Zonulin, regulation of tight junctions, and autoimmune diseases
Recent studies indicate that besides digestion and absorption of nutrients and water and electrolytes homeostasis, another key function of the intestine is to regulate the trafficking of environmental antigens across the host mucosal barrier. Intestinal tight junctions (TJs) create gradients for the...
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| Published in | Annals of the New York Academy of Sciences Vol. 1258; no. 1; pp. 25 - 33 |
|---|---|
| Main Author | |
| Format | Journal Article |
| Language | English |
| Published |
Malden, USA
Blackwell Publishing Inc
01.07.2012
Wiley Subscription Services, Inc |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Recent studies indicate that besides digestion and absorption of nutrients and water and electrolytes homeostasis, another key function of the intestine is to regulate the trafficking of environmental antigens across the host mucosal barrier. Intestinal tight junctions (TJs) create gradients for the optimal absorption and transport of nutrients and control the balance between tolerance and immunity to nonself antigens. To meet diverse physiological challenges, intestinal epithelial TJs must be modified rapidly and in a coordinated fashion by regulatory systems that orchestrate the state of assembly of the TJ multiprotein network. While considerable knowledge exists about TJ ultrastructure, relatively little is known about their physiological and pathophysiological regulation. Our discovery of zonulin, the only known physiologic modulator of intercellular TJs described so far, has increased our understanding of the intricate mechanisms that regulate the intestinal epithelial paracellular pathway and has led us to appreciate that its upregulation in genetically susceptible individuals leads to autoimmune diseases. |
|---|---|
| AbstractList | Recent studies indicate that besides digestion and absorption of nutrients and water and electrolytes homeostasis, another key function of the intestine is to regulate the trafficking of environmental antigens across the host mucosal barrier. Intestinal tight junctions (TJs) create gradients for the optimal absorption and transport of nutrients and control the balance between tolerance and immunity to nonself antigens. To meet diverse physiological challenges, intestinal epithelial TJs must be modified rapidly and in a coordinated fashion by regulatory systems that orchestrate the state of assembly of the TJ multiprotein network. While considerable knowledge exists about TJ ultrastructure, relatively little is known about their physiological and pathophysiological regulation. Our discovery of zonulin, the only known physiologic modulator of intercellular TJs described so far, has increased our understanding of the intricate mechanisms that regulate the intestinal epithelial paracellular pathway and has led us to appreciate that its upregulation in genetically susceptible individuals leads to autoimmune diseases. Recent studies indicate that beside digestion and absorption of nutrients and water and electrolytes homeostasis, another key function of the intestine is to regulate the trafficking of environmental antigens across the host mucosal barrier. Intestinal tight junctions (TJ) create gradients for the optimal absorption and transport of nutrients and control the balance between tolerance and immunity to non-self antigens. To meet diverse physiological challenges, intestinal epithelial TJ must be modified rapidly and in a coordinated fashion by regulatory systems that orchestrate the state of assembly of the TJ multi-protein network. While considerable knowledge exists about TJ ultrastructure, relatively little is known about their physiological and pathophysiological regulation. Our discovery of zonulin, the only known physiologic modulator of intercellular TJ described so far, increased understanding of the intricate mechanisms that regulate the intestinal epithelial paracellular pathway and led us appreciate that its up-regulation in genetically susceptible individuals leads to autoimmune diseases. Recent studies indicate that besides digestion and absorption of nutrients and water and electrolytes homeostasis, another