The role of curcumin in modulating colonic microbiota during colitis and colon cancer prevention

Inflammatory Bowel Diseases

Volumn 21, Issue 11, 2015, Pages 2483-2494

  Mcfadden, Rita Marie T ^a,b   Larmonier, Claire B ^a   Shehab, Kareem W ^a   Midura Kiela, Monica ^a   Ramalingam, Rajalakshmy ^a   Harrison, Christy A ^a   Besselsen, David G ^c   Chase, John H ^d   Caporaso, J Gregory ^d   Jobin, Christian ^e   Ghishan, Fayez K ^a   Kiela, Pawel R ^a,f  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

^d NORTHERN ARIZONA UNIVERSITY   (United States)

^e UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF ARIZONA   (United States)

Author keywords

16S; colitis associated colon cancer; curcumin; diet; microbiota; ribosomal RNA

Indexed keywords

ABC TRANSPORTER; ARACHIDONIC ACID; AZOXYMETHANE; BETA CATENIN; CURCUMIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; MESSENGER RNA; PHOSPHATE BUFFERED SALINE; STYRENE; TUMOR NECROSIS FACTOR ALPHA; CARCINOGEN;

129/SVEV MOUSE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CANCER PREVENTION; CHEMOPROPHYLAXIS; COLITIS; COLON CANCER; COLON FLORA; CONTROLLED STUDY; DIET SUPPLEMENTATION; DISEASE ASSOCIATION; DRUG BIOAVAILABILITY; DRUG EFFECT; FECES ANALYSIS; HISTOPATHOLOGY; IMMUNE RESPONSE; INFECTION PREVENTION; INTESTINE FLORA; LACTOBACILLALES; MICROBIAL COMMUNITY; MICROBIOLOGICAL EXAMINATION; MOUSE; NONHUMAN; ORGAN WEIGHT; PRIORITY JOURNAL; SURVIVAL RATE; TAXONOMIC RANK; TUMOR VOLUME; WEIGHT GAIN; WEIGHT HEIGHT RATIO; WILD TYPE; 129 MOUSE; ANIMAL; CELL TRANSFORMATION; CHEMICALLY INDUCED; COLON; COLORECTAL NEOPLASMS; DIETARY SUPPLEMENT; DISEASE MODEL; DRUG EFFECTS; INTESTINE MUCOSA; KNOCKOUT MOUSE; MICROBIOLOGY; MICROFLORA; MUCOSAL IMMUNITY; PATHOLOGY;

ANIMALS; AZOXYMETHANE; CARCINOGENS; CELL TRANSFORMATION, NEOPLASTIC; COLITIS; COLON; COLORECTAL NEOPLASMS; CURCUMIN; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; IMMUNITY, MUCOSAL; INTESTINAL MUCOSA; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; MICROBIOTA;

EID: 84945279241     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000000522     Document Type: Article

References (74)

