{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,15]],"date-time":"2026-11-15T06:59:59Z","timestamp":1794725999017,"version":"4.9.1"},"reference-count":52,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,3,19]],"date-time":"2021-03-19T00:00:00Z","timestamp":1616112000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2021,3,19]],"date-time":"2021-03-19T00:00:00Z","timestamp":1616112000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31800811"],"award-info":[{"award-number":["31800811"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81873987"],"award-info":[{"award-number":["81873987"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002858","name":"China Postdoctoral Science Foundation","doi-asserted-by":"publisher","award":["2019M653353"],"award-info":[{"award-number":["2019M653353"]}],"id":[{"id":"10.13039\/501100002858","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005230","name":"Natural Science Foundation of Chongqing","doi-asserted-by":"publisher","award":["cstc2019jcyj-msxmX0248"],"award-info":[{"award-number":["cstc2019jcyj-msxmX0248"]}],"id":[{"id":"10.13039\/501100005230","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Nanobiotechnol"],"published-print":{"date-parts":[[2021,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>Osteosarcoma (OS) is the most common primary malignant bone tumor occurring in children and young adults. Drug-resistant osteosarcoma often results in chemotherapy failure. Therefore, new treatments aimed at novel therapeutic targets are urgently needed for the treatment of drug-resistant osteosarcoma. Mitochondria-targeted phototherapy, i.e., synergistic photodynamic\/photothermal therapy, has emerged as a highly promising strategy for treating drug-resistant tumors. This study proposed a new nano-drug delivery system based on near-infrared imaging and multifunctional graphene, which can target mitochondria and show synergistic phototherapy, with preferential accumulation in tumors.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods and results<\/jats:title>\n                    <jats:p>Based on our previous study, (4-carboxybutyl) triphenyl phosphonium bromide (TPP), a mitochondria-targeting ligand, was conjugated to indocyanine green (ICG)-loaded, polyethylenimine-modified PEGylated nanographene oxide sheets (TPP-PPG@ICG) to promote mitochondrial accumulation after cellular internalization. Thereafter, exposure to a single dose of near-infrared irradiation enabled synergistic photodynamic and photothermal therapy, which simultaneously inhibited adenosine triphosphate synthesis and mitochondrial function. Induction of intrinsic apoptosis assisted in surmounting drug resistance and caused tumor cell death. After fluorescence imaging-guided synergistic phototherapy, the mitochondria-targeting, multifunctional graphene-based, drug-delivery system showed highly selective anticancer efficiency in vitro and in vivo, resulting in marked inhibition of tumor progression without noticeable toxicity in mice bearing doxorubicin-resistant MG63 tumor cells.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>The mitochondria-targeting TPP-PPG@ICG nanocomposite constitutes a new class of nanomedicine for fluorescence imaging-guided synergistic phototherapy and shows promise for treating drug-resistant osteosarcoma.