Cell and Tissue Research

, Volume 210, Issue 3, pp 371–382 | Cite as

Hormone-induced filopodium formation and movement of pigment, carotenoid droplets, into newly formed filopodia

  • Szecheng J. Lo
  • T. T. Tchen
  • John D. Taylor


Treatment of cultured goldfish xanthophores by hormone (ACTH) or c-AMP induces not only pigment dispersion, but subsequent outgrowth of processes, and pigment translocation into these processes. These latter effects are shown to proceed as follows: First the edge of the cytoplasmic lamellae takes on a scalloped contour with numerous protrusions. These presumably serve as nucleation centers where short microfilament bundles are assembled, Later, the microfilament bundles elongate (“grow”), often resulting in an extension of the protrusions to become filopodia while the proximal end of the microfilaments penetrates into the thicker portion of the cellular process which now houses the pigment, i.e., the carotenoid droplets. Carotenoid droplets appear to migrate along the microfilament bundles, or cytoplasmic channels associated with them, into the filopodia. Finally, some of the filopodia become broader, thicker and laden with carotenoid droplets and are then recognized by light microscopy as pigmented cellular processes. The microfilaments have been shown to be actin filaments by their thickness, the size of their subunits, and decoration by heavy meromyosin. Evidence is presented which suggests that the growth of these actin filaments may come about by recruitment from short F-actin strands found in random orientation in adjacent areas.

