Dorsal Horn Circuits for Persistent Mechanical Pain

Neuron

Volumn 87, Issue 4, 2015, Pages 797-812

  Peirs, Cedric ^a   Williams, Sean Paul G ^a   Zhao, Xinyi ^a,b   Walsh, Claire E ^a   Gedeon, Jeremy Y ^a   Cagle, Natalie E ^a   Goldring, Adam C ^a   Hioki, Hiroyuki ^c   Liu, Zheng ^a   Marell, Paulina S ^a   Seal, Rebecca P ^a  

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

^b University of Pittsburgh School of Medicine ^*  (China)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALRETININ; PROTEIN C FOS; VESICULAR GLUTAMATE TRANSPORTER 3; AMINO ACID TRANSPORTER; VESICULAR GLUTAMATE TRANSPORTER 3, MOUSE;

ADULT; ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONNECTOME; CONTROLLED STUDY; INFLAMMATORY PAIN; INTERNEURON; MECHANICAL ALLODYNIA; MOUSE; NERVE INJURY; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL LAMINA II; SPINAL LAMINA III; SYNAPTIC TRANSMISSION; TOUCH; ANIMAL; BIOSYNTHESIS; HYPERALGESIA; KNOCKOUT MOUSE; METABOLISM; NERVE CELL NETWORK; ORGAN CULTURE TECHNIQUE; PAIN; PATHOLOGY;

AMINO ACID TRANSPORT SYSTEMS, ACIDIC; ANIMALS; HYPERALGESIA; MICE; MICE, KNOCKOUT; NERVE NET; ORGAN CULTURE TECHNIQUES; PAIN; SPINAL CORD DORSAL HORN; TOUCH;

EID: 84951574876     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.07.029     Document Type: Article

References (50)

