The role for gut permeability in the pathogenesis of type 1 diabetes - a solid or leaky concept?

Pediatric Diabetes

Volumn 16, Issue 7, 2015, Pages 485-492

  Li, Xia ^a   Atkinson, Mark A ^b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Barrier function diabetes; Beta cell autoimmunity; Intestinal permeability

Indexed keywords

ANTIBIOTIC AGENT; GLUCAGON LIKE PEPTIDE 1 DERIVATIVE; PROBIOTIC AGENT; BIOLOGICAL MARKER;

AGE; ANTIBIOTIC THERAPY; DIET; HUMAN; HYPERGLYCEMIA; IMMUNE RESPONSE; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; INTESTINE BIOPSY; INTESTINE MUCOSA PERMEABILITY; MICROFLORA; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; RODENT MODEL; ANIMAL; AUTOIMMUNITY; BIOLOGICAL MODEL; BLOOD; CHILD; DIABETES MELLITUS, TYPE 1; DYSBIOSIS; GASTROINTESTINAL TRACT; IMMUNOLOGY; INFANT; METABOLISM; MICROBIOLOGY; PANCREAS ISLET; PATHOPHYSIOLOGY; PEDIATRICS; PERMEABILITY; PRESCHOOL CHILD; PROCEDURES; TRENDS;

ANIMALS; AUTOIMMUNITY; BIOMARKERS; CHILD; CHILD, PRESCHOOL; DIABETES MELLITUS, TYPE 1; DYSBIOSIS; GASTROINTESTINAL TRACT; HUMANS; INFANT; ISLETS OF LANGERHANS; MODELS, BIOLOGICAL; PEDIATRICS; PERMEABILITY;

EID: 84942984042     PISSN: 1399543X     EISSN: 13995448     Source Type: Journal    
DOI: 10.1111/pedi.12305     Document Type: Review

References (63)

