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Review

Ciliate pheromone structures and activity: a review

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Pages 3-14 | Received 18 Jun 2014, Accepted 01 Oct 2014, Published online: 03 Nov 2014

References

  • Afon’kin SY, Yudin AL. 1987. Distribution of Dileptus anser (Ciliata, Holotricha, Gymnostomatida) of various genotypes for mat locus in the concentration gradient of their gamones. Acta Protozoologica 26:91–100.
  • Agamaliev FG. 1966. New species of the psammobiotic ciliates of the Western cost of the Caspian Sea. Acta Protozoologica 4:169–183.
  • Akada R. 1985. Mating types and mating-inducing factors (gamones) in the ciliate Euplotes patella syngen 2. Genetical Research 46:125–132. doi:10.1017/S0016672300022618.
  • Akada R. 1986. Partial characterization of the mating‐inducing factors (gamones) produced by mating type VI cells in the ciliate Euplotes patella syngen 2. Journal of Experimental Zoology 237:287–290. doi:10.1002/jez.1402370215.
  • Alimenti C, Ortenzi C, Carratore V, Luporini P. 2002. Structural characterization of a protein pheromone from a cold-adapted (Antarctic) single-cell eukaryote, the ciliate Euplotes nobilii. FEBS Letters 514:329–332. doi:10.1016/S0014-5793(02)02393-1.
  • Alimenti C, Ortenzi C, Carratore V, Luporini P. 2003. Structural characterization of En-1, a cold-adapted protein pheromone isolated from the Antarctic ciliate Euplotes nobilii. Biochimica et Biophysica Acta (BBA) - General Subjects 1621:17–21. doi:10.1016/S0304-4165(03)00011-4.
  • Alimenti C, Vallesi A, Federici S, Di Giuseppe G, Fernando D, Carratore V, Luporini P. 2011. 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 58:234–241. doi:10.1111/j.1550-7408.2011.00535.x.
  • 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. doi:10.1002/iub.228.
  • Aury J-M, Jaillon O, Duret L, Noel B, Jubin C et al. 2006. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444:171–178.
  • Brown LR, Mronga S, Bradshaw RA, Ortenzi C, Luporini P, Wüthrich K. 1993. Nuclear magnetic resonance solution structure of the pheromone Er-10 from the ciliated protozoan Euplotes raikovi. Journal of Molecular Biology 231:800–816. doi:10.1006/jmbi.1993.1327.
  • Brünen-Nieweier C, Christoph Weiligmann J, Hansen B, Kuhlmann H-W, Möllenbeck M, Heckmann K. 1998. The pheromones and pheromone genes of new stocks of the Euplotes octocarinatus species complex. European Journal of Protistology 34:124–132. doi:10.1016/S0932-4739(98)80022-9.
  • Cazzolli G, Škrbić T, Guella G, Faccioli P. 2013. Unfolding thermodynamics of cysteine-rich proteins and molecular thermal-adaptation of marine ciliates. Biomolecules 3:967–985. doi:10.3390/biom3040967.
  • Cervantes MD, Hamilton EP, Xiong J, Lawson MJ, Yuan D et al. 2013. Selecting one of several mating types through gene segment joining and deletion in Tetrahymena thermophila. PLoS Biology 11:e1001518.
  • Cervia D, Catalani E, Belardinelli MC, Perrotta C, Picchietti S, Alimenti C, Casini G, Fausto AM, Vallesi A. 2013. The protein pheromone Er-1 of the ciliate Euplotes raikovi stimulates human T-cell activity: Involvement of interleukin-2 system. Experimental Cell Research 319:56–67. doi:10.1016/j.yexcr.2012.10.007.
  • Cheek S, Krishna SS, Grishin NV. 2006. Structural classification of small, disulfide-rich protein domains. Journal of Molecular Biology 359:215–237. doi:10.1016/j.jmb.2006.03.017.
  • Di Giuseppe G, Barbieri M, Vallesi A, Luporini P, Dini F. 2013. Phylogeographical pattern of Euplotes nobilii, a protist ciliate with a bipolar biogeographical distribution. Molecular Ecology 22:4029–4037. doi:10.1111/mec.12363.
  • Di Giuseppe G, Erra F, Dini F, Alimenti C, Vallesi A, Pedrini B, Wuthrich K, Luporini P. 2011. Antarctic and Arctic populations of the ciliate Euplotes nobilii show common pheromone-mediated cell-cell signaling and cross-mating. Proceedings of the National Academy of Sciences USA 108:3181–3186. doi:10.1073/pnas.1019432108.
