Disulfide cross-linked micelles of novel HDAC inhibitor thailandepsin A for the treatment of breast cancer

Biomaterials

Volumn 67, Issue , 2015, Pages 183-193

  Xiao, Kai ^a,b   Li, Yuan Pei ^b   Wang, Cheng ^c,d   Ahmad, Sarah ^b   Vu, Michael ^b   Kuma, Krishneel ^b   Cheng, Yi Qiang ^c   Lam, Kit S ^b  

^a SICHUAN UNIVERSITY   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^d Cambridge Major Laboratories Inc   (United States)

Author keywords

Breast cancer; Disulfide cross linked micelle; HDAC inhibitor; Targeted delivery; Thailandepsin A

Indexed keywords

CELL DEATH; CELL PROLIFERATION; DRUG PRODUCTS; MICELLES; PARTICLE SIZE; SULFUR COMPOUNDS;

BREAST CANCER; CROSS-LINKED MICELLES; HDAC INHIBITORS; TARGETED DELIVERY; THAILANDEPSIN A;

DISEASES;

ANTINEOPLASTIC AGENT; BORTEZOMIB; CASPASE 3; DISULFIDE; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; ROMIDEPSIN; THAILANDEPSIN A; UNCLASSIFIED DRUG; CROSS LINKING REAGENT; DEPSIPEPTIDE; HISTONE; MICELLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER INHIBITION; CELL CYCLE ARREST; CONTROLLED STUDY; CROSS LINKING; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG FORMULATION; DRUG POTENTIATION; DRUG SOLUBILITY; DRUG STABILITY; DRUG TOLERABILITY; DRUG UPTAKE; ENCAPSULATION; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MICELLE; MOUSE; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SINGLE DRUG DOSE; SUSTAINED DRUG RELEASE; TUMOR XENOGRAFT; ACETYLATION; ANIMAL; BREAST NEOPLASMS; CELL CYCLE; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; ENDOCYTOSIS; METABOLISM; MITOCHONDRION; NUDE MOUSE; PATHOLOGY; TISSUE DISTRIBUTION; TUMOR CELL LINE;

ACETYLATION; ANIMALS; APOPTOSIS; BORTEZOMIB; BREAST NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CROSS-LINKING REAGENTS; DEPSIPEPTIDES; DISULFIDES; ENDOCYTOSIS; FEMALE; HISTONE DEACETYLASE INHIBITORS; HISTONES; HUMANS; MICE, NUDE; MICELLES; MITOCHONDRIA; PARTICLE SIZE; REACTIVE OXYGEN SPECIES; TISSUE DISTRIBUTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84939640778     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.07.033     Document Type: Article

References (48)

