Targeted ablation, silencing, and activation establish glycinergic dorsal horn neurons as key components of a spinal gate for pain and itch

Neuron

Volumn 85, Issue 6, 2015, Pages 1289-1304

  Foster, Edmund ^a   Wildner, Hendrik ^a   Tudeau, Laetitia ^a,d   Haueter, Sabine ^a,d   Ralvenius, William T ^a   Jegen, Monika ^a,d   Johannssen, Helge ^a   Hösli, Ladina ^a   Haenraets, Karen ^a,d   Ghanem, Alexander ^b   Conzelmann, Karl Klaus ^b   Bösl, Michael ^c   Zeilhofer, Hanns Ulrich ^a,d  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE; CRE RECOMBINASE; DIPHTHERIA TOXIN; GLYCINE; HISTAMINE; TETANUS TOXIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVERSIVE BEHAVIOR; BITE; CELL ACTIVATION; GATE CONTROL THEORY; GLYCINERGIC DORSAL HORN NEURON; HYPERALGESIA; LICKING; MALE; MOUSE; NEUROPATHIC PAIN; NONHUMAN; PAIN; PRIORITY JOURNAL; PRURITUS; SENSORY GATING; SENSORY NERVE CELL; SPINAL CORD DORSAL HORN; SPINAL CORD NERVE CELL; SPINAL GANGLION; ANIMAL; CYTOLOGY; DISEASE MODEL; GENETICS; METABOLISM; NERVE CELL; NERVE CELL NETWORK; PATHOLOGY; PATHOPHYSIOLOGY; PERIPHERAL NEUROPATHY; PHYSIOLOGY; POSTERIOR HORN CELL; TRANSGENIC MOUSE;

ANIMALS; DISEASE MODELS, ANIMAL; GLYCINE; HYPERALGESIA; MICE; MICE, TRANSGENIC; NERVE NET; NEURONS; PAIN; PERIPHERAL NERVOUS SYSTEM DISEASES; POSTERIOR HORN CELLS; PRURITUS; SPINAL CORD DORSAL HORN;

EID: 84925278477     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.02.028     Document Type: Article

References (70)

