Synergistic decrease of clonal proliferation, induction of differentiation, and apoptosis of acute promyelocytic leukemia cells after combined treatment with novel 20-epi vitamin D3 analogs and 9-cis retinoic acid

Journal of Clinical Investigation

Volumn 99, Issue 2, 1997, Pages 349-360

  Elstner, Elena ^a   Linker Israeli, Mariana ^a   Le, Jennifer ^a   Umiel, Tehila ^a   Michl, Patrick ^a   Said, Johnathan W ^a   Binderup, Lise ^b   Reed, John C ^c   Koeffler, H Phillip ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LEO PHARMA A S   (Denmark)

^c BURNHAM INSTITUTE   (United States)

Author keywords

acute promyelocytic leukemia; retinoid (9 cis retinoic acid); vitamin D3 analog (KH 1060)

Indexed keywords

ALITRETINOIN; CALCITRIOL; COLECALCIFEROL; LEXACALCITOL; SR 11236; SR 11238; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; DATA ANALYSIS; GRANULOCYTE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LIGAND BINDING; MONOCYTE; PHENOTYPE; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; RELAPSE;

EID: 0031036661     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119164     Document Type: Article

References (73)

1. Warrell, R.P., Jr. 1993. Retinoid resistance in acute promyelocytic leukemia: new mechanisms, strategies, and implications. Blood. 82:1949-1953.
2. Raza, A., Y. Maheshwari, and H.D. Preisler. 1987. Differences in cell cycle characteristics among patients with nonlymphocytic leukemia. Blood. 69: 1637-1653.
3. Raza, A., N. Yousuf, A. Abbas, A. Umerani, A. Mehdi, S.A.J. Bokhari, Y. Sheikh, K. Qadir, J. Freeman, M. Masterson, et al. 1992. High expression of transforming growth factor β, long cycle times and a unique clustering of S-phase cells in patients with acute promyelocitic leukemia. Blood. 79:1037-1048.
4. 3-induced differentiation and increases proliferation and survival of cells in low serum concentration. Cell. 74:423-431.
5. Fagioli, M., F. Grignani, P.F. Ferrucci, M. Alcallay, A. Mencarelli, I. Nicoletti, and G. Pelicci. 1994. Effect of the acute promyelocytic leukemia PML/RARα protein on differentiation and survival of myeloid precursors. Leukemia (Baltimore). 8(Suppl. 1):S7-11.
6. Marx, J. 1993. Cell death studies yield cancer clues. Science (Wash. DC). 259:760-761.
7. Wyllie, A.H., J.F.R. Kerr, and A.R. Currie. 1980. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:251-306.
8. Hockenbery, D., G. Nufiez, C. Milliman, R.D. Schreiber, and S.J. Korsmeyer. 1990. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature (Lond.). 348:334-339.
9. Vaux, D.L., S. Cory, and J.M. Adams. 1988. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B-cells. Nature (Lond.). 335:440-446.
10. Oltvai, Z., C. Milliman, and S.J. Korsmeyer. 1993. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax that accelerates programmed cell death. Cell. 74:609-619.
11. Heyman, R., D. Mangelsdorf, J. Dyck, R.B. Stein, G. Eichele, and R.M. Evans. 1992. 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell. 68:397-406.
12. Levin, A., L. Strzenbecker, S. Kazmer, T. Bosakowski, C. Huselton, G. Allenby, J. Speck, C. Kratzeisen, M. Rosenberger, A. Lovey, and J.F. Grippo. 1992. 9-cis retinoic acid stereoisomer binds and activates the nuclear receptor RXR-α. Nature (Lond.). 335:359-361.
13. Kizaki, M., Y. Ikeda, R. Tanosaki, H. Nikajama, M. Morikawa, A. Sakashita, and H.P. Koeffler. 1993. Effects of novel retinoic acid compound, 9-cis-retinoic acid, on proliferation, differentiation and expression of retinoic acid receptor RNA by HL-60 cells. Blood. 83:3592-3599.
