Differential contribution of TRPA1, TRPV4 and TRPM8 to colonic nociception in mice

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Mueller Tribbensee, Sonja M ^a   Karna, Manoj ^a   Khalil, Mohammad ^b   Neurath, Markus F ^b   Reeh, Peter W ^a   Engel, Matthias A ^b  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMILORIDE; CALCITONIN GENE RELATED PEPTIDE; GADOLINIUM; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8; VANILLOID RECEPTOR 4; 2-(1,3-DIMETHYL-2,6-DIOXO-1,2,3,6-TETRAHYDRO-7H-PURIN-7-YL)-N-(4-ISOPROPYLPHENYL)ACETAMIDE; ACETANILIDE DERIVATIVE; BENZAMIDE DERIVATIVE; N-(3-AMINOPROPYL)-2-(((3-METHYLPHENYL) METHYL)OXY)-N-(2-THIENYLMETHYL)BENZAMIDE HYDROCHLORIDE SALT; PURINE DERIVATIVE; RN 1734; RUTHENIUM RED; SULFONAMIDE; THIOPHENE DERIVATIVE; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRPA1 PROTEIN, MOUSE; TRPM8 PROTEIN, MOUSE; TRPV4 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLON DILATATION; COLONIC MECHANONOCICEPTION; COLORECTAL DISTENSION; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME IMMUNOASSAY; EX VIVO STUDY; FEMALE; IN VIVO STUDY; MALE; MOLECULAR DYNAMICS; MOUSE; NERVOUS SYSTEM PARAMETERS; NOCICEPTION; NONHUMAN; PROTEIN FUNCTION; PROTEIN SECRETION; RECEPTOR BLOCKING; VISCEROMOTOR RESPONSE; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; COLON; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; MECHANORECEPTOR; METABOLISM; NOCICEPTIVE PAIN; PATHOPHYSIOLOGY; PHYSIOLOGY; SECRETION (PROCESS);

ACETANILIDES; ANIMALS; BENZAMIDES; CALCITONIN GENE-RELATED PEPTIDE; COLON; FEMALE; MALE; MECHANORECEPTORS; MICE, INBRED C57BL; MICE, KNOCKOUT; NOCICEPTION; NOCICEPTIVE PAIN; PURINES; RUTHENIUM RED; SULFONAMIDES; THIOPHENES; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TRPM CATION CHANNELS; TRPV CATION CHANNELS;

EID: 84941662560     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128242     Document Type: Article

References (56)

1. Choung RS, Locke GR 3rd. Epidemiology of IBS. Gastroenterol Clin North Am. 2011; 40:1-10.
2. Holzer P. Transient receptor potential (TRP) channels as drug targets for diseases of the digestive system. Pharmacol Ther. 2011; 131:142-70. doi:10.1016/j.pharmthera.2011.03.006 PMID: 21420431.
3. Hamill OP, McBride DW Jr. The pharmacology of mechanogated membrane ion channels. Pharmacol Rev. 1996; 48:231-52. PMID: 8804105.
4. Brierley SM. Molecular basis of mechanosensitivity. Auton Neurosci. 2010; 153:58-68. doi:10.1016/j.autneu.2009.07.017 PMID: 19683967.
5. Alessandri-Haber N, Dina OA, Joseph EK, Reichling DB, Levine JD. Interaction of transient receptor potential vanilloid 4, integrin, and SRC tyrosine kinase in mechanical hyperalgesia. J Neurosci. 2008; 28:1046-57. doi:10.1523/JNEUROSCI.4497-07.2008 PMID: 18234883.
6. Brierley SM, Hughes PA, Page AJ, Kwan KY, Martin CM, O'Donnell TA., et al. The ion channel TRPA1 is required for normal mechanosensation and is modulated by algesic stimuli. Gastroenterology. 2009; 137:2084-95. doi:10.1053/j.gastro.2009.07.048 PMID: 19632231.