key function of the intestine is to regulate the trafficking of environmental antigens across the host mucosal barrier. Intestinal tight junctions (TJs) create gradients for the optimal absorption and transport of nutrients and control the balance between tolerance and immunity to nonself antigens. To meet diverse physiological challenges, intestinal epithelial TJs must be modified rapidly and in a coordinated fashion by regulatory systems that orchestrate the state of assembly of the TJ multiprotein network. While considerable knowledge exists about TJ ultrastructure, relatively little is known about their physiological and pathophysiological regulation. Our discovery of zonulin, the only known physiologic modulator of intercellular TJs described so far, has increased our understanding of the intricate mechanisms that regulate the intestinal epithelial paracellular pathway and has led us to appreciate that its upregulation in genetically susceptible individuals leads to autoimmune diseases.Recent studies indicate that besides digestion and absorption of nutrients and water and electrolytes homeostasis, another key function of the intestine is to regulate the trafficking of environmental antigens across the host mucosal barrier. Intestinal tight junctions (TJs) create gradients for the optimal absorption and transport of nutrients and control the balance between tolerance and immunity to nonself antigens. To meet diverse physiological challenges, intestinal epithelial TJs must be modified rapidly and in a coordinated fashion by regulatory systems that orchestrate the state of assembly of the TJ multiprotein network. While considerable knowledge exists about TJ ultrastructure, relatively little is known about their physiological and pathophysiological regulation. Our discovery of zonulin, the only known physiologic modulator of intercellular TJs described so far, has increased our understanding of the intricate mechanisms that regulate the intestinal epithelial paracellular pathway and has led us to appreciate that its upregulation in genetically susceptible individuals leads to autoimmune diseases. |
| Author | Fasano, Alessio |
| Author_xml | – sequence: 1 givenname: Alessio surname: Fasano fullname: Fasano, Alessio organization: Mucosal Biology Research Center and Center for Celiac Research, University of Maryland School of Medicine, Baltimore, Maryland |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22731712$$D View this record in MEDLINE/PubMed |
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Gluten-free but also gluten-enriched (gluten+) diet prevent diabetes in NOD mice; the gluten enigma in type 1 diabetes. Diabetes Metab. Res. Rev. 24: 59-63. Watts, T., I. Berti, A. Sapone, et al . 2005. 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 102: 2916-2921. Monsuur, A.J., P.I. de Bakker, B.Z. Alizadeh, et al . 2005. Myosin IXB variant increases the risk of celiac disease and points toward a primary intestinal barrier defect. Nat. Genet. 37: 1341-1344. Wicher, K.B. & E. Fries. 2004. Prohaptoglobin is proteolytically cleaved in the endoplasmic reticulum by the complement C1r-like protein. Proc. Natl. Acad. Sci. USA 101: 14390-14395. Paterson, B.M., K.M. Lammers, M.C. Arrieta, et al . 2007. The safety, tolerance, pharmacokinetic and pharmacodynamic effects of single doses of AT-1001 in celiac disease subjects: a proof of concept study. Aliment. Pharmacol. Ther. 26: 757-766. 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Bistritz & J.B. Meddings. 2006. Alterations in intestinal permeability. Gut 55: 1512-1520. Sapone, A., L. de Magistris, M. Pietzak, et al . 2006. Zonulin upregulation is associated with increased gut permeability in subjects with type 1 diabetes and their relatives. Diabetes 55: 1443-1449. Márquez, L. et al . 2012. Effects of haptoglobin polymorphisms and deficiency on susceptibility to inflammatory bowel disease and on severity of murine colitis. Gut 61: 528-534. Wolters, V.M., B.Z. Alizadeh, M.E. Weijerman, et al . 2010. Intestinal barrier gene variants may not explain the increased levels of antigliadin antibodies, suggesting other mechanisms than altered permeability. Hum. Immunol. 71: 392-396. Melamed-Frank, M., O. Lache, B.I. Enav, et al . 