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Spectrin and Ankyrin-Based Pathways: Metazoan Inventions for Integrating Cells Into Tissues
Abstract
The spectrin-based membrane skeleton of the humble mammalian erythrocyte has provided biologists with a set of interacting proteins with diverse roles in organization and survival of cells in metazoan organisms. This review deals with the molecular physiology of spectrin, ankyrin, which links spectrin to the anion exchanger, and two spectrin-associated proteins that promote spectrin interactions with actin: adducin and protein 4.1. The lack of essential functions for these proteins in generic cells grown in culture and the absence of their genes in the yeast genome have, until recently, limited advances in understanding their roles outside of erythrocytes. However, completion of the genomes of simple metazoans and application of homologous recombination in mice now are providing the first glimpses of the full scope of physiological roles for spectrin, ankyrin, and their associated proteins. These functions now include targeting of ion channels and cell adhesion molecules to specialized compartments within the plasma membrane and endoplasmic reticulum of striated muscle and the nervous system, mechanical stabilization at the tissue level based on transcellular protein assemblies, participation in epithelial morphogenesis, and orientation of mitotic spindles in asymmetric cell divisions. These studies, in addition to stretching the erythrocyte paradigm beyond recognition, also are revealing novel cellular pathways essential for metazoan life. Examples are ankyrin-dependent targeting of proteins to excitable membrane domains in the plasma membrane and the Ca 2+homeostasis compartment of the endoplasmic reticulum. Exciting questions for the future relate to the molecular basis for these pathways and their roles in a clinical context, either as the basis for disease or more positively as therapeutic targets.
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The structure and function of band 3 (AE1): Recent developments (Review)
Tanner, M. J. A. (1997) · Molecular Membrane Biology · doi:10.3109/09687689709048178 · Cited by 202
α-spectrin is required for germline cell division and differentiation in the Drosophila ovary
Cuevas, M. D., Lee, J. K., & Spradling, A. C. (1996) · Development · doi:10.1242/dev.122.12.3959 · Cited by 199
Kuhlman, P. A., Hughes, C. A., Bennett, V., & Fowler, V. M. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.14.7986 · Cited by 198
Self-citationMarfatia, S. M., Lue, R. A., Branton, D., & Chishti, A. H. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.2.715 · Cited by 196
Partial deficiency of erythrocyte spectrin in hereditary spherocytosis
Agre, P., Casella, J. F., Zinkham, W. H., McMillan, C., & Bennett, V. (1985) · Nature · doi:10.1038/314380a0 · Cited by 191
Self-citationLamb, R. S., Ward, R. E., Schweizer, L., & Fehon, R. G. (1998) · Molecular Biology of the Cell · doi:10.1091/mbc.9.12.3505 · Cited by 189
Brain spectrin binding to the NMDA receptor is regulated by phosphorylation, calcium and calmodulin
Wechsler, A., & Teichberg, V. I. (1998) · The EMBO Journal · doi:10.1093/emboj/17.14.3931 · Cited by 188
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Scotland, P., Zhou, D., Benveniste, H., & Bennett, V. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.143.5.1305 · Cited by 185
Self-citationA structural model of human erythrocyte protein 4.1.
Leto, T. L., & Marchesi, V. T. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)43089-4 · Cited by 181
Mouse T lymphoma cells contain a transmembrane glycoprotein (GP85) that binds ankyrin
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Neuregulin receptors, erbB3 and erbB4, are localized at neuromuscular synapses.
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Integrators of the Cytoskeleton that Stabilize Microtubules
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Ankyrin binds to the 15th repetitive unit of erythroid and nonerythroid beta-spectrin.
