Chemotherapy of glioblastoma in rats using doxorubicin-loaded nanoparticles

International Journal of Cancer

Volumn 109, Issue 5, 2004, Pages 759-767

  Steiniger, Sebastian C J ^a   Kreuter, Jörg ^a   Khalansky, Alexander S ^b   Skidan, Igor N ^c   Bobruskin, Alexey I ^c   Smirnova, Zoya S ^d   Severin, Sergey E ^c   Uhl, Reiner ^e   Kock, Martin ^f   Geiger, Kathrin D ^a,g   Gelperina, Svetlana E ^c  

^a GOETHE UNIVERSITY   (Germany)

^b RESEARCH INSTITUTE OF HUMAN MORPHOLOGY   (Russian Federation)

^c Moscow Research Institute of Medical Ecology   (Russian Federation)

^d N N BLOKHIN RUSSIAN CANCER RESEARCH CENTER   (Russian Federation)

^e Novartis Vaccines and Diagnostics   (Germany)

^f GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

^g UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Chemotherapy; Doxorubicin; Glioblastoma; Histology; Nanoparticles

Indexed keywords

DOXORUBICIN; EZRIN; GLIAL FIBRILLARY ACIDIC PROTEIN; NANOPARTICLE; POLYSORBATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD BRAIN BARRIER; CANCER CHEMOTHERAPY; CANCER SURVIVAL; CELL PROLIFERATION; CONTROLLED STUDY; DRUG COATING; DRUG EFFECT; DRUG FORMULATION; GLIOBLASTOMA; IMMUNOHISTOCHEMISTRY; IMPLANTATION; IN VIVO STUDY; INFLAMMATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SURVIVAL TIME; TREATMENT OUTCOME; TUMOR VOLUME;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BRAIN NEOPLASMS; DOXORUBICIN; GLIOBLASTOMA; IMMUNOHISTOCHEMISTRY; MALE; NANOTECHNOLOGY; RATS; RATS, WISTAR;

EID: 12144288634     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.20048     Document Type: Article

References (56)

