Preprodynorphin-expressing neurons constitute a large subgroup of somatostatin-expressing GABAergic interneurons in the mouse neocortex

Journal of Comparative Neurology

Volumn 522, Issue 7, 2014, Pages 1506-1526

  Sohn, Jaerin ^a,b   Hioki, Hiroyuki ^a   Okamoto, Shinichiro ^a   Kaneko, Takeshi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

Author keywords

Combined labeling of immunofluorescence and fluorescent mRNA signals; Double immunofluorescence labeling; GABAergic neuron; Opioid peptide; Somatostatin

Indexed keywords

PREPRODYNORPHIN; REELIN; SOMATOSTATIN; 4 AMINOBUTYRIC ACID RECEPTOR; CALB2 PROTEIN, MOUSE; CALRETININ; DYNORPHIN; GLUTAMATE DECARBOXYLASE; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; NEUROPEPTIDE Y; NITRIC OXIDE SYNTHASE; PRE-PRODYNORPHIN; PROTEIN PRECURSOR; REELIN PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE; VESICULAR GLUTAMATE TRANSPORTER;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL COUNTING; CELL POPULATION; CONTROLLED STUDY; GABAERGIC SYSTEM; IMMUNOREACTIVITY; INTERNEURON; MALE; MOLECULAR DYNAMICS; MOTOR CORTEX; MOUSE; NEOCORTEX; NONHUMAN; ORBITAL CORTEX; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; STRIATE CORTEX; ANIMAL; C57BL MOUSE; CELL COUNT; CYTOLOGY; ENZYME IMMUNOASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; NERVE CELL; SOMATOSENSORY CORTEX;

ANIMALS; CALBINDIN 2; CELL ADHESION MOLECULES, NEURONAL; CELL COUNT; DYNORPHINS; EXTRACELLULAR MATRIX PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; GABAERGIC NEURONS; GLUTAMATE DECARBOXYLASE; IMMUNOENZYME TECHNIQUES; INTERNEURONS; MALE; MICE; MICE, INBRED C57BL; NEOCORTEX; NERVE TISSUE PROTEINS; NEURONS; NEUROPEPTIDE Y; NITRIC OXIDE SYNTHASE; PROTEIN PRECURSORS; RNA, MESSENGER; SERINE ENDOPEPTIDASES; SOMATOSENSORY CORTEX; SOMATOSTATIN; VESICULAR GLUTAMATE TRANSPORT PROTEINS;

EID: 84896272943     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23477     Document Type: Article

References (90)

