Multiscale kinetic modeling of liposomal doxorubicin delivery quantifies the role of tumor and drug-specific parameters in local delivery to tumors

CPT: Pharmacometrics and Systems Pharmacology

Volumn 1, Issue 1, 2012, Pages

  Hendriks, B S ^a   Reynolds, J G ^a   Klinz, S G ^a   Geretti, E ^a   Lee, H ^a   Leonard, S C ^a   Gaddy, D F ^a   Espelin, C W ^a   Nielsen, U B ^a   Wickham, T J ^a  

^a MERRIMACK PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN;

AREA UNDER THE CURVE; ARTICLE; CANCER CELL CULTURE; DOSE RESPONSE; DRUG SPECIFICITY; HUMAN; LIPOSOMAL DELIVERY; NONHUMAN; PRIORITY JOURNAL; TRANSPORT KINETICS;

EID: 84875419452     PISSN: None     EISSN: 21638306     Source Type: Journal    
DOI: 10.1038/psp.2012.16     Document Type: Article

References (100)

1. Lefrak, E.A., Pitha, J., Rosenheim, S. & Gottlieb, J.A. A clinicopathologic analysis of adriamycin cardiotoxicity. Cancer 32, 302-314 (1973
2. Von Hoff, D.D. et al. Risk factors for doxorubicin-induced congestive heart failure. Ann. Intern. Med. 91, 710-717 (1979
3. O'Brien, M.E. et al. Reduced cardiotoxicity and comparable efficacy in a phase III trial of pegylated liposomal doxorubicin HCl (Caelyx/Doxil) versus conventional doxorubicin for first-line treatment of metastatic breast cancer. Ann. Oncol. 15, 440-449 (2004
4. Colbern, G.T., Hiller, A.J., Musterer, R.S., Pegg, E., Henderson, I.C. & Working, P.K. Significant increase in antitumor potency of doxorubicin Hc1 by its encapsulation in pegylated liposomes. J. Liposome Res. 9, 523 (1999
5. Hong, R.L. et al. Direct comparison of liposomal doxorubicin with or without polyethylene glycol coating in C-26 tumor-bearing mice: Is surface coating with polyethylene glycol beneficial? Clin. Cancer Res. 5, 3645-3652 (1999
6. Northfelt, D.W. et al. Pegylated-liposomal doxorubicin versus doxorubicin, bleomycin, and vincristine in the treatment of AIDS-related Kaposi's sarcoma: Results of a randomized phase III clinical trial. J. Clin. Oncol. 16, 2445-2451 (1998
7. Doxil package insert. wwwdoxilcom
8. Harrington, K.J. et al. Effective targeting of solid tumors in patients with locally advanced cancers by radiolabeled pegylated liposomes. Clin. Cancer Res. 7, 243-254 (2001
9. Koukourakis, M.I. et al. Liposomal doxorubicin and conventionally fractionated radiotherapy in the treatment of locally advanced non-small-cell lung cancer and head and neck cancer. J. Clin. Oncol. 17, 3512-3521 (1999
10. Karathanasis, E. et al. Imaging nanoprobe for prediction of outcome of nanoparticle chemotherapy by using mammography. Radiology 250, 398-406 (2009
11. Minchinton, A.I. & Tannock, I.F. Drug penetration in solid tumours. Nat. Rev. Cancer 6, 583-592 (2006
12. Jain, R.K. & Stylianopoulos, T. Delivering nanomedicine to solid tumors. Nat. Rev. Clin. Oncol. 7, 653-664 (2010
13. Jain, R.K., Tong, R.T. & Munn, L.L. 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
14. Zunino, F., Gambetta, R., Di Marco, A. & Zaccara, A. Interaction of daunomycin and its derivatives with DNA. Biochim. Biophys. Acta 277, 489-498 (1972
15. Jain, R.K. Transport of molecules in the tumor interstitium: A review. Cancer Res. 47, 3039-3051 (1987
16. Baxter, L.T., Zhu, H., Mackensen, D.G., Butler, W.F. & Jain, R.K. Biodistribution of monoclonal antibodies: Scale-up from mouse to human using a physiologically based pharmacokinetic model. Cancer Res. 55, 4611-4622 (1995
17. Mac Gabhann, F. & Popel, A.S. Targeting neuropilin-1 to inhibit VEGF signaling in cancer: Comparison of therapeutic approaches. PLoS Comput. Biol. 2, e180 (2006
18. Harashima, H., Iida, S., Urakami, Y., Tsuchihashi, M. & Kiwada, H. Optimization of antitumor effect of liposomally encapsulated doxorubicin based on simulations by pharmacokinetic/ pharmacodynamic modeling. J. Control. Release 61, 93-106 (1999
