Cathelicidin-mediated lipopolysaccharide signaling via intracellular TLR4 in colonic epithelial cells evokes CXCL8 production

References

• Kosciuczuk EM, Lisowski P, Jarczak J, Strzalkowska N, Jozwik A, Horbanczuk J, Krzyzewski J, Zwierzchowski L, Bagnicka E. Cathelicidins: family of antimicrobial peptides. A review. Mol Biol Rep. 2012;39:10957–24. doi:10.1007/s11033-012-1997-x.
   PubMed Web of Science ®Google Scholar
• Hancock RE, Haney EF, Gill EE. The immunology of host defence peptides: beyond antimicrobial activity. Nat Rev Immunol. 2016;16:321–334. doi:10.1038/nri.2016.29.
   PubMed Web of Science ®Google Scholar
• Reinholz M, Ruzicka T, Schauber J. Cathelicidin LL-37: an antimicrobial peptide with a role in inflammatory skin disease. Ann Dermatol. 2012;24:126–135. doi:10.5021/ad.2012.24.2.126.
   PubMed Web of Science ®Google Scholar
• Nizet V, Ohtake T, Lauth X, Trowbridge J, Rudisill J, Dorschner RA, Pestonjamasp V, Piraino J, Huttner K, Gallo RL. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature. 2001;414(6862):454–457. doi: 10.1038/35106587.
   PubMed Web of Science ®Google Scholar
• Coorens M, Scheenstra MR, Veldhuizen EJ, Haagsman HP. Interspecies cathelicidin comparison reveals divergence in antimicrobial activity, TLR modulation, chemokine induction and regulation of phagocytosis. Sci Rep. 2017;7(1):40874. doi: 10.1038/srep40874.
   PubMedGoogle Scholar
• Zanetti M. The role of cathelicidins in the innate host defenses of mammals. Curr Issues Mol Biol. 2005; 7(2): 179–196. http://www.ncbi.nlm.nih.gov/pubmed/16053249
   PubMed Web of Science ®Google Scholar
• Barlow PG, Svoboda P, Mackellar A, Nash AA, York IA, Pohl J, Davidson DJ, Donis RO, Kovats S. Antiviral activity and increased host defense against influenza infection elicited by the human cathelicidin LL-37. PLoS One. 2011;6(10):e25333. doi: 10.1371/journal.pone.0025333.
   PubMed Web of Science ®Google Scholar
• Alt JA, Qin X, Pulsipher A, Orb Q, Orlandi RR, Zhang J, Schults A, Jia W, Presson AP, Prestwich GD, et al. Topical cathelicidin (LL-37) an innate immune peptide induces acute olfactory epithelium inflammation in a mouse model. Int Forum Allergy Rhinol. 2015;5(12):1141–1150. doi:10.1002/alr.21634.
   PubMed Web of Science ®Google Scholar
• Kao C, Lin X, Yi G, Zhang Y, Rowe-Magnus DA, Bush K Cathelicidin antimicrobial peptides with reduced activation of Toll-like receptor signaling have potent bactericidal activity against colistin-resistant bacteria. mBio 2016; 7. doi: 10.1128/mBio.01418-16.
   PubMed Web of Science ®Google Scholar
• Scheenstra MR, van den Belt M, Tjeerdsma-van Bokhoven JLM, Schneider VAF, Ordonez SR, van Dijk A, Veldhuizen EJA, Haagsman HP. Cathelicidins PMAP-36, LL-37 and CATH-2 are similar peptides with different modes of action. Sci Rep. 2019;9:4780. 10.1038/s41598-019-41246-6
   PubMed Web of Science ®Google Scholar
• Bommineni YR, Dai H, Gong YX, Soulages JL, Fernando SC, Desilva U, Prakash O, Zhang G. Fowlicidin-3 is an alpha-helical cationic host defense peptide with potent antibacterial and lipopolysaccharide-neutralizing activities. The FEBS Journal. 2007;274:418–428. doi:10.1111/j.1742-4658.2006.05589.x.
   PubMed Web of Science ®Google Scholar
• Smith JJ, Travis SM, Greenberg EP, Welsh MJ. Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid. Cell. 1996;85:229–236. doi:10.1016/s0092-8674(00)81099-5.
