Polymer donors of nitric oxide improve the treatment of experimental solid tumours with nanosized polymer therapeutics

References

• Vasey PA, Kaye SB, Morrison R, et al. Phase I clinical and pharmacokinetic study of PK1 [N-(2-hydroxypropyl)methacrylamide copolymer doxorubicin]: first member of a new class of chemotherapeutic agents–drug–polymer conjugates. Cancer Research Campaign Phase I/II Committee. Clin Cancer Res. 1999;5:83–94.
   PubMed Web of Science ®Google Scholar
• Kopecek J, Kopeckova P. HPMA copolymers: origins, early developments, present, and future. Adv Drug Deliv Rev. 2010;62:122–149.
   PubMed Web of Science ®Google Scholar
• Duncan R, Vicent MJ. Do HPMA copolymer conjugates have a future as clinically useful nanomedicines? A critical overview of current status and future opportunities. Adv Drug Deliv Rev. 2010;62:272–282.
   PubMed Web of Science ®Google Scholar
• Kopecek J. Polymer–drug conjugates: origins, progress to date and future directions. Adv Drug Deliv Rev. 2013;65:49–59.
   PubMed Web of Science ®Google Scholar
• Ulbrich K, Subr V. Structural and chemical aspects of HPMA copolymers as drug carriers. Adv Drug Deliv Rev. 2010;62:150–166.
   PubMed Web of Science ®Google Scholar
• Rihova B, Kubackova K. Clinical implications of N-(2-hydroxypropyl)methacrylamide copolymers. CPB. 2003;4:311–322.
   Google Scholar
• Mrkvan T, Sirova M, Etrych T, et al. Chemotherapy based on HPMA copolymer conjugates with pH-controlled release of doxorubicin triggers anti-tumor immunity. J Control Release. 2005;110:119–129.
   PubMed Web of Science ®Google Scholar
• Sirova M, Strohalm J, Subr V, et al. Treatment with HPMA copolymer-based doxorubicin conjugate containing human immunoglobulin induces long-lasting systemic anti-tumour immunity in mice. Cancer Immunol Immunother. 2007;56:35–47.
   PubMed Web of Science ®Google Scholar
• Rihova B, Kovar M. Immunogenicity and immunomodulatory properties of HPMA-based polymers. Adv Drug Deliv Rev. 2010;62:184–191.
   PubMed Web of Science ®Google Scholar
• Rihova B, Kovar L, Kovar M, et al. Cytotoxicity and immunostimulation: double attack on cancer cells with polymeric therapeutics. Trends Biotechnol. 2009;27:11–17.
   PubMed Web of Science ®Google Scholar
• Sirova M, Kabesova M, Kovar L, et al. HPMA copolymer-bound doxorubicin induces immunogenic tumor cell death. Curr Med Chem. 2013;20:4815–4826.
   PubMed Web of Science ®Google Scholar
• Greish K. Enhanced permeability and retention of macromolecular drugs in solid tumors: a royal gate for targeted anticancer nanomedicines. J Drug Target. 2007;15:457–464.
   PubMed Web of Science ®Google Scholar
• Maeda H. Toward a full understanding of the EPR effect in primary and metastatic tumors as well as issues related to its heterogeneity. Adv Drug Deliv Rev. 2015;91:3–6.
   PubMed Web of Science ®Google Scholar
• Nakamura H, Fang J, Maeda H. Development of next-generation macromolecular drugs based on the EPR effect: challenges and pitfalls. Expert Opin Drug Deliv. 2015;12:53–64.
   PubMed Web of Science ®Google Scholar
• Seki T, Fang J, Maeda H. Enhanced delivery of macromolecular antitumor drugs to tumors by nitroglycerin application. Cancer Sci. 2009;100:2426–2430.
   PubMed Web of Science ®Google Scholar
• Maeda H. Vascular permeability in cancer and infection as related to macromolecular drug delivery, with emphasis on the EPR effect for tumor-selective drug targeting. Proc Jpn Acad Ser B. 2012;88:53–71.
   PubMed Web of Science ®Google Scholar
• Stevens EV, Carpenter AW, Shin JH, et al. Nitric oxide-releasing silica nanoparticle inhibition of ovarian cancer cell growth. Mol Pharm. 2010;7:775–785.
