Cadherin expression in the developing mouse olfactory system

Journal of Comparative Neurology

Volumn 501, Issue 4, 2007, Pages 483-497

  Akins, Michael R ^a   Benson, Deanna L ^b   Greer, Charles A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Axon guidance; Catenin; Olfaction; Olfactory nerve layer; Olfactory sensory neuron; Plakoglobin

Indexed keywords

CADHERIN; CADHERIN 1; CADHERIN 10; CADHERIN 11; CADHERIN 13; CADHERIN 15; CADHERIN 2; CADHERIN 3; CADHERIN 4; CADHERIN 6; CADHERIN 8; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; FEMALE; GLIA CELL; MOUSE; NERVE CELL; NERVE FIBER; NEUROPIL; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY BULB; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SENSORY NERVE CELL;

ANIMALS; ANIMALS, NEWBORN; CADHERINS; EMBRYO; FEMALE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS, AFFERENT; OLFACTORY PATHWAYS; PREGNANCY;

EID: 34247265019     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21270     Document Type: Article

References (82)

1. Akins MR, Greer CA. 2006. Axon behavior in the olfactory nerve reflects the involvement of catenin-cadherin mediated adhesion. J Comp Neurol 499: 979-989.
2. Arndt K, Nakagawa S, Takeichi M, Redies C. 1998. Cadherin-denned segments and parasagittal cell Ribbons in the developing chicken cerebellum. Mol Cell Neurosci 10:211-228.
3. Au WW, Treloar HB, Greer CA. 2002. Sublaminar organization of the mouse olfactory bulb nerve layer. J Comp Neurol 446:68-80.
4. Bailey MS, Puche AC, Shipley MT. 1999. Development of the olfactory bulb: evidence for glia-neuron interactions in glomerular formation. J Comp Neurol 415:423-448.
5. Baker H, Cummings DM, Munger SD, Margolis JW, Franzen L, Reed RR, Margolis FL. 1999. Targeted deletion of a cyclic nucleotide-gated channel subunit (OCNC1): biochemical and morphological consequences in adult mice. J Neurosci 19:9313-9321.
6. Beesley PW, Mummery R, Tibaldi J. 1995. N-cadherin is a major glycoprotein component of isolated rat forebrain postsynaptic densities. J Neurochem 64:2288-2294.
7. 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.
8. Bozdagi 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.
9. Breier G, Breviario F, Caveda L, Berthier R, Schnurch H, Gotsch U, Vestweber D, Risau W, Dejana E. 1996. Molecular cloning and expression of murine vascular endothelial-cadherin in early stage development of cardiovascular system. Blood 87:630-641.
10. Cepek KL, Shaw SK, Parker CM, Russell GJ, Morrow JS, Rimm DL, Brenner MB. 1994. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature 372:190-193.
11. Chuah MI, David S, Blaschuk O. 1991. Differentiation and survival of rat olfactory epithelial neurons in dissociated cell culture. Brain Res Dev Brain Res 60:123-132.
12. Cifuentes-Diaz C, Nicolet M, Alameddine H, Goudou D, Dehaupas M, Rieger F, Mege RM. 1995. M-cadherin localization in developing adult and regenerating mouse skeletal muscle: possible involvement in secondary myogenesis. Mech Dev 50:85-97.
13. Doherty P, Ashton SV, Skaper SD, Leon A, Walsh FS. 1992. Ganglioside modulation of neural cell adhesion molecule and N-cadherin-dependent neurite outgrowth. J Cell Biol 117:1093-1099.
14. Duguay D, Foty RA, Steinberg MS. 2003. Cadherin-mediated cell adhesion and tissue segregation: qualitative and quantitative determinants. Dev Biol 253:309-323.
15. Fannon AM, Colman DR. 1996. A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins. Neuron 17:423-434.
