Improving anti-angiogenic therapy via selective delivery of cationic liposomes to tumour vasculature

International Journal of Pharmaceutics

Volumn 267, Issue 1-2, 2003, Pages 1-12

  Dass, Crispin R ^a,b  

^a JOHNSON AND JOHNSON   (United States)

^b GeneType Research Laboratories   (Australia)

Author keywords

Cancer; Lipoplex; Liposome; Tumour; Vasculature

Indexed keywords

AMMONIUM DERIVATIVE; ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; CISPLATIN; CREMOPHOR; DIMETHYLDIOCTADECYLAMMONIUM BROMIDE; DIOLEOYLTRIMETHYLAMMONIUM PROPANE; DNA; DOXORUBICIN; FERRITIN; LIPID; LIPOSOME; MYC PROTEIN; NUCLEIC ACID; PACLITAXEL; PROTEIN P53; UNCLASSIFIED DRUG; VINBLASTINE; VIRUS VECTOR;

ADVANCED CANCER; ANGIOGENESIS; COMPLEX FORMATION; DNA TRANSFER; DRUG DELIVERY SYSTEM; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; ENCAPSULATION; GENE CONSTRUCT; GENE THERAPY; HUMAN; INTERSTITIUM; NONHUMAN; NUCLEIC ACID TRANSPORT; PRIORITY JOURNAL; REVIEW; SIDE EFFECT; SOLID TUMOR; TREATMENT OUTCOME; TUMOR VASCULARIZATION; VIRAL GENE DELIVERY SYSTEM;

EID: 0242361237     PISSN: 03785173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2003.08.010     Document Type: Review

References (105)

