J. Cell Biol., Volume 143, Number 5, November 30, 1998 1305-1315

Nervous System Defects of Ankyrin_B (/) Mice Suggest Functional Overlap between the Cell Adhesion Molecule L1 and 440-kD Ankyrin_B in Premyelinated Axons

Paula Scotland,^* Daixing Zhou,^* Helene Benveniste, and Vann Bennett^*

^* Howard Hughes Medical Institute and ^*Departments of Cell Biology, ^*Biochemistry,   Neurobiology, Anesthesiology, and Radiology, Duke University Medical Center, Durham, North Carolina 27710

The L1 CAM family of cell adhesion molecules and the ankyrin family of spectrin-binding proteins are candidates to collaborate in transcellular complexes used in diverse contexts in nervous systems of vertebrates and invertebrates. This report presents evidence for functional coupling between L1 and 440-kD ankyrin_B in premyelinated axons in the mouse nervous system. L1 and 440-kD ankyrin_B are colocalized in premyelinated axon tracts in the developing nervous system and are both down-regulated after myelination. Ankyrin_B (/) mice exhibit a phenotype similar to, but more severe, than L1 (/) mice and share features of human patients with L1 mutations. Ankyrin_B (/) mice exhibit hypoplasia of the corpus callosum and pyramidal tracts, dilated ventricles, and extensive degeneration of the optic nerve, and they die by postnatal day 21. Ankyrin_B (/) mice have reduced L1 in premyelinated axons of long fiber tracts, including the corpus callosum, fimbria, and internal capsule in the brain, and pyramidal tracts and lateral columns of the spinal cord. L1 was evident in the optic nerve at postnatal day 1 but disappeared by postnatal day 7 in mutant mice while NCAM was unchanged. Optic nerve axons of ankyrin_B (/) mice become dilated with diameters up to eightfold greater than normal, and they degenerated by day 20. These findings provide the first evidence for a role of ankyrin_B in the nervous system and support an interaction between 440-kD ankyrin_B and L1 that is essential for maintenance of premyelinated axons in vivo.

CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    What's this?

This article has been cited by other articles:

