Phenotyping the function of TRPV1-expressing sensory neurons by targeted axonal silencing

Journal of Neuroscience

Volumn 33, Issue 1, 2013, Pages 315-326

  Brenneis, Christian ^a,b   Kistner, Katrin ^c   Puopolo, Michelino ^d,e   Segal, David ^a   Roberson, David ^a   Sisignano, Marco ^b   Labocha, Sandra ^b   Ferreirós, Nerea ^b   Strominger, Amanda ^a   Cobos, Enrique J ^a,f   Ghasemlou, Nader ^a   Geisslinger, Gerd ^b   Reeh, Peter W ^c   Bean, Bruce P ^d   Woolf, Clifford J ^a,d  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d HARVARD MEDICAL SCHOOL   (United States)

^e Stony Brook Medicine   (United States)

^f UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSAICIN; LIDOCAINE ETHOBROMIDE; VANILLOID RECEPTOR 1;

ACTION POTENTIAL; ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ELECTROSPRAY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; MALE; MOUSE; NERVE FIBER; NONHUMAN; PERIPHERAL NERVE INJURY; PHENOTYPE; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; TANDEM MASS SPECTROMETRY;

ACTION POTENTIALS; ANESTHETICS, LOCAL; ANIMALS; AXONS; BEHAVIOR, ANIMAL; CAPSAICIN; CHRONIC PAIN; DISEASE MODELS, ANIMAL; LIDOCAINE; MALE; PAIN MEASUREMENT; PAIN THRESHOLD; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE; SENSORY RECEPTOR CELLS; TRPV CATION CHANNELS;

EID: 84871820171     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2804-12.2013     Document Type: Article

References (48)