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s12951-021-00831-6","type":"journal-article","created":{"date-parts":[[2021,3,19]],"date-time":"2021-03-19T16:10:50Z","timestamp":1616170250000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":74,"title":["Mitochondria-targeting graphene oxide nanocomposites for fluorescence imaging-guided synergistic phototherapy of drug-resistant osteosarcoma"],"prefix":"10.1186","volume":"19","author":[{"given":"Wei-Nan","family":"Zeng","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiu-Ping","family":"Yu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Duan","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jun-Li","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qing-Jun","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zong-Ke","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7017-7352","authenticated-orcid":false,"given":"Yi-Ping","family":"Zeng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,3,19]]},"reference":[{"key":"831_CR1","doi-asserted-by":"publisher","first-page":"3853","DOI":"10.2147\/IJN.S150017","volume":"13","author":"F Haghiralsadat","year":"2018","unstructured":"Haghiralsadat F, Amoabediny G, Naderinezhad S, Zandieh-Doulabi B, Forouzanfar T, Helder MN. Codelivery of doxorubicin and JIP1 siRNA with novel EphA2-targeted PEGylated cationic nanoliposomes to overcome osteosarcoma multidrug resistance. Int J Nanomed. 2018;13:3853\u201366.","journal-title":"Int J Nanomed"},{"key":"831_CR2","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1007\/s11864-008-0057-1","volume":"9","author":"SS Bielack","year":"2008","unstructured":"Bielack SS, Carrle D, Hardes J, Schuck A, Paulussen M. Bone tumors in adolescents and young adults. Curr Treat Options Oncol. 2008;9:67\u201380.","journal-title":"Curr Treat Options Oncol"},{"key":"831_CR3","doi-asserted-by":"publisher","first-page":"673","DOI":"10.2217\/fon-2016-0519","volume":"13","author":"CM Hattinger","year":"2017","unstructured":"Hattinger CM, Fanelli M, Tavanti E, Vella S, Riganti C, Picci P, Serra M. Doxorubicin-resistant osteosarcoma: novel therapeutic approaches in sight? Future Oncol. 2017;13:673\u20137.","journal-title":"Future Oncol"},{"issue":"3","key":"831_CR4","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1517\/14728214.2015.1051965","volume":"20","author":"CM Hattinger","year":"2015","unstructured":"Hattinger CM, Fanelli M, Tavanti E, Vella S, Ferrari S, Picci P, Serra M. Advances in emerging drugs for osteosarcoma. Expert Opin Emerg Drugs. 2015;20(3):495\u2013514.","journal-title":"Expert Opin Emerg Drugs"},{"issue":"29","key":"831_CR5","doi-asserted-by":"publisher","first-page":"7204","DOI":"10.1016\/j.biomaterials.2013.06.007","volume":"34","author":"HW Yang","year":"2013","unstructured":"Yang HW, Lu YJ, Lin KJ, Hsu SC, Huang CY, She SH, Liu HL, Lin CW, Xiao MC, Wey SP, Chen PY, Yen TC, Wei KC, Ma CC. EGRF conjugated PEGylated nanographene oxide for targeted chemotherapy and photothermal therapy. Biomaterials. 2013;34(29):7204\u201314.","journal-title":"Biomaterials"},{"key":"831_CR6","doi-asserted-by":"publisher","first-page":"755","DOI":"10.1038\/nrc2499","volume":"8","author":"JE Visvader","year":"2008","unstructured":"Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer. 2008;8:755\u201368.","journal-title":"Nat Rev Cancer"},{"issue":"6","key":"831_CR7","doi-asserted-by":"publisher","first-page":"500","DOI":"10.1016\/j.tcb.2019.02.004","volume":"29","author":"YC Wong","year":"2019","unstructured":"Wong YC, Kim S, Peng W, Krainc D. Regulation and function of mitochondria-lysosome membrane contact sites in cellular homeostasis. Trends Cell Biol. 2019;29(6):500\u201313.","journal-title":"Trends Cell Biol"},{"key":"831_CR8","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1038\/s41580-019-0173-8","volume":"21","author":"FJ Bock","year":"2020","unstructured":"Bock FJ, Tait SWG. Mitochondria as multifaceted regulators of cell death. Nat Rev Mol Cell Biol. 2020;21:85\u2013100.","journal-title":"Nat Rev Mol Cell Biol"},{"key":"831_CR9","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1038\/s41586-019-1715-0","volume":"575","author":"M Momcilovic","year":"2019","unstructured":"Momcilovic M, Jones A, Bailey ST, Waldmann CM, Li R, Lee JT, Abdelhady G, Gomez A, Holloway T, Schmid E, Stout D, Fishbein MC, Stiles L, Dabir DV, Dubinett SM, Christofk H, Shirihai O, Koehler CM, Sadeghi S, Shackelford DB. In vivo imaging of mitochondrial membrane potential in non-small-cell lung cancer. Nature. 2019;575:380\u20134.","journal-title":"Nature"},{"key":"831_CR10","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.jconrel.2015.10.023","volume":"240","author":"P Lu","year":"2016","unstructured":"Lu P, Bruno BJ, Rabenau M, Lim CS. Delivery of drugs and macromolecules to the mitochondria for cancer therapy. J Control Release. 2016;240:38\u201351.","journal-title":"J Control Release"},{"issue":"23","key":"831_CR11","doi-asserted-by":"publisher","first-page":"7739","DOI":"10.1002\/ange.201901699","volume":"131","author":"P Yuan","year":"2019","unstructured":"Yuan P, Mao X, Wu X, Liew SS, Li L, Yao SQ. Mitochondria-targeting, intracellular delivery of native proteins using biodegradable silica nanoparticles. Angew Chem Int Ed Engl. 2019;131(23):7739\u201343.","journal-title":"Angew Chem Int Ed Engl"},{"key":"831_CR12","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1016\/j.biomaterials.2016.11.056","volume":"117","author":"S Chen","year":"2017","unstructured":"Chen S, Lei Q, Qiu WX, Liu LH, Zheng DW, Fan JX, Rong L, Sun YX, Zhang XZ. Mitochondria-targeting \u201cNanoheater\u201d for enhanced photothermal\/chemo-therapy. Biomaterials. 2017;117:92\u2013104.","journal-title":"Biomaterials"},{"key":"831_CR13","doi-asserted-by":"publisher","first-page":"119219","DOI":"10.1016\/j.biomaterials.2019.05.030","volume":"213","author":"T Qi","year":"2019","unstructured":"Qi T, Chen B, Wang Z, Du H, Liu D, Yin Q, Liu B, Zhang Q, Wang Y. A pH-activatable nanoparticle for dual-stage precisely mitochondria-targeted photodynamic anticancer therapy. Biomaterials. 2019;213:119219.","journal-title":"Biomaterials"},{"issue":"46","key":"831_CR14","doi-asserted-by":"publisher","first-page":"e1905825","DOI":"10.1002\/adma.201905825","volume":"31","author":"S Yan","year":"2019","unstructured":"Yan S, Zeng X, Tang Y, Liu BF, Wang Y, Liu X. Activating antitumor immunity and antimetastatic effect through polydopamine-encapsulated core-shell upconversion nanoparticles. Adv Mater. 2019;31(46):e1905825.","journal-title":"Adv Mater"},{"issue":"16","key":"831_CR15","doi-asserted-by":"publisher","first-page":"4656","DOI":"10.1016\/j.biomaterials.2014.02.018","volume":"35","author":"M Guo","year":"2014","unstructured":"Guo M, Mao H, Li Y, Zhu A, He H, Yang H, Wang Y, Tian X, Ge C, Peng Q, Wang X, Yang X, Chen X, Liu G, Chen H. Dual imaging-guided photothermal\/photodynamic therapy using micelles. Biomaterials. 