Epigenetic therapy overcomes treatment resistance in T cell prolymphocytic leukemia

Science Translational Medicine

Volumn 7, Issue 293, 2015, Pages

  Hasanali, Zainul S ^a   Saroya, Bikramajit Singh ^b   Stuart, August ^a   Shimko, Sara ^a   Evans, Juanita ^a   Shah, Mithun Vinod ^c   Sharma, Kamal ^d   Leshchenko, Violetta V ^e   Parekh, Samir ^e   Loughran, Thomas P ^f   Epner, Elliot M ^g  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b ST GEORGE S UNIVERSITY   (Grenada)

^c MAYO CLINIC   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF VIRGINIA   (United States)

^g NEW MEXICO VA HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALEMTUZUMAB; BRENTUXIMAB VEDOTIN; CD30 ANTIBODY; CD30 ANTIGEN; CLADRIBINE; CYCLOPHOSPHAMIDE; PRALATREXATE; PREDNISONE; PROTEIN ANTIBODY; ROMIDEPSIN; UNCLASSIFIED DRUG; VALPROIC ACID; VINCRISTINE; VORINOSTAT; ANTIBODY CONJUGATE; ANTINEOPLASTIC AGENT; CHROMATIN; MESSENGER RNA; MONOCLONAL ANTIBODY; STAT5 PROTEIN;

ADULT; AGED; ARTICLE; CANCER IMMUNOTHERAPY; CLINICAL ARTICLE; EPIGENETICS; FEMALE; HUMAN; HUMAN CELL; MALE; MULTIPLE CYCLE TREATMENT; PILOT STUDY; PRIORITY JOURNAL; PROLYMPHOCYTIC LEUKEMIA; PROTEIN EXPRESSION; TREATMENT DURATION; TREATMENT OUTCOME; TREATMENT RESPONSE; BLOOD; CELL PROLIFERATION; CHROMATIN; CLINICAL TRIAL; DNA MICROARRAY; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; LEUKEMIA, PROLYMPHOCYTIC, T-CELL; LEUKOCYTE COUNT; METABOLISM; MIDDLE AGED; PATHOLOGY; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SKIN;

AGED; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, CD30; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL PROLIFERATION; CHROMATIN; DRUG RESISTANCE, NEOPLASM; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, LEUKEMIC; HUMANS; IMMUNOCONJUGATES; LEUKEMIA, PROLYMPHOCYTIC, T-CELL; LEUKOCYTE COUNT; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SKIN; STAT5 TRANSCRIPTION FACTOR; TREATMENT OUTCOME;

EID: 84937598746     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aaa5079     Document Type: Article

References (62)