16. Gong Q, Shipley MT. 1996. Expression of extracellular matrix molecules and cell surface molecules in the olfactory nerve pathway during early development. J Comp Neurol 366:1-14.
17. Halpern M, Jia C, Shapiro LS. 1998. Segregated pathways in the vomeronasal system. Microsc Res Tech 41:519-529.
18. Hino H, Mori K, Yoshihara Y, Iseki E, Akiyama H, Nishimura T, Ikeda K, Kosaka K. 1997. Reduction of telencephalin immunoreactivity in the brain of patients with Alzheimer's disease. Brain Res 753:353-357.
19. Hisaoka T, Morikawa Y, Kitamura T, Senba E. 2004. Expression of a member of tumor necrosis factor receptor superfamily, TROY, in the developing olfactory system. Glia 45:313-324.
20. 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.
21. 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.
22. Inoue A, Sanes JR. 1997. Lamina-specific connectivity in the brain: regulation by N-cadherin, neurotrophins, and glycoconjugates. Science 276: 1428-1431.
23. Inoue T, Chisaka O, Matsunami H, Takeichi M. 1997. Cadherin-6 expression transiently delineates specific rhombomeres, other neural tube subdivisions, and neural crest subpopulations in mouse embryos. Dev Biol 183:183-194.
24. Inoue T, Tanaka T, Suzuki SC, Takeichi M. 1998. Cadherin-6 in the developing mouse brain: expression along restricted connection systems and synaptic localization suggest a potential role in neuronal circuitry. Dev Dyn 211:338-351.
25. Jontes JD, Phillips GR. 2006. Selective stabilization and synaptic specificity: a new cell-biological model. Trends Neurosci 29:186-191.
26. Kasowski HJ, Kim H, Greer CA. 1999. Compartmental organization of the olfactory bulb glomerulus. J Comp Neurol 407:261-274.
27. Kimura Y, Matsunami H, Inoue T, Shimamura K, Uchida N, Ueno T, Miyazaki T, Takeichi M. 1995. Cadherin-11 expressed in association with mesenchymal morphogenesis in the head, somite, and limb bud of early mouse embryos. Dev Biol 169:47-358.
28. Lee CH, Herman T, Clandinin TR, Lee R, Zipursky SL. 2001. N-cadherin regulates target specificity in the Drosophila visual system. Neuron 30:437-450.
29. Lemmon V, Burden SM, Payne HR, Elmslie GJ, Hlavin ML. 1992. Neurite growth on different substrates: permissive versus instructive influences and the role of adhesive strength. J Neurosci 12:818-826.
30. Lin DM, Yang YH, Scolnick JA, Brunet LJ, Marsh H, Peng V, Okazaki Y, Hayashizaki Y, Speed TP, Ngai J. 2004. Spatial patterns of gene expression in the olfactory bulb. Proc Natl Acad Sci U S A 101:12718-12723.
31. Liu Q, Marrs JA, Azodi E, Kerstetter AE, Babb SG, Hashmi L. 2004. Differential expression of cadherins in the developing and adult zebrafish olfactory system. J Comp Neurol 478:269-281.
32. Lledo PM, Alonso M, Grubb MS. 2006. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:79-193.
33. Malnic B, Hirono J, Sato T, Buck LB. 1999. Combinatorial receptor codes for odors. Cell 96:713-723.
34. Manabe T, Togashi H, Uchida N, Suzuki SC, Hayakawa Y. 2000. Loss of cadherin-11 adhesion receptor enhances plastic changes in hippocampal synapses and modifies behavioral responses. Mol Cell Neurosci 15:534-546.
35. Marthiens V, Padilla F, Lambert M, Mege RM. 2002. Complementary expression and regulation of cadherins 6 and 11 during specific steps of motoneuron differentiation. Mol Cell Neurosci 20:458-475.
36. Matsunami H, Miyatani S, Inoue T, Copeland NG, Gilbert DJ, Jenkins NA, Takeichi M. 1993. Cell binding specificity of mouse R-cadherin and chromosomal mapping of the gene. J Cell Sci 106(Pt 1):401-409.
