Polymeric micelles for enhanced lymphatic drug delivery to treat metastatic tumors

Journal of Controlled Release

Volumn 171, Issue 2, 2013, Pages 133-142

  Qin, Lei ^a   Zhang, Fayun ^a   Lu, Xiaoyan ^d   Wei, Xiuli ^a   Wang, Jing ^a   Fang, Xiaocui ^a   Si, Duanyun ^b   Wang, Yiguang ^a   Zhang, Chunling ^a   Yang, Rong ^c   Liu, Changxiao ^b   Liang, Wei ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b TIANJIN INSTITUTE OF PHARMACEUTICAL RESEARCH   (China)

^c NATIONAL CENTER FOR NANOSCIENCE AND TECHNOLOGY   (China)

^d ZHEJIANG UNIVERSITY   (China)

Author keywords

Biodistribution; Extravasation; Lymphatic drug delivery; Metastatic tumor; Polymeric micelles

Indexed keywords

BLOOD VESSELS; BODY FLUIDS; MAMMALS; MEDICAL IMAGING; MICELLES; PATHOLOGY; TISSUE; TUMORS;

BIODISTRIBUTIONS; BIOLUMINESCENT IMAGING; EXTRAVASATION; METASTATIC TUMORS; PHOSPHATIDYLETHANOLAMINE; POLYMERIC MICELLE; SYSTEMIC ADMINISTRATION; TWO PHOTON MICROSCOPY;

POLYMERS;

DOXORUBICIN; MACROGOL; NANOVIN; NAVELBINE; PHOSPHATIDYLETHANOLAMINE; UNCLASSIFIED DRUG;

ACUTE TOXICITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOLUMINESCENCE; BREAST TUMOR; CANCER INHIBITION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG EXTRAVASATION; ENCAPSULATION; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; INTERSTITIUM; LUNG METASTASIS; LYMPH NODE; LYMPH NODE METASTASIS; LYMPH VESSEL; MICELLE; MOUSE; NONHUMAN; POLYMERIZATION; PRIMARY TUMOR; PRIORITY JOURNAL;

AXI; AXILLARY; BIODISTRIBUTION; DISTEAROYL-SN-GLYCERO-3-PHOSPHOETHANOLAMINE-N-[METHOXY (POLYETHYLENE GLYCOL)-2000]; DOX; DOXORUBICIN; EXTRAVASATION; I.V; ICG; INDOCYANINE GREEN; ING; INGUINAL; INTRAVENOUS; LN; LYMPH NODE; LYMPHATIC DRUG DELIVERY; MES; MESENTERY; METASTATIC TUMOR; PEG-PE; POLYMERIC MICELLES; VIN; VINORELBINE;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; DRUG DELIVERY SYSTEMS; FEMALE; HUMANS; LUNG NEOPLASMS; LYMPH NODES; LYMPHATIC METASTASIS; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, INBRED BALB C; MICE, NUDE; MICELLES; PHOSPHATIDYLETHANOLAMINES; POLYETHYLENE GLYCOLS; TUMOR BURDEN; VINBLASTINE;

EID: 84881169872     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.07.005     Document Type: Article

References (67)

