Artemin growth factor increases nicotinic cholinergic receptor subunit expression and activity in nociceptive sensory neurons

Molecular Pain

Volumn 10, Issue 1, 2014, Pages

  Albers, Kathryn M ^a   Zhang, Xiu L ^a   Diges, Charlotte M ^a   Schwartz, Erica S ^a   Yang, Charles I ^a   Davis, Brian M ^a   Gold, Michael S ^a  

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

Author keywords

Artemin; Growth factor; Inflammation; Nicotinic receptor; Skin

Indexed keywords

ARTEMIN; BUNGAROTOXIN RECEPTOR; FREUND ADJUVANT; GREEN FLUORESCENT PROTEIN; GROWTH FACTOR; HEXAMETHONIUM; MECAMYLAMINE; MESSENGER RNA; NICOTINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA2; NICOTINIC RECEPTOR ALPHA3; NICOTINIC RECEPTOR ALPHA4; NICOTINIC RECEPTOR ALPHA5; NICOTINIC RECEPTOR ALPHA6; NICOTINIC RECEPTOR ALPHA9; NICOTINIC RECEPTOR BETA2; NICOTINIC RECEPTOR BETA3; NICOTINIC RECEPTOR BETA4; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; ASSAY; BEHAVIORAL TESTING ASSAY; BIOPHYSICS; CELL LABELING; CONTROLLED STUDY; DERMATITIS; EVOKED RESPONSE; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HYPERALGESIA; IMMUNOREACTIVITY; KNOCKOUT MOUSE; MALE; MOUSE; NOCICEPTION; NONHUMAN; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORY NERVE; SENSORY NERVE CELL; SENSORY SYSTEM ELECTROPHYSIOLOGY; SKIN NERVE; SPINAL GANGLION; TEMPERATURE SENSITIVITY; TRANSGENIC MOUSE; TRIGEMINUS GANGLION; VALIDATION PROCESS;

ANIMALS; FEMALE; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; HEXAMETHONIUM; HYPERALGESIA; MALE; MECAMYLAMINE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NICOTINIC ANTAGONISTS; NOCICEPTORS; PROTEIN SUBUNITS; RECEPTORS, NICOTINIC; SKIN; TRIGEMINAL GANGLION;

EID: 84901603457     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-10-31     Document Type: Article

References (62)

