The cell adhesion molecule L1 regulates the expression of choline acetyltransferase and the development of septal cholinergic neurons

Brain and Behavior

Volumn 1, Issue 2, 2011, Pages 73-86

  Cui, Xuezhi ^a,f   Weng, Ying Qi ^a,g   Frappé, Isabelle ^a   Burgess, Alison ^a,b   Girão da Cruz, M Teresa ^a,h   Schachner, Melitta ^c,d,e   Aubert, Isabelle ^a,b  

^a Canada   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c RUTGERS UNIVERSITY   (United States)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^e SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^f HOSPITAL FOR SICK CHILDREN   (Canada)

^g UNIVERSITÉ DE POITIERS   (France)

^h UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Caudate putamen; Cell adhesion molecule L1; Choline acetyltransferase; Cholinergic neurons; L1 deficient mice; Medial septum; Stereology; Striatum; Vertical limb of diagonal band of Broca

Indexed keywords

CHOLINE ACETYLTRANSFERASE; KI 67 ANTIGEN; NERVE CELL ADHESION MOLECULE L1; NEURON SPECIFIC NUCLEAR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAUDATE NUCLEUS; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DIAGONAL BAND OF BROCA; ENZYME ACTIVITY; ENZYME REGULATION; FEMALE; IN VITRO STUDY; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PUTAMEN; SEPTUM PELLUCIDUM; WILD TYPE;

EID: 84863780137     PISSN: 21623279     EISSN: 21579032     Source Type: Journal    
DOI: 10.1002/brb3.15     Document Type: Article

References (54)

