Non digestible oligosaccharides modulate the gut microbiota to control the development of leukemia and associated cachexia in mice

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Bindels, Laure B ^a   Neyrinck, Audrey M ^a   Salazar, Nuria ^a   Taminiau, Bernard ^b   Druart, Céline ^a   Muccioli, Giulio G ^a   François, Emmanuelle ^b   Blecker, Christophe ^b   Richel, Aurore ^b   Daube, Georges ^b   Mahillon, Jacques ^a   De Los Reyes Gavilán, Clara G ^c   Cani, Patrice D ^a   Delzenne, Nathalie M ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; BUTYRIC ACID; INULIN; OLIGOSACCHARIDE; PECTIC OLIGOSACCHARIDE; PROPIONIC ACID; RNA 16S; UNCLASSIFIED DRUG; ACETIC ACID DERIVATIVE;

16S RRNA GENE; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOREXIA; ARTICLE; BACTEROIDES; BACTEROIDES DOREI; BIFIDOBACTERIUM; CACHEXIA; CANCER CELL; CANCER GROWTH; CELL INVASION; CELL SPREADING; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; DIET SUPPLEMENTATION; FAT MASS; FATTY ACID OXIDATION; GENE EXPRESSION; INFLAMMATION; INTESTINE FLORA; LEUKEMIA; MALE; MICROBIAL DIVERSITY; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PYROSEQUENCING; ROSEBURIA; ANIMAL; BAGG ALBINO MOUSE; CECUM; CELL CULTURE; DIETARY SUPPLEMENT; DISEASE COURSE; DRUG EFFECTS; GENETICS; LIVER; METABOLISM; MICROBIOLOGY; MICROFLORA; PATHOLOGY; TUMOR INVASION;

BACTEROIDES SP.; BIFIDOBACTERIUM; MUS; ROSEBURIA;

ACETATES; ANIMALS; BACTEROIDES; BIFIDOBACTERIUM; CACHEXIA; CECUM; CELLS, CULTURED; DIETARY SUPPLEMENTS; DISEASE PROGRESSION; GASTROINTESTINAL MICROBIOME; INULIN; LEUKEMIA; LIVER; MALE; MICE; MICE, INBRED BALB C; MICROBIOTA; NEOPLASM INVASIVENESS; OLIGOSACCHARIDES; RNA, RIBOSOMAL, 16S;

EID: 84938942266     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0131009     Document Type: Article

References (42)

