Targeting c-FOS and DUSP1 abrogates intrinsic resistance to tyrosine-kinase inhibitor therapy in BCR-ABL-induced leukemia

Nature Medicine

Volumn 23, Issue 4, 2017, Pages 472-482

  Kesarwani, Meenu ^a   Kincaid, Zachary ^a   Gomaa, Ahmed ^a   Huber, Erika ^a   Rohrabaugh, Sara ^a   Siddiqui, Zain ^a   Bouso, Muhammad F ^a   Latif, Tahir ^b   Xu, Ming ^c   Komurov, Kakajan ^a   Mulloy, James C ^a   Cancelas, Jose A ^a   Grimes, H Leighton ^a   Azam, Mohammad ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; GROWTH FACTOR; IMATINIB; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; PROTEIN C FOS; PROTEIN TYROSINE KINASE INHIBITOR; DUSP1 PROTEIN, MOUSE; PROTEIN KINASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BCR ABL INDUCED LEUKEMIA; CHRONIC MYELOID LEUKEMIA; CHRONIC MYELOID LEUKEMIA CELL LINE; CONTROLLED STUDY; DRUG EFFICACY; EXPERIMENTAL MODEL; GENE DELETION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR GROWTH; ADULT; ANIMAL; APOPTOSIS; CANCER TRANSPLANTATION; CELL PROLIFERATION; DRUG EFFECTS; DRUG RESISTANCE; EXPERIMENTAL NEOPLASM; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETICS; KNOCKOUT MOUSE; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MALE; MIDDLE AGED; MINIMAL RESIDUAL DISEASE; ONCOGENE; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; TUMOR STEM CELL ASSAY; WESTERN BLOTTING;

ADULT; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; DUAL SPECIFICITY PHOSPHATASE 1; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENES, ABL; HUMANS; IMATINIB MESYLATE; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MIDDLE AGED; NEOPLASM TRANSPLANTATION; NEOPLASM, RESIDUAL; NEOPLASMS, EXPERIMENTAL; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-FOS; REAL-TIME POLYMERASE CHAIN REACTION; TUMOR STEM CELL ASSAY;

EID: 85015711618     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.4310     Document Type: Article

References (61)

