Epiplasmins and Epiplasm in Paramecium: The Building of a Submembraneous Cytoskeleton

Protist

Volumn 164, Issue 4, 2013, Pages 451-469

  Aubusson Fleury, Anne ^a,b   Bricheux, Geneviève ^c,d   Damaj, Raghida ^c,d   Lemullois, Michel ^a   Coffe, Gérard ^c,d   Donnadieu, Florence ^c,d   Koll, France ^a,b   Viguès, Bernard ^c,d   Bouchard, Philippe ^c,d  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UNIVERSITÉ CLERMONT AUVERGNE   (France)

^d UNIVERSITÉ BLAISE PASCAL   (France)

Author keywords

Basal body docking; Cell morphogenesis; Ciliates.; Ciliogenesis; Structural heredity; Transition zone

Indexed keywords

CILIOPHORA; PARAMECIUM;

EID: 84879397304     PISSN: 14344610     EISSN: 16180941     Source Type: Journal    
DOI: 10.1016/j.protis.2013.04.003     Document Type: Article

References (46)

1. Allen R.D. The morphogenesis of basal bodies and accessory structures of the cortex of the ciliated protozoan Tetrahymena pyriformis. J Cell Biol 1969, 40:716-733.
2. Allen R.D. Fine structure of membraneous and microfibrillar systems in the cortex of Paramecium caudatum. J Cell Biol 1971, 49:1-20.
3. Aubusson-Fleury A., Lemullois M., De Loubresse N.G., Laligné C., Cohen J., Rosnet O., Jerka-Dziadosz M., Beisson J., Koll F. The conserved centrosomal protein FOR20 is required for assembly of the transition zone and basal body docking at the cell surface. J Cell Sci 2012, 125:4395-4404.
4. Aury J.-M., Jaillon O., Duret L., Noel B., Jubin C., Porcel B.M., Ségurens B., Daubin V., Anthouard V., Aiach N., Arnaiz O., Billaut A., Beisson J., Blanc I., Bouhouche K., Câmara F., Duharcourt S., Guigo R., Gogendeau D., Katinka M., Keller A.-M., Kissmehl R., Klotz C., Koll F., Le Mouël A., Lepère G., Malinsky S., Nowacki M., Nowak J.K., Plattner H., Poulain J., Ruiz F., Serrano V., Zagulski M., Dessen P., Bétermier M., Weissenbach J., Scarpelli C., Schächter V., Sperling L., Meyer E., Cohen J., Wincker P. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 2006, 444:171-178.
5. Beisson J., Sonneborn T.M. Cytoplasmic inheritance of the organization of the cell cortex in Paramecium aurelia. Proc Natl Acad Sci USA 1965, 53:275-282.
6. Bouchard P., Chomilier J., Ravet V., Mornon J.P., Viguès B. Molecular characterization of the major membrane skeletal protein in the ciliate Tetrahymena pyriformis suggests n-plication of an early evolutionary intermediate filament protein subdomain. J Cell Sci 2001, 114:101-110.
7. Coffe G., Le Caer J.P., Lima O., Adoutte A. Purification, in vitro reassembly, and preliminary sequence analysis of epiplasmins, the major constituent of the membrane skeleton of Paramecium. Cell Motil Cytoskeleton 1996, 34:137-151.
8. Collins T., Baker R.L., Wilhelm J.M., Olmsted J.B. A cortical scaffold in the ciliate Tetrahymena. J Ultrastruct Res 1980, 70:92-103.
9. Damaj R., Pomel S., Bricheux G., Coffe G., Viguès B., Ravet V., Bouchard P. Cross-study analysis of genomic data defines the ciliate multigenic epiplasmin family: strategies for functional analysis in Paramecium tetraurelia. BMC Evol Biol 2009, 9:125.
10. Dippell R.V. The development of basal bodies in Paramecium. Proc Natl Acad Sci USA 1968, 61:461-468.
11. Fauré-Fremiet E. Le Genre Paranassula Kahl (Ciliata cyrtophorina). Cahiers de Biologie Marine III 1962, 61-77.
