All-trans retinoic acid activity in acute myeloid leukemia: Role of cytochrome P450 enzyme expression by the microenvironment

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Su, Meng ^a   Alonso, Salvador ^a   Jones, Jace W ^b   Yu, Jianshi ^b   Kane, Maureen A ^b   Jones, Richard J ^a   Ghiaur, Gabriel ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450 26A1; RETINOIC ACID; ANTINEOPLASTIC AGENT; CD34 ANTIGEN; CD38 ANTIGEN; CYTOCHROME P450; CYTOCHROME P450 FAMILY 26;

ACUTE MYELOBLASTIC LEUKEMIA; ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BONE MARROW STROMA CELL; CANCER REGRESSION; CANCER STEM CELL; CELL DIFFERENTIATION; CELL FATE; CHEMOSENSITIVITY; COLONY FORMING UNIT C; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HEMATOPOIETIC STEM CELL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TANDEM MASS SPECTROMETRY; TUMOR MICROENVIRONMENT; BONE MARROW CELL; CELL CULTURE; COCULTURE; CYTOLOGY; DRUG EFFECTS; LEUKEMIA, MYELOID, ACUTE; METABOLISM; PATHOLOGY;

ANTIGENS, CD34; ANTIGENS, CD38; ANTINEOPLASTIC AGENTS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOCHROME P-450 ENZYME SYSTEM; HUMANS; LEUKEMIA, MYELOID, ACUTE; NEOPLASTIC STEM CELLS; RETINOIC ACID 4-HYDROXYLASE; TRETINOIN;

EID: 84935021347     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0127790     Document Type: Article

References (48)

1. Estey E, Dohner H. Acute myeloid leukaemia. Lancet. 2006; 368(9550):1894-907. Epub 2006/11/28. doi: S0140-6736(06)69780-8 [pii] doi: 10.1016/S0140-6736(06)69780-8 PMID: 17126723.
2. Dos Santos GA, Kats L, Pandolfi PP. Synergy against PML-RARa: targeting transcription, proteolysis, differentiation, and self-renewal in acute promyelocytic leukemia. The Journal of experimental medicine. 2013; 210(13):2793-802. doi: 10.1084/jem.20131121 PMID: 24344243; PubMed Central PMCID: PMC3865469.
3. Wang ZY, Chen Z. Acute promyelocytic leukemia: from highly fatal to highly curable. Blood. 2008; 111 (5):2505-15. Epub 2008/02/27. doi: 111/5/2505 [pii] doi: 10.1182/blood-2007-07-102798 PMID: 18299451.
4. Rice AM, Holtz KM, Karp J, Rollins S, Sartorelli AC. Analysis of the relationship between Scl transcription factor complex protein expression patterns and the effects of LiCl on ATRA-induced differentiation in blast cells from patients with acute myeloid leukemia. Leukemia research. 2004; 28(11):1227-37. doi: 10.1016/j.leukres.2004.03.017 PMID: 15380350.
5. Petrie K, Zelent A, Waxman S. Differentiation therapy of acute myeloid leukemia: past, present and future. Current opinion in hematology. 2009; 16(2):84-91. doi: 10.1097/MOH.0b013e3283257aee PMID: 19468269.
6. Bullinger L, Schlenk RF, Gotz M, Botzenhardt U, Hofmann S, Russ AC, et al. PRAME-induced inhibition of retinoic acid receptor signaling-mediated differentiation-a possible target for ATRA response in AML without t(15;17). Clinical cancer research: an official journal of the American Association for Cancer Research. 2013; 19(9):2562-71. doi: 10.1158/1078-0432.CCR-11-2524 PMID: 23444226.
7. Altucci L, Gronemeyer H. The promise of retinoids to fight against cancer. Nature reviews Cancer. 2001; 1(3):181-93. doi: 10.1038/35106036 PMID: 11902573.
8. Seiter K, Feldman EJ, Dorota Halicka H, Deptala A, Traganos F, Burke HB, et al. Clinical and laboratory evaluation of all-trans retinoic acid modulation of chemotherapy in patients with acute myelogenous leukaemia. British journal of haematology. 2000; 108(1):40-7. PMID: 10651722.
9. Sakashita A, Kizaki M, Pakkala S, Schiller G, Tsuruoka N, Tomosaki R, et al. 9-cis-retinoic acid: effects on normal and leukemic hematopoiesis in vitro. Blood. 1993; 81(4):1009-16. PMID: 8427982.
