Resistance to spontaneous apoptosis in acute myeloid leukaemia blasts is associated with p-glycoprotein expression and function, but not with the presence of FLT3 internal tandem duplications

British Journal of Haematology

Volumn 120, Issue 6, 2003, Pages 1009-1016

  Pallis, Monica ^a,b   Turzanski, Julie ^a   Grundy, Martin ^a   Seedhouse, Claire ^a   Russell, Nigel ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b NOTTINGHAM CITY HOSPITAL   (United Kingdom)

Author keywords

Acute myeloid leukaemia (AML); Apoptosis; FLT3 internal tandem duplication; P glycoprotein; Rhodamine 123

Indexed keywords

FLT3 LIGAND; GLYCOPROTEIN P;

ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; ARTICLE; BLAST CELL; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; INCUBATION TIME; MAJOR CLINICAL STUDY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REMISSION;

ACUTE DISEASE; APOPTOSIS; CYCLOSPORINS; DRUG RESISTANCE, MULTIPLE; FLOW CYTOMETRY; FLUORESCENT DYES; FMS-LIKE TYROSINE KINASE 3; HUMANS; LEUKEMIA, MYELOID; P-GLYCOPROTEIN; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RECURRENCE; REMISSION INDUCTION; REPETITIVE SEQUENCES, NUCLEIC ACID; RHODAMINE 123; STATISTICS, NONPARAMETRIC; TUMOR CELLS, CULTURED;

EID: 0037353767     PISSN: 00071048     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2141.2003.04210.x     Document Type: Article

References (38)

