Generic placeholder image

Current Pharmaceutical Biotechnology


ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Review Article

The Possible Role of Pathogenic and Non-Pathogenic Bacteria in Initiation and Exacerbation of Celiac Disease; A Comprehensive Review

Author(s): Taher Azimi*, Ahmad Nasser, Aref Shariati, Seyedeh M.J. Shiadeh, Hossein Safari, Mahmood Alizade-Sani, Ali Taghipour and Amin Dehghan

Volume 21, Issue 6, 2020

Page: [452 - 466] Pages: 15

DOI: 10.2174/1389201021666191219160729

Price: $65


Celiac Disease (CD) is an immune-mediated enteropathy, generally of the proximal intestine, that occurs in genetically susceptible individuals triggered by the ingestion of gluten. The incidence and frequency of CD are increasing, and it is predicted that CD affects approximately 1% of the people worldwide. The common clinical manifestations of CD are divided in two sections, including classic and non-classic symptoms that can be created in childhood and adulthood. The relationship between pathogenic and non-pathogenic bacteria with CD is complex and multidirectional. In previous published studies, results demonstrated the triggering impact of bacteria, viruses, and parasites on initiation and development of Inflammatory Bowel Disease (IBD) and Irritable Bowel Syndrome (IBS). Different studies revealed the inducing effect of pathogenic and non-pathogenic bacteria on CD. However, increasing evidence proposes that some of these microorganisms can also play several positive roles in CD process. Although information of the pathogenesis of the CD is quickly expanding, the possible role of bacteria needs further examination. In conclusion, with respect to the possible correlation between different bacteria in CD, the current review-based study aims to discuss the possible relationship between CD and pathogenic and non-pathogenic bacteria and to show various and significant aspects of mechanisms involved in the CD process.

Keywords: Celiac disease, gluten, bacterial infection, dysbiosis, Irritable Bowel Syndrome (IBS), dysbiosis.

Graphical Abstract
Gibson, G.R.; Roberfroid, M.B. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. J. Nutr., 1995, 125(6), 1401-1412.
De Angelis, M.; Vannini, L.; Di Cagno, R.; Cavallo, N.; Minervini, F.; Francavilla, R.; Ercolini, D.; Gobbetti, M. Salivary and fecal microbiota and metabolome of celiac children under gluten-free diet. Int. J. Food Microbiol., 2016, 239, 125-132.
Lindfors, K.; Ciacci, C.; Kurppa, K.; Lundin, K.E.; Makharia, G.K.; Mearin, M.L.; Murray, J.A.; Verdu, E.F.; Kaukinen, K. Coeliac disease. Nat. Rev. Dis. Primers, 2019, 5(1), 3.
Di Cagno, R.; Rizzello, C.G.; Gagliardi, F.; Ricciuti, P.; Ndagijimana, M.; Francavilla, R.; Guerzoni, M.E.; Crecchio, C.; Gobbetti, M.; De Angelis, M. Different fecal microbiotas and volatile organic compounds in treated and untreated children with celiac disease. Appl. Environ. Microbiol., 2009, 75(12), 3963-3971.
Rostami Nejad, M.; Rostami, K.; Yamaoka, Y.; Mashayekhi, R.; Molaei, M.; Dabiri, H.; Al Dulaimi, D.; Mirsattari, D.; Zojaji, H.; Norouzinia, M.; Zali, M.R. Clinical and histological presentation of Helicobacter pylori and gluten related gastroenteropathy. Arch. Iran Med., 2011, 14(2), 115-118.
Setty, M.; Hormaza, L.; Guandalini, S. Celiac disease. Mol. Diagn.Ther., 2008, 12(5), 289-298.
Mustalahti, K.; Catassi, C.; Reunanen, A.; Fabiani, E.; Heier, M.; McMillan, S.; Murray, L.; Metzger, M.H.; Gasparin, M.; Bravi, E.; Maki, M. The prevalence of celiac disease in Europe: Results of a centralized, international mass screening project. Ann. Med., 2010, 42(8), 587-595.
Choung, R.S.; Ditah, I.C.; Nadeau, A.M.; Rubio-Tapia, A.; Marietta, E.V.; Brantner, T.L.; Camilleri, M.J.; Rajkumar, S.V.; Landgren, O.; Everhart, J.E.; Murray, J.A. Trends and racial/ethnic disparities in gluten-sensitive problems in the United States: Findings from the National Health and Nutrition Examination Surveys from 1988 to 2012. Am. J. Gastroenterol., 2015, 110(3), 455-461.
