Human Intestinal Epithelial Cells Are Broadly Unresponsive to Toll-Like Receptor 2-Dependent Bacterial Ligands: Implications for Host-Microbial Interactions in the Gut

Melmed, Gil; Thomas, Lisa S; Lee, Nahee; Tesfay, Samuel Y; Lukasek, Katie; Michelsen, Kathrin S; Zhou, Yuehua; Hu, Bing; Arditi, Moshe; Abreu, Maria T

doi:10.4049/jimmunol.170.3.1406

Cited by 431Immune Response and InflammationGut microbiota and healthGastrointestinal motility and disorders

Human Intestinal Epithelial Cells Are Broadly Unresponsive to Toll-Like Receptor 2-Dependent Bacterial Ligands: Implications for Host-Microbial Interactions in the Gut

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Melmed, Gil, Thomas, Lisa S, Lee, Nahee, Tesfay, Samuel Y, Lukasek, Katie, Michelsen, Kathrin S, Zhou, Yuehua, Hu, Bing +2 more·2003·The Journal of Immunology

DOI 10.4049/jimmunol.170.3.1406

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Abstract

Intestinal epithelial cells (IEC) interact with a high density of Gram-positive bacteria and are active participants in mucosal immune responses. Recognition of Gram-positive organisms by Toll-like receptor (TLR)2 induces proinflammatory gene expression by diverse cells. We hypothesized that IEC are unresponsive to Gram-positive pathogen-associated molecular patterns and sought to characterize the functional responses of IEC to TLR2-specific ligands. Human colonic epithelial cells isolated by laser capture microscopy and IEC lines (Caco-2, T84, HT-29) were analyzed for expression of TLR2, TLR6, TLR1, and Toll inhibitory protein (Tollip) mRNA by RT-PCR and quantitative real-time PCR. Response to Gram-positive bacterial ligands was measured by NF-κB reporter gene activation and IL-8 secretion. TLR2 protein expression was analyzed by immunofluorescence and flow cytometry. Colonic epithelial cells and lamina propria cells from both uninflamed and inflamed tissue demonstrate low expression of TLR2 mRNA compared with THP-1 monocytes. IECs were unresponsive to TLR2 ligands including the staphylococcal-derived Ags phenol soluble modulin, peptidoglycan, and lipotechoic acid and the mycobacterial-derived Ag soluble tuberculosis factor. Transgenic expression of TLR2 and TLR6 restored responsiveness to phenol soluble modulin and peptidoglycan in IEC. In addition to low levels of TLR2 protein expression, IEC also express high levels of the inhibitory molecule Tollip. We conclude that IEC are broadly unresponsive to TLR2 ligands secondary to deficient expression of TLR2 and TLR6. The relative absence of TLR2 protein expression by IEC and high level of Tollip expression may be important in preventing chronic proinflammatory cytokine secretion in response to commensal Gram-positive bacteria in the gut.

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Respiratory viruses can modulate the Th1/Th2 balance in favor of a Th2 response, resulting in the development or exacerbation of chronic airway diseases such as asthma.
“Respiratory viruses can modulate the Th1/Th2 balance in favor of a Th2 response, resulting in the development or exacerbation of chronic airway diseases such as asthma (36, 179).”
