Зонулин-регулируемая барьерная функция кишечника и полиморбидность
Аннотация
Одним из главных достижений в понимании роли проницаемости кишечника является открытие человеческого аналога токсина zonulaoccludens, названного зонулином. В данном обзоре литературы описаны различные заболевания, в том числе и инфекция COVID-19, в патогенезе которых участвует физиологический модулятор межклеточных плотных контактов - зонулин. Обсуждается возможная роль зонулина в развитии полиморбидности.
Об авторах
К. Н. Халаиджева
ФГАОУ ВО Первый Московский государственный медицинский университет им. И. М. Сеченова Минздрава России (Сеченовский Университет)
Россия
Россия
В. Н. Дроздов
ФГАОУ ВО Первый Московский государственный медицинский университет им. И. М. Сеченова Минздрава России (Сеченовский Университет)
Россия
Россия
Е. В. Ших
ФГАОУ ВО Первый Московский государственный медицинский университет им. И. М. Сеченова Минздрава России (Сеченовский Университет)
Россия
Россия
Л. Б. Лазебник
ФГБОУ ВО «Московский государственный медико- стоматологический университет им. А. И. Евдокимова» Минздрава России
Россия
Россия
Список литературы
1. Lazebnik L.B., Drozdov V. N. Genez Polimorbidnosti [Polymorbidity Genesis]. Klinicheskaya gerontologiya - Clinical Gerontology, 2001, no. 1-2, 3 p. (in Russ.)
2. Lazebnik L.B., Drozdov V. N. Zabolevaniya Organov Pishchevareniya U Pozhilykh [Diseases of the Digestive Organs in the Elderly]. Mosсow, 2003. (in Russ.)
3. Lazebnik L.B., Konev Yu.V., Drozdov V. N., Efremov L. I. Polipragmaziya: Geriatricheskii Aspekt Problemy [Polypragmasia: Geriatric Aspect of The Problem]. Consilium Medicum. 2007, vol.9, no.12, pp. 29-34. (in Russ.)
4. Farquhar M.G., Palade G. E. Junctional complexes in various epithelia. Journal of Cell Biology. 1963;17:375-412. doi:10.1083/jcb.17.2.375
5. Turner J. R.Intestinal mucosal barrier function in health and disease. Nature Reviews Immunology. 2009;9:799-809. doi:10.1038/nri2653
6. Furuse M., Hirase T., Itoh M., Nagafuchi A., Yonemura S., Tsukita S., et al. Occludin: a novel integral membrane protein localizing at tight junctions. Journal of Cell Biology. 1993;123:1777-88. doi:10.1083/jcb.123.6.1777
7. Furuse M., Fujita K., Hiiragi T., Fujimoto K., Tsukita S. Claudin-1 and -2: Novel Integral Membrane Proteins Localizing at Tight Junctions with No Sequence Similarity to Occludin. Journal of Cell Biology. 1998;141:1539-50. doi:10.1083/jcb.141.7.1539
8. Martìn-Padura I., Lostaglio S., Schneemann M., Williams L., Romano M., Fruscella P., et al. Junctional Adhesion Molecule, a Novel Member of the Immunoglobulin Superfamily That Distributes at Intercellular Junctions and Modulates Monocyte Transmigration. Journal of Cell Biology. 1998;142:117-27. doi:10.1083/jcb.142.1.117
9. Ikenouchi J., Furuse M., Furuse K., Sasaki H., Tsukita S., Tsukita S. Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. Journal of Cell Biology. 2005;171:939-45. doi:10.1083/jcb.200510043
10. Higashi T., Tokuda S., Kitajiri S., Masuda S., Nakamura H., Oda Y., et al. Analysis of the ‘angulin’ proteins LSR, ILDR1 and ILDR2 - tricellulin recruitment, epithelial barrier function and implication in deafness pathogenesis. Journal of Cell Science. 2013;126:3797-3797. doi:10.1242/jcs.138271
11. Fasano A., Baudry B., Pumplin D. W., Wasserman S. S., Tall B. D., Ketley J. M., et al. Vibrio cholerae produces a second enterotoxin, which affects intestinal tight junctions. Proc Natl Acad Sci U S A. 1991;88:5242-6. doi:10.1073/pnas.88.12.5242
12. Fasano A., Fiorentini C., Donelli G., Uzzau S., Kaper J. B., Margaretten K., et al. Zonula occludens toxin modulates tight junctions through protein kinase C-dependent actin reorganization, in vitro. Journal of Clinical Investigation. 1995;96:710-20. doi:10.1172/JCI118114
13. Fasano A., Not T., Wang W., Uzzau S., Berti I., Tommasini A., et al. Zonulin, a newly discovered modulator of intestinal permeability, and its expression in coeliac disease. The Lancet. 2000;355:1518-9. doi:10.1016/S0140-6736(00)02169-3
