Modulation of visceral hypersensitivity by glial cell line-derived neurotrophic factor family receptor α-3 in colorectal afferents

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 300, Issue 3, 2011, Pages 418-424

  Tanaka, T ^a,b   Shinoda, M ^a   Feng, B ^a   Albers, K M ^a   Gebhart, G F ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b TAKEDA PHARMACEUTICAL COMPANY LIMITED   (Japan)

Author keywords

Growth factors; Irritable bowel syndrome; Visceral pain

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; SODIUM CHLORIDE; TRINITROBENZENESULFONIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLITIS; COLON DILATATION; COLORECTAL HYPERSENSITIVITY; CONTROLLED STUDY; HYPERSENSITIVITY; INFLAMMATION; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SENSITIZATION; SENSORY NERVE; SPINAL GANGLION;

ANIMALS; COLITIS; COLON; DISEASE MODELS, ANIMAL; ELECTROMYOGRAPHY; EVOKED POTENTIALS; GANGLIA, SPINAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; HYPERALGESIA; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS, AFFERENT; PRESSURE; RECTUM; TIME FACTORS; TRINITROBENZENESULFONIC ACID;

EID: 79953138460     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00456.2010     Document Type: Article

References (33)

1. Azpiroz F, Bouin M, Camilleri M, Mayer EA, Poitras P, Serra J, Spiller RC. Mechanisms of hypersensitivity in IBS and functional disorders. Neurogastroenterol Motil 19: 62-88, 2007.
2. Bielefeldt K, Ozaki N, Gebhart GF. Role of nerve growth factor in modulation of gastric afferent neurons in the rat. Am J Physiol Gastrointest Liver Physiol 284: G499-G507, 2003.
3. Brierley SM, Jones 3rd RC, Gebhart GF, Blackshaw LA. Splanchnic and pelvic mechanosensory afferents signal different qualities of colonic stimuli in mice. Gastroenterology 127: 166-178, 2004.
4. Brierley SM, Page AJ, Hughes PA, Adam B, Liebregts T, Cooper NJ, Holtmann G, Liedtke W, Blackshaw LA. Selective role for TRPV4 ion channels in visceral sensory pathways. Gastroenterology 134: 2059-2069, 2008.
5. Brierley SM, Hughes PA, Page AJ, Kwan KY, Martin CM, O'Donnell TA, Cooper NJ, Harrington AM, Adam B, Liebregts T, Holtmann G, Corey DP, Rychkov GY, Blackshaw LA. The ion channel TRPA1 is required for normal mechanosensation and is modulated by algesic stimuli. Gastroenterology 137: 2084-2095, 2009.
6. Camilleri M. Drug development and IBS drugs: experience from the past, current challenges, and proposal for the future. Curr Opin Pharmacol 8: 671-676, 2008.
7. Cattaruzza F, Spreadbury I, Miranda-Morales M, Grady EF, Vanner SJ, Bunnett NW. Transient receptor potential ankyrin-1 has a major role in mediating visceral pain in mice. Am J Physiol Gastrointest Liver Physiol 298: G81-G91, 2010.
8. Cenac N, Altier C, Chapman K, Liedtke W, Zamponi G, Vergnolle N. Transient receptor potential vanilloid-4 has a major role in visceral hypersensitivity symptoms. Gastroenterology 135: 937-946, 2008.
9. Ceyhan GO, Bergmann F, Kadihasanoglu M, Erkan M, Park W, Hinz U, Giese T, Müller MW, Büchler MW, Giese NA, Friess H. The neurotrophic factor artemin influences the extent of neural damage and growth in chronic pancreatitis. Gut 56: 534-544, 2007.
10. Christianson JA, Gebhart GF. Assessment of colon sensitivity by luminal distension in mice. Nat Protoc 2: 2624-2631, 2007.
11. Delafoy L, Raymond F, Doherty AM, Eschalier A, Diop L. Role of nerve growth factor in the trinitrobenzene sulfonic acid-induced colonic hypersensitivity. Pain 105: 489-497, 2003.
12. Dorn SD, Palsson OS, Thiwan SI, Kanazawa M, Clark WC, van Tilburg MA, Drossman DA, Scarlett Y, Levy RL, Ringel Y, Crowell MD, Olden KW, Whitehead WE. Increased colonic pain sensitivity in irritable bowel syndrome is the result of an increased tendency to report pain rather than increased neurosensory sensitivity. Gut 56: 1202-1209, 2007.
