Fructose malabsorption induces cholecystokinin expression in the ileum and cecum by changing microbiota composition and metabolism

FASEB Journal

Volumn 33, Issue 6, 2019, Pages 7126-7142

  Zhang, Xufei ^a,b   Grosfeld, Alexandra ^b   Williams, Edek ^c   Vasiliauskas, Daniel ^d   Barretto, Sharon ^e   Smith, Lorraine ^e   Mariadassou, Mahendra ^f   Philippe, Catherine ^a   Devime, Fabienne ^a   Melchior, Chloé ^g   Gourcerol, Guillaume ^g   Dourmap, Nathalie ^h   Lapaque, Nicolas ^a   Larraufie, Pierre ^a   Blottière, Hervé M ^a   Herberden, Christine ^a   Gerard, Philippe ^a   Rehfeld, Jens F ⁱ   Ferraris, Ronaldo P ^c   Fritton, J Christopher ^c   Ellero Simatos, Sandrine ^e   Douard, Veronique ^a   more..

^a UNIVERSITÉ PARIS SACLAY   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c RUTGERS UNIVERSITY   (United States)

^d CNRS   (France)

^e TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

^f INRA Institut National de la Recherche Agronomique   (France)

^g UNIVERSITÉ DE ROUEN   (France)

^h ROUEN UNIVERSITY HOSPITAL   (France)

ⁱ UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

CCK; KHK; propionate

Indexed keywords

BETA ACTIN; CHOLECYSTOKININ; FRUCTOSE; GASTRIC INHIBITORY POLYPEPTIDE; GLUCAGON LIKE PEPTIDE 1; KETOHEXOKINASE; LACTIC ACID; LEPTIN; MESSENGER RNA; NERVE CELL DIFFERENTIATION 1; NEUROGENIN 3; NEUROTENSIN; PEPTIDE YY; PREPROGLUCAGON; PROPIONIC ACID; RNA 16S; SECRETIN; SOMATOSTATIN; SUCCINIC ACID; TRANSCRIPTION FACTOR PAX4; TRANSCRIPTION FACTOR PAX6; TRYPTOPHAN HYDROXYLASE; TRYPTOPHAN HYDROXYLASE 1; TWIST RELATED PROTEIN 1; UNCLASSIFIED DRUG; FRUCTOKINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; CARBOHYDRATE INTOLERANCE; CECUM; CONTROLLED STUDY; ENTEROENDOCRINE CELL; FRUCTOSE METABOLISM; GLUCOSE INTAKE; GLUTAG CELL LINE; ILEUM; IMMUNOHISTOCHEMISTRY; INTESTINE FLORA; MOUSE; MRNA EXPRESSION LEVEL; NCI-H716 CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; SPECIES COMPOSITION; UPREGULATION; ANIMAL; CELL LINE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; CECUM; CELL LINE; CHOLECYSTOKININ; FRUCTOKINASES; FRUCTOSE; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION REGULATION; HUMANS; ILEUM; MICE; MICE, KNOCKOUT;

EID: 85067269703     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.201801526RR     Document Type: Article

References (69)

1. Marriott, B. P., Cole, N., and Lee, E. (2009) National estimates of dietary fructose intake increased from 1977 to 2004 in the United States. J. Nutr. 139, 1228S–1235S
2. Tappy, L., and Lê, K. A. (2010) Metabolic effects of fructose and the worldwide increase in obesity. Physiol. Rev. 90, 23–46
3. Jones, H. F., Butler, R. N., and Brooks, D. A. (2011) Intestinal fructose transport and malabsorption in humans. Am. J. Physiol. Gastrointest. Liver Physiol. 300, G202–G206
4. Douard, V., and Ferraris, R. P. (2013) The role of fructose transporters in diseases linked to excessive fructose intake. J. Physiol. 591, 401–414
5. Jones, H. F., Burt, E., Dowling, K., Davidson, G., Brooks, D. A., and Butler, R. N. (2011) Effect of age on fructose malabsorption in children presenting with gastrointestinal symptoms. J. Pediatr. Gastroenterol. Nutr. 52, 581–584
6. Putkonen, L., Yao, C. K., and Gibson, P. R. (2013) Fructose malabsorption syndrome. Curr. Opin. Clin. Nutr. Metab. Care 16, 473–477
7. Manolescu, A. R., Witkowska, K., Kinnaird, A., Cessford, T., and Cheeseman, C. (2007) Facilitated hexose transporters: new perspectives on form and function. Physiology (Bethesda) 22, 234–240
8. Davidson, N. O., Hausman, A. M., Ifkovits, C. A., Buse, J. B., Gould, G. W., Burant, C. F., and Bell, G. I. (1992) Human intestinal glucose transporter expression and localization of GLUT5. Am. J. Physiol. 262, C795–C800
9. Patel, C., Douard, V., Yu, S., Tharabenjasin, P., Gao, N., and Ferraris, R. P. (2015) Fructose-induced increases in expression of intestinal fructolytic and gluconeogenic genes are regulated by GLUT5 and KHK. Am. J. Physiol. Regul. Integr. Comp. Physiol. 309, R499–R509
10. Patel, C., Sugimoto, K., Douard, V., Shah, A., Inui, H., Yamanouchi, T., and Ferraris, R. P. (2015) Effect of dietary fructose on portal and systemic serum fructose levels in rats and in KHK-/- and GLUT5-/- mice. Am. J. Physiol. Gastrointest. Liver Physiol. 309, G779–G790
11. Douard, V., and Ferraris, R. P. (2008) Regulation of the fructose transporter GLUT5 in health and disease. Am. J. Physiol. Endocrinol. Metab. 295, E227–E237
12. Jang, C., Hui, S., Lu, W., Cowan, A J., Morscher, R. J., Lee, G., Liu, W., Tesz, G. J., Birnbaum, M. J., and Rabinowitz, J. D. (2018) The small intestine converts dietary fructose into glucose and organic acids. Cell Metab. 27, 351–361.e3
13. Nergård, B. J., Lindqvist, A., Gislason, H. G., Groop, L., Ekelund, M., Wierup, N., and Hedenbro, J. L. (2015) Mucosal glucagon-like peptide-1 and glucose-dependent insulinotropic polypeptide cell numbers in the super-obese human foregut after gastric bypass. Surg. Obes. Relat. Dis. 11, 1237–1246
14. Cavin, J. B., Couvelard, A., Lebtahi, R., Ducroc, R., Arapis, K., Voitellier, E., Cluzeaud, F., Gillard, L., Hourseau, M., Mikail, N., Ribeiro-Parenti, L., Kapel, N., Marmuse, J. P., Bado, A., and Le Gall, M. (2016) Differences in alimentary glucose absorption and intestinal disposal of blood glucose after Roux-en-Y gastric bypass vs sleeve gastrectomy. Gastroenterology 150, 454–464.e9
