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Temporal variations in protein tyrosine kinase activity in leukaemic cells: Response to all-trans retinoic acid

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Abstract

Protein tyrosine kinases (PTKs) play a critical role in the modulation of a wide variety of cellular events such as cell division, differentiation and metabolism. Regulation of PTK activity must be tightly controlled as over-stimulation is known to impair normal cell growth, resulting in oncogenic transformation. Since evidence suggests that dynamic oscillatory behaviour occurs in metabolic control processes, we investigated the patterns of oscillatory behaviour in the total protein content and enzyme activity of PTK exhibited by proliferating and differentiating human acute promyelocytic cells. Distinct rhythmic patterns of oscillatory behaviour were observed in both the amount of extractable protein and PTK enzyme activity. Rhythmic characteristics such as period and amplitude were significantly modulated following treatment with all-trans retinoic acid, an inducing agent. These results support the view that dynamic oscillatory control processes may play an important role in regulating cellular behaviour.

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References

  1. Hunter T: Protein kinases and phosphatases: The yin and yang of protein phosphorylation and signaling. Cell 80: 225-236, 1995

    Google Scholar 

  2. Den Hertog J: Protein tyrosine phosphatases in development. Mech Dev 85: 3-14, 1999

    Google Scholar 

  3. Bovolenta C, Camorali L, Lorini AL, Ghezzi S, Vicenzi E, Lazzarin Poli G: Constitutive activation of STATs upon in vivo human immunodeficiency virus infection. Blood 15,94: 4202-4209, 1999

    Google Scholar 

  4. Kirken RA, Erwin RA, Wang L, Wang Y, Rui H, Farrar WL: Functional uncoupling of the Janus kinase 3-Stat5 pathway malignant growth of human T cell leukaemia virus type 1-transformed human T cells. J Immunol 165: 5097-5104, 2000

    Google Scholar 

  5. Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI, Puc J, Miliaresis C, Rodgers L, Mccombie R, Bigner SH, Giovanella BC, Ittmann M, Tycko B, Hibshoosh H, Wigler MH, Parsons R: PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 275: 1943-1947, 1997

    Google Scholar 

  6. Bouras T, Southey MC, Venter DJ: Overexpression of the steroid receptor coactivator AIB1 in breast cancer correlates with the absence of estrogen and progesterone receptors and positivity for p53 and HER2/neu. Cancer Res 61: 903-907, 2001

    Google Scholar 

  7. Hiratsuka S, Maru Y, Okada A, Seiki M, Noda T, Shibuya M: Involvement of Flt-1 tyrosine kinase (vascular endothelial growth factor receptor-1) in pathological angiogenesis. Cancer Res 61: 1207-1213, 2001

    Google Scholar 

  8. Brickell PM: Receptor and non-receptor protein tyrosine kinases. In: R.J. Clemens (ed). Protein Phosphorylation in Cell Growth Regulation. Harwood Academic Publishers, 1996, pp 19-57

  9. Hubbard SR, Mohammadi M, Schlessinger J: Autoregulatory mechanisms in protein tyrosine kinases. J Biol Chem 273: 11987-11990, 1998

    Google Scholar 

  10. Sun H, Sharma AK, Budde RJ: Autophosphorylation of Src and Yes blocks their activation by Csk phosphorylation. Oncogene 17: 1587-1595, 1998

    Google Scholar 

  11. Andersen JN, Elson A, Lammers R, Romers J, Clausen JT, Moller KB, Moller NPH: Comparative study of protein tyrosine phosphatase-ε isoforms: Membrane localization confers specificity in cellular signalling. Biochem J 354: 581-590, 2001

    Google Scholar 

  12. Hammond KD, Wollbrandt RK, Gilbert DA: Acid phosphatase and phosphoamino acid phosphatases in murine erythroleukaemic cells. Int J Biochem 17: 259-264, 1985

    Google Scholar 

  13. Hammond KD, Cloutman L, Mindel B, Gilbert DA: Temporal variations in phosphoamino acid phosphatase activities in murine erythroleukaemic cells. Int J Biochem 21: 197-201, 1989

    Google Scholar 

  14. Hammond KD, Cloutman L, Gilbert DA: Cancer reversal: Regulation of phosphotyrosine phosphatase. Biochem Soc Trans 17: 1048-1049, 1989

    Google Scholar 

  15. Hammond KD: Oscillations and cancer: Control of proteins kinases during proliferation and differentiation of leukaemic cells. 17th Int Cancer Congress, Rio de Janeiro, Brazil, 1998

  16. Brodsky VY, Boikov PY, Nechaeva NV, Yurovitsky YG, Novikova TE, Fateeva VI, Shevchenko NA: The rhythm of protein synthesis does not depend on oscillations of ATP level. J Cell Science 103: 363-370, 1992

    Google Scholar 

  17. Brodsky VY, Nechaeva NV, Zvezdina ND, Novikova TE, Gvasava IG, Fateeva VI, Prokazova NV, Golovanova NK: Ganglioside-mediated synchronization of protein synthesis oscillation in cultured hepatocytes. Cell Biol Int 25: 211-222, 2000