1. Agarwal N., Offermanns S., Kuner R. Conditional gene deletion in primary nociceptive neurons of trigeminal ganglia and dorsal root ganglia. Genesis 2004, 38:122-129.
2. Baba H., Doubell T.P., Moore K.A., Woolf C.J. Silent NMDA receptor-mediated synapses are developmentally regulated in the dorsal horn of the rat spinal cord. J. Neurophysiol. 2000, 83:955-962.
3. Baba H., Ji R.R., Kohno T., Moore K.A., Ataka T., Wakai A., Okamoto M., Woolf C.J. Removal of GABAergic inhibition facilitates polysynaptic A fiber-mediated excitatory transmission to the superficial spinal dorsal horn. Mol. Cell. Neurosci. 2003, 24:818-830.
4. Braz J.M., Rico B., Basbaum A.I. Transneuronal tracing of diverse CNS circuits by Cre-mediated induction of wheat germ agglutinin in transgenic mice. Proc. Natl. Acad. Sci. USA 2002, 99:15148-15153.
5. Braz J., Solorzano C., Wang X., Basbaum A.I. Transmitting pain and itch messages: a contemporary view of the spinal cord circuits that generate gate control. Neuron 2014, 82:522-536.
6. Craig A.D. Pain mechanisms: labeled lines versus convergence in central processing. Annu. Rev. Neurosci. 2003, 26:1-30.
7. Delfini M.C., Mantilleri A., Gaillard S., Hao J., Reynders A., Malapert P., Alonso S., François A., Barrere C., Seal R., et al. TAFA4, a chemokine-like protein, modulates injury-induced mechanical and chemical pain hypersensitivity in mice. Cell Rep. 2013, 5:378-388.
8. Duan B., Cheng L., Bourane S., Britz O., Padilla C., Garcia-Campmany L., Krashes M., Knowlton W., Velasquez T., Ren X., et al. Identification of spinal circuits transmitting and gating mechanical pain. Cell 2014, 159:1417-1432.
9. Fitzgerald M. The development of nociceptive circuits. Nat. Rev. Neurosci. 2005, 6:507-520.
10. Gao Y.J., Ji R.R. Light touch induces ERK activation in superficial dorsal horn neurons after inflammation: involvement of spinal astrocytes and JNK signaling in touch-evoked central sensitization and mechanical allodynia. J. Neurochem. 2010, 115:505-514.
11. Grimes W.N., Seal R.P., Oesch N., Edwards R.H., Diamond J.S. Genetic targeting and physiological features of VGLUT3+ amacrine cells. Vis. Neurosci. 2011, 28:381-392.
12. Hafner M., Wenk J., Nenci A., Pasparakis M., Scharffetter-Kochanek K., Smyth N., Peters T., Kess D., Holtkötter O., Shephard P., et al. Keratin 14 Cre transgenic mice authenticate keratin 14 as an oocyte-expressed protein. Genesis 2004, 38:176-181.
13. Hasegawa H., Abbott S., Han B.X., Qi Y., Wang F. Analyzing somatosensory axon projections with the sensory neuron-specific Advillin gene. J. Neurosci. 2007, 27:14404-14414.
14. Kato G., Kawasaki Y., Koga K., Uta D., Kosugi M., Yasaka T., Yoshimura M., Ji R.R., Strassman A.M. Organization of intralaminar and translaminar neuronal connectivity in the superficial spinal dorsal horn. J. Neurosci. 2009, 29:5088-5099.
15. Kuner R. Central mechanisms of pathological pain. Nat. Med. 2010, 16:1258-1266.
16. Li P., Zhuo M. Silent glutamatergic synapses and nociception in mammalian spinal cord. Nature 1998, 393:695-698.
17. Li L., Rutlin M., Abraira V.E., Cassidy C., Kus L., Gong S., Jankowski M.P., Luo W., Heintz N., Koerber H.R., et al. The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 2011, 147:1615-1627.
18. Liljencrantz J., Björnsdotter M., Morrison I., Bergstrand S., Ceko M., Seminowicz D.A., Cole J., Bushnell M.C., Olausson H. Altered C-tactile processing in human dynamic tactile allodynia. Pain 2013, 154:227-234.
19. Löken L.S., Wessberg J., Morrison I., McGlone F., Olausson H. Coding of pleasant touch by unmyelinated afferents in humans. Nat. Neurosci. 2009, 12:547-548.
20. Lou S., Duan B., Vong L., Lowell B.B., Ma Q. Runx1 controls terminal morphology and mechanosensitivity of VGLUT3-expressing C-mechanoreceptors. J. Neurosci. 2013, 33:870-882.
21. Lu Y., Perl E.R. Modular organization of excitatory circuits between neurons of the spinal superficial dorsal horn (laminae I and II). J. Neurosci. 2005, 25:3900-3907.
22. Lu Y., Dong H., Gao Y., Gong Y., Ren Y., Gu N., Zhou S., Xia N., Sun Y.Y., Ji R.R., Xiong L. A feed-forward spinal cord glycinergic neural circuit gates mechanical allodynia. J. Clin. Invest. 2013, 123:4050-4062.
23. Madisen L., Zwingman T.A., Sunkin S.M., Oh S.W., Zariwala H.A., Gu H., Ng L.L., Palmiter R.D., Hawrylycz M.J., Jones A.R., et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 2010, 13:133-140.
24. Malmberg A.B., Chen C., Tonegawa S., Basbaum A.I. Preserved acute pain and reduced neuropathic pain in mice lacking PKCgamma. Science 1997, 278:279-283.
25. Melzack R., Wall P.D. Pain mechanisms: a new theory. Science 1965, 150:971-979.
26. Miraucourt L.S., Dallel R., Voisin D.L. Glycine inhibitory dysfunction turns touch into pain through PKCgamma interneurons. PLoS ONE 2007, 2:e1116.
