HSP32 (HO-1) inhibitor, copoly(styrene-maleic acid)-zinc protoporphyrin IX, a water-soluble micelle as anticancer agent: In vitro and in vivo anticancer effect

European Journal of Pharmaceutics and Biopharmaceutics

Volumn 81, Issue 3, 2012, Pages 540-547

  Fang, Jun ^a   Greish, Khaled ^a,b   Qin, Haibo ^a   Liao, Long ^a   Nakamura, Hideaki ^a   Takeya, Motohiro ^c   Maeda, Hiroshi ^a  

^a SOJO UNIVERSITY   (Japan)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c KUMAMOTO UNIV SCHOOL OF MEDICINE   (Japan)

Author keywords

Cancer chemotherapy; EPR effect; Heme oxygenase 1; HSP32; Styrene maleic acid copolymer; Zinc protoporphyrin

Indexed keywords

ANTINEOPLASTIC AGENT; HEAT SHOCK PROTEIN 32; HEME OXYGENASE 1; HEME OXYGENASE INHIBITOR; STYRENE MALEIC ANHYDRIDE COPOLYMER; UNCLASSIFIED DRUG; ZINC PROTOPORPHYRIN IX;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG CYTOTOXICITY; DRUG DISTRIBUTION; DRUG HALF LIFE; DRUG MEGADOSE; DRUG SAFETY; DRUG SOLUBILITY; DRUG TUMOR LEVEL; ENCAPSULATION; FEMALE; FIBROSARCOMA; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; IN VIVO STUDY; LIVER CANCER; MALE; MELANOMA; MICELLE; MOUSE; NONHUMAN; RABBIT; TUMOR MODEL; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; CHICK EMBRYO; FEMALE; HEME OXYGENASE-1; HUMANS; INHIBITORY CONCENTRATION 50; INJECTIONS, INTRAVENOUS; LIVER; MALE; MALEATES; METALLOPORPHYRINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICELLES; NEOPLASMS; POLYSTYRENES; RABBITS; TISSUE DISTRIBUTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84863775348     PISSN: 09396411     EISSN: 18733441     Source Type: Journal    
DOI: 10.1016/j.ejpb.2012.04.016     Document Type: Article

References (38)

