Bacterial TLR4 and NOD2 signaling linked to reduced mitochondrial energy function in active inflammatory bowel disease

References

• Ponder A, Long MD. A clinical review of recent findings in the epidemiology of inflammatory bowel disease. Clin Epidemiol. 2013;5:237–247. doi:10.2147/CLEP.S33961.
   Google Scholar
• Liu TC, Stappenbeck TS. Genetics and pathogenesis of inflammatory bowel disease. Annu Rev Pathol. 2016;11:127–148. doi:10.1146/annurev-pathol-012615-044152.
   Google Scholar
• Coleman OI, Haller D. Bacterial signaling at the intestinal epithelial interface in inflammation and cancer. Front Immunol. 2017;8:1927. doi:10.3389/fimmu.2017.01927.
   Google Scholar
• Roediger WE. The colonic epithelium in ulcerative colitis: an energy-deficiency disease? Lancet. 1980;2:712–715.
   Google Scholar
• Geremia A, Biancheri P, Allan P, Corazza GR, Di Sabatino A. Innate and adaptive immunity in inflammatory bowel disease. Autoimmun Rev. 2014;13:3–10. doi:10.1016/j.autrev.2013.06.004.
   Google Scholar
• Yu X, Wieczorek S, Franke A, Yin H, Pierer M, Sina C, Karlsen TH, Boberg KM, Bergquist A, Kunz M, et al. Association of UCP2-866 G/A polymorphism with chronic inflammatory diseases. Genes Immun. 2009;10:601–605. doi:10.1038/gene.2009.29.
   Google Scholar
• Bar F, Bochmann W, Widok A, von Medem K, Pagel R, Hirose M, Yu X, Kalies K, König P, Böhm R, et al. Mitochondrial gene polymorphisms that protect mice from colitis. Gastroenterology. 2013;145:1055–1063 e3. doi:10.1053/j.gastro.2013.07.015.
   Google Scholar
• Ananthakrishnan AN, Bernstein CN, Iliopoulos D, Macpherson A, Neurath MF, Ali RAR, Vavricka SR, Fiocchi C. Environmental triggers in IBD: a review of progress and evidence. Nat Rev Gastroenterol Hepatol. 2018;15:39–49. doi:10.1038/nrgastro.2017.136.
   Google Scholar
• Cario E. Bacterial interactions with cells of the intestinal mucosa: toll-like receptors and NOD2. Gut. 2005;54:1182–1193. doi:10.1136/gut.2004.062794.
   Google Scholar
• Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature. 2001;410:1099–1103. doi:10.1038/35074106.
   Google Scholar
• Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, Thomas G, Philpott DJ, Sansonetti PJ. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem. 2003;278:8869–8872. doi:10.1074/jbc.C200651200.
   Google Scholar
• Takeshita F, Gursel I, Ishii KJ, Suzuki K, Gursel M, Klinman DM. Signal transduction pathways mediated by the interaction of CpG DNA with Toll-like receptor 9. Semin Immunol. 2004;16:17–22.
   Google Scholar
• Suliman HB, Piantadosi CA. Mitochondrial quality control as a therapeutic target. Pharmacol Rev. 2016;68:20–48. doi:10.1124/pr.115.011502.
   Google Scholar
• Vyas S, Zaganjor E, Haigis MC. Mitochondria and cancer. Cell. 2016;166:555–566. doi:10.1016/j.cell.2016.07.002.
   Google Scholar
• Cani PD, Knauf C. How gut microbes talk to organs: the role of endocrine and nervous routes. Mol Metab. 2016;5:743–752. doi:10.1016/j.molmet.2016.05.011.
   Google Scholar
• Heller S, Penrose HM, Cable C, Biswas D, Nakhoul H, Baddoo M, Flemington E, Crawford SE, Savkovic SD. Reduced mitochondrial activity in colonocytes facilitates AMPKalpha2-dependent inflammation. FASEB J. 2017. doi:10.1096/fj.201600976R.
   Google Scholar
• Delpre G, Avidor I, Steinherz R, Kadish U, Ben-Bassat M. Ultrastructural abnormalities in endoscopically and histologically normal and involved colon in ulcerative colitis. Am J Gastroenterol. 1989;84:1038–1046.
   Google Scholar
• Meyer RR, Simpson MV. DNA biosynthesis in mitochondria. Differential inhibition of mitochondrial and nuclear DNA polymerases by the mutagenic dyes ethidium bromide and acriflavin. Biochem Biophys Res Commun. 1969;34:238–244.
   Google Scholar
• King MP, Attardi G. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science. 1989;246:500–503.
   Google Scholar
• Gautier L, Cope L, Bolstad BM, Irizarry RA. affy–analysis of affymetrix geneChip data at the probe level. Bioinformatics. 2004;20:307–315. doi:10.1093/bioinformatics/btg405.
   Google Scholar
• Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43:e47. doi:10.1093/nar/gkv007.
   Google Scholar
• Ma C, Ritian W, Yadong L, Zhang G, Sun S, Cong Y, Li X, Liu Z. Critical role of CD6highCD4+ T cells in driving Th1/Th17 cell immune responses and mucosal inflammation in IBD. J Crohns Colitis. 2018;13:510–524. doi:10.1093/ecco-jcc/jjy179.
