748
Views
37
CrossRef citations to date
0
Altmetric
Review

Advances in Multiple Stimuli-Responsive Drug-Delivery Systems for Cancer Therapy

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, , & show all
Pages 1525-1551 | Published online: 25 Feb 2021

References

  • 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. doi:10.3322/caac.21492
  • Iyer AK, Singh A, Ganta S, Amiji MM. Role of integrated cancer nanomedicine in overcoming drug resistance. Adv Drug Deliv Rev. 2013;65(13–14):1784–1802. doi:10.1016/j.addr.2013.07.012
  • Yang Z, Shi J, Xie J, et al. Large-scale generation of functional mRNA-encapsulating exosomes via cellular nanoporation. Nat Biomed Eng. 2020;4(1):69–83. doi:10.1038/s41551-019-0485-1
  • Chanmee T, Ontong P, Konno K, Itano N. Tumor-associated macrophages as major players in the tumor microenvironment. Cancers. 2014;6(3):1670–1690. doi:10.3390/cancers6031670
  • Wu J, Chen J, Feng Y, Tian H, Chen X. Tumor microenvironment as the “regulator” and “target” for gene therapy. J Gene Med. 2019;21(7):e3088. doi:10.1002/jgm.3088
  • Karagiannis GS, Poutahidis T, Erdman SE, Kirsch R, Riddell RH, Diamandis EP. Cancer-associated fibroblasts drive the progression of metastasis through both paracrine and mechanical pressure on cancer tissue. Mol Cancer Res. 2012;10(11):1403–1418. doi:10.1158/1541-7786.Mcr-12-0307
  • Ivey JW, Bonakdar M, Kanitkar A, Davalos RV, Verbridge SS. Improving cancer therapies by targeting the physical and chemical hallmarks of the tumor microenvironment. Cancer Lett. 2016;380(1):330–339. doi:10.1016/j.canlet.2015.12.019
  • Cabral H, Matsumoto Y, Mizuno K, et al. Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size. Nat Nanotechnol. 2011;6(12):815–823. doi:10.1038/nnano.2011.166
  • Rosenblum D, Joshi N, Tao W, Karp JM, Peer D. Progress and challenges towards targeted delivery of cancer therapeutics. Nat Commun. 2018;9(1):1410. doi:10.1038/s41467-018-03705-y
  • Li L, Wang J, Kong H, Zeng Y, Liu G. Functional biomimetic nanoparticles for drug delivery and theranostic applications in cancer treatment. Sci Technol Adv Mater. 2018;19(1):771–790. doi:10.1080/14686996.2018.1528850
  • Jain RK, Stylianopoulos T. Delivering nanomedicine to solid tumors. Nat Rev Clin Oncol. 2010;7(11):653–664. doi:10.1038/nrclinonc.2010.139
  • El-Sawy HS, Al-Abd AM, Ahmed TA, El-Say KM, Torchilin VP. Stimuli-responsive nano-architecture drug-delivery systems to solid tumor micromilieu: past, present, and future perspectives. ACS Nano. 2018;12(11):10636–10664. doi:10.1021/acsnano.8b06104
  • Li F, Yang H, Bie N, et al. Zwitterionic temperature/redox-sensitive nanogels for near-infrared light-triggered synergistic thermo-chemotherapy. ACS Appl Mater Interfaces. 2017;9(28):23564–23573. doi:10.1021/acsami.7b08047
  • Vo KT, Matthay KK, DuBois SG. Targeted antiangiogenic agents in combination with cytotoxic chemotherapy in preclinical and clinical studies in sarcoma. Clin Sarcoma Res. 2016;6:9. doi:10.1186/s13569-016-0049-z
  • Jhaveri A, Deshpande P, Torchilin V. Stimuli-sensitive nanopreparations for combination cancer therapy. J Control Release. 2014;190:352–370. doi:10.1016/j.jconrel.2014.05.002
  • Mura S, Nicolas J, Couvreur P. Stimuli-responsive nanocarriers for drug delivery. Nat Mater. 2013;12(11):991–1003. doi:10.1038/nmat3776
  • Chen B, Dai W, He B, et al. Current multistage drug delivery systems based on the tumor microenvironment. Theranostics. 2017;7(3):538–558. doi:10.7150/thno.16684
  • Raza A, Rasheed T, Nabeel F, Hayat U, Bilal M, Iqbal HMN. Endogenous and exogenous stimuli-responsive drug delivery systems for programmed site-specific release. Molecules (Basel, Switzerland). 2019;24(6):1117. doi:10.3390/molecules24061117
  • Wang M, Liang Y, Zhang Z, et al. Ag@Fe(3)O(4)@C nanoparticles for multi-modal imaging-guided chemo-photothermal synergistic targeting for cancer therapy. Anal Chim Acta. 2019;1086:122–132. doi:10.1016/j.aca.2019.08.035
  • Reguera J, Jiménez de Aberasturi D, Henriksen-Lacey M, et al. Janus plasmonic-magnetic gold-iron oxide nanoparticles as contrast agents for multimodal imaging. Nanoscale. 2017;9(27):9467–9480. doi:10.1039/c7nr01406f