   PubMed Web of Science ®Google Scholar
• Scott A, Weldon S, Buchanan PJ, Schock B, Ernst RK, McAuley DF, Tunney MM, Irwin CR, Elborn JS, Taggart CC. Evaluation of the ability of LL-37 to neutralise LPS in vitro and ex vivo. PLoS One. 2011;6:e26525. doi:10.1371/journal.pone.0026525.
   PubMed Web of Science ®Google Scholar
• Guo L, Lim KB, Poduje CM, Daniel M, Gunn JS, Hackett M, Miller SI. Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell. 1998;95:189–198. doi:10.1016/s0092-8674(00)81750-x.
   PubMed Web of Science ®Google Scholar
• Bowdish DM, Davidson DJ, Speert DP, Hancock RE. The human cationic peptide LL-37 induces activation of the extracellular signal-regulated kinase and p38 kinase pathways in primary human monocytes. J Immunol. 2004;172:3758–3765. doi:10.4049/jimmunol.172.6.3758.
   PubMed Web of Science ®Google Scholar
• Mookherjee N, Hamill P, Gardy J, Blimkie D, Falsafi R, Chikatamarla A, Arenillas DJ, Doria S, Kollmann TR, Hancock RE Systems biology evaluation of immune responses induced by human host defence peptide LL-37 in mononuclear cells. Mol Biosyst 2009; 5:483–496. doi: 10.1039/b813787k.
   PubMedGoogle Scholar
• Scott MG, Davidson DJ, Gold MR, Bowdish D, Hancock RE. The human antimicrobial peptide LL-37 is a multifunctional modulator of innate immune responses. J Immunol. 2002;169:3883–3891. doi:10.4049/jimmunol.169.7.3883.
   PubMed Web of Science ®Google Scholar
• Tjabringa GS, Ninaber DK, Drijfhout JW, Rabe KF, Hiemstra PS. Human cathelicidin LL-37 is a chemoattractant for eosinophils and neutrophils that acts via formyl-peptide receptors. Int Arch Allergy Immunol. 2006;140:103–112. doi:10.1159/000092305.
   PubMed Web of Science ®Google Scholar
• Kurosaka K, Chen Q, Yarovinsky F, Oppenheim JJ, Yang D. Mouse cathelin-related antimicrobial peptide chemoattracts leukocytes using formyl peptide receptor-like 1/mouse formyl peptide receptor-like 2 as the receptor and acts as an immune adjuvant. J Immunol. 2005;174:6257–6265. doi:10.4049/jimmunol.174.10.6257.
   PubMed Web of Science ®Google Scholar
• Beaumont PE, McHugh B, Gwyer Findlay E, Mackellar A, Mackenzie KJ, Gallo RL, Govan JR, Simpson AJ, Davidson DJ. Cathelicidin host defence peptide augments clearance of pulmonary Pseudomonas aeruginosa infection by its influence on neutrophil function in vivo. PLoS One. 2014;9:e99029. doi:10.1371/journal.pone.0099029.
   PubMedGoogle Scholar
• Tjabringa GS, Aarbiou J, Ninaber DK, Drijfhout JW, Sorensen OE, Borregaard N, Rabe KF, Hiemstra PS. The antimicrobial peptide LL-37 activates innate immunity at the airway epithelial surface by transactivation of the epidermal growth factor receptor. J Immunol. 2003;171:6690–6696. doi:10.4049/jimmunol.171.12.6690.
   PubMed Web of Science ®Google Scholar
• Abreu MT, Vora P, Faure E, Thomas LS, Arnold ET, Arditi M. Decreased expression of Toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. J Immunol. 2001;167:1609–1616. doi:10.4049/jimmunol.167.3.1609.
   PubMed Web of Science ®Google Scholar
• Khan MA, Ma C, Knodler LA, Valdez Y, Rosenberger CM, Deng W, Finlay BB, Vallance BA. Toll-like receptor 4 contributes to colitis development but not to host defense during Citrobacter rodentium infection in mice. Infect Immun. 2006;74:2522–2536. doi:10.1128/IAI.74.5.2522-2536.2006.
   PubMed Web of Science ®Google Scholar
• Mumy KL, McCormick BA. The role of neutrophils in the event of intestinal inflammation. Curr Opin Pharmacol. 2009;9:697–701. doi:10.1016/j.coph.2009.10.004.
