Efficacy of Retinoids in IKZF1-Mutated BCR-ABL1 Acute Lymphoblastic Leukemia

Cancer Cell

Volumn 28, Issue 3, 2015, Pages 343-356

  Churchman, Michelle L ^a   Low, Jonathan ^a   Qu, Chunxu ^a   Paietta, Elisabeth M ^b   Kasper, Lawryn H ^a   Chang, Yunchao ^a   Payne Turner, Debbie ^a   Althoff, Mark J ^a   Song, Guangchun ^a   Chen, Shann Ching ^a   Ma, Jing ^a   Rusch, Michael ^a   McGoldrick, Dan ^a   Edmonson, Michael ^a   Gupta, Pankaj ^a   Wang, Yong Dong ^a   Caufield, William ^a   Freeman, Burgess ^a   Li, Lie ^a   Panetta, John C ^a   Baker, Sharyn ^a   Yang, Yung Li ^a   Roberts, Kathryn G ^a   McCastlain, Kelly ^a   Iacobucci, Ilaria ^a   Peters, Jennifer L ^a   Centonze, Victoria E ^a   Notta, Faiyaz ^c,d   Dobson, Stephanie M ^c,d   Zandi, Sasan ^c,d   Dick, John E ^c,d   Janke, Laura ^a   Peng, Junmin ^a   Kodali, Kiran ^a   Pagala, Vishwajeeth ^a   Min, Jaeki ^a   Mayasundari, Anand ^a   Williams, Richard T ^e   Willman, Cheryl L ^f   Rowe, Jacob ^g   Luger, Selina ^h   Dickins, Ross A ⁱ   Guy, R Kiplin ^a   Chen, Taosheng ^a   Mullighan, Charles G ^a   more..

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

^b MONTEFIORE MEDICAL CENTER   (United States)

^c PRINCESS MARGARET HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e Puma Biotechnology Inc   (United States)

^f UNIVERSITY OF NEW MEXICO   (United States)

^g SHAARE ZEDEK MEDICAL CENTER   (Israel)

^h HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

ⁱ WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

6 [1 (5,6,7,8 TETRAHYDRO 3,5,5,8,8 PENTAMETHYL 2 NAPHTHYL)CYCLOPROPYL]NICOTINIC ACID; AGN 195183; ALITRETINOIN; ANTINEOPLASTIC AGENT; ARF PROTEIN; ASPARAGINASE; BCR ABL PROTEIN; BEXAROTENE; CARBACYCLIN; DASATINIB; DEXAMETHASONE; FOCAL ADHESION KINASE INHIBITOR; IKAROS TRANSCRIPTION FACTOR; ISOTRETINOIN; NVPTAE 226; PF 562271; PF 573228; RETINOIC ACID; RETINOID; RETINOID X RECEPTOR; RIVIPANSEL; UNCLASSIFIED DRUG; RETINOIC ACID RECEPTOR;

ACUTE LYMPHOBLASTIC LEUKEMIA; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BONE MARROW; CANCER GROWTH; CANCER STEM CELL; CANCER SURVIVAL; CELL ADHESION; CELL AGGREGATION; CELL CYCLE ARREST; CELL RENEWAL; CHILD; COLONY FORMATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; DRUG POTENTIATION; GENOTYPE; HAPLOINSUFFICIENCY; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; LEUKEMIA CELL; LEUKEMOGENESIS; MAJOR CLINICAL STUDY; MOUSE; MOUSE MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POINT MUTATION; PRE B LYMPHOCYTE; PRIORITY JOURNAL; SURVIVAL TIME; TUMOR VOLUME; YOUNG ADULT; ANIMAL; CELL CYCLE CHECKPOINT; GENETICS; METABOLISM; MUTATION;

ANIMALS; CELL CYCLE CHECKPOINTS; FUSION PROTEINS, BCR-ABL; HUMANS; IKAROS TRANSCRIPTION FACTOR; MICE; MUTATION; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; RECEPTORS, RETINOIC ACID; RETINOIDS;

EID: 84942371671     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2015.07.016     Document Type: Article

References (53)