1. Agnati LF, Guidolin D, Guescini M, Genedani S, Fuxe K. 2010. Understanding wiring and volume transmission. Brain Res Rev 64:137-159.
2. Alcántara S, Ruiz M, D'Arcangelo G, Ezan F, de Lecea L, Curran T, Sotelo C, Soriano E. 1998. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 18:7779-7799.
3. Allen JP, Hathway GJ, Clarke NJ, Jowett MI, Topps S, Kendrick KM, Humphrey PP, Wilkinson LS, Emson PC. 2003. Somatostatin receptor 2 knockout/lacZ knockin mice show impaired motor coordination and reveal sites of somatostatin action within the striatum. Eur J Neurosci 17:1881-1895.
4. Alvarez-Bolado G, Fairén A, Douglass J, Naranjo JR. 1990. Expression of the prodynorphin gene in the developing and adult cerebral cortex of the rat: an in situ hybridization study. J Comp Neurol 300:287-300.
5. Anderson CR, Furness JB, Woodman HL, Edwards SL, Crack PJ, Smith AI. 1995. Characterisation of neurons with nitric oxide synthase immunoreactivity that project to prevertebral ganglia. J Auton Nerv Syst 52:107-116.
6. Arvidsson U, Riedl M, Chakrabarti S, Vulchanova L, Lee JH, Nakano AH, Lin X, Loh HH, Law PY, Wessendorf MW, Elde R. 1995. The kappa-opioid receptor is primarily postsynaptic: combined immunohistochemical localization of the receptor and endogenous opioids. Proc Natl Acad Sci U S A 92:5062-5066.
7. Bayraktar T, Staiger JF, Acsady L, Cozzari C, Freund TF, Zilles K. 1997. Co-localization of vasoactive intestinal polypeptide, gamma-aminobutyric acid and choline acetyltransferase in neocortical interneurons of the adult rat. Brain Res 757:209-217.
8. Breder CD, Yamada Y, Yasuda K, Seino S, Saper CB, Bell GI. 1992. Differential expression of somatostatin receptor subtypes in brain. J Neurosci 12:3920-3934.
9. Burette AC, Strehler EE, Weinberg RJ. 2009. "Fast" plasma membrane calcium pump PMCA2a concentrates in GABAergic terminals in the adult rat brain. J Comp Neurol 512:500-513.
10. Cavinesss VS Jr. 1975. Architectonic map of neocortex of the normal mouse. J Comp Neurol 164:247-264.
11. Chavkin C. 2013. Dynorphin-still an extraordinary potent opioid peptide. Mol Pharmacol 83:729-736.
12. Chédotal A, Cozzari C, Faure MP, Hartman BK, Hamel E. 1994. Distinct choline acetyltransferase (ChAT) and vasoactive intestinal polypeptide (VIP) bipolar neurons project to local blood vessels in the rat cerebral cortex. Brain Res 646:181-193.
13. DePaoli AM, Hurley KM, Yasada K, Reisine T, Bell G. 1994. Distribution of kappa opioid receptor mRNA in adult mouse brain: an in situ hybridization histochemistry study. Mol Cell Neurosci 5:327-335.
14. Dournaud P, Gu YZ, Schonbrunn A, Mazella J, Tannenbaum GS, Beaudet A. 1996. Localization of the somatostatin receptor SST2A in rat brain using a specific anti-peptide antibody. J Neurosci 16:4468-4478.
15. Drake CT, Patterson TA, Simmons ML, Chavkin C, Milner TA. 1996. Kappa opioid receptor-like immunoreactivity in guinea pig brain: ultrastructural localization in presynaptic terminals in hippocampal formation. J Comp Neurol 370:377-395.
16. Eckenstein F, Baughman RW. 1984. Two types of cholinergic innervation in cortex, one colocalized with vasoactive intestinal polypeptide. Nature 309:153-155.
17. Fairén A, DeFelipe J, Regidor J. 1984. Nonpyramidal neurons. General account. In: Cerebral cortex. Vol. 1. Cellular components of the cerebral cortex. New York: Plenum Press.
18. Fallon JH, Leslie FM. 1986. Distribution of dynorphin and enkephalin peptides in the rat brain. J Comp Neurol 249:293-336.
19. Férézou I, Hill EL, Cauli B, Gibelin N, Kaneko T, Rossier J, Lambolez B. 2007. Extensive overlap of mu-opioid and nicotinic sensitivity in cortical interneurons. Cereb Cortex 17:1948-1957.
20. Franklin KBJ, Paxinos G. 2008. The mouse brain, 3rd ed. New York: Academic Press.
21. Furuta T, Kaneko T, Deschênes M. 2009. Septal neurons in barrel cortex derive their receptive field input from the lemniscal pathway. J Neurosci 29:4089-4095.