14. Tripathi A., Lammers K. M., Goldblum S., Shea-Donohue T., Netzel-Arnett S., Buzza M. S., et al. Identification of human zonulin, a physiological modulator of tight junctions, as prehaptoglobin-2. Proceedings of the National Academy of Sciences of the United States of America. 2009;106:16799-804. doi:10.1073/pnas.0906773106
15. Asmar R. el, Panigrahi P., Bamford P., Berti I., Not T., Coppa G. V., et al. Host-dependent zonulin secretion causes the impairment of the small intestine barrier function after bacterial exposure. Gastroenterology. 2002;123:1607-15. doi:10.1053/GAST.2002.36578
16. Parfenov A.I., Bykova S. V., Sabelnikova E. A., Maev I. V., Baranov A. A., Bakulin I. G., et al. All-Russian consensus on diagnosis and treatment of celiac disease in children and adults. Terapevticheskii Arkhiv. 2017;89:94-107. (in Russ.) doi:10.17116/terarkh201789394-107
17. Fasano A., Not T., Wang W., Uzzau S., Berti I., Tommasini A., et al. Zonulin, a newly discovered modulator of intestinal permeability, and its expression in coeliac disease. Lancet (London, England). 2000;355:1518-9. doi:10.1016/S0140-6736(00)02169-3
18. Clemente M. G. Early effects of gliadin on enterocyte intracellular signalling involved in intestinal barrier function. Gut. 2003;52:218-23. doi:10.1136/gut.52.2.218
19. Vogel S.N., Thomas K. E., Sapone A., Fasano A. Disease the Innate Immune Response in Celiac Permeability Are MyD88-Dependent: Role of Intestinal Inflammatory Gene Expression and Gliadin Stimulation of Murine Macrophage 2006. doi:10.4049/jimmunol.176.4.2512
20. Lammers K.M., Lu R., Brownley J., Lu B., Gerard C., Thomas K., et al. Gliadin Induces an Increase in Intestinal Permeability and Zonulin Release by Binding to the Chemokine Receptor CXCR3 n. d. doi:10.1053/j.gastro.2008.03.023
21. Gopalakrishnan S., Tripathi A., Tamiz A. P., Alkan S. S., Pandey N. B. Larazotide acetate promotes tight junction assembly in epithelial cells. Peptides. 2012;35:95-101. doi:10.1016/j.peptides.2012.02.016
22. Gopalakrishnan S., Durai M., Kitchens K., Tamiz A. P., Somerville R., Ginski M., et al. Larazotide acetate regulates epithelial tight junctions in vitro and in vivo. Peptides. 2012;35:86-94. doi:10.1016/j.peptides.2012.02.015
23. Paterson B.M., Lammers K. M., Arrieta M. C., Fasano A., Meddings J. B. The safety, tolerance, pharmacokinetic and pharmacodynamic effects of single doses of AT-1001 in coeliac disease subjects: A proof of concept study. Alimentary Pharmacology and Therapeutics. 2007;26:757-66. doi:10.1111/J.1365-2036.2007.03413.X/FORMAT/PDF
24. Kelly C.P., Green P. H.R., Murray J. A., Dimarino A., Colatrella A., Leffler D. A., et al. Larazotide acetate in patients with coeliac disease undergoing a gluten challenge: A randomised placebo-controlled study. Alimentary Pharmacology and Therapeutics. 2013;37:252-62. doi:10.1111/APT.12147/FORMAT/PDF
25. Leffl Er D. A., Kelly C. P., Abdallah H. Z., Colatrella A. M., Harris L. A., Leon F., et al. A Randomized, Double-Blind Study of Larazotide Acetate to Prevent the Activation of Celiac Disease During Gluten Challenge. The American Journal of Gastroenterology. 2012;107:1554-62. doi:10.1038/ajg.2012.211
26. Leffler D.A., Kelly C. P., Green P. H.R., Fedorak R. N., Dimarino A., Perrow W., et al. Larazotide Acetate for Persistent Symptoms of Celiac Disease Despite a Gluten-Free Diet: A Randomized Controlled Trial. Gastroenterology. 2015;148:1311. doi:10.1053/J.GASTRO.2015.02.008
27. Volta U., Caio G., Tovoli F., de Giorgio R. Non-celiac gluten sensitivity: questions still to be answered despite increasing awareness. Cellular and Molecular Immunology. 2013;10:383-92. doi:10.1038/cmi.2013.28
28. Bueno L. Protease activated receptor 2: a new target for IBS treatment. European Review for Medical and Pharmacological Sciences. 2008;12 Suppl 1:95-102.