1. T. Robak, P. Robak, Current treatment options in prolymphocytic leukemia. Med. Sci. Monit. 13, RA69-RA80 (2007).
2. C. E. Dearden, T-cell prolymphocytic leukemia. Med. Oncol. 23, 17-22 (2006).
3. E. Matutes, V. Brito-Babapulle, J. Swansbury, J. Ellis, R. Morilla, C. Dearden, A. Sempere, D. Catovsky, Clinical and laboratory features of 78 cases of T-prolymphocytic leukemia. Blood 78, 3269-3274 (1991).
4. R. Pawson, T. F. Schulz, E. Matutes, D. Catovsky, The human T-cell lymphotropic viruses types I/II are not involved in T prolymphocytic leukemia and large granular lymphocytic leukemia. Leukemia 11, 1305-1311 (1997).
5. C. Dearden, How I treat prolymphocytic leukemia. Blood 120, 538-551 (2012).
6. J. Mercieca, E. Matutes, C. Dearden, K. MacLennan, D. Catovsky, The role of pentostatin in the treatment of T-cell malignancies: Analysis of response rate in 145 patients according to disease subtype. J. Clin. Oncol. 12, 2588-2593 (1994).
7. S. Spurgeon, M. Yu, J. D. Phillips, E. M. Epner, Cladribine: Not just another purine analogue? Expert Opin. Investig. Drugs 18, 1169-1181 (2009).
8. L. Ginaldi, M. De Martinis, E. Matutes, N. Farahat, R. Morilla, M. J. Dyer, D. Catovsky, Levels of expression of CD52 in normal and leukemic B and T cells: Correlation with in vivo therapeutic responses to Campath-1H. Leuk. Res. 22, 185-191 (1998).
9. M. J. Keating, B. Cazin, S. Coutré, R. Birhiray, T. Kovacsovics, W. Langer, B. Leber, T. Maughan, K. Rai, G. Tjønnfjord, M. Bekradda, M. Itzhaki, P. Hérait, Campath-1H treatment of T-cell prolymphocytic leukemia in patients for whom at least one prior chemotherapy regimen has failed. J. Clin. Oncol. 20, 205-213 (2002).
10. H. Y. Lin, C. S. Chen, S. P. Lin, J. R. Weng, C. S. Chen, Targeting histone deacetylase in cancer therapy. Med. Res. Rev. 26, 397-413 (2006).
11. H. Fukuda, N. Sano, S. Muto, M. Horikoshi, Simple histone acetylation plays a complex role in the regulation of gene expression. Brief. Funct. Genomic. Proteomic. 5, 190-208 (2006).
12. D. Wyczechowska, K. Fabianowska-Majewska, The effects of cladribine and fludarabine on DNA methylation in K562 cells. Biochem. Pharmacol. 65, 219-225 (2003).
13. H. Gowher, A. Jeltsch, Mechanism of inhibition of DNA methyltransferases by cytidine analogs in cancer therapy. Cancer Biol. Ther. 3, 1062-1068 (2004).
14. O. Khan, N. B. La Thangue, HDAC inhibitors in cancer biology: Emerging mechanisms and clinical applications. Immunol. Cell Biol. 90, 85-94 (2012).
15. E. E. Cameron, K. E. Bachman, S. Myöhänen, J. G. Herman, S. B. Baylin, Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat. Genet. 21, 103-107 (1999).
16. S. Y. Lee, C. G. Park, Y. Choi, T cell receptor-dependent cell death of T cell hybridomas mediated by the CD30 cytoplasmic domain in association with tumor necrosis factor receptor-associated factors. J. Exp. Med. 183, 669-674 (1996).
17. S. Han, J. Koo, J. Bae, S. Kim, S. Baik, M. Y. Kim, Modulation of TNFSF expression in lymphoid tissue inducer cells by dendritic cells activated with Toll-like receptor ligands. BMB Rep. 44, 129-134 (2011).
18. P. Biswas, A. Galli, B. Capiluppi, D. Ciuffreda, A. Lazzarin, G. Tambussi, Selective enrichment of CD30-expressing cells within the blast region of lymphocytes from patients with primary HIV infection (PHI). J. Biol. Regul. Homeost. Agents 16, 33-36 (2002).
19. D. Saini, S. Ramachandran, A. Nataraju, N. Benshoff, W. Liu, N. Desai, W. Chapman, T. Mohanakumar, Activated effector and memory T cells contribute to circulating sCD30: Potential marker for islet allograft rejection. Am. J. Transplant. 8, 1798-1808 (2008).