7. Brierley SM, Page AJ, Hughes PA, Adam B, Liebregts T, Cooper NJ., et al. Selective role for TRPV4 ion channels in visceral sensory pathways. Gastroenterology. 2008; 134:2059-69. doi:10.1053/j.gastro.2008.01.074 PMID: 18343379.
8. Cattaruzza F, Spreadbury I, Miranda-Morales M, Grady EF, Vanner S, Bunnett NW. Transient receptor potential ankyrin-1 has a major role in mediating visceral pain in mice. Am J Physiol Gastrointest Liver Physiol. 2010; 298:81-91.
9. 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. 2008; 135:937-46. doi:10.1053/j.gastro.2008.05.024 PMID: 18565335.
10. Chan CL, Facer P, Davis JB, Smith GD, Egerton J, Bountra C, et al. Sensory fibres expressing capsaicin receptor TRPV1 in patients with rectal hypersensitivity and faecal urgency. Lancet. 2003; 361:385- 91. PMID: 12573376.
11. Gonlachanvit S, Mahayosnond A, Kullavanijaya P. Effects of chili on postprandial gastrointestinal symptoms in diarrhoea predominant irritable bowel syndrome: Evidence for capsaicin-sensitive visceral nociception hypersensitivity. Neurogastroenterol Motil. 2009; 21:23-32. doi:10.1111/j.1365-2982.2008.01167.xPMID: 18647268.
12. Harrington AM, Hughes PA, Martin CM, Yang J, Castro J, Isaacs NJ, et al. A novel role for TRPM8 in visceral afferent function. Pain. 2011; 152:1459-68. doi:10.1016/j.pain.2011.01.027 PMID: 21489690.
13. Jones RC 3rd, 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. 2005; 25:10981-9. PMID: 16306411.
14. Jones RC 3rd, 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. 2007; 133:184-94. PMID: 17553498.
15. Sipe WE, Brierley SM, Martin CM, Phillis BD, Cruz FB, Grady EF, et al. Transient receptor potential vanilloid 4 mediates protease activated receptor 2-induced sensitization of colonic afferent nerves and visceral hyperalgesia. Am J Physiol Gastrointest Liver Physiol. 2008; 294:1288-98.
16. Blackshaw LA, Brierley SM, Hughes PA. TRP channels: new targets for visceral pain. Gut. 2010; 59:126-35. doi:10.1136/gut.2009.179523 PMID: 20007960.
17. Loukin S, Zhou X, Su Z, Saimi Y, Kung C. Wild-type and brachyolmia-causing mutant TRPV4 channels respond directly to stretch force. J Biol Chem. 2010; 285:27176-81. doi:10.1074/jbc.M110.143370 PMID: 20605796.
18. Liedtke W, Choe Y, Martí-Renom MA, Bell AM, Denis CS, Sali A, et al. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell. 2000; 103:525-35. PMID: 11081638.
19. Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD. OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol. 2000; 2:695-702. PMID: 11025659.
20. Liedtke W, Tobin DM, Bargmann CI, Friedman JM. Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2003; 100 Suppl 2:14531-6. PMID: 14581619.
21. Vollrath MA, Kwan KY, Corey DP. The micromachinery of mechanotransduction in hair cells. Annu Rev Neurosci. 2007; 30:339-65. PMID: 17428178.
22. Karashima Y, Prenen J, Meseguer V, Owsianik G, Voets T, Nilius B. Modulation of the transient receptor potential channel TRPA1 by phosphatidylinositol 4, 5-biphosphate manipulators. Pflugers Arch. 2008; 457:77-89. doi:10.1007/s00424-008-0493-6PMID: 18461353.
23. Hill K, Schaefer M. TRPA1 is differentially modulated by the amphipathic molecules trinitrophenol and chlorpromazine. J Biol Chem. 2007; 282:7145-53. PMID: 17218316.
24. Meseguer V, Alpizar YA, Luis E, Tajada S, Denlinger B, Fajardo O, et al. TRPA1 channels mediate acute neurogenic inflammation and pain produced by bacterial endotoxins. Nat Commun. 2014; 5:3125. doi:10.1038/ncomms4125 PMID: 24445575.
