The protein pheromone Er-1 of the ciliate Euplotes raikovi stimulates human T-cell activity: Involvement of interleukin-2 system

Experimental Cell Research

Volumn 319, Issue 3, 2013, Pages 56-67

  Cervia, Davide ^a,b   Catalani, Elisabetta ^a   Belardinelli, Maria Cristina ^a   Perrotta, Cristiana ^b   Picchietti, Simona ^a   Alimenti, Claudio ^c   Casini, Giovanni ^a   Fausto, Anna Maria ^a   Vallesi, Adriana ^c  

^a UNIVERSITY OF TUSCIA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF CAMERINO   (Italy)

Author keywords

Cell growth; Ciliate pheromones; Cytokines; ERK1 2; IL 2 receptor; Jurkat cells

Indexed keywords

AMINO ACID; DNA; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 2 RECEPTOR BETA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHEROMONE; PROTEIN PHEROMONE ER 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DNA SYNTHESIS; DOWN REGULATION; ENDOCYTOSIS; EUPLOTES; EUPLOTES RAIKOVI; GLIOMA CELL; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE;

CILIOPHORA; EUKARYOTA; EUPLOTES; EUPLOTES RAIKOVI;

EID: 84872394634     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.10.007     Document Type: Article

References (58)

1. Luporini P., Alimenti C., Ortenzi C., Vallesi A. Ciliate mating and their specific protein pheromones. Acta Protozool. 2005, 44:89-101.
2. Luporini P., Vallesi A., Alimenti C., Ortenzi C. The cell type-specific signal proteins (pheromones) of protozoan ciliates. Curr. Pharm. Des. 2006, 12:3015-3024.
3. Luporini P., Vallesi A., Miceli C., Bradshaw R.A. Chemical signaling in ciliates. J. Eukaryot. Microbiol. 1995, 42:208-212.
4. Alimenti C., Vallesi A., Federici S., di Giuseppe G., Fernando D., Carratore V., Luporini P. Isolation and structural characterization of two water-borne pheromones from Euplotes crassus, a ciliate commonly known to carry membrane-bound pheromones. J. Eukaryot. Microbiol. 2011, 58:234-241.
5. Vallesi A., Alimenti C., La Terza A., Di Giuseppe G., Dini F., Luporini P. Characterization of the pheromone gene family of an Antarctic and Arctic protozoan ciliate, Euplotes nobilii. Mar. Genomics 2009, 2:27-32.
6. Ortenzi C., Alimenti C., Vallesi A., Di Pretoro B., Terza A.L., Luporini P. 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. Mol. Biol. Cell 2000, 11:1445-1455.
7. Luginbuhl P., Ottiger M., Mronga S., Wuthrich K. Structure comparison of the pheromones Er-1, Er-10, and Er-2 from Euplotes raikovi. Protein Sci. 1994, 3:1537-1546.
8. Mronga S., Luginbuhl P., Brown L.R., Ortenzi C., Luporini P., Bradshaw R.A., Wuthrich K. The NMR solution structure of the pheromone Er-1 from the ciliated protozoan Euplotes raikovi. Protein Sci. 1994, 3:1527-1536.
9. Ottiger M., Szyperski T., Luginbuhl P., Ortenzi C., Luporini P., Bradshaw R.A., Wuthrich K. The NMR solution structure of the pheromone Er-2 from the ciliated protozoan Euplotes raikovi. Protein Sci. 1994, 3:1515-1526.
10. Alimenti C., Vallesi A., Pedrini B., Wuthrich K., Luporini P. Molecular cold-adaptation: comparative analysis of two homologous families of psychrophilic and mesophilic signal proteins of the protozoan ciliate, Euplotes. IUBMB Life 2009, 61:838-845.
11. Ortenzi C., Luporini P. Competition among homologous polypeptide pheromones of the ciliate Euplotes raikovi for binding to each other's cell receptors. J. Euk. Microbiol. 1995, 42:242-248.
12. Vallesi A., Giuli G., Bradshaw R.A., Luporini P. Autocrine mitogenic activity of pheromones produced by the protozoan ciliate Euplotes raikovi. Nature 1995, 376:522-524.
13. Pertseva M.N., Shpakov A.O. The prokaryotic origin and evolution of eukaryotic chemosignaling systems. Neurosci. Behav. Physiol. 2009, 39:793-804.
14. Shpakov A.O., Pertseva M.N. Signaling systems of lower eukaryotes and their evolution. Int. Rev. Cell Mol. Biol. 2008, 269:151-282.
15. Ortenzi C., Miceli C., Bradshaw R.A., Luporini P. Identification and initial characterization of an autocrine pheromone receptor in the protozoan ciliate Euplotes raikovi. J. Cell Biol. 1990, 111:607-614.
16. Vallesi A., Giuli G., Ghiara P., Scapigliati G., Luporini P. Structure-function relationships of pheromones of the ciliate Euplotes raikovi with mammalian growth factors: cross-reactivity between Er-1 and interleukin-2 systems. Exp. Cell Res. 1998, 241:253-259.
