Laminin selectively enhances axonal growth and accelerates the development of polarity by hippocampal neurons in culture.

We have examined the effects of laminin on the morphological development of embryonic rat hippocampal neurons maintained in tissue culture. Forty-eight hours after plating, neurons grown on a polylysine-coated substrate had become polarized, typically having one long axon and 4 or 5 minor processes. Adsorption of laminin to the substrate did not cause changes in the number of axons extended by hippocampal neurons but did cause significant increases in the length of the axonal plexus and in axonal branching. In contrast to its effects on axons, laminin did not influence the number, length, or branching of the minor processes that eventually become dendrites or the morphology of definite dendrites as assessed after 7 days in culture. In addition to selectively enhancing axonal growth, laminin greatly increased the rate of polarization of hippocampal neurons such that most became polarized within 18 h. Analysis of the time course of laminin's effects revealed that the acceleration of polarization was not associated with a change in the time of initial process formation, but rather with a selective stimulation of the growth of the longest process at all times from the 12th through the 48th h in vitro. These data suggest that even though the basic shape of hippocampal neurons may be intrinsically programmed, critical aspects of their morphological development may be modulated by extracellular matrix molecules such as laminin.

[1]  J. Skene Axonal growth-associated proteins. , 1989, Annual review of neuroscience.

[2]  H. Kleinman,et al.  Two different laminin domains mediate the differentiation of human endothelial cells into capillary-like structures in vitro , 1989, Cell.

[3]  L. Reichardt,et al.  Embryonic neural retinal cell response to extracellular matrix proteins: developmental changes and effects of the cell substratum attachment antibody (CSAT) , 1987, The Journal of cell biology.

[4]  D. Higgins,et al.  The NC1 domain of type IV collagen promotes axonal growth in sympathetic neurons through interaction with the alpha 1 beta 1 integrin , 1991, The Journal of cell biology.

[5]  G. Banker,et al.  The establishment of polarity by hippocampal neurons in culture , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  G. Banker,et al.  Experimentally induced alteration in the polarity of developing neurons , 1987, Nature.

[7]  O. Steward,et al.  MAP2 is localized to the dendrites of hippocampal neurons which develop in culture. , 1984, Brain research.

[8]  S. B. Kater,et al.  Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  H. Thoenen,et al.  The heparin‐binding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival. , 1984, The EMBO journal.

[10]  D. Higgins,et al.  Morphological differentiation of embryonic rat sympathetic neurons in tissue culture. I. Conditions under which neurons form axons but not dendrites. , 1988, Developmental biology.

[11]  V. Quaranta,et al.  Laminin receptors in the retina: sequence analysis of the chick integrin alpha 6 subunit. Evidence for transcriptional and posttranslational regulation , 1991, The Journal of cell biology.

[12]  H. Kleinman,et al.  Laminin neural activity and binding proteins. , 1989, Developmental neuroscience.

[13]  E. Rodriguez-Boulan,et al.  Morphogenesis of the polarized epithelial cell phenotype. , 1989, Science.

[14]  J. Sanes,et al.  Extracellular matrix molecules that influence neural development. , 1989, Annual review of neuroscience.

[15]  A. Prochiantz,et al.  Influence of extracellular matrix proteins on the expression of neuronal polarity. , 1989, Development.

[16]  P C Letourneau,et al.  Growth cone guidance by substrate-bound laminin pathways is correlated with neuron-to-pathway adhesivity. , 1988, Developmental biology.

[17]  G. Banker,et al.  Experimental observations on the development of polarity by hippocampal neurons in culture , 1989, The Journal of cell biology.

[18]  E Ruoslahti,et al.  Laminin promotes neuritic regeneration from cultured peripheral and central neurons , 1983, The Journal of cell biology.

[19]  D. Higgins,et al.  Thrombospondin promotes process outgrowth in neurons from the peripheral and central nervous systems. , 1992, Developmental biology.

[20]  H. Thoenen,et al.  Laminin increases both levels and activity of tyrosine hydroxylase in calf adrenal chromaffin cells , 1986, The Journal of cell biology.

[21]  G. Banker,et al.  The establishment of polarity by hippocampal neurons: the relationship between the stage of a cell's development in situ and its subsequent development in culture. , 1989, Developmental biology.

[22]  G. Banker,et al.  An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. I. Cells which develop without intercellular contacts , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  G. Banker,et al.  An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. II. Synaptic relationships , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  G. Banker,et al.  Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  G. Banker,et al.  Rapid changes in the distribution of GAP-43 correlate with the expression of neuronal polarity during normal development and under experimental conditions , 1990, The Journal of cell biology.

[26]  W M Cowan,et al.  Further observations on hippocampal neurons in dispersed cell culture , 1979, The Journal of comparative neurology.

[27]  D. Higgins,et al.  Morphological differentiation of embryonic rat sympathetic neurons in tissue culture. II. Serum promotes dendritic growth. , 1988, Developmental biology.

[28]  W. Maxwell Cowan,et al.  Rat hippocampal neurons in dispersed cell culture , 1977, Brain Research.

[29]  D. Higgins,et al.  Laminin and a basement membrane extract have different effects on axonal and dendritic outgrowth from embryonic rat sympathetic neurons in vitro. , 1989, Developmental biology.

[30]  D. Higgins,et al.  Glial cells promote dendritic development in rat sympathetic neurons in vitro , 1988, Glia.

[31]  P C Letourneau,et al.  Neurite extension by peripheral and central nervous system neurons in response to substratum-bound fibronectin and laminin. , 1983, Developmental biology.

[32]  D. Monard,et al.  Glia-derived nexin potentiates neurite extension in hippocampal pyramidal cells in vitro. , 1990, Developmental neuroscience.

[33]  M. Bunge,et al.  Linkage between axonal ensheathment and basal lamina production by Schwann cells. , 1986, Annual review of neuroscience.

[34]  A. Prochiantz,et al.  Rat mesencephalic neurons in culture exhibit different morphological traits in the presence of media conditioned on mesencephalic or striatal astroglia. , 1988, Developmental biology.

[35]  T. Jessell,et al.  Axon guidance and the patterning of neuronal projections in vertebrates. , 1988, Science.

[36]  S. Denis‐Donini,et al.  Interneurons versus efferent neurons: heterogeneity in their neurite outgrowth response to glia from several brain regions. , 1988, Developmental biology.