Bacterial Activation of Epithelial Signaling Prof. Alice Prince
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1 rof. Alice rince Bacterial Activation of Epithelial Signaling rof. Alice rince Columbia University New York, NY 1 Introduction Airway epithelial cells recognize bacterial components in the airway lumen Signal the expression of pro inflammatory cytokines and chemokines Recruitment of MNs Recognition of bacteria by airway epithelial cells signals rapid Ca 2+ fluxes (Ratner et al., 21) What role does Ca 2+ release have in epithelial signaling? 2 CF airway MNs Mucin Bacteria E.. Greenberg 3 1
2 rof. Alice rince 1. How do epithelial cells signal the presence of bacteria in the airway? 2. Do adjacent cell communicate? How is this regulated? 3. How do MNs get to the airway lumen to eradicate the bacteria? 4 1. How do epithelial cells signal the presence of bacteria in the airway? oll-like receptors Recognition of AMs - pathogen associated molecular patterns; Conserved microbial components - DNA, LS, cell wall fragments - lipoproteins LR1 LR2 LR3 LR4 LR5 U S U - Unstimulated -. aeruginosa S - S. aureus LR6 LR7 LR8 LR9 MD2 MYD88 Actin 5 1. How do epithelial cells signal the presence of bacteria in the airway? Signaling at the cell surface ili Cell wall components Lipopeptides ulmonary pathogens S. pneumoniae S. aureus. aeruginosa B. cenocepacia pili flagella LR2 GalNAc-Gal asialogm1 NF-κB IL-8 Inflammation 6 2
3 rof. Alice rince Characteristics of airway epithelial cells LR1/2 MyD88 LR4 RIF Barrier function: no passage of macromolecules (J) Fence function: keeps apical and basolateral separate (J) olarity: apical and basolateral Gap Junction: ciliary beat frequency (Cx) Specific localization of RR s (apical, basolateral, intracellular) 7 1. How do epithelial cells signal the presence of bacteria in the airway? Bacterial activation of transcription factors NF-Κ lucifearse activity (Fold increase) * 3. * Unstimulated S. aureus. aeruginosa A-1 lucifearse activity (Fold increase) 14 * * Unstimulated S. aureus. aeruginosa -CREB * <.5 Bacterial products stimulate IL How do epithelial cells signal the presence of bacteria in the airway? Bacteria stimulate mobilization of receptors Mobilize LR2 to the cell surface NHNs. aeruginosa S. aureus agm1 Lipid receptor LR2 LR4 Relative Cell Number Cell wall fragments LS receptor 9 3
4 rof. Alice rince How is epithelial signaling coordinated? How is the recognition phase of signaling linked to the effector stage? Does Ca 2+ function as a messenger? 1 Calcium as a second messenger LR2 Ca 2+ Chemokine secretion Junctional changes MN recruitment MN paracellular migration 11 How is Ca 2+ released in the cell? Y Y I(4,5)2 I3K I(3,4,5)3 I(4,5)2 SH2 SH2 DAG I3 SH3 H LC-g1 X Y SH3 ER Ca 2+ I3R 12 4
5 rof. Alice rince LR2 stimulation mediates intracellular Ca 2+ release Untreated AA 2-AB EGA BA 8 Unstimulated 3C hapsigargin Minutes 13 R2 W Control LR Bacterial induction of Ca 2+ fluxes is LR2 dependent Unstimulated 3C hapsigargin LR2 DN LR2 Y616A/Y761A Minutes 14 ANF-κB luciferase activity C IL-8 (ng/15 µg protein) LR2 mediated Ca 2+ release signals proinflammatory responses No Inhibitor 6 μm BAA Unstim 3C haps No Inhibitor.5 mm EGA 1 mm EGA Unstim 3C B IL-8 (ng/15 µg protein) D IL-8 (ng/15 µg protein) No Inhibitor 6 μm BAA * * Unstim 3C haps rotein A No Inhibitor 75 µm 2-AB 1 µm 2-AB * Unstim 3C AO1 *p<.1, p<.1, *p<
6 rof. Alice rince Bacterial induction of NF-8B signaling is LR2 dependent 3 Fold Increase of NF-κB * * W DN Y616A/Y LR2 stimulation signals Ca 2+ fluxes C A LR2 scrambled sirna Unstimulated LR2 Actin 3C %LR scrambled LR2 sirna hapsigargin B Fold increase in IL * 4 2 scrambled LR2 sirna Scrambled LR2 sirna Minutes *p<.1 17 I3K is required for LR2 mediated Ca 2+ fluxes and IL-8 expression I:LR2-flag 1 IB s 3C IB s 3C I3K I3K Flag (LR2) Flag (LR2) 1 LY2942 Untreated Minutes IL-8 (ng/15 µg protein) No Inhibitor 5 µm LY µm LY2942 * Unstim 3C AO1 *p<.5, p<
7 rof. Alice rince LCγ is required for LR2 mediated Ca 2+ fluxes and IL-8 expression U U Inactive analog LC γ inhibitor Minutes IL-8 (ng/15 µg pr rotein) No Inhibitor.5 µm U µm U µm U73343 * * Unstim 3C AO1 *p<.5, p<.1 19 LR2 sirna LY2942 U73122 Y616 I3K Y761 Src H SH2 SH2 LC-γ1 X Y SH3 1/2 LR2 Mutant NF-κB IKB Ca 2+ BAA haps p5 65 IL-8 p5 65 Chun, J. and rince, A. J Immunol (26) 177:133 2 Junctional components of epithelial cells E-Cadherin/ZO-1 ZO-1/Cx43 Cardiovascular Research 24 May 1;62(2):
8 rof. Alice rince 2. Do adjacent cell communicate? How is this regulated? Does Ca 2+ act as an inter-cellular messenger? 22 Connexins and gap junction intercellular communication Family of >2 proteins Each member has unique permeability, expression patterns and regulation ermeable to ions and small molecules l <1 kda (Ca 2+, I3, sirna) Required for wound healing, ciliary beat frequency, spread of A in heart, surfactant secretion in alveolae Disregulated in cancer, CF, deafness 23 Connexin structural organization Biochimica et Biophysica Acta: Biomembranes 1711(2)
9 Bacterial Activation of Epithelial Signaling rof. Alice rince Hypothesis: proinflammatory signaling moves from cell to cell via gap junctions Convey Ca 2+ via gap junctions Regulated to prevent excessive proinflammatory responses Martin, F. and rince, A., J Immunol. 28 Apr 1; 18(7): Gap junction (GJ) inhibition attenuates IL-8 secretion by airway epithelial cells 26 A B C Scramble LR2 sirna Untreated Do LR2 Ca 2+ fluxes travel through gap junctions? Unstim 3C haps Fluorescence Fluorescence Fluorescenc ce D Coculture AGA Fluorescence E Apyrase Fluorescence Seconds 27 9
10 rof. Alice rince Airway cells can communicate LR2 signals via GJ But what is the functional consequence of this communication? 28 Is gap junction communication biologically significant? Mice 29 A WB: c-src py416 What is a possible mechanism for this regulation? Scramble LR2 sirna 3m 1h 2h 4h 3m 1h 2h 4h Fold increase WB: Src LR2 Cx43 Scramble LR2 sirna B I: c-src Scramble LR2 sirna 3m 1h 2h 4h 3m 1h 2h 4h Cx26 WB: Cx43 Actin WB: Src C Scramble LR2 sirna I: Cx43 2h 4h 2h 4h WB: pyr WB: Cx43 3 1
11 rof. Alice rince Unstimulated. aeruginosa (4h) 31 Calcium involvement in epithelial signaling: LR2 - dependent activation of IL-8 expression MN chemokine LR2 - dependent signaling from cell to cell via gap junctions ransient amplification of signal Is Ca 2+ involved in the recruitment of MNs from the vasculature to the airway lumen? 32. aeruginosa modifies epithelial permeability Media alone AO1 Apical Apical Basolateral Basolateral Apical Basal Apical Basal Red - Biotin-streptavidin Green -ZO
12 rof. Alice rince Occludin and E-cadherin are altered in response to. aeruginosa Media alone AO1 Media alone AO1 Occludin E-cadherin Blue - DAI 34 AO1 (heat killed) does not alter barrier properties of the airway epithelium Media alone AO1 ransepithelial resistance Dextran permeability % inoculum Bacterial invasion 35 Epithelial junctions Cingulin Occludin Actin LR2 Apical Ca2+ J AJ Claudin-1 E-Cadherin JAM-1 IL-8 IL8 Actin ZO-1 Basolateral Apical junctional complex tight junction & adherens junction Barrier: solute & macromolecules Fence Bacteria mediate changes in epithelial barrier function Modifying J and AJ proteins 36 12
13 rof. Alice rince Occludin and E-cadherin Occludin E-cadherin ight junction 4 M spanning Adherens junction Ca 2+ dependent homotypic interaction KO phenotype Form intact J ost natal growth retardation Reproductive defects Chronic Gastritis KO mice are embryonic lethal 37 Epithelial signaling modulates the properties of the junction Facilitate MN recruitment - without disrupting barrier function ostulate - activation of a selective protease argets Occludin, E-cadherin 38 Bacterial ligands activate epithelial proteases that alter barrier proteins: Ca 2+ fluxes generated by LR2 signaling Calpain - Ca 2+ activated protease Does calpain target junctional proteins? 39 13
14 rof. Alice rince Calpain is a Ca 2+ dependent protease Inactive calpain Ca 2+ Autolysis hosphorylation hospholipid binding Calpastatin Active calpain Substrates: Occludin E-cadherin Integrins Catenin MLCK 4 Calpain directly targets specific junctional proteins kd 6 Calpain 1 + Ca 2+ Calpain (min) Occludin 12 4 E-cadherin* Jam-1 22 Claudin-1 In vitro protease assay: Is from 1HAEo- airway cell lysates 41 Calpain activation in airway epithelial cells 42 14
15 rof. Alice rince LR2 dependent Calpain activation 43 Calpain association with Occludin Calpain Occludin Merge Enlarge Media I : Occludin WB: M 3C AO1 ancalpain AO1 Calpain 1 Calpain 2 Occludin 3C 44 LR2 stimulation signals calpain cleavage of Occludin 45 15
16 rof. Alice rince Bacteria mediates decrease in hyperphosphorylated Occludin I : Occludin High molecular weight Low molecular weight Cleavage product HKAO h 4h WB: Occludin WB: calpain 46 Calpain cleaves Occludin at the intracellular N-terminal tail xf: Occ myc6 RF Occ 66kD* 51kD # 88kD Not detected kd M AO1 M AO1 kd Biotin labeled Biotin labeled 66* 51 # 88 I:Neutravidin WB: myc6 WB: RF myc6 6kD myc6 6kD RF 28kD RF 28kD 47 Calpain association with E-cadherin I: Calpain kd M hapsao 12 8 E-cadherin Calpain I:E-cadherin M haps kd 12 1 Full length Cleavage product I:E-cadherin + Calpeptin M AO 3C M AO 3C kd 12 1 Full length Cleavage product 48 16
17 rof. Alice rince Does calpain change the properties of the epithelial junctions? Costar 3.µm pore transwells Epithelial monolayer Apical basolateral Basolateral Apical How is junctional permeability measured? 49 Calpain activation facilitates MN transepithelial migration 5 Calpain activity contributes to inflammation in vivo Mice % MN Wild type tlr2 -/- * BS Un Cpep BS Un Cpep AO1 AO1 *p<.5, p<.1 WB: Occludin WB: E-cadherin AO1 Untreated Calpeptin AO1 kd Control Untreated Calpeptin 6 kd Full Length Control 12 Full Length 19 Cleavage product 1 Cleavage product 51 17
18 rof. Alice rince Calpain activity contributes to inflammation in vivo 52 Occludin LR2 Ca 2+ Calpain E-cadherin IL-8 Chun, J and rince, AS, LR2-induced calpain cleavage of epithelial junctional proteins facilitates leukocyte transmigration; Cell Host Microbe 5:47-58, Calpain Ca 2+ activated in response to LR2 signaling Mediates Occludin and E-cadherin cleavage Facilitates MN migration 54 18
19 rof. Alice rince 1. How do epithelial cells signal the presence of bacteria in the airway? LR2 activation - generation of Ca 2+ fluxes 2. Do adjacent cell communicate? How is this regulated? LR2 - Ca 2+ fluxes activate t adjacent cells via gap junctions 3. How do MNs get to the airway lumen to eradicate the bacteria? LR2 activated Ca 2+ fluxes - stimulate calpain - targets junctional proteins - facilitate MN transmigration 55 Acknowledgements
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