1. Jemal A., Center M.M., DeSantis C., Ward E.M. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol. Biomarkers Prev. 2010 Aug, 19(8):1893-1907.
2. Ozdag H., Teschendorff A.E., Ahmed A.A., Hyland S.J., Blenkiron C., Bobrow L., et al. Differential expression of selected histone modifier genes in human solid cancers. BMC Genomics 2006, 7:90.
3. Weichert W., Roske A., Niesporek S., Noske A., Buckendahl A.C., Dietel M., et al. Class I histone deacetylase expression has independent prognostic impact in human colorectal cancer: specific role of class I histone deacetylases in vitro and in vivo. Clin. Cancer Res. 2008 Mar 15, 14(6):1669-1677.
4. Krusche C.A., Wulfing P., Kersting C., Vloet A., Bocker W., Kiesel L., et al. Histone deacetylase-1 and -3 protein expression in human breast cancer: a tissue microarray analysis. Breast Cancer Res. Treat. 2005 Mar, 90(1):15-23.
5. Weichert W., Roske A., Gekeler V., Beckers T., Stephan C., Jung K., et al. Histone deacetylases 1, 2 and 3 are highly expressed in prostate cancer and HDAC2 expression is associated with shorter PSA relapse time after radical prostatectomy. Br. J. Cancer 2008 Feb 12, 98(3):604-610.
6. Minamiya Y., Ono T., Saito H., Takahashi N., Ito M., Mitsui M., et al. Expression of histone deacetylase 1 correlates with a poor prognosis in patients with adenocarcinoma of the lung. Lung Cancer 2011 Nov, 74(2):300-304.
7. Rikimaru T., Taketomi A., Yamashita Y., Shirabe K., Hamatsu T., Shimada M., et al. Clinical significance of histone deacetylase 1 expression in patients with hepatocellular carcinoma. Oncology 2007, 72(1-2):69-74.
8. Weichert W., Roske A., Gekeler V., Beckers T., Ebert M.P., Pross M., et al. Association of patterns of class I histone deacetylase expression with patient prognosis in gastric cancer: a retrospective analysis. Lancet Oncol. 2008 Feb, 9(2):139-148.
9. Duvic M., Talpur R., Ni X., Zhang C., Hazarika P., Kelly C., et al. Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood 2007 Jan 1, 109(1):31-39.
10. Lee H.Z., Kwitkowski V.E., Del Valle P.L., Ricci M.S., Saber H., Habtemariam B.A., et al. FDA approval: belinostat for the treatment of patients with relapsed or refractory peripheral T-cell lymphoma. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2015 Jun 15, 21(12):2666-2670.
11. VanderMolen K.M., McCulloch W., Pearce C.J., Oberlies N.H. Romidepsin (Istodax, NSC 630176, FR901228, FK228, depsipeptide): a natural product recently approved for cutaneous T-cell lymphoma. J. Antibiot. 2011 Aug, 64(8):525-531.
12. Wang C., Henkes L.M., Doughty L.B., He M., Wang D., Meyer-Almes F.J., et al. Thailandepsins: bacterial products with potent histone deacetylase inhibitory activities and broad-spectrum antiproliferative activities. J. Nat. Prod. 2011 Oct 28, 74(10):2031-2038.
13. Wilson A.J., Cheng Y.Q., Khabele D. Thailandepsins are new small molecule class I HDAC inhibitors with potent cytotoxic activity in ovarian cancer cells: a preclinical study of epigenetic ovarian cancer therapy. J. Ovarian Res. 2012, 5(1):12.
14. Weinlander E., Somnay Y., Harrison A.D., Wang C., Cheng Y.Q., Jaskula-Sztul R., et al. The novel histone deacetylase inhibitor thailandepsin A inhibits anaplastic thyroid cancer growth. J. Surg. Res. 2014 Jul, 190(1):191-197.
15. Li Y., Xiao K., Luo J., Xiao W., Lee J.S., Gonik A.M., et al. Well-defined, reversible disulfide cross-linked micelles for on-demand paclitaxel delivery. Biomaterials 2011 Sep, 32(27):6633-6645.