1. Gold MS, Gebhart GF. Nociceptor sensitization in pain pathogenesis. Nat Med 2010, 16:1248-1257. 10.1038/nm.2235, 20948530.
2. Forrest SL, Keast JR. Expression of receptors for glial cell line-derived neurotrophic factor family ligands in sacral spinal cord reveals separate targets of pelvic afferent fibers. J Comp Neurol 2008, 506:989-1002. 10.1002/cne.21535, 3049865, 18085594.
3. Orozco OE, Walus L, Sah DW, Pepinsky RB, Sanicola M. GFRalpha3 is expressed predominantly in nociceptive sensory neurons. Eur J Neurosci 2001, 13:2177-2182. 10.1046/j.0953-816x.2001.01596.x, 11422460.
4. Weinkauf B, Rukwied R, Quiding H, Dahllund L, Johansson P, Schmelz M. Local gene expression changes after UV-irradiation of human skin. PLoS One 2012, 7:e39411. 10.1371/journal.pone.0039411, 3382209, 22761785.
5. Murota H, Izumi M, Abd El-Latif MI, Nishioka M, Terao M, Tani M, Matsui S, Sano S, Katayama I. Artemin causes hypersensitivity to warm sensation, mimicking warmth-provoked pruritus in atopic dermatitis. J Allergy Clin Immunol 2012, 130:671-682. e674, 10.1016/j.jaci.2012.05.027, 22770266.
6. 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 2006, 26:8588-8599. 10.1523/JNEUROSCI.1726-06.2006, 16914685.
7. Thornton P, Hatcher JP, Robinson I, Sargent B, Franzen B, Martino G, Kitching L, Glover CP, Anderson D, Forsmo-Bruce H, Low CP, Cusdin F, Dosanijh B, Williams W, Steffen AC, Thommpson S, Eklund M, Lloyd C, Chessell I, Hughes J. Artemin-GFRalpha3 interactions partially contribute to acute inflammatory hypersensitivity. Neurosci Lett 2013, 545:23-28.
8. 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 2009, 161:148-156. 10.1016/j.neuroscience.2009.03.006, 2832305, 19285119.
9. Elitt CM, Malin SA, Koerber HR, Davis BM, Albers KM. 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 2008, 1230:80-90. 2570744, 18652806.
10. 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 2006, 26:8578-8587. 10.1523/JNEUROSCI.2185-06.2006, 16914684.
11. Hurst R, Rollema H, Bertrand D. Nicotinic acetylcholine receptors: from basic science to therapeutics. Pharmacol Ther 2013, 137:22-54. 10.1016/j.pharmthera.2012.08.012, 22925690.
12. Dussor GO, Leong AS, Gracia NB, Kilo S, Price TJ, Hargreaves KM, Flores CM. Potentiation of evoked calcitonin gene-related peptide release from oral mucosa: a potential basis for the pro-inflammatory effects of nicotine. Eur J Neurosci 2003, 18:2515-2526. 10.1046/j.1460-9568.2003.02935.x, 2914552, 14622152.
13. Flores CM. The promise and pitfalls of a nicotinic cholinergic approach to pain management. Pain 2000, 88:1-6. 10.1016/S0304-3959(00)00389-4, 11098093.
14. Flores CM, DeCamp RM, Kilo S, Rogers SW, Hargreaves KM. Neuronal nicotinic receptor expression in sensory neurons of the rat trigeminal ganglion: demonstration of alpha3beta4, a novel subtype in the mammalian nervous system. J Neurosci 1996, 16:7892-7901.
15. Rau KK, Johnson RD, Cooper BY. Nicotinic AChR in subclassified capsaicin-sensitive and -insensitive nociceptors of the rat DRG. J Neurophysiol 2005, 93:1358-1371.
16. Roberts RG, Stevenson JE, Westerman RA, Pennefather J. Nicotinic acetylcholine receptors on capsaicin-sensitive nerves. Neuroreport 1995, 6:1578-1582. 10.1097/00001756-199507310-00028, 7579153.
17. Steen KH, Reeh PW. Actions of cholinergic agonists and antagonists on sensory nerve endings in rat skin, in vitro. J Neurophysiol 1993, 70:397-405.
