Mechanisms of persistence, innate immune activation and immunomodulation by the gastric pathogen Helicobacter pylori

Backert, 2010, What a disorder: proinflammatory signaling pathways induced by Helicobacter pylori, Trends Microbiol, 18, 479, 10.1016/j.tim.2010.08.003 Newton, 2012, Signaling in innate immunity and inflammation, Cold Spring Harb Perspect Biol, 4, 10.1101/cshperspect.a006049 Salama, 2013, Life in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori, Nat Rev Microbiol, 11, 385, 10.1038/nrmicro3016 Andersen-Nissen, 2005, Evasion of toll-like receptor 5 by flagellated bacteria, Proc Natl Acad Sci U S A, 102, 9247, 10.1073/pnas.0502040102 Cullen, 2012, Helicobacter pylori versus the host: remodeling of the bacterial outer membrane is required for survival in the gastric mucosa, PLoS Pathog, 7 Zhang, 2010, Helicobacter pylori directs tolerogenic programming of dendritic cells, Gut Microbes, 1, 325, 10.4161/gmic.1.5.13052 Luther, 2011, Helicobacter pylori DNA decreases pro-inflammatory cytokine production by dendritic cells and attenuates dextran sodium sulphate-induced colitis, Gut, 60, 1479, 10.1136/gut.2010.220087 Gall, 2017, TIFA signaling in gastric epithelial cells initiates the cag Type 4 secretion system-dependent innate immune response to helicobacter pylori infection, mBio, 8, 10.1128/mBio.01168-17 Zimmermann, 2017, ALPK1- and TIFA-dependent innate immune response triggered by the Helicobacter pylori Type IV secretion system, Cell Rep, 20, 2384, 10.1016/j.celrep.2017.08.039 Stein, 2017, Helicobacter pylori modulates host cell responses by CagT4SS-dependent translocation of an intermediate metabolite of LPS inner core heptose biosynthesis, PLoS Pathog, 13, 10.1371/journal.ppat.1006514 Gaudet, 2015, Cytosolic detection of the bacterial metabolite HBP activates TIFA-dependent innate immunity, Science, 348, 1251, 10.1126/science.aaa4921 Milivojevic, 2017, ALPK1 controls TIFA/TRAF6-dependent innate immunity against heptose-1,7-bisphosphate of gram-negative bacteria, PLoS Pathog, 13, 10.1371/journal.ppat.1006224 Zhou, 2018, Alpha-kinase 1 is a cytosolic innate immune receptor for bacterial ADP-heptose, Nature, 561, 122, 10.1038/s41586-018-0433-3 Pfannkuch, 2019, ADP heptose, a novel pathogen-associated molecular pattern identified in Helicobacter pylori, FASEB J, 33, 9087, 10.1096/fj.201802555R Greten, 2004, IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer, Cell, 118, 285, 10.1016/j.cell.2004.07.013 Pikarsky, 2004, NF-kappaB functions as a tumour promoter in inflammation-associated cancer, Nature, 431, 461, 10.1038/nature02924 Taniguchi, 2018, NF-kappaB, inflammation, immunity and cancer: coming of age, Nat Rev Immunol, 18, 309, 10.1038/nri.2017.142 Grivennikov, 2010, Immunity, inflammation, and cancer, Cell, 140, 883, 10.1016/j.cell.2010.01.025 Luo, 2005, IKK/NF-kappaB signaling: balancing life and death–a new approach to cancer therapy, J Clin Invest, 115, 2625, 10.1172/JCI26322 Grivennikov, 2009, IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer, Cancer Cell, 15, 103, 10.1016/j.ccr.2009.01.001 Hartung, 2015, H. pylori-induced DNA strand breaks are introduced by nucleotide excision repair endonucleases and promote NF-kappaB target gene expression, Cell Rep, 13, 70, 10.1016/j.celrep.2015.08.074 Arnold, 2017, NLRP3 controls the development of gastrointestinal CD11b(+) dendritic cells in the steady state and during chronic bacterial infection, Cell Rep, 21, 3860, 10.1016/j.celrep.2017.12.015 Kabisch, 2014, Involvement of toll-like receptors on Helicobacter pylori-induced immunity, PLoS One, 9, 10.1371/journal.pone.0104804 Kabisch, 2016, Helicobacter pylori gamma-glutamyltranspeptidase induces tolerogenic human dendritic cells by activation of glutamate receptors, J Immunol, 196, 4246, 10.4049/jimmunol.1501062 Rizzuti, 2015, Helicobacter pylori inhibits dendritic cell maturation via interleukin-10-mediated activation of the signal transducer and activator of transcription 3 pathway, J Innate Immun, 7, 199, 10.1159/000368232 Oertli, 2012, DC-derived IL-18 drives Treg differentiation, murine Helicobacter pylori-specific immune tolerance, and asthma protection, J Clin Invest, 122, 1082, 10.1172/JCI61029 