The microtubule-depolymerizing agent ansamitocin P3 programs dendritic cells toward enhanced anti-tumor immunity

Cancer Immunology, Immunotherapy

Volumn 63, Issue 9, 2014, Pages 925-938

  Martin, Kea ^a   Müller, Philipp ^a   Schreiner, Jens ^a   Prince, Spasenija Savic ^b   Lardinois, Didier ^a   Heinzelmann Schwarz, Viola A ^a   Thommen, Daniela S ^a   Zippelius, Alfred ^a  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

Ansamitocin P3; Anti tumor immunity; Chemotherapy; Dendritic cell maturation; Immunotherapy; Microtubule depolymerizing agent

Indexed keywords

ANSAMITOCIN P 3; CD86 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCLONAL ANTIBODY; OVALBUMIN; PROGRAMMED DEATH 1 RECEPTOR; PROGRAMMED DEATH 1 RECEPTOR ANTIBODY; UNCLASSIFIED DRUG; ANSAMITOCIN; CD11 ANTIGEN; GAMMA INTERFERON; MAYTANSINE; TUBULIN MODULATOR;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CELL HOMING; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; EFFECTOR CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; LANGERHANS CELL; LYMPH NODE; MONOCYTE; MOUSE; MOUSE MODEL; NEOPLASM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPLEEN; T LYMPHOCYTE ACTIVATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR IMMUNITY; TUMOR MODEL; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; DRUG EFFECTS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MICROTUBULE; NEOPLASMS, EXPERIMENTAL; T LYMPHOCYTE; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD11; ANTIGENS, CD86; CELL LINE, TUMOR; CTLA-4 ANTIGEN; DENDRITIC CELLS; HUMANS; INTERFERON-GAMMA; LYMPH NODES; LYMPHOCYTE ACTIVATION; MAYTANSINE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROTUBULES; NEOPLASMS, EXPERIMENTAL; PROGRAMMED CELL DEATH 1 RECEPTOR; T-LYMPHOCYTES; TUBULIN MODULATORS;

EID: 84906939261     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-014-1565-4     Document Type: Article

References (49)