  • Zhou S, Ding C, Wang C, Fu J. UV-light cross-linked and pH de-cross-linked coumarin-decorated cationic copolymer grafted mesoporous silica nanoparticles for drug and gene co-delivery in vitro. Mater Sci Eng C Mater Biol Appl. 2020;108:110469. doi:10.1016/j.msec.2019.110469
  • Lei Q, Wang SB, Hu JJ, et al. Stimuli-responsive “Cluster bomb” for programmed tumor therapy. ACS Nano. 2017;11(7):7201–7214. doi:10.1021/acsnano.7b03088
  • Cheng L, Liu J, Gu X, et al. PEGylated WS(2) nanosheets as a multifunctional theranostic agent for in vivo dual-modal CT/photoacoustic imaging guided photothermal therapy. Adv Mater. 2014;26(12):1886–1893. doi:10.1002/adma.201304497
  • Sun X, Dong S, Li X, et al. Delivery of siRNA using folate receptor-targeted pH-sensitive polymeric nanoparticles for rheumatoid arthritis therapy. Nanomedicine. 2019;20:102017. doi:10.1016/j.nano.2019.102017
  • Kakwere H, Materia ME, Curcio A, et al. Dually responsive gold-iron oxide heterodimers: merging stimuli-responsive surface properties with intrinsic inorganic material features. Nanoscale. 2018;10(8):3930–3944. doi:10.1039/c7nr06726g
  • Guardia P, Nitti S, Materia ME, et al. Gold-iron oxide dimers for magnetic hyperthermia: the key role of chloride ions in the synthesis to boost the heating efficiency. J Mater Chem B. 2017;5(24):4587–4594. doi:10.1039/c7tb00968b
  • Truong NP, Gu W, Prasadam I, et al. An influenza virus-inspired polymer system for the timed release of siRNA. Nat Commun. 2013;4:1902. doi:10.1038/ncomms2905
  • Dreaden EC, Alkilany AM, Huang X, Murphy CJ, El-Sayed MA. The golden age: gold nanoparticles for biomedicine. Chem Soc Rev. 2012;41(7):2740–2779. doi:10.1039/c1cs15237h
  • Hatakeyama H, Akita H, Kogure K, et al. Development of a novel systemic gene delivery system for cancer therapy with a tumor-specific cleavable PEG-lipid. Gene Ther. 2007;14(1):68–77. doi:10.1038/sj.gt.3302843
  • Zhou M, Huang H, Wang D, et al. Light-triggered PEGylation/dePEGylation of the nanocarriers for enhanced tumor penetration. Nano Lett. 2019;19(6):3671–3675. doi:10.1021/acs.nanolett.9b00737
  • Lee Y, Lee S, Lee DY, Yu B, Miao W, Jon S. Multistimuli-responsive bilirubin nanoparticles for anticancer therapy. Angew Chem Int Ed Engl. 2016;55(36):10676–10680. doi:10.1002/anie.201604858
  • Maisels MJ, McDonagh AF. Phototherapy for neonatal jaundice. N Engl J Med. 2008;358(9):920–928. doi:10.1056/NEJMct0708376
  • Sedlak TW, Saleh M, Higginson DS, Paul BD, Juluri KR, Snyder SH. Bilirubin and glutathione have complementary antioxidant and cytoprotective roles. Proc Natl Acad Sci U S A. 2009;106(13):5171–5176. doi:10.1073/pnas.0813132106
  • Zhou X, Chen L, Nie W, et al. Dual-responsive mesoporous silica nanoparticles mediated codelivery of doxorubicin and Bcl-2 SiRNA for targeted treatment of breast cancer. J Phys Chem C. 2016;120(39):22375–22387. doi:10.1021/acs.jpcc.6b06759
  • Feng W, Nie W, He C, et al. Effect of pH-responsive alginate/chitosan multilayers coating on delivery efficiency, cellular uptake and biodistribution of mesoporous silica nanoparticles based nanocarriers. ACS Appl Mater Interfaces. 2014;6(11):8447–8460. doi:10.1021/am501337s
  • Ma X, Zhao Y, Ng KW, Zhao Y. Integrated hollow mesoporous silica nanoparticles for target drug/siRNA co-delivery. Chemistry. 2013;19(46):15593–15603. doi:10.1002/chem.201302736
  • Huschka R, Zuloaga J, Knight MW, Brown LV, Nordlander P, Halas NJ. Light-induced release of DNA from gold nanoparticles: nanoshells and nanorods. J Am Chem Soc. 2011;133(31):12247–12255. doi:10.1021/ja204578e
  • Wang F, Shen Y, Zhang W, et al. Efficient, dual-stimuli responsive cytosolic gene delivery using a RGD modified disulfide-linked polyethylenimine functionalized gold nanorod. J Control Release. 2014;196:37–51. doi:10.1016/j.jconrel.2014.09.026
  • Wang F, Huang Q, Wang Y, Shi L, Shen Y, Guo S. NIR-light and GSH activated cytosolic p65-shRNA delivery for precise treatment of metastatic cancer. J Control Release. 2018;288:126–135. doi:10.1016/j.jconrel.2018.09.002
  • Junttila MR, de Sauvage FJ. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature. 2013;501(7467):346–354. doi:10.1038/nature12626