    Google Scholar 

  18. Berridge MJ, Bootman MD, Lipp P: Calcium—a life and death signal. Nature 395: 645-648, 1998

    Google Scholar 

  19. Berridge MJ: Signal transduction. The calcium entry pas de deux. Science 287: 1604-1605, 2000

    Google Scholar 

  20. Lloyd D, Gilbert DA: Temporal organisation of the cell division cycle in eukaryotic microbes. In: M.X. Caddick, S. Baumberg, D.A. Hodgson, M.J. Phillips-Jones (eds). Microbial Responses to Light and Time. Cambridge, UK, Cambridge University Press, 1998, pp 251-278

    Google Scholar 

  21. Norel R, Agur Z: A model for the adjustment of the mitotic clock by cyclin and MPF levels. Science 251: 1076-1078, 1991

    Google Scholar 

  22. Tyson JJ: Modeling the cell division cycle: cdc2 and cyclin interactions. Proc Natl Acad Sci USA 88: 7328-7332, 1991

    Google Scholar 

  23. Goldbeter A: A minimal cascade model for the mitotic oscillator involving cyclin and cd2 kinase. Proc Natl Acad Sci USA 88: 9107-9111, 1991

    Google Scholar 

  24. Tyson JJ, Novak B, Odell GM, Chen K, Thron CD: Chemical kinetic theory: Understanding cell-cycle regulation. TIBS 21: 89-96, 1996

    Google Scholar 

  25. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the folin phenol reagent. J Biol Chem 193: 265-275, 1951

    Google Scholar 

  26. Tsilimigras CWA, Gilbert DA: High frequency, high amplitude oscillations in the amount of protein extractable from cultured cells. S Afr Sci 73: 123-125, 1977

    Google Scholar 

  27. Ferreira GMN, Hammond KD, Gilbert DA: Insulin stimulation of high frequency phosphorylation dynamics in murine erythroleukaemia cells. Biosystems 33: 31-33, 1994

    Google Scholar 

  28. Ferreira GMN, Hammond KD, Gilbert DA: Oscillatory variations in the amount of protein extractable from murine erythroleukameia cells: Stimulation by insulin. BioSystems 32: 183-190, 1994

    Google Scholar 

  29. Calvert-Evers JL, Hammond KD: Temporal variations in protein tyrosine phosphatase activity during cell proliferation and differentiation. Cell Biol Int 24: 559-567, 2000

    Google Scholar 

  30. Gilbert DA, Lloyd D: The living cell: a complex autodynamic multioscillator system? Cell Biol Int. 24: 501-514, 2000

    Google Scholar 

  31. Faille A, Poirier O, Turmel P, Chomienne C, Charron D, Abita J-P: Changes in the patterns of protein phosphorylation associated with granulocytic and monocytic-induced differentiation of HL-60 cells. Anticancer Res 6: 1053-1064, 1986

    Google Scholar 

  32. Frank DA, Sartorelli AC: Biochemical characterisation of tyrosine kinase and phosphotyrosine phosphatase activities of HL-60 leukaemia cells. Cancer Res 48: 4299-4306, 1988

    Google Scholar 

  33. Gineitis A, Treigyte G, Savickiene J, Shanbhag VP, Stigbrandt T: Long-term changes in tyrosine phosphorylation of the abundant nuclear proteins during granulocytic differentiation of HL-60 cells. Cell Mol Life Sci 55: 317-326, 1999

    Google Scholar 

  34. Gilbert DA: The temporal response of the dynamic cell to disturbance and its possible relationship to differentiation and cancer. S Afr Sci 70: 234-244, 1974

    Google Scholar 

  35. Gilbert DA: The nature of the cell cycle and the control of cell proliferation. Biosystems 5: 197-206, 1974

    Google Scholar 

  36. Gilbert DA: Temporal organisation, reorganisation and disorganisation in cells. In: L.N. Edmunds (ed). Cell Cycle Clocks. Marcel Dekker Inc., New York, 1974b, pp 5-25

    Google Scholar 

  37. Ferreira GMN, Wölfe H, Hammond KD, Gilbert DA: High frequency oscillations in the activity of phosphotyrosine phosphatase in murine erythroleukaemic cells: Action of insulin and hexamethylene bis-acetamide. Cell Biol Int 20: 559-605, 1996

    Google Scholar 

  38. Hammond KD, Bhoola R, Bodalina U, Gilbert DA: Dynamic cells: Temporal organisation and control of phosphorylation. Trends Comp Biochem Physiol 4: 75-88, 1998

    Google Scholar 

  39. Gilbert DA, Visser G, Ferreira GMN, Hammond KD: Transient chaos in intracellular dynamics? Cell Biol Int 24: 589-591, 2000

    Google Scholar 

  40. Ferreira GMN, Hammond KD, Gilbert DA: Independent high frequency oscillations in the amounts of individual isozymes of lactate dehydrogenase in HL-60 cells. Cell Biol Int 20: 607-611, 1996

    Google Scholar 

  41. Ferreira GMN, Hammond KD, Gilbert DA: Distinct, very high frequency oscillations in the activity and amount of active isozyme of lactate dehydrogenase in murine erythroleukaemic cells and a cell-free system. Cell Biol Int 20: 625-633, 1996

    Google Scholar 

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Calvert-Evers, J., Hammond, K. Temporal variations in protein tyrosine kinase activity in leukaemic cells: Response to all-trans retinoic acid. Mol Cell Biochem 245, 23–30 (2003). https://doi.org/10.1023/A:1022806129035

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