Cadherin-8 and N-cadherin differentially regulate pre- and postsynaptic development of the hippocampal mossy fiber pathway

Hippocampus

Volumn 18, Issue 4, 2008, Pages 349-363

  Bekirov, Iddil H ^a   Nagy, Vanja ^a   Svoronos, Alexandra ^a   Huntley, George W ^a   Benson, Deanna L ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Axon guidance; Dendritic arborization; DG; Hippocampus; Synaptogenesis

Indexed keywords

CADHERIN; CADHERIN 8; NERVE CELL ADHESION MOLECULE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; DENDRITIC SPINE; GRANULE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MOSSY FIBER; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNAPTOGENESIS;

ANIMALS; ANIMALS, NEWBORN; CADHERINS; CELL ADHESION; CELL DIFFERENTIATION; CELL POLARITY; DENDRITES; GROWTH CONES; HIPPOCAMPUS; MOSSY FIBERS, HIPPOCAMPAL; NEURAL PATHWAYS; ORGAN CULTURE TECHNIQUES; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; SYNAPTIC MEMBRANES;

EID: 42149093906     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20395     Document Type: Article

References (99)

1. Amaral DG. 1979. Synaptic extensions from the mossy fibers of the fascia dentata. Anat Embryol (Berl) 155:241-251.
2. Amaral DG, Dent JA. 1981. Development of the mossy fibers of the dentate gyrus. I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195:51-86.
3. Andrews GL, Mastick GS. 2003. R-cadherin is a Pax6-regulated, growth-promoting cue for pioneer axons. J Neurosci 23:9873-9880.
4. Balsamo J, Lilien J. 1990. N-cadherin is stably associated with and is an acceptor for a cell surface N-acetylgalactosaminylphosphotransferase. J Biol Chem 265:2923-2928.
5. Bekirov IH. 2004. The role of classic cadherins in the development of hippocampal circuitry [Ph.D.]. New York: Mount Sinai School of Medicine of New York University. 107 p.
6. Bekirov IH, Needleman LA, Zhang W, Benson DL. 2002. Identification and localization of multiple classic cadherins in developing rat limbic system. Neuroscience 115:213-227.
7. Benson DL, Tanaka H. 1998. N-cadherin redistribution during synaptogenesis in hippocampal neurons. J. Neurosci 18:6892-6904.
8. Bixby JL, Zhang R. 1990. Purified N-cadherin is a potent substrate for the rapid induction of neurite outgrowth. J Cell Biol 110: 1253-1260.
9. Blaschuk OW, Sullivan R, David S, Pouliot Y. 1990. Identification of a cadherin cell adhesion recognition sequence. Dev Biol 139:227-229.
10. Bözdagi O, Shan W, Tanaka H, Benson DL, Huntley GW. 2000. Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites and required for potentiation. Neuron 28:245-259.
11. Bozdagi O, Valcin M, Poskanzer K, Tanaka H, Benson DL. 2004. Temporally distinct demands for classic cadherins in synapse formation and maturation. Mol Cell Neurosci 27:509-521.
12. Brady-Kalnay SM, Rimm DL, Tonks NK. 1995. Receptor protein tyrosine phosphatase PTPmu associates with cadherins and catenins in vivo. J Cell Biol 130:977-986.
13. Burden-Gulley SM, Brady-Kalnay SM. 1999. PTPmu regulates N-cadherin-dependent neurite outgrowth. J Cell Biol 144:1323-1336.
14. Butler CD, Schnetz SA, Yu EY, Davis JB, Temple K, Silver J, Malouf AT. 2004. Keratan sulfate proteoglycan phosphacan regulates mossy fiber outgrowth and regeneration. J Neurosci 24:462-473.
15. Chappuis-Flament S, Wong E, Hicks LD, Kay CM, Gumbiner BM. 2001. Multiple cadherin extracellular repeats mediate homophilic binding and adhesion. J Cell Biol 154:231-243.
16. Cline HT. 2001. Dendritic arbor development and synaptogenesis. Curr Opin Neurobiol 11:118-126.
17. Cremer H, Chazal G, Goridis C, Represa A. 1997. NCAM is essential for axonal growth and fasciculation in the hippocampus. Mol Cell Neurosci 8:323-335.
