Neurochemical characterisation of lamina II inhibitory interneurons that express GFP in the PrP-GFP mouse

Molecular Pain

Volumn 9, Issue 1, 2013, Pages

  Iwagaki, Noboru ^a   Garzillo, Francesca ^a   Polgár, Erika ^a   Riddell, John S ^a   Todd, Andrew J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GALANIN; GREEN FLUORESCENT PROTEIN; NEURONAL NITRIC OXIDE SYNTHASE; PRION PROTEIN; SOMATOSTATIN; SOMATOSTATIN RECEPTOR; SOMATOSTATIN RECEPTOR 2A; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; INHIBITORY INTERNEURON; INTERNEURON; MALE; MOUSE; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD DORSAL HORN; SPINAL CORD NERVE CELL;

ANIMALS; FEMALE; GREEN FLUORESCENT PROTEINS; HUMANS; INTERNEURONS; MALE; MICE; POSTERIOR HORN CELLS;

EID: 84888054067     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-9-56     Document Type: Article

References (78)

1. Todd AJ. Neuronal circuitry for pain processing in the dorsal horn. Nat Rev Neurosci 2010, 11:823-836. 3277941, 21068766.
2. Polgár E, Hughes DI, Riddell JS, Maxwell DJ, Puskar Z, Todd AJ. Selective loss of spinal GABAergic or glycinergic neurons is not necessary for development of thermal hyperalgesia in the chronic constriction injury model of neuropathic pain. Pain 2003, 104:229-239. 10.1016/S0304-3959(03)00011-3, 12855333.
3. Todd AJ, Sullivan AC. Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivities in the spinal cord of the rat. J Comp Neurol 1990, 296:496-505. 10.1002/cne.902960312, 2358549.
4. Polgár E, Durrieux C, Hughes DI, Todd AJ. A quantitative study of inhibitory interneurons in laminae I-III of the mouse spinal dorsal horn. PloS one 2013, e78309.
5. Basbaum AI, Bautista DM, Scherrer G, Julius D. Cellular and molecular mechanisms of pain. Cell 2009, 139:267-284. 10.1016/j.cell.2009.09.028, 2852643, 19837031.
6. Ross SE, Mardinly AR, McCord AE, Zurawski J, Cohen S, Jung C, Hu L, Mok SI, Shah A, Savner EM, et al. Loss of inhibitory interneurons in the dorsal spinal cord and elevated itch in Bhlhb5 mutant mice. Neuron 2010, 65:886-898. 10.1016/j.neuron.2010.02.025, 2856621, 20346763.
7. Sandkuhler J. Models and mechanisms of hyperalgesia and allodynia. Physiol Rev 2009, 89:707-758. 10.1152/physrev.00025.2008, 19342617.
8. Zeilhofer HU, Wildner H, Yevenes GE. Fast synaptic inhibition in spinal sensory processing and pain control. Physiol Rev 2012, 92:193-235. 10.1152/physrev.00043.2010, 3590010, 22298656.
9. Gobel S. Golgi studies of the neurons in layer II of the dorsal horn of the medulla (trigeminal nucleus caudalis). J Comp Neurol 1978, 180:395-413. 10.1002/cne.901800213, 659668.
10. Graham BA, Brichta AM, Callister RJ. Moving from an averaged to specific view of spinal cord pain processing circuits. J Neurophysiol 2007, 98:1057-1063. 10.1152/jn.00581.2007, 17567772.
11. Grudt TJ, Perl ER. Correlations between neuronal morphology and electrophysiological features in the rodent superficial dorsal horn. J Physiol 2002, 540:189-207. 10.1113/jphysiol.2001.012890, 2290200, 11927679.
12. Heinke B, Ruscheweyh R, Forsthuber L, Wunderbaldinger G, Sandkuhler J. Physiological, neurochemical and morphological properties of a subgroup of GABAergic spinal lamina II neurones identified by expression of green fluorescent protein in mice. J Physiol 2004, 560:249-266. 10.1113/jphysiol.2004.070540, 1665197, 15284347.
13. Polgár E, Sardella TCP, Tiong SYX, Locke S, Watanabe M, Todd AJ. Functional differences between neurochemically-defined populations of inhibitory interneurons in the rat spinal cord. Pain 2013, 2606-2615. in press.
14. Yasaka T, Tiong SYX, Hughes DI, Riddell JS, Todd AJ. Populations of inhibitory and excitatory interneurons in lamina II of the adult rat spinal dorsal horn revealed by a combined electrophysiological and anatomical approach. Pain 2010, 151:475-488. 10.1016/j.pain.2010.08.008, 3170912, 20817353.
