Evolution of spectrin function in cytoskeletal and membrane networks

Biochemical Society Transactions

Volumn 37, Issue 4, 2009, Pages 796-803

  Baines, Anthony J ^a  

^a UNIVERSITY OF KENT   (United Kingdom)

Author keywords

Anaemia; Ankyrin; Evolution; Genetic disease; Protein 4.1; Spectrin

Indexed keywords

ACTIN; ANKYRIN; ERYTHROCYTE BAND 4.1 PROTEIN; EXCITATORY AMINO ACID TRANSPORTER 4; FODRIN; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; REGULATOR PROTEIN; SODIUM CHANNEL; SPECTRIN; SPECTRIN BETA; SPECTRIN BETA HEAVY; SPETRIN BETA1; SPETRIN BETA2; TETRAMER; UNCLASSIFIED DRUG; CYTOSKELETON PROTEIN; MEMBRANE PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE TRANSPORT; CONFERENCE PAPER; CYTOSKELETON; DNA SPLICING; ERYTHROCYTE; FLAGELLATE; GENE DUPLICATION; GENE REARRANGEMENT; GENETIC ANALYSIS; MOLECULAR EVOLUTION; MONOSIGA BREVICOLLIS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; ANIMAL; BIOLOGICAL MODEL; CLASSIFICATION; GENETICS; METABOLISM; PHYLOGENY; REVIEW;

ANIMALIA; MAMMALIA; MONOSIGA BREVICOLLIS; VERTEBRATA;

ANIMALS; ANKYRINS; CYTOSKELETAL PROTEINS; EVOLUTION, MOLECULAR; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PHYLOGENY; SPECTRIN;

EID: 70349290728     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0370796     Document Type: Conference Paper

References (92)