27. Nagi S.S., Rubin T.K., Chelvanayagam D.K., Macefield V.G., Mahns D.A. Allodynia mediated by C-tactile afferents in human hairy skin. J. Physiol. 2011, 589:4065-4075.
28. Peirs C., Patil S., Bouali-Benazzouz R., Artola A., Landry M., Dallel R. Protein kinase C gamma interneurons in the rat medullary dorsal horn: distribution and synaptic inputs to these neurons, and subcellular localization of the enzyme. J. Comp. Neurol. 2014, 522:393-413.
29. Polgár E., Fowler J.H., McGill M.M., Todd A.J. The types of neuron which contain protein kinase C gamma in rat spinal cord. Brain Res. 1999, 833:71-80.
30. Polgár E., Campbell A.D., MacIntyre L.M., Watanabe M., Todd A.J. Phosphorylation of ERK in neurokinin 1 receptor-expressing neurons in laminae III and IV of the rat spinal dorsal horn following noxious stimulation. Mol. Pain 2007, 3:4.
31. Polgár E., Thomson S., Maxwell D.J., Al-Khater K., Todd A.J. A population of large neurons in laminae III and IV of the rat spinal cord that have long dorsal dendrites and lack the neurokinin 1 receptor. Eur. J. Neurosci. 2007, 26:1587-1598.
32. Prescott S.A., Ma Q., De Koninck Y. Normal and abnormal coding of somatosensory stimuli causing pain. Nat. Neurosci. 2014, 17:183-191.
33. Ross S.E., Mardinly A.R., McCord A.E., Zurawski J., Cohen S., Jung C., Hu L., Mok S.I., Shah A., Savner E.M., et al. Loss of inhibitory interneurons in the dorsal spinal cord and elevated itch in Bhlhb5 mutant mice. Neuron 2010, 65:886-898.
34. Scherrer G., Low S.A., Wang X., Zhang J., Yamanaka H., Urban R., Solorzano C., Harper B., Hnasko T.S., Edwards R.H., Basbaum A.I. VGLUT2 expression in primary afferent neurons is essential for normal acute pain and injury-induced heat hypersensitivity. Proc. Natl. Acad. Sci. USA 2010, 107:22296-22301.
35. Schneider S.P. Local circuit connections between hamster laminae III and IV dorsal horn neurons. J. Neurophysiol. 2008, 99:1306-1318.
36. Seal R.P., Akil O., Yi E., Weber C.M., Grant L., Yoo J., Clause A., Kandler K., Noebels J.L., Glowatzki E., et al. Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3. Neuron 2008, 57:263-275.
37. Seal R.P., Wang X., Guan Y., Raja S.N., Woodbury C.J., Basbaum A.I., Edwards R.H. Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors. Nature 2009, 462:651-655.
38. Sieber M.A., Storm R., Martinez-de-la-Torre M., Müller T., Wende H., Reuter K., Vasyutina E., Birchmeier C. Lbx1 acts as a selector gene in the fate determination of somatosensory and viscerosensory relay neurons in the hindbrain. J. Neurosci. 2007, 27:4902-4909.
39. Todd A.J. Neuronal circuitry for pain processing in the dorsal horn. Nat. Rev. Neurosci. 2010, 11:823-836.
40. Torsney C., MacDermott A.B. Disinhibition opens the gate to pathological pain signaling in superficial neurokinin 1 receptor-expressing neurons in rat spinal cord. J. Neurosci. 2006, 26:1833-1843.
41. Varrassi G., Müller-Schwefe G., Pergolizzi J., Orónska A., Morlion B., Mavrocordatos P., Margarit C., Mangas C., Jaksch W., Huygen F., et al. Pharmacological treatment of chronic pain-the need for CHANGE. Curr. Med. Res. Opin. 2010, 26:1231-1245.
42. von Hehn C.A., Baron R., Woolf C.J. Deconstructing the neuropathic pain phenotype to reveal neural mechanisms. Neuron 2012, 73:638-652.
43. Vrontou S., Wong A.M., Rau K.K., Koerber H.R., Anderson D.J. Genetic identification of C fibres that detect massage-like stroking of hairy skin in vivo. Nature 2013, 493:669-673.
44. Wang X., Zhang J., Eberhart D., Urban R., Meda K., Solorzano C., Yamanaka H., Rice D., Basbaum A.I. Excitatory superficial dorsal horn interneurons are functionally heterogeneous and required for the full behavioral expression of pain and itch. Neuron 2013, 78:312-324.
45. Witschi R., Johansson T., Morscher G., Scheurer L., Deschamps J., Zeilhofer H.U. Hoxb8-Cre mice: a tool for brain-sparing conditional gene deletion. Genesis 2010, 48:596-602.
46. Xu Y., Lopes C., Wende H., Guo Z., Cheng L., Birchmeier C., Ma Q. Ontogeny of excitatory spinal neurons processing distinct somatic sensory modalities. J. Neurosci. 2013, 33:14738-14748.
47. Yasaka T., Tiong S.Y., Polgár E., Watanabe M., Kumamoto E., Riddell J.S., Todd A.J. A putative relay circuit providing low-threshold mechanoreceptive input to lamina I projection neurons via vertical cells in lamina II of the rat dorsal horn. Mol. Pain 2014, 10:3.
48. Zeilhofer H.U., Wildner H., Yévenes G.E. Fast synaptic inhibition in spinal sensory processing and pain control. Physiol. Rev. 2012, 92:193-235.
49. Zhao C., Leitges M., Gereau R.W. Isozyme-specific effects of protein kinase C in pain modulation. Anesthesiology 2011, 115:1261-1270.
50. Zou W., Song Z., Guo Q., Liu C., Zhang Z., Zhang Y. Intrathecal lentiviral-mediated RNA interference targeting PKCγ attenuates chronic constriction injury-induced neuropathic pain in rats. Hum. Gene Ther. 2011, 22:465-475.