12. Fleury A., Delgado P., Iftode F., Adoutte A. Molecular phylogeny of ciliates: What does it tell us about the evolution of the cytoskeleton and of developmental strategies?. Dev Genet 1992, 13:247-254.
13. Galvani A., Sperling L. RNA interference by feeding in Paramecium. Trends Genet 2002, 18:11-12.
14. Hauser K., Haynes W.J., Kung C., Plattner H., Kissmehl R. Expression of the green fluorescent protein in Paramecium tetraurelia. Eur J Cell Biol 2000, 79:144-149.
15. Huttenlauch I., Peck R.K., Stick R. Articulins and epiplasmins: two distinct classes of cytoskeletal proteins of the membrane skeleton in protists. J Cell Sci 1998, 111:3367-3378.
16. Huttenlauch I., Peck R.K., Plessmann U., Weber K., Stick R. Characterisation of two articulins, the major epiplasmic proteins comprising the membrane skeleton of the ciliate Pseudomicrothorax. J Cell Sci 1998, 111:1909-1919.
17. Iftode F., Fleury-Aubusson A. Structural inheritance in Paramecium: Ultrastructural evidence for basal body and associated rootlets polarity transmission through binary fission. Biol Cell 2003, 95:39-51.
18. Iftode F., Adoutte A., Fleury A. The surface pattern of Paramecium tetraurelia in interphase: an electron microscopic study of basal body variability, connections with associated ribbons and their epiplasmic environment. Eur J Protistol 1996, 32(Suppl 1):46-57.
19. Iftode F., Fleury A., Adoutte A. Development of surface pattern during division in Paramecium: III. Study of stomatogenesis in the wild type using antitubulin antibodies and confocal microscopy. Eur J Protistol 1997, 33:145-167.
20. Iftode F., Cohen J., Ruiz F., Torres Rueda A., Chen-Shan L., Adoutte A., Beisson J. Development of surface pattern during division in Paramecium. I. Mapping of duplication and reorganisation of cortical cytoskeletal structures in the wild type. Development 1989, 105:191-211.
21. Jeanmaire-Wolf R., Clérot J.C., Nahon P., Iftode F., Fleury A., Adoutte A. Isolation and characterization of monoclonal antibodies to cytoskeletal and membrane proteins of the Paramecium cortex. Eur J Protistol 1993, 29:311-333.
22. Kaczanowska J., Iftode F., Coffe G., Prajer M., Kosciuszko H., Adoutte A. The protein kinase inhibitor 6-dimethylaminopurine does not inhibit micronuclear mitosis, but impairs the rearrangement of cytoplasmic MTOCs and execution of cytokinesis in the ciliate Paramecium during transition to interphase. Eur J Protistol 1996, 32:2-17.
23. Keryer G., Davis F.M., Rao P.N., Beisson J. Protein phosphorylation and dynamics of cytoskeletal structures associated with basal bodies in Paramecium. Cell Motil Cytoskeleton 1987, 8:44-54.
24. Kloetzel J.A., Baroin-Tourancheau A., Miceli C., Barchetta S., Farmar J., Banerjee D., Fleury-Aubusson A. Plateins: a novel family of signal peptide-containing articulins in euplotid ciliates. J Eukaryot Microbiol 2003, 50:19-33.
25. Kurz S., Tiedtke A. The Golgi apparatus of Tetrahymena thermophila. J Eukaryot Microbiol 1993, 40:10-13.
26. Marrs J.A., Bouck G.B. The two major membrane skeletal proteins (articulins) of Euglena gracilis define a novel class of cytoskeletal proteins. J Cell Biol 1992, 118:1465-1475.
27. Mitchell B., Jacobs R., Li J., Chien S., Kintner C. A positive feedback mechanism governs the polarity and motion of motile cilia. Nature 2007, 447:97-101.
