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Barone, M.V.;  Auricchio, R.;  Nanayakkara, M.;  Greco, L.;  Troncone, R.;  Auricchio, S. Pivotal Role of Inflammation in Celiac Disease. Encyclopedia. Available online: https://encyclopedia.pub/entry/25277 (accessed on 20 June 2024).
Barone MV,  Auricchio R,  Nanayakkara M,  Greco L,  Troncone R,  Auricchio S. Pivotal Role of Inflammation in Celiac Disease. Encyclopedia. Available at: https://encyclopedia.pub/entry/25277. Accessed June 20, 2024.
Barone, Maria Vittoria, Renata Auricchio, Merlin Nanayakkara, Luigi Greco, Riccardo Troncone, Salvatore Auricchio. "Pivotal Role of Inflammation in Celiac Disease" Encyclopedia, https://encyclopedia.pub/entry/25277 (accessed June 20, 2024).
Barone, M.V.,  Auricchio, R.,  Nanayakkara, M.,  Greco, L.,  Troncone, R., & Auricchio, S. (2022, July 19). Pivotal Role of Inflammation in Celiac Disease. In Encyclopedia. https://encyclopedia.pub/entry/25277
Barone, Maria Vittoria, et al. "Pivotal Role of Inflammation in Celiac Disease." Encyclopedia. Web. 19 July, 2022.
Pivotal Role of Inflammation in Celiac Disease
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Celiac disease (CD) is an immune mediate disease characterised by gluten dependent T-cell mediated activation, autoimmunity and derangement of the intestinal mucosa in a specific genetic background. Although the activation of the T-cells has been studied in dept, the central question remains still unanswered, namely, why a pro-inflammatory T cell response to gluten is generated instead of a regulatory response, which normally promotes oral tolerance to dietary protein antigens. There is an inflamed environment in CD intestine, enriched in cytokines, such as IL-15, or type I interferons, in which T cells tend to acquire a pro- inflammatory phenotype. The factors that create a pro-inflammatory environment in the CD intestine, leading to an expansion of gliadin-specific T cells in genetically susceptible individuals and further shifting them towards a pro-inflammatory phenotype, remain to be identified. Gluten exacerbates these constitutive alterations, by increasing the same markers already altered before the gluten introduction, both in vitro and in vivo. All these new observations add this disease tout court” to the big family of increasing chronic inflammatory diseases where nutrients can have pro-inflammatory or anti-inflammatory effects, directly or indirectly mediated by the intestinal microbiota, where the intestine functions as a cross road for the control of the inflammation both local and at distance.

celiac disease gluten inflammation microbiota

1. Celiac Disease as an Inflammatory Chronic Disease

The recent literature describes in celiac disease (CD) a meeting of several different factors such as cellular vulnerability, pro-inflammatory effects of gluten and other wheat proteins, Western diet, and other environmental triggers such as viruses that prepare and/or amplify the T cell-mediated response to gluten. The factors that create a pro-inflammatory environment in the CD intestines, leading to an expansion of gliadin-specific T cells in genetically susceptible individuals and further shifting them toward a pro-inflammatory phenotype, could have multiple origins: the pro-inflammatory environment (exogenous stimuli), such as diet, viruses and other pro-inflammatory factors; and the constitutive cellular alterations (endogenous predisposition) that by themselves induce and/or render the cells more sensitive to pro-inflammatory stimuli. All these factors, both exogenous and endogenous, can contribute to the generation of “sterile” inflammation in CD (Figure 1). 
Figure 1. Both exogenous and endogenous factors can generate low-grade chronic inflammation in CD, initiating a series of events that will eventually induce an intestinal lesion.

2. Endogenous Alterations in CD Independent of Gluten

Endogenous alterations, defining a celiac cellular phenotype, have been described in different tissues and cells from CD patients, including intestinal organoids [1]. Gluten exacerbates these constitutive alterations by increasing the same markers already altered in the absence of gluten, both in vitro and in vivo. This phenotype confers the vulnerability to the CD cells to several different triggers that have effects on different pathways, including innate immunity activation. Many of these constitutive alterations are now regarded as biomarkers of clinical relevance, as they can be used to intervene in the “at risk” population before the onset of the disease [1][2].
The recent literature is starting to address the question of endogenous alterations, independent of gluten, in CD by in vivo studies and in cellular models. From these studies, it clearly appears that subtle alterations of the CD cells are also present in the absence of gluten as well as in the absence of T cell activation.