1. American Cancer Society. Cancer Facts and Figures 2015. Atlanta, Georgia: American Cancer Society; 2015.
2. Brenner H, Kloor M, Pox CP. Colorectal cancer. Lancet. 2014;383:1490-1502.
3. Watson AJ, Collins PD. Colon cancer: a civilization disorder. Dig Dis. 2011;29:222-228.
4. Heidland A, Klassen A, Rutkowski P, et al. The contribution of Rudolf Virchow to the concept of inflammation: what is still of importance? J Nephrol. 2006;19(suppl 10):S102-S109.
5. Feagins LA, Souza RF, Spechler SJ. Carcinogenesis in IBD: potential targets for the prevention of colorectal cancer. Nat Rev Gastroenterol Hepatol. 2009;6:297-305.
6. Gupta RB, Harpaz N, Itzkowitz S, et al. Histologic inflammation is a risk factor for progression to colorectal neoplasia in ulcerative colitis: a cohort study. Gastroenterology. 2007;133:1099-1105; quiz 340-1.
7. Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol. 2004;287:G7-G17.
8. Rutter M, Saunders B, Wilkinson K, et al. Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology. 2004;126:451-459.
9. Huttenhower C, Kostic AD, Xavier RJ. Inflammatory bowel disease as a model for translating the microbiome. Immunity. 2014;40:843-854.
10. Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer. 2013;13:800-812.
11. Arthur JC, Jobin C. The complex interplay between inflammation, the microbiota and colorectal cancer. Gut Microbes. 2013;4:253-258.
12. Sears CL, Garrett WS. Microbes, microbiota, and colon cancer. Cell Host Microbe. 2014;15:317-328.
13. Garrett WS, Gallini CA, Yatsunenko T, et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe. 2010;8:292-300.
14. Ramamoorthi G, Sivalingam N. Molecular mechanism of TGF-b signaling pathway in colon carcinogenesis and status of curcumin as chemopreventive strategy. Tumour Biol. 2014;5:7295-7305.
15. Goel A, Aggarwal BB. Curcumin, the golden spice from Indian saffron, is a chemosensitizer and radiosensitizer for tumors and chemoprotector and radioprotector for normal organs. Nutr Cancer. 2010;62:919-930.
16. Shehzad A, Wahid F, Lee YS. Curcumin in cancer chemoprevention: molecular targets, pharmacokinetics, bioavailability, and clinical trials. Arch Pharm (Weinheim). 2010;343:489-499.
17. Billerey-Larmonier C, Uno JK, Larmonier N, et al. Protective effects of dietary curcumin in mouse model of chemically induced colitis are strain dependent. Inflamm Bowel Dis. 2008;14:780-793.
18. Larmonier CB, Midura-Kiela MT, Ramalingam R, et al. Modulation of neutrophil motility by curcumin: implications for inflammatory bowel disease. Inflamm Bowel Dis. 2011;17:503-515.
19. Midura-Kiela MT, Radhakrishnan VM, Larmonier CB, et al. Curcumin inhibits interferon-g signaling in colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2012;302:G85-G96.
20. Radhakrishnan VM, Kojs P, Young G, et al. pTyr421 cortactin is overexpressed in colon cancer and is dephosphorylated by curcumin: involvement of non-receptor type 1 protein tyrosine phosphatase (PTPN1). PLoS One. 2014;9:e85796.
21. Villegas I, Sanchez-Fidalgo S, de la Lastra CA. Chemopreventive effect of dietary curcumin on inflammation-induced colorectal carcinogenesis in mice. Mol Nutr Food Res. 2011;55:259-267.
22. Harlan Laboratories. NIH-31 Modified Open Formula Mouse/Rat Sterilizable Diet. Available at: http://www.harlan.com/download. axd/267f1ea0f91446c49cb6cdda2c93c216.pdf?d7013%20datasheet. Accessed June 26, 2015.
23. Sharma RA, Euden SA, Platton SL, et al. Phase I clinical trial of oral curcumin: biomarkers of systemic activity and compliance. Clin Cancer Res. 2004;10:6847-6854.
24. Cheng AL, Hsu CH, Lin JK, et al. Phase I clinical trial of curcumin, a chemopreventive agent, in patients with high-risk or pre-malignant lesions. Anticancer Res. 2001;21:2895-2900.
25. Kanneganti M, Mino-Kenudson M, Mizoguchi E. Animal models of colitisassociated carcinogenesis. J Biomed Biotechnol. 2011;2011:342637.