1. Banker, D.E., Groudine, M., Norwood, T. & Appelbaum, F.R. (1997) Measurement of spontaneous and therapeutic agent-induced apoptosis with bcl-2 protein expression in acute myeloid-leukemia. Blood, 89, 243-255.
2. Borst, P., Zelcer, N. & van Helvoort, A. (2000) ABC transporters in lipid transport. Biochimica et Biophysica Acta, 1486, 128-144.
3. Broxterman, H.J., Sonneveld, P., Feller, N., Ossenkoppele, G.J., Wahrer, D.C., Eekman, C.A., Schoester, M., Lankelma, J., Pinedo, H.M., Lowenberg, B. & Schuurhuis, G.J. (1996) Quality control of multidrug resistance assays in adult acute leukemia: correlation between assays for P-glycoprotein expression and activity. Blood, 87, 4809-4816.
4. Bunting, K., Galipeau, J., Topham, D., Benaim, E. & Sorrentino, B. (1998) Transduction of murine bone marrow cells with an MDR1 vector enables ex vivo stem cell expansion, but these expanded grafts cause a myeloproliferative syndrome in transplanted mice. Blood, 92, 2269-2279.
5. Bunting, K.D., Zhou, S., Lu, T. & Sorrentino, B.P. (2000) Enforced P-glycoprotein pump function in murine bone marrow cells results in expansion of side population stem cells in vitro and repopulating cells in vivo. Blood, 96, 902-909.
6. Campos, L., Guyotat, D., Archimbaud, E., Calmard-Oriol, P., Tsuruo. T., Troncy, J., Treille, D. & Fiere, D. (1992) Clinical significance of multidrug resistance P-glycoprotein expression on acute nonlymphoblastic leukaemia cells at diagnosis. Blood, 79, 473-476.
7. Del Poeta, G., Stasi, R., Aronica, G., Venditti, A., Cox, M.C., Bruno, A., Buccisano, F., Masi, M., Tribalto, M., Amadori, S. & Papa, G. (1996) Clinical relevance of P-glycoprotein expression in de novo acute myeloid leukemia. Blood, 87, 1997-2004.
8. Drexler, H.G., Meyer, C. & Quentmeier, H. (1999) Effects of FLT3 ligand on proliferation and survival of myeloid leukemia cells. Leukemia and Lymphoma, 33, 83-91.
9. Garrido, S.M., Cooper, J.J., Appelbaum, F.R., Willman, C.L., Kopecky, K. & Banker, D.E. (2001) Blasts from elderly acute myeloid leukemia patients are characterized by low levels of culture- and drug-induced apoptosis. Leukemia Research, 25, 23-32.
10. Gilliland, D. (2001) Hematologic malignancies. Current Opinions in Hematology, 8, 189-191.
11. Grimwade, D., Walker, H., Oliver, F., Wheatley, K. Harrison, C., Harrison, G., Rees, J., Hann, I., Stevens, R., Burnett, A. & Goldstone, A. (1998) The importance of diagnostic cytogenetics on outcome in AML: analysis of 1612 patients entered into the MRC AML 10 trial. The Medical Research Council Adult and Children's Leukaemia Working Parties. Blood, 92, 2322-2333.
12. Hayakawa, F., Towatari, M., Kiyoi, H., Tanimoto, M., Kitamura, T., Saito, H. & Naoe, T. (2000) Tandem-duplicated Flt3 constitutively activates STATS and MAP kinase and introduces autonomous cell growth in IL-3-dependent cell lines. Oncogene, 19, 624-631.
13. Hunault, M., Zhou, D., Delmer, A., Ramond, S., Viguie, F., Cadiou, M., Perrot, J.Y., Levy, V., Rio, B., Cymbalista, F., Zittoun, R. & Marie, J.P. (1997) Multidrug resistance gene expression in acute myeloid leukemia: major prognosis significance for in vivo drug resistance to induction treatment. Annals of Hematology, 74, 65-71.
14. Idriss, H.T., Hannun, Y.A., Boulpaep, E. & Basavappa, S. (2000) Regulation of volume-activated chloride channels by P-glycoprotein: phosphorylation has the final say!. Journal of Physiology, 524 Part 3, 629-636.
15. Johnstone, R., Cretney, E. & Smyth, M. (1999) P-glycoprotein protects leukemia cells against caspase-dependent, but not caspase-independent, cell death. Blood, 93, 1075-1085.
16. Johnstone, R.W., Ruefli, A.A., Tainton, K.M. & Smyth, M.J. (2000) A role for P-glycoprotein in regulating cell death. Leukemia and Lymphoma, 38, 1-11.
17. Kiyoi, H., Naoe, T., Nakano, Y., Yokota, S., Minami, S., Miyawaki, S., Asou, N., Kuriyama, K., Jinnai, I., Shimazaki, C., Akiyama, H., Saito, K., Oh, H., Motoji, T., Omoto, E., Saito, H., Ohno, R. & Ueda, R. (1999) Prognostic implication of FLT3 and N-RAS gene mutations in acute myeloid leukemia. Blood, 93, 3074-3080.
18. Kottaridis, P.D., Gale, R.E., Frew, M.E., Harrison, G., Langabeer, S.E., Belton, A.A., Walker, H., Wheatley, K., Bowen, D.T., Burnett, A.K., Goldstone, A.H. & Linch, D.C. (2001) The presence of a FLT3 internal tandem duplication in patients with acute myelold leukemia (AML) adds important prognostic information to cytogenetic risk group and response to the first cycle of chemotherapy: analysis of 854 patients from the United Kingdom Medical Research Council AML 10 and 12 trials. Blood, 98, 1752-1759.
19. Leith, C. (1998) Multidrug resistance in leukemia. Current Opinions in Hematology, 5, 287-291.
20. Leith, C.P., Kopecky, K.J., Godwin, J., McConnell, T., Slovak, M.L., Chen, I.M., Head, D.R., Appelbaum, F.R. & Willman, C.L. (1997) Acute myeloid leukemia in the elderly: assessment of multidrug resistance (MDR1) and cytogenetics distinguishes biologic subgroups with remarkably distinct responses to standard chemotherapy. A Southwest Oncology Group Study. Blood, 89. 3323-3329.