1. Altucci L., Leibowitz M.D., Ogilvie K.M., de Lera A.R., Gronemeyer H. RAR and RXR modulation in cancer and metabolic disease. Nat. Rev. Drug Discov. 2007, 6:793-810.
2. Barker T.H., Hagood J.S. Getting a grip on Thy-1 signaling. Biochim. Biophys. Acta 2009, 1793:921-923.
3. Boulos N., Mulder H.L., Calabrese C.R., Morrison J.B., Rehg J.E., Relling M.V., Sherr C.J., Williams R.T. Chemotherapeutic agents circumvent emergence of dasatinib-resistant BCR-ABL kinase mutations in a precise mouse model of Philadelphia chromosome-positive acute lymphoblastic leukemia. Blood 2011, 117:3585-3595.
4. Cobb B.S., Morales-Alcelay S., Kleiger G., Brown K.E., Fisher A.G., Smale S.T. Targeting of Ikaros to pericentromeric heterochromatin by direct DNA binding. Genes Dev. 2000, 14:2146-2160.
5. Connolly R.M., Nguyen N.K., Sukumar S. Molecular pathways: current role and future directions of the retinoic acid pathway in cancer prevention and treatment. Clin. Cancer Res. 2013, 19:1651-1659.
6. Craig W., Kay R., Cutler R.L., Lansdorp P.M. Expression of Thy-1 on human hematopoietic progenitor cells. J. Exp. Med. 1993, 177:1331-1342.
7. Daley G.Q., Van Etten R.A., Baltimore D. Induction of chronic myelogenous leukemia in mice by the P210bcr/abl gene of the Philadelphia chromosome. Science 1990, 247:824-830.
8. Den Boer M.L., van Slegtenhorst M., De Menezes R.X., Cheok M.H., Buijs-Gladdines J.G., Peters S.T., Van Zutven L.J., Beverloo H.B., Van der Spek P.J., Escherich G., et al. A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol. 2009, 10:125-134.
9. Doulatov S., Notta F., Eppert K., Nguyen L.T., Ohashi P.S., Dick J.E. Revised map of the human progenitor hierarchy shows the origin of macrophages and dendritic cells in early lymphoid development. Nat. Immunol. 2010, 11:585-593.
10. Ferreirós-Vidal I., Carroll T., Taylor B., Terry A., Liang Z., Bruno L., Dharmalingam G., Khadayate S., Cobb B.S., Smale S.T., et al. Genome-wide identification of Ikaros targets elucidates its contribution to mouse B-cell lineage specification and pre-B-cell differentiation. Blood 2013, 121:1769-1782.
11. Georgopoulos K., Bigby M., Wang J.H., Molnar A., Wu P., Winandy S., Sharpe A. The Ikaros gene is required for the development of all lymphoid lineages. Cell 1994, 79:143-156.
12. Greenbaum A., Hsu Y.M., Day R.B., Schuettpelz L.G., Christopher M.J., Borgerding J.N., Nagasawa T., Link D.C. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 2013, 495:227-230.
13. Hsieh Y.T., Gang E.J., Geng H., Park E., Huantes S., Chudziak D., Dauber K., Schaefer P., Scharman C., Shimada H., et al. Integrin alpha4 blockade sensitizes drug resistant pre-B acute lymphoblastic leukemia to chemotherapy. Blood 2013, 121:1814-1818.
14. Inaba H., Greaves M., Mullighan C.G. Acute lymphoblastic leukaemia. Lancet 2013, 381:1943-1955.
15. Joshi I., Yoshida T., Jena N., Qi X., Zhang J., Van Etten R.A., Georgopoulos K. Loss of Ikaros DNA-binding function confers integrin-dependent survival on pre-B cells and progression to acute lymphoblastic leukemia. Nat. Immunol. 2014, 15:294-304.
16. Kamijo T., Zindy F., Roussel M.F., Quelle D.E., Downing J.R., Ashmun R.A., Grosveld G., Sherr C.J. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 1997, 91:649-659.
17. Kuiper R.P., Waanders E., van der Velden V.H., van Reijmersdal S.V., Venkatachalam R., Scheijen B., Sonneveld E., van Dongen J.J., Veerman A.J., van Leeuwen F.N., et al. IKZF1 deletions predict relapse in uniformly treated pediatric precursor B-ALL. Leukemia 2010, 24:1258-1264.
18. Lamb J., Crawford E.D., Peck D., Modell J.W., Blat I.C., Wrobel M.J., Lerner J., Brunet J.P., Subramanian A., Ross K.N., et al. The Connectivity Map: using gene-expression signatures to connect small molecules, genes, and disease. Science 2006, 313:1929-1935.
