Isolation and structural characterization of two water-borne pheromones from Euplotes crassus, a ciliate commonly known to carry membrane-bound pheromones

Journal of Eukaryotic Microbiology

Volumn 58, Issue 3, 2011, Pages 234-241

  Alimenti, Claudio ^a   Vallesi, Adriana ^a   Federici, Sergio ^b   Di Giuseppe, Graziano ^b   Fernando, Dini ^b   Carratore, Vitale ^c   Luporini, Pierangelo ^a  

^a UNIVERSITY OF CAMERINO   (Italy)

^b UNIVERSITY OF PISA   (Italy)

^c INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

Author keywords

Chemical cell signaling; Ciliate mating types; Macronuclear gene structure; Protein structure; Water borne pheromones

Indexed keywords

PHEROMONE; WATER;

ALLELE; AMINO ACID; CELL ORGANELLE; CILIATE; ENVIRONMENTAL FACTOR; FILTRATION; GENE EXPRESSION; GENETIC ANALYSIS; GENOME; MATING BEHAVIOR; MEMBRANE; MOLECULAR ANALYSIS; PHEROMONE;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; DNA SEQUENCE; EUPLOTES; FILTRATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; MOLECULAR WEIGHT; NUCLEOTIDE SEQUENCE; PARASITOLOGY; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; BASE SEQUENCE; EUPLOTES; FILTRATION; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PHEROMONES; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, PROTEIN; WATER;

CILIOPHORA; EUPLOTES; MONEUPLOTES CRASSUS;

EID: 79959839907     PISSN: 10665234     EISSN: 15507408     Source Type: Journal    
DOI: 10.1111/j.1550-7408.2011.00535.x     Document Type: Article

References (50)

