The ratio of 'deleted in colorectal cancer' to 'uncoordinated-5A' netrin-1 receptors on the growth cone regulates mossy fibre directionality

Brain

Volumn 133, Issue 1, 2010, Pages 60-75

  Muramatsu, Rieko ^a   Nakahara, Soichiro ^a   Ichikawa, Junya ^a   Watanabe, Keisuke ^b   Matsuki, Norio ^a   Koyama, Ryuta ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Axon guidance; Granule cell; Hippocampus; Slice culture; Temporal lobe epilepsy

Indexed keywords

CYCLIC AMP; GREEN FLUORESCENT PROTEIN; MEMBRANE RECEPTOR; NETRIN 1; NETRIN 1 ANTIBODY; NETRIN 1 RECEPTOR; PROTEIN ANTIBODY; UNCLASSIFIED DRUG; UNCOORDINATED 5A RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; COLORECTAL CANCER; CONTROLLED STUDY; GRANULE CELL; GROWTH CONE; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; MOSSY FIBER; NERVE EXCITABILITY; NERVE FIBER; NERVE PROJECTION; NERVE SPROUTING; NEUROPATHOLOGY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TARGET CELL; TEMPORAL LOBE EPILEPSY;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; COCULTURE TECHNIQUES; CYCLIC AMP; GROWTH CONES; MOSSY FIBERS, HIPPOCAMPAL; NERVE GROWTH FACTORS; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 74249114412     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awp266     Document Type: Article

References (78)