• Tuvim, M. J., Mospan, A. R., Burns, K. A., Chua, M., Mohler, P. J., Melicoff, E., Adachi, R., Ammar-Aouchiche, Z., Davis, C. W., Dickey, B. F. (2009). Synaptotagmin 2 Couples Mucin Granule Exocytosis to Ca2+ Signaling from Endoplasmic Reticulum. J. Biol. Chem. 284: 9781-9787 [Abstract] [Full Text]  
• Cunha, S. R., Mohler, P. J. (2008). Obscurin Targets Ankyrin-B and Protein Phosphatase 2A to the Cardiac M-line. J. Biol. Chem. 283: 31968-31980 [Abstract] [Full Text]  
• Zhou, S., Opperman, K., Wang, X., Chen, L. (2008). unc-44 Ankyrin and stn-2 {gamma}-Syntrophin Regulate sax-7 L1CAM Function in Maintaining Neuronal Positioning in Caenorhabditis elegans. Genetics 180: 1429-1443 [Abstract] [Full Text]  
• Zonta, B., Tait, S., Melrose, S., Anderson, H., Harroch, S., Higginson, J., Sherman, D. L., Brophy, P. J. (2008). Glial and neuronal isoforms of Neurofascin have distinct roles in the assembly of nodes of Ranvier in the central nervous system. JCB 181: 1169-1177 [Abstract] [Full Text]  
• Sohet, F., Colin, Y., Genetet, S., Ripoche, P., Metral, S., Le Van Kim, C., Lopez, C. (2008). Phosphorylation and Ankyrin-G Binding of the C-terminal Domain Regulate Targeting and Function of the Ammonium Transporter RhBG. J. Biol. Chem. 283: 26557-26567 [Abstract] [Full Text]  
• Liu, X., Spicarova, Z., Rydholm, S., Li, J., Brismar, H., Aperia, A. (2008). Ankyrin B Modulates the Function of Na,K-ATPase/Inositol 1,4,5-Trisphosphate Receptor Signaling Microdomain. J. Biol. Chem. 283: 11461-11468 [Abstract] [Full Text]  
• Buhusi, M., Schlatter, M. C., Demyanenko, G. P., Thresher, R., Maness, P. F. (2008). L1 Interaction with Ankyrin Regulates Mediolateral Topography in the Retinocollicular Projection. J. Neurosci. 28: 177-188 [Abstract] [Full Text]  
• Mohler, P. J., Wehrens, X. H. T. (2007). Mechanisms of Human Arrhythmia Syndromes: Abnormal Cardiac Macromolecular Interactions. Physiology 22: 342-350 [Abstract] [Full Text]  
• Bhasin, N., Cunha, S. R., Mudannayake, M., Gigena, M. S., Rogers, T. B., Mohler, P. J. (2007). Molecular basis for PP2A regulatory subunit B56{alpha} targeting in cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 293: H109-H119 [Abstract] [Full Text]  
• Bao, L., Peirce, J. L., Zhou, M., Li, H., Goldowitz, D., Williams, R. W., Lu, L., Cui, Y. (2007). An integrative genomics strategy for systematic characterization of genetic loci modulating phenotypes. Hum Mol Genet 16: 1381-1390 [Abstract] [Full Text]  
• Boiko, T., Vakulenko, M., Ewers, H., Yap, C. C., Norden, C., Winckler, B. (2007). Ankyrin-Dependent and -Independent Mechanisms Orchestrate Axonal Compartmentalization of L1 Family Members Neurofascin and L1/Neuron-Glia Cell Adhesion Molecule. J. Neurosci. 27: 590-603 [Abstract] [Full Text]  
• Das, A., Base, C., Dhulipala, S., Dubreuil, R. R. (2006). Spectrin functions upstream of ankyrin in a spectrin cytoskeleton assembly pathway. JCB 175: 325-335 [Abstract] [Full Text]  
• Cunha, S. R., Mohler, P. J. (2006). Cardiac ankyrins: Essential components for development and maintenance of excitable membrane domains in heart. Cardiovasc Res 71: 22-29 [Abstract] [Full Text]  
• Ogawa, Y., Schafer, D. P., Horresh, I., Bar, V., Hales, K., Yang, Y., Susuki, K., Peles, E., Stankewich, M. C., Rasband, M. N. (2006). Spectrins and ankyrinB constitute a specialized paranodal cytoskeleton.. J. Neurosci. 26: 5230-5239 [Abstract] [Full Text]  
• Meadows, L.S., Isom, L.L. (2005). Sodium channels as macromolecular complexes: Implications for inherited arrhythmia syndromes. Cardiovasc Res 67: 448-458 [Abstract] [Full Text]  
• Lopez, C., Metral, S., Eladari, D., Drevensek, S., Gane, P., Chambrey, R., Bennett, V., Cartron, J.-P., Le Van Kim, C., Colin, Y. (2005). The Ammonium Transporter RhBG: REQUIREMENT OF A TYROSINE-BASED SIGNAL AND ANKYRIN-G FOR BASOLATERAL TARGETING AND MEMBRANE ANCHORAGE IN POLARIZED KIDNEY EPITHELIAL CELLS. J. Biol. Chem. 280: 8221-8228 [Abstract] [Full Text]  
• Mohler, P. J., Splawski, I., Napolitano, C., Bottelli, G., Sharpe, L., Timothy, K., Priori, S. G., Keating, M. T., Bennett, V. (2004). A cardiac arrhythmia syndrome caused by loss of ankyrin-B function. Proc. Natl. Acad. Sci. USA 101: 9137-9142 [Abstract] [Full Text]  
• Mohler, P. J., Hoffman, J. A., Davis, J. Q., Abdi, K. M., Kim, C.-R., Jones, S. K., Davis, L. H., Roberts, K. F., Bennett, V. (2004). Isoform Specificity among Ankyrins: AN AMPHIPATHIC {alpha}-HELIX IN THE DIVERGENT REGULATORY DOMAIN OF ANKYRIN-B INTERACTS WITH THE MOLECULAR CO-CHAPERONE Hdj1/Hsp40. J. Biol. Chem. 279: 25798-25804 [Abstract] [Full Text]  
• Wiencken-Barger, A.E., Mavity-Hudson, J., Bartsch, U., Schachner, M., Casagrande, V.A. (2004). The Role of L1 in Axon Pathfinding and Fasciculation. Cereb Cortex 14: 121-131 [Abstract] [Full Text]  
