A Novel Healing Filament in Ciliate Regeneration
Corresponding Author
MARIA JERKA-DZIADOSZ
Polish Academy of Sciences, M. Nencki Institute of Experimental Biology, Department of Cell Biology, 3 Pasteur Str. 02–093 Warsaw, Poland
Corresponding Author. M. Jerka-Dziadosz—Telephone Number: (48-22) 668 62 48; FAX Number: (48-22) 822 53 42; Email: dziadosz@ nencki.gov.plSearch for more papers by this authorKATARZYNA MUSZYNSKA
Polish Academy of Sciences, M. Nencki Institute of Experimental Biology, Department of Cell Biology, 3 Pasteur Str. 02–093 Warsaw, Poland
Search for more papers by this authorWANDA KRAWCZYńSKA
Polish Academy of Sciences, M. Nencki Institute of Experimental Biology, Department of Cell Biology, 3 Pasteur Str. 02–093 Warsaw, Poland
Search for more papers by this authorCorresponding Author
MARIA JERKA-DZIADOSZ
Polish Academy of Sciences, M. Nencki Institute of Experimental Biology, Department of Cell Biology, 3 Pasteur Str. 02–093 Warsaw, Poland
Corresponding Author. M. Jerka-Dziadosz—Telephone Number: (48-22) 668 62 48; FAX Number: (48-22) 822 53 42; Email: dziadosz@ nencki.gov.plSearch for more papers by this authorKATARZYNA MUSZYNSKA
Polish Academy of Sciences, M. Nencki Institute of Experimental Biology, Department of Cell Biology, 3 Pasteur Str. 02–093 Warsaw, Poland
Search for more papers by this authorWANDA KRAWCZYńSKA
Polish Academy of Sciences, M. Nencki Institute of Experimental Biology, Department of Cell Biology, 3 Pasteur Str. 02–093 Warsaw, Poland
Search for more papers by this authorABSTRACT
The interphase cells of the hypotrich ciliate Paraurostyla weissei possess a complex fibrillar system surrounding basal bodies in the compound ciliary assemblages, cirri and membranelles. During replacement of the ciliature at cell division, transient filaments precede and accompany the development of ciliary primordia and participate in the formation of the fission furrow. Both fibrillar systems are recognized by monoclonal antibody FXXXIX 12G9. We studied regeneration of cellular fragments after transection employing the mAb 12G9 and found a new cytoskeletal structure involved in healing of the excisional wound. The healing filament is formed at the wound edge, distally and in connection with the bases of cirri closest to the wound. It is visible 5 min after transection. Concomitant with development of new ciliary primordia, the healing filament shrinks and finally disappears together with other transient fibers formed in this process. Ultrastructural analysis of immunolabeled regenerating cells revealed that structures recognized by mAbl2G9 contain fine filaments whose packing and arrangement depends on accompanying cytoplasmic elements and the developmental status of a fragment. Assembly of the healing fiber does not depend on microtubules and microfilaments since it develops in cellular fragments exposed to cold, nocodazole, and Cytochalasin D. On Western blots of whole cell and cytoskeletal extracts of P. weissei the 12G9 antibody identified one protein band whose molecular weight corresponds to 60 kDa.
References
- Ayscough, K. R. & Drubin, D. G. 1996. ACTIN: general principles from studies in Yeast. Ann. Rev. Cell Dev. Biol., 2: 129–160.
- Balamuth, W. 1940. Regeneration in Protozoa: a problem of morphogenesis. Quart Rev. Biol., 15: 290–337.
- Balbiani, E. G. 1893. Nouvelles recherches experimentales sur la mer-otomie des Infusoires cilies. Ann. Microgr., 5: 1–25, 49–84, 113–137.
- Bement, W. M., Forscher, P & Mooseker, M. 1993. Novel cytoskeletal structure involved in purse-string wound closure and cell polarity maintenance. J. Cell Biol., 121: 565–578.
