Extracellular microRNAs Activate nociceptor neurons to elicit pain via TLR7 and TRPA1

Neuron

Volumn 82, Issue 1, 2014, Pages 47-54

  Park, Chul Kyu ^a   Xu, Zhen Zhong ^a   Berta, Temugin ^a   Han, Qingjian ^a   Chen, Gang ^a   Liu, Xing Jun ^a   Ji, Ru Rong ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA LETHAL 7B; TOLL LIKE RECEPTOR 7; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL ACTIVITY; CELL STRAIN HEK293; CONTROLLED STUDY; INTRACELLULAR SIGNALING; MALE; MOLECULAR PATHOLOGY; MOUSE; NERVE CELL EXCITABILITY; NERVE POTENTIAL; NONHUMAN; PAIN; PAIN RECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN RNA BINDING; SPINAL GANGLION;

ANIMALS; DISEASE MODELS, ANIMAL; FORMALDEHYDE; GANGLIA, SPINAL; HEK293 CELLS; HUMANS; MEMBRANE GLYCOPROTEINS; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; MYELOID DIFFERENTIATION FACTOR 88; NOCICEPTORS; PAIN; PAIN MANAGEMENT; PATCH-CLAMP TECHNIQUES; TOLL-LIKE RECEPTOR 7; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TRPV CATION CHANNELS;

EID: 84897467553     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.02.011     Document Type: Article

References (29)

1. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
2. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
3. Basbaum A.I., Bautista D.M., Scherrer G., Julius D. Cellular and molecular mechanisms of pain. Cell 2009, 139:267-284.
4. Bautista D.M., Jordt S.E., Nikai T., Tsuruda P.R., Read A.J., Poblete J., Yamoah E.N., Basbaum A.I., Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 2006, 124:1269-1282.
5. Caterina M.J., Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu. Rev. Neurosci. 2001, 24:487-517.
6. Eacker S.M., Dawson T.M., Dawson V.L. Understanding microRNAs in neurodegeneration. Nat. Rev. Neurosci. 2009, 10:837-841.
7. Fabbri M., Paone A., Calore F., Galli R., Gaudio E., Santhanam R., Lovat F., Fadda P., Mao C., Nuovo G.J., et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc. Natl. Acad. Sci. USA 2012, 109:E2110-E2116.
8. Heil F., Hemmi H., Hochrein H., Ampenberger F., Kirschning C., Akira S., Lipford G., Wagner H., Bauer S. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004, 303:1526-1529.
9. Hucho T., Levine J.D. Signaling pathways in sensitization: toward a nociceptor cell biology. Neuron 2007, 55:365-376.
10. Jordt S.E., Bautista D.M., Chuang H.H., McKemy D.D., Zygmunt P.M., Högestätt E.D., Meng I.D., Julius D. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 2004, 427:260-265.
11. Kang K., Pulver S.R., Panzano V.C., Chang E.C., Griffith L.C., Theobald D.L., Garrity P.A. Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. Nature 2010, 464:597-600.
12. Lehmann S.M., Krüger C., Park B., Derkow K., Rosenberger K., Baumgart J., Trimbuch T., Eom G., Hinz M., Kaul D., et al. An unconventional role for miRNA: let-7 activates Toll-like receptor 7 and causes neurodegeneration. Nat. Neurosci. 2012, 15:827-835.
13. Liu T., Ji R.R. New insights into the mechanisms of itch: are pain and itch controlled by distinct mechanisms?. Pflugers Arch. 2013, 465:1671-1685.
14. Liu T., Xu Z.Z., Park C.K., Berta T., Ji R.R. Toll-like receptor 7 mediates pruritus. Nat. Neurosci. 2010, 13:1460-1462.
15. Liu T., Berta T., Xu Z.Z., Park C.K., Zhang L., Lü N., Liu Q., Liu Y., Gao Y.J., Liu Y.C., et al. TLR3 deficiency impairs spinal cord synaptic transmission, central sensitization, and pruritus in mice. J. Clin. Invest. 2012, 122:2195-2207.
16. Liu T., Gao Y.J., Ji R.R. Emerging role of Toll-like receptors in the control of pain and itch. Neurosci. Bull. 2012, 28:131-144.
17. Macpherson L.J., Dubin A.E., Evans M.J., Marr F., Schultz P.G., Cravatt B.F., Patapoutian A. Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 2007, 445:541-545.
18. McNamara C.R., Mandel-Brehm J., Bautista D.M., Siemens J., Deranian K.L., Zhao M., Hayward N.J., Chong J.A., Julius D., Moran M.M., Fanger C.M. TRPA1 mediates formalin-induced pain. Proc. Natl. Acad. Sci. USA 2007, 104:13525-13530.
19. Orlova I.A., Alexander G.M., Qureshi R.A., Sacan A., Graziano A., Barrett J.E., Schwartzman R.J., Ajit S.K. MicroRNA modulation in complex regional pain syndrome. J. Transl. Med. 2011, 9:195.
20. Pasquinelli A.E., Reinhart B.J., Slack F., Martindale M.Q., Kuroda M.I., Maller B., Hayward D.C., Ball E.E., Degnan B., Müller P., et al. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000, 408:86-89.
21. Patapoutian A., Tate S., Woolf C.J. Transient receptor potential channels: targeting pain at the source. Nat. Rev. Drug Discov. 2009, 8:55-68.
22. Qin N., Neeper M.P., Liu Y., Hutchinson T.L., Lubin M.L., Flores C.M. TRPV2 is activated by cannabidiol and mediates CGRP release in cultured rat dorsal root ganglion neurons. J. Neurosci. 2008, 28:6231-6238.
23. Reinhart B.J., Slack F.J., Basson M., Pasquinelli A.E., Bettinger J.C., Rougvie A.E., Horvitz H.R., Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403:901-906.
24. Schmidt M., Dubin A.E., Petrus M.J., Earley T.J., Patapoutian A. Nociceptive signals induce trafficking of TRPA1 to the plasma membrane. Neuron 2009, 64:498-509.
25. Story G.M., Peier A.M., Reeve A.J., Eid S.R., Mosbacher J., Hricik T.R., Earley T.J., Hergarden A.C., Andersson D.A., Hwang S.W., et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 2003, 112:819-829.
26. Takeuchi O., Akira S. Pattern recognition receptors and inflammation. Cell 2010, 140:805-820.
27. von Schack D., Agostino M.J., Murray B.S., Li Y., Reddy P.S., Chen J., Choe S.E., Strassle B.W., Li C., Bates B., et al. Dynamic changes in the microRNA expression profile reveal multiple regulatory mechanisms in the spinal nerve ligation model of neuropathic pain. PLoS ONE 2011, 6:e17670.
28. Woolf C.J., Ma Q. Nociceptors-noxious stimulus detectors. Neuron 2007, 55:353-364.
29. Zhao J., Lee M.C., Momin A., Cendan C.M., Shepherd S.T., Baker M.D., Asante C., Bee L., Bethry A., Perkins J.R., et al. Small RNAs control sodium channel expression, nociceptor excitability, and pain thresholds. J. Neurosci. 2010, 30:10860-10871.