  • Miao L, Lin CM, Huang L. Stromal barriers and strategies for the delivery of nanomedicine to desmoplastic tumors. J Control Release. 2015;219:192–204. doi:10.1016/j.jconrel.2015.08.017
  • Wang Y, Zhang T, Hou C, et al. Mitochondria-specific anticancer drug delivery based on reduction-activated polyprodrug for enhancing the therapeutic effect of breast cancer chemotherapy. ACS Appl Mater Interfaces. 2019;11(32):29330–29340. doi:10.1021/acsami.9b10211
  • Ruan S, Cao X, Cun X, et al. Matrix metalloproteinase-sensitive size-shrinkable nanoparticles for deep tumor penetration and pH triggered doxorubicin release. Biomaterials. 2015;60:100–110. doi:10.1016/j.biomaterials.2015.05.006
  • Yu B, Song N, Hu H, Chen G, Shen Y, Cong H. A degradable triple temperature-, pH-, and redox-responsive drug system for cancer chemotherapy. J Biomed Mater Res A. 2018;106(12):3203–3210. doi:10.1002/jbm.a.36515
  • Wang Z, Xu Z, Zhu G. A Platinum(IV) anticancer prodrug targeting nucleotide excision repair to overcome cisplatin resistance. Angew Chem Int Ed Engl. 2016;55(50):15564–15568. doi:10.1002/anie.201608936
  • Mo R, Sun Q, Xue J, et al. Multistage pH-responsive liposomes for mitochondrial-targeted anticancer drug delivery. Adv Mater. 2012;24(27):3659–3665. doi:10.1002/adma.201201498
  • Callahan J, Kopečkov P, Kopeček J. Intracellular trafficking and subcellular distribution of a large array of HPMA copolymers. Biomacromolecules. 2009;10(7):1704–1714. doi:10.1021/bm801514x
  • Pan L, He Q, Liu J, et al. Nuclear-targeted drug delivery of TAT peptide-conjugated monodisperse mesoporous silica nanoparticles. J Am Chem Soc. 2012;134(13):5722–5725. doi:10.1021/ja211035w
  • Xie J, Bi Y, Zhang H, et al. Cell-penetrating peptides in diagnosis and treatment of human diseases: from preclinical research to clinical application. Front Pharmacol. 2020;11:697. doi:10.3389/fphar.2020.00697
  • Lian L, Sun W, Zhong J, et al. Multistage nanovehicle delivery system based on stepwise size reduction and charge reversal for programmed nuclear targeting of systemically administered anticancer drugs. Adv Funct Mater. 2015;25(26):4101–4113. doi:10.1002/adfm.201501248
  • Beheshti F, Hassanian SM, Khazaei M, et al. Genetic variation in the DNA repair pathway as a potential determinant of response to platinum-based chemotherapy in breast cancer. J Cell Physiol. 2018;233(4):2752–2758. doi:10.1002/jcp.26091
  • Liu J, Guo X, Luo Z, Zhang J, Li M, Cai K. Hierarchically stimuli-responsive nanovectors for improved tumor penetration and programed tumor therapy. Nanoscale. 2018;10(28):13737–13750. doi:10.1039/c8nr02971g
  • Liu M, Shen S, Wen D, et al. Hierarchical nanoassemblies-assisted combinational delivery of cytotoxic protein and antibiotic for cancer treatment. Nano Lett. 2018;18(4):2294–2303. doi:10.1021/acs.nanolett.7b04976
  • Zhao M, Liu Y, Hsieh RS, et al. Clickable protein nanocapsules for targeted delivery of recombinant p53 protein. J Am Chem Soc. 2014;136(43):15319–15325. doi:10.1021/ja508083g
  • Li HJ, Du JZ, Du XJ, et al. Stimuli-responsive clustered nanoparticles for improved tumor penetration and therapeutic efficacy. Proc Natl Acad Sci U S A. 2016;113(15):4164–4169. doi:10.1073/pnas.1522080113
  • Wang M, Alberti K, Sun S, Arellano CL, Xu Q. Combinatorially designed lipid-like nanoparticles for intracellular delivery of cytotoxic protein for cancer therapy. Angew Chem Int Ed Engl. 2014;53(11):2893–2898. doi:10.1002/anie.201311245
  • Lamb R, Ozsvari B, Lisanti CL, et al. Antibiotics that target mitochondria effectively eradicate cancer stem cells, across multiple tumor types: treating cancer like an infectious disease. Oncotarget. 2015;6(7):4569–4584. doi:10.18632/oncotarget.3174
  • Zhang L, Xu L, Zhang F, Vlashi E. Doxycycline inhibits the cancer stem cell phenotype and epithelial-to-mesenchymal transition in breast cancer. Cell Cycle (Georgetown, Tex). 2017;16(8):737–745. doi:10.1080/15384101.2016.1241929
  • Li Y, Li W, Bao W, et al. Bioinspired peptosomes with programmed stimuli-responses for sequential drug release and high-performance anticancer therapy. Nanoscale. 2017;9(27):9317–9324. doi:10.1039/c7nr00598a
