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The Journal of Neuroscience, May 10, 2006, 26(19):5230-5239; doi:10.1523/JNEUROSCI.0425-06.2006

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Cellular/Molecular
Spectrins and AnkyrinB Constitute a Specialized Paranodal Cytoskeleton

Yasuhiro Ogawa,^1 * Dorothy P. Schafer,^1 * Ido Horresh,² Vered Bar,² Kimberly Hales,¹ Yang Yang,¹ Keiichiro Susuki,¹ Elior Peles,² Michael C. Stankewich,³ and Matthew N. Rasband¹

¹Department of Neuroscience, University of Connecticut Health Center, Farmington, Connecticut 06030, ²Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel 76100, and ³Department of Pathology, Yale University, New Haven, Connecticut 06520

Correspondence should be addressed to either of the following: Dr. Matthew N. Rasband, Department of Neuroscience, University of Connecticut Health Center, 263 Farmington Avenue, Farmington, CT 06032, Email: rasband{at}uchc.edu

Dr. Michael C. Stankewich, Department of Pathology, Yale University School of Medicine, P.O. Box 208023, 310 Cedar Street, BML 150, New Haven, CT 06520, michael.stankewich{at}yale.edu

Paranodal junctions of myelinated nerve fibers are important for saltatory conduction and function as paracellular and membrane protein diffusion barriers flanking nodes of Ranvier. The formation of these specialized axoglial contacts depends on the presence of three cell adhesion molecules: neurofascin 155 on the glial membrane and a complex of Caspr and contactin on the axon. We isolated axonal and glial membranes highly enriched in these paranodal proteins and then used mass spectrometry to identify additional proteins associated with the paranodal axoglial junction. This strategy led to the identification of three novel components of the paranodal cytoskeleton: ankyrinB, II spectrin, and II spectrin. Biochemical and immunohistochemical analyses revealed that these proteins associate with protein 4.1B in a macromolecular complex that is concentrated at central and peripheral paranodal junctions in the adult and during early myelination. Furthermore, we show that the paranodal localization of ankyrinB is disrupted in Caspr-null mice with aberrant paranodal junctions, demonstrating that paranodal neuron–glia interactions regulate the organization of the underlying cytoskeleton. In contrast, genetic disruption of the juxtaparanodal protein Caspr2 or the nodal cytoskeletal protein IV spectrin did not alter the paranodal cytoskeleton. Our results demonstrate that the paranodal junction contains specialized cytoskeletal components that may be important to stabilize axon–glia interactions and contribute to the membrane protein diffusion barrier found at paranodes.

Key words: myelin; node of Ranvier; axoglial junction; scaffold; ankyrin; paranode

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Received Jan. 30, 2006; revised March 22, 2006; accepted March 29, 2006.

Correspondence should be addressed to either of the following: Dr. Matthew N. Rasband, Department of Neuroscience, University of Connecticut Health Center, 263 Farmington Avenue, Farmington, CT 06032, Email: rasband{at}uchc.edu

Dr. Michael C. Stankewich, Department of Pathology, Yale University School of Medicine, P.O. Box 208023, 310 Cedar Street, BML 150, New Haven, CT 06520, michael.stankewich{at}yale.edu

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