29. Bykova S.V., Sabelnikova E. A., Gudkova R. B., Drozdov V. N., Shcherbakov P. L., Kirova M. V., et al. Celiac disease detection rate in gastroenterological patients. Terapevticheskii Arkhiv. 2016;88:39-43. doi:10.17116/terarkh201688239-43
30. Hollon J., Puppa E. L., Greenwald B., Goldberg E., Guerrerio A., Fasano A. Effect of Gliadin on Permeability of Intestinal Biopsy Explants from Celiac Disease Patients and Patients with Non-Celiac Gluten Sensitivity. Nutrients. 2015;7:1565. doi:10.3390/NU7031565
31. Barbaro M.R., Cremon C., Morselli-Labate A.M., di Sabatino A., Giuffrida P., Corazza G. R., et al. Serum zonulin and its diagnostic performance in non-coeliac gluten sensitivity. Gut. 2020;69:1966-74. doi:10.1136/GUTJNL-2019-319281
32. Laukoetter M.G., Nava P., Nusrat A. Role of the intestinal barrier in inflammatory bowel disease. World Journal of Gastroenterology. 2008;14:401-7. doi:10.3748/wjg.14.401
33. Schulzke J.D., Ploeger S., Amasheh M., Fromm A., Zeissig S., Troeger H., et al. Epithelial tight junctions in intestinal inflammation. Annals of the New York Academy of Sciences. 2009;1165:294-300. doi:10.1111/j.1749-6632.2009.04062.x
34. Mankertz J., Schulzke J-D. Altered permeability in inflammatory bowel disease: pathophysiology and clinical implications. Current Opinion in Gastroenterology. 2007;23:379-83. doi:10.1097/MOG.0b013e32816aa392
35. McGuckin M.A., Eri R., Simms L. A., Florin T. H.J., Radford-Smith G.Intestinal barrier dysfunction in inflammatory bowel diseases. Inflammatory Bowel Diseases. 2009;15:100-13. doi:10.1002/IBD.20539
36. Wyatt J., Vogelsang H., Hübl W., Waldhöer T., Lochs H.Intestinal permeability and the prediction of relapse in Crohn’s disease. Lancet (London, England). 1993;341:1437-9. doi:10.1016/0140-6736(93)90882-h
37. Teahon K., Smethurst P., Levi A. J., Menzies I. S., Bjarnason I.Intestinal permeability in patients with Crohn’s disease and their first degree relatives. Gut. 1992;33:320-3. doi:10.1136/GUT.33.3.320
38. Gerova V.A., Stoynov S. G., Katsarov S., Svinarov D. A., Katsarov D. S., Keshavarzian A., et al. Increased intestinal permeability in inflammatory bowel diseases assessed by iohexol test. World Journal of Gastroenterology: WJG. 2011;17:2211. doi:10.3748/wjg.v17.i17
39. Arrieta M.C., Madsen K., Doyle J., Meddings J. Reducing small intestinal permeability attenuates colitis in the IL10 gene-deficient mouse n. d. doi:10.1136/gut.2008.150888
40. Malíčková K., Francová I., Lukáš M., Kolář M., Králíková E., Bortlík M., et al. Fecal zonulin is elevated in Crohn’s disease and in cigarette smokers. Pract Lab Med. 2017;9:39-44. Published 2017 Sep 23. doi:10.1016/j.plabm.2017.09.001
41. Caviglia G.P., Dughera F., Ribaldone D. G., Rosso C., Abate M. L., Pellicano R., et al. Serum zonulin in patients with inflammatory bowel disease: a pilot study. Minerva Medica. 2019;110:95-100. doi:10.23736/S0026-4806.18.05787-7
42. Szymanska E., Wierzbicka A., Dadalski M., Kierkus J. Clinical Medicine Fecal Zonulin as a Noninvasive Biomarker of Intestinal Permeability in Pediatric Patients with Inflammatory Bowel Diseases-Correlation with Disease Activity and Fecal Calprotectin 2021. doi:10.3390/jcm10173905
43. De Munck T. J.I., Xu P., Verwijs H. J.A., et al.Intestinal permeability in human nonalcoholic fatty liver disease: A systematic review and meta-analysis. Liver Int. 2020;40(12):2906-2916. doi:10.1111/liv.14696
44. Pacifico L., Romaggioli S., Bascetta S., Chiesa C., Bonci E., Marandola L. CASE CONTROL STUDY Increased circulating zonulin in children with biopsy-proven nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20:17107-14. doi:10.3748/wjg.v20.i45.17107
45. Kim A-S., Ko H-J. Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy Dovepress Plasma concentrations of zonulin are elevated in obese men with fatty liver disease. Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy. 2018;11:149-157. doi:10.2147/DMSO.S163062
