Intermittent metronomic drug schedule is essential for activating antitumor innate immunity and tumor xenograft regression

Neoplasia (United States)

Volumn 16, Issue 1, 2014, Pages 84-96

  Chen, Chong Sheng ^a   Doloff, Joshua C ^a   Waxman, David J ^a  

^a Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHOSPHAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLOOD SAMPLING; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CANCER SURGERY; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; MALE; METRONOMIC DRUG ADMINISTRATION; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RNA ISOLATION; TISSUE CHARACTERIZATION; TUMOR MICROENVIRONMENT; TUMOR REGRESSION; TUMOR XENOGRAFT;

ADMINISTRATION, METRONOMIC; ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS; AREA UNDER CURVE; CELL LINE, TUMOR; CHEMOKINES; CYCLOPHOSPHAMIDE; CYTOKINES; DRUG ADMINISTRATION SCHEDULE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNITY, INNATE; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED ICR; MICE, SCID; NEOPLASM TRANSPLANTATION; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PATHOLOGIC; RATS;

EID: 84900395848     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.131910     Document Type: Article

References (50)

1. Browder T, Butterfield CE, Kräling BM, Shi B, Marshall B, O'Reilly MS, and Folkman J (2000). Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. Cancer Res 60, 1878-1886.
2. Hanahan D, Bergers G, and Bergsland E (2000). Less is more, regularly: metronomic dosing of cytotoxic drugs can target tumor angiogenesis in mice. J Clin Invest 105, 1045-1047.
3. Klement G, Baruchel S, Rak J, Man S, Clark K, Hicklin DJ, Bohlen P, and Kerbel RS (2000). Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity. J Clin Invest 105, R15-R24.
4. Hahnfeldt P, Hlatky L, and Klement GL (2013). Center of cancer systems biology second annual workshop-tumor metronomics: timing and dose level dynamics. Cancer Res 73, 2949-2954.
5. Man S, Bocci G, Francia G, Green SK, Jothy S, Hanahan D, Bohlen P, Hicklin DJ, Bergers G, and Kerbel RS (2002). Antitumor effects in mice of low-dose (metronomic) cyclophosphamide administered continuously through the drinking water. Cancer Res 62, 2731-2735.
6. Emmenegger U, Shaked Y, Man S, Bocci G, Spasojevic I, Francia G, Kouri A, Coke R, Cruz-Munoz W, Ludeman SM, et al. (2007). Pharmacodynamic and pharmacokinetic study of chronic low-dose metronomic cyclophosphamide therapy in mice. Mol Cancer Ther 6, 2280-2289.
7. Pasquier E, Kavallaris M, and André N (2010). Metronomic chemotherapy: new rationale for new directions. Nat Rev Clin Oncol 7, 455-465.
8. Penel N, Adenis A, and Bocci G (2012). Cyclophosphamide-based metronomic chemotherapy: after 10 years of experience, where do we stand and where are we going? Crit Rev Oncol Hematol 82, 40-50.
9. André N, Banavali S, Snihur Y, and Pasquier E (2013). Has the time come for metronomics in low-income and middle-income countries? Lancet Oncol 14, e239-e248.
10. Kodumudi KN, Woan K, Gilvary DL, Sahakian E, Wei S, and Djeu JY (2010). A novel chemoimmunomodulating property of docetaxel: suppression of myeloidderived suppressor cells in tumor bearers. Clin Cancer Res 16, 4583-4594.
11. Le HK, Graham L, Cha E, Morales JK, Manjili MH, and Bear HD (2009). Gemcitabine directly inhibits myeloid derived suppressor cells in BALB/c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice. Int Immunopharmacol 9, 900-909.
12. Banissi C, Ghiringhelli F, Chen L, and Carpentier AF (2009). Treg depletion with a low-dose metronomic temozolomide regimen in a rat glioma model. Cancer Immunol Immunother 58, 1627-1634.
13. Briasoulis E, Pappas P, Puozzo C, Tolis C, Fountzilas G, Dafni U, Marselos M, and Pavlidis N (2009). Dose-ranging study of metronomic oral vinorelbine in patients with advanced refractory cancer. Clin Cancer Res 15, 6454-6461.
