Tyrosine kinase inhibitor-induced CD70 expression mediates drug resistance in leukemia stem cells by activating Wnt signaling

Science Translational Medicine

Volumn 7, Issue 298, 2015, Pages

  Riether, Carsten ^a   Schürch, Christian M ^a,b   Flury, Christoph ^a   Hinterbrandner, Magdalena ^a   Drück, Linda ^a   Huguenin, Anne Laure ^a   Baerlocher, Gabriela M ^c   Radpour, Ramin ^a   Ochsenbein, Adrian F ^a,c  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; CD70 ANTIGEN; IMATINIB; MICRORNA 29; NILOTINIB; PONATINIB; PROTEIN TYROSINE KINASE INHIBITOR; TRANSCRIPTION FACTOR SP1; WNT PROTEIN; CD27 ANTIGEN; CD70 PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CANCER STEM CELL; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; HUMAN; HUMAN CELL; LEUKEMIA RELAPSE; LEUKEMIA REMISSION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; TUMOR XENOGRAFT; UPREGULATION; WNT SIGNALING PATHWAY; ANIMAL; ANTAGONISTS AND INHIBITORS; CANCER TRANSPLANTATION; DRUG EFFECTS; DRUG RESISTANCE; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; METABOLISM; MOUSE; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD27; ANTIGENS, CD70; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MICE; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; WNT SIGNALING PATHWAY;

EID: 84938352209     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aab1740     Document Type: Article

References (53)

1. E. Kavalerchik, D. Goff, C. H. Jamieson, Chronic myeloid leukemia stem cells. J. Clin. Oncol. 26, 2911-2915 (2008).
2. B. J. Druker, M. Talpaz, D. J. Resta, B. Peng, E. Buchdunger, J. M. Ford, N. B. Lydon, H. Kantarjian, R. Capdeville, S. Ohno-Jones, C. L. Sawyers, Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N. Engl. J. Med. 344, 1031-1037 (2001).
3. A. S. Corbin, A. Agarwal, M. Loriaux, J. Cortes, M. W. Deininger, B. J. Druker, Human chronic myeloid leukemia stem cells are insensitive to imatinib despite inhibition of BCR-ABL activity. J. Clin. Invest. 121, 396-409 (2011).
4. A. Hamilton, G. V. Helgason, M. Schemionek, B. Zhang, S. Myssina, E. K. Allan, F. E. Nicolini, C. Müller-Tidow, R. Bhatia, V. G. Brunton, S. Koschmieder, T. L. Holyoake, Chronic myeloid leukemia stem cells are not dependent on Bcr-Abl kinase activity for their survival. Blood 119, 1501-1510 (2012).
5. M. Savona, M. Talpaz, Getting to the stem of chronic myeloid leukaemia. Nat. Rev. Cancer 8, 341-350 (2008).
6. S. Faderl, M. Talpaz, Z. Estrov, S. O'Brien, R. Kurzrock, H. M. Kantarjian, The biology of chronic myeloid leukemia. N. Engl. J. Med. 341, 164-172 (1999).
7. A. M. Coluccia, A. Vacca, M. Duñach, L. Mologni, S. Redaelli, V. H. Bustos, D. Benati, L. A. Pinna, C. Gambacorti-Passerini, Bcr-Abl stabilizes β-catenin in chronic myeloid leukemia through its tyrosine phosphorylation. EMBO J. 26, 1456-1466 (2007).
8. C. Zhao, J. Blum, A. Chen, H. Y. Kwon, S. H. Jung, J. M. Cook, A. Lagoo, T. Reya, Loss of β-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell 12, 528-541 (2007).
9. F. H. Heidel, L. Bullinger, Z. Feng, Z. Wang, T. A. Neff, L. Stein, D. Kalaitzidis, S. W. Lane, S. A. Armstrong, Genetic and pharmacologic inhibition of β-catenin targets imatinib-resistant leukemia stem cells in CML. Cell Stem Cell 10, 412-424 (2012).
10. M. A. Nolte, R. W. van Olffen, K. P. van Gisbergen, R. A. van Lier, Timing and tuning of CD27-CD70 interactions: The impact of signal strength in setting the balance between adaptive responses and immunopathology. Immunol. Rev. 229, 216-231 (2009).
