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. 1991 Feb 2;112(4):641–651. doi: 10.1083/jcb.112.4.641

Three different actin filament assemblies occur in every hair cell: each contains a specific actin crosslinking protein

PMCID: PMC2288863  PMID: 1993735

Abstract

The apex of hair cells of the chicken auditory organ contains three different kinds of assemblies of actin filaments in close spatial proximity. These are (a) paracrystals of actin filaments with identical polarity in stereocilia, (b) a dense gellike meshwork of actin filaments forming the cuticular plate, and (c) a bundle of parallel actin filaments with mixed polarities that constitute the circumferential filament belt attached to the cytoplasmic aspect of the zonula adhaerens (ZA). Each different supramolecular assembly of actin filaments contains a specific actin filament cross-linking protein which is unique to that particular assembly. Thus fimbrin appears to be responsible for paracrystallin packing of actin filaments in stereocillia; an isoform of spectrin resides in the cuticular plate where it forms the whisker-like crossbridges, and alpha actinin is the actin crosslinking protein of the circumferential ZA bundle. Tropomyosin, which stabilizes actin filaments, is present in all the actin filament assemblies except for the stereocilia. Another striking finding was that myosin appears to be absent from the ZA ring and cuticular plate of hair cells although present in the ZA ring of supporting cells. The abundance of myosin in the ZA ring of the surrounding supporting cells means that it may be important in forming a supporting tensile cellular framework in which the hair cells are inserted.

