Artemin, a glial cell line-derived neurotrophic factor family member, induces TRPM8-dependent cold pain

Journal of Neuroscience

Volumn 33, Issue 30, 2013, Pages 12543-12552

  Lippoldt, Erika K ^a   Elmes, Russell R ^a   McCoy, Daniel D ^a   Knowlton, Wendy M ^a   McKemy, David D ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTEMIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR ALPHA 3; PROTEIN TYROSINE KINASE A; PURINERGIC P2X3 RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; COLD PAIN; COLD SENSITIVITY; CONTROLLED STUDY; COOLING; FEMALE; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PAIN; PAIN RECEPTOR; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; THERMORECEPTOR;

ANIMALS; CHRONIC PAIN; COLD TEMPERATURE; FEMALE; GANGLIA, SPINAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; HOT TEMPERATURE; HYPERALGESIA; MALE; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NOCICEPTION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SENSORY RECEPTOR CELLS; TRANSCRIPTIONAL ACTIVATION; TRIGEMINAL GANGLION; TRPM CATION CHANNELS;

EID: 84880621886     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5765-12.2013     Document Type: Article

References (69)

1. Abrahamsen B, Zhao J, Asante CO, Cendan CM, Marsh S, Martinez-Barbera JP, Nassar MA, Dickenson AH, Wood JN (2008) The cell and molecular basis of mechanical, cold, and inflammatory pain. Science 321:702-705. CrossRef Medline
2. Airaksinen MS, Saarma M (2002) The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci 3:383-394. CrossRef Medline
3. Attal N, Bouhassira D, Gautron M, Vaillant JN, Mitry E, Lepère C, Rougier P, Guirimand F (2009) Thermal hyperalgesia as a marker of oxaliplatin neurotoxicity: a prospective quantified sensory assessment study. Pain 144:245-252. CrossRef Medline
4. Babes A, Zorzon D, Reid G (2004) Two populations of cold-sensitive neurons in rat dorsal root ganglia and their modulation by nerve growth factor. Eur J Neurosci 20:2276-2282. CrossRef Medline
5. Baloh RH, Tansey MG, Lampe PA, Fahrner TJ, Enomoto H, Simburger KS, Leitner ML, Araki T, Johnson EM Jr, Milbrandt J (1998) Artemin, a novel member of the GDNF ligand family, supports peripheral and central neurons and signals through the GFRalpha3-RET receptor complex. Neuron 21:1291-1302. CrossRef Medline
6. Baloh RH, Enomoto H, Johnson EM Jr, Milbrandt J (2000) The GDNF family ligands and receptors-implications for neural development. Curr Opin Neurobiol 10:103-110. CrossRef Medline
7. Basbaum AI, Bautista DM, Scherrer G, Julius D (2009) Cellular and molecular mechanisms of pain. Cell 139:267-284. CrossRef Medline
8. Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt SE, Julius D (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448:204-208. CrossRef Medline
9. Bennett DL, Boucher TJ, Michael GJ, Popat RJ, Malcangio M, Averill SA, Poulsen KT, Priestley JV, Shelton DL, McMahon SB (2006) Artemin has potent neurotrophic actions on injured C-fibres. J Peripher Nerv Syst 11:330-345. CrossRef Medline
10. Brenneis C, Kistner K, Puopolo M, Segal D, Roberson D, Sisignano M, Labocha S, Ferreirós N, Strominger A, Cobos EJ, Ghasemlou N, Geisslinger G, Reeh PW, Bean BP, Woolf CJ (2013) Phenotyping the function of TRPV1-expressing sensory neurons by targeted axonal silencing. J Neurosci 33:315-326. CrossRef Medline
11. Carmillo P, Dagø L, Day ES, Worley DS, Rossomando A, Walus L, Orozco O, Buckley C, Miller S, Tse A, Cate RL, Rosenblad C, Sah DW, Grønborg M, Whitty A (2005) Glial cell line-derived neurotrophic factor (GDNF) receptor alpha-1 (GFR alpha 1) is highly selective for GDNF versus artemin. Biochemistry 44:2545-2554. CrossRef Medline
12. Cavanaugh DJ, Lee H, Lo L, Shields SD, Zylka MJ, Basbaum AI, Anderson DJ (2009) Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc Natl Acad Sci U S A 106:9075-9080. CrossRef Medline
13. 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. CrossRef Medline
14. Chung MK, Caterina MJ (2007) TRP channel knock-out mice lose their cool. Neuron 54:345-347. CrossRef Medline
15. Colburn RW, Lubin ML, Stone DJ Jr, Wang Y, Lawrence D, D'Andrea MR, Brandt MR, Liu Y, Flores CM, Qin N (2007) Attenuated cold sensitivity in TRPM8 null mice. Neuron 54:379-386. CrossRef Medline
16. 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. CrossRef Medline
17. Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A (2007) TRPM8 is required for cold sensation in mice. Neuron 54:371-378. CrossRef Medline
