Semaphorin 3C is not required for the establishment and target specificity of the GABAergic septohippocampal pathway in vitro

European Journal of Neuroscience

Volumn 34, Issue 12, 2011, Pages 1923-1933

  Rubio, Sara E ^a,b,c   Martínez, Albert ^a,b,c   Chauvet, Sophie ^d   Mann, Fanny ^d   Soriano, Eduardo ^a,b,c   Pascual, Marta ^a,b,c  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^d AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Hippocampal interneurons; Mouse; Organotypic cultures; Synaptogenesis

Indexed keywords

SEMAPHORIN; SEMAPHORIN C; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE CELL; CHOLINERGIC SYSTEM; COCULTURE; CONTROLLED STUDY; GABAERGIC SYSTEM; HIPPOCAMPUS; IN VITRO STUDY; INTERNEURON; MOUSE; NERVE FIBER; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEPTOHIPPOCAMPAL PATHWAY; SEPTUM PELLUCIDUM; SYNAPSE;

ANIMALS; AXONS; CELLS, CULTURED; CHOLINERGIC NEURONS; COCULTURE TECHNIQUES; GABAERGIC NEURONS; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; NEURAL PATHWAYS; SEMAPHORINS; SEPTUM OF BRAIN; TISSUE CULTURE TECHNIQUES;

EID: 83555178415     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07906.x     Document Type: Article

References (41)