19. El-Kareh, A.W. & Secomb, T.W. A mathematical model for comparison of bolus injection, continuous infusion, and liposomal delivery of doxorubicin to tumor cells. Neoplasia 2, 325-338 (2000
20. Eytan, G.D. & Kuchel, P.W. Mechanism of action of P-glycoprotein in relation to passive membrane permeation. Int. Rev. Cytol. 190, 175-250 (1999
21. Northfelt, D.W. et al. Doxorubicin encapsulated in liposomes containing surface-bound polyethylene glycol: Pharmacokinetics, tumor localization, and safety in patients with AIDSrelated Kaposi's sarcoma. J. Clin. Pharmacol. 36, 55-63 (1996
22. Baek, H.M., Yu, H.J., Chen, J.H., Nalcioglu, O. & Su, M.Y. Quantitative correlation between (1)H MRS and dynamic contrast-enhanced MRI of human breast cancer. Magn. Reson. Imaging 26, 523-531 (2008
23. Ah-See, M.L. et al. Early changes in functional dynamic magnetic resonance imaging predict for pathologic response to neoadjuvant chemotherapy in primary breast cancer. Clin. Cancer Res. 14, 6580-6589 (2008
24. Yankeelov, T.E. et al. Integration of quantitative DCE-MRI and ADC mapping to monitor treatment response in human breast cancer: Initial results. Magn. Reson. Imaging 25, 1-13 (2007
25. Chauhan, V.P. et al. Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner. Nat. Nanotechnol. 7, 383-388 (2012
26. Petersen, A.L. et al. 64Cu loaded liposomes as positron emission tomography imaging agents. Biomaterials 32, 2334-2341 (2011
27. Kubo, A. et al. Indium-111-labelled liposomes: Dosimetry and tumour detection in patients with cancer. Eur. J. Nucl. Med. 20, 107-113 (1993
28. Koukourakis, M.I. et al. High intratumoural accumulation of stealth liposomal doxorubicin (Caelyx) in glioblastomas and in metastatic brain tumours. Br. J. Cancer 83, 1281-1286 (2000
29. Kirpotin, D.B. et al. Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localization but does increase internalization in animal models. Cancer Res. 66, 6732-6740 (2006
30. Reynolds, J.G. et al. HER2-targeted liposomal doxorubicin (MM-302) displays enhanced anti-tumorigenic effects without associated cardiotoxicity. Toxicol Appl Pharmacol, 262, 1-10 (2012
31. Charrois, G.J. & Allen, T.M. Drug release rate influences the pharmacokinetics, biodistribution, therapeutic activity, and toxicity of pegylated liposomal doxorubicin formulations in murine breast cancer. Biochim. Biophys. Acta 1663, 167-177 (2004
32. Koning, G.A., Morselt, H.W., Kamps, J.A. & Scherphof, G.L. Uptake and intracellular processing of PEG-liposomes and PEG-immunoliposomes by kupffer cells in vitro 1 .*. J. Liposome Res. 11, 195-209 (2001
33. Lee, K.D., Nir, S. & Papahadjopoulos, D. Quantitative analysis of liposome-cell interactions in vitro: Rate constants of binding and endocytosis with suspension and adherent J774 cells and human monocytes. Biochemistry 32, 889-899 (1993
34. Lauffenburger, D.A. & Linderman, J.J. Receptors (Oxford University Press, New York, 1993
35. Schneider, Y.J., Baurain, R., Zenebergh, A. & Trouet, A. DNA-binding parameters of daunorubicin and doxorubicin in the conditions used for studying the interaction of anthracycline- DNA complexes with cells in vitro. Cancer Chemother. Pharmacol. 2, 7-10 (1979
36. Frezard, F. & Garnier-Suillerot, A. Comparison of the binding of anthracycline derivatives to purified DNA and to cell nuclei. Biochim. Biophys. Acta 1036, 121-127 (1990
37. Tarasiuk, J., Frézard, F., Garnier-Suillerot, A. & Gattegno, L. Anthracycline incorporation in human lymphocytes. Kinetics of uptake and nuclear concentration. Biochim. Biophys. Acta 1013, 109-117 (1989
