Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1981 Jun 1;89(3):517–524. doi: 10.1083/jcb.89.3.517

Actin-dependent cell elongation in teleost retinal rods: requirement for actin filament assembly

PMCID: PMC2111817  PMID: 6894759

Abstract

Teleost retinal rods elongate when exposed to light. Elongation is mediated by a narrow necklike region called the myoid. In the cichlid Sarotherodon mossambicus, the rod inner segment (composed of the myoid with adjacent ellipsoid) increases in length from 12 micrometers in the dark to 41 micrometers in the light. Long light-adapted myoids contain longitudinally oriented microtubules and bundles of parallel 60-A filaments that we have identified as actin by their ability to bind myosin subfragment 1. In short dark-adapted myoids, only microtubules are recognizable. Colchicine experiments reveal that light-induced rod elongation can occur in the absence of myoid microtubules. Intraocular injections of colchicine at concentrations that disrupt virtually all rod myoid microtubules do not block rod elongation. However, rod elongation is blocked by intraocular injections of cytochalasin B or cytochalasin D. The hierarchy of effectiveness of these drugs is consistent with their effectiveness in inhibiting actin assembly and in disrupting other actin-dependent motile processes. On the basis of ultrastructural observations and the results of these inhibitor studies, we propose that the forces responsible for rod elongation are dependent not on microtubules but on actin filament assembly.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ali M. A. Les réponses rétinomotrices: caractères et mécanismes. Vision Res. 1971 Nov;11(11):1225–1288. doi: 10.1016/0042-6989(71)90010-1. [DOI] [PubMed] [Google Scholar]
  2. Aronson J., Inoué S. Reversal by light of the action of N-methyl N-desacetyl colchicine on mitosis. J Cell Biol. 1970 May;45(2):470–477. doi: 10.1083/jcb.45.2.470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BYERS B., PORTER K. R. ORIENTED MICROTUBULES IN ELONGATING CELLS OF THE DEVELOPING LENS RUDIMENT AFTER INDUCTION. Proc Natl Acad Sci U S A. 1964 Oct;52:1091–1099. doi: 10.1073/pnas.52.4.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beebe D. C., Feagans D. E., Blanchette-Mackie E. J., Nau M. E. Lens epithelial cell elongation in the absence of microtubules: evidence for a new effect of colchicine. Science. 1979 Nov 16;206(4420):836–838. doi: 10.1126/science.493982. [DOI] [PubMed] [Google Scholar]
  5. Begg D. A., Rebhun L. I. pH regulates the polymerization of actin in the sea urchin egg cortex. J Cell Biol. 1979 Oct;83(1):241–248. doi: 10.1083/jcb.83.1.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Borisy G. G., Taylor E. W. The mechanism of action of colchicine. Binding of colchincine-3H to cellular protein. J Cell Biol. 1967 Aug;34(2):525–533. doi: 10.1083/jcb.34.2.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brown S. S., Spudich J. A. Cytochalasin inhibits the rate of elongation of actin filament fragments. J Cell Biol. 1979 Dec;83(3):657–662. doi: 10.1083/jcb.83.3.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Burnside B. Microtubules and actin filaments in teleost visual cone elongation and contraction. J Supramol Struct. 1976;5(3):257–275. doi: 10.1002/jss.400050302. [DOI] [PubMed] [Google Scholar]
  9. Burnside B. The form and arrangement of microtubules: an historical, primarily morphological, review. Ann N Y Acad Sci. 1975 Jun 30;253:14–26. doi: 10.1111/j.1749-6632.1975.tb19189.x. [DOI] [PubMed] [Google Scholar]
  10. Burnside B. Thin (actin) and thick (myosinlike) filaments in cone contraction in the teleost retina. J Cell Biol. 1978 Jul;78(1):227–246. doi: 10.1083/jcb.78.1.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Edds K. T. Dynamic aspects of filopodial formation by reorganization of microfilaments. J Cell Biol. 1977 May;73(2):479–491. doi: 10.1083/jcb.73.2.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Garland D., Teller D. C. A reexamination of the reaction between colchicine and tubulin. Ann N Y Acad Sci. 1975 Jun 30;253:232–238. doi: 10.1111/j.1749-6632.1975.tb19202.x. [DOI] [PubMed] [Google Scholar]
  13. Ishikawa H., Bischoff R., Holtzer H. Formation of arrowhead complexes with heavy meromyosin in a variety of cell types. J Cell Biol. 1969 Nov;43(2):312–328. [PMC free article] [PubMed] [Google Scholar]
  14. Lin D. C., Lin S. Actin polymerization induced by a motility-related high-affinity cytochalasin binding complex from human erythrocyte membrane. Proc Natl Acad Sci U S A. 1979 May;76(5):2345–2349. doi: 10.1073/pnas.76.5.2345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lin S., Lin D. C., Flanagan M. D. Specificity of the effects of cytochalasin B on transport and motile processes. Proc Natl Acad Sci U S A. 1978 Jan;75(1):329–333. doi: 10.1073/pnas.75.1.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. MacLean-Fletcher S., Pollard T. D. Mechanism of action of cytochalasin B on actin. Cell. 1980 Jun;20(2):329–341. doi: 10.1016/0092-8674(80)90619-4. [DOI] [PubMed] [Google Scholar]
  17. Snyder J. A., McIntosh J. R. Biochemistry and physiology of microtubules. Annu Rev Biochem. 1976;45:699–720. doi: 10.1146/annurev.bi.45.070176.003411. [DOI] [PubMed] [Google Scholar]
  18. Tilney L. G. Actin filaments in the acrosomal reaction of Limulus sperm. Motion generated by alterations in the packing of the filaments. J Cell Biol. 1975 Feb;64(2):289–310. doi: 10.1083/jcb.64.2.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Tilney L. G., Hatano S., Ishikawa H., Mooseker M. S. The polymerization of actin: its role in the generation of the acrosomal process of certain echinoderm sperm. J Cell Biol. 1973 Oct;59(1):109–126. doi: 10.1083/jcb.59.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Tilney L. G., Kiehart D. P., Sardet C., Tilney M. Polymerization of actin. IV. Role of Ca++ and H+ in the assembly of actin and in membrane fusion in the acrosomal reaction of echinoderm sperm. J Cell Biol. 1978 May;77(2):536–550. doi: 10.1083/jcb.77.2.536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Wagner H. J., Ali M. A. Retinal organisation in goldeye and mooneye (Teleostei: hiodontidae). Rev Can Biol. 1978 Jun;37(2):65–84. [PubMed] [Google Scholar]
  22. Warren R. H., Brunside B. Microtubules in cone myoid elongation in the teleost retina. J Cell Biol. 1978 Jul;78(1):247–259. doi: 10.1083/jcb.78.1.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Warren R. H. Microtubular organization in elongating myogenic cells. J Cell Biol. 1974 Nov;63(2 Pt 1):550–566. doi: 10.1083/jcb.63.2.550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wilson L., Friedkin M. The biochemical events of mitosis. II. The in vivo and in vitro binding of colchicine in grasshopper embryos and its possible relation to inhibition of mitosis. Biochemistry. 1967 Oct;6(10):3126–3135. doi: 10.1021/bi00862a021. [DOI] [PubMed] [Google Scholar]
  25. Yamada K. M., Spooner B. S., Wessells N. K. Axon growth: roles of microfilaments and microtubules. Proc Natl Acad Sci U S A. 1970 Aug;66(4):1206–1212. doi: 10.1073/pnas.66.4.1206. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES