Reversal of microRNA-150 silencing disadvantages crizotinib-resistant NPM-ALK(+) cell growth

Journal of Clinical Investigation

Volumn 125, Issue 9, 2015, Pages 3505-3518

  Hoareau Aveilla, Coralie ^a,b   Valentin, Thibaud ^a,b   Daugrois, Camille ^a,b   Quelen, Cathy ^a,b   Mitou, Géraldine ^a,b   Quentin, Samuel ^c   Jia, Jinsong ^d   Spicuglia, Salvatore ^d   Ferrier, Pierre ^d   Ceccon, Monica ^e,f   Giuriato, Sylvie ^a,b,f   Gambacorti Passerini, Carlo ^e,f   Brousset, Pierre ^a,b,f,g,h   Lamant, Laurence ^a,b,f,g,h   Meggetto, Fabienne ^a,b,f,g,h  

^a UNIVERSITÉ PAUL SABATIER   (France)

^b CANCER RESEARCH CENTER OF TOULOUSE   (France)

^c SAINT LOUIS HOSPITAL   (France)

^d CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^e UNIVERSITY OF MILANO BICOCCA   (Italy)

^f European Research Initiative on ALK Related Malignancies (ERIA)   (Italy)

^g Institut Carnot Lymphome CALYM   (France)

^h Laboratoire d'Excellence Toulouse Cancer (TOUCAN)   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; CRIZOTINIB; DECITABINE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; MICRORNA; MICRORNA 150; NUCLEOPHOSMIN; PROTEIN MYB; SMALL INTERFERING RNA; STAT3 PROTEIN; UNCLASSIFIED DRUG; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; MIRN150 MICRORNA, HUMAN; P80(NPM-ALK) PROTEIN; PROTEIN TYROSINE KINASE; PYRAZOLE DERIVATIVE; PYRIDINE DERIVATIVE; RNA; STAT3 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER RESISTANCE; CELL PROLIFERATION; CELL VIABILITY; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; CROSS RESISTANCE; DNA METHYLATION; DOWN REGULATION; ENZYME ACTIVITY; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LARGE CELL LYMPHOMA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE MYB; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA METHYLATION; TRANSCRIPTION INITIATION; TUMOR XENOGRAFT; UPREGULATION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; DRUG RESISTANCE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; LYMPHOMA, LARGE-CELL, ANAPLASTIC; MALE; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; LYMPHOMA, LARGE-CELL, ANAPLASTIC; MALE; MICE; MICE, TRANSGENIC; MICRORNAS; PROTEIN-TYROSINE KINASES; PYRAZOLES; PYRIDINES; RNA, NEOPLASM; STAT3 TRANSCRIPTION FACTOR;

EID: 84941702578     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI78488     Document Type: Article

References (81)