38. Rizzo, V., Sacchi, N. & Valentini, L. Fluorescence stopped-flow kinetic analysis of anthracyclines- DNA interaction. Biochem. Pharmacol. 37, 1819-1820 (1988
39. Zunino, F., Di Marco, A., Zaccara, A. & Gambetta, R.A. The interaction of daunorubicin and doxorubicin with DNA and chromatin. Biochim. Biophys. Acta 607, 206-214 (1980
40. Gigli, M., Doglia, S.M., Millot, J.M., Valentini, L. & Manfait, M. Quantitative study of doxorubicin in living cell nuclei by microspectrofluorometry. Biochim. Biophys. Acta 950, 13-20 (1988
41. Spoelstra, E.C., Westerhoff, H.V., Dekker, H. & Lankelma, J. Kinetics of daunorubicin transport by P-glycoprotein of intact cancer cells. Eur. J. Biochem. 207, 567-579 (1992
42. Rizzo, V., Sacchi, N. & Menozzi, M. Kinetic studies of anthracycline-DNA interaction by fluorescence stopped flow confirm a complex association mechanism. Biochemistry 28, 274-282 (1989
43. Gandecha, B.M., Brown, J.R. & Crampton, M.R. Dissociation kinetics of DNA-anthracycline and DNA-anthraquinone complexes determined by stopped-flow spectrophotometry. Biochem. Pharmacol. 34, 733-736 (1985
44. Yang, M., Chan, H.L., Lam, W. & Fong, W.F. Cytotoxicity and DNA binding characteristics of dextran-conjugated doxorubicins. Biochim. Biophys. Acta 1380, 329-335 (1998
45. Peterson, C. & Trouet, A. Transport and storage of daunorubicin and doxorubicin in cultured fibroblasts. Cancer Res. 38, 4645-4649 (1978
46. Laboratory, T.J. Animal resources body weight study of 1993. JAX® NOTES, http:// jaxmice.jax.org/jaxnotes/archive/457a.html (1994
47. Laboratory, T.J. MGI-Mouse Facts. http://www.informatics.jax.org/mgihome/ other/ mouse-facts1.shtml
48. Baxter, L.T., Zhu, H., Mackensen, D.G. & Jain, R.K. Physiologically based pharmacokinetic model for specific and nonspecific monoclonal antibodies and fragments in normal tissues and human tumor xenografts in nude mice. Cancer Res. 54, 1517-1528 (1994
49. Charrois, G.J. & Allen, T.M. Rate of biodistribution of STEALTH liposomes to tumor and skin: Influence of liposome diameter and implications for toxicity and therapeutic activity. Biochim. Biophys. Acta 1609, 102-108 (2003
50. Stefanini, M.O., Wu, F.T., Mac Gabhann, F. & Popel, A.S. A compartment model of VEGF distribution in blood, healthy and diseased tissues. BMC Syst. Biol. 2, 77 (2008
51. Lefrak, E.A., Pitha, J., Rosenheim, S. & Gottlieb, J.A. A clinicopathologic analysis of adriamycin cardiotoxicity. Cancer 32, 302-314 (1973
52. Von Hoff, D.D. et al. Risk factors for doxorubicin-induced congestive heart failure. Ann. Intern. Med. 91, 710-717 (1979
53. O'Brien, M.E. et al. Reduced cardiotoxicity and comparable efficacy in a phase III trial of pegylated liposomal doxorubicin HCl (Caelyx/Doxil) versus conventional doxorubicin for first-line treatment of metastatic breast cancer. Ann. Oncol. 15, 440-449 (2004
54. Colbern, G.T., Hiller, A.J., Musterer, R.S., Pegg, E., Henderson, I.C. & Working, P.K. Significant increase in antitumor potency of doxorubicin Hc1 by its encapsulation in pegylated liposomes. J. Liposome Res. 9, 523 (1999
55. Hong, R.L. et al. Direct comparison of liposomal doxorubicin with or without polyethylene glycol coating in C-26 tumor-bearing mice: Is surface coating with polyethylene glycol beneficial? Clin. Cancer Res. 5, 3645-3652 (1999
56. Northfelt, D.W. et al. Pegylated-liposomal doxorubicin versus doxorubicin, bleomycin, and vincristine in the treatment of AIDS-related Kaposi's sarcoma: Results of a randomized phase III clinical trial. J. Clin. Oncol. 16, 2445-2451 (1998
57. Doxil package insert. wwwdoxilcom
58. Harrington, K.J. et al. Effective targeting of solid tumors in patients with locally advanced cancers by radiolabeled pegylated liposomes. Clin. Cancer Res. 7, 243-254 (2001