18. Dailey ME, Buchanan J, Bergles DE, Smith SJ. 1994. Mossy fiber growth and synaptogenesis in rat hippocampal slices in vitro. J Neurosci 14(3 Part 1):1060-1078.
19. Doherty P, Rowett LH, Moore SE, Mann DA, Walsh FS. 1991. Neurite outgrowth in response to transfected N-CAM and N-cadherin reveals fundamental differences in neuronal responsiveness to CAMs. Neuron 6:247-258.
20. Drazba J, Lemmon V. 1990. The role of cell adhesion molecules in neurite outgrowth on Muller cells. Dev Biol 138:82-93.
21. Elste AM, Benson DL. 2006. Structural basis for developmentally regulated changes in cadherin function at synapses. J Comp Neurol 495:324-335.
22. Esch T, Lemmon V, Banker G. 1999. Local presentation of substrate molecules directs axon specification by cultured hippocampal neurons. J Neurosci 19:6417-6426.
23. Esch T, Lemmon V, Banker G. 2000. Differential effects of NgCAM and N-cadherin on the development of axons and dendrites by cultured hippocampal neurons. J Neurocytol 29:215-223.
24. Espeseth A, Marnellos G, Kintner C. 1998. The role of F-cadherin in localizing cells during neural tube formation in Xenopus embryos. Development 125:301-312.
25. Evans GJ, Cousin MA. 2007. Simultaneous monitoring of three key neuronal functions in primary neuronal cultures. J Neurosci Methods 160:197-205.
26. Friedlander DR, Mege RM, Cunningham BA, Edelman GM. 1989. Cell sorting-out is modulated by both the specificity and amount of different cell adhesion molecules (CAMs) expressed on cell surfaces. Proc Natl Acad Sci USA 86:7043-7047.
27. Frotscher M, Heimrich B. 1995. Lamina-specific synaptic connections of hippocampal neurons in vitro. J Neurobiol 26:350-359.
28. Gahwiler BH. 1981. Organotypic monolayer cultures of nervous tissue. J Neurosci Methods 4:329-342.
29. Gahwiler BH. 1984a. Development of the hippocampus in vitro: Cell types, synapses and receptors. Neuroscience 11:751-760.
30. Gahwiler BH. 1984b. Slice cultures of cerebellar, hippocampal and hypothalamic tissue. Experientia 40:235-243.
31. Gil OD, Needleman L, Huntley GW. 2002. Developmental patterns of cadherin expression and localization in relation to compartmentalized thalamocortical terminations in rat barrel cortex. J Comp Neurol 453:372-388.
32. Goslin K, Banker G. 1989a. Experimental observations on the development of polarity by hippocampal neurons in culture. J Cell Biol 108:1507-1516.
33. Goslin K, Banker G. 1989b. Experimental observations on the development of polarity by hippocampal neurons in culture. J Cell Biol 108:1507-1516.
34. Goslin K, Schreyer DJ, Skene JHP, Banker G. 1990. Changes in the distribution of GAP-43 during the development of neuronal polarity. J Neurosci 10:588-602.
35. Haspel J, Blanco C, Jacob J, Grumet M. 2001. System for cleavable Fc fusion proteins using tobacco etch virus (TEV) protease. Biotechniques 30:60-61,64-66.
36. Hatta K, Takeichi M. 1986. Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature 320:447-449.
37. Hirano S, Suzuki ST, Redies CM. 2003. The cadherin superfamily in neural development: Diversity, function and interaction with other molecules. Front Biosci 8:D306-D355.
38. Hummel T, Zipursky SL. 2004. Afferent induction of olfactory glomeruli requires N-cadherin. Neuron 42:77-88.
39. Huntley GW, Benson DL. 1999. Neural (N)-cadherin at developing thalamocortical synapses provides an adhesion mechanism for the formation of somatopically organized connections. J Comp Neurol 407:453-471.
40. Inoue A, Sanes JR. 1997. Lamina-specific connectivity in the brain: regulation by N-cadherin, neurotrophins, and glycoconjugates. Science 276:1428-1431.