28. Nahon P., Coffe G., Guyader H., Darmanaden-Delorme J., Jeanmaire-Wolf R., Clerot J.C., Adoutte A. Identification of the epiplasmins, a new set of cortical proteins of the membrane cytoskeleton in Paramecium. J Cell Sci 1993, 104:975-990.
29. Omary M.B., Ku N.-O., Tao G.-Z., Toilova D., Liao J. "Heads and tails" of intermediate filament phosphorylation: multiple sites and functional insights. Trends Biochem Sci 2006, 31:383-394.
30. Peck R.K. The ultrastructure of the somatic cortex of Pseudomicrothorax dubius: Structure and function of the epiplasm in ciliated protozoa. J Cell Sci 1977, 25:367-385.
31. Pomel S., Diogon M., Bouchard P., Pradel L., Ravet V., Coffe G., Viguès B. The membrane skeleton in Paramecium: Molecular characterization of a novel epiplasmin family and preliminary GFP expression results. Protist 2006, 157:61-75.
32. Przybos E., Tarcz S., Potekhin A., Rautian M., Prajer M. A two-locus molecular characterization of Paramecium calkinsi. Protist 2012, 163:263-273.
33. Romero M.R., Torres A. Cortical development associated with conjugation of Paramecium. Development 1993, 117:1099-1112.
34. Skouri F., Cohen J. Genetic approach to regulated exocytosis using functional complementation in Paramecium: Identification of the ND7 gene required for membrane fusion. Mol Biol Cell 1997, 8:1063-1071.
35. Sonneborn T. Methods in Paramecium Research. Methods in Cell Physiology 1970, Vol. 4:242-339. Academic Press, New York, London.
36. Sperling L., Keryer G., Ruiz F., Beisson J. Cortical morphogenesis in Paramecium: A transcellular wave of protein phosphorylation involved in ciliary rootlet disassembly. Dev Biol 1991, 148:205-218.
37. Strüder-Kypke M.C., Wright A.D., Fokin S.I., Lynn D.H. Phylogenetic relationships of the Subclass Peniculia (Oligohymenophorea, Ciliophora) inferred from small subunit rRNA gene sequences. J Eukaryot Microbiol 2000, 47:419-429.
38. Vladar E.K., Axelrod J.D. Dishevelled links basal body docking and orientation in ciliated epithelial cells. Trends Cell Biol 2008, 18:517-520.
39. Vladar E.K., Bayly R.D., Sangoram A.M., Scott M.P., Axelrod J.D. Microtubules enable the planar cell polarity of airway cilia. Curr Biol 2012, 22:2203-2212.
40. Wehland J., Weber K. Turnover of the carboxy-terminal tyrosine of alpha-tubulin and means of reaching elevated levels of detyrosination in living cells. J Cell Sci 1987, 88:185-203.
41. Werner M.E., Mitchell B.J. Planar cell polarity: microtubules make the connection with cilia. Curr Biol 2012, 22:R1001-R1004.
42. Williams N.E. The epiplasm gene EPC1 influences cell shape and cortical pattern in Tetrahymena thermophila. J Eukaryot Microbiol 2004, 51:201-206.
43. Williams N.E., Honts J.E., Jaeckel-Williams R.F. Regional differentiation of the membrane skeleton in Tetrahymena. J Cell Sci 1987, 87:457-463.
44. Williams N.E., Honts J.E., Kaczanowska J. The formation of basal body domains in the membrane skeleton of Tetrahymena. Development 1990, 109:935-942.
45. Williams N.E., Vaudaux P.E., Skriver L. Cytoskeletal proteins of the cell surface in Tetrahymena. I. Identification and localization of major proteins. Exp Cell Res 1979, 123:311-320.
46. Williams N.E., Honts J.E., Dress V.M., Nelsen E.M., Frankel J. Monoclonal antibodies reveal complex structure in the membrane skeleton of Tetrahymena. J Eukaryot Microbiol 1995, 42:422-427.