46. Zahorska-Markiewicz B., Janowska J., Olszanecka-Glinianowicz M., Zurakowski A. Serum concentrations of TNF-α and soluble TNF-α receptors in obesity.International Journal of Obesity. 2000;24:1392-5. doi:10.1038/sj.ijo.0801398
47. Olszanecka-Glinianowicz M., Zahorska-Markiewicz B., Janowska J., Zurakowski A. Serum concentrations of nitric oxide, tumor necrosis factor (TNF)-α and TNF soluble receptors in women with overweight and obesity. Metabolism: Clinical and Experimental. 2004;53:1268-73. doi:10.1016/j.metabol.2004.07.001
48. Olszanecka-Glinianowicz M., Chudek J., Kocełak P., Szromek A., Zahorska-Markiewicz B. Body fat changes and activity of tumor necrosis factor α system-a 5-year follow-up study. Metabolism: Clinical and Experimental. 2011;60:531-6. doi:10.1016/j.metabol.2010.04.023
49. Zak-Gołąb A., Kocełak P., Aptekorz M., Zientara M., Juszczyk L., Martirosian G., et al. Gut microbiota, microinflammation, metabolic profile, and zonulin concentration in obese and normal weight subjects.International Journal of Endocrinology. 2013;2013:674106. doi:10.1155/2013/674106
50. Mokkala K., Röytiö H., Munukka E., Pietilä S., Ekblad U., Rönnemaa T., et al. Gut Microbiota Richness and Composition and Dietary Intake of Overweight Pregnant Women Are Related to Serum Zonulin Concentration, a Marker for Intestinal Permeability. The Journal of Nutrition. 2016;146:1694-700. doi:10.3945/jn.116.235358
51. Stenman L.K., Lehtinen M. J., Meland N., Christensen J. E., Yeung N., Saarinen M. T., et al. Probiotic With or Without Fiber Controls Body Fat Mass, Associated With Serum Zonulin, in Overweight and Obese Adults-Randomized Controlled Trial. EBioMedicine. 2016;13:190-200. doi:10.1016/j.ebiom.2016.10.036
52. Küme T., Acar S., Tuhan H., Çatlı G., Anık A., Gürsoy Çalan Ö., et al. The Relationship between Serum Zonulin Level and Clinical and Laboratory Parameters of Childhood Obesity. Journal of Clinical Research in Pediatric Endocrinology. 2017;9:31-8. doi:10.4274/jcrpe.3682
53. Houttu N., Mokkala K., Laitinen K. Overweight and obesity status in pregnant women are related to intestinal microbiota and serum metabolic and inflammatory profiles. Clinical Nutrition. 2018;37:1955-66. doi:10.1016/j.clnu.2017.12.013
54. Mörkl S., Lackner S., Meinitzer A., Mangge H., Lehofer M., Halwachs B., et al. Gut microbiota, dietary intakes and intestinal permeability reflected by serum zonulin in women. European Journal of Nutrition. 2018;57:2985-97. doi:10.1007/s00394-018-1784-0
55. Janczy A., Aleksandrowicz-Wrona E., Kochan Z., Małgorzewicz S. Impact of diet and synbiotics on selected gut bacteria and intestinal permeability in individuals with excess body weight - A Prospective, Randomized Study. Acta Biochimica Polonica. 2020;67:571-8. doi:10.18388/abp.2020_5443
56. Zhang D., Zhang L., Yue F., Zheng Y., Russell R. Serum zonulin is elevated in women with polycystic ovary syndrome and correlates with insulin resistance and severity of anovulation. European Journal of Endocrinology. 2015;172:29-36. doi:10.1530/EJE-14-0589
57. Cetin Z., Kosem A., Can B., Baser O., Catak M., Turhan T., et al. Serum zonulin level is not elevated in patients with polycystic ovary syndrome without metabolic syndrome. Archives of Gynecology and Obstetrics. 2019;300:1785-90. doi:10.1007/s00404-019-05345-z
58. Lingaiah S., Arffman R. K., Morin-Papunen L., Tapanainen J. S., Piltonen T. Markers of gastrointestinal permeability and dysbiosis in premenopausal women with PCOS: a case-control study. BMJ Open. 2021;11: e045324. doi:10.1136/bmjopen-2020-045324
59. Camilleri M., Gorman H.Intestinal permeability and irritable bowel syndrome. Neurogastroenterology and Motility. 2007;19:545-52. doi:10.1111/j.1365-2982.2007.00925.x
60. Kim J.A., Choi S. C., Yun K. J., Kim D. K., Han M. K., Seo G. S., et al. Expression of protease-activated receptor 2 in ulcerative colitis. Inflammatory Bowel Diseases. 2003;9:224-9. doi:10.1097/00054725-200307000-00002
61. Bueno L. Protease activated receptor 2: a new target for IBS treatment. European Review for Medical and Pharmacological Sciences. 2008;12 Suppl 1:95-102.
