Tubulin polyglycylation in platyhelminthes: Diversity among stable microtubule networks and very late occurrence during spermiogenesis

Cell Motility and the Cytoskeleton

Volumn 39, Issue 4, 1998, Pages 318-330

  Iomini, Carlo ^a   Bré, Marie Hélène ^b   Levilliers, Nicolette ^b   Justine, Jean Lou ^a,c  

^a CNRS   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Platyhelminthes; Polyglycylation; Posttranslational modifications; Spermatozoa; Stable microtubules

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AXONEME; CELL MATURATION; CELL MOTILITY; CELL SELECTION; GLYCATION; MICROTUBULE ASSEMBLY; NERVE CELL NETWORK; NONHUMAN; PLATYHELMINTH; PRIORITY JOURNAL; PROTEIN PROCESSING; SPERMATID; SPERMATOGENESIS; TISSUE DISTRIBUTION;

ANIMALS; ECHINOSTOMA; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENT ANTIBODY TECHNIQUE; GLYCINE; IMMUNOBLOTTING; ISOMERISM; MALE; MICROSCOPY, IMMUNOELECTRON; MICROTUBULES; SPERMATOGENESIS; TUBULIN;

EID: 0031966304     PISSN: 08861544     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0169(1998)39:4<318::AID-CM6>3.0.CO;2-Z     Document Type: Article

References (51)