18. 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. CrossRef Medline
19. Ernsberger U (2008) The role of GDNF family ligand signalling in the differentiation of sympathetic and dorsal root ganglion neurons. Cell Tissue Res 333:353-371. CrossRef Medline
20. Gaus S, Moriwaki K, Suyama H, Kawamoto M, Yuge O (2003) Capsaicin treatment inhibits osteopenia and heat hyperalgesia induced by chronic constriction injury to the sciatic nerve in rats. Hiroshima J Med Sci 52: 43-51. Medline
21. Golden JP, Hoshi M, Nassar MA, Enomoto H, Wood JN, Milbrandt J, Gereau RW 4th, Johnson EM Jr, Jain S (2010) RET signaling is required for survival and normal function of nonpeptidergic nociceptors. J Neurosci 30:3983-3994. CrossRef Medline
22. Goldstein ME, House SB, Gainer H (1991) NF-L and peripherin immunoreactivities define distinct classes of rat sensory ganglion cells. J Neurosci Res 30:92-104. CrossRef Medline
23. 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. CrossRef Medline
24. Jing S, Yu Y, Fang M, Hu Z, Holst PL, Boone T, Delaney J, Schultz H, Zhou R, Fox GM (1997) GFRalpha-2 and GFRalpha-3 are two new receptors for ligands of the GDNF family. J Biol Chem 272:33111-33117. CrossRef Medline
25. Julius D, Basbaum AI (2001) Molecular mechanisms of nociception. Nature 413:203-210. CrossRef Medline
26. Katanosaka K, Banik RK, Giron R, Higashi T, Tominaga M, Mizumura K (2008) Contribution of TRPV1 to the bradykinin-evoked nociceptive behavior and excitation of cutaneous sensory neurons. Neurosci Res 62: 168-175. CrossRef Medline
27. 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: 340-350. CrossRef Medline
28. 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:e25894. CrossRef Medline
29. Knowlton WM, Palkar R, Lippoldt EK, McCoy DD, Baluch F, Chen J, McKemy DD (2013) A sensory-labeled line for cold: TRPM8-expressing sensory neurons define the cellular basis for cold, cold pain, and coolingmediated analgesia. J Neurosci 33:2837-2848. CrossRef Medline
30. Linley JE, Rose K, Ooi L, Gamper N (2010) Understanding inflammatory pain: ion channels contributing to acute and chronic nociception. Pflugers Arch 459:657-669. CrossRef Medline
31. Linte RM, Ciobanu C, Reid G, Babes A (2007) Desensitization of coldand menthol-sensitive rat dorsal root ganglion neurones by inflammatory mediators. Exp Brain Res 178:89-98. CrossRef Medline
32. Madrid R, de la Peña E, Donovan-Rodriguez T, Belmonte C, Viana F (2009) Variable threshold of trigeminal cold-thermosensitive neurons is determined by a balance between TRPM8 and Kv1 potassium channels. J Neurosci 29:3120-3131. CrossRef Medline
33. 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. CrossRef Medline
34. McKemy DD (2013) The molecular and cellular basis of cold sensation. ACS Chem Neurosci 4:238-247. CrossRef Medline
35. 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. CrossRef Medline
36. Naveilhan P, Baudet C, Mikaels A, Shen L, Westphal H, Ernfors P (1998) Expression and regulation of GFRalpha3, a glial cell line-derived neurotrophic factor family receptor. Proc Natl Acad Sci U S A 95:1295-1300. CrossRef Medline
37. North RA (2004) P2X3 receptors and peripheral pain mechanisms. J Physiol 554:301-308. CrossRef Medline
38. 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. CrossRef Medline
39. 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. CrossRef Medline
40. Paratcha G, Ledda F (2008) GDNF and GFRalpha: a versatile molecular complex for developing neurons. Trends Neurosci 31:384-391. CrossRef Medline
41. Paratcha G, Ledda F, Ibáñez CF (2003) The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 113:867-879. CrossRef Medline
42. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A (2002) A TRP channel that senses cold stimuli and menthol. Cell 108:705-715. CrossRef Medline
43. Pezet S, McMahon SB (2006) Neurotrophins: mediators and modulators of pain. Annu Rev Neurosci 29:507-538. CrossRef Medline
44. Ramachandran R, Hyun E, Zhao L, Lapointe TK, Chapman K, Hirota CL, Ghosh S, McKemy DD, Vergnolle N, Beck PL, Altier C, Hollenberg MD (2013) TRPM8 activation attenuates inflammatory responses in mouse models of colitis. Proc Natl Acad Sci U S A 110:7476-7481. CrossRef Medline
45. Reid G, Babes A, Pluteanu F (2002) A coldand menthol-activated current in rat dorsal root ganglion neurones: properties and role in cold transduction. J Physiol 545:595-614. CrossRef Medline