1. 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 247, 824-830 (1990).
2. Druker, B.J. et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat. Med. 2, 561-566 (1996).
3. O'Hare, T., Zabriskie, M.S., Eiring, A.M. & Deininger, M.W. Pushing the limits of targeted therapy in chronic myeloid leukaemia. Nat. Rev. Cancer 12, 513-526 (2012).
4. Rousselot, P. et al. Imatinib mesylate discontinuation in patients with chronic myelogenous leukemia in complete molecular remission for more than 2 years. Blood 109, 58-60 (2007).
5. Mahon, F.X. et al. Discontinuation of imatinib in patients with chronic myeloid leukaemia who have maintained complete molecular remission for at least 2 years: the prospective, multicentre Stop Imatinib (STIM) trial. Lancet Oncol. 11, 1029-1035 (2010).
6. Ross, D.M. et al. Safety and efficacy of imatinib cessation for CML patients with stable undetectable minimal residual disease: results from the TWISTER study. Blood 122, 515-522 (2013).
7. Chu, S. et al. Detection of BCR-ABL kinase mutations in CD34+ cells from chronic myelogenous leukemia patients in complete cytogenetic remission on imatinib mesylate treatment. Blood 105, 2093-2098 (2005).
8. Savona, M. & Talpaz, M. Getting to the stem of chronic myeloid leukaemia. Nat. Rev. Cancer 8, 341-350 (2008).
9. Azam, M., Latek, R.R. & Daley, G.Q. Mechanisms of autoinhibition and STI-571/imatinib resistance revealed by mutagenesis of BCR-ABL. Cell 112, 831-843 (2003).
10. Krause, D.S. & Van Etten, R.A. Tyrosine kinases as targets for cancer therapy. N. Engl. J. Med. 353, 172-187 (2005).
11. Weinstein, I.B. Cancer. Addiction to oncogenes - the Achilles heal of cancer. Science 297, 63-64 (2002).
12. Sawyers, C.L. Shifting paradigms: the seeds of oncogene addiction. Nat. Med. 15, 1158-1161 (2009).
13. Pagliarini, R., Shao, W. & Sellers, W.R. Oncogene addiction: pathways of therapeutic response, resistance, and road maps toward a cure. EMBO Rep. 16, 280-296 (2015).
14. Reddy, A. & Kaelin, W.G., Jr. Using cancer genetics to guide the selection of anticancer drug targets. Curr. Opin. Pharmacol. 2, 366-373 (2002).
15. Kaelin, W.G., Jr. The concept of synthetic lethality in the context of anticancer therapy. Nat. Rev. Cancer 5, 689-698 (2005).
16. Kamb, A. Consequences of nonadaptive alterations in cancer. Mol. Biol. Cell 14, 2201-2205 (2003).
17. Mills, G.B., Lu, Y. & Kohn, E.C. Linking molecular therapeutics to molecular diagnostics: inhibition of the FRAP/RAFT/TOR component of the PI3K pathway preferentially blocks PTEN mutant cells in vitro and in vivo. Proc. Natl. Acad. Sci. USA 98, 10031-10033 (2001).
18. Sharma, S.V. & Settleman, J. Exploiting the balance between life and death: targeted cancer therapy and "oncogenic shock". Biochem. Pharmacol. 80, 666-673 (2010).
19. Sharma, S.V. & Settleman, J. Oncogene addiction: setting the stage for molecularly targeted cancer therapy. Genes Dev. 21, 3214-3231 (2007).
20. Corbin, A.S. et al. Human chronic myeloid leukemia stem cells are insensitive to imatinib despite inhibition of BCR-ABL activity. J. Clin. Invest. 121, 396-409 (2011).
21. Straussman, R. et al. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 487, 500-504 (2012).
22. Wilson, T.R. et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 487, 505-509 (2012).
23. Bruennert, D. et al. Early in vivo changes of the transcriptome in Philadelphia chromosome-positive CD34+ cells from patients with chronic myelogenous leukaemia following imatinib therapy. Leukemia 23, 983-985 (2009).
24. Eferl, R. & Wagner, E.F. AP-1: a double-edged sword in tumorigenesis. Nat. Rev. Cancer 3, 859-868 (2003).
25. Lawan, A., Shi, H., Gatzke, F. & Bennett, A.M. Diversity and specificity of the mitogen-activated protein kinase phosphatase-1 functions. Cell. Mol. Life Sci. 70, 223-237 (2013).
26. Jeffrey, K.L., Camps, M., Rommel, C. & Mackay, C.R. Targeting dual-specificity phosphatases: manipulating MAP kinase signalling and immune responses. Nat. Rev. Drug Discov. 6, 391-403 (2007).
27. Brooks, S.A. & Blackshear, P.J. Tristetraprolin (TTP): interactions with mRNA and proteins, and current thoughts on mechanisms of action. Biochim. Biophys. Acta 1829, 666-679 (2013).
28. Dorfman, K. et al. Disruption of the erp/mkp-1 gene does not affect mouse development: normal MAP kinase activity in ERP/MKP-1-deficient fibroblasts. Oncogene 13, 925-931 (1996).
29. Zhang, J. et al. c-fos regulates neuronal excitability and survival. Nat. Genet. 30, 416-420 (2002).
30. Zhao, C. et al. Hedgehog signalling is essential for maintenance of cancer stem cells in myeloid leukaemia. Nature 458, 776-779 (2009).
31. Ransone, L.J., Visvader, J., Wamsley, P. & Verma, I.M. Trans-dominant negative mutants of Fos and Jun. Proc. Natl. Acad. Sci. USA 87, 3806-3810 (1990).
32. Molina, G. et al. Zebrafish chemical screening reveals an inhibitor of Dusp6 that expands cardiac cell lineages. Nat. Chem. Biol. 5, 680-687 (2009).