There are many literatures including the population studies, such as patients at risk of CD, CD patients with GFD–CD (gluten-free diet–celiac disease) and in vitro studies on biopsies, intestinal organoids and CD cells from compartments different from the intestines (Table 1).
Table 1. Endogenous, constitutive alterations of several pathways have been described in different cellular models of CD. Most of these endogenous alterations can predispose one to inflammation. Some of these constitutive alterations can be regarded as biomarkers of CD. CD: celiac disease; Wnt: Wingless and Int 1; NFkB: nuclear factor kappa-light-chain-enhancer of activated B cells; EGFR: epithelial growth factor receptor; ERK: extracellular signal-regulated kinases; ECM: extracellular matrix; pNFkB: phosphorylated (active) form of NFkB; pERK: phosphorylated (active) form of ERK; IL1 beta: interleukin beta 1; IL6: interleukin 6; LPP: lipoma-preferred partner; IL15: interleukin 15; IL15R alpha: IL15 receptor alpha; tTg: tissue transglutaminase.

References

  1. Porpora, M.; Conte, M.; Lania, G.; Bellomo, C.; Rapacciuolo, L.; Chirdo, F.G.; Auricchio, R.; Troncone, R.; Auricchio, S.; Barone, M.V.; et al. Inflammation Is Present, Persistent and More Sensitive to Proinflammatory Triggers in Celiac Disease Enterocytes. Int. J. Mol. Sci. 2022, 23, 1973.
  2. Auricchio, R.; Troncone, R. Can Celiac Disease Be Prevented? Front. Immunol. 2021, 12, 672148.
  3. Auricchio, R.; Galatola, M.; Cielo, D.; Amoresano, A.; Caterino, M.; De Vita, E.; Illiano, A.; Troncone, R.; Greco, L.; Ruoppolo, M. A Phospholipid Profile at 4 Months Predicts the Onset of Celiac Disease in at-Risk Infants. Sci. Rep. 2019, 9, 14303.
  4. Sen, P.; Carlsson, C.; Virtanen, S.M.; Simell, S.; Hyöty, H.; Ilonen, J.; Toppari, J.; Veijola, R.; Hyötyläinen, T.; Knip, M.; et al. Persistent Alterations in Plasma Lipid Profiles Before Introduction of Gluten in the Diet Associated with Progression to Celiac Disease. Clin. Transl. Gastroenterol. 2019, 10, 1–10.
  5. Auricchio, R.; Stellato, P.; Bruzzese, D.; Cielo, D.; Chiurazzi, A.; Galatola, M.; Castilljeo, G.; Crespo Escobar, P.; Gyimesi, J.; Hartman, C.; et al. Growth rate of coeliac children is compromised before the onset of the disease. Arch. Dis. Child. 2020, 105, 964–968.
  6. Auricchio, R.; Calabrese, I.; Galatola, M.; Cielo, D.; Carbone, F.; Mancuso, M.; Matarese, G.; Troncone, R.; Auricchio, S.; Greco, L. Author Correction: Gluten consumption and inflammation affect the development of celiac disease in at-risk children. Sci. Rep. 2022, 12, 8157.
  7. Galatola, M.; Cielo, D.; Panico, C.; Stellato, P.; Malamisura, B.; Carbone, L.; Gianfrani, C.; Troncone, R.; Greco, L.; Auricchio, R. Presymptomatic Diagnosis of Celiac Disease in Predisposed Children: The Role of Gene Expression Profile. J. Pediatr. Gastroenterol. Nutr. 2017, 65, 314–320.
  8. Olivares, M.; Walker, A.W.; Capilla, A.; Benítez-Páez, A.; Palau, F.; Parkhill, J.; Castillejo, G.; Sanz, Y. Gut microbiota trajectory in early life may predict development of celiac disease. Microbiome 2018, 6, 36.
  9. Dotsenko, V.; Oittinen, M.; Taavela, J.; Popp, A.; Peräaho, M.; Staff, S.; Sarin, J.; Leon, F.; Isola, J.; Mäki, M.; et al. Genome-Wide Transcriptomic Analysis of Intestinal Mucosa in Celiac Disease Patients on a Gluten-Free Diet and Postgluten Challenge. Cell. Mol. Gastroenterol. Hepatol. 2021, 11, 13–32.
