Toxicity and efficacy evaluation of multiple targeted polymalic acid conjugates for triple-negative breast cancer treatment

Journal of Drug Targeting

Volumn 21, Issue 10, 2013, Pages 956-967

  Ljubimova, Julia Y ^a,b,c,d   Portilla Arias, Jose ^a   Patil, Rameshwar ^a   Ding, Hui ^a   Inoue, Satoshi ^a   Markman, Janet L ^a   Rekechenetskiy, Arthur ^a   Konda, Bindu ^a   Gangalum, Pallavi R ^a   Chesnokova, Alexandra ^a   Ljubimov, Alexander V ^b,c,d   Black, Keith L ^a,c,d   Holler, Eggehard ^a,c,d  

^a Samuel Oschin Comprehensive Cancer Institute   (United States)

^b Department of Biomedical Sciences ^*  (United States)

^c CEDARS SINAI MEDICAL CENTER   (United States)

^d Arrogene Inc   (United States)

Author keywords

Hematologic; Immunogenicity; in vivo treatment; Nanoconjugate drugs; Polymalic acid; Toxicity; Triple negative breast cancer

Indexed keywords

DOXORUBICIN; MALIC ACID; NANOCONJUGATE; POLY BETA MALIC ACID; POLYCEFIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSAY; CANCER PATIENT; CANCER THERAPY; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; FEMALE; HUMAN; HUMAN CELL; IMMUNOASSAY; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; TRIPLE NEGATIVE BREAST CANCER;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; DRUG EVALUATION, PRECLINICAL; FEMALE; HUMANS; LAMININ; MALATES; MICE; MICE, NUDE; NANOCONJUGATES; NANOPARTICLES; POLYESTERS; POLYMERS; RABBITS; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84887214090     PISSN: 1061186X     EISSN: 10292330     Source Type: Journal    
DOI: 10.3109/1061186X.2013.837470     Document Type: Article

References (53)