1. Amaral DG, Scharfman HE, Lavenex P. The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 2007; 163: 3-22.
2. Andersen P, Bliss TV, Lomo T, Olsen LI, Skrede KK. Lamellar organization of hippocampal excitatory pathways. Acta Physiol Scand 1969; 76: 4A-5A.
3. Barallobre MJ, Del Rio JA, Alcantara S, Borrell V, Aguado F, Ruiz M, et al. Aberrant development of hippocampal circuits and altered neural activity in netrin 1-deficient mice. Development 2000; 127: 4797-4810
4. Barnes G, Puranam RS, Luo Y, McNamara JO. Temporal specific patterns of semaphorin gene expression in rat brain after kainic acid-induced status epilepticus. Hippocampus 2003; 13: 1-20.
5. Bartoe JL, McKenna WL, Quan TK, Stafford BK, Moore JA, Xia J, et al. Protein interacting with C-kinase 1/protein kinase Calpha-mediated endocytosis converts netrin-1-mediated repulsion to attraction. J Neurosci 2006; 26: 3192-3205
6. Bausch SB, McNamara JO. Contributions of mossy fiber and CA1 pyramidal cell sprouting to dentate granule cell hyperexcitability in kainic acid-treated hippocampal slice cultures. J Neurophysiol 2004; 92: 3582-3595
7. Blaabjerg M, Zimmer J. The dentate mossy fibers: structural organization, development and plasticity. Prog Brain Res 2007; 163: 85-107.
8. Bouchard JF, Horn KE, Stroh T, Kennedy TE. Depolarization recruits DCC to the plasma membrane of embryonic cortical neurons and enhances axon extension in response to netrin-1. J Neurochem 2008; 107: 398-417.
9. Buckmaster PS, Zhang GF, Yamawaki R. Axon sprouting in a model of temporal lobe epilepsy creates a predominantly excitatory feedback circuit. J Neurosci 2002; 22: 6650-6658
10. Cavazos JE, Zhang P, Qazi R, Sutula TP. Ultrastructural features of sprouted mossy fiber synapses in kindled and kainic acid-treated rats. J Comp Neurol 2003; 458: 272-292
11. Cavazos JE, Jones SM, Cross DJ. Sprouting and synaptic reorganization in the subiculum and CA1 region of the hippocampus in acute and chronic models of partial-onset epilepsy. Neuroscience 2004; 126: 677-688
12. Cronin J, Dudek FE. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res 1988; 474: 181-184
13. Cross DJ, Cavazos JE. Synaptic reorganization in subiculum and CA3 after early-life status epilepticus in the kainic acid rat model. Epilepsy Res 2007; 73: 156-65.
14. de la Torre JR, Hopker VH, Ming GL, Poo MM, Tessier-Lavigne M, Hemmati-Brivanlou A, et al. Turning of retinal growth cones in a netrin-1 gradient mediated by the netrin receptor DCC. Neuron 1997; 19: 1211-1224
15. Dailey ME, Buchanan J, Bergles DE, Smith SJ. Mossy fiber growth and synaptogenesis in rat hippocampal slices in vitro. J Neurosci 1994; 14: 1060-1078
16. El Bahh B, Lespinet V, Lurton D, Coussemacq M, Le Gal LS, Rougier A. Correlations between granule cell dispersion, mossy fiber sprouting, and hippocampal cell loss in temporal lobe epilepsy. Epilepsia 1999; 40: 1393-1401
17. Esclapez M, Hirsch JC, Ben Ari Y, Bernard C. Newly formed excitatory pathways provide a substrate for hyperexcitability in experimental temporal lobe epilepsy. J Comp Neurol 1999; 408: 449-460
18. Fagan KA, Graf RA, Tolman S, Schaack J, Cooper DM. Regulation of a Ca2+-sensitive adenylyl cyclase in an excitable cell. Role of voltage-gated versus capacitative Ca2+ entry. J Biol Chem 2000; 275: 40187-40194
19. Fan CM, Tessier-Lavigne M. Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog. Cell 1994; 79: 1175-1186
20. Fazeli A, Dickinson SL, Hermiston ML, Tighe RV, Steen RG, Small CG, et al. Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 1997; 386: 796-804.
21. Feng L, Molnar P, Nadler JV. Short-term frequency-dependent plasticity at recurrent mossy fiber synapses of the epileptic brain. J Neurosci 2003; 23: 5381-5390
22. Franck JE, Pokorny J, Kunkel DD, Schwartzkroin PA. Physiologic and morphologic characteristics of granule cell circuitry in human epileptic hippocampus. Epilepsia 1995; 36: 543-558
23. Holtmaat AJ, Gorter JA, De Wit J, Tolner EA, Spijker S, Giger RJ, et al. Transient downregulation of Sema3A mRNA in a rat model for temporal lobe epilepsy. A novel molecular event potentially contributing to mossy fiber sprouting. Exp Neurol 2003; 182: 142-150
24. Holz GG, Kang G, Harbeck M, Roe MW, Chepurny OG. Cell physiology of cAMP sensor Epac. J Physiol 2006; 577: 5-15.
25. Hong K, Hinck L, Nishiyama M, Poo MM, Tessier-Lavigne M, Stein E. A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 1999; 97: 927-941
