Adducin: Structure, function and regulation

Cellular and Molecular Life Sciences

Volumn 57, Issue 6, 2000, Pages 884-895

  Matsuoka, Y ^a   Li, X ^b   Bennett, V ^c  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c NONE

Author keywords

Actin; Adducin; Membrane skeleton; Spectrin

Indexed keywords

ACTIN; ADDUCIN; CALMODULIN BINDING PROTEIN; GELSOLIN; MARCKS PROTEIN; PROTEIN KINASE C; RHO KINASE; SPECTRIN;

ACTIN MYOSIN INTERACTION; CELL MOTILITY; DROSOPHILA; ENZYME PHOSPHORYLATION; HUMAN; NONHUMAN; OLIGOMERIZATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN STRUCTURE; PROTEIN SYNTHESIS REGULATION; REVIEW; SEQUENCE HOMOLOGY;

EID: 0033929093     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/PL00000731     Document Type: Review

References (80)

1. 1 Bennett V. (1990) Spectrin-based membrane skeleton: a multi-potential adapter between plasma membrane and cytoplasm. Phys. Rev. 70: 1029-1065
2. 2 Bennett V. and Gilligan D. M. (1993) The spectrin-based membrane skeleton and micron-scale organization of the plasma membrane. Annu. Rev. Cell Biol. 9: 7-66
3. 3 Yu J., Fischman D. A. and Steck T. L. (1973) Selective solubilization of proteins and phospholipids from red blood cell membranes by nonionic detergents. J. Supramol. Struct. I: 233-248
4. 4 Byers T. J. and Branton D. (1985) Visualization of the protein association in the erythrocyte membrane skeleton. Proc. Natl. Acad. Sci. USA 82: 6153-6157
5. 5 Shen B. W., Josephs R. and Steck T. L. (1986) Ultrastructure of the intact skeleton of the human erythrocyte membrane. J. Cell Biol. 102: 997-1006
6. 6 Liu S.-C, Derick L. H. and Palek J. (1987) Visualization of the hexagonal lattice in the erythrocyte membrane skeleton. J. Cell Biol. 104: 527-536
7. 7 Fowler V. M. (1996) Regulation of actin filament length in erythrocytes and striated muscle. Curr. Opin. Cell Biol. 8: 86-96
8. 8 Tyler J. M., Hargreaves W. R. and Branton A. (1979) Purification of two spectrin-binding proteins: biochemical and electron microscopic evidence for site-specific reassociation between spectrin and bands 2.1 and 4.1. Proc. Natl. Acad. Sci. USA 76: 5192-5196
9. 9 Bennett V. and Stenbuck P. J. (1979) The membrane attachment protein for spectrin is associated with band 3 in human erythrocyte membranes. Nature 280: 468-473
10. 10 Bennett V. and Stenbuck P. J. (1980) Association between ankyrin and the cytoplasmic domain of band 3 isolated from the human erythrocyte membrane. J. Biol. Chem. 255: 6424-6432
11. 11 Reid M. E., Takakuwa Y., Conboy J., Tchernia G. and Mohandas N. (1990) Glycophorin C content of human erythrocyte membrane is regulated by protein 4.1. Blood 75: 2229-2234
12. 12 Workman R. F. and Low P. S. (1998) Biochemical analysis of potential sites for protein 4.1-mediated anchoring of the spectrin-actin skeleton to the erythrocyte membrane. J. Biol. Chem. 273: 6171-6176
13. 13 Fowler V. M. and Bennett V. (1984) Erythrocyte membrane tropomyosin. Purification and properties. J. Biol. Chem. 259: 5978-5989
14. 14 Kuhlman P. A., Hughes C. A., Bennett V. and Fowler V. M. (1996) A new function for adducin, calcium calmodulin regulated capping of the barbed ends of actin filaments. J. Biol. Chem. 271: 7986-7991
15. 15 Weber A., Pennise C. R., Babcokk G. G. and Fowler V. M. (1994) Tropomodulin caps the pointed ends of actin filaments. J. Cell Biol. 127: 1635-1672
16. 16 Fowler V. M. and Taylor D. L. (1980) Spectrin plus band 4.1 cross-link actin. Regulation by micromolar calcium. J. Cell. Biol. 85: 361-376
17. 17 Gardner K. and Bennett V. (1988) Erythrocyte adducin: a new calmodulin regulated membrane-skeletal protein that modulates spectrin-actin assembly. In: Signal Transduction in Cytoplasmic Organization and Cell Moulity, pp. 293-311. Satir P., Condeelis J. and Lazarides E. (eds), Alan R. Liss, New York