1. Fasano A. Leaky gut and autoimmune diseases. Clin Rev Allergy Immunol 2012: 42: 71-78.
2. Vaarala O, Atkinson MA, Neu J. The "perfect storm" for type 1 diabetes: the complex interplay between intestinal microbiota, gut permeability, and mucosal immunity. Diabetes 2008: 57: 2555-2562.
3. Vaarala O. Leaking gut in type 1 diabetes. Curr Opin Gastroenterol 2008: 24: 701-706.
4. de Kort S, Keszthelyi D, Masclee AA. Leaky gut and diabetes mellitus: what is the link? Obes Rev 2011: 12: 449-458.
5. Vaarala O. Is the origin of type 1 diabetes in the gut? Immunol Cell Biol 2012: 90: 271-276.
6. Meddings JB, Jarand J, Urbanski SJ, Hardin J, Gall DG. Increased gastrointestinal permeability is an early lesion in the spontaneously diabetic BB rat. Am J Physiol 1999: 276: G951-G957.
7. Neu J, Reverte CM, Mackey AD et al. Changes in intestinal morphology and permeability in the biobreeding rat before the onset of type 1 diabetes. J Pediatr Gastroenterol Nutr 2005: 40: 589-595.
8. Hardin JA, Donegan L, Woodman RC, Trevenen C, Gall DG. Mucosal inflammation in a genetic model of spontaneous type I diabetes mellitus. Can J Physiol Pharmacol 2002: 80: 1064-1070.
9. Todd DJ, Forsberg EM, Greiner DL, Mordes JP, Rossini AA, Bortell R. Deficiencies in gut NK cell number and function precede diabetes onset in BB rats. J Immunol 2004: 172: 5356-5362.
10. Malaisse WJ, Courtois P, Scott FW. Insulin-dependent diabetes and gut dysfunction: the BB rat model. Horm Metab Res 2004: 36: 585-594.
11. Vanuytsel T, Vanormelingen C, Vanheel H et al. From intestinal permeability to dysmotility: the biobreeding rat as a model for functional gastrointestinal disorders. PLoS One 2014: 9: e111132.
12. Demedts I, Masaoka T, Kindt S et al. Gastrointestinal motility changes and myenteric plexus alterations in spontaneously diabetic biobreeding rats. J Neurogastroenterol Motil 2013: 19: 161-170.
13. Vaarala O. The role of the gut in beta-cell autoimmunity and type 1 diabetes: a hypothesis. Pediatr Diabetes 2000: 1: 217-225.
14. Visser JT, Lammers K, Hoogendijk A et al. Restoration of impaired intestinal barrier function by the hydrolysed casein diet contributes to the prevention of type 1 diabetes in the diabetes-prone BioBreeding rat. Diabetologia 2010: 53: 2621-2628.
15. Patrick C, Wang GS, Lefebvre DE et al. Promotion of autoimmune diabetes by cereal diet in the presence or absence of microbes associated with gut immune activation, regulatory imbalance, and altered cathelicidin antimicrobial Peptide. Diabetes 2013: 62: 2036-2047.
16. Funda DP, Kaas A, Bock T, Tlaskalová-Hogenová H, Buschard K. Gluten-free diet prevents diabetes in NOD mice. Diabetes Metab Res Rev 1999: 15: 323-327.
17. Li N, Hatch M, Wasserfall CH et al. Butyrate and type 1 diabetes mellitus: can we fix the intestinal leak? J Pediatr Gastroenterol Nutr 2010: 51: 414-417.
18. Hadjiyanni I, Li KK, Drucker DJ. Glucagon-like peptide-2 reduces intestinal permeability but does not modify the onset of type 1 diabetes in the nonobese diabetic mouse. Endocrinology 2009: 150: 592-599.
19. Visser JT, Bos NA, Harthoorn LF et al. Potential mechanisms explaining why hydrolyzed casein-based diets outclass single amino acid-based diets in the prevention of autoimmune diabetes in diabetes-prone BB rats. Diabetes Metab Res Rev 2012: 28: 505-513.
20. Hansen CH, Krych L, Buschard K et al. A maternal gluten-free diet reduces inflammation and diabetes incidence in the offspring of NOD mice. Diabetes 2014: 63: 2821-2832.
21. Lee AS, Gibson DL, Zhang Y, Sham HP, Vallance BA, Dutz JP. Gut barrier disruption by an enteric bacterial pathogen accelerates insulitis in NOD mice. Diabetologia 2010: 53: 741-748.
22. Wen L, Ley RE, Volchkov PY et al. Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature 2008: 455: 1109-1113.
23. Carratù R, Secondulfo M, de Magistris L et al. Altered intestinal permeability to mannitol in diabetes mellitus type I. J Pediatr Gastroenterol Nutr 1999: 28: 264-269.
24. Kuitunen M, Saukkonen T, Ilonen J, Akerblom HK, Savilahti E. Intestinal permeability to mannitol and lactulose in children with type 1 diabetes with the HLA-DQB1*02 allele. Autoimmunity 2002: 35: 365-368.
25. Bosi E, Molteni L, Radaelli MG et al. Increased intestinal permeability precedes clinical onset of type 1 diabetes. Diabetologia 2006: 49: 2824-2827.
26. Uibo R, Panarina M, Teesalu K et al. Celiac disease in patients with type 1 diabetes: a condition with distinct changes in intestinal immunity? Cell Mol Immunol 2011: 8: 150-156.
27. Westerholm-Ormio M, Vaarala O, Pihkala P, Ilonen J, Savilahti E. Immunologic activity in the small intestinal mucosa of pediatric patients with type 1 diabetes. Diabetes 2003: 52: 2287-2295.
28. Fasano A. Intestinal permeability and its regulation by zonulin: diagnostic and therapeutic implications. Clin Gastroenterol Hepatol 2012: 10: 1096-1100.
29. Fasano A. Zonulin and its regulation of intestinal barrier function: the biological door to inflammation, autoimmunity, and cancer. Physiol Rev 2011: 91: 151-175.
30. Watts T, Berti I, Sapone A et al. Role of the intestinal tight junction modulator zonulin in the pathogenesis of type I diabetes in BB diabetic-prone rats. Proc Natl Acad Sci USA 2005: 102: 2916-2921.
31. Sapone A, de Magistris L, Pietzak M et al. Zonulin upregulation is associated with increased gut permeability in subjects with type 1 diabetes and their relatives. Diabetes 2006: 55: 1443-1449.
32. de Goffau MC, Luopajärvi K, Knip M et al. Fecal microbiota composition differs between children with β-cell autoimmunity and those without. Diabetes 2013: 62: 1238-1244.
33. Pang T, Leach ST, Katz T, Day AS, Ooi CY. Fecal biomarkers of intestinal health and disease in children. Front Pediatr 2014: 2: 6.