Key words

Filopodia Microfilaments Cellular processes Xanthophores Pigment cells 


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  1. Albrecht-Buehler G (1976) The function of filopodia in spreading 3T3 mouse fibroblasts. In: Cell Motility, Book A, pp 247–264: Cold Spring Harbor LaboratoryGoogle Scholar
  2. Axline SH, Reaven EP (1974) Inhibition of phagocytosis and plasma membrane mobility of the cultivated macrophage by cytochalasin B. role of subplasmalemmal microfilament. J Cell Biol 62:647–659Google Scholar
  3. Bagnara JT, Hadley ME (1973) Chromatophores and color change. Prentice Hall, New JerseyGoogle Scholar
  4. Buckley IK (1975) Three-dimensional fine structure of cultured cells: possible implication for subcellular motility. Tissue Cell 7:51–72Google Scholar
  5. Buckley IK, Porter KR (1975) Electron microscopy of critical dried whole cultured cells. J Microsc (Oxf) 104:107–120Google Scholar
  6. Butman BT, Obika M, Tchen TT, Taylor JD (1979) Hormone-induced pigment translocation in amphibian dermal iridophores, in vitro: Changes in cell shape. J Exp Zool 208:17–34Google Scholar
  7. Byers HR, Porter KR (1977) Transformation in the structure of the cytoplasmic ground substance in erythrophores during pigment aggregation and dispersion. I. A study using whole-cell preparation in stereo high voltage electron microscopy. J Cell Biol 75:541–558Google Scholar
  8. Edds KT (1977) Dynamic aspects of filopodial formation by reorganization of microfilaments. J Cell Biol 73:479–491Google Scholar
  9. Fujii R (1966) Correlation between fine structure and activity in fish melanophores. In: Prota G, Muehlbock O (eds) Structure and control of the melanocyte. Springer, Berlin Heidelberg, New York, pp 114–123Google Scholar
  10. Kuczmarski ER, Rosenbaum JL (1979) Studies on the organization and localization of actin and myosin in neurons. J Cell Biol 80:356–371Google Scholar
  11. Lazarides E (1976) Two general classes of cytoplasmic actin filaments in tissue cells: the role of tropomyosin. J Supramolec Struc 5:531–563Google Scholar
  12. Lo SJ, Tchen TT, Taylor JD (1979) ACTH-induced internalization of plasma membrane in xanthophores of the goldfish, Carassius auratus L. Biochem Biophys Res Com 86:748–754Google Scholar
  13. Malawista SZ (1971) Cytochalasin B reversibly inhibits melanin granule movement in melanocytes. Nature (Lond) 234:354–355Google Scholar
  14. Maupin-Szamier P, Pollard TD (1978) Actin filament destruction by osmium tetroxide. J Cell Biol 77:837–852Google Scholar
  15. McGuire J, Moellmann G (1972) Cytochalasin B: effects on microfilaments and movement of melanin granules within melanocytes. Science 175:642–644Google Scholar
  16. McGuire J, Moellmann G, McKeon H (1972) Cytochalasin B and pigment granule translocation. J Cell Biol 52:754–758Google Scholar
  17. Mooseker MS, Tilney LG (1975) Organization of an actin filament-membrane complex. Filament polarity and membrane attachment in the microvilli of intestinal epithelial cells. J Cell Biol 67:725–743Google Scholar
  18. Novales RR, Novales BJ (1965) The effects of osmotic pressure and calcium deficiency on the response of tissue-cultured melanocytes to melanocyte-stimulating hormone. Gen comp Endocrinol 5:568–576Google Scholar
  19. Novales RR, Novales BJ (1972) Effect of Cytochalasin B on the response of the chromatophores of isolated frog skin to MSH, theophylline, and dibutyryl cyclic AMP. Gen Comp Endocrinol 19:363–366Google Scholar
  20. Obika M (1975) The change in cell shape during pigment migration in melanophores of a teleost, Oryzias latipes. J. Exp Zool 191:427–432Google Scholar
  21. Obika M (1976) Pigment migration in isolated fish melanophores. Annot Zool Jpn 49:157–163Google Scholar
  22. Obika M, Menter DG, Tchen TT, Taylor JD (1978a) Actin microfilaments in melanophores of Fundulus heteroclitus their possible involvement in melanosome migration. Cell Tissue Res 193:387–397Google Scholar
  23. Obika M, Lo SJ, Tchen TT, Taylor JD (1978b) Ultrastructural demonstration of hormone-induced movement of carotenoid droplets and endoplasmic reticulum in xanthophores of the goldfish, Carassius auratus L. Cell Tissue Res 190:409–416Google Scholar
  24. Otto JJ, Kane RZ, Bryan J (1979) Formation of filopodia in coelomocytes: localization of fascin, a 58,000 dalton actin cross-linking protein. Cell 17:285–293Google Scholar
  25. Palevitz BA, Hepler PK (1975) Identification of actin in situ at the ectoplasm-endoplasm interface of Nitella. Microfilament chloroplast association. J Cell Biol 65:29–38Google Scholar
  26. Perry MM, John HA, Thomas NST (1971) Actin-like filaments in the clevage furrow of newt egg. Exp Cell Res 65:249–253Google Scholar
  27. Pollard TD (1976) Cytoskeletal functions of cytoplasmic contractile proteins. J Supramolec Struc 5:317–334Google Scholar
  28. Sanger JW (1975) Presence of actin during chromosomal movement. Pro Natl Acad Sci (USA) 72:2451–2455Google Scholar
  29. Schliwa M (1975) Microtubule distribution and melanosome movements in fish melanophores. In: Borgers M, de Branbander M (eds) Microtubules and microtubule inhibitors. North-Holland Pub Co, Amsterdam, pp 215–228Google Scholar
  30. Schliwa M (1978) Microtubular apparatus of melanophores. Three-dimensional organization. J Cell Biol 76:605–614Google Scholar
  31. Schliwa M (1979) Stero high voltage electron microscopy of melanophores: matrix transformations during pigment movements and the effects of cold and colchicine. Exp Cell Res 118:323–340Google Scholar
  32. Schliwa M, Bereiter-Hahn J (1973a) Pigment movements in fish melanophores: morphological and physiological studies. II. Cell shape and microtubules. Z Zellforsch 147:107–125Google Scholar
  33. Schliwa M, Bereiter-Hahn J (1973b) Pigment movements in fish melanophores: morphological and physiological studies. III. The effects of colchicine and vinblastine. Z Zellforsch 147:127–148Google Scholar
  34. Schliwa M, Osborn M, Weber K (1978) Microtubule system of isolated fish melanophores as revealed immunofluorescence microscopy. J Cell Biol 76:229–236Google Scholar
  35. Schollmeyer JZ, Goll DZ, Tilney LG, Mooseker M, Robson R, Stromer M (1974) Localization of -actinin in non-muscle material. J Cell Biol 63:304aGoogle Scholar
  36. Taylor JD, Bagnara JT (1972) Dermal chromatophores. Am Zool 12:43–62Google Scholar
  37. Tilney LG (1976) The polymerization of actin. II. Aggregates of nonfilamentous actin and its associated proteins: a storage form of actin. J Cell Biol 69:73–89Google Scholar
  38. Tilney LG, Cardell RR, Jr (1970) Factors controlling the reassembly of the microvillus border of the small intestine of the salamander. J Cell Biol 47:408–422Google Scholar
  39. Willingham MC (1976) Cyclic AMP and cell behavior in cultured cells. Int Rev Cytol 44:318–363Google Scholar
  40. Willingham MC, Pastan I (1975) Cyclic AMP modulates microvillus formation and agglutinability in transformed and normal mouse fibroblasts. Proc Natl Acad Sci (USA) 72:1263–1267Google Scholar
  41. Winchester JD, Ngo F, Tchen TT, Taylor JD (1976) Hormone-induced dispersion or aggregation of carotenoid-containing smooth endoplasmic reticulum in cultured xanthophores from the goldfish, Carassius auratus L. Endocrinol Res Comm 3:335–342Google Scholar

Copyright information

© Springer-Verlag 1980

Authors and Affiliations

  • Szecheng J. Lo
    • 1
  • T. T. Tchen
    • 1
  • John D. Taylor
    • 1
  1. 1.Departments of Biological Sciences and ChemistryWayne State UniversityDetroitUSA

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