Kao, 2010, Helicobacter pylori immune escape is mediated by dendritic cell-induced Treg skewing and Th17 suppression in mice, Gastroenterology, 138, 1046, 10.1053/j.gastro.2009.11.043 Hitzler, 2011, Dendritic cells prevent rather than promote immunity conferred by a helicobacter vaccine using a mycobacterial adjuvant, Gastroenterology, 141, 186, 10.1053/j.gastro.2011.04.009 Arnold, 2019, BATF3-dependent dendritic cells drive both effector and regulatory T-cell responses in bacterially infected tissues, PLoS Pathog, 15, 10.1371/journal.ppat.1007866 Edelson, 2010, Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells, J Exp Med, 207, 823, 10.1084/jem.20091627 Haniffa, 2012, Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103+ nonlymphoid dendritic cells, Immunity, 37, 60, 10.1016/j.immuni.2012.04.012 Sanchez-Paulete, 2016, Cancer immunotherapy with immunomodulatory anti-CD137 and anti-PD-1 monoclonal antibodies requires BATF3-dependent dendritic cells, Cancer Discov, 6, 71, 10.1158/2159-8290.CD-15-0510 Spranger, 2017, Tumor-residing Batf3 dendritic cells are required for effector T cell trafficking and adoptive T cell therapy, Cancer Cell, 31, 711, 10.1016/j.ccell.2017.04.003 de Mingo Pulido, 2018, TIM-3 regulates CD103(+) dendritic cell function and response to chemotherapy in breast cancer, Cancer Cell, 33, 60, 10.1016/j.ccell.2017.11.019 Weber, 2014, Host-derived CD8(+) dendritic cells protect against acute graft-versus-host disease after experimental allogeneic bone marrow transplantation, Biol Blood Marrow Transplant, 20, 1696, 10.1016/j.bbmt.2014.08.005 Perry, 2014, Distinct contributions of Aire and antigen-presenting-cell subsets to the generation of self-tolerance in the thymus, Immunity, 41, 414, 10.1016/j.immuni.2014.08.007 Khare, 2013, Cutting edge: inhaled antigen upregulates retinaldehyde dehydrogenase in lung CD103+ but not plasmacytoid dendritic cells to induce Foxp3 de novo in CD4+ T cells and promote airway tolerance, J Immunol, 191, 25, 10.4049/jimmunol.1300193 Chevalier, 1999, Essential role of Helicobacter pylori gamma-glutamyltranspeptidase for the colonization of the gastric mucosa of mice, Mol Microbiol, 31, 1359, 10.1046/j.1365-2958.1999.01271.x Rossi, 2012, Evidence for conserved function of gamma-glutamyltranspeptidase in Helicobacter genus, PLoS One, 7, 10.1371/journal.pone.0030543 Wustner, 2017, Helicobacter pylori gamma-glutamyl transferase contributes to colonization and differential recruitment of T cells during persistence, Sci Rep, 7, 10.1038/s41598-017-14028-1 Shibayama, 2007, Metabolism of glutamine and glutathione via gamma-glutamyltranspeptidase and glutamate transport in Helicobacter pylori: possible significance in the pathophysiology of the organism, Mol Microbiol, 64, 396, 10.1111/j.1365-2958.2007.05661.x Wischmeyer, 2006, Glutamine: role in gut protection in critical illness, Curr Opin Clin Nutr Metab Care, 9, 607, 10.1097/01.mco.0000241672.09676.03 Fallarino, 2010, Metabotropic glutamate receptor-4 modulates adaptive immunity and restrains neuroinflammation, Nat Med, 16, 897, 10.1038/nm.2183 Amagase, 2010, New frontiers in gut nutrient sensor research: prophylactic effect of glutamine against Helicobacter pylori-induced gastric diseases in Mongolian gerbils, J Pharmacol Sci, 112, 25, 10.1254/jphs.09R11FM Oertli, 2013, Helicobacter pylori gamma-glutamyl transpeptidase and vacuolating cytotoxin promote gastric persistence and immune tolerance, Proc Natl Acad Sci U S A, 110, 3047, 10.1073/pnas.1211248110 Altobelli, 2019, Helicobacter pylori VacA targets myeloid cells in the gastric lamina propria to promote peripherally induced regulatory T-cell differentiation and persistent infection, mBio, 10, 10.1128/mBio.00261-19 Winter, 2014, A role for the vacuolating cytotoxin, VacA, in colonization and Helicobacter pylori-induced metaplasia in the stomach, J Infect Dis, 210, 954, 10.1093/infdis/jiu154 Capurro, 2019, VacA generates a protective intracellular reservoir for Helicobacter pylori that is eliminated by activation of the lysosomal calcium channel TRPML1, Nat Microbiol, 4, 1411, 10.1038/s41564-019-0441-6 Foegeding, 2016, An overview of Helicobacter pylori VacA toxin biology, Toxins (Basel), 8, 10.3390/toxins8060173 Dubois, 2007, Helicobacter pylori is invasive and it may be a facultative intracellular organism, Cell Microbiol, 9, 1108, 10.1111/j.1462-5822.2007.00921.x Necchi, 2010, In vivo accumulation of Helicobacter pylori products, NOD1, ubiquitinated proteins and proteasome in a novel cytoplasmic structure, PLoS One, 5, 10.1371/journal.pone.0009716 Arnold, 2018, Eosinophils suppress Th1 responses and restrict bacterially induced gastrointestinal inflammation, J Exp Med, 215, 2055, 10.1084/jem.20172049 Linch, 2009, Mouse eosinophils possess potent antibacterial properties in vivo, Infect Immun, 77, 4976, 10.1128/IAI.00306-09 McGovern, 1991, Eosinophil infiltration and degranulation in Helicobacter pylori-associated chronic gastritis, Dig Dis Sci, 36, 435, 10.1007/BF01298871 Blaser, 2008, Does Helicobacter pylori protect against asthma and allergy?, Gut, 57, 561, 10.1136/gut.2007.133462 Reibman, 2008, Asthma is inversely associated with Helicobacter pylori status in an urban population, PLoS One, 3, 10.1371/journal.pone.0004060 Amberbir, 2014, Exposure to Helicobacter pylori infection in early childhood and the risk of allergic disease and atopic sensitization: a longitudinal birth cohort study, Clin Exp Allergy, 44, 563, 10.1111/cea.12289 Amberbir, 2011, Effects of Helicobacter pylori, geohelminth infection and selected commensal bacteria on the risk of allergic disease and sensitization in 3-year-old Ethiopian children, Clin Exp Allergy, 10.1111/j.1365-2222.2011.03831.x Taye, 2017, Association between infection with Helicobacter pylori and atopy in young Ethiopian children: a longitudinal study, Clin Exp Allergy, 47, 1299, 10.1111/cea.12995 Fouda, 2018, Helicobacter pylori seropositivity protects against childhood asthma and inversely correlates to its clinical and functional severity, Allergol Immunopathol (Madr), 46, 76, 10.1016/j.aller.2017.03.004 Chen, 2017, Accumulated evidence on Helicobacter pylori infection and the risk of asthma: a meta-analysis, Ann Allergy Asthma Immunol, 119, 137, 10.1016/j.anai.2017.05.021 Kyburz, 2017, Helicobacter pylori and its secreted immunomodulator VacA protect against anaphylaxis in experimental models of food allergy, Clin Exp Allergy, 47, 1331, 10.1111/cea.12996 Arnold, 2011, Helicobacter pylori infection prevents allergic asthma in mouse models through the induction of regulatory T cells, J Clin Invest, 121, 3088, 10.1172/JCI45041 Koch, 2015, Helicobacter urease-induced activation of the TLR2/NLRP3/IL-18 axis protects against asthma, J Clin Invest, 125, 3297, 10.1172/JCI79337 Hussain, 2016, Helicobacter pylori-mediated protection from allergy is associated with IL-10-secreting peripheral blood regulatory T cells, Front Immunol, 7, 71, 10.3389/fimmu.2016.00071 Cook, 2014, CCL20/CCR6-mediated migration of regulatory T cells to the Helicobacter pylori-infected human gastric mucosa, Gut, 63, 1550, 10.1136/gutjnl-2013-306253 Cook, 2015, Helicobacter pylori infection reduces disease severity in an experimental model of multiple sclerosis, Front Microbiol, 6, 52, 10.3389/fmicb.2015.00052 Luther, 2010, Association between Helicobacter pylori infection and inflammatory bowel disease: a meta-analysis and systematic review of the literature, Inflamm Bowel Dis, 16, 1077, 10.1002/ibd.21116 Engler, 2015, Helicobacter pylori-specific protection against inflammatory bowel disease requires the NLRP3 inflammasome and IL-18, Inflamm Bowel Dis, 21, 854, 10.1097/MIB.0000000000000318 Bhattacharjee, 2019, Concomitant infection of S. mansoni and H. pylori promotes promiscuity of antigen-experienced cells and primes the liver for a lower fibrotic response, Cell Rep, 28, 231, 10.1016/j.celrep.2019.05.108 Fox, 2000, Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces helicobacter-induced gastric atrophy, Nat Med, 6, 536, 10.1038/75015 Xu, 2018, c-MAF-dependent regulatory T cells mediate immunological tolerance to a gut pathobiont, Nature, 554, 373, 10.1038/nature25500 Majlessi, 2017, Colonization with Helicobacter is concomitant with modified gut microbiota and drastic failure of the immune control of Mycobacterium tuberculosis, Mucosal Immunol, 10, 1178, 10.1038/mi.2016.140