18. Wang Y, Erickson RP, Simon SA. Selectivity of lingual nerve fibers to chemical stimuli. J Gen Physiol 1993, 101:843-866. 10.1085/jgp.101.6.843, 2216747, 8331321.
19. Jancso N, Jancso-Gabor A, Takats I. Pain and inflammation induced by nicotine, acetylcholine and structurally related compounds and their prevention by desensitizing agents. Acta Physiol Acad Sci Hung 1961, 19:113-132.
20. Jancso N, Jancso-Gabor A, Szolcsanyi J. Direct evidence for neurogenic inflammation and its prevention by denervation and by pretreatment with capsaicin. Br J Pharmacol Chemother 1967, 31:138-151. 10.1111/j.1476-5381.1967.tb01984.x, 1557289, 6055248.
21. Dessirier JM, O'Mahony M, Carstens E. Oral irritant effects of nicotine. Psychophysical evidence for decreased sensation following repeated application of and lack of cross-desensitization to capsaicin. Ann N Y Acad Sci 1998, 855:828-830. 10.1111/j.1749-6632.1998.tb10669.x, 9929695.
22. Grando SA, Kist DA, Qi M, Dahl MV. Human keratinocytes synthesize, secrete, and degrade acetylcholine. J Invest Dermatol 1993, 101:32-36. 10.1111/1523-1747.ep12358588, 8331294.
23. Schmelz M, Schmidt R, Weidner C, Hilliges M, Torebjork HE, Handwerker HO. Chemical response pattern of different classes of C-nociceptors to pruritogens and algogens. J Neurophysiol 2003, 89:2441-2448. 10.1152/jn.01139.2002, 12611975.
24. Carstens E, Kuenzler N, Handwerker HO. Activation of neurons in rat trigeminal subnucleus caudalis by different irritant chemicals applied to oral or ocular mucosa. J Neurophysiol 1998, 80:465-492.
25. Peterziel H, Paech T, Strelau J, Unsicker K, Krieglstein K. Specificity in the crosstalk of TGFbeta/GDNF family members is determined by distinct GFR alpha receptors. J Neurochem 2007, 103:2491-2504. 10.1111/j.1471-4159.2007.04962.x, 17953664.
26. Baloh RH, Gorodinsky A, Golden JP, Tansey MG, Keck CL, Popescu NC, Johnson EM, Milbrandt J. GFRalpha3 is an orphan member of the GDNF/neurturin/persephin receptor family. Proc Natl Acad Sci U S A 1998, 95:5801-5806. 10.1073/pnas.95.10.5801, 20460, 9576965.
27. Baloh RH, Tansey MG, Lampe PA, Fahrner TJ, Enomoto H, Simburger KS, Leitner ML, Araki T, Johnson EM, Milbrandt J. Artemin, a novel member of the GDNF ligand family, supports peripheral and central neurons and signals through the GFRalpha3-RET receptor complex. Neuron 1998, 21:1291-1302. 10.1016/S0896-6273(00)80649-2, 9883723.
28. Enomoto H. Regulation of neural development by glial cell line-derived neurotrophic factor family ligands. Anat Sci Int 2005, 80:42-52. 10.1111/j.1447-073x.2005.00099.x, 15794130.
29. Albers KM, Perrone TN, Goodness TP, Jones ME, Green MA, Davis BM. Cutaneous overexpression of NT-3 increases sensory and sympathetic neuron number and enhances touch dome and hair follicle innervation. J Cell Biol 1996, 134:487-497. 10.1083/jcb.134.2.487, 2120868, 8707832.
30. Wang T, Jing X, Schwartz ES, Molliver DC, DeBerry JJ, Albers KM, Davis BM. Neurturin Overexpression in Skin Enhances Expression of TRPM8 in Cutaneous Sensory Neurons and Leads to Behavioral Sensitivity to Cold and Menthol. J Neurosci 2012, In press.
31. Talavera K, Gees M, Karashima Y, Meseguer VM, Vanoirbeek JA, Damann N, Everaerts W, Benoit M, Janssens A, Vennekens R, Viana F, Nemery B, Nilius B, Voets T. Nicotine activates the chemosensory cation channel TRPA1. Nat Neurosci 2009, 12:1293-1299. 10.1038/nn.2379, 19749751.
32. Zoli M, Lena C, Picciotto MR, Changeux JP. Identification of four classes of brain nicotinic receptors using beta2 mutant mice. J Neurosci 1998, 18:4461-4472.
