Cytoskeletal proteins with N-terminal signal peptides: Plateins in the ciliate Euplotes define a new family of articulins

Journal of Cell Science

Volumn 116, Issue 7, 2003, Pages 1291-1303

  Kloetzel, John A ^a   Baroin Tourancheau, Anne ^b   Miceli, Cristina ^c   Barchetta, Sabrina ^c   Farmar, James ^d   Banerjee, Deben ^d   Fleury Aubusson, Anne ^b  

^a UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UNIVERSITY OF CAMERINO   (Italy)

^d NEW YORK BLOOD CENTER   (United States)

Author keywords

Alveolata; Ciliate expression library; Cortical cytoskeleton; Epiplasm; Membrane skeleton; Pellicle; Protist; Repetitive protein domains; Signal sequence

Indexed keywords

ARTICULIN; CYTOSKELETON PROTEIN; PLATEIN; PROLINE; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; VALINE;

ACIDITY; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CILIATE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DINOFLAGELLATE; EUKARYOTE; EUPLOTES; FLAGELLATE; HYDROPHOBICITY; IMMUNOASSAY; IMMUNOFLUORESCENCE MICROSCOPY; MEMBRANE STRUCTURE; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN POLYMERIZATION; PROTEIN STRUCTURE; REVIEW; SOLUBILITY;

ANIMALS; CELL COMPARTMENTATION; CELL MEMBRANE; CELL SIZE; CYTOSKELETAL PROTEINS; CYTOSKELETON; DNA, COMPLEMENTARY; EUPLOTES; EVOLUTION, MOLECULAR; FLUORESCENT ANTIBODY TECHNIQUE; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID;

ALVEOLATA; CILIOPHORA; DINOPHYCEAE; EUKARYOTA; EUPLOTES; MASTIGOPHORA (FLAGELLATES); PROTISTA;

EID: 0037383724     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00333     Document Type: Review

References (68)