37. Matsunami H, Takeichi M. 1995. Fetal brain subdivisions defined by R-and E-cadherin expressions: evidence for the role of cadherin activity in region-specific, cell-cell adhesion. Dev Biol 172:466-478.
38. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R. 1996. Visualizing an olfactory sensory map. Cell 87:675-686.
39. Mori K, von Campenhausen H, Yoshihara Y. 2000. Zonal organization of the mammalian main and accessory olfactory systems. Philos Trans R Soc Lond B Biol Sci 355:1801-1812.
40. Murakami F, Tada Y, Mori K, Oka S, Katsumaru H. 1991. Ultrastructural-localization of telencephalin, a telencephalon-specific membrane glycoprotein, in rabbit olfactory-bulb. J Neurosci Res 11:141-145.
41. Nollet F, Kools P, van Roy F. 2000. Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol 299:551-572.
42. Norgren RB, Brackenbury R. 1993. Cell adhesion molecules and the migration of LHRH neurons during development. Dev Biol 160:377-387.
43. Nose A, Takeichi M. 1986. A novel cadherin cell adhesion molecule: its expression patterns associated with implantation and organogenesis of mouse embryos. J Cell Biol 103:2649-2658.
44. Nose A, Nagafuchi A, Takeichi M. 1988. Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54:993-1001.
45. Obst-Pernberg K, Redies C. 1999. Cadherins and synaptic specificity. J Neurosci Res 58:130-138.
46. Obst-Pernberg K, Medina L, Redies C. 2001. Expression of R-cadherin and N-cadherin by cell groups and fiber tracts in the developing mouse forebrain: relation to the formation of functional circuits. Neuroscience 106:505-533.
47. Oland LA, Pott WM, Higgins MR, Tolbert LP. 1998. Targeted ingrowth and glial relationships of olfactory receptor axons in the primary olfactory pathway of an insect. J Comp Neurol 398:119-138.
48. 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.
49. Poskanzer K, Needleman LA, Bozdagi O, Huntley GW. 2003. N-cadherin regulates ingrowth and laminar targeting of thalamocortical axons. J Neurosci 23:2294-2305.
50. Potter SM, Zheng C, Koos DS, Feinstein P, Fraser SE, Mombaerts P. 2001. Structure and emergence of specific olfactory glomeruli in the mouse. J Neurosci 21:9713-9723.
51. Price JL. 1973. An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex. J Comp Neurol 150:87-108.
52. 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.
53. Redies C, Muller HA. 1994. Similarities in structure and expression between mouse P-cadherin and frog XB/U-cadherin. Cell Adhes Commun 2:511-520.
54. Redies C, Takeichi M. 1993. Expression of N-cadherin mRNA during development of the mouse brain. Dev Dyn 197:26-39.
55. Ressler KJ, Sullivan SL, Buck LB. 1993. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73:597-609.
56. Royal SJ, Key B. 1999. Development of P2 olfactory glomeruli in P2-internal ribosome entry site-tau-LacZ transgenic mice. J Neurosci 19: 9856-9864.
57. Schwob JE, Price JL. 1984a. The development of axonal connections in the central olfactory system of rats. J Comp Neurol 223:177-202.
58. Schwob JE, Price JL. 1984b. The development of lamination of afferent fibers to the olfactory cortex in rats, with additional observations in the adult. J Comp Neurol 223:203-222.
59. Shan WS, Tanaka H, Phillips GR, Arndt K, Yoshida M, Colman DR, Shapiro L. 2000. Functional cis-heterodimers of N- and R-cadherins. J Cell Biol 148:579-590.