33. Michelmore S, Croskery K, Nozulak J, Hoyer D, Longato R, Weber A, Bouhelal R, Feuerbach D. Study of the calcium dynamics of the human alpha4beta2, alpha3beta4 and alpha1beta1gammadelta nicotinic acetylcholine receptors. Naunyn Schmiedebergs Arch Pharmacol 2002, 366:235-245. 10.1007/s00210-002-0589-z, 12172706.
34. Spies M, Lips KS, Kurzen H, Kummer W, Haberberger RV. Nicotinic acetylcholine receptors containing subunits alpha3 and alpha5 in rat nociceptive dorsal root ganglion neurons. J Mol Neurosci 2006, 30:55-56. 10.1385/JMN:30:1:55, 17192625.
35. Albuquerque EX, Pereira EF, Castro NG, Alkondon M, Reinhardt S, Schroder H, Maelicke A. Nicotinic receptor function in the mammalian central nervous system. Ann N Y Acad Sci 1995, 757:48-72. 10.1111/j.1749-6632.1995.tb17464.x, 7611705.
36. Zhang XL, Gold MS, Albers KM. Persistent inflammation is associated with an increase of nicotine evoked current in cutaneous nociceptive DRG neurons from the adult rat. Program No. 179.08 pp. Online. Neuroscience Meeting Planner. 2012, New Orleans, LA: Society for Neuroscience.
37. Martinou JC, Falls DL, Fischbach GD, Merlie JP. Acetylcholine receptor-inducing activity stimulates expression of the epsilon-subunit gene of the muscle acetylcholine receptor. Proc Natl Acad Sci U S A 1991, 88:7669-7673. 10.1073/pnas.88.17.7669, 52363, 1881908.
38. Kim HG, Lee CK, Cho SM, Whang K, Cha BH, Shin JH, Song KH, Jeong SW. Neuregulin 1 up-regulates the expression of nicotinic acetylcholine receptors through the ErbB2/ErbB3-PI3K-MAPK signaling cascade in adult autonomic ganglion neurons. J Neurochem 2013, 124:502-513. 10.1111/jnc.12109, 23199222.
39. Henderson LP, Gdovin MJ, Liu C, Gardner PD, Maue RA. Nerve growth factor increases nicotinic ACh receptor gene expression and current density in wild-type and protein kinase A-deficient PC12 cells. J Neurosci 1994, 14:1153-1163.
40. Airaksinen MS, Saarma M. The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci 2002, 3:383-394. 10.1038/nrn812, 11988777.
41. Stucky CL, Rossi J, Airaksinen MS, Lewin GR. GFR alpha2/neurturin signalling regulates noxious heat transduction in isolectin B4-binding mouse sensory neurons. J Physiol 2002, 545:43-50. 10.1113/jphysiol.2002.027656, 2290664, 12433948.
42. Wessler I, Reinheimer T, Kilbinger H, Bittinger F, Kirkpatrick CJ, Saloga J, Knop J. Increased acetylcholine levels in skin biopsies of patients with atopic dermatitis. Life Sci 2003, 72:2169-2172. 10.1016/S0024-3205(03)00079-1, 12628475.
43. Bernardini N, Sauer SK, Haberberger R, Fischer MJ, Reeh PW. Excitatory nicotinic and desensitizing muscarinic (M2) effects on C-nociceptors in isolated rat skin. J Neurosci 2001, 21:3295-3302.
44. Thomas E, Silman AJ, Croft PR, Papageorgiou AC, Jayson MI, Macfarlane GJ. Predicting who develops chronic low back pain in primary care: a prospective study. BMJ 1999, 318:1662-1667. 10.1136/bmj.318.7199.1662, 28145, 10373170.
45. Eliasson B. Cigarette smoking and diabetes. Prog Cardiovasc Dis 2003, 45:405-413. 10.1016/S0033-0620(03)80004-X, 12704597.
46. Yunus MB, Arslan S, Aldag JC. Relationship between fibromyalgia features and smoking. Scand J Rheumatol 2002, 31:301-305. 10.1080/030097402760375214, 12455822.
47. Hart AR, Kennedy H, Harvey I. Pancreatic cancer: a review of the evidence on causation. Clin Gastroenterol Hepatol 2008, 6:275-282. 10.1016/j.cgh.2007.12.041, 18328435.