1. G.P. Gupta, J. Massague, Cancer metastasis: building a framework, Cell 127 (2006) 679-695. (Pubitemid 44781029)
2. S.N. Markovic, L.A. Erickson, R.D. Rao, R.H. Weenig, B.A. Pockaj, A. Bardia, C.M. Vachon, S.E. Schild, R.R. McWilliams, J.L. Hand, S.D. Laman, L.A. Kottschade, W.J. Maples, M.R. Pittelkow, J.S. Pulido, J.D. Cameron, E.T. Creagan, Malignant melanoma in the 21st century, part 1: epidemiology, risk factors, screening, prevention, and diagnosis, Mayo Clin. Proc. 82 (2007) 364-380. (Pubitemid 46348938)
3. Y. Xie, T.R. Bagby, M.S. Cohen, M.L. Forrest, Drug delivery to the lymphatic system: importance in future cancer diagnosis and therapies, Expert Opin. Drug Deliv. 6 (2009) 785-792.
4. S.L. Chen, D.M. Iddings, R.P. Scheri, A.J. Bilchik, Lymphatic mapping and sentinel node analysis: current concepts and applications, CA Cancer J. Clin. 56 (2006) 292-309, (quiz 316-297). (Pubitemid 44527491)
5. M.A. Swartz, The physiology of the lymphatic system, Adv. Drug Deliv. Rev. 50 (2001) 3-20. (Pubitemid 32727274)
6. V.I. Kaledin, N.A. Matienko, V.P. Nikolin, Y.V. Gruntenko, V.G. Budker, Intralymphatic administration of liposome-encapsulated drugs to mice - possibility for suppression of the growth of tumor-metastases in the lymph-nodes, J. Natl Cancer Inst. 66 (1981) 881-887. (Pubitemid 11096540)
7. Z.Q. Yan, C.Y. Zhan, Z.Y. Wen, L.L. Feng, F. Wang, Y. Liu, X.K. Yang, Q. Dong, M. Liu, W.Y. Lu, LyP-1-conjugated doxorubicin-loaded liposomes suppress lymphatic metastasis by inhibiting lymph node metastases and destroying tumor lymphatics, Nanotechnology 22 (2011).
8. C.K. Kim, J.H. Han, Lymphatic delivery and pharmacokinetics of methotrexate after intramuscular injection of differently charged liposome-entrapped methotrexate to rats, J. Microencapsul. 12 (1995) 437-446.
9. J.S. Karajgi, S.P. Vyas, A lymphotropic colloidal carrier system for diethylcarbama-zine: preparation and performance evaluation, J. Microencapsul. 11 (1994) 539-545. (Pubitemid 24276817)
10. S.T. Reddy, A.J. van der Vlies, E. Simeoni, V. Angeli, G.J. Randolph, C.P. O'Neil, L.K. Lee, M.A. Swartz, J.A. Hubbell, Exploiting lymphatic transport and complement activation in nanoparticle vaccines, Nat. Biotechnol. 25 (2007) 1159-1164. (Pubitemid 47538111)
11. B. Lu, S.B. Xiong, H. Yang, X.D. Yin, R.B. Chao, Solid lipid nanoparticles of mitoxantrone for local injection against breast cancer and its lymph node metastases, Eur. J. Pharm. Sci. 28 (2006) 86-95.
12. N. Ohtsuka, T. Konno, Y. Miyauchi, H. Maeda, Anticancer effects of arterial administration of the anticancer agent SMANCS with lipiodol on metastatic lymph nodes, Cancer 59 (1987) 1560-1565. (Pubitemid 17060095)
13. H. Maeda, SMANCS and polymer-conjugated macromolecular drugs: advantages in cancer chemotherapy, Adv. Drug Deliv. Rev. 46 (2001) 169-185.
14. H. Maeda, Y. Matsumura, Tumoritropic and lymphotropic principles of macromo-lecular drugs, Crit. Rev. Ther. Drug Carrier Syst. 6 (1989) 193-210. (Pubitemid 20065994)
15. K. Yamasaki, T. Konno, Y. Miyauchi, H. Maeda, Reduction of hepatic metastases in rabbits by administration of an oily anticancer agent into the portal vein, Cancer Res. 47 (1987) 852-855. (Pubitemid 17027985)