  • Dieckhoff HS, Freiburg M, Heckmann K. 1987. The isolation of gamones 3 and 4 of Euplotes octocarinatus. European Journal of Biochemistry 168:89–94. doi:10.1111/j.1432-1033.1987.tb13391.x.
  • Dini F, Nyberg D. 1993. Sex in ciliates. In: Jones JG, editor. Advances in microbial ecology. New York: Plenum Press. pp. 85–153. doi:10.1007/978-1-4615-2858-6_3.
  • Downs LE. 1956. The breeding system in Stylonychia putrina. Proceedings of the Society for Experimental Biology and Medicine 93:586–587. doi:10.3181/00379727-93-22829.
  • Eisen JA, Coyne RS, Wu M, Wu D, Thiagarajan M et al. 2006. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biology 4:1620–1642.
  • Elliott AM, Nanney DL. 1952. Conjugation in Tetrahymena. Science 116:33–34. doi:10.1126/science.116.3002.33.
  • Entzeroth M, Jaenicke L. 1981. Synthese von Blepharismon, dem wiedermolekularen konjugationshormon von Blepharisma japonicum. Zeitschrift für Naturforschung 36c:180–182.
  • Esposito F, Ricci N, Nobili R. 1976. Mating-type-specific soluble factors (gamones) in cell interaction of conjugation in the ciliate Oxytricha bifaria. Journal of Experimental Zoology 197:275–281. doi:10.1002/jez.1401970208.
  • Felici A, Alimenti C, Ortenzi C, Luporini P. 1999. Purification and initial characterization of two pheromones from the marine Antarctic ciliate, Euplotes nobilii. Italian Journal of Zoology 66:355–360. doi:10.1080/11250009909356277.
  • Geralt M, Alimenti C, Vallesi A, Luporini P, Wüthrich K. 2013. Thermodynamic stability of psychrophilic and mesophilic pheromones of the protozoan ciliate Euplotes. Biology 2:142–150. doi:10.3390/biology2010142.
  • Giuseppe G, Miceli C, Zahn R, Damberger F, Wuthrich K, Luporini P. 2002. A structurally deviant member of the Euplotes raikovi pheromone family: Er-23. The Journal of Eukaryotic Microbiology 49:86–92. doi:10.1111/j.1550-7408.2002.tb00347.x.
  • Hartmann M, Schartau O. 1939. Untersuchungen über die Befruchtungsstoffe der Seeigel. I. Biologischen Zentralblatt 59:571–587.
  • Isquith IR, Hirshfield HI. 1968. Non-Mendelian inheritance in Blepharisma intermedium. The Journal of Protozoology 15:513–516. doi:10.1111/j.1550-7408.1968.tb02165.x.
  • Jahn CL, Klobutcher LA. 2002. Genome remodeling in ciliated protozoa. Annual Review of Microbiology 56:489–520. doi:10.1146/annurev.micro.56.012302.160916.
  • Jiang J, Zhang Q, Warren A, Al-Rasheid KAS, Song W. 2010. Morphology and SSU rRNA gene-based phylogeny of two marine Euplotes species, E. orientalis spec. nov. and E. raikovi Agamaliev, 1966 (Ciliophora, Euplotida). European Journal of Protistology 46:121–132. doi:10.1016/j.ejop.2009.11.003.
  • Karlson P, Lüscher M. 1959. ‘Pheromones’: A new term for a class of biologically active substances. Nature 183:55–56. doi:10.1038/183055a0.
  • Kimball RF. 1942. The nature and inheritance of mating types in Euplotes patella. Genetics 27:269–285.
  • Kosaka T. 1990. Methods for inducing selfing, selfing and its role in the life cycle of Euplotes woodruffi syngen 3 (Ciliophora). Journal of Eukaryotic Microbiology 37:33–39.
  • Kubota T, Tokoroyama T, Tsukuda Y, Koyama H, Miyake A. 1973. Isolation and structure determination of blepharismin, a conjugation initiating gamone in the ciliate Blepharisma. Science 179:400–402. doi:10.1126/science.179.4071.400.
  • Kuhlmann H-W, Brünen-Nieweler C, Heckmann K. 1997. Pheromones of the ciliate Euplotes octocarinatus not only induce conjugation but also function as chemoattractants. The Journal of Experimental Zoology 277:38–48. doi:10.1002/(SICI)1097-010X(19970101)277:1<38::AID-JEZ4>3.0.CO;2-C.