20. M. A. Halim, T. Al-Otaibi, I. Al-Muzairai, M. Mansour, K. A. Tawab, W. H. Awadain, M. A. Balaha, T. Said, P. Nair, M. R. Nampoory, Serial soluble CD30 measurements as a predictor of kidney graft outcome. Transplant. Proc. 42, 801-803 (2010).
21. E. Kocabaş, A. Türel Ermertcan, S. Akinci, P. Temiz, K. Gündüz, Primary cutaneous CD30-positive anaplastic large cell lymphoma in a 16-year-old girl. Int. J. Dermatol. 51, 1353-1358 (2012).
22. R. Hussain, A. Bajoghli, Primary cutaneous CD30-positive large T-cell lymphoma in an 80-year-old man: A case report. ISRN Dermatol. 2011, 634042 (2011).
23. I. Maric, K. R. Calvo, Mastocytosis: The new differential diagnosis of CD30-positive neoplasms. Leuk. Lymphoma 52, 732-733 (2011).
24. M. Tarkowski, Expression and a role of CD30 in regulation of T-cell activity. Curr. Opin. Hematol. 10, 267-271 (2003).
25. J. A. Francisco, C. G. Cerveny, D. L. Meyer, B. J. Mixan, K. Klussman, D. F. Chace, S. X. Rejniak, K. A. Gordon, R. DeBlanc, B. E. Toki, C. L. Law, S. O. Doronina, C. B. Siegall, P. D. Senter, A. F. Wahl, cAC10-vcMMAE, an anti-CD30-monomethyl auristatin E conjugate with potent and selective antitumor activity. Blood 102, 1458-1465 (2003).
26. S.O.Doronina,B.E.Toki,M.Y.Torgov,B.A.Mendelsohn,C.G.Cerveny,D.F.Chace,R.L.DeBlanc, R. P. Gearing, T. D. Bovee, C. B. Siegall, J. A. Francisco, A. F. Wahl, D. L. Meyer, P. D. Senter, Development of potent monoclonal antibody auristatin conjugates for cancer therapy. Nat. Biotechnol. 21, 778-784 (2003).
27. A. Younes, U. Yasothan, P. Kirkpatrick, Brentuximab vedotin. Nat. Rev. Drug Discov. 11, 19-20 (2012).
28. V. V. Leshchenko, Z. Hasanali, A. Stuart, S. Shimko, S. E. Spurgeon, S. Parekh, E. M. Epner, Combined epigenetic and immunotherapy for newly diagnosed mantle cell lymphoma: Correlative studies suggest the importance of enhanced ADCC, mechanisms of resistance and cyclin D1 nuclear localization genotype. 2013 Annual Meeting Abstracts, American Society of Hematology, New Orleans, LA, 7 to 10 December 2013, abstract 3063.
29. X. Sun, Z. S. Hasanali, A. Chen, D. Zhang, X. Liu, H. G. Wang, D. J. Feith, T. P. Loughran Jr., K. Xu, Suberoylanilide hydroxamic acid (SAHA) and cladribine synergistically induce apoptosis in NK-LGL leukaemia. Br. J. Haematol. 168, 371-383 (2014).
30. K. Sharma, Z. Hasanali, S. Spurgeon, C. Okada, A. Stuart, S. Shimko, V. Leshchenko, S. Parekh, Y. Chen, M. Kirschbaum, E. M. Epner, Proceedings: AACR 104th Annual Meeting 2013, American Association for Cancer Research, Washington, DC, 6 to 10 April 2013, abstract LBA140.
31. B. Krawczyk, K. Rudnicka, K. Fabianowska-Majewska, The effects of nucleoside analogues on promoter methylation of selected tumor suppressor genes in MCF-7 and MDA-MB-231 breast cancer cell lines. Nucleosides Nucleotides Nucleic Acids 26, 1043-1046 (2007).
32. M. Göttlicher, S. Minucci, P. Zhu, O. H. Krämer, A. Schimpf, S. Giavara, J. P. Sleeman, F. Lo Coco, C. Nervi, P. G. Pelicci, T. Heinzel, Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J. 20, 6969-6978 (2001).
33. A. Cuker, A. J. Coles, H. Sullivan, E. Fox, M. Goldberg, P. Oyuela, A. Purvis, D. S. Beardsley, D. H. Margolin, A distinctive form of immune thrombocytopenia in a phase 2 study of alemtuzumab for the treatment of relapsing-remitting multiple sclerosis. Blood 118, 6299-6305 (2011).
34. L. E. Ludlow, R. W. Johnstone, C. J. Clarke, The HIN-200 family: More than interferoninducible genes? Exp. Cell Res. 308, 1-17 (2005).