11. A. Wiesmann, R. L. Phillips, M. Mojica, L. J. Pierce, A. E. Searles, G. J. Spangrude, I. Lemischka, Expression of CD27 on murine hematopoietic stem and progenitor cells. Immunity 12, 193-199 (2000).
12. C. Schürch, C. Riether, M. S. Matter, A. Tzankov, A. F. Ochsenbein, CD27 signaling on chronic myelogenous leukemia stem cells activates Wnt target genes and promotes disease progression. J. Clin. Invest. 122, 624-638 (2012).
13. C. Riether, C. M. Schürch, A. F. Ochsenbein, Regulation of hematopoietic and leukemic stem cells by the immune system. Cell Death Differ. 22, 187-198 (2015).
14. I. S. Grewal, CD70 as a therapeutic target in human malignancies. Expert Opin. Ther. Targets 12, 341-351 (2008).
15. Q. Lu, A. Wu, B. C. Richardson, Demethylation of the same promoter sequence increases CD70 expression in lupus T cells and T cells treated with lupus-inducing drugs. J. Immunol. 174, 6212-6219 (2005).
16. M. W. Deininger, Optimizing therapy of chronic myeloid leukemia. Exp. Hematol. 35, 144-154 (2007).
17. M. Koren-Michowitz, Y. Volchek, E. Naparstek, I. Gavish, I. Levi, J. M. Rowe, A. Shimoni, A. Nagler, Imatinib plasma trough levels in chronic myeloid leukaemia: Results of a multicentre study CSTI571AIL11TGLIVEC. Hematol. Oncol. 30, 200-205 (2012).
18. T. O'Hare, W. C. Shakespeare, X. Zhu, C. A. Eide, V. M. Rivera, F. Wang, L. T. Adrian, T. Zhou, W. S. Huang, Q. Xu, C. A. Metcalf III, J. W. Tyner, M. M. Loriaux, A. S. Corbin, S. Wardwell, Y. Ning, J. A. Keats, Y. Wang, R. Sundaramoorthi, M. Thomas, D. Zhou, J. Snodgrass, L. Commodore, T. K. Sawyer, D. C. Dalgarno, M. W. Deininger, B. J. Druker, T. Clackson, AP24534, a pan-BCR-ABL inhibitor for chronic myeloid leukemia, potently inhibits the T315I mutant and overcomes mutation-based resistance. Cancer Cell 16, 401-412 (2009).
19. J. E. Cortes, H. Kantarjian, N. P. Shah, D. Bixby, M. J. Mauro, I. Flinn, T. O'Hare, S. Hu, N. I. Narasimhan, V. M. Rivera, T. Clackson, C. D. Turner, F. G. Haluska, B. J. Druker, M. W. Deininger, M. Talpaz, Ponatinib in refractory Philadelphia chromosome-positive leukemias. N. Engl. J. Med. 367, 2075-2088 (2012).
20. C. M. Hedgepeth, L. J. Conrad, J. Zhang, H. C. Huang, V. M. Lee, P. S. Klein, Activation of the Wnt signaling pathway: A molecular mechanism for lithium action. Dev. Biol. 185, 82-91 (1997).
21. K. A. Kim, M. Wagle, K. Tran, X. Zhan, M. A. Dixon, S. Liu, D. Gros, W. Korver, S. Yonkovich, N. Tomasevic, M. Binnerts, A. Abo, R-Spondin family members regulate the Wnt pathway by a common mechanism. Mol. Biol. Cell 19, 2588-2596 (2008).
22. S. Liu, L. C. Wu, J. Pang, R. Santhanam, S. Schwind, Y. Z. Wu, C. J. Hickey, J. Yu, H. Becker, K. Maharry, M. D. Radmacher, C. Li, S. P. Whitman, A. Mishra, N. Stauffer, A. M. Eiring, R. Briesewitz, R. A. Baiocchi, K. K. Chan, P. Paschka, M. A. Caligiuri, J. C. Byrd, C. M. Croce, C. D. Bloomfield, D. Perrotti, R. Garzon, G. Marcucci, Sp1/NFκB/HDAC/miR-29b regulatory network in KIT-driven myeloid leukemia. Cancer Cell 17, 333-347 (2010).
