Guidepost neurons for the lateral olfactory tract: Expression of metabotropic glutamate receptor 1 and innervation by glutamatergic olfactory bulb axons

Developmental Neurobiology

Volumn 72, Issue 12, 2012, Pages 1559-1576

  Hirata, Tatsumi ^a,b   Kumada, Tatsuro ^c   Kawasaki, Takahiko ^a,b   Furukawa, Tomonori ^c   Aiba, Atsu ^d   Conquet, François ^e,f   Saga, Yumiko ^a   Fukuda, Atsuo ^c  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e GlaxoSmithKline   (Switzerland)

^f MERCK SERONO S A   (Switzerland)

Author keywords

Activity dependent development; Axon gui dance; Calcium ion; Glutamatergic excitatory neuron; Guidepost neuron

Indexed keywords

IONOTROPIC RECEPTOR; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR AGONIST;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; MOUSE; NEOCORTEX; NERVE FIBER; NEUROTRANSMISSION; NONHUMAN; OLFACTORY BULB; OLFACTORY TRACT; PRIORITY JOURNAL;

ANIMALS; CELL COMMUNICATION; CELLS, CULTURED; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED ICR; NEUROGENESIS; NEURONS; OLFACTORY BULB; OLFACTORY PATHWAYS; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPTIC TRANSMISSION; TRANSFECTION;

EID: 84868554801     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22030     Document Type: Article

References (86)