  10. Stamnaes, J.; Stray, D.; Stensland, M.; Sarna, V.K.; Nyman, T.A.; Lundin, K.E.A.; Sollid, L.M. Quantitative proteomics of coeliac gut during 14-day gluten challenge: Low-level baseline inflammation despite clinical and histological normality predicts subsequent response. medRxiv 2020.
  11. Stamnaes, J.; Stray, D.; Stensland, M.; Sarna, V.K.; Nyman, T.A.; Lundin, K.E.A.; Sollid, L.M. In Well-Treated Celiac Patients Low-Level Mucosal Inflammation Predicts Response to 14-day Gluten Challenge. Adv. Sci. 2021, 8, 2003526.
  12. Trynka, G.; Zhernakova, A.; Romanos, J.; Franke, L.; Hunt, K.A.; Turner, G.; Bruinenberg, M.; Heap, G.A.; Platteel, M.; Ryan, A.W.; et al. Coeliac disease-associated risk variants in TNFAIP3 and REL implicate altered NF-kappaB signalling. Gut 2009, 58, 1078–1083.
  13. Fernandez-Jimenez, N.; Castellanos-Rubio, A.; Plaza-Izurieta, L.; Irastorza, I.; Elcoroaristizabal, X.; Jauregi-Miguel, A.; Lopez-Euba, T.; Tutau, C.; de Pancorbo, M.M.; Vitoria, J.C.; et al. Coregulation and modulation of NFκB-related genes in celiac disease: Uncovered aspects of gut mucosal inflammation. Hum. Mol. Genet. 2014, 23, 1298–1310.
  14. Castellanos-Rubio, A.; Bilbao, J.R. Profiling Celiac Disease-Related Transcriptional Changes. Int. Rev. Cell. Mol. Biol. 2018, 336, 149–174.
  15. Castellanos-Rubio, A.; Ghosh, S. Disease-Associated SNPs in Inflammation-Related lncRNAs. Front. Immunol. 2019, 10, 420.
  16. Jabri, B.; Sollid, L.M. Mechanisms of disease: Immunopathogenesis of celiac disease. Nat. Clin. Pract. Gastroenterol. Hepatol. 2006, 3, 516–525.
  17. Sziksz, E.; Veres, G.; Vannay, A.; Prókai, A.; Gál, K.; Onody, A.; Korponay-Szabó, I.R.; Reusz, G.; Szabó, A.; Tulassay, T.; et al. Increased heat shock protein 72 expression in celiac disease. J. Pediatr. Gastroenterol. Nutr. 2010, 51, 573–578.
  18. Abadie, V.; Jabri, B. IL-15: A central regulator of celiac disease immunopathology. Immunol. Rev. 2014, 260, 221–234.
  19. Bernardo, D.; Garrote, J.A.; Allegretti, Y.; León, A.; Gómez, E.; Bermejo-Martin, J.F.; Calvo, C.; Riestra, S.; Fernández-Salazar, L.; Blanco-Quirós, A.; et al. Higher constitutive IL15R alpha expression and lower IL-15 response threshold in coeliac disease patients. Clin. Exp. Immunol. 2008, 154, 64–73.
  20. Nanayakkara, M.; Lania, G.; Maglio, M.; Auricchio, R.; De Musis, C.; Discepolo, V.; Miele, E.; Jabri, B.; Troncone, R.; Auricchio, S.; et al. P31-43, an undigested gliadin peptide, mimics and enhances the innate immune response to viruses and interferes with endocytic trafficking: A role in celiac disease. Sci. Rep. 2018, 8, 10821.
  21. Allard-Chamard, H.; Mishra, H.K.; Nandi, M.; Mayhue, M.; Menendez, A.; Ilangumaran, S.; Ramanathan, S. Interleukin-15 in autoimmunity. Cytokine 2020, 136, 155258.
  22. Abadie, V.; Kim, S.M.; Lejeune, T.; Palanski, B.A.; Ernest, J.D.; Tastet, O.; Voisine, J.; Discepolo, V.; Marietta, E.V.; Hawash, M.B.F.; et al. IL-15, gluten and HLA-DQ8 drive tissue destruction in coeliac disease. Nature 2020, 578, 600–604.