18. 18 Gardner K. and Bennett V. (1986) A new erythrocyte membrane-associated protein with calmodulin binding activity. J. Biol. Chem. 261: 1339-1348
19. 19 Gardner K. and Bennett V. (1987) Modulation of spectrin-actin assembly by erythrocyte adducin. Nature 328: 359-362
20. 20 Cohen C. M., Tyler J. M. and Branton D. (1980) Spectrinactin associations studied by electron microscopy of shadowed preparations. Cell 21: 875-883
21. 21 Li X. and Bennett V. (1996) Identification of the spectrin subunit domains required for formation of spectrin adducin actin complexes. J. Biol. Chem. 271: 15695-15702
22. 22 Joshi R., Gilligan D. M., Otto E., McLaughlin T. and Bennett V. (1991) Primary structure and domain organization of human alpha and beta adducin. J. Cell Biol. 115: 665-675
23. 23 Dong L., Chapline C., Mousseau B., Fowler L., Ramsay M. K., Stevens J. L. et al. (1995) 35H, a sequence isolated as a protein kinase C binding protein, is a novel member of the adducin family. J. Biol. Chem. 270: 25534-25540
24. 24 Joshi R. and Bennett V. (1990) Mapping the domain structure of human erythrocyte adducin. J. Biol. Chem, 265: 13130-13136
25. 25 Hughes C. A. and Bennett V. (1995) Adducin: a physical model with implication for function in assembly of spectrin-actin complexes. J. Biol. Chem. 270: 18990-18996
26. 26 Lin B., Nasir J., McDonald H., Graham R., Rommens J. M., Goldberg Y. P. et al. (1995) Genomic organization of the human alpha-adducin gene and its alternately spliced isoforms. Genomics 25: 93-99
27. 27 Gilligan D. M., Lieman J. and Bennett V. (1995) Assignment of the human beta-adducin gene (ADD2) to 2p13-p14 by in situ hybridization. Genomics 28: 610-612
28. 28 Tisminetzky S., Devescovi G., Tripodi G., Muro A., Bianchi G., Colombi M. et al. (1995) Genomic organisation and chromosomal localisation of the gene encoding human beta adducin. Gene 167: 313-316
29. 29 Li X., Matsuoka Y. and Bennett V. (1998) Adducin preferentially recruits spectrin to the fast growing ends of actin filaments in a complex requiring MARCKS-related domain and a newly defined oligomcrization domain. J. Biol. Chem. 273: 19329-19338
30. 30 Bennett V., Gardner K. and Steiner J. P. (1988) Brain adducin: a protein kinase C substrate that may mediate site-directed assembly at the spectrin-actin junction. J. Biol. Chem. 263: 5860-5869
31. 31 Mische S. M., Mooseker M. S. and Morrow J. S. (1987) Erythrocyle adducin: a calmodulin-rcgulated actin-bundling protein that stimulates spectrin-actin binding. J. Cell Biol. 105: 2837-2845
32. 32 Taylor K. A. and Taylor D. W. (1994) Formation of two-dimensional complexes of F-actin and crosslinking proteins on lipid monolayers: demonstration of unipolar alpha-actinin-F-actin crosslinking. Biophys. J. 67: 1976-1983
33. 33 Matsuoka Y., Li X. and Bennett V. (1998) Adducin is an in vivo substrate for protein kinase C: phosphorylation in the MARCKS-related domain inhibits activity in promoting spectrin-actin complexes and occurs in many cells, including dendritic spines of neurons. J. Cell Biol. 142: 485-497
34. 34 Kuhlman P. A. and Fowler V. M. (1997) Purification and characterization of an alpha 1 beta 2 isoform of CapZ from human erythrocytes: cytosolic location and inability to bind to Mg2 + ghosts suggest that erythrocyte actin filaments are capped by adducin. Biochemistry 36: 13461-13472
35. 35 Aderem A. (1992) The MARCKS brothers: a family of protein kinase C substrates. Cell 71: 713-716
36. 36 Blackshear P. J. (1993) The MARCKS family of cellular protein kinase C substrates. J. Biol. Chem. 268: 1501-1504
37. 37 Hartwig J. H., Thelen M., Rosen A., Janmcy P. A., Nairn A. C. and Aderem A. (1992) MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. Nature 356: 618-622
