Polyglutamylation and polyglycylation of α- and β-tubulins during in vitro ciliated cell differentiation of human respiratory epithelial cells

Journal of Cell Science

Volumn 112, Issue 23, 1999, Pages 4357-4366

  Million, Karine ^a   Larcher, Jean Christophe ^b   Laoukili, Jamila ^a   Bourguignon, David ^a,c   Marano, Francelyne ^a   Tournier, Frédéric ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b PSL Research University   (France)

^c Imagis GRAVIR IMAG   (France)

Author keywords

Centriole basal body; Ciliogenesis; Primary culture; Tubulin post translational modification

Indexed keywords

ALPHA TUBULIN; BETA TUBULIN; GOLD; MONOCLONAL ANTIBODY; POLYGLUTAMINE;

ARTICLE; AXONEME; CELL DIFFERENTIATION; CENTRIOLE; CILIARY MOTILITY; CILIATED EPITHELIUM; CONTROLLED STUDY; GLYCATION; HUMAN; HUMAN CELL; IMMUNOELECTRON MICROSCOPY; NOSE MUCOSA; PRIORITY JOURNAL; TWO DIMENSIONAL ELECTROPHORESIS;

CELL DIFFERENTIATION; CILIA; GLYCOSYLATION; HUMANS; MICROTUBULES; NASAL POLYPS; POLYGLUTAMIC ACID; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RESPIRATORY MUCOSA; TUBULIN; TURBINATES;

EID: 0033491915     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (55)