41. Iwai Y, Usui T, Hirano S, Steward R, Takeichi M, Uemura T. 1997. Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron 19:77-89.
42. Kido M, Obata S, Tanihara H, Rochelle JM, Seldin MF, Taketani S, Suzuki ST. 1998. Molecular properties and chromosomal location of cadherin-8. Genomics 48:186-194.
43. Knudsen KA, Peralta Soler A, Johnson KR, Wheelock MJ. 1995. Interaction of α-actinin with the cadherin/catenin cell-cell adhesion complex via α-catenin. J Cell Biol 130:67-77.
44. Korematsu K, Redies C. 1997. Expression of cadherin-8 mRNA in the developing mouse central nervous system. J Comp Neurol 387:291-306.
45. Kurazono S, Okamoto M, Sakiyama J, Mori S, Nakata Y, Fukuoka J, Amano S, Oohira A, Matsui H. 2001. Expression of brain specific chondroitin sulfate proteoglycans, neurocan and phosphacan, in the developing and adult hippocampus of Ihara's epileptic rats. Brain Res 898:36-48.
46. Laake JH, Haug FM, Wieloch T, Ottersen OP. 1999. A simple in vitro model of ischemia based on hippocampal slice cultures and propidium iodide fluorescence. Brain Res Brain Res Protoc 4:173-184.
47. Lee C, Herman T, Clandinin TR, Lee R, Zipursky SL. 2001. N-cadherin regulates target specificity in the Drosophila visual system. Neuron 30:437-450.
48. Li H, Leung TC, Hoffman S, Balsamo J, Lilien J. 2000. Coordinate regulation of cadherin and integrin function by the chondroitin sulfate proteoglycan neurocan. J Cell Biol 149:1275-1288.
49. Marthiens V, Gavard J, Padilla F, Monnet C, Castellani V, Lambert M, Mege RM. 2005. A novel function for cadherin-11 in the regulation of motor axon elongation and fasciculation. Mol Cell Neurosci 28:715-726.
50. Masai I, Lele Z, Yamaguchi M, Komori A, Nakata A, Nishiwaki Y, Wada H, Tanaka H, Nojima Y, Hammerschmidt M, Wilson SW, Okamoto H. 2003. N-cadherin mediates retinal lamination, maintenance of forebrain compartments and patterning of retinal neurites. Development 130:2479-2494.
51. Meng K, Rodriguez-Pena A, Dimitrov T, Chen W, Yamin M, Noda M, Deuel TF. 2000. Pleiotrophin signals increased tyrosine phosphorylation of beta beta-catenin through inactivation of the intrinsic catalytic activity of the receptor-type protein tyrosine phosphatase beta/zeta. Proc Natl Acad Sci USA 97:2603-2608.
52. Meyer MP, Smith SJ. 2006. Evidence from in vivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms. J Neurosci 26:3604-3614.
53. Miskevich F, Zhu Y, Ranscht B, Sanes JR. 1998. Expression of multiple cadherins and catenins in the chick optic tectum. Mol Cell Neurosci 12:240-255.
54. Montag-Sallaz M, Schachner M, Montag D. 2002. Misguided axonal projections, neural cell adhesion molecule 180 mRNA upregulation, and altered behavior in mice deficient for the close homolog of L1. Mol Cell Biol 22:7967-7981.
55. Nawroth R, Poell G, Ranft A, Kloep S, Samulowitz U, Fachinger G, Golding M, Shima DT, Deutsch U, Vestweber D. 2002. VE-PTP and VE-cadherin ectodomains interact to facilitate regulation of phosphorylation and cell contacts. Embo J 21:4885-4895.
56. Neugebauer KM, Tomaselli KJ, Lilien J, Reichardt LF. 1988. N-cadherin, NCAM, and integrins promote retinal neurite outgrowth on astrocytes in vitro J Cell Biol 107:1177-1187.
57. Noe V, Willems J, Vandekerckhove J, Roy FV, Bruyneel E, Mareel M. 1999. Inhibition of adhesion and induction of epithelial cell invasion by HAV-containing E-cadherin-specific peptides. J Cell Sci 112 (Part 1):127-135.
58. Nose A, Nagafuchi A, Takeichi M. 1988. Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54:993-1001.
59. Nose A, Tsuji K, Takeichi M. 1990. Localization of specificity determining sites in cadherin cell adhesion molecules. Cell 61:147-155.
60. Ozawa M, Baribault H, Kemler R. 1989. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. Embo J 8:1711-1717.