1. Drake CG, Lipson EJ, Brahmer JR (2014) Breathing new life into immunotherapy: review of melanoma, lung and kidney cancer. Nat Rev Clin Oncol 11(1):24-37. doi:10.1038/nrclinonc.2013.208
2. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, Wolchok JD, Hersey P, Joseph RW, Weber JS, Dronca R, Gangadhar TC, Patnaik A, Zarour H, Joshua AM, Gergich K, Elassaiss-Schaap J, Algazi A, Mateus C, Boasberg P, Tumeh PC, Chmielowski B, Ebbinghaus SW, Li XN, Kang SP, Ribas A (2013) Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med. doi:10.1056/NEJMoa1305133
3. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K, Burke MM, Caldwell A, Kronenberg SA, Agunwamba BU, Zhang X, Lowy I, Inzunza HD, Feely W, Horak CE, Hong Q, Korman AJ, Wigginton JM, Gupta A, Sznol M (2013) Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. doi:10.1056/NEJMoa1302369
4. Bracci L, Schiavoni G, Sistigu A, Belardelli F (2014) Immune-based mechanisms of cytotoxic chemotherapy: implications for the design of novel and rationale-based combined treatments against cancer. Cell Death Differ 21(1):15-25. doi:10.1038/cdd.2013.67
5. Chen G, Emens LA (2013) Chemoimmunotherapy: reengineering tumor immunity. Cancer Immunol Immunother 62(2):203-216. doi:10.1007/s00262-012-1388-0
6. Lake RA, Robinson BW (2005) Immunotherapy and chemotherapy - a practical partnership. Nat Rev Cancer 5(5):397-405 (Pubitemid 40637831)
7. Gajewski TF, Schreiber H, Fu YX (2013) Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol 14(10):1014-1022. doi:10.1038/ni.2703
8. Zitvogel L, Galluzzi L, Smyth MJ, Kroemer G (2013) Mechanism of action of conventional and targeted anticancer therapies: reinstating immunosurveillance. Immunity 39(1):74-88. doi:10.1016/j.immuni.2013.06.014
9. Palucka K, Banchereau J (2012) Cancer immunotherapy via dendritic cells. Nat Rev Cancer 12(4):265-277. doi:10.1038/nrc3258
10. Hargadon KM (2013) Tumor-altered dendritic cell function: implications for anti-tumor immunity. Front Immunol 4:192. doi: 10.3389/fimmu.2013.00192
11. Kroemer G, Galluzzi L, Kepp O, Zitvogel L (2013) Immunogenic cell death in cancer therapy. Annu Rev Immunol 31:51-72. doi:10.1146/annurev-immunol- 032712-100008
12. van de Ven R, Reurs AW, Wijnands PG, van Wetering S, Kruisbeek AM, Hooijberg E, Scheffer GL, Scheper RJ, de Gruijl TD (2012) Exposure of CD34+ precursors to cytostatic anthraquinone-derivatives induces rapid dendritic cell differentiation: implications for cancer immunotherapy. Cancer Immunol Immunother 61(2):181-191. doi:10.1007/s00262-011-1039-x
13. Mizumoto N, Gao J, Matsushima H, Ogawa Y, Tanaka H, Takashima A (2005) Discovery of novel immunostimulants by dendritic-cell-based functional screening. Blood 106(9):3082-3089. doi:10.1182/blood-2005-03-1161 (Pubitemid 41565904)
14. Tanaka H, Matsushima H, Mizumoto N, Takashima A (2009) Classification of chemotherapeutic agents based on their differential in vitro effects on dendritic cells. Cancer Res 69(17):6978-6986. doi:10.1158/0008-5472.CAN-09-1101
15. Tanaka H, Matsushima H, Nishibu A, Clausen BE, Takashima A (2009) Dual therapeutic efficacy of vinblastine as a unique chemotherapeutic agent capable of inducing dendritic cell maturation. Cancer Res 69(17):6987-6994. doi:10.1158/0008-5472.CAN-09-1106
16. Nalbandian G, Paharkova-Vatchkova V, Mao A, Nale S, Kovats S (2005) The selective estrogen receptor modulators, tamoxifen and raloxifene, impair dendritic cell differentiation and activation. J Immunol 175(4):2666-2675 (Pubitemid 41113882)
17. Hipp MM, Hilf N, Walter S, Werth D, Brauer KM, Radsak MP, Weinschenk T, Singh-Jasuja H, Brossart P (2008) Sorafenib, but not sunitinib, affects function of dendritic cells and induction of primary immune responses. Blood 111(12):5610-5620. doi:10.1182/blood-2007-02-075945