16. V.P. Torchilin, Recent advances with liposomes as pharmaceutical carriers, Nat. Rev. Drug Discov. 4 (2005) 145-160. (Pubitemid 40282557)
17. H.M. Aliabadi, M. Shahin, D.R. Brocks, A. Lavasanifar, Disposition of drugs in block copolymer micelle delivery systems: from discovery to recovery, Clin. Pharmacokinet. 47 (2008) 619-634.
18. F. Alexis, E. Pridgen, L.K. Molnar, O.C. Farokhzad, Factors affecting the clearance and biodistribution of polymeric nanoparticles, Mol. Pharm. 5 (2008) 505-515.
19. R. Savic, L. Luo, A. Eisenberg, D. Maysinger, Micellar nanocontainers distribute to defined cytoplasmic organelles, Science 300 (2003) 615-618. (Pubitemid 36520581)
20. Y.H. Bae, H. Yin, Stability issues of polymeric micelles, J. Control. Release 131 (2008) 2-4.
21. R.K. Jain, Delivery of molecular and cellular medicine to solid tumors, Adv. Drug Deliv. Rev. 46 (2001) 149-168.
22. K. Hori, M. Nishihara, M. Yokoyama, Vital microscopic analysis of polymeric micelle extravasation from tumor vessels: macromolecular delivery according to tumor vascular growth stage, J. Pharm. Sci. 99 (2010) 549-562.
23. A.I. Minchinton, I.F. Tannock, Drug penetration in solid tumours, Nat. Rev. Cancer 6 (2006) 583-592. (Pubitemid 44140857)
24. N. Tang, G. Du, N. Wang, C. Liu, H. Hang, W. Liang, Improving penetration in tumors with nanoassemblies of phospholipids and doxorubicin, J. Natl. Cancer Inst. 99 (2007) 1004-1015. (Pubitemid 47232602)
25. Y. Wang, R. Wang, X. Lu, W. Lu, C. Zhang, W. Liang, Pegylated phospholipids-based self-assembly with water-soluble drugs, Pharm. Res. 27 (2010) 361-370.
26. H. Dafni, T. Israely, Z.M. Bhujwalla, L.E. Benjamin, M. Neeman, Overexpression of vascular endothelial growth factor 165 drives peritumor interstitial convection and induces lymphatic drain: magnetic resonance imaging, confocal microscopy, and histological tracking of triple-labeled albumin, Cancer Res. 62 (2002) 6731-6739. (Pubitemid 35364145)
27. C.A. Kunder, A.L. St John, G. Li, K.W. Leong, B. Berwin, H.F. Staats, S.N. Abraham, Mast cell-derived particles deliver peripheral signals to remote lymph nodes, J. Exp. Med. 206 (2009) 2455-2467.
28. D. Wang, X. Liu, J. Bai, Analysis of fast full angle fluorescence diffuse optical tomography with beam-forming illumination, Opt. Express 17 (2009) 21376-21395.
29. F. Liu, X. Liu, D. Wang, B. Zhang, J. Bai, A parallel excitation based fluorescence molecular tomography system for whole-body simultaneous imaging of small animals, Ann. Biomed. Eng. 38 (2010) 3440-3448.
30. T. Mosmann, Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays, J. Immunol. Methods 65 (1983) 55-63. (Pubitemid 14203433)
31. A.N. Lukyanov, Z. Gao, L. Mazzola, V.P. Torchilin, Polyethylene glycol-diacyllipid micelles demonstrate increased acculumation in subcutaneous tumors in mice, Pharm. Res. 19 (2002) 1424-1429. (Pubitemid 35266545)
32. T. Wang, V.A. Petrenko, V.P. Torchilin, Paclitaxel-loaded polymeric micelles modified with MCF-7 cell-specific phage protein: enhanced binding to target cancer cells and increased cytotoxicity, Mol. Pharm. 7 (2010) 1007-1014.
33. X. Wei, Y. Wang, W. Zeng, F. Huang, L. Qin, C. Zhang, W. Liang, Stability influences the biodistribution, toxicity, and anti-tumor activity of doxorubicin encapsulated in PEG-PE micelles in mice, Pharm. Res. 29 (2012) 1977-1989.
