Topoisomerase inhibitors modulate expression of melanocytic antigens and enhance T cell recognition of tumor cells

Cancer Immunology, Immunotherapy

Volumn 60, Issue 1, 2011, Pages 133-144

  Haggerty, Timothy J ^a,b   Dunn, Ian S ^a   Rose, Lenora B ^a   Newton, Estelle E ^a   Martin, Sunil ^c   Riley, James L ^c   Kurnick, James T ^b  

^a CytoCure LLC   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Immunotherapy; Melan A MART 1; Melanoma; Topoisomerase inhibitors

Indexed keywords

AG 1387; APIGENIN; BETA LAPACHONE; CAMPTOTHECIN; DAUNORUBICIN; DNA TOPOISOMERASE INHIBITOR; DOXORUBICIN; ELLIPTICINE; EPIRUBICIN; ETOPOSIDE; GAMMA INTERFERON; HYDROXYCAMPTOTHECIN; IDARUBICIN; INTERLEUKIN 2; KAEMPFEROL; MELAN A; MELANOMA ANTIGEN; MERBARONE; NOVOBIOCIN; RUBITECAN; SOBUZOXANE; T LYMPHOCYTE RECEPTOR; TOPOTECAN; UNCLASSIFIED DRUG; XK 469;

ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG MECHANISM; GENETIC TRANSFECTION; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; LYMPHOCYTE FUNCTION; MELANOMA CELL; PRIORITY JOURNAL; T LYMPHOCYTE; UPREGULATION;

ANTIGEN PRESENTATION; CD8-POSITIVE T-LYMPHOCYTES; COCULTURE TECHNIQUES; DAUNORUBICIN; DNA TOPOISOMERASES; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; IMMUNOTHERAPY; INTERFERON-GAMMA; INTERLEUKIN-2; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MART-1 ANTIGEN; MELANOMA; RECEPTORS, ANTIGEN, T-CELL; TRANSGENES;

EID: 79953744905     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-010-0926-x     Document Type: Article

References (64)