60. Shepherd GM, Chen WR, Greer CA. 2004. Olfactory bulb. In: Shepherd GM, editor. The synaptic organization of the brain. New York: Oxford University Press. p 165-216.
61. 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 349:159-167.
62. Simonneau L, Kitagawa M, Suzuki S, Thiery JP. 1995. Cadherin 11 expression marks the mesenchymal phenotype: towards new functions for cadherins? Cell Adhes Commun 3:115-130.
63. Suzuki SC, Inoue T, Kimura Y, Tanaka T, Takeichi M. 1997. Neuronal circuits are subdivided by differential expression of type-II classic cadherins in postnatal mouse brains. Mol Cell Neurosci 9:433-447.
64. Tepass U, Truong K, Godt D, Ikura M, Peifer M. 2000. Cadherins in embryonic and neural morphogenesis. Nat Rev Mol Cell Biol 1:91-100.
65. Treloar H, Tomasiewicz H, Magnuson T, Key B. 1997. The central pathway of primary olfactory axons is abnormal in mice lacking the N-CAM-180 isoform. J Neurobiol 32:643-658.
66. Treloar HB, Purcell AL, Greer CA. 1999. Glomerular formation in the developing rat olfactory bulb. J Comp Neurol 413:289-304.
67. Treloar HB, Feinstein P, Mombaerts P, Greer CA. 2002. Specificity of glomerular targeting by olfactory sensory axons. J Neurosci 22:2469-2477.
68. 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.
69. Tucker ES, Tolbert LP. 2003. Reciprocal interactions between olfactory receptor axons and olfactory nerve glia cultured from the developing moth Manduca sexta. Dev Biol 260:9-30.
70. Tucker ES, Oland LA, Tolbert LP. 2004. In vitro analyses of interactions between olfactory receptor growth cones and glial cells that mediate axon sorting and glomerulus formation. J Comp Neurol 472:478-495.
71. Uchida N, Honjo Y, Johnson KR, Wheelock MJ, Takeichi M. 1996. The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones. J Cell Biol 135:767-779.
72. Vassar R, Ngai J, Axel R. 1993. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74:309-318.
73. Wang F, Nemes A, Mendelsohn M, Axel R. 1998. Odorant receptors govern the formation of a precise topographic map. Cell 93:47-60.
74. Whitesides JG, LaMantia AS. 1996. Differential adhesion and the initial assembly of the mammalian olfactory nerve. J Comp Neurol 373:240-254.
75. Whitley M, Treloar H, De Arcangelis A, Georges Labouesse E, Greer CA. 2005. The alpha6 integrin subunit in the developing mouse olfactory bulb. J Neurocytol 34:1-96.
76. Wohrn 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.
77. Xu L, Overbeek PA, Reneker LW. 2002. Systematic analysis of E-, N- and P-cadherin expression in mouse eye development. Exp Eye Res 74:753-760.
78. Yamagata M, Herman JP, Sanes JR. 1995. Lamina-specific expression of adhesion molecules in developing chick optic tectum. J Neurosci 15: 4556-4571.
79. Yoshihara Y, Kawasaki M, Tamada A, Fujita H, Hayashi H, Kagamiyama H, Mori K. 1997. OCAM: a new member of the neural cell adhesion molecule family related to zone-to-zone projection of olfactory and vomeronasal axons. J Neurosci 17:5830-5842.
80. Young P, Boussadia O, Halfter H, Grose R, Berger P, Leone DP, Robenek H, Charnay P, Kemler R, Suter U. 2003. E-cadherin controls adherens junctions in the epidermis and the renewal of hair follicles. EMBO J 22:5723-5733.
81. Zhou DJ, Greer CA, Firestein S. 2002. Expression pattern of alpha CaMKII in the mouse main olfactory bulb. J Comp Neurol 443:226-236.
82. Zhou DJ, Feinstein P, Rivers AL, Mathews GA, Kim A, Greer CA, Mombaerts P, Firestein S. 2004. Postnatal refinement of peripheral olfactory projections. Science 304:1976-1979.