2014;35(16):4656\u201366.","journal-title":"Biomaterials"},{"issue":"8","key":"831_CR16","doi-asserted-by":"publisher","first-page":"1800049","DOI":"10.1002\/advs.201800049","volume":"5","author":"L Zhang","year":"2018","unstructured":"Zhang L, Wang D, Yang K, Sheng D, Tan B, Wang Z, Ran H, Yi H, Zhong Y, Lin H, Chen Y. Mitochondria-targeted artificial \u201cNano-RBCs\u201d for amplified synergistic cancer phototherapy by a single NIR irradiation. Adv Sci. 2018;5(8):1800049.","journal-title":"Adv Sci"},{"issue":"4","key":"831_CR17","doi-asserted-by":"publisher","first-page":"250","DOI":"10.3322\/caac.20114","volume":"61","author":"P Agostinis","year":"2011","unstructured":"Agostinis P, Berg K, Cengel KA, Foster TH, Girotti AW, Gollnick SO, Hahn SM, Hamblin MR, Juzeniene A, Kessel D, Korbelik M, Moan J, Mroz P, Nowis D, Piette J, Wilson BC, Golab J. Photodynamic therapy of cancer: an update. CA Cancer J Clin. 2011;61(4):250\u201381.","journal-title":"CA Cancer J Clin"},{"issue":"4","key":"831_CR18","doi-asserted-by":"publisher","first-page":"2475","DOI":"10.1021\/acs.nanolett.8b00040","volume":"18","author":"G Yang","year":"2018","unstructured":"Yang G, Xu L, Xu J, Zhang R, Song G, Chao Y, Feng L, Han F, Dong Z, Li B, Liu Z. Smart nanoreactors for pH-responsive tumor homing, mitochondria-targeting, and enhanced photodynamic-immunotherapy of cancer. Nano Lett. 2018;18(4):2475\u201384.","journal-title":"Nano Lett"},{"issue":"33","key":"831_CR19","doi-asserted-by":"publisher","first-page":"4541","DOI":"10.1002\/smll.201601094","volume":"12","author":"R Guo","year":"2016","unstructured":"Guo R, Peng H, Tian Y, Shen S, Yang W. Mitochondria-targeting magnetic composite nanoparticles for enhanced phototherapy of cancer. Small. 2016;12(33):4541\u201352.","journal-title":"Small"},{"issue":"12","key":"831_CR20","doi-asserted-by":"publisher","first-page":"3596","DOI":"10.1021\/acsbiomaterials.7b00480","volume":"3","author":"GY Pan","year":"2017","unstructured":"Pan GY, Jia HR, Zhu YX, Wang RH, Wu FG, Chen Z. Dual channel activatable cyanine dye for mitochondrial imaging and mitochondria-targeted cancer theranostics. ACS Biomater Sci Eng. 2017;3(12):3596\u2013606.","journal-title":"ACS Biomater Sci Eng"},{"issue":"3","key":"831_CR21","doi-asserted-by":"publisher","first-page":"1801122","DOI":"10.1002\/advs.201801122","volume":"6","author":"X Zhang","year":"2019","unstructured":"Zhang X, Du J, Guo Z, Yu J, Gao Q, Yin W, Zhu S, Gu Z, Zhao Y. Efficient near infrared light triggered nitric oxide release nanocomposites for sensitizing mild photothermal therapy. Adv Sci. 2019;6(3):1801122.","journal-title":"Adv Sci"},{"issue":"12","key":"831_CR22","doi-asserted-by":"publisher","first-page":"12310","DOI":"10.1021\/nn5062386","volume":"8","author":"Z Sheng","year":"2014","unstructured":"Sheng Z, Hu D, Zheng M, Zhao P, Liu H, Gao D, Gong P, Gao G, Zhang P, Ma Y, Cai L. Smart human serum albumin-indocyanine green nanoparticles generated by programmed assembly for dual-modal imaging-guided cancer synergistic phototherapy. ACS Nano. 2014;8(12):12310\u201322.","journal-title":"ACS Nano"},{"issue":"22","key":"831_CR23","doi-asserted-by":"publisher","first-page":"3055","DOI":"10.1002\/adma.201204623","volume":"25","author":"S Wang","year":"2013","unstructured":"Wang S, Huang P, Nie L, Xing R, Liu D, Wang Z, Lin J, Chen S, Niu G, Lu G, Chen X. Single continuous wave laser induced photodynamic\/plasmonic photothermal therapy using photosensitizer-functionalized gold nanostars. Adv Mater. 2013;25(22):3055\u201361.","journal-title":"Adv Mater"},{"issue":"47","key":"831_CR24","doi-asserted-by":"publisher","first-page":"12558","DOI":"10.1002\/ange.201307358","volume":"125","author":"P Kalluru","year":"2013","unstructured":"Kalluru P, Vankayala R, Chiang CS, Hwang KC. Photosensitization of singlet oxygen and in vivo photodynamic therapeutic effects mediated by PEGylated W18O49 nanowires. Angew Chem Int Ed Engl. 2013;125(47):12558\u201362.","journal-title":"Angew Chem Int Ed Engl"},{"issue":"43","key":"831_CR25","doi-asserted-by":"publisher","first-page":"1704196","DOI":"10.1002\/adma.201704196","volume":"29","author":"X Tan","year":"2017","unstructured":"Tan X, Luo S, Long L, Wang Y, Wang D, Fang S, Ouyang Q, Su Y, Cheng T, Shi C. Structure-guided design and synthesis of a mitochondria-targeting near-infrared fluorophore with multimodal therapeutic activities. Adv Mater. 