1. Abe T, Sugihara H, Nawa H, Shigemoto R, Mizuno N, Nakanishi S. 1992. Molecular characterization of a novel metabotropic glutamate receptor mGluR5 coupled to inositol phosphate/Ca2+ signal transduction. J Biol Chem 267: 13361-13368.
2. Aiba A, Chen C, Herrup K, Rosenmund C, Stevens CF, Tonegawa S. 1994a. Reduced hippocampal long-term potentiation and context-specific deficit in associative learning in mGluR1 mutant mice. Cell 79: 365-375.
3. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, et al. 1994b. Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79: 377-388.
4. Allendoerfer KL, Shatz CJ. 1994. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu Rev Neurosci 17: 185-218.
5. Amphoux A, Vialou V, Drescher E, Bruss M, Mannoury La Cour C, Rochat C, Millan MJ, et al. 2006. Differential pharmacological in vitro properties of organic cation transporters and regional distribution in rat brain. Neuropharmacology 50: 941-952.
6. Behar TN, Scott CA, Greene CL, Wen X, Smith SV, Maric D, Liu QY, et al. 1999. Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J Neurosci 19: 4449-4461.
7. Catalano SM, Shatz CJ. 1998. Activity-dependent cortical target selection by thalamic axons. Science 281: 559-562.
8. Chan WY, Soloviev MM, Ciruela F, McIlhinney RA. 2001. Molecular determinants of metabotropic glutamate receptor 1B trafficking. Mol Cell Neurosci 17: 577-588.
9. Chowdhury TG, Jimenez JC, Bomar JM, Cruz-Martin A, Cantle JP, Portera-Cailliau C. 2010. Fate of cajal-retzius neurons in the postnatal mouse neocortex. Front Neuroanat 4: 10.
10. Chun JJM, Shatz CJ. 1989. Interstitial cells of the adult neocortical white matter are the remnant of the early generated subplate neuron population. J Comp Neurol 282: 555-569.
11. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, et al. 1994. Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372: 237-243.
12. Del Río JA, Heimrich B, Borrell V, Förster E, Drakew A, Alcántara S, Nakajima K, et al. 1997. A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 385: 70-74.
13. Del Rio JA, Heimrich B, Super H, Borrell V, Frotscher M, Soriano E. 1996. Differential survival of Cajal-Retzius cells in organotypic cultures of hippocampus and neocortex. J Neurosci 16: 6896-6907.
14. Del Rio JA, Martinez A, Fonseca M, Auladell C, Soriano E. 1995. Glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the murine cortex as identified with calretinin antibody. Cereb Cortex 5: 13-21.
15. 2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron 36: 1051-1061.
16. Derer P, Caviness VSJr., Sidman RL. 1977. Early cortical histogenesis in the primary olfactory cortex of the mouse. Brain Res 123: 27-40.
17. Derer P, Derer M. 1990. Cajal-Retzius cells ontogenesis and death in mouse brain visualized with horseradish peroxidase and electron microscopy. Neuroscience 36: 839-856.
18. Engel K, Zhou M, Wang J. 2004. Identification and characterization of a novel monoamine transporter in the human brain. J Biol Chem 279: 50042-50049.
19. Flint AC, Dammerman RS, Kriegstein AR. 1999. Endogenous activation of metabotropic glutamate receptors in neocortical development causes neuronal calcium oscillations. Proc Natl Acad Sci USA 96: 12144-12149.
20. Fouquet C, Di Meglio T, Ma L, Kawasaki T, Long H, Hirata T, Tessier-Lavigne M, et al. 2007. Robo1 and robo2 control the development of the lateral olfactory tract. J Neurosci 27: 3037-3045.
21. Francesconi A, Duvoisin RM. 2002. Alternative splicing unmasks dendritic and axonal targeting signals in metabotropic glutamate receptor 1. J Neurosci 22: 2196-2205.
22. Friauf E, McConnell SK, Shatz CJ. 1990. Functional synaptic circuits in the subplate during fetal and early postnatal development of cat visual cortex. J Neurosci 10: 2601-2613.
23. Ghosh A, Antonini A, McCornnell SK, Shatz CJ. 1990. Requirement for subplate neurons in the formation of thalamocortical connections. Nature 347: 179-181.
24. Ghosh A, Shatz CJ. 1992a. Involvement of subplate neurons in the formation of ocular dominance columns. Science 255: 1441-1443.
25. Ghosh A, Shatz CJ. 1992b. Pathfinding and target selection by developing geniculocortical axons. J Neurosci 12: 39-55.
26. Ghosh A, Shatz CJ. 1993. A role for subplate neurons in the patterning of connections from thalamus to neocortex. Development 117: 1031-1047.
27. Ghosh S, Larson SD, Hefzi H, Marnoy Z, Cutforth T, Dokka K, Baldwin KK. 2011. Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 472.
28. Grundemann D, Schechinger B, Rappold GA, Schomig E. 1998. Molecular identification of the corticosterone-sensitive extraneuronal catecholamine transporter. Nat Neurosci 1: 349-351.
29. Haberly LB, Hansen DJ, Feig SL, Presto S. 1987. Distribution and ultrastructure of neurons in opossum piriform cortex displaying immunoreactivity to GABA and GAD and high-affinity tritiated GABA uptake. J Comp Neurol 266: 269-290.
30. Hanganu IL, Kilb W, Luhmann HJ. 2002. Functional synaptic projections onto subplate neurons in neonatal rat somatosensory cortex. J Neurosci 22: 7165-7176.