19. Lamkin T., Brooks J., Annett G., Roberts W., Weinberg K. Immunophenotypic differences between putative hematopoietic stem cells and childhood B-cell precursor acute lymphoblastic leukemia cells. Leukemia 1994, 8:1871-1878.
20. Li G., Ruan X., Auerbach R.K., Sandhu K.S., Zheng M., Wang P., Poh H.M., Goh Y., Lim J., Zhang J., et al. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 2012, 148:84-98.
21. Lin T.L., Vala M.S., Barber J.P., Karp J.E., Smith B.D., Matsui W., Jones R.J. Induction of acute lymphocytic leukemia differentiation by maintenance therapy. Leukemia 2007, 21:1915-1920.
22. Martinelli G., Iacobucci I., Storlazzi C.T., Vignetti M., Paoloni F., Cilloni D., Soverini S., Vitale A., Chiaretti S., Cimino G., et al. IKZF1 (Ikaros) deletions in BCR-ABL1-positive acute lymphoblastic leukemia are associated with short disease-free survival and high rate of cumulative incidence of relapse: a GIMEMA AL WP report. J. Clin. Oncol. 2009, 27:5202-5207.
23. Mayani H., Lansdorp P.M. Thy-1 expression is linked to functional properties of primitive hematopoietic progenitor cells from human umbilical cord blood. Blood 1994, 83:2410-2417.
24. McLaughlin J., Chianese E., Witte O.N. In vitro transformation of immature hematopoietic cells by the P210 BCR/ABL oncogene product of the Philadelphia chromosome. Proc. Natl. Acad. Sci. USA 1987, 84:6558-6562.
25. Miller P.G., Al-Shahrour F., Hartwell K.A., Chu L.P., Järås M., Puram R.V., Puissant A., Callahan K.P., Ashton J., McConkey M.E., et al. In Vivo RNAi screening identifies a leukemia-specific dependence on integrin beta 3 signaling. Cancer Cell 2013, 24:45-58.
26. Mullighan C.G. Single nucleotide polymorphism microarray analysis of genetic alterations in cancer. Methods Mol. Biol. 2011, 730:235-258.
27. Mullighan C.G. Genomic characterization of childhood acute lymphoblastic leukemia. Semin. Hematol. 2013, 50:314-324.
28. Mullighan C.G., Goorha S., Radtke I., Miller C.B., Coustan-Smith E., Dalton J.D., Girtman K., Mathew S., Ma J., Pounds S.B., et al. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature 2007, 446:758-764.
29. Mullighan C.G., Miller C.B., Radtke I., Phillips L.A., Dalton J., Ma J., White D., Hughes T.P., Le Beau M.M., Pui C.H., et al. BCR-ABL1 lymphoblastic leukaemia is characterized by the deletion of Ikaros. Nature 2008, 453:110-114.
30. Mullighan C.G., Su X., Zhang J., Radtke I., Phillips L.A., Miller C.B., Ma J., Liu W., Cheng C., Schulman B.A., et al. Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia. N. Engl. J. Med. 2009, 360:470-480. Children's Oncology Group.
31. Nishii K., Katayama N., Miwa H., Shikami M., Usui E., Masuya M., Araki H., Lorenzo F., Ogawa T., Kyo T., et al. Non-DNA-binding Ikaros isoform gene expressed in adult B-precursor acute lymphoblastic leukemia. Leukemia 2002, 16:1285-1292.
32. Notta F., Doulatov S., Laurenti E., Poeppl A., Jurisica I., Dick J.E. Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science 2011, 333:218-221.
33. Novershtern N., Subramanian A., Lawton L.N., Mak R.H., Haining W.N., McConkey M.E., Habib N., Yosef N., Chang C.Y., Shay T., et al. Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell 2011, 144:296-309.
34. Park J.H., Tallman M.S. Treatment of acute promyelocytic leukemia without cytotoxic chemotherapy. Oncology (Huntingt.) 2011, 25:733-741.
35. Rege T.A., Hagood J.S. Thy-1, a versatile modulator of signaling affecting cellular adhesion, proliferation, survival, and cytokine/growth factor responses. Biochim. Biophys. Acta 2006, 1763:991-999.
36. Roberts K.G., Morin R.D., Zhang J., Hirst M., Zhao Y., Su X., Chen S.C., Payne-Turner D., Churchman M.L., Harvey R.C., et al. Genetic alterations activating kinase and cytokine receptor signaling in high-risk acute lymphoblastic leukemia. Cancer Cell 2012, 22:153-166.