62. Gecse K., Róka R., Ferrier L., Leveque M., Eutamene H., Cartier C., et al. Increased faecal serine protease activity in diarrhoeic IBS patients: a colonic lumenal factor impairing colonic permeability and sensitivity. Gut. 2008;57:591-8. doi:10.1136/GUT.2007.140210
63. Singh P., Silvester J., Chen X., Xu H., Sawhney V., Rangan V., et al. Serum zonulin is elevated in IBS and correlates with stool frequency in IBS-D. United European Gastroenterology Journal. 2019;7:709-15. doi:10.1177/2050640619826419
64. Korpe P.S., Petri W. A. Environmental Enteropathy: Critical implications of a poorly understood condition. Trends Mol Med. 2012;18(6):328-336. doi:10.1016/j.molmed.2012.04.007
65. Prendergast A., Kelly P. Enteropathies in the Developing World: Neglected Effects on Global Health. The American Journal of Tropical Medicine and Hygiene. 2012;86:756. doi:10.4269/AJTMH.2012.11-0743
66. Keusch G.T., Rosenberg I. H., Denno D. M., Duggan C., Guerrant R. L., Lavery J. V., et al. Implications of Acquired Environmental Enteric Dysfunction for Growth and Stunting in Infants and Children Living in Low- and Middle-Income Countries. Food and Nutrition Bulletin. 2013;34:357-64. doi:10.1177/156482651303400308
67. Guerrant R.L., Leite A. M., Pinkerton R., Medeiros PHQS, Cavalcante P. A., Deboer M., et al. Biomarkers of Environmental Enteropathy, Inflammation, Stunting, and Impaired Growth in Children in Northeast Brazil. PLoS One. 2016;11(9): e0158772. Published 2016 Sep 30. doi:10.1371/journal.pone.0158772
68. Shiou S.R., Yu Y., Chen S., Ciancio M. J., Petrof E. O., Sun J., et al. Erythropoietin Protects Intestinal Epithelial Barrier Function and Lowers the Incidence of Experimental Neonatal Necrotizing Enterocolitis. The Journal of Biological Chemistry. 2011;286:12123. doi:10.1074/JBC.M110.154625
69. Högberg N., Stenbäck A., Carlsson P. O., Wanders A., Lilja H. E. Genes regulating tight junctions and cell adhesion are altered in early experimental necrotizing enterocolitis. Journal of Pediatric Surgery. 2013;48:2308-12. doi:10.1016/j.jpedsurg.2013.06.027
70. Bergmann K.R., Liu S. X.L., Tian R., Kushnir A., Turner J. R., Li H. L., et al. Bifidobacteria Stabilize Claudins at Tight Junctions and Prevent Intestinal Barrier Dysfunction in Mouse Necrotizing Enterocolitis. The American Journal of Pathology. 2013;182:1595. doi:10.1016/J.AJPATH.2013.01.013
71. Clark J.A., Doelle S. M., Halpern M. D., Saunders T. A., Holubec H., Dvorak K., et al.Intestinal barrier failure during experimental necrotizing enterocolitis: protective effect of EGF treatment. American Journal of Physiology Gastrointestinal and Liver Physiology. 2006;291. doi:10.1152/AJPGI.00090.2006
72. Ling X., Linglong P., Weixia D., Hong W. Protective Effects of Bifidobacterium on Intestinal Barrier Function in LPS-Induced Enterocyte Barrier Injury of Caco-2 Monolayers and in a Rat NEC Model. PLoS One. 2016;11(8): e0161635. Published 2016 Aug 23. doi:10.1371/journal.pone.0161635
73. Tarko A., Suchojad A., Michalec M., Majcherczyk M., Brzozowska A., Maruniak-Chudek I. Zonulin: A Potential Marker of Intestine Injury in Newborns. Dis Markers. 2017;2017:2413437. doi:10.1155/2017/2413437
74. Carratù R., Secondulfo M., de Magistris L., Iafusco D., Urio A., Carbone M. G., et al. Altered intestinal permeability to mannitol in diabetes mellitus type I. Journal of Pediatric Gastroenterology and Nutrition. 1999;28:264-9. doi:10.1097/00005176-199903000-00010