1. M.D. Maines, Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications, FASEB J. 2 (1988) 2257-2268.
2. J. Fang, T. Akaike, H. Maeda, Antiapoptotic role of heme oxygenase (HO) and the potential of HO as a target in anticancer treatment, Apoptosis 9 (2004) 27-35. (Pubitemid 38270426)
3. S.M. Keyse, R.M. Tyrrell, Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite, Proc. Natl. Acad. Aci. USA 86 (1989) 99-103. (Pubitemid 19036341)
4. R. Motterlini, R. Foresti, R. Bassi, B. Calabrese, J.E. Clark, C.J. Green, Endothelial heme oxygenase-1 induction by hypoxia. Modulation by inducible nitric oxide synthase and S-nitrosothiols, J. Biol. Chem. 275 (2000) 13613-13620. (Pubitemid 30257429)
5. K. Doi, T. Akaike, S. Fujii, S. Tanaka, N. Ikebe, T. Beppu, S. Shibahara, M. Ogawa, H. Maeda, Induction of haem oxygenase-1 by nitric oxide and ischaemia in experimental solid tumours and implications for tumour growth, Br. J. Cancer 80 (1999) 1945-1954. (Pubitemid 29391278)
6. S. Tanaka, T. Akaike, J. Fang, T. Beppu, M. Ogawa, F. Tamura, Y. Miyamoto, H. Maeda, Antiapoptotic effect of haem oxygenase-1 induced by nitric oxide in experimental solid tumour, Br. J. Cancer 88 (2003) 902-909. (Pubitemid 36520878)
7. J.P. Greenstein, Biochemistry of Cancer, second ed., Academic Press, New York, 1954.
8. Y. Hasegawa, T. Takano, A. Miyauchi, F. Matsuzaka, H. Yoshida, K. Kuma, N. Amino, Decreased expression of glutathione peroxidase mRNA in thyroid anaplastic carcinoma, Cancer Lett. 182 (2002) 69-74. (Pubitemid 34518658)
9. N. Yamanaka, D. Deamer, Superoxide dismutase activity in WI-38 cell cultures: effect of age, trypsinization and SV-40 transformation, Physiol. Chem. Phus. 6 (1974) 95-106.
10. K. Sato, K. Ito, H. Kohara, Y. Yamaguchi, K. Adachi, H. Endo, Negative regulation of catalase gene expression in hepatoma cells, Mol. Cell. Biol. 12 (1992) 2525-2533.
11. J. Fang, D. Deng, H. Nakamura, T. Akuta, H. Qin, A.K. Iyer, K. Greish, H. Maeda, Oxystress inducing antitumor therapeutics via tumor-targeted delivery of PEG-conjugated D-amino acid oxidase, Int. J. Cancer 122 (2008) 1135-1144. (Pubitemid 351214014)
12. S.K. Sahoo, T. Sawa, J. Fang, S. Tanaka, Y. Miyamoto, T. Akaike, H. Maeda, Pegylated zinc protoporphyrin: a water-soluble heme oxygenase inhibitor with tumor-targeting capacity, Bioconjug. Chem. 13 (2002) 1031-1038.
13. J. Fang, T. Sawa, T. Akaike, T. Akuta, S.K. Sahoo, G. Khaled, A. Hamada, H. Maeda, In vivo antitumor activity of pegylated zinc protoporphyrin: targeted inhibition of heme oxygenase in solid tumor, Cancer Res. 63 (2003) 3567-3574. (Pubitemid 36793037)
14. A.K. Iyer, K. Greish, J. Fang, R. Murakami, H. Maeda, High-loading nanosized micelles of copoly(styrene-maleic acid)-zinc protoporphyrin for targeted delivery of a potent heme oxygenase inhibitor, Biomaterials 28 (2007) 1871-1881. (Pubitemid 46123550)
15. A. Kobayashi, T. Oda, H. Maeda, Protein binding of macromolecular anticancer agent SMANCS: characterization of poly(styrene-co-maleic acid) derivatives as an albumin binding ligand, J. Bioact. Compat. Polym. 3 (1988) 319-333. (Pubitemid 19059729)
16. K. Greish, A. Nagamitsu, J. Fang, H. Maeda, Copoly(styrene-maleic acid)-pirarubicin micelles: high tumor-targeting efficiency with little toxicity, Bioconjug. Chem. 16 (2005) 230-236. (Pubitemid 40129698)
17. H. Nakamura, J. Fang, B. Gahininath, K. Tsukigawa, H. Maeda, Intracellular uptake and behavior of two types zinc protoporphyrin (ZnPP) micelles, SMA-ZnPP and PEG-ZnPP as anticancer agents; unique intracellular disintegration of SMA micelles, J. Control. Release 155 (2011) 367-375.
18. H. Hatakeyama, H. Akita, H. Harashima, A multifunctional envelope type nano device (MEND) for gene delivery to tumours based on the EPR effect: a strategy for overcoming the PEG dilemma, Adv. Drug Deliv. Rev. 63 (2011) 152-160.
19. Y. Matsumura, H. Maeda, A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent SMANCS, Cancer Res. 46 (1986) 6387-6392. (Pubitemid 17221789)
20. H. Maeda, T. Sawa, T. Konno, Mechanism of tumor-targeted delivery of macromolecular drugs, including the EPR effect in solid tumor and clinical overview of the prototype polymeric drug SMANCS, J. Control. Release 74 (2001) 47-61. (Pubitemid 32727608)
