HPMA-based polymer therapeutics improve the efficacy of surgery, of radiotherapy and of chemotherapy combinations

Nanomedicine

Volumn 5, Issue 10, 2010, Pages 1501-1523

  Lammers, Twan ^a,b,c   Subr, Vladimir ^d   Ulbrich, Karel ^d   Peschke, Peter ^c   Huber, Peter E ^c   Hennink, Wim E ^b   Storm, Gert ^b   Kiessling, Fabian ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b UTRECHT UNIVERSITY   (Netherlands)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d INSTITUTE OF MACROMOLECULAR CHEMISTRY   (Czech Republic)

Author keywords

chemotherapy; combination therapy; drug targeting; hpma copolymers; image guided drug delivery; nanomedicine; polymer therapeutics; radiotherapy; surgery; theranostics

Indexed keywords

AMINOGLUTETHIMIDE; ANTINEOPLASTIC AGENT; AP 5280; AP 5346; CAPLOSTATIN; CISPLATIN; COPOLYMER; CORTICOSTEROID; CYTARABINE; DAUNORUBICIN; DOXORUBICIN; DOXORUBICIN DERIVATIVE; DRUG CARRIER; FLOXURIDINE; FUMAGILLOL CHLOROACETYLCARBAMATE; GEMCITABINE; IRINOTECAN; LIPOSOME; N (2 HYDROXYPROPYL)METHACRYLAMIDE; OXALIPLATIN; PACLITAXEL; PACLITAXEL DERIVATIVE; PACLITAXEL POLIGLUMEX; PK 1; PLATINUM DERIVATIVE; PNU 166945; POLYMER; UNCLASSIFIED DRUG; VINCRISTINE;

ADVANCED CANCER; ALOPECIA; AREA UNDER THE CURVE; BONE MARROW SUPPRESSION; BREAST CANCER; CANCER CELL DESTRUCTION; CANCER COMBINATION CHEMOTHERAPY; CANCER LOCALIZATION; CANCER RADIOTHERAPY; CANCER RESISTANCE; CANCER SURGERY; CARDIOTOXICITY; CHEMORADIOTHERAPY; CLINICAL EFFECTIVENESS; COLORECTAL CANCER; DRUG CONJUGATION; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG FORMULATION; DRUG RETENTION; DRUG STRUCTURE; DRUG TOLERABILITY; ESOPHAGUS CANCER; HUMAN; LIPOSOMAL DELIVERY; LUNG NON SMALL CELL CANCER; MOLECULARLY TARGETED THERAPY; MULTIMODALITY CANCER THERAPY; MULTIPLE CYCLE TREATMENT; NANOENCAPSULATION; NANOMEDICINE; NAUSEA; NEUROTOXICITY; NONHUMAN; OVARY CARCINOMA; PRIORITY JOURNAL; RADIOSENSITIZATION; REVIEW; SINGLE DRUG DOSE; STOMACH CANCER; TUMOR LOCALIZATION;

ACRYLAMIDES; ANIMALS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; HUMANS; NANOMEDICINE; NEOPLASMS; POLYMERS;

EID: 78650541819     PISSN: 17435889     EISSN: None     Source Type: Journal    
DOI: 10.2217/nnm.10.130     Document Type: Review

References (93)