26. Uronis JM, Muhlbauer M, Herfarth HH, et al. Modulation of the intestinal microbiota alters colitis-Associated colorectal cancer susceptibility. PLoS One. 2009;4:e6026.
27. Kuhn R, Lohler J, Rennick D, et al. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75:263-274.
28. Gomes-Santos AC, Moreira TG, Castro-Junior AB, et al. New insights into the immunological changes in IL-10-deficient mice during the course of spontaneous inflammation in the gut mucosa. Clin Dev Immunol. 2012; 2012:560817.
29. Kiela PR, Midura AJ, Kuscuoglu N, et al. Effects of Boswellia serrata in mouse models of chemically induced colitis. Am J Physiol Gastrointest Liver Physiol. 2005;288:G798-G808.
30. Caporaso JG, Lauber CL, Walters WA. Ultra-high-Dhroughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6:1621-1624.
31. Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-Dhroughput community sequencing data. Nat Methods. 2010;7:335-336.
32. Bokulich NA, Subramanian S, Faith JJ, et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods. 2013;10:57-59.
33. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460-2461.
34. Rideout JR, He Y, Navas-Molina JA, et al. Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. PeerJ. 2014;2:e545.
35. McDonald D, Price MN, Goodrich J, et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 2012; 6:610-618.
36. Caporaso JG, Bittinger K, Bushman FD, et al. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010;26: 266-267.
37. Price MN, Dehal PS, Arkin AP. FastTree 2-Approximately maximumlikelihood trees for large alignments. PLoS One. 2010;5:e9490.
38. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005;71:8228-8235.
39. Faith DP. Conservation evaluation and phylogenetic diversity. Biol Conserv. 1992;61:1-10.
40. Chao A. Nonparametric estimation of the number of classes in a population. Scand J Stat. 1984;11:265-270.
41. Langille MG, Zaneveld J, Caporaso JG, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31:814-821.
42. Parks DH, Tyson GW, Hugenholtz P, et al. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014;30: 3123-3124.
43. Ostanin DV, Bao J, Koboziev I, et al. T cell transfer model of chronic colitis: concepts, considerations, and tricks of the trade. Am J Physiol Gastrointest Liver Physiol. 2009;296:G135-G146.
44. Neufert C, Becker C, Neurath MF. An inducible mouse model of colon carcinogenesis for the analysis of sporadic and inflammation-driven tumor progression. Nat Protoc. 2007;2:1998-2004.
45. Miyaki M, Iijima T, Kimura J, et al. Frequent mutation of beta-catenin and APC genes in primary colorectal tumors from patients with hereditary nonpolyposis colorectal cancer. Cancer Res. 1999;59:4506-4509.
46. Foersch S, Neurath MF. Colitis-Associated neoplasia: molecular basis and clinical translation. Cell Mol Life Sci. 2014;71:3523-3535.
47. Arthur JC, Perez-Chanona E, Muhlbauer M, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science. 2012;338: 120-123.
48. Larmonier CB, Uno JK, Lee KM, et al. Limited effects of dietary curcumin on Th-1 driven colitis in IL-10 deficient mice suggest an IL-10-dependent mechanism of protection. Am J Physiol Gastrointest Liver Physiol. 2008;295:G1079-G1091.
49. Murphy EA, Davis JM, McClellan JL, et al. Curcumin's effect on intestinal inflammation and tumorigenesis in the ApcMin/+ mouse. J Interferon Cytokine Res. 2011;31:219-226.
50. Shehzad A, Lee J, Lee YS. Curcumin in various cancers. Biofactors. 2013;39:56-68.
51. Arthur JC, Jobin C. The struggle within: microbial influences on colorectal cancer. Inflamm Bowel Dis. 2011;17:396-409.
52. Lightfoot YL, Yang T, Sahay B, et al. Targeting aberrant colon cancerspecific DNA methylation with lipoteichoic acid-deficient Lactobacillus acidophilus. Gut Microbes. 2013;4:84-88.
