Butyrate Produced by Commensal Bacteria Potentiates Phorbol Esters Induced AP-1 Response in Human Intestinal Epithelial Cells

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Nepelska, Malgorzata ^a   Cultrone, Antonietta ^a   Béguet Crespel, Fabienne ^a   Le Roux, Karine ^a   Doré, Joël ^a   Arulampalam, Vermulugesan ^b   Blottière, Hervé M ^a  

^a UMR1319 MICALIS   (France)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; BUTYRIC ACID; CYCLIN D1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PHORBOL 13 ACETATE 12 MYRISTATE; PROPIONIC ACID; PROTEIN C FOS; PROTEIN KINASE C; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1;

ARTICLE; BACTERIUM CULTURE; BIFIDOBACTERIUM ADOLESCENTIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRAIN CACO 2; CELL STRAIN HT29; COMMENSAL; COMMENSAL BACTERIUM; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FIRMICUTES; FUSOBACTERIA; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; INTRACELLULAR SIGNALING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PROTEIN EXPRESSION; REGULATORY MECHANISM;

ANTIGENS, DIFFERENTIATION; BUTYRATES; CACO-2 CELLS; CELL DIFFERENTIATION; CELL PROLIFERATION; CULTURE MEDIA, CONDITIONED; CYCLIN D1; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FATTY ACIDS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENES, REPORTER; HISTONE DEACETYLASE INHIBITORS; HT29 CELLS; HUMANS; HYDROXAMIC ACIDS; INTESTINAL MUCOSA; LUCIFERASES; MAP KINASE SIGNALING SYSTEM; METAGENOME; PROTO-ONCOGENE PROTEINS C-FOS; TETRADECANOYLPHORBOL ACETATE; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTIONAL ACTIVATION;

BACTERIA (MICROORGANISMS);

EID: 84871667241     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052869     Document Type: Article

References (60)