From The airway epithelium: soldier in the fight against respiratory viruses (2011) · cites this paper as [179]

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The Extracellular Toll-like Receptor 2 Domain Directly Binds Peptidoglycan Derived from Staphylococcus aureus
Iwaki, D., Mitsuzawa, H., Murakami, S., Sano, H. I., Konishi, M., Akino, T., & Kuroki, Y. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m107057200 · Cited by 182 · see citing works
Molecular Analysis of the Microbial Diversity Present in the Colonic Wall, Colonic Lumen, and Cecal Lumen of a Pig
Pryde, S. E., Richardson, A. J., Stewart, C. S., & Flint, H. J. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.12.5372-5377.1999 · Cited by 179 · see citing works
Toll-like receptors: a growing family of immune receptors that are differentially expressed and regulated by different leukocytes
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Absence of Toll-Like Receptor 4 Explains Endotoxin Hyporesponsiveness in Human Intestinal Epithelium
Naik, S., Kelly, E. J., Meijer, L., Pettersson, S., & Sanderson, I. (2001) · Journal of Pediatric Gastroenterology and Nutrition - JPGN · doi:10.1097/00005176-200104000-00011 · Cited by 174 · see citing works
Micrococci and Peptidoglycan Activate TLR2→MyD88→IRAK→TRAF→NIK→IKK→NF-κB Signal Transduction Pathway That Induces Transcription of Interleukin-8
Wang, Q., Dziarski, R., Kirschning, C. J., Muzio, M., & Gupta, D. (2001) · Infection and Immunity · doi:10.1128/iai.69.4.2270-2276.2001 · Cited by 169 · see citing works
Probiotics and inflammatory bowel diseases
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Attachment of a noninvasive enteric pathogen, enteropathogenic Escherichia coli, to cultured human intestinal epithelial monolayers induces transmigration of neutrophils
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Glucocorticoids Synergistically Enhance NontypeableHaemophilus influenzae-induced Toll-like Receptor 2 Expression via a Negative Cross-talk with p38 MAP Kinase
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Varying cecal bacterial loads influences colitis and gastritis in HLA-B27 transgenic rats
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Modulation of barrier function during Fas-mediated apoptosis in human intestinal epithelial cells
Abreu, M. T., Palladino, A., Arnold, E. T., Kwon, R. S., & McRoberts, J. A. (2000) · Gastroenterology · doi:10.1053/gast.2000.20232 · Cited by 131 · see citing works
Self-citation
NF-κB Signaling Proteins as Therapeutic Targets for Inflammatory Bowel Diseases
Jobin, C., & Sartor, R. B. (2000) · Inflammatory Bowel Diseases · doi:10.1097/00054725-200008000-00007 · Cited by 120 · see citing works
Rectal Dialysate and Fecal Concentrations of Neutrophil Gelatinase-Associated Lipocalin, Interleukin-8, and Tumor Necrosis Factor-α in Ulcerative Colitis
Nielsen, O. H., Gionchetti, P., Ainsworth, M. A., Vainer, B., Campieri, M., Borregaard, N., & Kjeldsen, L. (1999) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.1999.01439.x · Cited by 117 · see citing works
Human intestinal epithelial cells secrete interleukin-1 receptor antagonist and interleukin-8 but not interleukin-1 or interleukin-6
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The Role of the Fecal Stream in Crohnʼs Disease: An Historical and Analytic Review
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Heat-shock protein 72 protects against oxidant-induced injury of barrier function of human colonic epithelial Caco2/bbe cells
Musch, M. W., Sugi, K., Straus, D., & Chang, E. B. (1999) · Gastroenterology · doi:10.1016/s0016-5085(99)70557-3 · Cited by 100 · see citing works
hPepT1-mediated epithelial transport of bacteria-derived chemotactic peptides enhances neutrophil-epithelial interactions.
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Evolutionary perspective on innate immune recognition
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Co-operative induction of pro-inflammatory signaling by Toll-like receptors
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High IL-13 production by human neonatal T cells: neonate immune system regulator?
