Olive oil bioactives protect pigs against experimentally-induced chronic inflammation independently of alterations in gut microbiota

PLoS ONE

Volumn 12, Issue 3, 2017, Pages

  Liehr, Martin ^a   Mereu, Alessandro ^b,d   Pastor, Jose Javier ^b   Quintela, Jose Carlos ^c   Staats, Stefanie ^a   Rimbach, Gerald ^a   Ipharraguerre, Ignacio Rodolfo ^a,b  

^a UNIVERSITY OF KIEL   (Germany)

^b Lucta SA   (Spain)

^c ProNutra Solutions   (Spain)

^d Yara International ASA   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ADHEREN JUNCTION PROTEIN; INTERLEUKIN 1BETA; MEMBRANE PROTEIN; OLIVE OIL; TIGHT JUNCTION PROTEIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ANTIINFLAMMATORY AGENT; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIDEPRESSANT ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL CULTURE; CHRONIC INFLAMMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG CYTOTOXICITY; ELECTRIC RESISTANCE; ENTERITIS; ESCHERICHIA COLI; GROWTH RATE; HUMAN; HUMAN CELL; IN VIVO STUDY; INGESTION; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; MACROPHAGE; MALE; NONHUMAN; PORCINE MODEL; TRANSEPITHELIAL ELECTRICAL RESISTANCE; WEIGHT GAIN; ANIMAL; BLOOD; CACO-2 CELL LINE; CHEMISTRY; CHRONIC DISEASE; GROWTH, DEVELOPMENT AND AGING; INFLAMMATION; MICROBIOLOGY; MOUSE; PIG; RAW 264.7 CELL LINE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CACO-2 CELLS; CHRONIC DISEASE; CYTOKINES; GASTROINTESTINAL MICROBIOME; HUMANS; INFLAMMATION; MALE; MICE; OLIVE OIL; RAW 264.7 CELLS; SWINE;

EID: 85016441144     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0174239     Document Type: Article

References (84)