1. Adams, M. D., Celniker, S. E., Holt, R. A., Evans, C. A., Gocayne, J. D., Amanatides, P. G., Scherer, S. E., Li, P. W., Hoskins, R. A., Galle, R. F. et al. (2000). The genome sequence of Drosophila melanogaster. Science 287, 2185-2195.
2. Adoutte, A. and Fleury, A. (1996). Cytoskeleton of ciliates. In Ciliates: Cells as Organisms (ed. K. Hausmann and P. Bradbury), pp. 41-49. Stuttgart: Fischer Verlag.
3. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
4. Bennett, V. and Gilligan, D. M. (1993). The spectrin-based membrane structure and micron-scale organization of the plasma membrane. Ann. Rev. Cell Biol. 9, 27-66.
5. Blom, N., Gammeltoft, S. and Brunak, S. (1999). Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294, 1351-1362.
6. Böhm, P. and Hausmann, K. (1981). Cytochemical investigations of the alveolar plates of the Euplotidae (Ciliophora, Hypotrichida). Protoplasma 106, 309-316.
7. Bouchard, P., Chomilier, J., Ravet, V., Mornon, J.-P. and Viguès, B. (2001). 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. 114, 101-110.
8. Bouck, G. B. and Ngô, H. (1996). Cortical structure and function in euglenoids with reference to trypanosomes, ciliates, and dinoflagellates. Int. Rev. Cytol. 169, 267-318.
9. Bowman, S., Lawson, D., Basham, D., Brown, D., Chillingworth, T., Churcher, C. M., Craig, A., Davies, R. M., Devlin, K., Feltwell, T. et al. (1999). The complete nucleotide sequence of chromosome 3 of Plasmodium falciparum. Nature 400, 532-538.
10. Bricheux, G., Mahoney, D. and Gibbs, S. (1992). Development of the pellicle and thecal plates following ecdysis in the dinoflagellate Glenodinium foliaceum. Protoplasma 168, 159-171.
11. Brimmer, A. and Weber, K. (2000). The cDNA sequences of three tetrins, the structural proteins of the Tetrahymena oral filaments, show that they are novel cytoskeletal proteins. Protist 151, 171-180.
12. Casu, R., Eisemann, C., Pearson, R., Riding, G., East, I., Donaldson, A., Cadogan, L. and Tellam, R. (1997). Antibody-mediated inhibition of the growth of larvae from an insect causing cutaneous myiasis in a mammalian host. Proc. Natl. Acad. Sci. USA 94, 8938-8944.
13. Chapman, M. J., Dolan, M. F. and Margulis, L. (2000). Centrioles and kinetosomes: form, function and evolution. Q. Rev. Biol. 75, 409-429.
14. Chatton, E. and Seguela, J. (1940). La continuité génétique des formations ciliaires chez les Ciliés hypotriches. Le cinétome et l'argyrome an cours de la division. Bull. Biol. Fr. Belg. 74, 349-442.
15. Coffe, G., le Caer, J.-P., Lima, O. and Adoutte, A. (1996). Purification, in vitro reassembly, and preliminary sequence analysis of epiplasmins, the major constituent of the membrane skeleton of Paramecium. Cell Motil. Cytoskel. 34, 137-151.
16. Curtenaz, S., Nahon, P., Iftode, F. and Fleury, A. (1994). Interspecific immunological cross-reactions among cortical proteins of four ciliates. Eur. J. Protistol. 30, 440-450.
17. Di Giuseppe, G., Miceli, C., Zahn, R., Damberger, F., Wüthrich, K. and Luporini, P. (2002). A structurally deviant member of the Euplotes raikovi pheromone family: Er-23. J. Eukaryot. Microbiol. 49, 86-92.
18. Dubreuil, R. R., MacVicar, G. R. and Maddux, P. B. (1997). Functional studies of the membrane skeleton in Drosophila: identification of a positional cue that targets polarized membrane skeleton assembly. Soc. Gen. Physiol. Ser. 52, 91-106.
19. Drzymala, L., Castle, A., Cheung, J. C. and Bennick, A. (2000). Cellular phosphorylation of an acidic proline-rich protein, PRP1, a secreted salivary phosphoprotein. Biochemistry 39, 2023-2031.
20. Fernandez, J., Andrews, L. and Mische, S. (1994), Protease digest: protein on PVDF. In Techniques in Protein Chemistry, Vol. V (ed. J. W. Crabb), pp. 215-222. San Diego: Academic Press.
21. Fleury, A. (1991). Dynamics of the cytoskeleton during morphogenesis in the ciliate Euplotes. II. Cortex and continuous microtubular systems. Eur. J. Protistol. 27, 220-237.
22. Fleury, A. and Laurent, M. (1995). Microtubule dynamics and morphogenesis in Paramecium. I. Deployment and dynamic properties of a cortical network of acetylated microtubules in relation to the invariance of a morphogenetic field. Eur. J. Protistol. 31, 190-200.
