Prostate-specific membrane antigen-targeted liposomes specifically deliver the Zn²⁺ chelator TPEN inducing oxidative stress in prostate cancer cells

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References

• 1 Kirby M, Hirst C, Crawford ED. Characterising the castration-resistant prostate cancer population: a systematic review. Int. J. Clin. Pract. 65(11), 1180–1192 (2011).
  Medline CASGoogle Scholar
• 2 Costello LC, Franklin RB. Novel role of zinc in the regulation of prostate citrate metabolism and its implications in prostate cancer. Prostate 35(4), 285–296 (1998).
  Medline CASGoogle Scholar
• 3 Costello LC, Franklin RB. The clinical relevance of the metabolism of prostate cancer; zinc and tumor suppression: connecting the dots. Mol. Cancer doi:10.1186/1476-4598-5-17 (2006) (Epub ahead of print). • Zinc is identified as an important factor for advanced prostate cancer development, and a possible novel target for future treatments.
  Google Scholar
• 4 Golovine K, Uzzo RG, Makhov P, Crispen PL, Kunkle D, Kolenko VM. Depletion of intracellular zinc increases expression of tumorigenic cytokines VEGF, IL-6 and IL-8 in prostate cancer cells via NF-kappaB-dependent pathway. Prostate 68(13), 1443–1449 (2008).
  Medline CASGoogle Scholar
• 5 Shah MR, Kriedt CL, Lents NH et al. Direct intra-tumoral injection of zinc-acetate halts tumor growth in a xenograft model of prostate cancer. J. Exp. Clin. Canc. Res. doi:10.1186/1756-9966-28-84 (2009) (Epub ahead of print).
  MedlineGoogle Scholar
• 6 Makhov P, Golovine K, Uzzo RG et al. Zinc chelation induces rapid depletion of the X-linked inhibitor of apoptosis (XIAP) and sensitizes prostate cancer cells to TRAIL-mediated apoptosis. Cell Death Differ. 15(11), 1745–1751 (2008).
  Medline CASGoogle Scholar
• 7 Carraway RE, Dobner PR. Zinc pyrithione induces ERK- and PKC-dependent necrosis distinct from TPEN-induced apoptosis in prostate cancer cells. Biochim. Biophys. Acta 1823(2), 544–557 (2012).
  Medline CASGoogle Scholar
• 8 Gmeiner WH, Boyacioglu O, Stuart CH, Jennings-Gee J, Balaji KC. The cytotoxic and pro-apoptotic activities of the novel fluoropyrimidine F10 towards prostate cancer cells are enhanced by Zn2þ-chelation and inhibiting the serine protease Omi/HtrA2. Prostate 75(4), 360–369 (2015).• N,N,N’,N’-tetrakis(2-pyridylmethyl)-ethylenediamine is identified to induce apoptosis in a zinc-dependent manner, and can increase apoptotic activity of other drugs in advanced prostate cancer cell lines.
  Medline CASGoogle Scholar
• 9 Hashemi M, Ghavami S, Eshraghi M, Booy EP, Los M. Cytotoxic effects of intra and extracellular zinc chelation on human breast cancer cells. Eur. J. Pharmacol. 557(1), 9–19 (2007).
  Medline CASGoogle Scholar
• 10 Mendivil-Perez M, Velez-Pardo C, Jimenez-Del-Rio M. TPEN induces apoptosis independently of Zinc chelator activity in a model of acute lymphoblastic leukemia and ex vivo acute leukemia cells through oxidative stress and mitochondria caspase-3- and AIF-dependent pathways. Oxid. Med. Cell Longev. 2012, e313275 (2012).
  MedlineGoogle Scholar
• 11 Khandrika L, Kumar B, Koul S, Maroni P, Koul HK. Oxidative stress in prostate cancer. Cancer Lett. 282(2), 125–136 (2009).
  Medline CASGoogle Scholar
• 12 Adler M, Dinterman RE, Wannemacher RW. Protection by the heavy metal chelator N,N,N’,N’-tetrakis (2-pyridylmethyl)ethylenediamine (TPEN) against the lethal action of botulinum neurotoxin A and B. Toxicon 35(7), 1089–1100 (1997).
  Medline CASGoogle Scholar
• 13 Safra T, Muggia F, Jeffers S et al. Pegylated liposomal doxorubicin (doxil): reduced clinical cardiotoxicity in patients reaching or exceeding cumulative doses of 500 mg/m2. Ann. Oncol. 11(8), 1029–1033 (2000).
  Medline CASGoogle Scholar
• 14 Awasthi VD, Goins B, Klipper R, Phillips WT. Dual radiolabeled liposomes: biodistribution studies and localization of focal sites of infection in rats. Nucl. Med. Biol. 25(2), 155–160 (1998).
  Medline CASGoogle Scholar
• 15 Seo JW, Mahakian LM, Kheirolomoom A et al. Liposomal Cu-64 labeling method using bifunctional chelators: poly(ethylene glycol) spacer and chelator effects. Bioconjug. Chem. 21(7), 1206–1215 (2010).
  Medline CASGoogle Scholar
• 16 Cao Z, Tong R, Mishra A et al. Reversible cell-specific drug delivery with aptamer-functionalized liposomes. Angew. Chem Int. Ed. Engl. 48(35), 6494–6498 (2009).
  Medline CASGoogle Scholar
• 17 Kang H, O’Donoghue MB, Liu H, Tan W. A liposome-based nanostructure for aptamer directed delivery. Chem. Commun. 46(2), 249–251 (2009).