33. Huang, T.S., Lee, S.C. & Lin, J.K. Suppression of c-Jun/AP-1 activation by an inhibitor of tumor promotion in mouse fibroblast cells. Proc. Natl. Acad. Sci. USA 88, 5292-5296 (1991).
34. Park, S., Lee, D.K. & Yang, C.H. Inhibition of fos-jun-DNA complex formation by dihydroguaiaretic acid and in vitro cytotoxic effects on cancer cells. Cancer Lett. 127, 23-28 (1998).
35. Padhye, S. et al. Fluorocurcumins as cyclooxygenase-2 inhibitor: molecular docking, pharmacokinetics and tissue distribution in mice. Pharm. Res. 26, 2438-2445 (2009).
36. Koschmieder, S. et al. Inducible chronic phase of myeloid leukemia with expansion of hematopoietic stem cells in a transgenic model of BCR-ABL leukemogenesis. Blood 105, 324-334 (2005).
37. Li, L. et al. Activation of p53 by SIRT1 inhibition enhances elimination of CML leukemia stem cells in combination with imatinib. Cancer Cell 21, 266-281 (2012).
38. Copland, M. et al. BMS-214662 potently induces apoptosis of chronic myeloid leukemia stem and progenitor cells and synergizes with tyrosine kinase inhibitors. Blood 111, 2843-2853 (2008).
39. Angel, P. & Karin, M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim. Biophys. Acta 1072, 129-157 (1991).
40. Owens, D.M. & Keyse, S.M. Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases. Oncogene 26, 3203-3213 (2007).
41. Boutros, T., Chevet, E. & Metrakos, P. Mitogen-activated protein (MAP) kinase/MAP kinase phosphatase regulation: roles in cell growth, death, and cancer. Pharmacol. Rev. 60, 261-310 (2008).
42. Groom, L.A., Sneddon, A.A., Alessi, D.R., Dowd, S. & Keyse, S.M. Differential regulation of the MAP, SAP and RK/p38 kinases by Pyst1, a novel cytosolic dual-specificity phosphatase. EMBO J. 15, 3621-3632 (1996).
43. Fjeld, C.C., Rice, A.E., Kim, Y., Gee, K.R. & Denu, J.M. Mechanistic basis for catalytic activation of mitogen-activated protein kinase phosphatase 3 by extracellular signal-regulated kinase. J. Biol. Chem. 275, 6749-6757 (2000).
44. Zhao, Q. et al. MAP kinase phosphatase 1 controls innate immune responses and suppresses endotoxic shock. J. Exp. Med. 203, 131-140 (2006).
45. Hirsch, D.D. & Stork, P.J. Mitogen-activated protein kinase phosphatases inactivate stress-activated protein kinase pathways in vivo. J. Biol. Chem. 272, 4568-4575 (1997).
46. Young, P.R. et al. Pyridinyl imidazole inhibitors of p38 mitogen-activated protein kinase bind in the ATP site. J. Biol. Chem. 272, 12116-12121 (1997).
47. Bennett, B.L. et al. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. USA 98, 13681-13686 (2001).
48. Shojaee, S. et al. Erk negative feedback control enables pre-B cell transformation and represents a therapeutic target in acute lymphoblastic leukemia. Cancer Cell 28, 114-128 (2015).
49. Hrustanovic, G. et al. RAS-MAPK dependence underlies a rational polytherapy strategy in EML4-ALK-positive lung cancer. Nat. Med. 21, 1038-1047 (2015).
50. Zhang, B. et al. Altered microenvironmental regulation of leukemic and normal stem cells in chronic myelogenous leukemia. Cancer Cell 21, 577-592 (2012).
51. Reynaud, D. et al. IL-6 controls leukemic multipotent progenitor cell fate and contributes to chronic myelogenous leukemia development. Cancer Cell 20, 661-673 (2011).
52. Welner, R.S. et al. Treatment of chronic myelogenous leukemia by blocking cytokine alterations found in normal stem and progenitor cells. Cancer Cell 27, 671-681 (2015).
53. Roberts, K.G. et al. Genetic alterations activating kinase and cytokine receptor signaling in high-risk acute lymphoblastic leukemia. Cancer Cell 22, 153-166 (2012).
54. Druker, B.J. et al. Activity of a specific inhibitor of the BCR-ABL tyrosine kinase in the blast crisis of chronic myeloid leukemia and acute lymphoblastic leukemia with the Philadelphia chromosome. N. Engl. J. Med. 344, 1038-1042 (2001).
55. Chang, K.H. et al. Vav3 collaborates with p190-BCR-ABL in lymphoid progenitor leukemogenesis, proliferation, and survival. Blood 120, 800-811 (2012).
56. Bagger, F.O. et al. BloodSpot: a database of gene expression profiles and transcriptional programs for healthy and malignant haematopoiesis. Nucleic Acids Res. 44D1, D917-D924 (2016).
57. Jørgensen, H.G., Allan, E.K., Jordanides, N.E., Mountford, J.C. & Holyoake, T.L. Nilotinib exerts equipotent antiproliferative effects to imatinib and does not induce apoptosis in CD34+ CML cells. Blood 109, 4016-4019 (2007).
58. Holyoake, T.L. & Vetrie, D. The chronic myeloid leukemia stem cell: stemming the tide of persistence. Blood https://dx.doi.org/10.1182/blood-2016-09-696013 (2017).
59. Kesarwani, M. et al. Targeting substrate-site in Jak2 kinase prevents emergence of genetic resistance. Sci. Rep. 5, 14538 (2015).
60. Azam, M., Seeliger, M.A., Gray, N.S., Kuriyan, J. & Daley, G.Q. Activation of tyrosine kinases by mutation of the gatekeeper threonine. Nat. Struct. Mol. Biol. 15, 1109-1118 (2008).
61. Komurov, K., Dursun, S., Erdin, S. & Ram, P.T. NetWalker: a contextual network analysis tool for functional genomics. BMC Genomics 13, 282 (2012).