1. Medzhitov R. Origin and physiological roles of inflammation. Nature. 2008; 454: 428-435. https://doi.org/10.1038/nature07201 PMID: 18650913
2. Jiminez JA, Uwiera TC, Douglas Inglis G, Uwiera RRE. Animal models to study acute and chronic intestinal inflammation in mammals. Gut Pathog. 2015; 7: 29. https://doi.org/10.1186/s13099-015-0076-y PMID: 26561503
3. Murakami M, Hirano T. The molecular mechanisms of chronic inflammation development. Front Immunol. 2012; 3: 323. https://doi.org/10.3389/fimmu.2012.00323 PMID: 23162547
4. Ashley NT, Weil ZM, Nelson RJ. Inflammation. Mechanisms, Costs, and Natural Variation. Annu. Rev. Ecol. Evol. Syst. 2012; 43: 385-406.
5. Dinarello CA. Historical insights into cytokines. Eur J Immunol. 2007; 37 Suppl 1: S34-45.
6. Mantovani G, Anker SD, Inui A, Morley JE, Fanelli FR, Scevola D, et al. Cachexia and Wasting: A Modern Approach. Milano: Springer Milan; 2006.
7. Papadakis KA, Targan SR. Role of cytokines in the pathogenesis of inflammatory bowel disease. Annu Rev Med. 2000; 51: 289-298. https://doi.org/10.1146/annurev.med.51.1.289 PMID: 10774465
8. Feghali CA, Wright TM. Cytokines in acute and chronic inflammation. Front Biosci. 1997; 2: d12-26. PMID: 9159205
9. Hanada T, Yoshimura A. Regulation of cytokine signaling and inflammation. Cytokine & Growth Factor Reviews. 2002; 13: 413-421.
10. Rakhshandeh A, Htoo JK, de Lange C. Immune system stimulation of growing pigs does not alter apparent ileal amino acid digestibility but reduces the ratio between whole body nitrogen and sulfur retention. Livestock Science. 2010; 134: 21-23.
11. Ghanbari R, Anwar F, Alkharfy KM, Gilani A-H, Saari N. Valuable nutrients and functional bioactives in different parts of olive (Olea europaea L.)-a review. Int J Mol Sci. 2012; 13: 3291-3340. https://doi.org/10.3390/ijms13033291 PMID: 22489153
12. Bayram B, Ozcelik B, Schultheiss G, Frank J, Rimbach G. A validated method for the determination of selected phenolics in olive oil using high-performance liquid chromatography with coulometric electrochemical detection and a fused-core column. Food Chemistry. 2013; 138: 1663-1669. https://doi.org/10.1016/j.foodchem.2012.11.122 PMID: 23411296
13. Bayram B, Esatbeyoglu T, Schulze N, Ozcelik B, Frank J, Rimbach G. Comprehensive analysis of polyphenols in 55 extra virgin olive oils by HPLC-ECD and their correlation with antioxidant activities. Plant Foods Hum Nutr. 2012; 67: 326-336. https://doi.org/10.1007/s11130-012-0315-z PMID: 23070730
14. Piroddi M, Albini A, Fabiani R, Giovannelli L, Luceri C, Natella F, et al. Nutrigenomics of extra-virgin olive oil: A review. Biofactors. 2016.
15. Visioli F, Galli C. Biological properties of olive oil phytochemicals. Crit Rev Food Sci Nutr. 2002; 42: 209-221. https://doi.org/10.1080/10408690290825529 PMID: 12058980
16. Sanchez-Quesada C, Lopez-Biedma A, Warleta F, Campos M, Beltran G, Gaforio JJ. Bioactive properties of the main triterpenes found in olives, virgin olive oil, and leaves of Olea europaea. J Agric Food Chem. 2013; 61: 12173-12182. https://doi.org/10.1021/jf403154e PMID: 24279741
17. Caramia G, Gori A, Valli E, Cerretani L. Virgin olive oil in preventive medicine. From legend to epigenetics. Eur. J. Lipid Sci. Technol. 2012; 114: 375-388.
18. El SN, Karakaya S. Olive tree (Olea europaea) leaves: potential beneficial effects on human health. Nutr Rev. 2009; 67: 632-638. https://doi.org/10.1111/j.1753-4887.2009.00248.x PMID: 19906250
19. Pereira AP, Ferreira IC, Marcelino F, Valentão P, Andrade PB, Seabra R, et al. Phenolic Compounds and Antimicrobial Activity of Olive (Olea europaea L. Cv. Cobrançosa) Leaves. Molecules. 2007; 12: 1153-1162. PMID: 17873849
20. Benavente-García O, Castillo J, Lorente J, Ortuño A, Del Rio J. Antioxidant activity of phenolics extracted from Olea europaea L. leaves. Food Chemistry. 2000; 68: 457-462.
21. Cardona F, Andres-Lacueva C, Tulipani S, Tinahones FJ, Queipo-Ortuno MI. Benefits of polyphenols on gut microbiota and implications in human health. J Nutr Biochem. 2013; 24: 1415-1422. https://doi.org/10.1016/j.jnutbio.2013.05.001 PMID: 23849454
22. Morton DB, Griffiths PH. Guidelines on the recognition of pain, distress and discomfort in experimental animals and an hypothesis for assessment. Vet Rec. 1985; 116: 431-436. PMID: 3923690