16. Matsumura Y., Maeda H. A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res. 1986 Dec, 46(12 Pt 1):6387-6392.
17. Orlowski R.Z., Kuhn D.J. Proteasome inhibitors in cancer therapy: lessons from the first decade. Clin. Cancer Res. 2008 Mar 15, 14(6):1649-1657.
18. Voorhees P.M., Orlowski R.Z. The proteasome and proteasome inhibitors in cancer therapy. Annu. Rev. Pharmacol. Toxicol. 2006, 46:189-213.
19. Cardoso F., Ross J.S., Picart M.J., Sotiriou C., Durbecq V. Targeting the ubiquitin-proteasome pathway in breast cancer. Clin. Breast Cancer 2004 Jun, 5(2):148-157.
20. Codony-Servat J., Tapia M.A., Bosch M., Oliva C., Domingo-Domenech J., Mellado B., et al. Differential cellular and molecular effects of bortezomib, a proteasome inhibitor, in human breast cancer cells. Mol. Cancer Ther. 2006 Mar, 5(3):665-675.
21. Yang C.H., Gonzalez-Angulo A.M., Reuben J.M., Booser D.J., Pusztai L., Krishnamurthy S., et al. Bortezomib (VELCADE) in metastatic breast cancer: pharmacodynamics, biological effects, and prediction of clinical benefits. Ann. Oncol. 2006 May, 17(5):813-817.
22. Irvin W.J., Orlowski R.Z., Chiu W.K., Carey L.A., Collichio F.A., Bernard P.S., et al. Phase II study of bortezomib and pegylated liposomal doxorubicin in the treatment of metastatic breast cancer. Clin. Breast Cancer 2010 Dec 1, 10(6):465-470.
23. Schmid P., Kuhnhardt D., Kiewe P., Lehenbauer-Dehm S., Schippinger W., Greil R., et al. A phase I/II study of bortezomib and capecitabine in patients with metastatic breast cancer previously treated with taxanes and/or anthracyclines. Ann. Oncol. 2008 May, 19(5):871-876.
24. Awada A., Albanell J., Canney P.A., Dirix L.Y., Gil T., Cardoso F., et al. Bortezomib/docetaxel combination therapy in patients with anthracycline-pretreated advanced/metastatic breast cancer: a phase I/II dose-escalation study. Br. J. Cancer 2008 May 6, 98(9):1500-1507.
25. Wesener S.R., Potharla V.Y., Cheng Y.Q. Reconstitution of the FK228 biosynthetic pathway reveals cross talk between modular polyketide synthases and fatty acid synthase. Appl. Environ. Microbiol. 2011 Feb, 77(4):1501-1507.
26. Xiao K., Luo J., Li Y., Lee J.S., Fung G., Lam K.S. PEG-oligocholic acid telodendrimer micelles for the targeted delivery of doxorubicin to B-cell lymphoma. J. Control Release 2011 Oct 30, 155(2):272-281.
27. Dasmahapatra G., Lembersky D., Kramer L., Fisher R.I., Friedberg J., Dent P., et al. The pan-HDAC inhibitor vorinostat potentiates the activity of the proteasome inhibitor carfilzomib in human DLBCL cells in vitro and in vivo. Blood 2010 Jun 3, 115(22):4478-4487.
28. Xiao K., Luo J., Fowler W.L., Li Y., Lee J.S., Xing L., et al. A self-assembling nanoparticle for paclitaxel delivery in ovarian cancer. Biomaterials 2009 Oct, 30(30):6006-6016.
29. Koo A.N., Lee H.J., Kim S.E., Chang J.H., Park C., Kim C., et al. Disulfide-cross-linked PEG-poly(amino acid)s copolymer micelles for glutathione-mediated intracellular drug delivery. Chem. Commun. (Camb) 2008 Dec, 28(48):6570-6572.
30. Nishida K., Komiyama T., Miyazawa S., Shen Z.N., Furumatsu T., Doi H., et al. Histone deacetylase inhibitor suppression of autoantibody-mediated arthritis in mice via regulation of p16INK4a and p21(WAF1/Cip1) expression. Arthritis Rheum. 2004 Oct, 50(10):3365-3376.
31. Fang X., Yu S., Eder A., Mao M., Bast R.C., Boyd D., et al. Regulation of BAD phosphorylation at serine 112 by the Ras-mitogen-activated protein kinase pathway. Oncogene 1999 Nov 18, 18(48):6635-6640.
