AKR1C3 is a biomarker of sensitivity to PR-104 in preclinical models of T-cell acute lymphoblastic leukemia

Blood

Volumn 126, Issue 10, 2015, Pages 1193-1202

  Manesh, Donya Moradi ^a   El Hoss, Jad ^a   Evans, Kathryn ^a   Richmond, Jennifer ^a   Toscan, Cara E ^a   Bracken, Lauryn S ^a   Hedrick, Ashlee ^a   Sutton, Rosemary ^a   Marshall, Glenn M ^b   Wilson, William R ^c   Kurmasheva, Raushan T ^d   Billups, Catherine ^e   Houghton, Peter J ^d   Smith, Malcolm A ^f   Carol, Hernan ^a   Lock, Richard B ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b SYDNEY CHILDREN'S HOSPITAL   (Australia)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

^d NATIONWIDE CHILDREN S HOSPITAL   (United States)

^e ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^f NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDO KETO REDUCTASE 1C3; ANTINEOPLASTIC AGENT; ASPARAGINASE; BIOLOGICAL MARKER; DEXAMETHASONE; OXIDOREDUCTASE; PR 104; PR 104A; PRODRUG; UNCLASSIFIED DRUG; VINCRISTINE; 15 HYDROXYPROSTAGLANDIN DEHYDROGENASE; 3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; AKR1C3 PROTEIN, HUMAN; CHLORMETHINE DERIVATIVE; PR-104A; TUMOR MARKER;

ACUTE LYMPHOBLASTIC LEUKEMIA; ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CHILD; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; ANIMAL; BIOSYNTHESIS; CELL SURVIVAL; DRUG EFFECTS; DRUG SCREENING; IMMUNOBLOTTING; METABOLISM; PATHOLOGY; PRESCHOOL CHILD; REAL TIME POLYMERASE CHAIN REACTION;

3-HYDROXYSTEROID DEHYDROGENASES; ADOLESCENT; ANIMALS; ANTINEOPLASTIC AGENTS; BIOMARKERS, TUMOR; CELL SURVIVAL; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; HYDROXYPROSTAGLANDIN DEHYDROGENASES; IMMUNOBLOTTING; MALE; MICE; NITROGEN MUSTARD COMPOUNDS; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; REAL-TIME POLYMERASE CHAIN REACTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84942518612     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-12-618900     Document Type: Article

References (47)

1. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2008. CA Cancer J Clin. 2008;58(2):71-96.
2. Pui CH, Evans WE. Treatment of acute lymphoblastic leukemia. N Engl J Med. 2006;354(2):166-178.
3. Graux C. Biology of acute lymphoblastic leukemia (ALL): clinical and therapeutic relevance. Transfus Apheresis Sci. 2011;44(2):183-189.
4. Smith MA, Altekruse SF, Adamson PC, Reaman GH, Seibel NL. Declining childhood and adolescent cancer mortality. Cancer. 2014;120(16):2497-2506.
5. Goldberg JM, Silverman LB, Levy DE, et al. Childhood T-cell acute lymphoblastic leukemia: the Dana-Farber Cancer Institute acute lymphoblastic leukemia consortium experience. J Clin Oncol. 2003;21(19):3616-3622.
6. Van Vlierberghe P, Ferrando A. The molecular basis of T cell acute lymphoblastic leukemia. J Clin Invest. 2012;122(10):3398-3406.
7. Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci USA. 2007;104(13):5431-5436.
8. Winkler IG, Barbier V, Wadley R, Zannettino AC, Williams S, Lévesque JP. Positioning of bone marrow hematopoietic and stromal cells relative to blood flow in vivo: serially reconstituting hematopoietic stem cells reside in distinct nonperfused niches. Blood. 2010;116(3):375-385.
9. Chow DC, Wenning LA, Miller WM, Papoutsakis ET. Modeling pO(2) distributions in the bone marrow hematopoietic compartment. II. Modified Kroghian models. Biophys J. 2001;81(2):685-696.
10. Morrison SJ, Scadden DT. The bone marrow niche for haematopoietic stem cells. Nature. 2014;505(7483):327-334.
11. Giuntoli S, Rovida E, Gozzini A, et al. Severe hypoxia defines heterogeneity and selects highly immature progenitors within clonal erythroleukemia cells. Stem Cells. 2007;25(5):1119-1125.
12. Eliasson P, Jönsson JI. The hematopoietic stem cell niche: low in oxygen but a nice place to be. J Cell Physiol. 2010;222(1):17-22.
13. Frolova O, Samudio I, Benito JM, et al. Regulation of HIF-1α signaling and chemoresistance in acute lymphocytic leukemia under hypoxic conditions of the bone marrow microenvironment. Cancer Biol Ther. 2012;13(10):858-870.
14. Matsunaga T, Imataki O, Torii E, et al. Elevated HIF-1α expression of acute myelogenous leukemia stem cells in the endosteal hypoxic zone may be a cause of minimal residual disease in bone marrow after chemotherapy. Leuk Res. 2012;36(6):e122-e124.
15. Guise CP, Mowday AM, Ashoorzadeh A, et al. Bioreductive prodrugs as cancer therapeutics: targeting tumor hypoxia. Chin J Cancer. 2014;33(2):80-86.
16. Weiss GJ, Infante JR, Chiorean EG, et al. Phase 1 study of the safety, tolerability, and pharmacokinetics of TH-302, a hypoxia-activated prodrug, in patients with advanced solid malignancies. Clin Cancer Res. 2011;17(9):2997-3004.
17. Ganjoo KN, Cranmer LD, Butrynski JE, et al. A phase I study of the safety and pharmacokinetics of the hypoxia-activated prodrug TH-302 in combination with doxorubicin in patients with advanced soft tissue sarcoma. Oncology. 2011;80(1-2):50-56.
18. Patterson AV, Ferry DM, Edmunds SJ, et al. Mechanism of action and preclinical antitumor activity of the novel hypoxia-activated DNA cross-linking agent PR-104. Clin Cancer Res. 2007;13(13):3922-3932.
19. Konopleva M, Thall PF, Arana Yi C, et al. Phase I/II study of the hypoxia-activated prodrug PR104 in refractory/relapsed acute myeloid leukemia and acute lymphoblastic leukemia. Haematologica. 2015;100:927-934.
20. Guise CP, Abbattista MR, Tipparaju SR, et al. Diflavin oxidoreductases activate the bioreductive prodrug PR-104A under hypoxia. Mol Pharmacol. 2012;81(1):31-40.
21. Guise CP, Abbattista MR, Singleton RS, et al. The bioreductive prodrug PR-104A is activated under aerobic conditions by human aldo-keto reductase 1C3. Cancer Res. 2010;70(4):1573-1584.
22. Penning TM, Drury JE. Human aldo-keto reductases: function, gene regulation, and single nucleotide polymorphisms. Arch Biochem Biophys. 2007;464(2):241-250.
23. Penning TM, Burczynski ME, Jez JM, et al. Human 3alpha-hydroxysteroid dehydrogenase isoforms (AKR1C1-AKR1C4) of the aldo-keto reductase superfamily: functional plasticity and tissue distribution reveals roles in the inactivation and formation of male and female sex hormones. Biochem J. 2000;351(Pt 1):67-77.
24. Chen WD, Zhang Y. Regulation of aldo-keto reductases in human diseases. Front Pharmacol. 2012;3:35.
25. Penning TM, Byrns MC. Steroid hormone transforming aldo-keto reductases and cancer. Ann N Y Acad Sci. 2009;1155:33-42.
26. Fung KM, Samara EN, Wong C, et al. Increased expression of type 2 3alpha-hydroxysteroid dehydrogenase/type 5 17beta-hydroxysteroid dehydrogenase (AKR1C3) and its relationship with androgen receptor in prostate carcinoma. Endocr Relat Cancer. 2006;13(1):169-180.