1. Claesson MJ, Jeffery IB, Conde S, Power SE, O'Connor EM, Cusack S, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012; 488(7410):178-84. doi: 10.1038/nature11319 PMID: 22797518
2. Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Backhed HK, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012; 150(3):470-80. doi: 10.1016/j.cell. 2012.07.008 PMID: 22863002
3. Bindels LB, Delzenne NM, Cani PD, Walter J. Towards a more comprehensive concept for prebiotics. Nat Rev Gastroenterol Hepatol. 2015.
4. Roberfroid M, Gibson GR, Hoyles L, McCartney AL, Rastall R, Rowland I, et al. Prebiotic effects: metabolic and health benefits. Br J Nutr. 2010; 104 Suppl 2:S1-63. doi: 10.1017/S0007114510003363 PMID: 20920376
5. Neyrinck AM, Possemiers S, Druart C, Van de Wiele T, De Backer F, Cani PD, et al. Prebiotic effects of wheat arabinoxylan related to the increase in bifidobacteria, Roseburia and Bacteroides/Prevotella in diet-induced obese mice. PLoS One. 2011; 6(6):e20944. doi: 10.1371/journal.pone.0020944 PMID: 21695273
6. Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GG, Neyrinck AM, et al. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes. 2011; 60(11):2775-86. doi: 10.2337/db11-0227 PMID: 21933985
7. Druart C, Alligier M, Salazar N, Neyrinck AM, Delzenne NM. Modulation of the gut microbiota by nutrients with prebiotic and probiotic properties. Adv Nutr. 2014; 5(5):624S-33S. doi: 10.3945/an.114. 005835 PMID: 25225347
8. Wanders AJ, Feskens EJ, Jonathan MC, Schols HA, de Graaf C, Mars M. Pectin is not pectin: a randomized trial on the effect of different physicochemical properties of dietary fiber on appetite and energy intake. Physiol Behav. 2014; 128:212-9. doi: 10.1016/j.physbeh.2014.02.007 PMID: 24534170
9. Sanaka M, Yamamoto T, Anjiki H, Nagasawa K, Kuyama Y. Effects of agar and pectin on gastric emptying and post-prandial glycaemic profiles in healthy human volunteers. Clin Exp Pharmacol Physiol. 2007; 34(11):1151-5. PMID: 17880369
10. Olano-Martin E, Gibson GR, Rastell RA. Comparison of the in vitro bifidogenic properties of pectins and pectic-oligosaccharides. J Appl Microbiol. 2002; 93(3):505-11. PMID: 12174051
11. Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med. 2014; 20(2):159-66. doi: 10.1038/nm.3444 PMID: 24390308
12. Onumpai C, Kolida S, Bonnin E, Rastall RA. Microbial utilization and selectivity of pectin fractions with various structures. Appl Environ Microbiol. 2011; 77(16):5747-54. doi: 10.1128/AEM.00179-11 PMID: 21724897
13. Bindels LB, Beck R, Schakman O, Martin JC, De Backer F, Sohet FM, et al. Restoring specific lactobacilli levels decreases inflammation and muscle atrophy markers in an acute leukemia mouse model. PLoS One. 2012; 7(6):e37971. doi: 10.1371/journal.pone.0037971 PMID: 22761662
14. Dewys WD, Begg C, Lavin PT, Band PR, Bennett JM, Bertino JR, et al. Prognostic effect of weight loss prior to chemotherapy in cancer patients. Eastern Cooperative Oncology Group. Am J Med. 1980; 69 (4):491-7. PMID: 7424938
15. Sessions J. Chronic myeloid leukemia in 2007. J Manag Care Pharm. 2007; 13(8 Suppl A):4-7. PMID: 17970608
16. Moschovi M, Trimis G, Vounatsou M, Katsibardi K, Margeli A, Dimitriadi F, et al. Serial plasma concentrations of PYY and ghrelin during chemotherapy in children with acute lymphoblastic leukemia. J Pediatr Hematol Oncol. 2008; 30(10):733-7. doi: 10.1097/MPH.0b013e318179a1d8 PMID: 19011469
17. Fearon K, Arends J, Baracos V. Understanding the mechanisms and treatment options in cancer cachexia. Nat Rev Clin Oncol. 2013; 10(2):90-9. doi: 10.1038/nrclinonc.2012.209 PMID: 23207794
18. Baracos VE, Pichard C, Attaix D. Survival: the relevant primary outcome for nutrition therapy in cancer patients. Curr Opin Clin Nutr Metab Care. 2012; 15(3):211-2. doi: 10.1097/MCO.0b013e328352dc41 PMID: 22466928
19. Argiles JM, Busquets S, Stemmler B, Lopez-Soriano FJ. Cancer cachexia: understanding the molecular basis. Nat Rev Cancer. 2014; 14(11):754-62. doi: 10.1038/nrc3829 PMID: 25291291
20. Bindels LB, Porporato P, Dewulf EM, Verrax J, Neyrinck AM, Martin JC, et al. Gut microbiota-derived propionate reduces cancer cell proliferation in the liver. Br J Cancer. 2012; 107(8):1337-44. doi: 10. 1038/bjc.2012.409 PMID: 22976799
21. Fiskus W, Pranpat M, Balasis M, Bali P, Estrella V, Kumaraswamy S, et al. Cotreatment with vorinostat (suberoylanilide hydroxamic acid) enhances activity of dasatinib (BMS-354825) against imatinib mesylate-sensitive or imatinib mesylate-resistant chronic myelogenous leukemia cells. Clin Cancer Res. 2006; 12(19):5869-78. PMID: 17020995
22. Fiskus W, Pranpat M, Bali P, Balasis M, Kumaraswamy S, Boyapalle S, et al. Combined effects of novel tyrosine kinase inhibitor AMN107 and histone deacetylase inhibitor LBH589 against Bcr-Ablexpressing human leukemia cells. Blood. 2006; 108(2):645-52. PMID: 16537804
