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Photothermal Therapy Mediated Hybrid Membrane Derived Nano-formulation for Enhanced Cancer Therapy

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Abstract

Emodin is applied as an antitumor drug in many tumor therapies. However, its pharmacology performances are limited due to its low solubility. Herein, we fused erythrocyte and macrophage to form a hybrid membrane (EMHM) and encapsulated emodin to form hybrid membrane-coated nanoparticles. We employed glycyrrhizin to increase the solubility of emodin first and prepared the hybrid membrane nanoparticle-coated emodin and glycyrrhizin (EG@EMHM NPs) which exhibited an average particle size of 170 ± 20 nm and encapsulation efficiency of 98.13 ± 0.67%. The half-inhibitory concentrations (IC50) of EG@EMHM NPs were 1.166 μg/mL, which is half of the free emodin. Based on the photosensitivity of emodin, the reactive oxygen species (ROS) results disclosed that ROS levels of the photodynamic therapy (PDT) section were higher than the normal section (P < 0.05). Compared to the normal section, PDT-mediated EG@EMHM NPs could induce an early stage of apoptosis of B16. The western blot and flow cytometry results verified that PDT-mediated EG@EMHM NPs can significantly improve the solubility of emodin and perform a remarkably antitumor effect on melanoma via BAX and BCL-2 pathway. The application of the combined chemical and PDT therapy could provide an improving target therapy for cutaneous melanoma and also may offer an idea for other insoluble components sources of traditional Chinese medicine.

Graphical abstract

Schematic of EG@EMHM NPs formulation

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References

  1. Chen YK, Xu YK, Zhang H, Yin JT, Fan X, Liu DD, et al. Emodin alleviates jejunum injury in rats with sepsis by inhibiting inflammation response. Biomed Pharm Biomed Pharmacotherapie. 2016;84:1001–7. https://doi.org/10.1016/j.biopha.2016.10.031.

    Article  CAS  Google Scholar 

  2. Gu J, Cui CF, Yang L, Wang L, Jiang XH. Emodin inhibits colon cancer cell invasion and migration by suppressing epithelial-mesenchymal transition via the Wnt/β-catenin pathway. Oncol Res. 2019;27(2):193–202. https://doi.org/10.3727/096504018x15150662230295.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Cha TL, Qiu L, Chen CT, Wen Y, Hung MC. Emodin down-regulates androgen receptor and inhibits prostate cancer cell growth. Cancer Res. 2005;65(6):2287–95. https://doi.org/10.1158/0008-5472.Can-04-3250.

    Article  CAS  PubMed  Google Scholar 

  4. Ma W, Liu F, Yuan L, Zhao C, Chen C. Emodin and AZT synergistically inhibit the proliferation and induce the apoptosis of leukemia K562 cells through the EGR1 and the Wnt/β-catenin pathway. Oncol Rep. 2020;43(1):260–9. https://doi.org/10.3892/or.2019.7408.

    Article  CAS  PubMed  Google Scholar 

  5. Chen S, Zhang Z, Zhang J. Emodin enhances antitumor effect of paclitaxel on human non-small-cell lung cancer cells in vitro and in vivo. Drug Des Dev Ther. 2019;13:1145–53. https://doi.org/10.2147/dddt.S196319.

    Article  CAS  Google Scholar 

  6. Zu C, Qin G, Yang C, Liu N, He A, Zhang M, et al. Low dose emodin induces tumor senescence for boosting breast cancer chemotherapy via silencing NRARP. Biochem Biophys Res Commun. 2018;505(4):973–8. https://doi.org/10.1016/j.bbrc.2018.09.045.

    Article  CAS  PubMed  Google Scholar 

  7. Hwang SY, Heo K, Kim JS, Im JW, Lee SM, Cho M, et al. Emodin attenuates radioresistance induced by hypoxia in HepG2 cells via the enhancement of PARP1 cleavage and inhibition of JMJD2B. Oncol Rep. 2015;33(4):1691–8. https://doi.org/10.3892/or.2015.3744.

    Article  CAS  PubMed  Google Scholar 

  8. Ma W, Zhang M, Cui Z, Wang X, Niu X, Zhu Y, et al. Aloe-emodin-mediated antimicrobial photodynamic therapy against dermatophytosis caused by Trichophyton rubrum. Microb Biotechnol. 2022;15(2):499–512. https://doi.org/10.1111/1751-7915.13875.

    Article  CAS  PubMed  Google Scholar 

  9. Yuan Z, Fan G, Wu H, Liu C, Zhan Y, Qiu Y, et al. Photodynamic therapy synergizes with PD-L1 checkpoint blockade for immunotherapy of CRC by multifunctional nanoparticles. Mol Ther J Am Soc Gene Ther. 2021;29(10):2931–48. https://doi.org/10.1016/j.ymthe.2021.05.017.

