TRPV1 and TRPA1 function and modulation are target tissue dependent

Journal of Neuroscience

Volumn 31, Issue 29, 2011, Pages 10516-10528

  Malin, Sacha ^a   Molliver, Derek ^a   Christianson, Julie A ^b   Schwartz, Erica S ^a   Cornuet, Pam ^a   Albers, Kathryn M ^a   Davis, Brian M ^a  

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

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLYL ISOTHIOCYANATE; ARTEMIN; CAPSAICIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; NERVE GROWTH FACTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; VANILLOID RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLITIS; CONTROLLED STUDY; FEMALE; IN VIVO STUDY; MALE; MODULATION; MOUSE; MUSCLE SPINDLE AFFERENT NERVE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SKIN INFLAMMATION; SPINAL GANGLION; TACHYPHYLAXIS;

ANIMALS; CALCIUM; CHOLERA TOXIN; COLITIS; COLON; CYTOKINES; DERMATITIS; DISEASE MODELS, ANIMAL; FLUORESCENT DYES; FREUND'S ADJUVANT; GENE EXPRESSION REGULATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MUSCLES; NEURAL PATHWAYS; PEROXIDASE; RECEPTORS, CYTOKINE; RNA, MESSENGER; SKIN; TIME FACTORS; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TRPV CATION CHANNELS; WHEAT GERM AGGLUTININS;

EID: 79960688619     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2992-10.2011     Document Type: Article

References (82)