31. Herrmann K, Antonini A, Shatz CJ. 1994. Ultrastructural evidence for synaptic interactions between thalamocortical axons and subplate neurons. Eur J Neurosci 6: 1729-1742.
32. Hevner RF, Shi L, Justice N, Hsueh Y, Sheng M, Smiga S, Bulfone A, et al. 2001. Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29: 353-366.
33. Hirata T, Fujisawa H. 1999. Environmental control of collateral branching and target invasion of mitral cell axons during development. J Neurobiol 38: 93-104.
34. Houamed KM, Kuijper JL, Gilbert TL, Haldeman BA, O'Hara PJ, Mulvihill ER, Almers W, et al. 1991. Cloning, expression, and gene structure of a G protein-coupled glutamate receptor from rat brain. Science 252: 1318-1321.
35. Ichise T, Kano M, Hashimoto K, Yanagihara D, Nakao K, Shigemoto R, Katsuki M, et al. 2000. mGluR1 in cerebellar Purkinje cells essential for long-term depression, synapse elimination, and motor coordination. Science 288: 1832-1835.
36. - homeostasis contributes to differential GABAergic actions between developing rat visual cortex and dorsal lateral geniculate nucleus. Brain Res 984: 149-159.
37. Imamura F, Ayoub AE, Rakic P, Greer CA. 2011. Timing of neurogenesis is a determinant of olfactory circuitry. Nat Neurosci 14: 331-337.
38. Inaki K, Nishimura S, Nakashiba T, Itohara S, Yoshihara Y. 2004. Laminar organization of the developing lateral olfactory tract revealed by differential expression of cell recognition molecules. J Comp Neurol 479: 243-256.
39. Ito K, Kawasaki T, Takashima S, Matsuda I, Aiba A, Hirata T. 2008. Semaphorin 3F confines ventral tangential migration of lateral olfactory tract neurons onto the telencephalon surface. J Neurosci 28: 4414-4422.
40. Kano M, Hashimoto K, Chen C, Abeliovich A, Aiba A, Kurihara H, Watanabe M, et al. 1995. Impaired synapse elimination during cerebellar development in PKC gamma mutant mice. Cell 83: 1223-1231.
41. Kawabata S, Kohara A, Tsutsumi R, Itahana H, Hayashibe S, Yamaguchi T, Okada M. 1998. Diversity of calcium signaling by metabotropic glutamate receptors. J Biol Chem 273: 17381-17385.
42. Kawabata S, Tsutsumi R, Kohara A, Yamaguchi T, Nakanishi S, Okada M. 1996. Control of calcium oscillations by phosphorylation of metabotropic glutamate receptors. Nature 383: 89-92.
43. Kawakami A, Kitsukawa T, Takagi S, Fujisawa H. 1996. Developmentally regulated expression of a cell surface protein, neuropilin, in the mouse nervous system. J Neurobiol 29: 1-17.
44. Kawasaki T, Ito K, Hirata T. 2006. Netrin 1 regulates ventral tangential migration of guidepost neurons in the lateral olfactory tract. Development 133: 845-853.
45. Kawasaki T, Takagi Y, Yamatani H, Hirata T. 2005. Systematic screening and identification of antigens recognized by monoclonal antibodies raised against the developing lateral olfactory tract. J Neurobiol 62: 330-340.
46. 2+ transients control CNS neuronal migration. Cell Calcium 37: 387-393.
47. Komuro H, Rakic P. 1993. Modulation of neuronal migration by NMDA receptors. Science 260: 95-97.
48. Kostovic I, Rakic P. 1990. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 297: 441-470.
49. Kreibich TA, Chalasani SH, Raper JA. 2004. The neurotransmitter glutamate reduces axonal responsiveness to multiple repellents through the activation of metabotropic glutamate receptor 1. J Neurosci 24: 7085-7095.
50. 2+ transients. Proc Natl Acad Sci USA 101: 8479-8484.
51. Lopez-Bendito G, Cautinat A, Sanchez JA, Bielle F, Flames N, Garratt AN, Talmage DA, et al. 2006. Tangential neuronal migration controls axon guidance: A role for neuregulin-1 in thalamocortical axon navigation. Cell 125: 127-142.
52. Lopez-Bendito G, Shigemoto R, Fairen A, Lujan R. 2002. Differential distribution of group I metabotropic glutamate receptors during rat cortical development. Cereb Cortex 12: 625-638.
53. Macdonald R, Xu Q, Barth KA, Mikkola I, Holder N, Fjose A, Krauss S, et al. 1994. Regulatory gene expression boundaries demarcate sites of neuronal differentiation in the embryonic zebrafish forebrain. Neuron 13: 1039-1053.
54. Manent JB, Demarque M, Jorquera I, Pellegrino C, Ben-Ari Y, Aniksztejn L, Represa A. 2005. A noncanonical release of GABA and glutamate modulates neuronal migration. J Neurosci 25: 4755-4765.
55. Manent JB, Jorquera I, Ben-Ari Y, Aniksztejn L, Represa A. 2006. Glutamate acting on AMPA but not NMDA receptors modulates the migration of hippocampal interneurons. J Neurosci 26: 5901-5909.
56. Martin LJ, Blackstone CD, Huganir RL, Price DL. 1992. Cellular localization of a metabotropic glutamate receptor in rat brain. Neuron 9: 259-270.
57. Martinez-Galan JR, Lopez-Bendito G, Lujan R, Shigemoto R, Fairen A, Valdeolmillos M. 2001. Cajal-Retzius cells in early postnatal mouse cortex selectively express functional metabotropic glutamate receptors. Eur J Neurosci 13: 1147-1154.
58. Masu M, Tanabe Y, Tsuchida K, Shigemoto R, Nakanishi S. 1991. Sequence and expression of a metabotropic glutamate receptor. Nature 349: 760-765.
