEUTROPHIL COUNT; NONHUMAN; PATHOGENESIS; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; T LYMPHOCYTE ACTIVATION; WILD TYPE; ACUTE DISEASE; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CASE CONTROL STUDY; CHEMICALLY INDUCED; DEFICIENCY; FLOW CYTOMETRY; IMMUNOLOGY; MACROPHAGE; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEVERITY OF ILLNESS INDEX; TRANSGENIC MOUSE; ULCERATIVE COLITIS;

ACUTE DISEASE; ANIMALS; BIOMARKERS; CASE-CONTROL STUDIES; COLITIS; COLITIS, ULCERATIVE; COLON; CYTOKINES; DEXTRAN SULFATE; FLOW CYTOMETRY; GALECTIN 3; HUMANS; INFLAMMASOMES; INTERLEUKIN-1BETA; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEVERITY OF ILLNESS INDEX;

EID: 84982223827     PISSN: 18739946     EISSN: 18764479     Source Type: Journal    
DOI: 10.1093/ecco-jcc/jjw013     Document Type: Article

References (41)

1. Volarevic V, Milovanovic M, Ljujic B, et al. Galectin-3 Deficiency Prevents Concanavalin A-Induced Hepatitis in Mice. Hepatology 2012;55:1954-64.
2. Jiang H-R, Al Rasebi Z, Mensah-Brown E, et al. Galectin-3 Deficiency Reduces the Severity of Experimental Autoimmune Encephalomyelitis. J Immunol 2009;182;1167-73.
3. Mensah-Brown EP, Al Rabesi Z, Shahin A, et al. Targeted disruption of the galectin-3 gene results in decreased susceptibility to multiple low dose streptozotocin-induced diabetes in mice. Clin Immunol 2009;130;83-8.
4. Radosavljevic G, Jovanovic I, Majstorovic I, et al. Deletion of galectin-3 in the host attenuates metastasis of murine melanoma by modulating tumor adhesion and NK cell activity. Clin Exp Metastasis 2011;28:451-62.
5. Radosavljevic G, Volarevic V, Jovanovic I, et al. The roles of Galectin-3 in autoimmunity and tumor progression. Immunol Res 2012;52:100-10.
6. Volarevic V, Lukic ML. Autoimmune disorders in galectin-3 deficient mice. In: Klyosov A, Traber P, editors. Galectins and Disease Implications in Targeted Therapeutics. Washington, DC: American Chemical Society; 2012:359-76.
7. Pejnovic N, Pantic J, Jovanovic I, et al. Galectin-3 Deficiency Accelerates High-Fat Diet Induced Obesity and Amplifies Inflammation in Adipose Tissue and Pancreatic Islets. Diabetes 2013;62:1932-44.
8. Frol'ová L, Smetana K Jr, Borovská D, et al. Detection of galectin-3 in patients with inflammatory bowel diseases: new serum marker of active forms of IBD? Inflamm Res 2009;58:503-12.
9. Müller S, Schaffer T, Flogerzi B, et al. Galectin-3 modulates T cell activity and is reduced in the inflamed intestinal epithelium in IBD. Inflamm Bowel Dis 2006;12:588-97.
10. Brazowski E, Dotan I, Tulchinsky H, et al. Galectin-3 expression in pouchitis in patients with ulcerative colitis who underwent ileal pouch-anal anastomosis [IPAA]. Pathol Res Pract 2009;205:551-8.
11. Perše M, Cerar A. Dextran sodium sulphate colitis mouse model: traps and tricks. J Biomed Biotechnol 2012;2012:718617.
12. Berndt BE, Zhang M, Chen GH, et al. The role of dendritic cells in the development of acute dextran sulfate sodium colitis. J Immunol 2007;179:6255-62.
13. Dieleman LA, Ridwan BU, Tennyson GS, et al. Dextran sulfate sodiuminduced colitis occurs in severe combined immunodeficient mice. Gastroenterology 1994;107:1643-52.
14. Liu FT, Hsu DK. The role of galectin-3 in promotion of the inflammatory response. Drug News Perspect 2007;20:455-60.
15. Hsu DK, Chernyavsky AI, Chen HY, et al. Endogenous galectin-3 is localized in membrane lipid rafts and regulates migration of dendritic cells. J Invest Dermatol 2009;129:573-83.
16. Mathieu A, Nagy N, Decaestecker C, et al. Expression of galectins-1,-3 and-4 varies with strain and type of experimental colitis in mice. Int J Exp Pathol 2008;89:438-46.
17. Volarevic V, Markovic BS, Bojic S, et al. Gal-3 regulates the capacity of dendritic cells to promote NKT-cell-induced liver injury. Eur J Immunol 2014;45:531-43.