35. J. Tsukada, Y. Yoshida, Y. Kominato, P. E. Auron, The CCAAT/enhancer (C/EBP) family of basic-leucine zipper (bZIP) transcription factors is a multifaceted highly-regulated system for gene regulation. Cytokine 54, 6-19 (2011).
36. J. Kim, H. Kim, Recruitment and biological consequences of histone modification of H3K27me3 and H3K9me3. ILAR J. 53, 232-239 (2012).
37. E. Le Toriellec, G. Despouy, G. Pierron, N. Gaye, M. Joiner, D. Bellanger, A. Vincent-Salomon, M. H. Stern, Haploinsufficiency of CDKN1B contributes to leukemogenesis in T-cell prolymphocytic leukemia. Blood 111, 2321-2328 (2008).
38. A. Yokohama, A. Saitoh, H. Nakahashi, T. Mitsui, H. Koiso, Y. Kim, H. Uchiumi, T. Saitoh, H. Handa, T. Jimbo, K. Murayama, T. Sakura, H. Murakami, M. Karasawa, Y. Nojima, N. Tsukamoto, TCL1A gene involvement in T-cell prolymphocytic leukemia in Japanese patients. Int. J. Hematol. 95, 77-85 (2012).
39. P. J. De Schouwer, M. J. Dyer, V. B. Brito-Babapulle, E. Matutes, D. Catovsky, M. R. Yuille, T-cell prolymphocytic leukaemia: Antigen receptor gene rearrangement and a novel mode of MTCP1 B1 activation. Br. J. Haematol. 110, 831-838 (2000).
40. J. Roos, I. Hennig, J. Schwaller, J. Zbären, R. Dummer, G. Burg, A. Tobler, L. Virgilio, C. M. Croce, M. F. Fey, B. Borisch, Expression of TCL1 in hematologic disorders. Pathobiology 69, 59-66 (2001).
41. Y. Pekarsky, C. Hallas, C. M. Croce, Targeting mature T cell leukemia: New understanding of molecular pathways. Am. J. Pharmacogenomics 3, 31-36 (2003).
42. C. E. Dearden, A. Khot, M. Else, M. Hamblin, E. Grand, A. Roy, S. Hewamana, E. Matutes, D. Catovsky, Alemtuzumab therapy in T-cell prolymphocytic leukemia: Comparing efficacy in a series treated intravenously and a study piloting the subcutaneous route. Blood 118, 5799-5802 (2011).
43. C. E. Dearden, E. Matutes, B. Cazin, G. E. Tjønnfjord, A. Parreira, B. Nomdedeu, P. Leoni, F. J. Clark, D. Radia, S. M. Rassam, T. Roques, N. Ketterer, V. Brito-Babapulle, M. J. Dyer, D. Catovsky, High remission rate in T-cell prolymphocytic leukemia with CAMPATH-1H. Blood 98, 1721-1726 (2001).
44. Z. S. Hasanali, E. M. Epner, D. J. Feith, T. P. Loughran Jr., C. E. Sample, Vorinostat down-regulates CD30 and decreases brentuximab vedotin efficacy in human lymphocytes. Mol. Cancer Ther. 13, 2784-2792 (2014).
45. R. A. Clark, R. Watanabe, J. E. Teague, C. Schlapbach, M. C. Tawa, N. Adams, A. A. Dorosario, K. S. Chaney, C. S. Cutler, N. R. Leboeuf, J. B. Carter, D. C. Fisher, T. S. Kupper, Skin effector memory T cells do not recirculate and provide immune protection in alemtuzumab-treated CTCL patients. Sci. Transl. Med. 4, 117ra117 (2012).
46. P. Gade, S. K. Roy, H. Li, S. C. Nallar, D. V. Kalvakolanu, Critical role for transcription factor C/EBP-β in regulating the expression of death-associated protein kinase 1. Mol. Cell Biol. 28, 2528-2548 (2008).
47. H. Li, P. Gade, W. Xiao, D. V. Kalvakolanu, The interferon signaling network and transcription factor C/EBP-b. Cell. Mol. Immunol. 4, 407-418 (2007).
48. E. Kiss-Toth, S. M. Bagstaff, H. Y. Sung, V. Jozsa, C. Dempsey, J. C. Caunt, K. M. Oxley, D. H. Wyllie, T. Polgar, M. Harte, L. A. O'Neill, E. E. Qwarnstrom, S. K. Dower, Human tribbles, a protein family controlling mitogen-activated protein kinase cascades. J. Biol. Chem. 279, 42703-42708 (2004).
49. H. Y. Sung, S. E. Francis, D. C. Crossman, E. Kiss-Toth, Regulation of expression and signalling modulator function of mammalian tribbles is cell-type specific. Immunol. Lett. 104, 171-177 (2006).
50. M. Yamamoto, S. Uematsu, T. Okamoto, Y. Matsuura, S. Sato, H. Kumar, T. Satoh, T. Saitoh, K. Takeda, K. J. Ishii, O. Takeuchi, T. Kawai, S. Akira, Enhanced TLR-mediated NF-IL6-dependent gene expression by Trib1 deficiency. J. Exp. Med. 204, 2233-2239 (2007). Downloaded from on June 25, 2015
