TRPM8 activation attenuates inflammatory responses in mouse models of colitis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 18, 2013, Pages 7476-7481

  Ramachandran, Rithwik ^a   Hyun, Eric ^a,b   Zhao, Liena ^a   Lapointe, Tamia K ^a   Chapman, Kevin ^a   Hirot, Christina L ^a   Ghosh, Subrata ^a   McKemy, David D ^c   Vergnolle, Nathalie ^a,d,e,f   Beck, Paul L ^a   Altier, Christophe ^a   Hollenberg, Morley D ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d TOULOUSE UNIVERSITY HOSPITAL   (France)

^e CNRS   (France)

^f France   (France)

Author keywords

CGRP; Crohn's disease; IBD; TRPV1

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; DEXTRAN SULFATE; MYELOPEROXIDASE; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8; VANILLOID RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; COLITIS; COLON; CONTROLLED STUDY; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCORING SYSTEM; UPREGULATION;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CALCIUM SIGNALING; CHEMOKINES; COLITIS; COLON; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; ION CHANNEL GATING; MICE; MICE, KNOCKOUT; PYRIMIDINONES; TRINITROBENZENESULFONIC ACID; TRPM CATION CHANNELS; TRPV CATION CHANNELS;

ANIMALIA; MURINAE; MUS;

EID: 84876908893     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1217431110     Document Type: Article

References (57)

