Genetic and transcriptional analysis of inflammatory bowel disease-associated pathways in patients with GUCY2C-linked familial diarrhea

References

• Priyamvada S, Gomes R, Gill RK, et al. Mechanisms underlying dysregulation of electrolyte absorption in inflammatory bowel disease-associated diarrhea. Inflamm Bowel Dis. 2015;21:2926–2935.
   PubMed Web of Science ®Google Scholar
• Fiskerstrand T, Arshad N, Haukanes BI, et al. Familial diarrhea syndrome caused by an activating GUCY2C mutation. N Engl J Med. 2012;366:1586–1595.
   PubMed Web of Science ®Google Scholar
• Basu N, Arshad N, Visweswariah SS. Receptor guanylyl cyclase C (GC-C): regulation and signal transduction. Mol Cell Biochem. 2010;334:67–80.
   PubMed Web of Science ®Google Scholar
• Chey WD, Lembo AJ, Lavins BJ, et al. Linaclotide for irritable bowel syndrome with constipation: a 26-week, randomized, double-blind, placebo-controlled trial to evaluate efficacy and safety. Am J Gastroenterol. 2012;107:1702–1712.
   PubMed Web of Science ®Google Scholar
• Muller T, Rasool I, Heinz-Erian P, et al. Congenital secretory diarrhoea caused by activating germline mutations in GUCY2C. Gut. 2016;8:1306–1313.
   Web of Science ®Google Scholar
• Steinbrecher KA, Harmel-Laws E, Garin-Laflam MP, et al. Murine guanylate cyclase C regulates colonic injury and inflammation. J Immunol. 2011;186:7205–7214.
   PubMed Web of Science ®Google Scholar
• Harmel-Laws E, Mann EA, Cohen MB, et al. Guanylate cyclase C deficiency causes severe inflammation in a murine model of spontaneous colitis. PLoS One. 2013;8:e79180.
   PubMed Web of Science ®Google Scholar
• Lin JE, Snook AE, Li P, et al. GUCY2C opposes systemic genotoxic tumorigenesis by regulating AKT-dependent intestinal barrier integrity. PLoS One. 2012;7:e31686.
   PubMed Web of Science ®Google Scholar
• Brenna O, Bruland T, Furnes MW, et al. The guanylate cyclase-C signaling pathway is down-regulated in inflammatory bowel disease. Scand J Gastroenterol 2015;50:1241–1252.
   PubMed Web of Science ®Google Scholar
• Lan D, Niu J, Miao J, et al. Expression of guanylate cyclase-C, guanylin, and uroguanylin is downregulated proportionally to the ulcerative colitis disease activity index. Sci Rep. 2016;6:25034.
   PubMed Web of Science ®Google Scholar
• Amarachintha S, Harmel-Laws E, Steinbrecher KA. Guanylate cyclase C reduces invasion of intestinal epithelial cells by bacterial pathogens. Sci Rep. 2018;8:1521.
   PubMed Web of Science ®Google Scholar
• Majumdar S, Mishra V, Nandi S, et al. Absence of receptor guanylyl cyclase C enhances ileal damage and reduces cytokine and antimicrobial peptide production during oral Salmonella Typhimurium infection. Infection and Immunity 2018;86:799–817.
   Web of Science ®Google Scholar
• Janecke AR, Heinz-Erian P, Yin J, et al. Reduced sodium-proton exchanger NHE3 activity causes congenital sodium diarrhea. Hum Mol Genet 2015;24:6614–6623.
   PubMed Web of Science ®Google Scholar
• Hihnala S, Höglund P, Lammi L, et al. Long-term clinical outcome in patients with congenital chloride diarrhea. J Pediatr Gastroenterol Nutr. 2006;42:369.
   PubMed Web of Science ®Google Scholar
• Larmonier CB, Laubitz D, Hill FM, et al. Reduced colonic microbial diversity is associated with colitis in NHE3-deficient mice. Am J Physiol Gastrointest Liver Physiol. 2013;305:G667–G677.
   PubMed Web of Science ®Google Scholar
• Laubitz D, Harrison CA, Midura-Kiela MT, et al. reduced epithelial na+/h + exchange drives gut microbial dysbiosis and promotes inflammatory response in t cell-mediated murine colitis. PLoS One. 2016;11:e0152044.
   PubMed Web of Science ®Google Scholar
• Tronstad RR, Kummen M, Holm K, et al. Guanylate cyclase c activation shapes the intestinal microbiota in patients with familial diarrhea and increased susceptibility for Crohn's disease. Inflamm Bowel Dis. 2017;23:1752–1761.
