Functional aspects and mechanisms of TRPV1 involvement in neurogenic inflammation that leads to thermal hyperalgesia

Pflugers Archiv European Journal of Physiology

Volumn 451, Issue 1, 2005, Pages 151-159

  Planells Cases, Rosa ^a   Garcìa Sanz, Nuria ^b   Morenilla Palao, Cruz ^b   Ferrer Montiel, Antonio ^b  

^a CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^b MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE GROWTH FACTOR; PROTEIN KINASE; TRANSIENT RECEPTOR POTENTIAL CHANNEL;

ENDOTHELIUM CELL; EXCITABILITY; HYPERALGESIA; HYPERSENSITIVITY; INJURY; LYMPHOCYTE; NERVE ENDING; NEUROGENIC INFLAMMATION; NOCICEPTIVE RECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; SENSITIZATION; SENSORY NERVE; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; VASODILATATION;

ANIMALS; HYPERALGESIA; INFLAMMATION; INFLAMMATION MEDIATORS; NERVE GROWTH FACTOR; NEURONS, AFFERENT; PROTEIN KINASES; RATS; SNARE PROTEINS; TRPV CATION CHANNELS;

EID: 24644470357     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-005-1423-5     Document Type: Review

References (82)

1. Ahmari SE, Buchanan J, Smith SJ (2000) Assembly of pre-synaptic active zones from cytoplasmic transport packets. Nat Neurosci 3:445-451
2. Akiba Y, Furukawa O, Guth PH, Engel E, Nastaskin I, Kaunitz JD (2001) Sensory pathways and cyclooxygenase regulate mucus gel thickness in rat duodenum. Am J Physiol 280:G470-G474
3. Alstergren P, Appelgren A, Appelgren B, Kopp S, Lundeberg T, Theodorsson E (1995) Co-variation of neuropeptide Y, calcitonin gene-related peptide, substance P and neurokinin A in joint fluid from patients with temporomandibular joint arthritis. Arch Oral Biol 40:127-135
4. Amaya F, Oh-jasjo K, Naruse Y, Iijima N, Ueda M, Shimosato G, Tominaga M, Tanaka Y, Tanaka M (2003) Local inflammation increases vanilloid receptor I expression within distinct subgroups of DRG neurons. Brain Res 963:190-196
5. Amaya F, Shimosato G, Nagano M, Ueda M, Hashimoto S, Tanaka Y, Suzuki H, Tanaka M (2004) NGF and GDNF differentially regulate TRPV1 expression that contribute to development of inflammatory thermal hyperalgesia. Eur J Neurosci 20:2303-2310
6. Avelino A, Cruz C, Nagy I, Cruz F (2002) Vanilloid receptor 1 expression in the rat urinary tract. Neuroscience 109:787-798
7. Bernardini N, Neuhuber W, Reeh PW, Sauer SK (2004) Morphological evidence for functional capsaicin receptor expression and calcitonin gene-related peptide exocytosis in isolated peripheral nerve axons of the mouse. Neuroscience 126:585-590
8. Bhave G, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW IV (2002) cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 35:721-731
9. Bhave G, Hu HJ, Glauner KS, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW IV (2003) Protein kinase C phosphorylation sensitizes but does not activate the capsaicin receptor transient receptor potential vanilloid 1 (TRPV1). Proc Natl Acad Sci USA 100:12480-12485
10. Bhave G, Gereau RW IV (2004) Posttranslational mechanisms of peripheral sensitization. Int J Neurobiol 61:88-106
11. Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai AJ, Wang E, Ruiz G, De Groat WC, Apodaca G, Watkins S, Caterina MJ (2002) Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci 5:856-860
12. Bonnington JK, McNaughton PA (2003) Signalling pathways involved in the sensitization of mouse nociceptive neurones by nerve growth factor. J Physiol 551:433-446
13. Brain SD, Williams TJ, Tippins JR, Morris HR, MacIntyre I (1985) Calcitonin gene-related peptide is a potent vasodilator. Nature 313:54-56
14. Brain SD (1997) Sensory neuropeptides in inflammation and wound healing. Immunopharmacology 37:133-152
