Intestinal Sulfation Is Essential to Protect Against Colitis and Colonic Carcinogenesis

Bray, 2018, Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries, CA Cancer J Clin, 68, 394, 10.3322/caac.21492 Siegel, 2020, Cancer statistics, 2020, CA Cancer J Clin, 70, 7, 10.3322/caac.21590 Ten Broeke, 2018, Molecular background of colorectal tumors from patients with Lynch syndrome associated with germline variants in PMS2, Gastroenterology, 155, 844, 10.1053/j.gastro.2018.05.020 Luo, 2019, Intestinal PPARalpha protects against colon carcinogenesis via regulation of methyltransferases DNMT1 and PRMT6, Gastroenterology, 157, 744, 10.1053/j.gastro.2019.05.057 Rhodes, 2002, Inflammation and colorectal cancer: IBD-associated and sporadic cancer compared, Trends Mol Med, 8, 10, 10.1016/S1471-4914(01)02194-3 De Robertis, 2011, The AOM/DSS murine model for the study of colon carcinogenesis: from pathways to diagnosis and therapy studies, J Carcinog, 10, 9 Murphy, 2019, Lifestyle and dietary environmental factors in colorectal cancer susceptibility, Mol Aspects Med, 69, 2, 10.1016/j.mam.2019.06.005 Kauffman, 2004, Sulfonation in pharmacology and toxicology, Drug Metab Rev, 36, 823, 10.1081/DMR-200033496 Leung, 2016, Sulfonation, an underexploited area: from skeletal development to infectious diseases and cancer, Oncotarget, 7, 55811, 10.18632/oncotarget.10046 Mueller, 2018, Human DHEA sulfation requires direct interaction between PAPS synthase 2 and DHEA sulfotransferase SULT2A1, J Biol Chem, 293, 9724, 10.1074/jbc.RA118.002248 Miyake, 2012, PAPSS2 mutations cause autosomal recessive brachyolmia, J Med Genet, 49, 533, 10.1136/jmedgenet-2012-101039 Faiyaz ul Haque, 1998, Mutations in orthologous genes in human spondyloepimetaphyseal dysplasia and the brachymorphic mouse, Nat Genet, 20, 157, 10.1038/2458 Oostdijk, 2015, PAPSS2 deficiency causes androgen excess via impaired DHEA sulfation—in vitro and in vivo studies in a family harboring two novel PAPSS2 mutations, J Clin Endocrinol Metab, 100, E672, 10.1210/jc.2014-3556 Noordam, 2009, Inactivating PAPSS2 mutations in a patient with premature pubarche, N Engl J Med, 360, 2310, 10.1056/NEJMoa0810489 Dawson, 2009, Reduced mucin sulfonation and impaired intestinal barrier function in the hyposulfataemic NaS1 null mouse, Gut, 58, 910, 10.1136/gut.2007.147595 Corfield, 1996, Colonic mucins in ulcerative colitis: evidence for loss of sulfation, Glycoconj J, 13, 809, 10.1007/BF00702345 Raouf, 1992, Sulphation of colonic and rectal mucin in inflammatory bowel disease: reduced sulphation of rectal mucus in ulcerative colitis, Clin Sci (Lond), 83, 623, 10.1042/cs0830623 Hong, 2007, A susceptibility gene set for early onset colorectal cancer that integrates diverse signaling pathways: implication for tumorigenesis, Clin Cancer Res, 13, 1107, 10.1158/1078-0432.CCR-06-1633 Kim, 2012, Investigating intestinal inflammation in DSS-induced model of IBD, J Vis Exp, 60, e3678 Chen, 2008, Rectal prolapse as initial clinical manifestation of colon cancer, Z Gastroenterol, 46, 348 Lee, 2016, The effect of sex on the azoxymethane/dextran sulfate sodium-treated mice model of colon cancer, J Cancer Prev, 21, 271, 10.15430/JCP.2016.21.4.271 Martinez, 2010, Quantification by computerized morphometry of tissue levels of sulfomucins and sialomucins in diversion colitis in rats, Acta Cir Bras, 25, 231, 10.1590/S0102-86502010000300004 Deplancke, 2001, Microbial modulation of innate defense: goblet cells and the intestinal mucus layer, Am J Clin Nutr, 73, 1131S, 10.1093/ajcn/73.6.1131S Matsuo, 1997, Histochemistry of the surface mucous gel layer of the human colon, Gut, 40, 782, 10.1136/gut.40.6.782 Garbacz, 2018, Chronic activation of liver X receptor sensitizes mice to high cholesterol diet-induced gut toxicity, Mol Pharmacol, 94, 1145, 10.1124/mol.118.112672 Li, 2018, Nanoliposome C6-ceramide increases the anti-tumor immune response and slows growth of liver tumors in mice, Gastroenterology, 154, 1024, 10.1053/j.gastro.2017.10.050 Johansson, 2014, Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis, Gut, 