34. Thuijls G, Derikx JP, van Wijck K et al. Non-invasive markers for early diagnosis and determination of the severity of necrotizing enterocolitis. Ann Surg 2010: 251: 1174-1180.
35. Vaarala O. Is type 1 diabetes a disease of the gut immune system triggered by cow's milk insulin? Adv Exp Med Biol 2005: 569: 151-156.
36. Cani PD, Possemiers S, Van de Wiele T et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 2009: 58: 1091-1103.
37. Brugman S, Klatter FA, Visser JT et al. Antibiotic treatment partially protects against type 1 diabetes in the bio-breeding diabetes-prone rat. Is the gut flora involved in the development of type 1 diabetes? Diabetologia 2006: 49: 2105-2108.
38. Alkanani AK, Hara N, Gottlieb PA et al. Alterations in intestinal microbiota correlate with susceptibility to type 1 diabetes. Diabetes 2015: pii: db141847. [Epub ahead of print].
39. Atkinson MA, Chervonsky A. Does the gut microbiota have a role in type 1 diabetes? Early evidence from humans and animal models of the disease. Diabetologia 2012: 55: 2868-2877.
40. Clarke G, Stilling RM, Kennedy PJ, Stanton C, Cryan JF, Dinan TG. Minireview: gut microbiota: the neglected endocrine organ. Mol Endocrinol 2014: 28: 1221-1238.
41. Valentini L, Ramminger S, Haas V et al. Small intestinal permeability in older adults. Physiol Rep 2014: 2: e00281.
42. Xue Y, Wang H, Du M, Zhu MJ. Maternal obesity induces gut inflammation and impairs gut epithelial barrier function in nonobese diabetic mice. J Nutr Biochem 2014: 25: 758-764.
43. Arnal ME, Zhang J, Erridge C, Smidt H, Lallès JP. Maternal antibiotic-induced early changes in microbial colonization selectively modulate colonic permeability and inducible heat shock proteins, and digesta concentrations of alkaline phosphatase and TLR-stimulants in swine offspring. PLoS One 2015: 10: e0118092.
44. Horton F, Wright J, Smith L, Hinton PJ, Robertson MD. Increased intestinal permeability to oral chromium (51 Cr) -EDTA in human type 2 diabetes. Diabet Med 2014: 31: 559-563.
45. Jayashree B, Bibin YS, Prabhu D et al. Increased circulatory levels of lipopolysaccharide (LPS) and zonulin signify novel biomarkers of proinflammation in patients with type 2 diabetes. Mol Cell Biochem 2014: 388: 203-210.
46. Spångéus A, Suhr O, El-Salhy M. Diabetic state affects the innervation of gut in an animal model of human type 1 diabetes. Histol Histopathol 2000: 15: 739-744.
47. Oikarinen M, Tauriainen S, Oikarinen S et al. Type 1 diabetes is associated with enterovirus infection in gut mucosa. Diabetes 2012: 61: 687-691.
48. Oikarinen M, Tauriainen S, Honkanen T et al. Detection of enteroviruses in the intestine of type 1 diabetic patients. Clin Exp Immunol 2008: 151: 71-75.
49. Mercalli A, Lampasona V, Klingel K et al. No evidence of enteroviruses in the intestine of patients with type 1 diabetes. Diabetologia 2012: 55: 2479-2488.
50. Daft JG, Lorenz RG. Role of the gastrointestinal ecosystem in the development of type 1 diabetes. Pediatr Diabetes 2015: doi: 10.1111/pedi.12282. [Epub ahead of print].
51. Knip M, Akerblom HK, Becker D et al. Hydrolyzed infant formula and early beta-cell autoimmunity: a randomized clinical trial. JAMA 2014: 311: 2279-2287.
52. Akerblom HK, Virtanen SM, Ilonen J et al. Dietary manipulation of beta cell autoimmunity in infants at increased risk of type 1 diabetes: a pilot study. Diabetologia 2005: 48: 829-837.
53. Knip M, Virtanen SM, Seppa K et al. Dietary intervention in infancy and later signs of beta-cell autoimmunity. N Engl J Med 2010: 363: 1900-1908.
54. Paronen J, Knip M, Savilahti E et al., Finnish Trial to Reduce IDDM in the Genetically at Risk Study Group. Effect of cow's milk exposure and maternal type 1 diabetes on cellular and humoral immunization to dietary insulin in infants at genetic risk for type 1 diabetes. Diabetes 2000: 49: 1657-1665.
55. Hummel S, Pfluger M, Hummel M, Bonifacio E, Ziegler AG. Primary dietary intervention study to reduce the risk of islet autoimmunity in children at increased risk for type 1 diabetes: the BABYDIET study. Diabetes Care 2011: 34: 1301-1305.
56. Hummel M, Bonifacio E, Naserke HE, Ziegler AG. Elimination of dietary gluten does not reduce titers of type 1 diabetes-associated autoantibodies in high-risk subjects. Diabetes Care 2002: 25: 1111-1116.
57. Norris JM, Yin X, Lamb MM et al. Omega-3 polyunsaturated fatty acid intake and islet autoimmunity in children at increased risk for type 1 diabetes. JAMA 2007: 298: 1420-1428.
58. Hsieh CY, Osaka T, Moriyama E, Date Y, Kikuchi J, Tsuneda S. Strengthening of the intestinal epithelial tight junction by Bifidobacterium bifidum. Physiol Rep 2015: 3: e12327; doi: 10.14814/phy2.12327.
59. Ghosh SS, Bie J, Wang J, Ghosh S. Oral supplementation with non-absorbable antibiotics or curcumin attenuates western diet-induced atherosclerosis and glucose intolerance in LDLR-/- mice - role of intestinal permeability and macrophage activation. PLoS One 2014: 9: e108577.
60. Calcinaro F, Dionisi S, Marinaro M et al. Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the non-obese diabetic mouse. Diabetologia 2005: 48: 1565-1575.
61. Kielgast U, Holst JJ, Madsbad S. Antidiabetic actions of endogenous and exogenous GLP-1 in type 1 diabetic patients with and without residual β-cell function. Diabetes 2011: 60: 1599-1607.
62. Kielgast U, Krarup T, Holst JJ, Madsbad S. Four weeks of treatment with liraglutide reduces insulin dose without loss of glycemic control in type 1 diabetic patients with and without residual beta-cell function. Diabetes Care 2011: 34: 1463-1468.
63. Ljungberg M, Korpela R, Ilonen J, Ludvigsson J, Vaarala O. Probiotics for the prevention of beta cell autoimmunity in children at genetic risk of type 1 diabetes - the PRODIA study. Ann N Y Acad Sci 2006: 1079: 360-364.