1. DeAngelis LM. Brain tumors. N Engl J Med 2001;344:114-23.
2. Nelson DF, Nelson JS, Davis DR, Chang CH, Griffin TW, Pajak TF. Survival and prognosis of patients with astrocytoma with atypical or anaplastic features. J Neurooncol 1985;3:99-103.
3. Kornblith PL, Walker M, Chemotherapy for malignant gliomas. J Neurosurg 1988;68:1-17.
4. Huncharek M, Muscat J, Geschwind JF. Multi-drug versus single agent chemotherapy for high grade astrocytoma: results of a meta-analysis. Anticancer Res 1998;18:4693-7.
5. Brandes AA, Pasetto LM, Monfardini S. New drugs in recurrent high grade gliomas. Anticancer Res 2000;20:1913-20.
6. Donelli MG, Zucchetti M, D'Incalci M. Do anticancer agents reach the tumor target in the human brain? Cancer Chemother Pharmacol 1992;30:251-60.
7. Robinson PJ. Osmotic opening of the blood-brain barrier and brain tumor chemotherapy. Methods Neurosci 1994;21:35-50.
8. Doolittle ND, Abrey LE, Ferrari N, Hall WA, Laws ER, McLendon RE, Muldoon LL, Peereboom D, Peterson DR, Reynolds CP, Senter P, Neuwelt EA. Targeted delivery in primary and metastatic brain tumors: summary report of the seventh annual meeting of the blood-brain barrier disruption consortium. Clin Cancer Res 2002;8:1702-9.
9. Khalifa A, Dodds D, Rampling R, Paterson J, Murray T. Liposomal distribution in malignant glioma: possibilities for therapy. Nucl Med Commun 1997;18:17-23.
10. Boiardi A, Pozzi A, Salmaggi A, Eoli M, Zucchetti M, Silvani A. Safety and potential effectiveness of daunorubicin-containing liposomes in patients with advanced recurrent malignant CNS tumors. Cancer Chemother Pharmacol 1999;43:178-9.
11. Lippens RJ. Liposomal daunorubicin (DaunoXome) in children with recurrent or progressive brain tumors. Pediatr Hematol Oncol 1999; 16:131-9.
12. Fundaro A, Cavalli R, Bargoni A, Vighetto D, Zara GP, Gasco MR. Non-stealth and stealth solid lipid nanoparticles (SLN) carrying doxorubicin: pharmacokinetics and tissue distribution after i.v. administration to rats. Pharmacol Res 2000;42:337-43.
13. Koukourakis MI, Koukouraki S, Giatromanolaki A, Kakolyris S, Georgoulias V, Velidaki A, Archimandritis S, Karkavitsas NN. High intratumoral accumulation of stealth liposomal doxorubicin in sarcomas: rationale for combination with radiotherapy. Acta Oncol 2000; 39:207-11.
14. Koukourakis MI, Koukouraki S, Fezoulidis I, Kelekis N, Kyrias G, Archimandritis S, Karkavitsas N. High intratumoural accumulation of stealth liposomal doxorubicin (Caelyx) in glioblastomas and in metastatic brain tumours. Br J Cancer 2000;83:1281-6.
15. Stan AC, Casares S, Radu D, Walter GF, Brumeanu TD. Doxorubicin-induced cell death in highly invasive human gliomas. Anticancer Res 1999;19:941-50.
16. Walter KA, Tamargo RJ, Olivi A, Burger PC, Brem H. Intratumoral chemotherapy. Neurosurgery 1995;37:1128-45.
17. von Holst H, Knochenhauer E, Blomgren H, Collins VP, Ehn L, Lindquist M, Noren G, Peterson C. Uptake of adriamycin in tumour and surrounding brain tissue in patients with malignant gliomas. Acta Neurochir 1990;104:13-6.
18. Schackert G, Fan D, Nayar R, Fidler IJ. Arrest and retention of multilamellar liposomes in the brain of normal mice or mice bearing experimental brain metastases. Sel Cancer Ther 1989;5:73-9.
19. Shibata S, Ochi A, Mori K. Liposomes as carriers of cisplatin into the central nervous system: experiments with 9L gliomas in rats. Neurol Med Chir 1990;30:242-5.
20. Fabel K, Dietrich J, Hau P, Wismeth C, Winner B, Przywara S, Steinbrecher A, Ullrich W, Bogdahn U. Long-term stabilization in patients with malignant glioma after treatment with liposomal doxorubicin. Cancer 2001;92:1936-42.
21. Gulyaev AE, Gelperina SE, Skidan IN, Antropov AS, Kivman GY, Kreuter J. Significant transport of doxorubicin into the brain with polysorbate 80-coated nanoparticles. Pharm Res 1999;16:1564-9.
22. Alyautdin RN, Petrov VE, Langer K, Berthold A, Kharkevich DA, Kreuter J. Delivery of loperamide across the blood-brain barrier with polysorbate 80-coated polybutylcyanoacrylate nanoparticles. Pharm Res 1997;14:325-8.
23. Alyautdin RN, Tezikov EB, Ramge P, Kharkevich DA, Begley DJ, Kreuter J. Significant entry of tubocurarine into the brain of rats by adsorption to polysorbate 80-coated polybutylcyanoacrylate nanoparticles: an in situ brain perfusion study. J Microencapsul 1998;15:67-74.
24. Kreuter J, Alyautdin RN, Kharkevich DA, Ivanov AA. Passage of peptides through the blood-brain barrier with colloidal polymer particles (nanoparticles). Brain Res 1995;674:171-4.
25. Friese A, Seiller E, Quack G, Lorenz B, Kreuter J. Increase of the duration of the anticonvulsive activity of a novel NMDA receptor antagonist using poly (butylcyanoacrylate) nanoparticles as a parenteral controlled release system. Eur J Pharm Biopharm 2000;49: 103-9.
26. Matsumura Y, Maeda H. A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res 1986; 46:6387-92.
27. Maeda H, Matsumura Y. Tumoritropic and lymphotropic principles of macromolecular drugs. Crit Rev Ther Drug Carrier Syst 1989;6:193-210.