Ramakrishna, B.S.; Makharia, G.K.; Chetri, K.; Dutta, S.; Mathur, P.; Ahuja, V.; Amarchand, R.; Balamurugan, R.; Chowdhury, S.D.; Daniel, D.; Das, A.; George, G.; Gupta, S.D.; Krishnan, A.; Prasad, J.H.; Kaur, G.; Pugazhendhi, S.; Pulimood, A.; Ramakrishna, K.; Verma, A.K. Prevalence of adult celiac disease in India: Regional variations and associations. Am. J. Gastroenterol., 2016, 111(1), 115-123.
Ludvigsson, J.F.; Leffler, D.A.; Bai, J.C.; Biagi, F.; Fasano, A.; Green, P.H.; Hadjivassiliou, M.; Kaukinen, K.; Kelly, C.P.; Leonard, J.N. The Oslo definitions for coeliac disease and related terms. Gut, 2013, 62(1), 43-52.
Downey, L.; Houten, R.; Murch, S.; Longson, D. Recognition, assessment, and management of coeliac disease: Summary of updated NICE guidance. BMJ, 2015, 351, h4513.
Lebwohl, B.; Sanders, D.S.; Green, P.H. Coeliac disease. Lancet, 2018, 391(10115), 70-81.
Durante-Mangoni, E.; Iardino, P.; Resse, M.; Cesaro, G.; Sica, A.; Farzati, B.; Ruggiero, G.; Adinolfi, L.E. Silent celiac disease in chronic hepatitis C: Impact of interferon treatment on the disease onset and clinical outcome. J. Clin. Gastroenterol., 2004, 38(10), 901-905.
Rubio-Tapia, A.; Hill, I.D.; Kelly, C.P.; Calderwood, A.H.; Murray, J.A. ACG clinical guidelines: Diagnosis and management of celiac disease. Am. J. Gastroenterol., 2013, 108(5), 656.
Ludvigsson, J.F.; Bai, J.C.; Biagi, F.; Card, T.R.; Ciacci, C.; Ciclitira, P.J.; Green, P.H.; Hadjivassiliou, M.; Holdoway, A.; Van Heel, D.A. Diagnosis and management of adult coeliac disease: Guidelines from the British Society of Gastroenterology. Gut, 2014, 2014
Leffler, D.A.; Schuppan, D. Update on serologic testing in celiac disease. Am. J. Gastroenterol., 2010, 105(12), 2520.
Sánchez, E.; Laparra, J.; Sanz, Y. Discerning the role of Bacteroides fragilis in celiac disease pathogenesis. Appl. Environ. Microbiol., 2012, 78, 6507-6515.
Rockert Tjernberg, A.; Bonnedahl, J.; Inghammar, M.; Egesten, A.; Kahlmeter, G.; Naucler, P.; Henriques-Normark, B.; Ludvigsson, J.F. Coeliac disease and invasive pneumococcal disease: A population-based cohort study. Epidemiol. Infect., 2017, 145(6), 1203-1209.
Trovato, C.M.; Montuori, M.; Valitutti, F.; Leter, B.; Cucchiara, S.; Oliva, S. The challenge of treatment in potential celiac disease.Gastroent. Res. Pract, 2019. Article ID 8974751, 6 pages.
Shariati, A.; Aslani, H.R.; Shayesteh, M.R.; Taghipour, A.; Nasser, A.; Safari, H.; Alizade-Sani, M.; Dehghan, A.; Azimi, T. Are viruses and parasites linked to celiac disease? A question that still has no definite answer. Curr. Pharm. Biotechnol, 2019, 20(14), 1181-1193.
Lerner, A.; Arleevskaya, M.; Schmiedl, A.; Matthias, T. Microbes and viruses are bugging the gut in celiac disease. Are they friends or foes? Front. Microbiol., 2017, 8, 1392.
Lerner, A.; Matthias, T. Microbial transglutaminase is immunogenic and potentially pathogenic in pediatric celiac disease. Front Pediatr., 2018, 6, 389.
Azimi, T.; Nasiri, M.J.; Chirani, A.S.; Pouriran, R.; Dabiri, H. The role of bacteria in the inflammatory bowel disease development: A narrative review. APMIS, 2018, 126(4), 275-283.
Shariati, A.; Fallah, F.; Pormohammad, A.; Taghipour, A.; Safari, H. chirani, A.S.; Sabour, S.; Alizadeh‐Sani, M.; Azimi, T. The possible role of bacteria, viruses, and parasites in initiation and exacerbation of irritable bowel syndrome. J. Cell. Physiol., 2018, 234(6), 8550-8569.
Lu, H.; Yamaoka, Y.; Graham, D.Y. Helicobacter pylori virulence factors: Facts and fantasies. Curr. Opin. Gastroenterol., 2005, 21(6), 653-659.
Lebwohl, B.; Blaser, M.J.; Ludvigsson, J.F.; Green, P.H.R.; Rundle, A.; Sonnenberg, A.; Genta, R.M. Decreased risk of celiac disease in patients with Helicobacter pylori colonization. Am. J. Epidemiol., 2013, 178(12), 1721-1730.
