Intestinal invalidation of the glucose transporter GLUT2 delays tissue distribution of glucose and reveals an unexpected role in gut homeostasis

Molecular Metabolism

Volumn 6, Issue 1, 2017, Pages 61-72

  Schmitt, Charlotte C ^a   Aranias, Thomas ^a   Viel, Thomas ^b   Chateau, Danielle ^a   Le Gall, Maude ^a,g   Waligora Dupriet, Anne Judith ^c   Melchior, Chloé ^d   Rouxel, Ophélie ^e   Kapel, Nathalie ^f   Gourcerol, Guillaume ^d   Tavitian, Bertrand ^b   Lehuen, Agnès ^e   Brot Laroche, Edith ^a   Leturque, Armelle ^a   Serradas, Patricia ^a   Grosfeld, Alexandra ^a  

^a SORBONNE UNIVERSITÉ   (France)

^b PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d ROUEN UNIVERSITY HOSPITAL   (France)

^e INSTITUT COCHIN   (France)

^f PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^g CENTRE DE RECHERCHE SUR L INFLAMMATION   (France)

Author keywords

GLP 1; Glucose homeostasis; Intestinal adaptation; Malabsorption; Microbiota

Indexed keywords

GLUCAGON LIKE PEPTIDE 1; GLUCOSE; GLUCOSE TRANSPORTER 2; HORMONE; KETONE BODY; GLUCOSE TRANSPORTER; SLC2A2 PROTEIN, MOUSE; SODIUM GLUCOSE COTRANSPORTER 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEROIDES; CALORIC RESTRICTION; CARBOHYDRATE INTAKE; CELL DENSITY; CLOSTRIDIUM; CONTROLLED STUDY; ENTEROCOCCUS; ENTEROENDOCRINE CELL; FECES MICROFLORA; FOOD INTAKE; GENE DELETION; GLUCOSE ABSORPTION; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; INFLAMMATION; INTESTINE BRUSH BORDER; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; INTESTINE TISSUE; INTESTINE TRANSIT TIME; KETOGENESIS; L CELL LINE; LACTOBACILLUS; LEUCONOSTOC; MALABSORPTION; METABOLIC REGULATION; MOUSE; NONHUMAN; PREVOTELLA; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAPHYLOCOCCUS; TISSUE DISTRIBUTION; TISSUE SPECIFICITY; WEIGHT GAIN; ANIMAL; GENETICS; GLUCOSE BLOOD LEVEL; HOMEOSTASIS; INTESTINE; INTESTINE ABSORPTION; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALS; BLOOD GLUCOSE; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; GLUCOSE TRANSPORTER TYPE 2; HOMEOSTASIS; INTESTINAL ABSORPTION; INTESTINES; MICE; MICE, KNOCKOUT; SODIUM-GLUCOSE TRANSPORTER 1; TISSUE DISTRIBUTION;

EID: 85006802518     PISSN: None     EISSN: 22128778     Source Type: Journal    
DOI: 10.1016/j.molmet.2016.10.008     Document Type: Article

References (27)