1. Alimenti, C., Vallesi, A., Pedrini, B., Wüthrich, K. & Luporini, P. 2009. Molecular cold-adaptation: comparative analysis of two homologous families of psychrophilic and mesophilic signal proteins of the protozoan ciliate, Euplotes. IUBMB Life, 61:838-845.
2. Balhorn, R. 2007. The protamine family of sperm nuclear proteins. Genome Biol., 8:227.
3. Bendtsen, J. D., Nielsen, H., von Heijne, G. & Brunak, S. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol., 340:783-795.
4. Borror, A. C. & Hill, B. F. 1995. The order Euplotida (Ciliophora): taxonomy, with division of Euplotes into several genera. J. Eukaryot. Microbiol., 42:457-466, doi: 10.1186/gb-2007-8-9-227.
5. Brünen-Nieweler, C., Weiligmann, J. C., Hansen, B., Kuhlmann, H. W., Möllenbeck, M. & Heckmann, K. 1998. The pheromones and pheromone genes of new stocks of E. octocarinatus species complex. Eur. J. Protistol., 34:124-132.
6. Choo, K. H. & Ranganathan, S. 2008. Flanking signal and mature peptide residues influence signal peptide cleavage. BMC Bioinformat., 9(Suppl. 12):S15, doi: 10.1186/1471-2105-9-S12-S15.
7. Di Giuseppe, G., Miceli, C., Zahn, R., Dambeger, F., Wüthrich, K. & Luporini, P. 2002. A structurally deviant member of the Euplotes raikovi pheromone family: Er-23. J. Eukaryot. Microbiol., 49:86-92.
8. Dini, F. & Luporini, P. 1985. Mating-type polimorphic variation in Euplotes minuta (Ciliophora: Hypotrichida). J. Protozool., 32:111-117.
9. Dini, F. & Miyake, A. 1982. Preconjugant cell interaction in Euplotes crassus: an analysis by temporary cycloheximide treatments. J. Exp. Zool., 220:153-162.
10. Dini, F. & Nyberg, D. 1993. Sex in ciliates. In: Jones, J. G. (ed.), Advances in Microbial Ecology. Vol. 13. Plenum Press, New York. p. 85-153.
11. Eisenberg, D., Schwarz, E., Komarony, M. & Wall, R. 1984. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J. Mol. Biol., 179:125-142.
12. Felici, A., Alimenti, C., Ortenzi, C. & Luporini, P. 1999. Purification and initial characterization of two pheromones from the marine Antarctic ciliate, Euplotes nobilii, Ital. J. Zool., 66:355-360.
13. Heckmann, K. 1964. Experimentelle Untersuchungen an Euplotes crassus I. Paarungssystem, Konjugation und Determination der Paarungstypen. Z. VererbLehre, 95:114-124.
14. Heckmann, K. & Kuhlmann, H.-W. 1986. Mating types and mating inducing substances in Euplotes octocarinatus. J. Exp. Zool., 237:87-96.
15. Heckmann, K. & Siegel, R. W. 1964. Evidence for the induction of mating type substances by cell to cell contacts. Exp. Cell Res., 36:688-691.
16. Kimball, R. F. 1942. The nature and inheritance of mating types in Euplotes patella. Genetics, 27:269-285.
17. Kimball, R. F. 1943. Mating types in ciliate protozoa. Q. Rev. Biol., 18:30-45.
18. Kosaka, T. 1990. Methods for inducing selfing, selfing and its role in the life cycle of Euplotes woodruffi syngen 3 (Ciliophora). J. Protozool., 37:33-39.
19. Kuhlmann, H. W. & Sato, K. 1993. Interspecific mating reactions between Euplotes octocarinatus and Euplotes patella syngen 2. Eur. J. Protistol., 29:24-31.
20. La Terza, A., Dobri, N., Alimenti, C., Vallesi, A. & Luporini, P. 2009. The water-borne protein signals (pheromones) of the Antarctic ciliated protozoan Euplotes nobilii: structure of the gene coding for the En-6 pheromone. Can. J. Microbiol., 55:57-62.
21. Lueken, W. & Oelgemöller, B. 1986. Graded morphogenetic response to preparing cell-cell interactions in Euplotes vannus. Acta Protozool., 25:187-193.
22. Lueken, W., Gaertner, M. & Breer, H. 1983. Mating-type specific loss of conjugation competence by irritation in Euplotes vannus. J. Exp. Zool., 226:11-17.
23. Luporini, P., Miceli, C. & Ortenzi, C. 1983. Evidence that the ciliate Euplotes raikovi releases mating inducing factors (gamones). J. Exp. Zool., 226:1-9.
24. Luporini, P., Alimenti, C., Ortenzi, C. & Vallesi, A. 2005. Ciliate mating types and their specific protein pheromones. Acta Protozool., 44:89-101. (Pubitemid 40595552)
25. Luporini, P., Raffioni, S., Concetti, A. & Miceli, C. 1986. The ciliate Euplotes raikovi heterozygous at the mat genetic locus co-releases two individual species of mating pheromones: genetic and biochemical evidence. Proc. Natl. Acad. Sci. USA, 83:2889-2893.
26. Meyer, F., Schmidt, H. J., Plumber, E., Hasilik, A., Mersmann, G., Meyer, H., Engstrom, A. & Heckmann, K. 1991. UGA is translated as cysteine in pheromone 3 of Euplotes octocarinatus. Proc. Natl. Acad. Sci. USA, 88:3758-3761.
