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Physiol. Rev. 81: 1353-1392, 2001;
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Physiological Reviews, Vol. 81, No. 3, July 2001, pp. 1353-1392
Copyright ©2001 by the American Physiological Society

Spectrin and Ankyrin-Based Pathways: Metazoan Inventions for Integrating Cells Into Tissues

Vann Bennett and Anthony J. Baines

Howard Hughes Medical Institute and Departments of Cell Biology and Biochemistry, Duke University Medical Center, Durham, North Carolina; and Department of Biosciences, University of Kent, Canterbury, United Kingdom

Bennett, Vann and Anthony J. Baines. Spectrin and Ankyrin-Based Pathways: Metazoan Inventions for Integrating Cells Into Tissues. Physiol. Rev. 81: 1353-1392, 2001.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 Ca2+ 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 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., March 4, 2005; 280(9): 8221 - 8228.
[Abstract] [Full Text] [PDF]

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 Mol. Biol. CellHome page
H.-H. Lim and C.-S. Park
Identification and Functional Characterization of Ankyrin-Repeat Family Protein ANKRA as a Protein Interacting with BKCa Channel
Mol. Biol. Cell, March 1, 2005; 16(3): 1013 - 1025.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
E. Y. Wong, J. Lin, B. G. Forget, D. M. Bodine, and P. G. Gallagher
Sequences Downstream of the Erythroid Promoter Are Required for High Level Expression of the Human {alpha}-Spectrin Gene
J. Biol. Chem., December 31, 2004; 279(53): 55024 - 55033.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
C. Southwood, C. He, J. Garbern, J. Kamholz, E. Arroyo, and A. Gow
CNS Myelin Paranodes Require Nkx6-2 Homeoprotein Transcriptional Activity for Normal Structure
J. Neurosci., December 15, 2004; 24(50): 11215 - 11225.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
M. De Rycker and C. M. Price
Tankyrase Polymerization Is Controlled by Its Sterile Alpha Motif and Poly(ADP-Ribose) Polymerase Domains
Mol. Cell. Biol., November 15, 2004; 24(22): 9802 - 9812.
[Abstract] [Full Text] [PDF]

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 JCBHome page
S. Lacas-Gervais, J. Guo, N. Strenzke, E. Scarfone, M. Kolpe, M. Jahkel, P. De Camilli, T. Moser, M. N. Rasband, and M. Solimena
{beta}IV{Sigma}1 spectrin stabilizes the nodes of Ranvier and axon initial segments
J. Cell Biol., October 4, 2004; (2004) jcb.200408007.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
P. J. Mohler, W. Yoon, and V. Bennett
Ankyrin-B Targets {beta}2-Spectrin to an Intracellular Compartment in Neonatal Cardiomyocytes
J. Biol. Chem., September 17, 2004; 279(38): 40185 - 40193.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. J. Hartshorne, M. Ito, and F. Erdodi
Role of Protein Phosphatase Type 1 in Contractile Functions: Myosin Phosphatase
J. Biol. Chem., September 3, 2004; 279(36): 37211 - 37214.
[Full Text] [PDF]

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 J. Neurosci.Home page
Y. Yang, S. Lacas-Gervais, D. K. Morest, M. Solimena, and M. N. Rasband
{beta}IV Spectrins Are Essential for Membrane Stability and the Molecular Organization of Nodes of Ranvier
J. Neurosci., August 18, 2004; 24(33): 7230 - 7240.
[Abstract] [Full Text] [PDF]