  • Arpel A, Sawma P, Spenlé C, et al. Transmembrane domain targeting peptide antagonizing ErbB2/Neu inhibits breast tumor growth and metastasis. Cell Rep. 2014;8(6):1714–1721. doi:10.1016/j.celrep.2014.07.044
  • Lächelt U, Wagner E. Nucleic acid therapeutics using polyplexes: a journey of 50 years (and Beyond). Chem Rev. 2015;115(19):11043–11078. doi:10.1021/cr5006793
  • Hao F, Dong S, Yang C, et al. Targeted and efficient delivery of siRNA using tunable polymeric hybrid micelles for tumor therapy. Anticancer Res. 2019;39(3):1169–1178. doi:10.21873/anticanres.13226
  • Patnaik S, Gupta KC. Novel polyethylenimine-derived nanoparticles for in vivo gene delivery. Expert Opin Drug Deliv. 2013;10(2):215–228. doi:10.1517/17425247.2013.744964
  • Xu F, Zhong H, Chang Y, et al. Targeting death receptors for drug-resistant cancer therapy: codelivery of pTRAIL and monensin using dual-targeting and stimuli-responsive self-assembling nanocomposites. Biomaterials. 2018;158:56–73. doi:10.1016/j.biomaterials.2017.12.018
  • Tan J, Wang H, Xu F, et al. Poly-γ-glutamic acid-based GGT-targeting and surface camouflage strategy for improving cervical cancer gene therapy. J Mater Chem B. 2017;5(6):1315–1327. doi:10.1039/c6tb02990f
  • Choi KY, Silvestre OF, Huang X, et al. A nanoparticle formula for delivering siRNA or miRNAs to tumor cells in cell culture and in vivo. Nat Protoc. 2014;9(8):1900–1915. doi:10.1038/nprot.2014.128
  • Saw PE, Yao H, Lin C, Tao W, Farokhzad OC, Xu X. Stimuli-responsive polymer-prodrug hybrid nanoplatform for multistage siRNA delivery and combination cancer therapy. Nano Lett. 2019;19(9):5967–5974. doi:10.1021/acs.nanolett.9b01660
  • Zhao Y, Wang W, Guo S, et al. PolyMetformin combines carrier and anticancer activities for in vivo siRNA delivery. Nat Commun. 2016;7:11822. doi:10.1038/ncomms11822
  • Augustine R, Kalva N, Kim HA, Zhang Y, Kim I. pH-responsive polypeptide-based smart nano-carriers for theranostic applications. Molecules (Basel, Switzerland). 2019;24(16):2961. doi:10.3390/molecules24162961
  • Benjaminsen RV, Mattebjerg MA, Henriksen JR, Moghimi SM, Andresen TL. The possible “proton sponge “ effect of polyethylenimine (PEI) does not include change in lysosomal pH. Mol Ther. 2013;21(1):149–157. doi:10.1038/mt.2012.185
  • Oh JK. Disassembly and tumor-targeting drug delivery of reduction-responsive degradable block copolymer nanoassemblies. Polym Chem. 2019;10(13):1554–1568. doi:10.1039/c8py01808a
  • Karimi M, Ghasemi A, Sahandi Zangabad P, et al. Smart micro/nanoparticles in stimulus-responsive drug/gene delivery systems. Chem Soc Rev. 2016;45(5):1457–1501. doi:10.1039/c5cs00798d
  • Ataullakhanov FI, Vitvitsky VM. What determines the intracellular ATP concentration. Biosci Rep. 2002;22(5–6):501–511. doi:10.1023/a:1022069718709
  • Wu Y, Zhang X, Li H, et al. A core/shell stabilized polysaccharide-based nanoparticle with intracellular environment-sensitive drug delivery for breast cancer therapy. J Mater Chem B. 2018;6(41):6646–6659. doi:10.1039/c8tb00633d
  • Liu KS, Liu H, Qi JH, et al. SNX-2112, an Hsp90 inhibitor, induces apoptosis and autophagy via degradation of Hsp90 client proteins in human melanoma A-375 cells. Cancer Lett. 2012;318(2):180–188. doi:10.1016/j.canlet.2011.12.015
  • Lu HH, Huang CH, Shiue TY, et al. Highly efficient gene release in spatiotemporal precision approached by light and pH dual responsive copolymers. Chem Sci. 2019;10(1):284–292. doi:10.1039/c8sc01494a
  • He H, Zhu R, Sun W, Cai K, Chen Y, Yin L. Selective cancer treatment via photodynamic sensitization of hypoxia-responsive drug delivery. Nanoscale. 2018;10(6):2856–2865. doi:10.1039/c7nr07677k
  • Tiwari AP, Hwang TI, Oh JM, et al. pH/NIR-responsive polypyrrole-functionalized fibrous localized drug-delivery platform for synergistic cancer therapy. ACS Appl Mater Interfaces. 2018;10(24):20256–20270. doi:10.1021/acsami.7b17664
  • Zeng X, Wang Y, Han J, et al. Fighting against drug-resistant tumors using a dual-responsive Pt(IV)/Ru(II) bimetallic polymer. Adv Mater. 2020:e2004766. doi:10.1002/adma.202004766.