1. [1] Thorens, B., GLUT2, glucose sensing and glucose homeostasis. Diabetologia 58:2 (2015), 221–232, 10.1007/s00125-014-3451-1.
2. [2] Gouyon, F., Caillaud, L., Carriere, V., Klein, C., Dalet, V., Citadelle, D., et al. Simple-sugar meals target GLUT2 at enterocyte apical membranes to improve sugar absorption: a study in GLUT2-null mice. The Journal of Physiology 552:Pt 3 (2003), 823–832, 10.1113/jphysiol.2003.049247.
3. [3] Kellett, G.L., Helliwell, P.A., The diffusive component of intestinal glucose absorption is mediated by the glucose-induced recruitment of GLUT2 to the brush-border membrane. The Biochemical Journal 350:Pt 1 (2000), 155–162.
4. [4] Ait-Omar, A., Monteiro-Sepulveda, M., Poitou, C., Le Gall, M., Cotillard, A., Gilet, J., et al. GLUT2 accumulation in enterocyte apical and intracellular membranes: a study in morbidly obese human subjects and ob/ob and high fat-fed mice. Diabetes 60:10 (2011), 2598–2607, 10.2337/db10-1740.
5. [5] Reimann, F., Habib, A.M., Tolhurst, G., Parker, H.E., Rogers, G.J., Gribble, F.M., Glucose sensing in L cells: a primary cell study. Cell Metabolism 8:6 (2008), 532–539, 10.1016/j.cmet.2008.11.002.
6. [6] Helander, H.F., Fändriks, L., The enteroendocrine “letter cells” – time for a new nomenclature?. Scandinavian Journal of Gastroenterology 47:1 (2012), 3–12, 10.3109/00365521.2011.638391.
7. [7] Kieffer, T.J., Habener, J.F., The glucagon-like peptides. Endocrine Reviews 20:6 (1999), 876–913, 10.1210/edrv.20.6.0385.
8. [8] Wang, Z., Wang, R.M., Owji, A.A., Smith, D.M., Ghatei, M.A., Bloom, S.R., Glucagon-like peptide-1 is a physiological incretin in rat. The Journal of Clinical Investigation 95:1 (1995), 417–421, 10.1172/JCI117671.
9. [9] Pais, R., Gribble, F.M., Reimann, F., Stimulation of incretin secreting cells. Therapeutic Advances in Endocrinology and Metabolism 7:1 (2016), 24–42, 10.1177/2042018815618177.
10. [10] Stümpel, F., Burcelin, R., Jungermann, K., Thorens, B., Normal kinetics of intestinal glucose absorption in the absence of GLUT2: evidence for a transport pathway requiring glucose phosphorylation and transfer into the endoplasmic reticulum. Proceedings of the National Academy of Sciences of the United States of America 98:20 (2001), 11330–11335, 10.1073/pnas.211357698.
11. [11] Cani, P.D., Holst, J.J., Drucker, D.J., Delzenne, N.M., Thorens, B., Burcelin, R., et al. GLUT2 and the incretin receptors are involved in glucose-induced incretin secretion. Molecular and Cellular Endocrinology 276:1–2 (2007), 18–23, 10.1016/j.mce.2007.06.003.
12. [12] El Marjou, F., Janssen, K.-P., Chang, B.H.-J., Li, M., Hindie, V., Chan, L., et al. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39:3 (2004), 186–193, 10.1002/gene.20042 (New York, N.Y.: 2000).
13. [13] Neau, E., Delannoy, J., Marion, C., Cottart, C.-H., Labellie, C., Holowacz, S., et al. Three novel candidate probiotic strains with prophylactic properties in a murine model of Cow's milk allergy. Applied and Environmental Microbiology 82:6 (2016), 1722–1733, 10.1128/AEM.03440-15.
14. [14] Aranias, T., Grosfeld, A., Poitou, C., Omar, A.A., Le Gall, M., Miquel, S., et al. Lipid-rich diet enhances L-cell density in obese subjects and in mice through improved L-cell differentiation. Journal of Nutritional Science, 4, 2015, e22, 10.1017/jns.2015.11.
15. [15] Heilbronn, L.K., Ravussin, E., Calorie restriction and aging: review of the literature and implications for studies in humans. The American Journal of Clinical Nutrition 78:3 (2003), 361–369.
16. [16] Santer, R., Steinmann, B., Schaub, J., Fanconi-Bickel syndrome–a congenital defect of facilitative glucose transport. Current Molecular Medicine 2:2 (2002), 213–227.
17. [17] Meydani, S.N., Das, S.K., Pieper, C.F., Lewis, M.R., Klein, S., Dixit, V.D., et al. Long-term moderate calorie restriction inhibits inflammation without impairing cell-mediated immunity: a randomized controlled trial in non-obese humans. Aging 8:7 (2016), 1416–1431, 10.18632/aging.100994.
18. [18] Most, J., Tosti, V., Redman, L.M., Fontana, L., Calorie restriction in humans: an update. Ageing Research Reviews, 2016, 10.1016/j.arr.2016.08.005.
19. [19] Ravindran, R., Loebbermann, J., Nakaya, H.I., Khan, N., Ma, H., Gama, L., et al. The amino acid sensor GCN2 controls gut inflammation by inhibiting inflammasome activation. Nature 531:7595 (2016), 523–527, 10.1038/nature17186.
20. [20] Wang, T., Hung, C.C.Y., Randall, D.J., The comparative physiology of food deprivation: from feast to famine. Annual Review of Physiology 68 (2006), 223–251, 10.1146/annurev.physiol.68.040104.105739.
21. [21] Lopetuso, L.R., Scaldaferri, F., Petito, V., Gasbarrini, A., Commensal Clostridia: leading players in the maintenance of gut homeostasis. Gut Pathogens, 5(1), 2013, 23, 10.1186/1757-4749-5-23.
22. [22] Lührs, H., Gerke, T., Schauber, J., Dusel, G., Melcher, R., Scheppach, W., et al. Cytokine-activated degradation of inhibitory kappaB protein alpha is inhibited by the short-chain fatty acid butyrate. International Journal of Colorectal Disease 16:4 (2001), 195–201.
23. [23] Segain, J.P., Raingeard de la Blétière, D., Bourreille, A., Leray, V., Gervois, N., Rosales, C., et al. Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut 47:3 (2000), 397–403.
24. [24] Junker, A.E., Gluud, L., Holst, J.J., Knop, F.K., Vilsbøll, T., Diabetic and nondiabetic patients with nonalcoholic fatty liver disease have an impaired incretin effect and fasting hyperglucagonaemia. Journal of Internal Medicine 279:5 (2016), 485–493, 10.1111/joim.12462.
25. [25] Dalla Man, C., Micheletto, F., Sathananthan, M., Vella, A., Cobelli, C., Model-based quantification of glucagon-like peptide-1-induced potentiation of insulin secretion in response to a mixed meal challenge. Diabetes Technology & Therapeutics 18:1 (2016), 39–46, 10.1089/dia.2015.0146.
26. [26] Nguyen, N.Q., Debreceni, T.L., Bambrick, J.E., Chia, B., Wishart, J., Deane, A.M., et al. Accelerated intestinal glucose absorption in morbidly obese humans: relationship to glucose transporters, incretin hormones, and glycemia. The Journal of Clinical Endocrinology and Metabolism 100:3 (2015), 968–976, 10.1210/jc.2014-3144.
27. [27] Schmitt, C., Aranias, T., Carriere, V., Ribeiro, A., Garbin, K., Le Gall, M., et al. Intestinal GLUT2 invalidation leads to glucose malabsorption and reduces enteroendocrine cell density. Diabetologia, 58, 2015 S273–S273.