46. Rosenbaum T, Gordon-Shaag A, Munari M, Gordon SE (2004) Ca2 /calmodulin modulates TRPV1 activation by capsaicin. J Gen Physiol 123: 53-62. CrossRef Medline
47. Sariola H, Saarma M (2003) Novel functions and signalling pathways for GDNF. J Cell Sci 116:3855-3862. CrossRef Medline
48. Sarria I, Ling J, Xu GY, Gu JG (2012) Sensory discrimination between innocuous and noxious cold by TRPM8-expressing DRG neurons of rats. Mol Pain 8:79. CrossRef Medline
49. 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. CrossRef Medline
50. Schmutzler BS, Roy S, Pittman SK, Meadows RM, Hingtgen CM (2011) Ret-dependent and Ret-independent mechanisms of FGL-induced sensitization. Mol Pain 7:22. CrossRef Medline
51. Silverman JD, Kruger L (1988) Lectin and neuropeptide labeling of separate populations of dorsal root ganglion neurons and associated "nociceptor" thin axons in rat testis and cornea whole-mount preparations. Somatosens Res 5:259-267. CrossRef Medline
52. Spofford CM, Brennan TJ (2012) Gene expression in skin, muscle, and dorsal root ganglion after plantar incision in the rat. Anesthesiology 117:161-172. CrossRef Medline
53. Tahmoush AJ, Schwartzman RJ, Hopp JL, Grothusen JR (2000) Quantitative sensory studies in complex regional pain syndrome type 1/RSD. Clin J Pain 16:340-344. CrossRef Medline
54. Takahashi M (2001) The GDNF/RET signaling pathway and human diseases. Cytokine Growth Factor Rev 12:361-373. CrossRef Medline
55. Takashima Y, Daniels RL, Knowlton W, Teng J, Liman ER, McKemy DD (2007) Diversity in the neural circuitry of cold sensing revealed by genetic axonal labeling of transient receptor potential melastatin 8 neurons. J Neurosci 27:14147-14157. CrossRef Medline
56. Takashima Y, Ma L, McKemy DD (2010) The development of peripheral cold neural circuits based on TRPM8 expression. Neuroscience 169:828-842. CrossRef Medline
57. Vinik AI (2004) Advances in diabetes for the millennium: new treatments for diabetic neuropathies. MedGenMed 6:13. Medline
58. Vulchanova L, Riedl MS, Shuster SJ, Stone LS, Hargreaves KM, Buell G, Surprenant A, North RA, Elde R (1998) P2X3 is expressed by DRG neurons that terminate in inner lamina II. Eur J Neurosci 10:3470-3478. CrossRef Medline
59. Wang H, Kohno T, Amaya F, Brenner GJ, Ito N, Allchorne A, Ji RR, Woolf CJ (2005) Bradykinin produces pain hypersensitivity by potentiating spinal cord glutamatergic synaptic transmission. J Neurosci 25:7986-7992. CrossRef Medline
60. Wang T, Molliver DC, Jing X, Schwartz ES, Yang FC, Samad OA, Ma Q, Davis BM (2011) Phenotypic switching of nonpeptidergic cutaneous sensory neurons following peripheral nerve injury. PLoS One 6:e28908. CrossRef Medline
61. Wang T, Jing X, DeBerry JJ, Schwartz ES, Molliver DC, Albers KM, Davis BM (2013) Neurturin overexpression in skin enhances expression of TRPM8 in cutaneous sensory neurons and leads to behavioral sensitivity to cool and menthol. J Neurosci 33:2060-2070. CrossRef Medline
62. Woolf CJ (2007) Central sensitization: uncovering the relation between pain and plasticity. Anesthesiology 106:864-867. CrossRef Medline
63. 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. CrossRef Medline
64. Xing H, Ling J, Chen M, Gu JG (2006) Chemical and cold sensitivity of two distinct populations of TRPM8-expressing somatosensory neurons. J Neurophysiol 95:1221-1230. CrossRef Medline
65. Yoshida N, Kobayashi K, Yu L, Wang S, Na R, Yamamoto S, Noguchi K, Dai Y (2011) Inhibition of TRPA1 channel activity in sensory neurons by the glial cell line-derived neurotrophic factor family member, artemin. Mol Pain 7:41. CrossRef Medline
66. Zhang X, Huang J, McNaughton PA (2005) NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J 24:4211-4223. CrossRef Medline
67. Zhang X, Mak S, Li L, Parra A, Denlinger B, Belmonte C, McNaughton PA (2012) Direct inhibition of the cold-activated TRPM8 ion channel by G q. Nat Cell Biol 14:851-858. CrossRef Medline
68. Zhuang ZY, Xu H, Clapham DE, Ji RR (2004) Phosphatidylinositol 3-kinase activates ERK in primary sensory neurons and mediates inflammatory heat hyperalgesia through TRPV1 sensitization. J Neurosci 24:8300-8309. CrossRef Medline
69. Zimmermann K, Leffler A, Babes A, Cendan CM, Carr RW, Kobayashi J, Nau C, Wood JN, Reeh PW (2007) Sensory neuron sodium channel Nav1.8 is essential for pain at low temperatures. Nature 447:855-858. CrossRef Medline