23. Geyer, J. J. and Kloetzel, J. A. (1987). Cellular dynamics of conjugation in the ciliate Euplotes aediculatus. II. Cellular membranes. J. Morphol. 192, 43-61.
24. Grim, J. N. (1982). Subpellicular microtubules of Euplotes eurystomus: their geometry relative to cell form, surface contours, and ciliary organelles. J. Cell Sci. 56, 471-484.
25. Gumpel, N. and Smith, A. G. (1992). A novel calcium-binding protein from Euglena gracilis. Eur. J. Biochem. 210, 721-727.
26. Hanisch, F. G. (2001). O-glycosylation of the mucin type. Biol. Chem. 382, 143-149.
27. Hansen, J. E., Lund, O., Tolstrup, N., Gooley, A. A., Williams, K. L. and Brunak, S. (1998). NetOglyc: Prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility. Glycoconjugate J. 15, 115-130.
28. Harlow, E. and Lane, D. (1988). Antibodies: A Laboratory Manual. New York: Cold Spring Harbor Laboratory.
29. Hausmann, K. and Hülsmann, N. (1996). Protozoology, 2nd edn. New York: Thieme Medical Publishers.
30. Hausmann, K. and Kaiser, J. (1979). Arrangement and structure of plates in the cortical alveoli of the hypotrich ciliate Euplotes vannus. J. Ultrastruct. Res. 67, 15-22.
31. Hong, J. C., Nagao, R. T. and Key, J. L. (1987). Characterization and sequence analysis of a developmentally regulated putative cell wall protein gene isolated from soybean. J. Biol. Chem. 262, 8367-8376.
32. Honts, J. E. and Williams, N. E. (1990). Tetrins: polypeptides that form bundled filaments in Tetrahymena. J. Cell Sci. 96, 293-302.
33. Huttenlauch, I. (1985). SEM study of the skeletal plates of Coleps nolandi Kahl, 1930. Protistologica 21, 499-503.
34. Huttenlauch, I., Geisler, N., Plessmann, U., Peck, R. K., Weber, K. and Stick, R. (1995). Major epiplasmic proteins of ciliates are articulins: cloning, recombinant expression, and structural characterization. J. Cell Biol. 130, 1401-1412.
35. Huttenlauch, I., Peck, R. K., Plessmann, U., Weber, K. and Stick, R. (1998a). Characterisation of two articulins, the major epiplasmic proteins comprising the membrane skeleton of the ciliate Pseudomicrothorax. J. Cell Sci. 111, 1909-1919.
36. Huttenlauch, I., Peck, R. K. and Stick, R. (1998b). Articulins and epiplasmins: two distinct classes of cytoskeletal proteins of the membrane skeleton in protists. J. Cell Sci. 111, 3367-3378.
37. Jeanmaire-Wolf, R., Clérot, J. C., Nahon, P., Iftode, F., Fleury, A. and Adoutte, A. (1993). Isolation and characterization of monoclonal antibodies to cytoskeletal and membrane proteins of the Paramecium cortex. Eur. J. Protistol. 29, 311-333.
38. Kloetzel, J. A. (1991). Identification and properties of plateins, major proteins in the cortical alveolar plates of Euplotes. J. Protozool. 38, 392-401.
39. Kloetzel, J. A. (1993). Alleleic segregation of alveolar plate protein (platein) variants in Euplotes aediculatus. J. Eukaryot. Microbiol. 40, 43a.
40. Kloetzel, J. A., Hill, B. E. and Kosaka, T. (1992). Genetic variants of plateins (alveolar plate proteins) among and within species of Euplotes. J. Protozool. 39, 92-101.
41. Kordeli, E. (2000). The spectrin-based skeleton at the postsynaptic membrane of the neuromuscular junction. Microsc. Res. Tech. 49, 101-107.
42. Lynn, D. and Small, E. B. (2000). Phylum Ciliophora, Doflein, 1901. In Illustrated Guide to the Protozoa, 2nd edn (ed. J. J. Lee, G. Leedale and P. Bradbury), pp. 371-656. Lawrence, Kansas: Society of Protozoologists, Allen Press.
43. Mann, T. and Beckers, C. (2001). Characterization of the subpellicular network, a filamentous membrane skeletal component in the parasite Toxoplasma gondii. Mol. Biochem. Parasitol. 115, 257-268.
44. Marrs, J. A. and Bouck, G. B. (1992). The two major membrane skeletal proteins (articulins) of Euglena gracilis define a novel class of cytoskeletal proteins. J. Cell Biol. 118, 1465-1475.
45. Matsudaira, P. (1993). A Practical Guide to Protein and Peptide Purification for Microsequencing, 2nd edn. San Diego: Academic Press.
46. Muñoz, F. J., Dopico, B. and Labrador, E. (1998). A cDNA encoding a proline-rich protein from Cicer arietinum. Changes in expression during development and abiotic stresses. Physiol. Plantarum 102, 582-590.
