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Journal of Neuroscience, Vol 8, 1454-1468, Copyright © 1988 by Society for Neuroscience

ARTICLE

The establishment of polarity by hippocampal neurons in culture

CG Dotti, CA Sullivan and GA Banker
Department of Anatomy, Cell Biology and Neurobiology, Albany Medical College, New York 12208.

By the end of the first week in culture, hippocampal neurons have established a single axon and several dendrites. These 2 classes of processes differ in their morphology, in their molecular composition, and in their synaptic polarity (Bartlett and Banker, 1984a, b; Caceres et al., 1984). We examined the events during the first week in culture that lead to the establishment of this characteristic form. Hippocampal cells were obtained from 18 d fetal rats, plated onto polylysine- treated coverslips, and maintained in a serum-free medium. The development of individual cells was followed by sequential photography at daily intervals until both axons and dendrites had been established; identification of the processes was confirmed by immunostaining for MAP2, a dendritic marker. Time-lapse video recording was used to follow the early stages of process formation. Hippocampal neurons acquired their characteristic form by a stereotyped sequence of developmental events. The cells first established several, apparently identical, short processes. After several hours, one of the short processes began to grow very rapidly; it became the axon. The remaining processes began to elongate a few days later and grew at a much slower rate. They became the cell's dendrites. Neurons that arose following mitosis in culture underwent this same sequence of developmental events. In a few instances, 2 processes from a cell exhibited the rapid growth typical of axons, but only one maintained this growth; the other retracted and became a dendrite. Axons branched primarily by the formation of collaterals, not by bifurcation of growth cones. As judged by light microscopy, processes are not specified as axons or dendrites when they arise. The first manifestation of neuronal polarity is the acquisition of axonal characteristics by one of the initial processes; subsequently the remaining processes become dendrites.

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				S. B. Jones, H. Y. Lu, and Q. Lu Abl Tyrosine Kinase Promotes Dendrogenesis by Inducing Actin Cytoskeletal Rearrangements in Cooperation with Rho Family Small GTPases in Hippocampal Neurons J. Neurosci., September 29, 2004; 24(39): 8510 - 8521. [Abstract] [Full Text] [PDF]

				M. Rigoni, G. Schiavo, A. E. Weston, P. Caccin, F. Allegrini, M. Pennuto, F. Valtorta, C. Montecucco, and O. Rossetto Snake presynaptic neurotoxins with phospholipase A2 activity induce punctate swellings of neurites and exocytosis of synaptic vesicles J. Cell Sci., July 15, 2004; 117(16): 3561 - 3570. [Abstract] [Full Text] [PDF]

				G. A. Wayman, S. Kaech, W. F. Grant, M. Davare, S. Impey, H. Tokumitsu, N. Nozaki, G. Banker, and T. R. Soderling Regulation of Axonal Extension and Growth Cone Motility by Calmodulin-Dependent Protein Kinase I J. Neurosci., April 14, 2004; 24(15): 3786 - 3794. [Abstract] [Full Text] [PDF]

				J. Kim, A. Krichevsky, Y. Grad, G. D. Hayes, K. S. Kosik, G. M. Church, and G. Ruvkun Identification of many microRNAs that copurify with polyribosomes in mammalian neurons PNAS, January 6, 2004; 101(1): 360 - 365. [Abstract] [Full Text] [PDF]

				D. J. Hernandez-Deviez, M. G. Roth, J. E. Casanova, and J. M. Wilson ARNO and ARF6 Regulate Axonal Elongation and Branching through Downstream Activation of Phosphatidylinositol 4-Phosphate 5-Kinase {alpha} Mol. Biol. Cell, January 1, 2004; 15(1): 111 - 120. [Abstract] [Full Text] [PDF]

				K. Hayashi, R. Kawai-Hirai, A. Harada, and K. Takata Inhibitory neurons from fetal rat cerebral cortex exert delayed axon formation and active migration in vitro J. Cell Sci., November 1, 2003; 116(21): 4419 - 4428. [Abstract] [Full Text] [PDF]

				H. Wang, V. V. Pineda, G. C. K. Chan, S. T. Wong, L. J. Muglia, and D. R. Storm Type 8 Adenylyl Cyclase Is Targeted to Excitatory Synapses and Required for Mossy Fiber Long-Term Potentiation J. Neurosci., October 29, 2003; 23(30): 9710 - 9718. [Abstract] [Full Text] [PDF]

				L. Dehmelt, F. M. Smart, R. S. Ozer, and S. Halpain The Role of Microtubule-Associated Protein 2c in the Reorganization of Microtubules and Lamellipodia during Neurite Initiation J. Neurosci., October 22, 2003; 23(29): 9479 - 9490. [Abstract] [Full Text] [PDF]

				C. Potel, K. Kaelin, L. Danglot, A. Triller, C. Vannier, and F. Rozenberg Herpes simplex virus type 1 glycoprotein B sorting in hippocampal neurons J. Gen. Virol., October 1, 2003; 84(10): 2613 - 2624. [Abstract] [Full Text] [PDF]

				J. S. Da Silva, M. Medina, C. Zuliani, A. Di Nardo, W. Witke, and C. G. Dotti RhoA/ROCK regulation of neuritogenesis via profilin IIa-mediated control of actin stability J. Cell Biol., September 29, 2003; 162(7): 1267 - 1279. [Abstract] [Full Text] [PDF]

				G. Ruthel and P. J. Hollenbeck Response of Mitochondrial Traffic to Axon Determination and Differential Branch Growth J. Neurosci., September 17, 2003; 23(24): 8618 - 8624. [Abstract] [Full Text] [PDF]

				A. C. Horton and M. D. Ehlers Dual Modes of Endoplasmic Reticulum-to-Golgi Transport in Dendrites Revealed by Live-Cell Imaging J. Neurosci., July 16, 2003; 23(15): 6188 - 6199. [Abstract] [Full Text] [PDF]

				S. Yunoue, H. Tokuo, K. Fukunaga, L. Feng, T. Ozawa, T. Nishi, A. Kikuchi, S. Hattori, J. Kuratsu, H. Saya, et al. Neurofibromatosis Type I Tumor Suppressor Neurofibromin Regulates Neuronal Differentiation via Its GTPase-activating Protein Function toward Ras J. Biol. Chem., July 11, 2003; 278(29): 26958 - 26969. [Abstract] [Full Text] [PDF]

				J. L. Goldberg How does an axon grow? Genes & Dev., April 15, 2003; 17(8): 941 - 958. [Full Text] [PDF]

				T. Stepanova, J. Slemmer, C. C. Hoogenraad, G. Lansbergen, B. Dortland, C. I. De Zeeuw, F. Grosveld, G. van Cappellen, A. Akhmanova, and N. Galjart Visualization of Microtubule Growth in Cultured Neurons via the Use of EB3-GFP (End-Binding Protein 3-Green Fluorescent Protein) J. Neurosci., April 1, 2003; 23(7): 2655 - 2664. [Abstract] [Full Text] [PDF]

				K. H. Pfenninger, L. Laurino, D. Peretti, X. Wang, S. Rosso, G. Morfini, A. Caceres, and S. Quiroga Regulation of membrane expansion at the nerve growth cone J. Cell Sci., April 1, 2003; 116(7): 1209 - 1217. [Abstract] [Full Text] [PDF]

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