   PubMed Web of Science ®Google Scholar
• Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology. 2008;134:577–594.
   PubMed Web of Science ®Google Scholar
• Liu JZ, van Sommeren S, Huang H, et al. Association analyses identify 38 susceptibility loci for inflammatory bowel disease and highlight shared genetic risk across populations. Nat Genet. 2015;47:979–986.
   PubMed Web of Science ®Google Scholar
• Van Limbergen J, Radford-Smith G, Satsangi J. Advances in IBD genetics. Nat Rev Gastroenterol Hepatol. 2014;11:372–385.
   PubMed Web of Science ®Google Scholar
• Hugot JP, Chamaillard M, Zouali H, et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature. 2001;411:599–603.
   PubMed Web of Science ®Google Scholar
• Ogura Y, Bonen DK, Inohara N, et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature. 2001;411:603–606.
   PubMed Web of Science ®Google Scholar
• Cleynen I, Boucher G, Jostins L, et al. Inherited determinants of Crohn's disease and ulcerative colitis phenotypes: a genetic association study. Lancet. 2016;387:156–167.
   PubMed Web of Science ®Google Scholar
• Silverberg MS, Satsangi J, Ahmad T, et al. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol. 2005;19:5A–36A.
   PubMed Web of Science ®Google Scholar
• Christoforou A, Dondrup M, Mattingsdal M, et al. Linkage-disequilibrium-based binning affects the interpretation of GWASs. Am J Hum Genet. 2012;90:727–733.
   PubMed Web of Science ®Google Scholar
• Moskvina V, O'Dushlaine C, Purcell S, et al. Evaluation of an approximation method for assessment of overall significance of multiple-dependent tests in a genomewide association study. Genet Epidemiol. 2011;35:861–866.
   PubMed Web of Science ®Google Scholar
• Network, Pathway Analysis Subgroup of Psychiatric Genomics. Psychiatric genome-wide association study analyses implicate neuronal, immune and histone pathways. Nat Neurosci. 2015;18:199–209.
   PubMed Web of Science ®Google Scholar
• Jostins L, Ripke S, Weersma RK, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012;491:119–124.
   PubMed Web of Science ®Google Scholar
• Trynka G, Hunt KA, Bockett NA, et al. Dense genotyping identifies and localizes multiple common and rare variant association signals in celiac disease. Nat Genet. 2011;43:1193–1201.
   PubMed Web of Science ®Google Scholar
• Jorgensen SF, Reims HM, Frydenlund D, et al. A cross-sectional study of the prevalence of gastrointestinal symptoms and pathology in patients with common variable immunodeficiency. Am J Gastroenterol. 2016;111:1467–1475.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402–408.
   PubMed Web of Science ®Google Scholar
• Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102:15545–15550.
   PubMed Web of Science ®Google Scholar
• Ananthakrishnan AN, Huang H, Nguyen DD, et al. Differential effect of genetic burden on disease phenotypes in Crohn's disease and ulcerative colitis: analysis of a North American cohort. Am J Gastroenterol. 2014;109:395–400.
   PubMed Web of Science ®Google Scholar
• Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA. 2001;98:5116–5121.
   PubMed Web of Science ®Google Scholar
• Dysvik B, Jonassen I. J-Express: exploring gene expression data using Java. Bioinformatics. 2001;17:369–370.
   PubMed Web of Science ®Google Scholar
• Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44–57.
   PubMed Web of Science ®Google Scholar
• Rivas MA, Beaudoin M, Gardet A, et al. Deep resequencing of GWAS loci identifies independent rare variants associated with inflammatory bowel disease. Nat Genet. 2011;43:1066–1073.
   PubMed Web of Science ®Google Scholar
• Chen T, Kocinsky HS, Cha B, et al. Cyclic GMP kinase II (cGKII) inhibits NHE3 by altering its trafficking and phosphorylating NHE3 at three required sites: identification of a multifunctional phosphorylation site. J Biol Chem. 2015;290:1952–1965.
   PubMed Web of Science ®Google Scholar
• Alper SL, Sharma AK. The SLC26 gene family of anion transporters and channels. Mol Aspects Med. 2013;34:494–515.
   PubMed Web of Science ®Google Scholar
• Guggino WB, Stanton BA. New insights into cystic fibrosis: molecular switches that regulate CFTR. Nat Rev Mol Cell Biol. 2006;7:426–436.