1. 2 selectively blocks inhibitory glycinergic neurotransmission onto rat superficial dorsal horn neurons. Nat. Neurosci. 2002, 5:34-40.
2. Akiyama T., Carstens E. Neural processing of itch. Neuroscience 2013, 250:697-714.
3. Alexander G.M., Rogan S.C., Abbas A.I., Armbruster B.N., Pei Y., Allen J.A., Nonneman R.J., Hartmann J., Moy S.S., Nicolelis M.A., et al. Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 2009, 63:27-39.
4. Armbruster B.N., Li X., Pausch M.H., Herlitze S., Roth B.L. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl. Acad. Sci. USA 2007, 104:5163-5168.
5. Aschauer D.F., Kreuz S., Rumpel S. Analysis of transduction efficiency, tropism and axonal transport of AAV serotypes 1, 2, 5, 6, 8 and 9 in the mouse brain. PLoS ONE 2013, 8:e76310.
6. Atasoy D., Aponte Y., Su H.H., Sternson S.M. A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J.Neurosci. 2008, 28:7025-7030.
7. 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.
8. Bennett G.J., Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988, 33:87-107.
9. Betley J.N., Sternson S.M. Adeno-associated viral vectors for mapping, monitoring, and manipulating neural circuits. Hum. Gene Ther. 2011, 22:669-677.
10. Beyer C., Roberts L.A., Komisaruk B.R. Hyperalgesia induced by altered glycinergic activity at the spinal cord. Life Sci. 1985, 37:875-882.
11. Bráz J.M., Sharif-Naeini R., Vogt D., Kriegstein A., Alvarez-Buylla A., Rubenstein J.L., Basbaum A.I. Forebrain GABAergic neuron precursors integrate into adult spinal cord and reduce injury-induced neuropathic pain. Neuron 2012, 74:663-675.
12. Brooks A.R., Harkins R.N., Wang P., Qian H.S., Liu P., Rubanyi G.M. Transcriptional silencing is associated with extensive methylation of the CMV promoter following adenoviral gene delivery to muscle. J.Gene Med. 2004, 6:395-404.
13. Buch T., Heppner F.L., Tertilt C., Heinen T.J., Kremer M., Wunderlich F.T., Jung S., Waisman A. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat. Methods 2005, 2:419-426.
14. Chamberlin N.L., Du B., de Lacalle S., Saper C.B. Recombinant adeno-associated virus vector: use for transgene expression and anterograde tract tracing in the CNS. Brain Res. 1998, 793:169-175.
15. Clark A.K., Gentry C., Bradbury E.J., McMahon S.B., Malcangio M. Role of spinal microglia in rat models of peripheral nerve injury and inflammation. Eur. J. Pain 2007, 11:223-230.
16. Coull J.A., Boudreau D., Bachand K., Prescott S.A., Nault F., Sík A., De Koninck P., De Koninck Y. Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 2003, 424:938-942.
17. Coull J.A., Beggs S., Boudreau D., Boivin D., Tsuda M., Inoue K., Gravel C., Salter M.W., De Koninck Y. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 2005, 438:1017-1021.
18. Coyle D.E. Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior. Glia 1998, 23:75-83.
19. Davidson S., Zhang X., Khasabov S.G., Simone D.A., Giesler G.J. Relief of itch by scratching: state-dependent inhibition of primate spinothalamic tract neurons. Nat. Neurosci. 2009, 12:544-546.
20. Drew G.M., Siddall P.J., Duggan A.W. Mechanical allodynia following contusion injury of the rat spinal cord is associated with loss of GABAergic inhibition in the dorsal horn. Pain 2004, 109:379-388.
21. 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.
22. Gomeza J., Ohno K., Hülsmann S., Armsen W., Eulenburg V., Richter D.W., Laube B., Betz H. Deletion of the mouse glycine transporter 2 results in a hyperekplexia phenotype and postnatal lethality. Neuron 2003, 40:797-806.
23. Goulding M. Circuits controlling vertebrate locomotion: moving in a new direction. Nat. Rev. Neurosci. 2009, 10:507-518.
24. Graeber M.B., Christie M.J. Multiple mechanisms of microglia: a gatekeeper's contribution to pain states. Exp. Neurol. 2012, 234:255-261.
25. Hanisch U.K., Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 2007, 10:1387-1394.
26. 2-mediated inflammatory pain sensitization. Science 2004, 304:884-887.
27. Hossaini M., French P.J., Holstege J.C. Distribution of glycinergic neuronal somata in the rat spinal cord. Brain Res. 2007, 1142:61-69.
28. Hutson T.H., Verhaagen J., Yáñez-Muñoz R.J., Moon L.D. Corticospinal tract transduction: a comparison of seven adeno-associated viral vector serotypes and a non-integrating lentiviral vector. Gene Ther. 2012, 19:49-60.
29. Isaacson J.S., Scanziani M. How inhibition shapes cortical activity. Neuron 2011, 72:231-243.
30. Kardon A.P., Polgár E., Hachisuka J., Snyder L.M., Cameron D., Savage S., Cai X., Karnup S., Fan C.R., Hemenway G.M., et al. Dynorphin acts as a neuromodulator to inhibit itch in the dorsal horn of the spinal cord. Neuron 2014, 82:573-586.
31. Keller A.F., Coull J.A., Chery N., Poisbeau P., De Koninck Y. Region-specific developmental specialization of GABA-glycine cosynapses in laminas I-II of the rat spinal dorsal horn. J.Neurosci. 2001, 21:7871-7880.
32. Keller A.F., Beggs S., Salter M.W., De Koninck Y. Transformation of the output of spinal lamina I neurons after nerve injury and microglia stimulation underlying neuropathic pain. Mol. Pain 2007, 3:27.
33. A receptor subtypes. Nature 2008, 451:330-334.
34. Kuner R. Central mechanisms of pathological pain. Nat. Med. 2010, 16:1258-1266.
35. Laing I., Todd A.J., Heizmann C.W., Schmidt H.H. Subpopulations of GABAergic neurons in laminae I-III of rat spinal dorsal horn defined by coexistence with classical transmitters, peptides, nitric oxide synthase or parvalbumin. Neuroscience 1994, 61:123-132.
36. Loomis C.W., Khandwala H., Osmond G., Hefferan M.P. Coadministration of intrathecal strychnine and bicuculline effects synergistic allodynia in the rat: an isobolographic analysis. J.Pharmacol. Exp. Ther. 2001, 296:756-761.