  23. Lania, G.; Nanayakkara, M.; Maglio, M.; Auricchio, R.; Porpora, M.; Conte, M.; De Matteis, M.A.; Rizzo, R.; Luini, A.; Discepolo, V.; et al. Constitutive alterations in vesicular trafficking increase the sensitivity of cells from celiac disease patients to gliadin. Commun. Biol. 2019, 2, 190.
  24. Barone, M.V.; Troncone, R.; Auricchio, S. Gliadin peptides as triggers of the proliferative and stress/innate immune response of the celiac small intestinal mucosa. Int. J. Mol. Sci. 2014, 15, 20518–20537.
  25. Juuti-Uusitalo, K.; Mäki, M.; Kainulainen, H.; Isola, J.; Kaukinen, K. Gluten affects epithelial differentiation-associated genes in small intestinal mucosa of coeliac patients. Clin. Exp. Immunol. 2007, 150, 294–305.
  26. Nanayakkara, M.; Lania, G.; Maglio, M.; Kosova, R.; Sarno, M.; Gaito, A.; Discepolo, V.; Troncone, R.; Auricchio, S.; Auricchio, R.; et al. Enterocyte proliferation and signaling are constitutively altered in celiac disease. PLoS ONE 2013, 8, e76006.
  27. Thorburn, A.N.; Macia, L.; Mackay, C.R. Diet, metabolites, and “western-lifestyle” inflammatory diseases. Immunity 2014, 40, 833–842.
  28. Bjarnason, I.; Marsh, M.N.; Price, A.; Levi, A.J.; Peters, T.J. Intestinal permeability in patients with coeliac disease and dermatitis herpetiformis. Gut 1985, 26, 1214–1219.
  29. Bjarnason, I.; Peters, T.J. In vitro determination of small intestinal permeability: Demonstration of a persistent defect in patients with coeliac disease. Gut 1984, 25, 145–150.
  30. Ciccocioppo, R.; Finamore, A.; Ara, C.; Di Sabatino, A.; Mengheri, E.; Corazza, G.R. Altered expression, localization, and phosphorylation of epithelial junctional proteins in celiac disease. Am. J. Clin. Pathol. 2006, 125, 502–511.
  31. Schulzke, J.D.; Bentzel, C.J.; Schulzke, I.; Riecken, E.O.; Fromm, M. Epithelial tight junction structure in the jejunum of children with acute and treated celiac sprue. Pediatr. Res. 1998, 43, 435–441.
  32. Jauregi-Miguel, A.; Fernandez-Jimenez, N.; Irastorza, I.; Plaza-Izurieta, L.; Vitoria, J.C.; Bilbao, J.R. Alteration of tight junction gene expression in celiac disease. J. Pediatr. Gastroenterol. Nutr. 2014, 58, 762–767.
  33. Freire, R.; Ingano, L.; Serena, G.; Cetinbas, M.; Anselmo, A.; Sapone, A.; Sadreyev, R.I.; Fasano, A.; Senger, S. Human gut derived-organoids provide model to study gluten response and effects of microbiota-derived molecules in celiac disease. Sci. Rep. 2019, 9, 7029.
  34. Dieterich, W.; Neurath, M.F.; Zopf, Y. Intestinal ex vivo organoid culture reveals altered programmed crypt stem cells in patients with celiac disease. Sci. Rep. 2020, 10, 3535.
  35. Nanayakkara, M.; Kosova, R.; Lania, G.; Sarno, M.; Gaito, A.; Galatola, M.; Greco, L.; Cuomo, M.; Troncone, R.; Auricchio, S.; et al. A celiac cellular phenotype, with altered LPP sub-cellular distribution, is inducible in controls by the toxic gliadin peptide P31-43. PLoS ONE 2013, 8, e79763.
  36. Paolella, G.; Nanayakkara, M.; Sposito, S.; Lepretti, M.; Auricchio, S.; Esposito, C.; Barone, M.V.; Martucciello, S.; Caputo, I. Constitutive Differential Features of Type 2 Transglutaminase in Cells Derived from Celiac Patients and from Healthy Subjects. Int. J. Mol. Sci. 2020, 21, 1231.
  37. Discepolo, V.; Lania, G.; Ten Eikelder, M.L.G.; Nanayakkara, M.; Sepe, L.; Tufano, R.; Troncone, R.; Auricchio, S.; Auricchio, R.; Paolella, G.; et al. Pediatric Celiac Disease Patients Show Alterations of Dendritic Cell Shape and Actin Rearrangement. Int. J. Mol. Sci. 2021, 22, 2708.