1. Adair T.H., Gay W.J., Montani J.P. Growth regulation of the vascular system: evidence for a metabolic hypothesis. Am. J. Physiol. 259:1990;R393-R404.
2. Almofti M.R., Harashima H., Shinohara Y., Almofti A., Baba Y., Kiwada H. Cationic liposome-mediated gene delivery: biophysical study and mechanism of internalisation. Arch. Biochem. Biophys. 410:2003;246-253.
3. Aoki K., Yoshida T., Matsumoto N., Ide H., Hosokawa K., Sugimura T., Terada M. Gene therapy for peritoneal dissemination of pancreatic cancer by liposome-mediated transfer of herpes simplex virus thymidine kinase gene. Hum. Gene Ther. 8:1997;1105-1113.
4. Arap W., Pasqualini R., Ruoslahti E. Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model. Science. 279:1998;377-380.
5. Arap W., Haedicke W., Bernasconi M., Kain R., Rajotte D., Krajewski S., Ellerby H.M., Bredesen D.E., Pasqualini R., Ruoslahti E. Targeting the prostate for destruction through a vascular address. Proc. Natl. Acad. Sci. U.S.A. 99:2002;1527-1531.
6. Audouy S.A., de Leij L.F., Hoekstra D., Molema G. In vivo characteristics of cationic liposomes as delivery vectors for gene therapy. Pharm. Res. 19:2002;1599-1605.
7. Augustin H.G., Braun K., Telemenakis I., Modlich U., Kuhn W. Ovarian angiogenesis. Phenotypic characterization of endothelial cells in a physiological model of blood vessel growth and regression. Am. J. Pathol. 147:1995;339-351.
8. Baillie C.T., Winslet M.C., Bradley N.J. Tumour vasculature: a potential therapeutic target. Br. J. Cancer. 72:1995;257-267.
9. Bangham A.D., Standish M.M., Watkins J.C. Diffusion of univalent ions across the lamellae of swollen phospholipids. J. Mol. Biol. 13:1965;238-252.
10. Bankston P.W., Milici A.J. A survey of the binding of polycationic ferritin in several fenestrated capillary beds: indication of heterogeneity in the luminal glycocalyx of fenestral diaphragms. Microvasc. Res. 26:1983;36-48.
11. Bocci G., Nicolaou K.C., Kerbel R.S. Protracted low-dose effects on human endothelial cell proliferation and survival in vitro reveal a selective antiangiogenic window for various chemotherapeutic drugs. Cancer Res. 62:2002;6938-6943.
12. Boucher Y., Leunig M., Jain R.K. Tumor angiogenesis and interstitial hypertension. Cancer Res. 56(18):1996;4264-4266.
13. Brien S.E., Zagzag D., Brem S. Rapid in situ cellular kinetics of intracerebral tumor angiogenesis using a monoclonal antibody to bromodeoxyuridine. Neurosurgery. 25:1989;715-719.
14. Briozzo P., Badet J., Capony F., Pieri I., Montcourrier P., Barritault D. MCF7 mammary cancer cells respond to bFGF and internalize it following its release from the extracellular matrix: a permissive role for cathepsin D. Exp. Cell Res. 194:1991;252-259.
15. 2+ and von Willebrand factor release in human endothelial cells. Am. J. Pathol. 138:1991;213-221.
16. Brooks P.C., Clark R.A., Cheresh D.A. Requirement of vascular integrin αvβ3 for angiogenesis. Science. 264:1994;569-571.
17. Calabretta B., Sims R.B., Valtieri M., Caracciolo D., Szczylik C., Venturelli D., Ratajczak M., Beran M., Gerwitz A.M. Normal and leukemic hematopoietic cells manifest differential sensitivity to inhibitory effects of c-myb antisense oligodeoxynucleotides: an in vivo study relevant to bone marrow purging. Proc. Natl. Acad. Sci. U.S.A. 88:1991;2351-2357.
18. Campbell R.B., Fukumura D., Brown E.B., Mazzola L.M., Izumi Y., Jain R.K., Torchilin V.P., Munn L.L. Cationic charge determines the distribution of liposomes between the vascular and extravascular compartments of tumors. Cancer Res. 62:2002;6831-6836.
19. Chang Y.S., di Tomaso E., McDonald D.M., Jones R., Jain R.K., Munn L.L. Mosaic blood vessels in tumors: frequency of cancer cells in contact with flowing blood. Proc. Natl. Acad. Sci. U.S.A. 97:2000;14608-14613.
20. Chonn A., Cullis P., Devine D. The role of surface charge in the activation of the classical and alternative pathways of complement by liposomes. J. Immunol. 146:1991;4234-4241.