15. Carr MJ, Hunter DD, Jacoby DB, Undem BJ (2002) Expression of tachykinins in nociceptive vagal afferent neurons during respiratory viral infection in guinea pigs. Am J Respir 165:1071-1075
16. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824
17. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306-313
18. Caterina MJ, Julius D (2001) The vanilloid receptor: A molecular gateway to the pain pathway. Annu Rev Neurosci 24:487-517
19. Cesare P, McNaughton P (1997) Peripheral pain mechanisms. Curr Opin Neurobiol 7:457-482
20. Chleda MG, Ashery U, Thakur P, Rettig J, Sheng ZH (2001) Phosphorylation of Snapin by PKA modulates its interaction with the SNARE complex. Nat Cell Biol 3:331-338
21. Chu CJ, Huang SM, De Petrocellis L, Bisogno T, Ewing SA, Miller JA, Zipkin RE, Daddario N, Appendino G, Di Marzo V, Walker JM (2003) N-oleoyldopamine, a novel endogenous capsaicin-like lipid that produces hyperalgesia. J Biol Chem 278:13633-13639
22. Chuang HH, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, Chao MV, Julius D (2001) Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411:957-962
23. Crandall M, Kwash J, Yu W, White G (2002) Activation of protein kinase C sensitizes human VR1 to capsaicin and to moderate decreases in pH at physiological temperatures in Xenopus oocytes. Pain 98:109-117
24. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA (2000) Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405(6783):183-187
25. Durnett, Richardson J, Vasko MR (2002) Cellular mechanisms of neurogenic inflammation. J Pharmacol Exp Ther 304:88-98
26. Fukuda M, Kowalchyk JA, Zhang X, Martin TF, Mikoshiba K (2002) Vesicle-associated membrane protein-2/synaptobrevin binding to synaptotagmin I promotes O-glycosylation of synaptotagmin I. J Biol Chem 277:30351-30358
27. Ganju P, Davis A, Patel S, Nuñez X, Fox A (2001) p38 stress-activated protein kinase inhibitor reverses bradykinin B1 receptor-mediated component of inflammatory hyperalgesia. Eur J Pharmacol 421:191-199
28. García-Martínez C, Humet M, Planells-Cases R, Gomis A, Caprini M, Viana F, De La Pena E, Sanchez-Baeza F, Carbonell T, De Felipe C, Perez-Paya E, Belmonte C, Messeguer A, Ferrer-Montiel A (2002) Attenuation of thermal nociception and hyperalgesia by VR1 blockers. Proc Natl Acad Sci USA 99:2374-2379
29. Garcia-Sanz N, Ferández-Carvajal A, Morenilla-Palao C, Planells-Cases R, Fajardo-Sanche E, Fernández-Ballester G, Ferrer-Montiel A (2004) Identification of tetramerization domain in the C terminus of the vanilloid receptor. J Neurosci 24:5306-5314
30. Geppetti P, Trevisani M (2004) Activation and sensitisation of the vanilloid receptor: role in gastrointestinal inflammation and function. Br J Pharmacol 141:1313-1320
31. Greka A, Navarro B, Oancea E, Duggan A, Clapham DE (2003) TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nat Neurosci 6:837-845
32. Haberman Y, Grimberg E, Fukuda M, Sagi-Eisenberg R (2003) Synaptotagmin IX, a possible linker between the perinuclear endocytic recycling compartment and the microtubules. J Cell Sci 116:4307-4318
33. Holzer P (1988) Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24:739-768
34. Holzer P, Holzer-Petsche U (1997) Tachykinins and in the gut. Roles in neural excitation, secretion and inflammation. Pharmacol Ther 73:219-263
35. Holzer P (1991) Capsaicin: cellular targets, mechanisms of action, and selectivity for thin sensory neurons. Pharmacol Rev 43:143-201
36. Holzer P (2004) TRPV1 and the gut: from a tasty receptor for a painful vanilloid to a key player in hyperalgesia. Eur J Pharmacol 500:231-241
37. Huang SM, Bisogno T, Trevisani M, Al-Hayani A, De Petrocellis L, Fezza F, Tognetto M, Petros TJ, Krey JF, Chu CI, Miller JD, Davies SN, Geppetti P, Walker JM Di Marzo V (2002) An endogenous capsaicin-like substance with high potency at recombinant and native VR1 receptors. Proc Natl Acad Sci USA 99:8400-8405
