Targeted doxorubicin delivery to brain tumors via minicells: Proof of principle using dogs with spontaneously occurring tumors as a model

PLoS ONE

Volumn 11, Issue 4, 2016, Pages

  MacDiarmid, Jennifer A ^a   Langova, Veronika ^b   Bailey, Dale ^c   Pattison, Scott T ^a   Pattison, Stacey L ^a   Christensen, Neil ^b   Armstrong, Luke R ^a   Brahmbhatt, Vatsala N ^a   Smolarczyk, Katarzyna ^a   Harrison, Matthew T ^a   Costa, Marylia ^a   Mugridge, Nancy B ^a   Sedliarou, Ilya ^a   Grimes, Nicholas A ^a   Kiss, Debra L ^a   Stillman, Bruce ^d   Hann, Christine L ^e   Gallia, Gary L ^e,f   Graham, Robert M ^g,h   Brahmbhatt, Himanshu ^a  

^a EnGeneIC Pty Ltd   (Australia)

^b Small Animal Specialist Hospital   (Australia)

^c ROYAL NORTH SHORE HOSPITAL   (Australia)

^d Simons Center for Quantitative Biology   (United States)

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^h UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; DRUG CARRIER; EPIDERMAL GROWTH FACTOR RECEPTOR; MINICELL; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIBIOTIC; EGFR PROTEIN, HUMAN; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; BLOOD SAMPLING; BRAIN TUMOR; CANCER CELL; CELL POPULATION; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG POTENCY; DRUG RESPONSE; DRUG SAFETY; DRUG TARGETING; FEMALE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IN VITRO STUDY; LIVER FUNCTION; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OVERALL SURVIVAL; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SURVIVAL TIME; TUMOR REGRESSION; TUMOR VOLUME; ANIMAL; BRAIN NEOPLASMS; CANCER STAGING; CELL PROLIFERATION; DISEASE MODEL; DOG; DRUG EFFECTS; GLIOBLASTOMA; MOLECULARLY TARGETED THERAPY; MORTALITY; PATHOLOGY; SURVIVAL RATE; TISSUE DISTRIBUTION; TUMOR CELL CULTURE;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; ANTIBODIES, MONOCLONAL; BRAIN NEOPLASMS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DOGS; DOXORUBICIN; DRUG DELIVERY SYSTEMS; FEMALE; GLIOBLASTOMA; HUMANS; MALE; MOLECULAR TARGETED THERAPY; NEOPLASM STAGING; RECEPTOR, EPIDERMAL GROWTH FACTOR; SURVIVAL RATE; TISSUE DISTRIBUTION; TUMOR CELLS, CULTURED;

EID: 84962859648     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0151832     Document Type: Article

References (54)

