A role for intestinal TLR4-driven inflammatory response during activity-based anorexia

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Belmonte, Liliana ^a,b,c,d   Achamrah, Najate ^a,b,c,d   Nobis, Séverine ^a,b,c   Guérin, Charlène ^a,b,c   Riou, Gaëtan ^a,c,e   Bôle Feysot, Christine ^a,b,c   Boyer, Olivier ^a,b,c,e   Richard, Vincent ^a,c,f   Do Rego, Jean Claude ^a,c,g   Déchelotte, Pierre ^a,b,c,d   Goichon, Alexis ^a,b,c   Coëffier, Moïse ^a,b,c,d  

^a NORMANDIE UNIVERSITÉ   (France)

^b Faculté de Médecine Pharmacie   (France)

^c UNIVERSITY OF ROUEN   (France)

^d ROUEN UNIVERSITY HOSPITAL   (France)

^e Flow Cytometry Facility (CyFlow)   (France)

^f Université Normandie de Rouen   (France)

^g Animal Behavior Platform (SCAC)   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; TLR4 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 4;

ANIMAL; ANIMAL EXPERIMENT; ANOREXIA; BODY WEIGHT LOSS; C57BL MOUSE; COLON; DISEASE MODEL; FEMALE; GASTROENTERITIS; GENETICS; HYPOTHALAMUS; IMMUNOLOGY; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANOREXIA; COLON; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; GASTROENTERITIS; HYPOTHALAMUS; INTESTINAL MUCOSA; MICE, INBRED C57BL; MICE, KNOCKOUT; PHYSICAL CONDITIONING, ANIMAL; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; WEIGHT LOSS;

EID: 84992663918     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep35813     Document Type: Article

References (50)

