Maternal obesity induces gut inflammation and impairs gut epithelial barrier function in nonobese diabetic mice

Journal of Nutritional Biochemistry

Volumn 25, Issue 7, 2014, Pages 758-764

  Xue, Yansong ^a   Wang, Hui ^a,b   Du, Min ^a   Zhu, Mei Jun ^a,c  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WYOMING   (United States)

^c UNIVERSITY OF IDAHO   (United States)

Author keywords

Inflammation; Intestine; Maternal obesity; NOD; Offspring; Oxidative stress; Permeability; Tight junction proteins

Indexed keywords

CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; PEROXIREDOXIN 4; TUMOR NECROSIS FACTOR ALPHA; ANTIOXIDANT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENTERITIS; EPITHELIUM; FEMALE; ILEUM; INFLAMMATORY BOWEL DISEASE; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE CRYPT; INTESTINE VILLUS; MATERNAL OBESITY; MEMBRANE PERMEABILITY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROGENY; WEANING; ANIMAL; ILEITIS; LIPID DIET; MATERNAL NUTRITION; METABOLISM; NONOBESE DIABETIC MOUSE; OBESITY; PATHOLOGY; PATHOPHYSIOLOGY; PERMEABILITY; PREGNANCY;

ANIMALS; ANTIOXIDANTS; DIET, HIGH-FAT; FEMALE; ILEITIS; ILEUM; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MICE, INBRED NOD; OBESITY; PERMEABILITY; PREGNANCY;

EID: 84901837235     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2014.03.009     Document Type: Article

References (56)