1. Lamant L, et al. Prognostic impact of morphologic and phenotypic features of childhood ALK-positive anaplastic large-cell lymphoma: results of the ALCL99 study. J Clin Oncol. 2011;29 (35) :4669-4676.
2. Savage KJ, et al. ALK-Anaplastic large-cell lymphoma is clinically and immunophenotypically different from both ALK+ ALCL and peripheral T cell lymphoma, not otherwise specified: report from the International Peripheral T cell Lymphoma Project. Blood. 2008;111 (12) :5496-5504.
3. Hallberg B, Palmer RH. Mechanistic insight into ALK receptor tyrosine kinase in human cancer biology. Nat Rev Cancer. 2013;13 (10) :685-700.
4. Ferreri AJ, Govi S, Pileri SA, Savage KJ. Anaplastic large cell lymphoma, ALK-negative. Crit Rev Oncol Hematol. 2013;85 (2) :206-215.
5. Lai R, Ingham RJ. The pathobiology of the oncogenic tyrosine kinase NPM-ALK: A brief update. Ther Adv Hematol. 2013;4 (2) :119-131.
6. Jacobsen E. Anaplastic large-cell lymphoma, T-/null-cell type. Oncologist. 2006;11 (7) :831-840.
7. Kruczynski A, Delsol G, Laurent C, Brousset P, Lamant L. Anaplastic lymphoma kinase as a therapeutic target. Expert Opin Ther Targets. 2012;16 (11) :1127-1138.
8. Camidge DR, Doebele RC. Treating ALK-positive lung cancer-early successes and future challenges. Nat Rev Clin Oncol. 2012;9 (5) :268-277.
9. Christensen JG, et al. Cytoreductive antitumor activity of PF-2341066, a novel inhibitor of anaplastic lymphoma kinase and c-Met, in experimental models of anaplastic large-cell lymphoma. Mol Cancer Ther. 2007;6 (12 pt 1) :3314-3322.
10. Mologni L. Inhibitors of the anaplastic lymphoma kinase. Expert Opin Investig Drugs. 2012;21 (7) :985-994.
11. Gambacorti Passerini C, et al. Crizotinib in advanced, chemoresistant anaplastic lymphoma kinase-positive lymphoma patients. J Natl Cancer Inst. 2014;106 (2) :djt378.
12. Sahu A, Prabhash K, Noronha V, Joshi A, Desai S. Crizotinib: A comprehensive review. South Asian J Cancer. 2013;2 (2) :91-97.
13. Katayama R, et al. Therapeutic strategies to overcome crizotinib resistance in non-small cell lung cancers harboring the fusion oncogene EML4-ALK. Proc Natl Acad Sci U S A. 2011;108 (18) :7535-7540.
14. Han C, Yu Z, Duan Z, Kan Q. Role of microRNA-1 in human cancer and its therapeutic potentials. Biomed Res Int. 2014;2014:428371.
15. Han L, Witmer PD, Casey E, Valle D, Sukumar S. DNA methylation regulates MicroRNA expression. Cancer Biol Ther. 2007;6 (8) :1284-1288.
16. Han Y, et al. Restoration of shp1 expression by 5-AZA-2-deoxycytidine is associated with downregulation of JAK3/STAT3 signaling in ALK-positive anaplastic large cell lymphoma. Leukemia. 2006;20 (9) :1602-1609.
17. Hayes J, Peruzzi PP, Lawler S. MicroRNAs in cancer: biomarkers, functions and 655 therapy. Trends Mol Med. 2014;20 (8) :460-469.
18. Lopez-Serra P, Esteller M. DNA methylation-Associated silencing of tumor-suppressor microRNAs in cancer. Oncogene. 2012;31 (13) :1609-1622.
19. Baer C, Claus R, Plass C. Genome-wide epigenetic regulation of miRNAs in cancer. Cancer Res. 2013;73 (2) :473-477.
20. Fabbri M, Calin GA. Epigenetics and miRNAs in human cancer. Adv Genet. 2010;70:87-99.
21. Subramaniam D, Thombre R, Dhar A, Anant S. DNA methyltransferases: A novel target for prevention and therapy. Front Oncol. 2014;4:80.
22. Karahoca M, Momparler RL. Pharmacokinetic and pharmacodynamic analysis of 5-Aza-2-deoxycytidine (decitabine) in the design of its dose-schedule for cancer therapy. Clin Epigenetics. 2013;5 (1) :3.
23. Suzuki H, Maruyama R, Yamamoto E, Kai M. DNA methylation and microRNA dysregulation in cancer. Mol Oncol. 2012;6 (6) :567-578.
24. Henry JC, Azevedo-Pouly AC, Schmittgen TD. MicroRNA replacement therapy for cancer. Pharm Res. 2011;28 (12) :3030-3042.
25. Rebucci M, Michiels C. Molecular aspects of cancer cell resistance to chemotherapy. Biochem Pharmacol. 2013;85 (9) :1219-1226.
26. Ma J, Dong C, Ji C. MicroRNA and drug resistance. Cancer Gene Ther. 2010;17 (8) :523-531.
27. Zheng T, Wang J, Chen X, Liu L. Role of microRNA in anticancer drug resistance. Int J Cancer. 2010;126 (1) :2-10.
28. Merkel O, et al. Identification of differential and functionally active miRNAs in both anaplastic lymphoma kinase (ALK) + and ALK-Anaplastic large-cell lymphoma. Proc Natl Acad Sci U S A. 2010;107 (37) :16228-16233.