    Article  CAS  Google Scholar 

  10. Jia S, Wang S, Li S, Hu P, Yu S, Shi J, et al. Specific modification and self-transport of porphyrins and their multi-mechanism cooperative antitumor studies. J Mater Chem B. 2021;9(14):3180–91. https://doi.org/10.1039/d0tb02847a.

    Article  CAS  PubMed  Google Scholar 

  11. Jin F, Qi J, Liu D, You Y, Shu G, Du Y, et al. Cancer-cell-biomimetic upconversion nanoparticles combining chemo-photodynamic therapy and CD73 blockade for metastatic triple-negative breast cancer. J Controlled Release Official J Controlled Release Soc. 2021;337:90–104. https://doi.org/10.1016/j.jconrel.2021.07.021.

    Article  CAS  Google Scholar 

  12. Sajjad F, Liu XY, Yan YJ, Zhou XP, Chen ZL. The photodynamic anti-tumor effects of new PPa-CDs conjugate with pH sensitivity and improved biocompatibility. Anti-Cancer Agents Med Chem. 2022;22(7):1286–95. https://doi.org/10.2174/1871520621666210513162457.

    Article  CAS  Google Scholar 

  13. Wu W, Shi L, Duan Y, Xu S, Shen L, Zhu T, et al. Nanobody modified high-performance AIE photosensitizer nanoparticles for precise photodynamic oral cancer therapy of patient-derived tumor xenograft. Biomater. 2021;274:120870. https://doi.org/10.1016/j.biomaterials.2021.120870.

    Article  CAS  Google Scholar 

  14. Davidson S, Coles M, Thomas T, Kollias G, Ludewig B, Turley S, et al. Fibroblasts as immune regulators in infection, inflammation and cancer. Nat Rev Immun. 2021;21(11):704–17. https://doi.org/10.1038/s41577-021-00540-z.

    Article  CAS  Google Scholar 

  15. Xie M, Xu Y, Shen H, Shen S, Ge Y, Xie J. Negative-charge-functionalized mesoporous silica nanoparticles as drug vehicles targeting hepatocellular carcinoma. Int J Pharm. 2014;474(1-2):223–31. https://doi.org/10.1016/j.ijpharm.2014.08.027.

    Article  CAS  PubMed  Google Scholar 

  16. Rui M, Xin Y, Li R, Ge Y, Feng C, Xu X. Targeted biomimetic nanoparticles for synergistic combination chemotherapy of paclitaxel and doxorubicin. Mol Pharm. 2017;14(1):107–23. https://doi.org/10.1021/acs.molpharmaceut.6b00732.

    Article  CAS  PubMed  Google Scholar 

  17. Liu S, Li W, Dong S, Zhang F, Dong Y, Tian B, et al. An all-in-one theranostic nanoplatform based on upconversion dendritic mesoporous silica nanocomposites for synergistic chemodynamic/photodynamic/gas therapy. Nanoscale. 2020;12(47):24146–61. https://doi.org/10.1039/d0nr06790c.

    Article  CAS  PubMed  Google Scholar 

  18. Zhang HY, Firempong CK, Wang YW, Xu WQ, Wang MM, Cao X, et al. Ergosterol-loaded poly(lactide-co-glycolide) nanoparticles with enhanced in vitro antitumor activity and oral bioavailability. Acta Pharm Sin. 2016;37(6):834–44. https://doi.org/10.1038/aps.2016.37.

    Article  CAS  Google Scholar 

  19. Cao X, Deng W, Wei Y, Su W, Yang Y, Wei Y, et al. Encapsulation of plasmid DNA in calcium phosphate nanoparticles: stem cell uptake and gene transfer efficiency. Int J Nanomed. 2011;6:3335–49. https://doi.org/10.2147/ijn.S27370.

    Article  CAS  Google Scholar 

  20. Wang D, Dong H, Li M, Cao Y, Yang F, Zhang K, et al. Erythrocyte-cancer hybrid membrane camouflaged hollow copper sulfide nanoparticles for prolonged circulation life and homotypic-targeting photothermal/chemotherapy of melanoma. ACS Nano. 2018;12(6):5241–52. https://doi.org/10.1021/acsnano.7b08355.

    Article  CAS  PubMed  Google Scholar 

  21. Fang RH, Hu CM, Chen KN, Luk BT, Carpenter CW, Gao W, et al. Lipid-insertion enables targeting functionalization of erythrocyte membrane-cloaked nanoparticles. Nanoscale. 2013;5(19):8884-8. https://doi.org/10.1039/c3nr03064d.