1. Langer R: Drug delivery and targeting. Nature 392, S5-S10 (1998). (Pubitemid 28215187)
2. Torchilin VP: Drug targeting. Eur. J. Pharm. Sci. 11, S81-S91 (2000).
3. Allen TM, Cullis PR: Drug delivery systems: entering the mainstream. Science 303, 1818-22 (2004).
4. Peer D, Karp JM, Hong S, Farokhzad O, Margalit R, Langer R: Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2, 751-760 (2007). (Pubitemid 350223348)
5. Davis ME, Chen ZG, Shin DM: Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat. Rev. Drug Discov. 7, 771-782 (2008).
6. Lammers T, Hennink WE, Storm G: Tumour-targeted nanomedicines: principles and practice. Br. J. Cancer 99, 392-397 (2008).
7. Maeda H, Matsumura Y: A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent Smancs. Cancer Res. 46, 6387-6392 (1986). (Pubitemid 17221789)
8. Maeda H, Wu J, Sawa T, Matsumura Y, Hori K: Tumour vascular permeability and the EPR effect in macromolecular therapeutics: a review. J. Control. Release 65, 271-284 (2000). (Pubitemid 30122932)
9. Crommelin DJA, Scherphof G, Storm G: Active targeting with particulate carrier systems in the blood compartment. Adv. Drug Deliv. Rev. 17, 49-60 (1995).
10. Allen TM: Ligand-targeted therapeutics in anticancer therapy. Nat. Rev. Cancer 2, 750-763 (2002).
11. Marcucci F, Lefoulon L: Active targeting with particulate drug carriers in tumor therapy: fundamentals and recent progress. Drug Discov. Today 9, 219-228 (2004). (Pubitemid 38230021)
12. Arap W, Pasqualini R, Ruoslahti E: Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model. Science 279, 377-380 (1998). (Pubitemid 28063372)
13. Neri D, Bicknell R: Tumour vascular targeting. Nat. Rev. Cancer 5, 436-446 (2005). (Pubitemid 40791486)
14. Temming K, Schiffelers RM, Molema G, Kok RJ: RGD-based strategies for selective delivery of therapeutics and imaging agents to the tumour vasculature. Drug Resist. Updat. 8, 381-402 (2005). (Pubitemid 43358061)
15. Guo X, Szoka FC Jr: Chemical approaches to triggerable lipid vesicles for drug and gene delivery. Acc. Chem. Res. 36, 335-341 (2003).
16. Ganta S, Devalapally H, Shahiwala A, Amiji M: A review of stimuli-responsive nanocarriers for drug and gene delivery. J. Control. Release 126, 187-204 (2008).
17. Torchilin V: Multifunctional and stimuli-sensitive pharmaceutical nanocarriers. Eur. J. Pharm. Biopharm. 71, 431-444 (2009).
18. Langer RS, Peppas NA: Present and future applications of biomaterials in controlled drug delivery systems. Biomaterials 2, 201-214 (1981).
19. Peppas NA, Bures P, Leobandung W, Ichikawa H: Hydrogels in pharmaceutical formulations. Eur. J. Pharm. Biopharm. 50(1), 27-46 (2000). (Pubitemid 30326687)
20. Hoffman AS: Hydrogels for biomedical applications. Adv. Drug Deliv. Rev. 54, 3-12 (2002).
21. Harris L, Batist G, Belt R et al.: Liposome-encapsulated doxorubicin compared with conventional doxorubicin in a randomized multicenter trial as first-line therapy of metastatic breast carcinoma. Cancer 94, 25-36 (2002). (Pubitemid 34049039)
22. Drummond DC, Meyer O, Hong K, Kirpotin DB, Papahadjopoulos D: Optimizing liposomes for delivery of chemotherapeutic agents to solid tumours. Pharmacol. Rev. 51, 691-743 (1999).
23. Hofheinz RD, Gnad-Vogt SU, Beyer U, Hochhaus A: Liposomal encapsulated anti-cancer drugs. Anticancer Drugs 16, 691-707 (2005). (Pubitemid 41104918)