38. 38 Kim J., Blackshear P. J., Johnson J. D. and McLaughlin S. (1994) Phosphorylation reverses the membrane association of peptides that correspond to the basic domains of MARCKS and neuromodulin. Biophys. J. 67: 227-237
39. 39 McLaughlin S. and Aderem A. (1995) The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20: 272-276
40. 40 Wolf M. and Sahyoun N. (1986) Protein kinase C and phosphatidylserine bind to Mr 110,000,115,000 polypeptides enriched in cytoskeletal and postsynaptic density preparations. J. Biol. Chem. 261: 13327-13332
41. 41 Chapline C., Ramsay K., Klauck T. and Jaken S. (1993) Interaction cloning of protein kinase C substrates. J. Biol. Chem. 268: 6858-6861
42. 42 Kabsch W., Mannherz H. G., Suck D., Pai E. F. and Holmes K. C. (1990) Atomic structure of the actin: DNase I complex. Nature 347: 37-44
43. 43 Holmes K. C., Popp D., Gebhard W. and Kabsch W. (1990) Atomic model of the actin filament. Nature 3-47: 44-49
44. 44 Schröder R. R., Manstein D. J., Jahn W. J., Holden H., Rayment L, Holmes K. C. et al. (1993) Three-dimensional atomic model of F-actin decorated with Dictyostelium myosin S1. Nature 364: 171-174
45. 45 Rayment I., Holden H. M., Whittaker M., Yohn C. B., Lorenz M., Holmes K. C. et al. (1993) Structure of the actin-myosin complex and its implications for muscle contraction. Science 261: 58-65
46. 46 Yue L. and Spradling A. C. (1992) Hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin. Genes Dev. 6: 2443-2454
47. 47 Lupas A., Van Dyke M. and Stock J. (1991) Predicting coiled coil from protein sequences. Science 252: 1162-1164
48. 48 Li X. (1998) Towards the assembly of the membrane skeleton: structural and functional studies of spectrin-actin-adducin complexes, thesis, Duke University, Durham NC
49. 49 Lo S. H., Janmey P. A., Hartwig J. H. and Chen L. B. (1994) Interaction of tensin with actin and identification of its three distinct actin-binding domains. J. Cell Biol. 125: 1067-1075
50. 50 Waseem A. and Palfrey H. C. (1988) Erythrocyte adducin. Comparison of the alpha-and beta-subunits and multiple-site phosphorylation by protein kinase C and cAMP-dependent protein kinase. Eur. J. Biochem. 178: 563-573
51. 51 Ling E., Gardner K. and Bennett V. (1986) Protein kinase C phosphorylates a recently identified membrane skeleton-associated calmodulin-binding protein in human erythrocytes. J. Biol. Chem. 261: 13875-13878
52. 52 Matsuoka Y., Hughes C. A. and Bennett V. (1996) Adducin regulation, definition of the calmodulin-binding domain and sites of phospliorylation by protein kinases A and C. J. Biol. Chem. 271: 25157-25166
53. 53 Fukata Y., Oshiro N., Kinoshita N., Kawano Y., Matsuoka Y., Bennett V. et al. (1999) Pliosphorylation of adducin by Rho-kinase plays a crucial role in cell motility. J. Coll Biol. 145: 347-361
54. 54 Kimura K., Fukata Y., Matsuoka Y., Bennett V., Matsuura Y., Okawa K. et al. (1998) Regulation of the association of adducin with actin filaments by rho-associated kinase (Rho-kinase) and myosin phosphatase. J. Biol. Chem. 273: 5542-5548
55. 55 Siegel D. L. and Branton D. J. (1985) Partial purification and characterization of an actin-bundling protein, band 4.9, from human crythrocytes. J. Cell Biol. 100: 775-785
56. 56 Lazarides E. (1987) From genes to structural morphogenesis: the genesis and epigenesis of a red blood cell. Cell 51: 345-356
57. 57 Derick L. H., Lui S. C., Chishti A. H. and Palek J. (1992) Protein immunolocalization in the spread erythrocyte membrane skeleton. Eur. J. Cell Biol. 57: 317-320
58. 58 Nehls V., Drenckhahn D., Joshi R. and Bennett V. (1991) Adducin in erythrocyte precursor cells of rats and humans: expression and compartmentalizalion. Blood 78: 1692-1696
59. 2+ -dependent association with sites of cell-cell contact. J. Cell Biol. 109: 557-569