25. Engel MA, Leffler A, Niedermirtl F, Babes A, Zimmermann K, Filipović MR, et al. TRPA1 and substance P mediate colitis in mice. Gastroenterology. 2011; 141:1346-58. doi:10.1053/j.gastro.2011.07.002PMID: 21763243.
26. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, et al. TRPA1 contributes to cold, mechanical and chemical nociception but is not essential for hair-cell transduction. Neuron. 2006; 50:277-89. PMID: 16630838.
27. Liedtke W, Friedman JM. Abnormal osmotic regulation in trpv4-/- mice. Proc Natl Acad Sci U S A. 2003; 100:13698-703. PMID: 14581612.
28. Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A. TRPM8 is required for cold sensation in mice. Neuron. 2007; 54:371-8. PMID: 17481391.
29. Bretag AH. Synthetic interstitial fluid for isolated mammalian tissue. Life Sci. 1969; 8:319-29. PMID: 4305588.
30. Roza C, Reeh PW. Substance P, calcitonin gene related peptide and PGE2 co-released from the mouse colon: A new model to study nociceptive and inflammatory responses in viscera, in vitro. Pain. 2001; 93:213-9. PMID: 11514080.
31. Christianson JA, Gebhart GF. Assessment of colon sensitivity by luminal distension in mice. Nature Protocols. 2007; 2:2624-31. PMID: 17948005.
32. Caceres AI, Brackmann M, Elia MD, Bessac BF, del Camino D, D'Amours M, et al. A sensory neuronal ion channel essential for airway inflammation and hyperreactivity in asthma. Proc Natl Acad Sci U S A. 2009; 106:9099-104. doi:10.1073/pnas.0900591106 PMID: 19458046.
33. Trevisani M, Siemens J, Materazzi S, Bautista DM, Nassini R, Campi B, et al. 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1. Proc Natl Acad Sci U S A. 2007; 104:13519-24. PMID: 17684094.
34. Winget JM, Pan YH, Bahnson BJ. The interfacial binding surface of phospholipase A2s. Biochim Biophys Acta. 2006; 1761:1260-9. PMID: 16962825.
35. Pedersen SF, Poulsen KA, Lambert IH. Roles of phospholipase A2 isoforms in swelling- And melittin-induced arachidonic acid release and taurine efflux in NIH3T3 fibroblasts. Am J Physiol Cell Physiol. 2006; 291:C1286-96. PMID: 16855215.
36. Munaron L. Shuffling the cards in signal transduction: Calcium, arachidonic acid and mechanosensitivity. World J Biol Chem. 2011; 2:59-66. doi:10.4331/wjbc.v2.i4.59 PMID: 21537474.
37. Mochizuki T, Sokabe T, Araki I, Fujishita K, Shibasaki K, Uchida K, et al. The TRPV4 cation channel mediates stretch-evoked Ca2+ influx and ATP release in primary urothelial cell cultures. J Biol Chem. 2009; 284:21257-64. doi:10.1074/jbc.M109.020206 PMID: 19531473.
38. Gao X, Wu L, O'Neil RG. Temperature-modulated diversity of TRPV4 channel gating: Activation by physical stresses and phorbol ester derivatives through protein kinase C-dependent and-independent pathways. J Biol Chem. 2003; 278:27129-37. PMID: 12738791.
39. Suzuki M, Mizuno A, Kodaira K, Imai M. Impaired pressure sensation in mice lacking TRPV4. J Biol Chem. 2003; 278:22664-8. PMID: 12692122.
40. Rock MJ, Prenen J, Funari VA, Funari TL, Merriman B, Nelson SF, et al. Gain-of-function mutations in TRPV4 cause autosomal dominant brachyolmia. Nat Genet. 2008; 40:999-1003. doi:10.1038/ng.166 PMID: 18587396.
41. Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, et al. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature. 2007; 448:204-8. PMID: 17538622.
42. Hosoya T, Matsumoto K, Tashima K, Nakamura H, Fujino H, Murayama T, et al. TRPM8 has a key role in experimental colitis-induced visceral hyperalgesia in mice. Neurogastroenterol Motil. 2014; 26:1112- 21. doi:10.1111/nmo.12368 PMID: 24832648.
