Hypocrellin B triggered sonodynamic therapy reverses multidrug resistance of doxorubicin-resistant SGC7901/ADR cells via down-regulation of P-gp expression

References

• Siegel RL, Miller KD, Jemal A. Cancer Statistics, 2018. CA Cancer J Clin. 2018;68(1):7–30.
   PubMed Web of Science ®Google Scholar
• Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424.
   PubMed Web of Science ®Google Scholar
• Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer. 2002;2(1):48–58.
   PubMed Web of Science ®Google Scholar
• Bart J, Hollema H, Groen HJM, de Vries EGE, Hendrikse NH, Sleijfer DT, et al. The distribution of drug-efflux pumps, P-gp, BCRP, MRP1 and MRP2, in the normal blood-testis barrier and in primary testicular tumours. Eur J Cancer. 2004;40(14):2064–70.
   PubMed Web of Science ®Google Scholar
• Schrader AJ, Seger M, Konrad L, Olbert P, Hegele A, Hofmann R, et al. Clinical impact of MDR1-expression in testicular germ cell cancer. Exp Oncol. 2007;29(3):212–6.
   PubMedGoogle Scholar
• Kimura Y, Matsuo M, Takahashi K, Saeki T, Kioka N, Amachi T, et al. ATP hydrolysis-dependent multidrug efflux transporter: MDR1/P-glycoprotein. Curr Drug Metab. 2004;5(1):1–10.
   PubMed Web of Science ®Google Scholar
• Sivapackiam J, Harpstrite SE, Prior JL, Gu H, Rath NP, Sharma V. Synthesis, molecular structure, and validation of metalloprobes for assessment of MDR1 P-glycoprotein-mediated functional transport. Dalton Trans. 2010;39(25):5842–50.
   PubMed Web of Science ®Google Scholar
• Wang F, Zhang D, Zhang Q, Chen Y, Zheng D, Hao L, et al. Synergistic effect of folate-mediated targeting and verapamil-mediated P-gp inhibition with paclitaxel -polymer micelles to overcome multi-drug resistance . Biomaterials. 2011;32(35):9444–56.
   PubMed Web of Science ®Google Scholar
• Meng H, Mai WX, Zhang H, Xue M, Xia T, Lin S, et al. Codelivery of an optimal drug/siRNA combination using mesoporous silica nanoparticles to overcome drug resistance in breast cancer in vitro and in vivo. ACS Nano. 2013;7(2):994–1005.
   PubMed Web of Science ®Google Scholar
• Wang L, Lin X, Wang J, Hu Z, Ji Y, Hou S, et al. Cancer treatment: Novel insights into combating cancer chemotherapy resistance using a plasmonic nanocarrier: enhancing drug sensitiveness and accumulation simultaneously with localized mild photothermal stimulus of femtosecond pulsed laser. Adv Funct Mater. 2014;24(27):4229–39.
   Web of Science ®Google Scholar
• Yu H, Xu Z, Chen X, Xu L, Yin Q, Zhang Z, et al. Reversal of lung cancer multidrug resistance by pH-responsive micelleplexes mediating co-delivery of siRNA and paclitaxel. Macromol Biosci. 2014;14(1):100–9.
   PubMed Web of Science ®Google Scholar
• Gao Y, Chen Y, Ji X, He X, Yin Q, Zhang Z, et al. Controlled intracellular release of doxorubicin in multidrug-resistant cancer cells by tuning the shell-pore sizes of mesoporous silica nanoparticles. ACS Nano. 2011;5(12):9788–98.
   PubMed Web of Science ®Google Scholar
• Huang Y, Fan CQ, Dong H, Wang SM, Yang XC, Yang SM. Current applications and future prospects of nanomaterials in tumor therapy. Int J Nanomedicine. 2017;12:1815–25.
   PubMed Web of Science ®Google Scholar
• Qi W, Yan J, Sun H, Wang H. Nanocomposite plasters for the treatment of superficial tumors by chemo-photothermal combination therapy. Int J Nanomedicine. 2018;13:6235–47.
   PubMed Web of Science ®Google Scholar
• Akerfelt M, Morimoto RI, Sistonen L. Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol. 2010;11(8):545–55.
   PubMed Web of Science ®Google Scholar
• Shi J, Su Y, Liu W, Chang JB, Zhang ZZ. A nanoliposome-based photoactivable drug delivery system for enhanced cancer therapy and overcoming treatment resistance. Int J Nanomedicine. 2017;12:8257–75.
   PubMed Web of Science ®Google Scholar
• Yue W, Chen L, Yu L, Zhou B, Yin H, Ren W, et al. Checkpoint blockade and nanosonosensitizer-augmented noninvasive sonodynamic therapy combination reduces tumour growth and metastases in mice. Nat Commun. 2019;10(1):2025
   PubMedGoogle Scholar
• Wang L, Sun Q, Wang X, Wen T, Yin J-J, Wang P, et al. Using hollow carbon nanospheres as a light-induced free radical generator to overcome chemotherapy resistance. J Am Chem Soc. 2015;137(5):1947–55.
   PubMed Web of Science ®Google Scholar
• Zhang K, Li H‐Y, Lang J‐Y, Li X‐T, Yue W‐W, Yin Y‐F, et al. Quantum yield-engineered biocompatible probes illuminate lung tumor based on viscosity confinement-mediated antiaggregation. Adv Funct Mater. 2019;29(44):1905124.
   Web of Science ®Google Scholar
• Zhang K, Fang Y, He Y, Yin H, Guan X, Pu Y, et al. Extravascular gelation shrinkage-derived internal stress enables tumor starvation therapy with suppressed metastasis and recurrence. Nat Commun. 2019;10(1):5380
   PubMedGoogle Scholar
• Liu Y, Wan G, Guo H, Liu Y, Zhou P, Wang H, et al. A multifunctional nanoparticle system combines sonodynamic therapy and chemotherapy to treat hepatocellular carcinoma. Nano Res. 2017;10(3):834–55.
   Web of Science ®Google Scholar
• Liu Y, Bai L, Guo K, Jia Y, Zhang K, Liu Q, et al. Focused ultrasound-augmented targeting delivery of nanosonosensitizers from homogenous exosomes for enhanced sonodynamic cancer therapy. Theranostics. 2019;9(18):5261–81.
   PubMed Web of Science ®Google Scholar
• Yang Z, Cheng R, Zhao C, Sun N, Luo H, Chen Y, et al. Thermo- and pH-dual responsive polymeric micelles with upper critical solution temperature behavior for photoacoustic imaging-guided synergistic chemo-photothermal therapy against subcutaneous and metastatic breast tumors . Theranostics. 2018;8(15):4097–115.
   PubMed Web of Science ®Google Scholar
• Qian X, Zheng Y, Chen Y. Micro/Nanoparticle-augmented sonodynamic therapy (SDT): breaking the depth shallow of photoactivation. Adv Mater Weinheim. 2016;28(37):8097–129.
   PubMed Web of Science ®Google Scholar
• Mchale AP, Callan JF, Nomikou N, Fowley C, Callan B. Sonodynamic therapy: concept, mechanism and application to cancer treatment. Adv Exp Med Biol. 2016;880:429–50.
   PubMed Web of Science ®Google Scholar
• Li Y, An H, Wang X, Wang P, Qu F, Jiao Y, et al. Ultrasound-triggered release of sinoporphyrin sodium from liposome-microbubble complexes and its enhanced sonodynamic toxicity in breast cancer. Nano Res. 2018;11(2):1038–56.
   Web of Science ®Google Scholar
• Chen J, Luo H, Liu Y, Zhang W, Li H, Luo T, et al. Oxygen-self-produced nanoplatform for relieving hypoxia and breaking resistance to sonodynamic treatment of pancreatic cancer. ACS Nano. 2017;11(12):12849–62.
   PubMed Web of Science ®Google Scholar
• Huang C, Huang S, Li H, Li X, Li B, Zhong L, et al. The effects of ultrasound exposure on P-glycoprotein-mediated multidrug resistance in vitro and in vivo. J Exp Clin Cancer Res. 2018;37(1):232
   PubMedGoogle Scholar
• Jia Y, Yuan W, Zhang K, Wang J, Wang P, Liu Q, Wang X. Comparison of cell membrane damage induced by the therapeutic ultrasound on human breast cancer MCF-7 and MCF-7/ADR cells. Ultrason Sonochem. 2015;26:128–35.
   PubMed Web of Science ®Google Scholar
• Zheng X, Ge J, Wu J, Liu W, Guo L, Jia Q, et al. Biodegradable hypocrellin derivative nanovesicle as a near-infrared light-driven theranostic for dually photoactive cancer imaging and therapy. Biomaterials. 2018;185:133–41.
   PubMed Web of Science ®Google Scholar
• Qin C, Fei J, Wang A, Yang Y, Li J. Rational assembly of a biointerfaced core@shell nanocomplex towards selective and highly efficient synergistic photothermal/photodynamic therapy. Nanoscale. 2015;7(47):20197–210.
   PubMed Web of Science ®Google Scholar
• Deng H, Liu X, Xie J, Yin R, Huang N, Gu Y, Zhao J. Quantitative and site-directed chemical modification of hypocrellins toward direct drug delivery and effective photodynamic activity. J Med Chem. 2012;55(5):1910–9.
   PubMed Web of Science ®Google Scholar
• Wang P, Xu CS, Xu J, Wang X, Leung AW. Hypocrellin B enhances ultrasound-induced cell death of nasopharyngeal carcinoma cells. Ultrasound Med Biol. 2010;36(2):336–42.
   PubMed Web of Science ®Google Scholar
• Wang X, Leung AW, Jiang Y, Jiang Y, Yu H, Li X. Hypocrellin B-mediated sonodynamic action induces apoptosis of hepatocellular carcinoma cells. Ultrasonics. 2012;52(4):543–6.
   PubMed Web of Science ®Google Scholar
• Liu Y, Bai H, Wang H, Wang X, Liu Q, Zhang K, et al. Comparison of hypocrellin B-mediated sonodynamic responsiveness between sensitive and multidrug-resistant human gastric cancer cell lines . J Med Ultrason (2001)). 2019;46(1):15–26.
   PubMed Web of Science ®Google Scholar
• Liu Y, Wang P, Liu Q, Wang X. Sinoporphyrin sodium triggered sono-photodynamic effects on breast cancer both in vitro and in vivo. Ultrason Sonochem. 2016;31:437–48.
   PubMed Web of Science ®Google Scholar
• Li Y, Wang P, Wang X, Su X, Liu Q. Involvement of mitochondrial and reactive oxygen species in the sonodynamic toxicity of chlorin e6 in human leukemia K562 cells. Ultrasound Med Biol. 2014;40(5):990–1000.
   PubMed Web of Science ®Google Scholar
• Guertin AD, O'Neil J, Stoeck A, Reddy JA, Cristescu R, Haines BB, et al. High levels of expression of P-glycoprotein/multidrug resistance protein result in resistance to vintafolide . Mol Cancer Ther. 2016;15(8):1998–2008.
   PubMed Web of Science ®Google Scholar
• Alfarouk KO, Stock C-M, Taylor S, Walsh M, Muddathir AK, Verduzco D, et al. Resistance to cancer chemotherapy: failure in drug response from ADME to P-gp. Cancer Cell Int. 2015;15:71
   PubMed Web of Science ®Google Scholar
• Silva R, Vilas-Boas V, Carmo H, Dinis-Oliveira RJ, Carvalho F, de Lourdes Bastos M, et al. Modulation of P-glycoprotein efflux pump: induction and activation as a therapeutic strategy. Pharmacol Ther. 2015;149:1–123.
   PubMed Web of Science ®Google Scholar
• Marcoux J, Wang SC, Politis A, Reading E, Ma J, Biggin PC, et al. Mass spectrometry reveals synergistic effects of nucleotides, lipids, and drugs binding to a multidrug resistance efflux pump. Proc Natl Acad Sci Usa. 2013;110(24):9704–9.
   PubMed Web of Science ®Google Scholar
• Abdallah HM, Al-Abd AM, El-Dine RS, El-Halawany AM. P-glycoprotein inhibitors of natural origin as potential tumor chemo-sensitizers: A review. J Adv Res. 2015;6(1):45–62.
   PubMed Web of Science ®Google Scholar
• Fu L, Liang Y, Deng L, Ding Y, Chen L, Ye Y, et al. Characterization of tetrandrine, a potent inhibitor of P-glycoprotein-mediated multidrug resistance. Cancer Chemother Pharmacol. 2004;53(4):349–56.
   PubMed Web of Science ®Google Scholar
• Tian W, Deng Y, Li L, He H, Sun J, Xu D. Honokiol synergizes chemotherapy drugs in multidrug resistant breast cancer cells via enhanced apoptosis and additional programmed necrotic death. Int J Oncol. 2013;42(2):721–32.
   PubMed Web of Science ®Google Scholar
• Singh MS, Lamprecht A. Cargoing P-gp inhibitors via nanoparticle sensitizes tumor cells against doxorubicin. Int J Pharm. 2015;478(2):745–52.
   PubMedGoogle Scholar
• Cho H, Lee H-Y, Han M, Choi J-R, Ahn S, Lee T, et al. Localized Down-regulation of P-glycoprotein by focused ultrasound and microbubbles induced blood-brain barrier disruption in rat brain. Sci Rep. 2016;6:31201
   PubMed Web of Science ®Google Scholar
• Yang S, Wang P, Wang X, Zhang K, Zhang X, Liu Q. Efficacy of combined therapy with paclitaxel and low-level ultrasound in human chronic myelogenous leukemia cell line K562. J Drug Targeting. 2013;21(9):874–84.
   PubMed Web of Science ®Google Scholar
• Ruiz-Ramos R, Lopez-Carrillo L, Rios-Perez AD, De Vizcaya-Ruiz A, Cebrain ME. Sodium arsenite induces ROS generation, DNA oxidative damage, HO-1 and c-Myc proteins, NF-kappaB activation and cell proliferation in human breast cancer MCF-7 cells. Mutat Res. 2009;674(1-2):109–15.
   PubMed Web of Science ®Google Scholar
• Galluzzi L, Larochette N, Zamzami N, Kroemer G. Mitochondria as therapeutic targets for cancer chemotherapy. Oncogene. 2006;25(34):4812–30.
   PubMed Web of Science ®Google Scholar
• Wang H, Wang X, Zhang S, Wang P, Zhang K, Liu Q. Sinoporphyrin sodium, a novel sensitizer, triggers mitochondrial-dependent apoptosis in ECA-109 cells via production of reactive oxygen species. Int J Nanomedicine. 2014;9:3077–90.
   PubMed Web of Science ®Google Scholar
• Maya BZ, Assaraf YG, Livney YD. β-casein nanovehicles for oral delivery of chemotherapeutic drug combinations overcoming P-glycoprotein-mediated multidrug resistance in human gastric cancer cells. Oncotarget. 2016;7(17):23322–34.
   PubMedGoogle Scholar