15. Maxwell DJ, Belle MD, Cheunsuang O, Stewart A, Morris R. Morphology of inhibitory and excitatory interneurons in superficial laminae of the rat dorsal horn. J Physiol 2007, 584:521-533. 10.1113/jphysiol.2007.140996, 2277171, 17717012.
16. Davies AJ, North RA. Electrophysiological and morphological properties of neurons in the substantia gelatinosa of the mouse trigeminal subnucleus caudalis. Pain 2009, 146:214-221. 10.1016/j.pain.2009.07.038, 19703729.
17. Laing I, Todd AJ, Heizmann CW, Schmidt HH. 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. 10.1016/0306-4522(94)90065-5, 7526265.
18. Light AR, Trevino DL, Perl ER. Morphological features of functionally defined neurons in the marginal zone and substantia gelatinosa of the spinal dorsal horn. J Comp Neurol 1979, 186:151-171. 10.1002/cne.901860204, 447881.
19. Lu Y, Perl ER. A specific inhibitory pathway between substantia gelatinosa neurons receiving direct C-fiber input. J Neurosci 2003, 23:8752-8758.
20. Lu Y, Perl ER. Modular organization of excitatory circuits between neurons of the spinal superficial dorsal horn (laminae I and II). J Neurosci 2005, 25:3900-3907. 10.1523/JNEUROSCI.0102-05.2005, 15829642.
21. Réthelyi M, Light AR, Perl ER. Synaptic ultrastructure of functionally and morphologically characterized neurons of the superficial spinal dorsal horn of cat. J Neurosci 1989, 9:1846-1863.
22. Santos SF, Rebelo S, Derkach VA, Safronov BV. Excitatory interneurons dominate sensory processing in the spinal substantia gelatinosa of rat. J Physiol 2007, 581:241-254. 10.1113/jphysiol.2006.126912, 2075233, 17331995.
23. Todd AJ, Lewis SG. The morphology of Golgi-stained neurons in lamina II of the rat spinal cord. J Anat 1986, 149:113-119. 1261638, 2447052.
24. Wang H, Zylka MJ. Mrgprd-expressing polymodal nociceptive neurons innervate most known classes of substantia gelatinosa neurons. J Neurosci 2009, 29:13202-13209. 10.1523/JNEUROSCI.3248-09.2009, 2789299, 19846708.
25. Woolf CJ, Fitzgerald M. The properties of neurones recorded in the superficial dorsal horn of the rat spinal cord. J Comp Neurol 1983, 221:313-328. 10.1002/cne.902210307, 6197429.
26. Hu HJ, Gereau RW. ERK integrates PKA and PKC signaling in superficial dorsal horn neurons. II. Modulation of neuronal excitability. J Neurophysiol 2003, 90:1680-1688. 10.1152/jn.00341.2003, 12750418.
27. Brohl D, Strehle M, Wende H, Hori K, Bormuth I, Nave KA, Muller T, Birchmeier C. A transcriptional network coordinately determines transmitter and peptidergic fate in the dorsal spinal cord. Dev Biol 2008, 322:381-393. 10.1016/j.ydbio.2008.08.002, 18721803.
28. Wildner H, Das Gupta R, Brohl D, Heppenstall PA, Zeilhofer HU, Birchmeier C. Genome-wide expression analysis of Ptf1a- and Ascl1-deficient mice reveals new markers for distinct dorsal horn interneuron populations contributing to nociceptive reflex plasticity. J Neurosci 2013, 33:7299-7307. 10.1523/JNEUROSCI.0491-13.2013, 3684736, 23616538.
29. Todd AJ, McKenzie J. GABA-immunoreactive neurons in the dorsal horn of the rat spinal cord. Neuroscience 1989, 31:799-806. 10.1016/0306-4522(89)90442-9, 2594201.
30. Yasaka T, Kato G, Furue H, Rashid MH, Sonohata M, Tamae A, Murata Y, Masuko S, Yoshimura M. Cell-type-specific excitatory and inhibitory circuits involving primary afferents in the substantia gelatinosa of the rat spinal dorsal horn in vitro. J Physiol 2007, 581:603-618. 10.1113/jphysiol.2006.123919, 2075204, 17347278.
