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Inflammation without pain: Immune-derived opioids hold the key.

Carbone SE, Poole DP.

Neurogastroenterol Motil. 2020 Feb;32(2):e13787. doi: 10.1111/nmo.13787. Review.


Internalized GPCRs as Potential Therapeutic Targets for the Management of Pain.

Retamal JS, Ramírez-García PD, Shenoy PA, Poole DP, Veldhuis NA.

Front Mol Neurosci. 2019 Nov 12;12:273. doi: 10.3389/fnmol.2019.00273. eCollection 2019.


Mu and Delta Opioid Receptors Are Coexpressed and Functionally Interact in the Enteric Nervous System of the Mouse Colon.

DiCello JJ, Carbone SE, Saito A, Rajasekhar P, Ceredig RA, Pham V, Valant C, Christopoulos A, Veldhuis NA, Canals M, Massotte D, Poole DP.

Cell Mol Gastroenterol Hepatol. 2020;9(3):465-483. doi: 10.1016/j.jcmgh.2019.11.006. Epub 2019 Nov 20.


A pH-responsive nanoparticle targets the neurokinin 1 receptor in endosomes to prevent chronic pain.

Ramírez-García PD, Retamal JS, Shenoy P, Imlach W, Sykes M, Truong N, Constandil L, Pelissier T, Nowell CJ, Khor SY, Layani LM, Lumb C, Poole DP, Lieu T, Stewart GD, Mai QN, Jensen DD, Latorre R, Scheff NN, Schmidt BL, Quinn JF, Whittaker MR, Veldhuis NA, Davis TP, Bunnett NW.

Nat Nanotechnol. 2019 Dec;14(12):1150-1159. doi: 10.1038/s41565-019-0568-x. Epub 2019 Nov 4.


Activation of pruritogenic TGR5, MrgprA3, and MrgprC11 on colon-innervating afferents induces visceral hypersensitivity.

Castro J, Harrington AM, Lieu T, Garcia-Caraballo S, Maddern J, Schober G, O'Donnell T, Grundy L, Lumsden AL, Miller P, Ghetti A, Steinhoff MS, Poole DP, Dong X, Chang L, Bunnett NW, Brierley SM.

JCI Insight. 2019 Oct 17;4(20). pii: 131712. doi: 10.1172/jci.insight.131712.


Application of a chemical probe to detect neutrophil elastase activation during inflammatory bowel disease.

Anderson BM, Poole DP, Aurelio L, Ng GZ, Fleischmann M, Kasperkiewicz P, Morissette C, Drag M, van Driel IR, Schmidt BL, Vanner SJ, Bunnett NW, Edgington-Mitchell LE.

Sci Rep. 2019 Sep 16;9(1):13295. doi: 10.1038/s41598-019-49840-4.


Protein kinase D and Gβγ mediate sustained nociceptive signaling by biased agonists of protease-activated receptor-2.

Zhao P, Pattison LA, Jensen DD, Jimenez-Vargas NN, Latorre R, Lieu T, Jaramillo JO, Lopez-Lopez C, Poole DP, Vanner SJ, Schmidt BL, Bunnett NW.

J Biol Chem. 2019 Jul 5;294(27):10649-10662. doi: 10.1074/jbc.RA118.006935. Epub 2019 May 29.


Clathrin and GRK2/3 inhibitors block δ-opioid receptor internalization in myenteric neurons and inhibit neuromuscular transmission in the mouse colon.

DiCello JJ, Rajasekhar P, Eriksson EM, Saito A, Gondin AB, Veldhuis NA, Canals M, Carbone SE, Poole DP.

Am J Physiol Gastrointest Liver Physiol. 2019 Aug 1;317(2):G79-G89. doi: 10.1152/ajpgi.00085.2019. Epub 2019 May 15.


Agonist-dependent development of delta opioid receptor tolerance in the colon.

DiCello JJ, Saito A, Rajasekhar P, Sebastian BW, McQuade RM, Gondin AB, Veldhuis NA, Canals M, Carbone SE, Poole DP.

Cell Mol Life Sci. 2019 Aug;76(15):3033-3050. doi: 10.1007/s00018-019-03077-6. Epub 2019 Mar 23.


G-Protein-Coupled Receptors Are Dynamic Regulators of Digestion and Targets for Digestive Diseases.

Canals M, Poole DP, Veldhuis NA, Schmidt BL, Bunnett NW.

Gastroenterology. 2019 May;156(6):1600-1616. doi: 10.1053/j.gastro.2019.01.266. Epub 2019 Feb 13. Review.


G protein-coupled receptor trafficking and signaling: new insights into the enteric nervous system.

Carbone SE, Veldhuis NA, Gondin AB, Poole DP.

Am J Physiol Gastrointest Liver Physiol. 2019 Apr 1;316(4):G446-G452. doi: 10.1152/ajpgi.00406.2018. Epub 2019 Jan 31. Review.


Protease-activated receptor-2 in endosomes signals persistent pain of irritable bowel syndrome.

Jimenez-Vargas NN, Pattison LA, Zhao P, Lieu T, Latorre R, Jensen DD, Castro J, Aurelio L, Le GT, Flynn B, Herenbrink CK, Yeatman HR, Edgington-Mitchell L, Porter CJH, Halls ML, Canals M, Veldhuis NA, Poole DP, McLean P, Hicks GA, Scheff N, Chen E, Bhattacharya A, Schmidt BL, Brierley SM, Vanner SJ, Bunnett NW.

Proc Natl Acad Sci U S A. 2018 Jul 31;115(31):E7438-E7447. doi: 10.1073/pnas.1721891115. Epub 2018 Jul 16.


Inflammation-associated changes in DOR expression and function in the mouse colon.

DiCello JJ, Saito A, Rajasekhar P, Eriksson EM, McQuade RM, Nowell CJ, Sebastian BW, Fichna J, Veldhuis NA, Canals M, Bunnett NW, Carbone SE, Poole DP.

Am J Physiol Gastrointest Liver Physiol. 2018 Oct 1;315(4):G544-G559. doi: 10.1152/ajpgi.00025.2018. Epub 2018 Jun 21.


The potentially beneficial central nervous system activity profile of ivacaftor and its metabolites.

Schneider EK, McQuade RM, Carbone VC, Reyes-Ortega F, Wilson JW, Button B, Saito A, Poole DP, Hoyer D, Li J, Velkov T.

ERJ Open Res. 2018 Mar 13;4(1). pii: 00127-2017. doi: 10.1183/23120541.00127-2017. eCollection 2018 Jan. Erratum in: ERJ Open Res. 2018 Dec 21;4(4):.


INSL5 activates multiple signalling pathways and regulates GLP-1 secretion in NCI-H716 cells.

Ang SY, Evans BA, Poole DP, Bron R, DiCello JJ, Bathgate RAD, Kocan M, Hutchinson DS, Summers RJ.

J Mol Endocrinol. 2018 Apr;60(3):213-224. doi: 10.1530/JME-17-0152.


Endosomal signaling of the receptor for calcitonin gene-related peptide mediates pain transmission.

Yarwood RE, Imlach WL, Lieu T, Veldhuis NA, Jensen DD, Klein Herenbrink C, Aurelio L, Cai Z, Christie MJ, Poole DP, Porter CJH, McLean P, Hicks GA, Geppetti P, Halls ML, Canals M, Bunnett NW.

Proc Natl Acad Sci U S A. 2017 Nov 14;114(46):12309-12314. doi: 10.1073/pnas.1706656114. Epub 2017 Oct 30.


Synergistic effect of IL-12 and IL-18 induces TIM3 regulation of γδ T cell function and decreases the risk of clinical malaria in children living in Papua New Guinea.

Schofield L, Ioannidis LJ, Karl S, Robinson LJ, Tan QY, Poole DP, Betuela I, Hill DL, Siba PM, Hansen DS, Mueller I, Eriksson EM.

BMC Med. 2017 Jun 15;15(1):114. doi: 10.1186/s12916-017-0883-8.


Neurokinin 1 receptor signaling in endosomes mediates sustained nociception and is a viable therapeutic target for prolonged pain relief.

Jensen DD, Lieu T, Halls ML, Veldhuis NA, Imlach WL, Mai QN, Poole DP, Quach T, Aurelio L, Conner J, Herenbrink CK, Barlow N, Simpson JS, Scanlon MJ, Graham B, McCluskey A, Robinson PJ, Escriou V, Nassini R, Materazzi S, Geppetti P, Hicks GA, Christie MJ, Porter CJH, Canals M, Bunnett NW.

Sci Transl Med. 2017 May 31;9(392). pii: eaal3447. doi: 10.1126/scitranslmed.aal3447.


Role of Nonneuronal TRPV4 Signaling in Inflammatory Processes.

Rajasekhar P, Poole DP, Veldhuis NA.

Adv Pharmacol. 2017;79:117-139. doi: 10.1016/bs.apha.2017.03.002. Epub 2017 Apr 24. Review.


G-CSF Receptor Blockade Ameliorates Arthritic Pain and Disease.

Lee MC, McCubbin JA, Christensen AD, Poole DP, Rajasekhar P, Lieu T, Bunnett NW, Garcia-Caraballo S, Erickson A, Brierley SM, Saleh R, Achuthan A, Fleetwood AJ, Anderson RL, Hamilton JA, Cook AD.

J Immunol. 2017 May 1;198(9):3565-3575. doi: 10.4049/jimmunol.1602127. Epub 2017 Mar 20.


Effects of Food Components That Activate TRPA1 Receptors on Mucosal Ion Transport in the Mouse Intestine.

Fothergill LJ, Callaghan B, Rivera LR, Lieu T, Poole DP, Cho HJ, Bravo DM, Furness JB.

Nutrients. 2016 Oct 10;8(10). pii: E623.


Antagonism of the proinflammatory and pronociceptive actions of canonical and biased agonists of protease-activated receptor-2.

Lieu T, Savage E, Zhao P, Edgington-Mitchell L, Barlow N, Bron R, Poole DP, McLean P, Lohman RJ, Fairlie DP, Bunnett NW.

Br J Pharmacol. 2016 Sep;173(18):2752-65. doi: 10.1111/bph.13554. Epub 2016 Aug 3.


G Protein-Coupled Receptor Trafficking and Signalling in the Enteric Nervous System: The Past, Present and Future.

Poole DP, Bunnett NW.

Adv Exp Med Biol. 2016;891:145-52. doi: 10.1007/978-3-319-27592-5_14. Review.


Distribution and trafficking of the μ-opioid receptor in enteric neurons of the guinea pig.

Lay J, Carbone SE, DiCello JJ, Bunnett NW, Canals M, Poole DP.

Am J Physiol Gastrointest Liver Physiol. 2016 Aug 1;311(2):G252-66. doi: 10.1152/ajpgi.00184.2016. Epub 2016 Jun 30.


Protein Kinase D and Gβγ Subunits Mediate Agonist-evoked Translocation of Protease-activated Receptor-2 from the Golgi Apparatus to the Plasma Membrane.

Jensen DD, Zhao P, Jimenez-Vargas NN, Lieu T, Gerges M, Yeatman HR, Canals M, Vanner SJ, Poole DP, Bunnett NW.

J Biol Chem. 2016 May 20;291(21):11285-99. doi: 10.1074/jbc.M115.710681. Epub 2016 Mar 30.


Plasma membrane localization of the μ-opioid receptor controls spatiotemporal signaling.

Halls ML, Yeatman HR, Nowell CJ, Thompson GL, Gondin AB, Civciristov S, Bunnett NW, Lambert NA, Poole DP, Canals M.

Sci Signal. 2016 Feb 9;9(414):ra16. doi: 10.1126/scisignal.aac9177.


P2Y1 Receptor Activation of the TRPV4 Ion Channel Enhances Purinergic Signaling in Satellite Glial Cells.

Rajasekhar P, Poole DP, Liedtke W, Bunnett NW, Veldhuis NA.

J Biol Chem. 2015 Nov 27;290(48):29051-62. doi: 10.1074/jbc.M115.689729. Epub 2015 Oct 16.


Transient receptor potential vanilloid 4 inhibits mouse colonic motility by activating NO-dependent enteric neurotransmission.

Fichna J, Poole DP, Veldhuis N, MacEachern SJ, Saur D, Zakrzewski PK, Cygankiewicz AI, Mokrowiecka A, Małecka-Panas E, Krajewska WM, Liedtke W, Steinhoff MS, Timmermans JP, Bunnett NW, Sharkey KA, Storr MA.

J Mol Med (Berl). 2015 Dec;93(12):1297-309. doi: 10.1007/s00109-015-1336-5. Epub 2015 Sep 2.


Demonstration of elevated levels of active cathepsin S in dextran sulfate sodium colitis using a new activatable probe.

Barlow N, Nasser Y, Zhao P, Sharma N, Guerrero-Alba R, Edgington-Mitchell LE, Lieu T, Veldhuis NA, Poole DP, Conner JW, Lindström E, Craig AW, Graham B, Vanner SJ, Bunnett NW.

Neurogastroenterol Motil. 2015 Nov;27(11):1675-80. doi: 10.1111/nmo.12656. Epub 2015 Aug 24.


Detection and Quantification of Intracellular Signaling Using FRET-Based Biosensors and High Content Imaging.

Halls ML, Poole DP, Ellisdon AM, Nowell CJ, Canals M.

Methods Mol Biol. 2015;1335:131-61. doi: 10.1007/978-1-4939-2914-6_10.


Inflammation-induced abnormalities in the subcellular localization and trafficking of the neurokinin 1 receptor in the enteric nervous system.

Poole DP, Lieu T, Pelayo JC, Eriksson EM, Veldhuis NA, Bunnett NW.

Am J Physiol Gastrointest Liver Physiol. 2015 Aug 15;309(4):G248-59. doi: 10.1152/ajpgi.00118.2015. Epub 2015 Jul 2.


Quantification and Potential Functions of Endogenous Agonists of Transient Receptor Potential Channels in Patients With Irritable Bowel Syndrome.

Cenac N, Bautzova T, Le Faouder P, Veldhuis NA, Poole DP, Rolland C, Bertrand J, Liedtke W, Dubourdeau M, Bertrand-Michel J, Zecchi L, Stanghellini V, Bunnett NW, Barbara G, Vergnolle N.

Gastroenterology. 2015 Aug;149(2):433-44.e7. doi: 10.1053/j.gastro.2015.04.011. Epub 2015 Apr 22.


Biological redundancy of endogenous GPCR ligands in the gut and the potential for endogenous functional selectivity.

Thompson GL, Canals M, Poole DP.

Front Pharmacol. 2014 Nov 28;5:262. doi: 10.3389/fphar.2014.00262. eCollection 2014. Review.


The G protein-coupled receptor-transient receptor potential channel axis: molecular insights for targeting disorders of sensation and inflammation.

Veldhuis NA, Poole DP, Grace M, McIntyre P, Bunnett NW.

Pharmacol Rev. 2015;67(1):36-73. doi: 10.1124/pr.114.009555. Review.


The bile acid receptor TGR5 activates the TRPA1 channel to induce itch in mice.

Lieu T, Jayaweera G, Zhao P, Poole DP, Jensen D, Grace M, McIntyre P, Bron R, Wilson YM, Krappitz M, Haerteis S, Korbmacher C, Steinhoff MS, Nassini R, Materazzi S, Geppetti P, Corvera CU, Bunnett NW.

Gastroenterology. 2014 Dec;147(6):1417-28. doi: 10.1053/j.gastro.2014.08.042. Epub 2014 Sep 3.


Endothelin-converting enzyme 1 and β-arrestins exert spatiotemporal control of substance P-induced inflammatory signals.

Jensen DD, Halls ML, Murphy JE, Canals M, Cattaruzza F, Poole DP, Lieu T, Koon HW, Pothoulakis C, Bunnett NW.

J Biol Chem. 2014 Jul 18;289(29):20283-94. doi: 10.1074/jbc.M114.578179. Epub 2014 Jun 4.


Localisation and activation of the neurokinin 1 receptor in the enteric nervous system of the mouse distal colon.

Pelayo JC, Veldhuis NA, Eriksson EM, Bunnett NW, Poole DP.

Cell Tissue Res. 2014 May;356(2):319-32. doi: 10.1007/s00441-014-1822-z. Epub 2014 Apr 12.


Feeding-dependent activation of enteric cells and sensory neurons by lymphatic fluid: evidence for a neurolymphocrine system.

Poole DP, Lee M, Tso P, Bunnett NW, Yo SJ, Lieu T, Shiu A, Wang JC, Nomura DK, Aponte GW.

Am J Physiol Gastrointest Liver Physiol. 2014 Apr 15;306(8):G686-98. doi: 10.1152/ajpgi.00433.2013. Epub 2014 Feb 27.


Agonist-biased trafficking of somatostatin receptor 2A in enteric neurons.

Zhao P, Canals M, Murphy JE, Klingler D, Eriksson EM, Pelayo JC, Hardt M, Bunnett NW, Poole DP.

J Biol Chem. 2013 Sep 6;288(36):25689-700. doi: 10.1074/jbc.M113.496414. Epub 2013 Aug 2.


The bile acid receptor TGR5 does not interact with β-arrestins or traffic to endosomes but transmits sustained signals from plasma membrane rafts.

Jensen DD, Godfrey CB, Niklas C, Canals M, Kocan M, Poole DP, Murphy JE, Alemi F, Cottrell GS, Korbmacher C, Lambert NA, Bunnett NW, Corvera CU.

J Biol Chem. 2013 Aug 9;288(32):22942-60. doi: 10.1074/jbc.M113.455774. Epub 2013 Jul 1.


The TGR5 receptor mediates bile acid-induced itch and analgesia.

Alemi F, Kwon E, Poole DP, Lieu T, Lyo V, Cattaruzza F, Cevikbas F, Steinhoff M, Nassini R, Materazzi S, Guerrero-Alba R, Valdez-Morales E, Cottrell GS, Schoonjans K, Geppetti P, Vanner SJ, Bunnett NW, Corvera CU.

J Clin Invest. 2013 Apr;123(4):1513-30. doi: 10.1172/JCI64551. Epub 2013 Mar 25.


Arresting inflammation: contributions of plasma membrane and endosomal signalling to neuropeptide-driven inflammatory disease.

Cattaruzza F, Poole DP, Bunnett NW.

Biochem Soc Trans. 2013 Feb 1;41(1):137-43. doi: 10.1042/BST20120343. Review.


Protease-activated receptor 2 (PAR2) protein and transient receptor potential vanilloid 4 (TRPV4) protein coupling is required for sustained inflammatory signaling.

Poole DP, Amadesi S, Veldhuis NA, Abogadie FC, Lieu T, Darby W, Liedtke W, Lew MJ, McIntyre P, Bunnett NW.

J Biol Chem. 2013 Feb 22;288(8):5790-802. doi: 10.1074/jbc.M112.438184. Epub 2013 Jan 3.


The receptor TGR5 mediates the prokinetic actions of intestinal bile acids and is required for normal defecation in mice.

Alemi F, Poole DP, Chiu J, Schoonjans K, Cattaruzza F, Grider JR, Bunnett NW, Corvera CU.

Gastroenterology. 2013 Jan;144(1):145-54. doi: 10.1053/j.gastro.2012.09.055. Epub 2012 Oct 3.


Knock out of neuronal nitric oxide synthase exacerbates intestinal ischemia/reperfusion injury in mice.

Rivera LR, Pontell L, Cho HJ, Castelucci P, Thacker M, Poole DP, Frugier T, Furness JB.

Cell Tissue Res. 2012 Aug;349(2):565-76. doi: 10.1007/s00441-012-1451-3. Epub 2012 Jun 12.


N-glycosylation determines ionic permeability and desensitization of the TRPV1 capsaicin receptor.

Veldhuis NA, Lew MJ, Abogadie FC, Poole DP, Jennings EA, Ivanusic JJ, Eilers H, Bunnett NW, McIntyre P.

J Biol Chem. 2012 Jun 22;287(26):21765-72. doi: 10.1074/jbc.M112.342022. Epub 2012 May 8.


Nonruminant Nutrition Symposium: Involvement of gut neural and endocrine systems in pathological disorders of the digestive tract.

Furness JB, Poole DP.

J Anim Sci. 2012 Apr;90(4):1203-12. doi: 10.2527/jas.2011-4825. Epub 2011 Dec 16. Review.


The involvement of nitric oxide synthase neurons in enteric neuropathies.

Rivera LR, Poole DP, Thacker M, Furness JB.

Neurogastroenterol Motil. 2011 Nov;23(11):980-8. doi: 10.1111/j.1365-2982.2011.01780.x. Epub 2011 Sep 4. Review.


Endothelin-converting enzyme-1 regulates trafficking and signalling of the neurokinin 1 receptor in endosomes of myenteric neurones.

Pelayo JC, Poole DP, Steinhoff M, Cottrell GS, Bunnett NW.

J Physiol. 2011 Nov 1;589(Pt 21):5213-30. doi: 10.1113/jphysiol.2011.214452. Epub 2011 Aug 30.


Localization and regulation of fluorescently labeled delta opioid receptor, expressed in enteric neurons of mice.

Poole DP, Pelayo JC, Scherrer G, Evans CJ, Kieffer BL, Bunnett NW.

Gastroenterology. 2011 Sep;141(3):982-991.e18. doi: 10.1053/j.gastro.2011.05.042. Epub 2011 May 27.

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