21. Levis, M., Allebach, J., Tse, K.F., Zheng, R., Baldwin, B.R., Smith, B.D., Jones-Bolin, S., Ruggeri, B., Dionne, C. & Small, D. (2002) A FLT3-targeted tyrosine kinase inhibitor is cytotoxic to leukemia cells in vitro and in vivo. Blood, 99, 3885-3891.
22. Lisovsky, M., Estrov, Z., Zhang, X., Consoli, U., Sanchez-Williams, G., Snell, V., Munker, R., Coodacre, A., Savchenko, V. & Andreeff, M. (1996) Flt3 ligand stimulates proliferation and inhibits apoptosis of acute myeloid leukemia cells: regulation of Bcl-2 and Bax. Blood, 88, 3987-3997.
23. Milella, M., Kornblau, S.M., Estrov, Z., Carter, B.Z., Lapillonne, H., Harris, D., Konopleva, M., Zhao, S., Estey, E. & Andreeff, M. (2001) Therapeutic targeting of the MEK/MAPK signal transduction module in acute myeloid leukemia. Journal of Clinical Investigation. 108, 851-859.
24. Mizuki, M., Fenski, R., Halfter, H., Matsumura, I., Schmidt, R., Muller, C., Gruning, W., Kratz-Albers, K., Serve, S., Steur, C., Buchner, T., Kienast, J., Kanakura, Y., Berdel, W.E. & Serve, H. (2000) Flt3 mutations from patients with acute myeloid leukemia induce transformation of 32D cells mediated by the Ras and STAT5 pathways. Blood, 96, 3907-3914.
25. Nussler, V., Pelka-Fleischer, R., Zwierzina, H., Nerl, C., Beckert, B., Gieseler, F., Diem, H., Ledderose, G., Gullis, E., Sauer, H. & Wilmanns, W. (1996) P-glycoprotein expression in patients with acute leukemia - clinical relevance. Leukemia, 10, S23-S31.
26. Pallis, M. & Russell, N. (2000) P-glycoprotein plays a drug-efflux-independent role in augmenting cell survival in acute myeloblastic leukemia and is associated with modulation of a sphingomyelin-ceramide apoptotic pathway. Blood, 95, 2897-2904.
27. Pallis, M., Syan, J. & Russell, N.H. (1999a) Flow cytometric chemosensitivity analysis of blasts from patients with acute myeloblastic leukemia and myelodysplastic syndromes: the use of 7AAD with antibodies to CD45 or CD34. Cytometry, 37, 308-313.
28. Pallis, M., Turzanski, J., Langabeer, S. & Russell, N.H. (1999b) Reproducible flow cytometric methodology for measuring multi-drug resistance in leukaemic blasts. Advances in Experimental Medicine and Biology, 457, 77-88.
29. Pallis, M., Turzanski, T., Harrison, G., Wheatley, K., Langabeer, S., Burnett, A. & Russell, N. (1999c) Use of standardised flow cytometric determinants of multidrug resistance to analyse response to remission induction chemotherapy in patients with acute myeloblastic leukaemia. British Journal of Haematology, 104, 307-312.
30. Pallis, M., Grundy, M., Turzanski, J., Kofler, R. & Russell, N. (2001) Mitochondrial membrane sensitivity to depolarization in acute myeloblastic leukemia is associated with spontaneous in vitro apoptosis, wild-type TP53, and vicinal thiol/disulfide status. Blood, 98, 405-413.
31. Pallis, M., Turzanski, J., Higashi, Y. & Russell, N. (2002) P-glycoprotein in acute myeloid leukaemia: therapeutic implications of its association with both a multidrug-resistant and an apoptosis-resistant phenotype. Leukemia and Lymphoma, 43, 1221-1228.
32. Robinson, L.J., Roberts, W.K., Ling, T.T., Lamming, D., Sternberg, S.S. & Roepe, P.D. (1997) Human MDR 1 protein overexpression delays the apoptotic cascade in Chinese hamster ovary fibroblasts. Biochemistry, 36, 11169-11178.
33. Sincock, P.M. & Ashman, L.K. (1997) Expression of c-kit and functional drug efflux are correlated in de novo acute myeloid leukaemia. Leukemia, 11, 1850-1857.
34. Smeets, M.E., Raymakers, R.A., Vierwinden, G., Pennings, A.H., Wessels, H. & de Witte, T. (1999) Triggering noncycling hematopoietic progenitors and leukemic blasts to proliferate increases anthracycline retention and toxicity by downregulating multi-drug resistance. Blood, 94, 2414-2423.
35. Smith, B.D., Bambach, B.J., Vala, M.S., Barber, J.P., Enger, C., Brodsky, R.A., Burke, P.J., Gore, S.D. & Jones, R.J. (1998) Inhibited apoptosis and drug resistance in acute myeloid leukaemia. British Journal of Haematology, 102, 1042-1049.
36. Smyth, M., Krasovskis, E., Sutton, V. & Johstone, R. (1998) The drug efflux protein, P-glycoprotein, additionally protects drug-resistant tumor cells from multiple forms of caspase-dependent apoptosis. Proceedings of the National Academy of Sciences of the USA, 95, 7024-7029.
37. van den Heuvel-Eibrink, M.M., van der Holt, B., te Boekhorst, P.A.W., Pieters, R., Schoester, M., Lowenberg, B. & Sonneveld, P. (1997) MDR 1 expression is an independent prognostic factor for response and survival in de novo acute myeloid leukaemia. British Journal of Haematology, 99, 76-83.
38. Wuchter, C., Karawajew, L., Ruppert, V., Buchner, T., Schoch, C., Haferlach, T., Ratei, R., Dorken, B. & Ludwig, W.D. (1999) Clinical significance of CD95, Bcl-2 and Bax expression and CD95 function in adult de novo acute myeloid leukemia in context of P- glycoprotein function, maturation stage, and cytogenetics. Leukemia, 13, 1943-1953.