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Regulation of Nerve Growth Mediated by Inositol 1,4,5-Trisphosphate Receptors in Growth Cones
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Deficient Red-Cell Spectrin in Severe, Recessively Inherited Spherocytosis
Agre, P., Orringer, E. P., & Bennett, V. (1982) · New England Journal of Medicine · doi:10.1056/nejm198205133061906 · Cited by 171
Self-citationMatsuoka, Y., Hughes, C. A., & Bennett, V. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.41.25157 · Cited by 171
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Davis, J. Q., McLaughlin, T., & Bennett, V (1993) · The Journal of cell biology · doi:10.1083/jcb.121.1.121 · Cited by 170
Self-citationMarfatia, S. M., Lue, R. A., Branton, D., & Chishti, A. H. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)37012-6 · Cited by 166
Adducin: a Physical Model with Implications for Function in Assembly of Spectrin-Actin Complexes
Hughes, C. A., & Bennett, V. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.32.18990 · Cited by 166
Self-citationBourguignon, L. Y., Jin, H., Iida, N., Brandt, N. R., & Zhang, S. H. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53175-6 · Cited by 165
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An Epidermal Plakin That Integrates Actin and Microtubule Networks at Cellular Junctions
Karakesisoglou, I., Yang, Y., & Fuchs, E. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.149.1.195 · Cited by 164
cDNA sequence for human erythrocyte ankyrin.
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Kordeli, E., Davis, J., Trapp, B., & Bennett, V (1990) · The Journal of cell biology · doi:10.1083/jcb.110.4.1341 · Cited by 160
Self-citationErythroid and nonerythroid spectrins
Winkelmann, J., & Forget, B. (1993) · Blood · doi:10.1182/blood.v81.12.3173.3173 · Cited by 159
Localization of sodium channels in axon hillocks and initial segments of retinal ganglion cells.
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Adducin: Ca++-dependent association with sites of cell-cell contact.
Kaiser, H. W., O’Keefe, E. J., & Bennett, V. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.109.2.557 · Cited by 157
Self-citationMcGough, A. M., Way, M., & DeRosier, D. J. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.126.2.433 · Cited by 157
Regulatory domains of erythrocyte ankyrin.
Hall, T. G., & Bennett, V. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)60995-0 · Cited by 156
Self-citationStructural comparisons of calponin homology domains: implications for actin binding
Bañuelos, S., Saraste, M., & Djinović‐Carugo, K. (1998) · Structure · doi:10.1016/s0969-2126(98)00141-5 · Cited by 156
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Otto, E., Kunimoto, M., McLaughlin, T. M., & Bennett, V. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.114.2.241 · Cited by 153
Self-citationOut of the ER—outfitters, escorts and guides
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The Clustering of Axonal Sodium Channels during Development of the Peripheral Nervous System
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The calmodulin-binding site in alpha-fodrin is near the calcium-dependent protease-I cleavage site.
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Regulation of actin filament length in erythrocytes and striated muscle
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The single CH domain of calponin is neither sufficient nor necessary for F-actin binding
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Does Vav bind to F‐actin through a CH domain?
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sma-1 encodes a βH-spectrin homolog required for Caenorhabditis elegans morphogenesis
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Cell shape and interaction defects in alpha-spectrin mutants of Drosophila melanogaster.
Lee, J. K., Coyne, R. S., Dubreuil, R. R., Goldstein, L. S. B., & Branton, D. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.123.6.1797 · Cited by 145
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A Novel Neuron-Enriched Homolog of the Erythrocyte Membrane Cytoskeletal Protein 4.1
Walensky, L. D., Blackshaw, S., Liao, D., Watkins, C. C., Weier, H.-U. G., Parra, M., Huganir, R. L., Conboy, J. G., Mohandas, N., & Snyder, S. H. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-15-06457.1999 · Cited by 144
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Correas, I., Leto, T. L., Speicher, D. W., & Marchesi, V. T. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)35783-6 · Cited by 142
Characterization of the Interaction between Protein 4.1R and ZO-2
Mattagajasingh, S. N., Huang, S.-C., Hartenstein, J. S., & Benz, E. J. J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m004578200 · Cited by 142
Ryanodine Receptor-Ankyrin Interaction Regulates Internal Ca2+ Release in Mouse T-lymphoma Cells
Bourguignon, L., Chu, A. J., Jin, H., & Brandt, N. R. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.30.17917 · Cited by 142
A widely expressed βIII spectrin associated with Golgi and cytoplasmic vesicles
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Primary structure and domain organization of human alpha and beta adducin.
