Thermal targeting of an acid-sensitive doxorubicin conjugate of elastin-like polypeptide enhances the therapeutic efficacy compared with the parent compound in vivo

Molecular Cancer Therapeutics

Volumn 11, Issue 7, 2012, Pages 1547-1556

  Moktan, Shama ^a   Perkins, Eddie ^b   Kratz, Felix ^c   Raucher, Drazen ^a  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^b UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^c TUMOR BIOLOGY CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

6 MALEIMIDOCAPROYL HYDRAZONE DERIVATIVE; BIOPOLYMER; CELL PENETRATING PEPTIDE; DOXORUBICIN; DOXORUBICIN DERIVATIVE; ELASTIN LIKE POLYPEPTIDE; POLYPEPTIDE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER INHIBITION; CARBOXY TERMINAL SEQUENCE; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE MODEL; DRUG BLOOD LEVEL; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG HALF LIFE; DRUG POTENCY; DRUG RELEASE; DRUG TARGETING; DRUG UPTAKE; ENDOSOME; FEMALE; HEART; HYPERTHERMIC THERAPY; IN VIVO STUDY; LYSOSOME; MAXIMUM TOLERATED DOSE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE, TUMOR; CELL-PENETRATING PEPTIDES; COMBINED MODALITY THERAPY; DISEASE MODELS, ANIMAL; DOXORUBICIN; ELASTIN; FEMALE; HUMANS; HYPERTHERMIA, INDUCED; MAXIMUM TOLERATED DOSE; MICE; MICE, INBRED C57BL; NEOPLASMS;

EID: 84863803540     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-11-0998     Document Type: Article

References (41)