  22. Fang RH, Kroll AV, Gao W, Zhang L. Cell membrane coating nanotechnology. Advanced materials (Deerfield Beach, Fla). 2018;30(23):e1706759. https://doi.org/10.1002/adma.201706759.

    Article  CAS  PubMed  Google Scholar 

  23. Hu CM, Zhang L, Aryal S, Cheung C, Fang RH, Zhang L. Erythrocyte membrane-camouflaged polymeric nanoparticles as a biomimetic delivery platform. Proceed National Acad Sci Unit States Am. 2011;108(27):10980–5. https://doi.org/10.1073/pnas.1106634108.

    Article  Google Scholar 

  24. Madsen SJ, Christie C, Hong SJ, Trinidad A, Peng Q, Uzal FA, et al. Nanoparticle-loaded macrophage-mediated photothermal therapy: potential for glioma treatment. Lasers Med Sci. 2015;30(4):1357–65. https://doi.org/10.1007/s10103-015-1742-5.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Gao C, Huang Q, Liu C, Kwong CHT, Yue L, Wan JB, et al. Treatment of atherosclerosis by macrophage-biomimetic nanoparticles via targeted pharmacotherapy and sequestration of proinflammatory cytokines. Nat Commun. 2020;11(1):2622. https://doi.org/10.1038/s41467-020-16439-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Oldenborg PA, Zheleznyak A, Fang YF, Lagenaur CF, Gresham HD, Lindberg FP. Role of CD47 as a marker of self on red blood cells. Sci (New York, NY). 2000;288(5473):2051–4. https://doi.org/10.1126/science.288.5473.2051.

    Article  CAS  Google Scholar 

  27. Jiang Q, Liu Y, Guo R, Yao X, Sung S, Pang Z, et al. Erythrocyte-cancer hybrid membrane-camouflaged melanin nanoparticles for enhancing photothermal therapy efficacy in tumors. Biomater. 2019;192:292–308. https://doi.org/10.1016/j.biomaterials.2018.11.021.

    Article  CAS  Google Scholar 

  28. Xuan M, Shao J, Dai L, Li J, He Q. Macrophage cell membrane camouflaged Au nanoshells for in vivo prolonged circulation life and enhanced cancer photothermal therapy. ACS Appl Mater Interfaces. 2016;8(15):9610–8. https://doi.org/10.1021/acsami.6b00853.

    Article  CAS  PubMed  Google Scholar 

  29. Li R, He Y, Zhu Y, Jiang L, Zhang S, Qin J, et al. Route to rheumatoid arthritis by macrophage-derived microvesicle-coated nanoparticles. Nano Lett. 2019;19(1):124–34. https://doi.org/10.1021/acs.nanolett.8b03439.

    Article  CAS  PubMed  Google Scholar 

  30. Gong C, Yu X, You B, Wu Y, Wang R, Han L, et al. Macrophage-cancer hybrid membrane-coated nanoparticles for targeting lung metastasis in breast cancer therapy. J Nanobiotechnol. 2020;18(1):92. https://doi.org/10.1186/s12951-020-00649-8.

    Article  CAS  Google Scholar 

  31. Tucker IM, Burley A, Petkova RE, Hosking SL, Penfold J, Thomas RK, et al. Adsorption and self-assembly properties of the plant based biosurfactant, glycyrrhizic acid. J Colloid Interface Sci. 2021;598:444–54. https://doi.org/10.1016/j.jcis.2021.03.101.

    Article  CAS  PubMed  Google Scholar 

  32. Wang L, Yang R, Yuan B, Liu Y, Liu C. The antiviral and antimicrobial activities of licorice, a widely-used Chinese herb. Acta Pharm Sin B. 2015;5(4):310–5. https://doi.org/10.1016/j.apsb.2015.05.005.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Shi W, Cao X, Liu Q, Zhu Q, Liu K, Deng T, et al. Hybrid membrane-derived nanoparticles for isoliquiritin enhanced glioma therapy. Pharmaceuticals (Basel, Switzerland). 2022;15(9). https://doi.org/10.3390/ph15091059.

  34. Yang Y, Zhang Y, Thakur A, Li R, Xu H, Wang Z, et al. One-pot synthesis and characterization of ovalbumin-conjugated gold nanoparticles: a comparative study of adjuvanticity against the physical mixture of ovalbumin and gold nanoparticles. Int J Pharm. 2019;571:118704. https://doi.org/10.1016/j.ijpharm.2019.118704.