23. Rakhshandeh A, de Lange C F M. Evaluation of chronic immune system stimulation models in growing pigs. Animal. 2012; 6: 305-310. https://doi.org/10.1017/S1751731111001522 PMID: 22436189
24. Sánchez P, Dobarganes MA, Ruiz-Méndez MV. Edible olive pomace oil concentrated in triterpenic acids, procedure of physical refining utilised for obtainment thereof and recovery of functional components present in the crude oil. US Patent No.: US8361518B2
25. Romero C, García A, Medina E, Ruíz-Méndez MV, Castro Ad, Brenes M. Triterpenic acids in table olives. Food Chemistry. 2010; 118: 670-674.
26. Mulinacci N, Romani A, Galardi C, Pinelli P, Giaccherini C, Vincieri FF. Polyphenolic Content in Olive Oil Waste Waters and Related Olive Samples. J. Agric. Food Chem. 2001; 49: 3509-3514. PMID: 11513620
27. Uden P, Colucci PE, van Soest PJ. Investigation of chromium, cerium and cobalt as markers in digesta. Rate of passage studies. J Sci Food Agric. 1980; 31: 625-632. PMID: 6779056
28. Mereu A, Tedo G, Moeser AJ, Rimbach G, Ipharraguerre IR. Cromolyn-mediated improvement of intestinal barrier function is associated with enhanced piglet performance after weaning. BMC Vet Res. 2015; 11: 274. https://doi.org/10.1186/s12917-015-0588-1 PMID: 26510713
29. Chantret I, Rodolosse A, Barbat A, Dussaulx E, Brot-Laroche E, Zweibaum A, et al. Differential expression of sucrase-isomaltase in clones isolated from early and late passages of the cell line Caco-2: evidence for glucose-dependent negative regulation. J Cell Sci. 1994; 107 (Pt 1): 213-225.
30. Ralph P, Nakoinz I. Antibody-dependent killing of erythrocyte and tumor targets by macrophage-related cell lines: enhancement by PPD and LPS. J Immunol. 1977; 119: 950-954. PMID: 894031
31. Borenfreund E, Shopsis C. Toxicity monitored with a correlated set of cell-culture assays. Xenobiotica. 1985; 15: 705-711. https://doi.org/10.3109/00498258509047431 PMID: 4072257
32. Hidalgo IJ, Raub TJ, Borchardt RT. Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology. 1989; 96: 736-749. PMID: 2914637
33. Srinivasan B, Kolli AR, Esch MB, Abaci HE, Shuler ML, Hickman JJ. TEER measurement techniques for in vitro barrier model systems. J Lab Autom. 2015; 20: 107-126. https://doi.org/10.1177/2211068214561025 PMID: 25586998
34. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010; 7: 335-336. https://doi.org/10.1038/nmeth.f.303 PMID: 20383131
35. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007; 73: 5261-5267. https://doi.org/10.1128/AEM.00062-07 PMID: 17586664
36. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010; 26: 266-267. https://doi.org/10.1093/bioinformatics/btp636 PMID: 19914921
37. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013; 31: 814-821. https://doi.org/10.1038/nbt.2676 PMID: 23975157
38. Kim HB, Isaacson RE. The pig gut microbial diversity: Understanding the pig gut microbial ecology through the next generation high throughput sequencing. Vet Microbiol. 2015; 177: 242-251. https://doi.org/10.1016/j.vetmic.2015.03.014 PMID: 25843944
39. Pastorelli H, van Milgen J, Lovatto P, Montagne L. Meta-analysis of feed intake and growth responses of growing pigs after a sanitary challenge. Animal. 2012; 6: 952-961. https://doi.org/10.1017/S175173111100228X PMID: 22558966
40. Cray C, Zaias J, Altman NH. Acute phase response in animals: a review. Comp Med. 2009; 59: 517-526. PMID: 20034426
41. van Heugten E, Spears JW, Coffey MT. The effect of dietary protein on performance and immune response in weanling pigs subjected to an inflammatory challenge. J Anim Sci. 1994; 72: 2661-2669. PMID: 7883625
42. Wyns H, Plessers E, de Backer P, Meyer E, Croubels S. In vivo porcine lipopolysaccharide inflammation models to study immunomodulation of drugs. Vet Immunol Immunopathol. 2015; 166: 58-69. https://doi.org/10.1016/j.vetimm.2015.06.001 PMID: 26099806
43. Jain S, Gautam V, Naseem S. Acute-phase proteins: As diagnostic tool. J Pharm Bioallied Sci. 2011; 3: 118-127. https://doi.org/10.4103/0975-7406.76489 PMID: 21430962
44. Pomorska-Mol M, Kwit K, Pejsak Z, Markowska-Daniel I. Analysis of the acute-phase protein response in pigs to clinical and subclinical infection with H3N2 swine influenza virus. Influenza Other Respir Viruses. 2014; 8: 228-234. https://doi.org/10.1111/irv.12186 PMID: 24734294
45. Suto G, Kiraly A, Tache Y. Interleukin 1 beta inhibits gastric emptying in rats: mediation through prostaglandin and corticotropin-releasing factor. Gastroenterology. 1994; 106: 1568-1575. PMID: 8194703