1. Raucher D, Massodi I, Bidwell GL. Thermally targeted delivery of chemotherapeutics and anti-cancer peptides by elastin-like polypeptide. Expert Opin Drug Deliv 2008;5:353-69. (Pubitemid 351454384)
2. Bidwell GL 3rd, Davis AN, Fokt I, Priebe W, Raucher D. A thermally targeted elastin-like polypeptide-doxorubicin conjugate overcomes drug resistance. Invest New Drugs 2007;25:313-26. (Pubitemid 46944856)
3. Bidwell GL 3rd, Fokt I, Priebe W, Raucher D. Development of elastin-like polypeptide for thermally targeted delivery of doxorubicin. Biochem Pharmacol 2007;73:620-31. (Pubitemid 46161374)
4. Dreher MR, Raucher D, Balu N, Michael Colvin O, Ludeman SM, Chilkoti A. Evaluation of an elastin-like polypeptide-doxorubicin conjugate for cancer therapy. J Control Release 2003;91:31-43. (Pubitemid 37303992)
5. Chilkoti A, Dreher MR, Meyer DE, Raucher D. Targeted drug delivery by thermally responsive polymers. Adv Drug Deliv Rev 2002;54:613-30. (Pubitemid 35247519)
6. Bidwell GL 3rd, Perkins E, Raucher D. A thermally targeted c-Myc inhibitory polypeptide inhibits breast tumor growth. Cancer Lett 2012;319:136-43.
7. Yamaoka T, Tamura T, Seto Y, Tada T, Kunugi S, Tirrell DA. Mechanism for the phase transition of a genetically engineered elastin model peptide (VPGIG)40 in aqueous solution. Biomacromolecules 2003;4:1680-5. (Pubitemid 37455580)
8. Meyer DE, Chilkoti A. Quantification of the effects of chain length and concentration on the thermal behavior of elastin-like polypeptides. Biomacromolecules 2004;5:846-51. (Pubitemid 38702255)
9. Liu W, Dreher MR, Furgeson DY, Peixoto KV, Yuan H, Zalutsky MR, et al. Tumor accumulation, degradation and pharmacokinetics of elastin-like polypeptides in nude mice. J Control Release 2006;116:170-8. (Pubitemid 44854277)
10. Maeda H, Seymour LW, Miyamoto Y. Conjugates of anticancer agents and polymers: advantages of macromolecular therapeutics in vivo. Bioconjug Chem 1992;3:351-62.
11. Bidwell GL 3rd, Raucher D. Application of thermally responsive polypeptides directed against c-Myc transcriptional function for cancer therapy. Mol Cancer Ther 2005;4:1076-85. (Pubitemid 41079101)
12. MacKay JA, Chen M, McDaniel JR, Liu W, Simnick AJ, Chilkoti A. Self-assembling chimeric polypeptide-doxorubicin conjugate nanoparticles that abolish tumours after a single injection. Nat Mater 2009;8:993-9.
13. Rousselle C, Clair P, Lefauconnier JM, Kaczorek M, Scherrmann JM, Temsamani J. New advances in the transport of doxorubicin through the blood-brain barrier by a peptide vector-mediated strategy. Mol Pharmacol 2000;57:679-86. (Pubitemid 30183706)
14. Bidwell GL 3rd, Raucher D. Cell penetrating elastin-like polypeptides for therapeutic peptide delivery. Adv Drug Deliv Rev 2010;62:1486-96.
15. Bidwell GL 3rd, WhittomAA, Thomas E, Lyons D, Hebert MD, Raucher D. A thermally targeted peptide inhibitor of symmetrical dimethylation inhibits cancer-cell proliferation. Peptides 2010;31:834-41.
16. Graeser R, Esser N, Unger H, Fichtner I, Zhu A, Unger C, et al. INNO- 206, the (6-maleimidocaproyl hydrazone derivative of doxorubicin), shows superior antitumor efficacy compared to doxorubicin in different tumor xenograft models and in an orthotopic pancreas carcinoma model. Invest New Drugs 2010;28:14-9.
17. Kratz F, Warnecke A, Scheuermann K, Stockmar C, Schwab J, Lazar P, et al. Probing the cysteine-34 position of endogenous serum albumin with thiol-binding doxorubicin derivatives. Improved efficacy of an acid-sensitive doxorubicin derivative with specific albumin-binding properties compared to that of the parent compound. J Med Chem 2002;45:5523-33. (Pubitemid 35424970)
18. Kratz F, Ehling G, Kauffmann HM, Unger C. Acute and repeat-dose toxicity studies of the (6-maleimidocaproyl)hydrazone derivative of doxorubicin (DOXO-EMCH), an albumin-binding prodrug of the anticancer agent doxorubicin. Hum Exp Toxicol 2007;26:19-35.
19. Lebrecht D, Geist A, Ketelsen UP, Haberstroh J, Setzer B, Kratz F, et al. The 6-maleimidocaproyl hydrazone derivative of doxorubicin (DOXOEMCH) is superior to free doxorubicin with respect to cardiotoxicity and mitochondrial damage. Int J Cancer 2007;120:927-34. (Pubitemid 46175416)
20. Kratz F.DOXO-EMCH(INNO-206): the first albumin-binding prodrug of doxorubicin to enter clinical trials. Expert Opin Investig Drugs 2007;16:855-66. (Pubitemid 46882358)
