A bronze-tomato enriched diet affects the intestinal microbiome under homeostatic and inflammatory conditions

Nutrients

Volumn 10, Issue 12, 2018, Pages

  Liso, Marina ^a   De Santis, Stefania ^b   Scarano, Aurelia ^c   Verna, Giulio ^a   Dicarlo, Manuela ^a   Galleggiante, Vanessa ^a   Campiglia, Pietro ^b   Mastronardi, Mauro ^a   Lippolis, Antonio ^a   Vacca, Mirco ^d   Sobolewski, Anastasia ^e   Serino, Grazia ^a   Butelli, Eugenio ^f   De Angelis, Maria ^d   Martin, Cathie ^f   Santino, Angelo ^c   Chieppa, Marcello ^a  

^a S de Bellis Research Hospital   (Italy)

^b UNIVERSITY OF SALERNO   (Italy)

^c INSTITUTE OF SCIENCES OF FOOD PRODUCTION   (Italy)

^d UNIVERSITY OF BARI   (Italy)

^e UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^f JOHN INNES CENTRE   (United Kingdom)

Author keywords

Bronze tomatoes; Inflammatory bowel disease (IBD); Microbiota; Murine models; Polyphenols

Indexed keywords

HEME OXYGENASE 1; INTERLEUKIN 17; POLYPHENOL; RNA 16S; ANTIINFLAMMATORY AGENT; GAMMA INTERFERON;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL FLORA; BRONZE TOMATO ENRICHED DIET; CONTROLLED STUDY; CYTOFLUOROMETRY; DIET; DNA EXTRACTION; DYSBIOSIS; ENTERITIS; HOMEOSTASIS; IMMUNE RESPONSE; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; ULCERATIVE COLITIS; ANIMAL; BACTERIUM; BIOSYNTHESIS; C57BL MOUSE; CD4+ T LYMPHOCYTE; CHEMISTRY; CLASSIFICATION; DIET THERAPY; DISEASE MODEL; FRUIT; GENETICS; INFLAMMATION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; TOMATO;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BACTERIA; CD4-POSITIVE T-LYMPHOCYTES; COLITIS, ULCERATIVE; DIET; DISEASE MODELS, ANIMAL; DYSBIOSIS; FRUIT; GASTROINTESTINAL MICROBIOME; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; INTERFERON-GAMMA; INTERLEUKIN-17; LYCOPERSICON ESCULENTUM; MICE; MICE, INBRED C57BL; POLYPHENOLS; RNA, RIBOSOMAL, 16S;

EID: 85057964806     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu10121862     Document Type: Article

References (52)