46. Plata-Salaman CR, Oomura Y, Kai Y. Tumor necrosis factor and interleukin-1 beta: suppression of food intake by direct action in the central nervous system. Brain Res. 1988; 448: 106-114. PMID: 3260533
47. Plata-Salaman CR. Immunoregulators in the nervous system. Neurosci Biobehav Rev. 1991; 15: 185-215. PMID: 1852312
48. Swiergiel AH, Dunn AJ. The roles of IL-1, IL-6, and TNFalpha in the feeding responses to endotoxin and influenza virus infection in mice. Brain Behav Immun. 1999; 13: 252-265. https://doi.org/10.1006/brbi. 1999.0565 PMID: 10469526
49. Bret-Dibat JL, Bluthe RM, Kent S, Kelley KW, Dantzer R. Lipopolysaccharide and interleukin-1 depress food-motivated behavior in mice by a vagal-mediated mechanism. Brain Behav Immun. 1995; 9: 242-246. PMID: 8590821
50. Jofre-Monseny L, Loboda A, Wagner AE, Huebbe P, Boesch-Saadatmandi C, Jozkowicz A, et al. Effects of apoE genotype on macrophage inflammation and heme oxygenase-1 expression. Biochem Biophys Res Commun. 2007; 357: 319-324. https://doi.org/10.1016/j.bbrc.2007.03.150 PMID: 17416347
51. Caamano J, Hunter CA. NF-kappaB family of transcription factors: central regulators of innate and adaptive immune functions. Clin Microbiol Rev. 2002; 15: 414-429. https://doi.org/10.1128/CMR.15.3. 414-429.2002 PMID: 12097249
52. Hwang J-H, Lim S-B. Antioxidant and Anti-inflammatory Activities of Broccoli Florets in LPS-stimulated RAW 264.7 Cells. Prev Nutr Food Sci. 2014; 19: 89-97. https://doi.org/10.3746/pnf.2014.19.2.089 PMID: 25054107
53. Chen Y, Lin Y, Li Y, Li C. Total flavonoids of Hedyotis diffusa Willd inhibit inflammatory responses in LPS-activated macrophages via suppression of the NF-kappaB and MAPK signaling pathways. Exp Ther Med. 2016; 11: 1116-1122. https://doi.org/10.3892/etm.2015.2963 PMID: 26998046
54. Gessner DK, Ringseis R, Eder K. Potential of plant polyphenols to combat oxidative stress and inflammatory processes in farm animals. J Anim Physiol Anim Nutr (Berl). 2016.
55. Scalbert A, Morand C, Manach C, Rémésy C. Absorption and metabolism of polyphenols in the gut and impact on health. Biomedicine & Pharmacotherapy. 2002; 56: 276-282.
56. Marin L, Miguelez EM, Villar CJ, Lombo F. Bioavailability of dietary polyphenols and gut microbiota metabolism: antimicrobial properties. Biomed Res Int. 2015; 2015: 905215. https://doi.org/10.1155/2015/905215 PMID: 25802870
57. Pastor A, Rodriguez-Morato J, Olesti E, Pujadas M, Perez-Mana C, Khymenets O, et al. Analysis of free hydroxytyrosol in human plasma following the administration of olive oil. J Chromatogr A. 2016; 1437: 183-190. https://doi.org/10.1016/j.chroma.2016.02.016 PMID: 26877176
58. Catalan U, Lopez de Las Hazas Maria-Carmen, Rubio L, Fernandez-Castillejo S, Pedret A, de La Torre R, et al. Protective effect of hydroxytyrosol and its predominant plasmatic human metabolites against endothelial dysfunction in human aortic endothelial cells. Mol Nutr Food Res. 2015; 59: 2523-2536. https://doi.org/10.1002/mnfr.201500361 PMID: 26390376
59. Bjarnason I, MacPherson A, Hollander D. Intestinal permeability: an overview. Gastroenterology. 1995; 108: 1566-1581. PMID: 7729650
60. Menard S, Cerf-Bensussan N, Heyman M. Multiple facets of intestinal permeability and epithelial handling of dietary antigens. Mucosal Immunol. 2010; 3: 247-259. https://doi.org/10.1038/mi.2010.5 PMID: 20404811
61. Blair SA, Kane SV, Clayburgh DR, Turner JR. Epithelial myosin light chain kinase expression and activity are upregulated in inflammatory bowel disease. Lab Invest. 2006; 86: 191-201. https://doi.org/10.1038/labinvest.3700373 PMID: 16402035
62. Laukoetter MG, Nava P, Nusrat A. Role of the intestinal barrier in inflammatory bowel disease. World J Gastroenterol. 2008; 14: 401-407. https://doi.org/10.3748/wjg.14.401 PMID: 18200662
63. Pastorelli L, de Salvo C, Mercado JR, Vecchi M, Pizarro TT. Central role of the gut epithelial barrier in the pathogenesis of chronic intestinal inflammation: lessons learned from animal models and human genetics. Front Immunol. 2013; 4: 280. https://doi.org/10.3389/fimmu.2013.00280 PMID: 24062746
64. Corona G, Deiana M, Incani A, Vauzour D, Dessi MA, Spencer JPE. Inhibition of p38/CREB phosphorylation and COX-2 expression by olive oil polyphenols underlies their anti-proliferative effects. Biochem Biophys Res Commun. 2007; 362: 606-611. https://doi.org/10.1016/j.bbrc.2007.08.049 PMID: 17727817