  38. Vriezinga, S.L.; Auricchio, R.; Bravi, E.; Castillejo, G.; Chmielewska, A.; Crespo Escobar, P.; Kolaček, S.; Koletzko, S.; Korponay-Szabo, I.R.; Mummert, E.; et al. Randomized feeding intervention in infants at high risk for celiac disease. N. Engl. J. Med. 2014, 371, 1304–1315.
  39. Chirdo, F.G.; Auricchio, S.; Troncone, R.; Barone, M.V. The gliadin P31-43 peptide: Inducer of multiple proinflammatory effects. Int. Rev. Cell Mol. Biol. 2021, 358, 165–205.
  40. Barone, M.V.; Nanayakkara, M.; Paolella, G.; Maglio, M.; Vitale, V.; Troiano, R.; Ribecco, M.T.; Lania, G.; Zanzi, D.; Santagata, S.; et al. Gliadin peptide P31-43 localises to endocytic vesicles and interferes with their maturation. PLoS ONE 2010, 5, e12246.
  41. Wenk, M.R. Lipidomics: New tools and applications. Cell 2010, 143, 888–895.
  42. Oresic, M.; Simell, S.; Sysi-Aho, M.; Näntö-Salonen, K.; Seppänen-Laakso, T.; Parikka, V.; Katajamaa, M.; Hekkala, A.; Mattila, I.; Keskinen, P.; et al. Dysregulation of lipid and amino acid metabolism precedes islet autoimmunity in children who later progress to type 1 diabetes. J. Exp. Med. 2008, 205, 2975–2984.
  43. Lamichhane, S.; Ahonen, L.; Dyrlund, T.S.; Kemppainen, E.; Siljander, H.; Hyöty, H.; Ilonen, J.; Toppari, J.; Veijola, R.; Hyötyläinen, T.; et al. Dynamics of Plasma Lipidome in Progression to Islet Autoimmunity and Type 1 Diabetes—Type 1 Diabetes Prediction and Prevention Study (DIPP). Sci. Rep. 2018, 8, 10635.
  44. Perochon, J.; Carroll, L.R.; Cordero, J.B. Wnt Signalling in Intestinal Stem Cells: Lessons from Mice and Flies. Genes 2018, 9, 138.
  45. Hayden, M.S.; Ghosh, S. NF-κB in immunobiology. Cell. Res. 2011, 21, 223–244.
  46. Barone, M.V.; Auricchio, S. A Cumulative Effect of Food and Viruses to Trigger Celiac Disease (CD): A Commentary on the Recent Literature. Int. J. Mol. Sci. 2021, 22, 2027.
  47. Marsh, M.; Loft, D.; Garner, V.; Gordon, D. Time/dose responses of coeliac mucosae to graded oral challenges with Frazer’s fraction III of gliadin. Eur. J. Gastroenterol. Hepatol. 1992, 4, 667–673.
  48. Mulder, C.J.; Mearin, M.L.; Peña, A.S. Clinical and pathological spectrum of coeliac disease. Gut 1993, 34, 1740–1741.
  49. Marsh, M.N.; Crowe, P.T. Morphology of the mucosal lesion in gluten sensitivity. Baillieres Clin. Gastroenterol. 1995, 9, 273–293.
  50. Barone, M.V.; Gimigliano, A.; Castoria, G.; Paolella, G.; Maurano, F.; Paparo, F.; Maglio, M.; Mineo, A.; Miele, E.; Nanayakkara, M.; et al. Growth factor-like activity of gliadin, an alimentary protein: Implications for coeliac disease. Gut 2007, 56, 480–488.
  51. Taavela, J.; Viiri, K.; Popp, A.; Oittinen, M.; Dotsenko, V.; Peräaho, M.; Staff, S.; Sarin, J.; Leon, F.; Mäki, M.; et al. Histological, immunohistochemical and mRNA gene expression responses in coeliac disease patients challenged with gluten using PAXgene fixed paraffin-embedded duodenal biopsies. BMC Gastroenterol. 2019, 19, 189.
  52. Cervio, E.; Volta, U.; Verri, M.; Boschi, F.; Pastoris, O.; Granito, A.; Barbara, G.; Parisi, C.; Felicani, C.; Tonini, M.; et al. Sera of patients with celiac disease and neurologic disorders evoke a mitochondrial-dependent apoptosis in vitro. Gastroenterology 2007, 133, 195–206.