22. Ge SN, Ma YF, Hioki H, Wei YY, Kaneko T, Mizuno N, Gao GD, Li JL. 2010. Coexpression of VGLUT1 and VGLUT2 in trigeminothalamic projection neurons in the principal sensory trigeminal nucleus of the rat. J Comp Neurol 518:3149-3168.
23. Glavas MM, Grayson BE, Allen SE, Copp DR, Smith MS, Cowley MA, Grove KL. 2008. Characterization of brainstem peptide YY (PYY) neurons. J Comp Neurol 506:194-210.
24. Goldberg JH, Lacefield CO, Yuste R. 2004. Global dendritic calcium spikes in mouse layer 5 low threshold spiking interneurones: implications for control of pyramidal cell bursting. J Physiol 558:465-478.
25. Gonchar Y, Burkhalter A. 1997. Three distinct families of GABAergic neurons in rat visual cortex. Cereb Cortex 7:347-358.
26. Gonchar Y, Wang Q, Burkhalter A. 2007. Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front Neuroanat 1:1-11.
27. Goodman RR, Snyder SH. 1982. Kappa opiate receptors localized by autoradiography to deep layers of cerebral cortex: relation to sedative effects. Proc Natl Acad Sci U S A 79:5703-5707.
28. Guillery RW. 2002. On counting and counting errors. J Comp Neurol 447:1-7.
29. Hackney CM, Mahendrasingam S, Penn A, Fettiplace R. 2005. The concentrations of calcium buffering proteins in mammalian cochlear hair cells. J Neurosci 25:7867-7875.
30. Helboe L, Hay-Schmidt A, Stidsen CE, Møller M. 1999. Immunohistochemical localization of the somatostatin receptor subtype 2 (sst2) in the central nervous system of the golden hamster (Mesocricetus auratus). J Comp Neurol 405:247-261.
31. Hendry SH, Jones EG, Emson PC. 1984. Morphology, distribution, and synaptic relations of somatostatin- and neuropeptide Y-immunoreactive neurons in rat and monkey neocortex. J Neurosci 4:2497-2517.
32. Hioki H, Nakamura H, Ma Y-F, Konno M, Hayakawa T, Nakamura KC, Fujiyama F, Kaneko T. 2010. Vesicular glutamate transporter 3-expressing nonserotonergic projection neurons constitute a subregion in the rat midbrain raphe nuclei. J Comp Neurol 518:668-686.
33. Hioki H, Okamoto S, Konno M, Kameda H, Sohn J, Kuramoto E, Fujiyama F, Kaneko T. 2013. Cell type-specific inhibitory inputs to dendritic and somatic compartments of parvalbumin-expressing neocortical interneuron. J Neurosci 33:544-555.
34. Hökfelt T, Dahlström A. 1971. Effects of two mitosis inhibitors (colchicine and vinblastine) on the distribution and axonal transport of noradrenaline storage particles, studied by fluorescence and electron microscopy. Z Zellforsch 119:460-482.
35. Höllt V. 1983. Multiple endogenous opioid peptides. Trends Neurosci 6:24-26.
36. Janecka A, Fichna J, Janecki T. 2004. Opioid receptors and their ligands. Curr Top Med Chem 4:1-17.
37. Kawaguchi Y, Kondo S. 2002. Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J Neurocytol 31:277-287.
38. Kawaguchi Y, Kubota Y. 1996. Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J Neurosci 16:2701-2715.
39. Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476-486.
40. Kawaguchi Y, Kubota Y. 1998. Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 85:677-701.
41. Kosaka T, Heizmann CW, Tateishi K, Hamaoka Y, Hama K. 1987. An aspect of the organizational principle of the gamma-aminobutyric acidergic system in the cerebral cortex. Brain Res 409:403-408.
42. Kubota Y, Kawaguchi Y. 1997. Two distinct subgroups of cholecystokinin-immunoreactive cortical interneurons. Brain Res 752:175-183.
43. Kubota Y, Hattori R, Yui Y. 1994. Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res 649:159-173.
44. Kubota Y, Shigematsu N, Karube F, Sekigawa A, Kato S, Yamaguchi N, Hirai Y, Morishima M, Kawaguchi Y. 2011. Selective coexpression of multiple chemical markers defines discrete populations of neocortical GABAergic neurons. Cereb Cortex 21:1803-1817.
45. Kuramoto E, Furuta T, Nakamura KC, Unzai T, Hioki H, Kaneko T. 2009. Two types of thalamocortical projections from the motor thalamic nuclei of the rat: a single neuron tracing study using viral vectors. Cereb Cortex 9:2065-2077.
46. Lee T, Kaneko T, Taki K, Mizuno N. 1997. Preprodynorphin-, preproenkephalin-, and preprotachykinin-expressing neurons in the rat neostriatum: an analysis by immunocytochemistry and retrograde tracing. J Comp Neurol 386:229-244.