Grad, Y.H.; Lipsitch, M.; Aiello, A.E. Secular trends in Helicobacter pylori seroprevalence in adults in the United States: Evidence for sustained race/ethnic disparities. Am. J. Epidemiol., 2011, 175(1), 54-59.
Robinson, K.; Kenefeck, R.; Pidgeon, E.; Shakib, S.; Patel, S.; Polson, R.; Zaitoun, A.M.; Atherton, J.C. Helicobacter pylori-induced peptic ulcer disease is associated with inadequate regulatory T-cell responses. Gut, 2008, 57(10), 1375-1385.
Jansson-Knodell, C.L.; Hujoel, I.A.; Rubio-Tapia, A.; Murray, J.A. Not all that flattens villi is celiac disease: A review of enteropathies. Mayo Clin. Proc., 2018, 93(4), 509-517.
Nishikawa, H.; Hatakeyama, M. Sequence polymorphism and intrinsic structural disorder as related to pathobiological performance of the Helicobacter pylori CagA oncoprotein. Toxins (Basel), 2017, 9(4)pii: E136
Matysiak-Budnik, T.; van Niel, G.; Mégraud, F.; Mayo, K.; Bevilacqua, C.; Gaboriau-Routhiau, V.; Moreau, M-C.; Heyman, M. Gastric helicobacter infection inhibits development of oral tolerance to food antigens in mice. Infect. Immun., 2003, 71(9), 5219-5224.
Villanacci, V.; Bassotti, G.; Liserre, B.; Lanzini, A.; Lanzarotto, F.; Genta, R.M. Helicobacter pylori infection in patients with celiac disease. Am. J. Gastroenterol., 2006, 101(8), 1880.
Dore, M.P.; Salis, R.; Loria, M.F.; Villanacci, V.; Bassotti, G.; Pes, G.M. Helicobacter pylori infection and occurrence of celiac disease in subjects HLA-DQ2/DQ8 positive: A prospective study. Helicobacter, 2018, 23(2) e12465
Rizzello, C.G.; De Angelis, M.; Di Cagno, R.; Camarca, A.; Silano, M.; Losito, I.; De Vincenzi, M.; De Bari, M.D.; Palmisano, F.; Maurano, F. Highly efficient gluten degradation by lactobacilli and fungal proteases during food processing: New perspectives for celiac disease. Appl. Environ. Microbiol., 2007, 73(14), 4499-4507.
Di Cagno, R.; De Angelis, M.; Auricchio, S.; Greco, L.; Clarke, C.; De Vincenzi, M.; Giovannini, C.; D’Archivio, M.; Landolfo, F.; Parrilli, G.; Minervini, F.; Arendt, E.; Gobbetti, M. Sourdough bread made from wheat and nontoxic flours and started with selected lactobacilli is tolerated in celiac sprue patients. Appl. Environ. Microbiol., 2004, 70(2), 1088-1096.
Nelson, W.; Harris, B. Campylo bacteriosis rates show age-related static bimodal and seasonality trends. N. Z. Med. J., 2011, 124(1337), 33-39.
Hugdahl, M.B.; Beery, J.; Doyle, M. Chemotactic behavior of Campylobacter jejuni. Infect. Immun., 1988, 56(6), 1560-1566.
Riddle, M.S.; Murray, J.A.; Cash, B.D.; Pimentel, M.; Porter, C.K. Pathogen-specific risk of celiac disease following bacterial causes of foodborne illness: A retrospective cohort study. Dig. Dis. Sci., 2013, 58(11), 3242-3245.
Sabayan, B.; Foroughinia, F.; Imanieh, M-H. Can Campylobacter jejuni play a role in development of celiac disease? A hypothesis. World J. Gastroenterol., 2007, 13(35), 4784-4785.
Thomas, K.E.; Sapone, A.; Fasano, A.; Vogel, S.N. Gliadin stimulation of murine macrophage inflammatory gene expression and intestinal permeability are MyD88-dependent: Role of the innate immune response in Celiac disease. J. Immunol., 2006, 176(4), 2512-2521.
Jabri, B.; Sollid, L.M. Tissue-mediated control of immunopathology in coeliac disease. Nat. Rev. Immunol., 2009, 9, 858.
MacCallum, A.; Hardy, S.P.; Everest, P.H. Campylobacter jejuni inhibits the absorptive transport functions of Caco-2 cells and disrupts cellular tight junctions. Microbiology, 2005, 151(7), 2451-2458.
Jin, S.; Song, Y.C.; Emili, A.; Sherman, P.M.; Chan, V.L. JlpA of Campylobacter jejuni interacts with surface‐exposed heat shock protein 90α and triggers signaling pathways leading to the activation of NF‐κB and p38 MAP kinase in epithelial cells. Cell. Microbiol., 2003, 5(3), 165-174.