1. Pandolfi F, Cianci R, Lolli S, Dunn IS, Newton EE, Haggerty TJ, Boyle LA, Kurnick JT (2008) Strategies to overcome obstacles to successful immunotherapy of melanoma. Int J Immunopathol Pharmacol 21:493-500
2. Durda PJ, Dunn IS, Rose LB, Butera D, Benson EM, Pandolfi F, Kurnick JT (2003) Induction of "Antigen silencing" in melanomas by oncostatin M: down-modulation of melanocyte antigen expression. Mol Cancer Res 1:411-419
3. Dunn GP, Bruce AT, Sheehan KC, Shankaran V, Uppaluri R, Bui JD, Diamond MS, Koebel CM, Arthur C, White JM, Schreiber RD (2005) A critical function for type I interferons in cancer immunoediting. Nat Immunol 6:722-729 (Pubitemid 41716746)
4. Levy C, Khaled M, Fisher DE (2006) Mitf: master regulator of melanocyte development and melanoma oncogene. Trends Mol Med 12:406-414 (Pubitemid 44291572)
5. Cheli Y, Ohanna M, Ballotti R, Bertolotto C (2010) Fifteen-year quest for microphthalmia-associated transcription factor target genes. Pigment Cell Melanoma Res 23:27-40
6. Kurnick JT, Ramirez-Montagut T, Boyle LA, Andrews DM, Pandolfis F, Durda PJ, Butera D, Dunn IS, Benson EM, Gobin SJ, van den Elsen PJ (2001) A novel autocrine pathway of tumor escape from immune recognition: melanoma cell lines produce a soluble protein that diminishes expression of the gene encoding the melanocyte lineage Melan-a/Mart-1 antigen through down-modulation of its promoter. J Immunol 167:1204-1211 (Pubitemid 32703114)
7. Kono M, Dunn I, Durda P, Butera D, Rose LB, Haggerty T, Benson E, Kurnick J (2006) Role of the MAP kinase signaling pathway in the regulation of human melanocytic antigen expression. Mol Cancer Res 4:779-792 (Pubitemid 44683317)
8. Dunn IS, Haggerty TJ, Kono M, Durda PJ, Butera D, Macdonald DB, Benson EM, Rose LB, Kurnick JT (2007) Enhancement of human melanoma antigen expression by IFN-β. J Immunol 179:2134-2142
9. Scharovsky OG, Mainetti LE, Rozados VR (2009) Metronomic chemotherapy: changing the paradigm that more is better. Curr Oncol 16:7-15
10. Kerbel RS, Kamen BA (2004) The anti-angiogenic basis of metronomic chemotherapy. Nat Rev Cancer 4:423-436 (Pubitemid 38745528)
11. Menard C, Martin F, Apetoh L, Bouyer F, Ghiringhelli F (2008) Cancer chemotherapy: not only a direct cytotoxic effect, but also an adjuvant for antitumor immunity. Cancer Immunol Immunother 57:1579-1587
12. Ghiringhelli F, Menard C, Puig PE, Ladoire S, Roux S, Martin F, Solary E, Le Cesne A, Zitvogel L, Chauffert B (2007) Metronomic cyclophosphamide regimen selectively depletes CD4+ CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol Immunother 56:641-648 (Pubitemid 46348738)
13. Banissi C, Ghiringhelli F, Chen L, Carpentier AF (2009) Treg depletion with a low-dose metronomic temozolomide regimen in a rat glioma model. Cancer Immunol Immunother 58:1627-1634
14. Ju BG, Lunyak VV, Perissi V, Garcia-Bassets I, Rose DW, Glass CK, Rosenfeld MG (2006) A topoisomerase II beta-mediated dsDNA break required for regulated transcription. Science 312:1798-1802 (Pubitemid 43962898)
15. Lotito L, Russo A, Chillemi G, Bueno S, Cavalieri D, Capranico G (2008) Global transcription regulation by DNA topoisomerase I in exponentially growing Saccharomyces cerevisiae cells: activation of telomere-proximal genes by top1 deletion. J Mol Biol 377:311-322
16. Eller MS, Ostrom K, Gilchrest BA (1996) DNA damage enhances melanogenesis. Proc Natl Acad Sci USA 93:1087-1092 (Pubitemid 26052846)
17. Park HY, Kosmadaki M, Yaar M, Gilchrest BA (2009) Cellular mechanisms regulating human melanogenesis. Cell Mol Life Sci 66:1493-1506
18. Inomata K, Aoto T, Binh NT, Okamoto N, Tanimura S, Wakayama T, Iseki S, Hara E, Masunaga T, Shimizu H, Nishimura EK (2009) Genotoxic stress abrogates renewal of melanocyte stem cells by triggering their differentiation. Cell 137:1088-1099
19. Wilstermann AM, Osheroff N (2003) Stabilization of eukaryotic topoisomerase II-DNA cleavage complexes. Curr Top Med Chem 3:321-338
20. Pommier Y (2006) Topoisomerase I inhibitors: camptothecins and beyond. Nat Rev Cancer 6:789-802
21. Deweese JE, Osheroff N (2009) The DNA cleavage reaction of topoisomerase II: Wolf in sheep's clothing. Nucleic Acids Res 37:738-748
22. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55-63
23. Dietrich PY, Le Gal FA, Dutoit V, Pittet MJ, Trautman L, Zippelius A, Cognet I, Widmer V, Walker PR, Michielin O, Guillaume P, Connerotte T, Jotereau F, Coulie PG, Romero P, Cerottini JC, Bonneville M, Valmori D (2003) Prevalent role of TCR alphachain in the selection of the preimmune repertoire specific for a human tumor-associated self-antigen. J Immunol 170:5103-5109 (Pubitemid 36554741)