32. Datta S.R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y., et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997 Oct 17, 91(2):231-241.
33. Harada H., Becknell B., Wilm M., Mann M., Huang L.J., Taylor S.S., et al. Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol. Cell 1999 Apr, 3(4):413-422.
34. del Peso L., Gonzalez-Garcia M., Page C., Herrera R., Nunez G. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 1997 Oct 24, 278(5338):687-689.
35. Li Y.L., Zhu L., Liu Z., Cheng R., Meng F., Cui J.H., et al. Reversibly stabilized multifunctional dextran nanoparticles efficiently deliver doxorubicin into the nuclei of cancer cells. Angew. Chem. Int. Ed. Engl. 2009, 48(52):9914-9918.
36. Xiao K., Li Y., Lee J.S., Gonik A.M., Dong T., Fung G., et al. "OA02" peptide facilitates the precise targeting of paclitaxel-loaded micellar nanoparticles to ovarian cancer in vivo. Cancer Res. 2012 Apr 15, 72(8):2100-2110.
37. Zhang Z., Yamashita H., Toyama T., Sugiura H., Ando Y., Mita K., et al. Quantitation of HDAC1 mRNA expression in invasive carcinoma of the breast. Breast Cancer Res. Treat. 2005 Nov, 94(1):11-16.
38. Haberland M., Johnson A., Mokalled M.H., Montgomery R.L., Olson E.N. Genetic dissection of histone deacetylase requirement in tumor cells. Proc. Natl. Acad. Sci. U. S. A. 2009 May 12, 106(19):7751-7755.
39. Dickinson M., Johnstone R.W., Prince H.M. Histone deacetylase inhibitors: potential targets responsible for their anti-cancer effect. Invest. New Drugs 2010 Dec, 28(Suppl. 1):S3-S20.
40. Pyo C.W., Choi J.H., Oh S.M., Choi S.Y. Oxidative stress-induced cyclin D1 depletion and its role in cell cycle processing. Biochim. Biophys. Acta 2013 Nov, 1830(11):5316-5325.
41. Petruccelli L.A., Dupere-Richer D., Pettersson F., Retrouvey H., Skoulikas S., Miller W.H. Vorinostat induces reactive oxygen species and DNA damage in acute myeloid leukemia cells. PLoS One 2011, 6(6):e20987.
42. Liu F., Yu G., Wang G., Liu H., Wu X., Wang Q., et al. An NQO1-initiated and p53-independent apoptotic pathway determines the anti-tumor effect of tanshinone IIA against non-small cell lung cancer. PLoS One 2012, 7(7):e42138.
43. Li Y., Xiao K., Zhu W., Deng W., Lam K.S. Stimuli-responsive cross-linked micelles for on-demand drug delivery against cancers. Adv. Drug Deliv. Rev. 2013 Feb, 66:58-73.
44. Kato J., Li Y., Xiao K., Lee J.S., Luo J., Tuscano J.M., et al. Disulfide cross-linked micelles for the targeted delivery of vincristine to B-cell lymphoma. Mol. Pharm. 2012 Jun 4, 9(6):1727-1735.
45. Xiao K., Li Y., Luo J., Lee J.S., Xiao W., Gonik A.M., et al. The effect of surface charge on in vivo biodistribution of PEG-oligocholic acid based micellar nanoparticles. Biomaterials 2011 May, 32(13):3435-3446.
46. Tseng L.M., Liu C.Y., Chang K.C., Chu P.Y., Shiau C.W., Chen K.F. CIP2A is a target of bortezomib in human triple negative breast cancer cells. Breast Cancer Res. 2012, 14(2):R68.
47. Feng R., Oton A., Mapara M.Y., Anderson G., Belani C., Lentzsch S. The histone deacetylase inhibitor, PXD101, potentiates bortezomib-induced anti-multiple myeloma effect by induction of oxidative stress and DNA damage. Br. J. Haematol. 2007 Nov, 139(3):385-397.
48. Bhalla S., Balasubramanian S., David K., Sirisawad M., Buggy J., Mauro L., et al. PCI-24781 induces caspase and reactive oxygen species-dependent apoptosis through NF-kappaB mechanisms and is synergistic with bortezomib in lymphoma cells. Clin. Cancer Res. 2009 May 15, 15(10):3354-3365.