29. Desjobert C, et al. MiR-29a down-regulation in ALK-positive anaplastic large cell lymphomas contributes to apoptosis blockade through MCL-1 overexpression. Blood. 2011;117 (24) :6627-6637.
30. Matsuyama H, et al. miR-135b mediates NPMALK-driven oncogenicity and renders IL-17-producing immunophenotype to anaplastic large cell lymphoma. Blood. 2011;118 (26) :6881-6892.
31. Dejean E, et al. Hypoxia-microRNA-16 downregulation induces VEGF expression in anaplastic lymphoma kinase (ALK)-positive anaplastic large-cell lymphomas. Leukemia. 2011;25 (12) :1882-1890.
32. Bissels U, Bosio A, Wagner W. MicroRNAs are shaping the hematopoietic landscape. Haematologica. 2012;97 (2) :160-167.
33. Tili E, Michaille JJ, Costinean S, Croce CM. MicroRNAs, the immune system and rheumatic disease. Nat Clin Pract Rheumatol. 2008;4 (10) :534-541.
34. Monticelli S, et al. MicroRNA profiling of the murine hematopoietic system. Genome Biol. 2005;6 (8) :R71.
35. Undi RB, Kandi R, Gutti RK. MicroRNAs as haematopoiesis regulators. Adv Hematol. 2013;2013:695754.
36. Watanabe A, et al. The role of microRNA-150 as a tumor suppressor in malignant lymphoma. Leukemia. 2011;25 (8) :1324-1334.
37. Ito M, et al. MicroRNA-150 inhibits tumor invasion and metastasis by targeting the chemokine receptor CCR6, in advanced cutaneous T cell lymphoma. Blood. 2014;123 (10) :1499-1511.
38. Mishra A, Garzon R. The (miR) e of CTCL. Blood. 2014;123 (10) :1438.
39. He Y, Jiang X, Chen J. The role of miR-150 in normal and malignant hematopoiesis. Oncogene. 2014;33 (30) :3887-3893.
40. Honda N, et al. miR-150 down-regulation contributes to the constitutive type I collagen overexpression in scleroderma dermal fibroblasts via the induction of integrin β3. Am J Pathol. 2013;182 (1) :206-216.
41. Hassler MR, et al. Antineoplastic activity of the DNA methyltransferase inhibitor 5-Aza-2-deoxycytidine in anaplastic large cell lymphoma. Biochimie. 2012;94 (11) :2297-2307.
42. Kasprzycka M, Marzec M, Liu X, Zhang Q, Wasik MA. Nucleophosmin/anaplastic lymphoma kinase (NPM/ALK) oncoprotein induces the T regulatory cell phenotype by activating STAT3. Proc Natl Acad Sci U S A. 2006;103 (26) :9964-9969.
43. Levy DE, Inghirami G. STAT3: A multifaceted oncogene. Proc Natl Acad Sci U S A. 2006;103 (27) :10151-10152.
44. Zhang Q, et al. Multilevel dysregulation of STAT3 activation in anaplastic lymphoma kinase-positive T/null-cell lymphoma. J Immunol. 2002;168 (1) :466-474.
45. Dawson MA, Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell. 2012;150 (1) :12-27.
46. Wang LQ, Liang R, Chim CS. Methylation of tumor suppressor microRNAs: lessons from lymphoid malignancies. Expert Rev Mol Diagn. 2012;12 (7) :755-765.
47. Maia BM, Rocha RM, Calin GA. Clinical significance of the interaction between non-coding RNAs and the epigenetics machinery: challenges and opportunities in oncology. Epigenetics. 2014;9 (1) :75-80.
48. Ambrogio C, et al. NPM-ALK oncogenic tyrosine kinase controls T cell identity by transcriptional regulation and epigenetic silencing in lymphoma cells. Cancer Res. 2009;69 (22) :8611-8619.
49. Piazza R, et al. Epigenetic silencing of the proapoptotic gene BIM in anaplastic large cell lymphoma through an MeCP2/SIN3a deacetylating complex. Neoplasia. 2013;15 (5) :511-522.
50. Zhang Q, Wang HY, Liu XB, Wasik MA. STAT5A is epigenetically silenced by the tyrosine kinase NPM1-ALK and acts as a tumor suppressor by reciprocally inhibiting NPM1-ALK expression. Nat Med. 2007;13 (11) :1341-1348.
51. Zhang Q, Wang HY, Marzec M, Raghunath PN, Nagasawa T, Wasik MA. STAT3-And DNA methyltransferase 1-mediated epigenetic silencing of SHP-1 tyrosine phosphatase tumor suppressor gene in malignant T lymphocytes. Proc Natl Acad Sci U S A. 2005;102 (19) :6948-6953.
52. Goffin J, Eisenhauer E. DNA methyltransferase inhibitors-state of the art. Ann Oncol. 2002;13 (11) :1699-1716.
53. Boumber Y, Issa JP. Epigenetics in cancer: whats the future? Oncology (Williston Park) . 2011;25 (3) :220-226.
54. Edlin R, et al. Azacitidine for the treatment of myelodysplastic syndrome, chronic myelomonocytic leukaemia and acute myeloid leukaemia. Health Technol Asses. 2010;14 (suppl 1) :69-74.