38. Hunter DD, Myers AC, Undem BJ (2000) Nerve-growth factor induced phenotypic switch in guinea pig airway sensory neurons. Am J Respir 161:1985-1990
39. Hwang SW, Cho J, Kwak J, Lee SY, Kang J, Jung S, Cho KH, Min YG, Suh D, Kim U, Oh U (2000) Direct activation of capsaicin receptors by products of lipooxygenases: endogenous capsaicin-like substances. Proc Natl Acad Sci USA 97:6155-6056
40. Ilardi JM, Mochida S, Sheng ZH (1999) Snapin: a SNARE-associated protein implicated in synaptic transmission. Nat Neurosci 2:119-124
41. Inoue K, Koizumi S, Fuziwara S, Denda S, Inoue K, Denda M (2002) Functional vanilloid receptors in cultured normal human epidermal keratinocytes. Biochem Biophys Res Commun 291:124-129
42. Ji R-R, Samad TA, Jin S-X, Schmoll R, Woolf C (2002) p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36:57-68
43. Jin X, Morsy N, Winston J, Pasricha PJ, Garret K, Akbarali HI (2004) Modulation of TRPV1 by non-receptor tyrosine kinase, c-Src kinase. Am J Physiol 287:C558-C563
44. Julius D, Basbaum AI (2001) Molecular mechanisms of nociception. Nature 413:203-210
45. 2+/calmodulin-dependent kinase II regulates its vanilloid binding. J Biol Chem 279:7048-7054
46. Karlsson JA (1993) A role for capsaicin sensitive, tachykinin-containing nerves in chronic coughing and sneezing but not in asthma: a hypothesis. Thorax 48:396-400
47. Lan JY, Skeberdis VA, Jover T, Grooms SY, Lin Y, Araneda RC, Zheng X, Bennett MV, Zukin RS (2001) Protein kinase C modulates. NMDA receptor trafficking and gating. Nature Neurosci 4:382-390
48. Lundberg JM, Franco-Cereceda A, Hua X, Hokfelt T, Fischer JA (1985) Co-existence of substance P and calcitonin gene-related peptide-like immunoreactivities in sensory nerves in relation to cardiovascular and bronchoconstrictor effects of capsaicin. Eur J Pharmacol 108:315-319
49. Malmberg AB, Brandom EP, Idzerda RL, Liu H, McKnight GS, Basbaum AI (1997) Diminished inflammation and nociceptive pain with preservation of neuropathic pain in mice with a targeted mutation of the type I regulatory subunit of cAMP-dependent protein kinase. J Neuroscience 17:7462-7470
50. 2+-dependent desensitization in the vanilloid receptor TRPV1 by calcineurin and cAMP-dependent protein kinase. J Biol Chem 280:13424-13432
51. Morenilla-Palao C, Planells-Cases R, García-Sanz N, Ferrer-Montiel A (2004) Regulated exocytosis contributes to protein kinase C potentiation of vanilloid receptor activity. J Biol Chem 279:25665-25672
52. Morenilla-Palao C, Planells-Cases R, García-Sanz N, Fernán-dez-Carvajal A, Ferrer-Montiel A (2001) A member of the HIT family interacts with TRPV1. Soc Neurosci Abs 27, P 56.2
53. Nagy I, Sàntha P, Jancsò G, Urbàn L (2004) The role of vanilloid (capsaicin) receptor (TRPV1) in physiology and pathology. Eur J Pharmacol 500:351-369
54. Nakata T, Terada S, Hirokawa N (1998) Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons. J Cell Biol 140:659-674
55. Numazaki M, Tominaga T, Toyooka H, Tominaga M (2002) Direct phosphorylation of capsaicin receptor VR1 by protein kinase Cepsilon and identification of two target serine residues. J Biol Chem 277:13375-13378
56. Numazaki M, Tominaga T, Takeuchi K, Murayama N, Toyooka H, Tominaga M (2003) Structural determinant of TRPV1 desensitization interacts with calmodulin. Proc Natl Acad Sci USA 100:8002-8006
57. Obreja O, Rathee KP, Lips KS, Distler C, Kress M (2002) IL-1β potentiates heat-activated currents in rat sensory neurons: involvement of IL-1R1, tyrosine kinase and protein kinase C. FASEB J 16:1497-1503