   PubMed Web of Science ®Google Scholar
• Luo Y, de Lange KM, Jostins L, et al. Exploring the genetic architecture of inflammatory bowel disease by whole-genome sequencing identifies association at ADCY7. Nat Genet. 2017;49:186–192.
   PubMed Web of Science ®Google Scholar
• Meddens CA, Harakalova M, van den Dungen NA, et al. Systematic analysis of chromatin interactions at disease associated loci links novel candidate genes to inflammatory bowel disease. Genome Biol. 2016;17:247.
   PubMed Web of Science ®Google Scholar
• Anderson CA, Boucher G, Lees CW, et al. Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet. 2011;43:246–252.
   PubMed Web of Science ®Google Scholar
• Borowitz D, Gelfond D. Intestinal complications of cystic fibrosis. Curr Opin Pulm Med. 2013;19:676–680.
   PubMed Web of Science ®Google Scholar
• Romi H, Cohen I, Landau D, et al. Meconium ileus caused by mutations in GUCY2C, encoding the CFTR-activating guanylate cyclase 2C. Am J Hum Genet. 2012;90:893–899.
   PubMed Web of Science ®Google Scholar
• Shailubhai K, Palejwala V, Arjunan KP, et al. Plecanatide and dolcanatide, novel guanylate cyclase-C agonists, ameliorate gastrointestinal inflammation in experimental models of murine colitis. World J Gastrointest Surg. 2015;6:213–222.
   Google Scholar
• Waeytens A, De Vos M, Laukens D. Evidence for a potential role of metallothioneins in inflammatory bowel diseases. Mediators Inflamm. 2009;2009:1.
   Web of Science ®Google Scholar
• Lahiri A, Abraham C. Activation of Pattern Recognition Receptors Upregulates Metallothioneins, Thereby Increasing Intracellular Accumulation of Zinc, Autophagy, and Bacterial Clearance by Macrophages. Gastroenterology 2014;147:835–846.
   PubMed Web of Science ®Google Scholar
• King JC. Zinc: an essential but elusive nutrient. Am J Clin Nutr. 2011;94:679S–684S.
   PubMed Web of Science ®Google Scholar
• Blanchard RK, Moore JB, Green CL, et al. Modulation of intestinal gene expression by dietary zinc status: effectiveness of cDNA arrays for expression profiling of a single nutrient deficiency. Proc Natl Acad Sci USA. 2001;98:13507–13513.
   PubMed Web of Science ®Google Scholar
• Fukushima K, Ogawa H, Takahashi K, et al. Non-pathogenic bacteria modulate colonic epithelial gene expression in germ-free mice. Scand J Gastroenterol. 2003;38:626–634.
   PubMed Web of Science ®Google Scholar
• Perez-Torras S, Iglesias I, Llopis M, et al. Transportome Profiling Identifies Profound Alterations in Crohn's Disease Partially Restored by Commensal Bacteria. Eccojc. 2016;10:850–859.
   Web of Science ®Google Scholar
• Quevrain E, Maubert MA, Michon C, et al. Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn's disease. Gut. 2015;65:415–425.
   PubMed Web of Science ®Google Scholar
• Rossi O, van Berkel LA, Chain F, et al. Faecalibacterium prausnitzii A2-165 has a high capacity to induce IL-10 in human and murine dendritic cells and modulates T cell responses. Sci Rep. 2016;6:18507.
   PubMed Web of Science ®Google Scholar
• Darfeuille-Michaud A, Boudeau J, Bulois P, et al. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology. 2004;127:412–421.
   PubMed Web of Science ®Google Scholar
• Khan MT, van Dijl JM, Harmsen HJ. Antioxidants keep the potentially probiotic but highly oxygen-sensitive human gut bacterium Faecalibacterium prausnitzii alive at ambient air. PLoS One. 2014;9:e96097.
   PubMed Web of Science ®Google Scholar
• Duncan SH, Louis P, Thomson JM, et al. The role of pH in determining the species composition of the human colonic microbiota. Environ Microbiol. 2009;11:2112–2122.
   PubMed Web of Science ®Google Scholar
• von Volkmann HL, Bronstad I, Gilja OH, et al. Prolonged intestinal transit and diarrhea in patients with an activating GUCY2C mutation. PLoS One. 2017;12:e0185496.
   PubMed Web of Science ®Google Scholar
• Asano K, Matsushita T, Umeno J, et al. A genome-wide association study identifies three new susceptibility loci for ulcerative colitis in the Japanese population. Nat Genet. 2009;41:1325–1329.
   PubMed Web of Science ®Google Scholar