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Bacterial Regulation of Intestinal Immune Responses
MacDonald, T. T., & Pettersson, S. (2000) · Inflammatory Bowel Diseases · doi:10.1097/00054725-200005000-00008 · Cited by 71 · see citing works
Molecular cross talk between epithelial cells and pathogenic microorganisms
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Extracellular Toll-Like Receptor 2 Region Containing Ser40-Ile64 but Not Cys30-Ser39 Is Critical for the Recognition ofStaphylococcus aureus Peptidoglycan
Mitsuzawa, H., Wada, I., Sano, H. I., Iwaki, D., Murakami, S., Himi, T., Matsushima, N., & Kuroki, Y. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104177200 · Cited by 58 · see citing works
Selective kallikrein-kinin system activation in inbred rats differentially susceptible to granulomatous enterocolitis
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Postoperative recurrence of Crohn's disease: The enemy is within the fecal stream
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Probiotics in chronic pouchitis: Restoring luminal microbial balance
Sartor, R. B. (2000) · Gastroenterology · doi:10.1053/gast.2000.9866 · Cited by 52 · see citing works
IMMUNOREGULATORY POTENTIAL OF UROTHELIUM: CHARACTERIZATION OF NF-κB SIGNAL TRANSDUCTION
Rackley, R. R., Bandyopadhyay, S. K., Matin, S. F., Shin, M. S., & Appell, R. A. (1999) · The Journal of Urology · doi:10.1016/s0022-5347(05)68243-2 · Cited by 50 · see citing works
REVIEW: Antibacterial Therapy for Crohn's Disease: A Review Emphasizing Therapy Directed Against Mycobacteria
Hultén, K. G., Almashhrawi, A. A., El-Zaatari, F. A., & Graham, D. Y. (2000) · Digestive Diseases and Sciences · doi:10.1023/a:1005453409445 · Cited by 47 · see citing works
Pharmacotherapy for induction and maintenance of remission in pouchitis
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Co-operative induction of pro-inflammatory signaling by Toll-like receptors
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Microbe-host interactions in the alimentary tract: the gateway to understanding inflammatory bowel disease
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Immunostimulation by the synthetic lipopeptide P3CSK4: TLR4‐independent activation of the ERK1/2 signal transduction pathway in macrophages
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Low Endogenous Prostaglandin E2 Predisposes to Relapsing Inflammation in Experimental Rat Enterocolitis
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IMMUNOREGULATORY POTENTIAL OF UROTHELIUM:
Rackley, R. R., Bandyopadhyay, S. K., Matin, S. F., Shin, M. S., & Appell, R. A. (1999) · The Journal of Urology · doi:10.1097/00005392-199911000-00075 · Cited by 6 · see citing works
Corrigendum: Animal models of mucosal inflammation and their relation to human inflammatory bowel disease
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Cutting edge: recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2.
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Signaling to NF-κB
Hayden, M. S., & Ghosh, S. (2004) · Genes & Development · doi:10.1101/gad.1228704 · Cited by 3,842 · see citing works
Inflammatory bowel disease
Abraham, C., & Cho, J. H. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0804647 · Cited by 2,712 · see citing works
Negative regulation of Toll-like receptor-mediated immune responses
Liew, F. Y., Xu, D., Brint, E. K., & O'Neill, L. A. J. (2005) · Nature Reviews Immunology · doi:10.1038/nri1630 · Cited by 1,509 · see citing works
Microbes in Gastrointestinal Health and Disease
Neish, A. S. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.10.080 · Cited by 1,388 · see citing works
Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function
Abreu, M. T. (2010) · Nature Reviews Immunology · doi:10.1038/nri2707 · Cited by 1,288 · see citing works
Self-citation
NF-κB and the immune response
Hayden, M. S., West, A. P., & Ghosh, S. (2006) · Oncogene · doi:10.1038/sj.onc.1209943 · Cited by 1,178 · see citing works
Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut
Artis, D. (2008) · Nature reviews. Immunology · doi:10.1038/nri2316 · Cited by 1,136 · see citing works
Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens
Lebeer, S., Vanderleyden, J., & De Keersmaecker, S. C. J. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2297 · Cited by 1,062 · see citing works
Signalling pathways and molecular interactions of NOD1 and NOD2
Strober, W., Murray, P. J., Kitani, A., & Watanabe, T. (2005) · Nature reviews. Immunology · doi:10.1038/nri1747 · Cited by 856 · see citing works
NOD-Like Receptors: Role in Innate Immunity and Inflammatory Disease
Chen, G., Shaw, M. H., Kim, Y., & Núñez, G. (2008) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev.pathol.4.110807.092239 · Cited by 770 · see citing works
Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function
Cario, E., Gerken, G., & Podolsky, D. K. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.02.056 · Cited by 697 · see citing works
Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier
Karczewski, J., Troost, F. J., Konings, I., Dekker, J., Kleerebezem, M., Brummer, R.-J. M., & Wells, J. M. (2010) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00327.2009 · Cited by 676 · see citing works
The airway epithelium: soldier in the fight against respiratory viruses
Vareille, M., Kieninger, E., Edwards, M. R., & Regamey, N. (2011) · Clinical Microbiology Reviews · doi:10.1128/cmr.00014-10 · Cited by 655 · see citing works
Intestinal Bacteria and the Regulation of Immune Cell Homeostasis
Hill, D. A., & Artis, D. (2010) · Annual Review of Immunology · doi:10.1146/annurev-immunol-030409-101330 · Cited by 586 · see citing works
TLR Signaling in the Gut in Health and Disease
Abreu, M. T., Fukata, M., & Arditi, M. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.8.4453 · Cited by 577 · see citing works
Self-citation
Characteristics of Intestinal Dendritic Cells in Inflammatory Bowel Diseases
Hart, A. L., Al-Hassi, H. O., Rigby, R. J., Bell, S., Emmanuel, A. V., Knight, S. C., Kamm, M. A., & Stagg, A. J. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.05.013 · Cited by 562 · see citing works
Toll-like receptor-4 is required for intestinal response to epithelial injury and limiting bacterial translocation in a murine model of acute colitis
Fukata, M., Michelsen, K. S., Eri, R. D., Thomas, L. S., Hu, B., Lukasek, K., Nast, C. C., Lechago, J., Xu, R., Naiki, Y., et al. (2005) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00328.2004 · Cited by 508 · see citing works
Self-citation
Mechanisms of cross hyporesponsiveness to toll-like receptor bacterial ligands in intestinal epithelial cells☆
Otte, J., Cario, E., & Podolsky, D. K. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.01.007 · Cited by 506 · see citing works
Recognition ofStaphylococcus aureusby the Innate Immune System
Fournier, B., & Philpott, D. J. (2005) · Clinical Microbiology Reviews · doi:10.1128/cmr.18.3.521-540.2005 · Cited by 475 · see citing works
Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C
Cario, E., Gerken, G., & Podolsky, D. K. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.04.015 · Cited by 475 · see citing works
Immune Responses to the Microbiota at the Intestinal Mucosal Surface
Duerkop, B. A., Vaishnava, S., & Hooper, L. V. (2009) · Immunity · doi:10.1016/j.immuni.2009.08.009 · Cited by 424 · see citing works
Epithelial Toll-like receptors and their role in gut homeostasis and disease
Burgueño, J. F., & Abreu, M. T. (2020) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0261-4 · Cited by 399 · see citing works
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The Roles of Bacteria and TLR4 in Rat and Murine Models of Necrotizing Enterocolitis
Jilling, T., Simon, D., Lu, J. N., Meng, F. J., Li, D., Schy, R., Thomson, R. B., Soliman, A., Arditi, M., & Caplan, M. S. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.5.3273 · Cited by 395 · see citing works
Self-citation
Commensal gut bacteria: mechanisms of immune modulation
Kelly, D., Conway, S., & Aminov, R. I. (2005) · Trends in Immunology · doi:10.1016/j.it.2005.04.008 · Cited by 394 · see citing works
β-Defensin-2 Expression Is Regulated by TLR Signaling in Intestinal Epithelial Cells
