Activity-dependent silencing reveals functionally distinct itch-generating sensory neurons

Nature Neuroscience

Volumn 16, Issue 7, 2013, Pages 910-918

  Roberson, David P ^a,b   Gudes, Sagi ^c,d   Sprague, Jared M ^a,e   Patoski, Haley A W ^a   Robson, Victoria K ^a   Blasl, Felix ^c   Duan, Bo ^b,f   Oh, Seog Bae ^a,g   Bean, Bruce P ^b   Ma, Qiufu ^b,f   Binshtok, Alexander M ^c,d   Woolf, Clifford J ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^e HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^f DANA FARBER CANCER INSTITUTE   (United States)

^g Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALLYL ISOTHIOCYANATE; CAPSAICIN; CHLOROQUINE; HISTAMINE; LIDOCAINE ETHOBROMIDE; SODIUM CHANNEL BLOCKING AGENT; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; VANILLOID RECEPTOR 1; ANTIPRURITIC AGENT; ANTIRHEUMATIC AGENT; HISTAMINE AGONIST; LOCAL ANESTHETIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; MECHANICAL STIMULATION; MOUSE; NERVE BLOCK; NERVE FIBER; NONHUMAN; PAIN; PAIN RECEPTOR; PERIPHERAL NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PRURITUS; SCRATCHING; SENSATION; SENSORY NERVE CELL; SODIUM CURRENT; SPINAL GANGLION; THERMAL STIMULATION; TRIGEMINAL NERVE; TRIGEMINUS GANGLION; ACTION POTENTIAL; ANIMAL; ANIMAL BEHAVIOR; CELL CULTURE; CHEMICALLY INDUCED DISORDER; CLASSIFICATION; CYTOLOGY; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECT; DRUG INTERACTION; MALE; PATHOLOGY; PHYSIOLOGY; SENSORY RECEPTOR; TIME; CHEMICALLY INDUCED; DRUG EFFECTS; TOXICITY;

ACTION POTENTIALS; ANESTHETICS, LOCAL; ANIMALS; ANTIPRURITICS; ANTIRHEUMATIC AGENTS; BEHAVIOR, ANIMAL; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; GANGLIA, SPINAL; HISTAMINE; HISTAMINE AGONISTS; MALE; MICE; PAIN; PRURITUS; SENSORY RECEPTOR CELLS; SODIUM CHANNEL BLOCKERS; TIME FACTORS; TRIGEMINAL GANGLION;

EID: 84879651573     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3404     Document Type: Article

References (43)