  • Zhou J, Han Y, Yang Y, et al. Phospholipid-decorated glycogen nanoparticles for stimuli-responsive drug release and synergetic chemophotothermal therapy of hepatocellular carcinoma. ACS Appl Mater Interfaces. 2020;12(20):23311–23322. doi:10.1021/acsami.0c02785
  • Chen W, Achazi K, Schade B, Haag R. Charge-conversional and reduction-sensitive poly(vinyl alcohol) nanogels for enhanced cell uptake and efficient intracellular doxorubicin release. J Control Release. 2015;205:15–24. doi:10.1016/j.jconrel.2014.11.012
  • Guo Z, Sui J, Ma M, et al. pH-Responsive charge switchable PEGylated ε-poly-l-lysine polymeric nanoparticles-assisted combination therapy for improving breast cancer treatment. J Control Release. 2020;326:350–364. doi:10.1016/j.jconrel.2020.07.030
  • Yoo J, Sanoj Rejinold N, Lee D, Jon S, Kim YC. Protease-activatable cell-penetrating peptide possessing ROS-triggered phase transition for enhanced cancer therapy. J Control Release. 2017;264:89–101. doi:10.1016/j.jconrel.2017.08.026
  • Li Y, Xu X, Zhang X, Li Y, Zhang Z, Gu Z. Tumor-specific multiple stimuli-activated dendrimeric nanoassemblies with metabolic blockade surmount chemotherapy resistance. ACS Nano. 2017;11(1):416–429. doi:10.1021/acsnano.6b06161
  • Han H, Valdepérez D, Jin Q, et al. Dual enzymatic reaction-assisted gemcitabine delivery systems for programmed pancreatic cancer therapy. ACS Nano. 2017;11(2):1281–1291. doi:10.1021/acsnano.6b05541
  • Gao Y, Jia L, Wang Q, et al. pH/Redox dual-responsive polyplex with effective endosomal escape for codelivery of siRNA and doxorubicin against drug-resistant cancer cells. ACS Appl Mater Interfaces. 2019;11(18):16296–16310. doi:10.1021/acsami.9b02016
  • Hyun LJ, Woo CH, Joon MS, Geun CB. Dual-stimuli responsive mesoporous copper (II) sulfide nanocomposite for chemo-photothermal synergistic therapy. Micropor Mesopor Mater. 2020;302. doi:10.1016/j.micromeso.2020.110228.