1. Hiller, G. and Weber, K. (1977) Spectrin is absent in various tissue culture cells. Nature 266, 181-183
2. Pinder, J.C., Phethean, J. and Gratzer, W.B. (1978) Spectrin in primitive erythrocytes. FEBS Lett. 92, 278-282
3. Bennett, V. and Baines, A.J. (2001) Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 81, 1353-1392
4. Perrotta, S., Gallagher, P.G. and Mohandas, N. (2008) Hereditary spherocytosis. Lancet 372, 1411-1426
5. Hammarlund, M., Davis, W.S. and Jorgensen, E.M. (2000) Mutations in β-spectrin disrupt axon outgrowth and sarcomere structure. J. Cell Biol. 149, 931-942
6. Moorthy, S., Chen, L. and Bennett, V. (2000) Caenorhabditis elegans β-G spectrin is dispensable for establishment of epithelial polarity, but essential for muscular and neuronal function. J. Cell Biol. 149, 915-930
7. Hammarlund, M., Jorgensen, E.M. and Bastiani, M.J. (2007) Axons break in animals lacking β-spectrin. J. Cell Biol. 176, 269-275
8. Pielage, J., Fetter, R.D. and Davis, G.W. (2005) Presynaptic spectrin is essential for synapse stabilization. Curr. Biol. 15, 918-928
9. Pielage, J., Fetter, R.D. and Davis, G.W. (2006) A postsynaptic spectrin scaffold defines active zone size, spacing, and efficacy at the Drosophila neuromuscular junction. J. Cell Biol. 175, 491-503
10. Pielage, J., Cheng, L., Fetter, R.D., Carlton, P.M., Sedat, J.W. and Davis, G.W. (2008) A presynaptic giant ankyrin stabilizes the NMJ through regulation of presynaptic microtubules and transsynaptic cell adhesion. Neuron 58, 195-209
11. Kizhatil, K. and Bennett, V. (2004) Lateral membrane biogenesis in human bronchial epithelial cells requires 190-kDa ankyrin-G. J. Biol. Chem. 279, 16706-16714
12. Kizhatil, K., Yoon, W., Mohler, P.J., Davis, L.H., Hoffman, J.A. and Bennett, V. (2007) Ankyrin-G and β2-spectrin collaborate in biogenesis of lateral membrane of human bronchial epithelial cells. J. Biol. Chem. 282, 2029-2037
13. Zarnescu, D.C. and Thomas, G.H. (1999) Apical spectrin is essential for epithelial morphogenesis but not apicobasal polarity in Drosophila. J. Cell Biol. 146, 1075-1086
14. Heavy-spectrin in the apical membrane skeleton of Drosophila. J. Cell Biol. 158, 941-951
15. Bruce, L.J., Beckmann, R., Ribeiro, M.L., Peters, L.L., Chasis, J.A., Delaunay, J., Mohandas, N., Anstee, D.J. and Tanner, M.J. (2003) A band 3-based macrocomplex of integral and peripheral proteins in the RBC membrane. Blood 101, 4180-4188
16. Salomao, M., Zhang, X., Yang, Y., Lee, S., Hartwig, J.H., Chasis, J.A., Mohandas, N. and An, X. (2008) Protein 4.1R-dependent multiprotein complex: new insights into the structural organization of the red blood cell membrane. Proc. Natl. Acad. Sci. U.S.A. 105, 8026-8031
17. v1.5 on the surface of cardiomyocytes. Proc. Natl. Acad. Sci. U.S.A. 101, 17533-17538
18. Stagg, M.A., Carter, E., Sohrabi, N., Siedlecka, U., Soppa, G.K., Mead, F., Mohandas, N., Taylor-Harris, P., Baines, A., Bennett, P. et al. (2008) Cytoskeletal protein 4.1R affects repolarization and regulates calcium handling in the heart. Circ. Res. 103, 855-863
19. Jenkins, S.M. and Bennett, V. (2001) Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J. Cell Biol. 155, 739-746
20. v channel targeting in the heart requires an ankyrin-G dependent cellular pathway. J. Cell Biol. 180, 173-186
21. Shen, L., Liang, F., Walensky, L.D. and Huganir, R.L. (2000) Regulation of AMPA receptor GluR1 subunit surface expression by a 4.1N-linked actin cytoskeletal association. J. Neurosci. 20, 7932-7940
22. Coleman, S.K., Cai, C., Mottershead, D.G., Haapalahti, J.P. and Keinanen, K. (2003) Surface expression of GluR-D AMPA receptor is dependent on an interaction between its C-terminal domain and a 4.1 protein. J. Neurosci. 23, 798-806
23. Lu, D., Yan, H., Othman, T. and Rivkees, S.A. (2004) Cytoskeletal protein 4.1G is a binding partner of the metabotropic glutamate receptor subtype 1α. J. Neurosci. Res. 78, 49-55
24. Hill, A.S., Nishino, A., Nakajo, K., Zhang, G., Fineman, J.R., Selzer, M.E., Okamura, Y. and Cooper, E.C. (2008) Ion channel clustering at the axon initial segment and node of Ranvier evolved sequentially in early chordates. PLoS Genet. 4, e1000317