1. Negrato C.A., Dias J.P., Teixeira M.F., Dias A., Salgado M.H., Lauris J.R., et al. Temporal trends in incidence of type 1 diabetes between 1986 and 2006 in Brazil. J Endocrinol Invest 2010, 33:373-377.
2. Sobel-Maruniak A., Grzywa M., Orlowska-Florek R., Staniszewski A. The rising incidence of type 1 diabetes in south-eastern Poland. A study of the 0-29 year-old age group, 1980-1999. Endokrynol Pol 2006, 57:127-130.
3. D'Angeli M.A., Merzon E., Valbuena L.F., Tirschwell D., Paris C.A., Mueller B.A. Environmental factors associated with childhood-onset type 1 diabetes mellitus: an exploration of the hygiene and overload hypotheses. Arch Pediatr Adolesc Med 2010, 164:732-738.
4. Flegal K.M., Carroll M.D., Kit B.K., Ogden C.L. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA 2012, 307:491-497.
5. Yan X., Huang Y., Wang H., Du M., Hess B.W., Ford S.P., et al. Maternal obesity induces sustained inflammation in both fetal and offspring large intestine of sheep. Inflamm Bowel Dis 2011, 17:1513-1522.
6. Bilbo S.D., Tsang V. Enduring consequences of maternal obesity for brain inflammation and behavior of offspring. FASEB J 2010, 24:2104-2115.
7. Jager S., Stange E.F., Wehkamp J. Inflammatory bowel disease: an impaired barrier disease. Langenbecks Arch Surg 2013, 398:1-12.
8. Vaarala O. Is the origin of type 1 diabetes in the gut?. Immunol Cell Biol 2012, 90:271-276.
9. Yu L.C. The epithelial gatekeeper against food allergy. Pediatr Neonatol 2009, 50:247-254.
10. Bosi E., Molteni L., Radaelli M.G., Folini L., Fermo I., Bazzigaluppi E., et al. Increased intestinal permeability precedes clinical onset of type 1 diabetes. Diabetologia 2006, 49:2824-2827.
11. Irvine E.J., Marshall J.K. Increased intestinal permeability precedes the onset of Crohn's disease in a subject with familial risk. Gastroenterology 2000, 119:1740-1744.
12. Ohman L., Simren M. Pathogenesis of IBS: role of inflammation, immunity and neuroimmune interactions. Nat Rev Gastroenterol Hepatol 2010, 7:163-173.
13. Weber C.R., Raleigh D.R., Su L., Shen L., Sullivan E.A., Wang Y., et al. Epithelial myosin light chain kinase activation induces mucosal interleukin-13 expression to alter tight junction ion selectivity. J Biol Chem 2010, 285:12037-12046.
14. Schulzke J.D., Ploeger S., Amasheh M., Fromm A., Zeissig S., Troeger H., et al. Epithelial tight junctions in intestinal inflammation. Ann N Y Acad Sci 2009, 1165:294-300.
15. Ma T.Y., Iwamoto G.K., Hoa N.T., Akotia V., Pedram A., Boivin M.A., et al. TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol 2004, 286:G367-G376.
16. Lamkanfi M, Dixit VM. Inflammasomes and Their Roles in Health and Disease. Annu Rev Cell Dev Bi, Vol 28. 2012;28:137-61.
17. Vande Walle L., Lamkanfi M. Inflammasomes: caspase-1-activating platforms with critical roles in host defense. Front Microbiol 2011, 2:3.
18. Mahida Y.R., Wu K., Jewell D.P. Enhanced production of interleukin 1-beta by mononuclear cells isolated from mucosa with active ulcerative colitis of Crohn's disease. Gut 1989, 30:835-838.
19. Pizarro T.T., Michie M.H., Bentz M., Woraratanadharm J., Smith M.F., Foley E., et al. IL-18, a novel immunoregulatory cytokine, is up-regulated in Crohn's disease: expression and localization in intestinal mucosal cells. J Immunol 1999, 162:6829-6835.
20. Stienstra R., van Diepen J.A., Tack C.J., Zaki M.H., van de Veerdonk F.L., Perera D., et al. Inflammasome is a central player in the induction of obesity and insulin resistance. Proc Natl Acad Sci U S A 2011, 108:15324-15329.
21. Rezaie A., Parker R.D., Abdollahi M. Oxidative stress and pathogenesis of inflammatory bowel disease: an epiphenomenon or the cause?. Dig Dis Sci 2007, 52:2015-2021.
22. Wicker L.S., Todd J.A., Peterson L.B. Genetic control of autoimmune diabetes in the NOD mouse. Annu Rev Immunol 1995, 13:179-200.
23. Vijay-Kumar M., Sanders C.J., Taylor R.T., Kumar A., Aitken J.D., Sitaraman S.V., et al. Deletion of TLR5 results in spontaneous colitis in mice. J Clin Invest 2007, 117:3909-3921.
24. Wang H., Zhao J.X., Hu N., Ren J., Du M., Zhu M.J. Side-stream smoking reduces intestinal inflammation and increases expression of tight junction proteins. World J Gastroenterol 2012, 18:2180-2187.
25. Wellen K.E., Fucho R., Gregor M.F., Furuhashi M., Morgan C., Lindstad T., et al. Coordinated regulation of nutrient and inflammatory responses by STAMP2 is essential for metabolic homeostasis. Cell 2007, 129:537-548.
26. Wang H., Xue Y., Zhang H., Huang Y., Yang G., Du M., et al. Dietary grape seed extract ameliorates symptoms of inflammatory bowel disease in IL10-deficient mice. Mol Nutr Food Res 2013, 57:2253-2257.
27. Cani P.D., Bibiloni R., Knauf C., Waget A., Neyrinck A.M., Delzenne N.M., et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 2008, 57:1470-1481.
28. Pellegrinet L, Rodilla V, Liu Z, Chen S, Koch U, Espinosa L, et al. Dll1- and dll4-mediated notch signaling are required for homeostasis of intestinal stem cells. Gastroenterology. 2011;140:1230-40 e1-7.
29. Seki E., Schnabl B. Role of innate immunity and the microbiota in liver fibrosis: crosstalk between the liver and gut. J Physiol 2012, 590:447-458.
30. Ferrier L., Mazelin L., Cenac N., Desreumaux P., Janin A., Emilie D., et al. Stress-induced disruption of colonic epithelial barrier: role of interferon-gamma and myosin light chain kinase in mice. Gastroenterology 2003, 125:795-804.