47. Lorente de Nó R. 1992. The cerebral cortex of the mouse (a first contribution-the "acoustic" cortex). Somatosens Mot Res 9:3-36 (first published in Trabajos del Laboratorio de Investigaciones Biológicas de la Universidad de Madrid 20:41-78, 1922).
48. Ma Y, Hu H, Berrebi AS, Mathers PH, Agmon A. 2006. Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci 26:5069-5082.
49. Ma Y, Hioki H, Konno M, Pan S, Nakamura H, Nakamura KC, Furuta T, Li J-L, Kaneko T. 2011. Expression of gap junction protein connexin36 in multiple subtypes of GABAergic neurons in adult rat somatosensory cortex. Cereb Cortex 21:2539-2549.
50. Mansour A, Khachaturian H, Lewis ME, Akil H, Watson SJ. 1988. Anatomy of CNS opioid receptors. Trends Neurosci 11:308-314.
51. Mansour A, Fox CA, Burke S, Meng F, Thompson RC, Akil H, Watson SJ. 1994a. Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J Comp Neurol 350:412-438.
52. Mansour A, Fox CA, Meng F, Akil H, Watson SJ. 1994b. Kappa 1 receptor mRNA distribution in the rat CNS: comparison to kappa receptor binding and prodynorphin mRNA. Mol Cell Neurosci 5:124-144.
53. Mansour A, Fox CA, Akil H, Watson SJ. 1995a. Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci 18:22-29.
54. Mansour A, Hoversten MT, Taylor LP, Watson SJ, Akil H. 1995b. The cloned mu, delta and kappa receptors and their endogenous ligands: evidence for two opioid peptide recognition cores. Brain Res 700:89-98.
55. Marinelli S, Pacioni S, Bisogno T, Di Marzo V, Prince DA, Huguenard JR, Bacci A. 2008. The endocannabinoid 2-arachidonoylglycerol is responsible for the slow self-inhibition in neocortical interneurons. J Neurosci 28:13532-13541.
56. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.
57. McGinty JF, van der Kooy D, Bloom FE. 1984. The distribution and morphology of opioid peptide immunoreactive neurons in the cerebral cortex of rats. J Neurosci 4:1104-1117.
58. Meis S. 2003. Nociceptin/orphanin FQ: actions within the brain. Neuroscientist 9:158-168.
59. Meng F, Xie GX, Thompson RC, Mansour A, Goldstein A, Watson SJ, Akil H. 1993. Cloning and pharmacological characterization of a rat kappa opioid receptor. Proc Natl Acad Sci U S A 90:9954-9958.
60. Merchenthaler I, Maderdrut JL, Cianchetta P, Shughrue P, Bronstein D. 1997. In situ hybridization histochemical localization of prodynorphin messenger RNA in the central nervous system of the rat. J Comp Neurol 384:211-232.
61. Minami M, Hosoi Y, Toya T, Katao Y, Maekawa K, Katsumata S, Yabuuchi K, Onogi T, Satoh M. 1993. In situ hybridization study of kappa-opioid receptor mRNA in the rat brain. Neurosci Lett 162:161-164.
62. Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J, Johnson JE, Machold RP, Fishell G. 2010. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 30:1582-1594.
63. Nakamura K, Watakabe A, Hioki H, Fujiyama F, Tanaka Y, Yamamori T, Kaneko T. 2007. Transiently increased colocalization of vesicular glutamate transporters 1 and 2 at single axon terminals during postnatal development of mouse neocortex: a quantitative analysis with correlation coefficient. Eur J Neurosci 26:3054-3067.
64. Ohno S, Kuramoto E, Furuta T, Hioki H, Tanaka YR, Fujiyama F, Sonomura T, Uemura M, Sugiyama K, Kaneko T. 2011. Morphological analysis of thalamocortical axon fibers of rat posterior thalamic nuclei: a single neuron tracing study with viral vectors. Cereb Cortex 22:2840-2857.
65. Papadopoulos GC, Parnavelas JG, Cavanagh ME. 1987. Extensive co-existence of neuropeptides in the rat visual cortex. Brain Res 420:95-99.
66. Perrenoud Q, Geoffroy H, Gauthier B, Rancillac A, Alfonsi F, Kessaris N, Rossier J, Vitalis T, Gallopin T. 2012. Characterization of type I and type II nNOS-expressing interneurons in the barrel cortex of mouse. Front Neural Circuits 6:36.
67. Reubi JC, Maurer R. 1985. Autoradiographic mapping of somatostatin receptors in the rat central nervous system and pituitary. Neuroscience 15:1183-1193.