1. Cummings JH, (1984) Microbial Digestion of Complex Carbohydrates in Man. Proceedings of the Nutrition Society 43: 35-44 Available:http://www.journals.cambridge.org/abstract_S0029665184000094.
2. Albert MJ, Mathan VI, Baker SJ, (1980) Vitamin B12 synthesis by human small intestinal bacteria. Nature 283: 781-782 Available:http://dx.doi.org/10.1038/283781a0.
3. Hooper LV, Midtvedt T, Gordon JI, (2002) How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annual Review of Nutrition 22: 283-307 Available:http://www.ncbi.nlm.nih.gov/pubmed/12055347.
4. Kelly D, Delday MI, Mulder I, (2012) Microbes and microbial effector molecules in treatment of inflammatory disorders. Immunological Reviews 245: 27-44 Available:http://www.ncbi.nlm.nih.gov/pubmed/22168412.
5. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, et al. (2004) The gut microbiota as an environmental factor that regulates fat storage. Proceedings of the National Academy of Sciences of the United States of America 101: 15718-15723 Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=524219&tool=pmcentrez&rendertype=abstract.
6. Desreumaux P, Dubuquoy L, Nutten S, Peuchmaur M, Englaro W, et al. (2001) Attenuation of colon inflammation through activators of the retinoid X receptor (RXR)/peroxisome proliferator-activated receptor gamma (PPARgamma) heterodimer. A basis for new therapeutic strategies. The Journal of Experimental Medicine 193: 827-838 Available:http://www.jem.org/cgi/doi/10.1084/jem.193.7.827.
7. Kelly D, Campbell JI, King TP, Grant G, Jansson E, et al. (2004) Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nature Immunology 5: 104-112 Available:http://www.ncbi.nlm.nih.gov/pubmed/14691478.
8. Lundin A, Bok CM, Aronsson L, Björkholm B, Gustafsson J-A, et al. (2008) Gut flora, Toll-like receptors and nuclear receptors: a tripartite communication that tunes innate immunity in large intestine. Cellular Microbiology 10: 1093-1103 Available:http://www.ncbi.nlm.nih.gov/pubmed/18088401.
9. Qiu J, Heller JJ, Guo X, Chen ZE, Fish K, et al. (2012) The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 36: 92-104 Available:http://www.ncbi.nlm.nih.gov/pubmed/22177117.
10. Dalmasso G, Nguyen HTT, Yan Y, Charrier-Hisamuddin L, Sitaraman SV, et al. (2008) Butyrate transcriptionally enhances peptide transporter PepT1 expression and activity. PloS one 3: e2476 Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2423477&tool=pmcentrez&rendertype=abstract.
11. Mandal M, Olson DJ, Sharma T, Vadlamudi RK, Kumar R, (2001) Butyric acid induces apoptosis by up-regulating Bax expression via stimulation of the c-Jun N-terminal kinase/activation protein-1 pathway in human colon cancer cells. Gastroenterology 120: 71-78 Available:http://www.gastrojournal.org/article/S0016-5085(01)98906-1/abstract.
12. Blottière HM, Buecher B, Galmiche J-P, Cherbut C, (2003) Molecular analysis of the effect of short-chain fatty acids on intestinal cell proliferation. The Proceedings of the Nutrition Society 62: 101-106 Available:http://www.ncbi.nlm.nih.gov/pubmed/12740064.
13. Kida Y, Shimizu T, Kuwano K, (2006) Sodium butyrate up-regulates cathelicidin gene expression via activator protein-1 and histone acetylation at the promoter region in a human lung epithelial cell line, EBC-1. Molecular Immunology 43: 1972-1981 Available:http://dx.doi.org/10.1016/j.molimm.2005.11.014.
14. Angel P, Karin M, (1991) The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochimica et Biophysica Acta 1072: 129-157.
15. Angel P, Karin M, (1991) The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochimica et Biophysica Acta 1072: 129-157 Available:http://dx.doi.org/10.1016/0304-419X(91)90011-9.
16. Karin M, Liu Z, Zandi E, (1997) AP-1 function and regulation. Current Opinion in Cell Biology 9: 240-246 Available:http://www.ncbi.nlm.nih.gov/pubmed/9069263.
17. Leppä S, Bohmann D, (1999) Diverse functions of JNK signaling and c-Jun in stress response and apoptosis. Oncogene 18: 6158-6162 Available:http://www.ncbi.nlm.nih.gov/pubmed/10557107.
18. Hess J, Angel P, Schorpp-Kistner M, (2004) AP-1 subunits: quarrel and harmony among siblings. Journal of Cell Science 117: 5965-5973 Available:http://www.ncbi.nlm.nih.gov/pubmed/15564374.
19. Chauhan D, Kharbanda S, Uchiyama H, Urashima M, Fragoso R, et al. (1994) Identification of upstream signals regulating interleukin-6 gene expression during in vitro treatment of human B cells with pokeweed mitogen. Blood 84: 2243-2252 Available:http://www.ncbi.nlm.nih.gov/pubmed/7919342.
20. Faisst S, Meyer S, (1992) Compilation of vertebrate-encoded transcription factors. Nucleic Acids Research 20: 3-26 Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=310320&tool=pmcentrez&rendertype=abstract.