31. Tiong SYX, Polgár E, van Kralingen JC, Watanabe M, Todd AJ. Galanin-immunoreactivity identifies a distinct population of inhibitory interneurons in laminae I-III of the rat spinal cord. Mol Pain 2011, 7:36. 10.1186/1744-8069-7-36, 3118366, 21569622.
32. Todd AJ, Spike RC, Polgar E. A quantitative study of neurons which express neurokinin-1 or somatostatin sst2a receptor in rat spinal dorsal horn. Neuroscience 1998, 85:459-473. 10.1016/S0306-4522(97)00669-6, 9622244.
33. Daniele CA, MacDermott AB. Low-threshold primary afferent drive onto GABAergic interneurons in the superficial dorsal horn of the mouse. J Neurosci 2009, 29:686-695. 10.1523/JNEUROSCI.5120-08.2009, 2826179, 19158295.
34. Hantman AW, Perl ER. Molecular and genetic features of a labeled class of spinal substantia gelatinosa neurons in a transgenic mouse. J Comp Neurol 2005, 492:90-100. 10.1002/cne.20709, 16175558.
35. Hantman AW, van den Pol AN, Perl ER. Morphological and physiological features of a set of spinal substantia gelatinosa neurons defined by green fluorescent protein expression. J Neurosci 2004, 24:836-842. 10.1523/JNEUROSCI.4221-03.2004, 14749428.
36. Hughes DI, Sikander S, Kinnon CM, Boyle KA, Watanabe M, Callister RJ, Graham BA. Morphological, neurochemical and electrophysiological features of parvalbumin-expressing cells: a likely source of axo-axonic inputs in the mouse spinal dorsal horn. J Physiol 2012, 590:3927-3951. 10.1113/jphysiol.2012.235655, 3476641, 22674718.
37. Leitner J, Westerholz S, Heinke B, Forsthuber L, Wunderbaldinger G, Jager T, Gruber-Schoffnegger D, Braun K, Sandkuhler J. Impaired excitatory drive to spinal GABAergic neurons of neuropathic mice. PloS one 2013, 8:e73370. 10.1371/journal.pone.0073370, 3751881, 24009748.
38. Mesnage B, Gaillard S, Godin AG, Rodeau JL, Hammer M, Von Engelhardt J, Wiseman PW, De Koninck Y, Schlichter R, Cordero-Erausquin M. Morphological and functional characterization of cholinergic interneurons in the dorsal horn of the mouse spinal cord. J Comp Neurol 2011, 519:3139-3158. 10.1002/cne.22668, 21618225.
39. Zeilhofer HU, Studler B, Arabadzisz D, Schweizer C, Ahmadi S, Layh B, Bosl MR, Fritschy JM. Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice. J Comp Neurol 2005, 482:123-141. 10.1002/cne.20349, 15611994.
40. Zheng J, Lu Y, Perl ER. Inhibitory neurones of the spinal substantia gelatinosa mediate interaction of signals from primary afferents. J Physiol 2010, 588:2065-2075. 10.1113/jphysiol.2010.188052, 2911212, 20403977.
41. van den Pol AN, Ghosh PK, Liu RJ, Li Y, Aghajanian GK, Gao XB. Hypocretin (orexin) enhances neuron activity and cell synchrony in developing mouse GFP-expressing locus coeruleus. J Physiol 2002, 541:169-185. 10.1113/jphysiol.2002.017426, 2290314, 12015428.
42. Kim SJ, Chung WH, Rhim H, Eun SY, Jung SJ, Kim J. Postsynaptic action mechanism of somatostatin on the membrane excitability in spinal substantia gelatinosa neurons of juvenile rats. Neuroscience 2002, 114:1139-1148. 10.1016/S0306-4522(02)00245-2, 12379266.
43. Ottersen OP, Storm-Mathiesen J. Localization of amino acid neurotransmitters by immunocytochemistry. Trends Neurosci 1987, 10:250-255.
44. Somogyi P, Hodgson AJ, Chubb IW, Penke B, Erdei A. Antisera to gamma-aminobutyric acid. II. Immunocytochemical application to the central nervous system. J Histochem Cytochem 1985, 33:240-248. 10.1177/33.3.2579123, 2579123.
45. Sardella TC, Polgar E, Watanabe M, Todd AJ. A quantitative study of neuronal nitric oxide synthase expression in laminae I-III of the rat spinal dorsal horn. Neuroscience 2011, 192:708-720. 3183229, 21763759.