24. Torchilin VP: Recent advances with liposomes as pharmaceutical carriers. Nat. Rev. Drug Discov. 4, 145-160 (2005).
25. Northfelt DW, Dezube BJ, Thommes JA et al.: PEGylated-liposomal doxorubicin versus doxorubicin, bleomycin, and vincristine in the treatment of AIDS-related Kaposis sarcoma: results of a randomized Phase III clinical trial. J. Clin. Oncol. 16, 2445-2451 (2005).
26. Vasey PA, Kaye SB, Morrison R et al.: Phase I clinical and pharmacokinetic study of PK1: first member of a new class of chemotherapeutic agents-drug-polymer conjugates. Clin. Cancer Res. 5, 83-94 (1999).
27. Kopecek J, Kopeckova P, Minko T, Lu ZR, Peterson CM: Water soluble polymers in tumor targeted delivery. J. Control. Release 74, 147-158 (2001). (Pubitemid 32727617)
28. Duncan R: Polymer conjugates as anticancer nanomedicines. Nat. Rev. Cancer 6, 688-701 (2006). (Pubitemid 44286001)
29. Duncan R: Development of HPMA copolymer-anticancer conjugates: clinical experience and lessons learnt. Adv. Drug Deliv. Rev. 61, 1131-1148 (2009).
30. Lammers T, Ulbrich K: HPMA copolymers: 30 years of advances. Adv. Drug Deliv. Rev. 62, 119-121 (2010).
31. Lammers T, Kühnlein R, Kissel M et al.: Effect of physicochemical modification on the biodistribution and tumor accumulation of HPMA copolymers. J. Control. Release 110, 103-118 (2005). (Pubitemid 41713935)
32. Kiessling F, Heilmann M, Lammers T et al.: Synthesis and characterization of HE-24.8: a polymeric contrast agent for magnetic resonance angiography. Bioconj. Chem. 17, 42-51 (2006). (Pubitemid 43157583)
33. Lammers T, Subr V, Ulbrich K et al.: Long-circulating and passively tumor-targeted polymer-drug conjugates improve the efficacy and reduce the toxicity of radiochemotherapy. Adv. Biomat. 99(6), 900-910 (2010).
34. Lammers T, Subr V, Peschke P et al.: Image-guided and passively tumour-targeted polymeric nanomedicines for radiochemotherapy. Br. J. Cancer 99, 900-910 (2008).
35. Lammers T: Drug targeting to tumors using HPMA copolymers; revisiting PK1 and partners. PhD Thesis. Utrecht University, Utrecht, The Netherlands (2009).
36. Lammers T, Peschke P, Kühnlein R et al.: Effect of intratumoral injection on the biodistribution and the therapeutic potential of HPMA copolymer-based drug delivery systems. Neoplasia 8, 788-795 (2006). (Pubitemid 44564834)
37. Vokes EE, Weichselbaum RR: Concomitant chemoradiotherapy: rationale and clinical experience in patients with solid tumors. J. Clin. Oncol. 8, 911-934 (2008).
38. Seiwert TY, Salama JK, Vokes EE: The concurrent chemoradiation paradigm - general principles. Nat. Clin. Pract. Oncol. 4, 86-100 (2007).
39. Lammers T, Peschke P, Kühnlein R et al.: Effect of radiotherapy and hyperthermia on the tumor accumulation of HPMA copolymer-based drug delivery systems. J. Control. Release 117, 333-341 (2007). (Pubitemid 46216581)
40. Park JS, Qiao L, Su ZZ, Hinman D, Willoughby K, McKinstry R: Ionizing radiation modulates vascular endothelial growth factor expression through multiple mitogen activated protein kinase dependent pathways. Oncogene 25, 3266-3280 (2001). (Pubitemid 32553679)
41. Dvorak HF, Brown LF, Detmar M, Dvorak AM: Vascular permeability factor/ vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am. J. Pathol. 146, 1029-1039 (1995).
42. Feng D, Nagy JA, Pyne K, Hammel I, Dvorak HF, Dvorak AM: Pathways of macromolecular extravasation across microvascular endothelium in response to VPF/VEGF and other vasoactive mediators. Microcirculation 6, 23-44 (1999). (Pubitemid 129672560)