18. Bros M, Jahrling F, Renzing A, Wiechmann N, Dang NA, Sutter A, Ross R, Knop J, Sudowe S, Reske-Kunz AB (2007) A newly established murine immature dendritic cell line can be differentiated into a mature state, but exerts tolerogenic function upon maturation in the presence of glucocorticoid. Blood 109(9):3820-3829. doi:10.1182/blood-2006-07-035576 (Pubitemid 46641733)
19. Abeyama K, Eng W, Jester JV, Vink A, Edelbaum D, Cockerell CJ, Bergstresser PR, Takashima A (2000) A role for NF-kappaB-dependent gene transactivation in sunburn. J Clin Invest 105(12):1751-1759. doi:10.1172/JCI9745 (Pubitemid 30421756)
20. Daniels MA, Teixeiro E, Gill J, Hausmann B, Roubaty D, Holmberg K, Werlen G, Hollander GA, Gascoigne NR, Palmer E (2006) Thymic selection threshold defined by compartmentalization of Ras/MAPK signalling. Nature 444(7120):724-729. doi:10.1038/nature05269 (Pubitemid 44949596)
21. Meidenbauer N, Zippelius A, Pittet MJ, Laumer M, Vogl S, Heymann J, Rehli M, Seliger B, Schwarz S, Le Gal FA, Dietrich PY, Andreesen R, Romero P, Mackensen A (2004) High frequency of functionally active melan-a-specific T cells in a patient with progressive immunoproteasome-deficient melanoma. Cancer Res 64(17):6319-6326. doi:10.1158/0008-5472.CAN-04-1341 (Pubitemid 39129437)
22. West MA, Wallin RP, Matthews SP, Svensson HG, Zaru R, Ljunggren HG, Prescott AR, Watts C (2004) Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 305(5687):1153-1157. doi:10.1126/science.1099153 (Pubitemid 39100328)
23. West AC, Mattarollo SR, Shortt J, Cluse LA, Christiansen AJ, Smyth MJ, Johnstone RW (2013) An intact immune system is required for the anticancer activities of histone deacetylase inhibitors. Cancer Res. doi:10.1158/0008-5472. CAN-13-0890
24. Mattarollo SR, Loi S, Duret H, Ma Y, Zitvogel L, Smyth MJ (2011) Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res 71(14):4809-4820. doi:10.1158/0008-5472.CAN-11- 0753
25. Probst HC, McCoy K, Okazaki T, Honjo T, van den Broek M (2005) Resting dendritic cells induce peripheral CD8+ T cell tolerance through PD-1 and CTLA-4. Nat Immunol 6(3):280-286. doi:10.1038/ni1165 (Pubitemid 41724765)
26. Nishikawa H, Sakaguchi S (2010) Regulatory T cells in tumor immunity. Int J Cancer 127(4):759-767. doi:10.1002/ijc.25429
27. Waitz R, Solomon SB, Petre EN, Trumble AE, Fasso M, Norton L, Allison JP (2012) Potent induction of tumor immunity by combining tumor cryoablation with anti-CTLA-4 therapy. Cancer Res 72(2):430-439. doi:10.1158/0008-5472.CAN-11-1782
28. Mantovani A, Germano G, Marchesi F, Locatelli M, Biswas SK (2011) Cancer-promoting tumor-associated macrophages: new vistas and open questions. Eur J Immunol 41(9):2522-2525. doi:10.1002/eji.201141894
29. Liu C, Chari RV (1997) The development of antibody delivery systems to target cancer with highly potent maytansinoids. Expert Opin Investig Drugs 6(2):169-172. doi:10.1517/13543784.6.2.169 (Pubitemid 27101468)
30. Cassady JM, Chan KK, Floss HG, Leistner E (2004) Recent developments in the maytansinoid antitumor agents. Chem Pharm Bull (Tokyo) 52(1):1-26 (Pubitemid 41685545)
31. Issell BF, Crooke ST (1978) Maytansine. Cancer Treat Rev 5(4):199-207 (Pubitemid 9109517)
32. Alley SC, Okeley NM, Senter PD (2010) Antibody-drug conjugates: targeted drug delivery for cancer. Curr Opin Chem Biol 14(4):529-537. doi:10.1016/j.cbpa.2010.06.170
33. Chari RV, Martell BA, Gross JL, Cook SB, Shah SA, Blattler WA, McKenzie SJ, Goldmacher VS (1992) Immunoconjugates containing novel maytansinoids: promising anticancer drugs. Cancer Res 52(1):127-131