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. Audebert, S., Desbruyères, E., Gruszczynsky, C., Koulakoff, A., Gros, F., Denoulet, P. and Eddé, B. (1993). Reversible glutamylation of α- and β-tubulin and microtubule dynamics in mouse brain neurons. Mol. Biol. Cell. 4, 615-026.
3. Audebert, S., White, D., Cosson, J., Huitorel, P., Eddé, B. and Gagnon, C. (1999). The carboxy-terminal sequence Asp427-Glu432 of beta-tubulin plays an important function in axonemal motility. Eur. J. Biochem. 261, 48-56.
4. Barra, H. S., Arce, C. A. and Argarana, C. E. (1988). Post-translational tyrosination/detyrosination of tubulin. Mol. Neurobiol. 2, 133-153.
5. Bobinnec, Y., Moudjou, M., Fouquet, J. P., Desbruyères, E., Edde, B. and Bornens, M. (1998a). Glutamylation of centriole and cytoplasmic tubulin in proliferating non-neuronal cells. Cell Motil. Cytoskel. 39, 223-232.
6. Bobinnec, Y., Khodjakov, A., Mir, L. M., Rieder, C. L., Eddé, B. and Bornens, M. (1998b). Centriole disassembly in vivo and its effect on centrosome structure and function in vertebrate cells. J. Cell Biol. 143, 1575-1589.
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 as a probe in ciliates with the monoclonal antibody GT335. Cell Motil. Cytoskel. 27, 337-349.
9. Bré, M. H., Redeker, V., Quibel, M., Darmanaden-Delorme, J., Bressac, C., Cosson, J., Vuitorel, 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. Bré, M. H., Redeker, V., Vinh, J., Rossier, J. and Levilliers, N. (1998). Tubulin polyglycylation: differential post-translational modification of dynamic cytoplasmic and stable axonemal microtubules in Paramecium. Mol. Biol. Cell 9, 2655-2665.
11. Bressac, C., Bré, M. H., Darmanaden-Delorme, J., Laurent, M., Levilliers, N. and Fleury, A. (1995). A massive new post-translational modification occurs on axonemal tubulin at the final step of spermatogenesis in Drosophila. Eur. J. Cell Biol. 67, 346-355.
12. Bulinski, J. C. and Gundersen, G. G. (1991). Stabilisation and post-translational modification of microtubules during cellular morphogenesis. BioEssays 13, 285-293.
13. Callen, A. M., Adoutte, A., Andreu, J. M., Baroin-Tourancheau, A., Bré, M. H., Calvo-Ruir, P., Clérot, J. C., Delgado, J. C., 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.
14. Clary-Meinesz, C. F., Cosson, J., Huitorel, P. and Blaive, B. (1992). Temperature effect on ciliary beat frequency of human nasal and tracheal ciliated cells. Biol. Cell 76, 335-338.
15. Cosson, J., White, D., Huitorel, P., Eddé, B., Cibert, B., Audebert, S. and Gagnon, C. (1996). Inhibition of flagellar beat frequency by a new anti-β-tubulin antibody. Cell Motil. Cytoskel. 35, 100-112.
16. De Jong, P. M., Van Sterkenburg, M. A. J. A., Hesseling, S. C., Kempenaar, J. A., Mulder, A. A., Mommaas, A. M., Dijkman, J. H. and Ponec, M. (1994). Ciliogenesis in human bronchial epithelial cells cultured at the air-liquid interface. Am. J. Respir. Cell Mol. Biol. 10, 271-277.
17. Dirksen, E. R. (1991). Centriole and basal body formation during ciliogenesis revisited. Biol. Cell 72, 31-38.
18. Eddé, B., Rossier, J., Le Caer, J. P., Desbruyères, E., Gros, F. and Denoulet, P. (1990). Post-translational glutamylation of α-tubulin. Science 247, 83-85.
19. Eddé, B., Rossier, J., Le Caer, J. P., Desbruyères, E., Gros, F. and Denoulet, P. (1992). Polyglutamylated α-tubulin can enter the tyrosination/detyrosination cycle. Biochemistry 31, 403-410.
20. 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.
21. Fouquet, J. P., Eddé, B., Kann, M. L., Wolff A., Desbruyères E. and Denoulet, P. (1994). Differential distribution of glutamylated tubulin during spermatogenesis in mammalian testis. Cell Motil. Cytoskel. 27, 49-58.
22. Gagnon, C., White, D., Cosson, J., Huitorel, P., Eddé, B., Desbruyères, E., Paturle-Lafanechère, L., Multigner, L., Job, D. and Cibert C. (1996). The polyglutamylaled chain of α-tubulin plays a key role in flagellar motility. J. Cell Sci. 109, 1545-1553.
23. Jorissen, M., Van Der Schueren, B., Van Der Berghe, H. and Cassiman, J. J. (1991). Contribution of in vitro culture methods for respiratory epithelial cells to the study of the physiology of the respiratory tract. Eur. Respir. J. 4, 210-217.
24. Kaartinen, L., Nettesheim, P., Adler, K. B. and Randell, S. H. (1993). Rat tracheal epithelial cell differentiation in vitro. In Vitro Cell. Dev. Biol. 29A, 481-492.
25. Kann, M. L., Prigent, Y., Levilliers, N., Bré, M. H. and Fouquet, J. P. (1998). Expression of glycylated tubulin during the differentiation of spermatozoa in mammals. Cell Motil. Cytoskel. 41, 341-352.
26. Khawaja, S., Gundersen, G. G. and Bulinski, J. C. (1988). Enhanced stability of microtubules enriched in tyrosinated tubulin is not a direct function of detyrosinalion level. J. Cell Biol. 106, 141-149.
27. Laemmli, U. K. (1970). Cleveage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