2001. Structure-function analysis of the antioxidant properties of haptoglobin. Blood 98: 3693-3698. Asleh, R., S. Marsh, M. Shilkrut, et al . 2003. Genetically determined heterogeneity in hemoglobin scavenging and susceptibility to diabetic cardiovascular disease. Circ. Res. 92: 1193-1200. Nikulina, M. et al . 2004. Wheat gluten causes dendritic cell maturation and chemokine secretion. J. Immunol. 173: 1925-1933. Goldblum, S.E., U. Rai, A. Tripathi, et al . 2011. The active Zot domain (aa 288-293) increases ZO-1 and myosin 1C serine/threonine phosphorylation, alters interaction between ZO-1 and its binding partners, and induces tight junction disassembly through proteinase activated receptor 2 activation. FASEB J. 25: 144-158. Clemente, M.G., S. De Virgiliis, J.S. Kang, et al . 2003. Early effects of gliadin on enterocyte intracellular signaling involved in intestinal barrier function. Gut 52: 218-223. Feldman, M. & L.R. Schiller. 1983. Disorders of gastrointestinal motility associated with diabetes mellitus. Ann. Intern. Med. 98: 378-384. De Magistris, L., M. Secondulfo, D. Iafusco, et al . 1996. 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Germain. 2006. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J. Exp. Med. 203: 2841-2852. Fasano, A. 2009. Surprises from celiac disease. Sci. Am. 301: 54-61. Simpson, M., M. Mojibian, K. Barriga, et al . 2009. An exploration of Glo-3A antibody levels in children at increased risk for type 1 diabetes mellitus. Pediatr. Diabetes 10: 563-572. Tripathi, A., K.M. Lammers, S. Goldblum, et al . 2009. Identification of human zonulin, a physiological modulator of tight junctions, as prehaptoglobin-2. Proc. Natl. Acad. Sci. USA 106: 16799-16804. Wan, C. et al . 2007. Abnormal changes of plasma acute phase proteins in schizophrenia and the relation between schizophrenia and haptoglobin (Hp) gene. Amino. Acids 32: 101-108. Fasano, A. & T. Shea-Donohue. 2005. Mechanisms of disease: the role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat. Clin. Pract. Gastroenterol. Hepatol. 2: 416-422. El Asmar, R., P. Panigrahi, P. Bamford, et al . 2002. Host-dependent activation of the Zonulin system is involved in the impairment of the gut barrier function following bacterial colonization. Gastroenterology 123: 1607-1615. Schumann, M., D. Günzel, N. Buergel, et al . 2012. Cell polarity-determining proteins Par-3 and PP-1 are involved in epithelial tight junction defects in coeliac disease. Gut 61: 220-228. Wapenaar, M.C., A.J. Monsuur, A.A. van Bodegraven, et al . 2008. Associations with tight junction genes PARD3 and MAGI2 in Dutch patients point to a common barrier defect for coeliac disease and ulcerative colitis. Gut 57: 463-467. Branski, D., A. Fasano & R. Troncone. 2006. Latest developments in the pathogenesis and treatment of celiac disease. J. Pediatr. 149: 295-300 Mooradian, A.D., J.E. Morley, A.S. Levine, et al . 1996. Abnormal intestinal permeability to sugars in diabetes mellitus. Diabetologia 29: 221-224. Fasano, A., T. Not, W. Wang, et al . 2000. Zonulin, a newly discovered modulator of intestinal permeability, and its expression in coeliac disease. Lancet 355: 1518-1519. Hollande, F., E.M. Blanc, J.P. Bali, et al . 2001. HGF regulates tight junctions in new nontumorigenic gastric epithelial cell line. Am. J. Physiol. Gastrointest. Liver Physiol. 280: G910-G921. Blum, S., U. Milman, C. Shapira & A.P. Levy. 2008. Pharmacogenomic application of the haptoglobin genotype in the prevention of diabetic cardiovascular disease. Pharmacogenomics 9: 989-991. Kelly, C.P., P.H. Green, J.A. Murray, et al . 2009. Safety, tolerability and effects on intestinal permeability of larazotide acetate in celiac disease: results of a phase IIB 6-week gluten-challenge clinical trial. Gastro. 136,5: A-474. Jin, M., E. Barron, S. He, et al . 2002. Regulation of RPE intercellular junction integrity and function by hepatocyte growth factor. Invest. Ophthalmol. Vis. Sci. 43: 2782-2790. Ménard, S., N. Cerf-Bensussan & M. Heyman. 2010. Multiple facets of intestinal permeability and epithelial handling of dietary antigens. Mucosal. Immunol. 3: 247-259. Mowat, A.M., O.R. Millington & F.G. Chirdo. 