1. Stewart LA. Chemotherapy in adult high-grade glioma: a systematic review and meta-analysis of individual patient data from 12 randomised trials. Lancet. 2002;359(9311):1011-8. Epub 2002/04/09. PMID: 11937180.
2. Stupp R, Mason WP, Van Den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. The New England journal of medicine. 2005;352(10):987-96. Epub 2005/03/11. doi: 10.1056/NEJMoa043330 PMID: 15758009.
3. Ong BY, Ranganath SH, Lee LY, Lu F, Lee HS, Sahinidis NV, et al. Paclitaxel delivery from PLGA foams for controlled release in post-surgical chemotherapy against glioblastoma multiforme. Biomaterials. 2009;30(18):3189-96. Epub 2009/03/17. doi: 10.1016/j.biomaterials.2009.02.030 PMID: 19285718.
4. Yang Y, Yan Z, Wei D, Zhong J, Liu L, Zhang L, et al. Tumor-penetrating peptide functionalization enhances the anti-glioblastoma effect of doxorubicin liposomes. Nanotechnology. 2013;24(40):405101. Epub 2013/09/14. doi: 10.1088/0957-4484/24/40/405101 PMID: 24029287.
5. Liu Y, Lu W. Recent advances in brain tumor-targeted nano-drug delivery systems. Expert opinion on drug delivery. 2012;9(6):671-86. Epub 2012/05/23. doi: 10.1517/17425247.2012.682726 PMID: 22607535.
6. Hobbs SK, Monsky WL, Yuan F, Roberts WG, Griffith L, Torchilin VP, et al. Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proceedings of the National Academy of Sciences of the United States of America. 1998;95(8):4607-12. Epub 1998/05/16. PMID: 9539785; PubMed Central PMCID: PMCPmc22537.
7. Fokas E, Steinbach JP, Rodel C. Biology of brain metastases and novel targeted therapies: time to translate the research. Biochimica et biophysica acta. 2013;1835(1):61-75. Epub 2012/11/13. doi: 10. 1016/j.bbcan. 2012.10.005 PMID: 23142311.
8. Pardridge WM. Blood-brain barrier delivery. Drug discovery today. 2007;12(1-2):54-61. Epub 2007/01/03. doi: 10.1016/j.drudis.2006.10.013 PMID: 17198973.
9. Agarwal S, Sane R, Oberoi R, Ohlfest JR, Elmquist WF. Delivery of molecularly targeted therapy to malignant glioma, a disease of the whole brain. Expert reviews in molecular medicine. 2011;13:e17. Epub 2011/06/17. doi: 10.1017/s1462399411001888 PMID: 21676290.
10. Pardridge WM. Biopharmaceutical drug targeting to the brain. Journal of drug targeting. 2010;18(3):157-67. Epub 2010/01/13. doi: 10.3109/10611860903548354 PMID: 20064077.
11. Juillerat-Jeanneret L. The targeted delivery of cancer drugs across the blood-brain barrier: chemical modifications of drugs or drug-nanoparticles? Drug discovery today. 2008;13(23-24):1099-106. Epub 2008/10/14. doi: 10.1016/j.drudis.2008.09.005 PMID: 18848640.
12. Kreuter J. Nanoparticulate systems for brain delivery of drugs. Advanced drug delivery reviews. 2001;47(1):65-81. Epub 2001/03/17. PMID: 11251246.
13. Deeken JF, Loscher W. The blood-brain barrier and cancer: transporters, treatment, and Trojan horses. Clinical cancer research: an official journal of the American Association for Cancer Research. 2007;13(6):1663-74. Epub 2007/03/17. doi: 10.1158/1078-0432.ccr-06-2854 PMID: 17363519.
14. Sarin H, Kanevsky AS, Wu H, Brimacombe KR, Fung SH, Sousa AA, et al. Effective transvascular delivery of nanoparticles across the blood-brain tumor barrier into malignant glioma cells. Journal of translational medicine. 2008;6:80. Epub 2008/12/20. doi: 10.1186/1479-5876-6-80 PMID: 19094226; PubMed Central PMCID: PMCPmc2639552.
15. Laquintana V, Trapani A, Denora N, Wang F, Gallo JM, Trapani G. New strategies to deliver anticancer drugs to brain tumors. Expert opinion on drug delivery. 2009;6(10):1017-32. Epub 2009/09/08. doi: 10. 1517/17425240903167942 PMID: 19732031; PubMed Central PMCID: PMCPmc2752842.
