CCL11 exacerbates colitis and inflammation-associated colon tumorigenesis.
Journal
Oncogene
ISSN: 1476-5594
Titre abrégé: Oncogene
Pays: England
ID NLM: 8711562
Informations de publication
Date de publication:
11 2021
11 2021
Historique:
received:
24
03
2021
accepted:
28
09
2021
revised:
14
09
2021
pubmed:
10
10
2021
medline:
4
1
2022
entrez:
9
10
2021
Statut:
ppublish
Résumé
CCL11, also known as eotaxin-1, is described as an eosinophil chemoattractant, which has been implicated in allergic and Th2 inflammatory diseases. We have reported that CCL11 is significantly increased in the serum of inflammatory bowel disease (IBD) patients, colonic eosinophils are increased and correlate with tissue CCL11 levels in ulcerative colitis patients, and CCL11 is increased in dextran sulfate sodium (DSS)-induced murine colitis. Here, we show that CCL11 is involved in the pathogenesis of DSS-induced colitis and in colon tumorigenesis in the azoxymethane (AOM)-DSS model of colitis-associated carcinogenesis (CAC). Ccl11
Identifiants
pubmed: 34625710
doi: 10.1038/s41388-021-02046-3
pii: 10.1038/s41388-021-02046-3
pmc: PMC8629429
mid: NIHMS1757187
doi:
Substances chimiques
Carcinogens
0
Ccl11 protein, mouse
0
Chemokine CCL11
0
Azoxymethane
MO0N1J0SEN
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
6540-6546Subventions
Organisme : NCI NIH HHS
ID : P01 CA028842
Pays : United States
Organisme : NIDDK NIH HHS
ID : T32 DK007673
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK128200
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA190612
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK058404
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA116087
Pays : United States
Organisme : BLRD VA
ID : IK2 BX002126
Pays : United States
Organisme : NCI NIH HHS
ID : P50 CA236733
Pays : United States
Organisme : BLRD VA
ID : I01 BX004366
Pays : United States
Organisme : NIDDK NIH HHS
ID : U24 DK059637
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA068485
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM008554
Pays : United States
Organisme : CSRD VA
ID : I01 CX002171
Pays : United States
Informations de copyright
© 2021. This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply.
Références
Dahlhamer JM, Zammitti EP, Ward BW, Wheaton AG, Croft JB. Prevalence of inflammatory bowel disease among adults aged >/=18 years—United States, 2015. MMWR Morb Mortal Wkly Rep. 2016;65:1166–9.
doi: 10.15585/mmwr.mm6542a3
Eaden JA, Abrams KR, Mayberry JF. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut. 2001;48:526–35.
doi: 10.1136/gut.48.4.526
Sartor RB. Cytokines in intestinal inflammation: pathophysiological and clinical considerations. Gastroenterology. 1994;106:533–9.
doi: 10.1016/0016-5085(94)90614-9
Olen O, Erichsen R, Sachs MC, Pedersen L, Halfvarson J, Askling J, et al. Colorectal cancer in ulcerative colitis: a Scandinavian population-based cohort study. Lancet. 2020;395:123–31.
doi: 10.1016/S0140-6736(19)32545-0
Coburn LA, Horst SN, Chaturvedi R, Brown CT, Allaman MM, Scull BP, et al. High-throughput multi-analyte Luminex profiling implicates eotaxin-1 in ulcerative colitis. PLoS ONE. 2013;8:e82300.
doi: 10.1371/journal.pone.0082300
Ahrens R, Waddell A, Seidu L, Blanchard C, Carey R, Forbes E, et al. Intestinal macrophage/epithelial cell-derived CCL11/eotaxin-1 mediates eosinophil recruitment and function in pediatric ulcerative colitis. J Immunol. 2008;181:7390–9.
doi: 10.4049/jimmunol.181.10.7390
Scoville EA, Allaman MM, Adams DW, Motley AK, Peyton SC, Ferguson SL, et al. Serum polyunsaturated fatty acids correlate with serum cytokines and clinical disease activity in Crohn’s disease. Sci Rep. 2019;9:2882.
doi: 10.1038/s41598-019-39232-z
Gobert AP, Al-Greene NT, Singh K, Coburn LA, Sierra JC, Verriere TG, et al. Distinct immunomodulatory effects of spermine oxidase in colitis induced by epithelial injury or infection. Front Immunol. 2018;9:1242.
doi: 10.3389/fimmu.2018.01242
Manousou P, Kolios G, Valatas V, Drygiannakis I, Bourikas L, Pyrovolaki K, et al. Increased expression of chemokine receptor CCR3 and its ligands in ulcerative colitis: the role of colonic epithelial cells in in vitro studies. Clin Exp Immunol. 2010;162:337–47.
doi: 10.1111/j.1365-2249.2010.04248.x
Coburn LA, Singh K, Asim M, Barry DP, Allaman MM, Al-Greene NT, et al. Loss of solute carrier family 7 member 2 exacerbates inflammation-associated colon tumorigenesis. Oncogene. 2019;38:1067–79.
doi: 10.1038/s41388-018-0492-9
Hol J, Wilhelmsen L, Haraldsen G. The murine IL-8 homologues KC, MIP-2, and LIX are found in endothelial cytoplasmic granules but not in Weibel-Palade bodies. J Leukoc Biol. 2010;87:501–8.
doi: 10.1189/jlb.0809532
Chandrasekar B, Deobagkar-Lele M, Victor ES, Nandi D. Regulation of chemokines, CCL3 and CCL4, by interferon gamma and nitric oxide synthase 2 in mouse macrophages and during Salmonella enterica serovar Typhimurium infection. J Infect Dis. 2013;207:1556–68.
doi: 10.1093/infdis/jit067
Zimmerman NP, Vongsa RA, Wendt MK, Dwinell MB. Chemokines and chemokine receptors in mucosal homeostasis at the intestinal epithelial barrier in inflammatory bowel disease. Inflamm Bowel Dis. 2008;14:1000–11.
doi: 10.1002/ibd.20480
Singh K, Chaturvedi R, Barry DP, Coburn LA, Asim M, Lewis ND, et al. The apolipoprotein E-mimetic peptide COG112 inhibits NF-kappaB signaling, proinflammatory cytokine expression, and disease activity in murine models of colitis. J Biol Chem. 2011;286:3839–50.
doi: 10.1074/jbc.M110.176719
Rmali KA, Puntis MC, Jiang WG. Tumour-associated angiogenesis in human colorectal cancer. Colorectal Dis. 2007;9:3–14.
doi: 10.1111/j.1463-1318.2006.01089.x
Quante M, Varga J, Wang TC, Greten FR. The gastrointestinal tumor microenvironment. Gastroenterology. 2013;145:63–78.
doi: 10.1053/j.gastro.2013.03.052
Karki R, Kanneganti TD. Diverging inflammasome signals in tumorigenesis and potential targeting. Nat Rev Cancer. 2019;19:197–214.
doi: 10.1038/s41568-019-0123-y
Adar T, Shteingart S, Ben Ya’acov A, Bar-Gil Shitrit A, Goldin E. From airway inflammation to inflammatory bowel disease: eotaxin-1, a key regulator of intestinal inflammation. Clin Immunol. 2014;153:199–208.
doi: 10.1016/j.clim.2014.04.012
Beck LA, Tancowny B, Brummet ME, Asaki SY, Curry SL, Penno MB, et al. Functional analysis of the chemokine receptor CCR3 on airway epithelial cells. J Immunol. 2006;177:3344–54.
doi: 10.4049/jimmunol.177.5.3344
Popivanova BK, Kostadinova FI, Furuichi K, Shamekh MM, Kondo T, Wada T, et al. Blockade of a chemokine, CCL2, reduces chronic colitis-associated carcinogenesis in mice. Cancer Res. 2009;69:7884–92.
doi: 10.1158/0008-5472.CAN-09-1451
Forbes E, Murase T, Yang M, Matthaei KI, Lee JJ, Lee NA, et al. Immunopathogenesis of experimental ulcerative colitis is mediated by eosinophil peroxidase. J Immunol. 2004;172:5664–75.