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. Agarwal N, Pacher P, Tegeder I, Amaya F, Constantin CE, Brenner GJ, Rubino T, Michalski CW, Marsicano G, Monory K, Mackie K, Marian C, Batkai S, Parolaro D, Fischer MJ, Reeh P, Kunos G, Kress M, Lutz B, Woolf CJ, et al. (2007) Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nat Neurosci 10: 870-879. CrossRef Medline
3. Allchorne AJ, Broom DC, Woolf CJ (2005) Detection of cold pain, cold allodynia and cold hyperalgesia in freely behaving rats. Mol Pain 1:36. CrossRef Medline
4. Banke TG, Chaplan SR, Wickenden AD (2010) Dynamic changes in the TRPA1 selectivity filter lead to progressive but reversible pore dilation. Am J Physiol Cell Physiol 298:C1457-C1468. Medline
5. 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
6. Binshtok AM, Bean BP, Woolf CJ (2007) Inhibition of nociceptors by TRPV1-mediated entry of impermeant sodium channel blockers. Nature 449:607-610. CrossRef Medline
7. Binshtok AM, Gerner P, Oh SB, Puopolo M, Suzuki S, Roberson DP, Herbert T, Wang CF, Kim D, Chung G, Mitani AA, Wang GK, Bean BP, Woolf CJ (2009) Coapplication of lidocaine and the permanently charged sodium channel blocker QX-314 produces a long-lasting nociceptive blockade in rodents. Anesthesiology 111:127-137. CrossRef Medline
8. Bráz JM, Basbaum AI (2009) Triggering genetically-expressed transneuronal tracers by peripheral axotomy reveals convergent and segregated sensory neuron-spinal cord connectivity. Neuroscience 163:1220-1232. CrossRef Medline
9. Bremer M, Fröb F, Kichko T, Reeh P, Tamm ER, Suter U, Wegner M (2011) Sox10 is required for Schwann-cell homeostasis and myelin maintenance in the adult peripheral nerve. Glia 59:1022-1032. CrossRef Medline
10. Bretag AH (1969) Synthetic interstitial fluid for isolated mammalian tissue. Life Sci 8:319-329. CrossRef Medline
11. 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. 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. Chen J, Kim D, Bianchi BR, Cavanaugh EJ, Faltynek CR, Kym PR, Reilly RM (2009) Pore dilation occurs in TRPA1 but not in TRPM8 channels. Mol Pain 5:3. CrossRef Medline
14. Clapham DE (2007) SnapShot: mammalian TRP channels. Cell 129:220. Medline
15. 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
16. Decosterd I, Woolf CJ (2000) Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87:149-158. CrossRef Medline
17. del Camino D, Murphy S, Heiry M, Barrett LB, Earley TJ, Cook CA, Petrus MJ, Zhao M, D'Amours M, Deering N, Brenner GJ, Costigan M, Hayward NJ, Chong JA, Fanger CM, Woolf CJ, Patapoutian A, Moran MM (2010) TRPA1 contributes to cold hypersensitivity. J Neurosci 30:15165-15174. Medline
18. Handwerker HO (2008) What is a polymodal nociceptor? J Pain 9:309-310. CrossRef Medline
19. Hargreaves K, Dubner R, Brown F, Flores C, Joris J (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88. CrossRef Medline
20. Hille B (1977) Local anesthetics: hydrophilic and hydrophobic pathways for the drug-receptor reaction. J Gen Physiol 69:497-515. CrossRef Medline
21. Jasmin L, Kohan L, Franssen M, Janni G, Goff JR (1998) The cold plate as a test of nociceptive behaviors: description and application to the study of chronic neuropathic and inflammatory pain models. Pain 75:367-382. CrossRef Medline
22. Ji RR, Befort K, Brenner GJ, Woolf CJ (2002) ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity. J Neurosci 22:478-485. Medline
23. Kistner K, Zimmermann K, Ehnert C, Reeh PW, Leffler A (2010) The tetrodotoxin-resistant Na+ channel Na (v)1.8 reduces the potency of local anesthetics in blocking C-fiber nociceptors. Pflugers Arch 459:751-763. CrossRef Medline
24. Koerber HR, McIlwrath SL, Lawson JJ, Malin SA, Anderson CE, Jankowski MP, Davis BM (2010) Cutaneous C-polymodal fibers lacking TRPV1 are sensitized to heat following inflammation, but fail to drive heat hyperalgesia in the absence of TPV1 containing C-heat fibers. Mol Pain 6:58. CrossRef Medline
25. 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. CrossRef Medline
26. Latremoliere A, Woolf CJ (2009) Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 10:895-926. CrossRef Medline
27. Lawson JJ, McIlwrath SL, Woodbury CJ, Davis BM, Koerber HR (2008) TRPV1 unlike TRPV2 is restricted to a subset of mechanically insensitive cutaneous nociceptors responding to heat. J Pain 9:298-308. CrossRef Medline
28. Leffler A, Lattrell A, Kronewald S, Niedermirtl F, Nau C (2011) Activation of TRPA1 by membrane permeable local anesthetics. Mol Pain 7:62. CrossRef Medline
29. Luis-Delgado OE, Barrot M, Rodeau JL, Schott G, Benbouzid M, Poisbeau P, Freund-Mercier MJ, Lasbennes F (2006) Calibrated forceps: a sensitive and reliable tool for pain and analgesia studies. J Pain 7:32-39. CrossRef Medline
30. Matsumoto M, Xie W, Ma L, Ueda H (2008) Pharmacological switch in Abeta-fiber stimulation-induced spinal transmission in mice with partial sciatic nerve injury. Mol Pain 4:25. CrossRef Medline
31. Mishra SK, Hoon MA (2010) Ablation of TrpV1 neurons reveals their selective role in thermal pain sensation. Mol Cell Neurosci 43:157-163. CrossRef Medline
32. Mishra SK, Tisel SM, Orestes P, Bhangoo SK, Hoon MA (2011) TRPV1-lineage neurons are required for thermal sensation. EMBO J 30:582-593. CrossRef Medline
33. Perl ER (1996) Cutaneous polymodal receptors: characteristics and plasticity. Prog Brain Res 113:21-37. CrossRef Medline
34. Petsche U, Fleischer E, Lembeck F, Handwerker HO (1983) The effect of capsaicin application to a peripheral nerve on impulse conduction in functionally identified afferent nerve fibres. Brain Res 265:233-240. CrossRef Medline
35. Price TJ, Flores CM (2007) Critical evaluation of the colocalization between calcitonin gene-related peptide, substance P, transient receptor potential vanilloid subfamily type 1 immunoreactivities, and isolectin B4 binding in primary afferent neurons of the rat and mouse. J Pain 8:263-272. CrossRef Medline
36. Ragsdale DS, McPhee JC, Scheuer T, Catterall WA (1994) Molecular determinants of state-dependent block of Na+ channels by local anesthetics. Science 265:1724-1728. CrossRef Medline
37. Roberson DP, Binshtok AN, Blasl F, Bean BP, Woolf CJ (2011) Targeting of sodium channel blockers into nociceptors to produce long-duration analgesia: a systematic study and review. Br J Pharmacol 164:48-58. CrossRef Medline
38. Sándor Z, Varga A, Horváth P, Nagy B, Szolcsányi J (2005) Construction of a stable cell line uniformly expressing the rat TRPV1 receptor. Cell Mol Biol Lett 10:499-514. Medline
39. Scherrer G, Imamachi N, Cao YQ, Contet C, Mennicken F, O'Donnell D, Kieffer BL, Basbaum AI (2009) Dissociation of the opioid receptor mechanisms that control mechanical and heat pain. Cell 137:1148-1159. CrossRef Medline
40. Schmelz M (2011) Neuronal sensitivity of the skin. Eur J Dermatol 21 [Suppl 2]:43-47. Medline
41. Seal RP, Wang X, Guan Y, Raja SN, Woodbury CJ, Basbaum AI, Edwards RH (2009) Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors. Nature 462:651-655. CrossRef Medline
42. St Pierre M, Reeh PW, Zimmermann K (2009) Differential effects of TRPV channel block on polymodal activation of rat cutaneous nociceptors in vitro. Exp Brain Res 196:31-44. CrossRef Medline
43. Szolcsanyi J, Anton F, Reeh PW, Handwerker HO (1988) Selective excitation by capsaicin of mechano-heat sensitive nociceptors in rat skin. Brain Res 446:262-268. CrossRef Medline
44. Wang H, Woolf CJ (2005) Pain TRPs. Neuron 46:9-12. CrossRef Medline
45. 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. CrossRef Medline
46. Woolf CJ, Ma Q (2007) Nociceptors-noxious stimulus detectors. Neuron 55:353-364. CrossRef Medline
47. Xie W, Matsumoto M, Chun J, Ueda H (2008) Involvement of LPA1 receptor signaling in the reorganization of spinal input through Abeta-fibers in mice with partial sciatic nerve injury. Mol Pain 4:46. CrossRef Medline
48. Zimmermann K, Leffler A, Fischer MM, Messlinger K, Nau C, Reeh PW (2005) The TRPV1/2/3 activator 2-aminoethoxydiphenyl borate sensitizes native nociceptive neurons to heat in wild-type but not TRPV1 deficient mice. Neuroscience 135:1277-1284. CrossRef Medline