27. Miceli, C., Luporini, P. & Bracchi, P. 1981. Morphological description, breeding system, and nuclear changes during conjugation of Euplotes raikovi Agamaliev from Mediterranean Sea. Acta Protozool., 20:215-224.
28. Miceli, C., La Terza, A., Bradshaw, R. A. & Luporini, P. 1991. Structural characterization of mating pheromone precursors of the ciliate protozoan Euplotes raikovi. Eur. J. Biochem., 202:759-764.
29. Miceli, C., La Terza, A., Bradshaw, R. A. & Luporini, P. 1992. Identification and structural characterization of a cDNA clone encoding a membrane-bound form of the polypeptide pheromone Er-1 in the ciliate protozoan Euplotes raikovi. Proc. Natl. Acad. Sci. USA, 89:1988-1992.
30. Miyake, A. 1968. Induction of conjugation union by cell-free fluid in the ciliate Blepharisma. Proc. Jpn. Acad., 44:837-841.
31. Miyake, A. 1981. Physiology and biochemistry of conjugation in ciliates. In: Levandovsky, M. & Hunter, S. H. (ed.), Biochemistry and Physiology of Protozoa. 2nd ed. Academic Press, New York. p. 125-198.
32. Miyake, A. 1996. Fertilization and sexuality in ciliates. In: Hausmann, K. & Bradbury, P. C. (ed.), Ciliates, Cells as Organisms. Gustav Fischer, Stuttgart. p. 243-290.
33. Miyake, A. & Nobili, R. 1974. Mating reaction and its daily rhythm in Euplotes crassus. J. Protozool., 21:584-587.
34. Möllenbeck, M. & Heckmann, K. 1999. Characterization of two genes encoding a fifth so far unknown pheromone of Euplotes octocarinatus. Eur. J. Protistol., 35:225-230.
35. Nanney, D. L. 1980. Experimental Ciliatology. John Wiley & Sons, New Jersey.
36. Nobili, R. 1964. On conjugation between Euplotes vannus O. F. Müller and Euplotes minuta Yocom. Caryologia, 17:393-397.
37. Nobili, R., Luporini, P. & Dini, F. 1978. Breeding systems, species relationships and evolutionary trends in some marine species of Euplotidae (Hypotrichida, Ciliata). In: Battaglia, B. & Beardmore, J. (ed.), Nato Conference Series. Marine Organisms. Genetics, Ecology and Evolution. Plenum Press, New York. p. 591-616.
38. Ognibene, M., Della Giovampaola, C., Trielli, F., Focarelli, R., Rosati, F. & Delmonte Corrado, M. U. 2007. Identification and characterization of a 38 kDa glycoprotein functionally associated with mating activity in Paramecium primaurelia. Eur. J. Protistol., 44:81-90.
39. Raffioni, S., Miceli, C., Concetti, A., Barra, D. & Luporini, P. 1987. Purification and characterization of new mating pheromones of the ciliate Euplotes raikovi. Exp. Cell Res., 172:417-424.
40. Schulze-Dieckhoff, H., Freiburg, M. & Heckmann, K. 1987. The isolation of gamones 3 and 4 of Euplotes octocarinatus. Eur. J. Biochem., 168:89-94.
41. Sonneborn, T. M. 1937. Sex, sex inheritance and sex determination in Paramecium aurelia. Proc. Natl. Acad. Sci. USA, 23:378-385.
42. Thompson, J. D., Higgins, D. G. & Gibson, T. J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22:4673-4680. (Pubitemid 24354800)
43. Turanov, A. A., Lobanov, A. V., Fomenko, D. E., Morrison, H. G., Sogin, M. L., Klobutcher, L. A., Hatfield, D. L. & Gladyshev, V. N. 2009. Genetic code supports targeted insertion of two amino acids by one codon. Science, 323:259-261.
44. Valbonesi, A., Ortenzi, C. & Luporini, P. 1992. The species problem in a ciliate with a high-multiple mating type system, Euplotes crassus. J. Protozool., 39:45-54.
45. Vallesi, A., Di Giuseppe, G., Dini, F. & Luporini, P. 2008. Pheromone evolution in the protozoan ciliate Euplotes: the ability to synthesize diffusible forms is ancestral and secondarily lost. Mol. Phylogenet. Evol., 47:439-442.
46. Vallesi, A., Giuli, G., Bradshaw, R. A. & Luporini, P. 1995. Autocrine mitogenic activity of pheromones produced by the protozoan ciliate Euplotes raikovi. Nature, 376:522-524.
47. Vallesi, A., Alimenti, C., La Terza, A., Di Giuseppe, G., Dini, F. & Luporini, P. 2009. Characterization of the pheromone gene family of an Antarctic and Arctic protozoan ciliate, Euplotes nobilii. Mar. Genomics, 2:27-32.
48. Verni, F. & Rosati, G. 1987. Adenylate cyclase and cyclic AMP in the ciliate Euplotes crassus: involvement in both cell cycle and sexual reproduction. J. Exp. Zool., 244:289-298.
49. Vinnikova, N. V. & Tavrovskaja, M. V. 1973. Some data on the conjugation of the ciliate Dileptus anser. In: Structure, Function and Reactivity of the Cell. Institute of Cytology, Academy of Science of the URSS, Leningrad. p. 43-46.
50. Walne, P. R. 1966. Experiments in the large-scale culture of larvae of Ostrea edulis L. Fish. Invest. London, Ser. 2, 25:1-10.