28. Larcher, J. C., Boucher, D., Lazereg, S., Gros, F. and Denoulet, P. (1996). Interaction of kinesin motor domains with α- and β-tubulin subunits as a Tau-independent binding site. Regulation by polyglutamylation. J. Biol. Chem. 271, 22117-22124.
29. LeDizet, M. and Piperno G. (1987). Identification of an acetylation site of Chlamydornonas α-tubulin. Proc. Natl. Acad. Sci. USA 84, 5720-5724.
30. 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.
31. L'Hernault, S. W. and Rosenbaum, J. L. (1985). Reversal of the post-translational modification on Chlamydomonas α-tubulin occurs during flagellar resorbtion. J. Cell Biol. 100, 457-462.
32. Luduena, R. F., Zimmermann, H. S. and Little, M. (1988). Identification of the phosphorylated β-tubulin in differentiated neuroblastoma cell. FEBS Lett. 230, 142-146.
33. MacRae, T. H. (1997). Tubulin post-translational modifications. Enzymes and their mechanisms of action. Eur. J. Biochem. 244, 265-278.
34. Mary J., Redeker, V., Le Caer, J. P., Rossier, J. and Schmitter, J. M. (1996). Post-translational modifications in the C-terminal tail of axonemal tubulin from sea urchin sperm. J. Biol. Chem. 271, 9928-9933.
35. Multigner, L., Pignot-Paintrand, I., Saoudi, Y., Job, D., Plessman, A., Rüdiger, M. and Weber, K. (1996). The A and B tubules of the outer doublets of sea urchin axonemes are composed of different tubulin variants. Biochemistry 35, 10862-10871.
36. Nasr, G., Schoevaert, D., Marano, F., Venant, A. and Legrand, J. J. (1995). Progress in the measurement of ciliary beat frequency by automated image analysis: application to mammalian tracheal epithelium. Anal. Cell. Pathol. 9, 165-177.
37. O'Farrel, P. H. (1975). High-resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250, 4007-4021.
38. 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 which cannot be tyrosinated. Biochemistry 30, 10523-10528.
39. Paturle-Lafanechère, L., Manier, M., Trigault, N., Pirollet, F., Mazarguil, H. and Job, D. (1994). Accumulation of delta2-tubulin, a major tubulin variant which cannot be tyrosinated, in neuronal tissues and in stable microtubule assemblies. J. Cell Sci. 107, 1529-1543.
40. Rabilloud, T., Adessi, C., Giraudel, A. and Lunardi, J. (1997). Improvement of the solubilization of proteins in two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 18, 307-316.
41. Redeker, V., Melki, R., Prome, D., Le Caer, J. P. and Rossier, J. (1992). Structure of tubulin C-terminal domain obtained by subtilisin treatment. The major α- and β- tubulin isotypes from pig brain are polyglutamylated. FEBS Lett. 313, 185-192.
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 post-translational modification in axonemal microtubules. Science 266, 1688-1690.
43. Redeker, V., Rossier, J. and Frankfurter, A. (1998). Post-translational modifications of the C-terminus of α-tubulin in adult rat brain: alpha 4 is glutamylated at two residues. Biochemistry 37, 14838-14844.
44. Regnard, C., Audebert, S., Desbruyères, E., Denoulet, P. and Eddé, B. (1998). Tubulin polyglutamylase: partial purification and enzymatic properties. Biochemistry 37, 8395-8404.
45. Rüdiger, M., Plessman, U., Klöppel, K. D., Wehland, J. and Weber, K. (1992). Class II tubulin, the major brain β-tubulin isotype is polyglutamylated on glutamic acid residue 435. FEBS Lett. 308, 101-105.
46. Rüdiger, M., Plessman, U., Rüdiger, A. H. and Weber, K. (1995). β-tubulin of bull sperm is polyglycylated. FEBS Lett. 364, 147-151.
47. Schneider, A., Plessman, U. and Weber, K. (1997). Subpellicular and flagellar microtubules of Tryptmasoma brucei are extensively glutamylated. J. Cell Sci. 110, 431-437.
48. Schneider, A., Plessman, U., Felleisen, R. and Weber, K. (1998). Post-translational modifications of trichomonad tubulins; identification of multiple glutamylation sites. FEBS Lett. 429, 399-402.
49. Sullivan, K. F. (1988). Structure and utilization of tubulin isotypes. Ann. Rev. Cell Biol. 4, 687-716.
50. Tournier, F., Laoukili, J., Giuliani, I., Gendron, M. C., Guennou, C. and Marano, F. (1998). Ciliated differentiation of rabbit tracheal epithelial cells in vitro. Eur. J. Cell Biol. 77, 205-213.
51. Towbin, H., Stahelin, T. and 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.
52. Weber, K., Schneider, A., Müller, N. and Plessman, U. (1996). Polyglycylation of tubulin in the diplomonad Giardia lamblia, one of the oldest eukaryotes. FEBS Lett. 393, 27-30.
53. Webster, D. R. and Borisy, G. G. (1989). Microtubules are acetylated in domains that turn over slowly. J. Cell Sci. 92, 57-65.
54. Wehland, J. and Weber, K. (1987). Turnover of the carboxy-terminal tyrosine of α-tubulin and means of reaching elevated levels of dctyrosination in living cells. J. Cell Sci. 88, 185-203.
55. Wolff, A., De Néchaud, B., Chillet, D., Mazarguil, H., Desbruyères, E., Audebert, S., Eddé, B., Gros, F. and Denoulet, P. (1992). Distribution of glutamylated α- and β-tubulin in mouse tissue using a specific monoclonal antibody, GT335. Eur. J. Cell Biol. 59, 425-432.