25. Chung, H.J., Jan, Y.N. and Jan, L.Y. (2006) Polarized axonal surface expression of neuronal KCNQ channels is mediated by multiple signals in the KCNQ2 and KCNQ3 C-terminal domains. Proc. Natl. Acad. Sci. U.S.A. 103, 8870-8875
26. v channels at electrically active domains of the axon. J. Neurosci. 26, 2599-2613
27. An, X., Gauthier, E., Zhang, X., Guo, X., Anstee, D.J., Mohandas, N. and Chasis, J.A. (2008) Adhesive activity of Lu glycoproteins is regulated by interaction with spectrin. Blood 112, 5212-5218
28. Kroviarski, Y., El Nemer, W., Gane, P., Rahuel, C., Gauthier, E., Lecomte, M.C., Cartron, J.P., Colin, Y. and Le Van Kim, C. (2004) Direct interaction between the Lu/B-CAM adhesion glycoproteins and erythroid spectrin. Br. J. Haematol. 126, 255-264
29. Bauer, P., Schols, L. and Riess, O. (2006) Spectrin mutations in spinocerebellar ataxia (SCA). BioEssays 28, 785-787
30. Ikeda, Y., Dick, K.A., Weatherspoon, M.R., Gincel, D., Armbrust, K.R., Dalton, J.C., Stevanin, G., Durr, A., Zuhlke, C., Burk, K. et al. (2006) Spectrin mutations cause spinocerebellar ataxia type 5. Nat. Genet. 38, 184-190
31. Leshchyns'ka, I., Sytnyk, V., Morrow, J.S. and Schachner, M. (2003) Neural cell adhesion molecule (NCAM) association with PKCβ2 via βI spectrin is implicated in NCAM-mediated neurite outgrowth. J. Cell Biol. 161, 625-639
32. Shotton, D.M., Burke, B.E. and Branton, D. (1979) The molecular structure of human erythrocyte spectrin: biophysical and electron microscopic studies. J. Mol. Biol. 131, 303-329
33. Ungewickell, E. and Gratzer, W. (1978) Self-association of human spectrin: a thermodynamic and kinetic study. Eur. J. Biochem. 88, 379-385
34. Shahbakhti, F. and Gratzer, W.B. (1986) Analysis of the self-association of human red cell spectrin. Biochemistry 25, 5969-5975
35. Speicher, D.W. and Marchesi, V.T. (1984) Erythrocyte spectrin is comprised of many homologous triple helical segments. Nature 311, 177-180
36. Yan, Y., Winograd, E., Viel, A., Cronin, T., Harrison, S.C. and Branton, D. (1993) Crystal structure of the repetitive segments of spectrin. Science 262, 2027-2030
37. Pascual, J., Pfuhl, M., Rivas, G., Pastore, A. and Saraste, M. (1996) The spectrin repeat folds into a three-helix bundle in solution. FEBS Lett. 383, 201-207
38. An, X., Debnath, G., Guo, X., Liu, S., Lux, S.E., Baines, A., Gratzer, W. and Mohandas, N. (2005) Identification and functional characterization of protein 4.1R and actin-binding sites in erythrocyte β-spectrin: regulation of the interactions by phosphatidylinositol-4,5-bisphosphate. Biochemistry 44, 10681-10688
39. Viel, A., Gee, M.S., Tomooka, L. and Branton, D. (1998) Motifs involved in interchain binding at the tail-end of spectrin. Biochim. Biophys. Acta 1384, 396-404
40. Ursitti, J.A., Kotula, L., DeSilva, T.M., Curtis, P.J. and Speicher, D.W. (1996) Mapping the human erythrocyte β-spectrin dimer initiation site using recombinant peptides and correlation of its phasing with the α-actinin dimer site. J. Biol. Chem. 271, 6636-6644
41. Cherry, L., Menhart, N. and Fung, L.W. (1999) Interactions of the α-spectrin N-terminal region with β-spectrin: implications for the spectrin tetramerization reaction. J. Biol. Chem. 274, 2077-2084
42. Kotula, L., DeSilva, T.M., Speicher, D.W. and Curtis, P.J. (1993) Functional characterization of recombinant human red cell α-spectrin polypeptides containing the tetramer binding site. J. Biol. Chem. 268, 14788-14793
43. Kennedy, S.P., Warren, S.L., Forget, B.G. and Morrow, J.S. (1991) Ankyrin binds to the 15th repetitive unit of erythroid and nonerythroid β-spectrin. J. Cell Biol. 115, 267-277
44. Davis, L., Abdi, K., Machius, M., Brautigam, C., Tomchick, D.R., Bennett, V. and Michaely, P. (2009) Localization and structure of the ankyrin-binding site on β2-spectrin. J. Biol. Chem. 284, 6982-6987
45. Ipsaro, J.J., Huang, L. and Mondragon, A. (2009) Structures of the spectrin-ankyrin interaction binding domains. Blood 113, 5385-5393
46. Cianci, C.D., Giorgi, M. and Morrow, J.S. (1988) Phosphorylation of ankyrin down-regulates its cooperative interaction with spectrin and protein 3. J. Cell Biochem. 37, 301-315