23. Salazar N, Binetti A, Gueimonde M, Alonso A, Garrido P, Gonzalez del Rey C, et al. Safety and intestinal microbiota modulation by the exopolysaccharide-producing strains Bifidobacterium animalis IPLA R1 and Bifidobacterium longum IPLA E44 orally administered to Wistar rats. Int J Food Microbiol. 2011; 144(3):342-51. doi: 10.1016/j.ijfoodmicro.2010.10.016 PMID: 21078530
24. Neyrinck AM, Possemiers S, Verstraete W, De Backer F, Cani PD, Delzenne NM. Dietary modulation of clostridial cluster XIVa gut bacteria (Roseburia spp.) by chitin-glucan fiber improves host metabolic alterations induced by high-fat diet in mice. J Nutr Biochem. 2012; 23(1):51-9. doi: 10.1016/j.jnutbio. 2010.10.008 PMID: 21411304
25. Druart C, Neyrinck AM, Vlaeminck B, Fievez V, Cani PD, Delzenne NM. Role of the lower and upper intestine in the production and absorption of gut microbiota-derived PUFA metabolites. PLoS One. 2014; 9(1):e87560. doi: 10.1371/journal.pone.0087560 PMID: 24475308
26. Smith MI, Yatsunenko T, Manary MJ, Trehan I, Mkakosya R, Cheng J, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science. 2013; 339(6119):548-54. doi: 10.1126/science. 1229000 PMID: 23363771
27. Monira S, Nakamura S, Gotoh K, Izutsu K, Watanabe H, Alam NH, et al. Gut microbiota of healthy and malnourished children in bangladesh. Front Microbiol. 2011; 2:228. doi: 10.3389/fmicb.2011.00228 PMID: 22125551
28. Sheridan PO, Bindels LB, Saulnier DM, Reid G, Nova E, Holmgren K, et al. Can prebiotics and probiotics improve therapeutic outcomes for undernourished individuals? Gut Microbes. 2014; 5(1):74-82. doi: 10.4161/gmic.27252 PMID: 24637591
29. Leijdekkers AG, Aguirre M, Venema K, Bosch G, Gruppen H, Schols HA. In vitro fermentability of sugar beet pulp derived oligosaccharides using human and pig fecal inocula. J Agric Food Chem. 2014; 62(5):1079-87. doi: 10.1021/jf4049676 PMID: 24437353
30. Bakir MA, Sakamoto M, Kitahara M, Matsumoto M, Benno Y. Bacteroides dorei sp. nov., isolated from human faeces. Int J Syst Evol Microbiol. 2006; 56(Pt 7):1639-43. PMID: 16825642
31. Ryan KK, Tremaroli V, Clemmensen C, Kovatcheva-Datchary P, Myronovych A, Karns R, et al. FXR is a molecular target for the effects of vertical sleeve gastrectomy. Nature. 2014; 509(7499):183-8. doi: 10.1038/nature13135 PMID: 24670636
32. Dewulf EM, Cani PD, Claus SP, Fuentes S, Puylaert PG, Neyrinck AM, et al. Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut. 2013; 62(8):1112-21. doi: 10.1136/gutjnl-2012-303304 PMID: 23135760
33. Everard A, Lazarevic V, Gaia N, Johansson M, Stahlman M, Backhed F, et al. Microbiome of prebiotictreated mice reveals novel targets involved in host response during obesity. ISME J. 2014.
34. Louis P, Scott KP, Duncan SH, Flint HJ. Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol. 2007; 102(5):1197-208. PMID: 17448155
35. Ge H, Li X, Weiszmann J, Wang P, Baribault H, Chen JL, et al. Activation of G protein-coupled receptor 43 in adipocytes leads to inhibition of lipolysis and suppression of plasma free fatty acids. Endocrinology. 2008; 149(9):4519-26. doi: 10.1210/en.2008-0059 PMID: 18499755
36. Das SK, Eder S, Schauer S, Diwoky C, Temmel H, Guertl B, et al. Adipose triglyceride lipase contributes to cancer-associated cachexia. Science. 2011; 333(6039):233-8. doi: 10.1126/science.1198973 PMID: 21680814
37. Das SK, Hoefler G. The role of triglyceride lipases in cancer associated cachexia. Trends Mol Med. 2013; 19(5):292-301. doi: 10.1016/j.molmed.2013.02.006 PMID: 23499576
38. Cabassi A, Tedeschi S. Zinc-alpha2-glycoprotein as a marker of fat catabolism in humans. Curr Opin Clin Nutr Metab Care. 2013; 16(3):267-71. doi: 10.1097/MCO.0b013e32835f816c PMID: 23448999
39. Agustsson T, Ryden M, Hoffstedt J, van Harmelen V, Dicker A, Laurencikiene J, et al. Mechanism of increased lipolysis in cancer cachexia. Cancer Res. 2007; 67(11):5531-7. PMID: 17545636
40. Druart C, Neyrinck AM, Dewulf EM, De Backer FC, Possemiers S, Van de Wiele T, et al. Implication of fermentable carbohydrates targeting the gut microbiota on conjugated linoleic acid production in highfat-fed mice. Br J Nutr. 2013:1-14. doi: 10.1017/S000711451300278X PMID: 23953879
41. Inoue Y, Izawa K, Tojo A, Nomura Y, Sekine R, Oyaizu N, et al. Monitoring of disease progression by bioluminescence imaging and magnetic resonance imaging in an animal model of hematologic malignancy. Exp Hematol. 2007; 35(3):407-15. PMID: 17309821
42. Peters DG, Hoover RR, Gerlach MJ, Koh EY, Zhang H, Choe K, et al. Activity of the farnesyl protein transferase inhibitor SCH66336 against BCR/ABL-induced murine leukemia and primary cells from patients with chronic myeloid leukemia. Blood. 2001; 97(5):1404-12. PMID: 11222387