15. Rhee, N. A., Wahlgren, C. D., Pedersen, J., Mortensen, B., Langholz, E., Wandall, E. P., Friis, S. U., Vilmann, P., Paulsen, S. J., Kristiansen, V. B., Jelsing, J., Dalbøge, L. S., Poulsen, S. S., Hoist, J. J., Vilsbøll, T., and Knop, F. K. (2015) Effect of Roux-en-Y gastric bypass on the distribution and hormone expression of small-intestinal enteroendocrine cells in obese patients with type 2 diabetes. Diabetobgia 58, 2254–2258
16. Mumphrey, M. B., Patterson, L. M., Zheng, H., and Berthoud, H. R. (2013) Roux-en-Y gastric bypass surgery increases number but not density of CCK-, GLP-1-, 5-HT-, and neurotensin-expressing enteroendocrine cells in rats. Neurogastroenterol. Motil. 25, e70–e79
17. Gillard, L., Billiauws, L., Stan-Iuga, B., Ribeiro-Parenti, L., Jarry, A. C., Cavin, J. B., Cluzeaud, F., Mayeur, C., Thomas, M., Freund, J. N., Lacorte, J. M., Le Gall, M., Bado, A, Joly, F., and Le Beyec, J. (2016) Enhanced ghrelin levels and hypothalamic orexigenic AgRP and NPY neuropeptide expression in models of Jejuno-colonic short bowel syndrome. Sci. Rep. 6, 28345
18. Gillard, L., Mayeur, C., Robert, V., Pingenot, I., Le Beyec, J., Bado, A., Lepage, P., Thomas, M., and Joly, F. (2017) Microbiota is involved in post-resection adaptation in humans with short bowel syndrome. Front. Physiol. 8, 224
19. Plovier, H., and Cani, P. D. (2017) Enteroendocrine cells: metabolic relays between microbes and their host. Endocr. Dev. 32, 139–164
20. Wichmann, A., Allahyar, A., Greiner, T. U., Plovier, H., Lundén, G. O., Larsson, T., Drucker, D. J., Delzenne, N. M., Cani, P. D., and Bäckhed, F. (2013) Microbial modulation of energy availability in the colon regulates intestinal transit. Cell Host Microbe 14, 582–590
21. Arora, T., Akrami, R., Pais, R., Bergqvist, L., Johansson, B. R., Schwartz, T. W., Reimann, F., Gribble, F. M., and Bäckhed, F. (2018) Microbial regulation of the L cell transcriptome. Sci. Rep. 8, 1207
22. Gribble, F. M., and Reimann, F. (2016) Enteroendocrine cells: chemosensors in the intestinal epithelium. Annu. Rev. Physiol. 78, 277–299
23. Patel, C., Douard, V., Yu, S., Gao, N., and Ferraris, R. P. (2015) Transport, metabolism, and endosomal trafficking-dependent regulation of intestinal fructose absorption. FASEB J. 29, 4046–4058
24. Ishimoto, T., Lanaspa, M. A., Le, M. T., Garcia, G. E., Diggle, C. P., Maclean, P. S., Jackman, M. R., Asipu, A., Roncal-Jimenez, C. A., Kosugi, T., Rivard, C. J., Maruyama, S., Rodriguez-Iturbe, B., Sánchez-Lozada, L. G., Bonthron, D. T., Sautin, Y. Y., and Johnson, R. J. (2012) Opposing effects of fructokinase C and A isoforms on fructose-induced metabolic syndrome in mice. Proc. Natl. Acad. Sci. USA 109, 4320–4325
25. Diggle, C. P., Shires, M., McRae, C., Crellin, D., Fisher, J., Carr, I. M., Markham, A. F., Hayward, B. E., Asipu, A., and Bonthron, D. T. (2010) Both isoforms of ketohexokinase are dispensable for normal growth and development. Physiol. Genomics 42A, 235–243
26. Rehfeld J. F. (1998) How to measure cholecystokinin in tissue, plasma and cerebrospinal fluid. Regul. Pept. 78, 31–39
27. Lan, A., Bruneau, A., Bensaada, M., Philippe, C., Bellaud, P., Rabot, S., and Jan, G. (2008) Increased induction of apoptosis by Propionibacterium freudenreichii TL133 in colonic mucosal crypts of human microbiota-associated rats treated with 1,2-dimethylhydrazine. Br. J. Nutr. 100, 1251–1259