75. Meddings J.B., Jarand J., Urbanski S. J., Hardin J., Gall D. G. Increased gastrointestinal permeability is an early lesion in the spontaneously diabetic BB rat. American Journal of Physiology-Gastrointestinal and Liver Physiology. 1999;276: G951-7. doi:10.1152/ajpgi.1999.276.4.G951
76. Watts T., Berti I., Sapone A., Gerarduzzi T., Not T., Zielke R., et al. Role of the intestinal tight junction modulator zonulin in the pathogenesis of type I diabetes in BB diabetic-prone rats. Proceedings of the National Academy of Sciences. 2005;102:2916-21. doi:10.1073/pnas.0500178102
77. Sapone A., de Magistris L., Pietzak M., Clemente M. G., Tripathi A., Cucca F., et al. Zonulin Upregulation Is Associated With Increased Gut Permeability in Subjects With Type 1 Diabetes and Their Relatives. Diabetes. 2006;55:1443-9. doi:10.2337/DB05-1593
78. Ho J., Nicolucci A. C., Virtanen H., Schick A., Meddings J., Reimer R. A., et al. Effect of Prebiotic on Microbiota, Intestinal Permeability, and Glycemic Control in Children With Type 1 Diabetes. 2019. doi:10.1210/jc.2019-00481
79. Rittirsch D., Flierl M. A., Nadeau B. A., Day D. E., Huber-Lang M.S., Grailer J. J., et al. Zonulin as prehaptoglobin2 regulates lung permeability and activates the complement system. American Journal of Physiology - Lung Cellular and Molecular Physiology. 2013;304: L863. doi:10.1152/AJPLUNG.00196.2012
80. Benard A., Desreumeaux P., Huglo D., Hoorelbeke A., Tonnel A. B., Wallaert B. Increased intestinal permeability in bronchial asthma. Journal of Allergy and Clinical Immunology. 1996;97:1173-8. doi:10.1016/S0091-6749(96)70181-1
81. Hijazi Z., Molla A. M., Al-Habashi H., Muawad W. M., Molla A. M., Sharma P. N.Intestinal permeability is increased in bronchial asthma. Arch Dis Child. 2004;89(3):227-229. doi:10.1136/adc.2003.027680
82. Fasano A. Zonulin and its regulation of intestinal barrier function: the biological door to inflammation, autoimmunity, and cancer. Physiological Reviews. 2011;91:151-75. doi:10.1152/physrev.00003.2008
83. Baioumy S.A., Elgendy A., Ibrahim S. M., Taha S. I., Fouad S. H. Association between serum zonulin level and severity of house dust mite allergic asthma. Allergy Asthma Clin Immunol. 2021;17:86. doi:10.1186/s13223-021-00586-7
84. Dirajlal-Fargo S., El-Kamari V., Weiner L., Shan L., Sattar A., Kulkarni M., et al. Altered Intestinal Permeability and Fungal Translocation in Ugandan Children With Human Immunodeficiency Virus. Clinical Infectious Diseases. 2020;70:2413-22. doi:10.1093/cid/ciz561
85. Pastor L., Langhorst J., Schröder D., Casellas A., Ruffer A., Carrillo J., et al. Different pattern of stool and plasma gastrointestinal damage biomarkers during primary and chronic HIV infection. Plos ONE. 2019;14: e0218000. doi:10.1371/journal.pone.0218000
86. Deeks S.G., Tracy R., Douek D. C. Systemic Effects of Inflammation on Health during Chronic HIV Infection. Immunity. 2013;39:633. doi:10.1016/J.IMMUNI.2013.10.001
87. Hunt P.W., Sinclair E., Rodriguez B., Shive C., Clagett B., Funderburg N., et al. Gut Epithelial Barrier Dysfunction and Innate Immune Activation Predict Mortality in Treated HIV Infection. The Journal of Infectious Diseases. 2014;210:1228-38. doi:10.1093/infdis/jiu238
88. Shirey K.A., Lai W., Patel M. C., Pletneva L. M., Pang C., Kurt-Jones E., et al. Novel Strategies for Targeting Innate Immune Responses to Influenza HHS Public Access. Mucosal Immunol. 2016;9:1173-82. doi:10.1038/mi.2015.141
89. Oliva A., Cammisotto V., Cangemi R., Ferro D., Miele M. C., de Angelis M., et al. Low-Grade Endotoxemia and Thrombosis in COVID-19. Clinical and Translational Gastroenterology. 2021;12: e00348. doi:10.14309/CTG.0000000000000348
