Lipid-based nanoformulation of irinotecan: Dual mechanism of action allows for combination chemo/angiogenic therapy

Nanomedicine

Volumn 6, Issue 9, 2011, Pages 1645-1654

  Waterhouse, Dawn N ^a,b   Yapp, Donald ^a,b   Verreault, Maite ^a   Anantha, Malathi ^a   Sutherland, Brent ^a   Bally, Marcel B ^a,b,c  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c Centre for Drug Research and Development   (Canada)

Author keywords

antiangiogenic therapy; cytotoxic therapy; dual mechanism; irinotecan; liposome; metronomic dosing; nanoformulation; vascular normalization

Indexed keywords

ALPHA INTERFERON; ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; BEVACIZUMAB; CARBOPLATIN; CILENGITIDE; CPX 1; CPX 351; CYCLOPHOSPHAMIDE; CYTARABINE; DAUNORUBICIN; DOXORUBICIN; ETARACIZUMAB; FLUOROURACIL; GEMCITABINE; IM 1C11; IRINOPHORE C; IRINOTECAN; LIPID; METHOTREXATE; NANOPARTICLE; NANOVNB; OXALIPLATIN; PACLITAXEL; PAZOPANIB; SEMAXINIB; SORAFENIB; SUNITINIB; TEMOZOLOMIDE; TOPOTECAN; UNCLASSIFIED DRUG; UNINDEXED DRUG; VANDETANIB; VINCRISTINE SULFATE; VOLOCIXIMAB;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER PATIENT; COLORECTAL CANCER; DRUG ACCUMULATION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG FORMULATION; DRUG MECHANISM; GLIOBLASTOMA; GLIOMA; HUMAN; KAPOSI SARCOMA; KIDNEY CANCER; LIPOSOMAL DELIVERY; LUNG NON SMALL CELL CANCER; MELANOMA; MULTIPLE CYCLE TREATMENT; NANOTECHNOLOGY; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; REVIEW; SLOW DRUG RELEASE; TUMOR VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS; CAMPTOTHECIN; CHEMISTRY, PHARMACEUTICAL; HUMANS; LIPIDS; LIPOSOMES; MODELS, BIOLOGICAL; MODELS, CHEMICAL; NEOPLASMS;

EID: 81255143255     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.11.140     Document Type: Review