28. Lukowicz, C., Ellero-Simatos, S., Régnier, M., Polizzi, A., Lasserre, F., Montagner, A., Lippi, Y., Jamin, E. L., Martin, J. F., Naylies, C., Canlet, C., Debrauwer, L., Bertrand-Michel, J., Al Saati, T., Théodorou, V., Loiseau, N., Mselli-Lakhal, L., Guillou, H., and Gamet-Payrastre, L. (2018) Metabolic effects of a chronic dietary exposure to a low-dose pesticide cocktail in mice: sexual dimorphism and role of the constitutive androstane receptor. Environ. Health Perspect. 126, 067007
29. Furet, J. P., Firmesse, O., Gourmelon, M., Bridonneau, C., Tap, J., Mondot, S., Doré, J., and Corthier, G. (2009) Comparative assessment of human and farm animal faecal microbiota using real-time quantitative PCR. FEMS Microbiol. Ecol. 68, 351–362
30. Bacchetti De Gregoris, T., Aldred, N., Clare, A. S., and Burgess, J. G. (2011) Improvement of phylum- and class-specific primers for realtime PCR quantification of bacterial taxa. J. Microbiol. Methods 86, 351–356
31. Nakanishi, Y., Murashima, K., Ohara, H., Suzuki, T., Hayashi, H., Sakamoto, M., Fukasawa, T., Kubota, H., Hosono, A., Kono, T., Kaminogawa, S., and Benno, Y. (2006) Increase in terminal restriction fragments of Bacteroidetes-derived 16S rRNA genes after administration of short-chain fructooligosaccharides. Appt. Environ. Microbial. 72, 6271–6276
32. Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K., and Schloss, P. D. (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol. 79, 5112–5120
33. Escudié, F., Auer, L., Bernard, M., Mariadassou, M., Cauquil, L., Vidal, K., Maman, S., Hernandez-Raquet, G., Combes, S., and Pascal, G. (2018) FROGS: find, rapidly, OTUs with galaxy solution. Bioinformatics 34, 1287–1294
34. Bokulich, N. A., Subramanian, S., Faith, J. J., Gevers, D., Gordon, J. I., Knight, R., Mills, D. A., and Caporaso, J. G. (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10, 57–59
35. Wickham, H. (2009) ggpbt2: Elegant Graphics for Data Analysis, Springer-Verlag, New York, NY, USA
36. Love, M. I., Huber, W., and Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550
37. Habib, A. M., Richards, P., Cairns, L. S., Rogers, G. J., Bannon, C. A., Parker, H. E., Morley, T. C., Yeo, G. S., Reimann, F., and Gribble, F. M. (2012) Overlap of endocrine hormone expression in the mouse intestine revealed by transcriptional profiling and flow cytometry. Endocrinology 153, 3054–3065
38. Fakhry, J., Wang, J., Martins, P., Fothergill, L. J., Hunne, B., Prieur, P., Shulkes, A., Rehfeld, J. F., Callaghan, B., and Furness, J. B. (2017) Distribution and characterisation of CCK containing enteroendocrine cells of the mouse small and large intestine. Cell Tissue Res. 369, 245–253
39. Aiken, K. D., Kisslinger, J. A., and Roth, K. A. (1994) Immunohistochemical studies indicate multiple enteroendocrine cell differentiation pathways in the mouse proximal small intestine. Dev. Dyn. 201, 63–70
40. Egerod, K. L., Engelstoft, M. S., Grunddal, K. V., Nøhr, M. K., Secher, A., Sakata, I., Pedersen, J., Windeløv, J. A., Füchtbauer, E. M., Olsen, J., Sundler, F., Christensen, J. P., Wierup, N., Olsen, J. V., Hoist, J. J., Zigman, J. M., Poulsen, S. S., and Schwartz, T. W. (2012) A major lineage of enteroendocrine cells coexpress CCK., secretin, GIP, GLP-1, PYY, and neurotensin but not somatostatin. Endocrinology 153, 5782–5795