1. Battle, D. E. Diagnostic and Statistical Manual of Mental Disorders (DSM). CoDAS 25, 191-192 (2013).
2. Rigaud, D., Pennacchio, H., Bizeul, C., Reveillard, V. & Vergès, B. Outcome in AN adult patients: a 13-year follow-up in 484 patients. Diabetes Metab. 37, 305-311 (2011).
3. Arcelus, J., Mitchell, A. J., Wales, J. & Nielsen, S. Mortality rates in patients with anorexia nervosa and other eating disorders. A meta-analysis of 36 studies. Arch. Gen. Psychiatry 68, 724-731 (2011).
4. Tennoune, N. et al. Bacterial ClpB heat-shock protein, an antigen-mimetic of the anorexigenic peptide α -MSH, at the origin of eating disorders. Transl. Psychiatry 4, e458 (2014).
5. Fetissov, S. O. et al. Autoantibodies against alpha-MSH, ACTH, and LHRH in anorexia and bulimia nervosa patients. Proc. Natl. Acad. Sci. USA 99, 17155-17160 (2002).
6. Sinno, M. H. et al. Regulation of feeding and anxiety by alpha-MSH reactive autoantibodies. Psychoneuroendocrinology 34, 140-149 (2009).
7. Fetissov, S. O. et al. Autoantibodies against neuropeptides are associated with psychological traits in eating disorders. Proc. Natl. Acad. Sci. USA 102, 14865-14870 (2005).
8. Terashi, M. et al. Ghrelin reactive autoantibodies in restrictive anorexia nervosa. Nutr. Burbank Los Angel. Cty. Calif 27, 407-413 (2011).
9. Fetissov, S. O. et al. Autoantibodies against appetite-regulating peptide hormones and neuropeptides: putative modulation by gut microflora. Nutr. Burbank Los Angel. Cty. Calif 24, 348-359 (2008).
10. Jésus, P. et al. Alteration of intestinal barrier function during activity-based anorexia in mice. Clin. Nutr. Edinb. Scotl. 33, 1046-1053 (2014).
11. Pisetsky, D. et al. The Expression of Cytokines and Chemokines in the Blood of Patients with Severe Weight Loss from Anorexia Nervosa. Cytokine 69, 110-115 (2014).
12. Agnello, E. et al. Tumour necrosis factor alpha and oxidative stress as maintaining factors in the evolution of anorexia nervosa. Eat. Weight Disord. EWD 17, e194-e199 (2012).
13. Davis, J. E., Gabler, N. K., Walker-Daniels, J. & Spurlock, M. E. Tlr-4 deficiency selectively protects against obesity induced by diets high in saturated fat. Obes. Silver Spring Md 16, 1248-1255 (2008).
14. Poggi, M. et al. C3H/HeJ mice carrying a toll-like receptor 4 mutation are protected against the development of insulin resistance in white adipose tissue in response to a high-fat diet. Diabetologia 50, 1267-1276 (2007).
15. Shi, H. et al. TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116, 3015-3025 (2006).
16. Kim, K.-A., Gu, W., Lee, I.-A., Joh, E.-H. & Kim, D.-H. High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PloS One 7, e47713 (2012).
17. Wong, S. & Pinkney, J. Role of cytokines in regulating feeding behaviour. Curr. Drug Targets 5, 251-263 (2004).
18. Torsello, A. et al. Central dysregulations in the control of energy homeostasis and endocrine alterations in anorexia and bulimia nervosa. J. Endocrinol. Invest. 30, 962-976 (2007).
19. Lawson, E. A. & Klibanski, A. Endocrine abnormalities in anorexia nervosa. Nat. Clin. Pract. Endocrinol. Metab. 4, 407-414 (2008).
20. Lewis, D. Y. & Brett, R. R. Activity-based anorexia in C57/BL6 mice: effects of the phytocannabinoid, Delta9-tetrahydrocannabinol (THC) and the anandamide analogue, OMDM-2. Eur. Neuropsychopharmacol. J. Eur. Coll. Neuropsychopharmacol. 20, 622-631 (2010).
21. Klenotich, S. J. & Dulawa, S. C. The activity-based anorexia mouse model. Methods Mol. Biol. Clifton NJ 829, 377-393 (2012).
22. Fasano, A. Intestinal permeability and its regulation by zonulin: diagnostic and therapeutic implications. Clin. Gastroenterol. Hepatol. Off. Clin. Pract. J. Am. Gastroenterol. Assoc. 10, 1096-1100 (2012).
23. Takeda, K. & Akira, S. TLR signaling pathways. Semin. Immunol. 16, 3-9 (2004).
24. Hueston, C. M. & Deak, T. The inflamed axis: the interaction between stress, hormones, and the expression of inflammatory-related genes within key structures comprising the hypothalamic-pituitary-adrenal axis. Physiol. Behav. 124, 77-91 (2014).
25. Ding, S. et al. High-fat diet: bacteria interactions promote intestinal inflammation which precedes and correlates with obesity and insulin resistance in mouse. PloS One 5, e12191 (2010).
26. Luo, H., Guo, P. & Zhou, Q. Role of TLR4/NF-κ B in damage to intestinal mucosa barrier function and bacterial translocation in rats exposed to hypoxia. PloS One 7, e46291 (2012).