1. Acheson, A., and U. Rutishauser. 1988. Neural cell adhesion molecule regulates cell contact-mediated changes in choline acetyltransferase activity of embryonic chick sympathetic neurons. J. Cell Biol. 106:479-486.
2. Alderson, R. F., A. L. Alterman, Y. A. Barde, and R.M. Lindsay. 1990. Brain-derived neurotrophic factor increases survival and differentiated functions of rat septal cholinergic neurons in culture. Neuron 5:297-306.
3. Arami, S., M. Jucker, M. Schachner, and H.Welzl. 1996. The effect of continuous intraventricular infusion of L1 and NCAM antibodies on spatial learning in rats. Behav. Brain Res. 81:81-87.
4. Aubert, I., J. L. Ridet, M. Schachner, G. Rougon, and F. H. Gage. 1998. Expression of L1 and PSA during sprouting and regeneration in the adult hippocampal formation. J. Comp. Neurol. 399:1-19.
5. Auld, D. S., F. Mennicken, and R. Quirion. 2001. Nerve growth factor rapidly induces prolonged acetylcholine release from cultured basal forebrain neurons: differentiation between neuromodulatory and neurotrophic influences. J. Neurosci. 21:3375-3382.
6. Bernreuther, C., M. Dihné, V. Johann, J. Schiefer, Y. Cui, G. Hargus, J. S. Schmid, J. Xu, C. M. Kosinski, and M. Schachner. 2006. Neural cell adhesion molecule L1-transfected embryonic stem cells promote functional recovery after excitotoxic lesion of the mouse striatum. J. Neurosci. 26:11532-11539.
7. Bock, E., C. Richter-Landsberg, A. Faissner, and M. Schachner. 1985. Demonstration of immunochemical identity between the nerve growth factor-inducible large external (NILE) glycoprotein and the cell adhesion molecule L1. EMBO J. 4:2765-2768.
8. Br̈ummendorf, T., S. Kenwrick, and F. G. Rathjen. 1998. Neural cell recognition molecule L1: from cell biology to human hereditary brain malformations. Curr. Opin. Neurobiol. 8:87-97.
9. Burgess, A., and I. Aubert. 2006. Polysialic acid limits choline acetyltransferase activity induced by brain-derived neurotrophic factor. J. Neurochem. 99:797-806.
10. Burgess, A., S. Saini, Y. Q.Weng, and I. Aubert. 2009. Stimulation of choline acetyltransferase by C3d, a neural cell adhesion molecule ligand. J. Neurosci. Res. 87:609-616.
11. Chen, K. S., M. C. Nishimura, M. P. Armanini, C. Crowley, S. D. Spencer, and H. S. Phillips. 1997. Disruption of a single allele of the nerve growth factor gene results in atrophy of basal forebrain cholinergic neurons and memory deficits. J. Neurosci. 17:7288-7296.
12. Cheng, L., and V. Lemmon. 2004. Pathological missense mutations of neural cell adhesion molecule L1 affect neurite outgrowth and branching on an L1 substrate. Mol. Cell Neurosci. 27:522-530.
13. Cohen, N. R., J. S. H. Taylor, L. B. Scott, R.W. Guillery, P. Soriano, and A. J.W. Furley. 1997. Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Curr. Biol. 8:26-33.
14. Dahmé, M., U. Bartsch, R. Martini, B. Anliker, M. Schachner, and N. Mantei. 1997. Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat. Genet. 17:346-349.
15. Demyanenko, G. P., and P. F. Maness. 2003. The L1 cell adhesion molecule is essential for topographic mapping of retinal axons. J. Neurosci. 23:530-538.
16. Demyanenko, G. P., A. Y. Tsai, and P. F. Maness. 1999. Abnormalities in neuronal process extension, hippocampal development, and the ventricular system of L1 knockout mice. J. Neurosci. 19:4907-4920.
17. Demyanenko, G. P., Y. Shibata, and P. F. Maness. 2001. Altered distribution of dopaminergic neurons in the brain of L1 null mice. Dev. Brain Res. 126:21-30.
18. Dihné, M., C. Bernreuther, M. Sibbe, W. Paulus, and M. Schachner. 2003. A new role for the cell adhesion molecule L1 in neural precursor cell proliferation, differentiation, and transmitter-specific subtype generation. J. Neurosci. 23:6638-6650.
19. Fonnum, F. 1969. Radiochemical micro assays for the determination of choline acetyltransferase and acetylcholinesterase activities. Biochem J. 115: 465-472.
20. Fransen, E., R. D'Hooge, G. van Camp, M. Verhoye, J. Sijbers, E. Reyniers, P. Soriano, H. Kamiguchi, R. Willemsen, and S. K. Koekkoek. 1998. L1 knockout mice show dilated ventricles, vermis hypoplasia and impaired exploration patterns. Hum. Mol. Genet. 7:999-1009.
21. Frappé, I., C.Wang, G. Caines, S. Rideout-Gros, and I. Aubert. 2004. Cell adhesion molecule L1 promotes neurite outgrowth of septal neurons. J. Neurosci. Res. 75:667-677.
22. Frotscher, M., and C. Leranth. 1985. Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J. Comp. Neurol. 239:237-246.
23. Gould, E., N. J.Woolf, and L. L. Butcher. 1991. Postnatal development of cholinergic neurons in the rat: I. forebrain. Brain Res. Bull. 27:767-789.
24. Grothe, C., D. Otto, and K. Unsicker. 1989. Basic fibroblast growth factor promotes in vitro survival and cholinergic development of rat septal neurons: comparison with the effects of nerve growth factor. Neuroscience 31:649-661.
25. Hefti, F., J. Hartikka, and J. Sanchez-Ramos. 1989. Dissociated cholinergic neurons of the basal forebrain in culture. Pp.172-182 in A. Shahar, J. de Vellis, A. Vernadakis, and B. Haber, eds. A dissection and tissue culture manual of the nervous system. Allan R. Liss Inc, New York.