  MedlineGoogle Scholar
• 18 Boyacioglu O, Stuart CH, Kulik G, Gmeiner WH. Dimeric DNA aptamer complexes for high-capacity-targeted drug delivery using pH-sensitive covalent linkages. Mol. Ther. Nucleic Acids 2(7), e107 (2013).•• The prostate-specific membrane antigen-specific aptamer SZTI01 is identified and displays differential binding to cells that express the target versus those that do not.
  MedlineGoogle Scholar
• 19 Foy JW, Rittenhouse K, Modi M, Patel, M. Local tolerance and systemic safety of pegaptanib sodium in the dog and rabbit. J. Ocul. Pharmacol. Ther. 23, 452–466 (2003).
  Google Scholar
• 20 Silver DA, Pellicer I, Fair WR, Heston WD, Cordon-Cardo C. Prostate-specific membrane antigen expression in normal and malignant human tissues. Clin. Cancer Res. 3(1), 81–85 (1997).
  Medline CASGoogle Scholar
• 21 Wright Jr. GL, Mayer Grob B, Haley C et al. Upregulation of prostate-specific membrane antigen after androgen-deprivation therapy. Urology 48(2), 326–334 (1996).
  MedlineGoogle Scholar
• 22 Tang H, Arulsamy N, Radosz M et al. Highly active copper-based catalyst for atom transfer radical polymerization. J. Am. Chem. Soc. 128(50), 16277–16285 (2006).
  Medline CASGoogle Scholar
• 23 Crow JP. Dichlorodihydrofluorescein and dihydrorhodamine 123 are sensitive indicators of peroxynitrite in vitro: implications for intracellular measurement of reactive nitrogen and oxygen species. Nitric Oxide 1(2), 145–157 (1997).
  Medline CASGoogle Scholar
• 24 Faulkner KM, Liochev SI, Fridovich I. Stable Mn(III) porphyrins mimic superoxide dismutase in vitro and substitute for it in vivo. J. Biol. Chem. 269(38), 23471–23476 (1994).
  Medline CASGoogle Scholar
• 25 Batinić-Haberle I, Cuzzocrea S, Rebouças JS et al. Pure MnTBAP selectively scavenges peroxynitrite over superoxide: comparison of pure and commercial MnTBAP samples to MnTE-2-PyP in two models of oxidative stress injury, an SOD-specific Escherichia coli model and carrageenan-induced pleurisy. Free Radic. Biol. Med. 46(2), 192–201 (2009).
  Medline CASGoogle Scholar
• 26 Costello LC, Feng P, Milon B, Tan M, Franklin RB. Role of zinc in the pathogenesis and treatment of prostate cancer: critical issues to resolve. Prostate Cancer Prostatic Dis. 7(2), 111–117 (2004).
  Medline CASGoogle Scholar
• 27 Chai F, Truong-Tran AQ, Evdokiou A, Young GP, Zalewski PD. Intracellular zinc depletion induces caspase activation and p21 ^Waf1/Cip1 cleavage in human epithelial cell lines. J. Infect. Diss. 182(s1), S85–S92 (2000).
  Medline CASGoogle Scholar
• 28 López JJ, Redondo PC, Salido GM, Pariente JA, Rosado JA. N,N,N′,N′-tetrakis(2-pyridylmethyl)ethylenediamine induces apoptosis through the activation of caspases-3 and -8 in human platelets. A role for endoplasmic reticulum stress. J. Thromb. Haemost. 7(6), 992–999 (2009).
  Medline CASGoogle Scholar
• 29 Gorrini C, Harris IS, Mak TW. Modulation of oxidative stress as an anticancer strategy. Nat. Rev. Drug Discov. 12(12), 931–947 (2013).
  Medline CASGoogle Scholar
• 30 Trzeciak AR, Nyaga SG, Jaruga P, Lohani A, Dizdaroglu M, Evans MK. Cellular repair of oxidatively induced DNA base lesions is defective in prostate cancer cell lines, PC-3 and DU-145. Carcinogenesis 25(8), 1359–1370 (2004).
  Medline CASGoogle Scholar
• 31 Fatfat M, Merhi RA, Rahal O et al. Copper chelation selectively kills colon cancer cells through redox cycling and generation of reactive oxygen species. BMC Cancer 14, 527 (2014).
  MedlineGoogle Scholar
• 32 Arslan P, Di Virgilio F, Beltrame M, Tsien RY, Pozzan T. Cytosolic Ca²⁺ homeostasis in Ehrlich and Yoshida carcinomas. A new, membrane-permeant chelator of heavy metals reveals that these ascites tumor cell lines have normal cytosolic free Ca²⁺. J. Biol. Chem. 260(5), 2719–2727 (1985).
  Medline CASGoogle Scholar
• 33 Haga N, Fujita N, Tsuruo T. Mitochondrial aggregation precedes cytochrome c release from mitochondria during apoptosis. Oncogene 22(36), 5579–5585 (2003).
  Medline CASGoogle Scholar
• 34 Lin J, Zahurak M, Beer TM et al. A non-comparative randomized Phase II study of 2 doses of ATN-224, a copper/zinc superoxide dismutase inhibitor, in patients with biochemically recurrent hormone-naïve prostate cancer. Urol. Oncol. 31(5), 581–588 (2013).
  Medline CASGoogle Scholar