1. Hudson D, Margaritis A. Biopolymer nanoparticle production for controlled release of biopharmaceuticals. Crit Rev Biotechnol 2013. [Epub ahead of print]. doi: 10.3109/07388551.2012.743503.
2. Gu FX, Karnik R, Wang AZ, et al. Targeted nanoparticles for cancer therapy. Nano Today 2007;2:14-21.
3. Chandna P, Khandare JJ, Ber E, et al. Multifunctional tumortargeted polymer-peptide-drug delivery system for treatment of primary and metastatic cancers. Pharm Res 2010;27:2296-306.
4. Sandoval MA, Sloat BR, Lansakara PD, et al. EGFR-targeted stearoyl gemcitabine nanoparticles show enhanced anti-tumor activity. J Control Release 2012;157:287-96.
5. Ljubimova JY, Fujita M, Ljubimov AV, et al. Poly(malic acid) nanoconjugates containing various antibodies and oligonucleotides for multitargeting drug delivery. Nanomedicine 2008;3:247-65.
6. Ruiz F, Alvarez G, Ramos M, et al. Cyclosporin A targets involved in protection against glutamate excitotoxicity. Eur J Pharmacol 2000;404:29-39.
7. Kumar DM, Perez E, Cai ZY, et al. Role of nonfeminizingestrogen analogues in neuroprotection of rat retinal ganglion cells against glutamate-induced cytotoxicity. Free Radic Biol Med 2005;38: 1152-63.
8. Zhang Y, Bhavnani BR. Glutamate-induced apoptosis in neuronal cells is mediated via caspase-dependent and independent mechanisms involving calpain and caspase-3 proteases as well as apoptosis inducing factor (AIF) and this process is inhibited by equine estrogens. BMC Neurosci 2006;7:49-71.
9. Gupta N, Yücel YH. Glaucoma as a neurodegenerative disease. Curr Opin Ophthalmol 2007;18:110-14.
10. Kishore BK, Lambricht P, Laurent G, et al. Mechanism of protection afforded by polyaspartic acid against gentamicininduced phospholipidosis. II. Comparative in vitro and in vivo studies with poly-L-Aspartic, poly-L-glutamic and poly-D-glutamic acids. J Pharmacol Exp Ther 1990;255:875-85.
11. Kishore BK, Maldague P, Tulkens PM, Courtoy PJ. Poly-Dglutamic acid induces an acute lysosomal thesaurismosis of proximal tubules and a marked proliferation of interstitium in rat kidney. Lab Invest 1996;74:1013-23.
12. Schneerson R, Kubler-Kielb J, Liu TY, et al. Poly(g-D-glutamic acid) protein conjugates induce IgG antibodies in mice to the capsule of Bacillus anthracis: a potential addition to the anthrax vaccine. Proc Natl Acad Sci USA 2003;100:8945-50.
13. Hudson SP, Padera PF, Langer R, Kohane DS. The biocompatibility of mesoporous silicates. Biomaterials 2008;29:4045-55.
14. Liu T, Li L, Teng X, et al. Single and repeated dose toxicity of mesoporous hollow silica nanoparticles in intravenously exposed mice. Biomaterials 2011;32:1657-68.
15. Fujita M, Lee BS, Khazenzon NM, et al. Brain tumor tandem targeting using a combination of monoclonal antibodies attached to biopoly(b-L-malic acid). J Control Release 2007;122:356-63.
16. Baselga J. Why the epidermal growth factor receptor? The rationale for cancer therapy. Oncologist 2002;7:2-8.
17. Ljubimova JY, Fujita M, Khazenzon NM, et al. Association between laminin-8 and glial tumor grade, recurrence, and patient survival. Cancer 2004;101:604-12.
18. Fujita M, Khazenzon NM, Bose S, et al. Overexpression of b1-chain-containing laminins in capillary basement membranes of human breast cancer and its metastases. Breast Cancer Res 2005;7: R411-21.
19. Ljubimova JY, Lakhter AJ, Loksh A, et al. Overexpression of a4 chain-containing laminins in human glial tumors identified by gene microarray analysis. Cancer Res 2001;61:5601-10.
20. Ding H, Inoue S, Ljubimov AV, et al. Inhibition of brain tumor growth by intravenous poly(b-L-malic acid) nanobioconjugate with pH-dependent drug release. Proc Natl Acad Sci USA 2010;107: 18143-8.
21. Pal SK, Childs BH, Pegram M. Triple negative breast cancer: unmet medical needs. Breast Cancer Res Treat 2011;125:627-36.
22. Esposito CL, Passaro D, Longobardo I, et al. A neutralizing RNA aptamer against EGFR causes selective apoptotic cell death. PLoS One 2011;6:e24071.
23. Agrawal A, Gutteridge E, Gee JM, et al. Overview of tyrosine kinase inhibitors in clinical breast cancer. Endocr Relat Cancer 2005;12:S135-44.
24. Huang S, Armstrong EA, Benavente S, et al. Dual-Agent molecular targeting of the epidermal growth factor receptor (EGFR): combining anti-EGFR antibody with tyrosine kinase inhibitor. Cancer Res 2004;64:5355-62.
25. Widakowich C, de Castro Jr G, de Azambuja E, et al. Side effects of approved molecular targeted therapies in solid cancers. Oncologist 2007;12:1443-55.
26. Inoue S, Ding H, Portilla-Arias J, et al. Polymalic acid-based nanobiopolymer provides efficient systemic breast cancer treatment by inhibiting both HER2/neu receptor synthesis and activity. Cancer Res 2011;71:1454-64.