14. Sakashita, A., M. Kizaki, S. Pakkala, G. Schiller, N. Tsuroka, R. Tomosaki, J.F. Cameron, M.I. Dawson, and H.P. Koeffler. 1993. 9-cis-retinoic acid: effects on normal and leukemic hematopoiesis in vitro. Blood. 81:1009-1016.
15. Miller, W.H., Jr., A. Jakubowski, W.P. Tong, V.A. Miller, J.R. Rigas, F. Benedetti, G.M. Gill, J.A. Truglia, E. Ulm, M. Shirley, and R.P. Warrell, Jr. 1995. 9-cis retinoic acid induces complete remission but does not reverse clinically acquired retinoid resistance in acute promyelocytic leukemia. Blood. 85: 3021-3027.
16. Baker, A.R., D.P. McDonnell, M. Hughes, T.M. Crisp, D.J. Mangelsdorf, M.R. Haussler, J.W. Pike, J. Shine, and B.W. O'Malley. 1988. Cloning and expression of full-length cDNA encoding human vitamin D receptor. Proc. Natl. Acad. Sci. USA. 85:3294-3298.
17. 3 response element. Leuk. Res. 19:147-158.
18. Carlberg, C., I. Bendik, A. Wyss, E. Meier, L.J. Sturzenbecker, J.F. Grippo, and W. Hunziker. 1993. Two nuclear signaling pathways for vitamin D. Nature (Lond.). 361:657-660.
19. Schräder, M., I. Bendik, M. Becker-André, and C. Carlberg. 1993. Interaction between retinoic acid and vitamin D signaling pathways. J. Biol. Chem. 268:17830-17836.
20. Schräder, M., K.M. Müller, and C. Carlberg. 1994. Specificity and flexibility of vitamin D signaling. J. Biol. Chem. 269:5501-5505.
21. 3: in vivo and in vitro effects on human preleukemic and leukemic cells. Cancer Treat. Rep. 69:1399-1407.
22. Bar-Shavit, Z., A.J. Kahn, K.R. Stone, J. Trial, T. Hilliard, P. Reitsma, and S.L. Teitelbaum. 1986. Reversibility of vitamin D-induced human leukemia cell maturation. Endocrinology. 118:679-686.
23. Studzinski, G.P., and Z.S. Brelvi. 1987. Changes in proto-oncogene expression associated with reversal of macrophage-like differentiation of HL-60 cells. J. Natl. Cancer Inst. (Bethesda). 79:67-76.
24. 3 analogues: a novel class of potent regulators of cell growth and immune responses. Biochem. Pharmac. 42:1569-1575.
25. 3: an extraordinarily potent inhibitor of leukemic cell growth in vitro. Blood. 84:1960-1968.
26. 3 analog (KH 1060) and 9-cis-retinoic acid inhibits irreversibly clonal growth, decreases bcl-2 expression and induces apoptosis in HL-60 leukemic cells. Cancer Res. 56:3570-3576.
27. 3 analogs: a novel class of potent inhibitors of proliferation and inducers of differentiation of human breast cancer cell lines. Cancer Res. 55:2822-2830.
28. 3 analogs potently affect prostate cancer cells. Proc. Am. Assoc. Cancer Res. 37:387. (Abstr. 2640).
29. 3 analogs on clonal proliferation of human prostate cancer cell lines. Prostate. In press.
30. Lennon, S.V., S.J. Martin, and T.G. Cotter. 1991. Dose-dependent induction of apoptosis in human tumor cell lines by widely diverging stimuli. Cell Prolif. 24:203-214.
31. Martin, S.J., and D.R. Green. 1994. Apoptosis as a goal of cancer therapy. Curr. Opin. Oncol. 6:616-621.
32. Nagy, L., V. Thomázy, P. Syka, R. Heyman, R. Chandraratna, and P. Davies. 1995. Activation of retinoid X receptors induces apoptosis in HL-60 cell lines. Mol. Cell. Biol. 15:3540-3551.
33. Mehta, K., T. McQueen, N. Neamati, S. Collins, and M. Andreeff. 1996. Activation of retinoid receptors RARα and RXRα induces differentiation and apoptosis, respectively, in HL-60 cells. Cell Growth Differ. 7:179-186.
34. Lanotte, M., V. Martin-Thouvenin, S. Najman, P. Ballerini, F. Valensi, and R. Berger. 1991. NB4, a maturation inducible cell line with t(15,17) marker isolated from a human acute promyelocytic leukemia (M3). Blood. 77:1080-1086.
35. Collins, S.J., F.W. Ruscetti, R.E. Gallagher, and R.C. Gallo. 1979. Normal functional characteristics of cultured human promyelocytic leukemia cells (HL-60) after induction of differentiation by dimethylsulfoxide. J. Exp. Med. 149:969-974.
