Modulation of protein synthesis relative to DNA synthesis alters the timing of differentiation in the protozoan parasite Theileria annulata

Journal of Cell Science

Volumn 110, Issue 13, 1997, Pages 1441-1451

  Shiels, Brian ^a   Aslam, Nasreen ^a   McKellar, Sue ^a   Smyth, Audra ^a   Kinnaird, Jane ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Corruptible time; Eukaryotic differentiation; Growth and division; Mitotic clock; Protozoan parasite

Indexed keywords

APHIDICOLIN; OXYTETRACYCLINE;

ARTICLE; CELL DIFFERENTIATION; DNA SYNTHESIS; MEROZOITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; THEILERIA;

ANIMALS; APHIDICOLIN; CELL DIVISION; DNA, PROTOZOAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; METHIONINE; NUCLEIC ACID SYNTHESIS INHIBITORS; OXYTETRACYCLINE; PROTEIN SYNTHESIS INHIBITORS; PROTOZOAN PROTEINS; TEMPERATURE; THEILERIA ANNULATA;

EUKARYOTA; PROTOZOA; THEILERIA; THEILERIA ANNULATA;

EID: 0030875958     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (47)

1. Aller, P., Rius, C., Mata, F., Zorrilla, A., Cabanas, C., Bellon, T. and Benabeu, C. (1992). Camptothecin induces differentiation and stimulates the expression of differentiation-related genes in U-937 human promonocytic leukemia cells. Cancer Res. 52, 1245-1251.
2. Ball, S. J. and Warren, E. W. (1966). Effects of chlortetracycline, oxytetracycline and spiramycine on Eimeria tenella in chicks. J. Comp Path. 76, 255-259.
3. Bass, K. E. and Wang, C. C. (1992). Transient inhibition for protein synthesis accompanies differentiation of Trypanosoma brucei from bloodstream to procyclic forms. Mol. Biochem. Parasitol. 56, 129-140.
4. Blau, H. M. (1992). Differentiation requires continuous active control. Annu. Rev. Biochem. 61, 1213-1230.
5. Bogler, O., Wren, D., Barnett, S. C., Land, H. and Noble, M. (1990). Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (0-2A) progenitor cells. Proc. Nat. Acad. Sci. USA 87, 6368-6372.
6. Bohne, W., Heesemann, J. and Gross, U. (1994). Reduced replication of Toxoplasma gondii is necessary for induction of bradyzoite-specific antigens: a possible role for nitric oxide in triggering stage conversion. Infect. Immunol. 62, 1761-1767.
7. Bruce, M. C., Allano, P., Duthie, S. and Carter, R. (1990). Commitment of the malaria parasite Plasmodium falciparum to sexual and asexual development. Parasitology 100, 191-200.
8. Brun, R. and Schonenberger, M. (1981). Stimulating effect of citrate and cisaconitate on the transformation of Trypanosoma brucei bloodstream forms to procyclic forms in vitro. Z. Parasitenkd. 66, 17-24.
9. Cinatl, J. J., Cinatl, J., Driever, P. H., Rabenau, H., Novak, M., Stefanik, M., Kornhuber, B. and Doerr, H. W. (1994). Aphidicolin induces myogenic differentiation in the human rhabdomyosarcoma cell line KFR. Cell Biol. Int. 18, 271-278.
10. De Gee, A. L. W., Causten, P. H. B., McCann, P. P. and Mansfield, J. M. (1984). Morphological changes in Trypanosoma brucei rhodesiense following inhibition of polyamine biosynthesis in vivo. Tissue & Cell 16, 731-738.
11. Friend, C., Scher, W., Holland, J. G. and Sato, T. (1971). Hemoglobin synthesis in murine virus-induced leukemic cells in vitro: stimulation of erythroid differentiation by dimethyl sulfoxide. Proc. Nat. Acad. Sci. USA 68, 378-382.
