Redox signaling mediates symbiosis between the gut microbiota and the intestine

Gut Microbes

Volumn 5, Issue 2, 2014, Pages 250-253

  Jones, Rheinallt M ^a   Neish, Andrew S ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Lactobacilli; Microbiota; Proliferation; ROS; Symbiosis

Indexed keywords

CYSTEINE; PROBIOTIC AGENT; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2;

ARTICLE; CELL PROLIFERATION; HOST PATHOGEN INTERACTION; HUMAN; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; INTESTINE FUNCTION; LACTOBACILLUS; NONHUMAN; OXIDATION REDUCTION REACTION; SIGNAL TRANSDUCTION; SYMBIOSIS; ANIMAL; INTESTINE; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY;

ANIMALS; HUMANS; INTESTINES; MICROBIOTA; OXIDATION-REDUCTION; SIGNAL TRANSDUCTION; SYMBIOSIS;

EID: 84899444625     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.27917     Document Type: Article

References (41)

1. Neish AS. Microbes in gastrointestinal health and disease. Gastroenterology 2009; 136: 65-80; PMID: 19026645; http://dx. doi. org/10. 1053/j. gastro. 2008. 10. 080.
2. Dethlefsen L, McFall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 2007; 449: 811-8; PMID: 17943117; http://dx. doi. org/10. 1038/nature06245.
3. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE. Metagenomic analysis of the human distal gut microbiome. Science 2006; 312: 1355-9; PMID: 16741115; http://dx. doi. org/10. 1126/science. 1124234.
4. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science 2005; 307: 1915-20; PMID: 15790844; http://dx. doi. org/10. 1126/science. 1104816.
5. Xu J, Mahowald MA, Ley RE, Lozupone CA, Hamady M, Martens EC, Henrissat B, Coutinho PM, Minx P, Latreille P, et al. Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol 2007; 5: e156; PMID: 17579514; http://dx. doi. org/10. 1371/journal. pbio. 0050156.
6. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, Wei D, Goldfarb KC, Santee CA, Lynch SV, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009; 139: 485-98; PMID: 19836068; http://dx. doi. org/10. 1016/j. cell. 2009. 09. 033.
7. Smith K, McCoy KD, Macpherson AJ. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin Immunol 2007; 19: 59-69; PMID: 17118672; http://dx. doi. org/10. 1016/j. smim. 2006. 10. 002.
8. Ismail AS, Hooper LV. Epithelial cells and their neighbors. IV. Bacterial contributions to intestinal epithelial barrier integrity. Am J Physiol Gastrointest Liver Physiol 2005; 289: G779-84; PMID: 16227525; http://dx. doi. org/10. 1152/ajpgi. 00203. 2005.
9. Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, Doyle J, Jewell L, De Simone C. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 2001; 121: 580-91; PMID: 11522742; http://dx. doi. org/10. 1053/gast. 2001. 27224.
10. Stappenbeck TS, Hooper LV, Gordon JI. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci U S A 2002; 99: 15451-5; PMID: 12432102; http://dx. doi. org/10. 1073/pnas. 202604299.
11. Pull SL, Doherty JM, Mills JC, Gordon JI, Stappenbeck TS. Activated macrophages are an adaptive element of the colonic epithelial progenitor niche necessary for regenerative responses to injury. Proc Natl Acad Sci U S A 2005; 102: 99-104; PMID: 15615857; http://dx. doi. org/10. 1073/pnas. 0405979102.
12. Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology 2008; 134: 577-94; PMID: 18242222; http://dx. doi. org/10. 1053/j. gastro. 2007. 11. 059.
13. Noverr MC, Huffnagle GB. Does the microbiota regulate immune responses outside the gut? Trends Microbiol 2004; 12: 562-8; PMID: 15539116; http://dx. doi. org/10. 1016/j. tim. 2004. 10. 008.
14. Wills-Karp M, Santeliz J, Karp CL. The germless theory of allergic disease: revisiting the hygiene hypothesis. Nat Rev Immunol 2001; 1: 69-75; PMID: 11905816; http://dx. doi. org/10. 1038/35095579.
15. Sansonetti PJ. War and peace at mucosal surfaces. Nat Rev Immunol 2004; 4: 953-64; PMID: 15573130; http://dx. doi. org/10. 1038/nri1499.
16. Cheng G, Lambeth JD. NOXO1, regulation of lipid binding, localization, and activation of Nox1 by the Phox homology (PX) domain. J Biol Chem 2004; 279: 4737-42; PMID: 14617635; http://dx. doi. org/10. 1074/jbc. M305968200.
17. Lambeth JD. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 2004; 4: 181-9; PMID: 15039755; http://dx. doi. org/10. 1038/nri1312.
18. Lambeth JD, Neish AS. Nox Enzymes and New Thinking on Reactive Oxygen: A Double-Edged Sword Revisited. Annu Rev Pathol 2013; PMID: 24050626; http://dx. doi. org/10. 1146/annurev-pathol-012513-104651.
19. Ogier-Denis E, Mkaddem SB, Vandewalle A. NOX enzymes and Toll-like receptor signaling. Semin Immunopathol 2008; 30: 291-300; PMID: 18493762; http://dx. doi. org/10. 1007/s00281-008-0120-9.
20. Owusu-Ansah E, Banerjee U. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 2009; 461: 537-41; PMID: 19727075; http://dx. doi. org/10. 1038/nature08313.
21. Tsukagoshi H, Busch W, Benfey PN. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 2010; 143: 606-16; PMID: 21074051; http://dx. doi. org/10. 1016/j. cell. 2010. 10. 020.
22. Love NR, Chen Y, Ishibashi S, Kritsiligkou P, Lea R, Koh Y, Gallop JL, Dorey K, Amaya E. Amputation-induced reactive oxygen species are required for successful Xenopus tadpole tail regeneration. Nat Cell Biol 2013; 15: 222-8; PMID: 23314862; http://dx. doi. org/10. 1038/ncb2659.
23. Jones RM, Luo L, Ardita CS, Richardson AN, Kwon YM, Mercante JW, Alam A, Gates CL, Wu H, Swanson PA, et al. Symbiotic lactobacilli stimulate gut epithelial proliferation via Nox-mediated generation of reactive oxygen species. EMBO J 2013; 32: 3017-28; PMID: 24141879; http://dx. doi. org/10. 1038/emboj. 2013. 224.
24. Buchon N, Broderick NA, Poidevin M, Pradervand S, Lemaitre B. Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 2009; 5: 200-11; PMID: 19218090; http://dx. doi. org/10. 1016/j. chom. 2009. 01. 003.
25. Alam A, Leoni G, Wentworth CC, Kwal JM, Wu H, Ardita CS, Swanson PA, Lambeth JD, Jones RM, Nusrat A, et al. Redox signaling regulates commensal-mediated mucosal homeostasis and restitution and requires formyl peptide receptor 1. Mucosal Immunol 2013; 2013: (Accepted for publication); PMID: 24192910.
26. nd, Kumar A, Samarin S, Vijay-Kumar M, Kundu K, Murthy N, Hansen J, Nusrat A, Neish AS. Enteric commensal bacteria potentiate epithelial restitution via reactive oxygen species-mediated inactivation of focal adhesion kinase phosphatases. Proc Natl Acad Sci U S A 2011; 108: 8803-8; PMID: 21555563; http://dx. doi. org/10. 1073/pnas. 1010042108.