63, 281, 10.1136/gutjnl-2012-303207 Gadaleta, 2017, Bile acids and colon cancer: is FXR the solution of the conundrum?, Mol Aspects Med, 56, 66, 10.1016/j.mam.2017.04.002 Alnouti, 2009, Bile acid sulfation: a pathway of bile acid elimination and detoxification, Toxicol Sci, 108, 225, 10.1093/toxsci/kfn268 Tang, 2017, GEPIA: a web server for cancer and normal gene expression profiling and interactive analyses, Nucleic Acids Res, 45, W98, 10.1093/nar/gkx247 Martens, 2018, Interactions of commensal and pathogenic microorganisms with the intestinal mucosal barrier, Nat Rev Microbiol, 16, 457, 10.1038/s41579-018-0036-x Gendler, 1995, Epithelial mucin genes, Annu Rev Physiol, 57, 607, 10.1146/annurev.ph.57.030195.003135 McGuckin, 2011, Mucin dynamics and enteric pathogens, Nat Rev Microbiol, 9, 265, 10.1038/nrmicro2538 Van der Sluis, 2006, Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection, Gastroenterology, 131, 117, 10.1053/j.gastro.2006.04.020 Velcich, 2002, Colorectal cancer in mice genetically deficient in the mucin Muc2, Science, 295, 1726, 10.1126/science.1069094 Tobisawa, 2010, Sulfation of colonic mucins by N-acetylglucosamine 6-O-sulfotransferase-2 and its protective function in experimental colitis in mice, J Biol Chem, 285, 6750, 10.1074/jbc.M109.067082 Lee, 2000, The human renal sodium sulfate cotransporter (SLC13A1; hNaSi-1) cDNA and gene: organization, chromosomal localization, and functional characterization, Genomics, 70, 354, 10.1006/geno.2000.6404 Jia, 2018, Bile acid-microbiota crosstalk in gastrointestinal inflammation and carcinogenesis, Nat Rev Gastroenterol Hepatol, 15, 111, 10.1038/nrgastro.2017.119 Modica, 2008, Nuclear bile acid receptor FXR protects against intestinal tumorigenesis, Cancer Res, 68, 9589, 10.1158/0008-5472.CAN-08-1791 Maran, 2009, Farnesoid X receptor deficiency in mice leads to increased intestinal epithelial cell proliferation and tumor development, J Pharmacol Exp Ther, 328, 469, 10.1124/jpet.108.145409 Fu, 2019, FXR regulates intestinal cancer stem cell proliferation, Cell, 176, 1098, 10.1016/j.cell.2019.01.036 Wang, 2017, Analyzing the properties of murine intestinal mucins by electrophoresis and histology, BioProtocol, 7, e2394 Haque, 2004, Early interactions of Salmonella enterica serovar typhimurium with human small intestinal epithelial explants, Gut, 53, 1424, 10.1136/gut.2003.037382 Hudson, 2013, Role for cytoplasmic nucleotide hydrolysis in hepatic function and protein synthesis, Proc Natl Acad Sci U S A, 110, 5040, 10.1073/pnas.1205001110 Jiang, 2015, Intestinal farnesoid X receptor signaling promotes nonalcoholic fatty liver disease, J Clin Invest, 125, 386, 10.1172/JCI76738 Zhu, 2018, Identification of novel pathways in idelalisib metabolism and bioactivation, Chem Res Toxicol, 31, 548, 10.1021/acs.chemrestox.8b00023 Kim, 2012, Investigating intestinal inflammation in DSS-induced model of IBD, J Vis Exp, 60, e3678 Cooper, 1993, Clinicopathologic study of dextran sulfate sodium experimental murine colitis, Lab Invest, 69, 238 Garbacz, 2018, Chronic activation of liver X receptor sensitizes mice to high cholesterol diet-induced gut toxicity, Mol Pharmacol, 94, 1145, 10.1124/mol.118.112672 Johansson, 2008, The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria, Proc Natl Acad Sci U S A, 105, 15064, 10.1073/pnas.0803124105 Godinho-Silva, 2019, Light-entrained and brain-tuned circadian circuits regulate ILC3s and gut homeostasis, Nature, 574, 254, 10.1038/s41586-019-1579-3 Fu, 2019, FXR regulates intestinal cancer stem cell proliferation, Cell, 176, 1098, 10.1016/j.cell.2019.01.036 Viennois, 2018, Purification of total RNA from DSS-treated murine tissue via lithium chloride precipitation, Bio Protoc, 8, e2829, 10.21769/BioProtoc.2829 Yan, 2019, Aryl hydrocarbon receptor signaling prevents activation of hepatic stellate cells and liver fibrogenesis in mice, Gastroenterology, 157, 793, 10.1053/j.gastro.2019.05.066 Xu, 2017, Melatonin prevents obesity through modulation of gut microbiota in mice, J Pineal Res, 62, e12399, 10.1111/jpi.12399