References (72)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 144(5), 646-674 (2011).
2. Heppner GH, Miller BE. Tumor heterogeneity: biological implications and therapeutic consequences. Cancer Metastasis Rev. 2(1), 5-23 (1983).
3. Frei E 3rd: Combination chemotherapy. Proc. R. Soc. Med. 67(6 Pt 1), 425-436 (1974).
4. Harasym TO, Tardi PG, Harasym NL, Harvie P, Johnstone SA, Mayer LD. Increased preclinical efficacy of irinotecan and floxuridine coencapsulated inside liposomes is associated with tumor delivery of synergistic drug ratios. Oncol. Res. 16(8), 361-374 (2007).
5. Ramsay E, Alnajim J, Anantha M et al. A novel liposomal irinotecan formulation with significant anti-tumour activity: use of the divalent cation ionophore A23187 and copper-containing liposomes to improve drug retention. Eur. J. Pharm. Biopharm. 68(3), 607-617 (2008).
6. Baker JH, Lam J, Kyle AH et al. Irinophore C, a novel nanoformulation of irinotecan, alters tumor vascular function and enhances the distribution of 5-fluorouracil and doxorubicin. Clin. Cancer Res. 14(22), 7260-7271 (2008).
7. Waterhouse DN, Gelmon KA, Klasa R et al. Development and assessment of conventional and targeted drug combinations for use in the treatment of aggressive breast cancers. Curr. Cancer Drug Targets 6(6), 455-489 (2006).
8. Ramsay EC, Dos Santos N, Dragowska WH, Laskin JJ, Bally MB. The formulation of lipid-based nanotechnologies for the delivery of fixed dose anticancer drug combinations. Curr. Drug Deliv. 2(4), 341-351 (2005).
9. Holash J, Wiegand SJ, Yancopoulos GD. New model of tumor angiogenesis: dynamic balance between vessel regression and growth mediated by angiopoietins and VEGF. Oncogene 18(38), 5356-5362 (1999).
10. Jain RK. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat. Med. 7(9), 987-989 (2001).
11. Izumi Y, Xu L, Di Tomaso E, Fukumura D, Jain RK. Tumour biology: herceptin acts as an anti-angiogenic cocktail. Nature 416(6878), 279-280 (2002).
12. Verreault M, Strutt D, Masin D et al. Vascular normalization in orthotopic glioblastoma following intravenous treatment with lipid-based nanoparticulate formulations of irinotecan (Irinophore C), doxorubicin (Caelyx®) or vincristine. BMC Cancer 11, 124 (2011).
13. Tailor TD, Hanna G, Yarmolenko PS et al. Effect of pazopanib on tumor microenvironment and liposome delivery. Mol. Cancer Ther. 9(6), 1798-1808 (2010).
14. Folkman J. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 285(21), 1182-1186 (1971).
15. Gerber HP, Ferrara N. Pharmacology and pharmacodynamics of bevacizumab as monotherapy or in combination with cytotoxic therapy in preclinical studies. Cancer Res. 65(3), 671-680 (2005).
16. Cao S, Durrani FA, Toth K, Rustum YM, Seshadri M. Bevacizumab enhances the therapeutic efficacy of Irinotecan against human head and neck squamous cell carcinoma xenografts. Oral Oncol. 47(6), 459-466 (2011).
17. Comella P, Massidda B, Natale D et al. Efficacy and tolerability of biweekly bevacizumab, irinotecan, folinic acid and fluorouracil intravenous bolus (BIFF Regimen) in patients with metastatic colorectal cancer: the southern Italy cooperative oncology group experience. Clin. Colorectal Cancer 10(1), 42-47 (2011).
18. Gately S, Kerbel R. Antiangiogenic scheduling of lower dose cancer chemotherapy. Cancer J. 7(5), 427-436 (2001).
19. Nelius T, Klatte T, De Riese W, Haynes A, Filleur S. Clinical outcome of patients with docetaxel-resistant hormone-refractory prostate cancer treated with second-line cyclophosphamide-based metronomic chemotherapy. Med. Oncol. 27(2), 363-367 (2010).