  • Kuhlmann H-W, Sato K. 1993. Interspecific mating reactions between Euplotes octocarinatus and Euplotes patella syngen 2. European Journal of Protistology 29:24–31. doi:10.1016/S0932-4739(11)80293-2.
  • Liu A, Luginbühl P, Zerbe O, Ortenzi C, Luporini P, Wüthrich K. 2001. NMR structure of the pheromone Er-22 from Euplotes raikovi. Journal of Biomolecular NMR 19:75–78. doi:10.1023/A:1008332922256.
  • Luginbühl P, Ottiger M, Mronga S, Wüthrich K. 1994. Structure comparison of the pheromones Er-1, Er-10, and Er-2 from Euplotes raikovi. Protein Science 3:1537–1546. doi:10.1002/pro.5560030919.
  • Luporini P, Alimenti C, Ortenzi C, Luporini P. 2005. Ciliate mating types and their specific protein pheromones. Acta Protozoologica 44:89–101.
  • Luporini P, Miceli C. 1986. Mating pheromones. In: Gall JG, editor. The molecular biology of ciliated protozoa. New York: Academic Press. pp. 263–299.
  • Luporini P, Miceli C, Ortenzi C. 1983. Evidence that the ciliate Euplotes raikovi releases mating inducing factors (gamones). Journal of Experimental Zoology 226:1–9. doi:10.1002/jez.1402260102.
  • Luporini P, Raffioni S, Concetti A, Miceli C. 1986. The ciliate Euplotes raikovi heterozygous at the mat genetic locus coreleases two individual species of mating pheromone: Genetic and biochemical evidence. Proceedings of the National Academy of Sciences USA 83:2889–2893. doi:10.1073/pnas.83.9.2889.
  • Miceli C, Concetti A, Luporini P. 1983. Isolation of the mating-inducing factor of the ciliate Euplotes. Experimental Cell Research 149:593–598. doi:10.1016/0014-4827(83)90371-3.
  • Miceli C, La Terza A, Bradshaw RA, Luporini P. 1991. Structural characterization of mating pheromone precursors of the ciliate protozoan Euplotes raikovi. High conservation of pre and pro regions versus high variability of secreted regions. European Journal of Biochemistry 202:759–764. doi:10.1111/j.1432-1033.1991.tb16430.x.
  • Miceli C, La Terza A, Bradshaw RA, 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. Proceedings of the National Academy of Sciences USA 89:1988–1992. doi:10.1073/pnas.89.5.1988.
  • Miceli C, Luporini P, Bracchi P. 1981. Morphological description, breeding system, and nuclear changes during conjugation of Euplotes raikovi Agamaliev from Mediterranean Sea. Acta Protozoologica 20:215–224.
  • Miyake A. 1974. Cell interaction in conjugation of ciliates. Current Topics in Microbiology and Immunology. 64:49–77.
  • Miyake A. 1981. Physiology and biochemistry of conjugation in ciliates. In: Levandowsky M, Hutner SH, editors. Biochemistry and physiology of protozoa. 2nd ed. New York: Academic Press. pp. 125–198.
  • Miyake A, Beyer J. 1973. Cell interaction by means of soluble factors (gamones) in conjugation of Blepharisma intermedium. Experimental Cell Research 76:15–24. doi:10.1016/0014-4827(73)90413-8.
  • Miyake A, Beyer J. 1974. Blepharmone: A conjugation-inducing glycoprotein in the ciliate Blepharisma. Science 185:621–623. doi:10.1126/science.185.4151.621.
  • Miyake A, Bleyman L K. 1976. Gamones and mating types in the genus Blepharisma and their possible taxonomic application. Genetical Research 27:267–275. doi:10.1017/S0016672300016451.
  • Möllenbeck M, Heckmann K. 1999. Characterization of two genes encoding a fifth so far unknown pheromone of Euplotes octocarinatus. European Journal of Protistology 35:225–230. doi:10.1016/S0932-4739(99)80041-8.
  • Mronga S, Luginbühl P, Brown LR, Ortenzi C, Luporini P, Bradshaw RA, Wüthrich K. 1994. The NMR solution structure of the pheromone Er-1 from the ciliated protozoan Euplotes raikovi-NMR structure of the pheromone Er-1. Protein Science 3:1527–1536. doi:10.1002/pro.5560030918.