    Article  CAS  PubMed  Google Scholar 

  35. Kim AV, Shelepova EA, Selyutina OY, Meteleva ES, Dushkin AV, Medvedev NN, et al. Glycyrrhizin-assisted transport of praziquantel anthelmintic drug through the lipid membrane: an experiment and MD simulation. Mol Pharm. 2019;16(7):3188–98. https://doi.org/10.1021/acs.molpharmaceut.9b00390.

    Article  CAS  PubMed  Google Scholar 

  36. Xia Q, Zhang Y, Li Z, Hou X, Feng N. Red blood cell membrane-camouflaged nanoparticles: a novel drug delivery system for antitumor application. Acta Pharm Sin B. 2019;9(4):675–89. https://doi.org/10.1016/j.apsb.2019.01.011.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Wang Q, Yang Q, Cao X, Wei Q, Firempong CK, Guo M, et al. Enhanced oral bioavailability and anti-gout activity of [6]-shogaol-loaded solid lipid nanoparticles. Int J Pharm. 2018;550(1-2):24–34. https://doi.org/10.1016/j.ijpharm.2018.08.028.

    Article  CAS  PubMed  Google Scholar 

  38. Wei Y, Wang L, Wang D, Wang D, Wen C, Han B, et al. Characterization and anti-tumor activity of a polysaccharide isolated from Dendrobium officinale grown in the Huoshan County. Chin Med. 2018;13:47. https://doi.org/10.1186/s13020-018-0205-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Li X, Xia X, Zhang J, Adu-Frimpong M, Shen X, Yin W, et al. Preparation, physical characterization, pharmacokinetics and anti-hyperglycemic activity of esculetin-loaded mixed micelles. J Pharm Sci. 2023;112(1):148–57. https://doi.org/10.1016/j.xphs.2022.06.022.

    Article  CAS  PubMed  Google Scholar 

  40. Liu B, Wang W, Fan J, Long Y, Xiao F, Daniyal M, et al. RBC membrane camouflaged prussian blue nanoparticles for gamabutolin loading and combined chemo/photothermal therapy of breast cancer. Biomater. 2019;217:119301. https://doi.org/10.1016/j.biomaterials.2019.119301.

    Article  CAS  Google Scholar 

  41. Liu J, Wang Q, Omari-Siaw E, Adu-Frimpong M, Liu J, Xu X, et al. Enhanced oral bioavailability of bisdemethoxycurcumin-loaded self-microemulsifying drug delivery system: formulation design, in vitro and in vivo evaluation. Int J Pharm. 2020;590:119887. https://doi.org/10.1016/j.ijpharm.2020.119887.

    Article  CAS  PubMed  Google Scholar 

  42. Yi C, Fu M, Cao X, Tong S, Zheng Q, Firempong CK, et al. Enhanced oral bioavailability and tissue distribution of a new potential anticancer agent, Flammulina velutipes sterols, through liposomal encapsulation. J Agric Food Chem. 2013;61(25):5961–71. https://doi.org/10.1021/jf3055278.

    Article  CAS  PubMed  Google Scholar 

  43. Fan X, Chen J, Zhang Y, Wang S, Zhong W, Yuan H, et al. Alpinetin promotes hair regeneration via activating hair follicle stem cells. Chin Med. 2022;17(1):63. https://doi.org/10.1186/s13020-022-00619-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Sun X, Lv W, Wang Y, Zhang X, Ouyang Z, Yin R, et al. Mrgprb2 gene plays a role in the anaphylactoid reactions induced by Houttuynia cordata injection. J Ethnopharm. 2022;289:115053. https://doi.org/10.1016/j.jep.2022.115053.

    Article  CAS  Google Scholar 

  45. Zhou H, Yang L, Wang C, Li Z, Ouyang Z, Shan M, et al. CYP2D1 Gene knockout reduces the metabolism and efficacy of venlafaxine in rats. Drug Metabol Dispos Biol Fate Chem. 2019;47(12):1425–32. https://doi.org/10.1124/dmd.119.088526.

    Article  CAS  Google Scholar 

  46. Zeouk I, Ouedrhiri W, Sifaoui I, Bazzocchi IL, Piñero JE, Jiménez IA, et al. Bioguided isolation of active compounds from Rhamnus alaternus against methicillin-resistant Staphylococcus aureus (MRSA) and panton-valentine leucocidin positive strains (MSSA-PVL). Molecules (Basel, Switzerland). 2021;26(14). https://doi.org/10.3390/molecules26144352.