23. M. Tan, J. Wu, Y. Cai, Suppression of Wnt signaling by the miR-29 family is mediated by demethylation of WIF-1 in non-small-cell lung cancer. Biochem. Biophys. Res. Commun. 438, 673-679 (2013).
24. K. Kapinas, C. Kessler, T. Ricks, G. Gronowicz, A. M. Delany, miR-29 modulates Wnt signaling in human osteoblasts through a positive feedback loop. J. Biol. Chem. 285, 25221-25231 (2010).
25. J. K. Christman, 5-Azacytidine and 5-aza-2'-deoxycytidine as inhibitors of DNA methylation: Mechanistic studies and their implications for cancer therapy. Oncogene 21, 5483-5495 (2002).
26. F. Belloc, F. Moreau-Gaudry, M. Uhalde, L. Cazalis, M. Jeanneteau, F. Lacombe, V. Praloran, F. X. Mahon, Imatinib and nilotinib induce apoptosis of chronic myeloid leukemia cells through a Bim-dependant pathway modulated by cytokines. Cancer Biol. Ther. 6, 912-919 (2007).
27. T. C. Chou, Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res. 70, 440-446 (2010).
28. K. Silence, T. Dreier, M. Moshir, P. Ulrichts, S. M. Gabriels, M. Saunders, H. Wajant, P. Brouckaert, L. Huyghe, T. Van Hauwermeiren, A. Thibault, H. J. De Haard, ARGX-110, a highly potent antibody targeting CD70, eliminates tumors via both enhanced ADCC and immune checkpoint blockade. mAbs 6, 523-532 (2014).
29. B. Zhang, A. C. Strauss, S. Chu, M. Li, Y. Ho, K. D. Shiang, D. S. Snyder, C. S. Huettner, L. Shultz, T. Holyoake, R. Bhatia, Effective targeting of quiescent chronic myelogenous leukemia stem cells by histone deacetylase inhibitors in combination with imatinib mesylate. Cancer Cell 17, 427-442 (2010).
30. L. Li, L. Wang, L. Li, Z. Wang, Y. Ho, T. McDonald, T. L. Holyoake, W. Chen, R. Bhatia, Activation of p53 by SIRT1 inhibition enhances elimination of CML leukemia stem cells in combination with imatinib. Cancer Cell 21, 266-281 (2012).
31. null mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 174, 6477-6489 (2005).
32. A. Wilson, E. Laurenti, G. Oser, R. C. van der Wath, W. Blanco-Bose, M. Jaworski, S. Offner, C. F. Dunant, L. Eshkind, E. Bockamp, P. Lió, H. R. Macdonald, A. Trumpp, Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135, 1118-1129 (2008).
33. S. J. Neering, T. Bushnell, S. Sozer, J. Ashton, R. M. Rossi, P. Y. Wang, D. R. Bell, D. Heinrich, A. Bottaro, C. T. Jordan, Leukemia stem cells in a genetically defined murine model of blast-crisis CML. Blood 110, 2578-2585 (2007).
34. A. Nakajima, H. Oshima, C. Nohara, S. Morimoto, S. Yoshino, T. Kobata, H. Yagita, K. Okumura, Involvement of CD70-CD27 interactions in the induction of experimental autoimmune encephalomyelitis. J. Neuroimmunol. 109, 188-196 (2000).
35. J. M. Kelly, P. K. Darcy, J. L. Markby, D. I. Godfrey, K. Takeda, H. Yagita, M. J. Smyth, Induction of tumor-specific T cell memory by NK cell-mediated tumor rejection. Nat. Immunol. 3, 83-90 (2002).
36. B. Zhang, Y. W. Ho, Q. Huang, T. Maeda, A. Lin, S. U. Lee, A. Hair, T. L. Holyoake, C. Huettner, R. Bhatia, Altered microenvironmental regulation of leukemic and normal stem cells in chronic myelogenous leukemia. Cancer Cell 21, 577-592 (2012).
37. M. Y. Konopleva, C. T. Jordan, Leukemia stem cells and microenvironment: Biology and therapeutic targeting. J. Clin. Oncol. 29, 591-599 (2011).