Ashgar, S.S.; Oldfield, N.J.; Wooldridge, K.G.; Jones, M.A.; Irving, G.J.; Turner, D.P. Ala’Aldeen, D.A. CapA, an autotransporter protein of Campylobacter jejuni, mediates association with human epithelial cells and colonization of the chicken gut. J. Bacteriol., 2007, 189(5), 1856-1865.
Kalischuk, L.D.; Inglis, G.D.; Buret, A.G. Strain-dependent induction of epithelial cell oncosis by Campylobacter jejuni is correlated with invasion ability and is independent of cytolethal distending toxin. Microbiology, 2007, 153(9), 2952-2963.
Hatayama, S.; Shimohata, T.; Amano, S.; Kido, J.; Nguyen, A.Q.; Sato, Y.; Kanda, Y.; Tentaku, A.; Fukushima, S.; Nakahashi, M.; Uebanso, T.; Mawatari, K.; Takahashi, A. Cellular tight junctions prevent effective Campylobacter jejuni invasion and inflammatory barrier disruption promoting bacterial invasion from lateral membrane in polarized intestinal epithelial cells. Front. Cell. Infect. Microbiol., 2018, 8(15)
Nasser, A.; Zamirnasta, M.; Jalilian, F.A. Bacterial nanoparticle as a vaccine for meningococcal disease. Biosci. Biotechnol. Res. Asia, 2014, 11(2), 449-453.
Elmi, A.; Nasher, F.; Jagatia, H.; Gundogdu, O.; Bajaj‐Elliott, M.; Wren, B.; Dorrell, N. Campylobacter jejuni outer membrane vesicle‐associated proteolytic activity promotes bacterial invasion by mediating cleavage of intestinal epithelial cell E‐cadherin and occludin. Cell. Microbiol., 2016, 18(4), 561-572.
Friis, L.M.; Keelan, M.; Taylor, D.E. Campylobacter jejuni drives MyD88-independent interleukin-6 secretion via Toll-like receptor 2. Infect. Immun., 2009, 77(4), 1553-1560.
Suzuki, T.; Yoshinaga, N.; Tanabe, S. IL-6 regulates claudin-2 expression and tight junction permeability in intestinal epithelium. J. Biol. Chem., 2011, M111238147
He, F.; Peng, J.; Deng, X-l.; Yang, L-f.; Camara, A.D.; Omran, A.; Wang, G-l.; Wu, L-w.; Zhang, C-L.; Yin, F. Mechanisms of tumor necrosis factor-alpha-induced leaks in intestine epithelial barrier. Cytokine, 2012, 59(2), 264-272.
Lamb-Rosteski, J.M.; Kalischuk, L.D.; Inglis, G.D.; Buret, A.G. Epidermal growth factor inhibits Campylobacter jejuni-induced claudin-4 disruption, loss of epithelial barrier function, and Escherichia coli translocation. Infect. Immun., 2008, 76(8), 3390-3398.
Rees, L.E.; Cogan, T.A.; Dodson, A.L.; Birchall, M.A.; Bailey, M.; Humphrey, T.J. Campylobacter and IFNγ interact to cause a rapid loss of epithelial barrier integrity. Inflamm. Bowel Dis., 2007, 14(3), 303-309.
Johnston, D.G.; Corr, S.C. Toll-like receptor signalling and the control of intestinal barrier function. Methods Mol. Biol., 2016, 1390, 287-300.
D’argenio, V.; Casaburi, G.; Precone, V.; Pagliuca, C.; Colicchio, R.; Sarnataro, D.; Discepolo, V.; Kim, S.M.; Russo, I.; Blanco, G.D.V. Metagenomics reveals dysbiosis and a potentially pathogenic N. flavescens strain in duodenum of adult celiac patients. Am. J. Gastroenterol., 2016, 111(6), 879.
Backert, S.; Bernegger, S.; Skórko‐Glonek, J.; Wessler, S. Extracellular HtrA serine proteases: An emerging new strategy in bacterial pathogenesis. Cell. Microbiol., 2018, 20(6)e12845
Boehm, M.; Haenel, I.; Hoy, B.; Brøndsted, L.; Smith, T.G.; Hoover, T.; Wessler, S.; Tegtmeyer, N. Extracellular secretion of protease HtrA from Campylobacter jejuni is highly efficient and independent of its protease activity and flagellum. Eur. J. Microbiol. Immunol. (Bp.), 2013, 3(3), 163-173.