1. Ungaro, R.; Mehandru, S.; Allen, P.B.; Peyrin-Biroulet, L.; Colombel, J.F. Ulcerative colitis. Lancet 2017, 389, 1756–1770. [CrossRef]
2. Torres, J.; Mehandru, S.; Colombel, J.F.; Peyrin-Biroulet, L. Crohn’s disease. Lancet 2017, 389, 1741–1755. [CrossRef]
3. De Souza, H.S.; Fiocchi, C. Immunopathogenesis of IBD: Current state of the art. Nat. Rev. Gastroenterol. Hepatol. 2016, 13, 13–27. [CrossRef] [PubMed]
4. Ananthakrishnan, A.N. Epidemiology and risk factors for IBD. Nat. Rev. Gastroenterol. Hepatol. 2015, 12, 205–217. [CrossRef] [PubMed]
5. Luo, Y.; de Lange, K.M.; Jostins, L.; Moutsianas, L.; Randall, J.; Kennedy, N.A.; Lamb, C.A.; McCarthy, S.; Ahmad, T.; Edwards, C.; et al. Exploring the genetic architecture of inflammatory bowel disease by whole-genome sequencing identifies association at ADCY7. Nat. Genet. 2017, 49, 186–192. [CrossRef] [PubMed]
6. Zanello, G.; Goethel, A.; Forster, K.; Geddes, K.; Philpott, D.J.; Croitoru, K. Nod2 activates NF-kB in CD4+ T cells but its expression is dispensable for T cell-induced colitis. PLoS ONE 2013, 8, e82623. [CrossRef] [PubMed]
7. Philpott, D.J.; Sorbara, M.T.; Robertson, S.J.; Croitoru, K.; Girardin, S.E. NOD proteins: Regulators of inflammation in health and disease. Nat. Rev. Immunol. 2014, 14, 9–23. [CrossRef] [PubMed]
8. McGovern, D.; Kugathasan, S.; Cho, J.H. Genetics of Inflammatory Bowel Diseases. Gastroenterology 2015, 149, 1163–1176.e2. [CrossRef] [PubMed]
9. Ananthakrishnan, A.N.; Bernstein, C.N.; Iliopoulos, D.; Macpherson, A.; Neurath, M.F.; Ali, R.A.R.; Vavricka, S.R.; Fiocchi, C. Environmental triggers in IBD: A review of progress and evidence. Nat. Rev. Gastroenterol. Hepatol. 2018, 15, 39–49. [CrossRef] [PubMed]
10. Virta, L.; Auvinen, A.; Helenius, H.; Huovinen, P.; Kolho, K.L. Association of repeated exposure to antibiotics with the development of pediatric Crohn’s disease—A nationwide, register-based finnish case-control study. Am. J. Epidemiol. 2012, 175, 775–784. [CrossRef] [PubMed]
11. Kronman, M.P.; Zaoutis, T.E.; Haynes, K.; Feng, R.; Coffin, S.E. Antibiotic exposure and IBD development among children: A population-based cohort study. Pediatrics 2012, 130, e794–e803. [CrossRef] [PubMed]
12. Lee, D.; Albenberg, L.; Compher, C.; Baldassano, R.; Piccoli, D.; Lewis, J.D.; Wu, G.D. Diet in the pathogenesis and treatment of inflammatory bowel diseases. Gastroenterology 2015, 148, 1087–1106. [CrossRef] [PubMed]
13. Knight-Sepulveda, K.; Kais, S.; Santaolalla, R.; Abreu, M.T. Diet and Inflammatory Bowel Disease. Gastroenterol. Hepatol. 2015, 11, 511–520.
14. Dixon, L.J.; Kabi, A.; Nickerson, K.P.; McDonald, C. Combinatorial effects of diet and genetics on Inflammatory Bowel Disease pathogenesis. Inflamm. Bowel Dis. 2015, 21, 912–922. [CrossRef] [PubMed]
15. Basson, A.; Trotter, A.; Rodriguez-Palacios, A.; Cominelli, F. Mucosal Interactions between Genetics, Diet, and Microbiome in Inflammatory Bowel Disease. Front. Immunol. 2016, 7, 290. [CrossRef] [PubMed]
16. Zhang, S.L.; Wang, S.N.; Miao, C.Y. Influence of microbiota on intestinal immune system in Ulcerative Colitis and its intervention. Front. Immunol. 2017, 8, 1674. [CrossRef] [PubMed]
17. Rapozo, D.C.; Bernardazzi, C.; de Souza, H.S. Diet and microbiota in inflammatory bowel disease: The gut in disharmony. World J. Gastroenterol. 2017, 23, 2124–2140. [CrossRef] [PubMed]
18. Dolan, K.T.; Chang, E.B. Diet, gut microbes, and the pathogenesis of inflammatory bowel diseases. Mol. Nutr. Food Res. 2017, 61. [CrossRef] [PubMed]
19. Scarano, A.; Butelli, E.; De Santis, S.; Cavalcanti, E.; Hill, L.; De Angelis, M.; Giovinazzo, G.; Chieppa, M.; Martin, C.; Santino, A. Combined dietary anthocyanins, flavonols, and stilbenoids alleviate inflammatory bowel disease symptoms in mice. Front. Nutr. 2018, 4, 75. [CrossRef] [PubMed]