10. Sakamoto K, Imamura T, Yano M, Yoshida H, Fujiki A, Hirashima Y, et al. Sensitivity of MLL-rearranged AML cells to all-trans retinoic acid is associated with the level of H3K4me2 in the RARalpha promoter region. Blood cancer journal. 2014; 4:e205. doi: 10.1038/bcj.2014.25 PMID: 24769646; PubMed Central PMCID: PMC4003419.
11. Lehmann S, Paul C, Torma H. The expression of cellular retinoid binding proteins in non-APL leukemic cells and its association with retinoid sensitivity. Leukemia & lymphoma. 2002; 43(4):851-8. doi: 10.1080/10428190290016999 PMID: 12153175.
12. Lehmann S, Bengtzen S, Broberg U, Paul C. Effects of retinoids on cell toxicity and apoptosis in leukemic blast cells from patients with non-M3 AML. Leukemia research. 2000; 24(1):19-25. PMID: 10634641.
13. Venditti A, Stasi R, Del Poeta G, Buccisano F, Aronica G, Bruno A, et al. All-trans retinoic acid and low-dose cytosine arabinoside for the treatment of 'poor prognosis' acute myeloid leukemia. Leukemia. 1995; 9(7):1121-5. PMID: 7630182.
14. Schlenk RF, Frohling S, Hartmann F, Fischer JT, Glasmacher A, del Valle F, et al. Phase III study of alltrans retinoic acid in previously untreated patients 61 years or older with acute myeloid leukemia. Leukemia. 2004; 18(11):1798-803. doi: 10.1038/sj.leu.2403528 PMID: 15385923.
15. Schlenk RF, Dohner K, Kneba M, Gotze K, Hartmann F, Del Valle F, et al. Gene mutations and response to treatment with all-trans retinoic acid in elderly patients with acute myeloid leukemia. Results from the AMLSG Trial AML HD98B. Haematologica. 2009; 94(1):54-60. doi: 10.3324/haematol.13378 PMID: 19059939; PubMed Central PMCID: PMC2625424.
16. Milligan DW, Wheatley K, Littlewood T, Craig JI, Burnett AK, Group NHOCS. Fludarabine and cytosine are less effective than standard ADE chemotherapy in high-risk acute myeloid leukemia, and addition of G-CSF and ATRA are not beneficial: results of the MRC AML-HR randomized trial. Blood. 2006; 107 (12):4614-22. doi: 10.1182/blood-2005-10-4202 PMID: 16484584.
17. Estey EH, Thall PF, Pierce S, Cortes J, Beran M, Kantarjian H, et al. Randomized phase II study of fludarabine + cytosine arabinoside + idarubicin +/- all-trans retinoic acid +/- granulocyte colony-stimulating factor in poor prognosis newly diagnosed acute myeloid leukemia and myelodysplastic syndrome. Blood. 1999; 93(8):2478-84. PMID: 10194425.
18. Burnett AK, Milligan D, Prentice AG, Goldstone AH, McMullin MF, Hills RK, et al. A comparison of low-dose cytarabine and hydroxyurea with or without all-trans retinoic acid for acute myeloid leukemia and high-risk myelodysplastic syndrome in patients not considered fit for intensive treatment. Cancer. 2007; 109(6):1114-24. doi: 10.1002/cncr.22496 PMID: 17315155.
19. Warrell RP, Frankel SR, Miller WH, Scheinberg DA, Itri LM, Hittelman WN, et al. Differentiation Therapy of Acute Promyelocytic Leukemia with Tretinoin (All-trans-Retinoic Acid). New England Journal of Medicine. 1991; 324(20):1385-93. doi: 10.1056/NEJM199105163242002 PMID: 1850498.
20. Wang ZY, Sun GL, Lu JX, Gu LJ, Huang ME, Chen SR. Treatment of acute promyelocytic leukemia with all-trans retinoic acid in China. Nouvelle revue francaise d'hematologie. 1990; 32(1):34-6. PMID: 2349080.
21. Lo-Coco F, Avvisati G, Vignetti M, Thiede C, Orlando SM, Iacobelli S, et al. Retinoic acid and arsenic trioxide for acute promyelocytic leukemia. The New England journal of medicine. 2013; 369(2):111-21. doi: 10.1056/NEJMoa1300874 PMID: 23841729.