  • Yin W, Ke W, Lu N, et al. Glutathione and reactive oxygen species dual-responsive block copolymer prodrugs for boosting tumor site-specific drug release and enhanced antitumor efficacy. Biomacromolecules. 2020;21(2):921–929. doi:10.1021/acs.biomac.9b01578
  • Mondal B, Pandey B, Parekh N, et al. Amphiphilic mannose-6-phosphate glycopolypeptide-based bioactive and responsive self-assembled nanostructures for controlled and targeted lysosomal cargo delivery. Biomater Sci. 2020;8(22):6322–6336. doi:10.1039/d0bm01469a
  • Han X, Wang L, Du J, Dou J, Yuan J, Shen J. Keratin-dopamine conjugate nanoparticles as pH/GSH dual responsive drug carriers. J Biomater Sci Polym Ed. 2020;1–13. doi:10.1080/09205063.2020.1803182
  • Song Y, Cai L, Tian Z, Wu Y, Chen J. Phytochemical curcumin-coformulated, silver-decorated melanin-like polydopamine/mesoporous silica composites with improved antibacterial and chemotherapeutic effects against drug-resistant cancer cells. ACS Omega. 2020;5(25):15083–15094. doi:10.1021/acsomega.0c00912
  • Li Y, Hou H, Zhang P, Zhang Z. Co-delivery of doxorubicin and paclitaxel by reduction/pH dual responsive nanocarriers for osteosarcoma therapy. Drug Deliv. 2020;27(1):1044–1053. doi:10.1080/10717544.2020.1785049
  • Su M, Xiao S, Shu M, et al. Enzymatic multifunctional biodegradable polymers for pH- and ROS-responsive anticancer drug delivery. Colloids Surf B Biointerfaces. 2020;193:111067. doi:10.1016/j.colsurfb.2020.111067
  • Jiang D, Mu W, Pang X, et al. Cascade cytosol delivery of dual-sensitive micelle-tailored vaccine for enhancing cancer immunotherapy. ACS Appl Mater Interfaces. 2018;10(44):37797–37811. doi:10.1021/acsami.8b09946
  • Kim J, Lee YM, Kim H, Park D, Kim J, Kim WJ. Phenylboronic acid-sugar grafted polymer architecture as a dual stimuli-responsive gene carrier for targeted anti-angiogenic tumor therapy. Biomaterials. 2016;75:102–111. doi:10.1016/j.biomaterials.2015.10.022
  • Zhao Y, Shi C, Yang X, et al. pH- and temperature-sensitive hydrogel nanoparticles with dual photoluminescence for bioprobes. ACS Nano. 2016;10(6):5856–5863. doi:10.1021/acsnano.6b00770
  • Lu N, Huang P, Fan W, et al. Tri-stimuli-responsive biodegradable theranostics for mild hyperthermia enhanced chemotherapy. Biomaterials. 2017;126:39–48. doi:10.1016/j.biomaterials.2017.02.025
  • Zhang L, Sheng D, Wang D, et al. Bioinspired multifunctional melanin-based nanoliposome for photoacoustic/magnetic resonance imaging-guided efficient photothermal ablation of cancer. Theranostics. 2018;8(6):1591–1606. doi:10.7150/thno.22430
  • Feng T, Zhou L, Wang Z, et al. Dual-stimuli responsive nanotheranostics for mild hyperthermia enhanced inhibition of Wnt/β-catenin signaling. Biomaterials. 2020;232:119709. doi:10.1016/j.biomaterials.2019.119709
  • Wu S, Butt HJ. Near-infrared-sensitive materials based on upconverting nanoparticles. Adv Mater. 2016;28(6):1208–1226. doi:10.1002/adma.201502843
  • Zhang H, Jiao X, Chen Q, et al. A multi-functional nanoplatform for tumor synergistic phototherapy. Nanotechnology. 2016;27(8):085104. doi:10.1088/0957-4484/27/8/085104
  • Xu J, Kuang Y, Lv R, et al. Charge convertibility and near infrared photon co-enhanced cisplatin chemotherapy based on upconversion nanoplatform. Biomaterials. 2017;130:42–55. doi:10.1016/j.biomaterials.2017.03.041
  • Yong Y, Zhou L, Zhang S, et al. Gadolinium polytungstate nanoclusters: a new theranostic with ultrasmall size and versatile properties for dual-modal MR/CT imaging and photothermal therapy/radiotherapy of cancer. NPG Asia Mater. 2016;8(5):e273. doi:10.1038/am.2016.63
  • Yu J, Yin W, Peng T, et al. Biodistribution, excretion, and toxicity of polyethyleneimine modified NaYF(4): yb, Erupconversion nanoparticles in mice via different administration routes. Nanoscale. 2017;9(13):4497–4507. doi:10.1039/c7nr00078b
  • Dong X, Yin W, Zhang X, et al. Intelligent MoS(2) nanotheranostic for targeted and enzyme-/pH-/NIR-responsive drug delivery to overcome cancer chemotherapy resistance guided by PET imaging. ACS Appl Mater Interfaces. 2018;10(4):4271–4284. doi:10.1021/acsami.7b17506
  • Wang S, Li X, Chen Y, et al. A facile one-pot synthesis of a two-dimensional MoS2/Bi2S3 composite theranostic nanosystem for multi-modality tumor imaging and therapy. Adv Mater. 2015;27(17):2775–2782. doi:10.1002/adma.201500870