59. Matsugami TR, Tanemura K, Mieda M, Nakatomi R, Yamada K, Kondo T, Ogawa M, et al. 2006. From the Cover: Indispensability of the glutamate transporters GLAST and GLT1 to brain development. Proc Natl Acad Sci USA 103: 12161-12166.
60. Metin C, Deleglise D, Serafini T, Kennedy TE, Tessier-Lavigne M. 1997. A role for netrin-1 in the guidance of cortical efferents. Development 124: 5063-5074.
61. Metin C, Godement P. 1996. The ganglionic eminence may be an intermediate target for corticofugal and thalamocortical axons. J Neurosci 16: 3219-3235.
62. Mienville JM, Pesold C. 1999. Low resting potential and postnatal upregulation of NMDA receptors may cause Cajal-Retzius cell death. J Neurosci 19: 1636-1646.
63. Miyamichi K, Amat F, Moussavi F, Wang C, Wickersham I, Wall NR, Taniguchi H, et al. 2011. Cortical representations of olfactory input by trans-synaptic tracing. Nature 472: 191-196.
64. Nakanishi S. 1994. Metabotropic glutamate receptors: Synaptic transmission, modulation, and plasticity. Neuron 13: 1031-1037.
65. Niwa H, Yamamura K-I, Miyazaki J-I. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-200.
66. Nomura T, Holmberg J, Frisen J, Osumi N. 2006. Pax6-dependent boundary defines alignment of migrating olfactory cortex neurons via the repulsive activity of ephrin A5. Development 133: 1335-1345.
67. Pin JP, Duvoisin R. 1995. The metabotropic glutamate receptors: Structure and functions. Neuropharmacology 34: 1-26.
68. Sato Y, Hirata T, Ogawa M, Fujisawa H. 1998. Requirement for early-generated neurons recognized by monoclonal antibody lot1 in the formation of lateral olfactory tract. J Neurosci 18: 7800-7810.
69. Shigemoto R, Nakanishi S, Mizuno N. 1992. Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: An in situ hybridization study in adult and developing rat. J Comp Neurol 322: 121-135.
70. Simonian SX, Herbison AE. 2001. Differing, spatially restricted roles of ionotropic glutamate receptors in regulating the migration of gnrh neurons during embryogenesis. J Neurosci 21: 934-943.
71. Smitt PS, Kinoshita A, De Leeuw B, Moll W, Coesmans M, Jaarsma D, Henzen-Logmans S, et al. 2000. Paraneoplastic cerebellar ataxia due to autoantibodies against a glutamate receptor. N Engl J Med 342: 21-27.
72. Soloviev MM, Ciruela F, Chan WY, McIlhinney RA. 1999. Identification, cloning and analysis of expression of a new alternatively spliced form of the metabotropic glutamate receptor mGluR1 mRNA1. Biochim Biophys Acta 1446: 161-166.
73. Sosulski DL, Lissitsyna Bloom M, Cutforth T, Axel R, Datta SR. 2011. Distinct representations of olfactory information in different cortical centres. Nature 472: 217-220.
74. Sretavan DW, Feng L, Pure E, Reichardt LF. 1994. Embryonic neurons of the developing optic chiasm express L1 and CD44, cell surface molecules with opposing effects on retinal axon growth. Neuron 12: 957-975.
75. Sretavan DW, Puré E, Siegel MW, Reichardt LF. 1995. Disruption of retinal axon ingrowth by ablation of embryonic mouse optic chiasm neurons. Science 269: 98-101.
76. Stokes CC, Isaacson JS. 2010. From dendrite to soma: dynamic routing of inhibition by complementary interneuron microcircuits in olfactory cortex. Neuron 67: 452-465.
77. Sugisaki N, Hirata T, Naruse I, Kawakami A, Kitsukawa T, Fujisawa H. 1996. Positional cues that are strictly localized in the telencephalon induce preferential growth of mitral cell axons. J Neurobiol 29: 127-137.
78. Super H, Martinez A, Del Rio JA, Soriano E. 1998. Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus. J Neurosci 18: 4616-4626.
79. Supèr H, Martínez A, Soriano E. 1997. Degeneration of Cajal-Retzius cells in the developing cerebral cortex of the mouse after ablation of meningeal cells by 6-hydroxydopamine. Dev Brain Res 98: 15-20.
80. Tanabe Y, Masu M, Ishii T, Shigemoto R, Nakanishi S. 1992. A family of metabotropic glutamate receptors. Neuron 8: 169-179.
81. Tomioka N, Osumi N, Sato Y, Inoue T, Nakamura S, Fujisawa H, Hirata T. 2000. Neocortical origin and tangential migration of guidepost neurons in the lateral olfactory tract. J Neurosci 20: 5802-5812.
82. Uemura M, Nakao S, Suzuki ST, Takeichi M, Hirano S. 2007. OL-protocadherin is essential for growth of striatal axons and thalamocortical projections. Nat Neurosci 10: 1151-1159.
83. Valverde F, Facal-Valverde MV. 1988. Postnatal development of interstitial (subplate) cells in the white matter of the temporal cortex of kittens: A correlated Golgi and electron microscopic study. J Comp Neurol 269: 168-192.
84. Yamatani H, Kawasaki T, Mita S, Inagaki N, Hirata T. 2010. Proteomics analysis of the temporal changes in axonal proteins during maturation. Dev Neurobiol 70: 523-537.
85. Yamatani H, Sato Y, Fujisawa H, Hirata T. 2004. Chronotopic organization of olfactory bulb axons in the lateral olfactory tract. J Comp Neurol 475: 247-260.
86. Yozu M, Tabata H, Konig N, Nakajima K. 2008. Migratory behavior of presumptive interneurons is affected by AMPA receptor activation in slice cultures of embryonic mouse neocortex. Dev Neurosci 30: 105-116.