   PubMed Web of Science ®Google Scholar
• Cheminay C, Chakravortty D, Hensel M. Role of neutrophils in murine salmonellosis. Infect Immun. 2004;72:468–477. doi:10.1128/IAI.72.1.468-477.2004.
   PubMed Web of Science ®Google Scholar
• Maier L, Diard M, Sellin ME, Chouffane ES, Trautwein-Weidner K, Periaswamy B, Slack E, Dolowschiak T, Stecher B, Loverdo C, et al. Granulocytes impose a tight bottleneck upon the gut luminal pathogen population during Salmonella typhimurium colitis. PLoS Pathog. 2014;10:e1004557. doi:10.1371/journal.ppat.1004557.
   PubMed Web of Science ®Google Scholar
• Lebeis SL, Bommarius B, Parkos CA, Sherman MA, Kalman D. TLR signaling mediated by MyD88 is required for a protective innate immune response by neutrophils to Citrobacter rodentium. J Immunol. 2007;179:566–577. doi:10.4049/jimmunol.179.1.566.
   PubMed Web of Science ®Google Scholar
• De Filippo K, Dudeck A, Hasenberg M, Nye E, van Rooijen N, Hartmann K, Gunzer M, Roers A, Hogg N. Mast cell and macrophage chemokines CXCL1/CXCL2 control the early stage of neutrophil recruitment during tissue inflammation. Blood. 2013;121:4930–4937. doi:10.1182/blood-2013-02-486217.
   PubMed Web of Science ®Google Scholar
• Spehlmann ME, Dann SM, Hruz P, Hanson E, McCole DF, Eckmann L. CXCR2-dependent mucosal neutrophil influx protects against colitis-associated diarrhea caused by an attaching/effacing lesion-forming bacterial pathogen. J Immunol. 2009;183:3332–3343. doi:10.4049/jimmunol.0900600.
   PubMed Web of Science ®Google Scholar
• Im E, Riegler FM, Pothoulakis C, Rhee SH. Elevated lipopolysaccharide in the colon evokes intestinal inflammation, aggravated in immune modulator-impaired mice. Am J Physiol Gastrointest Liver Physiol. 2012;303:G490–7. doi:10.1152/ajpgi.00120.2012.
   PubMed Web of Science ®Google Scholar
• Otte JM, Cario E, Podolsky DK. Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology. 2004;126:1054–1070. doi:10.1053/j.gastro.2004.01.007.
   PubMed Web of Science ®Google Scholar
• Koon HW, Shih DQ, Chen J, Bakirtzi K, Hing TC, Law I, Ho S, Ichikawa R, Zhao D, Xu H, et al. Cathelicidin signaling via the Toll-like receptor protects against colitis in mice. Gastroenterology. 2011;141:1852–63 e1-3. doi:10.1053/j.gastro.2011.06.079.
   PubMed Web of Science ®Google Scholar
• Hing TC, Ho S, Shih DQ, Ichikawa R, Cheng M, Chen J, Chen X, Law I, Najarian R, Kelly CP, et al. The antimicrobial peptide cathelicidin modulates Clostridium difficile-associated colitis and toxin A-mediated enteritis in mice. Gut. 2013;62:1295–1305. doi:10.1136/gutjnl-2012-302180.
   PubMed Web of Science ®Google Scholar
• De Y, Chen Q, Schmidt AP, Anderson GM, Wang JM, Wooters J, Oppenheim JJ, Chertov O. LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J Exp Med. 2000;192:1069–1074. doi:10.1084/jem.192.7.1069.
   PubMed Web of Science ®Google Scholar
• Sharba S, Venkatakrishnan V, Padra M, Winther M, Gabl M, Sundqvist M, Wang J, Forsman H, Linden SK. Formyl peptide receptor 2 orchestrates mucosal protection against Citrobacter rodentium infection. Virulence. 2019;10:610–624. doi:10.1080/21505594.2019.1635417.
   PubMed Web of Science ®Google Scholar
• Bruno VM, Hannemann S, Lara-Tejero M, Flavell RA, Kleinstein SH, Galan JE. Salmonella Typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog. 2009;5:e1000538. doi:10.1371/journal.ppat.1000538.