21. Dass C.R. Cytotoxicity issues pertinent to lipoplex-mediated gene therapy in vivo. J. Pharm. Pharmacol. 54:2002a;593-601.
22. Dass C.R. Liposome-mediated delivery of oligodeoxynucleotides in vivo. Drug Deliv. 9:2002b;169-180.
23. Dass C.R. Biochemical and biophysical characteristics of lipoplexes pertinent to solid tumour gene therapy. Int. J. Pharm. 241:2002c;1-25.
24. Dass C.R., Burton M.A. Lipoplexes and tumours. J. Pharm. Pharmacol. 51:1999;755-770.
25. Dass C.R., Burton M.A. A model for evaluating selective delivery of plasmid DNA to tumours via the vasculature. Cancer Biother. Radiopharm. 17:2002;501-505.
26. Dass C.R., Burton M.A. Modified microplex vector enhances transfection of cells in culture while maintaining tumour-selective gene delivery in-vivo. J. Pharm. Pharmacol. 55:2003;19-25.
27. Dass C.R., Su T. Delivery of lipoplexes for genotherapy of solid tumours: role of vascular endothelial cells. J. Pharm. Pharmacol. 52:2000;1301-1317.
28. Dass C.R., Walker T.L., Burton M.A., DeCruz E.E. Cationic liposomes and gene therapy for solid tumors. Drug Deliv. 4:1997;151-166.
29. Dass C.R., Walker T.L., Burton M.A. Tumour vasculature - summary of recent findings and therapeutic implications. Cancer Forum. 22:1998;149-152.
30. Dass C.R., Walker T.L., Kalle W.H.J., Burton M.A. A microsphere-lipoplex (microplex) vector for targeted gene therapy of cancer. I. Construction and in vitro evaluation. Drug Deliv. 6:1999;259-270.
31. Dass C.R., Saravolac E.G., Li Y., Sun L.Q. Cellular uptake, distribution, and stability of 10-23 deoxyribozymes. Antisense Nucl. Acid Drug Dev. 12:2002a;289-299.
32. Dass C.R., Walker T.L., Burton M.A. Liposomes containing cationic dimethyl dioctadecyl ammonium bromide: formulation, quality control, and lipofection efficiency. Drug Deliv. 9:2002b;11-18.
33. Dass C.R., Walker T.L., Kalle W.H.J., Burton M.A. A microsphere-lipoplex (microplex) vector for targeted gene therapy of cancer. II. In vivo biodistribution study in a solid tumour model. Drug Deliv. 7:2000c;15-20.
34. Denekamp J. Vasculature as a target for tumor therapy. Prog. Appl. Microbiol. 4:1984;28-38.
35. Dewhirst M.W., LaRue S.M., Gerweck L. Tumor physiology and cell kinetics. Semin. Vet. Med. Surg. (Small Animal). 10:1995;148-157.
36. Farhood H., Serbina N., Huang L. The role of dioleoyl phosphatidylethanolamine in cationic liposome mediated gene transfer. Biochim. Biophys. Acta. 1235:1995;289-295.
37. Felgner J.H., Kumar R., Sridhar C.N., Wheeler C.J., Tsai Y.J., Border R., Ramsey P., Martin M., Felgner P.L. Enhanced gene delivery and mechanism studies with a novel series of cationic lipid formulations. J. Biol. Chem. 269:1994;2550-2561.
38. Fidler I.J. Orthotopic implantation of human colon carcinoma into nude mice provides a valuable model for the biology and therapy of metastasis. Cancer Metast. Rev. 10:1991;229-243.
39. Fidler I.J., Ellis L.M. The implications of angiogenesis for the biology and therapy of cancer metastases. Cell. 79:1994;185-188.
40. Folkman J. The role of angiogenesis in tumor growth. Semin. Cancer Biol. 3:1992;65-71.
41. Gastl G., Hermann T., Steurer M., Zmija J., Gunsilius E., Unger C., Kraft A. Angiogenesis as a target for tumor treatment. Oncology. 54:1997;177-184.
42. Hamada H., Tsuruo T. Characterization of the ATPase activity of the 170- to 180-kilodalton membrane glycoprotein associated with multidrug resistance: the 170- to 180-kilodalton membrane glycoprotein is an ATPase. J. Biol. Chem. 263:1988;1454-1458.
43. Hillen H.F.P., Hak L.E., Joosten-Achjanie S.R., Arends J.-W. Microvessel density in unknown primary tumors. Int. J. Cancer (Predict Oncol.). 74:1997;81-85.
44. Jain R.K. Transport of molecules in the tumor interstitium: a review. Cancer Res. 47:1987;3039-3051.