20. Eri, R.D.; Adams, R.J.; Tran, T.V.; Tong, H.; Das, I.; Roche, D.K.; Oancea, I.; Png, C.W.; Jeffery, P.L.; Radford-Smith, G.L.; et al. An intestinal epithelial defect conferring ER stress results in inflammation involving both innate and adaptive immunity. Mucosal Immunol. 2011, 4, 354–364. [CrossRef] [PubMed]
21. Klindworth, A.; Pruesse, E.; Schweer, T.; Peplies, J.; Quast, C.; Horn, M.; Glöckner, F.O. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013, 41, e1. [CrossRef]
22. Altschul, S.F.; Gish, W.; Miller, W.; Myers, E.W.; Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215, 403–410. [CrossRef]
23. Andreotti, R.; Pérez de León, A.; Dowd, S.E.; Guerrero, F.D.; Bendele, K.G.; Scoles, G. Assessment of bacterial diversity in the cattle tick Rhipicephalus (Boophilus) microplus through tag-encoded pyrosequencing. BMC Microbiol. 2011, 11, 6. [CrossRef] [PubMed]
24. Chao, A.; Bunge, J. Estimating the number of species in a stochastic abundance model. Biometrics 2002, 58, 531–539. [CrossRef] [PubMed]
25. Shannon, C.E.; Weaver, W. The Mathematical Theory of Communication; University of Illinois Press: Urbana, IL, USA, 1949.
26. Suchodolski, J.S.; Dowd, S.E.; Wilke, V.; Steiner, J.M.; Jergens, A.E. 16S rRNA gene pyrosequencing reveals bacterial dysbiosis in the duodenum of dogs with idiopathic inflammatory bowel disease. PLoS ONE 2012, 7, E39333. [CrossRef] [PubMed]
27. Gondalia, S.V.; Palombo, E.A.; Knowles, S.R.; Cox, S.B.; Meyer, D.; Austin, D.W. Molecular characterisation of gastrointestinal microbiota of children with autism (with and without gastrointestinal dysfunction) and their neurotypical siblings. Autism Res. 2012, 5, 419–427. [CrossRef] [PubMed]
28. De Angelis, M.; Piccolo, M.; Vannini, L.; Siragusa, S.; De Giacomo, A.; Serrazzanetti, D.I.; Cristofori, F.; Guerzoni, M.E.; Gobbetti, M.; Francavilla, R. Fecal Microbiota and Metabolome of Children with Autism and Pervasive Developmental Disorder Not Otherwise Specified. PLoS ONE 2013, 8, e76993. [CrossRef] [PubMed]
29. Finegold, S.M.; Dowd, S.E.; Gontcharova, V.; Liu, C.; Henley, K.E.; Wolcott, R.D.; Youn, E.; Summanen, P.H.; Granpeesheh, D.; Dixon, D.; et al. Pyrosequencing study of fecal microbiota of autistic and control children. Anaerobe 2010, 16, 444–453. [CrossRef] [PubMed]
30. Serino, M.; Luche, E.; Grès, S.; Baylac, A.; Bergé, M.; Cénac, C.; Waget, A.; Klopp, P.; Iacovoni, J.; Klopp, C.; et al. Metabolic adaptation to a high-fat diet is associated with a change in the gut microbiota. Gut 2012, 61, 543–553. [CrossRef] [PubMed]
31. De Santis, S.; Galleggiante, V.; Scandiffio, L.; Liso, M.; Sommella, E.; Sobolewski, A.; Spilotro, V.; Pinto, A.; Campiglia, P.; Serino, G.; et al. Secretory leukoprotease inhibitor (Slpi) expression is required for educating murine dendritic cells inflammatory response following Quercetin exposure. Nutrients 2017, 9, 706. [CrossRef] [PubMed]
32. De Santis, S.; Kunde, D.; Serino, G.; Galleggiante, V.; Caruso, M.L.; Mastronardi, M.; Cavalcanti, E.; Ranson, N.; Pinto, A.; Campiglia, P.; et al. Secretory leukoprotease inhibitor is required for efficient quercetin-mediated suppression of TNFα secretion. Oncotarget 2016, 7, 75800–75809. [CrossRef] [PubMed]
33. Shen, Z.H.; Zhu, C.X.; Quan, Y.S.; Yang, Z.Y.; Wu, S.; Luo, W.W.; Tan, B.; Wang, X.Y. Relationship between intestinal microbiota and ulcerative colitis: Mechanisms and clinical application of probiotics and fecal microbiota transplantation. World J. Gastroenterol. 2018, 24, 5–14. [CrossRef] [PubMed]
34. Lane, E.R.; Zisman, T.L.; Suskind, D.L. The microbiota in inflammatory bowel disease: Current and therapeutic insights. J. Inflamm. Res. 2017, 10, 63–73. [CrossRef] [PubMed]
35. Chen, W.X.; Ren, L.H.; Shi, R.H. Enteric microbiota leads to new therapeutic strategies for ulcerative colitis. World J. Gastroenterol. 2014, 20, 15657–15663. [CrossRef] [PubMed]