1. Adoutte, A., Delgado, P., Fleury, A., Levilliers, N., Lainé, M.-C., Marty, M.-C., Boisvieux-Ulrich, E., and Sandoz, D. (1991): Microtubule diversity in ciliated cells: evidence for its generation by post-translational modification in the axonemes of Paramecium and quail oviduct cells. Biol. Cell 71:227-245.
2. Alexander, J.E., Hunt, D.F., Lee, M.K., Shabanowitz, J., Michel, H., Berlin, S.C., MacDonald, T.L., Sundberg, R.J., Rebhun, L.I., and Frankfurter, A. (1991): Characterization of posttranslational modifications in neuron-specific class III beta-tubulin by mass spectrometry. Proc. Natl. Acad. Sci. USA 88:4685-1689.
3. Arevalo, M.A., Nieto, J.M., Andreu, D., and Andreu, J.M. (1990): Tubulin assembly probed with antibodies to synthetic peptides. J. Mol. Biol. 214:105-120.
4. Audebert, S., Desbruyères, E., Gruszczynski, C., Koulakoff, A., Gros, F., Denoulet, P., and Eddé, B. (1993): Reversible polyglutamylation of alpha- and beta-tubulin and microtubule dynamics in mouse brain neurons. Mol. Biol. Cell. 4:615-626.
5. Barra, H.S., Arce, C.A., Rodriguez, J.A., and Caputto, R. (1974): Some common properties of the protein that incorporate tyrosine as a single unit and the microtubule proteins. Biochem. Biophys. Res. Commun. 60:1384-1390.
6. Blose, S.H., Meltzer, D.I., and Feramisco, J.R. (1984): 10 nm filaments are induced to collapse in living cells microinjected with monoclonal and polyclonal antibodies against tubulin. J. Cell Biol., 98:847-858.
7. Boucher, D., Larcher, J.C., Gros, F., and Denoulet, P. (1994): Polyglutamylation of tubulin as a progressive regulator of in vitro interactions between the microtubule-associated protein Tau and tubulin. Biochemistry 33:12471-12477.
8. Bré, M.-H., de Néchaud, B., Wolff, A., and Fleury, A. (1994): Glutamylated tubulin probed in ciliates with the monoclonal antibody GT335. Cell Motil. Cytoskeleton 27:337-349.
9. Bré, M.-H., Redeker, V., Quibell, M., Darmanaden-Delorme, J., Bressac, C., Cosson, J., Huitorel, P., Schmitter, J.-M., Rossier, J., Johnson, T., Adoutte, A., and Levilliers, N. (1996): Axonemal tubulin polyglycylation probed with two monoclonal antibodies: widespread evolutionary distribution, appearance during spermatozoan maturation and possible function in motility. J. Cell Sci. 109:727-738.
10. Bressac, C., Bré, M.-H., Darmanaden-Delorme, J., Laurent, M., Levilliers, N., and Fleury, A. (1995): A massive new posttranslational modification occurs on axonemal tubulin at the final step of spermatogenesis in Drosophila. Eur. J. Cell Biol. 67:346-355.
11. Callen, A.-M., Adoutte, A., Andreu, J.M., Baroin-Tourancheau, A., Bré, M.-H., Ruiz, P.C., Clérot, J.-C., Delgado, P., Fleury, A., Jeanmaire-Wolf, R., Viklicky, V., Villalobo, E., and Levilliers, N. (1994): Isolation and characterization of libraries of monoclonal antibodies directed against various forms of tubulin in Paramecium. Biol. Cell 81:95-119.
12. Caron, J.M. (1997): Posttranslational modification of tubulin by palmitoylation: I. In vivo and cell-free studies. Mol. Biol. Cell 8:621-636.
13. Daddow, L.Y.M. (1986): An abbreviated method of the double lead stain technique. J. Submicrosc. Cytol. 18:221-224.
14. Duvaux-Miret, O., Baratte, B., Dissous, C., and Capron, A. (1991): Molecular cloning and sequencing of the alpha-tubulin gene from Schistosoma mansoni. Mol. Biochem. Parasitol. 49:337-340.
15. Eddé, B., Rossier, J., Le Caer, J.-P., Desbruyères, E., Gros, F., and Denoulet, P. (1990): Posttranslational glutamylation of alphatubulin. Science 247:83-85.
16. Eipper, B.A. (1974): Properties of rat brain tubulin. J. Biol. Chem. 249:1407-1416.
17. Fleury, A., Callen, A.-M., Bré, M.-H., Iftode, F., Jeanmaire-Wolf, R., Levilliers, N., and Clérot, J.-C. (1995): Where and when is microtubule diversity generated in Paramecium? Immunological properties of microtubular networks in the interphase and dividing cells. Protoplasma 189:37-60.
18. Fouquet, J.-P, Eddé, B., Kann, M.-L., Wolff, A., Desbruyéres, E., and Denoulet, P. (1994): Differential distribution of glutamylated tubulin during spermatogenesis in mammalian testis. Cell Motil. Cytoskeleton 27:49-58.
19. Fried, B., and Huffman, J.E. (1996): The biology of the intestinal trematode Echinostoma caproni. Adv. Parasitol. 38:311-368.
20. Fulton, C., and Simpson, P.A. (1976): Selective synthesis and utilisation of flagellar tubulin. The multitubulin hypothesis. In R. Goldman, T. Pollard, and J. Rosenbaum (eds): "Cell Motility." Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp. 987-1005.
21. Gagnon, C., White, D., Cosson, J., Huitorel, P., Eddé, B., Desbruyéres, E., Paturle-Lafanechère, L., Multigner, L., Job, D., and Cibert, C. (1996): The polyglutamylated chain of alpha-tubulin plays a key role in flagellar motility. J. Cell Sci. 109:1545-1553.
22. Gelfand, V.I., and Bershadsky, A.D. (1991): Microtubule dynamics: mechanim, regulation and function. Annu. Rev. Cell Biol. 7:93-116.
23. Greer, K., and Rosenbaum, J.L. (1989): Post-translational modifications of tubulin. In F.D. Warner and J.R. McIntosh (eds): "Cell Movement, Vol. 2: Kinesin, Dynein and Microtubule Dynamics." New York: Alan R. Liss, pp. 47-66.