Boehm, M.; Lind, J.; Backert, S.; Tegtmeyer, N. Campylobacter jejuni serine protease HtrA plays an important role in heat tolerance, oxygen resistance, host cell adhesion, invasion, and transmigration. Eur. J. Microbiol. Immunol. (Bp.), 2015, 5(1), 68-80.
van Putten, J.P.; van Alphen, L.B.; Wosten, M.M.; de Zoete, M.R. Molecular mechanisms of campylobacter infection. Curr. Top. Microbiol. Immunol., 2009, 337, 197-229.
Köhler, H.; Sakaguchi, T.; Hurley, B.P.; Kase, B.J.; Reinecker, H-C.; McCormick, B.A. Salmonella enterica serovar Typhimurium regulates intercellular junction proteins and facilitates transepithelial neutrophil and bacterial passage. Am. J. Physiol. Gastrointest. Liver Physiol., 2007, 293(1), G178-G187.
Chen, M.L.; Ge, Z.; Fox, J.G.; Schauer, D.B. Disruption of tight junctions and induction of proinflammatory cytokine responses in colonic epithelial cells by Campylobacter jejuni. Infect. Immun., 2006, 74(12), 6581-6589.
Zaas, D.W.; Duncan, M.; Wright, J.R.; Abraham, S.N. The role of lipid rafts in the pathogenesis of bacterial infections. Biochim. Biophys. Acta, 2005, 1746(3), 305-313.
Rahman, A.; Fahlgren, A.; Sundstedt, C.; Hammarström, S.; Danielsson, Å.; Hammarström, M.L. Chronic colitis induces expression of β‐defensins in murine intestinal epithelial cells. Clin. Exp. Immunol., 2011, 163(1), 123-130.
Golfetto, L.; de Senna, F.D.; Hermes, J.; Beserra, B.T.; Franca Fda, S.; Martinello, F. Lower bifidobacteria counts in adult patients with celiac disease on a gluten-free diet. Arq. Gastroenterol., 2014, 51(2), 139-143.
Olivares, M.; Laparra, M.; Sanz, Y. Influence of Bifidobacterium longum CECT 7347 and gliadin peptides on intestinal epithelial cell proteome. J. Agric. Food Chem., 2011, 59(14), 7666-7671.
de Sousa Moraes, L.F.; Grzeskowiak, L.M.; de Sales Teixeira, T.F.; Peluzio, G.; Mdo, C. Intestinal microbiota and probiotics in celiac disease. Clin. Microbiol. Rev., 2014, 27(3), 482-489.
De Palma, G.; Kamanova, J.; Cinova, J.; Olivares, M.; Drasarova, H.; Tuckova, L.; Sanz, Y. Modulation of phenotypic and functional maturation of dendritic cells by intestinal bacteria and gliadin: relevance for celiac disease. J. Leukoc. Biol., 2012, 92(5), 1043-1054.
Laparra, J.M.; Sanz, Y. Bifidobacteria inhibit the inflammatory response induced by gliadins in intestinal epithelial cells via modifications of toxic peptide generation during digestion. J. Cell. Biochem., 2010, 109(4), 801-807.
De Palma, G.; Cinova, J.; Stepankova, R.; Tuckova, L.; Sanz, Y. Pivotal advance: Bifidobacteria and Gram-negative bacteria differentially influence immune responses in the proinflammatory milieu of celiac disease. J. Leukoc. Biol., 2010, 87(5), 765-778.
Primec, M.; Klemenak, M.; Di Gioia, D.; Aloisio, I.; Bozzi Cionci, N.; Quagliariello, A.; Gorenjak, M.; Micetic-Turk, D.; Langerholc, T. Clinical intervention using Bifidobacterium strains in celiac disease children reveals novel microbial modulators of TNF-alpha and short-chain fatty acids; Clin. Nutr: Edinburgh, Scotland, 2018.
Cinova, J.; De Palma, G.; Stepankova, R.; Kofronova, O.; Kverka, M.; Sanz, Y.; Tuckova, L. Role of intestinal bacteria in gliadin-induced changes in intestinal mucosa: Study in germ-free rats. PLoS One, 2011, 6(1)e16169
Sakurai, T.; Yamada, A.; Hashikura, N.; Odamaki, T.; Xiao, J.Z. Degradation of food-derived opioid peptides by bifidobacteria. Benef. Microbes, 2018, 9(4), 675-682.
Cristofori, F.; Indrio, F.; Miniello, V.L.; De Angelis, M.; Francavilla, R. Probiotics in celiac disease. Nutrients, 2018, 10(12)pii: E1824
Pinto-Sanchez, M.I.; Smecuol, E.C.; Temprano, M.P.; Sugai, E.; Gonzalez, A.; Moreno, M.L.; Huang, X.; Bercik, P.; Cabanne, A.; Vazquez, H.; Niveloni, S.; Mazure, R.; Maurino, E.; Verdu, E.F.; Bai, J.C. Bifidobacterium infantis NLS super strain reduces the expression of alpha-defensin-5, a marker of innate immunity, in the mucosa of active celiac disease patients. J. Clin. Gastroenterol., 2017, 51(9), 814-817.