  47. Lee PJ, Ho CC, Ho H, Chen WJ, Lin CH, Lai YH, et al. Tumor microenvironment-based screening repurposes drugs targeting cancer stem cells and cancer-associated fibroblasts. Theranostics. 2021;11(19):9667–86. https://doi.org/10.7150/thno.62676.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Li Q, Gao J, Pang X, Chen A, Wang Y. Molecular mechanisms of action of emodin: as an anti-cardiovascular disease drug. Front Pharm. 2020;11:559607. https://doi.org/10.3389/fphar.2020.559607.

    Article  CAS  Google Scholar 

  49. Otieno W, Liu C, Ji Y. Aloe-emodin-mediated photodynamic therapy attenuates sepsis-associated toxins in selected gram-positive bacteria in vitro. J Microbiol Biotechnol. 2021;31(9):1200–9. https://doi.org/10.4014/jmb.2105.05024.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Mugas ML, Calvo G, Marioni J, Céspedes M, Martinez F, Sáenz D, et al. Photodynamic therapy of tumour cells mediated by the natural anthraquinone parietin and blue light. J Photochem Photobiol B, Biol. 2021;214:112089. https://doi.org/10.1016/j.jphotobiol.2020.112089.

    Article  CAS  Google Scholar 

  51. Song Y, Sheng Z, Xu Y, Dong L, Xu W, Li F, et al. Magnetic liposomal emodin composite with enhanced killing efficiency against breast cancer. Biomater Sci. 2019;7(3):867–75. https://doi.org/10.1039/c8bm01530a.

    Article  CAS  PubMed  Google Scholar 

  52. Freag MS, Elnaggar YS, Abdelmonsif DA, Abdallah OY. Stealth, biocompatible monoolein-based lyotropic liquid crystalline nanoparticles for enhanced aloe-emodin delivery to breast cancer cells: in vitro and in vivo studies. Int J Nanomed. 2016;11:4799–818. https://doi.org/10.2147/ijn.S111736.

    Article  CAS  Google Scholar 

  53. Shi F, Chen L, Wang Y, Liu J, Adu-Frimpong M, Ji H, et al. Enhancement of oral bioavailability and anti-hyperuricemic activity of aloe emodin via novel Soluplus®-glycyrrhizic acid mixed micelle system. Drug Deliv Transl Res. 2022;12(3):603–14. https://doi.org/10.1007/s13346-021-00969-8.

    Article  CAS  PubMed  Google Scholar 

  54. Kim AV, Shelepova EA, Evseenko VI, Dushkin AV, Medvedev NN, Polyakov NE. Mechanism of the enhancing effect of glycyrrhizin on nifedipine penetration through a lipid membrane. J Mol Liq. 2021;344:117759. https://doi.org/10.1016/j.molliq.2021.117759.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Selyutina OY, Apanasenko IE, Kim AV, Shelepova EA, Khalikov SS, Polyakov NE. Spectroscopic and molecular dynamics characterization of glycyrrhizin membrane-modifying activity. Colloids Surface B, Biointerfaces. 2016;147:459–66. https://doi.org/10.1016/j.colsurfb.2016.08.037.

    Article  CAS  PubMed  Google Scholar 

  56. Chhabria V, Beeton S. Development of nanosponges from erythrocyte ghosts for removal of streptolysin-O from mammalian blood. Nanomed (London, England). 2016;11(21):2797–807. https://doi.org/10.2217/nnm-2016-0180.

    Article  CAS  Google Scholar 

  57. Wang Y, Luan Z, Zhao C, Bai C, Yang K. Target delivery selective CSF-1R inhibitor to tumor-associated macrophages via erythrocyte-cancer cell hybrid membrane camouflaged pH-responsive copolymer micelle for cancer immunotherapy. Eur J Pharmaceutic Sci Official J Eur Feder Pharm Sci. 2020;142:105136. https://doi.org/10.1016/j.ejps.2019.105136.

    Article  CAS  Google Scholar 

  58. Zheng D, Yu P, Wei Z, Zhong C, Wu M, Liu X. RBC membrane camouflaged semiconducting polymer nanoparticles for near-infrared photoacoustic imaging and photothermal therapy. Nano-Micro Lett. 2020;12(1):94. https://doi.org/10.1007/s40820-020-00429-x.

    Article  CAS  Google Scholar 

  59. Tang Z, Wu J, Yu X, Hong R, Zu X, Lin X, et al. Fabrication of Au nanoparticle arrays on flexible substrate for tunable localized surface plasmon resonance. ACS Appl Mater Interfaces. 2021;13(7):9281–8. https://doi.org/10.1021/acsami.0c22785.