47. Nahon, P., Coffe, G., le Guyader, H., Darmanaden-Delorme, J., Jeanmaire-Wolf, R., Clérot, J.-C. and Adoutte, A. (1993). Identification of the epiplasmins, a new set of cortical proteins of the membrane cytoskeleton in Paramecium. J. Cell Sci. 104, 975-990.
48. Nielsen, H., Engelbrecht, J., Brunak, S. and von Heijne, G. (1997). Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10, 1-6.
49. Nierman, W. C., Feldblyum, T. V., Laub, M. T., Paulsen, I. T., Nelson, K. E., Eisen, J. A., Heidelberg, J. F., Alley, M. R., Ohta, N., Maddock, J. R. et al. (2001). Complete genome sequence of Caulobacter crescentus. Proc. Natl. Acad. Sci. USA 98, 4136-4141.
50. Peck, R. K., Duborgel, F., Huttenlauch, I. and de Haller, G. (1991). The membrane skeleton of Pseudomicrothorax, I. Isolation, structure, and composition. J. Cell Sci. 100, 693-706.
51. Plattner, H. and Klauke, N. (2001). Calcium in ciliated protozoa: sources, regulation, and calcium-regulated cell functions. Int. Rev. Cytol. 201, 115-208.
52. Plattner, H., Habermann, A., Kissmehl, R., Klauke, N., Majoul, I. and Söling, H. D. (1997). Differential distribution of calcium stores in Paramecium cells. Occurrence of a subplasmalemmal store with a calsequestrin-like protein. Eur. J. Cell Biol. 72, 297-306.
53. Rost, B. (1996). PHD: predicting one-dimensional protein structure by profile-based neural networks. Meth. Enzymol. 266, 525-539.
54. Ruffolo, J. J., Jr (1976). Cortical morphogenesis during the cell division cycle in Euplotes: an integrated study using light optical, scanning electron and transmission electron microscopy. J. Morphol. 148, 489-528.
55. Salisbury, J. L., Baron, A., Surek, B. and Melkonian, M. (1984). Striated flagellar roots: isolation and partial characterization of a calcium-modulated contractile organelle. J. Cell Biol. 99, 962-970.
56. Sambrook, J. R., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd edn. New York: Cold Spring Harbor Laboratory, Cold Spring Harbor.
57. Sanders, M. A. and Salisbury, J. L. (1994). Centrin plays an essential role in microtubule severing during flagellar excision in C. reinhardtii. J. Cell Biol. 127, 795-805.
58. Schliwa, M. and van Blerkom, J. (1981). Structural interaction of cytoskeletal components. J. Cell Biol. 90, 222-235.
59. Sperling, L., Keryer, G., Ruiz, F. and Beisson, J. (1991). Cortical morphogenesis in Paramecium: a transcellular wave of protein phosphorylation involved in ciliary rootlet disassembly. Dev. Biol. 148, 205-218.
60. Stahl, H.-D., Crewther, P. E., Anders, R. F. and Kemp, D. J. (1987). Structure of the FIRA gene of Plasmodium falciparum. Mol. Biol. Med. 4, 199-211.
61. Stelly, N., Mauger, J.-P., Claret, M. and Adoutte, A. (1991). Cortical alveoli of Paramecium: a vast submembranous calcium storage compartment. J. Cell Biol. 113, 103-112.
62. Tchavtchitch, M., Fischer, K., Juestis, R. and Saul, A. (2001). The sequence of a 200 kb portion of a Plasmodium vivax chromosome reveals a high degree of conservation with Plasmodium falciparum chromosome 3. Mol. Biochem. Parasitol. 118, 211-222.
63. Viguès, B., Bricheux, G., Metivier, C., Brugerolle, G. and Peck, R. K. (1987). Evidence for common epitopes among proteins of the membrane skeleton of a ciliate, an euglenoid and a dinoflagellate. Eur. J. Protistol. 23, 101-110.
64. Williams, N. E. (1991). A comparison of alveolar plate proteins in two species of Euplotes. Eur. J. Protistol. 27, 21-25.
65. Williams, N. E. and Hunts, J. E. (1995). Isolation and fractionation of the Tetrahymena cytoskeleton and oral apparatus. Methods Cell Biol. 47, 301-306.
66. Williams, N. E., Honts, J. E., Lu, Q., Olson, C. and Moore, K. (1989). Identification and localization of major cortical proteins in the ciliated protozoan, Euplotes eurystomus. J. Cell Sci. 92, 433-439.
67. Williamson, M. P. (1994). The structure and function of proline-rich regions in proteins. Biochem. J. 297, 249-260.
68. Wise, B. N. (1965). The morphogenetic cycle in Euplotes eurystomus and its bearing on problems of ciliate morphogenesis. J. Protozool. 12, 626-648.