1. Alcántara, S., Ruiz, M., D'Arcangelo, G., Ezan, F., De Lecea, L., Curran, T., Sotelo, C. & Soriano, E. (1998) Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J. Neurosci., 18, 7779-7799.
2. Amaral, D.G. & Witter, M.P. (2004) Hippocampal formation. In Paxinos, G. (ed), The Rat Nervous System. Elsevier Academic Press, Amsterdam, pp. Xvii.
3. Bagnard, D., Lohrum, M., Uziel, D., Puschel, A.W. & Bolz, J. (1998) Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections. Development, 125, 5043-5053.
4. Blankenship, A.G. & Feller, M.B. (2010) Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat. Rev., 11, 18-29.
5. Buzsaki, G. (2002) Theta oscillations in the hippocampus. Neuron, 33, 325-340.
6. Cantero, J.L., Atienza, M., Stickgold, R., Kahana, M.J., Madsen, J.R. & Kocsis, B. (2003) Sleep-dependent theta oscillations in the human hippocampus and neocortex. J. Neurosci., 23, 10897-10903.
7. Canto, C.B., Wouterlood, F.G. & Witter, M.P. (2008) What does the anatomical organization of the entorhinal cortex tell us? Neural Plast, 2008, 381243.
8. Chen, H., He, Z., Bagri, A. & Tessier-Lavigne, M. (1998) Semaphorin-neuropilin interactions underlying sympathetic axon responses to class iii semaphorins. Neuron, 21, 1283-1290.
9. Chrobak, J.J., Lörincz, A. & Buzsáki, G. (2000) Physiological patterns in the hippocampo-entorhinal cortex system. Hippocampus, 10, 457-465.
10. Del Rio, J.A. & Soriano, E. (2010) Regenerating cortical connections in a dish: the entorhino-hippocampal organotypic slice co-culture as tool for pharmacological screening of molecules promoting axon regeneration. Nat. Protoc., 5, 217-226.
11. Del Rio, J.A., Heimrich, B., Borrell, V., Forster, E., Drakew, A., Alcantara, S., Nakajima, K., Miyata, T., Ogawa, M., Mikoshiba, K., Derer, P., Frotscher, M. & Soriano, E. (1997) A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature, 385, 70-74.
12. Easter, S.S., Purves, D., Rakic, P. & Spitzer, N.C. (1985) The changing view of neural specificity. Science, 230, 507-511.
13. Feiner, L., Webber, A.L., Brown, C.B., Lu, M.M., Jia, L., Feinstein, P., Mombaerts, P., Epstein, J.A. & Raper, J.A. (2001) Targeted disruption of semaphorin 3C leads to persistent truncus arteriosus and aortic arch interruption. Development, 128, 3061-3070.
14. Freund, T.F. & Antal, M. (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature, 336, 170-173.
15. Frotscher, M. & Léránth, C. (1986) The cholinergic innervation of the rat fascia dentata: identification of target structures on granule cells by combining choline acetyltransferase immunocytochemistry and Golgi impregnation. J. Comp. Neurol., 243, 58-70.
16. Goodman, C.S. (1996) Mechanisms and molecules that control growth cone guidance. Annu. Rev. Neurosci., 19, 341-377.
17. Gulyás, A.I., Görcs, T.J. & Freund, T.F. (1990) Innervation of different peptide-containing neurons in the hippocampus by gabaergic septal afferents. Neuroscience, 37, 31-44.
18. Hangya, B., Borhegyi, Z., Szilagyi, N., Freund, T.F. & Varga, V. (2009) GABAergic neurons of the medial septum lead the hippocampal network during theta activity. J. Neurosci., 29, 8094-8102.
19. Heimrich, B., Papp, E.C., Freund, T.F. & Frotscher, M. (1996) Regeneration of the GABAergic septohippocampal projection in vitro. Neuroscience, 72, 409-417.
20. Huang, Z.J. (2009) Activity-dependent development of inhibitory synapses and innervation pattern: role of GABA signalling and beyond. J. Physiol., 587, 1881-1888.
21. Huang, Z.J. & Scheiffele, P. (2008) GABA and neuroligin signaling: linking synaptic activity and adhesion in inhibitory synapse development. Curr. Opin. Neurobiol., 18, 77-83.
22. Lu, B., Wang, K.H. & Nose, A. (2009) Molecular mechanisms underlying neural circuit formation. Curr. Opin. Neurobiol., 19, 162-167.
23. Niquille, M., Garel, S., Mann, F., Hornung, J.-P., Otsmane, B., Chevalley, S.B., Parras, C., Guillemot, F., Gaspar, P., Yanagawa, Y. & Lebrand, C.C. (2009) Transient neuronal populations are required to guide callosal axons: a role for semaphorin 3C. PLoS Biol., 7, e1000230.
24. Pascual, M., Rocamora, N., Acsady, L., Freund, T.F. & Soriano, E. (1998) Expression of nerve growth factor and neurotrophin-3 mRNAs in hippocampal interneurons: morphological characterization, levels of expression, and colocalization of nerve growth factor and neurotrophin-3. J. Comp. Neurol., 395, 73-90.
25. Pascual, M., Pérez-Sust, P. & Soriano, E. (2004a) The GABAergic septohippocampal pathway in control and reeler mice: target specificity and termination onto reelin-expressing interneurons. Mol. Cell. Neurosci., 25, 679-691.
26. Pascual, M., Pozas, E., Barallobre, M.J., Tessier-Lavigne, M. & Soriano, E. (2004b) Coordinated functions of Netrin-1 and Class 3 secreted Semaphorins in the guidance of reciprocal septohippocampal connections. Mol. Cell. Neurosci., 26, 24-33.
27. Pascual, M., Pozas, E. & Soriano, E. (2005) Role of class 3 semaphorins in the development and maturation of the septohippocampal pathway. Hippocampus, 15, 184-202.
28. Prinz, P.N., Vitaliano, P.P., Vitiello, M.V., Bokan, J., Raskind, M., Peskind, E. & Gerber, C. (1982) Sleep, EEG and mental function changes in senile dementia of the Alzheimer's type. Neurobiol. Aging, 3, 361-370.
29. Rocamora, N., Pascual, M., Acsady, L., de Lecea, L., Freund, T.F. & Soriano, E. (1996) Expression of NGF and NT3 mRNAs in hippocampal interneurons innervated by the GABAergic septohippocampal pathway. J. Neurosci., 16, 3991-4004.
30. Shen, K. & Cowan, C.W. (2010) Guidance molecules in synapse formation and plasticity. Cold Spring Harb. Perspect. Biol., 2, a001842.
31. Song, H.-J. & Poo, M.-M. (2001) The cell biology of neuronal navigation. Nat. Cell Biol., 3, E81-E88.
32. Spitzer, N.C. (2004) Coincidence detection enhances appropriate wiring of the nervous system. Proc. Natl. Acad. Sci. USA, 101, 5311-5312.
33. Stewart, M. & Fox, S.E. (1991) Hippocampal theta activity in monkeys. Brain Res., 538, 59-63.
34. Super, H. & Soriano, E. (1994) The organization of the embryonic and early postnatal murine hippocampus. II. Development of entorhinal, commissural, and septal connections studied with the lipophilic tracer DiI. J. Comp. Neurol., 344, 101-120.
35. Tago, H., Kimura, H. & Maeda, T. (1986) Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure. J. Histochem. Cytochem., 34, 1431-1438.
36. Tesche, C.D. & Karhu, J. (2000) Theta oscillations index human hippocampal activation during a working memory task. Proc. Natl. Acad. Sci. USA, 97, 919-924.
37. Tessier-Lavigne, M. & Goodman, C.S. (1996) The molecular biology of axon guidance. Science, 274, 1123-1133.
38. Tóth, K., Freund, T.F. & Miles, R. (1997) Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J. Physiol., 500, 463-474.
39. Waites, C.L., Craig, A.M. & Garner, C.C. (2005) Mechanisms of vertebrate synaptogenesis. Annu. Rev. Neurosci., 28, 251-274.
40. Wang, C.-L., Zhang, L., Zhou, Y., Zhou, J., Yang, X.-J., Duan, S.-M., Xiong, Z.-Q. & Ding, Y.-Q. (2007) Activity-dependent development of callosal projections in the somatosensory cortex. J. Neurosci., 27, 11334-11342.
41. Woolf, N.J., Eckenstein, F. & Butcher, L.L. (1984) Cholinergic systems in the rat brain: I. Projections to the limbic telencephalon. Brain Res. Bull., 13, 751-784.