27. Stanbrough M, Bubley GJ, Ross K, et al. Increased expression of genes converting adrenal androgens to testosterone in androgen-independent prostate cancer. Cancer Res. 2006;66(5):2815-2825.
28. Birtwistle J, Hayden RE, Khanim FL, et al. The aldo-keto reductase AKR1C3 contributes to 7,12-dimethylbenz(a)anthracene-3,4-dihydrodiol mediated oxidative DNA damage in myeloid cells: implications for leukemogenesis. Mutat Res. 2009;662(1-2):67-74.
29. Mahadevan D, DiMento J, Croce KD, et al. Transcriptosome and serum cytokine profiling of an atypical case of myelodysplastic syndrome with progression to acute myelogenous leukemia. Am J Hematol. 2006;81(10):779-786.
30. Jamieson SM, Gu Y, Manesh DM, et al. A novel fluorometric assay for aldo-keto reductase 1C3 predicts metabolic activation of the nitrogen mustard prodrug PR-104A in human leukaemia cells. Biochem Pharmacol. 2014;88(1):36-45.
31. Desmond JC, Mountford JC, Drayson MT, et al. The aldo-keto reductase AKR1C3 is a novel suppressor of cell differentiation that provides a plausible target for the non-cyclooxygenase-dependent antineoplastic actions of nonsteroidal anti-inflammatory drugs. Cancer Res. 2003;63(2):505-512.
32. Benito J, Shi Y, Szymanska B, et al. Pronounced hypoxia in models of murine and human leukemia: high efficacy of hypoxia-activated prodrug PR-104. PLoS One. 2011;6(8):e23108.
33. Houghton PJ, Lock R, Carol H, et al. Initial testing of the hypoxia-activated prodrug PR-104 by the pediatric preclinical testing program. Pediatr Blood Cancer. 2011;57(3):443-453.
34. Patel K, Choy SS, Hicks KO, Melink TJ, Holford NH, Wilson WR. A combined pharmacokinetic model for the hypoxia-targeted prodrug PR-104A in humans, dogs, rats and mice predicts species differences in clearance and toxicity. Cancer Chemother Pharmacol. 2011;67(5):1145-1155.
35. Szymanska B, Wilczynska-Kalak U, Kang MH, et al. Pharmacokinetic modeling of an induction regimen for in vivo combined testing of novel drugs against pediatric acute lymphoblastic leukemia xenografts. PLoS One. 2012;7(3):e33894.
36. Houghton PJ, Morton CL, Gorlick R, et al. Stage 2 combination testing of rapamycin with cytotoxic agents by the Pediatric Preclinical Testing Program. Mol Cancer Ther. 2010;9(1):101-112.
37. Houghton PJ, Morton CL, Tucker C, et al. The pediatric preclinical testing program: description of models and early testing results. Pediatr Blood Cancer. 2007;49(7):928-940.
38. Liem NL, Papa RA, Milross CG, et al. Characterization of childhood acute lymphoblastic leukemia xenograft models for the preclinical evaluation of new therapies. Blood. 2004;103(10):3905-3914.
39. Rose WC, Wild R. Therapeutic synergy of oral taxane BMS-275183 and cetuximab versus human tumor xenografts. Clin Cancer Res. 2004;10(21):7413-7417.
40. Suryani S, Carol H, Chonghaile TN, et al. Cell and molecular determinants of in vivo efficacy of the BH3 mimetic ABT-263 against pediatric acute lymphoblastic leukemia xenografts. Clin Cancer Res. 2014;20(17):4520-4531.
41. Bachmann PS, Gorman R, Papa RA, et al. Divergent mechanisms of glucocorticoid resistance in experimental models of pediatric acute lymphoblastic leukemia. Cancer Res. 2007;67(9):4482-4490.
42. Skarydova L, Hofman J, Chlebek J, et al. Isoquinoline alkaloids as a novel type of AKR1C3 inhibitors. J Steroid Biochem Mol Biol. 2014;143:250-258.
43. Endo S, Hu D, Matsunaga T, et al. Synthesis of non-prenyl analogues of baccharin as selective and potent inhibitors for aldo-keto reductase 1C3. Bioorg Med Chem. 2014;22(19):5220-5233.
44. Flanagan JU, Atwell GJ, Heinrich DM, et al. Morpholylureas are a new class of potent and selective inhibitors of the type 5 17-β-hydroxysteroid dehydrogenase (AKR1C3). Bioorg Med Chem. 2014;22(3):967-977.
45. Khanim F, Davies N, Veliça P, et al. Selective AKR1C3 inhibitors do not recapitulate the antileukaemic activities of the pan-AKR1C inhibitor medroxyprogesterone acetate. Br J Cancer. 2014;110(6):1506-1516.
46. Jameson MB, Rischin D, Pegram M, et al. A phase I trial of PR-104, a nitrogen mustard prodrug activated by both hypoxia and aldo-keto reductase 1C3, in patients with solid tumors. Cancer Chemother Pharmacol. 2010;65(4):791-801.
47. Lock RB, Liem N, Farnsworth ML, et al. The nonobese diabetic/severe combined immunodeficient (NOD/SCID) mouse model of childhood acute lymphoblastic leukemia reveals intrinsic differences in biologic characteristics at diagnosis and relapse. Blood. 2002;99(11):4100-4108.