16. Chen L, Zhang Y, Yang J, Hagan JP, Li M. Vertebrate animal models of glioma: understanding the mechanisms and developing new therapies. Biochimica et biophysica acta. 2013;1836(1):158-65. Epub 2013/04/27. doi: 10.1016/j.bbcan. 2013.04.003 PMID: 23618720; PubMed Central PMCID: PMCPmc3729034.
17. Ding H, Nagy A, Gutmann D, Guha A. Astrocytoma models. Neurosurgical Focus. 2000;8:1-7.
18. Gordon I, Paoloni M, Mazcko C, Khanna C. The Comparative Oncology Trials Consortium: using spontaneously occurring cancers in dogs to inform the cancer drug development pathway. PLoS medicine. 2009;6(10):e1000161. Epub 2009/10/14. doi: 10.1371/journal.pmed.1000161 PMID: 19823573; PubMed Central PMCID: PMCPmc2753665.
19. Paoloni M, Khanna C. Translation of new cancer treatments from pet dogs to humans. Nature reviews Cancer. 2008;8(2):147-56. Epub 2008/01/19. doi: 10.1038/nrc2273 PMID: 18202698.
20. Candolfi M, Curtin JF, Nichols WS, Muhammad AG, King GD, Pluhar GE, et al. Intracranial glioblastoma models in preclinical neuro-oncology: neuropathological characterization and tumor progression. Journal of neuro-oncology. 2007;85(2):133-48. Epub 2007/09/18. doi: 10.1007/s11060-007-9400-9 PMID: 17874037; PubMed Central PMCID: PMCPmc2384236.
21. Lipsitz D, Higgins RJ, Kortz GD, Dickinson PJ, Bollen AW, Naydan DK, et al. Glioblastoma multiforme: clinical findings, magnetic resonance imaging, and pathology in five dogs. Veterinary pathology. 2003;40(6):659-69. Epub 2003/11/11. doi: 10.1354/vp. 40-6-659 PMID: 14608019.
22. Kimmelman J, Nalbantoglu J. Faithful companions: a proposal for neurooncology trials in pet dogs. Cancer research. 2007;67(10):4541-4. Epub 2007/05/19. doi: 10.1158/0008-5472.can-06-3792 PMID: 17510377.
23. Foster ES, Carrillo JM, Patnaik AK. Clinical signs of tumors affecting the rostral cerebrum in 43 dogs. Journal of veterinary internal medicine/American College of Veterinary Internal Medicine. 1988;2(2):71-4. Epub 1988/04/01. PMID: 3221360.
24. Heidner GL, Kornegay JN, Page RL, Dodge RK, Thrall DE. Analysis of survival in a retrospective study of 86 dogs with brain tumors. Journal of veterinary internal medicine/American College of Veterinary Internal Medicine. 1991;5(4):219-26. Epub 1991/07/01. PMID: 1941756.
25. Pluhar GE, Grogan PT, Seiler C, Goulart M, Santacruz KS, Carlson C, et al. Anti-tumor immune response correlates with neurological symptoms in a dog with spontaneous astrocytoma treated by gene and vaccine therapy. Vaccine. 2010;28(19):3371-8. Epub 2010/03/04. doi: 10.1016/j.vaccine. 2010.02.082 PMID: 20197146; PubMed Central PMCID: PMCPmc2854671.
26. MacDiarmid JA, Mugridge NB, Weiss JC, Phillips L, Burn AL, Paulin RP, et al. Bacterially derived 400 nm particles for encapsulation and cancer cell targeting of chemotherapeutics. Cancer cell. 2007;11(5):431-45. Epub 2007/05/08. doi: 10.1016/j.ccr.2007.03.012 PMID: 17482133.
27. Kemper EM, Boogerd W, Thuis I, Beijnen JH, Van Tellingen O. Modulation of the blood-brain barrier in oncology: therapeutic opportunities for the treatment of brain tumours? Cancer treatment reviews. 2004;30(5):415-23. Epub 2004/07/13. doi: 10.1016/j.ctrv. 2004.04.001 PMID: 15245774.
28. Abe T, Hasegawa S, Taniguchi K, Yokomizo A, Kuwano T, Ono M, et al. Possible involvement of multidrugresistance-associated protein (MRP) gene expression in spontaneous drug resistance to vincristine, etoposide and adriamycin in human glioma cells. International journal of cancer Journal international du cancer. 1994;58(6):860-4. Epub 1994/09/15. PMID: 7927879.