21. Karin M, (1995) The regulation of AP-1 activity by mitogen-activated protein kinases. The Journal of Biological Chemistry 270: 16483-16486 Available:http://www.ncbi.nlm.nih.gov/pubmed/7622446.
22. Ip YT, Davis RJ, (1998) Signal transduction by the c-Jun N-terminal kinase (JNK)-from inflammation to development. Current Opinion in Cell Biology 10: 205-219 Available:http://www.ncbi.nlm.nih.gov/pubmed/9561845.
23. Wettschureck N, Offermanns S, (2005) Mammalian G proteins and their cell type specific functions. Physiological Reviews 85: 1159-1204 Available:http://www.ncbi.nlm.nih.gov/pubmed/16183910.
24. DeWire SM, Violin JD, (2011) Biased ligands for better cardiovascular drugs: dissecting G-protein-coupled receptor pharmacology. Circulation Research 109: 205-216 Available:http://www.ncbi.nlm.nih.gov/pubmed/21737816.
25. Kim YS, Tsao D, Siddiqui B, Whitehead JS, Arnstein P, et al. (1980) Effects of sodium butyrate and dimethylsulfoxide on biochemical properties of human colon cancer cells. Cancer 45: 1185-1192 Available:http://www.ncbi.nlm.nih.gov/pubmed/7357511.
26. Rivero JA, Adunyah SE, (1998) Sodium butyrate stimulates PKC activation and induces differential expression of certain PKC isoforms during erythroid differentiation. Biochemical and Biophysical Research Communications 248: 664-668 Available:http://www.ncbi.nlm.nih.gov/pubmed/9703983.
27. Nishizuka Y, (1992) Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science (New York, NY) 258: 607-614 Available:http://www.ncbi.nlm.nih.gov/pubmed/1411571.
28. Kyriakis JM, Banerjee P, Nikolakaki E, Dai T, Rubie EA, et al. (1994) The stress-activated protein kinase subfamily of c-Jun kinases. Nature 369: 156-160 Available:http://dx.doi.org/10.1038/369156a0.
29. Fang JY, Richardson BC, (2005) The MAPK signalling pathways and colorectal cancer. The Lancet Oncology 6: 322-327 Available:http://www.ncbi.nlm.nih.gov/pubmed/15863380.
30. Bryant MP, (1972) Commentary on the Hungate technique for culture of anaerobic bacteria. Am J Clin Nutr 25: 1324-8.
31. Lakhdari O, Tap J, Béguet-Crespel F, Le Roux K, de Wouters T, et al. (2011) Identification of NF-κB modulation capabilities within human intestinal commensal bacteria. Journal of Biomedicine & Biotechnology 2011: 282356 Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3134244&tool=pmcentrez&rendertype=abstract.
32. Le Blay G, Michel C, Blottière HM, Cherbut C, (1999) Enhancement of butyrate production in the rat caecocolonic tract by long-term ingestion of resistant potato starch. Br J Nutr 82: 419-26.
33. Chessel D, Dufour AB, Thioulouse J, (2004) The ade4 package-I- One-table methods. R News 4: 5-10.
34. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, et al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65 Available:http://www.ncbi.nlm.nih.gov/pubmed/20203603.
35. Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, et al. (2012) Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Research 22: 292-298 Available:http://www.ncbi.nlm.nih.gov/pubmed/22009990.
36. Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, et al. (2012) Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Research 22: 299-306 Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3266037&tool=pmcentrez&rendertype=abstract.
37. Morotomi M, Guillem JG, LoGerfo P, Weinstein IB, (1990) Production of diacylglycerol, an activator of protein kinase C, by human intestinal microflora. Cancer Research 50: 3595-3599 Available:http://www.ncbi.nlm.nih.gov/pubmed/2340507.
38. Fitzer CJ, O'Brian CA, Guillem JG, Weinstein IB, (1987) The regulation of protein kinase C by chenodeoxycholate, deoxycholate and several structurally related bile acids. Carcinogenesis 8: 217-220 Available:http://www.ncbi.nlm.nih.gov/pubmed/3802403.
39. Yoshida M, Kijima M, Akita M, Beppu T, (1990) Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. The Journal of Biological Chemistry 265: 17174-17179 Available:http://www.ncbi.nlm.nih.gov/pubmed/2211619.
40. Vidali G, Boffa LC, Bradbury EM, Allfrey VG, (1978) Butyrate suppression of histone deacetylation leads to accumulation of multiacetylated forms of histones H3 and H4 and increased DNase I sensitivity of the associated DNA sequences. Proceedings of the National Academy of Sciences of the United States of America 75: 2239-2243 Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=392527&tool=pmcentrez&rendertype=abstract.
41. Maier S, Daroqui MC, Scherer S, Roepcke S, Velcich A, et al. (2009) Butyrate and vitamin D3 induce transcriptional attenuation at the cyclin D1 locus in colonic carcinoma cells. Journal of Cellular Physiology 218: 638-642 Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2763190&tool=pmcentrez&rendertype=abstract.
42. Yang X-J, Seto E, (2008) The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nature reviews Molecular Cell Biology 9: 206-218 Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2667380&tool=pmcentrez&rendertype=abstract.