1. Akopian AN, Ruparel NB, Jeske NA, Hargreaves KM (2007) Transient receptor potential TRPA1 channel desensitization in sensory neurons is agonist dependent and regulated by TRPV1-directed internalization. J Physiol 583:175-193.
2. Amaya F, Oh-hashi K, Naruse Y, Iijima N, Ueda M, Shimosato G, Tominaga M, Tanaka Y, Tanaka M (2003) Local inflammation increases vanilloid receptor 1 expression within distinct subgroups ofDRGneurons. Brain Res 963:190-196.
3. 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 contributes to development of inflammatory thermal hyperalgesia. Eur J Neurosci 20:2303-2310.
4. Baron R, Jänig W (1991) Afferent and sympathetic neurons projecting into lumbar visceral nerves of the male rat. J Comp Neurol 314:429-436.
5. Bautista DM, Movahed P, Hinman A, Axelsson HE, Sterner O, Högestätt ED, Julius D, Jordt SE, Zygmunt PM (2005) Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci U S A 102:12248-12252.
6. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI, JuliusD (2006) TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124:1269-1282.
7. Bennett DL, Michael GJ, Ramachandran N, Munson JB, Averill S, Yan Q, McMahon SB, Priestley JV (1998) A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J Neurosci 18:3059-3072.
8. Berkley KJ (2005) A life of pelvic pain. Physiol Behav 86:272-280.
9. Berkley KJ, Robbins A, Sato Y (1988) Afferent fibers supplying the uterus in the rat. J Neurophysiol 59:142-163.
10. Berkley KJ, Hotta H, Robbins A, Sato Y (1990) Functional properties of afferent fibers supplying reproductive and other pelvic organs in pelvic nerve of female rat. J Neurophysiol 63:256-272.
11. Berkley KJ, Rapkin AJ, Papka RE (2005) The pains of endometriosis. Science 308:1587-1589.
12. Bielefeldt K, Ozaki N, Gebhart GF (2003) Role of nerve growth factor in modulation of gastric afferent neurons in the rat. Am J Physiol Gastrointest Liver Physiol 284:G499-G507.
13. Burns K, Clatworthy J, Martin L, Martinon F, Plumpton C, Maschera B, Lewis A, Ray K, Tschopp J, Volpe F (2000) Tollip, a new component of the IL-1RI pathway, links IRAK to the IL-1 receptor. Nat Cell Biol 2:346-351.
14. Burnstock G (1987) Mechanisms of interaction of peptide and nonpeptide vascular neurotransmitter systems. J Cardiovasc Pharmacol 10 [Suppl 12]:S74-S81.
15. Carr PA, Yamamoto T, Nagy JI (1990) Calcitonin gene-related peptide in primary afferent neurons of rat: co-existence with fluoride-resistant acid phosphatase and depletion by neonatal capsaicin. Neuroscience 36:751-760.
16. Caterina MJ (2007) Transient receptor potential ion channels as participants in thermosensation and thermoregulation. Am J Physiol Regul Integr Comp Physiol 292:R64-R76.
17. 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.
18. 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.
19. Cervero F (1994) Sensory innervation of the viscera: peripheral basis of visceral pain. Physiol Rev 74:95-138.
20. Christianson JA, Traub RJ, Davis BM (2006a) Differences in spinal distribution and neurochemical phenotype of colonic afferents in mouse and rat. J Comp Neurol 494:246-259.
21. Christianson JA, McIlwrath SL, Koerber HR, Davis BM (2006b) Transient receptor potential vanilloid 1-immunopositive neurons in the mouse are more prevalent within colon afferents compared to skin and muscle afferents. Neuroscience 140:247-257.
22. Christianson JA, Liang R, Ustinova EE, Davis BM, Fraser MO, Pezzone MA (2007) Convergence of bladder and colon sensory innervation occurs at the primary afferent level. Pain 128:235-243.
23. Ciarrocchi A, D'Angelo R, Cordiglieri C, Rispoli A, Santi S, Riccio M, Carone S, Mancia AL, Paci S, Cipollini E, Ambrosetti D, Melli M (2009) Tollip is a mediator of protein sumoylation. PLoS One 4:e4404.
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 405:183-187.
25. De Schepper HU, De Man JG, Ruyssers NE, Deiteren A, Van Nassauw L, Timmermans JP, Martinet W, Herman AG, Pelckmans PA, De Winter BY (2008a) TRPV1 receptor signaling mediates afferent nerve sensitization during colitis-induced motility disorders in rats. Am J Physiol Gastrointest Liver Physiol 294:G245-G253.
26. De Schepper HU, De Winter BY, Van Nassauw L, Timmermans JP, Herman AG, Pelckmans PA, De Man JG (2008b) TRPV1 receptors on unmyelinated C-fibres mediate colitis-induced sensitization of pelvic afferent nerve fibres in rats. J Physiol 586:5247-5258.
27. Diogenes A, Akopian AN, Hargreaves KM (2007) NGF up-regulates TRPA1: implications for orofacial pain. J Dent Res 86:550-555.
28. Elitt CM, McIlwrath SL, Lawson JJ, Malin SA, Molliver DC, Cornuet PK, Koerber HR, Davis BM, Albers KM (2006) 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.
29. Elitt CM, Malin SA, Koerber HR, Davis BM, AlbersKM (2008) Overexpression of artemin in the tongue increases expression of TRPV1 and TRPA1 in trigeminal afferents and causes oral sensitivity to capsaicin and mustard oil. Brain Res 1230:80-90.