46. Sloviter RS, Ali-Akbarian L, Horvath KD, Menkens KA. Substance P receptor expression by inhibitory interneurons of the rat hippocampus: enhanced detection using improved immunocytochemical methods for the preservation and colocalization of GABA and other neuronal markers. J Comp Neurol 2001, 430:283-305. 10.1002/1096-9861(20010212)430:3<283::AID-CNE1031>3.0.CO;2-V, 11169468.
47. Polgár E, Sardella T, Watanabe M, Todd AJ. A quantitative study of NPY-expressing GABAergic neurons and axons in rat spinal dorsal horn. J Comp Neurol 2011, 519:1007-1023. 10.1002/cne.22570, 3258544, 21344400.
48. Pow DV, Crook DK. Extremely high titre polyclonal antisera against small neurotransmitter molecules: rapid production, characterisation and use in light- and electron-microscopic immunocytochemistry. J Neurosci Methods 1993, 48:51-63. 10.1016/S0165-0270(05)80007-X, 8104259.
49. Herbison AE, Simonian SX, Norris PJ, Emson PC. Relationship of neuronal nitric oxide synthase immunoreactivity to GnRH neurons in the ovariectomized and intact female rat. J Neuroendocrinol 1996, 8:73-82. 10.1111/j.1365-2826.1996.tb00688.x, 8932739.
50. Rowan S, Todd AJ, Spike RC. Evidence that neuropeptide Y is present in GABAergic neurons in the superficial dorsal horn of the rat spinal cord. Neuroscience 1993, 53:537-545. 10.1016/0306-4522(93)90218-5, 8492914.
51. Simmons DR, Spike RC, Todd AJ. Galanin is contained in GABAergic neurons in the rat spinal dorsal horn. Neurosci Lett 1995, 187:119-122. 10.1016/0304-3940(95)11358-4, 7540270.
52. Makwana M, Werner A, Acosta-Saltos A, Gonitel R, Pararajasingham A, Ruff C, Rumajogee P, Cuthill D, Galiano M, Bohatschek M, et al. Peripheral facial nerve axotomy in mice causes sprouting of motor axons into perineuronal central white matter: time course and molecular characterization. J Comp Neurol 2010, 518:699-721. 10.1002/cne.22240, 20034058.
53. Mullen RJ, Buck CR, Smith AM. NeuN, a neuronal specific nuclear protein in vertebrates. Development 1992, 116:201-211.
54. Ruscheweyh R, Sandkuhler J. Lamina-specific membrane and discharge properties of rat spinal dorsal horn neurones in vitro. J Physiol 2002, 541:231-244. 10.1113/jphysiol.2002.017756, 2290304, 12015432.
55. Jiang N, Furue H, Katafuchi T, Yoshimura M. Somatostatin directly inhibits substantia gelatinosa neurons in adult rat spinal dorsal horn in vitro. Neurosci Res 2003, 47:97-107. 10.1016/S0168-0102(03)00183-4, 12941451.
56. Nakatsuka T, Fujita T, Inoue K, Kumamoto E. Activation of GIRK channels in substantia gelatinosa neurones of the adult rat spinal cord: a possible involvement of somatostatin. J Physiol 2008, 586:2511-2522. 10.1113/jphysiol.2007.146076, 2464335, 18356203.
57. Polgar E, Sardella TC, Watanabe M, Todd AJ. Quantitative study of NPY-expressing GABAergic neurons and axons in rat spinal dorsal horn. J Comp Neurol 2011, 519:1007-1023. 10.1002/cne.22570, 3258544, 21344400.
58. Polgár E, Shehab SA, Watt C, Todd AJ. GABAergic neurons that contain neuropeptide Y selectively target cells with the neurokinin 1 receptor in laminae III and IV of the rat spinal cord. J Neurosci 1999, 19:2637-2646.
59. Puskár Z, Polgár E, Todd AJ. A population of large lamina I projection neurons with selective inhibitory input in rat spinal cord. Neuroscience 2001, 102:167-176. 10.1016/S0306-4522(00)00445-0, 11226680.
60. Antal M, Freund TF, Polgar E. Calcium-binding proteins, parvalbumin- and calbindin-D 28 k-immunoreactive neurons in the rat spinal cord and dorsal root ganglia: a light and electron microscopic study. J Comp Neurol 1990, 295:467-484. 10.1002/cne.902950310, 2351764.
61. Spike RC, Todd AJ, Johnston HM. Coexistence of NADPH diaphorase with GABA, glycine, and acetylcholine in rat spinal cord. J Comp Neurol 1993, 335:320-333. 10.1002/cne.903350303, 8227522.