26. Houser CR, Miyashiro JE, Swartz BE, Walsh GO, Rich JR, Delgado-Escueta AV. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J Neurosci 1990; 10: 267-282
27. Hu Y, Barzilai A, Chen M, Bailey CH, Kandel ER. 5-HT and cAMP induce the formation of coated pits and vesicles and increase the expression of clathrin light chain in sensory neurons of aplysia. Neuron 1993; 10: 921-929
28. Huber AB, Kolodkin AL, Ginty DD, Cloutier JF. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci 2003; 26: 509-563
29. Isokawa M, Levesque MF, Babb TL, Engel J Jr. Single mossy fiber axonal systems of human dentate granule cells studied in hippocampal slices from patients with temporal lobe epilepsy. J Neurosci 1993; 13: 1511-1522
30. Jope RS, Song L, Kolasa K. Inositol trisphosphate, cyclic AMP, and cyclic GMP in rat brain regions after lithium and seizures. Biol Psychiatry 1992; 31: 505-514
31. Kamiguchi H, Lemmon V. Recycling of the cell adhesion molecule L1 in axonal growth cones. J Neurosci 2000; 20: 3676-3686
32. Keleman K, Dickson BJ. Short-and long-range repulsion by the Drosophila Unc5 netrin receptor. Neuron 2001; 32: 605-617
33. Kennedy TE, Serafini T, de lT JR, Tessier-Lavigne M. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 1994; 78: 425-435 (Pubitemid 24250807)
34. Kim JA, Koyama R, Yamada RX, Yamada MK, Nishiyama N, Matsuki N, et al. Environmental control of the survival and differentiation of dentate granule neurons. Cereb Cortex 2004; 14: 1358-1364
35. Koyama R, Ikegaya Y. Mossy fiber sprouting as a potential therapeutic target for epilepsy. Curr Neurovasc Res 2004; 1: 3-10.
36. Koyama R, Yamada MK, Fujisawa S, Katoh-Semba R, Matsuki N, Ikegaya Y. Brain-derived neurotrophic factor induces hyperexcitable reentrant circuits in the dentate gyrus. J Neurosci 2004a; 24: 7215-7224
37. Koyama R, Yamada MK, Nishiyama N, Matsuki N, Ikegaya Y. Developmental switch in axon guidance modes of hippocampal mossy fibers in vitro. Dev Biol 2004b; 267: 29-42.
38. Koyama R, Muramatsu R, Sasaki T, Kimura R, Ueyama C, Tamura M, et al. A low-cost method for brain slice cultures. J Pharmacol Sci 2007; 104: 191-194
39. Lehmann TN, Gabriel S, Eilers A, Njunting M, Kovacs R, Schulze K, et al. Fluorescent tracer in pilocarpine-treated rats shows widespread aberrant hippocampal neuronal connectivity. Eur J Neurosci 2001; 14: 83-95.
40. Lynch M, Sutula T. Recurrent excitatory connectivity in the dentate gyrus of kindled and kainic acid-treated rats. J Neurophysiol 2000; 83: 693-704.
41. Masuda T, Watanabe K, Sakuma C, Ikenaka K, Ono K, Yaginuma H. Netrin-1 acts as a repulsive guidance cue for sensory axonal projections toward the spinal cord. J Neurosci 2008; 28: 10380-10385
42. Mello LE, Cavalheiro EA, Tan AM, Kupfer WR, Pretorius JK, Babb TL, et al. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 1993; 34: 985-995
43. Ming G, Henley J, Tessier-Lavigne M, Song H, Poo M. Electrical activity modulates growth cone guidance by diffusible factors. Neuron 2001; 29: 441-452
44. Ming GL, Song HJ, Berninger B, Holt CE, Tessier-Lavigne M, Poo MM. cAMP-dependent growth cone guidance by netrin-1. Neuron 1997; 19: 1225-1235
45. Mizuhashi S, Nishiyama N, Matsuki N, Ikegaya Y. Cyclic nucleotide-mediated regulation of hippocampal mossy fiber development: a target-specific guidance. J Neurosci 2001; 21: 6181-6194
46. Molnar P, Nadler JV. Mossy fiber-granule cell synapses in the normal and epileptic rat dentate gyrus studied with minimal laser photostimulation. J Neurophysiol 1999; 82: 1883-1894
47. Moore SW, Kennedy TE. Protein kinase A regulates the sensitivity of spinal commissural axon turning to netrin-1 but does not switch between chemoattraction and chemorepulsion. J Neurosci 2006; 26: 2419-2423
48. Moore SW, Lai Wing SK, Xie F, Barker PA, Conti M, Kennedy TE. Soluble adenylyl cyclase is not required for axon guidance to netrin-1. J Neurosci 2008a; 28: 3920-3924
49. Moore SW, Correia JP, Lai Wing SK, Pool M, Fournier AE, Kennedy TE. Rho inhibition recruits DCC to the neuronal plasma membrane and enhances axon chemoattraction to netrin 1. Development 2008b; 135: 2855-2864
50. Muller M, Gahwiler BH, Rietschin L, Thompson SM. Reversible loss of dendritic spines and altered excitability after chronic epilepsy in hippocampal slice cultures. Proc Natl Acad Sci USA 1993; 90: 257-261
51. Muramatsu R, Ikegaya Y, Matsuki N, Koyama R. Neonatally born granule cells numerically dominate adult mice dentate gyrus. Neuroscience 2007; 148: 593-598