51. waf-1 and arrests macrophage cell cycle, preventing induction of apoptosis. Immunity 11, 103-113 (1999).
52. α2 to the membrane receptors of Daudi cells. Eur. J. Biochem. 134, 355-364 (1983).
53. H. L. Rajala, S. Eldfors, H. Kuusanmaki, A. J. van Adrichem, T. Olson, S. Lagström, E. I. Andersson, A. Jerez, M. J. Clemente, Y. Yan, D. Zhang, A. Awwad, P. Ellonen, O. Kallioniemi, K. Wennerberg, K. Porkka, J. P. Maciejewski, T. P. Loughran Jr., C. Heckman, S. Mustjoki, Discovery of somatic STAT5b mutations in large granular lymphocytic leukemia. Blood 121, 4541-4550 (2013).
54. O. R. Bandapalli, S. Schuessele, J. B. Kunz, T. Rausch, A. M. Stütz, N. Tal, I. Geron, N. Gershman, S. Izraeli, J. Eilers, N. Vaezipour, R. Kirschner-Schwabe, J. Hof, A. von Stackelberg, M. Schrappe, M. Stanulla, M. Zimmermann, R. Koehler, S. Avigad, R. Handgretinger, V. Frismantas, J. P. Bourquin, B. Bornhauser, J. O. Korbel, M. U. Muckenthaler, A. E. Kulozik, The activating STAT5B N642H mutation is a common abnormality in pediatric T-cell acute lymphoblastic leukemia and confers a higher risk of relapse. Haematologica 99, e188-e192 (2014).
55. C. Küçük, B. Jiang, X. Hu, W. Zhang, J. K. Chan, W. Xiao, N. Lack, C. Alkan, J. C. Williams, K. N. Avery, P. Kavak, A. Scuto, E. Sen, P. Gaulard, L. Staudt, J. Iqbal, A. Cornish, Q. Gong, Q. Yang, H. Sun, F. d'Amore, S. Leppä, W. Liu, K. Fu, L. de Leval, T. McKeithan, W. C. Chan, Activating mutations of STAT5B and STAT3 in lymphomas derived from gd-T or NK cells. Nat. Commun. 6, 6025 (2015).
56. M. J. Kiel, T. Velusamy, D. Rolland, A. A. Sahasrabuddhe, F. Chung, N. G. Bailey, A. Schrader, B. Li, J. Z. Li, A. B. Ozel, B. L. Betz, R. N. Miranda, L. J. Medeiros, L. Zhao, M. Herling, M. S. Lim, K. S. Elenitoba-Johnson, Integrated genomic sequencing reveals mutational landscape of T-cell prolymphocytic leukemia. Blood 124, 1460-1472 (2014).
57. B. Khulan, R. F. Thompson, K. Ye, M. J. Fazzari, M. Suzuki, E. Stasiek, M. E. Figueroa, J. L. Glass, Q. Chen, C. Montagna, E. Hatchwell, R. R. Selzer, T. A. Richmond, R. D. Green, A. Melnick, J. M. Greally, Comparative isoschizomer profiling of cytosine methylation: The HELP assay. Genome Res. 16, 1046-1055 (2006).
58. R. Shaknovich, M. E. Figueroa, A. Melnick, HELP (HpaII tiny fragment enrichment by ligation-mediated PCR) assay for DNA methylation profiling of primary normal and malignant B lymphocytes. Methods Mol. Biol. 632, 191-201 (2010).
59. V. V. Leshchenko, P. Y. Kuo, R. Shaknovich, D. T. Yang, T. Gellen, A. Petrich, Y. Yu, Y. Remache, M. A. Weniger, S. Rafiq, K. S. Suh, A. Goy, W. Wilson, A. Verma, I. Braunschweig, N. Muthusamy, B. S. Kahl, J. C. Byrd, A. Wiestner, A. Melnick, S. Parekh, Genomewide DNA methylation analysis reveals novel targets for drug development in mantle cell lymphoma. Blood 116, 1025-1034 (2010).
60. R. F. Thompson, M. Suzuki, K. W. Lau, J. M. Greally, A pipeline for the quantitative analysis of CG dinucleotide methylation using mass spectrometry. Bioinformatics 25, 2164-2170 (2009).
61. E. Tuset, E. Matutes, V. Brito-Babapulle, R. Morilla, D. Catovsky, Immunophenotype changes and loss of CD52 expression in two patients with relapsed T-cell prolymphocytic leukaemia. Leuk. Lymphoma 42, 1379-1383 (2001).
62. S. Göçmen, M. Kutlay, A. Erikçi, C. Atabey, O. Sayan, A. Haholu, Central nervous system involvement of T-cell prolymphocytic leukemia diagnosed with stereotactic brain biopsy: Case report. Turkish J. Haematol. 31, 75-78 (2014).