24. Jorritsma A, Gomez-Eerland R, Dokter M, van de Kasteele W, Zoet YM, Doxiadis II, Rufer N, Romero P, Morgan RA, Schumacher TN, Haanen JB (2007) Selecting highly affine and well-expressed TCRs for gene therapy of melanoma. Blood 110:3564-3572 (Pubitemid 350159623)
25. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, Naldini L (1998) A third-generation lentivirus vector with a conditional packaging system. J Virol 72:8463-8471 (Pubitemid 28471781)
26. Varela-Rohena A, Molloy PE, Dunn SM, Li Y, Suhoski MM, Carroll RG, Milicic A, Mahon T, Sutton DH, Laugel B, Moysey R, Cameron BJ, Vuidepot A, Purbhoo MA, Cole DK, Phillips RE, June CH, Jakobsen BK, Sewell AK, Riley JL (2008) Control of HIV-1 immune escape by CD8 T cells expressing enhanced T-cell receptor. Nat Med 14:1390-1395
27. Parry RV, Rumbley CA, Vandenberghe LH, June CH, Riley JL (2003) CD28 and inducible costimulatory protein src homology 2 binding domains show distinct regulation of phosphatidylinositol 3-kinase, Bcl-xL, and IL-2 expression in primary human CD4 T lymphocytes. J Immunol 171:166-174 (Pubitemid 36745285)
28. Romero P, Dunbar PR, Valmori D, Pittet M, Ogg GS, Rimoldi D, Chen JL, Lienard D, Cerottini JC, Cerundolo V (1998) Ex vivo staining of metastatic lymph nodes by class I major histocompatibility complex tetramers reveals high numbers of antigen-experienced tumor-specific cytolytic T lymphocytes. J Exp Med 188:1641-1650 (Pubitemid 28516109)
29. Cutts SM, Swift LP, Rephaeli A, Nudelman A, Phillips DR (2003) Sequence specificity of adriamycin-DNA adducts in human tumor cells. Mol Cancer Ther 2:661-670
30. Strumberg D, Nitiss JL, Dong J, Kohn KW, Pommier Y (1999) Molecular analysis of yeast and human type II topoisomerases. Enzyme-DNA and drug interactions. J Biol Chem 274:28246-28255
31. Zhang H, Gao YG, van der Marel GA, van Boom JH, Wang AH (1993) Simultaneous incorporations of two anticancer drugs into DNA. The structures of formaldehyde-cross-linked adducts of daunorubicin-d(CG(araC)GCG) and doxorubicin-d(CA(araC)GTG) complexes at high resolution. J Biol Chem 268:10095-10101 (Pubitemid 23150186)
32. Kuhns MS, Davis MM, Garcia KC (2006) Deconstructing the form and function of the TCR/CD3 complex. Immunity 24:133-139 (Pubitemid 43214583)
33. Larsen AK, Escargueil AE, Skladanowski A (2003) Catalytic topoisomerase II inhibitors in cancer therapy. Pharmacol Ther 99:167-181 (Pubitemid 36897748)
34. Stiborova M, Sejbal J, Borek-Dohalska L, Aimova D, Poljakova J, Forsterova K, Rupertova M, Wiesner J, Hudecek J, Wiessler M, Frei E (2004) The anticancer drug ellipticine forms covalent DNA adducts, mediated by human cytochromes P450, through metabolism to 13-hydroxyellipticine and ellipticine N2-oxide. Cancer Res 64:8374-8380 (Pubitemid 39496831)
35. Krishnan P, Bastow KF (2000) Novel mechanisms of DNA topoisomerase II inhibition by pyranonaphthoquinone derivatives - eleutherin, alpha lapachone, and beta lapachone. Biochem Pharmacol 60:1367-1379
36. Li CJ, Averboukh L, Pardee AB (1993) Beta-lapachone, a novel DNA topoisomerase I inhibitor with a mode of action different from camptothecin. J Biol Chem 268:22463-22468 (Pubitemid 23318296)
37. Morschhauser F, Dreyling M, Rohatiner A, Hagemeister F, Bischof Delaloye A (2009) Rationale for consolidation to improve progression-free survival in patients with non-Hodgkin's lymphoma: a review of the evidence. Oncologist 14(Suppl 2):17-29
38. Sebban C, Mounier N, Brousse N, Belanger C, Brice P, Haioun C, Tilly H, Feugier P, Bouabdallah R, Doyen C, Salles G, Coiffier B (2006) Standard chemotherapy with interferon compared with CHOP followed by high-dose therapy with autologous stem cell transplantation in untreated patients with advanced follicular lymphoma: the GELF-94 randomized study from the Groupe d'Etude des Lymphomes de l'Adulte (GELA). Blood 108:2540-2544
39. Tawbi HA, Kirkwood JM (2007) Management of metastatic melanoma. Semin Oncol 34:532-545 (Pubitemid 350236308)
40. Guano F, Pourquier P, Tinelli S, Binaschi M, Bigioni M, Animati F, Manzini S, Zunino F, Kohlhagen G, Pommier Y, Capranico G (1999) Topoisomerase poisoning activity of novel disaccharide anthracyclines. Mol Pharmacol 56:77-84 (Pubitemid 29309814)
41. Collins I, Weber A, Levens D (2001) Transcriptional consequences of topoisomerase inhibition. Mol Cell Biol 21:8437-8451 (Pubitemid 33108603)