24. Iomini, C., and Justine, J.-L. (1997): Spermiogenesis and spermatozoon of Echinostoma caproni (Platyhelminthes, Digenea): Transmission and scanning electron microscopy, and tubulin immuno-cytochemistry. Tissue & Cell 29:107-118.
25. Iomini, C., Raikova, O., Noury-Sraïri, N., and Justine, J.-L. (1995): Immunocytochemistry of tubulin in spermatozoa of Platyhelminthes. In B.G.M. Jamieson, J. Ausio, and J.-L. Justine (eds): "Advances in Spermatozoal Phylogeny and Taxonomy." Mém. Mus. Natn. Hist. Nat., 166:97-104.
26. Justine, J.-L. (1991): Phylogeny of parasitic Platyhelminthes: A critical study of synapomorphies proposed on the basis of the ultrastructure of Spermiogenesis and spermatozoa. Can. J. Zool. 69:1421-1440.
27. Khan, I.A., and Ludueña, R.F. (1996): Phosphorylation of beta III-tubulin. Biochemistry 35:3704-3711.
28. Kyhse-Andersen, J. (1984): Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J. Biochem. Biophys. Methods 10:203-209.
29. L'Hernault, S.W., and Rosenbaum, J.L. (1985): Chlamydomonas alpha-tubulin is posttranslationally modified by acetylation on the Sigma-amino group of a lysine. Biochemistry 24:473-478.
30. Laemmli, U.K. (1970): Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
31. LeDizet, M., and Piperno, G. (1987): Identification of an acetylation site of Chlamydomonas alpha-tubulin. Proc. Natl. Acad. Sci. USA 84:5720-5724.
32. LeDizet, M., and Piperno, G. (1991): Detection of acetylated alphatubulin by specific antibodies. Meth. Enzymol. 196:264-274.
33. Levilliers, N., Fleury, A., and Hill, A.-M. (1995): Monoclonal and polyclonal antibodies detect a new type of post-translational modification of axonemal tubulin. J. Cell Sci. 108:3013-3028.
34. Maruta, H., Green K., and Rosenbaum, J.L. (1986): The acetylation of alpha-tubulin and its relationship to the assembly and disassembly of microtubules. J. Cell Biol. 103:571-579.
35. Mary, J., Redeker, V., Le Caer, J.-P, Promé, J.-C., and Rossier, J. (1994): Class I and IVa beta-rubulin isotypes expressed in adult mouse brain are glutamylated. FEBS Lett. 353:89-94.
36. Mary, J., Redeker, V., Le Caer, J.-P., Rossier, J., and Schmitter, J.-M. (1996): Posttranslational modifications in the C-terminal tail of axonemal tubulin from sea urchin sperm. J. Biol. Chem. 271:9928-9933.
37. Multigner, L., Pignot-Paintrand, I., Saoudi, Y., Job, D., Plessmann, U., Rüdiger, M., and Weber, K. (1996): The A and B tubules of the outer doublets of sea urchin sperm axonemes are composed of different tubulin variants. Biochemistry 35:10862-10871.
38. Ozols, J., and Caron, J.M. (1997): Posttranslational modification of tubulin by palmitoylation: II. Identification of sites of palmitoylation. Mol Biol. Cell 8:637-645.
39. Paturle-Lafanechère, L., Eddé, B., Denoulet, P., Van Dorsselaer, A., Mazarguil, H., Le Caer, J.P., Wehland, J., and Job, D. (1991): Characterization of a major brain tubulin variant wich cannot be tyrosinated. Biochemistry 30:10523-10528.
40. Piperno, G., and Fuller, M.T. (1985): Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms. J. Cell Biol. 101:2085-2094.
41. Raff, E.C. (1994): The role of multiple tubulin isoforms in cellular microtubule function. In J.S. Hyams and C.W. Lloyd (eds): "Microtubules." New York: Wiley-Liss, pp. 85-109.
42. Redeker, V., Levilliers, N., Schmitter, J.-M., Le Caer, J.-P., Rossier, J., Adoutte, A. and Bré, M.-H. (1994): Polyglycylation of tubulin: A posttranslational modification in axonemal microtubules. Science 266:1688-1691.
43. Redeker, V., Melki, R., Promé, D., Le Caer, J.-P, and Rossier, J. (1992): Structure of tubulin C-terminal domain obtained by subtilisin treatment. The major alpha and beta tubulin isotypes from pig brain are glutamylated. FEBS Lett. 313:185-192.
44. Richard, J. (1964): Trématodes d'oiseaux de Madagascar (Note III) Espèces de la famille Echinostomatidae Poche 1926. Ann. Parasitol. Hum. Comp. 34:607-620.
45. Rohde, K. (1990): Phylogeny of Platyhelminthes, with special reference to parasitic groups. Int. J. Parasitol. 20:979-1007.
46. Rüdiger, M., Plessman, U., Kloppel, K.D., Wehland, J., and Weber, K. (1992): Class II tubulin, the major brain beta tubulin isotype is polyglutamylated on glutamic acid residue 435. FEBS Lett. 308:101-105.
47. Rüdiger, M., Plessmann, U., Rüdiger, A.H., and Weber, K. (1995): Beta tubulin of bull sperm is polyglycylated. FEBS Lett. 364:147-151.
48. Schneider, A., Plessmann, U., and Weber, K. (1997): Subpellicular and flagellar microtubules of Trypanosoma brucei are extensively glutamylated. J. Cell Sci. 110:431-437.
49. Thompson, W.C. (1982): The cyclic tyrosination/detyrosination of alpha tubulin. Meth. Cell Biol. 24:235-255.
50. Weber, K., Schneider, A., Müller, N., and Plessmann, U. (1996): Polyglycylation of tubulin in the diplomonad Giardia lamblia, one of the oldest eukaryotes. FEBS Lett. 393:27-30.
51. Wolff, A., de Néchaud, B., Chillet, D., Mazarguil, H., Desbruyères, E., Audebert, S., Eddé, B., Gros, F., and Denoulet, P. (1992): Distribution of glutamylated alpha and beta tubulin in mouse tissues using a specific monoclonal antibody, GT335. Eur. J. Cell Biol. 59:425-432.