   PubMed Web of Science ®Google Scholar
• Quinn JF, Whittaker MR, Davis TP. Delivering nitric oxide with nanoparticles. J Control Release. 2015;205:190–205.
   PubMed Web of Science ®Google Scholar
• Song Q, Tan S, Zhuang X, et al. Nitric oxide releasing d-alpha-tocopheryl polyethylene glycol succinate for enhancing antitumor activity of doxorubicin. Mol Pharm. 2014;11:4118–4129.
   PubMed Web of Science ®Google Scholar
• Ishima Y, Chen D, Fang J, et al. S-Nitrosated human serum albumin dimer is not only a novel anti-tumor drug but also a potentiator for anti-tumor drugs with augmented EPR effects. Bioconjug Chem. 2012;23:264–271.
   PubMed Web of Science ®Google Scholar
• Kinoshita R, Ishima Y, Ikeda M, et al. S-Nitrosated human serum albumin dimer as novel nano-EPR enhancer applied to macromolecular anti-tumor drugs such as micelles and liposomes. J Control Release. 2015;217:1–9.
   PubMed Web of Science ®Google Scholar
• Studenovsky M, Sivak L, Sedlacek O, et al. Polymer nitric oxide donors potentiate the treatment of experimental solid tumours by increasing drug accumulation in the tumour tissue. J Control Release. (submitted).
   Web of Science ®Google Scholar
• Etrych T, Strohalm J, Chytil P, et al. Novel star HPMA-based polymer conjugates for passive targeting to solid tumors. J Drug Target. 2011;19:874–889.
   PubMed Web of Science ®Google Scholar
• Barberis M, Pérez-Prieto J. Enantioselective synthesis of sabina ketone. Tetrahedron Lett. 2003;44:6683–6685.
   Web of Science ®Google Scholar
• Ulbrich K, Subr V, Strohalm J, et al. Polymeric drugs based on conjugates of synthetic and natural macromolecules. I. Synthesis and physico-chemical characterisation. J Control Release. 2000;64:63–79.
   PubMed Web of Science ®Google Scholar
• Hruby M, Kucka J, Lebeda O, et al. New bioerodable thermoresponsive polymers for possible radiotherapeutic applications. J Control Release. 2007;119:25–33.
   PubMed Web of Science ®Google Scholar
• Etrych T, Jelinkova M, Rihova B, et al. New HPMA copolymers containing doxorubicin bound via pH-sensitive linkage: synthesis and preliminary in vitro and in vivo biological properties. J Control Release. 2001;73:89–102.
   PubMed Web of Science ®Google Scholar
• Etrych T, Strohalm J, Chytil P, et al. Biodegradable star HPMA polymer conjugates of doxorubicin for passive tumor targeting. Eur J Pharm Sci. 2011;42:527–539.
   PubMed Web of Science ®Google Scholar
• Chytil P, Etrych T, Kostka L, et al. Hydrolytically degradable polymer micelles for anticancer drug delivery to solid tumors. Macromol Chem Phys. 2012;213:858–867.
   Web of Science ®Google Scholar
• Etrych T, Strohalm J, Sirova M, et al. High-molecular weight star conjugates containing docetaxel with high anti-tumor activity and low systemic toxicity in vivo. Polym Chem. 2015;6:160–170.
   Web of Science ®Google Scholar
• Kovar M, Mrkvan T, Strohalm J, et al. HPMA copolymer-bound doxorubicin targeted to tumor-specific antigen of BCL1 mouse B cell leukemia. J Control Release. 2003;92:315–330.
   PubMed Web of Science ®Google Scholar
• Helft J, Bottcher J, Chakravarty P, et al. GM-CSF mouse bone marrow cultures comprise a heterogeneous population of CD11c(+)MHCII(+) macrophages and dendritic cells. Immunity. 2015;42:1197–1211.
   PubMed Web of Science ®Google Scholar
• Tomalova B, Sirova M, Rossmann P, et al. The structure-dependent toxicity, pharmacokinetics and anti-tumour activity of HPMA copolymer conjugates in the treatment of solid tumours and leukaemia. J Control Release. 2016;223:1–10.