Joshi, R., Gilligan, D. M., Otto, E., McLaughlin, T. M., & Bennett, V. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.115.3.665 · Cited by 141
Self-citationLocalization of sodium channels in cultured neural cells
Catterall, W. A. (1981) · Journal of Neuroscience · doi:10.1523/jneurosci.01-07-00777.1981 · Cited by 140
Bellen, H. J., Lu, Y.-L., Beckstead, R. B., & Bhat, M. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01267-3 · Cited by 137
Immunoreactive forms of human erythrocyte ankyrin are present in diverse cells and tissues
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The role of ankyrin and spectrin in membrane transport and domain formation
Matteis, M. A. D., & Morrow, J. S. (1998) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(98)80071-9 · Cited by 131
Zhang, X., & Bennett, V. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.6.1571 · Cited by 131
Self-citationJoseph, S. K., & Samanta, S. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53276-2 · Cited by 130
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Neuroglian-mediated cell adhesion induces assembly of the membrane skeleton at cell contact sites.
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Tuvia, S., Garver, T. D., & Bennett, V. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.24.12957 · Cited by 129
Self-citationThe cardiac Na+-Ca2+ exchanger binds to the cytoskeletal protein ankyrin
Li, Z. P., Burke, E. P., Frank, J. S., Bennett, V., & Philipson, K. D. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)50223-x · Cited by 128
Self-citationThe structure of an actin-crosslinking domain from human fimbrin
Goldsmith, S. C., Pokala, N., Shen, W., et al. (1997) · Nature Structural Biology · doi:10.1038/nsb0997-708 · Cited by 128
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Ankyrin-B Is Required for Intracellular Sorting of Structurally Diverse Ca2+ Homeostasis Proteins
Tuvia, S., Buhusi, M., Davis, L., Reedy, M., & Bennett, V. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.147.5.995 · Cited by 127
Self-citationBennett, V., & Davis, J. Q. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.12.7550 · Cited by 127
Self-citationHanein, D., Volkmann, N., Goldsmith‐Fischman, S., Michon, A., Lehman, W., Craig, R. W., DeRosier, D. J., Almo, S. C., & Matsudaira, P. T. (1998) · Nature Structural Biology · doi:10.1038/1828 · Cited by 127
Structural Requirements for Association of Neurofascin with Ankyrin
Zhang, X., Davis, J. Q., Carpenter, S., & Bennett, V. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.46.30785 · Cited by 126
Self-citationMutations in β-Spectrin Disrupt Axon Outgrowth and Sarcomere Structure
Hammarlund, M., Davis, W. S., & Jørgensen, E. M. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.149.4.931 · Cited by 126
The identification and sequence of the actin-binding domain of human red blood cell beta-spectrin.
Karinch, A. M., Zimmer, W. E., & Goodman, S. R. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)38474-1 · Cited by 125
Regulation of CD44-Protein 4.1 Interaction by Ca2+and Calmodulin
Nunomura, W., Takakuwa, Y., Tokimitsu, R., Krauss, S. W., Kawashima, M., & Mohandas, N. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.48.30322 · Cited by 125
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A Nonerythroid Isoform of Protein 4.1R Interacts with the Nuclear Mitotic Apparatus (NuMA) Protein
Mattagajasingh, S. N., Huang, S.-C., Hartenstein, J. S., Snyder, M. P., Marchesi, V. T., & Benz, E. J. J. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.145.1.29 · Cited by 124
Kordeli, E., & Bennett, V. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.114.6.1243 · Cited by 123
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Mohler, P. J., Schott, J.-J., Gramolini, A. O., Dilly, K. W., Guatimosim, S., duBell, W. H., Song, L.-S., Haurogné, K., Kyndt, F., Ali, M. E., et al. (2003) · Nature · doi:10.1038/nature01335 · Cited by 957
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Metadata
- Authors
- Bennett, V., & Baines, A. J.
- Venue
- Physiological Reviews
- Publisher
- American Physiological Society
- Published
- 2001-07-01
- Volume
- 81
- Issue
- 3
- Pages
- 1353-1392
- ISSN
- 0031-9333 (ISSN-L)
- 1522-1210
- OpenAlex
- W2131255875
- Cited by
- 930
- References
- 339
- FWCI
- 2.60
- Type
- journal article
- Language
- en
- Open access
- closed
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.