45. Jain R.K. 1995 Whitaker Lecture: delivery of molecules, particles, and cells to solid tumors. Ann. Biomed. Eng. 24:1996;457-473.
46. Kan Z., Ivancev K., Lunderquist A., McCuskey P.A., Wright K.C., Wallace S., McCuskey R.S. In vivo microscopy of hepatic tumors in animal models: a dynamic investigation of blood supply to hepatic metastases. Radiology. 187:1993;621-626.
47. Kerbel R.S., Klement G., Pritchard K.I., Kamen B. Continuous low-dose anti-angiogenic/metronomic chemotherapy: from the research laboratory into the oncology clinic. Ann. Oncol. 13:2002;12-15.
48. Kikuchi A., Aoki Y., Sugaya S., Serikawa T., Takakuwa K., Tanaka K., Suzuki N., Kikuchi H. Development of novel cationic liposomes for efficient gene transfer into peritoneal disseminated tumor. Hum. Gene Ther. 10:1999;947-955.
49. Kiyasu Y., Kaneshima S., Koga S. Morphogenesis of peritoneal metastasis in human gastric cancer. Cancer Res. 41:1981;1236-1239.
50. Kohn S., Nagy J.A., Dvorak H.F., Dvorak A.M. Pathways of macromolecular tracer transport across venules and small veins. Lab. Invest. 67:1992;596-607.
51. Krol A., Maresca J., Dewhirst M.W., Yuan F. Available volume fraction of macromolecules in the extravascular space of a fibrosarcoma: implications for drug delivery. Cancer Res. 59(16):1999;4136-4141.
52. Kunstfeld R., Wickenhauser G., Michaelis U., Teifel M., Umek W., Naujoks K., Wolff K., Petzelbauer P. Paclitaxel encapsulated in cationic liposomes diminishes tumor angiogenesis and melanoma growth in a "humanized" SCID mouse model. J. Invest. Dermatol. 120:2003;476-482.
53. Lasic, D.D., Pearlman, R., 1996. Liposomes and lipidic particles in gene therapy. In: Rosoff, M. (Ed.), Vesicles. Marcel Dekker, Brooklyn, New York, pp. 477-489.
54. Leu A.J., Berk D.A., Lymboussaki A., Alitalo K., Jain R.K. Absence of functional lymphatics within murine sarcoma: a molecular and functional evaluation. Cancer Res. 60:2000;4324-4327.
55. Levchenko T.S., Rammohan R., Lukyanov A.N., Whiteman K.R., Torchilin V.P. Liposome clearance in mice: the effect of a separate and combined presence of surface charge and polymer coating. Int. J. Pharm. 240:2002;95-102.
56. Liotta L.A., Kleinerman J., Saidel G.M. The significance of heterogeneous tumor cell clumps in the metastatic process. Cancer Res. 36:1976;889-894.
57. Liu Y., Mounkes L.C., Liggitt H.D., Brown C.S., Solodin I., Heath T.D., Debs R.J. Factors influencing the efficiency of cationic liposome-mediated intravenous gene delivery. Nat. Biotechnol. 15:1997;167-173.
58. Matsui H., Johnson L.G., Randell S.H., Boucher R.C. Loss of binding and entry of liposome-DNA complexes decreases transfection efficiency in differentiated airway epithelial cells. J. Biol. Chem. 272:1997;1117-1126.
59. McLean J.W., Fox E.A., Baluk P., Bolton P.B., Haskell A., Pearlman R., Thurston G., Umemoto E.Y., McDonald D.M. Organ-specific endothelial cell uptake of cationic liposome-DNA complexes in mice. Am. J. Physiol. 273:1997;H387-H404.
60. Meltzer A. Dormancy and breast cancer. J. Surg. Oncol. 43:1990;181-188.
61. Meyer O., Kirpotin D., Hong K., Sternberg B., Park J.W., Woodle M.C., Papahadjopoulos D. Cationic liposomes coated with polyethylene glycol as carriers for oligonucleotides. J. Biol. Chem. 273:1998;15621-15627.
62. Milici A.J., L'Hernault N., Palade G.E. Surface densities of diaphragmed fenestrae and transendothelial channels in different murine capillary beds. Circ. Res. 56:1985;709-717.
63. Mollica F., Jain R.K., Netti P.A. A model for temporal heterogeneities of tumor blood flow. Microvasc. Res. 65(1):2003;56-60.
64. Monsky W.L., Fukumura D., Gohongi T., Ancukiewcz M., Weich H.A., Torchilin V.P., Jain R.K. Augmentation of transvascular transport of macromolecules and nanoparticles in tumors using vascular endothelial growth factor. Cancer Res. 59:1999;4129-4135.