34. F. Yuan,M. Leunig, S.K. Huang, D.A. Berk, D. Papahadjopoulos, R.K. Jain, Microvascular permeability and interstitial penetration of sterically stabilized (stealth) liposomes in a human tumor xenograft, Cancer Res. 54 (1994) 3352-3356. (Pubitemid 24225946)
35. H. Chen, S. Kim, W. He, H. Wang, P.S. Low, K. Park, J.X. Cheng, Fast release of lipophilic agents from circulating PEG-PDLLA micelles revealed by in vivo forster resonance energy transfer imaging, Langmuir 24 (2008) 5213-5217.
36. A. Supersaxo, W.R. Hein, H. Steffen, Mixed micelles as a proliposomal, lymphotropic drug carrier, Pharm. Res. 8 (1991) 1286-1291.
37. T. Okouneva, B.T. Hill, L. Wilson, M.A. Jordan, The effects of vinflunine, vinorelbine, and vinblastine on centromere dynamics, Mol. Cancer Ther. 2 (2003) 427-436.
38. V. Saxena, M. Sadoqi,J. Shao, Indocyanine green-loaded biodegradable nanoparticles: preparation, physicochemical characterization and in vitro release, Int. J. Pharm. 278 (2004) 293-301. (Pubitemid 38759502)
39. A. Romero, M.G. Rabinovich, C.T. Vallejo, J.E. Perez, R. Rodriguez, M.A. Cuevas, M. Machiavelli, J.A. Lacava, M. Langhi, L.R. Acuna, S. Amato, R. Barbieri, C. Sabatini, B.A. Leone, Vinorelbine as first-line chemotherapy for metastatic breast-carcinoma, J. Clin. Oncol. 12 (1994) 336-341. (Pubitemid 24056407)
40. X.Y. Lu, F.Y. Zhang, L. Qin, F.Y. Xiao, W. Liang, Polymeric micelles as a drug delivery system enhance cytotoxicity of vinorelbine through more intercellular accumulation, Drug Deliv. 17 (2010) 255-262.
41. C.J. Aslakson, F.R. Miller, Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor, Cancer Res. 52 (1992) 1399-1405.
42. B.A. Pulaski, S. Ostrand-Rosenberg, Mouse 4 T1 breast tumor model, Curr. Protoc. Immunol. (2001) 1-11, (Chapter 20, Unit 20.2).
43. A.E. Giuliano, P.S. Dale, R.R. Turner, D.L. Morton, S.W. Evans, D.L. Krasne, Improved axillary staging of breast cancer with sentinel lymphadenectomy, Ann. Surg. 222 (1995) 394-399, (discussion 399 - 401).
44. S.A. Johnson, P. Harper, G.N. Hortobagyi, P. Pouillart, Vinorelbine: an overview, Cancer Treat. Rev. 22 (1996) 127-142. (Pubitemid 26235725)
45. C. Oussoren, G. Storm, Liposomes to target the lymphatics by subcutaneous administration, Adv. Drug Deliv. Rev. 50 (2001) 143-156. (Pubitemid 32727280)
46. S. Cai, Q.H. Yang, T.R. Bagby, M.L. Forrest, Lymphatic drug delivery using engineered liposomes and solid lipid nanoparticles, Adv. Drug Deliv. Rev. 63 (2011) 901-908.
47. J. Rosenecker, W. Zhang, K. Hong, J. Lausier, P. Geppetti, S. Yoshihara, D. Papahadjopoulos, J.A. Nadel, Increased liposome extravasation in selected tissues: effect of substance P, Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 7236-7241. (Pubitemid 26243532)
48. M.G. Harisinghani, J. Barentsz, P.F. Hahn, W.M. Deserno, S. Tabatabaei, C.H. van de Kaa, J. de la Rosette, R. Weissleder, Noninvasive detection of clinically occult lymph-node metastases in prostate cancer, N. Engl. J. Med. 348 (2003) 2491-2499. (Pubitemid 36706536)
49. C.W. Jung, P. Jacobs, Physical and chemical properties of superparamagnetic iron oxide MR contrast agents: ferumoxides, ferumoxtran, ferumoxsil, Magn. Reson. Imaging 13 (1995) 661-674.