20. Sharp Jr, Bouffet E, Stempak D et al. A multi-centre Canadian pilot study of metronomic temozolomide combined with radiotherapy for newly diagnosed paediatric brainstem glioma. Eur. J. Cancer 46(18), 3271-3279 (2010).
21. Cham KK, Baker JH, Takhar KS et al. Metronomic gemcitabine suppresses tumour growth, improves perfusion, and reduces hypoxia in human pancreatic ductal adenocarcinoma. Br. J. Cancer 103(1), 52-60 (2010).
22. Merritt WM, Danes CG, Shahzad MM et al. Anti-angiogenic properties of metronomic topotecan in ovarian carcinoma. Cancer Biol. Ther. 8(16), 1596-1603 (2009).
23. Colleoni M, Orlando L, Sanna G et al. Metronomic low-dose oral cyclophosphamide and methotrexate plus or minus thalidomide in metastatic breast cancer: antitumor activity and biological effects. Ann. Oncol. 17(2), 232-238 (2006).
24. Colleoni M, Rocca A, Sandri MT et al. Low-dose oral methotrexate and cyclophosphamide in metastatic breast cancer: antitumor activity and correlation with vascular endothelial growth factor levels. Ann. Oncol. 13(1), 73-80 (2002).
25. Takano S, Kamiyama H, Mashiko R, Osuka S, Ishikawa E, Matsumura A. Metronomic treatment of malignant glioma xenografts with irinotecan (CPT-11) inhibits angiogenesis and tumor growth. J. Neurooncol. 99(2), 177-185 (2010).
26. Fioravanti A, Canu B, Ali G et al. Metronomic 5-fluorouracil, oxaliplatin and irinotecan in colorectal cancer. Eur. J. Pharmacol. 619(1-3), 8-14 (2009).
27. Allegrini G, Falcone A, Fioravanti A et al. A pharmacokinetic and pharmacodynamic study on metronomic irinotecan in metastatic colorectal cancer patients. Br. J. Cancer 98(8), 1312-1319 (2008).
28. Herben VM, Schellens JH, Swart M et al. Phase I and pharmacokinetic study of irinotecan administered as a low-dose, continuous intravenous infusion over 14 days in patients with malignant solid tumors. J. Clin. Oncol. 17(6), 1897-1905 (1999).
29. Bocci G, Falcone A, Fioravanti A et al. Antiangiogenic and anticolorectal cancer effects of metronomic irinotecan chemotherapy alone and in combination with semaxinib. Br. J. Cancer 98(10), 1619-1629 (2008).
30. Seymour LW. Passive tumor targeting of soluble macromolecules and drug conjugates. Crit. Rev. Ther. Drug Carrier Syst. 9(2), 135-187 (1992).
31. Maeda H, Wu J, Sawa T, Matsumura Y, Hori K. Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J. Control Release 65(1-2), 271-284 (2000).
32. D'Souza GG, Wang T, Rockwell K, Torchilin VP. Surface modification of pharmaceutical nanocarriers with ascorbate residues improves their tumor-cell association and killing and the cytotoxic action of encapsulated paclitaxel in vitro. Pharm. Res. 25(11), 2567-2572 (2008).
33. Kibria G, Hatakeyama H, Ohga N, Hida K, Harashima H. Dual-ligand modification of PEGylated liposomes shows better cell selectivity and efficient gene delivery. J. Control Release 153(2), 141-148 (2011).
34. Manjappa AS, Chaudhari KR, Venkataraju MP et al. Antibody derivatization and conjugation strategies: application in preparation of stealth immunoliposome to target chemotherapeutics to tumor. J. Control Release 150(1), 2-22 (2011).
35. Allen C, Dos Santos N, Gallagher R et al. Controlling the physical behavior and biological performance of liposome formulations through use of surface grafted poly(ethylene glycol).Biosci. Rep. 22(2), 225-250 (2002).
36. Teicher BA. Potentiation of cytotoxic cancer therapies by antiangiogenic agents. In: Antiangiogenic Agents in Cancer Therapy. Teicher BA (Ed.).Humana Press Inc., Totowa, NJ, USA, 277-316 (1999).
37. Ng SS, Sparreboom A, Shaked Y et al. Influence of formulation vehicle on metronomic taxane chemotherapy: albumin-bound versus cremophor EL-based paclitaxel. Clin. Cancer Res. 12(14 Pt 1), 4331-4338 (2006).