36. Munker, R., A.W. Norman, and H.P. Koeffler. 1986. Vitamin D compounds. Effects on clonal proliferation and differentiation of human myeloid cells. J. Clin. Invest. 87:424-430.
37. Sellins, K.S., and J.J. Cohen. 1987. Gene induction by gamma-irradiation leads to DNA fragmentation in lymphocytes. J. Immunology. 139:3199-3206.
38. Krajewski, S., C. Blomqvist, K. Franssila, M. Krajewska, V.M. Wasenius, E. Niskanen, S. Nordling, and J.C. Reed. 1995. Reduced expression of proapoptotic gene BAX is associated with poor response rates to combination chemotherapy and shorter survival in women with metastatic breast adenocarcinoma. Cancer Res. 55:4471-4478.
39. Delia, D., A. Aiello, D. Soligo, E. Fontanella, C. Melani, F. Pezzella, M.A. Pierotti, and G.D. Pota. 1992. bcl-2 proto-oncogene expression in normal and neoplastic human myeloid cells. Blood. 79:1291-1298.
40. Lagasse, E., and I.L. Weissman. 1994. bcl-2 inhibits apoptosis of neutrophils but not their engulfment by macrophages. J. Exp. Med. 179:1047-1052.
41. Selsted, M.E., C.W. Miller, M.J. Novotny, W.L. Morris, and H.P. Koeffler. 1993. Molecular analysis of myeloperoxidase deficiency shows heterogeneous patterns of the complete deficiency state manifested at the genomic, mRNA, and protein level. Blood. 82:1317-1322.
42. Territo, M.C., and M.J. Cline. 1977. Monocyte function in man. J. Immunol. 118:187-192.
43. Berenbaum, M.C. 1989. What is synergy? Pharmacol. Rev. 41:93-141.
44. Chen, Z.X., and T.R. Breitman. 1994. Tributyrin: a prodrug of butyric acid for potential clinical application in differentiation therapy. Cancer Res. 54: 3494-3499.
45. Lübbert, M., F. Herrmann, and H.P. Koeffler. 1991. Expression and regulation of myeloid-specific genes in normal and leukemic myeloid cells. Blood. 77:909-924.
46. Koeffler, H.P., J. Ranyard, L. Yelton, R. Billing, and R. Bohman. 1984. γ-Interferon induced expression of the HLA-D antigens on normal and leukemic human myeloid cells. Proc. Natl. Acad. Sci. USA. 81:4080-4084.
47. Koeffler, H.P. 1983. Study of normal and abnormal hematopoiesis using human leukemic cell lines. UCLA Symposium on Molecular and Cellular Biology. New series. Alan R. Liss Inc., New York. 19:179-195.
48. Warrell, R.P., Jr., H. de Thé, Z.Y. Wang, and L. Degos. 1993. Acute promyelocytic leukemia. N. Engl. J. Med. 329:177-189.
49. Midland, M.M., Y. Plumet, and W.H. Okamura. 1993. Effect of C20 stereochemistry on the conformational profile of the side chains of vitamin D analogs. Bioorg. Med. Chem. Lett. 3:1799-1804.
50. de Thé, H., A. Marachio, P. Tiollais, and A. Dejean. 1989. Differential expression and ligand regulation of the retinoic acid receptor α and β genes. EMBO (Eur. Mol. Biol. Organ.) J. 8:429-433.
51. Hoshimoto, Y., H. Kagechika, and K. Shudo. 1990. Expression of retinoic acid receptor genes and ligand-binding selectivity of retinoic acid receptors (RARs). Biochem. Biophys. Res. Commun. 166:1300-1307.
52. Kastner, P., A. Perez, Y. Lutz, C. Rochette-Egly, M.-P. Gaub, R. Berger, and P. Chambon. 1992. Structure, localization and transcriptional properties of two classes of retinoic acid receptor a fusion proteins in acute promyelocytic leukemia (APL): structural similarities with a new family of oncoproteins. EMBO (Eur. Mol. Biol. Organ.) J. 11:629-635.
53. Weis, K., S. Rambaud, C. Lavau, J. Jansen, T. Carvalho, M. Carmo-Fonseca, A. Lamond, and A. Dejean. 1994. Retinoic acid regulates aberrant nuclear localization of PML-RARα in acute promyelocytic leukemia cells. Cell. 76:345-356.