Kiseleva, E.P.; Mikhailopulo, K.I.; Zdorovenko, E.L.; Knirel, Y.A.; Novik, G.I. Linear alpha-(1-->6)-d-glucan from Bifidobacterium bifidum BIM capital VE, Cyrillic-733D is low molecular mass biopolymer with unique immunochemical properties. Carbohydr. Res., 2018, 466, 39-50.
Caminero, A.; Galipeau, H.J.; McCarville, J.L.; Johnston, C.W.; Bernier, S.P.; Russell, A.K.; Jury, J.; Herran, A.R.; Casqueiro, J.; Tye-Din, J.A.; Surette, M.G.; Magarvey, N.A.; Schuppan, D.; Verdu, E.F. Duodenal bacteria from patients with celiac disease and healthy subjects distinctly affect gluten breakdown and immunogenicity. Gastroenterology, 2016, 151(4), 670-683.
Lorenzo Pisarello, M.J.; Vintini, E.O.; Gonzalez, S.N.; Pagani, F.; Medina, M.S. Decrease in lactobacilli in the intestinal microbiota of celiac children with a gluten-free diet, and selection of potentially probiotic strains. Can. J. Microbiol., 2015, 61(1), 32-37.
Di Cagno, R.; De Angelis, M.; De Pasquale, I.; Ndagijimana, M.; Vernocchi, P.; Ricciuti, P.; Gagliardi, F.; Laghi, L.; Crecchio, C.; Guerzoni, M.E.; Gobbetti, M.; Francavilla, R. Duodenal and faecal microbiota of celiac children: Molecular, phenotype and metabolome characterization. BMC Microbiol., 2011, 11, 219.
Orlando, A.; Linsalata, M.; Notarnicola, M.; Tutino, V.; Russo, F. Lactobacillus GG restoration of the gliadin induced epithelial barrier disruption: The role of cellular polyamines. BMC Microbiol., 2014, 14, 19.
Sarno, M.; Lania, G.; Cuomo, M.; Nigro, F.; Passannanti, F.; Budelli, A.; Fasano, F.; Troncone, R.; Auricchio, S.; Barone, M.V.; Nigro, R.; Nanayakkara, M. Lactobacillus paracasei CBA L74 interferes with gliadin peptides entrance in Caco-2 cells. Int. J. Food Sci. Nutr., 2014, 65(8), 953-959.
Garcia-Mazcorro, J.F.; Rivera-Gutierrez, X.; Cobos-Quevedo, O.J.; Grube-Pagola, P.; Meixueiro-Daza, A.; Hernandez-Flores, K.; Cabrera-Jorge, F.J.; Vivanco-Cid, H.; Dowd, S.E.; Remes-Troche, J.M. First insights into the gut microbiota of Mexican patients with celiac disease and non-celiac gluten sensitivity. Nutrients, 2018, 10(11)pii: E1641
Wei, G.; Tian, N.; Valery, A.C.; Zhong, Y.; Schuppan, D.; Helmerhorst, E.J. Identification of Pseudolysin (lasB) as an aciduric gluten-degrading enzyme with high therapeutic potential for celiac disease. Am. J. Gastroenterol., 2015, 110(6), 899-908.
Sharahi, J.Y.; Azimi, T.; Shariati, A.; Safari, H.; Tehrani, M.K.; Hashemi, A. Advanced strategies for combating bacterial biofilms. J. Cell. Physiol., 2019.
Shariati, A.; Azimi, T.; Ardebili, A.; Chirani, A.; Bahramian, A.; Pormohammad, A.; Sadredinamin, M.; Erfanimanesh, S.; Bostanghadiri, N.; Shams, S. Insertional inactivation of oprD in carbapenem-resistant Pseudomonas aeruginosa strains isolated from burn patients in Tehran, Iran. New Microbes New Infect., 2018, 21, 75-80.
Galipeau, H.J.; McCarville, J.L.; Huebener, S.; Litwin, O.; Meisel, M.; Jabri, B.; Sanz, Y.; Murray, J.A.; Jordana, M.; Alaedini, A.; Chirdo, F.G.; Verdu, E.F. Intestinal microbiota modulates gluten-induced immunopathology in humanized mice. Am. J. Pathol., 2015, 185(11), 2969-2982.
Schippa, S.; Iebba, V.; Barbato, M.; Di Nardo, G.; Totino, V.; Checchi, M.P.; Longhi, C.; Maiella, G.; Cucchiara, S.; Conte, M.P. A distinctive ‘microbial signature’ in celiac pediatric patients. BMC Microbiol., 2010, 10, 175.