65. Mounkes L.C., Zhong W., Cipres-Palacin G., Heath T.D., Debs R. Proteoglycans mediate cationic liposome-DNA complex-based gene delivery in vitro and in vivo. J. Biol. Chem. 273:1998;26164-26170.
66. Murray J.C., Carmichael J. Targeting solid tumours: challenges, disappointments, and opportunities. Adv. Drug Deliv. Rev. 17:1995;117-127.
67. Niedbala M.J., Crickard K., Bernacki R.J. Interactions of human ovarian tumor cells with human mesothelial cells grown on extracellular matrix. An in vitro model system for studying tumor cell adhesion and invasion. Exp. Cell Res. 160:1985;499-513.
68. Nishi T., Yoshizato K., Yamashiro S., Takeshima H., Sato K., Hamada K., Kitamura I., Yoshimura T., Saya H., Kuratsu J., Ushio Y. High-efficiency in vivo gene transfer using intraarterial plasmid DNA injection following in vivo electroporation. Cancer Res. 56:1996;1050-1055.
69. Niven R., Pearlman R., Wedeking T., Mackeigan J., Noker P., Simpson-Herren L., Smith J.G. Biodistribution of radiolabeled lipid-DNA complexes and DNA in mice. J. Pharm. Sci. 87:1998;1292-1299.
70. Oberle V., Bakowsky U., Zuhorn I.S., Hoekstra D. Lipoplex formation under equilibrium conditions reveals a three-step mechanism. Biophys. J. 79:2000;1447-1454.
71. Olesen S.P. Rapid increase in blood-brain barrier permeability during severe hypoxia and metabolic inhibition. Brain Res. 368:1986;24-29.
72. Parker S.E., Ducharme S., Norman J., Wheeler C.J. Tissue distribution of the cytofectin component of a plasmid-DNA/cationic lipid complex following intravenous administration in mice. Hum. Gene Ther. 8:1997;393-401.
73. Plate K.H., Mennel H.D. Vascular morphology and angiogenesis in glial tumors. Exp. Toxicol. Pathol. 47:1995;89-94.
74. Plate K.H., Breier G., Risau W. Molecular mechanisms of developmental and tumor angiogenesis. Brain Pathol. 4:1994;207-218.
75. Polverini P.J. The pathophysiology of angiogenesis. Crit. Rev. Oral Biol. Med. 6:1995;230-247.
76. Polverini P.J., Leibovich S.J. Induction of neovascularization in vivo and endothelial cell proliferation in vitro by tumor-associated macrophages. Lab. Invest. 51:1984;635-642.
77. Qu H., Nagy J.A., Senger D.R., Dvorak H.F., Dvorak A.M. Ultrastructural localization of vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) to the abluminal plasma membrane and vesiculovacuolar organelles of tumor microvascular endothelium. J. Histochem. Cytochem. 43:1995;381-389.
78. Rainov N.G., Ikeda K., Qureshi N.H., Grover S., Herrlinger U., Pechan P., Chiocca E.A., Breakefield X.O., Barnett F.H. Intraarterial delivery of adenovirus vectors and liposome-DNA complexes to experimental brain neoplasms. Hum. Gene Ther. 10:1999;311-318.
79. Rak J.W., St. Croix B.D., Kerbel R.S. Consequences of angiogenesis for tumor progression, metastases and cancer therapy. Anti-Cancer Drugs. 6:1995;3-18.
80. Ramanujan S., Koenig G.C., Padera T.P., Stoll B.R., Jain R.K. Local imbalance of proangiogenic and antiangiogenic factors: a potential mechanism of focal necrosis and dormancy in tumors. Cancer Res. 60:2000;1442-1448.
81. Ramesh R., Saeki T., Templeton N.S., Ji L., Stephens L.C., Ito I., Wilson D.R., Wu Z., Branch C.D., Minna J.D., Roth J.A. Successful treatment of primary and disseminated human lung cancers by systemic delivery of tumor suppresser genes using an improved liposome vector. Mol. Ther. 3:2001;337-344.
82. Rastinejad F., Polverini P.J., Bouck N.P. Regulation of the activity of a new inhibitor of angiogenesis by a cancer suppressor gene. Cell. 56:1989;345-355.
83. Reddy J.A., Abburi C., Hofland S.J., Howard S.J., Vlahov I., Wils P., Leamon C.P. Folate-targeted, cationic liposome-mediated gene transfer into disseminated peritoneal tumors. Gene Ther. 9:2002;1542-1550.
84. Sakurai F., Terada T., Yasuda K., Yamashita F., Takakura Y., Hashida M. The role of tissue macrophages in the induction of proinflammatory cytokine production following intravenous injection of lipoplexes. Gene Ther. 9:2002;1120-1126.