18. Hsu DK, Yang RY, Pan Z, et al. Targeted disruption of the galectin-3 gene results in attenuated peritoneal inflammatory responses. Am J Pathol 2000;156:1073-83.
19. Okayasu I, Hatakeyama S, Yamada M, et al. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990;98:694-702.
20. Traber PG, Chou H, Zomer E, et al. Regression of fibrosis and reversal of cirrhosis in rats by galectin inhibitors in thioacetamide-induced liver disease. PLoS One 2013;8:e75361.
21. Murthy S, Cooper H, Shim H, et al. Treatment of dextran sulfate sodium-induced murine colitis by intracolonic cyclosporine. Dig Dis Sci 1993;38:1722-34.
22. Whittem CG, Williams AD, Williams CS. Murine Colitis Modeling using Dextran Sulfate Sodium. J Vis Exp 2010;35:1652.
23. Obermeier F, Kojouharoff G, Hans W, et al. Interferon-gamma [IFNgamma]-and tumour necrosis factor [TNF]-induced nitric oxide as toxic effector molecule in chronic dextran sulphate sodium [DSS]-induced colitis in mice. Clin Exp Immunol 1999;116:238-45.
24. Vandesompele J, De Preter K, Pattyn F, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002;3:research0034.
25. Viennois E, Chen F, Laroui H, et al. Dextran sodium sulfate inhibits the activities of both polymerase and reverse transcriptase: lithium chloride purification, a rapid and efficient technique to purify RNA. BMC Res Notes 2013;6:360.
26. Scheiffele F, Fuss IJ. Induction of TNBS Colitis in Mice. Curr Protoc Immunol 2002;15:15.19.
27. Bauer C, Duewell P, Mayer C, et al. Colitis induced in mice with dextran sulfate sodium [DSS] is mediated by the NLRP3 inflammasome. Gut 2010;59:1192-9.
28. Medina-Contreras O, Geem D, Laur O, et al. CX3CR1 regulates intestinal macrophage homeostasis, bacterial translocation, and colitogenic Th17 responses in mice. J Clin Invest 2011;121:4787-95.
29. Weisser SB, van Rooijen N, Sly LM. Depletion and reconstitution of macrophages in mice. J Vis Exp 2012;66:4105.
30. Murphy CT, Moloney G, Hall LJ, et al. Use of bioluminescence imaging to track neutrophil migration and its inhibition in experimental colitis. Clin Exp Immunol 2010;162:188-96.
31. Zindl CL, Lai JF, Lee YK, et al. IL-22-producing neutrophils contribute to antimicrobial defense and restitution of colonic epithelial integrity during colitis. Proc Natl Acad Sci U S A 2013;110:12768-73.
32. Abe K, Nguyen KP, Fine SD, et al. Conventional dendritic cells regulate the outcome of colonic inflammation independently of T cells. Proc Natl Acad Sci U S A 2007;104:17022-7.
33. Kim HS, Chung DH. IL-9-producing invariant NKT cells protect against DSS-induced colitis in an IL-4-dependent manner. Mucosal Immunol 2013;6:347-57.
34. Saubermann LJ, Beck P, De Jong YP, et al. Activation of natural killer T cells by alpha-galactosylceramide in the presence of CD1d provides protection against colitis in mice. Gastroenterology 2000;119:119-28.
35. Qiao Y, Wang P, Qi J, et al. TLR-induced NF-κB activation regulates NLRP3 expression in murine macrophages. FEBS Lett 2012;586:1022-6.
36. Guarda G, Zenger M, Yazdi AS, et al. Differential expression of NLRP3 among hematopoietic cells. J Immunol 2011;186:2529-34.
37. Chassaing B, Aitken JD, Malleshappa M, Vijay-Kumar M. Dextran sulfate sodium [DSS]-induced colitis in mice. Curr Protoc Immunol 2014;4;104:Unit 15.25.
38. Fermino ML, Polli CD, Toledo KA, et al. LPS-induced galectin-3 oligomerization results in enhancement of neutrophil activation. PLoS One 2011;6:e26004.
39. Jeftic I, Jovicic N, Pantic J, et al. Galectin-3 Ablation Enhances Liver Steatosis, but Attenuates Inflammation and IL-33 Dependent Fibrosis in Obesogenic Mouse Model of Nonalcoholic Steatohepatitis. Mol Med 2015; 21:453-65.
40. D'Odorico A, D'Inca R, Mestriner C, et al. Influence of disease site and activity on peripheral neutrophil function in inflammatory bowel disease. Dig Dis Sci 2000;45:1594-600.
41. Steinbeck MJ, Roth JA, Kaeberle ML. Activation of bovine neutrophils by recombinant interferon-gamma. Cell Immunol 1986;98:137-44.