1. Nathan C (2002) Points of control in inflammation. Nature 420(6917):846-852.
2. Nathan C, Ding A (2010) Nonresolving inflammation. Cell 140(6):871-882.
3. Khor B, Gardet A, Xavier RJ (2011) Genetics and pathogenesis of inflammatory bowel disease. Nature 474(7351):307-317.
4. Sartor RB (2006) Mechanisms of disease: Pathogenesis of Crohn's disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 3(7):390-407.
5. Xavier RJ, Podolsky DK (2007) Unravelling the pathogenesis of inflammatory bowel disease. Nature 448(7152):427-434. (Pubitemid 47123518)
6. Podolsky DK (2002) Inflammatory bowel disease. N Engl J Med 347(6):417-429.
7. Finley DS (2011) Basis for the use of localized hypothermia during radical pelvic surgery. Nat Rev Urol 8(6):345-350.
8. Chen Z, et al. (2005) Induction of profound hypothermia modulates the immune/inflammatory response in a swine model of lethal hemorrhage. Resuscitation 66(2):209-216. (Pubitemid 41033392)
9. Fujimoto K, et al. (2008) Early induction of moderate hypothermia suppresses systemic inflammatory cytokines and intracellular adhesion molecule-1 in rats with caerulein-induced pancreatitis and endotoxemia. Pancreas 37(2):176-181.
10. Polderman KH (2008) Induced hypothermia and fever control for prevention and treatment of neurological injuries. Lancet 371(9628):1955-1969.
11. McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416(6876):52-58. (Pubitemid 34215395)
12. Bautista DM, et al. (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448(7150):204-208. (Pubitemid 47067367)
13. Colburn RW, et al. (2007) Attenuated cold sensitivity in TRPM8 null mice. Neuron 54(3):379-386. (Pubitemid 46671410)
14. Dhaka A, et al. (2007) TRPM8 is required for cold sensation in mice. Neuron 54(3):371-378. (Pubitemid 46659806)
15. Peier AM, et al. (2002) A TRP channel that senses cold stimuli and menthol. Cell 108(5):705-715. (Pubitemid 34241429)
16. Harrington AM, et al. (2011) A novel role for TRPM8 in visceral afferent function. Pain 152(7):1459-1468.
17. Brignell JL, Chapman V, Kendall DA (2008) Comparison of icilin- and cold-evoked responses of spinal neurones, and their modulation of mechanical activity, in a model of neuropathic pain. Brain Res 1215:87-96.
18. Proudfoot CJ, et al. (2006) Analgesia mediated by the TRPM8 cold receptor in chronic neuropathic pain. Curr Biol 16(16):1591-1605. (Pubitemid 44233290)
19. Knowlton WM, Daniels RL, Palkar R, McCoy DD, McKemy DD (2011) Pharmacological blockade of TRPM8 ion channels alters cold and cold pain responses in mice. PLoS ONE 6(9):e25894.
20. Hyun E, Andrade-Gordon P, Steinhoff M, Vergnolle N (2008) Protease-activated receptor-2 activation: A major actor in intestinal inflammation. Gut 57(9):1222-1229.
21. Holzer M; Hypothermia after Cardiac Arrest Study Group (2002) Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest. N Engl J Med 346(8):549-556.
22. Gluckman PD, et al. (2005) Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: multicentre randomised trial. Lancet 365(9460):663-670. (Pubitemid 40260887)
23. Yenari MA, Han HS (2012) Neuroprotective mechanisms of hypothermia in brain ischaemia. Nat Rev Neurosci 13(4):267-278.
24. Deng H, Han HS, Cheng D, Sun GH, Yenari MA (2003) Mild hypothermia inhibits inflammation after experimental stroke and brain inflammation. Stroke 34(10):2495-2501. (Pubitemid 37221971)
25. Aslami H, et al. (2012) Mild hypothermia reduces ventilator-induced lung injury, irrespective of reducing respiratory rate. Transl Res 159(2):110-117.
26. Tsavaler L, Shapero MH, Morkowski S, Laus R (2001) Trp-p8, a novel prostate-specific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res 61(9):3760-3769. (Pubitemid 32694990)
27. Thebault S, et al. (2005) Novel role of cold/menthol-sensitive transient receptor potential melastatine family member 8 (TRPM8) in the activation of store-operated channels in LNCaP human prostate cancer epithelial cells. J Biol Chem 280(47):39423-39435. (Pubitemid 41713900)
28. Stein RJ, et al. (2004) Cool (TRPM8) and hot (TRPV1) receptors in the bladder and male genital tract. J Urol 172(3):1175-1178. (Pubitemid 39096495)
29. Sabnis AS, Shadid M, Yost GS, Reilly CA (2008) Human lung epithelial cells express a functional cold-sensing TRPM8 variant. Am J Respir Cell Mol Biol 39(4):466-474.
30. Sabnis AS, Reilly CA, Veranth JM, Yost GS (2008) Increased transcription of cytokine genes in human lung epithelial cells through activation of a TRPM8 variant by cold temperatures. Am J Physiol Lung Cell Mol Physiol 295(1):L194-L200.
31. Fonfria E, et al. (2006) Tissue distribution profiles of the human TRPM cation channel family. J Recept Signal Transduct Res 26(3):159-178.