61. Patel SD, Ciatto C, Chen CP, Bahna F, Rajebhosale M, Arkus N, Schieren I, Jessell TM, Honig B, Price SR, Shapiro L. 2006. Type II cadherin ectodomain structures: Implications for classical cadherin specificity. Cell 124:1255-1268.
62. Petersen MA, Dailey ME. 2004. Diverse microglial motility behaviors during clearance of dead cells in hippocampal slices. Glia 46:195-206.
63. Pimenta AF, Zhukareva V, Barbe MF, Reinoso BS, Grimley C, Henzel W, Fischer I, Levitt P. 1995. The limbic system-associated membrane protein is an Ig superfamily member that mediates selective neuronal growth and axon targeting. Neuron 15:287-297.
64. Poskanzer K, Needleman LA, Bozdagi O, Huntley GW. 2003. N-cadherin regulates ingrowth and laminar targeting of thalamocortical axons. J Neurosci 23:2294-2305.
65. Pozzo Miller LD, Mahanty NK, Connor JA, Landis DM. 1994. Spontaneous pyramidal cell death in organotypic slice cultures from rat hippocampus is prevented by glutamate receptor antagonists. Neuroscience 63:471-487.
66. Price SR, De Marco Garcia NV, Ranscht B, Jessell TM. 2002. Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109:205-216.
67. Rakic P. 1975. Role of cell interaction in development of dendritic patterns. Adv Neurol 12:117-134.
68. Redies C, Engelhart K, Takeichi M. 1993. Differential expression of N- and R-cadherin in functional neuronal systems and other structures of the developing chicken brain. J Comp Neurol 333:398-416.
69. Redies C, Takeichi M. 1993. Expression of N-cadherin mRNA during development of the mouse brain. Dev Dyn 197:26-39.
70. Rhee J, Mahfooz NS, Arregui C, Lilien J, Balsamo J, VanBerkum MF. 2002. Activation of the repulsive receptor roundabout inhibits N-cadherin-mediated cell adhesion. Nat Cell Biol 4:798-805.
71. Riehl R, Johnson K, Bradley R, Grunwald GB, Cornel E, Lilienbaum A, Holt CE. 1996. Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17:837-848.
72. Robain O, Barbin G, Billette de Villemeur T, Jardin L, Jahchan T, Ben-Ari Y. 1994. Development of mossy fiber synapses in hippocampal slice culture. Brain Res Dev Brain Res 80:244-250.
73. Ruthazer ES, Li J, Cline HT. 2006. Stabilization of axon branch dynamics by synaptic maturation. J Neurosci 26:3594-3603.
74. Seki T, Rutishauser U. 1998. Removal of polysialic acid-neural cell adhesion molecule induces aberrant mossy fiber innervation and ectopic synaptogenesis in the hippocampus. J Neurosci 18:3757-3766.
75. Shapiro L, Fannon AM, Kwong PD, Thompson A, Lehmann MS, Grubel G, Legrand JF, Als-Nielsen J, Colman DR, Hendrickson WA. 1995. Structural basis of cell-cell adhesion by cadherins. Nature 374:327-337.
76. Shimoyama Y, Tsujimoto G, Kitajima M, Natori M. 2000. Identification of three human type-II classic cadherins and frequent heterophilic interactions between different subclasses of type-II classic cadherins. Biochem J 349 (Part 1):159-167.
77. Snyder SE, Li J, Schauwecker PE, McNeill TH, Salton SR. 1996. Comparison of RPTP zeta/beta, phosphacan, and trkB mRNA expression in the developing and adult rat nervous system and induction of RPTP zeta/beta and phosphacan mRNA following brain injury. Brain Res Mol Brain Res 40:79-96.
78. Stearns ME, Binder LI. 1987. Evidence that MAP-2 may be involved in pigment granule transport in squirrel fish erythrophores. Cell Motil Cytoskeleton 7:221-234.
79. Steup A, Lohrum M, Hamscho N, Savaskan NE, Ninnemann O, Nitsch R, Fujisawa H, Puschel AW, Skutella T. 2000. Sema3C and netrin-1 differentially affect axon growth in the hippocampal formation. Mol Cell Neurosci 15:141-155.
80. Stoppini L, Buchs PA, Muller D. 1991. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182.