38. C. A. Huff, W. H. Matsui, B. D. Smith, R. J. Jones, Strategies to eliminate cancer stem cells: Clinical implications. Eur. J. Cancer 42, 1293-1297 (2006).
39. M. A. Essers, A. Trumpp, Targeting leukemic stem cells by breaking their dormancy. Mol. Oncol. 4, 443-450 (2010).
40. M. Dean, T. Fojo, S. Bates, Tumour stem cells and drug resistance. Nat. Rev. Cancer 5, 275-284 (2005).
41. M. B. Meads, L. A. Hazlehurst, W. S. Dalton, The bone marrow microenvironment as a tumor sanctuary and contributor to drug resistance. Clin. Cancer Res. 14, 2519-2526 (2008).
42. S. W. Lane, D. T. Scadden, D. G. Gilliland, The leukemic stem cell niche: Current concepts and therapeutic opportunities. Blood 114, 1150-1157 (2009).
43. B. Zhang, M. Li, T. McDonald, T. L. Holyoake, R. T. Moon, D. Campana, L. Shultz, R. Bhatia, Microenvironmental protection of CML stem and progenitor cells from tyrosine kinase inhibitors through N-cadherin and Wnt-β-catenin signaling. Blood 121, 1824-1838 (2013).
44. C. Schürch, C. Riether, M. A. Amrein, A. F. Ochsenbein, Cytotoxic T cells induce proliferation of chronic myeloid leukemia stem cells by secreting interferon-γ. J. Exp. Med. 210, 605-621 (2013).
45. J. Wischhusen, G. Jung, I. Radovanovic, C. Beier, J. P. Steinbach, A. Rimner, H. Huang, J. B. Schulz, H. Ohgaki, A. Aguzzi, H. G. Rammensee, M. Weller, Identification of CD70-mediated apoptosis of immune effector cells as a novel immune escape pathway of human glioblastoma. Cancer Res. 62, 2592-2599 (2002).
46. M. B. Bernstein, C. T. Garnett, H. Zhang, A. Velcich, M. M. Wattenberg, S. R. Gameiro, S. Kalnicki, J. W. Hodge, C. Guha, Radiation-induced modulation of costimulatory and coinhibitory T-cell signaling molecules on human prostate carcinoma cells promotes productive antitumor immune interactions. Cancer Biother. Radiopharm. 29, 153-161 (2014).
47. S. Dhut, B. Gibbons, T. Chaplin, B. D. Young, Establishment of a lymphoblastoid cell line, SD-1, expressing the p190 bcr-abl chimaeric protein. Leukemia 5, 49-55 (1991).
48. E. Klein, H. Ben-Bassat, H. Neumann, P. Ralph, J. Zeuthen, A. Polliack, F. Vánky, Properties of the K562 cell line, derived from a patient with chronic myeloid leukemia. Int. J. Cancer 18, 421-431 (1976).
49. B. Scappini, S. Gatto, F. Onida, C. Ricci, V. Divoky, W. G. Wierda, M. Andreeff, L. Dong, K. Hayes, S. Verstovsek, H. M. Kantarjian, M. Beran, Changes associated with the development of resistance to imatinib (STI571) in two leukemia cell lines expressing p210 Bcr/Abl protein. Cancer 100, 1459-1471 (2004).
50. R. Radpour, M. M. Haghighi, A. X. Fan, P. M. Torbati, S. Hahn, W. Holzgreve, X. Y. Zhong, High-throughput hacking of the methylation patterns in breast cancer by in vitro transcription and thymidine-specific cleavage mass array on MALDI-TOF silico-chip. Mol. Cancer Res. 6, 1702-1709 (2008).
51. I. M. Carr, J. I. Robinson, R. Dimitriou, A. F. Markham, A. W. Morgan, D. T. Bonthron, Inferring relative proportions of DNA variants from sequencing electropherograms. Bioinformatics 25, 3244-3250 (2009).
52. S. Mumprecht, C. Schürch, J. Schwaller, M. Solenthaler, A. F. Ochsenbein, Programmed death 1 signaling on chronic myeloid leukemia-specific T cells results in T-cell exhaustion and disease progression. Blood 114, 1528-1536 (2009).
53. H. Clevers, R. Nusse, Wnt/β-catenin signaling and disease. Cell 149, 1192-1205 (2012).