59. Koukourakis, M.I. et al. Liposomal doxorubicin and conventionally fractionated radiotherapy in the treatment of locally advanced non-small-cell lung cancer and head and neck cancer. J. Clin. Oncol. 17, 3512-3521 (1999
60. Karathanasis, E. et al. Imaging nanoprobe for prediction of outcome of nanoparticle chemotherapy by using mammography. Radiology 250, 398-406 (2009
61. Minchinton, A.I. & Tannock, I.F. Drug penetration in solid tumours. Nat. Rev. Cancer 6, 583-592 (2006
62. Jain, R.K. & Stylianopoulos, T. Delivering nanomedicine to solid tumors. Nat. Rev. Clin. Oncol. 7, 653-664 (2010
63. Jain, R.K., Tong, R.T. & Munn, L.L. 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
64. Zunino, F., Gambetta, R., Di Marco, A. & Zaccara, A. Interaction of daunomycin and its derivatives with DNA. Biochim. Biophys. Acta 277, 489-498 (1972
65. Jain, R.K. Transport of molecules in the tumor interstitium: A review. Cancer Res. 47, 3039-3051 (1987
66. Baxter, L.T., Zhu, H., Mackensen, D.G., Butler, W.F. & Jain, R.K. Biodistribution of monoclonal antibodies: Scale-up from mouse to human using a physiologically based pharmacokinetic model. Cancer Res. 55, 4611-4622 (1995
67. Mac Gabhann, F. & Popel, A.S. Targeting neuropilin-1 to inhibit VEGF signaling in cancer: Comparison of therapeutic approaches. PLoS Comput. Biol. 2, e180 (2006
68. Harashima, H., Iida, S., Urakami, Y., Tsuchihashi, M. & Kiwada, H. Optimization of antitumor effect of liposomally encapsulated doxorubicin based on simulations by pharmacokinetic/ pharmacodynamic modeling. J. Control. Release 61, 93-106 (1999
69. El-Kareh, A.W. & Secomb, T.W. A mathematical model for comparison of bolus injection, continuous infusion, and liposomal delivery of doxorubicin to tumor cells. Neoplasia 2, 325-338 (2000
70. Eytan, G.D. & Kuchel, P.W. Mechanism of action of P-glycoprotein in relation to passive membrane permeation. Int. Rev. Cytol. 190, 175-250 (1999
71. Northfelt, D.W. et al. Doxorubicin encapsulated in liposomes containing surface-bound polyethylene glycol: Pharmacokinetics, tumor localization, and safety in patients with AIDSrelated Kaposi's sarcoma. J. Clin. Pharmacol. 36, 55-63 (1996
72. Baek, H.M., Yu, H.J., Chen, J.H., Nalcioglu, O. & Su, M.Y. Quantitative correlation between (1)H MRS and dynamic contrast-enhanced MRI of human breast cancer. Magn. Reson. Imaging 26, 523-531 (2008
73. Ah-See, M.L. et al. Early changes in functional dynamic magnetic resonance imaging predict for pathologic response to neoadjuvant chemotherapy in primary breast cancer. Clin. Cancer Res. 14, 6580-6589 (2008
74. Yankeelov, T.E. et al. Integration of quantitative DCE-MRI and ADC mapping to monitor treatment response in human breast cancer: Initial results. Magn. Reson. Imaging 25, 1-13 (2007
75. Chauhan, V.P. et al. Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner. Nat. Nanotechnol. 7, 383-388 (2012
76. Petersen, A.L. et al. 64Cu loaded liposomes as positron emission tomography imaging agents. Biomaterials 32, 2334-2341 (2011
77. Kubo, A. et al. Indium-111-labelled liposomes: Dosimetry and tumour detection in patients with cancer. Eur. J. Nucl. Med. 20, 107-113 (1993
78. Koukourakis, M.I. et al. High intratumoural accumulation of stealth liposomal doxorubicin (Caelyx) in glioblastomas and in metastatic brain tumours. Br. J. Cancer 83, 1281-1286 (2000
79. Kirpotin, D.B. et al. Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localization but does increase internalization in animal models. Cancer Res. 66, 6732-6740 (2006
80. Reynolds, J.G. et al. HER2-targeted liposomal doxorubicin (MM-302) displays enhanced anti-tumorigenic effects without associated cardiotoxicity. Toxicol Appl Pharmacol, 262, 1-10 (2012