68. Rogers JH. 1992. Immunohistochemical markers in rat cortex: co-localization of calretinin and calbindin-D28k with neuropeptides and GABA. Brain Res 587:147-157.
69. Sato M, Morita Y, Saika T, Fujita M, Ohhata K, Tohyama M. 1991. Localization and ontogeny of cells expressing preprodynorphin mRNA in the rat cerebral cortex. Brain Res 541:41-49.
70. Schindler M, Sellers LA, Humphrey PP, Emson PC. 1997. Immunohistochemical localization of the somatostatin SST2(A) receptor in the rat brain and spinal cord. Neuroscience 76:225-240.
71. Schindler M, Humphrey PP, Löhrke S, Friauf E. 1999. Immunohistochemical localization of the somatostatin sst2(b) receptor splice variant in the rat central nervous system. Neuroscience 90:859-874.
72. Sohn J, Hioki H, Okamoto S, Kaneko T. 2012. Preprodynorphin-producing neocortical interneurons constitute a subpopulation of somatostatin-expressing neurons. Soc Neurosci Abs PDFs 377.20.
73. Standifer KM, Pasternak GW. 1997. G proteins and opioid receptor-mediated signalling. Cell Signal 9:237-248.
74. Steiner DF, Docherty K, Carroll R. 1984. Golgi/granule processing of peptide hormone and neuropeptide precursors: a minireview. J Cell Biochem 24:121-130.
75. Suzuki N, Bekkers JM. 2010. Inhibitory neurons in the anterior piriform cortex of the mouse: classification using molecular markers. J Comp Neurol 518:1670-1687.
76. Taki K, Kaneko T, Mizuno N. 2000. A group of cortical interneurons expressing mu-opioid receptor-like immunoreactivity: a double immunofluorescence study in the rat cerebral cortex. Neuroscience 98:221-231.
77. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T. 2003. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60-79.
78. Toledo-Rodriguez M, Goodman P, Illic M, Wu C, Markram H. 2005. Neuropeptide and calcium-binding protein gene expression profiles predict neuronal anatomical type in the juvenile rat. J Physiol 567:401-413.
79. Tomioka R, Okamoto K, Furuta T, Fujiyama F, Iwasato T, Yanagawa Y, Obata K, Kaneko T, Tamamaki N. 2005. Demonstration of long-range GABAergic connections distributed throughout the mouse neocortex. Eur J Neurosci 21:1587-1600.
80. Uematsu M, Hirai Y, Karube F, Ebihara S, Kato M, Abe K, Obata K, Yoshida S, Hirabayashi M, Yanagawa Y, Kawaguchi Y. 2008. Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats. Cereb Cortex 18:315-330.
81. Van De Werd HJJM, Rajkowska G, Evers P, Uylings HBM. 2010. Cytoarchitectonic and chemoarchitectonic characterization of the prefrontal cortical areas in the mouse. Brain Struct Funct 214:339-353.
82. 8-somatostatin binding in sst1- to sst4- and SRIF-gene-invalidated mouse brain. Naunyn Schmiedebergs Arch Pharmacol 367:562-571.
83. Viollet C, Lepousez G, Loudes C, Videau C, Simon A, Epelbaum J. 2008. Somatostatinergic systems in brain: networks and functions. Mol Cell Endocrinol 286:75-87.
84. Wang Y, Toledo-Rodriguez M, Gupta A, Wu C, Silberberg G, Luo J, Markram H. 2004. Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J Physiol 561:65-90.
85. Wyszynski M, Kharazia V, Shanghvi R, Rao A, Beggs AH, Craig AM, Weinberg R, Sheng M. 1998. Differential regional expression and ultrastructural localization of alpha-actinin-2, a putative NMDA receptor-anchoring protein, in rat brain. J Neurosci 18:1383-1392.
86. Xu H, Jeong HY, Tremblay R, Rudy B. 2013. Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron 77:155-167.
87. Xu X, Roby KD, Callaway EM. 2006. Mouse cortical inhibitory neuron type that coexpress somatostatin and calretinin. J Comp Neurol 499:144-160.
88. Xu X, Roby KD, Callaway EM. 2010. Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J Comp Neurol 518:389-404.
89. Yasuda K, Raynor K, Kong H, Breder CD, Takeda J, Reisine T, Bell GI. 1993. Cloning and functional comparison of kappa and delta opioid receptors from mouse brain. Proc Natl Acad Sci U S A 90:6736-6740.
90. Zhao Y, Flandin P, Long JE, Cuesta MD, Westphal H, Rubenstein JL. 2008. Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants. J Comp Neurol 510:79-99.