41. Grunddal, K. V., Ratner, C. F., Svendsen, B., Sommer, F., Engelstoft, M. S., Madsen, A. N., Pedersen, J., Nøhr, M. K., Egerod, K. L., Nawrocki, A. R., Kowalski, T., Howard, A. D., Poulsen, S. S., Offermanns, S., Bäckhed, F., Holst, J. J., Holst, B., and Schwartz, T. W. (2016) Neurotensin is coexpressed, coreleased, and acts together with GLP-1 and PYY in enteroendocrine control of metabolism. Endocrinology 157, 176–194
42. Lopez, M. J., Upchurch, B. H., Rindi, G., and Leiter, A. B. (1995) Studies in transgenic mice reveal potential relationships between secretin-producing cells and other endocrine cell types. J. Biol. Chem. 270, 885–891
43. Richards, P., Pais, R., Habib, A. M., Brighton, C. A., Yeo, G. S., Reimann, F., and Gribble, F. M. (2016) High fat diet impairs the function of glucagon-like peptide-1 producing L-cells. Peptides 77, 21–27
44. Naya, F. J., Stellrecht, C. M., and Tsai, M. J. (1995) Tissue-specific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor. Genes Dev. 9, 1009–1019
45. Hill, M. E., Asa, S. L., and Drucker, D. J. (1999) Essential requirement for Pax6 in control of enteroendocrine proglucagon gene transcription. Mol. Endocrinol. 13, 1474–1486
46. Schonhoff, S. E., Giel-Moloney, M., and Leiter, A. B. (2004) Minireview: development and differentiation of gut endocrine cells. Endocrinology 145, 2639–2644
47. Jenny, M., Uhl, C., Roche, C., Duluc, I., Guillermin, V., Guillemot, F., Jensen, J., Kedinger, M., and Gradwohl, G. (2002) Neurogenin3 is differentially required for endocrine cell fate specification in the intestinal and gastric epithelium. EMBO J. 21, 6338–6347
48. Cani, P. D., Hoste, S., Guiot, Y., and Delzenne, N. M. (2007) Dietary non-digestible carbohydrates promote L-cell differentiation in the proximal colon of rats. Br. J. Nutr. 98, 32–37
49. Delmée, E., Cani, P. D., Gual, G., Knauf, C., Burcelin, R., Maton, N., and Delzenne, N. M. (2006) Relation between colonic proglucagon expression and metabolic response to oligofructose in high fat diet-fed mice. Life Sci. 79, 1007–1013
50. Psichas, A., Sleeth, M. L., Murphy, K. G., Brooks, L., Bewick, G. A., Hanyaloglu, A. C., Ghatei, M. A., Bloom, S. R., and Frost, G. (2015) The short chain fatty acid propionate stimulates GLP-1 and PYY secretion via free fatty acid receptor 2 in rodents. Int. J. Obes. 39, 424–429
51. Tolhurst, G., Heffron, H., Lam, Y. S., Parker, H. E., Habib, A. M., Diakogiannaki, E., Cameron, J., Grosse, J., Reimann, F., and Gribble, F. M. (2012) Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes 61, 364–371
52. Brown, A. J., Goldsworthy, S. M., Barnes, A. A., Eilert, M. M., Tcheang, L., Daniels, D., Muir, A. I., Wigglesworth, M. J., Kinghorn, I., Fraser, N. J., Pike, N. B., Strum, J. C., Steplewski, K. M., Murdock, P. R., Holder, J. C., Marshall, F. H., Szekeres, P. G., Wilson, S., Ignar, D. M., Foord, S. M., Wise, A., and Dowell, S. J. (2003) The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J. Biol. Chem. 278, 11312–11319
53. Nøhr, M. K., Pedersen, M. H., Gille, A., Egerod, K. L., Engelstoft, M. S, Husted, A. S., Sichlau, R. M., Grunddal, K. V., Poulsen, S. S., Han, S., Jones, R. M., Offermanns, S., and Schwartz, T. W. (2013) GPR41/FFAR3 and GPR43/FFAR2 as cosensors for short-chain fatty acids in enteroendocrine cells vs FFAR3 in enteric neurons and FFAR2 in enteric leukocytes. Endocrinology 154, 3552–3564
