Expression and assembly of the erythroid membrane‐skeletal proteins ankyrin (goblin) and spectrin in the morphogenesis of chicken neurons

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Abstract
The membrane‐skeleton of adult chicken neurons in the cerebellum and optic system is composed of polypeptides structurally and functionally related to the erythroid proteins spectrin and ankyrin, respectively. Neuronal spectrin comprises two distinct complexes that share a common α subunit (Mr 240,000) but which have structurally distinct polymorphic subunits (β′β spectrin; Mr 220/225,000; γ spectrin, Mr 235,000): the brain‐specific form (αγ spectrin or fodrin) and an erythrocyte‐specific form (αβ′β spectrin). Two structurally related isoforms of ankyrin have also been identified and are termed α (Mr 260,000) and β (Mr 237,000) ankyrin. Immunofluorescence demonstrates that the variants of spectrin and ankyrin, respectively, have different distributions within neurons. On the one hand, αγ spectrin and β ankyrin are present throughout the neuron, in the perikaryon, dendrites and axon, whereas αβ′ spectrin and α ankyrin are localized exclusively in the perikaryon and dendrites where they are actively segregated from αγ spectrin and other components of axonal transport. This asymmetric distribution of spectrin and ankyrin isoforms is established in distinct stages during neuronal morphogenesis. Early in cerebellar and retinal development, αγ spectrin is expressed in mitotic cells. Subsequently β ankyrin and αγ spectrin are co‐expressed in postmitotic cells and gradually accumulate on the plasma membrane in a uniform pattern throughout the neuron during the phase of cell growth. At the onset of synaptogenesis and the cessation of cell growth, their levels of synthesis decline sharply while the assembled proteins remained as stable membrane components. Concomitantly, there is a dramatic induction in the accumulation of α ankyrin and αβ′ spectrin, whose assembly is limited to the plasma membrane of the perikarya and dendrites. These results demonstrate that two successive, developmentally regulated programs of ankyrin and spectrin expression and patterning on the plasma membrane are involved in the assembly of the spectrin‐based asymmetry in the neuronal membrane‐skeleton, and that their asymmetric distribution is actively maintained throughout the life of the neuron.