43. Ramachandran R, Hyun E, Zhao L, Lapointe TK, Chapman K, Hirota C, et al. TRPM8 activation attenuates inflammatory responses in mouse models of colitis. Proc Natl Acad Sci U S A. 2013; 110:7476-81. doi:10.1073/pnas.1217431110 PMID: 23596210.
44. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell. 2003; 112:819-29. PMID: 12654248.
45. Kim D, Cavanaugh EJ, Simkin D. Inhibition of transient receptor potential A1 channel by phosphatidylinositol- 4, 5-bisphosphate. Am J Physiol Cell Physiol. 2008; 295:92-9.
46. Doerner JF, Gisselmann G, Hatt H, Wetzel CH. Transient receptor potential channel A1 is directly gated by calcium ions. J Biol Chem. 2007; 282:13180-9. PMID: 17353192.
47. Xiao B, Dubin AE, Bursulaya B, Viswanath V, Jegla TJ, Patapoutian A. Identification of transmembrane domain 5 as a critical molecular determinant of menthol sensitivity in mammalian TRPA1 channels. J Neurosci. 2008; 28:9640-51. doi:10.1523/JNEUROSCI.2772-08.2008PMID: 18815250.
48. Kühn FJP, Kühn C, Lückhoff A. Inhibition of TRPM8 by icilin distinct from desensitization induced by menthol and menthol derivatives. J Biol Chem. 2009; 284:4102-11. doi:10.1074/jbc.M806651200PMID: 19095656.
49. Wrigley PJ, Jeong HJ, Vaughan CW. Primary afferents with TRPM8 and TRPA1 profiles target distinct subpopulations of rat superficial dorsal horn neurones. Br J Pharmacol. 2009; 157:371-80. doi:10.1111/j.1476-5381.2009.00167.x PMID: 19371346.
50. Proudfoot CJ, Garry EM, Cottrell DF, Rosie R, Anderson H, Robertson DC, et al. Analgesia mediated by the TRPM8 cold receptor in chronic neuropathic pain. Curr Biol. 2006; 16:1591-605. PMID: 16920620.
51. Liu B, Fan L, Balakrishna S, Sui A, Morris JB, Jordt SE. TRPM8 is the principal mediator of menthol-induced analgesia of acute and inflammatory pain. Pain. 2013; 154:2169-77doi:10.1016/j.pain.2013.06.043 PMID: 23820004.
52. Davidson JB, O'Grady G, Arkwright JW, Zarate N, Scott SM, Pullan AJ, et al. Anatomical registration and three-dimensional visualization of low and high-resolution pan-colonic manometry recordings. Neurogastroenterol Motil. 2011; 23:387-90. doi:10.1111/j.1365-2982.2010.01651.xPMID: 21199536.
53. Banke TG. The dilated TRPA1 channel pore state is blocked by amiloride and analogues. Brain Res. 2011; 1381:21-30. doi:10.1016/j.brainres.2011.01.021 PMID: 21241666.
54. Poole DP, Pelayo JC, Cattaruzza F, Kuo YM, Gai G, Chiu JV, et al. Transient receptor potential ankyrin 1 is expressed by inhibitory motoneurons of the mouse intestine. Gastroenterology. 2011; 141:565-75. doi:10.1053/j.gastro.2011.04.049 PMID: 21689654.
55. D'Aldebert E, Cenac N, Rousset P, Martin L, Rolland C, Chapman K, et al. Transient receptor potential vanilloid 4 activated inflammatory signals by intestinal epithelial cells and colitis in mice. Gastroenterology. 2011; 140:275-85. doi:10.1053/j.gastro.2010.09.045 PMID: 20888819.
56. Coste B, Xiao B, Santos JS, Syeda R, Grandl J, Spencer KS, et al. Piezo proteins are pore-forming subunits of mechanically activated channels. Nature. 2012; 483:176-81. doi:10.1038/nature10812 PMID: 22343900.