81. Suto F, Tsuboi M, Kamiya H, Mizuno H, Kiyama Y, Komai S, Shimizu M, Sanbo M, Yagi T, Hiromi Y, Chédotal A, Mitchell KJ, Manabe T, Fujisawa H. 2007. Interactions between Plexin-A2, Plexin-A4, and Semaphorin 6A control lamina-restricted projection of hippocampal mossy fibers. Neuron 53:535-547.
82. Suzuki SC, Inoue T, Kimura Y, Tanaka T, Takeichi M. 1997a. Neuronal circuits are subdivided by differential expression of type-II classic cadherins in postnatal mouse brains. Mol Cell Neurosci 9:433-447.
83. Suzuki SC, Inoue T, Kimura Y, Tanaka T, Takeichi M. 1997b. Neuronal circuits are subdivided by differential expression of type-II classic cadherins in postnatal mouse brains. Mol Cell Neurosci 9:433-447.
84. Tanabe K, Takahashi Y, Sato Y, Kawakami K, Takeichi M, Nakagawa S. 2006. Cadherin is required for dendritic morphogenesis and synaptic terminal organization of retinal horizontal cells. Development 133:4085-4096.
85. Toda M, Asou H, Miura M, Toya S, Uyemura K. 1994. GFAP transfected cells produce laminin, leading to neurite outgrowth promotion. Neuroreport 5:1969-1972.
86. Togashi H, Abe K, Mizoguchi A, Takaoka K, Chisaka O, Takeichi M. 2002. Cadherin regulates dendritic spine morphogenesis. Neuron 35:77-89.
87. Tomaselli KJ, Neugebauer KM, Bixby JL, Lilien J, Reichardt LF. 1988. N-cadherin and integrins: Two receptor systems that mediate neuronal process outgrowth on astrocyte surfaces. Neuron 1:33-43.
88. Treubert-Zimmermann U, Heyers D, Redies C. 2002. Targeting axons to specific fiber tracts in vivo by altering cadherin expression. J Neurosci 22:7617-7626.
89. Utton MA, Eickholt B, Howell FV, Wallis J, Doherty P. 2001. Soluble N-cadherin stimulates fibroblast growth factor receptor dependent neurite outgrowth and N-cadherin and the fibroblast growth factor receptor co-cluster in cells. J Neurochem 76:1421-1430.
90. Voigt T, De Lima AD, Beckmann M. 1993. Synaptophysin immunohistochemistry reveals inside-out pattern of early synaptogenesis in ferret cerebral cortex. J Comp Neurol 330:48-64.
91. Wilby MJ, Muir EM, Fok-Seang J, Gour BJ, Blaschuk OW, Fawcett JW. 1999. N-Cadherin inhibits Schwann cell migration on astrocytes. Mol Cell Neurosci 14:66-84.
92. Williams E, Williams G, Gour BJ, Blaschuk OW, Doherty P. 2000. A novel family of cyclic peptide antagonists suggests that N-cadherin specificity is determined by amino acids that flank the HAV motif. J Biol Chem 275:4007-4012.
93. Wilson MT, Snow DM. 2000. Chondroitin sulfate proteoglycan expression pattern in hippocampal development: Potential regulation of axon tract formation. J Comp Neurol 424:532-546.
94. Wöhrn JC, Nakagawa S, Ast M, Takeichi M, Redies C. 1999. Combinatorial expression of cadherins in the tectum and the sorting of neurites in the tectofugal pathways of the chicken embryo. Neuroscience 90:985-1000.
95. Yamagata M, Herman JP, Sanes JR. 1995. Lamina-specific expression of adhesion molecules in developing chick optic tectum. J Neurosci 15:4556-4571.
96. Yap AS, Brieher WM, Pruschy M, Gumbiner BM. 1997. Lateral clustering of the adhesive ectodomain: A fundamental determinant of cadherin function. Curr Biol 7:308-315.
97. Yap AS, Niessen CM, Gumbiner BM. 1998. The juxtamembrane region of the cadherin cytoplasmic tail supports lateral clustering, adhesive strengthening, and interaction with p120ctn. J Cell Biol 141:779-789.
98. Zhu H, Luo L. 2004. Diverse functions of N-cadherin in dendritic and axonal terminal arborization of olfactory projection neurons. Neuron 42:63-75.
99. Zimmer J, Gahwiler BH. 1984. Cellular and connective organization of slice cultures of the rat hippocampus and fascia dentata. J Comp Neurol 228:432-446.