Symbiotic lactobacilli stimulate gut epithelial proliferation via Nox-mediated generation of reactive oxygen species

EMBO Journal

Volumn 32, Issue 23, 2013, Pages 3017-3028

  Jones, Rheinallt M ^a   Luo, Liping ^a   Ardita, Courtney S ^a   Richardson, Arena N ^a   Kwon, Young Man ^a   Mercante, Jeffrey W ^a   Alam, Ashfaqul ^a   Gates, Cymone L ^a   Wu, Huixia ^a   Swanson, Phillip A ^a   David Lambeth, J ^a   Denning, Patricia W ^a   Neish, Andrew S ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Lactobacilli; Microbiota; Proliferation; ROS; Symbiosis

Indexed keywords

PROBIOTIC AGENT; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; HISTONE; OXIDOREDUCTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTEROIDES THETAIOTAOMICRON; CELL PROLIFERATION; COMMENSAL; CONTROLLED STUDY; DROSOPHILA; EMBRYO; ESCHERICHIA COLI; GENETIC CONSERVATION; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS BIFIDUS; LACTOBACILLUS CASEI; LACTOBACILLUS DELBRUECKII; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS; MIDGUT; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM; STEM CELL; SYMBIOSIS; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; INTESTINE; LARVA; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); EUKARYOTA; LACTOBACILLUS; METAZOA; MURINAE; PROKARYOTA;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; DROSOPHILA; HISTONES; HOST-PATHOGEN INTERACTIONS; INTESTINES; LACTOBACILLUS; LARVA; MICE; NADH, NADPH OXIDOREDUCTASES; OXIDATION-REDUCTION; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STEM CELLS; SYMBIOSIS;

EID: 84888864785     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.224     Document Type: Article

References (46)

1. Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313. (Pubitemid 46209993)
2. Buchon N, Broderick NA, Poidevin M, Pradervand S, Lemaitre B (2009) Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 5: 200-211.
3. Chakrabarti S, Liehl P, Buchon N, Lemaitre B (2012) Infectioninduced host translational blockage inhibits immune responses and epithelial renewal in the Drosophila gut. Cell Host Microbe 12: 60-70.
4. Chen X, Lee KA, Ha EM, Lee KM, Seo YY, Choi HK, Kim HN, Kim MJ, Cho CS, Lee SY, Lee WJ, Yoon J (2011) A specific and sensitive method for detection of hypochlorous acid for the imaging of microbe-induced HOCl production. Chem Commun (Camb) 47: 4373-4375.
5. Coant N, Ben Mkaddem S, Pedruzzi E, Guichard C, Treton X, Ducroc R, Freund JN, Cazals-Hatem D, Bouhnik Y, Woerther PL, Skurnik D, Grodet A, Fay M, Biard D, Lesuffleur T, Deffert C, Moreau R, Groyer A, Krause KH, Daniel F et al. (2010) NADPH oxidase 1 modulates WNT and NOTCH1 signaling to control the fate of proliferative progenitor cells in the colon. Mol Cell Biol 30: 2636-2650.
6. Geiszt M, Lekstrom K, Brenner S, Hewitt SM, Dana R, Malech HL, Leto TL (2003) NAD(P)H oxidase 1, a product of differentiated colon epithelial cells, can partially replace glycoprotein 91phox in the regulated production of superoxide by phagocytes. J Immunol 171: 299-306. (Pubitemid 36745301)
7. Ha EM, Oh CT, Bae YS, Lee WJ (2005a) A direct role for dual oxidase in Drosophila gut immunity. Science 310: 847-850. (Pubitemid 41567342)
8. Ha EM, Oh CT, Ryu JH, Bae YS, Kang SW, Jang IH, Brey PT, Lee WJ (2005b) An antioxidant system required for host protection against gut infection in Drosophila. Dev Cell 8: 125-132. (Pubitemid 40058012)
9. Hernandez-Garcia D, Wood CD, Castro-Obregon S, Covarrubias L (2010) Reactive oxygen species: a radical role in development? Free Radic Biol Med 49: 130-143.
10. Hooper LV, Littman DR, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336: 1268-1273.
11. Jiang H, Patel PH, Kohlmaier A, Grenley MO, McEwen DG, Edgar BA (2009) Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137: 1343-1355.
12. Jones RM, Mercante JW, Neish AS (2012) Reactive oxygen production induced by the gut microbiota: pharmacotherapeutic implications. Curr Med Chem 19: 1519-1529.
13. Kotchoni SO, Kuhns C, Ditzer A, Kirch HH, Bartels D (2006) Overexpression of different aldehyde dehydrogenase genes in Arabidopsis thaliana confers tolerance to abiotic stress and protects plants against lipid peroxidation and oxidative stress. Plant Cell Environ 29: 1033-1048. (Pubitemid 43727435)
14. Kumar A, Wu H, Collier-Hyams LS, Hansen JM, Li T, Yamoah K, Pan Z-Q, Jones DP, Neish AS (2007) Commensal bacteria modulate cullin-dependent signaling via generation of reactive oxygen species. EMBO J 26: 4457-4466. (Pubitemid 350036625)
15. Kumar A, Wu H, Collier-Hyams LS, Kwon YM, Hanson JM, Neish AS (2009) The bacterial fermentation product butyrate influences epithelial signaling via reactive oxygen species-mediated changes in cullin-1 neddylation. J Immunol 182: 538-546.
16. Kundu K, Knight SF, Willett N, Lee S, Taylor WR, Murthy N (2009) Hydrocyanines: a class of fluorescent sensors that can image reactive oxygen species in cell culture, tissue, and in vivo. Angew Chem Int Ed Engl 48: 299-303.
17. Lambeth JD (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4: 181-189. (Pubitemid 38339084)
18. Lee KA, Kim SH, Kim EK, Ha EM, You H, Kim B, Kim MJ, Kwon Y, Ryu JH, Lee WJ (2013) Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila. Cell 153: 797-811.
19. Leoni G, Alam A, Neumann PA, Lambeth JD, Cheng G, McCoy J, Hilgarth RS, Kundu K, Murthy N, Kusters D, Reutelingsperger C, Perretti M, Parkos CA, Neish AS, Nusrat A (2013) Annexin A1, formyl peptide receptor, and NOX1 orchestrate epithelial repair. J Clin Invest 123: 443-454.
20. Mathur D, Bost A, Driver I, Ohlstein B (2010) A transient niche regulates the specification of Drosophila intestinal stem cells. Science 327: 210-213.
21. Micchelli CA, Perrimon N (2006) Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439: 475-479. (Pubitemid 43152838)
22. Mitsuishi Y, Motohashi H, Yamamoto M (2012) The Keap1-Nrf2. system in cancers: stress response and anabolic metabolism. Front Oncol 2: 200.
23. Morgan NS, Skovronsky DM, Artavanis-Tsakonas S, Mooseker MS (1994) The molecular cloning and characterization of Drosophila melanogaster myosin-IA and myosin-IB. J Mol Biol 239: 347-356. (Pubitemid 24190365)
24. Neish AS (2009) Microbes in gastrointestinal health and disease. Gastroenterology 136: 65-80.
25. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S (2012) Host-gut microbiota metabolic interactions. Science 336: 1262-1267.
26. O'Callaghan J, O'Toole PW (2013) Lactobacillus: host-microbe relationships. Curr Top Microbiol Immunol 358: 119-154.
27. Ogier-Denis E, Mkaddem SB, Vandewalle A (2008) NOX enzymes and Toll-like receptor signaling. Semin Immunopathol 30: 291-300.
28. Ohlstein B, Spradling A (2006) The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439: 470-474. (Pubitemid 43152837)
29. Owusu-Ansah E, Banerjee U (2009) Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461: 537-541.
30. Park J, Floch MH (2007) Prebiotics, probiotics, and dietary fiber in gastrointestinal disease. Gastroenterol Clin North Am 36: 47-63. (Pubitemid 46654719)
31. Preidis GA, Saulnier DM, Blutt SE, Mistretta TA, Riehle KP, Major AM, Venable SF, Finegold MJ, Petrosino JF, Conner ME, Versalovic J (2012) Probiotics stimulate enterocyte migration and microbial diversity in the neonatal mouse intestine. FASEB J 26: 1960-1969.
32. Quinn MT, Gauss KA (2004) Structure and regulation of the neutrophil respiratory burst oxidase: comparison with nonphagocyte oxidases. J Leukoc Biol 76: 760-781. (Pubitemid 39313712)
33. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241. (Pubitemid 38962578)
34. Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24: 981-990.
35. Sadok A, Bourgarel-Rey V, Gattacceca F, Penel C, Lehmann M, Kovacic H (2008) Nox1-dependent superoxide production controls colon adenocarcinoma cell migration. Biochim Biophys Acta 1783: 23-33.
36. Sartor RB (2008) Microbial influences in inflammatory bowel diseases. Gastroenterology 134: 577-594. (Pubitemid 351173057)
37. Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F (2011) Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab 14: 403-414.
38. Suh YA, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, Chung AB, Griendling KK, Lambeth JD (1999) Cell transformation by the superoxide- generating oxidase Mox1. Nature 401: 79-82.
39. Swanson 2nd PA, Kumar A, Samarin S, Vijay-Kumar M, Kundu K, Murthy N, Hansen J, Nusrat A, Neish AS (2011) Enteric commensal bacteria potentiate epithelial restitution via reactive oxygen species-mediated inactivation of focal adhesion kinase phosphatases. Proc Natl Acad Sci USA 108: 8803-8808.
40. Sykiotis GP, Bohmann D (2008) Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila. Dev Cell 14: 76-85.
41. Takashima S, Mkrtchyan M, Younossi-Hartenstein A, Merriam JR, Hartenstein V (2008) The behaviour of Drosophila adult hindgut stem cells is controlled by Wnt and Hh signalling. Nature 454: 651-655.
42. Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143: 606-616.
43. van der Flier LG, Clevers H (2009) Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 71: 241-260.
44. Wentworth CC, Alam A, Jones RM, Nusrat A, Neish AS (2011) Enteric commensal bacteria induce ERK pathway signaling via formyl peptide receptor (FPR)-dependent redox modulation of Dual specific phosphatase 3 (DUSP3). J Biol Chem 286: 38448-38455.
45. Wentworth CC, Jones RM, Kwon YM, Nusrat A, Neish AS (2010) Commensal-epithelial signaling mediated via formyl peptide receptors. Am J Pathol 177: 2782-2790.
46. Wong CN, Ng P, Douglas AE (2011) Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environ Microbiol 13: 1889-1900