• Lencesova, L., O'Neill, A., Resneck, W. G., Bloch, R. J., Blaustein, M. P. (2004). Plasma Membrane-Cytoskeleton-Endoplasmic Reticulum Complexes in Neurons and Astrocytes. J. Biol. Chem. 279: 2885-2893 [Abstract] [Full Text]  
• Nishimura, K., Yoshihara, F., Tojima, T., Ooashi, N., Yoon, W., Mikoshiba, K., Bennett, V., Kamiguchi, H. (2003). L1-dependent neuritogenesis involves ankyrinB that mediates L1-CAM coupling with retrograde actin flow. JCB 163: 1077-1088 [Abstract] [Full Text]  
• Buhusi, M., Midkiff, B. R., Gates, A. M., Richter, M., Schachner, M., Maness, P. F. (2003). Close Homolog of L1 Is an Enhancer of Integrin-mediated Cell Migration. J. Biol. Chem. 278: 25024-25031 [Abstract] [Full Text]  
• Demyanenko, G. P., Maness, P. F. (2003). The L1 Cell Adhesion Molecule Is Essential for Topographic Mapping of Retinal Axons. J. Neurosci. 23: 530-538 [Abstract] [Full Text]  
• Dickson, T. C., Mintz, C. D., Benson, D. L., Salton, S. R.J. (2002). Functional binding interaction identified between the axonal CAM L1 and members of the ERM family. JCB 157: 1105-1112 [Abstract] [Full Text]  
• Mohler, P. J., Gramolini, A. O., Bennett, V. (2002). The Ankyrin-B C-terminal Domain Determines Activity of Ankyrin-B/G Chimeras in Rescue of Abnormal Inositol 1,4,5-Trisphosphate and Ryanodine Receptor Distribution in Ankyrin-B (-/-) Neonatal Cardiomyocytes. J. Biol. Chem. 277: 10599-10607 [Abstract] [Full Text]  
• Shen, Y., Mani, S., Donovan, S. L., Schwob, J. E., Meiri, K. F. (2002). Growth-Associated Protein-43 Is Required for Commissural Axon Guidance in the Developing Vertebrate Nervous System. J. Neurosci. 22: 239-247 [Abstract] [Full Text]  
• Sakurai, T., Lustig, M., Babiarz, J., Furley, A. J.W., Tait, S., Brophy, P. J., Brown, S. A., Brown, L. Y., Mason, C. A., Grumet, M. (2001). Overlapping functions of the cell adhesion molecules Nr-CAM and L1 in cerebellar granule cell development. JCB 154: 1259-1274 [Abstract] [Full Text]  
• More, M. I., Kirsch, F.-P., Rathjen, F. G. (2001). Targeted ablation of NrCAM or ankyrin-B results in disorganized lens fibers leading to cataract formation. JCB 154: 187-196 [Abstract] [Full Text]  
• Bennett, V., Baines, A. J. (2001). Spectrin and Ankyrin-Based Pathways: Metazoan Inventions for Integrating Cells Into Tissues. Physiol. Rev. 81: 1353-1392 [Abstract] [Full Text]  
• Weissleder, R., Mahmood, U. (2001). Molecular Imaging. Radiology 219: 316-333 [Abstract] [Full Text]  
• Needham, L. K., Thelen, K., Maness, P. F. (2001). Cytoplasmic Domain Mutations of the L1 Cell Adhesion Molecule Reduce L1-Ankyrin Interactions. J. Neurosci. 21: 1490-1500 [Abstract] [Full Text]  
• Kenwrick, S., Watkins, A., Angelis, E. D. (2000). Neural cell recognition molecule L1: relating biological complexity to human disease mutations. Hum Mol Genet 9: 879-886 [Abstract] [Full Text]  
• Bennett, P. B. (2000). Anchors Aweigh! : Ion Channels, Cytoskeletal Proteins, and Cellular Excitability. Circ. Res. 86: 367-368 [Full Text]  
• Chauhan, V. S., Tuvia, S., Buhusi, M., Bennett, V., Grant, A. O. (2000). Abnormal Cardiac Na+ Channel Properties and QT Heart Rate Adaptation in Neonatal AnkyrinB Knockout Mice. Circ. Res. 86: 441-447 [Abstract] [Full Text]  
• Barallobre, M., Del Rio, J., Alcantara, S, Borrell, V, Aguado, F, Ruiz, M, Carmona, M., Martin, M, Fabre, M, Yuste, R, Tessier-Lavigne, M, Soriano, E (2000). Aberrant development of hippocampal circuits and altered neural activity in netrin 1-deficient mice. Development 127: 4797-4810 [Abstract]  
• Tuvia, S., Buhusi, M., Davis, L., Reedy, M., Bennett, V. (1999). Ankyrin-B Is Required for Intracellular Sorting of Structurally Diverse Ca2+ Homeostasis Proteins. JCB 147: 995-1008 [Abstract] [Full Text]  
• Haney, C.A., Sahenk, Z., Li, C., Lemmon, V.P., Roder, J., Trapp, B.D. (1999). Heterophilic Binding of L1 on Unmyelinated Sensory Axons Mediates Schwann Cell Adhesion and Is Required for Axonal Survival. JCB 146: 1173-1184 [Abstract] [Full Text]  
• Bearer, C. F., Swick, A. R., O'Riordan, M. A., Cheng, G. (1999). Ethanol inhibits L1-mediated neurite outgrowth in postnatal rat cerebellar granule cells.. J. Biol. Chem. 274: 20046-20046 [Full Text]  
• Faivre-Sarrailh, C, Falk, J, Pollerberg, E, Schachner, M, Rougon, G (1999). NrCAM, cerebellar granule cell receptor for the neuronal adhesion molecule F3, displays an actin-dependent mobility in growth cones. J. Cell Sci. 112: 3015-3027 [Abstract]  
• Jefford, G., Dubreuil, R. R. (2000). Receptor Clustering Drives Polarized Assembly of Ankyrin. J. Biol. Chem. 275: 27726-27732 [Abstract] [Full Text]  

Home | Help | Feedback | Subscriptions | Archive | Search | Table of Contents