doi: 10.4049/jimmunol.172.9.5664
Adar T, Shteingart S, Ben-Ya’acov A, Shitrit AB, Livovsky DM, Shmorak S, et al. The importance of intestinal eotaxin-1 in inflammatory bowel disease: new insights and possible therapeutic implications. Dig Dis Sci. 2016;61:1915–24.
doi: 10.1007/s10620-016-4047-z
Hardbower DM, Coburn LA, Asim M, Singh K, Sierra JC, Barry DP, et al. EGFR-mediated macrophage activation promotes colitis-associated tumorigenesis. Oncogene. 2017;36:3807–19.
doi: 10.1038/onc.2017.23
Barrett CW, Fingleton B, Williams A, Ning W, Fischer MA, Washington MK, et al. MTGR1 is required for tumorigenesis in the murine AOM/DSS colitis-associated carcinoma model. Cancer Res. 2011;71:1302–12.
doi: 10.1158/0008-5472.CAN-10-3317
Beaugerie L, Itzkowitz SH. Cancers complicating inflammatory bowel disease. N. Engl J Med. 2015;372:1441–52.
doi: 10.1056/NEJMra1403718
Vieira AT, Fagundes CT, Alessandri AL, Castor MG, Guabiraba R, Borges VO, et al. Treatment with a novel chemokine-binding protein or eosinophil lineage-ablation protects mice from experimental colitis. Am J Pathol. 2009;175:2382–91.
doi: 10.2353/ajpath.2009.090093
Masterson JC, McNamee EN, Fillon SA, Hosford L, Harris R, Fernando SD, et al. Eosinophil-mediated signalling attenuates inflammatory responses in experimental colitis. Gut. 2015;64:1236–47.
doi: 10.1136/gutjnl-2014-306998
Reichman H, Itan M, Rozenberg P, Yarmolovski T, Brazowski E, Varol C, et al. Activated eosinophils exert antitumorigenic activities in colorectal cancer. Cancer Immunol Res. 2019;7:388–400.
doi: 10.1158/2326-6066.CIR-18-0494
Kaiko GE, Horvat JC, Beagley KW, Hansbro PM. Immunological decision-making: how does the immune system decide to mount a helper T-cell response? Immunology. 2008;123:326–38.
doi: 10.1111/j.1365-2567.2007.02719.x
Arango Duque G, Descoteaux A. Macrophage cytokines: involvement in immunity and infectious diseases. Front Immunol. 2014;5:491.
doi: 10.3389/fimmu.2014.00491
Ferhat M, Hablot J, Taieb M, Salem F, Netter P, Peyrin-Biroulet L, et al. Lack of protective effect of CCR3 blockade during experimental colitis may be related to CCR3 expression by colonic Tregs. Clin Transl Med. 2021;11:e455.
doi: 10.1002/ctm2.455
Levina V, Nolen BM, Marrangoni AM, Cheng P, Marks JR, Szczepanski MJ, et al. Role of eotaxin-1 signaling in ovarian cancer. Clin Cancer Res. 2009;15:2647–56.
doi: 10.1158/1078-0432.CCR-08-2024
Komura T, Yano M, Miyake A, Takabatake H, Miyazawa M, Ogawa N, et al. Immune condition of colorectal cancer patients featured by serum chemokines and gene expressions of CD4 + cells in blood. Can J Gastroenterol Hepatol. 2018;2018:7436205.
doi: 10.1155/2018/7436205
Wagsater D, Lofgren S, Hugander A, Dienus O, Dimberg J. Analysis of single nucleotide polymorphism in the promoter and protein expression of the chemokine eotaxin-1 in colorectal cancer patients. World J Surg Oncol. 2007;5:84.
doi: 10.1186/1477-7819-5-84
Heidegger I, Hofer J, Luger M, Pichler R, Klocker H, Horninger W, et al. Is eotaxin-1 a serum and urinary biomarker for prostate cancer detection and recurrence? Prostate. 2015;75:1904–9.
doi: 10.1002/pros.23086
Agarwal M, He C, Siddiqui J, Wei JT, Macoska JA. CCL11 (eotaxin-1): a new diagnostic serum marker for prostate cancer. Prostate. 2013;73:573–81.
doi: 10.1002/pros.22597