43. Herbst RS, (2004) Review of epidermal growth factor receptor biology. International Journal of Radiation Oncology, Biology, Physics 59: 21-26 Available:http://www.ncbi.nlm.nih.gov/pubmed/15142631.
44. Young D, Billingham O, Sampieri CL, Edwards DR, Clark IM, (2005) Differential effects of histone deacetylase inhibitors on phorbol ester- and TGF-beta1 induced murine tissue inhibitor of metalloproteinases-1 gene expression. The FEBS journal 272: 1912-1926 Available:http://www.ncbi.nlm.nih.gov/pubmed/15819885.
45. Siavoshian S, Segain JP, Kornprobst M, Bonnet C, Cherbut C, et al. (2000) Butyrate and trichostatin A effects on the proliferation/differentiation of human intestinal epithelial cells: induction of cyclin D3 and p21 expression. Gut 46: 507-514 Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1727889&tool=pmcentrez&rendertype=abstract.
46. Saunders N, Dicker A, Popa C, Jones S, Dahler A, (1999) Histone Deacetylase Inhibitors as Potential Anti-Skin Cancer Agents Cancer Research. 59: 399-404.
47. Wilson AJ, Chueh AC, Tögel L, Corner G, Ahmed N, et al. (2010) Apoptotic sensitivity of colon cancer cells to histone deacetylase inhibitors is mediated by an Sp1/Sp3-activated transcriptional program involving immediate-early gene induction. Cancer Research 70: 609-620 Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2939837&tool=pmcentrez&rendertype=abstract.
48. Rickard KL, Gibson PR, Young GP, Phillips W, (1999) Activation of protein kinase C augments butyrate-induced differentiation and turnover in human colonic epithelial cells in vitro. Carcinogenesis 20: 977-984 Available:http://www.ncbi.nlm.nih.gov/pubmed/10357776.
49. Gaschott T, Wächtershäuser A, Steinhilber D, Stein J, (2001) 1,25-Dihydroxycholecalciferol enhances butyrate-induced p21(Waf1/Cip1) expression. Biochemical and Biophysical Research Communications 283: 80-85 Available:http://www.ncbi.nlm.nih.gov/pubmed/11322770.
50. Chen-Deutsch X, Garay E, Zhang J, Harrison JS, Studzinski GP, (2009) c-Jun N-terminal kinase 2 (JNK2) antagonizes the signaling of differentiation by JNK1 in human myeloid leukemia cells resistant to vitamin D. Leukemia Research 33: 1372-1378 Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2706390&tool=pmcentrez&rendertype=abstract.
51. Murphy LO, Smith S, Chen R-H, Fingar DC, Blenis J, (2002) Molecular interpretation of ERK signal duration by immediate early gene products. Nature Cell Biology 4: 556-564 Available:http://www.ncbi.nlm.nih.gov/pubmed/12134156.
52. Chalmers CJ, Gilley R, March HN, Balmanno K, Cook SJ, (2007) The duration of ERK1/2 activity determines the activation of c-Fos and Fra-1 and the composition and quantitative transcriptional output of AP-1. Cellular Signalling 19: 695-704 Available:http://www.ncbi.nlm.nih.gov/pubmed/17052890.
53. Murphy LO, Blenis J, (2006) MAPK signal specificity: the right place at the right time. Trends in Biochemical Sciences 31: 268-275 Available:http://www.ncbi.nlm.nih.gov/pubmed/16603362.
54. Ebisuya M, Kondoh K, Nishida E, (2005) The duration, magnitude and compartmentalization of ERK MAP kinase activity: mechanisms for providing signaling specificity. Journal of Cell Science 118: 2997-3002 Available:http://www.ncbi.nlm.nih.gov/pubmed/16014377.
55. Bolden JE, Peart MJ, Johnstone RW, (2006) Anticancer activities of histone deacetylase inhibitors. Nature Reviews on Drug Discovery 5: 769-784 Available:http://www.ncbi.nlm.nih.gov/pubmed/16955068.
56. Morotomi MM, Guillem JG, Logerfo P, Weinstein IB, (1990) Production of Diacylglycerol, an Activator of Protein Kinase C, by Human Intestinal Microflora Cancer Research. 50: 3595-3599.
57. Pongracz J, Clark P, Neoptolemos JP, Lord JM, (1995) Expression of protein kinase C isoenzymes in colorectal cancer tissue and their differential activation by different bile acids. International Journal of Cancer 61: 35-39 Available:http://www.ncbi.nlm.nih.gov/pubmed/7705931.
58. Weisburger JH, Reddy BS, Barnes WS, Wynder EL, (1983) Bile acids, but not neutral sterols, are tumor promoters in the colon in man and in rodents. Environmental Health Perspectives 50: 101-107 Available:http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1569211&tool=pmcentrez&rendertype=abstract.
59. Ou J, DeLany JP, Zhang M, Sharma S, O'Keefe SJD, (2012) Association between low colonic short-chain fatty acids and high bile acids in high colon cancer risk populations. Nutrition & Cancer 64: 34-40 Available:http://www.ncbi.nlm.nih.gov/pubmed/22136517.
60. Tap J, Mondot S, Levenez F, Pelletier E, Caron C, et al. (2009) Towards the human intestinal microbiota phylogenetic core. Environmental Microbiology 11: 2574-2584 Available:http://www.ncbi.nlm.nih.gov/pubmed/19601958.