26. Itoh, K., R. Brackenbury, and R. A. Akeson. 1995. Induction of L1 mRNA in PC12 cells by NGF is modulated by cell-cell contact and does not require the high-affinity NGF receptor. J. Neurosci. 15:2504-2512.
27. Kamiguchi, H., M. L. Hlavin, M. Yamasaki, and V. Lemmon. 1998. Adhesion molecules and inherited diseases of the human nervous system. Annu. Rev. Neurosci. 21:97-125.
28. Law, J.W., A. Y. Lee, M. Sun, A. G. Nikonenko, S. K. Chung, A. Dityatev, M. Schachner, and F. Morellini. 2003. Decreased anxiety, altered place learning, and increased CA1 basal excitatory synaptic transmission in mice with conditional ablation of the neural cell adhesion molecule L1. J. Neurosci. 23:10419-10432.
29. Loers, G., S. Chen, M. Grumet, and M. Schachner. 2005. Signal transduction pathways implicated in neural recognition molecule L1 triggered neuroprotection and neuritogenesis. J. Neurochem. 92:1463-1476.
30. Maness, P. F., and M. Schachner. 2007. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat. Neurosci. 10:19-26.
31. Moulding, H. D., R. L. Martuza, and S. D. Rabkin. 2000. Clinical mutations in the L1 neural cell adhesion molecule affect cell-surface expression. J. Neurosci. 20:5696-5702.
32. Nonner, D., E. F. Barrett, and J. N. Barrett. 1996. Neurotrophin effects on survival and expression of cholinergic properties in cultured rat septal neurons under normal and stress conditions. J. Neurosci. 16:6665-6675.
33. Nonner, D., E. F. Barrett, and J. N. Barrett. 2000. Brief exposure to neurotrophins produces a calcium-dependent increase in choline acetyltransferase activity in cultured rat septal neurons. J. Neurochem. 74:988-999.
34. Ohyama, K., K. Tan-Takeuchi, M. Kutsche, M. Schachner, K. Uyemura, and K. Kawamura. 2004. Neural cell adhesion molecule L1 is required for fasciculation and routing of thalamocortical fibres and corticothalamic fibres. Neurosci. Res. 48:471-475.
35. Oosawa, H., T. Fujii, and K. Kawashima. 1999. Nerve growth factor increases the synthesis and release of acetylcholine and the expression of vesicular acetylcholine transporter in primary cultured rat embryonic septal cells. J. Neurosci. Res. 57:381-387.
36. Phelps, P. E., D. R. Brady, and J. E. Vaughn. 1989. The generation and differentiation of cholinergic neurons in rat caudate-putamen. Dev. Brain Res. 46:47-60.
37. Pongrac, J. L., and R. J. Rylett. 1998. Optimization of serum-free culture conditions for growth of embryonic rat cholinergic basal forebrain neurons. J. Neurosci. Methods. 84:69-76.
38. Prince, J. T., L. Alberti, P. A. Healy, S. J. Nauman, andW. B. Stallcup. 1991. Molecular cloning of NILE glycoprotein and evidence for its continued expression in mature rat CNS. J. Neurosci. Res. 30:567-581.
39. Rathjen, F. G., and M. Schachner. 1984. Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J. 3:1-10.
40. Rolf, B., M. Kutsche, and U. Bartsch. 2001. Severe hydrocephalus in L1-deficient mice. Brain Res. 891:247-252.
41. Saghatelyan, A. K., A. G. Nikonenko, M. Sun, B. Rolf, P. Putthoff, M. Kutsche, U. Bartsch, A. Dityatev, and M. Schachner. 2004. Reduced GABAergic transmission and number of hippocampal perisomatic inhibitory synapses in juvenile mice deficient in the neural cell adhesion molecule L1. Mol. Cell Neurosci. 26:191-203.
42. Salton, S. R., M. L. Shelanski, and L. A. Greene. 1983. Biochemical properties of the nerve growth factor-inducible large external (NILE) glycoprotein. J. Neurosci. 3:2420-2430.
43. Sandi, C. S. 2004. Cognitive impairment and cell adhesion molecules. Nat. Rev. Neurosci. 5:917-930.
44. Sarter, M., and V. Parikh. 2005. Choline transporters, cholinergic transmission and cognition. Nat. Rev. Neurosci. 6:48-56.
45. Semba, K., and H. C. Fibiger. 1988. Time and origin of cholinergic neurons in the rat basal forebrain. J. Comp. Neurol. 269:87-95.
46. Stallcup, W. B., L. L. Beasley, and J. M. Levine. 1985. Antibody against nerve growth factor-inducible large external (NILE) glycoprotein labels nerve fiber tracts in the developing rat nervous system. J. Neurosci. 5:1090-1101.
47. Tereshchenko, Y., F.Morellini, A.Dityatev, M. Schachner, and A. Irintchev. 2011. NCAM ablation in mice causes hippocampal dysplasia and loss of septal cholinergic neurons. J. Comp. Neurol. 519:2475-2492.
48. Tucek, S. 1978. Choline acetyltransferase. Acetylcholine synthesis in neurons. Chapman and Hall, London. pp. 1-258.
49. Wahlsten, D., and B. Bulman-Fleming. 1994. Retarded growth of the medial septum: a major gene effect in acallosal mice. Dev. Brain Res 77:203-214.
50. Walsh, G. S., K. Petruccelli, and M. D. Kawaja. 1998. p75-deficient sensory axons are immunoreactive for the glycoprotein L1 in mice overexpressing nerve growth factor. Brain Res. 798:184-194.
51. Ward, N. L., and T. Hagg. 2000. BDNF is needed for postnatal maturation of basal forebrain and neostriatum cholinergic neurons in vivo. Exp. Neurol. 162:297-310.
52. West, M. J. 1993. New stereological methods for counting neurons. Neurobiol. Aging 14:275-285.
53. Wong, E. V., S. Kenwrick, P.Willems, and V. Lemmon. 1995. Mutations in the cell adhesion molecule L1 cause mental retardation. Trends Neurosci. 18:168-172.
54. Ypsilanti, A. R., M. T. Girão da Cruz, A. Burgess, and I. Aubert. 2008. The length of hippocampal cholinergic fibers is reduced in the aging brain. Neurobiol. Aging 29:1666-1679. 86