58. Olah Z, Karai L, Iadarola MJ (2002) Protein kinase C(alpha) is required for vanilloid receptor 1 activation. Evidence for multiple signaling pathways. J Biol Chem 277:35752-35759
59. Premkumar LS, Ahern GP (2000) Induction of vanilloid receptor channel activity by protein kinase C. Nature 408:985-990
60. Prescott ED, Julius D (2003) A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300:1284-1288
61. s-mediated signalling to thermal hyperalgesia. J Neurosci 22:4740-4745
62. Richardson JD, Vasko MR (2002) Cellular mechanisms of neurogenic inflammation. J Pharmacol Exp Ther 302:839-845
63. Scholz J, Woolf CJ (2002) Can we conquer pain? Nat Neurosci 5:1062-1067
64. Stander S, Moormann C, Schumacher M, Buddenkotte J, Artuc M, Shpacovitc V, Brzoska T, Lippert U, Henz BM, Luger TA, Metze D, Steinhoff M (2004) Expression of vanilloid receptor subtype 1 in cutaneous sensory nerve fibers, mast cells, and epithelial cells of appendage structures. Exp Dermatol 13:129-139
65. Südhof TC (2002) Synaptotagmins: why so many? J Biol Chem 277:7629-7632
66. Sugiura T, Tominaga M, Katsuya H, Mizumura K (2002) Bradykinin lowers the threshold temperature for heat activation of vanilloid receptor 1. J Neurophysiol 88:544-548
67. Szallasi A, Di Marzo V (2000) New perspectives on enigmatic vanilloid receptors. Trends Neurosci 23:491-497
68. Szolcsanyi J (1996) Capsaicin-sensitive sensory nerve terminals with local and systemic efferent functions: facts and scopes of an unorthodox neuroregulatory mechanism. Prog Brain Res 113:343-359
69. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D (1998) The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21:531-543
70. Tominaga M, Wada M, Masu M (2001) Potentiation of capsaicin receptor activity by metabotropic ATP receptors as a possible mechanism for ATP-evoked pain and hyperalgesia. Proc Natl Acad Sci USA 98:6951-6956
71. Vellani V, Mapplebeck S, Moriondo A, Davis JB, McNaughton PA (2001) Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide. J Physiol 534:813-825
72. Vellani V, Zachrisson O, McNaughton PA (2004) Functional bradykinin B1 receptors are expressed in nociceptive neurones and are upregulated by the neurotrophin GDNF. J Physiol 560:391-401
73. Wang Y, Kedei N, Wang M, Wang QJ, Huppler AR, Toth A, Tran R, Blumberg PM (2004) Interaction between protein kinase Cmu and the vanilloid receptor type 1. J Biol Chem 279:53674-53682
74. Widman C, Gibson S, Jarpe MB, Jonhson GL (1999) Mitogen-activated protein kinase: a conservation of a three module from yeast to humans. Physiolol Rev 79:143-180
75. Williams M, Kowaluk EA, Arneric SP (1999) Emerging molecular approaches to pain therapy. J Med Chem 42:1481-1500
76. Wood JN, Docherthy R (1997) Chemical activators of sensory neurons. Rev Physiol 59:457-482
77. Woodbury CJ, Zwick M, Wang S, Lawson JJ, Caterina MJ, Koltzenburg M, Albers KM, Koerber HR, Davis BM (2004) Nociceptors lacking TRPV1 and TRPV2 have normal heat responses. J Neurosci 24:6410-6415
78. Woolf CJ, Safieh-Garabedian B, Ma QP, Crilly P, Winter J (1994) Nerve growth factor contributes to the generation of inflammatory sensory hypersensitivity. Neuroscience 62:327-331
79. Yang Y, Udayasankar S, Dunning J, Chen P, Gillis KD (2002) A highly Ca2+-sensitive pool of vesicles is regulated by protein kinase C in adrenal chromaffin cells. Proc Natl Acad Sci USA 99:17060-17065
80. 2+ current in Xenopus oocytes requires SNAP25 but not a diffusible messenger. Cell 98:475-485
81. Zhu H, Hille B, Xu T (2002) Sensitization of regulated exocytosis by protein kinase C. Proc Natl Acad Sci USA 99:17055-17059
82. Zhuang Z-Y, Xu H, Clapham DE, Ji R-R (2004) Phosphatidylinositol 3-kinase activates ERK in primary sensory neurons and mediates inflammatory heat hyperalgesia through TRPV1 sensitization. J Neurosci 24:8300-8309