  • Zhao X, Yang CX, Chen LG, Yan XP. Dual-stimuli responsive and reversibly activatable theranostic nanoprobe for precision tumor-targeting and fluorescence-guided photothermal therapy. Nat Commun. 2017;8:14998. doi:10.1038/ncomms14998
  • Poulose AC, Veeranarayanan S, Mohamed MS, et al. Multi-stimuli responsive Cu2S nanocrystals as trimodal imaging and synergistic chemo-photothermal therapy agents. Nanoscale. 2015;7(18):8378–8388. doi:10.1039/c4nr07139e
  • Cao H, Yang Y, Chen X, Shao Z. Intelligent Janus nanoparticles for intracellular real-time monitoring of dual drug release. Nanoscale. 2016;8(12):6754–6760. doi:10.1039/c6nr00987e
  • Lai J, Shah BP, Garfunkel E, Lee KB. Versatile fluorescence resonance energy transfer-based mesoporous silica nanoparticles for real-time monitoring of drug release. ACS Nano. 2013;7(3):2741–2750. doi:10.1021/nn400199t
  • Huang J, Zong C, Shen H, Cao Y, Ren B, Zhang Z. Tracking the intracellular drug release from graphene oxide using surface-enhanced Raman spectroscopy. Nanoscale. 2013;5(21):10591–10598. doi:10.1039/c3nr03264g
  • Kim H, Kim J, Lee M, Choi HC, Kim WJ. Stimuli-regulated enzymatically degradable smart graphene-oxide-polymer nanocarrier facilitating photothermal gene delivery. Adv Healthcare Mater. 2016;5(15):1918–1930. doi:10.1002/adhm.201600246
  • Ye S, Wang F, Fan Z, et al. Light/pH-triggered biomimetic red blood cell membranes camouflaged small molecular drug assemblies for imaging-guided combinational chemo-photothermal therapy. ACS Appl Mater Interfaces. 2019;11(17):15262–15275. doi:10.1021/acsami.9b00897
  • Ao L, Wu C, Liu K, et al. Polydopamine-derivated hierarchical nanoplatforms for efficient dual-modal imaging-guided combination in vivo cancer therapy. ACS Appl Mater Interfaces. 2018;10(15):12544–12552. doi:10.1021/acsami.8b02973
  • Hayashi K, Maruhashi T, Nakamura M, Sakamoto W, Yogo T. One-pot synthesis of dual stimulus-responsive degradable hollow hybrid nanoparticles for image-guided trimodal therapy. Adv Funct Mater. 2016;26(47):8613–8622. doi:10.1002/adfm.201603394
  • Fang S, Lin J, Li C, et al. Dual-stimuli responsive nanotheranostics for multimodal imaging guided trimodal synergistic therapy. Small. 2017;13(6). doi:10.1002/smll.201602580
  • Zhou Z, Hu K, Ma R, et al. Dendritic platinum-copper alloy nanoparticles as theranostic agents for multimodal imaging and combined chemophotothermal therapy. Adv Funct Mater. 2016;26(33):5971–5978. doi:10.1002/adfm.201601754
  • Lin X, Song X, Zhang Y, et al. Multifunctional theranostic nanosystems enabling photothermal-chemo combination therapy of triple-stimuli-responsive drug release with magnetic resonance imaging. Biomater Sci. 2020;8(7):1875–1884. doi:10.1039/c9bm01482a
  • Sun S, Chen Q, Tang Z, et al. Tumor microenvironment stimuli-responsive fluorescence imaging and synergistic cancer therapy by Carbon-Dot-Cu nanoassemblies. Angew Chem. 2020. doi:10.1002/anie.202007786
  • Massoumi B, Farnudiyan-Habibi A, Derakhshankhah H, et al. theranosticA novel multi-stimuli-responsive nanomedicine based on FeO@Au nanoparticles against cancer. Drug Dev Ind Pharm. 2020:1–12. doi:10.1080/03639045.2020.1821052.
  • Gou S, Yang J, Ma Y, et al. Multi-responsive nanococktails with programmable targeting capacity for imaging-guided mitochondrial phototherapy combined with chemotherapy. J Control Release. 2020;327:371–383. doi:10.1016/j.jconrel.2020.08.014
  • Kuang Y, Zhang Y, Zhao Y, et al. Dual-stimuli-responsive multifunctional GdHfO nanoparticles for MRI-guided combined chemo-/photothermal-/radiotherapy of resistant tumors. ACS Appl Mater Interfaces. 2020;12(32):35928–35939. doi:10.1021/acsami.0c09422
  • Kang S, Baskaran R, Ozlu B, et al. T-positive Mn-doped multi-stimuli responsive poly(L-DOPA) nanoparticles for photothermal and photodynamic combination cancer therapy. Biomedicines. 2020;8(10):417. doi:10.3390/biomedicines8100417
  • Wang J, Chang Y, Luo H, et al. Designing immunogenic nanotherapeutics for photothermal-triggered immunotherapy involving reprogramming immunosuppression and activating systemic antitumor responses. Biomaterials. 2020;255. doi:10.1016/j.biomaterials.2020.120153
