Histamine Receptor H1-Mediated Sensitization of TRPV1 Mediates Visceral Hypersensitivity and Symptoms in Patients with Irritable Bowel Syndrome

Gastroenterology

Volumn 150, Issue 4, 2016, Pages 875-887.e9

  Wouters, Mira M ^a   Balemans, Dafne ^a   Van Wanrooy, Sander ^a   Dooley, James ^b   Cibert Goton, Vincent ^d   Alpizar, Yeranddy A ^c   Valdez Morales, Eduardo E ^e   Nasser, Yasmin ^e   Van Veldhoven, Paul P ^c   Vanbrabant, Winde ^a   Van Der Merwe, Schalk ^a   Mols, Raf ^a   Ghesquière, Bart ^b   Cirillo, Carla ^a   Kortekaas, Inge ^b   Carmeliet, Peter ^b   Peetermans, Willy E ^a   Vermeire, Séverine ^a   Rutgeerts, Paul ^a   Augustijns, Patrick ^a   Hellings, Peter W ^b,f,g   Belmans, Ann ^b   Vanner, Stephen ^e   Bulmer, David C ^d   Talavera, Karel ^c   Vanden Berghe, Pieter ^a   Liston, Adrian ^b   Boeckxstaens, Guy E ^a   more..

^a UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^e QUEEN S UNIVERSITY   (Canada)

^f ACADEMIC MEDICAL CENTER   (Netherlands)

^g GHENT UNIVERSITY   (Belgium)

Author keywords

Drug; Sensory Neurons; Transient Receptor Potential Cation Channel Subfamily V Member 1; Treatment

Indexed keywords

ACETALDEHYDE; CAPSAICIN; EBASTINE; HISTAMINE H1 RECEPTOR; IMIDAZOLE; PLACEBO; VANILLOID RECEPTOR 1; ANALGESIC AGENT; BUTYROPHENONE DERIVATIVE; GASTROINTESTINAL AGENT; HISTAMINE H1 RECEPTOR ANTAGONIST; PIPERIDINE DERIVATIVE; TRPV1 PROTEIN, HUMAN; VANILLOID RECEPTOR;

ABDOMINAL PAIN; ADULT; AGED; ANIMAL EXPERIMENT; ARTICLE; ASTHENIA; CALCIUM CELL LEVEL; CLINICAL ARTICLE; COLON BIOPSY; CONSTIPATION; CONTROLLED STUDY; DIARRHEA; DOUBLE BLIND PROCEDURE; DRUG EFFICACY; DRUG SAFETY; FEMALE; GASTROINTESTINAL SYMPTOM; HEADACHE; HUMAN; HUMAN TISSUE; HYPERSENSITIVITY; IRRITABLE COLON; MEDICATION COMPLIANCE; MOUSE; NATURAL KILLER CELL; NATURAL KILLER T CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIAL; RECTUM BIOPSY; SENSORY NERVE CELL; SPINAL GANGLION; STOMACH DISEASE; TREATMENT DURATION; UNSPECIFIED SIDE EFFECT; VISCERAL HYPERSENSITIVITY; VISCERAL PAIN; ADOLESCENT; BELGIUM; BIOPSY; CALCIUM SIGNALING; DRUG EFFECTS; INNERVATION; IRRITABLE BOWEL SYNDROME; MALE; METABOLISM; MIDDLE AGED; NERVE CELL; PAIN MEASUREMENT; PAIN THRESHOLD; PATHOPHYSIOLOGY; QUESTIONNAIRE; RECTUM; REMISSION; SIGNAL TRANSDUCTION; TIME FACTOR; TREATMENT OUTCOME; YOUNG ADULT;

ABDOMINAL PAIN; ADOLESCENT; ADULT; AGED; ANALGESICS; BELGIUM; BIOPSY; BUTYROPHENONES; CALCIUM SIGNALING; DOUBLE-BLIND METHOD; FEMALE; GASTROINTESTINAL AGENTS; HISTAMINE H1 ANTAGONISTS; HUMANS; IRRITABLE BOWEL SYNDROME; MALE; MIDDLE AGED; NEURONS; PAIN MEASUREMENT; PAIN THRESHOLD; PIPERIDINES; QUALITY OF LIFE; RECEPTOR CROSS-TALK; RECEPTORS, HISTAMINE H1; RECTUM; REMISSION INDUCTION; SURVEYS AND QUESTIONNAIRES; TIME FACTORS; TREATMENT OUTCOME; TRPV CATION CHANNELS; YOUNG ADULT;

EID: 84959313115     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2015.12.034     Document Type: Article

References (50)

1. L. Ohman, and M. Simren Pathogenesis of IBS: role of inflammation, immunity and neuroimmune interactions Nat Rev Gastroenterol Hepatol 7 2010 163 173
2. S.D. Kuiken, R. Lindeboom, G.N. Tytgat, and et al. Relationship between symptoms and hypersensitivity to rectal distension in patients with irritable bowel syndrome Aliment Pharmacol Ther 22 2005 157 164
3. M. Camilleri, S. McKinzie, I. Busciglio, and et al. Prospective study of motor, sensory, psychologic, and autonomic functions in patients with irritable bowel syndrome Clin Gastroenterol Hepatol 6 2008 772 781
4. H. Mertz, B. Naliboff, J. Munakata, and et al. Altered rectal perception is a biological marker of patients with irritable bowel syndrome Gastroenterology 109 1995 40 52
5. M. Camilleri Pharmacological agents currently in clinical trials for disorders in neurogastroenterology J Clin Invest 123 2013 4111 4120
6. S.M. Brierley, and D.R. Linden Neuroplasticity and dysfunction after gastrointestinal inflammation Nat Rev Gastroenterol Hepatol 11 2014 611 627
7. J. Sousa-Valente, A.P. Andreou, L. Urban, and et al. Transient receptor potential ion channels in primary sensory neurons as targets for novel analgesics Br J Pharmacol 171 2014 2508 2527
8. R.C. Jones 3rd, L. Xu, and G.F. Gebhart The mechanosensitivity of mouse colon afferent fibers and their sensitization by inflammatory mediators require transient receptor potential vanilloid 1 and acid-sensing ion channel 3 J Neurosci 25 2005 10981 10989
9. R.M. van den Wijngaard, T.K. Klooker, O. Welting, and et al. Essential role for TRPV1 in stress-induced (mast cell-dependent) colonic hypersensitivity in maternally separated rats Neurogastroenterol Motil 21 2009 1107-e94
10. J. Winston, M. Shenoy, D. Medley, and et al. The vanilloid receptor initiates and maintains colonic hypersensitivity induced by neonatal colon irritation in rats Gastroenterology 132 2007 615 627
11. A. Miranda, E. Nordstrom, A. Mannem, and et al. The role of transient receptor potential vanilloid 1 in mechanical and chemical visceral hyperalgesia following experimental colitis Neuroscience 148 2007 1021 1032
12. S.J. van Wanrooij, M.M. Wouters, L. Van Oudenhove, and et al. sensitivity testing in irritable bowel syndrome with rectal capsaicin stimulations: role of TRPV1 upregulation and sensitization in visceral hypersensitivity? Am J Gastroenterol 109 2014 99 109
13. M. Hirth, R. Rukwied, A. Gromann, and et al. Nerve growth factor induces sensitization of nociceptors without evidence for increased intraepidermal nerve fiber density Pain 154 2013 2500 2511
14. S.L. Morales-Lazaro, S.A. Simon, and T. Rosenbaum The role of endogenous molecules in modulating pain through transient receptor potential vanilloid 1 (TRPV1) J Physiol 591 2013 3109 3121
15. G. Barbara, C. Cremon, V. Annese, and et al. Randomised controlled trial of mesalazine in IBS Gut 65 2016 82 90
16. C. Lam, W. Tan, M. Leighton, and et al. A mechanistic multicentre, parallel group, randomised placebo-controlled trial of mesalazine for the treatment of IBS with diarrhoea (IBS-D) Gut 65 2016 91 99
17. N. Cenac, C. Altier, J.P. Motta, and et al. Potentiation of TRPV4 signalling by histamine and serotonin: an important mechanism for visceral hypersensitivity Gut 59 2010 481 488
18. N. Cenac, C.N. Andrews, M. Holzhausen, and et al. Role for protease activity in visceral pain in irritable bowel syndrome J Clin Invest 117 2007 636 647
19. G. Barbara, V. Stanghellini, R. De Giorgio, and et al. Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome Gastroenterology 126 2004 693 702
20. T.K. Klooker, B. Braak, K.E. Koopman, and et al. The mast cell stabiliser ketotifen decreases visceral hypersensitivity and improves intestinal symptoms in patients with irritable bowel syndrome Gut 59 2010 1213 1221
21. J. Sastre Ebastine in allergic rhinitis and chronic idiopathic urticaria Allergy 63 Suppl 89 2008 1 20
22. E.E. Valdez-Morales, J. Overington, R. Guerrero-Alba, and et al. Sensitization of peripheral sensory nerves by mediators from colonic biopsies of diarrhea-predominant irritable bowel syndrome patients: a role for PAR2 Am J Gastroenterol 108 2013 1634 1643
23. G.F. Longstreth, W.G. Thompson, W.D. Chey, and et al. Functional bowel disorders Gastroenterology 130 2006 1480 1491
24. C. Cirillo, J. Tack, and P. Vanden Berghe Nerve activity recordings in routine human intestinal biopsies Gut 62 2013 227 235
25. K. Wieland, A.M. Laak, M.J. Smit, and et al. Mutational analysis of the antagonist-binding site of the histamine H(1) receptor J Biol Chem 274 1999 29994 30000
26. A.M. ter Laak, H. Timmerman, R. Leurs, and et al. Modelling and mutation studies on the histamine HRH1eceptor agonist binding site reveal different binding modes for H1-agonists: Asp116 (TM3) has a constitutive role in receptor stimulation J Comput Aided Mol Des 9 1995 319 330
27. M. Bruysters, H.H. Pertz, A. Teunissen, and et al. Mutational analysis of the histamine HRH1eceptor binding pocket of histaprodifens Eur J Pharmacol 487 2004 55 63
28. S. Rico, R. Antonijoan, and M. Barbanoj Ebastine in the light of CONGA recommendations for the development of third-generation antihistamines J Asthma Allergy 2 2009 73 92
29. M. Numazaki, T. Tominaga, H. Toyooka, and et al. Direct phosphorylation of capsaicin receptor VR1 by protein kinase Cepsilon and identification of two target serine residues J Biol Chem 277 2002 13375 13378
30. L.S. Premkumar, and G.P. Ahern Induction of vanilloid receptor channel activity by protein kinase C Nature 408 2000 985 990
31. E.D. Prescott, and D. Julius A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity Science 300 2003 1284 1288
32. T. Ohya, and M. Niitsu Relative reactivities of histamine and indoleamines with acetaldehyde Biol Pharm Bull 26 2003 1215 1218
33. M. Nori, S. Iwata, Y. Munakata, and et al. Ebastine inhibits T cell migration, production of Th2-type cytokines and proinflammatory cytokines Clin Exp Allergy 33 2003 1544 1554
34. E.M. Quigley, J. Tack, W.D. Chey, and et al. Randomised clinical trials: linaclotide phase 3 studies in IBS-C - a prespecified further analysis based on European Medicines Agency-specified endpoints Aliment Pharmacol Ther 37 2013 49 61
35. W.D. Chey, A.J. Lembo, B.J. Lavins, and et al. Linaclotide for irritable bowel syndrome with constipation: a 26-week, randomized, double-blind, placebo-controlled trial to evaluate efficacy and safety Am J Gastroenterol 107 2012 1702 1712
36. S. Rao, A.J. Lembo, S.J. Shiff, and et al. A 12-week, randomized, controlled trial with a 4-week randomized withdrawal period to evaluate the efficacy and safety of linaclotide in irritable bowel syndrome with constipation Am J Gastroenterol 107 2012 1714 1724 quiz 1725
37. N. Cenac, T. Bautzova, P. Le Faouder, and et al. Quantification and potential functions of endogenous agonists of transient receptor potential channels in patients with irritable bowel syndrome Gastroenterology 149 2015 433 444.e7
38. E.E. Valdez-Morales, J. Overington, R. Guerrero-Alba, and et al. Sensitization of peripheral sensory nerves by mediators from colonic biopsies of diarrhea-predominant irritable bowel syndrome patients: a role for PAR2 Am J Gastroenterol 108 2013 1634 1643
39. M.M. Garrity, S.J. Gibbons, T.C. Smyrk, and et al. Diagnostic challenges of motility disorders: optimal detection of CD117+ interstitial cells of Cajal Histopathology 54 2009 286 294
40. C. Cirillo, J. Tack, and P. Vanden Berghe Nerve activity recordings in routine human intestinal biopsies Gut 62 2013 227 235
41. J. Vriens, H. Watanabe, A. Janssens, and et al. Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4 Proc Natl Acad Sci U S A 101 2004 396 401
42. S.M. Brierley, R.C. Jones III, G.F. Gebhart, and et al. Splanchnic and pelvic mechanosensory afferents signal different qualities of colonic stimuli in mice Gastroenterology 127 2004 166 178
43. S.M. Brierley, A.J. Page, P.A. Hughes, and et al. Selective role for TRPV4 ion channels in visceral sensory pathways Gastroenterology 134 2008 2059 2069
44. R. Kapeller-Adler, and M. Fletcher The enzymic destruction of histamine in vitro Biochim Biophys Acta 33 1959 1 9
45. P.P. Van Veldhoven, and G.P. Mannaerts Subcellular localization and membrane topology of sphingosine-1-phosphate lyase in rat liver J Biol Chem 266 1991 12502 12507
46. S. Mezzar, S.E. de, and P.P. Van Veldhoven RP-HPLC-fluorescence analysis of aliphatic aldehydes: application to aldehyde-generating enzymes HACL1 and SGPL1 J Lipid Res 55 2014 573 582
47. G.F. Longstreth, W.G. Thompson, W.D. Chey, and et al. Functional bowel disorders Gastroenterology 130 2006 1480 1491
48. T.K. Klooker, B. Braak, K.E. Koopman, and et al. The mast cell stabiliser ketotifen decreases visceral hypersensitivity and improves intestinal symptoms in patients with irritable bowel syndrome Gut 59 2010 1213 1221
49. S.D. Kuiken, R. Lindeboom, G.N. Tytgat, and et al. Relationship between symptoms and hypersensitivity to rectal distension in patients with irritable bowel syndrome Aliment Pharmacol Ther 22 2005 157 164
50. D.B. Rubin Multiple imputation for nonresponse in surveys 1987 J. Wiley & Sons New York