85. Senger D.R., Galli S.J., Dvorak A.M., Perruzzi C.A., Harvey V.S., Dvorak H.F. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science. 219:1983;983-985.
86. Shi F., Wasungu L., Nomden A., Stuart M.C., Polushkin E., Engberts J.B., Hoekstra D. Interference of poly(ethylene glycol)-lipid analogues with cationic-lipid-mediated delivery of oligonucleotides role of lipid exchangeability and non-lamellar transitions. Biochem. J. 366:2002;333-341.
87. Stetler-Stevenson W.G., Aznavoorian S., Liotta L.A. Tumor cell interactions with the extracellular matrix during invasion and metastases. Ann. Rev. Cell Biol. 9:1993;541-573.
88. Stohrer M., Boucher Y., Stangassinger M., Jain R.K. Oncotic pressure in solid tumors is elevated. Cancer Res. 60:2000;4251-4255.
89. Szoka F., Papahadjopoulos D. Comparative properties and methods of preparation of lipid vesicles (liposomes). Ann. Rev. Biophys. Bioeng. 9:1980;467-508.
90. Taipale J., Keski-Oja J. Growth factors in the extracellular matrix. FASEB J. 11:1997;51-59.
91. Templeton N.S., Lasic D.D., Frederik P.M., Strey H.H., Roberts D.D., Pavlakis G.N. Improved DNA-liposome complexes for increased systemic delivery and gene expression. Nat. Biotechnol. 15:1997;647-652.
92. Thorpe P.E., Burrows F.J. Antibody-directed targeting of the vasculature of solid tumors. Breast Cancer Res. Treat. 36:1995;237-251.
93. Thurston G., McLean J.W., Rizen M., Baluk P., Haskell A., Murphy T.J., Hanahan D., McDonald D.M. Cationic liposomes target angiogenic endothelial cells in tumors and chronic inflammation in mice. J. Clin. Invest. 101:1998;1401-1413.
94. Tomisaki S., Ohno S., Ichiyoshi Y., Kuwano H., Maehara Y., Sugimachi K. Microvessel quantification and its possible relation with liver metastasis in colorectal cancer. Cancer. 77:1996;1722-1728.
95. Tsuruo T., Tomida A. Multidrug resistance. Anti-Cancer Drugs. 6:1995;213-218.
96. Uyechi L.S., Gagne L., Thurston G., Szoka F.C. Jr. Mechanism of lipoplex gene delivery in mouse lung: binding and internalization of fluorescent lipid and DNA components. Gene Ther. 8:2001;828-836.
97. van den Hooff A. The role of stromal cells in tumor metastasis: a new link. Cancer Cells. 3:1991;186-187.
98. Vincent S., DePace D., Finkelstein S. Distribution of anionic sites on the capillary endothelium in an experimental brain tumour model. Microcirc. Endothelium Lymphatics. 4:1988;45-67.
99. Weindel K., Moringlane J.R., Marme D., Weich H.A. Detection and quantification of vascular endothelial growth factor/vascular permeability factor in brain tumor tissue and cyst fluid: the key to angiogenesis? Neurosurgery. 35:1994;439-449.
100. Wheeler C.J., Felgner P.L., Tsai Y.J., Marshall J., Sukhu L., Doh S.G., Hartikka J., Nietupski J., Manthorpe M., Nichols M., Plewe M., Liang X., Norman J., Smith A., Cheng S.H. A novel cationic lipid greatly enhances plasmid DNA delivery and expression in mouse lung. Proc. Natl. Acad. Sci. U.S.A. 93:1996;11454-11459.
101. Willmott N., Goldberg J., Anderson J., Bessent R., McKillop J., McArdle C. Abnormal vasculature of solid tumours: significance for microsphere-based targeting strategies. Int. J. Rad. Biol. 60:1991;195-199.
102. Wong F.M.P., Reimer D.L., Bally M.B. Cationic lipid binding to DNA: characterization of complex formation. Biochemistry. 35:1996;5756-5763.
103. Yuan F., Dellian M., Fukumura D., Leunig M., Berk D.A., Torchilin V.P., Jain R.K. Vascular permeability in a human tumor xenograft: molecular size-dependence and cut-off size. Cancer Res. 55:1995;3752-3756.
104. Zhao Q., Song X., Waldschmidt T., Fisher E., Krieg A.M. Oligonucleotide uptake in human hematopoietic cells is increased in leukemia and is related to cellular activation. Blood. 88:1996;1788-1795.
105. Zhu N., Liggitt D., Liu Y., Debs R. Systemic gene expression after intravenous DNA delivery into adult mice. Science. 261:1993;209-211.