54. Perez, A., P. Kastner, S. Sethi, Y. Lutz, C. Reibel, and P. Chambon. 1993. PML/RAR homodimers: distinct DNA binding properties and heteromeric interactions with RXR. EMBO (Eur. Mol. Biol. Organ.) J. 12:3117-3182.
55. 3 (VD) analog MC903, EB1089 and KH1060 activate the VD receptor: homodimers show higher ligand sensitivity than heterodimers with retinoid X receptors. J. Steroid. Biochem. Mol. Biol. 51:137-142.
56. 3 are associated with enhanced activation of the vitamin D receptor. J. Biol. Chem. 270:3-8.
57. Dawson, M.I., E. Elstner, D. Chen, B. Kerner, and H.P. Koeffler. 1994. Myeloid differentiation mediated through RAR/RXR not RXR/RXR pathway. Blood. 84:446-452.
58. Kizaki, M., M.I. Dawson, R. Heyman, E. Elstner, R. Marosetti, S. Pakkala, D.L. Chen, H. Ueno, M. Morikawaq, Y. Ikeda, et al. 1996. Effects of novel retinoic X receptor (RXR) specific ligands on myeloid leukemic differentiation and proliferation in vitro. Blood. 89:1977-1984.
59. Fanjul, A., M.L. Dawson, P.D. Hobbs, L. Jong, J.F. Cameron, E. Harley, G. Graupner, X.P. Lu, and M. Pfahl. 1994. A new class of retinoids with selective inhibition of AP-1 inhibits proliferation. Nature (Lond.). 372:107-110.
60. de Vos, S., M.I. Dawson, S. Holden, T. Le, A. Wang, S.K. Cho, K.L. Chen, and H.P. Koeffler. 1997. Effects of novel, potent retinoid X receptor (RXR) specific ligands and ligands with anti-AP-1 activity on proliferation of prostate cancer cells. Prostate. In press.
61. Gianni, M., M. Terao, S. Zanotta, T. Barbui, A. Rambaldi, and E. Garattini. 1994. Retinoic acid and granulocyte colony-stimulating factor synergistically induce leukocyte alkaline phosphatase in acute promyelocytic leukemia cells. Blood. 83:1909-1921,
62. 3 retinoic acid and DMSO. Leuk. Res. 19:57-64.
63. Todd, R.F., L.M. Nadler, and S.F. Schlossman. 1981. Antigens on human monocytes identified by monoclonal antibodies. J. Immunol. 126:1435-1442.
64. Todd, R., and S.F. Schlossmann. 1982. Analysis of antigenic determinants on human monocytes and macrophages. Blood. 59:775-780.
65. Wright, S.D., R.A. Ramos, P.S. Tobias, R.J. Ulevitch, and J.C. Mathison. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science (Wash. DC). 249:1431-1433.
66. Carlos, T.M., and J.M. Harlan. 1994. Leukocyte-endothelial adhesion molecules. Blood. 84:2068-2101.
67. Amatruda, T.A., R. Bohman, J. Ranyard, and H.P. Koeffler. 1987. Pattern of expression of HLA-DR and HLA-DQ antigens and mRNA in myeloid differentiation. Blood. 69:1225-1236.
68. Hu, Z.B., W. Ma, C.C. Uphoff, M. Lanotte, and H.G. Drexler. 1993. Modulation of gene expression in the acute promyelocytic leukemia cell line NB4. Leukemia (Baltimore). 7:1817-1823.
69. Khanna-Gupta, A., K. Kolibaba, T. Zibello, and N. Berliner. 1994. NB4 cells show bilineage potential and an aberrant pattern of neutrophil secondary granule protein gene expression. Blood. 84:294-302.
70. Ruchaud, S., E. Duprez, M.C. Gendron, G. Houge, H.G. Genieser, B. Jastoff, S.O. Doskeland, and M. Lanotte. 1994. Two distinctly regulated events, priming and triggering, during retinoid-induced maturation and resistance of NB4 promyelocytic leukemia cell line. Proc. Natl. Acad. Sci. USA. 91:8428.
71. Hockenbery, D.M. 1992. The bcl-2 oncogene and apoptosis. Semin. Immunol. 4:413-420.
72. McDonnell, T.J., N. Deane, F.M. Platt, G. Nufiez, U. Jaeger, J.P. McKearn, and S.J. Korsmeyer. 1989. Bcl-2 immunoglobin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell. 57:79-88.
73. Martin, S.J., J.G. Bradley, and T.G. Cotter. 1990. HL-60 cells induced to differentiation towards neutrophils subsequently die via apoptosis. Clin. Exp. Immunol. 79:448-453.