   PubMed Web of Science ®Google Scholar
• Moxley RA, Smith DR. Attaching-effacing Escherichia coli infections in cattle. Vet Clin North Am Food Anim Pract. 2010;26:29–56. table of contents. doi:10.1016/j.cvfa.2009.10.011.
   PubMed Web of Science ®Google Scholar
• Hase K, Eckmann L, Leopard JD, Varki N, Kagnoff MF. Cell differentiation is a key determinant of cathelicidin LL-37/human cationic antimicrobial protein 18 expression by human colon epithelium. Infect Immun. 2002;70:953–963. doi:10.1128/IAI.70.2.953-963.2002.
   PubMed Web of Science ®Google Scholar
• Zhang J, Jiao Y, Hou S, Tian T, Yuan Q, Hao H, Wu Z, Bao X. S100A4 contributes to colitis development by increasing the adherence of Citrobacter rodentium in intestinal epithelial cells. Sci Rep. 2017;7:12099. 10.1038/s41598-017-12256-z
   PubMed Web of Science ®Google Scholar
• Marin M, Holani R, Shah CB, Odeon A, Cobo ER. Cathelicidin modulates synthesis of Toll-like receptors (TLRs) 4 and 9 in colonic epithelium. Mol Immunol. 2017;91:249–258. doi:10.1016/j.molimm.2017.09.011.
   PubMed Web of Science ®Google Scholar
• Marin M, Holani R, Blyth GAD, Drouin D, Odeon A, Cobo ER. Human cathelicidin improves colonic epithelial defenses against Salmonella Typhimurium by modulating bacterial invasion, TLR4 and pro-inflammatory cytokines. Cell Tissue Res. 2019;376(3):433–442. 10.1007/s00441-018-02984-7
   PubMed Web of Science ®Google Scholar
• Price AE, Shamardani K, Lugo KA, Deguine J, Roberts AW, Lee BL, Barton GM. A map of toll-like receptor expression in the intestinal epithelium reveals distinct spatial, cell type-specific, and temporal patterns. Immunity. 2018;49(3):560–75 e6. doi: 10.1016/j.immuni.2018.07.016.
   PubMed Web of Science ®Google Scholar
• Hornef MW, Frisan T, Vandewalle A, Normark S, Richter-Dahlfors A. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med. 2002;195(5):559–570. doi:10.1084/jem.20011788.
   PubMed Web of Science ®Google Scholar
• Seil M, Nagant C, Dehaye J-P, Vandenbranden M, Lensink MF. Spotlight on human LL-37, an immunomodulatory peptide with promising cell-penetrating properties. Pharmaceuticals (Basel). 2010;3(11):3435–3460. doi:10.3390/ph3113435.
   Google Scholar
• Hollenberg MD, Fishman PH, Bennett V, Cuatrecasas P. Cholera toxin and cell growth: role of membrane gangliosides. Proc Natl Acad Sci U S A. 1974;71(10):4224–4228. doi:10.1073/pnas.71.10.4224.
   PubMed Web of Science ®Google Scholar
• Bennett V, Craig S, Hollenberg MD, O’Keefe E, Sahyoun N, Cuatrecasas P. Structure and function of cholera toxin and hormone receptors. J Supramol Struct. 1976;4(1):99–120. doi: 10.1002/jss.400040110.
   PubMedGoogle Scholar
• Shaykhiev R, Sierigk J, Herr C, Krasteva G, Kummer W, Bals R. The antimicrobial peptide cathelicidin enhances activation of lung epithelial cells by LPS. Faseb J. 2010;24(12):4756–4766. doi: 10.1096/fj.09-151332.
   PubMed Web of Science ®Google Scholar
• Hagar JA, Powell DA, Aachoui Y, Ernst RK, Miao EA. Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science. 2013;341(6151):1250–1253. doi: 10.1126/science.1240988.
   PubMed Web of Science ®Google Scholar
• Toumi F, Neunlist M, Denis MG, Oreshkova T, Laboisse CL, Galmiche J-P, Jarry A. Vasoactive intestinal peptide induces IL-8 production in human colonic epithelial cells via MAP kinase-dependent and PKA-independent pathways. Biochem Biophys Res Commun. 2004;317(1):187–191. doi: 10.1016/j.bbrc.2004.03.033.