81. Charrois, G.J. & Allen, T.M. Drug release rate influences the pharmacokinetics, biodistribution, therapeutic activity, and toxicity of pegylated liposomal doxorubicin formulations in murine breast cancer. Biochim. Biophys. Acta 1663, 167-177 (2004
82. Koning, G.A., Morselt, H.W., Kamps, J.A. & Scherphof, G.L. Uptake and intracellular processing of PEG-liposomes and PEG-immunoliposomes by kupffer cells in vitro 1 .*. J. Liposome Res. 11, 195-209 (2001
83. Lee, K.D., Nir, S. & Papahadjopoulos, D. Quantitative analysis of liposome-cell interactions in vitro: Rate constants of binding and endocytosis with suspension and adherent J774 cells and human monocytes. Biochemistry 32, 889-899 (1993
84. Lauffenburger, D.A. & Linderman, J.J. Receptors (Oxford University Press, New York, 1993
85. Schneider, Y.J., Baurain, R., Zenebergh, A. & Trouet, A. DNA-binding parameters of daunorubicin and doxorubicin in the conditions used for studying the interaction of anthracycline- DNA complexes with cells in vitro. Cancer Chemother. Pharmacol. 2, 7-10 (1979
86. Frezard, F. & Garnier-Suillerot, A. Comparison of the binding of anthracycline derivatives to purified DNA and to cell nuclei. Biochim. Biophys. Acta 1036, 121-127 (1990
87. Tarasiuk, J., Frézard, F., Garnier-Suillerot, A. & Gattegno, L. Anthracycline incorporation in human lymphocytes. Kinetics of uptake and nuclear concentration. Biochim. Biophys. Acta 1013, 109-117 (1989
88. Rizzo, V., Sacchi, N. & Valentini, L. Fluorescence stopped-flow kinetic analysis of anthracyclines- DNA interaction. Biochem. Pharmacol. 37, 1819-1820 (1988
89. Zunino, F., Di Marco, A., Zaccara, A. & Gambetta, R.A. The interaction of daunorubicin and doxorubicin with DNA and chromatin. Biochim. Biophys. Acta 607, 206-214 (1980
90. Gigli, M., Doglia, S.M., Millot, J.M., Valentini, L. & Manfait, M. Quantitative study of doxorubicin in living cell nuclei by microspectrofluorometry. Biochim. Biophys. Acta 950, 13-20 (1988
91. Spoelstra, E.C., Westerhoff, H.V., Dekker, H. & Lankelma, J. Kinetics of daunorubicin transport by P-glycoprotein of intact cancer cells. Eur. J. Biochem. 207, 567-579 (1992
92. Rizzo, V., Sacchi, N. & Menozzi, M. Kinetic studies of anthracycline-DNA interaction by fluorescence stopped flow confirm a complex association mechanism. Biochemistry 28, 274-282 (1989
93. Gandecha, B.M., Brown, J.R. & Crampton, M.R. Dissociation kinetics of DNA-anthracycline and DNA-anthraquinone complexes determined by stopped-flow spectrophotometry. Biochem. Pharmacol. 34, 733-736 (1985
94. Yang, M., Chan, H.L., Lam, W. & Fong, W.F. Cytotoxicity and DNA binding characteristics of dextran-conjugated doxorubicins. Biochim. Biophys. Acta 1380, 329-335 (1998
95. Peterson, C. & Trouet, A. Transport and storage of daunorubicin and doxorubicin in cultured fibroblasts. Cancer Res. 38, 4645-4649 (1978
96. Laboratory, T.J. Animal resources body weight study of 1993. JAX® NOTES, http:// jaxmice.jax.org/jaxnotes/archive/457a.html (1994
97. Laboratory, T.J. MGI-Mouse Facts. http://www.informatics.jax.org/mgihome/ other/ mouse-facts1.shtml
98. Baxter, L.T., Zhu, H., Mackensen, D.G. & Jain, R.K. Physiologically based pharmacokinetic model for specific and nonspecific monoclonal antibodies and fragments in normal tissues and human tumor xenografts in nude mice. Cancer Res. 54, 1517-1528 (1994
99. Charrois, G.J. & Allen, T.M. Rate of biodistribution of STEALTH liposomes to tumor and skin: Influence of liposome diameter and implications for toxicity and therapeutic activity. Biochim. Biophys. Acta 1609, 102-108 (2003
100. Stefanini, M.O., Wu, F.T., Mac Gabhann, F. & Popel, A.S. A compartment model of VEGF distribution in blood, healthy and diseased tissues. BMC Syst. Biol. 2, 77 (2008