Parallel actin bundles and their multiple actin-bundling proteins

Current Opinion in Cell Biology

Volumn 12, Issue 1, 2000, Pages 72-78

  Bartles, James R ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN;

BRUSH BORDER; CELL ULTRASTRUCTURE; HAIR CELL; MICROVILLUS; PRIORITY JOURNAL; REVIEW; SENSORY NERVE CELL; SERTOLI CELL;

EID: 0033981223     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(99)00059-9     Document Type: Review

References (52)

1. Matsudaira P. Modular organization of actin crosslinking proteins. Trends Biochem Sci. 16:1991;87-92.
2. Furukawa R., Fechheimer M. The structure, function, and assembly of actin filament bundles. Int Rev Cytol. 175:1997;29-90.
3. Puius Y.A., Mahoney N.M., Almo S.C. The modular structure of actin-regulatory proteins. Curr Opin Cell Biol. 10:1998;23-34.
4. Tilney L.G., Tilney M.S., Guild G.M. F-Actin bundles in Drosophila bristles. I. Two filament cross-links are involved in bundling. J Cell Biol. 130:1995;629-638.
5. Tilney L.G., Connelly P., Smith S., Guild G.M. F-Actin bundles in Drosophila bristles are assembled from modules composed of short filaments. J Cell Biol. 135:1996;1291-1308.
6. Hoover K.K., Chien A.J., Corces V.J. Effect of transposable elements on the expression of the forked gene of Drosophila melanogaster. Genetics. 135:1993;507-526.
7. Petersen N.S., Lankenau D-H., Mitchell H.K., Young P., Corces V.G. Forked proteins are components of fiber bundles present in developing bristles of Drosophila melanogaster. Genetics. 136:1994;173-182.
8. Cant K., Knowles B.A., Mooseker M.S., Cooley L. Drosophila singed, a fascin homolog, is required for actin bundle formation during oogenesis and bristle extension. J Cell Biol. 125:1994;369-380.
9. ••] below).
10. ••]. In addition, by localizing forked and fascin at selected times during development, these authors confirm the prediction that forked appears in bristle actin bundles before fascin and provide some of the first evidence that fascin is present in excess within the bristle cytoplasm before being incorporated into the actin bundles.
11. •].
12. Bartles J.R., Zheng L., Li A., Wierda A., Chen B. Small espin: a third actin-bundling protein and potential forked protein ortholog in brush border microvilli. J Cell Biol. 143:1998;107-119. This article describes the identification and characterization of a ~30 kDa splice-isoform in the espin family of actin-binding/bundling proteins (see also [24]) that shows the properties expected for a third actin-bundling protein of brush border microvilli. It is the first demonstration that a member of the espin family can bundle actin filaments efficiently under physiological conditions in vitro.
13. Peterson N.S., Qin H. The forked protein is an actin binding protein involved in actin fiber formation in Drosophila bristles [suppl]. Mol Cell Biol. 7:1996;541a.
14. Bryan J., Kane R.E. Separation of interaction of the major components of sea urchin actin gel. J Mol Biol. 125:1978;207-224.
15. Edwards R.A., Herrera-Sosa H., Otto J., Bryan J. Cloning and expression of a murine fascin homolog from mouse brain. J Biol Chem. 270:1995;10764-10770.
16. Stokes D.L., DeRosier D.J. Growth conditions control the size and order of actin bundles in vitro. Biophys J. 59:1991;456-465.
17. Hanein D., Matsudaira P., DeRosier D.J. Evidence for a conformational change in actin induced by fimbrin (N375) binding. J Cell Biol. 139:1997;387-396.
18. McGough A., Pope B., Chiu W., Weeds A. Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J Cell Biol. 138:1997;771-781.
19. Sukow C., DeRosier D. How to analyze electron micrographs of rafts of actin filaments crosslinked by actin-binding proteins. J Mol Biol. 284:1998;1039-1050. The structural analysis of actin bundles is severely hampered by the disorder and polymorphism inherent in a three-dimensional bundle. In this article, the authors describe the development of a new method of structural analysis that examines the Fourier transforms of electron micrographs of two-dimensional bundles ('rafts') of actin filaments cross-linked by actin-bundling proteins. Both the theory and examples of the analysis of different kinds of rafts are presented.
20. Ono S., Yamakita Y., Yamashiro S., Matsudaira P.T., Gnarra J.R., Obinata T., Matsumura F. Identification of an actin binding region and a protein kinase C phosphorylation site on human fascin. J Biol Chem. 272:1997;2527-2533.
21. Ishikawa R., Yamashiro S., Kohama K., Matsumura F. Regulation of actin binding and actin bundling activities of fascin by caldesmon coupled with tropomyosin. J Biol Chem. 273:1998;26991-26997. The authors show that binding of fascin to actin filaments can be inhibited or reversed by other actin-binding proteins, in this case by caldesmon coupled with tropomyosin. This observation suggests one additional way, apart from phosphorylation [20], that the binding of an actin-bundling protein like fascin might be regulated.