52. Nakahara S, Tamura M, Matsuki N, Koyama R. Neuronal hyperactivity sustains the basal dendrites of immature dentate granule cells: time-lapse confocal analysis using hippocampal slice cultures. Hippocampus 2009; 19: 379-391
53. Nicol X, Voyatzis S, Muzerelle A, Narboux-Neme N, Sudhof TC, Miles R, et al. cAMP oscillations and retinal activity are permissive for ephrin signaling during the establishment of the retinotopic map. Nat Neurosci 2007; 10: 340-347
54. Okazaki MM, Evenson DA, Nadler JV. Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: visualization after retrograde transport of biocytin. J Comp Neurol 1995; 352: 515-534
55. Palm K, Belluardo N, Metsis M, Timmusk T. Neuronal expression of zinc finger transcription factor REST/NRSF/XBR gene. J Neurosci 1998; 18: 1280-1296
56. Pan E, Stringer JL. Role of potassium and calcium in the generation of cellular bursts in the dentate gyrus. J Neurophysiol 1997; 77: 2293-2299
57. Pleasure SJ, Collins AE, Lowenstein DH. Unique expression patterns of cell fate molecules delineate sequential stages of dentate gyrus development. J Neurosci 2000; 20: 6095-6105
58. Represa A, Robain O, Tremblay E, Ben Ari Y. Hippocampal plasticity in childhood epilepsy. Neurosci Lett 1989; 99: 351-355
59. Represa A, Ben Ari Y. Kindling is associated with the formation of novel mossy fibre synapses in the CA3 region. Exp Brain Res 1992; 92: 69-78.
60. Salin P, Tseng GF, Hoffman S, Parada I, Prince DA. Axonal sprouting in layer V pyramidal neurons of chronically injured cerebral cortex. J Neurosci 1995; 15: 8234-8245
61. Schlessinger AR, Cowan WM, Gottlieb DI. An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J Comp Neurol 1975; 159: 149-175
62. Schoenherr CJ, Anderson DJ. The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 1995; 267: 1360-1363
63. Serafini T, Kennedy TE, Galko MJ, Mirzayan C, Jessell TM, Tessier-Lavigne M. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 1994; 78: 409-424
64. Shetty AK, Zaman V, Hattiangady B. Repair of the injured adult hippocampus through graft-mediated modulation of the plasticity of the dentate gyrus in a rat model of temporal lobe epilepsy. J Neurosci 2005; 25: 8391-8401
65. Siddiqui AH, Joseph SA. CA3 axonal sprouting in kainate-induced chronic epilepsy. Brain Res 2005; 1066: 129-146
66. Smith BN, Dudek FE. Network interactions mediated by new excitatory connections between CA1 pyramidal cells in rats with kainate-induced epilepsy. J Neurophysiol 2002; 87: 1655-1658
67. Song HJ, Poo MM. Signal transduction underlying growth cone guidance by diffusible factors. Curr Opin Neurobiol 1999; 9: 355-363
68. Sutula T, Cascino G, Cavazos J, Parada I, Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 1989; 26: 321-330
69. Sutula T, Zhang P, Lynch M, Sayin U, Golarai G, Rod R. Synaptic and axonal remodeling of mossy fibers in the hilus and supragranular region of the dentate gyrus in kainate-treated rats. J Comp Neurol 1998; 390: 578-594
70. Vazquez-Lopez A, Sierra-Paredes G, Sierra-Marcuno G. Role of cAMP-dependent protein kinase on acute picrotoxin-induced seizures. Neurochem Res 2005; 30: 613-618
71. Watanabe K, Tamamaki N, Furuta T, Ackerman SL, Ikenaka K, Ono K. Dorsally derived netrin 1 provides an inhibitory cue and elaborates the 'waiting period' for primary sensory axons in the developing spinal cord. Development 2006; 133: 1379-1387
72. Wu KY, Zippin JH, Huron DR, Kamenetsky M, Hengst U, Buck J, et al. Soluble adenylyl cyclase is required for netrin-1 signaling in nerve growth cones. Nat Neurosci 2006; 9: 1257-1264 (Pubitemid 44454267)
73. Wuarin JP, Dudek FE. Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate-treated epileptic rats. J Neurosci 1996; 16: 4438-4448
74. Xia ZG, Refsdal CD, Merchant KM, Dorsa DM, Storm DR. Distribution of mRNA for the calmodulin-sensitive adenylate cyclase in rat brain: expression in areas associated with learning and memory. Neuron 1991; 6: 431-443
75. Yamada RX, Matsuki N, Ikegaya Y. cAMP differentially regulates axonal and dendritic development of dentate granule cells. J Biol Chem 2005; 280: 38020-38028
76. Yang F, Wang JC, Han JL, Zhao G, Jiang W. Different effects of mild and severe seizures on hippocampal neurogenesis in adult rats. Hippocampus 2008; 18: 460-468
77. Yuan XB, Jin M, Xu X, Song YQ, Wu CP, Poo MM, et al. Signalling and crosstalk of Rho GTPases in mediating axon guidance. Nat Cell Biol. 2003; 5: 38-45.
78. Zhao C, Teng EM, Summers RG Jr, Ming GL, Gage FH. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 2006; 26: 3-11.