27. Hernández-García D, Wood CD, Castro-Obregón S, Covarrubias L. Reactive oxygen species: A radical role in development? Free Radic Biol Med 2010; 49: 130-43; PMID: 20353819; http://dx. doi. org/10. 1016/j. freeradbiomed. 2010. 03. 020.
28. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007; 87: 245-313; PMID: 17237347; http://dx. doi. org/10. 1152/physrev. 00044. 2005.
29. Bedard K, Lardy B, Krause KH. NOX family NADPH oxidases: not just in mammals. Biochimie 2007; 89: 1107-12; PMID: 17400358; http://dx. doi. org/10. 1016/j. biochi. 2007. 01. 012.
30. Terada LS. Specificity in reactive oxidant signaling: think globally, act locally. J Cell Biol 2006; 174: 615-23; PMID: 16923830; http://dx. doi. org/10. 1083/jcb. 200605036.
31. Kim SC, Tonkonogy SL, Karrasch T, Jobin C, Sartor RB. Dual-association of gnotobiotic IL-10-/-mice with 2 nonpathogenic commensal bacteria induces aggressive pancolitis. Inflamm Bowel Dis 2007; 13: 1457-66; PMID: 17763473; http://dx. doi. org/10. 1002/ibd. 20246.
32. Barford D. The role of cysteine residues as redox-sensitive regulatory switches. Curr Opin Struct Biol 2004; 14: 679-86; PMID: 15582391; http://dx. doi. org/10. 1016/j. sbi. 2004. 09. 012.
33. Kamata H, Honda S, Maeda S, Chang L, Hirata H, Karin M. Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 2005; 120: 649-61; PMID: 15766528; http://dx. doi. org/10. 1016/j. cell. 2004. 12. 041.
34. Rhee SG, Kang SW, Jeong W, Chang TS, Yang KS, Woo HA. Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr Opin Cell Biol 2005; 17: 183-9; PMID: 15780595; http://dx. doi. org/10. 1016/j. ceb. 2005. 02. 004.
35. Chiarugi P, Buricchi F. Protein tyrosine phosphorylation and reversible oxidation: two cross-talking posttranslation modifications. Antioxid Redox Signal 2007; 9: 1-24; PMID: 17115885; http://dx. doi. org/10. 1089/ars. 2007. 9. 1.
36. Wentworth CC, Alam A, Jones RM, Nusrat A, Neish AS. Enteric commensal bacteria induce extracellular signal-regulated kinase pathway signaling via formyl peptide receptor-dependent redox modulation of dual specific phosphatase 3. J Biol Chem 2011; 286: 38448-55; PMID: 21921027; http://dx. doi. org/10. 1074/jbc. M111. 268938.
37. Wentworth CC, Jones RM, Kwon YM, Nusrat A, Neish AS. Commensal-epithelial signaling mediated via formyl peptide receptors. Am J Pathol 2010; 177: 2782-90; PMID: 21037077; http://dx. doi. org/10. 2353/ajpath. 2010. 100529.
38. Tonks NK. Redox redux: revisiting PTPs and the control of cell signaling. Cell 2005; 121: 667-70; PMID: 15935753; http://dx. doi. org/10. 1016/j. cell. 2005. 05. 016.
39. Kumar A, Wu H, Collier-Hyams LS, Hansen JM, Li T, Yamoah K, Pan ZQ, Jones DP, Neish AS. Commensal bacteria modulate cullin-dependent signaling via generation of reactive oxygen species. EMBO J 2007; 26: 4457-66; PMID: 17914462; http://dx. doi. org/10. 1038/sj. emboj. 7601867.
40. Lee WJ. Bacterial-modulated signaling pathways in gut homeostasis. Sci Signal 2008; 1: pe24; PMID: 18506033; http://dx. doi. org/10. 1126/stke. 121pe24.
41. Sethuraman M, McComb ME, Huang H, Huang S, Heibeck T, Costello CE, Cohen RA. Isotope-coded affinity tag (ICAT) approach to redox proteomics: identification and quantitation of oxidant-sensitive cysteine thiols in complex protein mixtures. J Proteome Res 2004; 3: 1228-33; PMID: 15595732; http://dx. doi. org/10. 1021/pr049887e.