30. Fasanella KE, Christianson JA, Chanthaphavong RS, Davis BM (2008) Distribution and neurochemical identification of pancreatic afferents in the mouse. J Comp Neurol 509:42-52.
31. Gebhart GF, Bielefeldt K (2006) Visceral pain: basic mechanisms. In: Wall and Melzack's textbook of pain, Ed 5 (McMahon SB, Koltzenburg M, eds), pp 721-736. Philedephia: Elsevier.
32. Gibbins IL, Furness JB, Costa M, MacIntyre I, Hillyard CJ, Girgis S (1985) Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pigs. Neurosci Lett 57:125-130.
33. Glabinski AR, Bielecki B, Kolodziejski P, Han Y, Selmaj K, Ransohoff RM (2003) TNF-alpha microinjection upregulates chemokines and chemokine receptors in the central nervous system without inducing leukocyte infiltration. J Interferon Cytokine Res 23:457-466.
34. Gold MS, Traub RJ (2004) Cutaneous and colonic rat DRG neurons differ with respect to both baseline and PGE2-induced changes in passive and active electrophysiological properties. J Neurophysiol 91:2524-2531.
35. Holzer P (1998) Neurogenic vasodilatation and plasma leakage in the skin. Gen Pharmacol 30:5-11.
36. Honma Y, Araki T, Gianino S, Bruce A, Heuckeroth R, Johnson E, Milbrandt J (2002) Artemin is a vascular-derived neurotropic factor for developing sympathetic neurons. Neuron 35:267-282.
37. Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ (2002) p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36:57-68.
38. Jordt SE, McKemy DD, Julius D (2003) Lessons from peppers and peppermint: the molecular logic of thermosensation. Curr Opin Neurobiol 13:487-492.
39. Kashiba H, Uchida Y, Senba E (2003) Distribution and colocalization of NGF andGDNFfamily ligand receptor mRNAs in dorsal root and nodose ganglion neurons of adult rats. Brain Res Mol Brain Res 110:52-62.
40. Keast JR, De Groat WC (1992) Segmental distribution and peptide content of primary afferent neurons innervating the urogenital organs and colon of male rats. J Comp Neurol 319:615-623.
41. Kobayashi K, Fukuoka T, Obata K, Yamanaka H, Dai Y, Tokunaga A, Noguchi K (2005) Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with aδ/c-fibers and colocalization with trk receptors. J Comp Neurol 493:596-606.
42. Kruger L, Silverman JD, Mantyh PW, Sternini C, Brecha NC (1989) Peripheral patterns of calcitonin-gene-related peptide general somatic sensory innervation: cutaneous and deep terminations. J Comp Neurol 280:291-302.
43. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, Corey DP (2006) TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277-289.
44. Latorre R, Brauchi S, Orta G, Zaelzer C, Vargas G (2007) ThermoTRP channels as modular proteins with allosteric gating. Cell Calcium 42:427-438.
45. Lawson SN (1992) Morphological and biochemical cell types of sensory neurons. In: Sensory neurons, diversity, development and plasticity (Scott SA, ed), pp 27-59. New York: Oxford.
46. Lewin GR, Mendell LM (1994) Regulation of cutaneous C-fiber heat nociceptors by nerve growth factor in the developing rat. J Neurophysiol 71:941-949.
47. Lewin GR, Rueff A, Mendell LM (1994) Peripheral and central mechanisms of NGF-induced hyperalgesia. Eur J Neurosci 6:1903-1912.
48. Light AR, Hughen RW, Zhang J, Rainier J, Liu Z, Lee J (2008) Dorsal root ganglion neurons innervating skeletal muscle respond to physiological combinations of protons, ATP, and lactate mediated by ASIC, P2X, and TRPV1. J Neurophysiol 100:1184-1201.
49. Lindfors PH, Vo ̃ikar V, Rossi J, Airaksinen MS (2006) Deficient nonpeptidergic epidermis innervation and reduced inflammatory pain in glial cell line-derived neurotrophic factor family receptorα2 knock-out mice. J Neurosci 26:1953-1960.
50. δδC (T) method. Methods 25:402-408.
51. Lu J, Zhou XF, Rush RA (2001) Small primary sensory neurons innervating epidermis and viscera display differential phenotype in the adult rat. Neurosci Res 41:355-363.
52. Malin SA, Molliver DC, Koerber HR, Cornuet P, Frye R, Albers KM, Davis BM (2006) Glial cell line-derived neurotrophic factor family members sensitize nociceptors in vitro and produce thermal hyperalgesia in vivo. J Neurosci 26:8588-8599.
53. Malin SA, Davis BM, Molliver DC (2007) Production of dissociated sensory neuron cultures and considerations for their use in studying neuronal function and plasticity. Nat Protoc 2:152-160.
54. McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52-58.
55. Molliver DC, Snider WD (1997) Nerve growth factor receptor TrkA is down-regulated during postnatal development by a subset of dorsal root ganglion neurons. J Comp Neurol 381:428-438.
56. Molliver DC, Radeke MJ, Feinstein SC, Snider WD (1995) Presence or absence of TrkA protein distinguishes subsets of small sensory neurons with unique cytochemical characteristics and dorsal horn projections. J Comp Neurol 361:404-416.
57. Molliver DC, Lindsay J, Albers KM, Davis BM (2005) Overexpression of NGF or GDNF alters transcriptional plasticity evoked by inflammation. Pain 113:277-284.