27. Achamrah, N. et al. Maintaining physical activity during refeeding improves body composition, intestinal hyperpermeability and behavior in anorectic mice. Sci. Rep. 6, 21887 (2016).
28. Moreno-Navarrete, J. M., Sabater, M., Ortega, F., Ricart, W. & Fernández-Real, J. M. Circulating zonulin, a marker of intestinal permeability, is increased in association with obesity-associated insulin resistance. PloS One 7, e37160 (2012).
29. Fasano, A. et al. Zonulin, a newly discovered modulator of intestinal permeability, and its expression in coeliac disease. Lancet Lond. Engl. 355, 1518-1519 (2000).
30. Suenaert, P. et al. The effects of smoking and indomethacin on small intestinal permeability. Aliment. Pharmacol. Ther. 14, 819-822 (2000).
31. Armougom, F., Henry, M., Vialettes, B., Raccah, D. & Raoult, D. Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and Methanogens in anorexic patients. PloS One 4, e7125 (2009).
32. Million, M. et al. Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli. Int. J. Obes. 2005 37, 1460-1466 (2013).
33. Queipo-Ortuño, M. I. et al. Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels. PloS One 8, e65465 (2013).
34. Solmi, M. et al. Inflammatory cytokines and anorexia nervosa: A meta-analysis of cross-sectional and longitudinal studies. Psychoneuroendocrinology 51, 237-252 (2015).
35. Ilyin, S. E. & Plata-Salamán, C. R. in vivo regulation of the IL-1 beta system (ligand, receptors I and II, receptor accessory protein, and receptor antagonist) and TNF-alpha mRNAs in specific brain regions. Biochem. Biophys. Res. Commun. 227, 861-867 (1996).
36. Plata-Salamán, C. R., Ilyin, S. E., Gayle, D. & Flynn, M. C. Gram-negative and gram-positive bacterial products induce differential cytokine profiles in the brain: analysis using an integrative molecular-behavioral in vivo model. Int. J. Mol. Med. 1, 387-397 (1998).
37. Inui, A. Eating behavior in anorexia nervosa-an excess of both orexigenic and anorexigenic signalling? Mol. Psychiatry 6, 620-624 (2001).
38. Nakai, Y., Hamagaki, S., Takagi, R., Taniguchi, A. & Kurimoto, F. Plasma concentrations of tumor necrosis factor-alpha (TNF-alpha) and soluble TNF receptors in patients with anorexia nervosa. J. Clin. Endocrinol. Metab. 84, 1226-1228 (1999).
39. Laviano, A., Meguid, M. M. & Rossi-Fanelli, F. Cancer anorexia: clinical implications, pathogenesis, and therapeutic strategies. Lancet Oncol. 4, 686-694 (2003).
40. Hu, G. et al. Release of luminal exosomes contributes to TLR4-mediated epithelial antimicrobial defense. PLoS Pathog. 9, e1003261 (2013).
41. Wang, N. et al. Expression and activity of the TLR4/NF-κ B signaling pathway in mouse intestine following administration of a short-term high-fat diet. Exp. Ther. Med. 6, 635-640 (2013).
42. Hyakushima, N. et al. Interaction of soluble form of recombinant extracellular TLR4 domain with MD-2 enables lipopolysaccharide binding and attenuates TLR4-mediated signaling. J. Immunol. Baltim. Md 1950 173, 6949-6954 (2004).
43. Ten Oever, J. et al. The discriminative capacity of soluble Toll-like receptor (sTLR)2 and sTLR4 in inflammatory diseases. BMC Immunol. 15, 55 (2014).
44. Candia, E. et al. Increased production of soluble TLR2 by lamina propria mononuclear cells from ulcerative colitis patients. Immunobiology 217, 634-642 (2012).
45. Achamrah, N. et al. Maintaining physical activity during refeeding improves body composition, intestinal hyperpermeability and behavior in anorectic mice. Sci. Rep. 6, 21887; doi: 10.1038/srep21887 (2016).
46. Kim, S. F. Animal models of eating disorders. Neuroscience 211, 2-12 (2012).
47. Tropp, J. & Markus, E. J. Effects of mild food deprivation on the estrous cycle of rats. Physiol. Behav. 73, 553-559 (2001).
48. Støving, R. K., Hangaard, J. & Hagen, C. Update on endocrine disturbances in anorexia nervosa. J. Pediatr. Endocrinol. Metab. JPEM 14, 459-480 (2001).
49. Wable, G. S., Min, J.-Y., Chen, Y.-W. & Aoki, C. Anxiety is correlated with running in adolescent female mice undergoing activitybased anorexia. Behav. Neurosci. 129, 170-182 (2015).
50. Belmonte, L. et al. Role of toll like receptors in irritable bowel syndrome: differential mucosal immune activation according to the disease subtype. PloS One 7, e42777 (2012).