65. Wells CL, Jechorek RP, Kinneberg KM, Debol SM, Erlandsen SL. The isoflavone genistein inhibits internalization of enteric bacteria by cultured Caco-2 and HT-29 enterocytes. J Nutr. 1999; 129: 634-640. PMID: 10082767
66. Suzuki T, Hara H. Role of flavonoids in intestinal tight junction regulation. J Nutr Biochem. 2011; 22: 401-408. https://doi.org/10.1016/j.jnutbio.2010.08.001 PMID: 21167699
67. Piegholdt S, Pallauf K, Esatbeyoglu T, Speck N, Reiss K, Ruddigkeit L, et al. Biochanin A and prunetin improve epithelial barrier function in intestinal CaCo-2 cells via downregulation of ERK, NF-kappaB, and tyrosine phosphorylation. Free Radic Biol Med. 2014; 70: 255-264. https://doi.org/10.1016/j. freeradbiomed.2014.02.025 PMID: 24631489
68. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol. 2009; 9: 799-809. https://doi.org/10.1038/nri2653 PMID: 19855405
69. Lee SH. Intestinal permeability regulation by tight junction: implication on inflammatory bowel diseases. Intest Res. 2015; 13: 11-18. https://doi.org/10.5217/ir.2015.13.1.11 PMID: 25691839
70. Suzuki T. Regulation of intestinal epithelial permeability by tight junctions. Cell Mol Life Sci. 2013; 70: 631-659. https://doi.org/10.1007/s00018-012-1070-x PMID: 22782113
71. Al-Sadi R, Ye D, Dokladny K, Ma TY. Mechanism of IL-1beta-induced increase in intestinal epithelial tight junction permeability. J Immunol. 2008; 180: 5653-5661. PMID: 18390750
72. Capaldo CT, Nusrat A. Cytokine regulation of tight junctions. Biochim Biophys Acta. 2009; 1788: 864-871. https://doi.org/10.1016/j.bbamem.2008.08.027 PMID: 18952050
73. Wang F, Graham WV, Wang Y, Witkowski ED, Schwarz BT, Turner JR. Interferon-gamma and tumor necrosis factor-alpha synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression. Am J Pathol. 2005; 166: 409-419. PMID: 15681825
74. Ma TY, Boivin MA, Ye D, Pedram A, Said HM. Mechanism of TNF-{alpha} modulation of Caco-2 intestinal epithelial tight junction barrier: role of myosin light-chain kinase protein expression. Am J Physiol Gastrointest Liver Physiol. 2005; 288: G422-30. https://doi.org/10.1152/ajpgi.00412.2004 PMID: 15701621
75. Yap WH, Lim YM. Mechanistic Perspectives of Maslinic Acid in Targeting Inflammation. Biochem Res Int. 2015; 2015: 279356. https://doi.org/10.1155/2015/279356 PMID: 26491566
76. Rodriguez-Rodriguez R. Oleanolic acid and related triterpenoids from olives on vascular function: molecular mechanisms and therapeutic perspectives. Curr Med Chem. 2015; 22: 1414-1425. PMID: 25515513
77. Martin MA, Ramos S, Granado-Serrano AB, Rodriguez-Ramiro I, Trujillo M, Bravo L, et al. Hydroxytyrosol induces antioxidant/detoxificant enzymes and Nrf2 translocation via extracellular regulated kinases and phosphatidylinositol-3-kinase/protein kinase B pathways in HepG2 cells. Mol Nutr Food Res. 2010; 54: 956-966. https://doi.org/10.1002/mnfr.200900159 PMID: 20166143
78. Tremaroli V, Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012; 489: 242-249. https://doi.org/10.1038/nature11552 PMID: 22972297
79. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. Host-gut microbiota metabolic interactions. Science. 2012; 336: 1262-1267. https://doi.org/10.1126/science.1223813 PMID: 22674330
80. Cani PD, Osto M, Geurts L, Everard A. Involvement of gut microbiota in the development of low-grade inflammation and type 2 diabetes associated with obesity. Gut Microbes. 2012; 3: 279-288. https://doi.org/10.4161/gmic.19625 PMID: 22572877
81. Cani PD. Crosstalk between the gut microbiota and the endocannabinoid system: impact on the gut barrier function and the adipose tissue. Clin Microbiol Infect. 2012; 18 Suppl 4: 50-53.
82. Frazier TH, DiBaise JK, McClain CJ. Gut microbiota, intestinal permeability, obesity-induced inflammation, and liver injury. JPEN J Parenter Enteral Nutr. 2011; 35: 14S-20S. https://doi.org/10.1177/0148607111413772 PMID: 21807932
83. Wang M, Donovan SM. Human microbiota-associated swine: current progress and future opportunities. ILAR J. 2015; 56: 63-73. https://doi.org/10.1093/ilar/ilv006 PMID: 25991699
84. Heinritz SN, Mosenthin R, Weiss E. Use of pigs as a potential model for research into dietary modulation of the human gut microbiota. Nutr Res Rev. 2013; 26: 191-209. https://doi.org/10.1017/S0954422413000152 PMID: 24134811