36. Zuo, T.; Ng, S.C. The gut microbiota in the pathogenesis and therapeutics of Inflammatory Bowel Disease. Front. Microbiol. 2018, 9, 2247. [CrossRef] [PubMed]
37. Marini, M.; Bamias, G.; Rivera-Nieves, J.; Moskaluk, C.A.; Hoang, S.B.; Ross, W.G.; Pizarro, T.T.; Cominelli, F. TNF-alpha neutralization ameliorates the severity of murine Crohn’s-like ileitis by abrogation of intestinal epithelial cell apoptosis. Proc. Natl. Acad. Sci. USA 2003, 100, 8366–8371. [CrossRef] [PubMed]
38. Rutgeerts, P.; Sandborn, W.J.; Feagan, B.G.; Reinisch, W.; Olson, A.; Johanns, J.; Travers, S.; Rachmilewitz, D.; Hanauer, S.B.; Lichtenstein, G.R.; et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N. Engl. J. Med. 2005, 353, 2462–2476. [CrossRef] [PubMed]
39. Flamant, M.; Roblin, X. Inflammatory bowel disease: Towards a personalized medicine. Therap. Adv. Gastroenterol. 2018, 11. [CrossRef] [PubMed]
40. Pineton de Chambrun, G.; Blanc, P.; Peyrin-Biroulet, L. Current evidence supporting mucosal healing and deep remission as important treatment goals for inflammatory bowel disease. Expert Rev. Gastroenterol. Hepatol. 2016, 10, 915–927. [CrossRef]
41. Dai, C.; Liu, W.X.; Jiang, M.; Sun, M.J. Mucosal healing did not predict sustained clinical remission in patients with IBD after discontinuation of one-year infliximab therapy. PLoS ONE 2014, 9, e110797. [CrossRef] [PubMed]
42. Nemoto, H.; Kataoka, K.; Ishikawa, H.; Ikata, K.; Arimochi, H.; Iwasaki, T.; Ohnishi, Y.; Kuwahara, T.; Yasutomo, K. Reduced diversity and imbalance of fecal microbiota in patients with ulcerative colitis. Dig. Dis. Sci. 2012, 57, 2955–2964. [CrossRef] [PubMed]
43. Sokol, H.; Seksik, P.; Furet, J.P.; Firmesse, O.; Nion-Larmurier, I.; Beaugerie, L.; Cosnes, J.; Corthier, G.; Marteau, P.; Doré, J. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm. Bowel Dis. 2009, 15, 1183–1189. [CrossRef] [PubMed]
44. James, S.L.; Christophersen, C.T.; Bird, A.R.; Conlon, M.A.; Rosella, O.; Gibson, P.R.; Muir, J.G. Abnormal fibre usage in UC in remission. Gut 2015, 64, 562–570. [CrossRef] [PubMed]
45. Galleggiante, V.; De Santis, S.; Cavalcanti, E.; Scarano, A.; De Benedictis, M.; Serino, G.; Caruso, M.L.; Mastronardi, M.; Pinto, A.; Campiglia, P.; et al. Dendritic cells modulate iron homeostasis and inflammatory abilities following Quercetin exposure. Curr. Pharm. Des. 2017, 23, 2139–2146. [CrossRef] [PubMed]
46. Casén, C.; Vebø, H.C.; Sekelja, M.; Hegge, F.T.; Karlsson, M.K.; Ciemniejewska, E.; Dzankovic, S.; Frøyland, C.; Nestestog, R.; Engstrand, L.; et al. Deviations in human gut microbiota: A novel diagnostic test for determining dysbiosis in patients with IBS or IBD. Aliment. Pharmacol. Ther. 2015, 42, 71–83. [CrossRef] [PubMed]
47. Fuentes, S.; Rossen, N.G.; van der Spek, M.J.; Hartman, J.H.; Huuskonen, L.; Korpela, K.; Salojärvi, J.; Aalvink, S.; de Vos, W.M.; D’Haens, G.R.; et al. Microbial shifts and signatures of long-term remission in ulcerative colitis after faecal microbiota transplantation. ISME J. 2017, 11, 1877–1889. [CrossRef] [PubMed]
48. Chieppa, M.; Giannelli, G. Immune Cells and Microbiota Response to Iron Starvation. Front. Med. 2018, 18, 109. [CrossRef]
49. Liso, M.; Chieppa, M. Complementary Nutritional Treatment for IBD. J. Mucosal Immunol. Res. 2018, 2, e104.
50. Rajendran, N.; Kumar, D. Role of diet in the management of inflammatory bowel disease. World J. Gastroenterol. 2010, 16, 1442–1448. [CrossRef] [PubMed]
51. Mijan, M.A.; Lim, B.O. Diets, functional foods, and nutraceuticals as alternative therapies for inflammatory bowel disease: Present status and future trends. World J. Gastroenterol. 2018, 24, 2673–2685. [CrossRef] [PubMed]
52. Halmos, E.P.; Gibson, P.R. Dietary management of IBD—Insights and advice. Nat. Rev. Gastroenterol. Hepatol. 2015, 12, 133–146. [CrossRef] [PubMed]