90. di Micco S., Musella S., Scala M. C., Sala M., Campiglia P., Bifulco G., et al. In silico Analysis Revealed Potential Anti-SARS-CoV-2 Main Protease Activity by the Zonulin Inhibitor Larazotide Acetate. Frontiers in Chemistry. 2020;8:628609. doi:10.3389/fchem.2020.628609
91. di Micco S., Musella S., Sala M., Scala M. C., Andrei G., Snoeck R., et al. Peptide Derivatives of the Zonulin Inhibitor Larazotide (AT1001) as Potential Anti SARS-CoV-2: Molecular Modelling, Synthesis and Bioactivity Evaluation.International Journal of Molecular Sciences. 2021;22:9427. doi:10.3390/ijms22179427
92. Serek P., Oleksy-Wawrzyniak M. The Effect of Bacterial Infections, Probiotics and Zonulin on Intestinal Barrier Integrity.International Journal of Molecular Sciences. 2021;22:11359. doi:10.3390/ijms222111359
93. Li C., Gao M., Zhang W., Chen C., Zhou F., Hu Z., et al. Zonulin Regulates Intestinal Permeability and Facilitates Enteric Bacteria Permeation in Coronary Artery Disease. Scientific Reports. 2016;6:29142. doi:10.1038/srep29142
94. Sanchez-Alcoholado L., Castellano-Castillo D., Jordán-Martínez L., Moreno-Indias I., Cardila-Cruz P., Elena D., et al. Role of Gut Microbiota on Cardio-Metabolic Parameters and Immunity in Coronary Artery Disease Patients with and without Type-2 Diabetes Mellitus. Frontiers in Microbiology. 2017;8:1936. doi:10.3389/fmicb.2017.01936
95. Fasano A. Zonulin and its regulation of intestinal barrier function: the biological door to inflammation, autoimmunity, and cancer. Physiological Reviews. 2011;91:151-75. doi:10.1152/physrev.00003.2008
96. Nouri M., Bredberg A., Weström B., Lavasani S.Intestinal barrier dysfunction develops at the onset of experimental autoimmune encephalomyelitis, and can be induced by adoptive transfer of auto-reactive T cells. PloS One. 2014;9: e106335. doi:10.1371/journal.pone.0106335
97. Camara-Lemarroy C.R., Silva C., Greenfield J., Liu W. Q., Metz L. M., Yong V. W. Biomarkers of intestinal barrier function in multiple sclerosis are associated with disease activity. Multiple Sclerosis Journal. 2020;26:1340-50. doi:10.1177/1352458519863133
98. Papa Pellizoni F., Zazeri Leite A., de Campos Rodrigues N., Jordão Ubaiz M., Ignácio Gonzaga M., Naomi Campos Takaoka N., et al. Detection of Dysbiosis and Increased Intestinal Permeability in Brazilian Patients with Relapsing-Remitting Multiple Sclerosis. Public Health. 2021;18:4621. doi:10.3390/ijerph18094621
99. Costello M.E., Ciccia F., Willner D., Warrington N., Robinson P. C., Gardiner B., et al. Brief Report: Intestinal dysbiosis in ankylosing spondylitis. Arthritis and Rheumatology. 2015;67:686-91. doi:10.1002/ART.38967/FORMAT/PDF
100. Tito R.Y., Cypers H., Joossens M., Varkas G., van Praet L., Glorieus E., et al. Brief Report: Dialister as a Microbial Marker of Disease Activity in Spondyloarthritis. Arthritis and Rheumatology. 2017;69:114-21. doi:10.1002/ART.39802/FORMAT/PDF
101. Ciccia F., Guggino G., Rizzo A., Alessandro R., Luchetti M. M., Milling S., et al. Dysbiosis and zonulin upregulation alter gut epithelial and vascular barriers in patients with ankylosing spondylitis. Annals of the Rheumatic Diseases. 2017;76:1123-32. doi:10.1136/annrheumdis-2016-210000
102. Wang X., Li M-M., Niu Y., Zhang X., Yin J-B., Zhao C-J., et al. Serum Zonulin in HBV-Associated Chronic Hepatitis, Liver Cirrhosis, and Hepatocellular Carcinoma. Disease Markers. 2019;2019:5945721. doi:10.1155/2019/5945721
103. Skardelly M., Armbruster F. P., Meixensberger J., Hilbig H. Expression of Zonulin, c-kit, and Glial Fibrillary Acidic Protein in Human Gliomas. Translational Oncology. 2009;2:117-20. doi:10.1593/tlo.09115