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 JCBHome page
M.-P. Fache, A. Moussif, F. Fernandes, P. Giraud, J. J. Garrido, and B. Dargent
Endocytotic elimination and domain-selective tethering constitute a potential mechanism of protein segregation at the axonal initial segment
J. Cell Biol., August 16, 2004; 166(4): 571 - 578.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
P. J. Mohler, I. Splawski, C. Napolitano, G. Bottelli, L. Sharpe, K. Timothy, S. G. Priori, M. T. Keating, and V. Bennett
A cardiac arrhythmia syndrome caused by loss of ankyrin-B function
PNAS, June 15, 2004; 101(24): 9137 - 9142.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
P. J. Mohler, J. A. Hoffman, J. Q. Davis, K. M. Abdi, C.-R. Kim, S. K. Jones, L. H. Davis, K. F. Roberts, and V. Bennett
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., June 11, 2004; 279(24): 25798 - 25804.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
S. P. Koushika, A. M. Schaefer, R. Vincent, J. H. Willis, B. Bowerman, and M. L. Nonet
Mutations in Caenorhabditis elegans Cytoplasmic Dynein Components Reveal Specificity of Neuronal Retrograde Cargo
J. Neurosci., April 21, 2004; 24(16): 3907 - 3916.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
K. Kizhatil and V. Bennett
Lateral Membrane Biogenesis in Human Bronchial Epithelial Cells Requires 190-kDa Ankyrin-G
J. Biol. Chem., April 16, 2004; 279(16): 16706 - 16714.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
P. J. Mohler, J. Q. Davis, L. H. Davis, J. A. Hoffman, P. Michaely, and V. Bennett
Inositol 1,4,5-Trisphosphate Receptor Localization and Stability in Neonatal Cardiomyocytes Requires Interaction with Ankyrin-B
J. Biol. Chem., March 26, 2004; 279(13): 12980 - 12987.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S.-H. Chen, M. R. Bubb, E. G. Yarmola, J. Zuo, J. Jiang, B. S. Lee, M. Lu, S. L. Gluck, I. R. Hurst, and L. S. Holliday
Vacuolar H+-ATPase Binding to Microfilaments: REGULATION IN RESPONSE TO PHOSPHATIDYLINOSITOL 3-KINASE ACTIVITY AND DETAILED CHARACTERIZATION OF THE ACTIN-BINDING SITE IN SUBUNIT B
J. Biol. Chem., February 27, 2004; 279(9): 7988 - 7998.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
J. A. Williams, B. MacIver, E. A. Klipfell, and G. H. Thomas
The C-terminal domain of Drosophila {beta}Heavy-spectrin exhibits autonomous membrane association and modulates membrane area
J. Cell Sci., February 15, 2004; 117(5): 771 - 782.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
R. I. MacDonald and J. A. Cummings
Stabilities of folding of clustered, two-repeat fragments of spectrin reveal a potential hinge in the human erythroid spectrin tetramer
PNAS, February 10, 2004; 101(6): 1502 - 1507.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
V. Sytnyk, I. Leshchyns'ka, A. Dityatev, and M. Schachner
Trans-Golgi network delivery of synaptic proteins in synaptogenesis
J. Cell Sci., January 22, 2004; 117(3): 381 - 388.
[Abstract] [Full Text] [PDF]

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 J. Am. Soc. Nephrol.Home page
M. Del Rio, A. Imam, M. DeLeon, G. Gomez, J. Mishra, Q. Ma, S. Parikh, and P. Devarajan
The Death Domain of Kidney Ankyrin Interacts with Fas and Promotes Fas-Mediated Cell Death in Renal Epithelia
J. Am. Soc. Nephrol., January 1, 2004; 15(1): 41 - 51.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
V. Nicolas, C. Le Van Kim, P. Gane, C. Birkenmeier, J.-P. Cartron, Y. Colin, and I. Mouro-Chanteloup
Rh-RhAG/Ankyrin-R, a New Interaction Site between the Membrane Bilayer and the Red Cell Skeleton, Is Impaired by Rhnull-associated Mutation
J. Biol. Chem., July 3, 2003; 278(28): 25526 - 25533.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. Buhusi, B. R. Midkiff, A. M. Gates, M. Richter, M. Schachner, and P. F. Maness
Close Homolog of L1 Is an Enhancer of Integrin-mediated Cell Migration
J. Biol. Chem., June 27, 2003; 278(27): 25024 - 25031.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Park, M. S. Caffrey, M. E. Johnson, and L. W.-M. Fung
Solution Structural Studies on Human Erythrocyte {alpha}-Spectrin Tetramerization Site
J. Biol. Chem., June 6, 2003; 278(24): 21837 - 21844.
[Abstract] [Full Text] [PDF]

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 JCBHome page
I. Leshchyns'ka, V. Sytnyk, J. S. Morrow, and M. Schachner
Neural cell adhesion molecule (NCAM) association with PKC{beta}2 via {beta}I spectrin is implicated in NCAM-mediated neurite outgrowth
J. Cell Biol., May 12, 2003; 161(3): 625 - 639.
[Abstract] [Full Text] [PDF]

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 Mol. Interv.Home page
S. Yong, X. Tian, and Q. Wang
LQT4 Gene: The "Missing" Ankyrin
Mol. Interv., May 1, 2003; 3(3): 131 - 136.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
T. Boiko, A. Van Wart, J. H. Caldwell, S. R. Levinson, J. S. Trimmer, and G. Matthews
Functional Specialization of the Axon Initial Segment by Isoform-Specific Sodium Channel Targeting
J. Neurosci., March 15, 2003; 23(6): 2306 - 2313.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. H. Chang and P. S. Low
Identification of a Critical Ankyrin-binding Loop on the Cytoplasmic Domain of Erythrocyte Membrane Band 3 by Crystal Structure Analysis and Site-directed Mutagenesis
J. Biol. Chem., February 21, 2003; 278(9): 6879 - 6884.
[Abstract] [Full Text] [PDF]


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