22. Theodosiou M, Laudet V, Schubert M. From carrot to clinic: an overview of the retinoic acid signaling pathway. Cellular and molecular life sciences: CMLS. 2010; 67(9):1423-45. Epub 2010/02/09. doi: 10.1007/s00018-010-0268-z PMID: 20140749.
23. Ray WJ, Bain G, Yao M, Gottlieb DI. CYP26, a novel mammalian cytochrome P450, is induced by retinoic acid and defines a new family. The Journal of biological chemistry. 1997; 272(30):18702-8. PMID: 9228041.
24. Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, et al. Retinoid signaling determines germ cell fate in mice. Science. 2006; 312(5773):596-600. doi: 10.1126/science.1125691 PMID: 16574820.
25. Ghiaur G, Yegnasubramanian S, Perkins B, Gucwa JL, Gerber JM, Jones RJ. Regulation of human hematopoietic stem cell self-renewal by the microenvironment's control of retinoic acid signaling. Proceedings of the National Academy of Sciences of the United States of America. 2013. doi: 10.1073/pnas.1305937110 PMID: 24043786.
26. Lanotte M, Martin-Thouvenin V, Najman S, Balerini P, Valensi F, Berger R. NB4, a maturation inducible cell line with t(15;17) marker isolated from a human acute promyelocytic leukemia (M3). Blood. 1991; 77(5):1080-6. PMID: 1995093.
27. Asou H, Tashiro S, Hamamoto K, Otsuji A, Kita K, Kamada N. Establishment of a human acute myeloid leukemia cell line (Kasumi-1) with 8;21 chromosome translocation. Blood. 1991; 77(9):2031-6. PMID: 2018839.
28. Gerber JM, Smith BD, Ngwang B, Zhang H, Vala MS, Morsberger L, et al. A clinically relevant population of leukemic CD34(+)CD38(-) cells in acute myeloid leukemia. Blood. 2012; 119(15):3571-7. Epub 2012/01/21. doi: blood-2011-06-364182 [pii] doi: 10.1182/blood-2011-06-364182 PMID: 22262762; PubMed Central PMCID: PMC3325044.
29. Breems DA, Blokland EA, Neben S, Ploemacher RE. Frequency analysis of human primitive haematopoietic stem cell subsets using a cobblestone area forming cell assay. Leukemia. 1994; 8(7):1095-104. PMID: 8035601.
30. Matsui WH, Gladstone DE, Vala MS, Barber JP, Brodsky RA, Smith BD, et al. The role of growth factors in the activity of pharmacological differentiation agents. Cell growth & differentiation: the molecular biology journal of the American Association for Cancer Research. 2002; 13(6):275-83. PMID: 12114217.
31. Bedi A, Barber JP, Bedi GC, el-Deiry WS, Sidransky D, Vala MS, et al. BCR-ABL-mediated inhibition of apoptosis with delay of G2/M transition after DNA damage: a mechanism of resistance to multiple anticancer agents. Blood. 1995; 86(3):1148-58. PMID: 7620167.
32. Kane MA, Napoli JL. Quantification of endogenous retinoids. Methods in molecular biology. 2010; 652:1-54. doi: 10.1007/978-1-60327-325-1-1 PMID: 20552420; PubMed Central PMCID: PMC4113000.
33. Kane MA, Folias AE, Wang C, Napoli JL. Quantitative profiling of endogenous retinoic acid in vivo and in vitro by tandem mass spectrometry. Analytical chemistry. 2008; 80(5):1702-8. doi: 10.1021/ac702030f PMID: 18251521; PubMed Central PMCID: PMC4086453.
34. Williams JB, Napoli JL. Metabolism of retinoic acid and retinol during differentiation of F9 embryonal carcinoma cells. Proceedings of the National Academy of Sciences of the United States of America. 1985; 82(14):4658-62. PMID: 3860815; PubMed Central PMCID: PMC390445.
35. Manfredini R, Trevisan F, Grande A, Tagliafico E, Montanari M, Lemoli R, et al. Induction of a functional vitamin D receptor in all-trans-retinoic acid-induced monocytic differentiation of M2-type leukemic blast cells. Cancer research. 1999; 59(15):3803-11. PMID: 10446999.