12. Gerhards, J., Gill, A. C., Ehrfeld, A. Y. B., Dobbelaere, D. A. E. and Williams, R. O. (1989). Isolation and characterization of RNA from the intracellular parasite Theileria parva. Mol. Biochem. Parasitol. 34, 15-24.
13. Gerhards, J., Ebel, T., Dobbelaere, O. O. A. E., Morzaria, S. P., Musoke, A. J., Williams, R. O. and Lipp, J. (1994). Sequence and expression of a 90-kilodalton heat-shock protein family member of Theileria parva. Mol. Biochem. Parasitol. 68, 177-358.
14. Gurnett, A. M., Dulski, P. M., Darkin-Rattray, D., Carrington, M. J. and Schmatz, D. M. (1995). Selective labeling of intracellular parasite proteins using ricin. Proc. Nat. Acad. Sci. USA 92, 2388-2392.
15. Gusella, J., Geller, R., Clarke, B., Weeks, V. and Housman, D. (1976). Commitment to erythroid differentiation by Friend erythroleukemic cells: a stochastic analysis. Cell 9, 221-229.
16. Harwood, A. J., Hopper, N. A., Simon, M. N., Driscoll, D. M., Veron, M. and Williams, J. G. (1992). Culmination in Dictyostelium is regulated by the cAMP-dependent protein kinase. Cell 69, 615-624.
17. Heath, S., Hieny, S. and Sher, A. (1990). A cyclic AMP inducible gene expressed during the development of infective stages of Trypanosoma cruzi. Mol. Biochem. Parasitol. 43, 133-142.
18. Hulliger, L. (1965). Cultivation of three species of Theileria in lymphoid cells in vitro. J. Protozool. 12, 649-655.
19. Hulliger, L., Brown, C. G. D. and Wilde, J. H. K. (1966). Transition of developmental stages of Theileria parva in vitro at high temperature. Nature 211, 328-329.
20. Inselburg, J. and Banyal, H. S. (1984). Synthesis of DNA during the asexual cycle of Plasmodium falciparum in culture. Mol. Biochem. Parasitol. 10, 79-87.
21. Irvin, A. D., Brown, C. G. D. and Stagg, D. A. (1975). Theileria parva: effects of irradiation on a culture of parasitised bovine lymphoid cells. Exp. Parasitol. 38, 64-74.
22. Jarrett, W. F. H., Crighton, G. W. and Pirie, H. M. (1969). Theileria parva: kinetics of replication. Exp. Parasitol. 24, 9-25.
23. Katagiri, K., Hattori, S., Nakamura, S., Yamamoto, T., Yoshida, T. and Katagiri, T. (1994). Activation of Ras and formation of GAP complex during TPA-induced monocytic differentiation of HL-60 cells. Blood 84, 1780-1789.
24. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
25. Laskin, D. L., Sirak, A. A. and Laskin, J. D. (1991). Differentiation of HL-60 myeloid leukaemia cells is associated with a transient block in the G2 phase of the cell cycle. Cell Prolif. 24, 341-353.
26. Lui, F., Hata, A., Baker, J. C., Doody, J., Carcamo, J., Harland, R. M. and Massague, J. (1996). A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381, 620-623.
27. Mason, P. J., Shiels, B. R., Tait, A., Beck, P. and Hall, R. (1989). Sequence and expression of a gene from Theileria annulata coding for a 70-kilodalton heat-shock protein. Mol. Biochem. Parasitol. 37, 27-36.
28. Matthews, K. R. and Gull, K. (1994). Evidence for an interplay between cell cycle progression and the initiation of differentiation between life cycle forms of African trypanosomes. J. Cell Biol. 125, 1147-1156.
29. McHardy, N., Wekesa, L. S., Hudson, A. T. and Randall, A. W. (1985). Antitheilerial activity of BW720C (buparvaquone): a comparison with parvaquone. Res. Vet. Sci. 39, 29-33.