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Selected References

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  1. Bennett J. P., Zaner K. S., Stossel T. P. Isolation and some properties of macrophage alpha-actinin: evidence that it is not an actin gelling protein. Biochemistry. 1984 Oct 9;23(21):5081–5086. doi: 10.1021/bi00316a039. [DOI] [PubMed] [Google Scholar]
  2. Broschat K. O., Burgess D. R. Low Mr tropomyosin isoforms from chicken brain and intestinal epithelium have distinct actin-binding properties. J Biol Chem. 1986 Oct 5;261(28):13350–13359. [PubMed] [Google Scholar]
  3. Broschat K. O., Weber A., Burgess D. R. Tropomyosin stabilizes the pointed end of actin filaments by slowing depolymerization. Biochemistry. 1989 Oct 17;28(21):8501–8506. doi: 10.1021/bi00447a035. [DOI] [PubMed] [Google Scholar]
  4. Burridge K., Feramisco J. R. Non-muscle alpha actinins are calcium-sensitive actin-binding proteins. Nature. 1981 Dec 10;294(5841):565–567. doi: 10.1038/294565a0. [DOI] [PubMed] [Google Scholar]
  5. Carlin R. K., Bartelt D. C., Siekevitz P. Identification of fodrin as a major calmodulin-binding protein in postsynaptic density preparations. J Cell Biol. 1983 Feb;96(2):443–448. doi: 10.1083/jcb.96.2.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cohen C. M., Foley S. F. Biochemical characterization of complex formation by human erythrocyte spectrin, protein 4.1, and actin. Biochemistry. 1984 Dec 4;23(25):6091–6098. doi: 10.1021/bi00320a029. [DOI] [PubMed] [Google Scholar]
  7. Coluccio L. M., Bretscher A. Reassociation of microvillar core proteins: making a microvillar core in vitro. J Cell Biol. 1989 Feb;108(2):495–502. doi: 10.1083/jcb.108.2.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. DeRosier D. J., Tilney L. G. The structure of the cuticular plate, an in vivo actin gel. J Cell Biol. 1989 Dec;109(6 Pt 1):2853–2867. doi: 10.1083/jcb.109.6.2853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Drenckhahn D., Dermietzel R. Organization of the actin filament cytoskeleton in the intestinal brush border: a quantitative and qualitative immunoelectron microscope study. J Cell Biol. 1988 Sep;107(3):1037–1048. doi: 10.1083/jcb.107.3.1037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Drenckhahn D., Franz H. Identification of actin-, alpha-actinin-, and vinculin-containing plaques at the lateral membrane of epithelial cells. J Cell Biol. 1986 May;102(5):1843–1852. doi: 10.1083/jcb.102.5.1843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Drenckhahn D., Kellner J., Mannherz H. G., Gröschel-Stewart U., Kendrick-Jones J., Scholey J. Absence of myosin-like immunoreactivity in stereocilia of cochlear hair cells. Nature. 1982 Dec 9;300(5892):531–532. doi: 10.1038/300531a0. [DOI] [PubMed] [Google Scholar]
  12. Drenckhahn D., Merte C. Restriction of the human kidney band 3-like anion exchanger to specialized subdomains of the basolateral plasma membrane of intercalated cells. Eur J Cell Biol. 1987 Dec;45(1):107–115. [PubMed] [Google Scholar]
  13. Flock A., Bretscher A., Weber K. Immunohistochemical localization of several cytoskeletal proteins in inner ear sensory and supporting cells. Hear Res. 1982 May;7(1):75–89. doi: 10.1016/0378-5955(82)90082-x. [DOI] [PubMed] [Google Scholar]
  14. Flock A., Flock B., Murray E. Studies on the sensory hairs of receptor cells in the inner ear. Acta Otolaryngol. 1977 Jan-Feb;83(1-2):85–91. doi: 10.3109/00016487709128817. [DOI] [PubMed] [Google Scholar]
  15. Glenney J. R., Jr, Glenney P. Fodrin is the general spectrin-like protein found in most cells whereas spectrin and the TW protein have a restricted distribution. Cell. 1983 Sep;34(2):503–512. doi: 10.1016/0092-8674(83)90383-5. [DOI] [PubMed] [Google Scholar]
  16. Hartwig J. H., Shevlin P. The architecture of actin filaments and the ultrastructural location of actin-binding protein in the periphery of lung macrophages. J Cell Biol. 1986 Sep;103(3):1007–1020. doi: 10.1083/jcb.103.3.1007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hartwig J. H., Yin H. L. The organization and regulation of the macrophage actin skeleton. Cell Motil Cytoskeleton. 1988;10(1-2):117–125. doi: 10.1002/cm.970100116. [DOI] [PubMed] [Google Scholar]
  18. Hirokawa N., Keller T. C., 3rd, Chasan R., Mooseker M. S. Mechanism of brush border contractility studied by the quick-freeze, deep-etch method. J Cell Biol. 1983 May;96(5):1325–1336. doi: 10.1083/jcb.96.5.1325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hirokawa N., Tilney L. G. Interactions between actin filaments and between actin filaments and membranes in quick-frozen and deeply etched hair cells of the chick ear. J Cell Biol. 1982 Oct;95(1):249–261. doi: 10.1083/jcb.95.1.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hudspeth A. J. How the ear's works work. Nature. 1989 Oct 5;341(6241):397–404. doi: 10.1038/341397a0. [DOI] [PubMed] [Google Scholar]