17. Abraham R.T., Weiss A. Jurkat T cells and development of the T-cell receptor signalling paradigm. Nat. Rev. Immunol. 2004, 4:301-308.
18. Antunes R.F., Brandao C., Maia M., Arosa F.A. Red blood cells release factors with growth and survival bioactivities for normal and leukemic T cells. Immunol. Cell Biol. 2011, 89:111-121.
19. Fenstermaker R.A., Ciesielski M.J. Immunotherapeutic strategies for malignant glioma. Cancer Control 2004, 11:181-191.
20. Alimenti C., Vallesi A., Luporini P., Buonanno F., Ortenzi C. Cell aging-induced methionine oxidation causes an autocrine to paracrine shift of the pheromone activity in the protozoan ciliate, Euplotes raikovi. Exp. Cell Res. 2012, 318:144-151.
21. Raffioni S., Miceli C., Concetti A., Barra D., Luporini P. Purification and characterization of new mating pheromones of the ciliate Euplotes raikovi. Exp. Cell Res. 1987, 172:417-424.
22. Cervia D., Garcia-Gil M., Simonetti E., Di Giuseppe G., Guella G., Bagnoli P., Dini F. Molecular mechanisms of euplotin C-induced apoptosis: involvement of mitochondrial dysfunction, oxidative stress and proteases. Apoptosis 2007, 12:1349-1363.
23. Cervia D., Martini D., Garcia-Gil M., Di Giuseppe G., Guella G., Dini F., Bagnoli P. Cytotoxic effects and apoptotic signalling mechanisms of the sesquiterpenoid euplotin C, a secondary metabolite of the marine ciliate Euplotes crassus, in tumour cells. Apoptosis 2006, 11:829-843.
24. Di Giuseppe G., Cervia D., Vallesi A. Divergences in the response to ultraviolet radiation between polar and non-polar ciliated protozoa: UV radiation effects in Euplotes. Microb. Ecol. 2011, 63:334-338.
25. Trielli F., Cervia D., Di Giuseppe G., Ristori C., Kruppel T., Burlando B., Guella G., Viarengo A., Bagnoli P., Delmonte Corrado M.U., Dini F. Action mechanisms of the secondary metabolite Euplotin C: signaling and functional role in Euplotes. J. Euk. Microbiol. 2008, 55:365-373.
26. Perrotta C., Bizzozero L., Cazzato D., Morlacchi S., Assi E., Simbari F., Zhang Y., Gulbins E., Bassi M.T., Rosa P., Clementi E. Syntaxin 4 is required for acid sphingomyelinase activity and apoptotic function. J. Biol. Chem. 2010, 285:40240-40251.
27. Perrotta C., Bizzozero L., Falcone S., Rovere-Querini P., Prinetti A., Schuchman E.H., Sonnino S., Manfredi A.A., Clementi E. Nitric oxide boosts chemoimmunotherapy via inhibition of acid sphingomyelinase in a mouse model of melanoma. Cancer Res. 2007, 67:7559-7564.
28. Cervia D., Martini D., Ristori C., Catalani E., Timperio A.M., Bagnoli P., Casini G. Modulation of the neuronal response to ischaemia by somatostatin analogues in wild-type and knock-out mouse retinas. J. Neurochem. 2008, 106:2224-2235.
29. Cervia D., Di Giuseppe G., Ristori C., Martini D., Gambellini G., Bagnoli P., Dini F. The secondary metabolite Euplotin C induces apoptosis-like death in the marine ciliated protist Euplotes vannus. J. Euk. Microbiol. 2009, 56:263-269.
30. Schefe J.H., Lehmann K.E., Buschmann I.R., Unger T., Funke-Kaiser H. Quantitative real-time RT-PCR data analysis: current concepts and the novel gene expression's CT difference formula. J. Mol. Med. (Berl.) 2006, 84:901-910.
31. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT. Method, Methods 2001, 25:402-408.
32. Armani C., Catalani E., Balbarini A., Bagnoli P., Cervia D. Expression, pharmacology, and functional role of somatostatin receptor subtypes 1 and 2 in human macrophages. J. Leukoc. Biol. 2007, 81:845-855.
33. Cervia D., Zizzari P., Pavan B., Schuepbach E., Langenegger D., Hoyer D., Biondi C., Epelbaum J., Bagnoli P. Biological activity of somatostatin receptors in GC rat tumour somatotrophs: evidence with sst1-sst5 receptor-selective nonpeptidyl agonists. Neuropharmacology 2003, 44:672-685.
34. Cervia D., Petrucci C., Bluet-Pajot M.T., Epelbaum J., Bagnoli P. Inhibitory control of growth hormone secretion by somatostatin in rat pituitary GC cells: sst(2) but not sst(1) receptors are coupled to inhibition of single-cell intracellular free calcium concentrations. Neuroendocrinology 2002, 76:99-110.
35. Cervia D. The beta isoenzyme of Ca(2+)/calmodulin-dependent kinase type II as possible mediator of somatostatin functions in pituitary tumour cells. Gen. Physiol. Biophys. 2011, 30:251-262.