22. Heintzelman M.B., Mooseker M.S. Assembly of the intestinal brush border cytoskeleton. Curr Top Dev Biol. 26:1992;93-122.
23. Shibayama T., Carboni J.M., Mooseker M.S. Assembly of the intestinal brush border: appearance and redistribution of microvillar core proteins in developing chick enterocytes. J Cell Biol. 105:1987;335-344.
24. Bartles J.R., Wierda A., Zheng L. Identification and characterization of espin, an actin-binding protein localized to the F-actin-rich junctional plaques of Sertoli cell ectoplasmic specializations. J Cell Sci. 109:1996;1229-1239.
25. ••]).
26. •]). However, they do notice some striking differences between villin knockout mice and the corresponding controls when the system is stressed by agents that either raise the intracellular concentration of calcium ion or otherwise damage the intestinal epithelium. These observations lead the authors to the unexpected conclusion that villin is not necessary for bundling of actin filaments in brush border microvilli, but for the reorganization of the microvillus actin cytoskeleton in response to injury or specific signals.
27. Goosney D.L., de Grado M., Finlay B.B. Putting E. coli on a pedestal: a unique system to study signal transduction and the cytoskeleton. Trends Cell Biol. 9:1999;11-14.
28. Raman N., Atkinson S.J. Rho controls actin cytoskeletal assembly in renal epithelial cells during ATP depletion and recovery. Am J Physiol. 276:1999;C1312-C1324.
29. Hanein D., Volkmann N., Goldsmith S., Michon A-M., Lehman W., Craig R., DeRosier D., Almo S., Matsudaira P. An atomic model of fimbrin binding to F-actin and its implications for filament crosslinking and regulation. Nat Struct Biol. 5:1998;787-792. By fitting the crystal structure of the amino-terminal actin-binding domain of human T-fimbrin to helical reconstructions of fimbrin-decorated actin filaments, the authors propose the first atomic working model of a fimbrin cross-link. The model not only suggests how the two actin-binding domains of fimbrin might be arranged to cross-link adjacent filaments to give the appropriate interfilament spacing, but also shows how the calcium-ion-binding domain might be positioned so as to affect the actin-binding properties of actin-binding domain 1.
30. Guild G.M., Connelly P.S., Shaw M.K., Tilney L.G. Actin filament cables in Drosophila nurse cells are composed of modules that slide passively past one another during dumping. J Cell Biol. 138:1997;783-797.
31. Mahajan-Miklos S., Cooley L. The villin-like protein encoded by the Drosophila quail gene is required for actin bundle assembly during oogenesis. Cell. 78:1994;291-301.
32. Cant K., Knowles B.A., Mahajan-Miklos S., Heintzelman M., Cooley L. Drosophila fascin mutants are rescued by overexpression of the villin-like protein, quail. J Cell Sci. 111:1998;213-221. The authors use P-element germline transformation to overexpress quail in singed mutants. They find that excess quail can rescue the formation of cytoplasmic actin bundles in nurse cells and conclude that fascin is partially redundant with quail in the Drosophila germline.
33. ••], illustrates the importance of assay selection and stressing the system when searching for a phenotype following targeted gene knockout.
34. Roberts W.M., Howard J., Hudspeth A.J. Hair cells: transduction, tuning, and transmission in the inner ear. Annu Rev Cell Biol. 4:1988;63-92.
35. Tilney L.G., Tilney M.S., DeRosier D.J. Actin filaments, stereocilia and hair cells: how cells count and measure. Annu Rev Cell Biol. 8:1992;257-274.
36. Tilney M.S., Tilney L.G., Stephens R.E., Merte C., Drenckhahn D., Cotanche D.A., Bretscher A. Preliminary characterization of the stereocilia and cuticular plate of hair cells in the chick cochlea. J Cell Biol. 109:1989;1711-1723.
37. Bartles J.R., Sekerkova G., Li A., Chen B., Vranich K., Mugnaini E., Tilney L.G. Espin is the missing crosslinker in the actin bundles of hair cells stereocilia [suppl]. Mol Biol Cell. 9:1998;135a.
38. Gibson F., Walsh J., Mburu P., Varela A., Brown K.A., Antonio M., Beisel K.W., Steel K.P., Brown S.D. A type VII myosin encoded by the mouse deafness gene shaker-1. Nature. 374:1995;62-64.
39. Weil D., Blanchard S., Kaplan J., Guilford P., Gibson F., Walsh J., Mburu P., Varela A., Levilliers J., Weston M.D.et al. Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature. 374:1995;60-61.
40. Avraham K.B., Hasson T., Steel K.P., Kingsley D.M., Russell L.B., Mooseker M.S., Copeland N.G., Jenkins N.A. The mouse Snell's waltzer deafness gene encodes an unconventional myosin required for structural integrity of the inner ear hair cells. Nat Genet. 11:1995;369-375.