Nouvenne, A.; Ticinesi, A.; Tana, C.; Prati, B.; Catania, P.; Miraglia, C. De’ Angelis, G. L.; Di Mario, F.; Meschi, T. Digestive disorders and intestinal microbiota. Acta Biomed., 2018, 89(9-s), 47-51.
Azimirad, M.; Rostami-Nejad, M.; Rostami, K.; Naji, T.; Zali, M.R. The susceptibility of celiac disease intestinal microbiota to Clostridium difficile infection. Am. J. Gastroenterol., 2015, 110(12), 1740-1741.
Olivares, M.; Benitez-Paez, A.; de Palma, G.; Capilla, A.; Nova, E.; Castillejo, G.; Varea, V.; Marcos, A.; Garrote, J.A.; Polanco, I.; Donat, E.; Ribes-Koninckx, C.; Calvo, C.; Ortigosa, L.; Palau, F.; Sanz, Y. Increased prevalence of pathogenic bacteria in the gut microbiota of infants at risk of developing celiac disease: The PROFICEL study. Gut Microbes, 2018, 9(6), 551-558.
Ou, G.; Hedberg, M.; Horstedt, P.; Baranov, V.; Forsberg, G.; Drobni, M.; Sandstrom, O.; Wai, S.N.; Johansson, I.; Hammarstrom, M.L.; Hernell, O.; Hammarstrom, S. Proximal small intestinal microbiota and identification of rod-shaped bacteria associated with childhood celiac disease. Am. J. Gastroenterol., 2009, 104(12), 3058-3067.
Lebwohl, B.; Nobel, Y.R.; Green, P.H.R.; Blaser, M.J.; Ludvigsson, J.F. Risk of Clostridium difficile infection in patients with celiac Disease: A Population-based study. Am. J. Gastroenterol., 2017, 112(12), 1878-1884.
Sanchez, E.; Laparra, J.M.; Sanz, Y. Discerning the role of Bacteroides fragilis in celiac disease pathogenesis. Appl. Environ. Microbiol., 2012, 78(18), 6507-6515.
Sanchez, E.; De Palma, G.; Capilla, A.; Nova, E.; Pozo, T.; Castillejo, G.; Varea, V.; Marcos, A.; Garrote, J.A.; Polanco, I.; Lopez, A.; Ribes-Koninckx, C.; Garcia-Novo, M.D.; Calvo, C.; Ortigosa, L.; Palau, F.; Sanz, Y. Influence of environmental and genetic factors linked to celiac disease risk on infant gut colonization by Bacteroides species. Appl. Environ. Microbiol., 2011, 77(15), 5316-5323.
Pozo-Rubio, T.; de Palma, G.; Mujico, J.R.; Olivares, M.; Marcos, A.; Acuna, M.D.; Polanco, I.; Sanz, Y.; Nova, E. Influence of early environmental factors on lymphocyte subsets and gut microbiota in infants at risk of celiac disease; the PROFICEL study. Nutr. Hosp., 2013, 28(2), 464-473.
Viitasalo, L.; Niemi, L.; Ashorn, M.; Ashorn, S.; Braun, J.; Huhtala, H.; Collin, P.; Maki, M.; Kaukinen, K.; Kurppa, K.; Iltanen, S. Early microbial markers of celiac disease. J. Clin. Gastroenterol., 2014, 48(7), 620-624.
Ashorn, S.; Valineva, T.; Kaukinen, K.; Ashorn, M.; Braun, J.; Raukola, H.; Rantala, I.; Collin, P.; Maki, M.; Luukkaala, T.; Iltanen, S. Serological responses to microbial antigens in celiac disease patients during a gluten-free diet. J. Clin. Immunol., 2009, 29(2), 190-195.
Thomas, H.J.; Wotton, C.J.; Yeates, D.; Ahmad, T.; Jewell, D.P.; Goldacre, M.J. Pneumococcal infection in patients with coeliac disease. Eur. J. Gastroenterol. Hepatol., 2008, 20(7), 624-628.
Ouseph, M.M.; Simons, M.; Treaba, D.O.; Yakirevich, E.; Green, P.H.; Bhagat, G.; Moss, S.F.; Mangray, S. Fatal Streptococcus pneumoniae sepsis in a patient with celiac disease-associated hyposplenism. ACG Case Rep. J., 2016, 3(4)
Baker, P.; Jones, J.V.; Peacock, D.; Read, A. The immune response of phiX 174 in man. III. Evidence for an association between hyposplenism and immunodeficiency in patients with coeliac disease. Gut, 1975, 16(7), 538-542.
Di Sabatino, A.; Carsetti, R.; Corazza, G.R. Post-splenectomy and hyposplenic states. Lancet, 2011, 378(9785), 86-97.
William, B.M.; Corazza, G.R. Hyposplenism: A comprehensive review. Part I: Basic concepts and causes. Hematology, 2007, 12(1), 1-13.