29. Muldoon LL, Neuwelt EA. BR96-DOX immunoconjugate targeting of chemotherapy in brain tumor models. Journal of neuro-oncology. 2003;65(1):49-62. Epub 2003/12/03. PMID: 14649885.
30. MacDiarmid JA, Amaro-Mugridge NB, Madrid-Weiss J, Sedliarou I, Wetzel S, Kochar K, et al. Sequential treatment of drug-resistant tumors with targeted minicells containing siRNA or a cytotoxic drug. Nature biotechnology. 2009;27(7):643-51. Epub 2009/06/30. doi: 10.1038/nbt.1547 PMID: 19561595.
31. Smith JS, Tachibana I, Passe SM, Huntley BK, Borell TJ, Iturria N, et al. PTEN mutation, EGFR amplification, and outcome in patients with anaplastic astrocytoma and glioblastoma multiforme. Journal of the National Cancer Institute. 2001;93(16):1246-56. Epub 2001/08/16. PMID: 11504770.
32. Higgins RJ, Dickinson PJ, Le Couteur RA, Bollen AW, Wang H, Wang H, et al. Spontaneous canine gliomas: overexpression of EGFR, PDGFRalpha and IGFBP2 demonstrated by tissue microarray immunophenotyping. Journal of neuro-oncology. 2010;98(1):49-55. Epub 2009/12/08. doi: 10.1007/s11060-009-0072-5 PMID: 19967449.
33. Lo HW. EGFR-targeted therapy in malignant glioma: novel aspects and mechanisms of drug resistance. Current molecular pharmacology. 2010;3(1):37-52. Epub 2009/12/25. PMID: 20030624; PubMed Central PMCID: PMCPmc3606625.
34. Taylor TE, Furnari FB, Cavenee WK. Targeting EGFR for treatment of glioblastoma: molecular basis to overcome resistance. Current cancer drug targets. 2012;12(3):197-209. Epub 2012/01/25. PMID: 22268382; PubMed Central PMCID: PMCPmc3464093.
35. Tacar O, Sriamornsak P, Dass CR. Doxorubicin: an update on anticancer molecular action, toxicity and novel drug delivery systems. The Journal of pharmacy and pharmacology. 2013;65(2):157-70. Epub 2013/01/03. doi: 10.1111/j.2042-7158.2012.01567.x PMID: 23278683.
36. Syakalima M, Takiguchi M, Yasuda J, Morita Y, Hashimoto A. Comparison of attenuation and liver-kidney contrast of liver ultrasonographs with histology and biochemistry in dogs with experimentally induced steroid hepatopathy. The Veterinary quarterly. 1998;20(1):18-22. Epub 1998/02/27. doi: 10. 1080/01652176.1998.9694829 PMID: 9477530.
37. Gieger TL, Hosgood G, Taboada J, Wolfsheimer KJ, Mueller PB. Thyroid function and serum hepatic enzyme activity in dogs after phenobarbital administration. Journal of veterinary internal medicine/American College of Veterinary Internal Medicine. 2000;14(3):277-81. Epub 2000/06/01. PMID: 10830541.
38. Sabat R, Grutz G, Warszawska K, Kirsch S, Witte E, Wolk K, et al. Biology of interleukin-10. Cytokine & growth factor reviews. 2010;21(5):331-44. Epub 2010/12/01. doi: 10.1016/j.cytogfr.2010.09.002 PMID: 21115385.
39. Seki S, Habu Y, Kawamura T, Takeda K, Dobashi H, Ohkawa T, et al. The liver as a crucial organ in the first line of host defense: the roles of Kupffer cells, natural killer (NK) cells and NK1.1 Ag+ T cells in T helper 1 immune responses. Immunological reviews. 2000;174:35-46. Epub 2000/05/12. PMID: 10807505.
40. Seki S, Nakashima H, Nakashima M, Kinoshita M. Antitumor immunity produced by the liver Kupffer cells, NK cells, NKT cells, and CD8 CD122 T cells. Clinical & developmental immunology. 2011;2011:868345. Epub 2011/12/23. doi: 10.1155/2011/868345 PMID: 22190974; PubMed Central PMCID: PMCPmc3235445.
41. Groothuis DR. The blood-brain and blood-tumor barriers: a review of strategies for increasing drug delivery. Neuro-oncology. 2000;2(1):45-59. Epub 2001/04/17. PMID: 11302254; PubMed Central PMCID: PMCPmc1920694.