28. Seymour LW, Miyamoto Y, Maeda H, Brereton M, Strohalm J, Ulbrich K, Duncan R. Influence of molecular weight on passive tumour accumulation of a soluble macromolecular drug carrier. Eur J Cancer 1995;31A:766-70.
29. Duncan R, Dimitrijevic S, Evagorou EG. The role of polymer conjugates in the diagnosis and treatment of cancer. Pharma Sci 1996;6: 237-63.
30. Iablonovskaia L, Spryshkova NA. Morphologic and biologic characteristics of experimental tumors of the cerebellum in rats. Arkh Patol 1970;33:50-3.
31. Kalbfleisch J, Prentice RL. The statistical analysis of failure time data. New York: John Wiley and Sons, 1980.
32. Holm S. A simple sequentially rejective multiple test procedure. Scand J Statist 1979;6:65-70.
33. SAS Institute. SAS/STAT users's guide, version 6, 4th ed. Cary, NC: SAS Institute, 1989.
34. Geiger KD, Stoldt P, Schlote W, Derouiche A. Ezrin immunoreactivity is associated with increasing malignancy of astrocytic tumors but is absent in oligodendrogliomas. Am J Pathol 2000;157:1785-93.
35. Gelperina SE, Khalansky AS, Skidan IN, Smirnova ZS, Bobruskin AI, Severin SE, Turowski B, Zanella FE, Kreuter J. Toxicological studies of doxorubicin bound to polysorbate 80-coated poly(butyl cyanoacrylate) nanoparticles in healthy rats and rats with intracranial glioblastoma. Toxicol Lett 2002;126:131-41.
36. Fazekas I, Kerekes E, Hegedus B, Nyary I. Identification of gliomas by morphological and immunocytochemical analysis in cell cultures. Ideggyogy Sz 2002;55:173-9.
37. Derouiche A, Frotscher M. Peripheral astrocyte processes: monitoring by selective immunostaining for the actin-binding ERM proteins. Glia 2001;36:330-41.
38. Zimmer C, Weissleder R, Poss K, Bogdanova A, Wright SC Jr, Enochs WS. MR imaging of phagocytosis in experimental gliomas. Radiology 1995;197:533-8.
39. Llesuy SF, Arnaiz SL. Hepatotoxicity of mitoxantrone and doxorubicin. Toxicology 1990;63:187-98.
40. Badr MZ. Controversial role of intracellular iron in the mechanisms of chemically-induced hepatotoxicity. J Biochem Toxicol 1994;9:25-9.
41. Perez EA. Doxorubicin and paclitaxel in the treatment of advanced breast cancer: efficacy and cardiac considerations. Cancer Invest 2001;19:155-64.
42. Rangan GK, Wang Y, Harris DC. Induction of proteinuric chronic glomerular disease in the rat (Rattus norvegicus) by intracardiac injection of doxorubicin hydrochloride. Contemp Top Lab Anim Sci 2001;40:44-9.
43. Kreuter J, Shamenkov D, Petrov V, Ramge P, Cychutek K, Koch-Brandt C, Alyautdin R. Apolipoprotein-mediated transport of nanoparticle-bound drugs across the blood-brain barrier. J Drug Targeting 2002;10:317-25.
44. Olivier JC, Fenart L, Chauvet R, Pariat C, Cecchelli R, Couet W. Indirect evidence that drug brain targeting using polysorbate 80-coated polybutylcyanoacrylate nanoparticles is related to toxicity. Pharm Res 1999;16:1836-42.
45. Alyaudtin RN, Reichel A, Löbenberg R, Ramge P, Kreuter J, Begley DJ. Interaction of poly(butylcyanoacrylate) nanoparticles with the blood-brain barrier in vivo and in vitro. J Drug Target 2001;9:209-21.
46. Kreuter J, Ramge P, Petrov V, Hamm S, Gelperina SE, Engelhardt B, Alyautdin R, von Briesen H, Begley DJ. Direct evidence that polysorbate-80-coated poly(butylcyanoacrylate) nanoparticles deliver drugs to the CNS via specific mechanisms requiring prior binding of drug to the nanoparticles. Pharm Res 2003;20:409-16.
47. Roullin VG, Deverre JR, Lemaire L, Hindre F, Venier-Julienne MC, Vienet R, Benoit JP. Anti-cancer drug diffusion within living rat brain tissue: an experimental study using [(3)H](6)-5-fluorouracil-loaded PLGA microspheres. Eur J Pharm Biopharm 2002;53:293-9.
48. Friesen C, Fulda S, Debatin KM. Cytotoxic drugs and the CD95 pathway. Leukemia 1999;13:1854-8.
49. Perego P, Corna E, De Cesare M, Gatti L, Polizzi D, Pratesi G, Supino R, Zunino F. Role of apoptosis and apoptosis-related genes in cellular response and antitumor efficacy of anthracyclines. Curr Med Chem 2001;8:31-7.
50. Mahaley MS Jr. Immunological considerations and the malignant glioma problem. Clin Neurosurg 1968;15:175-89.
51. Giometto B, Bozza F, Faresin F, Alessio L, Mingrino S, Tavolato B. Immune infiltrates and cytokines in gliomas. Acta Neurochir 1996; 138:50-6.
52. Tran CT, Wolz P, Egensperger R, Kosel S, Imai Y, Bise K, Kohsaka S, Mehraein P, Graeber MB. Differential expression of MHC class II molecules by microglia and neoplastic astroglia: relevance for the escape of astrocytoma cells from immune surveillance. Neuropathol Appl Neurobiol 1998;24:293-301.
53. Aldskogius H, Liu L, Svensson M. Glial responses to synaptic damage and plasticity. J Neurosci Res 1999;58:33-41.
54. Badie B, Schartner J. Role of microglia in glioma biology. Microsc Res Tech 2001;54:106-13.
55. Neuwelt EA, Pagel M, Barnett P, Glassberg M, Frenkel EP. Pharmacology and toxicity of intracarotid adriamycin administration following osmotic blood-brain barrier modification. Cancer Res 1981;41: 4466-70.
56. Kaaijk P, Troost D, de Boer OJ, Van Amstel P, Bakker PJ, Leenstra S, Bosch DA. Daunorubicin and doxorubicin but not BCNU have deleterious effects on organotypic multicellular spheroids of gliomas. Br J Cancer 1996;74:187-93.