21. K. Greish, J. Fang, T. Inutsuka, A. Nagamitsu, H. Maeda, Macromolecular therapeutics: advantages and prospects with special emphasis on solid tumour targeting, Clin. Pharmacokinet. 42 (2003) 1089-1105. (Pubitemid 37357647)
22. H. Maeda, Tumor-selective delivery of macromolecular drugs via the EPR effect: background and future prospects, Bioconjug. Chem. 21 (2010) 797-802.
23. R. Duncan, The dawning era of polymer therapeutics, Nat. Rev. Drug Discov. 2 (2003) 347-360. (Pubitemid 37361705)
24. H. Maeda, G.Y. Bharate, J. Daruwalla, Polymeric drugs for efficient tumortargeted drug delivery based on EPR-effect, Eur. J. Pharm. Biopharm. 71 (2009) 409-419.
25. T. Seki, J. Fang, H. Maeda, Tumor targeted macromolecular drug delivery based on the enhanced permeability and retention effect in solid tumor, in: Y. Lu, R.I. Mahato (Eds.), Pharmaceutical Perspectives of Cancer Therapeutics, AAPS-Springer Publishing, New York, 2009, pp. 93-102.
26. J. Fang, H. Nakamura, H. Maeda, The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect, Adv. Drug Deliv. Rev. 63 (2010) 136-151.
27. G. Yang, X. Nguyen, J. Qu, P. Rekulapelli, D.K. Stevenson, P.A. Dennery, Unique effects of zinc protoporphyrin on HO-1 induction and apoptosis, Blood 97 (2001) 1306-1313. (Pubitemid 32183753)
28. M. Mayerhofer, S. Florian, M.T. Krauth, K.J. Aichberger, M. Bilban, R. Marculescu, D. Printz, G. Fritsch, O. Wagner, E. Selzer, W.R. Sperr, P. Valent, C. Sillaber, Identification of heme oxygenase-1 as a novel BCR/ABL-dependent survival factor in chronic myeloid leukemia, Cancer Res. 64 (2004) 3148-3154. (Pubitemid 38581416)
29. R. Kondo, K.V. Gleixner, M. Mayerhofer, A. Vales, A. Gruze, P. Samorapoompichit, K. Greish, M.T. Krauth, K.J. Aichberger, W.F. Pickl, H. Esterbauer, C. Sillaber, H. Maeda, P. Valent, Identification of heat shock protein 32 (Hsp32) as a novel survival factor and therapeutic target in neoplastic mast cells, Blood 110 (2007) 661-669. (Pubitemid 47105405)
30. E. Hadzijusufovic, L. Rebuzzi, K.V. Gleixner, V. Ferenc, B. Peter, R. Kondo, A. Gruze, M. Kneidinger, M.T. Krauth, M. Mayerhofer, P. Samorapoompichit, K. Greish, A.K. Iyer, W.F. Pickl, H. Maeda, M. Willmann, P. Valent, Targeting of heat-shock protein 32/heme oxygenase-1 in canine mastocytoma cells is associated with reduced growth and induction of apoptosis, Exp. Hematol. 36 (2008) 1461-1470.
31. M. Mayerhofer, K.V. Gleixner, J. Mayerhofer, G. Hoermann, E. Jaeger, K.J. Aichberger, R.G. Ott, K. Greish, H. Nakamura, S. Derdak, P. Samorapoompichit, W.F. Pickl, V. Sexl, H. Esterbauer, I. Schwarzinger, C. Sillaber, H. Maeda, P. Valent, Targeting of heat shock protein 32 (Hsp32)/heme oxygenase-1 (HO-1) in leukemic cells in chronic myeloid leukemia: a novel approach to overcome resistance against imatinib, Blood 111 (2008) 2200-2210. (Pubitemid 351451534)
32. F. Suzuki, R.B. Pollard, S. Uchimura, T. Munakata, H. Maeda, Role of natural killer cells and macrophages in the nonspecific resistance to tumors in mice stimulated with SMANCS, a polymer-conjugated derivative of neocarzinostatin, Cancer Res. 50 (1990) 3897-3904. (Pubitemid 20225603)
33. F. Suzuki, T. Munakata, H. Maeda, Interferon induction by SMANCS: a polymerconjugated derivative of neocarzinostatin, Anticancer Res. 8 (1988) 97-103.
34. T. Oda, T. Morinaga, H. Maeda, Stimulation of macrophage by polyanions and its conjugated proteins and effect on cell membrane, Proc. Soc. Exp. Biol. Med. 181 (1986) 9-17. (Pubitemid 16139487)
35. H. Haase, J.L. Ober-Blöbaum, G. Engelhardt, S. Hebel, A. Heit, H. Heine, L. Rink, Zinc signals are essential for lipopolysaccharide-induced signal transduction in monocytes, J. Immunol. 181 (2008) 6491-6502.
36. L.C. Costello, R.B. Franklin, P. Feng, Mitochondrial function, zinc, and intermediary metabolism relationships in normal prostate and prostate cancer, Mitochondrion 5 (2005) 143-153. (Pubitemid 40823303)
37. P. Feng, T. Li, Z. Guan, R.B. Franklin, L.C. Costello, The involvement of Bax in zinc-induced mitochondrial apoptogenesis in malignant prostate cells, Mol. Cancer 7 (2008) 25.
38. S.F. Lin, H. Wei, D. Maeder, R.B. Franklin, P. Feng, Profiling of zinc-altered gene expression in human prostate normal vs. cancer cells: a time course study, J. Nutr. Biochem. 20 (2009) 1000-1012.