   PubMed Web of Science ®Google Scholar
• Sirova M, Strohalm J, Chytil P, et al. The structure of polymer carriers controls the efficacy of the experimental combination treatment of tumors with HPMA copolymer conjugates carrying doxorubicin and docetaxel. J Control Release. 2017;246:1–11.
   PubMed Web of Science ®Google Scholar
• Rihova B, Strohalm J, Kovar M, et al. Induction of systemic antitumour resistance with targeted polymers. Scand J Immunol. 2005;62 Suppl 1:100–105.
   PubMed Web of Science ®Google Scholar
• Yasuda H, Nakayama K, Watanabe M, et al. Nitroglycerin treatment may enhance chemosensitivity to docetaxel and carboplatin in patients with lung adenocarcinoma. Clin Cancer Res. 2006;12:6748–6757.
   PubMed Web of Science ®Google Scholar
• Riganti C, Miraglia E, Viarisio D, et al. Nitric oxide reverts the resistance to doxorubicin in human colon cancer cells by inhibiting the drug efflux. Cancer Res. 2005;65:516–525.
   PubMed Web of Science ®Google Scholar
• Chegaev K, Riganti C, Lazzarato L, et al. Nitric oxide donor doxorubicins accumulate into doxorubicin-resistant human colon cancer cells inducing cytotoxicity. ACS Med Chem Lett. 2011;2:494–497.
   PubMed Web of Science ®Google Scholar
• Zhao S, Tan S, Guo Y, et al. pH-sensitive docetaxel-loaded d-alpha-tocopheryl polyethylene glycol succinate-poly(beta-amino ester) copolymer nanoparticles for overcoming multidrug resistance. Biomacromolecules. 2013;14:2636–2646.
   PubMed Web of Science ®Google Scholar
• Frederiksen LJ, Sullivan R, Maxwell LR, et al. Chemosensitization of cancer in vitro and in vivo by nitric oxide signaling. Clin Cancer Res. 2007;13:2199–2206.
   PubMed Web of Science ®Google Scholar
• Adams C, McCarthy HO, Coulter JA, et al. Nitric oxide synthase gene therapy enhances the toxicity of cisplatin in cancer cells. J Gene Med. 2009;11:160–168.
   PubMed Web of Science ®Google Scholar
• Etrych T, Subr V, Laga R, et al. Polymer conjugates of doxorubicin bound through an amide and hydrazone bond: impact of the carrier structure onto synergistic action in the treatment of solid tumours. Eur J Pharm Sci. 2014;58:1–12.
   PubMed Web of Science ®Google Scholar
• Wu J, Akaike T, Maeda H. Modulation of enhanced vascular permeability in tumors by a bradykinin antagonist, a cyclooxygenase inhibitor, and a nitric oxide scavenger. Cancer Res. 1998;58:159–165.
   PubMed Web of Science ®Google Scholar
• Engels K, Knauer SK, Loibl S, et al. NO signaling confers cytoprotectivity through the survivin network in ovarian carcinomas. Cancer Res. 2008;68:5159–5166.
   PubMed Web of Science ®Google Scholar
• Fetz V, Bier C, Habtemichael N, et al. Inducible NO synthase confers chemoresistance in head and neck cancer by modulating survivin. Int J Cancer. 2009;124:2033–2041.
   PubMed Web of Science ®Google Scholar
• Sanhueza C, Wehinger S, Castillo Bennett J, et al. The twisted survivin connection to angiogenesis. Mol Cancer. 2015;14:198.
   PubMed Web of Science ®Google Scholar
• Sirova M, Mrkvan T, Etrych T, et al. Preclinical evaluation of linear HPMA-doxorubicin conjugates with pH-sensitive drug release: efficacy, safety, and immunomodulating activity in murine model. Pharm Res. 2010;27:200–208.
   PubMed Web of Science ®Google Scholar
• Obregon C, Graf L, Chung KF, et al. Nitric oxide sustains IL-1beta expression in human dendritic cells enhancing their capacity to induce IL-17-producing T-cells. PLoS One. 2015;10:e0120134.
   PubMed Web of Science ®Google Scholar