60. 60 Hu R. J., Moorthy S. and Bennett V. (1995) Expression of functional domains of betaG-spectrin disrupts epithelial morphology in cultured cells. J. Cell Biol. 128: 1069-1080
61. 61 Seidel B., Zuschratter W., Wex H., Garner C. C. and Gundelfinger E. D. (1995) Spatial and sub-cellular localization of the membrane cytoskeleton-associated protein alpha-adducin in the rat brain. Brain Res. 700: 13-24
62. 62 Schengrund C. L., DasGupta B. R., Hughes C. A. and Ringler N. J. (1996) Ganglioside-induced adherence of botulinum and tetanus ncurotoxins to addudn. J. Neurochem. 66: 2556-2561
63. 2+ and phosphatidylserine. Biochem. Biophys. Res. Commun. 205: 460-466
64. 64 Burns M. E., Sasaki T., Takai Y. and Augustine G. J. (1998) Rabphilin-3A: a multifunctional regulator of synaptic vesicle traffic. J. Gen. Physiol. 111: 243-255
65. 65 Gilligan D. M., Lozovatsky L., Mohandas N., Gwynn B. and Peters L. L. (1998) β-adducin null red cells show decreased dcformability and unexpected deficiency of α-adducin. Mol. Biol. Cell 9: 266a
66. 66 Fowler E., Everitt J., Stevens J. E. and Jaken S. (1998) Redistribution and enhanced protein kinase C-mediated phosphorylation of alpha-and gamma-adducin during renal tumor progression. Cell Growth Differ. 9: 405-413
67. 67 Bianchi G., Tripodi M. G., Casari G., Torielli E., Cusi D., Barlassina C. et al. (1995) Alpha-adducin may control blood pressure both in rats and humans. Clin. Exp. Pharmacol. Physiol. (Suppl.) 1: S7-S9
68. 68 Manunta P., Barlassina C. and Bianchi G. (1998) Adducin in essential hypertension. FEBS Lett. 430: 41-44
69. 69 Cusi D., Barlassina C., Azzani T., Casari G., Citterio L., Devoto M. et al. (1997) α-adducin polymorphism in primary hypertension: linkage and association studies-relationship to salt sensitivity. Lancet 349: 1353-1358
70. 70 Wang W. Y. S., Adams D. J., Glenn C. L. and Morris B. J. (1999) The Gly460Trp variant of α-adducin is not associated with hypertension in white Anglo-Australians. Am. J. Hypertension 12: 632-636
71. 71 Busch C. P., Harris S. B., Hanley A. J. G., Zinman B. and Hegele R. A. (1999) The ADD1 G460W polymorphism is not associated with variation in blood pressure in Canadian Oji-Cree. J. Hum. Genet. 44: 225-229
72. 72 Ishikawa K., Katsuya T., Sato N., Nakata Y., Takami S., Takiuchi S. et al. (1998) No association between α-adducin 460 polymorphism and essential hypertension in a Japanese population. Am. J. Hypertension 11: 502-506
73. 73 Kamitani A., Wong Z. Y. H., Fraser R., Davies D. L., Connor J. M., Foy C. J. W. et al. (1998) Human α-adducin gene, blood pressure, and sodium metabolism. Hypertension 32: 138-143
74. 74 Ding D., Parkhurst S. M. and Lipshitz H. D. (1993) Different genetic requirements for anterior RNA localization revealed by the distribution of adducin-like transcripts during Drosophila oogenesis. Proc. Natl. Acad. Sci. USA 90: 2512-2516
75. 75 Lin H., Yue L. and Spradling A. C. (1994) The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120: 947-956
76. 76 Cuevas M., Lee J. K. and Spradling A. C. (1996) Alpha-spectrin is required for germline cell division and differentiation in the Drosophila ovary. Development 122: 3959-3968
77. 77 Deng W. and Lin H. (1997) Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of a polarized microtubule array for oocyte specification in Drosophila. Dev. Biol. 189: 79-94
78. 78 Moorthy S., Chen L. and Bennett V. (1997) The spectrin-based membrane cyloskeleton in C. elegans. Mol. Biol. Cell 8: 274a
79. 79 Lorenz M., Poole K., Popp D., Rosenbaum G. and Holmes K. (1995) An atomic model of the unregulated thin filament obtained by X-ray fiber diffraction on oriented actin-tropomyosin gels. J. Mol. Biol. 246: 108-119
80. 80 Matsuoka Y., Li X. and Bennett V. (1998) A new adducin function: a molecular arbitrator between myosin and spectrin for access to cortical actin. Mol. Biol. Cell 9: 35a