- Brock, J., Midwinter, K., Lewis, J. & Martin, P. 1996. Healing of incisional wounds in the embryonic chick wing bud: characterization of the actin purse-string and demonstration of a requirement of Rho activation. J. Cell Biol., 135: 1097–1107.
- Chant, J. 1994. Cell polarity in yeast. Trends Genet., 10: 328–333.
- Chant, J. & Pringle, J. R. 1995. Patterns of bud-site selection in the yeast Saccharomyces cerevisiae. J. Cell Biol., 129: 751–765.
- Cooper, J. A. & Kiehart, D.P. 1996. Septins may form a ubiquitous family of cytoskeletal filaments. J. Cell Biol., 134: 1345–1348.
- De Brabander, M. J., Van de Vetre, R. M. L., Aerts, E. F., Borges, M. & Jansen, P A. J. 1976. The effects of methyl 5-(-thienylcarboxynyl)-1-H-benzimidazol-I-carbamate, (R. 17934#C 288159), a new synthetic antitumoral drug interfering with microtubules on mammalian cells cultured in vitro. Cancer Res., 36: 905–916.
- De Marini, D. J., Adams, A. E. M., Fares, H., De Virgilio, C., Calle, G., Chuang, J. S. & Pringle J. R. 1997. A septin-based hierarchy of proteins required for localized deposition of chitin in the Sacchnromyces cerevisiae cell wall. J. Cell Biol., 139: 75–93.
- Drubin, D. G. & Nelson, W. J. 1996. Origins of cell polarity. Cell, 84: 335–344.
- Edamatsu, M., Hirono, M. & Watanabe, Y. 1992. Tetrahymena profilin is localized in the division furrow. J. Biochem., 112: 637–642.
- Euteneuer, U. & Schliwa, M. 1992. Mechanism of centriole positioning during the wound response in BSC-1 cells. J. Cell Biol., 116: 1157–1166.
- Fares, H., Goetsch, L. & Pringle, J. 1996. Identification of a develop-mentally regulated septin and involvement of the septins in spore formation in Saccharomyces cerevisiae. J. Cell Biol., 132: 399–411.
- Fares, H., Peifer, M. & Pringle, J. 1995. Localization and possible functions of Drosophila septins. Mol. Biol. Cell., 6: 1843–1859.
- Fauré-Fremiet, E. 1967. La regeneration chez les Protozoaires. Bull. SOC. Zool. France., 92: 249–272.
- Field, C. M., Al-Alvar, O., Rosenblatt, J., Wong, M. L., Alberts, B. & Michison, T. J. 1996. A purified Drosophila septins complex forms filaments and exhibits GTPase activity. J. Cell Biol., 133: 605–616.
- Fleury, A., Lemullois, M. & Coffe, G. 1998. Distribution of a centro-somal antigen during morphogenesis in Euplotes (ciliata Hypotrichi-da). Biol. Cell. 90: 307–318.
- Fleury, A., Le Guyader, H., Iftode, E., Laurent, M. & Bornens, M. 1993. A scaffold for basal body patterning revealed by a monoclonal antibody in the hypotrich ciliate Paraurostyla weissei. Dev. Biol., 157: 285–302.
- Frankel, J. 1989. Pattern Formation. Ciliate Studies and Models. Oxford University Press. New York , Oxford . 314 p.
- Frazier, J. A., Wong, Mei Lie, Longtine, M. S., Pringle, J. R., Mann, M., Mitchison, T. J. & Field, C. 1998. Polymerization of purified yeast septins: Evidence that organized filament arrays may not be required for septin function. J. Cell Biol., 143: 737–749.
- Garreau de Loubresse, N., Keryer, G., Vigues, B. & Beisson, J. 1988. A contractile cytoskeletal network of Paramecium: the infraciliary lattice. J. Cell Sci., 90: 351–364.
- Golińska, K. & Doroszewski, M. 1964. The cell shape of Dileptus in the course of division and regeneration. Acta Protozool., 259–67.