30. Murate, T., Kagami, Y., Hotta, T., Yoshida, T., Saito, H. and Yoshida, S. (1990). Terminal differentiation of human erythroleukemia cell line K562 induced by apidicolin. Exp. Cell Res. 191, 45-50.
31. Ono, T., Ohnishi, Y., Nagamune, K. and Kano, M. (1993). Gametocytogenesis induction by berenil in cultured Plasmodium falciparum. Exp. Parasitol. 77, 74-78.
32. Orkin, S. H., Harosi, F. and Leder, P. (1975). Differentiation in erythroleukemic cells and their somatic hybrids. Proc. Nat. Acad. Sci. USA 72, 98-102.
33. Rueben, R. C., Wife, R. L., Breslow, R., Rifkind, R. A. and Marks, P. A. (1976). A new group of potent inducers of differentiation in murine erythroleukemia cells. Proc. Nat. Acad. Sci. USA 73, 862-866.
34. Ryley, J. F. and Wilson, R. G. (1976). Laboratory studies with some older anticoccidials. Parasitology 73, 287-309.
35. Sacks, D. L. and Perkins, P. V. (1984). Identification of an infective stage of Leishmania promastigotes. Science 223, 1417-1419.
36. Sanchez, L., Enea, V. and Eichinger, D. (1994). Identification of a developmentally regulated transcript expressed during encystation of Entamoeba invadens. Mol. Biochem. Parasitol. 67, 125-135.
37. Seed, J. R. and Sechelski, J. B. (1989). Mechanism of long slender (LS) to short stumpy (SS) transformation in the African trypanosomes. J. Protozool. 36, 572-577.
38. Shiels, B. R., Kinnaird, J., McKellar, S., Dickson, J., Ben-Miled, L., Melrose, R., Brown, D. and Tait, A. (1992). Disruption of synchrony between parasite growth and host cell division is a determinant of differentiation to the merozoite in Theileria annulata. J. Cell Sci. 101, 97-107.
39. Shiels, B. R., Smyth, A., Dickson, J., McKellar, S., Tetley, L., Fujisaki, K., Hutchinson, B. and Kinnaird, J. H. (1994). A stoichiometric model of stage differentiation in the protozoan parasite Theileria annulata. Mol. Cell Differ. 2, 101-125.
40. Soete, M., Camus, D. and Dubremetz, J. F. (1994). Experimental induction of bradyzoite-specific antigen expression and cyst formation by the RH strain of Toxoplasma gondii in vitro. Exp. Parasitol. 78, 361-370.
41. Spooner, P. R. (1990a). The effects of oxytetracycline on Theileria parva in vitro. Parasitology 100, 11-17.
42. Spooner, P. R. (1990b). Oxytetracyclin inhibition of mitochondrial protein synthesis in bovine lymphocytes infected with Theileria parva or stimulated by mitogen. Parasitology 101, 387-393.
43. Tarella, C., Ferrero, D., Gallo, E., Pagliardi, G. L. and Ruscetti, F. W. (1982). Induction of differentiation of HL-60 cells by dimethyl sulfoxide: evidence for a stochastic model not linked to the cell division cycle. Cancer Res. 42, 445-449.
44. Temple, S. and Raff, M. C. (1986). Clonal analysis of oligodendrocyte development in culture: evidence for a developmental clock that counts cell divisions. Cell 44, 773-779.
45. Van Der Ploeg, L. H. T., Gianni, S. H. and Cantor, C. R. (1985). Heat shock genes: regulatory role for differentiation in parasitic protozoa. Science 228, 1443-1446.
46. Walker, A. R. and McKellar, S. B. W. (1983). The maturation of Theileria annulata in Hyalomma anatolicum anatolicum stimulated by incubation or feeding to produce sporozoites. Vet. Parasitol. 13, 13-21.
47. Zilberstein, D., Blumenfeld, N., Liveanu, V., Gepstein, A. and Jaffe, C. L. (1991). Growth at acidic pH induces an amastigote stage-specific protein in Leishmania promastigotes. Mol. Biochem. Parasitol. 45, 175-178.