37. 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.
38. Melzack R., Wall P.D. Pain mechanisms: a new theory. Science 1965, 150:971-979.
39. Miraucourt L.S., Moisset X., Dallel R., Voisin D.L. Glycine inhibitory dysfunction induces a selectively dynamic, morphine-resistant, and neurokinin 1 receptor- independent mechanical allodynia. J.Neurosci. 2009, 29:2519-2527.
40. Moore K.A., Kohno T., Karchewski L.A., Scholz J., Baba H., Woolf C.J. Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J.Neurosci. 2002, 22:6724-6731.
41. Müller F., Heinke B., Sandkühler J. Reduction of glycine receptor-mediated miniature inhibitory postsynaptic currents in rat spinal lamina I neurons after peripheral inflammation. Neuroscience 2003, 122:799-805.
42. Osakada F., Callaway E.M. Design and generation of recombinant rabies virus vectors. Nat. Protoc. 2013, 8:1583-1601.
43. Palmiter R.D., Behringer R.R., Quaife C.J., Maxwell F., Maxwell I.H., Brinster R.L. Cell lineage ablation in transgenic mice by cell-specific expression of a toxin gene. Cell 1987, 50:435-443.
44. Polgár E., Durrieux C., Hughes D.I., Todd A.J. A quantitative study of inhibitory interneurons in laminae I-III of the mouse spinal dorsal horn. PLoS ONE 2013, 8:e78309.
45. Poyatos I., Ponce J., Aragón C., Giménez C., Zafra F. The glycine transporter GLYT2 is a reliable marker for glycine-immunoreactive neurons. Brain Res. Mol. Brain Res. 1997, 49:63-70.
46. Punnakkal P., von Schoultz C., Haenraets K., Wildner H., Zeilhofer H.U. Morphological, biophysical and synaptic properties of glutamatergic neurons of the mouse spinal dorsal horn. J.Physiol. 2014, 592:759-776.
47. 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.
48. Sandkühler J. Models and mechanisms of hyperalgesia and allodynia. Physiol. Rev. 2009, 89:707-758.
49. Sardella T.C., Polgár E., Garzillo F., Furuta T., Kaneko T., Watanabe M., Todd A.J. Dynorphin is expressed primarily by GABAergic neurons that contain galanin in the rat dorsal horn. Mol. Pain 2011, 7:76.
50. Scholz J., Broom D.C., Youn D.H., Mills C.D., Kohno T., Suter M.R., Moore K.A., Decosterd I., Coggeshall R.E., Woolf C.J. Blocking caspase activity prevents transsynaptic neuronal apoptosis and the loss of inhibition inlamina II of the dorsal horn after peripheral nerve injury. J.Neurosci. 2005, 25:7317-7323.
51. Sherman S.E., Loomis C.W. Morphine insensitive allodynia is produced by intrathecal strychnine in the lightly anesthetized rat. Pain 1994, 56:17-29.
52. Simmons D.R., Spike R.C., Todd A.J. Galanin is contained in GABAergic neurons in the rat spinal dorsal horn. Neurosci. Lett. 1995, 187:119-122.
53. A and glycine receptors to central sensitization: disinhibition and touch-evoked allodynia in the spinal cord. J.Neurophysiol. 1994, 72:169-179.
54. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
55. Sorkin L.S., Puig S., Jones D.L. Spinal bicuculline produces hypersensitivity of dorsal horn neurons: effects of excitatory amino acid antagonists. Pain 1998, 77:181-190.
56. Sweeney S.T., Broadie K., Keane J., Niemann H., O'Kane C.J. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 1995, 14:341-351.
57. Tamamaki N., Yanagawa Y., Tomioka R., Miyazaki J., Obata K., Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J.Comp. Neurol. 2003, 467:60-79.
58. Tanga F.Y., Raghavendra V., DeLeo J.A. Quantitative real-time RT-PCR assessment of spinal microglial and astrocytic activation markers in a rat model of neuropathic pain. Neurochem. Int. 2004, 45:397-407.
59. Taves S., Berta T., Chen G., Ji R.R. Microglia and spinal cord synaptic plasticity in persistent pain. Neural Plast. 2013, 2013:753656.
60. Todd A.J., Spike R.C. The localization of classical transmitters and neuropeptides within neurons in laminae I-III of the mammalian spinal dorsal horn. Prog. Neurobiol. 1993, 41:609-645.
61. 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.
62. Ward L., Wright E., McMahon S.B. A comparison of the effects of noxious and innocuous counterstimuli on experimentally induced itch and pain. Pain 1996, 64:129-138.
63. Wickersham I.R., Lyon D.C., Barnard R.J., Mori T., Finke S., Conzelmann K.K., Young J.A., Callaway E.M. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 2007, 53:639-647.
64. Woolf C.J., Salter M.W. Neuronal plasticity: increasing the gain inpain. Science 2000, 288:1765-1769.
65. Xiong W., Cheng K., Cui T., Godlewski G., Rice K.C., Xu Y., Zhang L. Cannabinoid potentiation of glycine receptors contributes to cannabis-induced analgesia. Nat. Chem. Biol. 2011, 7:296-303.
66. Xiong W., Cui T., Cheng K., Yang F., Chen S.R., Willenbring D., Guan Y., Pan H.L., Ren K., Xu Y., Zhang L. Cannabinoids suppress inflammatory and neuropathic pain by targeting α3 glycine receptors. J.Exp. Med. 2012, 209:1121-1134.
67. Yaksh T.L. Behavioral and autonomic correlates of the tactile evoked allodynia produced by spinal glycine inhibition: effects of modulatory receptor systems and excitatory amino acid antagonists. Pain 1989, 37:111-123.
68. Zeilhofer H.U., Studler B., Arabadzisz D., Schweizer C., Ahmadi S., Layh B., Bösl M.R., Fritschy J.M. Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice. J.Comp. Neurol. 2005, 482:123-141.
69. Zeilhofer H.U., Wildner H., Yévenes G.E. Fast synaptic inhibition in spinal sensory processing and pain control. Physiol. Rev. 2012, 92:193-235.
70. Zhao S., Ting J.T., Atallah H.E., Qiu L., Tan J., Gloss B., Augustine G.J., Deisseroth K., Luo M., Graybiel A.M., Feng G. Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function. Nat. Methods 2011, 8:745-752.