31. Koch S., Capaldo C.T., Hilgarth R.S., Fournier B., Parkos C.A., Nusrat A. Protein kinase CK2 is a critical regulator of epithelial homeostasis in chronic intestinal inflammation. Mucosal Immunol 2013, 6:136-145.
32. Shankar K., Harrell A., Liu X., Gilchrist J.M., Ronis M.J., Badger T.M. Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol 2008, 294:R528-R538.
33. Khalyfa A., Carreras A., Hakim F., Cunningham J.M., Wang Y., Gozal D. Effects of late gestational high-fat diet on body weight, metabolic regulation and adipokine expression in offspring. Int J Obes (Lond) 2013, 37:1481-1489.
34. Guberman C., Jellyman J.K., Han G., Ross M.G., Desai M. Maternal high-fat diet programs rat offspring hypertension and activates the adipose renin-angiotensin system. Am J Obstet Gynecol 2013, 209:262 e1-8.
35. Khan I., Dekou V., Hanson M., Poston L., Taylor P. Predictive adaptive responses to maternal high-fat diet prevent endothelial dysfunction but not hypertension in adult rat offspring. Circulation 2004, 110:1097-1102.
36. Wang H., Xue Y., Wang B., Zhao J., Yan X., Huang Y., et al. Maternal obesity exacerbates insulitis and type I diabetes in non-obese diabetic (NOD) mice. Reproduction 2014, in press.
37. Flohe S.B., Wasmuth H.E., Kerad J.B., Beales P.E., Pozzilli P., Elliott R.B., et al. A wheat-based, diabetes-promoting diet induces a Th1-type cytokine bias in the gut of NOD mice. Cytokine 2003, 21:149-154.
38. Maurano F., Mazzarella G., Luongo D., Stefanile R., D'Arienzo R., Rossi M., et al. Small intestinal enteropathy in non-obese diabetic mice fed a diet containing wheat. Diabetologia 2005, 48:931-937.
39. Lee A.S., Gibson D.L., Zhang Y., Sham H.P., Vallance B.A., Dutz J.P. Gut barrier disruption by an enteric bacterial pathogen accelerates insulitis in NOD mice. Diabetologia 2010, 53:741-748.
40. Sutterwala F.S., Ogura Y., Szczepanik M., Lara-Tejero M., Lichtenberger G.S., Grant E.P., et al. Critical role for NALP3/CIAS1/cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 2006, 24:317-327.
41. Bauer C., Duewell P., Mayer C., Lehr H.A., Fitzgerald K.A., Dauer M., et al. Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome. Gut 2010, 59:1192-1199.
42. Hirota S.A., Ng J., Lueng A., Khajah M., Parhar K., Li Y., et al. NLRP3 inflammasome plays a key role in the regulation of intestinal homeostasis. Inflamm Bowel Dis 2011, 17:1359-1372.
43. Monteleone G., Trapasso F., Parrello T., Biancone L., Stella A., Iuliano R., et al. Bioactive IL-18 expression is up-regulated in Crohn's disease. J Immunol 1999, 163:143-147.
44. Agostini L., Martinon F., Burns K., McDermott M.F., Hawkins P.N., Tschopp J. NALP3 forms an IL-1beta-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder. Immunity 2004, 20:319-325.
45. Di Sabatino A., Jackson C.L., Pickard K.M., Buckley M., Rovedatti L., Leakey N.A., et al. Transforming growth factor beta signalling and matrix metalloproteinases in the mucosa overlying Crohn's disease strictures. Gut 2009, 58:777-789.
46. Ruemmele F.M., Seidman E.G. Cytokine-intestinal epithelial cell interactions: implications for immune mediated bowel disorders. Zhonghua Min Guo Xiao Er Ke Yi Xue Hui Za Zhi 1998, 39:1-8.
47. Geier M.S., Smith C.L., Butler R.N., Howarth G.S. Small-intestinal manifestations of dextran sulfate sodium consumption in rats and assessment of the effects of Lactobacillus fermentum BR11. Dig Dis Sci 2009, 54:1222-1228.
48. Kruidenier L., Kuiper I., van Duijn W., Marklund S.L., van Hogezand R.A., Lamers C.B., et al. Differential mucosal expression of three superoxide dismutase isoforms in inflammatory bowel disease. J Pathol 2003, 201:7-16.
49. Kruidenier L., Kuiper I., Van Duijn W., Mieremet-Ooms M.A., van Hogezand R.A., Lamers C.B., et al. Imbalanced secondary mucosal antioxidant response in inflammatory bowel disease. J Pathol 2003, 201:17-27.
50. Michiels C., Raes M., Toussaint O., Remacle J. Importance of Se-glutathione peroxidase, catalase, and Cu/Zn-SOD for cell survival against oxidative stress. Free Radic Biol Med 1994, 17:235-248.
51. Conner E.M., Grisham M.B. Inflammation, free radicals, and antioxidants. Nutrition 1996, 12:274-277.
52. Beltran B., Nos P., Dasi F., Iborra M., Bastida G., Martinez M., et al. Mitochondrial dysfunction, persistent oxidative damage, and catalase inhibition in immune cells of naive and treated Crohn's disease. Inflamm Bowel Dis 2010, 16:76-86.
53. Krieglstein C.F., Cerwinka W.H., Laroux F.S., Salter J.W., Russell J.M., Schuermann G., et al. Regulation of murine intestinal inflammation by reactive metabolites of oxygen and nitrogen: divergent roles of superoxide and nitric oxide. J Exp Med 2001, 194:1207-1218.
54. Schulte J., Struck J., Kohrle J., Muller B. Circulating levels of peroxiredoxin 4 as a novel biomarker of oxidative stress in patients with sepsis. Shock 2011, 35:460-465.
55. Basu A., Banerjee H., Rojas H., Martinez S.R., Roy S., Jia Z.Y., et al. Differential expression of peroxiredoxins in prostate cancer: consistent upregulation of PRDX3 and PRDX4. Prostate 2011, 71:755-765.
56. Meissner F., Molawi K., Zychlinsky A. Superoxide dismutase 1 regulates caspase-1 and endotoxic shock. Nat Immunol 2008, 9:866-872.