54. Sealy, L., and Chalkley, R. (1978) The effect of sodium butyrate on histone modification. Cell 14, 115–121
55. Larraufie, P., Martin-Gallausiaux, C., Lapaque, N., Dore, J., Gribble, F. M., Reimann, F., and Blottiere, H. M. (2018) SCFAs strongly stimulate PYY production in human enteroendocrine cells. Sci. Rep. 8, 74
56. Akiba, Y., Inoue, T., Kaji, I., Higashiyama, M., Narimatsu, K., Iwamoto, K., Watanabe, M., Guth, P. H., Engel, E., Kuwahara, A., and Kaunitz, J. D. (2015) Short-chain fatty acid sensing in rat duodenum. J. Physiol. 593, 585–599
57. Daly, K., Al-Rammahi, M., Moran, A., Marcello, M., Ninomiya, Y., and Shirazi-Beechey, S. P. (2013) Sensing of amino acids by the gut-expressed taste receptor T1R1-T1R3 stimulates CCK secretion. Am. J. Physiol. Gastrointest. Liver Physiol. 304, G271–G282
58. Sun, S., Li, H., Chen, J., and Qian, Q. (2017) Lactic acid: no longer an inert and end-product of glycolysis. Physiology (Bethesda) 32, 453–463
59. Gill, R. K., Saksena, S., Alrefai, W. A., Sarwar, Z., Goldstein, J. L., Carroll, R. E., Ramaswamy, K., and Dudeja, P. K. (2005) Expression and membrane localization of MCT isoforms along the length of the human intestine. Am. J. Physiol. Cell Physiol. 289, C846–C852
60. Ranganathan, P., Shanmugam, A., Swafford, D., Suryawanshi, A., Bhattacharjee, P., Hussein, M. S., Koni, P. A., Prasad, P. D., Kurago, Z. B., Thangaraju, M., Ganapathy, V., and Manicassamy, S. (2018) GPR81, a cell-surface receptor for lactate, regulates intestinal homeostasis and protects mice from experimental colitis. J. Immunol. 200, 1781–1789
61. Diehl, J., Gries, B., Pfeil, U., Goldenberg, A., Mermer, P., Rummer, W., and Paddenberg, R. (2016) Expression and localization of GPR91 and GPR99 in murine organs. Cell Tissue Res. 364, 245–262
62. Gänzle, M. G., and Follador, R. (2012) Metabolism of oligosaccharides and starch in lactobacilli: a review. Front. Microbiol. 3, 340
63. Pouteau, E., Nguyen, P., Ballèvre, O., and Krempf, M. (2003) Production rates and metabolism of short-chain fatty acids in the colon and whole body using stable isotopes. Proc. Nutr. Soc. 62, 87–93
64. Reichardt, N., Duncan, S. H., Young, P., Belenguer, A., McWilliam Leitch, C., Scott, K. P., Flint, H. J., and Louis, P. (2014) Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME J. 8, 1323–1335; erratum: 1352
65. Harvey, R. F., and Read, A. E. (1973) Effect of cholecystokinin on colonic motility and symptoms in patients with the irritable-bowel syndrome. Lancet 1, 1–3
66. Chua, A. S., and Keeling, P. W. (2006) Cholecystokinin hyperresponsiveness in functional dyspepsia. World J. Gastroenterol. 12, 2688–2693
67. Cao, B., Zhang, X., Yan, N., Chen, S., and Li, Y. (2012) Cholecystokinin enhances visceral pain-related affective memory via vagal afferent pathway in rats. Mol. Brain 5, 19
68. Ledochowski, M., Murr, C., Lass-Flörl, C., and Fuchs, D. (2001) Increased serum amylase and lipase in fructose malabsorbers. Clin. Chim. Acta 311, 119–123
69. Barrett, T. D., Yan, W., Freedman, J. M., Lagaud, G. J., Breitenbucher, J. G., and Shankley, N. P. (2008) Role of CCK and potential utility of CCK1 receptor antagonism in the treatment of pancreatitis induced by biliary tract obstruction. Br. J. Pharmacol. 153, 1650–1658