Sanchez, E.; Donat, E.; Ribes-Koninckx, C.; Fernandez-Murga, M.L.; Sanz, Y. Duodenal-mucosal bacteria associated with celiac disease in children. Appl. Environ. Microbiol., 2013, 79(18), 5472-5479.
Francavilla, R.; Ercolini, D.; Piccolo, M.; Vannini, L.; Siragusa, S.; De Filippis, F.; De Pasquale, I.; Di Cagno, R.; Di Toma, M.; Gozzi, G.; Serrazanetti, D.I.; De Angelis, M.; Gobbetti, M. Salivary microbiota and metabolome associated with celiac disease. Appl. Environ. Microbiol., 2014, 80(11), 3416-3425.
Di Sabatino, A.; Rosado, M.M.; Cazzola, P.; Riboni, R.; Biagi, F.; Carsetti, R.; Corazza, G.R. Splenic hypofunction and the spectrum of autoimmune and malignant complications in celiac disease. Clin. Gastroenterol. Hepatol., 2006, 4(2), 179-186.
Di Sabatino, A.; Corazza, G.R. Coeliac disease. Lancet, 2009, 373(9673), 1480-1493.
Sollid, L.M.; Khosla, C. Future therapeutic options for celiac disease. Nat. Rev. Gastroenterol. Hepatol., 2005, 2(3), 140.
Kahaly, G.J.; Frommer, L.; Schuppan, D. Celiac disease and endocrine autoimmunity-the genetic link. Autoimmun. Rev., 2018, 17(12), 1169-1175.
Han, M.; Zhang, Y.; Fei, Y.; Xu, X.; Zhou, G. Effect of microbial transglutaminase on NMR relaxometry and microstructure of pork myofibrillar protein gel. Eur. Food Res. Technol., 2009, 228(4), 665-670.
Reif, S.; Lerner, A. Tissue transglutaminase-the key player in celiac disease: A review. Autoimmun. Rev., 2004, 3(1), 40-45.
Velikova, T.V.; Spassova, Z.A.; Tumangelova-Yuzeir, K.D.; Krasimirova, E.K.; Ivanova-Todorova, E.I.; Kyurkchiev, D.S.; Altankova, I.P. Serological update on celiac disease diagnostics in adults. Int. J., 2018, 6(1), 20-25.
Strop, P. Versatility of microbial transglutaminase. Bioconjug. Chem., 2014, 25(5), 855-862.
Matthias, T.; Jeremias, P.; Neidhöfer, S.; Lerner, A. The industrial food additive, microbial transglutaminase, mimics tissue transglutaminase and is immunogenic in celiac disease patients. Autoimmun. Rev., 2016, 15(12), 1111-1119.
Tagami, U.; Shimba, N.; Nakamura, M.; Yokoyama, K-I.; Suzuki, E-I.; Hirokawa, T. Substrate specificity of microbial transglutaminase as revealed by three-dimensional docking simulation and mutagenesis. Protein Eng. Des. Sel., 2009, 22(12), 747-752.
Yu, J.; Pian, Y.; Ge, J.; Guo, J.; Zheng, Y.; Jiang, H.; Hao, H.; Yuan, Y.; Jiang, Y.; Yang, M. Functional and structural characterization of the antiphagocytic properties of a novel transglutaminase from Streptococcus suis. J. Biol. Chem., 2015, 290(31), 19081-19092.
Cohavy, O.; Bruckner, D.; Gordon, L.; Misra, R.; Wei, B.; Eggena, M.; Targan, S.; Braun, J. Colonic bacteria express an ulcerative colitis pANCA-related protein epitope. Infect. Immun., 2000, 68(3), 1542-1548.
Bagheri, N.; Salimzadeh, L.; Shirzad, H. The role of T helper 1-cell response in Helicobacter pylori-infection. Microb. Pathog., 2018.
Trinchieri, G. Interleukin-12: a cytokine produced by antigen-presenting cells with immunoregulatory functions in the generation of T-helper cells type 1 and cytotoxic lymphocytes. Blood, 1994, 84(12), 4008-4027.
Parker, A.; Vaux, L.; Patterson, A.M.; Modasia, A.; Muraro, D.; Fletcher, A.G.; Byrne, H.M.; Maini, P.K.; Watson, A.J.; Pin, C. Elevated apoptosis impairs epithelial cell turnover and shortens villi in TNF-driven intestinal inflammation. Cell Death Dis., 2019, 10(2), 108.
Ieni, A.; Barresi, V.; Rigoli, L.; Fedele, F.; Tuccari, G.; Caruso, R. Morphological and cellular features of innate immune reaction in Helicobacter pylori gastritis: A brief review. Int. J. Mol. Sci., 2016, 17(1), 109.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy