Neuronal activation by mucosal biopsy supernatants from irritable bowel syndrome patients is linked to visceral sensitivity

Experimental Physiology

Volumn 99, Issue 10, 2014, Pages 1299-1311

  Buhner, Sabine ^a   Braak, Breg ^b   Li, Qin ^a,c   Kugler, Eva Maria ^a   Klooker, Tamira ^b   Wouters, Mira ^d   Donovan, Jemma ^e   Vignali, Sheila ^a   Mazzuoli Weber, Gemma ^a   Grundy, David ^e   Boeckxstaens, Guy ^b,d   Schemann, Michael ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c SHANDONG UNIVERSITY   (China)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVATION; CLINICAL ARTICLE; COLON BIOPSY; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; ENTERIC NEURON; HUMAN; HUMAN TISSUE; HYPERSENSITIVITY; IRRITABLE COLON; MALE; MIDDLE AGED; MOUSE; NERVE CELL; NERVOUS SYSTEM FUNCTION; NONHUMAN; PAIN THRESHOLD; RECTUM BIOPSY; SPIKE; SPINAL GANGLION; SUPERNATANT; VISCERA; VISCERAL SENSITIVITY; VOLTAGE SENSITIVE DYE IMAGING; YOUNG ADULT; ANIMAL; BIOPSY; CALCIUM SIGNALING; FEMALE; GUINEA PIG; INTESTINE INNERVATION; INTESTINE MUCOSA; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADULT; ANIMALS; BIOPSY; CALCIUM SIGNALING; ENTERIC NERVOUS SYSTEM; FEMALE; GANGLIA, SPINAL; GUINEA PIGS; HUMANS; INTESTINAL MUCOSA; IRRITABLE BOWEL SYNDROME; MALE; MICE; MIDDLE AGED; NEURONS; PAIN THRESHOLD; YOUNG ADULT;

EID: 84908486106     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/expphysiol.2014.080036     Document Type: Article

References (36)

1. Arebi N, Gurmany S, Bullas D, Hobson A, Stagg A & Kamm M (2008). Review article: the psychoneuroimmunology of irritable bowel syndrome - an exploration of interactions between psychological, neurological and immunological observations. Aliment Pharmacol Ther 28, 830-840.
2. Barbara G, Stanghellini V, de Giorgio R, Cremon C, Cottrell GS, Santini D, Pasquinelli G, Morselli-Labate AM, Grady EF, Bunnett NW, Collins SM & Corinaldesi R (2004). Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 126, 693-702.
3. Barbara G, Wang B, Stanghellini V, de Giorgio R, Cremon C, Di Nardo G, Trevisani M, Campi B, Geppetti P, Tonini M, Bunnett NW, Grundy D & Corinaldesi R (2007). Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome. Gastroenterology 132, 26-37.
4. Blackshaw LA, Brookes SJ, Grundy D & Schemann M (2007). Sensory transmission in the gastrointestinal tract. Neurogastroenterol Motility 19, 1-19.
5. Braak B, Klooker TK, Wouters MM, Welting O, van der Loos CM, Stanisor OI, van Diest S, van den Wijngaard RM & Boeckxstaens GE (2012). Mucosal immune cell numbers and visceral sensitivity in patients with irritable bowel syndrome: is there any relationship? Am J Gastroenterol 107, 715-726.
6. 4 receptors. J Physiol 583, 731-742.
7. Buhner S, Li Q, Berger T, Vignali S, Barbara G, de Giorgio R, Stanghellini V & Schemann M (2012). Submucous rather than myenteric neurons are activated by supernatants of mucosal biopsies from irritable bowel syndrome patients. Neurogastroenterol Motil 24, 1134-e572.
8. Buhner S, Li Q, Vignali S, Barbara G, de Giorgio R, Stanghellini V, Cremon C, Zeller F, Langer R, Daniel H, Michel K & Schemann M (2009). Activation of human enteric neurons by supernatants of colonic biopsy specimens from patients with irritable bowel syndrome. Gastroenterology. 137, 1425-1434.
9. Buhner S & Schemann M (2012). Mast cell-nerve axis with a focus on the human gut. Biochim Biophys Acta 1822, 85-92.
10. Camilleri M, McKinzie S, Busciglio I, Low PA, Sweetser S, Burton D, Baxter K, Ryks M & Zinsmeister AR (2008). Prospective study of motor, sensory, psychologic, and autonomic functions in patients with irritable bowel syndrome. Clin Gastroenterol Hepatol 6, 772-781.
11. Cenac N, Andrews CN, Holzhausen M, Chapman K, Cottrell G, Andrade-Gordon P, Steinhoff M, Barbara G, Beck P, Bunnett NW, Sharkey KA, Ferraz JG, Shaffer E & Vergnolle N (2007). Role for protease activity in visceral pain in irritable bowel syndrome. J Clin Invest 117, 636-647.
12. Cremon C, Carini G, Wang B, Vasina V, Cogliandro RF, de Giorgio R, Stanghellini V, Grundy D, Tonini M, De Ponti F, Corinaldesi R & Barbara G (2011). Intestinal serotonin release, sensory neuron activation, and abdominal pain in irritable bowel syndrome. Am J Gastroenterol 106, 1290-1298.
13. Gecse K, Róka R, Ferrier L, Leveque M, Eutamene H, Cartier C, Ait-Belgnaoui A, Rosztóczy A, Izbéki F, Fioramonti J, Wittmann T & Bueno L (2008). Increased faecal serine protease activity in diarrhoeic IBS patients: a colonic lumenal factor impairing colonic permeability and sensitivity. Gut 57, 591-599.
14. Gu JG & MacDermott AB (1997). Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature 389, 749-753.
15. Gwee KA, Collins SM, Read NW, Rajnakova A, Deng Y, Graham JC, McKendrick MW & Moochhala SM (2003). Increased rectal mucosal expression of interleukin 1β in recently acquired post-infectious irritable bowel syndrome. Gut 52, 523-526.
16. Hughes PA, Harrington AM, Castro J, Liebregts T, Adam B, Grasby DJ, Isaacs NJ, Maldeniya L, Martin CM, Persson J, Andrews JM, Holtmann G, Blackshaw LA & Brierley SM (2013a). Sensory neuro-immune interactions differ between irritable bowel syndrome subtypes. Gut 62, 1456-1465.
17. Hughes PA, Zola H, Penttila IA, Blackshaw LA, Andrews JM & Krumbiegel D (2013b). Immune activation in irritable bowel syndrome: can neuroimmune interactions explain symptoms? Am J Gastroenterol 108, 1066-1074.
18. Kerckhoffs AP, Ter Linde JJ, Akkermans LM & Samsom M (2008). Trypsinogen IV, serotonin transporter transcript levels and serotonin content are increased in small intestine of irritable bowel syndrome patients. Neurogastroenterol Motil 20, 900-907.