Vora, P., Youdim, A., Thomas, L. S., Fukata, M., Tesfay, S., Lukasek, K., Michelsen, K. S., Wada, A., Hirayama, T., Arditi, M., et al. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.9.5398 · Cited by 358 · see citing works
Self-citation
Toll‐like receptor (TLR) expression and TLR‐mediated cytokine/chemokine production by human uterine epithelial cells
Schaefer, T. M., Desouza, K., Fahey, J. V., Beagley, K. W., & Wira, C. R. (2004) · Immunology · doi:10.1111/j.1365-2567.2004.01898.x · Cited by 341 · see citing works
The Mechanism of Excessive Intestinal Inflammation in Necrotizing Enterocolitis: An Immature Innate Immune Response
Nanthakumar, N. N., Meng, D., Goldstein, A. M., Zhu, W., Lu, L., Uauy, R. D., Llanos, A. R., Claud, E. C., & Walker, W. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017776 · Cited by 335 · see citing works
Various human epithelial cells express functional Toll-like receptors, NOD1 and NOD2 to produce anti-microbial peptides, but not proinflammatory cytokines
Uehara, A., Fujimoto, Y., Fukase, K., & Takada, H. (2007) · Molecular Immunology · doi:10.1016/j.molimm.2007.02.007 · Cited by 330 · see citing works
The Toll–Interleukin-1 Receptor Member SIGIRR Regulates Colonic Epithelial Homeostasis, Inflammation, and Tumorigenesis
Xiao, H. Q., Gulen, M. F., Qin, J., Yao, J., Bulek, K., Kish, D. D., Altuntas, C. Z., Wald, D. N., Ma, C., Zhou, H., et al. (2007) · Immunity · doi:10.1016/j.immuni.2007.02.012 · Cited by 325 · see citing works
Toll-like receptors (TLRs) and Nod-like receptors (NLRs) in inflammatory disorders
Fukata, M., Vamadevan, A. S., & Abreu, M. T. (2009) · Seminars in Immunology · doi:10.1016/j.smim.2009.06.005 · Cited by 317 · see citing works
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The role of gut-associated lymphoid tissues and mucosal defence
Forchielli, M. L., & Walker, W. A. (2005) · British Journal Of Nutrition · doi:10.1079/bjn20041356 · Cited by 305 · see citing works
The role of TLRs, NLRs, and RLRs in mucosal innate immunity and homeostasis
Lavelle, E. C., Murphy, C. H., O'Neill, L. A. J., & Creagh, E. M. (2009) · Mucosal Immunology · doi:10.1038/mi.2009.124 · Cited by 291 · see citing works
Toll‐like receptors‐2, ‐3 and ‐4 expression patterns on human colon and their regulation by mucosal‐associated bacteria
Furrie, E., Macfarlane, S., Thomson, G., Macfarlane, G. T., & Microbiology & Gut Biology Group, T. T. &. T. B. (2005) · Immunology · doi:10.1111/j.1365-2567.2005.02200.x · Cited by 282 · see citing works
The Cytosolic Sensors Nod1 and Nod2 Are Critical for Bacterial Recognition and Host Defense after Exposure to Toll-like Receptor Ligands
Kim, Y., Park, J., Shaw, M. H., Franchi, L., Inohara, N., & Núñez, G. (2008) · Immunity · doi:10.1016/j.immuni.2007.12.012 · Cited by 280 · see citing works
Respiratory Syncytial Virus Up-regulates TLR4 and Sensitizes Airway Epithelial Cells to Endotoxin
Monick, M. M., Yarovinsky, T. O., Powers, L. S., Butler, N. S., Carter, A. B., Gudmundsson, G., & Hunninghake, G. W. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m308093200 · Cited by 276 · see citing works
Role of bacteria in health and disease of periodontal tissues
Feng, Z., & Weinberg, A. (2006) · Periodontology 2000 · doi:10.1111/j.1600-0757.2005.00148.x · Cited by 267 · see citing works
Innate Immunity in the Human Female Reproductive Tract: Antiviral Response of Uterine Epithelial Cells to the TLR3 Agonist Poly(I:C)
Schaefer, T. M., Fahey, J. V., Wright, J. A., & Wira, C. R. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.2.992 · Cited by 265 · see citing works
Toll-Like Receptors in Normal and Cystic Fibrosis Airway Epithelial Cells
Muir, A. B., Soong, G., Sokol, S., Reddy, B. D., Gómez, M. I., van Heeckeren, A. M., & Prince, A. S. (2003) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2003-0329oc · Cited by 259 · see citing works
The role of pattern recognition receptors in intestinal inflammation
Fukata, M., & Arditi, M. (2013) · Mucosal Immunology · doi:10.1038/mi.2013.13 · Cited by 255 · see citing works
Self-citation
Do symbiotic bacteria subvert host immunity?