36. Balusu R, Fiskus W, Rao R, Chong DG, Nalluri S, Mudunuru U, et al. Targeting levels or oligomerization of nucleophosmin 1 induces differentiation and loss of survival of human AML cells with mutant NPM1. Blood. 2011; 118(11):3096-106. doi: 10.1182/blood-2010-09-309674 PMID: 21719597.
37. Nazha A, Bueso-Ramos C, Estey E, Faderl S, O'Brien S, Fernandez MH, et al. The Addition of All-Trans Retinoic Acid to Chemotherapy May Not Improve the Outcome of Patient with NPM1 Mutated Acute Myeloid Leukemia. Frontiers in oncology. 2013; 3:218. doi: 10.3389/fonc.2013.00218 PMID: 24032106; PubMed Central PMCID: PMC3764477.
38. Burnett AK, Hills RK, Green C, Jenkinson S, Koo K, Patel Y, et al. The impact on outcome of the addition of all-trans retinoic acid to intensive chemotherapy in younger patients with nonacute promyelocytic acute myeloid leukemia: overall results and results in genotypic subgroups defined by mutations in NPM1, FLT3, and CEBPA. Blood. 2010; 115(5):948-56. doi: 10.1182/blood-2009-08-236588 PMID: 19965647.
39. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994; 367(6464):645-8. Epub 1994/02/17. doi: 10.1038/367645a0 PMID: 7509044.
40. Eckhoff C, Collins MD, Nau H. Human plasma all-trans-, 13-cis- and 13-cis-4-oxoretinoic acid profiles during subchronic vitamin A supplementation: comparison to retinol and retinyl ester plasma levels. J Nutr. 1991; 121(7):1016-25. Epub 1991/07/01. PMID: 2051220.
41. Ryningen A, Stapnes C, Paulsen K, Lassalle P, Gjertsen BT, Bruserud O. In vivo biological effects of ATRA in the treatment of AML. Expert opinion on investigational drugs. 2008; 17(11):1623-33. doi: 10.1517/13543784.17.11.1623 PMID: 18922099.
42. Wang Y, Zolfaghari R, Ross AC. Cloning of rat cytochrome P450RAI (CYP26) cDNA and regulation of its gene expression by all-trans-retinoic acid in vivo. Archives of biochemistry and biophysics. 2002; 401(2):235-43. doi: 10.1016/S0003-9861(02)00043-7 PMID: 12054474.
43. Ozpolat B, Mehta K, Lopez-Berestein G. Regulation of a highly specific retinoic acid-4-hydroxylase (CYP26A1) enzyme and all-trans-retinoic acid metabolism in human intestinal, liver, endothelial, and acute promyelocytic leukemia cells. Leukemia & lymphoma. 2005; 46(10):1497-506. doi: 10.1080/10428190500174737 PMID: 16194896.
44. Adamson PC, Reaman G, Finklestein JZ, Feusner J, Berg SL, Blaney SM, et al. Phase I trial and pharmacokinetic study of all-trans-retinoic acid administered on an intermittent schedule in combination with interferon-alpha2a in pediatric patients with refractory cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 1997; 15(11):3330-7. PMID: 9363862.
45. Turhan AG, Lemoine FM, Debert C, Bonnet ML, Baillou C, Picard F, et al. Highly purified primitive hematopoietic stem cells are PML-RARA negative and generate nonclonal progenitors in acute promyelocytic leukemia. Blood. 1995; 85(8):2154-61. PMID: 7536493.
46. Geria AN, Scheinfeld NS. Talarozole, a selective inhibitor of P450-mediated all-trans retinoic acid for the treatment of psoriasis and acne. Current opinion in investigational drugs. 2008; 9(11):1228-37. PMID: 18951302.
47. Tobita T, Takeshita A, Kitamura K, Ohnishi K, Yanagi M, Hiraoka A, et al. Treatment with a new synthetic retinoid, Am80, of acute promyelocytic leukemia relapsed from complete remission induced by alltrans retinoic acid. Blood. 1997; 90(3):967-73. PMID: 9242525.
48. Osanai M, Petkovich M. Expression of the retinoic acid-metabolizing enzyme CYP26A1 limits programmed cell death. Molecular pharmacology. 2005; 67(5):1808-17. doi: 10.1124/mol.104.005769 PMID: 15703382.