43. Lee YJ, Galoforo SS, Berns CM et al.: Effect of ionizing radiation on AP-1 binding activity and basic fibroblast growth factor gene expression in drug-sensitive human breast carcinoma MCF-7 and multidrug-resistant MCF-7/ADR cells. J. Biol. Chem. 270, 28790-28796 (1995).
44. Samaniego F, Markham PD, Gendelman R et al.: Vascular endothelial growth factor and basic fibroblast growth factor present in Kaposis sarcoma (KS) are induced by inflammatory cytokines and synergize to promote vascular permeability and KS lesion development. Am. J. Pathol. 152, 1433-1443 (1998). (Pubitemid 28275002)
45. Znati CM, Rosenstein M, Boucher Y, Epperly MW, Bloomer WD, Jain RK: Effect of radiation on interstitial fluid pressure and oxygenation in a human tumor xenograft. Cancer Res. 56, 964-968 (1996). (Pubitemid 26065386)
46. Netti PA, Baxter LT, Boucher Y, Skalak R, Jain RK: Time-dependent behavior of interstitial fluid pressure in solid tumors: implications for drug delivery. Cancer Res. 55, 5451-5458 (1995).
47. Peschke P, Klein V, Wolber G, Friedrich E, Hahn EW: Morphometric analysis of bromodeoxyuridine distribution and cell density in the rat Dunning prostate tumor R3327-AT1 following treatment with radiation and/or hyperthermia. Histol. Histopathol. 14, 461-469 (1999). (Pubitemid 29159014)
48. Au JL, Jang SH, Zheng J et al.: Determinants of drug delivery and transport to solid tumors. J. Control. Release 74, 31-46 (2001). (Pubitemid 32727607)
49. Langley RE, Bump EA, Quartuccio SG, Medeiros D, Braunhut SJ: Radiation-induced apoptosis in microvascular endothelial cells. Brit. J. Cancer 75, 666-672 (1997). (Pubitemid 27091079)
50. Garcia-Barros M, Paris F, Cordon-Cardo C, Lyden D, Rafii S, Haimovitz-Friedman A: Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 300, 1155-1159 (2003). (Pubitemid 36583102)
51. Yeung TK, Hopewell JW, Simmonds RH et al.: Reduced cardiotoxicity of doxorubicin given in the form off N-(2-hydroxypropyl) methacrylamide conjugates: and experimental study in the rat. Cancer Chemother. Pharmacol. 29, 105-111 (1991).
52. Ewer MS, Martin FJ, Henderson C, Shapiro CL, Benjamin RS, Gabizon AA: Cardiac safety of liposomal anthracyclines. Semin. Oncol. 31, 161-181 (2004).
53. Dipetrillo T, Milas L, Evans D et al.: Paclitaxel poliglumex (PPX-Xyotax) and concurrent radiation for esophageal and gastric cancer: a Phase I study. Am. J. Clin. Oncol. 29, 376-379 (2006). (Pubitemid 44197542)
54. Milas L, Mason KA, Hunter N et al.: Poly(l-glutamic acid)-paclitaxel conjugate is a potent enhancer of tumor radiocurability. Int. J. Radiat. Oncol. Biol. Phys. 55, 707-712 (2003). (Pubitemid 36170011)
55. Wiedenmann N, Valdecanas D, Hunter N et al.: 130-nm albumin-bound paclitaxel enhances tumor radiocurability and therapeutic gain. Clin. Cancer Res. 13, 1868-1874 (2007). (Pubitemid 46952957)
56. Mayer LD, Harasym TO, Tardi PG et al.: Ratiometric dosing of anticancer drug combinations: controlling drug ratios after systemic administration regulates therapeutic activity in tumor-bearing mice. Mol. Cancer Ther. 5, 1854-1863 (2006).
57. Abraham SA, McKenzie C, Masin D et al.: In vitro and in vivo characterization of doxorubicin and vincristine coencapsulated within liposomes through use of transition metal ion complexation and pH gradient loading. Clin. Cancer Res. 10, 728-738 (2004). (Pubitemid 38174011)