   Google Scholar
• Morgan ME, Koelink PJ, Zheng B, Den Brok MHMGM, van de Kant HJG, Verspaget HW, Folkerts G, Adema GJ, Kraneveld AD. Toll-like receptor 6 stimulation promotes T-helper 1 and 17 responses in gastrointestinal-associated lymphoid tissue and modulates murine experimental colitis. Mucosal Immunol. 2014;7:1266–1277. doi:10.1038/mi.2014.16.
   Google Scholar
• Stallhofer J, Friedrich M, Konrad-Zerna A, Wetzke M, Lohse P, Glas J, Tillack-Schreiber C, Schnitzler F, Beigel F, Brand S. Lipocalin-2 Is a disease activity marker in inflammatory bowel disease regulated by IL-17A, IL-22, and TNF-alpha and modulated by IL23R genotype status. Inflamm Bowel Dis. 2015;21:2327–2340. doi:10.1097/MIB.0000000000000515.
   Google Scholar
• Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, Ramos R, Britton H, Moran T, Karaliuskas R, Duerr RH, et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn‘s disease. Nature. 2001;411:603–606. doi:10.1038/35079114.
   Google Scholar
• Cario E. Toll-like receptors in inflammatory bowel diseases: a decade later. Inflamm Bowel Dis. 2010;16:1583–1597. doi:10.1002/ibd.21282.
   Google Scholar
• Mottawea W, Chiang CK, Muhlbauer M, Starr AE, Butcher J, Abujamel T, Deeke SA, Brandel A, Zhou H, Shokralla S, et al. Altered intestinal microbiota-host mitochondria crosstalk in new onset Crohn‘s disease. Nat Commun. 2016;7:13419. doi:10.1038/ncomms13419.
   Google Scholar
• Cunningham KE, Vincent G, Sodhi CP, Novak EA, Ranganathan S, Egan CE, Stolz DB, Rogers MB, Firek B, Morowitz MJ, et al. Peroxisome proliferator-activated receptor-gamma coactivator 1-alpha (PGC1alpha) protects against experimental murine colitis. J Biol Chem. 2016;291:10184–10200. doi:10.1074/jbc.M115.688812.
   Google Scholar
• Clark A, Mach N. The crosstalk between the gut microbiota and mitochondria during exercise. Front Physiol. 2017;8:319. doi:10.3389/fphys.2017.00319.
   Google Scholar
• Lobet E, Letesson JJ, Arnould T. Mitochondria: a target for bacteria. Biochem Pharmacol. 2015;94:173–185. doi:10.1016/j.bcp.2015.02.007.
   Google Scholar
• Den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud D-J, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54:2325–2340. doi:10.1194/jlr.R036012.
   Google Scholar
• Lee I, Huttemann M. Energy crisis: the role of oxidative phosphorylation in acute inflammation and sepsis. Biochim Biophys Acta. 2014;1842:1579–1586. doi:10.1016/j.bbadis.2014.05.031.
   Google Scholar
• Ma J, Coarfa C, Qin X, Bonnen PE, Milosavljevic A, Versalovic J, Aagaard K. mtDNA haplogroup and single nucleotide polymorphisms structure human microbiome communities. BMC Genomics. 2014;15:257. doi:10.1186/1471-2164-15-257.
   Google Scholar
• Saxena A, Lopes F, Poon KKH, McKay DM. Absence of the NOD2 protein renders epithelia more susceptible to barrier dysfunction due to mitochondrial dysfunction. Am J Physiol Gastrointest Liver Physiol. 2017;313:G26–G38. doi:10.1152/ajpgi.00070.2017.
   Google Scholar
• Phipson B, Lee S, Majewski IJ, Alexander WS, Smyth GK. Robust hyperparameter estimation protects against hypervariable genes and improves power to detect differential expression. Ann Appl Stat. 2016;10:946–963. doi:10.1214/16-AOAS920.
   Google Scholar
• Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011;12:323–339. doi:10.1186/1471-2105-12-323.
   Google Scholar
• Wang L, Feng Z, Wang X, Wang X, Zhang X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics. 2010;26:136–138. doi:10.1093/bioinformatics/btp612.
   Google Scholar
• de Hoon MJ, Imoto S, Nolan J, Miyano S. Open source clustering software. Bioinformatics. 2004;20:1453–1454. doi:10.1093/bioinformatics/bth078.
   Google Scholar
• Saldanha AJ. Java treeview–extensible visualization of microarray data. Bioinformatics. 2004;20:3246–3248. doi:10.1093/bioinformatics/bth349.
   Google Scholar
• Lê S, Josse J, Husson F. FactoMineR: an R package for multivariate analysis. Journal of Statistical Software. 2008;25:1–18. doi:10.18637/jss.v025.i01.
   Google Scholar
• Cancer Genome Atlas Research N. Integrated genomic characterization of papillary thyroid carcinoma. Cell. 2014;159:676–690. doi:10.1016/j.cell.2014.09.050.
   Google Scholar
• Team RC. R: A language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing; 2012.
   Google Scholar