  21. Jesaitis A. J., Bokoch G. M., Tolley J. O., Allen R. A. Lateral segregation of neutrophil chemotactic receptors into actin- and fodrin-rich plasma membrane microdomains depleted in guanyl nucleotide regulatory proteins. J Cell Biol. 1988 Sep;107(3):921–928. doi: 10.1083/jcb.107.3.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McGough A. M., Josephs R. On the structure of erythrocyte spectrin in partially expanded membrane skeletons. Proc Natl Acad Sci U S A. 1990 Jul;87(13):5208–5212. doi: 10.1073/pnas.87.13.5208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mooseker M. S. Organization, chemistry, and assembly of the cytoskeletal apparatus of the intestinal brush border. Annu Rev Cell Biol. 1985;1:209–241. doi: 10.1146/annurev.cb.01.110185.001233. [DOI] [PubMed] [Google Scholar]
  24. Nelson W. J., Lazarides E. Switching of subunit composition of muscle spectrin during myogenesis in vitro. 1983 Jul 28-Aug 3Nature. 304(5924):364–368. doi: 10.1038/304364a0. [DOI] [PubMed] [Google Scholar]
  25. Owaribe K., Kodama R., Eguchi G. Demonstration of contractility of circumferential actin bundles and its morphogenetic significance in pigmented epithelium in vitro and in vivo. J Cell Biol. 1981 Aug;90(2):507–514. doi: 10.1083/jcb.90.2.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sandig M., Kalnins V. I. Subunits in zonulae adhaerentes and striations in the associated circumferential microfilament bundles in chicken retinal pigment epithelial cells in situ. Exp Cell Res. 1988 Mar;175(1):1–14. doi: 10.1016/0014-4827(88)90250-9. [DOI] [PubMed] [Google Scholar]
  27. Sans A., Atger P., Cavadore C., Cavadore J. C. Immunocytochemical localization of myosin, tropomyosin and actin in vestibular hair cells of human fetuses and cats. Hear Res. 1989 Jun 15;40(1-2):117–125. doi: 10.1016/0378-5955(89)90105-6. [DOI] [PubMed] [Google Scholar]
  28. Scarfone E., Demêmes D., Perrin D., Aunis D., Sans A. Alpha-fodrin (brain spectrin) immunocytochemical localization in rat vestibular hair cells. Neurosci Lett. 1988 Oct 31;93(1):13–18. doi: 10.1016/0304-3940(88)90004-3. [DOI] [PubMed] [Google Scholar]
  29. Schnittler H. J., Wilke A., Gress T., Suttorp N., Drenckhahn D. Role of actin and myosin in the control of paracellular permeability in pig, rat and human vascular endothelium. J Physiol. 1990 Dec;431:379–401. doi: 10.1113/jphysiol.1990.sp018335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shepherd G. M., Barres B. A., Corey D. P. "Bundle blot" purification and initial protein characterization of hair cell stereocilia. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4973–4977. doi: 10.1073/pnas.86.13.4973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sobin A., Flock A. Immunohistochemical identification and localization of actin and fimbrin in vestibular hair cells in the normal guinea pig and in a strain of the waltzing guinea pig. Acta Otolaryngol. 1983 Nov-Dec;96(5-6):407–412. doi: 10.3109/00016488309132726. [DOI] [PubMed] [Google Scholar]
  32. Stendahl O. I., Hartwig J. H., Brotschi E. A., Stossel T. P. Distribution of actin-binding protein and myosin in macrophages during spreading and phagocytosis. J Cell Biol. 1980 Feb;84(2):215–224. doi: 10.1083/jcb.84.2.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tilney L. G., Egelman E. H., DeRosier D. J., Saunder J. C. Actin filaments, stereocilia, and hair cells of the bird cochlea. II. Packing of actin filaments in the stereocilia and in the cuticular plate and what happens to the organization when the stereocilia are bent. J Cell Biol. 1983 Mar;96(3):822–834. doi: 10.1083/jcb.96.3.822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tilney M. S., Tilney L. G., Stephens R. E., Merte C., Drenckhahn D., Cotanche D. A., Bretscher A. Preliminary biochemical characterization of the stereocilia and cuticular plate of hair cells of the chick cochlea. J Cell Biol. 1989 Oct;109(4 Pt 1):1711–1723. doi: 10.1083/jcb.109.4.1711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Weigt C., Schoepper B., Wegner A. Tropomyosin-troponin complex stabilizes the pointed ends of actin filaments against polymerization and depolymerization. FEBS Lett. 1990 Jan 29;260(2):266–268. doi: 10.1016/0014-5793(90)80119-4. [DOI] [PubMed] [Google Scholar]
  36. Ylikoski J., Pirvola U., Närvänen O., Virtanen I. Nonerythroid spectrin (fodrin) is a prominent component of the cochlear hair cells. Hear Res. 1990 Jan;43(2-3):199–203. doi: 10.1016/0378-5955(90)90228-h. [DOI] [PubMed] [Google Scholar]

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