    Article  CAS  PubMed  Google Scholar 

  60. Luo Y, Zhao J, Zhang X, Wang C, Wang T, Jiang M, et al. Size controlled fabrication of enzyme encapsulated amorphous calcium phosphate nanoparticle and its intracellular biosensing application. Colloids Surface B, Biointerfaces. 2021;201:111638. https://doi.org/10.1016/j.colsurfb.2021.111638.

    Article  CAS  Google Scholar 

  61. Kim HO, Na W, Yeom M, Lim JW, Bae EH, Park G, et al. Dengue virus-polymersome hybrid nanovesicles for advanced drug screening using real-time single nanoparticle-virus tracking. ACS Appl Mater Interfaces. 2020;12(6):6876–84. https://doi.org/10.1021/acsami.9b20492.

    Article  CAS  PubMed  Google Scholar 

  62. Dai X, Liao Y, Yang C, Zhang Y, Feng M, Tian Y, et al. Diammonium glycyrrhizinate-based micelles for improving the hepatoprotective effect of baicalin: characterization and biopharmaceutical study. Pharm. 2022;15(1) https://doi.org/10.3390/pharmaceutics15010125.

  63. Cho T, Han HS, Jeong J, Park EM, Shim KS. A novel computational approach for the discovery of drug delivery system candidates for COVID-19. Int J Mol Sci. 2021;22(6) https://doi.org/10.3390/ijms22062815.

  64. Yi C, Zhong H, Tong S, Cao X, Firempong CK, Liu H, et al. Enhanced oral bioavailability of a sterol-loaded microemulsion formulation of Flammulina velutipes, a potential antitumor drug. Int J Nanomed. 2012;7:5067–78. https://doi.org/10.2147/ijn.S34612.

    Article  CAS  Google Scholar 

  65. Lv Q, Li X, Shen B, Xu H, Shen C, Dai L, et al. Application of spray granulation for conversion of mixed phospholipid-bile salt micelles to dry powder form: influence of drug hydrophobicity on nanoparticle reagglomeration. Int J Nanomed. 2014;9:505–15. https://doi.org/10.2147/ijn.S56215.

    Article  Google Scholar 

  66. Guo C, Hou X, Liu Y, Zhang Y, Xu H, Zhao F, et al. Novel Chinese angelica polysaccharide biomimetic nanomedicine to curcumin delivery for hepatocellular carcinoma treatment and immunomodulatory effect. Phytomed Int J Phytotherapy Phytopharmacol. 2021;80:153356. https://doi.org/10.1016/j.phymed.2020.153356.

    Article  CAS  Google Scholar 

  67. Haggag YA, Yasser M, Tambuwala MM, El Tokhy SS, Isreb M, Donia AA. Repurposing of Guanabenz acetate by encapsulation into long-circulating nanopolymersomes for treatment of triple-negative breast cancer. Int J Pharm. 2021;600:120532. https://doi.org/10.1016/j.ijpharm.2021.120532.

    Article  CAS  PubMed  Google Scholar 

  68. Kaur J, Tuler S, Dasanu CA. Autoimmune hemolytic anemia in a patient with myelodysplastic syndrome: responding to 5-azacitidine therapy. J Oncol Pharm Practice Official Publication Int Soc Oncol Pharm Pract. 2021;27(7):1775–8. https://doi.org/10.1177/1078155220987616.

    Article  Google Scholar 

  69. Anandappa AJ, Stefely JA, Hasserjian RP, Dzik WH, Waheed A. Multiorgan failure in a fatal case of autoimmune hemolytic anemia. Transf. 2021;61(9):2795–8. https://doi.org/10.1111/trf.16513.

    Article  CAS  Google Scholar 

  70. Wang D, Song L, Shen L, Zhang K, Lv Y, Gao M, et al. Mutational characteristics of causative genes in Chinese hereditary spherocytosis patients: a report on fourteen cases and a review of the literature. Front Pharm. 2021;12:644352. https://doi.org/10.3389/fphar.2021.644352.

    Article  CAS  Google Scholar 

  71. Jakfar S, Lin TC, Wu SC, Wang YH, Sun YJ, Thacker M, et al. New design to remove leukocytes from platelet-rich plasma (PRP) based on cell dimension rather than density. Bioact Mater. 2021;6(10):3528–40. https://doi.org/10.1016/j.bioactmat.2021.03.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Ran L, Lu B, Qiu H, Zhou G, Jiang J, Hu E, et al. Erythrocyte membrane-camouflaged nanoworms with on-demand antibiotic release for eradicating biofilms using near-infrared irradiation. Bioact Mater. 2021;6(9):2956–68. https://doi.org/10.1016/j.bioactmat.2021.01.032.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Cheng X, Gu J, Zhang M, Yuan J, Zhao B, Jiang J, et al. Astragaloside IV inhibits migration and invasion in human lung cancer A549 cells via regulating PKC-α-ERK1/2-NF-κB pathway. Int Immunopharmacol. 2014;23(1):304–13. https://doi.org/10.1016/j.intimp.2014.08.027.

    Article  CAS  PubMed  Google Scholar 

  74. Yang XM, Wang YF, Li YY, Ma HL. Thermal stability of ginkgolic acids from Ginkgo biloba and the effects of ginkgol C17:1 on the apoptosis and migration of SMMC7721 cells. Fitoterapia. 2014;98:66–76. https://doi.org/10.1016/j.fitote.2014.07.003.

    Article  CAS  PubMed  Google Scholar 

  75. Zhou Z, Tang M, Liu Y, Zhang Z, Lu R, Lu J. Apigenin inhibits cell proliferation, migration, and invasion by targeting Akt in the A549 human lung cancer cell line. Anti-Cancer Drugs. 2017;28(4):446–56. https://doi.org/10.1097/cad.0000000000000479.

    Article  CAS  PubMed  Google Scholar 

  76. Wei Y, Wang D, Chen M, Ouyang Z, Wang S, Gu J. Extrahepatic cytochrome P450s play an insignificant role in triptolide-induced toxicity. Chin Med. 2018;13:23. https://doi.org/10.1186/s13020-018-0179-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Lee D, Jang SY, Kwon S, Lee Y, Park E, Koo H. Optimized combination of photodynamic therapy and chemotherapy using gelatin nanoparticles containing tirapazamine and pheophorbide a. ACS Appl Mater Interfaces. 2021;13(9):10812–21. https://doi.org/10.1021/acsami.1c02316.

    Article  CAS  PubMed  Google Scholar 

  78. Wei Y, Li L, Zhou X, Zhang QY, Dunbar A, Liu F, et al. Generation and characterization of a novel Cyp2a(4/5)bgs-null mouse model. Drug Metabol Dispos Biol Fate Chem. 2013;41(1):132–40. https://doi.org/10.1124/dmd.112.048736.

    Article  CAS  Google Scholar 

  79. Tian X, Xiao BB, Wu A, Yu L, Zhou J, Wang Y, et al. Hydroxylated-graphene quantum dots induce cells senescence in both p53-dependent and -independent manner. Toxicol Res. 2016;5(6):1639–48. https://doi.org/10.1039/c6tx00209a.

    Article  CAS  Google Scholar 

  80. Tuli HS, Aggarwal V, Tuorkey M, Aggarwal D, Parashar NC, Varol M, et al. Emodin: a metabolite that exhibits anti-neoplastic activities by modulating multiple oncogenic targets. Toxicol in vitro: An Int J Published Assoc BIBRA. 2021;73:105142. https://doi.org/10.1016/j.tiv.2021.105142.

    Article  CAS  Google Scholar 

  81. Wang KJ, Meng XY, Chen JF, Wang KY, Zhou C, Yu R, et al. Emodin induced necroptosis and inhibited glycolysis in the renal cancer cells by enhancing ROS. Oxidative Med Cell Longev. 2021;2021:8840590. https://doi.org/10.1155/2021/8840590.

    Article  CAS  Google Scholar 

  82. Liu H, Zhuang Y, Wang P, Zou T, Lan M, Li L, et al. Polymeric lipid hybrid nanoparticles as a delivery system enhance the antitumor effect of emodin in vitro and in vivo. J Pharm Sci. 2021;110(8):2986–96. https://doi.org/10.1016/j.xphs.2021.04.006.

    Article  CAS  PubMed  Google Scholar 

  83. Chen X, Sun L, Wei X, Lu H, Tan Y, Sun Z, et al. Antitumor effect and molecular mechanism of fucoidan in NSCLC. BMC Complement Med Ther. 2021;21(1):25. https://doi.org/10.1186/s12906-020-03191-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Chen Y, Wan Y, Wang Y, Zhang H, Jiao Z. Anticancer efficacy enhancement and attenuation of side effects of doxorubicin with titanium dioxide nanoparticles. Int J Nanomed. 2011;6:2321–6. https://doi.org/10.2147/ijn.S25460.

    Article  CAS  Google Scholar 

  85. Wei Y, Yang L, Zhang X, Sui D, Wang C, Wang K, et al. Generation and characterization of a CYP2C11-Null Rat Model by Using the CRISPR/Cas9 Method. Drug Metabol Disposition Biol Fate Chem. 2018;46(5):525–31. https://doi.org/10.1124/dmd.117.078444.

    Article  CAS  Google Scholar 

  86. Li Y, Wang Y, Yu X, Yu T, Zheng X, Chu Q. Radix tetrastigma inhibits the non-small cell lung cancer via Bax/Bcl-2/Caspase-9/Caspase-3 pathway. Nutrition Cancer. 2022;74(1):320–32. https://doi.org/10.1080/01635581.2021.1881569.

    Article  CAS  PubMed  Google Scholar 

  87. Xie J, Lai Z, Zheng X, Liao H, Xian Y, Li Q, et al. Apoptotic activities of brusatol in human non-small cell lung cancer cells: involvement of ROS-mediated mitochondrial-dependent pathway and inhibition of Nrf2-mediated antioxidant response. Toxicol. 2021;451:152680. https://doi.org/10.1016/j.tox.2021.152680.

    Article  CAS  Google Scholar 

  88. Sung TC, Li CY, Lai YC, Hung CL, Shih O, Yeh YQ, et al. Solution structure of apoptotic BAX oligomer: oligomerization likely precedes membrane insertion. Structure (London, England: 1993). 2015;23(10):1878-88. https://doi.org/10.1016/j.str.2015.07.013.

  89. Ye H, Sui D, Liu W, Yuan Y, Ouyang Z, Wei Y. Effects of CYP2C11 gene knockout on the pharmacokinetics and pharmacodynamics of warfarin in rats. Xenobiotica; Fate Foreign Compd Biol Syst. 2019;49(12):1478–84. https://doi.org/10.1080/00498254.2019.1579006.

    Article  CAS  Google Scholar 

  90. Antonsson B, Montessuit S, Sanchez B, Martinou JC. Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. The J Biol Chem. 2001;276(15):11615–23. https://doi.org/10.1074/jbc.M010810200.

    Article  CAS  PubMed  Google Scholar 

  91. Liu C, Chen L, Wang W, Qin D, Jia C, Yuan M, et al. Emodin suppresses the migration and invasion of melanoma cells. Biol Pharm Bull. 2021;44(6):771–9. https://doi.org/10.1248/bpb.b20-00807.

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was funded by the National Key R&D Program of China (2018YFE0208600), the National Natural Science Foundation of China (81720108030, 8217131836, and 82173785), the Jiangsu Postdoctoral Research Foundation in 2021 category A (2021K010A), the Natural Science Foundation of the Higher Education Institutions of Jiangsu Province (18KJB360001), and the Key planning social development projects of Zhenjiang in Jiangsu Province (SH2021024).

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Authors and Affiliations

  1. Department of Pharmaceutics, School of Pharmacy, Centre for Nano Drug/Gene Delivery and Tissue Engineering, Jiangsu University, Zhenjiang, People’s Republic of China

    Xia Cao, Tianwen Deng, Qin Zhu, Wenwan Shi, Qi Liu, Qintong Yu, Wenwen Deng, Jiangnan Yu, Qilong Wang & Ximing Xu

  2. Medicinal function development of new food resources, Jiangsu Provincial Research center, Jiangsu, People’s Republic of China

    Xia Cao, Tianwen Deng, Qin Zhu, Wenwan Shi, Qintong Yu, Wenwen Deng, Jiangnan Yu, Qilong Wang & Ximing Xu

  3. School of Life Sciences, Northwestern Polytechnical University, Xi’an, Shaanxi, 710072, People’s Republic of China

    Jianping Wang

  4. College of Environment and Safety Engineering, Fuzhou University, Fuzhou, 350108, Fujian, People’s Republic of China

    Gao Xiao

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  1. Xia Cao
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  2. Tianwen Deng
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  3. Qin Zhu
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  10. Qilong Wang
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  11. Gao Xiao
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  12. Ximing Xu
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Contributions

Cao Xia, Ximing Xu, and Qilong Wang contributed to the conceptualization. Tianwen Deng, Qin Zhu, Jianping Wang, and Wenwan Shi contributed to the data curation and methodology. Qintong Yu, Tianwen Deng, Qin Zhu, and Jianping Wang contributed to the formal analysis and validation. Qintong Yu, Wenwen Deng, and Gao Xiao contributed to the supervision. Xia Cao, Tianwen Deng, Qin Zhu, and Xiao Gao contributed to the writing. Xia Cao, Jiangnan Yu, and Ximing Xu contributed to the funding acquisition.

Corresponding authors

Correspondence to Qilong Wang, Gao Xiao or Ximing Xu.

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Cao, X., Deng, T., Zhu, Q. et al. Photothermal Therapy Mediated Hybrid Membrane Derived Nano-formulation for Enhanced Cancer Therapy. AAPS PharmSciTech 24, 146 (2023). https://doi.org/10.1208/s12249-023-02594-9

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