47. Ziemnicka-Kotula, D., Xu, J., Gu, H., Potempska, A., Kim, K.S., Jenkins, E.C., Trenkner, E. and Kotula, L. (1998) Identification of a candidate human spectrin Src homology 3 domain-binding protein suggests a general mechanism of association of tyrosine kinases with the spectrin-based membrane skeleton. J. Biol. Chem. 273, 13681-13692
48. 1176. J. Biol. Chem. 278, 7735-7741
49. Bournier, O., Kroviarski, Y., Rotter, B., Nicolas, G., Lecomte, M.C. and Dhermy, D. (2006) Spectrin interacts with EVL (Enabled/ vasodilator-stimulated phosphoprotein-like protein), a protein involved in actin polymerization. Biol. Cell 98, 279-293
50. Rotter, B., Bournier, O., Nicolas, G., Dhermy, D. and Lecomte, M.C. (2005) αII-spectrin interacts with Tes and EVL, two actin-binding proteins located at cell contacts. Biochem. J. 388, 631-638
51. An, X., Guo, X., Gratzer, W. and Mohandas, N. (2005) Phospholipid binding by proteins of the spectrin family: a comparative study. Biochem. Biophys. Res. Commun. 327, 794-800
52. Simonovic, M., Zhang, Z., Cianci, C.D., Steitz, T.A. and Morrow, J.S. (2006) Structure of the calmodulin αII-spectrin complex provides insight into the regulation of cell plasticity. J. Biol. Chem. 281, 34333-34340
53. Apweiler, R., Attwood, T.K., Bairoch, A., Bateman, A., Birney, E., Biswas, M., Bucher, P., Cerutti, L., Corpet, F., Croning, M.D. et al. (2000) InterPro: an integrated documentation resource for protein families, domains and functional sites. Bioinformatics 16, 1145-1150
54. Gimona, M. (2006) Protein linguistics: a grammar for modular protein assembly? Nat. Rev. Mol. Cell Biol. 7, 68-73
55. Virel, A. and Backman, L. (2007) A comparative and phylogenetic analysis of the α-actinin rod domain. Mol. Biol. Evol. 24, 2254-2265
56. Virel, A. and Backman, L. (2004) Molecular evolution and structure of α-actinin. Mol. Biol. Evol. 21, 1024-1031
57. Viel, A. (1999) α-Actinin and spectrin structures: an unfolding family story. FEBS Lett. 460, 391-394
58. Thomas, G.H., Newbern, E.C., Korte, C.C., Bales, M.A., Muse, S.V., Clark, A.G. and Kiehart, D.P. (1997) Intragenic duplication and divergence in the spectrin superfamily of proteins. Mol. Biol. Evol. 14, 1285-1295
59. Pascual, J., Castresana, J. and Saraste, M. (1997) Evolution of the spectrin repeat. BioEssays 19, 811-817
60. King, N. (2005) Choanoflagellates. Curr. Biol. 15, R113-R114
61. King, N. (2004) The unicellular ancestry of animal development. Dev. Cell 7, 313-325
62. King, N., Westbrook, M.J., Young, S.L., Kuo, A., Abedin, M., Chapman, J., Fairclough, S., Hellsten, U., Isogai, Y., Letunic, I. et al. (2008) The genome of the choanoflagellate Monosiga brevicollis and the origins of metazoan multicellularity. Nature 451, 783-788
63. Scott, C., Phillips, G.W. and Baines, A.J. (2001) Properties of the C-terminal domain of 4.1 proteins. Eur. J. Biochem. 268, 3709-3717
64. Stabach, P.R. and Morrow, J.S. (2000) Identification and characterization of βV spectrin, a mammalian ortholog of Drosophila βH spectrin. J. Biol. Chem. 275, 21385-21395
65. heavy-spectrin has a restricted tissue and subcellular distribution during Drosophila embryogenesis. Development 120, 2039-2050
66. Putnam, N.H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V.V. et al. (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86-94
67. Kasahara, M. (2007) The 2R hypothesis: an update. Curr. Opin. Immunol. 19, 547-552
68. Salomao, M., An, X., Guo, X., Gratzer, W.B., Mohandas, N. and Baines, A.J. (2006) Mammalian αI-spectrin is a neofunctionalized polypeptide adapted to small highly deformable erythrocytes. Proc. Natl. Acad. Sci. U.S.A. 103, 643-648
69. Bignone, P.A. and Baines, A.J. (2003) Spectrin αII and βII isoforms interact with high affinity at the tetramerization site. Biochem. J. 374, 613-624
70. An, X., Zhang, X., Salomao, M., Guo, X., Yang, Y., Wu, Y., Gratzer, W., Baines, A.J. and Mohandas, N. (2006) Thermal stabilities of brain spectrin and the constituent repeats of subunits. Biochemistry 45, 13670-13676