21. Moktan S, Ryppa C, Kratz F, Raucher D. A thermally responsive biopolymer conjugated to an acid-sensitive derivative of paclitaxel stabilizes microtubules, arrests cell cycle, and induces apoptosis. Invest New Drugs 2012;30:236-48.
22. Di Stefano G, Lanza M, Kratz F, Merina L, Fiume L. A novel method for coupling doxorubicin to lactosaminated human albumin by an acid sensitive hydrazone bond: synthesis, characterization and preliminary biological properties of the conjugate. Eur J Pharm Sci 2004;23:393-7. (Pubitemid 39573391)
23. Dunham LJ, Stewart HL. A survey of transplantable and transmissible animal tumors. J Natl Cancer Inst 1953;13:1299-377.
24. Ewens A, Mihich E, Ehrke MJ. Distant metastasis from subcutaneously grown E0771 medullary breast adenocarcinoma. Anticancer Res 2005;25:3905-15. (Pubitemid 41665163)
25. Dreher MR, Liu W, Michelich CR, Dewhirst MW, Chilkoti A. Thermal cycling enhances the accumulation of a temperature-sensitive biopolymer in solid tumors. Cancer Res 2007;67:4418-24. (Pubitemid 46815091)
26. Beyer U, Rothern-Rutishauser B, Unger C, Wunderli-Allenspach H, Kratz F. Differences in the intracellular distribution of acid-sensitive doxorubicin-protein conjugates in comparison to free and liposomal formulated doxorubicin as shown by confocal microscopy. Pharm Res 2001;18:29-38. (Pubitemid 32299619)
27. Rousselle C, Smirnova M, Clair P, Lefauconnier JM, Chavanieu A, Calas B, et al. Enhanced delivery of doxorubicin into the brain via a peptide-vector-mediated strategy: saturation kinetics and specificity. J Pharmacol Exp Ther 2001;296:124-31. (Pubitemid 32015070)
28. Xiong XB, Huang Y, Lu WL, Zhang H, Zhang X, Zhang Q. Enhanced intracellular uptake of sterically stabilized liposomal Doxorubicin in vitro resulting in improved antitumor activity in vivo. Pharm Res 2005;22:933-9. (Pubitemid 40898103)
29. Yarmolenko PS, Zhao Y, Landon C, Spasojevic I, Yuan F, Needham D, et al. Comparative effects of thermosensitive doxorubicin-containing liposomes and hyperthermia in human and murine tumours. Int J Hyperthermia 2010;26:485-98.
30. Hahn GM, Braun J, Har-Kedar I. Thermochemotherapy: synergism between hyperthermia (42-43 degrees) and adriamycin (of bleomycin) in mammalian cell inactivation. Proc Natl Acad Sci U S A 1975;72:937-40.
31. Herman TS. Temperature dependence of adriamycin, cis- diamminedichloroplatinum, bleomycin, and 1,3-bis(2-chloroethyl)-1-nitrosourea cytotoxicity in vitro. Cancer Res 1983;43:517-20. (Pubitemid 13193840)
32. Issels RD. Regional hyperthermia combined with systemic chemotherapy of locally advanced sarcomas: preclinical aspects and clinical results. Recent Results Cancer Res 1995;138:81-90.
33. Feyerabend T, Steeves R, Wiedemann GJ, Richter E, Robins HI. Rationale and clinical status of local hyperthermia, radiation, and chemotherapy in locally advanced malignancies. Anticancer Res 1997;17:2895-7. (Pubitemid 27434814)
34. van Vulpen M, Raaymakers BW, de Leeuw AA, van de Kamer JB, van Moorselaar RJ, Hobbelink MG, et al. Prostate perfusion in patients with locally advanced prostate carcinoma treated with different hyperthermia techniques. J Urol 2002;168:1597-602. (Pubitemid 35034196)
35. Raucher D, Chilkoti A. Enhanced uptake of a thermally responsive polypeptide by tumor cells in response to its hyperthermia-mediated phase transition. Cancer Res 2001;61:7163-70. (Pubitemid 32946510)
36. Massodi I, Raucher D. A thermally responsive Tat-elastin-like polypeptide fusion protein induces membrane leakage, apoptosis, and cell death in human breast cancer cells. J Drug Target 2007;15:611-22. (Pubitemid 350031085)
37. Vail DM, Amantea MA, Colbern GT, Martin FJ, Hilger RA, Working PK. Pegylated liposomal doxorubicin: proof of principle using preclinical animal models and pharmacokinetic studies. Semin Oncol 2004;31:16-35. (Pubitemid 40023240)
38. Gabizon A, Shmeeda H, Barenholz Y. Pharmacokinetics of pegylated liposomal Doxorubicin: review of animal and human studies. Clin Pharmacokinet 2003;42:419-36. (Pubitemid 36649037)
39. Falk MH, Issels RD. Hyperthermia in oncology. Int J Hyperthermia 2001;17:1-18. (Pubitemid 32058478)
40. Dewhirst MW, Prosnitz L, Thrall D, Prescott D, Clegg S, Charles C, et al. Hyperthermic treatment of malignant diseases: current status and a view toward the future. Semin Oncol 1997;24:616-25. (Pubitemid 28035878)
41. Takahashi I, Emi Y, Hasuda S, Kakeji Y, Maehara Y, Sugimachi K. Clinical application of hyperthermia combined with anticancer drugs for the treatment of solid tumors. Surgery 2002;131:S78-84. (Pubitemid 34118620)