14. Chen CA, Ho CM, Chang MC, Sun WZ, Chen YL, Chiang YC, Syu MH, Hsieh CY, and Cheng WF (2010). Metronomic chemotherapy enhances antitumor effects of cancer vaccine by depleting regulatory T lymphocytes and inhibiting tumor angiogenesis. Mol Ther 18, 1233-1243.
15. Ghiringhelli F, Menard C, Puig PE, Ladoire S, Roux S, Martin F, Solary E, Le Cesne A, Zitvogel L, and 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.
16. Doloff JC and Waxman DJ (2012). VEGF receptor inhibitors block the ability of metronomically dosed cyclophosphamide to activate innate immunity-induced tumor regression. Cancer Res 72, 1103-1115.
17. Addeo R, Sgambato A, Cennamo G, Montella L, Faiola V, Abbruzzese A, Capasso E, Leo L, Botti G, Caraglia M, et al. (2010). Low-dose metronomic oral administration of vinorelbine in the first-line treatment of elderly patients with metastatic breast cancer. Clin Breast Cancer 10, 301-306.
18. Pallis AG, Chandrinos V, Pavlakou G, Xenidis N, Varthalitis I, Vardakis N, Vamvakas L, Kontopodis E, Rovithi M, and Georgoulias V (2010). A multicenter phase I trial of metronomic oral vinorelbine plus cisplatin in patients with NSCLC. Cancer Chemother Pharmacol 67, 1239-1245.
19. Samaritani R, Corrado G, Vizza E, and Sbiroli C (2007). Cyclophosphamide "metronomic" chemotherapy for palliative treatment of a young patient with advanced epithelial ovarian cancer. BMC Cancer 7, 65.
20. Allegrini G, Falcone A, Fioravanti A, Barletta MT, Orlandi P, Loupakis F, Cerri E, Masi G, Di Paolo A, Kerbel RS, et al. (2008). A pharmacokinetic and pharmacodynamic study on metronomic irinotecan in metastatic colorectal cancer patients. Br J Cancer 98, 1312-1319.
21. Mross K and Steinbild S (2012). Metronomic anti-cancer therapy-an ongoing treatment option for advanced cancer patients. J Cancer Ther Res 2049, 1-18.
22. Ma J, Chen CS, Blute T, and Waxman DJ (2011). Antiangiogenesis enhances intratumoral drug retention. Cancer Res 71, 2675-2685.
23. Brownell J and Polyak SJ (2013). Molecular pathways: hepatitis C virus, CXCL10, and the inflammatory road to liver cancer. Clin Cancer Res 19, 1347-1352.
24. Wendel M, Galani IE, Suri-Payer E, and Cerwenka A (2008). Natural killer cell accumulation in tumors is dependent on IFN-γ and CXCR3 ligands. Cancer Res 68, 8437-8445.
25. Hara T and Tanegashima K (2012). Pleiotropic functions of the CXC-type chemokine CXCL14 in mammals. J Biochem 151, 469-476.
26. Chu CY and Tseng J (2000). Induction of Fas and Fas-ligand expression in plasmacytoma cells by a cytotoxic factor secreted by murine macrophages. J Biomed Sci 7, 58-63.
27. Chávez-Galán L, Arenas-Del Angel MC, Zenteno E, Chávez R, and Lascurain R (2009). Cell death mechanisms induced by cytotoxic lymphocytes. Cell Mol Immunol 6, 15-25.
28. Williams K, Schwartz A, Corey S, Orandle M, Kennedy W, Thompson B, Alvarez X, Brown C, Gartner S, and Lackner A (2002). Proliferating cellular nuclear antigen expression as a marker of perivascular macrophages in simian immunodeficiency virus encephalitis. Am J Pathol 161, 575-585.
29. Kammerer U, Eggert AO, Kapp M, McLellan AD, Geijtenbeek TB, Dietl J, van Kooyk Y, and Kampgen E (2003). Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am J Pathol 162, 887-896.
30. Najean Y, Ardaillou N, and Dresch C (1969). Platelet lifespan. Annu Rev Med 20, 47-62.
31. Faivre C, Barbolosi D, Pasquier E, and Andre N (2013). A mathematical model for the administration of temozolomide: comparative analysis of conventional and metronomic chemotherapy regimens. Cancer Chemother Pharmacol 71, 1013-1019.
32. Huang Z, Roy P, and Waxman DJ (2000). Role of human liver microsomal CYP3A4 and CYP2B6 in catalyzing N-dechloroethylation of cyclophosphamide and ifosfamide. Biochem Pharmacol 59, 961-972.