41. Probst F.J., Fridell R.A., Raphael Y., Sauders T.L., Wang A., Liang Y., Moreel R.J., Touchman J.W., Lyons R.H., Noben-Trauth K.et al. Correction of deafness in shaker-2 mice by an unconventional myosin in a BAC transgene. Science. 280:1998;1444-1447. Through the use of a BAC transgene, the authors track the shaker-2 mouse mutation, which causes deafness and circling behavior, to a point mutation that causes an amino acid substitution in a highly conserved position in the motor domain of a novel unconventional myosin, myosin XV. The auditory hair cells of shaker-2 mice have unusually short stereocilia and an abnormal, long, actin-containing protrusion that extends from their basal end.
42. Wang A., Liang Y., Fridell R.A., Probst F.J., Wilcox E.R., Touchman J.W., Morton C.C., Morell R.J., Noben-Trauth K., Camper S.A., Friedman T.B. Association of unconventional myosin MYO15 mutations with human nonsyndromic deafness DFNB3. Science. 280:1998;1447-1451.
43. Hasson T., Gillespie P.G., Garcia J.A., MacDonald R.B., Zhao Y., Yee A.G., Mooseker M.S., Corey D.P. Unconventional myosins in inner-ear sensory epithelia. J Cell Biol. 137:1997;1287-1307.
44. Metcalf A.B. Immunolocalization of myosin Iβ in the hair cell's hair bundle. Cell Motil Cytoskel. 39:1998;159-165.
45. Bearer E.L., Abraham M.T. 2E4 (kaptin): a novel actin-associated protein from human blood platelets found in lamellipodia and the tips of the stereocilia of the inner ear. Eur J Cell Biol. 78:1999;117-126.
46. Russell L.D., Peterson R.N. Sertoli cell junctions: morphological and functional correlates. Int Rev Cytol. 94:1985;177-211.
47. Vogl A.W., Pfeiffer D.C., Redenbach D.M. Ectoplasmic ('junctional') specializations in mammalian Sertoli cells: influence on spermatogenic cells. Ann NY Acad Sci. 637:1991;175-202.
48. Beach S.F., Vogl A.W. Spermatid translocation in the rat seminiferous epithelium: coupling membrane trafficking machinery to a junction plaque. Biol Reprod. 60:1999;1036-1046.
49. Chafel M.M., Shen W., Matsudaira P. Sequential expression and differential localization of I-, L-, and T-fimbrin during differentiation of the mouse intestine and yolk sac. Dev Dyn. 203:1995;141-151.
50. Matova N., Mahajan-Miklos S., Mooseker M.S., Cooley L. Drosophila Quail, a villin-related protein, bundles actin filaments in apoptotic nurse cells. Development. 126:1999;5645-5657. The authors show that quail is a divergent member of the villin family. In contrast to villin, recombinant quail does not appear to cap, sever or nucleate actin filaments at high concentrations of calcium ion. Instead it appears to bundle actin filaments irrespective of calcium ion concentration. This may reflect differences in amino acid sequence noted for repeat 1 (Figure 2). The differences in calcium ion sensitivity noted for quail and villin could explain why the cytoplasmic actin bundles in Drosophila nurse cells normally remain intact, despite the fact that they experience a significant increase in the concentration of calcium ion. Consistent with this idea, the authors demonstrate that the cytoplasmic actin bundles do indeed become unstable when human villin is expressed in nurse cells that contain a reduced level of quail protein. Finally, the authors remind us that quail expression is strictly restricted to the germline in Drosophila adults and suggest that a villin homolog, distinct from quail, is likely to exist in insect intestinal brush borders.
51. Chen B., Li A., Wang D., Wang M., Zheng L., Bartles J.R. Espin contains an additional actin-binding site in its N terminus and is a major actin-bundling protein of the Sertoli cell-spermatid ectoplasmic specialization junctional plaque. Mol Biol Cell. 10:1999;4327-4339. This article describes the basis for the differences in primary structure observed between espin and small espin, compares the actin-binding and -bundling properties of the two isoforms and presents the results of biochemical quantification and developmental immunolocalization experiments that support the hypothesis that espin is a major actin-bundling protein of the ectoplasmic specialization junctional plaque.
52. Sherman M.B., Jakana J., Sun S., Matsudaira P., Chiu W., Schmid M.F. The three-dimensional structure of the Limulus acrosomal process: a dynamic actin bundle. J Mol Biol. 294:1999;139-149. Using electron crystallographic reconstruction, the authors determined the three-dimensional structure of the actin bundle found at the core of the true discharge of Limulus sperm. They report the positions of the scruin crosslinks within the bundle, demonstrate that the scruin molecules have multiple patterns of interaction within the bundle and suggest how rearrangements could account for the remarkable transition of this actin bundle from its coiled to its true discharge form during the acrosome reaction.