62. Liuzzi FJ, Wu W, Scoville SA, Schinco FP. Development of nitric oxide synthase expression in the superficial dorsal horn of the rat spinal cord. Exp Neurol 1993, 121:275-278. 10.1006/exnr.1993.1096, 7687962.
63. Kemp T, Spike RC, Watt C, Todd AJ. The mu-opioid receptor (MOR1) is mainly restricted to neurons that do not contain GABA or glycine in the superficial dorsal horn of the rat spinal cord. Neuroscience 1996, 75:1231-1238. 10.1016/0306-4522(96)00333-8, 8938756.
64. Jeftinija S. Enkephalins modulate excitatory synaptic transmission in the superficial dorsal horn by acting at mu-opioid receptor sites. Brain research 1988, 460:260-268. 10.1016/0006-8993(88)90371-X, 2852045.
65. Yoshimura M, North RA. Substantia gelatinosa neurones hyperpolarized in vitro by enkephalin. Nature 1983, 305:529-530. 10.1038/305529a0, 6621700.
66. Schneider SP, Eckert WA, Light AR. Opioid-activated postsynaptic, inward rectifying potassium currents in whole cell recordings in substantia gelatinosa neurons. J Neurophysiol 1998, 80:2954-2962.
67. Grudt TJ, Williams JT. mu-Opioid agonists inhibit spinal trigeminal substantia gelatinosa neurons in guinea pig and rat. J Neurosci 1994, 14:1646-1654.
68. Imhof AK, Gluck L, Gajda M, Lupp A, Brauer R, Schaible HG, Schulz S. Differential antiinflammatory and antinociceptive effects of the somatostatin analogs octreotide and pasireotide in a mouse model of immune-mediated arthritis. Arthritis Rheum 2011, 63:2352-2362. 10.1002/art.30410, 21506098.
69. Schulz S, Schreff M, Schmidt H, Handel M, Przewlocki R, Hollt V. Immunocytochemical localization of somatostatin receptor sst2A in the rat spinal cord and dorsal root ganglia. Eur J Neurosci 1998, 10:3700-3708. 10.1046/j.1460-9568.1998.00386.x, 9875349.
70. Schindler M, Sellers LA, Humphrey PP, Emson PC. Immunohistochemical localization of the somatostatin SST2(A) receptor in the rat brain and spinal cord. Neuroscience 1997, 76:225-240.
71. Seybold VS, Hylden JL, Wilcox GL. Intrathecal substance P and somatostatin in rats: behaviors indicative of sensation. Peptides 1982, 3:49-54. 10.1016/0196-9781(82)90141-3, 6176976.
72. Wiesenfeld-Hallin Z. Intrathecal somatostatin modulates spinal sensory and reflex mechanisms: behavioral and electrophysiological studies in the rat. Neurosci Lett 1985, 62:69-74. 10.1016/0304-3940(85)90286-1, 2866475.
73. Wiesenfeld-Hallin Z. Somatostatin and calcitonin gene-related peptide synergistically modulate spinal sensory and reflex mechanisms in the rat: behavioral and electrophysiological studies. Neurosci Lett 1986, 67:319-323. 10.1016/0304-3940(86)90329-0, 2874534.
74. Chapman V, Dickenson AH. The effects of sandostatin and somatostatin on nociceptive transmission in the dorsal horn of the rat spinal cord. Neuropeptides 1992, 23:147-152. 10.1016/0143-4179(92)90115-D, 1361670.
75. Gaumann DM, Yaksh TL. Intrathecal somatostatin in rats: antinociception only in the presence of toxic effects. Anesthesiology 1988, 68:733-742. 10.1097/00000542-198805000-00011, 2897175.
76. Mollenholt P, Post C, Rawal N, Freedman J, Hokfelt T, Paulsson I. Antinociceptive and 'neurotoxic' actions of somatostatin in rat spinal cord after intrathecal administration. Pain 1988, 32:95-105. 10.1016/0304-3959(88)90028-0, 2893326.
77. Hokfelt T, Elde R, Johansson O, Luft R, Arimura A. Immunohistochemical evidence for presence of somatostatin, a powerful inhibitory peptide, in some primary sensory neurons. Neurosci Lett 1975, 1:231-235.
78. Proudlock F, Spike RC, Todd AJ. Immunocytochemical study of somatostatin, neurotensin, GABA, and glycine in rat spinal dorsal horn. J Comp Neurol 1993, 327:289-297. 10.1002/cne.903270210, 7678841.