42. Daigeler A, Klein-Hitpass L, Chromik MA, Muller O, Hauser J, Homann HH, Steinau HU, Lehnhardt M (2008) Heterogeneous in vitro effects of doxorubicin on gene expression in primary human liposarcoma cultures. BMC Cancer 8:313
43. Folgueira MA, Carraro DM, Brentani H, Patrao DF, Barbosa EM, Netto MM, Caldeira JR, Katayama ML, Soares FA, Oliveira CT, Reis LF, Kaiano JH, Camargo LP, Vencio RZ, Snitcovsky IM, Makdissi FB, e Silva PJ, Goes JC, Brentani MM (2005) Gene expression profile associated with response to doxorubicin-based therapy in breast cancer. Clin Cancer Res 11:7434-7443 (Pubitemid 41507704)
44. Reymann S, Borlak J (2008) Topoisomerase II inhibition involves characteristic chromosomal expression patterns. BMC Genomics 9:324
45. Zunino F, Capranico G (1990) DNA topoisomerase II as the primary target of anti-tumor anthracyclines. Anticancer Drug Des 5:307-317
46. Foglesong PD, Reckord C, Swink S (1992) Doxorubicin inhibits human DNA topoisomerase I. Cancer Chemother Pharmacol 30:123-125
47. Crow RT, Crothers DM (1994) Inhibition of topoisomerase I by anthracycline antibiotics: evidence for general inhibition of topoisomerase I by DNA-binding agents. J Med Chem 37:3191-3194 (Pubitemid 24317566)
48. Nitiss JL (2009) DNA topoisomerase II and its growing repertoire of biological functions. Nat Rev Cancer 9:327-337
49. Leppard JB, Champoux JJ (2005) Human DNA topoisomerase I: relaxation, roles, and damage control. Chromosoma 114:75-85 (Pubitemid 41030970)
50. Shah R, El-Deiry WS (2004) P53-dependent activation of a molecular beacon in tumor cells following exposure to doxorubicin chemotherapy. Cancer Biol Ther 3:871-875 (Pubitemid 41351054)
51. Montecucco A, Biamonti G (2007) Cellular response to etoposide treatment. Cancer Lett 252:9-18 (Pubitemid 46734551)
52. Gonzalez PA, Carreno LJ, Coombs D, Mora JE, Palmieri E, Goldstein B, Nathenson SG, Kalergis AM (2005) T cell receptor binding kinetics required for T cell activation depend on the density of cognate ligand on the antigen-presenting cell. Proc Natl Acad Sci USA 102:4824-4829 (Pubitemid 40471538)
53. Zitvogel L, Apetoh L, Ghiringhelli F, Andre F, Tesniere A, Kroemer G (2008) The anticancer immune response: indispensable for therapeutic success? J Clin Invest 118:1991-2001
54. Ramakrishnan R, Assudani D, Nagaraj S, Hunter T, Cho HI, Antonia S, Altiok S, Celis E, Gabrilovich DI (2010) Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J Clin Invest 120:1111-1124
55. Shurin GV, Tourkova IL, Kaneno R, Shurin MR (2009) Chemotherapeutic agents in noncytotoxic concentrations increase antigen presentation by dendritic cells via an IL-12-dependent mechanism. J Immunol 183:137-144
56. Ewens A, Luo L, Berleth E, Alderfer J, Wollman R, Hafeez BB, Kanter P, Mihich E, Ehrke MJ (2006) Doxorubicin plus interleukin-2 chemoimmunotherapy against breast cancer in mice. Cancer Res 66:5419-5426 (Pubitemid 43844969)
57. Ujhazy P, Zaleskis G, Mihich E, Ehrke MJ, Berleth ES (2003) Doxorubicin induces specific immune functions and cytokine expression in peritoneal cells. Cancer Immunol Immunother 52:463-472 (Pubitemid 36831368)
58. Ferraro C, Quemeneur L, Prigent AF, Taverne C, Revillard JP, Bonnefoy-Berard N (2000) Anthracyclines trigger apoptosis of both g0-g1 and cycling peripheral blood lymphocytes and induce massive deletion of mature T and B cells. Cancer Res 60:1901-1907 (Pubitemid 30207650)
59. Zitvogel L, Kroemer G (2008) The dilemma of anticancer therapy: tumor-specific versus immune effects. Blood 112:4364-4365
60. Creasey WA, McIntosh LS, Brescia T, Odujinrin O, Aspnes GT, Murray E, Marsh JC (1976) Clinical effects and pharmacokinetics of different dosage schedules of adriamycin. Cancer Res 36:216-221
61. Reich SD, Steinberg F, Bachur NR, Riggs CE Jr, Goebel R, Berman M (1979) Mathematical model for adriamycin (doxorubicin) pharmacokinetics. Cancer Chemother Pharmacol 3:125-131 (Pubitemid 10225501)
62. Zebedin E, Simma O, Schuster C, Putz EM, Fajmann S, Warsch W, Eckelhart E, Stoiber D, Weisz E, Schmid JA, Pickl WF, Baumgartner C, Valent P, Piekorz RP, Freissmuth M, Sexl V (2008) Leukemic challenge unmasks a requirement for PI3kdelta in NK cell-mediated tumor surveillance. Blood 112:4655-4664
63. June CH, Blazar BR, Riley JL (2009) Engineering lymphocyte subsets: tools, trials and tribulations. Nat Rev Immunol 9:704-716
64. Ashburn TT, Thor KB (2004) Drug repositioning: identifying and developing new uses for existing drugs. Nat Rev Drug Discov 3:673-683 (Pubitemid 39173508)