2004. Anatomical and cellular basis of immunity and tolerance in the intestine. J. Pediatr. Gastroenterol. Nutr. 39: S723-S724. Chen, Y. C. et al . 2011. Haptoglobin polymorphism as a 2012; 61 2010; 53 1980; 43 2008; 9 1983; 98 2007; 32 2003; 52 1996; 29 1996; 28 2009; 10 2003; 92 2001 2004; 39 2005; 102 2004; 173 2002; 43 2008; 24 2011; 25 2005; 37 2010; 3 2006; 203 2010; 5 2003; 123 2007; 26 2010; 71 2001; 98 2004; 101 2011; 412 2000; 915 2010; 2010 2000; 113 2000; 355 2010 2006; 55 2001; 280 1987; 329 2009; 136,5 2011; 33 2008; 57 2008; 54 2006; 41 2011; 91 2010; 456 2002; 123 1999; 276 2005; 2 2008; 135 2006; 149 2009; 301 2008; 294 2008; 173 2009; 106 e_1_2_7_5_2 e_1_2_7_3_2 e_1_2_7_9_2 e_1_2_7_7_2 e_1_2_7_19_2 e_1_2_7_17_2 e_1_2_7_15_2 e_1_2_7_41_2 e_1_2_7_11_2 e_1_2_7_43_2 Fasano A. (e_1_2_7_40_2) 2001 e_1_2_7_45_2 Kelly C.P. (e_1_2_7_59_2) 2009; 136 e_1_2_7_47_2 e_1_2_7_49_2 e_1_2_7_28_2 Madara J.L. (e_1_2_7_34_2) 1980; 43 Wang W. (e_1_2_7_13_2) 2000; 113 Jin M. (e_1_2_7_26_2) 2002; 43 e_1_2_7_50_2 e_1_2_7_25_2 e_1_2_7_52_2 e_1_2_7_23_2 e_1_2_7_31_2 e_1_2_7_54_2 e_1_2_7_21_2 e_1_2_7_33_2 e_1_2_7_56_2 e_1_2_7_35_2 e_1_2_7_58_2 e_1_2_7_37_2 e_1_2_7_39_2 De Magistris L. (e_1_2_7_44_2) 1996; 28 e_1_2_7_4_2 e_1_2_7_2_2 e_1_2_7_8_2 e_1_2_7_6_2 e_1_2_7_18_2 e_1_2_7_16_2 e_1_2_7_14_2 e_1_2_7_12_2 e_1_2_7_42_2 e_1_2_7_10_2 e_1_2_7_46_2 e_1_2_7_48_2 e_1_2_7_27_2 e_1_2_7_29_2 e_1_2_7_24_2 e_1_2_7_30_2 e_1_2_7_51_2 e_1_2_7_22_2 e_1_2_7_32_2 e_1_2_7_53_2 e_1_2_7_20_2 e_1_2_7_55_2 e_1_2_7_36_2 e_1_2_7_57_2 e_1_2_7_38_2 |
| References_xml | – reference: Schumann, M., D. Günzel, N. Buergel, et al . 2012. Cell polarity-determining proteins Par-3 and PP-1 are involved in epithelial tight junction defects in coeliac disease. Gut 61: 220-228. – reference: Jin, M., E. Barron, S. He, et al . 2002. Regulation of RPE intercellular junction integrity and function by hepatocyte growth factor. Invest. Ophthalmol. Vis. Sci. 43: 2782-2790. – reference: De Magistris, L., M. Secondulfo, D. Iafusco, et al . 1996. Altered mannitol absorption in diabetic children. Ital. J. Gastroenterol. 28: 367. – reference: Wan, C. et al . 2007. Abnormal changes of plasma acute phase proteins in schizophrenia and the relation between schizophrenia and haptoglobin (Hp) gene. Amino. Acids 32: 101-108. – reference: Márquez, L. et al . 2012. Effects of haptoglobin polymorphisms and deficiency on susceptibility to inflammatory bowel disease and on severity of murine colitis. Gut 61: 528-534. – reference: Ménard, S., N. Cerf-Bensussan & M. Heyman. 2010. Multiple facets of intestinal permeability and epithelial handling of dietary antigens. Mucosal. Immunol. 3: 247-259. – reference: Fasano, A. 2011. Zonulin and its regulation of intestinal barrier function: the biological door to inflammation, autoimmunity, and cancer. Physiol. Rev. 91: 151-175. – reference: Meddings, J.B., J. Jarand, S.J. Urbanski, et al . 1999. Increased gastrointestinal permeability is an early lesion in the spontaneously diabetic BB rat. Am. J. Physiol. 276: G951-G957. – reference: Melamed-Frank, M., O. Lache, B.I. Enav, et al . 2001. Structure-function analysis of the antioxidant properties of haptoglobin. Blood 98: 3693-3698. – reference: Brorsson, C., N. Tue Hansen, R. Bergholdt, et al . 2010. The type 1 diabetes-HLA susceptibility interactome-identification of HLA genotype-specific disease genes for type 1 diabetes. PLoS One. 5: e9576. – reference: Wicher, K.B. & E. Fries. 2004. Prohaptoglobin is proteolytically cleaved in the endoplasmic reticulum by the complement C1r-like protein. Proc. Natl. Acad. Sci. USA 101: 14390-14395. – reference: Branski, D., A. Fasano & R. Troncone. 2006. Latest developments in the pathogenesis and treatment of celiac disease. J. Pediatr. 149: 295-300 – reference: Arrieta, M.C., L. Bistritz & J.B. Meddings. 2006. Alterations in intestinal permeability. Gut 55: 1512-1520. – reference: Papp, M., I. Foldi, E. Nemes, et al . 2008. Haptoglobin polymorphism: a novel genetic risk factor for celiac disease development and its clinical manifestations. Clin. Chem. 54: 697-704. – reference: Mowat, A.M., O.R. Millington & F.G. Chirdo. 2004. Anatomical and cellular basis of immunity and tolerance in the intestine. J. Pediatr. Gastroenterol. Nutr. 39: S723-S724. – reference: Hollande, F., E.M. Blanc, J.P. Bali, et al . 