58. Tardi PG, Gallagher RC, Johnstone S et al.: Coencapsulation of irinotecan and floxuridine into low cholesterol-containing liposomes that coordinate drug release in vivo. Biochim. Biophys. Acta 1768, 678-687 (2007). (Pubitemid 46275599)
59. Tardi P, Johnstone S, Harasym N et al.: In vivo maintenance of synergistic cytarabine:daunorubicin ratios greatly enhances therapeutic efficacy. Leuk. Res. 33, 129-139 (2009).
60. Vicent MJ, Greco F, Nicholson RI, Paul A, Griffiths PC, Duncan R: Polymer therapeutics designed for a combination therapy of hormone-dependent cancer. Angew. Chem. Int. Ed. Engl. 44, 4061-4066 (2005). (Pubitemid 40886448)
61. Greco F, Vicent MJ, Gee S et al.: Investigating the mechanism of enhanced cytotoxicity of HPMA copolymer-Dox-AGM in breast cancer cells. J. Control. Release 117, 28-39 (2007). (Pubitemid 46164864)
62. Lammers T, Subr V, Ulbrich K et al.: Simultaneous delivery of doxorubicin and gemcitabine to tumors in vivo using prototypic polymeric drug carriers. Biomaterials 30, 3466-3475 (2009).
63. Jain RK: Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307, 58-62 (2005).
64. Jain RK, Tong RT, Munn LL: Effect of vascular normalization by antiangiogenic therapy on interstitial hypertension, peritumor edema, and lymphatic metastasis: insights from a mathematical model. Cancer Res. 67, 2729-2735 (2007).
65. Bangham AD, Standish MM, Watkins JC: Diffusion of univalent ions across the lamellae of swollen phospholipids. J. Mol. Biol. 13, 238-252 (1965).
66. Papahadjopoulos D, Allen TM, Gabizon A et al.: Sterically stabilized liposomes: improvements in pharmacokinetics and antitumor therapeutic efficacy. Proc. Natl Acad. Sci. USA 88, 11460-11464 (1991). (Pubitemid 21916061)
67. Klibanov AL, Maruyama K, Torchilin VP, Huang L: Amphipathicpolyethyleneglycols effectively prolong the circulation time of liposomes. FEBS Lett. 268(1), 235-237 (1990). (Pubitemid 20233874)
68. Ringsdorf H: Structure and properties of pharmacologically active polymers. J Polymer Sci. Polymer Symp. 51, 135-153 (1975).
69. Kopecek J, Kopeckova P: HPMA copolymers: origins, early developments, present, and future. Adv. Drug Deliv. Rev. 62, 122-149 (2010).
70. Thomson AH, Vasey PA, Murray LS et al.: Population pharmacokinetics in Phase I drug development: a Phase I study of PK1 in patients with solid tumours. Brit. J. Cancer 81, 99-107 (1999).
71. Julyan PJ, Seymour LW, Ferry DR et al.: Preliminary clinical study of the distribution of HPMA copolymers bearing doxorubicin and galactosamine. J. Control. Release 57, 281-290 (1999).
72. Seymour LW, Ferry DR, Anderson D et al.: Hepatic drug targeting: Phase I evaluation of polymer-bound doxorubicin. J. Clin. Oncol. 20. 1668-1676 (2002). (Pubitemid 34260549)
73. Meerum Terwogt JM, ten Bokkel Huinink WW, Schellens JH et al.: Phase I clinical and pharmacokinetic study of PNU166945, a novel water-soluble polymer-conjugated prodrug of paclitaxel. Anti-Cancer Drugs 12, 315-323 (2001).
74. Rademaker-Lakhai JM, Terret C, Howell SB et al.: A Phase I and pharmacological study of the platinum polymer AP5280 given as an intravenous infusion once every 3 weeks in patients with solid tumors. Clin. Cancer Res. 10, 3386-3395 (2004). (Pubitemid 38685444)