38. Horton JK, Houghton PJ, Houghton JA. Relationships between tumor responsiveness, vincristine pharmacokinetics and arrest of mitosis in human tumor xenografts. Biochem. Pharmacol. 37(20), 3995-4000 (1988).
39. Horton JK, Thimmaiah KN, Houghton JA, Horowitz ME, Houghton PJ. Modulation by verapamil of vincristine pharmacokinetics and toxicity in mice bearing human tumor xenografts. Biochem. Pharmacol. 38(11), 1727-1736 (1989).
40. Vaage J, Barbera-Guillem E, Abra R, Huang A, Working P. Tissue distribution and therapeutic effect of intravenous free or encapsulated liposomal doxorubicin on human prostate carcinoma xenografts. Cancer 73(5), 1478-1484 (1994).
41. Vaage J, Donovan D, Uster P, Working P. Tumour uptake of doxorubicin in polyethylene glycol-coated liposomes and therapeutic effect against a xenografted human pancreatic carcinoma. Br. J. Cancer 75(4), 482-486 (1997).
42. Lu Wl, Qi Xr, Zhang Q et al. A PEGylated liposomal platform: pharmacokinetics, pharmacodynamics, and toxicity in mice using doxorubicin as a model drug. J. Pharmacol. Sci. 95(3), 381-389 (2004).
43. Messerer CL, Ramsay EC, Waterhouse D et al. Liposomal irinotecan: formulation development and therapeutic assessment in murine xenograft models of colorectal cancer. Clin. Cancer Res. 10(19), 6638-6649 (2004).
44. Ramsay EC, Anantha M, Zastre J et al. Irinophore C: a liposome formulation of irinotecan with substantially improved therapeutic efficacy against a panel of human xenograft tumors. Clin. Cancer Res. 14(4), 1208-1217 (2008).
45. Serwer LP, Noble CO, Michaud K et al. Investigation of intravenous delivery of nanoliposomal topotecan for activity against orthotopic glioblastoma xenografts. Neuro Oncol. doi: 10.1093/neuonc/nor139 (2011) (Epub ahead of print).
46. Harrington KJ, Rowlinson-Busza G, Uster PS, Stewart JS. Pegylated liposome-encapsulated doxorubicin and cisplatin in the treatment of head and neck xenograft tumours. Cancer Chemother Pharmacol 46, 10-18 (2000)
47. Ramsay E, Alnajim J, Anantha M et al. Transition metal-mediated liposomal encapsulation of irinotecan (CPT-11) stabilizes the drug in the therapeutically active lactone conformation. Pharm. Res. 23(12), 2799-2808 (2006).
48. Vajkoczy P, Menger MD. Vascular microenvironment in gliomas. J. Neurooncol. 50(1-2), 99-108 (2000).
49. Bell-Mcguinn KM, Matthews CM, Ho SN et al. A Phase II, single-arm study of the anti-a5b1 integrin antibody volociximab as monotherapy in patients with platinum-resistant advanced epithelial ovarian or primary peritoneal cancer. Gynecol. Oncol. 121(2), 273-279 (2011).
50. Posey JA, Ng TC, Yang B et al. A Phase I study of anti-kinase insert domain-containing receptor antibody, IMC-1C11, in patients with liver metastases from colorectal carcinoma. Clin. Cancer Res. 9(4), 1323-1332 (2003).
51. Hersey P, Sosman J, O'Day S et al. A randomized Phase 2 study of etaracizumab, a monoclonal antibody against integrin avb3, + or - dacarbazine in patients with stage IV metastatic melanoma. Cancer 116(6), 1526-1534 (2010).
52. Mas-Moruno C, Rechenmacher F, Kessler H. Cilengitide: the first anti-angiogenic small molecule drug candidate design, synthesis and clinical evaluation. Anticancer Agents Med. Chem. 10(10), 753-768 (2010).
53. Matei D, Sill MW, Lankes HA et al. Activity of sorafenib in recurrent ovarian cancer and primary peritoneal carcinomatosis: a gynecologic oncology group trial. J. Clin. Oncol. 29(1), 69-75 (2011).
54. Abou-Alfa GK, Johnson P, Knox JJ et al. Doxorubicin plus sorafenib vs doxorubicin alone in patients with advanced hepatocellular carcinoma: a randomized trial. JAMA 304(19), 2154-2160 (2010).