2001. HGF regulates tight junctions in new nontumorigenic gastric epithelial cell line. Am. J. Physiol. Gastrointest. Liver Physiol. 280: G910-G921. – reference: Visser, J.T., K. Lammers, A. Hoogendijk, et al . 2010. 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. 53: 2621-2628. – reference: Chieppa, M., M. Rescigno, A.Y. Huang & R.N. Germain. 2006. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J. Exp. Med. 203: 2841-2852. – reference: Fasano, A. 2000. Regulation of intercellular tight junctions by zonula occludens toxin and its eukaryotic analogue zonulin. Ann. N. Y. Acad. Sci. 915: 214-222. – reference: Drago, S., A.R. El, P.M. Di, et al . 2006. Gliadin, zonulin and gut permeability: effects on celiac and non-celiac intestinal mucosa and intestinal cell lines. Scand. J. Gastroenterol. 41: 408-419. – reference: Wapenaar, M.C., A.J. Monsuur, A.A. van Bodegraven, et al . 2008. Associations with tight junction genes PARD3 and MAGI2 in Dutch patients point to a common barrier defect for coeliac disease and ulcerative colitis. Gut 57: 463-467. – reference: Funda, D.P. & A. Kaas, H. Tlaskalová-Hogenová & K. Buschard. 2008. Gluten-free but also gluten-enriched (gluten+) diet prevent diabetes in NOD mice; the gluten enigma in type 1 diabetes. Diabetes Metab. Res. Rev. 24: 59-63. – reference: Simpson, M., M. Mojibian, K. Barriga, et al . 2009. An exploration of Glo-3A antibody levels in children at increased risk for type 1 diabetes mellitus. Pediatr. Diabetes 10: 563-572. – reference: Bjorkman, P.J., M.A. Saper, B. Samraoui, et al . 1987. Structure of the human class I histocompatibility antigen, HLA-A2. Nature 329: 506-512. – reference: Chen, Y. C. et al . 2011. Haptoglobin polymorphism as a risk factor for chronic kidney disease: a case-control study. Am. J. Nephrol. 33: 510-514. – reference: Fasano, A. 2009. Surprises from celiac disease. Sci. Am. 301: 54-61. – reference: Monsuur, A.J., P.I. de Bakker, B.Z. Alizadeh, et al . 2005. Myosin IXB variant increases the risk of celiac disease and points toward a primary intestinal barrier defect. Nat. Genet. 37: 1341-1344. – reference: Arentz-Hansen, H., S. McAdam, O. Molberg, et al . 2003. Celiac lesion T cells recognized epitopes that cluster in regions of gliadin rich in proline residues. Gastroenterology 123:803-809. – reference: Asleh, R., S. Marsh, M. Shilkrut, et al . 2003. Genetically determined heterogeneity in hemoglobin scavenging and susceptibility to diabetic cardiovascular disease. Circ. Res. 92: 1193-1200. – reference: Mooradian, A.D., J.E. Morley, A.S. Levine, et al . 1996. Abnormal intestinal permeability to sugars in diabetes mellitus. Diabetologia 29: 221-224. – reference: Paterson, B.M., K.M. Lammers, M.C. Arrieta, et al . 2007. The safety, tolerance, pharmacokinetic and pharmacodynamic effects of single doses of AT-1001 in coeliac disease subjects: a proof of concept study. Aliment. Pharmacol. Ther. 26: 757-766. – reference: Goldblum, S.E., U. Rai, A. Tripathi, et al . 2011. The active Zot domain (aa 288-293) increases ZO-1 and myosin 1C serine/threonine phosphorylation, alters interaction between ZO-1 and its binding partners, and induces tight junction disassembly through proteinase activated receptor 2 activation. FASEB J. 25: 144-158. – reference: Fasano, A. 2008. Physiological, pathological, and therapeutic implications of zonulin-mediated intestinal barrier modulation: living life on the edge of the wall. Am. J. Pathol. 173: 1243-1252. – reference: Madara, J.L. & J.S. Trier. 1980. Structural abnormalities of jejunal epithelial cell membranes in celiac sprue. Lab. Inves. 43: 254-261. – reference: Fasano, A., T. Not, W. Wang, et al . 2000. 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| SubjectTerms | Absorption Amino Acid Sequence Antigens Autoimmune diseases Autoimmune Diseases - physiopathology autoimmunity Cholera Toxin - physiology Gliadin - chemistry Gliadin - metabolism Haptoglobins Humans Intestinal Mucosa - physiopathology intestine Molecular Sequence Data Nutrients Physiology Protein Precursors tight junctions Tight Junctions - physiology zonulin |
| Title | Zonulin, regulation of tight junctions, and autoimmune diseases |
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