   PubMed Web of Science ®Google Scholar
• De S, Zhou H, DeSantis D, Croniger CM, Li X, Stark GR. Erlotinib protects against LPS-induced endotoxicity because TLR4 needs EGFR to signal. Proc Natl Acad Sci U S A. 2015;112(31):9680–9685. doi: 10.1073/pnas.1511794112.
   PubMed Web of Science ®Google Scholar
• Verjans E-T, Zels S, Luyten W, Landuyt B, Schoofs L. Molecular mechanisms of LL-37-induced receptor activation: an overview. Peptides. 2016;85:16–26. doi:10.1016/j.peptides.2016.09.002.
   PubMed Web of Science ®Google Scholar
• Mukaida N, Okamoto S, Ishikawa Y, Matsushima K. Molecular mechanism of interleukin-8 gene expression. J Leukoc Biol. 1994;56(5):554–558. doi:10.1002/jlb.56.5.554.
   PubMed Web of Science ®Google Scholar
• Wiehler S, Proud D. Interleukin-17A modulates human airway epithelial responses to human rhinovirus infection. Am J Physiol Lung Cell Mol Physiol. 2007;293(2):L505–L15. doi: 10.1152/ajplung.00066.2007.
   PubMed Web of Science ®Google Scholar
• Wu D, LaRosa GJ, Simon MI. G protein-coupled signal transduction pathways for interleukin-8. Science. 1993;261(5117):101–103. doi:10.1126/science.8316840.
   PubMed Web of Science ®Google Scholar
• Gupta AK, Giaglis S, Hasler P, Hahn S, Palaniyar N. Efficient neutrophil extracellular trap induction requires mobilization of both intracellular and extracellular calcium pools and is modulated by cyclosporine A. PLoS One. 2014;9(5):e97088. doi: 10.1371/journal.pone.0097088.
   PubMed Web of Science ®Google Scholar
• Brinkmann V. Neutrophil extracellular traps kill bacteria. Science. 2004;303(5663):1532–1535. doi: 10.1126/science.1092385.
   PubMed Web of Science ®Google Scholar
• Mann EA, Harmel-Laws E, Cohen MB, Steinbrecher KA. Guanylate cyclase C limits systemic dissemination of a murine enteric pathogen. BMC Gastroenterol. 2013;13(1):135. doi: 10.1186/1471-230X-13-135.
   PubMedGoogle Scholar
• Iimura M, Gallo RL, Hase K, Miyamoto Y, Eckmann L, Kagnoff MF. Cathelicidin mediates innate intestinal defense against colonization with epithelial adherent bacterial pathogens. J Immunol. 2005;174(8):4901–4907. doi:10.4049/jimmunol.174.8.4901.
   PubMed Web of Science ®Google Scholar
• Szabady RL, McCormick BA. Control of neutrophil inflammation at mucosal surfaces by secreted epithelial products. Front Immunol. 2013;4:220. doi:10.3389/fimmu.2013.00220.
   PubMed Web of Science ®Google Scholar
• Thorsvik S, Bakke I, van Beelen Granlund A, Royset ES, Damas JK, Ostvik AE, Sandvik AK. Expression of neutrophil gelatinase-associated lipocalin (NGAL) in the gut in Crohn’s disease. Cell and Tissue Research. 2018;374(2):339–348. 10.1007/s00441-018-2860-8
   PubMed Web of Science ®Google Scholar
• Lee Y-S, Yang H, Yang J-Y, Kim Y, Lee S-H, Kim JH, Jang YJ, Vallance BA, Kweon M-N, Bäumler AJ. Interleukin-1 (IL-1) signaling in intestinal stromal cells controls KC/CXCL1 secretion, which correlates with recruitment of IL-22-secreting neutrophils at early stages of Citrobacter rodentium infection. Infect Immun. 2015;83(8):3257–3267. doi: 10.1128/IAI.00670-15.
   PubMed Web of Science ®Google Scholar
• Kamada N, Sakamoto K, Seo S-U, Zeng M, Kim Y-G, Cascalho M, Vallance BA, Puente JL, Nunez G. Humoral immunity in the gut selectively targets phenotypically virulent attaching-and-effacing bacteria for intraluminal elimination. Cell Host Microbe. 2015;17(5):617–627. doi: 10.1016/j.chom.2015.04.001.
   PubMed Web of Science ®Google Scholar
• Kovach MA, Ballinger MN, Newstead MW, Zeng X, Bhan U, Yu F-S, Moore BB, Gallo RL, Standiford TJ. Cathelicidin-related antimicrobial peptide is required for effective lung mucosal immunity in Gram-negative bacterial pneumonia. J Immunol. 2012;189(1):304–311. doi: 10.4049/jimmunol.1103196.
   PubMed Web of Science ®Google Scholar
• Coorens M, Schneider VAF, de Groot AM, van Dijk A, Meijerink M, Wells JM, Scheenstra MR, Veldhuizen EJA, Haagsman HP. Cathelicidins inhibit Escherichia coli –induced TLR2 and TLR4 activation in a viability-dependent manner. J Immunol. 2017;199(4):1418–1428. doi: 10.4049/jimmunol.1602164.
   PubMed Web of Science ®Google Scholar
• Mookherjee N, Brown KL, Bowdish DM, Doria S, Falsafi R, Hokamp K, Roche FM, Mu R, Doho GH, Pistolic J, et al. Modulation of the TLR-mediated inflammatory response by the endogenous human host defense peptide LL-37. J Immunol. 2006;176(4):2455–2464.doi:10.4049/jimmunol.176.4.2455.
   PubMed Web of Science ®Google Scholar
• Cirioni O, Giacometti A, Ghiselli R, Bergnach C, Orlando F, Silvestri C, Mocchegiani F, Licci A, Skerlavaj B, Rocchi M, et al. LL-37 protects rats against lethal sepsis caused by gram-negative bacteria. Antimicrob Agents Chemother. 2006;50(5):1672–1679. doi:10.1128/AAC.50.5.1672-1679.2006.
   PubMed Web of Science ®Google Scholar
• Hemshekhar M, Choi KYG, Mookherjee N. Host defense peptide LL-37-mediated chemoattractant properties, but not anti-inflammatory cytokine IL-1RA production, is selectively controlled by Cdc42 Rho GTPase via G protein-coupled receptors and JNK mitogen-activated protein kinase. Front Immunol. 2018;9:1871. doi:10.3389/fimmu.2018.01871.
   PubMed Web of Science ®Google Scholar
• De Oliveira S, Rosowski EE, Huttenlocher A. Neutrophil migration in infection and wound repair: going forward in reverse. Nat Rev Immunol. 2016;16(6):378–391. doi: 10.1038/nri.2016.49.
   PubMed Web of Science ®Google Scholar
• Sakoulas G, Kumaraswamy M, Kousha A, Nizet V Interaction of antibiotics with innate host defense factors against Salmonella enterica serotype newport. mSphere 2017; 2. doi: 10.1128/mSphere.00410-17
   PubMed Web of Science ®Google Scholar
• Lande R, Gregorio J, Facchinetti V, Chatterjee B, Wang Y-H, Homey B, Cao W, Wang Y-H, Su B, Nestle FO, et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature. 2007;449(7162):564–569. doi:10.1038/nature06116.
   PubMed Web of Science ®Google Scholar
• Filewod NC, Pistolic J, Hancock RE. Low concentrations of LL-37 alter IL-8 production by keratinocytes and bronchial epithelial cells in response to proinflammatory stimuli. FEMS Immunol Med Microbiol. 2009;56(3):233–240. doi: 10.1111/j.1574-695X.2009.00571.x.
   PubMedGoogle Scholar
• Lai Y, Adhikarakunnathu S, Bhardwaj K, Ranjith-Kumar CT, Wen Y, Jordan JL, Wu LH, Dragnea B, San Mateo L, Kao CC. LL37 and cationic peptides enhance TLR3 signaling by viral double-stranded RNAs. PLoS One. 2011;6(10):e26632. doi: 10.1371/journal.pone.0026632.
   PubMed Web of Science ®Google Scholar
• Vanaja SK, Russo AJ, Behl B, Banerjee I, Yankova M, Deshmukh SD, Rathinam VK. Bacterial outer membrane vesicles mediate cytosolic localization of LPS and caspase-11 activation. Cell. 2016;165(5):1106–1119. doi: 10.1016/j.cell.2016.04.015.