1. Grundmann, S. & Stander, S. Chronic pruritus: clinics and treatment. Ann. Dermatol. 23, 1-11 (2011).
2. Yosipovitch, G. & Papoiu, A.D. What causes itch in atopic dermatitis? Curr. Allergy Asthma Rep. 8, 306-311 (2008).
3. Lee, M.G. et al. Agonists of the MAS-related gene (Mrgs) orphan receptors as novel mediators of mast cell-sensory nerve interactions. J. Immunol. 180, 2251-2255 (2008).
4. Akiyama, T., Carstens, M.I. & Carstens, E. Enhanced scratching evoked by PAR-2 agonist and 5-HT but not histamine in a mouse model of chronic dry skin itch. Pain 151, 378-383 (2010).
5. Papoiu, A.D., Tey, H.L., Coghill, R.C., Wang, H. & Yosipovitch, G. Cowhage-induced itch as an experimental model for pruritus. A comparative study with histamine-induced itch. PLoS ONE 6, e17786 (2011).
6. Liu, Q. et al. Sensory neuron-specific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell 139, 1353-1365 (2009).
7. Akiyama, T., Carstens, M.I. & Carstens, E. Facial injections of pruritogens and algogens excite partly overlapping populations of primary and second-order trigeminal neurons in mice. J. Neurophysiol. 104, 2442-2450 (2010).
8. Patel, K.N. & Dong, X. Itch: cells, molecules and circuits. ACS Chem. Neurosci. 2, 17-25 (2011).
9. Liu, Q. et al. The distinct roles of two GPCRs, MrgprC11 and PAR2, in ich and hyperalgesia. Sci. Signal. 4, 45 (2011).
10. Han, S.-K., Mancino, V. & Simon, M.I. Phospholipase Cbeta 3 mediates the scratching response activated by the histamine H1 receptor on C-fiber nociceptive neurons. Neuron 52, 691-703 (2006).
11. Imamachi, N. et al. TRPV1-expressing primary afferents generate behavioral responses to pruritogens via multiple mechanisms. Proc. Natl. Acad. Sci. USA 106, 11330-11335 (2009).
12. Wilson, S.R. et al. TRPA1 is required for histamine-independent, Mas-related G protein-coupled receptor-mediated itch. Nat. Neurosci. 14, 595-602 (2011).
13. Akiyama, T., Carstens, M.I. & Carstens, E. Enhanced responses of lumbar superficial dorsal horn neurons to intradermal PAR-2 agonist but not histamine in a mouse hindpaw dry skin itch model. J. Neurophysiol. 105, 2811-2817 (2011).
14. Shim, W.-S. et al. TRPV1 mediates histamine-induced itching via the activation of phospholipase A2 and 12-lipoxygenase. J. Neurosci. 27, 2331-2337 (2007).
15. Han, L. et al. A subpopulation of nociceptors specifically linked to itch. Nat. Neurosci. 16, 174-182 (2013).
16. Namer, B. et al. Separate peripheral pathways for pruritus in man. J. Neurophysiol. 100, 2062-2069 (2008).
17. Liu, Q. et al. Mechanisms of itch evoked by beta-alanine. J. Neurosci. 32, 14532-14537 (2012).
18. Akiyama, T. et al. Cross-sensitization of histamine-independent itch in mouse primary sensory neurons. Neuroscience 226, 305-312 (2012).
19. Binshtok, A.M., Bean, B.P. & Woolf, C.J. Inhibition of nociceptors by TRPV1-mediated entry of impermeant sodium channel blockers. Nature 449, 607-610 (2007).
20. Brenneis, C. et al. Phenotyping the function of TRPV1-expressing sensory neurons by targeted axonal silencing. J. Neurosci. 33, 315-326 (2013).
21. Kim, H.Y. et al. Selectively targeting pain in the trigeminal system. Pain 150, 29-40 (2010).
22. Puopolo, M. et al. Permeation and block of TRPV1 channels by the cationic lidocaine derivative QX-314. J. Neurophysiol. 109, 1704-1723 (2013).
23. Binshtok, A.M. et al. Coapplication of lidocaine and the permanently charged sodium channel blocker QX-314 produces a long-lasting nociceptive blockade in rodents. Anesthesiology 111, 127-137 (2009).
24. Roberson, D.P., Binshtok, A.M., Blasl, F., Bean, B.P. & Woolf, C.J. Targeting of sodium channel blockers into nociceptors to produce long-duration analgesia: a systematic study and review. Br. J. Pharmacol. 164, 48-58 (2011).
25. Chen, J. et al. Pore dilation occurs in TRPA1 but not in TRPM8 channels. Mol. Pain 5, 3 (2009).
26. Shimada, S.G. & LaMotte, R.H. Behavioral differentiation between itch and pain in mouse. Pain 139, 681-687 (2008).
27. Brenner, D.S., Golden, J.P. & Gereau, R.W. A novel behavioral assay for measuring cold sensation in mice. PLoS ONE 7, e39765 (2012).
28. Ogle, M.E., Gu, X., Espinera, A.R. & Wei, L. Inhibition of prolyl hydroxylases by dimethyloxaloylglycine after stroke reduces ischemic brain injury and requires hypoxia inducible factor-1alpha. Neurobiol. Dis. 45, 733-742 (2012).
29. Petersen, L.J. Quantitative measurement of extracellular histamine concentrations in intact human skin in vivo by the microdialysis technique: methodological aspects. Allergy 52, 547-555 (1997).
30. Khalil, I.F. et al. Development of ELISA-based methods to measure the anti-malarial drug chloroquine in plasma and in pharmaceutical formulations. Malar. J. 10, 249 (2011).
31. Akiyama, T., Carstens, M.I. & Carstens, E. Differential itch- and pain-related behavioral responses and micro-opoid modulation in mice. Acta Derm. Venereol. 90, 575-581 (2010).
32. Ross, S.E. et al. Loss of inhibitory interneurons in the dorsal spinal cord and elevated itch in Bhlhb5 mutant mice. Neuron 65, 886-898 (2010).
33. Ohsawa, Y. & Hirasawa, N. The antagonism of histamine H1 and H4 receptors ameliorates chronic allergic dermatitis via anti-pruritic and anti-inflammatory effects in NC/Nga mice. Allergy 67, 1014-1022 (2012).
34. Liu, T. & Ji, R.R. Oxidative stress induces itch via activation of transient receptor potential subtype ankyrin 1 in mice. Neurosci. Bull. 28, 145-154 (2012).
35. Sun, Y.-G. et al. Cellular basis of itch sensation. Science 325, 1531-1534 (2009).
36. Schmelz, M. et al. Chemical response pattern of different classes of C-nociceptors to pruritogens and algogens. J. Neurophysiol. 89, 2441-2448 (2003).
37. Namer, B. & Reeh, P. Scratching an itch. Nat. Neurosci. 16, 117-118 (2013).
38. Sun, Y.G. & Chen, Z.F. A gastrin-releasing peptide receptor mediates the itch sensation in the spinal cord. Nature 448, 700-703 (2007).
39. Rudick, C.N., Bryce, P.J., Guichelaar, L.A., Berry, R.E. & Klumpp, D.J. Mast cell-derived histamine mediates cystitis pain. PLoS ONE 3, e2096 (2008).
40. Sikand, P., Shimada, S.G., Green, B.G. & LaMotte, R.H. Similar itch and nociceptive sensations evoked by punctate cutaneous application of capsaicin, histamine and cowhage. Pain 144, 66-75 (2009).
41. Koppert, W., Reeh, P.W. & Handwerker, H.O. Conditioning of histamine by bradykinin alters responses of rat nociceptor and human itch sensation. Neurosci. Lett. 152, 117-120 (1993).
42. Liu, Y. et al. VGLUT2-dependent glutamate release from nociceptors is required to sense pain and suppress itch. Neuron 68, 543-556 (2010).
43. Leffler, A. et al. The vanilloid receptor TRPV1 is activated and sensitized by local anesthetics in rodent sensory neurons. J. Clin. Invest. 118, 763-776 (2008).