58. Obata K, Katsura H, Mizushima T, Yamanaka H, Kobayashi K, Dai Y, Fukuoka T, Tokunaga A, Tominaga M, Noguchi K (2005) TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J Clin Invest 115:2393-2401.
59. Oh SB, Tran PB, Gillard SE, Hurley RW, Hammond DL, Miller RJ (2001) Chemokines and glycoprotein 120 produce pain hypersensitivity by directly exciting primary nociceptive neurons. J Neurosci 21:5027-5035.
60. Orozco OE, Walus L, Sah DW, Pepinsky RB, Sanicola M (2001) GFRalpha3 is expressed predominantly in nociceptive sensory neurons. Eur J Neurosci 13:2177-2182.
61. Ota M, Katsuyama Y, Hamano H, Umemura T, Kimura A, Yoshizawa K, Kiyosawa K, Fukushima H, Bahram S, Inoko H, Kawa S (2007) Two critical genes (HLA-DRB1 and ABCF1) in the HLA region are associated with the susceptibility to autoimmune pancreatitis. Immunogenetics 59:45-52.
62. Oyelese AA, Kocsis JD (1996) GABAA-receptor-mediated conductance and action potential waveform in cutaneous and muscle afferent neurons of the adult rat: differential expression and response to nerve injury. J Neurophysiol 76:2383-2392.
63. Paytubi S, Wang X, Lam YW, Izquierdo L, Hunter MJ, Jan E, Hundal HS, Proud CG (2009) ABC50 promotes translation initiation in mammalian cells. J Biol Chem 284:24061-24073.
64. Price TJ, Louria MD, Candelario-Soto D, Dussor GO, Jeske NA, Patwardhan AM, Diogenes A, Trott AA, Hargreaves KM, Flores CM (2005) Treatment of trigeminal ganglion neurons in vitro with NGF, GDNF or BDNF: effects on neuronal survival, neurochemical properties and TRPV1- mediated neuropeptide secretion. BMC Neurosci 6:4.
65. Richard M, Drouin R, Beaulieu AD (1998) ABC50, a novel human ATPbinding cassette protein found in tumor necrosis factor-alpha-stimulated synoviocytes. Genomics 53:137-145.
66. Robinson DR, McNaughton PA, Evans ML, Hicks GA (2004) Characterization of the primary spinal afferent innervation of the mouse colon using retrograde labelling. Neurogastroenterol Motil 16:113-124.
67. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101-1108.
68. Schmutzler BS, Roy S, Hingtgen CM (2009) Glial cell line-derived neurotrophic factor family ligands enhance capsaicin-stimulated release of calcitonin gene-related peptide from sensory neurons. Neuroscience 161:148-156.
69. Semov A, Semova N, Lacelle C, Marcotte R, Petroulakis E, Proestou G, Wang E (2002) Alterations in TNF- and IL-related gene expression in spaceflown WI38 human fibroblasts. FASEB J 16:899-901.
70. Shu X, Mendell LM (1999) Nerve growth factor acutely sensitizes the response of adult rat sensory neurons to capsaicin. Neurosci Lett 274:159-162.
71. Subang MC, Richardson PM (2001) Influence of injury and cytokines on synthesis of monocyte chemoattractant protein-1 mRNA in peripheral nervous tissue. Eur J Neurosci 13:521-528.
72. Tominaga M, Caterina MJ (2004) Thermosensation and pain. J Neurobiol 61:3-12.
73. Wang HF, Shortland P, Park MJ, Grant G (1998) Retrograde and transganglionic transport of horseradish peroxidase-conjugated cholera toxin B subunit, wheatgerm agglutinin and isolectin B4 from Griffonia simplicifolia I in primary afferent neurons innervating the rat urinary bladder. Neuroscience 87:275-288.
74. White FA, Sun J, Waters SM, Ma C, Ren D, Ripsch M, Steflik J, Cortright DN, Lamotte RH, Miller RJ (2005) Excitatory monocyte chemoattractant protein-1 signaling is up-regulated in sensory neurons after chronic compression of the dorsal root ganglion. Proc Natl Acad Sci U S A 102: 14092-14097.
75. Wick EC, Hoge SG, Grahn SW, Kim E, Divino LA, Grady EF, Bunnett NW, Kirkwood KS (2006) Transient receptor potential vanilloid 1, calcitonin gene-related peptide, and substance P mediate nociception in acute pancreatitis. Am J Physiol Gastrointest Liver Physiol 290:G959-G969.
76. Willis WD Jr (2007) The somatosensory system, with emphasis on structures important for pain. Brain Res Rev 55:297-313.
77. Winston J, Shenoy M, Medley D, Naniwadekar A, Pasricha PJ (2007) The vanilloid receptor initiates and maintains colonic hypersensitivity induced by neonatal colon irritation in rats. Gastroenterology 132:615-627.
78. 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.
79. 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.
80. Xu GY, Winston JH, Shenoy M, Yin H, Pendyala S, Pasricha PJ (2007) Transient receptor potential vanilloid 1 mediates hyperalgesia and is up-regulated in rats with chronic pancreatitis. Gastroenterology 133:1282-1292.
81. Yang J, Li Y, Zuo X, Zhen Y, Yu Y, Gao L (2008) Transient receptor potential ankyrin-1 participates in visceral hyperalgesia following experimental colitis. Neurosci Lett 440:237-241.
82. Zwick M, Davis BM, Woodbury CJ, Burkett JN, Koerber HR, Simpson JF, Albers KM (2002) Glial cell line-derived neurotrophic factor is a survival factor for isolectin B4-positive, but not vanilloid receptor 1-positive, neurons in the mouse. J Neurosci 22:4057-4065.