  53. Volta, U.; De Giorgio, R.; Granito, A.; Stanghellini, V.; Barbara, G.; Avoni, P.; Liguori, R.; Petrolini, N.; Fiorini, E.; Montagna, P.; et al. Anti-ganglioside antibodies in coeliac disease with neurological disorders. Dig. Liver. Dis. 2006, 38, 183–187.
  54. Barone, M.V.; Caputo, I.; Ribecco, M.T.; Maglio, M.; Marzari, R.; Sblattero, D.; Troncone, R.; Auricchio, S.; Esposito, C. Humoral immune response to tissue transglutaminase is related to epithelial cell proliferation in celiac disease. Gastroenterology 2007, 132, 1245–1253.
  55. Granito, A.; Muratori, P.; Cassani, F.; Pappas, G.; Muratori, L.; Agostinelli, D.; Veronesi, L.; Bortolotti, R.; Petrolini, N.; Bianchi, F.B.; et al. Anti-actin IgA antibodies in severe coeliac disease. Clin. Exp. Immunol. 2004, 137, 386–392.
  56. Zauli, D.; Grassi, A.; Granito, A.; Foderaro, S.; De Franceschi, L.; Ballardini, G.; Bianchi, F.B.; Volta, U. Prevalence of silent coeliac disease in atopics. Dig. Liver Dis. 2000, 32, 775–779.
  57. Wapenaar, M.C.; Monsuur, A.J.; van Bodegraven, A.A.; Weersma, R.K.; Bevova, M.R.; Linskens, R.K.; Howdle, P.; Holmes, G.; Mulder, C.J.; Dijkstra, G.; et al. Associations with tight junction genes PARD3 and MAGI2 in Dutch patients point to a common barrier defect for coeliac disease and ulcerative colitis. Gut 2008, 57, 463–467.
  58. Trynka, G.; Hunt, K.A.; Bockett, N.A.; Romanos, J.; Mistry, V.; Szperl, A.; Bakker, S.F.; Bardella, M.T.; Bhaw-Rosun, L.; Castillejo, G.; et al. Dense genotyping identifies and localizes multiple common and rare variant association signals in celiac disease. Nat. Genet. 2011, 43, 1193–1201.
  59. Kaminsky, L.W.; Al-Sadi, R.; Ma, T.Y. IL-1β and the Intestinal Epithelial Tight Junction Barrier. Front. Immunol. 2021, 12, 767456.
  60. De Matteis, M.A.; Luini, A. Mendelian disorders of membrane trafficking. N. Engl. J. Med. 2011, 365, 927–938.
  61. Adolph, T.E.; Tomczak, M.F.; Niederreiter, L.; Ko, H.J.; Böck, J.; Martinez-Naves, E.; Glickman, J.N.; Tschurtschenthaler, M.; Hartwig, J.; Hosomi, S.; et al. Paneth cells as a site of origin for intestinal inflammation. Nature 2013, 503, 272–276.
  62. Watkin, L.B.; Jessen, B.; Wiszniewski, W.; Vece, T.J.; Jan, M.; Sha, Y.; Thamsen, M.; Santos-Cortez, R.L.; Lee, K.; Gambin, T.; et al. COPA mutations impair ER-Golgi transport and cause hereditary autoimmune-mediated lung disease and arthritis. Nat. Genet. 2015, 47, 654–660.
  63. Fernandez-Jimenez, N.; Garcia-Etxebarria, K.; Plaza-Izurieta, L.; Romero-Garmendia, I.; Jauregi-Miguel, A.; Legarda, M.; Ecsedi, S.; Castellanos-Rubio, A.; Cahais, V.; Cuenin, C.; et al. The methylome of the celiac intestinal epithelium harbours genotype-independent alterations in the HLA region. Sci. Rep. 2019, 9, 1298.
  64. Pietz, G.; De, R.; Hedberg, M.; Sjöberg, V.; Sandström, O.; Hernell, O.; Hammarström, S.; Hammarström, M.L. Immunopathology of childhood celiac disease-Key role of intestinal epithelial cells. PLoS ONE 2017, 12, e0185025.
  65. Li, V.S.W. Modelling intestinal inflammation and infection using ‘mini-gut’ organoids. Nat. Rev. Gastroenterol. Hepatol. 2021, 18, 89–90.
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