19. Kerckhoffs AP, Ter Linde JJ, Akkermans LM & Samsom M (2012). SERT and TPH-1 mRNA expression are reduced in irritable bowel syndrome patients regardless of visceral sensitivity state in large intestine. Am J Physiol Gastrointest Liver Physiol 302, G1053-G1060.
20. Klooker TK, Braak B, Koopman KE, Welting O, Wouters MM, van der Heide S, Schemann M, Bischoff SC, van den Wijngaard RM & Boeckxstaens GE (2010). The mast cell stabiliser ketotifen decreases visceral hypersensitivity and improves intestinal symptoms in patients with irritable bowel syndrome. Gut 59, 1213-1221.
21. Kuiken SD, Lindeboom R, Tytgat GN & Boeckxstaens GE (2005). Relationship between symptoms and hypersensitivity to rectal distension in patients with irritable bowel syndrome. Aliment Pharmacol Ther 22, 157-164.
22. Labus JS, Naliboff BD, Berman SM, Suyenobu B, Vianna EP, Tillisch K & Mayer EA (2009). Brain networks underlying perceptual habituation to repeated aversive visceral stimuli in patients with irritable bowel syndrome. Neuroimage 47, 952-960.
23. Larsson MB, Tillisch K, Craig AD, Engström M, Labus J, Naliboff B, Lundberg P, Ström M, Mayer EA & Walter SA (2012). Brain responses to visceral stimuli reflect visceral sensitivity thresholds in patients with irritable bowel syndrome. Gastroenterology 142, 463-472.e3.
24. Ludidi S, Conchillo JM, Keszthelyi D, Van Avesaat M, Kruimel JW, Jonkers DM & Masclee AA (2012). Rectal hypersensitivity as hallmark for irritable bowel syndrome: defining the optimal cutoff. Neurogastroenterol Motil 24, 729-733, e345-e346.
25. Michel K, Michaelis M, Mazzuoli G, Mueller K, Vanden Berghe P & Schemann M (2011). Fast calcium and voltage-sensitive dye imaging in enteric neurones reveal calcium peaks associated with single action potential discharge. J Physiol 589, 5941-5947.
26. Piche T, Barbara G, Aubert P, Bruley des Varannes S, Dainese R, Nano JL, Cremon C, Stanghellini V, de Giorgio R, Galmiche JP & Neunlist M (2009). Impaired intestinal barrier integrity in the colon of patients with irritable bowel syndrome: involvement of soluble mediators. Gut 58, 196-201.
27. Posserud I, Syrous A, Lindström L, Tack J, Abrahamsson H & Simrén M (2007). Altered rectal perception in irritable bowel syndrome is associated with symptom severity. Gastroenterology 133, 1113-1123.
28. Price DD, Zhou Q, Moshiree B, Robinson ME & Verne GN (2006). Peripheral and central contributions to hyperalgesia in irritable bowel syndrome. J Pain 7, 529-535.
29. Róka R, Rosztóczy A, Leveque M, Izbéki F, Nagy F, Molnár T, Lonovics J, Garcia-Villar R, Fioramonti J, Wittmann T & Bueno L (2007). A pilot study of fecal serine-protease activity: a pathophysiologic factor in diarrhea-predominant irritable bowel syndrome. Clin Gastroenterol Hepatol 5, 550-555.
30. Schemann M & Camilleri M (2013). Functions and imaging of mast cell and neural axis of the gut. Gastroenterology 144, 698-704.
31. Schemann M, Kugler EM, Buhner S, Eastwood C, Donovan J, Jiang W & Grundy D (2012). The mast cell degranulator compound 48/80 directly activates neurons. PloS One 7, e52104.
32. Valdez-Morales EE, Overington J, Guerrero-Alba R, Ochoa-Cortes F, Ibeakanma CO, Spreadbury I, Bunnett NW, Beyak M & Vanner SJ (2013). 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, 1634-1643.
33. van Wanrooij SJ, Wouters MM, Van Oudenhove L, Vanbrabant W, Mondelaers S, Kollmann P, Kreutz F, Schemann M & Boeckxstaens GE (2014). Sensitivity testing in irritable bowel syndrome with rectal capsaicin stimulations: role of TRPV1 upregulation and sensitization in visceral hypersensitivity? Am J Gastroenterol 109, 99-109.
34. Verne GN, Robinson ME, Vase L & Price DD (2003). Reversal of visceral and cutaneous hyperalgesia by local rectal anesthesia in irritable bowel syndrome (IBS) patients. Pain 105, 223-230.
35. Wilder-Smith CH, Schindler D, Lovblad K, Redmond SM & Nirkko A (2004). Brain functional magnetic resonance imaging of rectal pain and activation of endogenous inhibitory mechanisms in irritable bowel syndrome patient subgroups and healthy controls. Gut 53, 1595-1601.
36. Zhou Q, Zhang B & Verne GN (2009). Intestinal membrane permeability and hypersensitivity in the irritable bowel syndrome. Pain 146, 41-46.