34. Sievers EL, Senter PD (2013) Antibody-drug conjugates in cancer therapy. Annu Rev Med 64:15-29. doi:10.1146/annurev-med-050311-201823
35. Prota AE, Bargsten K, Zurwerra D, Field JJ, Diaz JF, Altmann KH, Steinmetz MO (2013) Molecular mechanism of action of microtubule-stabilizing anticancer agents. Science 339(6119):587-590. doi:10.1126/science.1230582
36. Venghateri JB, Gupta TK, Verma PJ, Kunwar A, Panda D (2013) Ansamitocin p3 depolymerizes microtubules and induces apoptosis by binding to tubulin at the vinblastine site. PLoS one 8(10):e75182. doi:10.1371/journal.pone.0075182
37. John J, Ismail M, Riley C, Askham J, Morgan R, Melcher A, Pandha H (2010) Differential effects of paclitaxel on dendritic cell function. BMC Immunol 11:14. doi:10.1186/1471-2172-11-14
38. Kolomeichuk SN, Terrano DT, Lyle CS, Sabapathy K, Chambers TC (2008) Distinct signaling pathways of microtubule inhibitors-vinblastine and taxol induce JNK-dependent cell death but through AP-1-dependent and AP-1-independent mechanisms, respectively. FEBS J 275(8):1889-1899. doi:10.1111/j.1742-4658.2008. 06349.x (Pubitemid 351464008)
39. Banchereau J, Steinman RM (1998) Dendritic cells and the control of immunity. Nature 392(6673):245-252. doi:10.1038/32588 (Pubitemid 28155090)
40. Fiorentino DF, Zlotnik A, Vieira P, Mosmann TR, Howard M, Moore KW, O'Garra A (1991) IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J Immunol 146(10):3444-3451
41. Steinbrink K, Wolfl M, Jonuleit H, Knop J, Enk AH (1997) Induction of tolerance by IL-10-treated dendritic cells. J Immunol 159(10):4772-4780 (Pubitemid 127471012)
42. De Monte L, Reni M, Tassi E, Clavenna D, Papa I, Recalde H, Braga M, Di Carlo V, Doglioni C, Protti MP (2011) Intratumor T helper type 2 cell infiltrate correlates with cancer-associated fibroblast thymic stromal lymphopoietin production and reduced survival in pancreatic cancer. J Exp Med 208(3):469-478. doi:10.1084/jem.20101876
43. Cheong C, Matos I, Choi JH, Dandamudi DB, Shrestha E, Longhi MP, Jeffrey KL, Anthony RM, Kluger C, Nchinda G, Koh H, Rodriguez A, Idoyaga J, Pack M, Velinzon K, Park CG, Steinman RM (2010) Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209 (+) dendritic cells for immune T cell areas. Cell 143(3):416-429. doi:10.1016/j.cell.2010.09.039
44. Ma Y, Adjemian S, Mattarollo SR, Yamazaki T, Aymeric L, Yang H, Portela Catani JP, Hannani D, Duret H, Steegh K, Martins I, Schlemmer F, Michaud M, Kepp O, Sukkurwala AQ, Menger L, Vacchelli E, Droin N, Galluzzi L, Krzysiek R, Gordon S, Taylor PR, Van Endert P, Solary E, Smyth MJ, Zitvogel L, Kroemer G (2013) Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 38(4):729-741. doi:10.1016/j.immuni.2013.03.003
45. Robert C, Thomas L, Bondarenko I, O'Day S, M DJ, Garbe C, Lebbe C, Baurain JF, Testori A, Grob JJ, Davidson N, Richard J, Maio M, Hauschild A, Miller WH, Gascon P, Lotem M, Harmankaya K, Ibrahim R, Francis S, Chen T, Humphrey R, Hoos A, Wolchok JD (2011) Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 364(26):2517-2526. doi:10.1056/NEJMoa1104621
46. Topalian SL, Drake CG, Pardoll DM (2012) Targeting the PD-1/B7-H1 (PD-L1) pathway to activate anti-tumor immunity. Curr Opin Immunol 24(2):207-212. doi:10.1016/j.coi.2011.12.009
47. Hamid O, Carvajal RD (2013) Anti-programmed death-1 and anti-programmed death-ligand 1 antibodies in cancer therapy. Expert Opin Biol Ther 13(6):847-861. doi:10.1517/14712598.2013.770836
48. Curran MA, Montalvo W, Yagita H, Allison JP (2010) PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci 107(9):4275-4280. doi:10.1073/pnas.0915174107
49. Sica A, Mantovani A (2012) Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122(3):787-795. doi:10.1172/JCI59643