53. Asha A, Gayathri D. Synergistic impact of Lactobacillus fermentum, Lactobacillus plantarum and vincristine on 1,2-dimethylhydrazine-induced colorectal carcinogenesis in mice. Exp Ther Med. 2012;3:1049-1054.
54. Khazaie K, Zadeh M, Khan MW, et al. Abating colon cancer polyposis by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci U S A. 2012;109:10462-10467.
55. Chang JH, Shim YY, Cha SK, et al. Effect of Lactobacillus acidophilus KFRI342 on the development of chemically induced precancerous growths in the rat colon. J Med Microbiol. 2012;61:361-368.
56. Raman M, Ambalam P, Kondepudi KK, et al. Potential of probiotics, prebiotics and synbiotics for management of colorectal cancer. Gut Microbes. 2013;4:181-192.
57. Wan Y, Xin Y, Zhang C, et al. Fermentation supernatants of inhibit growth of human colon cancer cells and induce apoptosis through a caspase 3-dependent pathway. Oncol Lett. 2014;7:1738-1742.
58. Wang SM, Zhang LW, Fan RB, et al. Induction of HT-29 cells apoptosis by lactobacilli isolated from fermented products. Res Microbiol. 2014; 165:202-214.
59. Gianotti L, Morelli L, Galbiati F, et al. A randomized double-blind trial on perioperative administration of probiotics in colorectal cancer patients. World J Gastroenterol. 2010;16:167-175.
60. Ishikawa H, Akedo I, Otani T, et al. Randomized trial of dietary fiber and Lactobacillus casei administration for prevention of colorectal tumors. Int J Cancer. 2005;116:762-767.
61. Rafter J, Bennett M, Caderni G, et al. Dietary synbiotics reduce cancer risk factors in polypectomized and colon cancer patients. Am J Clin Nutr. 2007;85:488-496.
62. Liboredo JC, Anastacio LR, Peluzio Mdo C, et al. Effect of probiotics on the development of dimethylhydrazine-induced preneoplastic lesions in the mice colon. Acta Cir Bras. 2013;28:367-372.
63. Xu Z, Malmer D, Langille MG, et al. Which is more important for classifying microbial communities: who's there or what they can do? ISME J. 2014;8:2357-2359.
64. Tilg H, Kaser A. Gut microbiome, obesity, and metabolic dysfunction. J Clin Invest. 2011;121:2126-2132.
65. Turnbaugh PJ, Ridaura VK, Faith JJ, et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 2009;1:6ra14.
66. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, et al. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology. 2009;137:1716-1724.e1-2.
67. Mukhopadhya I, Hansen R, Nicholl CE, et al. A comprehensive evaluation of colonic mucosal isolates of Sutterella wadsworthensis from inflammatory bowel disease. PLoS One. 2011;6:e27076.
68. Houot L, Chang S, Absalon C, et al. Vibrio cholerae phosphoenolpyruvate phosphotransferase system control of carbohydrate transport, biofilm formation, and colonization of the germfree mouse intestine. Infect Immun. 2010;78:1482-1494.
69. Na HS, Cha MH, Oh DR, et al. Protective mechanism of curcumin against Vibrio vulnificus infection. FEMS Immunol Med Microbiol. 2011;63: 355-362.
70. De R, Kundu P, Swarnakar S, et al. Antimicrobial activity of curcumin against Helicobacter pylori isolates from India and during infections in mice. Antimicrob Agents Chemother. 2009;53:1592-1597.
71. Rudrappa T, Bais HP. Curcumin, a known phenolic from Curcuma longa, attenuates the virulence of Pseudomonas aeruginosa PAO1 in whole plant and animal pathogenicity models. J Agric Food Chem. 2008;56:1955-1962.
72. Rao CV, Simi B, Reddy BS. Inhibition by dietary curcumin of azoxymethane-induced ornithine decarboxylase, tyrosine protein kinase, arachidonic acid metabolism and aberrant crypt foci formation in the rat colon. Carcinogenesis. 1993;14:2219-2225.
73. Sorrell TC, Muller M, Sztelma K. Bacterial metabolism of human polymorphonuclear leukocyte-derived arachidonic acid. Infect Immun. 1992; 60:1779-1785.
74. Zhan Y, Chen PJ, Sadler WD, et al. Gut microbiota protects against gastrointestinal tumorigenesis caused by epithelial injury. Cancer Res. 2013;73:7199-7210.