55. Welch SA, Hirte HW, Elit L et al. Sorafenib in combination with gemcitabine in recurrent epithelial ovarian cancer: a study of the Princess Margaret Hospital Phase II Consortium. Int. J. Gynecol. Cancer 20(5), 787-793 (2010).
56. Wilhelm SM, Carter C, Tang L et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/ MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res. 64(19), 7099-7109 (2004).
57. Socinski MA. The current status and evolving role of sunitinib in non-small cell lung cancer. J. Thorac. Oncol. 3(6 Suppl 2), S119-123 (2008).
58. Mross K, Buchert M, Fasol U et al. A preliminary report of a Phase II study of folinic acid, 5-fluorouracil, irinotecan (FOLFIRI) plus sunitinib with toxicity, efficacy, pharmacokinetics, biomarker, imaging data in patients with colorectal cancer with liver metastases as 1st line treatment. Int. J. Clin. Pharmacol. Ther. 49(1), 96-98 (2011).
59. Mukherji D, Larkin J, Pickering L. Sunitinib for metastatic renal cell carcinoma. Future Oncol. 6(9), 1377-1385 (2010).
60. Fox E, Aplenc R, Bagatell R et al. A Phase 1 trial and pharmacokinetic study of cediranib, an orally bioavailable pan-vascular endothelial growth factor receptor inhibitor, in children and adolescents with refractory solid tumors. J. Clin. Oncol. 28(35), 5174-5181 (2010).
61. Ramalingam SS, Belani CP, Mack PC et al. Phase II study of Cediranib (AZD 2171), an inhibitor of the vascular endothelial growth factor receptor, for second-line therapy of small cell lung cancer (National Cancer Institute #7097).J. Thorac. Oncol. 5(8), 1279-1284 (2010).
62. Batchelor TT, Duda DG, Di Tomaso E et al. Phase II study of cediranib, an oral pan-vascular endothelial growth factor receptor tyrosine kinase inhibitor, in patients with recurrent glioblastoma. J. Clin. Oncol. 28(17), 2817-2823 (2010).
63. Tan AR, Dowlati A, Jones SF et al. Phase I study of pazopanib in combination with weekly paclitaxel in patients with advanced solid tumors. Oncologist 15(12), 1253-1261 (2010).
64. Ward JE, Stadler WM. Pazopanib in renal cell carcinoma. Clin. Cancer Res. 16(24), 5923-5927 (2010).
65. De Boer RH, Arrieta O, Yang CH et al. Vandetanib plus pemetrexed for the second-line treatment of advanced non-small-cell lung cancer: a randomized, double-blind Phase III trial. J. Clin. Oncol. 29(8), 1067-1074 (2011).
66. Blackhall FH, O'Brien M, Schmid P et al. A Phase I study of Vandetanib in combination with vinorelbine/cisplatin or gemcitabine/ cisplatin as first-line treatment for advanced non-small cell lung cancer. J. Thorac. Oncol. 5(8), 1285-1288 (2010).
67. Petre CE, Dittmer DP. Liposomal daunorubicin as treatment for Kaposi's sarcoma. Int. J. Nanomedicine 2(3), 277-288 (2007).
68. Abraham SA, Waterhouse DN, Mayer LD, Cullis PR, Madden TD, Bally MB. The liposomal formulation of doxorubicin. Methods Enzymol. 391, 71-97 (2005).
69. Tardi P, Johnstone S, Harasym N et al. In vivo maintenance of synergistic cytarabine:daunorubicin ratios greatly enhances therapeutic efficacy. Leuk. Res. 33(1), 129-139 (2009).
70. Batist G, Gelmon KA, Chi KN et al. Safety, pharmacokinetics, and efficacy of CPX-1 liposome injection in patients with advanced solid tumors. Clin. Cancer Res. 15(2), 692-700 (2009).
71. Bedikian AY, Silverman JA, Papadopoulos NE et al. Pharmacokinetics and safety of marqibo (vincristine sulfate liposomes injection) in cancer patients with impaired liver function. J. Clin. Pharmacol. 51(8), 1205-1212 (2011).
72. Yang SH, Lin CC, Lin ZZ, Tseng YL, Hong RL. A Phase I and pharmacokinetic study of liposomal vinorelbine in patients with advanced solid tumor. Invest. New Drugs doi: 10.1007/s10637-010-9522-3 (2010)