- Golińska, K. & Grain, J. 1969. Observations sur les modifications ul-trastructurales lors de la regeneration ches Dileptus cygnus Clap. et Lac., 59, Cilie holotriche gymnostome. Protistologica, 5: 447–464.
- Grain, J. & Bohatier, J. 1977. La regeneration chez les protozoaires cilies. Ann. Biol., 16: 13–240.
- Grgbecka, L., Pomorski, P & Opatowska. A. 1995. Differences in the motility of Amoeba proteus isolated fragments are determined by F-actin arrangement and cell nucleus presence. Cell Biol. Int., 19: 47–854.
- Hirono, M., Kumagai, Y., Numata, O. & Watanabe Y. 1989. Purification of Tetrahymenn actin reveals some unusual properties. Proc. Natl. Acad. Sci. USA, 86: 75–79.
- Hirono, M., Nakamura, M., Tsunemoto, M., Yasuda, T., Ohba, H., Nu- mata, O. & Watanabe, Y. 1987. Tetruhymena actin: localization and possible biological roles of actin in Tetruhymena cells. J. Biochem., 102: 537–545.
- Janish, R. 1967. Electron microscopy study of regeneration of surface structures of Paramecium caudatum. Folia Biol., 13: 386–392.
- Jeon, K. W. & Jeon, M. S. 1975. Cytoplasmic filaments and cellular wound healing in Amoeba proteus. J. Cell Biol., 17: 249–343.
- Jerka-Dziadosz, M. 1980. Ultrastructural study on development of the hypotrich ciliate Paraurostyla weissei. Formation and morphogenetic movements of ventral ciliary primordia. Protistologica, 16: 571–589.
- Jerka-Dziadosz, M. 1981. Cytoskeleton-related structures in Tetruhymena thermophila: microfilaments at the apical and division-furrow rings. J. Cell Sci., 51: 241–253.
- Jerka-Dziadosz, M. 1982. Ultrastructural study on development of the hypotrich ciliate Paraurostyla weissei. IV. Morphogenesis of dorsal bristles and caudal cirri. Protistologica, 18: 237–251.
-
Jerka-Dziadosz, M.
1985. Mirror-image configuration of the cortical pattern causes modification in propagation of microtubular structures in the hypotrich ciliate Paraurostyla weissei.
Wilhelm Roux's Arch. Dev. Biol, 194: 311–324.
10.1007/BF00877369 Google Scholar
- Jerka-Dziadosz, M. 1990. Domain-specific changes of ciliary striated rootlets during the cell cycle in the hypotrich ciliate Paraurostyla weissei. J. Cell Sci., 96: 613–630.
- Jerka-Dziadosz, M. & Czupryn, A. 1995. Development of ventral primordia in pervasive ciliary hypertrophy mutants (PCH) of the hypotrich ciliate Paraurostyla weissei. Acta Protozool., 34: 249–259.
- Jerka-Dziadosz, M. & Czupryn, A. 1997. The filaments supporting ciliary primordia and fission furrow in the hypotrich ciliate Paraurostyla weissei, revealed by the monoclonal antibody 12G9: studies on wild-type and ciliary hypertrophy mutant. Protoplasma, 197: 241–257.
- Jerka-Dziadosz, M. & Frankel, J. 1969. An analysis of the formation of ciliary primordia in the hypotrich ciliate Urostyla weissei. J. Protozool., 1: 512–537.
- Jerka-Dziadosz, M., Jenkins, L. M., Nelsen, E. M., Williams, N. E., Jaeckel-Williams, R. & Frankel, J. 1995. Cellular polarity in ciliates: persistence of global polarity in a mutant of Tetrahymena thermophila that disrupts cytoskeletal organization. Dev. Biol., 169: 644–661.
- Keryer, G., Iftode, E & Bornens, M. 1990. Identification of proteins associated with microtubule-organizing centres and filaments in the oral apparatus of the ciliate Paramecium tetraurelia. J. Cell Sci., 97: 553–563.