   PubMed Web of Science ®Google Scholar
• Meng D, Zhu W, Shi HN, Lu L, Wijendran V, Xu W, Walker WA. Toll-like receptor-4 in human and mouse colonic epithelium is developmentally regulated: a possible role in necrotizing enterocolitis. Pediatr Res. 2015;77(3):416–424. doi: 10.1038/pr.2014.207.
   PubMed Web of Science ®Google Scholar
• Abreu MT, Arnold ET, Thomas LS, Gonsky R, Zhou Y, Hu B, Arditi M. TLR4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells. J Biol Chem. 2002;277(23):20431–20437. doi: 10.1074/jbc.M110333200.
   PubMed Web of Science ®Google Scholar
• Vamadevan AS, Fukata M, Arnold ET, Thomas LS, Hsu D, Abreu MT. Regulation of toll-like receptor 4-associated MD-2 in intestinal epithelial cells: a comprehensive analysis. Innate Immunity. 2010;16(2):93–103. doi: 10.1177/1753425909339231.
   PubMed Web of Science ®Google Scholar
• Grondin V, Seksik P, Dumont S, Thomas G, Trugnan G, Flejou JF, Masliah J, Wendum D, Bachelet M. Regulation of colon cancer cell proliferation and migration by MD-2 activity. Innate Immunity. 2011;17(4):414–422. doi: 10.1177/1753425910375583.
   PubMed Web of Science ®Google Scholar
• Bocker U, Yezerskyy O, Feick P, Manigold T, Panja A, Kalina U, Herweck F, Rossol S, Singer MV. Responsiveness of intestinal epithelial cell lines to lipopolysaccharide is correlated with toll-like receptor 4 but not toll-like receptor 2 or CD14 expression. Int J Colorectal Dis. 2003;18(1):25–32. doi: 10.1007/s00384-002-0415-6.
   PubMed Web of Science ®Google Scholar
• Eckmann L, Jung HC, Schurer-Maly C, Panja A, Morzycka-Wroblewska E, Kagnoff MF. Differential cytokine expression by human intestinal epithelial cell lines: regulated expression of interleukin 8. Gastroenterology. 1993;105(6):1689–1697. doi: 10.1016/0016-5085(93)91064-O.
   PubMed Web of Science ®Google Scholar
• Bociek K, Ferluga S, Mardirossian M, Benincasa M, Tossi A, Gennaro R, Scocchi M. Lipopolysaccharide phosphorylation by the WaaY Kinase affects the susceptibility of Escherichia coli to the human antimicrobial peptide LL-37. J Biol Chem. 2015;290(32):19933–19941. doi: 10.1074/jbc.M114.634758.
   PubMed Web of Science ®Google Scholar
• Wang G. Structures of human host defense cathelicidin LL-37 and its smallest antimicrobial peptide KR-12 in lipid micelles. J Biol Chem. 2008;283(47):32637–32643. doi: 10.1074/jbc.M805533200.
   PubMed Web of Science ®Google Scholar
• Yamasaki K, Di Nardo A, Bardan A, Murakami M, Ohtake T, Coda A, Dorschner RA, Bonnart C, Descargues P, Hovnanian A, et al. Increased serine protease activity and cathelicidin promotes skin inflammation in rosacea. Nat Med. 2007;13(8):975–980. doi:10.1038/nm1616.
   PubMed Web of Science ®Google Scholar
• Hornef MW, Normark BH, Vandewalle A, Normark S. Intracellular recognition of lipopolysaccharide by toll-like receptor 4 in intestinal epithelial cells. J Exp Med. 2003;198(8):1225–1235. doi: 10.1084/jem.20022194.
   PubMed Web of Science ®Google Scholar
• Jijon HB, Panenka WJ, Madsen KL, Parsons HG. MAP kinases contribute to IL-8 secretion by intestinal epithelial cells via a posttranscriptional mechanism. Am J Physiol Cell Physiol. 2002;283(1):C31–41. doi: 10.1152/ajpcell.00113.2001.
   PubMed Web of Science ®Google Scholar
• Nakayama H, Fukuda S, Matsushita N, Nishida-Fukuda H, Inoue H, Shirakata Y, Hashimoto K, Higashiyama S. Human antigen R-mediated mRNA stabilization is required for ultraviolet B-induced autoinduction of amphiregulin in keratinocytes. J Biol Chem. 2013;288(15):10338–10348. doi: 10.1074/jbc.M112.417527.
   PubMed Web of Science ®Google Scholar
• Pinheiro da Silva F, Gallo RL, Nizet V. Differing effects of exogenous or endogenous cathelicidin on macrophage toll-like receptor signaling. Immunol Cell Biol. 2009;87(6):496–500. doi: 10.1038/icb.2009.19.
   PubMed Web of Science ®Google Scholar
• Kishida K, Kohyama M, Kurashima Y, Kogure Y, Wang J, Hirayasu K, Suenaga T, Kiyono H, Kunisawa J, Arase H. Negative regulation of DSS-induced experimental colitis by PILRα. Int Immunol. 2015;27(6):307–314. doi: 10.1093/intimm/dxv004.
   PubMed Web of Science ®Google Scholar
• Dann SM, Eckmann L. Innate immune defenses in the intestinal tract. Curr Opin Gastroenterol. 2007;23(2):115–120. doi: 10.1097/MOG.0b013e32803cadf4.
   PubMed Web of Science ®Google Scholar
• Vong L, Pinnell LJ, Maattanen P, Yeung CW, Lurz E, Sherman PM. Selective enrichment of commensal gut bacteria protects against Citrobacter rodentium induced colitis. Am J Physiol Gastrointest Liver Physiol. 2015;309(3):G181–92. doi: 10.1152/ajpgi.00053.2015.
   PubMed Web of Science ®Google Scholar
• Hansen KK, Sherman PM, Cellars L, Andrade-Gordon P, Pan Z, Baruch A, Wallace JL, Hollenberg MD, Vergnolle N. A major role for proteolytic activity and proteinase-activated receptor-2 in the pathogenesis of infectious colitis. Proc Natl Acad Sci U S A. 2005;102(23):8363–8368. doi: 10.1073/pnas.0409535102.
   PubMed Web of Science ®Google Scholar
• Pan D, Das A, Liu D, Veazey RS, Pahar B, Shoukry NH. Isolation and characterization of intestinal epithelial cells from normal and SIV-infected rhesus macaques. PLoS One. 2012;7(1):e30247. doi: 10.1371/journal.pone.0030247.
   PubMed Web of Science ®Google Scholar
• Sagaidak S, Taibi A, Wen B, Comelli EM. Development of a real-time PCR assay for quantification of Citrobacter rodentium. J Microbiol Methods. 2016;126:76–77. doi:10.1016/j.mimet.2016.05.008.
   PubMed Web of Science ®Google Scholar
• Fernando EH, Dicay M, Stahl M, Gordon MH, Vegso A, Baggio C, Alston L, Lopes F, Baker K, Hirota S, et al. A simple, cost-effective method for generating murine colonic 3D enteroids and 2D monolayers for studies of primary epithelial cell function. Am J Physiol Gastrointest Liver Physiol. 2017;313(5):G467–G75. doi:10.1152/ajpgi.00152.2017.
   PubMed Web of Science ®Google Scholar
• Weischenfeldt J, Porse B Bone Marrow-Derived Macrophages (BMM): isolation and applications. CSH Protoc 2008; 2008:pdb prot5080. doi: 10.1101/pdb.prot5080
   PubMedGoogle Scholar
• Starr T, Bauler TJ, Malik-Kale P, Steele-Mortimer O, Ko DC. The phorbol 12-myristate-13-acetate differentiation protocol is critical to the interaction of THP-1 macrophages with Salmonella typhimurium. PLoS One. 2018;13(3):e0193601. doi: 10.1371/journal.pone.0193601.
   PubMed Web of Science ®Google Scholar
• Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, Connelly PA. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J Biol Chem. 1996;271(2):695–701. doi: 10.1074/jbc.271.2.695.
   PubMed Web of Science ®Google Scholar
• Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009;55(4):611–622. doi:10.1373/clinchem.2008.112797.
   PubMed Web of Science ®Google Scholar