36. Levin A.M., Bates D.L., Ring A.M., Krieg C., Lin J.T., Su L., Moraga I., Raeber M.E., Bowman G.R., Novick P., Pande V.S., Fathman C.G., Boyman O., Garcia K.C. Exploiting a natural conformational switch to engineer an interleukin-2 'superkine'. Nature 2012, 484:529-533.
37. Malek T.R., Castro I. Interleukin-2 receptor signaling: at the interface between tolerance and immunity. Immunity 2010, 33:153-165.
38. Vallesi A., Di Pretoro B., Ballarini P., Apone F., Luporini P. 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 2010, 161:250-263.
39. Javed F., Qadir M.I., Janbaz K.H., Ali M. Novel drugs from marine microorganisms. Crit. Rev. Microbiol. 2011, 37:245-249.
40. Penesyan A., Kjelleberg S., Egan S. Development of novel drugs from marine surface associated microorganisms. Mar. Drugs 2010, 8:438-459.
41. Newman D.J., Cragg G.M. Advanced preclinical and clinical trials of natural products and related compounds from marine sources. Curr. Med. Chem. 2004, 11:1693-1713.
42. Guella G., Skropeta D., Di Giuseppe G., Dini F. Structures, biological activities and phylogenetic relationships of terpenoids from marine ciliates of the genus Euplotes. Mar. Drugs 2010, 8:2080-2116.
43. Savoia D., Avanzini C., Allice T., Callone E., Guella G., Dini F. Antimicrobial activity of Euplotin C, the sesquiterpene taxonomic marker from the marine ciliate Euplotes crassus. Antimicrob. Agents Chemother. 2004, 48:3828-3833.
44. Sand S.L., Oppegard C., Ohara S., Iijima T., Naderi S., Blomhoff H.K., Nissen-Meyer J., Sand O., Plantaricin A a peptide pheromone produced by Lactobacillus plantarum, permeabilizes the cell membrane of both normal and cancerous lymphocytes and neuronal cells. Peptides 2010, 31:1237-1244.
45. Oppenheim J.J. Cytokines: past, present, and future. Int. J. Hematol. 2001, 74:3-8.
46. Zhu J., Yamane H., Paul W.E. Differentiation of effector CD4 T cell populations (; *). Annu. Rev. Immunol. 2010, 28:445-489.
47. Romagnani S. Regulation of the T cell response. Clin. Exp. Allergy 2006, 36:1357-1366.
48. Liao W., Lin J.X., Leonard W.J. IL-2 family cytokines: new insights into the complex roles of IL-2 as a broad regulator of T helper cell differentiation. Curr. Opin. Immunol. 2011, 23:598-604.
49. Chizzolini C., Chicheportiche R., Burger D., Dayer J.M. Human Th1 cells preferentially induce interleukin (IL)-1beta while Th2 cells induce IL-1 receptor antagonist production upon cell/cell contact with monocytes. Eur. J. Immunol. 1997, 27:171-177.
50. Bradley L.M., Asensio V.C., Schioetz L.K., Harbertson J., Krahl T., Patstone G., Woolf N., Campbell I.L., Sarvetnick N., Th1 Islet-specific but not Th2, cells secrete multiple chemokines and promote rapid induction of autoimmune diabetes. J. Immunol. 1999, 162:2511-2520.
51. Burchill M.A., Yang J., Vang K.B., Farrar M.A. Interleukin-2 receptor signaling in regulatory T cell development and homeostasis. Immunol. Lett. 2007, 114:1-8.
52. Lee S.I., Kim B.S., Kim K.S., Lee S., Shin K.S., Lim J.S. Immune-suppressive activity of punicalagin via inhibition of NFAT activation. Biochem. Biophys. Res. Commun. 2008, 371:799-803.
53. Luongo D., Bergamo P., Rossi M. Effects of conjugated linoleic acid on growth and cytokine expression in Jurkat T cells. Immunol. Lett. 2003, 90:195-201.
54. Reddy J., Chastagner P., Fiette L., Liu X., Theze J. IL-2-induced tumor necrosis factor (TNF)-beta expression: further analysis in the IL-2 knockout model, and comparison with TNF-alpha, lymphotoxin-beta, TNFR1 and TNFR2 modulation. Int. Immunol. 2001, 13:135-147.
55. Gong D., Malek T.R. Cytokine-dependent Blimp-1 expression in activated T cells inhibits IL-2 production. J. Immunol. 2007, 178:242-252.
56. Rodriguez-Melendez R., Camporeale G., Griffin J.B., Zempleni J. Interleukin-2 receptor-gamma -dependent endocytosis depends on biotin in Jurkat cells. Am. J. Physiol. Cell Physiol. 2003, 284:C415-421.
57. Rincon M., Flavell R.A., Davis R.J. Signal transduction by MAP kinases in T lymphocytes. Oncogene 2001, 20:2490-2497.
58. Apone F., Vallesi A., Di Pretoro B., Luporini P. Cross-talk between the autocrine (mitogenic) pheromone loop of the ciliate Euplotes raikovi and the intracellular cyclic AMP concentration. Exp. Cell Res. 2003, 285:107-113.