75. Rice JR, Gerberich JL, Nowotnik DB, Howell SB: Preclinical efficacy and pharmacokinetics of AP5346, a novel diaminocyclohexane-platinum tumor-targeting drug delivery system. Clin. Cancer Res. 12, 2248-2254 (2006).
76. Campone M, Rademaker-Lakhai JM, Bennouna J et al.: Phase I and pharmacokinetic trial of AP5346, a DACH-platinum-polymer conjugate, administered weekly for three out of every 4 weeks to advanced solid tumor patients. Cancer Chemother. Pharmacol. 60, 523-533 (2007). (Pubitemid 47084263)
77. Nowotnik DP, Cvitkovic E: ProLindac (AP5346): a review of the development of an HPMA DACH platinum polymer therapeutic. Adv. Drug Deliv. Rev. 61, 1214-1219 (2009).
78. Kasuya Y, Lu ZR, Kopeckova P, Minko T, Tabibi SE, Kopecek J: Synthesis and characterization of HPMA copolymer-aminopropylgeldanamycin conjugates. J. Control. Release 74, 203-211 (2001). (Pubitemid 32727622)
79. Nishiyama N, Nori A, Malugin A, Kasuya Y, Kopeckova P, Kopecek J: Free and HPMA copolymer-bound geldanamycin derivative induce different stress responses in A2780 human ovarian carcinoma cells. Cancer Res. 63, 7876-7882 (2003). (Pubitemid 37466722)
80. Satchi-Fainaro R, Puder M, Davies JW et al.: Targeting angiogenesis with a conjugate of HPMA copolymer and TNP-470. Nat. Med. 10, 255-261 (2004). (Pubitemid 38667615)
81. Satchi-Fainaro R, Mamluk R, Wang L et al.: Inhibition of vessel permeability by TNP-470 and its polymer conjugate, caplostatin. Cancer Cell 3, 251-261 (2005). (Pubitemid 40568684)
82. Lammers T: Improving the efficacy of combined modality anticancer therapy using HPMA copolymer-based nanomedicine formulations. Adv. Drug Deliv. Rev. 62, 203-230 (2010).
83. Banciu M, Metselaar JM, Schiffelers RM, Storm G: Liposomal glucocorticoids as tumor-targeted anti-angiogenic nanomedicine in B16 melanoma-bearing mice. J. Steroid Biochem. Mol. Biol. 111, 101-110 (2008).
84. Banciu M, Metselaar JM, Schiffelers RM, Storm G: Antitumor activity of liposomal prednisolone phosphate depends on the presence of functional tumor-associated macrophages in tumor tissue. Neoplasia. 10, 108-117 (2008). (Pubitemid 351240876)
85. Adams GP, Weiner LM: Monoclonal antibody therapy of cancer. Nat. Biotechnol. 23, 1147-1157 (2005).
86. Sharkey RM, Goldenberg DM: Targeted therapy of cancer: new prospects for antibodies and immunoconjugates. CA Cancer J. Clin. 56226-56243 (2006).
87. Schiffelers RM, Ansari A, Xu J et al.: Cancer siRNA therapy by tumor selective delivery with ligand-targeted sterically stabilized nanoparticle. Nucleic Acids Res. 32, E149 (2004).
88. Davis ME, Zuckerman JE, Choi CH et al.: Evidence of RNAi in humans from systemically administered siRNA via targeted nanoparticles. Nature 464, 1067-1070 (2010).
89. Ozdemir V, Williams-Jones B, Glatt SJ, Tsuang MT, Lohr JB, Reist C: Shifting emphasis from pharmacogenomics to theragnostics. Nat. Biotechnol. 24, 942-946 (2006).
90. Shubayev VI, Pisanic TR, Jin S: Magnetic nanoparticles for theragnostics. Adv. Drug Deliv. Rev. 61, 467-477 (2009).
91. Lammers T, Subr V, Ulbrich K, Hennink WE, Storm G, Kiessling F: Polymeric nanomedicines for image-guided drug delivery and tumor-targeted combination therapy. Nano Today 5, 197-212 (2010).
92. Deng CX, Exner A: Image-guided therapeutics. Mol. Pharmaceut. 7, 1-2 (2010).
93. Lammers T, Kiessling F, Hennink WE, Storm G: Nanotheranostics and image-guided drug delivery: current concepts and future directions. Mol. Pharmaceut. DOI 10.101021/MP100228V (2010) (Epub ahead of print)