37. Roberts K.G., Li Y., Payne-Turner D., Harvey R.C., Yang Y.L., Pei D., McCastlain K., Ding L., Lu C., Song G., et al. Targetable kinase-activating lesions in Ph-like acute lymphoblastic leukemia. N. Engl. J. Med. 2014, 371:1005-1015.
38. Rowe J.M., Buck G., Burnett A.K., Chopra R., Wiernik P.H., Richards S.M., Lazarus H.M., Franklin I.M., Litzow M.R., Ciobanu N., et al. Induction therapy for adults with acute lymphoblastic leukemia: results of more than 1500 patients from the international ALL trial: MRC UKALL XII/ECOG E2993. Blood 2005, 106:3760-3767. ECOG, MRC/NCRI Adult Leukemia Working PartyMRC/NCRI Adult Leukemia Working Party.
39. Saalbach A., Wetzel A., Haustein U.F., Sticherling M., Simon J.C., Anderegg U. Interaction of human Thy-1 (CD 90) with the integrin alphavbeta3 (CD51/CD61): an important mechanism mediating melanoma cell adhesion to activated endothelium. Oncogene 2005, 24:4710-4720.
40. Schjerven H., McLaughlin J., Arenzana T.L., Frietze S., Cheng D., Wadsworth S.E., Lawson G.W., Bensinger S.J., Farnham P.J., Witte O.N., Smale S.T. Selective regulation of lymphopoiesis and leukemogenesis by individual zinc fingers of Ikaros. Nat. Immunol. 2013, 14:1073-1083.
41. + B-acute lymphoblastic leukemia. Blood 2010, 116:2522-2530.
42. Stock W. Adolescents and young adults with acute lymphoblastic leukemia. Hematology Am. Soc. Hematol. Educ. Program 2010, 2010:21-29.
43. van der Veer A., Zaliova M., Mottadelli F., De Lorenzo P., Te Kronnie G., Harrison C.J., Cavé H., Trka J., Saha V., Schrappe M., et al. IKZF1 status as a prognostic feature in BCR-ABL1-positive childhood ALL. Blood 2014, 123:1691-1698.
44. Virely C., Moulin S., Cobaleda C., Lasgi C., Alberdi A., Soulier J., Sigaux F., Chan S., Kastner P., Ghysdael J. Haploinsufficiency of the IKZF1 (IKAROS) tumor suppressor gene cooperates with BCR-ABL in a transgenic model of acute lymphoblastic leukemia. Leukemia 2010, 24:1200-1204.
45. Williams R.T., Roussel M.F., Sherr C.J. Arf gene loss enhances oncogenicity and limits imatinib response in mouse models of Bcr-Abl-induced acute lymphoblastic leukemia. Proc. Natl. Acad. Sci. USA 2006, 103:6688-6693.
46. +, Arf-null lymphoblastic leukemia. Genes Dev. 2007, 21:2283-2287.
47. Wong D.J., Liu H., Ridky T.W., Cassarino D., Segal E., Chang H.Y. Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2008, 2:333-344.
48. Yamazaki H., Nishida H., Iwata S., Dang N.H., Morimoto C. CD90 and CD110 correlate with cancer stem cell potentials in human T-acute lymphoblastic leukemia cells. Biochem. Biophys. Res. Commun. 2009, 383:172-177.
49. Yoshida T., Ng S.Y., Georgopoulos K. Awakening lineage potential by Ikaros-mediated transcriptional priming. Curr. Opin. Immunol. 2010, 22:154-160.
50. Zhang Y., Dawson M.I., Mohammad R., Rishi A.K., Farhana L., Feng K.C., Leid M., Peterson V., Zhang X.K., Edelstein M., et al. Induction of apoptosis of human B-CLL and ALL cells by a novel retinoid and its nonretinoidal analog. Blood 2002, 100:2917-2925.
51. Zhang J., Mullighan C.G., Harvey R.C., Wu G., Chen X., Edmonson M., Buetow K.H., Carroll W.L., Chen I.M., Devidas M., et al. Key pathways are frequently mutated in high-risk childhood acute lymphoblastic leukemia: a report from the Children's Oncology Group. Blood 2011, 118:3080-3087.
52. Zhang J., Ding L., Holmfeldt L., Wu G., Heatley S.L., Payne-Turner D., Easton J., Chen X., Wang J., Rusch M., et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 2012, 481:157-163.
53. Zhang J., Jackson A.F., Naito T., Dose M., Seavitt J., Liu F., Heller E.J., Kashiwagi M., Yoshida T., Gounari F., et al. Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat. Immunol. 2012, 13:86-94.