33. Ma J and Waxman DJ (2008). Modulation of the antitumor activity of metronomic cyclophosphamide by the angiogenesis inhibitor axitinib. Mol Cancer Ther 7, 79-89.
34. Jounaidi Y and Waxman DJ (2001). Frequent, moderate-dose cyclophosphamide administration improves the efficacy of cytochrome P-450/cytochrome P-450 reductase-based cancer gene therapy. Cancer Res 61, 4437-4444.
35. Schwartz PS and Waxman DJ (2001). Cyclophosphamide induces caspase 9- dependent apoptosis in 9L tumor cells. Mol Pharmacol 60, 1268-1279.
36. Tesniere A, Panaretakis T, Kepp O, Apetoh L, Ghiringhelli F, Zitvogel L, and Kroemer G (2008). Molecular characteristics of immunogenic cancer cell death. Cell Death Differ 15, 3-12.
37. Raulet DH and Guerra N (2009). Oncogenic stress sensed by the immune system: role of natural killer cell receptors. Nat Rev Immunol 9, 568-580.
38. Gasser S, Orsulic S, Brown EJ, and Raulet DH (2005). The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436, 1186-1190.
39. Martin-Manso G, Galli S, Ridnour LA, Tsokos M, Wink DA, and Roberts DD (2008). Thrombospondin 1 promotes tumor macrophage recruitment and enhances tumor cell cytotoxicity of differentiated U937 cells. Cancer Res 68, 7090-7099.
40. Zhao HY, Ooyama A, Yamamoto M, Ikeda R, Haraguchi M, Tabata S, Furukawa T, Che XF, Zhang S, Oka T, et al. (2008). Molecular basis for the induction of an angiogenesis inhibitor, thrombospondin-1, by 5-fluorouracil. Cancer Res 68, 7035-7041.
41. Guerriero JL, Ditsworth D, Fan Y, Zhao F, Crawford HC, and Zong WX (2008). Chemotherapy induces tumor clearance independent of apoptosis. Cancer Res 68, 9595-9600.
42. Rodier F, Coppé JP, Patil CK, Hoeijmakers WA, Muñoz DP, Raza SR, Freund A, Campeau E, Davalos AR, and Campisi J (2009). Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat Cell Biol 11, 973-979.
43. Chou TC, Zhang X, Zhong ZY, Li Y, Feng L, Eng S, Myles DR, Johnson R Jr, Wu N, Yin YI, et al. (2008). Therapeutic effect against human xenograft tumors in nude mice by the third generation microtubule stabilizing epothilones. Proc Natl Acad Sci USA 105, 13157-13162.
44. Daenen LG, Shaked Y, Man S, Xu P, Voest EE, Hoffman RM, Chaplin DJ, and Kerbel RS (2009). Low-dose metronomic cyclophosphamide combined with vascular disrupting therapy induces potent antitumor activity in preclinical human tumor xenograft models. Mol Cancer Ther 8, 2872-2881.
45. du Manoir JM, Francia G, Man S, Mossoba M, Medin JA, Viloria-Petit A, Hicklin DJ, Emmenegger U, and Kerbel RS (2006). Strategies for delaying or treating in vivo acquired resistance to trastuzumab in human breast cancer xenografts. Clin Cancer Res 12, 904-916.
46. Salem ML, El-Naggar SA, and Cole DJ (2010). Cyclophosphamide induces bone marrow to yield higher numbers of precursor dendritic cells in vitro capable of functional antigen presentation to T cells in vivo. Cell Immunol 261, 134-143.
47. Viaud S, Flament C, Zoubir M, Pautier P, LeCesne A, Ribrag V, Soria JC, Marty V, Vielh P, Robert C, et al. (2011). Cyclophosphamide induces differentiation of Th17 cells in cancer patients. Cancer Res 71, 661-665.
48. Tanaka H, Matsushima H, Nishibu A, Clausen BE, and Takashima A (2009). Dual therapeutic efficacy of vinblastine as a unique chemotherapeutic agent capable of inducing dendritic cell maturation. Cancer Res 69, 6987-6994.
49. Mattarollo SR, Loi S, Duret H, Ma Y, Zitvogel L, and Smyth MJ (2011). Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res 71, 4809-4820.
50. Tanaka H, Matsushima H, Mizumoto N, and Takashima A (2009). Classification of chemotherapeutic agents based on their differential in vitro effects on dendritic cells. Cancer Res 69, 6978-6986.