  • Nobili R, Luporini P, Dini F. 1978. Breeding system, species relationships and evolutionary trends in some marine species of Euplotidae (Ciliata Hypotrichida). In: Battaglia B, Beardmore J, editors. Marine Organisms: Genetics, Ecology and Evolution. New York: Plenum Press. pp. 591–616.
  • Ortenzi C, Alimenti C, Vallesi A, Di Pretoro B, La Terza A, Luporini P. 2000. The autocrine mitogenic loop of the ciliate Euplotes raikovi: The pheromone membrane-bound forms are the cell binding sites and potential signaling receptors of soluble pheromones. Molecular Biology of the Cell 11:1445–1455. doi:10.1091/mbc.11.4.1445.
  • Ortenzi C, Luporini P. 1995. Competition among homologous polypeptide pheromones of the ciliate Euplotes raikovi for binding to each other’s cell receptors. The Journal of Eukaryotic Microbiology 42:242–248. doi:10.1111/j.1550-7408.1995.tb01573.x.
  • Ottiger M, Szyperski T, Luginbühl P, Ortenzi C, Luporini P, Bradshaw RA, Wüthrich K. 1994. The NMR solution structure of the pheromone Er-2 from the ciliated protozoan Euplotes raikovi. Protein Science 3:1515–1526. doi:10.1002/pro.5560030917.
  • Pedrini B, Placzek WJ, Koculi E, Alimenti C, La Terza A, Luporini P, Wüthrich K. 2007. Cold-adaptation in sea-water-borne signal proteins: Sequence and NMR structure of the pheromone En-6 from the Antarctic ciliate Euplotes nobilii. Journal of Molecular Biology 372:277–286. doi:10.1016/j.jmb.2007.06.046.
  • Phadke SS, Zufall RA. 2009. Rapid diversification of mating systems in ciliates. Biological Journal of the Linnean Society 98:187–197. doi:10.1111/j.1095-8312.2009.01250.x.
  • Placzek WJ, Etezady-Esfarjani T, Herrmann T, Pedrini B, Peti W, Alimenti C, Luporini P, Wüthrich K. 2007. Cold-adapted signal proteins: NMR structures of pheromones from the Antarctic ciliate Euplotes nobilii. IUBMB Life 59:578–585. doi:10.1080/15216540701258165.
  • Raffioni S, Luporini P, Chait BT, Disper SS, Bradshaw RA. 1988. Primary structure of the mating pheromone Er-1 of the ciliate Euplotes raikovi. Journal of Biological Chemistry 263:18152–18159.
  • Raffioni S, Miceli C, Vallesi A, Chowdhury SK, Chait BT, Luporini P, Bradshaw RA. 1992. Primary structure of Euplotes raikovi pheromones: Comparison of five sequences of pheromones from cells with variable mating interactions. Proceedings of the National Academy of Sciences USA 89:2071–2075. doi:10.1073/pnas.89.6.2071.
  • Sato K. 1983. Induction of selfing by cell-free fluid from crosses in Euplotes patella syngen 2. Japanise Journal of Protozoology 16:20–21.
  • Singh DP, Saudemont B, Guglielmi G, Arnaiz O, Goût J-F, Prajer M, Potekhin A, Przybòs E, Aubusson-Fleury A, Bhullar S, Bouhouche K, Lhuillier-Akakpo M, Tanty V, Blugeon C, Alberti A, Labadie K, Aury J-M, Sperling L, Duharcourt S, Meyer E. 2014. Genome-defence small RNAs exapted for epigenetic mating-type inheritance. Nature 509:447–452. doi:10.1038/nature13318.
  • Sonneborn TM. 1978. Genetics of cell-cell interactions in ciliates. In: Lerner RA, Bergsma D, editors. The molecular basis of cell-cell interaction. New York: Alan R Riss. pp. 417–427.
  • Sugiura M, Harumoto T. 2001. Identification, characterization, and complete amino acid sequence of the conjugation-inducing glycoprotein (blepharmone) in the ciliate Blepharisma japonicum. Proceedings of the National Academy of Sciences USA 98:14446–14451. doi:10.1073/pnas.221457698.
  • Sugiura M, Shiotani H, Suzaki T, Harumoto T. 2010. Behavioural changes induced by the conjugation-inducing pheromones, gamone 1 and 2, in the ciliate Blepharisma japonicum. European Journal of Protistology 46:143–149. doi:10.1016/j.ejop.2010.01.002.
  • Tavrovskaja MV. 1979. Intraspecific intercellular interactions in the ciliate Dileptus anser. Journal of Protozoology 26:35A–36A.
  • Valbonesi A, Ortenzi C, Luporini P. 1992. The species problem in a ciliate with a high-multiple mating type system, Euplotes crassus. The Journal of Protozoology 39:45–54. doi:10.1111/j.1550-7408.1992.tb01282.x.
  • Vallesi A, Alimenti C, Di Giuseppe G, Dini F, Pedrini B, Wüthrich K, Luporini P. 2010b. The water-born protein pheromones of the polar protozoan ciliate, Euplotes nobilii: Coding genes and molecular structures. Polar Science 4:237–244. doi:10.1016/j.polar.2010.03.007.
  • Vallesi A, Alimenti C, Federici S, Di Giuseppe G, Dini F, Guella G, Luporini P. 2014. Evidence for gene duplication and allelic codominance (not hierarchical dominance) at the mating type locus of the ciliate, Euplotes crassus. Journal of Eukaryotic Microbiology 61: doi:10.1111/jeu.12140.
  • 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. Marine Genomics 2:27–32. doi:10.1016/j.margen.2009.04.001.
  • Vallesi A, Alimenti C, Pedrini B, Di Giuseppe G, Dini F, Wüthrich K, Luporini P. 2012. Coding genes and molecular structures of the diffusible signalling proteins (pheromones) of the polar ciliate, Euplotes nobilii. Marine Genomics 8:9–13. doi:10.1016/j.margen.2012.03.004.
  • Vallesi A, Ballarini P, Di Pretoro B, Alimenti C, Miceli C, Luporini P. 2005. The autocrine, mitogenic pheromone-receptor loop of the ciliate Euplotes raikovi: Pheromone-induced receptor internalization. Eukaryotic Cell 4:1221–1227. doi:10.1128/EC.4.7.1221-1227.2005.
  • Vallesi A, Di Pretoro B, Ballarini P, Apone F, Luporini P. 2010a. A novel protein kinase from the ciliate Euplotes raikovi with close structural identity to the mammalian intestinal and male-germ cell kinases: Characterization and functional implications in the autocrine pheromone signaling loop. Protist 161:250–263. doi:10.1016/j.protis.2009.12.002.
  • Vallesi A, Giuli G, Bradshaw RA, Luporini P. 1995. Autocrine mitogenic activity of pheromones produced by the protozoan ciliate Euplotes raikovi. Nature 376:522–524. doi:10.1038/376522a0.
  • Vallesi A, Giuli G, Ghiara P, Scapigliati G, Luporini P. 1998. Structure-function relationships of pheromones of the ciliate Euplotes raikovi with mammalian growth factors: Cross-reactivity between Er-1 and interleukin-2 systems. Experimental Cell Research 241:253–259. doi:10.1006/excr.1998.4056.
  • Weischer A, Freiburg M, Heckmann K. 1985. Isolation and partial characterization of gamone 1 of Euplotes octocarinatus. FEBS Letters 191:176–180. doi:10.1016/0014-5793(85)80003-X.
  • Weise L. 1961. Gamone. Fortschritte der Zoologie 13:119–145.
  • Weiss MS, Anderson DH, Raffioni S, Bradshaw RA, Ortenzi C, Luporini P, Eisenberg D. 1995. A cooperative model for receptor recognition and cell adhesion: Evidence from the molecular packing in the 1.6-Å crystal structure of the pheromone Er-1 from the ciliated protozoan Euplotes raikovi. Proceedings of the National Academy of Sciences USA 92:10172–10176. doi:10.1073/pnas.92.22.10172.
  • Yi Z, Kartz LA, Song W. 2012. Assessing whether alpha-tubulin sequences are suitable for phylogenetic reconstruction of Ciliophora with insights into its evolution in euplotids. PLoS ONE 7: e40635. doi:10.1371/journal.pone.0040635.
  • Yudin AL, Afon’kin SY, Parfenova EU. 1990. Mating pheromones in the ciliate Dileptus anser. Tsitologyia 32:107–116. (In Russian with English summary).
  • Zahn R, Damberger F, Ortenzi C, Luporini P, Wüthrich K. 2001. NMR structure of the Euplotes raikovi pheromone Er-23 and identification of its five disulfide bonds. Journal of Molecular Biology 313:923–931. doi:10.1006/jmbi.2001.5099.

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