104. Díaz-Coránguez M., Segovia J., López-Ornelas A., Puerta-Guardo H., Ludert J., Chávez B., et al. Transmigration of Neural Stem Cells across the Blood Brain Barrier Induced by Glioma Cells. PLoS ONE. 2013;8: e60655. doi:10.1371/journal.pone.0060655
105. Maes M., Sirivichayakul S., Kanchanatawan B., Vodjani A. Upregulation of the Intestinal Paracellular Pathway with Breakdown of Tight and Adherens Junctions in Deficit Schizophrenia. Molecular Neurobiology. 2019;56:7056-73. doi:10.1007/s12035-019-1578-2
106. Barber G.S., Sturgeon C., Fasano A., Cascella N. G., Eaton W. W., McMahon R.P., et al. Elevated zonulin, a measure of tight-junction permeability, may be implicated in schizophrenia. Schizophrenia Research. 2019;211:111-2. doi:10.1016/j.schres.2019.07.006
107. Usta A., Kılıç F., Demirdaş A., Işık Ü., Doğuç D. K., Bozkurt M. Serum zonulin and claudin-5 levels in patients with schizophrenia. European Archives of Psychiatry and Clinical Neuroscience. 2021;271:767-73. doi:10.1007/s00406-020-01152-9
108. Esnafoglu E., Cırrık S., Ayyıldız S. N., Erdil A., Ertürk E. Y., Daglı A., et al. Increased Serum Zonulin Levels as an Intestinal Permeability Marker in Autistic Subjects. The Journal of Pediatrics. 2017;188:240-4. doi:10.1016/j.jpeds.2017.04.004
109. Rose D.R., Yang H., Serena G., Sturgeon C., Ma B., Careaga M., et al. Differential immune responses and microbiota profiles in children with autism spectrum disorders and co-morbid gastrointestinal symptoms HHS Public Access. Brain Behav Immun. 2018;70:354-68. doi:10.1016/j.bbi.2018.03.025
110. Karagözlü S., Dalgıç B., İşeri E. The Relationship of Severity of Autism with Gastrointestinal Symptoms and Serum Zonulin Levels in Autistic Children. Journal of Autism and Developmental Disorders. 2021. doi:10.1007/s10803-021-04966-1
111. Stevens B.R., Goel R., Seungbum K., Richards E. M., Holbert R. C., Pepine C. J., et al. Increased human intestinal barrier permeability plasma biomarkers zonulin and FABP2 correlated with plasma LPS and altered gut microbiome in anxiety or depression HHS Public Access. Gut. 2018;67:1555-7. doi:10.1136/gutjnl-2017-314759
112. Alvarez-Mon M.A., Gómez A. M., Orozco A., Lahera G., Sosa M. D., Diaz D., et al. Abnormal Distribution and Function of Circulating Monocytes and Enhanced Bacterial Translocation in Major Depressive Disorder. Frontiers in Psychiatry. 2019;10:812. doi:10.3389/fpsyt.2019.00812
113. Klaus D.A., Motal M. C., Burger-Klepp U., Marschalek C., Schmidt E. M., Lebherz-Eichinger D., et al. Increased plasma zonulin in patients with sepsis. Biochemia Medica. 2013;23:107-11. doi:10.11613/bm.2013.013
114. Liu Z., Li C., Huang M., Tong C., Zhang X., Wang L., et al. Positive regulatory effects of perioperative probiotic treatment on postoperative liver complications after colorectal liver metastases surgery: a double-center and double-blind randomized clinical trial. BMC Gastroenterology. 2015;15:34. doi:10.1186/s12876-015-0260-z
Рецензия
Для цитирования:
Халаиджева К.Н., Дроздов В.Н., Ших Е.В., Лазебник Л.Б. Зонулин-регулируемая барьерная функция кишечника и полиморбидность. Экспериментальная и клиническая гастроэнтерология. 2022;(2):111-120. https://doi.org/10.31146/1682-8658-ecg-198-2-111-120
For citation:
Khalaidzheva K.N., Drozdov V.N., Shikh E.V., Lazebnik L.B. Zonulin-regulated intestinal barrier function and multymorbidity. Experimental and Clinical Gastroenterology. 2022;(2):111-120. (In Russ.) https://doi.org/10.31146/1682-8658-ecg-198-2-111-120
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