50. L.M. Kaminskas, J. Kota, V.M. McLeod, B.D. Kelly, P. Karellas, C.J. Porter, PEGylation of polylysine dendrimers improves absorption and lymphatic targeting following SC administration in rats, J. Control. Release 140 (2009) 108-116.
51. M. Rafi, H. Cabral, M.R. Kano, P. Mi, C. Iwata, M. Yashiro, K. Hirakawa, K. Miyazono, N. Nishiyama, K. Kataoka, Polymeric micelles incorporating (1,2-diaminocyclohexane) platinum (II) suppress the growth of orthotopic scirrhous gastric tumors and their lymph node metastasis, J. Control. Release 159 (2012) 189-196.
52. W.A. Muller, Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response, Trends Immunol. 24 (2003) 327-334.
53. B. Engelhardt, H. Wolburg, Mini-review: transendothelial migration of leukocytes: through the front door or around the side of the house? Eur. J. Immunol. 34 (2004) 2955-2963. (Pubitemid 39549374)
54. C.C. Huang, J.P. Ryckaert, H. Xu, Structure and dynamics of cylindrical micelles at equilibrium and under shear flow, Phys. Rev. E 79 (2009).
55. T. Musacchio, V. Laquintana, A. Latrofa, G. Trapani, V.P. Torchilin, PEG-PE micelles loaded with paclitaxel and surface-modified by a PBR-ligand: synergistic anticancer effect, Mol. Pharm. 6 (2009) 468-479.
56. T. Miller, R. Rachel, A. Besheer, S. Uezguen, M. Weigandt, A. Goepferich, Comparative investigations on in vitro serum stability of polymeric micelle formulations, Pharm. Res. 29 (2012) 448-459.
57. J. Lu, S.C. Owen, M.S. Shoichet, Stability of self-assembled polymeric micelles in serum, Macromolecules 44 (2011) 6002-6008.
58. D.K. Hsu, F.T. Liu, Regulation of cellular homeostasis by galectins, Glycoconj. J. 19 (2004) 507-515. (Pubitemid 38316524)
59. Y. He, K. Kozaki, T. Karpanen, K. Koshikawa, S. Yla-Herttuala, T. Takahashi, K. Alitalo, Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling, J. Natl. Cancer Inst. 94 (2002) 819-825. (Pubitemid 34705053)
60. B.A. Pulaski, M.J. Smyth, S. Ostrand-Rosenberg, Interferon-gamma- dependent phagocytic cells are a critical component of innate immunity against metastatic mammary carcinoma, Cancer Res. 62 (2002) 4406-4412. (Pubitemid 34827300)
61. S. You, L. Zuo, W. Li, Optimizing the time of Doxil injection to increase the drug retention in transplanted murine mammary tumors, Int. J. Nanomedicine 5 (2010) 221-229.
62. S.D. Perrault, C. Walkey, T. Jennings, H.C. Fischer, W.C. Chan, Mediating tumor targeting efficiencyofnanoparticles through design, Nano Lett. 9 (2009) 1909-1915.
63. R.K. Jain, Delivery of molecular and cellular medicine to solid tumors, J. Control. Release 53 (1998) 49-67. (Pubitemid 28218689)
64. C. Wong, T. Stylianopoulos, J. Cui, J. Martin, V.P. Chauhan, W. Jiang, Z. Popovic, R.K. Jain, M.G. Bawendi, D. Fukumura, Multistage nanoparticle delivery system for deep penetration into tumor tissue, Proc. Natl. Acad. Sci. U. S. A. 108 (2011) 2426-2431.
65. V.P. Chauhan, T. Stylianopoulos, J.D. Martin, Z. Popovic, O. Chen, W.S. Kamoun, M.G. Bawendi, D. Fukumura, R.K. Jain, Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner, Nat. Nanotechnol. 7 (2012) 383-388.
66. J. Wang, Y. Wang, W. Liang, Delivery of drugs to cell membranes by encapsulation in PEG-PE micelles, J. Control. Release 160 (2012) 637-651.
67. T. Schacker, The role of secondary lymphatic tissue in immune deficiency of HIV infection, AIDS 22 (Suppl. 3) (2008) S13-S18.