55. Curran MP. Decitabine: A review of its use in older patients with acute myeloid leukaemia. Drug Aging. 2013;30 (6) :447-458.
56. Daskalakis M, Blagitko-Dorfs N, Hackanson B. Decitabine. Recent Results Cancer Res. 2010;184:131-157.
57. Vijayaraghavalu S, Labhasetwar V. Efficacy of decitabine-loaded nanogels in overcoming cancer drug resistance is mediated via sustained DNA methyltransferase 1 (DNMT1) depletion. Cancer Lett. 2013;331 (1) :122-129.
58. Bezman NA, Chakraborty T, Bender T, Lanier LL. miR-150 regulates the development of NK and iNKT cells. J Exp Med. 2011;208 (13) :2717-2731.
59. Chen S, et al. Re-expression of microRNA-150 induces EBV-positive Burkitt lymphoma differentiation by modulating c-Myb in vitro. Cancer Sci. 2013;104 (7) :826-834.
60. Zhou Y, Ness SA. Myb proteins: Angels and demons in normal and transformed cells. Front Biosci (Landmark Ed) . 2011;16:1109-1131.
61. Cogswell JP, et al. Mechanism of c-Myc regulation by c-Myb in different cell lineages. Mol Cell Biol. 1993;13 (5) :2858-2869.
62. Zhang J, Luo N, Luo Y, Peng ZP, Zhang T, Li SL. microRNA-150 inhibits human CD133-positive liver cancer stem cells through negative regulation of the transcription factor c-Myb. Int J Oncol. 2012;40 (3) :747-756.
63. Fawal M, et al. A "liaison dangereuse" between AUF1/hnRNPD and the oncogenic tyrosine kinase NPM-ALK. Blood. 2006;108 (8) :2780-2788.
64. Gouble A, Grazide S, Meggetto F, Mercier P, Delsol G, Morello D. A new player in oncogenesis: AUF1/hnRNPD overexpression leads to tumorigenesis in transgenic mice. Cancer Res. 2002;62 (5) :1489-1495.
65. Jiang X, et al. Blockade of miR-150 maturation by MLL-fusion/MYC/LIN-28 is required for MLL-Associated leukemia. Blood. 2012;120 (4) :524-535.
66. Brenner C, et al. Myc represses transcription through recruitment of DNA methyltransferase corepressor. EMBO J. 2005;24 (2) :336-346.
67. Mutze K, et al. DNA methyltransferase 1 as a predictive biomarker and potential therapeutic target for chemotherapy in gastric cancer. Eur J Cancer. 2011;47 (12) :1817-1825.
68. Foyil KV, Bartlett NL. Brentuximab vedotin and crizotinib in anaplastic large-cell lymphoma. Cancer J. 2012;18 (5) :450-456.
69. Voena C, Chiarle R. The battle against ALK resistance: successes and setbacks. Expert Opin Investig Drugs. 2012;21 (12) :1751-1754.
70. Mosse YP, et al. Safety and activity of crizotinib for paediatric patients with refractory solid tumours or anaplastic large-cell lymphoma: A Childrens Oncology Group phase 1 consortium study. Lancet Oncol. 2013;14 (6) :472-480.
71. Zdzalik D, et al. Activating mutations in ALK kinase domain confer resistance to structurally unrelated ALK inhibitors in NPM-ALK-positive anaplastic large-cell lymphoma. J Cancer Res Clin Oncol. 2014;140 (4) :589-598.
72. Mummaneni P, Shord SS. Epigenetics and oncology. Pharmacotherapy. 2014;34 (5) :495-505.
73. Ceccon M, Mologni L, Bisson W, Scapozza L, Gambacorti-Passerini C. Crizotinib-resistant NPM-ALK mutants confer differential sensitivity to unrelated Alk inhibitors. Mol Cancer Res. 2013;11 (2) :122-132.
74. Gorre ME, et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science. 2001;293 (5531) :876-880.
75. Kobayashi S, et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med. 2005;352 (8) :786-792.
76. La Rosee P, et al. In vitro efficacy of combined treatment depends on the underlying mechanism of resistance in imatinib-resistant Bcr-Abl-positive cell lines. Blood. 2004;103 (1) :208-215.
77. Chen Y, et al. Oncogenic mutations of ALK kinase in neuroblastoma. Nature. 2008;455 (7215) :971-974.
78. Janoueix-Lerosey I, et al. Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma. Nature. 2008;455 (7215) :967-970.
79. George RE, et al. Activating mutations in ALK provide a therapeutic target in neuroblastoma. Nature. 2008;455 (7215) :975-978.
80. Mosse YP, et al. Identification of ALK as a major familial neuroblastoma predisposition gene. Nature. 2008;455 (7215) :930-935.
81. Liu C, et al. MicroRNA expression profiling identifies molecular signatures associated with anaplastic large cell lymphoma. Blood. 2013;122 (12) :2083-2092.