48. Benarroch EE, Low PA. The acetylcholine-induced flare response in evaluation of small fiber dysfunction. Ann Neurol 1991, 29:590-595. 10.1002/ana.410290604, 1892361.
49. Liu L, Zhu W, Zhang ZS, Yang T, Grant A, Oxford G, Simon SA. Nicotine inhibits voltage-dependent sodium channels and sensitizes vanilloid receptors. J Neurophysiol 2004, 91:1482-1491. 10.1152/jn.00922.2003, 14657192.
50. Liu L, Simon SA. Capsaicin and nicotine both activate a subset of rat trigeminal ganglion neurons. Am J Physiol 1996, 270:C1807-C1814.
51. Gao B, Hierl M, Clarkin K, Juan T, Nguyen H, Valk M, Deng H, Guo W, Lehto SG, Matson D, McDermott JS, Knop J, Gaida K, Cao L, Waldon D, Albrecht BK, Boezio AA, Copeland KW, Harmange JC, Springer SK, Malmberg AB, McDonough SI. Pharmacological effects of nonselective and subtype-selective nicotinic acetylcholine receptor agonists in animal models of persistent pain. Pain 2010, 149:33-49. 10.1016/j.pain.2010.01.007, 20167427.
52. Vincler M. Neuronal nicotinic receptors as targets for novel analgesics. Expert Opin Investig Drugs 2005, 14:1191-1198. 10.1517/13543784.14.10.1191, 16185161.
53. Umana IC, Daniele CA, McGehee DS. Neuronal nicotinic receptors as analgesic targets: it's a winding road. Biochem Pharmacol 2013, 86:1208-1214. 10.1016/j.bcp.2013.08.001, 23948066.
54. Iwamoto ET, Marion L. Adrenergic, serotonergic and cholinergic components of nicotinic antinociception in rats. J Pharmacol Exp Ther 1993, 265:777-789.
55. Khan IM, Buerkle H, Taylor P, Yaksh TL. Nociceptive and antinociceptive responses to intrathecally administered nicotinic agonists. Neuropharmacology 1998, 37:1515-1525. 10.1016/S0028-3908(98)00143-9, 9886674.
56. Gardell LR, Wang R, Ehrenfels C, Ossipov MH, Rossomando AJ, Miller S, Buckley C, Cai AK, Tse A, Foley SF, Gong B, Walus L, Carmillo P, Worley D, Huang C, Engber T, Pepinsky B, Cate RL, Vanderah TW, Lai J, Sah DW, Porreca F. Multiple actions of systemic artemin in experimental neuropathy. Nat Med 2003, 9:1383-1389. 10.1038/nm944, 14528299.
57. Okkerse P, Hay J, Groeneveld G, Bersage E, Tang T, Galluppi G, Aycardi E. A randomized, blinded, placebo-controlled, multiple ascending dose study of the safety, pharmacokinetics, and efficacy of neublastin in subjects with sciatica. 2013, Toronto, Canada: 4th international Congress on Neuropathic Pain.
58. Hama A, Menzaghi F. Antagonist of nicotinic acetylcholine receptors (nAChR) enhances formalin-induced nociception in rats: tonic role of nAChRs in the control of pain following injury. Brain Res 2001, 888:102-106. 10.1016/S0006-8993(00)03022-5, 11146056.
59. Medhurst SJ, Hatcher JP, Hille CJ, Bingham S, Clayton NM, Billinton A, Chessell IP. Activation of the alpha7-nicotinic acetylcholine receptor reverses complete freund adjuvant-induced mechanical hyperalgesia in the rat via a central site of action. J Pain 2008, 9:580-587. 10.1016/j.jpain.2008.01.336, 18420461.
60. Vilceanu D, Stucky CL. TRPA1 mediates mechanical currents in the plasma membrane of mouse sensory neurons. PLoS One 2010, 5:e12177. 10.1371/journal.pone.0012177, 2922334, 20808441.
61. Zhang J, Xiao Y, Abdrakhmanova G, Wang W, Cleemann L, Kellar KJ, Morad M. Activation and Ca2+ permeation of stably transfected alpha3/beta4 neuronal nicotinic acetylcholine receptor. Mol Pharmacol 1999, 55:970-981.
62. Lopshire JC, Nicol GD. Activation and recovery of the PGE2-mediated sensitization of the capsaicin response in rat sensory neurons. J Neurophysiol 1997, 78:3154-3164.