42. Maeda H, Wu J, Sawa T, Matsumura Y, Hori K. Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. Journal of controlled release: official journal of the Controlled Release Society. 2000;65(1-2):271-84. Epub 2000/03/04. PMID: 10699287.
43. Gabizon AA, Shmeeda H, Zalipsky S. Pros and cons of the liposome platform in cancer drug targeting. Journal of liposome research. 2006;16(3):175-83. Epub 2006/09/06. doi: 10.1080/08982100600848769 PMID: 16952872.
44. Roberts NJ, Zhang L, Janku F, Collins A, Bai RY, Staedtke V, et al. Intratumoral injection of Clostridium novyi-NT spores induces antitumor responses. Science translational medicine. 2014;6(249):249ra111. Epub 2014/08/15. doi: 10.1126/scitranslmed.3008982 PMID: 25122639; PubMed Central PMCID: PMCPmc4399712.
45. Gaillard PJ, Appeldoorn CC, Dorland R, Van Kregten J, Manca F, Vugts DJ, et al. Pharmacokinetics, brain delivery, and efficacy in brain tumor-bearing mice of glutathione pegylated liposomal doxorubicin (2B3-101). PloS one. 2014;9(1):e82331. Epub 2014/01/15. doi: 10.1371/journal.pone.0082331 PMID: 24416140; PubMed Central PMCID: PMCPmc3885379.
46. Dietrich J, Rao K, Pastorino S, Kesari S. Corticosteroids in brain cancer patients: benefits and pitfalls. Expert review of clinical pharmacology. 2011;4(2):233-42. Epub 2011/06/15. doi: 10.1586/ecp. 11.1 PMID: 21666852; PubMed Central PMCID: PMCPmc3109638.
47. Heiss JD, Papavassiliou E, Merrill MJ, Nieman L, Knightly JJ, Walbridge S, et al. Mechanism of dexamethasone suppression of brain tumor-associated vascular permeability in rats. Involvement of the glucocorticoid receptor and vascular permeability factor. The Journal of clinical investigation. 1996;98(6):1400-8. Epub 1996/09/15. doi: 10.1172/jci118927 PMID: 8823305; PubMed Central PMCID: PMCPmc507566.
48. Ratain MJ, Eckhardt SG. Phase II studies of modern drugs directed against new targets: if you are fazed, too, then resist RECIST. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2004;22(22):4442-5. Epub 2004/10/16. doi: 10.1200/jco.2004.07.960 PMID: 15483011.
49. Wolchok JD, Hoos A, O'Day S, Weber JS, Hamid O, Lebbe C, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clinical cancer research: an official journal of the American Association for Cancer Research. 2009;15(23):7412-20. Epub 2009/11/26. doi: 10.1158/1078-0432.ccr-09-1624 PMID: 19934295.
50. Rainov NG, Koch S, Sena-Esteves M, Berens ME. Characterization of a canine glioma cell line as related to established experimental brain tumor models. Journal of neuropathology and experimental neurology. 2000;59(7):607-13. Epub 2000/07/20. PMID: 10901232.
51. Berens ME, Giese A, Shapiro JR, Coons SW. Allogeneic astrocytoma in immune competent dogs. Neoplasia (New York, NY). 1999;1(2):107-12. Epub 2000/08/10. PMID: 10933043; PubMed Central PMCID: PMCPmc1508127.
52. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). European journal of cancer (Oxford, England: 1990). 2009;45(2):228-47. Epub 2008/12/23. doi: 10.1016/j.ejca.2008.10.026 PMID: 19097774.
53. Veterinary Co-operative Oncology Group-Common Terminology Criteria for Adverse Events (VCOGCTCAE) following chemotherapy or biological antineoplastic therapy in dogs and cats v1.0. Veterinary and comparative oncology. 2004;2(4):195-213. Epub 2004/12/01. doi: 10.1111/j.1476-5810.2004. 0053b.x PMID: 19379294.
54. Koestner A, Higgins R. Tumors of the nervous system: Tumors in domestic animals. In: Meuten D, editor. 4 ed. Ames, IA: Iowa State Press; 2002. p. 697-738.