  • Topalian SL, Taube JM, Anders RA, Pardoll DM. Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy. Nat Rev Cancer. 2016;16(5):275–287. doi:10.1038/nrc.2016.36
  • Sau S, Alsaab HO, Bhise K, Alzhrani R, Nabil G, Iyer AK. Multifunctional nanoparticles for cancer immunotherapy: a groundbreaking approach for reprogramming malfunctioned tumor environment. J Control Release. 2018;274:24–34. doi:10.1016/j.jconrel.2018.01.028
  • Selvan SR, Dowling JP, Kelly WK, Lin J. Indoleamine 2,3-dioxygenase (IDO): biology and target in cancer immunotherapies. Curr Cancer Drug Targets. 2016;16(9):755–764. doi:10.2174/1568009615666151030102250
  • Cheng K, Ding Y, Zhao Y, et al. Sequentially responsive therapeutic peptide assembling nanoparticles for dual-targeted cancer immunotherapy. Nano Lett. 2018;18(5):3250–3258. doi:10.1021/acs.nanolett.8b01071
  • Ding Y, Ji T, Zhao Y, et al. Improvement of stability and efficacy of C16Y therapeutic peptide via molecular self-assembly into tumor-responsive nanoformulation. Mol Cancer Ther. 2015;14(10):2390–2400. doi:10.1158/1535-7163.Mct-15-0484
  • Chen DS, Mellman I. Elements of cancer immunity and the cancer-immune set point. Nature. 2017;541(7637):321–330. doi:10.1038/nature21349
  • Feng B, Zhou F, Hou B, et al. Binary cooperative prodrug nanoparticles improve immunotherapy by synergistically modulating immune tumor microenvironment. Adv Mater. 2018;30(38). doi:10.1002/adma.201803001
  • Zheng D-W, Chen J-L, Zhu J-Y, et al. Highly integrated nano-platform for breaking the barrier between chemotherapy and immunotherapy. Nano Lett. 2016;16(7):4341–4347. doi:10.1021/acs.nanolett.6b01432
  • Hou B, Zhou L, Wang H, et al. Engineering stimuli-activatable boolean logic prodrug nanoparticles for combination cancer immunotherapy. Adv Mater. 2020;32(12):e1907210. doi:10.1002/adma.201907210
  • Huynh E, Leung BY, Helfield BL, et al. In situ conversion of porphyrin microbubbles to nanoparticles for multimodality imaging. Nat Nanotechnol. 2015;10(4):325–332. doi:10.1038/nnano.2015.25
  • Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity. 2011;34(5):637–650. doi:10.1016/j.immuni.2011.05.006
  • Yin T, He S, Wang Y. Toll-like receptor 7/8 agonist, R848, exhibits antitumoral effects in a breast cancer model. Mol Med Rep. 2015;12(3):3515–3520. doi:10.3892/mmr.2015.3885
  • Liu Y, Qiao L, Zhang S, et al. Dual pH-responsive multifunctional nanoparticles for targeted treatment of breast cancer by combining immunotherapy and chemotherapy. Acta Biomater. 2018;66:310–324. doi:10.1016/j.actbio.2017.11.010
  • Hu Q, Chen Q, Gu Z. Advances in transformable drug delivery systems. Biomaterials. 2018;178:546–558. doi:10.1016/j.biomaterials.2018.03.056
  • 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/m(2). Ann Oncol. 2000;11(8):1029–1033. doi:10.1023/a:1008365716693
  • Blanco E, Shen H, Ferrari M. Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat Biotechnol. 2015;33(9):941–951. doi:10.1038/nbt.3330
  • Yan L, Shen J, Wang J, Yang X, Dong S, Lu S. Nanoparticle-based drug delivery system: a patient-friendly chemotherapy for oncology. Dose Response. 2020;18(3):1559325820936161. doi:10.1177/1559325820936161
  • Barnes LD, Giuliano EA, Ota J. Cellular localization of Visudyne as a function of time after local injection in an in vivo model of squamous cell carcinoma: an investigation into tumor cell death. Vet Ophthalmol. 2010;13(3):158–165. doi:10.1111/j.1463-5224.2010.00775.x
  • Caster JM, Patel AN, Zhang T, Wang A. Investigational nanomedicines in 2016: a review of nanotherapeutics currently undergoing clinical trials. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2017;9(1):e1416. doi:10.1002/wnan.1416
  • Liu D, Yang F, Xiong F, Gu N. The smart drug delivery system and its clinical potential. Theranostics. 2016;6(9):1306–1323. doi:10.7150/thno.14858
  • Ventola CL. Progress in nanomedicine: approved and investigational nanodrugs. P T. 2017;42(12):742–755.
  • Du J, Lane LA, Nie S. Stimuli-responsive nanoparticles for targeting the tumor microenvironment. J Control Release. 2015;219:205–214. doi:10.1016/j.jconrel.2015.08.050
  • Dai Y, Xu C, Sun X, Chen X. Nanoparticle design strategies for enhanced anticancer therapy by exploiting the tumour microenvironment. Chem Soc Rev. 2017;46(12):3830–3852. doi:10.1039/c6cs00592f