27. Inoue S, Patil R, Portilla-Arias J, et al. Nanobiopolymer for direct targeting and inhibition of EGFR expression in triple negative breast cancer. PLoS One 2012;7:e31070.
28. Popplewell L, Koo T, Leclerc X, et al. Gene correction of a Duchenne muscular dystrophy mutation by meganuclease-enhanced exon knock-in. Hum Gene Ther 2013;24:692-701.
29. Moulton HM. In vivo delivery of morpholino oligos by cellpenetrating peptides. Curr Pharm Des 2013;19:2963-9.
30. Li C. Poly(L-glutamic acid) anticancer drug conjugates. Adv Drug Deliv Rev 2002;54:695-713.
31. Lee BS, Fujita M, Khazenzon NM, et al. Polycefin, a new prototype of a multifunctional nanoconjugate based on poly(b-L-malic acid) for drug delivery. Bioconjug Chem 2006;17:317-26.
32. Ljubimova JY, Fujita M, Khazenzon NM, et al. Nanoconjugate based on polymalic acid for tumor targeting. Chem Biol Interact 2008;171:195-203.
33. Nag A, Mitra G, Ghosh PC. A colorimetric assay for estimation of polyethylene glycol and polyethylene glycolated protein using ammonium ferrothiocyanate. Anal Biochem 1996;237: 224-31.
34. Mullen DG, Desai AM, Waddell JN, et al. The implications of stochastic synthesis for the conjugation of functional groups to nanoparticles. Bioconjug Chem 2008;19:1748-52.
35. Dobrovolskaia MA, Neun BW, Clogston JD, et al. Ambiguities in applying traditional Limulus amebocyte lysate tests to quantify endotoxin in nanoparticle formulations. Nanomedicine 2010;5: 555-62.
36. Aida Y, Pabst MJ. Removal of endotoxin from protein solutions by phase separation using Triton X-114. J Immunol Methods 1990; 132:191-5.
37. Assay Cascade Protocols, Frederick National Lab, Nanotechnology Characterization Laboratory. Available from: http://ncl.cancer.gov/working- assay-cascade.asp [last accessed 14 Aug 2013].
38. Ding H, Portilla-Arias J, Patil R, et al. Polymalic acid peptide copolymers: design and optimization for endosomolytic drug delivery. Biomaterials 2011;32:5269-78.
39. Lorenz MR, Holzapfel V, Musyanovych A, et al. Uptake of functionalized, fluorescent-labeled polymeric particles in different cell lines and stem cells. Biomaterials 2006;27:2820-8.
40. Wilhelm C, Billotey C, Roger J, et al. Intracellular uptake of anionic superparamagnetic nanoparticles as a function of their surface coating. Biomaterials 2003;24:1001-11.
41. Ding H, Portilla-Arias J, Patil R, et al. Distinct mechanisms of membrane permeation induced by two polymalic acid copolymers. Biomaterials 2013;34:217-25.
42. Edick MJ, Tesfay L, Lamb LE, et al. Inhibition of integrinmediated crosstalk with epidermal growth factor receptor/Erk or Src signaling pathways in autophagic prostate epithelial cells induces caspase-independent death. Mol Biol Cell 2007;18: 2481-90.
43. Yu X, Miyamoto S, Mekada E. Integrin a2b1-dependent EGFR receptor activation at cell-cell contact sites. J Cell Sci 2000;113: 2139-47.
44. Elgue G, Sanchez J, Egberg N, et al. Effect of surface-immobilized heparin on the activation of adsorbed factor XII. Artif Organs 1993; 17:721-6.
45. Fujita M, Khazenzon NM, Ljubimov AV, et al. Inhibition of laminin-8 in vivo using a novel poly(malic acid)-based carrier reduces glioma angiogenesis. Angiogenesis 2006;9:183-91.
46. Kallergi G, Agelaki S, Kalykaki A, et al. Phosphorylated EGFR and PI3K/Akt signaling kinases are expressed in circulating tumor cells of breast cancer patients. Breast Cancer Res 2008;10:R80.
47. Liu D, He J, Yuan Z, et al. EGFR expression correlates with decreased disease-free survival in triple-negative breast cancer: a retrospective analysis based on a tissue microarray. Med Oncol 2012;29:401-5.
48. Mainelis G, Seshadri S, Garbuzenko OB, et al. Characterization and application of a nose-only exposure chamber for inhalation delivery of liposomal drugs and nucleic acids to mice. J Aerosol Med Pulm Drug Deliv 2013. [Epub ahead of print] PMID: 23530772.
49. Zhang M, Garbuzenko OB, Reuhl KR, et al. Two-in-one: combined targeted chemo and gene therapy for tumor suppression and prevention of metastases. Nanomedicine 2012;7:185-97.
50. Hiroi N, Funahashi A, Kitano H. Comparative studies of suppression of malignant cancer cell phenotype by antisense oligo DNA and small interfering RNA. Cancer Gene Ther 2006; 13:7-12.
51. Kinali M, Arechavala-Gomeza V, Feng L, et al. Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: a single-blind, placebo-controlled, dose-escalation, proof-of-concept study. Lancet Neurol 2009;8: 918-28.
52. Craft BS, Hortobagyi GN, Moulder SL. Adjuvant biologic therapy for breast cancer. Cancer J 2007;13:156-61.
53. Ding H, Helguera G, Rodr?́guez JA, et al. Polymalic acid nanobioconjugate for simultaneous immunostimulation and inhibition of tumor growth in HER2/neu-positive breast cancer. J Control Release 2013. [Epub ahead of print] PMID: 23770212.