13. Elitt CM, McIlwrath SL, Lawson JJ, Malin SA, Molliver DC, Cornuet PK, Koerber HR, Davis BM, Albers KM. Artemin overexpression in skin enhances expression of TRPV1 and TRPA1 in cutaneous sensory neurons and leads to behavioral sensitivity to heat and cold. J Neurosci 26: 8578-8587, 2006.
14. Feng B, Brumovsky PR, Gebhart GF. Differential roles of stretchsensitive pelvic nerve afferents innervating mouse distal colon and rectum. Am J Physiol Gastrointest Liver Physiol 298: G402-G409, 2010.
15. Honma Y, Araki T, Gianino S, Bruce A, Heuckeroth R, Johnson E, Milbrandt J. Artemin is a vascular-derived neurotropic factor for developing sympathetic neurons. Neuron 35: 267-282, 2002.
16. Hughes PA, Brierley SM, Martin CM, Brookes SJ, Linden DR, Blackshaw LA. Post-inflammatory colonic afferent sensitisation: different subtypes, different pathways and different time courses. Gut 58: 1333-1341, 2009.
17. Jones 3rd RC, Xu L, Gebhart GF. 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: 10981-10989, 2005.
18. Jones 3rd RC, Otsuka E, Wagstrom E, Jensen CS, Price MP, Gebhart GF. Short-term sensitization of colon mechanoreceptors is associated with long-term hypersensitivity to colon distention in the mouse. Gastroenterology 133: 184-194, 2007.
19. Josephson A, Widenfalk J, Trifunovski A, Widmer HR, Olson L, Spenger C. GDNF and NGF family members and receptors in human fetal and adult spinal cord and dorsal root ganglia. J Comp Neurol 440: 204-217, 2001.
20. Kamp EH, Jones 3rd RC, Tillman SR, Gebhart GF. Quantitative assessment and characterization of visceral nociception and hyperalgesia in mice. Am J Physiol Gastrointest Liver Physiol 284: G434-G444, 2003.
21. Lamb K, Kang YM, Gebhart GF, Bielefeldt K. Nerve growth factor and gastric hyperalgesia in the rat. Neurogastroenterol Motil 15: 355-361, 2003.
22. Lewin GR, Mendell LM. Nerve growth factor and nociception. Trends Neurosci 16: 353-359, 1993.
23. Malin SA, Molliver DC, Koerber HR, Cornuet P, Frye R, Albers KM, Davis BM. Glial cell line-derived neurotrophic factor family members sensitize nociceptors in vitro and produce thermal hyperalgesia in vivo. J Neurosci 26: 8588-8599, 2006.
24. Malin SA, Christianson JA, Bielefeldt K, Davis BM. TPRV1 expression defines functionally distinct pelvic colon afferents. J Neurosci 29: 743-752, 2009.
25. Malin SA, Molliver DC, Christianson JA, Albers KM, Davis BM. TRPV1 and TRPA1 function and modulation are target tissue-dependent. J Neurosci In press.
26. McMahon SB. NGF as a mediator of inflammatory pain. Philos Trans R Soc Lond B Biol Sci 351: 431-440, 1996.
27. Mendell LM, Albers KM, Davis BM. Neurotrophins, nociceptors, pain. Microsc Res Tech 45: 252-261, 1999.
28. Orozco OE, Walus L, Sah DW, Pepinsky RB, Sanicola M. GFRalpha3 is expressed predominantly in nociceptive sensory neurons. Eur J Neurosci 13: 2177-2182, 2001.
29. Ritchie J. Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome. Gut 14: 125-132, 1973.
30. Schmutzler BS, Roy S, Hingtgen CM. Glial cell line-derived neurotrophic factor family ligands enhance capsaicin-stimulated release of calcitonin gene-related peptide from sensory neurons. Neuroscience 161: 148-156, 2009.
31. Shinoda M, Feng B, Gebhart GF. Peripheral and central P2X receptor contributions to colon mechanosensitivity and hypersensitivity in the mouse. Gastroenterology 137: 2096-2104, 2009.
32. Verne GN, Robinson ME, Vase L, Price DD. Reversal of visceral and cutaneous hyperalgesia by local rectal anesthesia in irritable bowel syndrome (IBS) patients. Pain 105: 223-230, 2003.
33. Wynn G, Rong W, Xiang Z, Burnstock G. Purinergic mechanisms contribute to mechanosensory transduction in the rat colorectum. Gastroenterology 125: 1398-1409, 2003.