32. Yang XR, Lin MJ, McIntosh LS, Sham JS (2006) Functional expression of transient receptor potential melastatin- and vanilloid-related channels in pulmonary arterial and aortic smooth muscle. Am J Physiol Lung Cell Mol Physiol 290(6):L1267-L1276. (Pubitemid 43830872)
33. Johnson CD, et al. (2009) Transient receptor potential melastatin 8 channel involvement in the regulation of vascular tone. Am J Physiol Heart Circ Physiol 296(6):H1868-H1877.
34. De Blas GA, et al. (2009) TRPM8, a versatile channel in human sperm. PLoS ONE 4(6):e6095.
35. Brauchi S, et al. (2007) Dissection of the components for PIP2 activation and thermosensation in TRP channels. Proc Natl Acad Sci USA 104(24):10246-10251. (Pubitemid 47175294)
36. Daniels RL, Takashima Y, McKemy DD (2009) Activity of the neuronal cold sensor TRPM8 is regulated by phospholipase C via the phospholipid phosphoinositol 4,5-bisphosphate. J Biol Chem 284(3):1570-1582.
37. Liu B, Qin F (2005) Functional control of cold- and menthol-sensitive TRPM8 ion channels by phosphatidylinositol 4,5-bisphosphate. J Neurosci 25(7):1674-1681. (Pubitemid 40279272)
38. Prescott ED, Julius D (2003) A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300(5623):1284-1288. (Pubitemid 36618238)
39. De Petrocellis L, et al. (2007) Regulation of transient receptor potential channels of melastatin type 8 (TRPM8): Effect of cAMP, cannabinoid CB(1) receptors and endovanilloids. Exp Cell Res 313(9):1911-1920. (Pubitemid 46661844)
40. De Petrocellis L, et al. (2008) Plant-derived cannabinoids modulate the activity of transient receptor potential channels of ankyrin type-1 and melastatin type-8. J Pharmacol Exp Ther 325(3):1007-1015. (Pubitemid 351724325)
41. Andersson DA, Nash M, Bevan S (2007) Modulation of the cold-activated channel TRPM8 by lysophospholipids and polyunsaturated fatty acids. J Neurosci 27(12):3347-3355. (Pubitemid 46474120)
42. Minami T, et al. (1993) Elevation of phospholipase A2 protein in sera of patients with Crohn's disease and ulcerative colitis. Am J Gastroenterol 88(7):1076-1080. (Pubitemid 23191099)
43. Braun A, et al. (2009) Alterations of phospholipid concentration and species composition of the intestinal mucus barrier in ulcerative colitis: A clue to pathogenesis. Inflamm Bowel Dis 15(11):1705-1720.
44. Yiangou Y, et al. (2001) Vanilloid receptor 1 immunoreactivity in inflamed human bowel. Lancet 357(9265):1338-1339. (Pubitemid 32441536)
45. Akbar A, et al. (2010) Expression of the TRPV1 receptor differs in quiescent inflammatory bowel disease with or without abdominal pain. Gut 59(6):767-774.
46. Akbar A, et al. (2008) Increased capsaicin receptor TRPV1-expressing sensory fibres in irritable bowel syndrome and their correlation with abdominal pain. Gut 57(7):923-929. (Pubitemid 351919527)
47. Knowlton WM, Bifolck-Fisher A, Bautista DM, McKemy DD (2010) TRPM8, but not TRPA1, is required for neural and behavioral responses to acute noxious cold temperatures and cold-mimetics in vivo. Pain 150(2):340-350.
48. Bandell M, et al. (2006) High-throughput random mutagenesis screen reveals TRPM8 residues specifically required for activation by menthol. Nat Neurosci 9(4):493-500.
49. Kühn FJ, Kühn C, Lückhoff A (2009) Inhibition of TRPM8 by icilin distinct from desensitization induced by menthol and menthol derivatives. J Biol Chem 284(7):4102-4111.
50. Latorre R, Brauchi S, Orta G, Zaelzer C, Vargas G (2007) ThermoTRP channels as modular proteins with allosteric gating. Cell Calcium 42(4-5):427-438. (Pubitemid 47264003)
51. Bödding M, Wissenbach U, Flockerzi V (2007) Characterisation of TRPM8 as a pharmacophore receptor. Cell Calcium 42(6):618-628. (Pubitemid 47471362)
52. Ma S, G G, Ak VE, Jf D, H H (2008) Menthol derivative WS-12 selectively activates transient receptor potential melastatin-8 (TRPM8) ion channels. Pak J Pharm Sci 21(4):370-378.
53. Rawls SM, Gomez T, Ding Z, Raffa RB (2007) Differential behavioral effect of the TRPM8/TRPA1 channel agonist icilin (AG-3-5). Eur J Pharmacol 575(1-3):103-104. (Pubitemid 47576072)
54. Trevisani M, et al. (2007) 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1. Proc Natl Acad Sci USA 104(33):13519-13524. (Pubitemid 47293977)
55. Mitrovic M, Shahbazian A, Bock E, Pabst MA, Holzer P (2010) Chemo-nociceptive signalling from the colon is enhanced by mild colitis and blocked by inhibition of transient receptor potential ankyrin 1 channels. Br J Pharmacol 160(6):1430-1442.
56. Zhang X, et al. (2012) Direct inhibition of the cold-activated TRPM8 ion channel by Gαq. Nat Cell Biol 14(8):851-858.
57. Bidaux G, et al. (2012) Regulation of activity of transient receptor potential melastatin 8 (TRPM8) channel by its short isoforms. J Biol Chem 287(5):2948-2962.