- Kinoshita, M., Kumar, S., Mizoguchi, A., Ide, C., Kinoshita, A., Har-aguchi, T., Hiraoka, Y. & Noda, M. 1997. Nedd5, a mammalian septin, is a novel cytoskeletal component interacting with actin-based structures. Genes & Develop., 11: 1535–1547.
- Laemmli, U. K. 1970: Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature (London), 227: 680–685.
- Lippincot, J. & Li, R. 1998. Sequential assembly of Myosin II., and IQGAP-like protein, and filamentous actin to a ring structure involved in budding yeast cytokinesis. J. Cell Biol., 140: 335–366.
- Loncar, D. & Singer, S. J. 1995. Cell membrane formation during the cellularization of the syncytial blastoderm. Proc. Natl. Acad. Sci. USA, 92: 2199–2203.
- Longtine, M. S., DeMarini, D. J., Valencik, M. L., Al-Awar, O. S., Fares, H., De Virgilio, C. & Pringle, J. R. 1996. The septins: roles in cytokinesis and other processes. Curr. Opin. Cell Biol., 8: 106–119.
- Madeddu, I., Klotz, C., LeCaer, J. P. & Beisson, J. 1996. Characterization of centrin genes in Paramecium. Eur. J. Biochem., 238: 121–128.
- Martin, P & Lewis, J. 1992. Actin cables and epidermal movement in embryonic wound healing. Nature (London), 360: 179–183.
- Nelsen, E. M., Williams, N. E., Yi, H. & Frankel, J. 1994. “Fenestrin” and conjugation in Tetrahymena thermophila. J. Eukaryot. Micro-biol., 1: 483–495.
- Neufeld, T. P. & Rubin, G. M. 1994. The Drosophila peanut gene is required for cytokinesis and encodes a protein similar to yeast putative bud neck filament proteins. Cell, 77: 371–379.
- Ozsarac, N., Bhattacharyya, M., Dawes, I. W. & Clancy, M. J. 1995. The SPR3 gene encodes a sporulation-specific homologue of the yeast CDC3/10/12 family of bud neck microfilaments and is regulated by ABFI. Gene, 164: 157–162.
- Pringle, J. R., Adams, E. M., Drubin, D. G. & Haarer, B. K. 1991. Immunofluorescence methods in yeast. Meth. Enzymol., 194: 32–735.
- Sanders, S. L. & Field, C. 1994. Septins in common? Curr. Biol., 4: 907–910.
- Satterwhite, L. L. & Pollard, T. D. 1992. Cytokinesis. Curr. Op. Cell Biol., 4: 43–52.
- Scherbaum, O. & Zeuthen, E. 1954. Induction of synchronous division in mass cultures of Tetrahymena pyriformis. Exp. Cell Res., 6: 221–227.
- Schliwa, M. & van Blerkom, J. 1981. Structural interaction of cytoskeletal components. J. Cell Biol. 90: 222–235.
- Shelanski, M. L., Gaskin, E & Cantor, C. R. 1973. Microtubule assembly in the absence of added nucleotides. Proc. Natl. Acad. Sci. USA., 70: 765–768.
-
Tartar, V.
1961. The Biology of Stentor.
Oxford
, Pergamon Press. p.
1–413.
10.1016/B978-0-08-009343-7.50006-5 Google Scholar
- Towbin, H., Staehelin, T. & Gordon, J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci USA., 76: 4350–4354.
- Vigues, B., Metenier, G. & Senaud, J. 1984. Biochemical and immunological characterization of the microfibrillar ecto-endoplasmic boundary in the ciliate Isotricha prostoma. Biol. Cell., 51: 67–78.
- Weischer, A., Freiburg, M. & Heckmann, K. 1985. Isolation and partial characterization of gamone 1 of Euplotes octocarinatus. FEBS Lett., 191: 176–180.
- Wirnsberger, E., Foissner, W. & Adam, H. 1985. Cortical pattern in non-dividers and reorganizers of an Austrian population of Paraurostyla weissei (Ciliophora, Hypotricha): A comparative morphological and biometrical study. Zool. Scripta., 14: 1–10.