Hooper, L. V. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2114 · Cited by 256 · see citing works
Nod1 Is an Essential Signal Transducer in Intestinal Epithelial Cells Infected with Bacteria That Avoid Recognition by Toll-Like Receptors
Kim, J. G., Lee, S. J., & Kagnoff, M. F. (2004) · Infection and Immunity · doi:10.1128/iai.72.3.1487-1495.2004 · Cited by 249 · see citing works
Epithelial MHC Class II Expression and Its Role in Antigen Presentation in the Gastrointestinal and Respiratory Tracts
Wosen, J. E., Mukhopadhyay, D., Macaubas, C., & Mellins, E. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02144 · Cited by 228 · see citing works
Multiple TLRs Are Expressed in Human Cholangiocytes and Mediate Host Epithelial Defense Responses to Cryptosporidium parvum via Activation of NF-κB
Chen, X., O’Hara, S. P., Nelson, J. B., Splinter, P. L., Small, A. J., Tietz, P. S., LIMPER, A. H., & LaRusso, N. F. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.11.7447 · Cited by 231 · see citing works
Enteroendocrine cells express functional Toll-like receptors
Bogunovic, M., Davé, S. H., Tilstra, J. S., Chang, D. T. W., Harpaz, N., Xiong, H., Mayer, L. F., & Plevy, S. E. (2007) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00249.2006 · Cited by 230 · see citing works
Expression of Functional Toll-Like Receptor-2 and -4 on Alveolar Epithelial Cells
Armstrong, L., Medford, A. R. L., Uppington, K. M., Robertson, J. F. R., Witherden, I. R., Tetley, T. D., & Millar, A. (2004) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2004-0078oc · Cited by 228 · see citing works
Toll-Like Receptors: Regulators of the Immune Response in the Human Gut
Hug, H., Mohajeri, M., & La Fata, G. (2018) · Nutrients · doi:10.3390/nu10020203 · Cited by 217 · see citing works
TLR2 is mobilized into an apical lipid raft receptor complex to signal infection in airway epithelial cells
Soong, G., Reddy, B. D., Sokol, S., Adamo, R., & Prince, A. S. (2004) · Journal of Clinical Investigation · doi:10.1172/jci20773 · Cited by 211 · see citing works
The intestinal epithelial barrier: How to distinguish between the microbial flora and pathogens
Magalhaes, J. G., Tattoli, I., & Girardin, S. E. (2007) · Seminars in Immunology · doi:10.1016/j.smim.2006.12.006 · Cited by 209 · see citing works
Intestinal epithelial barrier and mucosal immunity
Müller, C. A., Autenrieth, I. B., & Peschel, A. (2005) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-005-5034-2 · Cited by 207 · see citing works
Defects in mucosal immunity leading to Crohn's disease
Cobrin, G. M., & Abreu, M. T. (2005) · Immunological Reviews · doi:10.1111/j.0105-2896.2005.00293.x · Cited by 208 · see citing works
Self-citation
Disruption of Tight Junctions and Induction of Proinflammatory Cytokine Responses in Colonic Epithelial Cells by Campylobacter jejuni
Chen, M. L., Ge, Z., Fox, J. G., & Schauer, D. B. (2006) · Infection and Immunity · doi:10.1128/iai.00958-06 · Cited by 197 · see citing works
Differential Recognition of TLR-Dependent Microbial Ligands in Human Bronchial Epithelial Cells
Mayer, A. K., Muehmer, M., Mages, J., Gueinzius, K., Hess, C., Heeg, K. M., Bals, R., Lang, R., & Dalpke, A. H. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.5.3134 · Cited by 198 · see citing works
Tollip Regulates Proinflammatory Responses to Interleukin-1 and Lipopolysaccharide
Didierlaurent, A. M., Brissoni, B., Velin, D., Aebi, N., Tardivel, A., Käslin, E., Sirard, J., Angelov, G. S., Tschopp, J., & Burns, K. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.3.735-742.2006 · Cited by 195 · see citing works
Role of Intestinal Epithelial Cells in Immune Effects Mediated by Gram-Positive Probiotic Bacteria: Involvement of Toll-Like Receptors
Vinderola, G., Matar, C., & Perdigón, G. (2005) · Clinical and Vaccine Immunology · doi:10.1128/cdli.12.9.1075-1084.2005 · Cited by 192 · see citing works
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Authors: Melmed, G., Thomas, L. S., Lee, N., Tesfay, S. Y., Lukasek, K., Michelsen, K. S., Zhou, Y., Hu, B., Arditi, M., & Abreu, M. T.
Affiliations: Cedars-Sinai Medical Center (US)
Inflammatory Bowel Disease Center, Division of Gastroenterology, Department of Medicine , Los Angeles, CA 90048
Division of Pediatric Infectious Diseases, Department of Pediatrics, Steven Spielberg Pediatric Research Center, Burns and Allen Research Institute , Los Angeles, CA 90048
Corresponding author: Melmed, Gil
Lee, Nahee
Lukasek, Katie
ORCID: Melmed, Gil
Michelsen, Kathrin S
Zhou, Yuehua
Arditi, Moshe
Abreu, Maria T
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2003-02-01
Volume: 170
Issue: 3
Pages: 1406-1415
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.170.3.1406
OpenAlex: W1902083634
Cited by: 431
References: 103
Citations by year: 2026: 4 · 2025: 3 · 2024: 5 · 2023: 4 · 2022: 7 · 2021: 6 · 2020: 4 · 2019: 12 · 2018: 12 · 2017: 15 · 2016: 11 · 2015: 13 · 2014: 17 · 2013: 20 · 2012: 18
FWCI: 12.15
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5k08dk002635-03, 5r29ai040275-02)
National Heart, Lung, and Blood Institute (HL66436, R01HL066436)
National Institute of Allergy and Infectious Diseases (AI-40275, R29 AI52266)
National Institute of Diabetes and Digestive and Kidney Diseases (DK02635)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords: TLR2, intestinal epithelial cells, Gram-positive bacteria, Tollip, TLR6, phenol-soluble modulins, peptidoglycan, lipoteichoic acid, NF-κB activation, IL-8 secretion, commensal bacteria, mucosal immunity, colonic epithelium, lamina propria, inflammatory cytokines
MeSH terms: Bacterial Toxins, Carrier Proteins, Cell Line, Gene Expression Regulation, Humans, Immune Tolerance, Intestinal Mucosa, Ligands, Lipopolysaccharides, Membrane Glycoproteins, Peptidoglycan, Receptors, Cell Surface, RNA, Messenger, Staphylococcus aureus, Staphylococcus epidermidis, Teichoic Acids, Transfection, Tumor Cells, Cultured, Signal Transduction, Transcriptional Activation, Caco-2 Cells, HT29 Cells, Transgenes, Drosophila Proteins, Intracellular Signaling Peptides and Proteins, Toll-Like Receptors, Toll-Like Receptor 1, Toll-Like Receptor 2, Toll-Like Receptor 6

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Human Intestinal Epithelial Cells Are Broadly Unresponsive to Toll-Like Receptor 2-Dependent Bacterial Ligands: Implications for Host-Microbial Interactions in the Gut

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