71. An, X., Guo, X., Zhang, X., Baines, A.J., Debnath, G., Moyo, D., Salomao, M., Bhasin, N., Johnson, C., Discher, D. et al. (2006) Conformational stabilities of the structural repeats of erythroid spectrin and their functional implications. J. Biol. Chem. 281, 10527-10532
72. Johnson, C.P., Tang, H.Y., Carag, C., Speicher, D.W. and Discher, D.E. (2007) Forced unfolding of proteins within cells. Science 317, 663-666
73. Thomas, G. (1998) Molecular evolution of spectrin repeats. BioeEssays 20, 600
74. Baines, A.J. (2003) Comprehensive analysis of all triple helical repeats in β-spectrins reveals patterns of selective evolutionary conservation. Cell. Mol. Biol. Lett. 8, 195-214
75. Djinovic-Carugo, K., Gautel, M., Ylanne, J. and Young, P. (2002) The spectrin repeat: a structural platform for cytoskeletal protein assemblies. FEBS Lett. 513, 119-123
76. Hsu, Y.J. and Goodman, S.R. (2005) Spectrin and ubiquitination: a review. Cell. Mol. Biol. Suppl. 51, OL801-OL807
77. Macias, M.J., Musacchio, A., Ponstingl, H., Nilges, M., Saraste, M. and Oschkinat, H. (1994) Structure of the pleckstrin homology domain from β-spectrin. Nature 369, 675-677
78. Hyvonen, M., Macias, M.J., Nilges, M., Oschkinat, H., Saraste, M. and Wilmanns, M. (1995) Structure of the binding site for inositol phosphates in a PH domain. EMBO J. 14, 4676-4685
79. Das, A., Base, C., Manna, D., Cho, W. and Dubreuil, R.R. (2008) Unexpected complexity in the mechanisms that target assembly of the spectrin cytoskeleton. J. Biol. Chem. 283, 12643-12653
80. Winkelmann, J.C., Chang, J.G., Tse, W.T., Scarpa, A.L., Marchesi, V.T. and Forget, B.G. (1990) Full-length sequence of the cDNA for human erythroid β-spectrin. J. Biol. Chem. 265, 11827-11832
81. Tang, H.Y. and Speicher, D.W. (2004) In vivo phosphorylation of human erythrocyte spectrin occurs in a sequential manner. Biochemistry 43, 4251-4262
82. Winkelmann, J.C., Costa, F.F., Linzie, B.L. and Forget, B.G. (1990) β-Spectrin in human skeletal muscle: tissue-specific differential processing of 3′ β-spectrin pre-mRNA generates a β-spectrin isoform with a unique carboxyl terminus. J. Biol. Chem. 265, 20449-20454
83. Manno, S., Takakuwa, Y., Nagao, K. and Mohandas, N. (1995) Modulation of erythrocyte membrane mechanical function by β-spectrin phosphorylation and dephosphorylation. J. Biol. Chem. 270, 5659-5665
84. Hayes, N.V., Scott, C., Heerkens, E., Ohanian, V., Maggs, A.M., Pinder, J.C., Kordeli, E. and Baines, A.J. (2000) Identification of a novel C-terminal variant of βII spectrin: two isoforms of βII spectrin have distinct intracellular locations and activities. J. Cell Sci. 113, 2023-2034
85. Bignone, P.A., King, M.D., Pinder, J.C. and Baines, A.J. (2007) Phosphorylation of a threonine unique to the short C-terminal isoform of βII-spectrin links regulation of α-β spectrin interaction to neuritogenesis. J. Biol. Chem. 282, 888-896
86. Collins, M.O., Yu, L., Coba, M.P., Husi, H., Campuzano, I., Blackstock, W.P., Choudhary, J.S. and Grant, S.G. (2005) Proteomic analysis of in vivo phosphorylated synaptic proteins. J. Biol. Chem. 280, 5972-5982
87. Olsen, J.V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P. and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648
88. Ohanian, V., Wolfe, L.C., John, K.M., Pinder, J.C., Lux, S.E. and Gratzer, W.B. (1984) Analysis of the ternary interaction of the red cell membrane skeletal proteins spectrin, actin, and 4.1. Biochemistry 23, 4416-4420
89. Correas, I., Leto, T.L., Speicher, D.W. and Marchesi, V.T. (1986) Identification of the functional site of erythrocyte protein 4.1 involved in spectrin-actin associations. J. Biol. Chem. 261, 3310-3315
90. Fehon, R.G., Dawson, I.A. and Artavanistsakonas, S. (1994) A Drosophila homolog of membrane-skeleton protein-4.1 is associated with septate junctions and is encoded by the coracle gene. Development 120, 545-557
91. Gimm, J.A., An, X., Nunomura, W. and Mohandas, N. (2002) Functional characterization of spectrin-actin-binding domains in 4.1 family of proteins. Biochemistry 41, 7275-7282
92. Han, B.G., Nunomura, W., Takakuwa, Y., Mohandas, N. and Jap, B.K. (2000) Protein 4.1R core domain structure and insights into regulation of cytoskeletal organization. Nat. Struct. Biol. 7, 871-875