2017;29(43):1704196.","journal-title":"Adv Mater"},{"issue":"28","key":"831_CR26","doi-asserted-by":"publisher","first-page":"e1707567","DOI":"10.1002\/adma.201707567","volume":"30","author":"W Shan","year":"2018","unstructured":"Shan W, Chen R, Zhang Q, Zhao J, Chen B, Zhou X, Ye S, Bi S, Nie L, Ren L. Improved stable indocyanine green (ICG)-mediated cancer optotheranostics with naturalized hepatitis B core particles. Adv Mater. 2018;30(28):e1707567.","journal-title":"Adv Mater"},{"issue":"12","key":"831_CR27","doi-asserted-by":"publisher","first-page":"3595","DOI":"10.1021\/mp300472y","volume":"9","author":"E Portnoy","year":"2012","unstructured":"Portnoy E, Gurina M, Magdassi S, Eyal S. Evaluation of the near infrared compound indocyanine green as a probe substrate of p-glycoprotein. Mol Pharm. 2012;9(12):3595\u2013601.","journal-title":"Mol Pharm"},{"issue":"12","key":"831_CR28","doi-asserted-by":"publisher","first-page":"2190","DOI":"10.1039\/C6TB00108D","volume":"4","author":"YP Zeng","year":"2016","unstructured":"Zeng YP, Luo SL, Yang ZY, Huang JW, Li R. A folic acid conjugated polyethylenimine-modified PEGylated nanographene loaded photosensitizer: photodynamic therapy and toxicity studies in vitro and in vivo. J Mater Chem B. 2016;4(12):2190\u20138.","journal-title":"J Mater Chem B"},{"issue":"71","key":"831_CR29","doi-asserted-by":"publisher","first-page":"57725","DOI":"10.1039\/C5RA07535A","volume":"5","author":"YP Zeng","year":"2015","unstructured":"Zeng YP, Yang ZY, Luo SL, Li H, Liu C, Hao YH, Liu J, Wang WD, Li R. Fast and facile preparation of PEGylated graphene from graphene oxide by lysosome targeting delivery of photosensitizer to efficiently enhance photodynamic therapy. RSC Adv. 2015;5(71):57725\u201334.","journal-title":"RSC Adv"},{"key":"831_CR30","doi-asserted-by":"publisher","first-page":"43506","DOI":"10.1038\/srep43506","volume":"7","author":"YP Zeng","year":"2017","unstructured":"Zeng YP, Yang ZY, Li H, Hao YH, Liu C, Zhu L, Liu J, Lu BH, Li R. Multifunctional nanographene oxide for targeted gene-mediated thermochemotherapy of drug-resistant tumour. Sci Rep. 2017;7:43506.","journal-title":"Sci Rep"},{"issue":"27","key":"831_CR31","doi-asserted-by":"publisher","first-page":"17176","DOI":"10.1021\/acsami.6b05383","volume":"8","author":"SL Luo","year":"2016","unstructured":"Luo SL, Yang ZY, Tan X, Wang Y, Zeng YP, Wang Y, Li C, Li R, Shi CM. Multifunctional photosensitizer grafted on polyethylene glycol and polyethylenimine dual-functionalized nanographene oxide for cancer-targeted near-infrared imaging and synergistic phototherapy. ACS Appl Mater Interfaces. 2016;8(27):17176\u201386.","journal-title":"ACS Appl Mater Interfaces"},{"issue":"11","key":"831_CR32","doi-asserted-by":"publisher","first-page":"1989","DOI":"10.1002\/smll.201202538","volume":"9","author":"L Feng","year":"2013","unstructured":"Feng L, Yang X, Shi X, Tan X, Peng R, Wang J, Liu Z. Polyethylene glycol and polyethylenimine dual-functionalized nano-graphene oxide for photothermally enhanced gene delivery. Small. 2013;9(11):1989\u201397.","journal-title":"Small"},{"issue":"33","key":"831_CR33","doi-asserted-by":"publisher","first-page":"8555","DOI":"10.1016\/j.biomaterials.2011.07.071","volume":"32","author":"W Zhang","year":"2011","unstructured":"Zhang W, Guo Z, Huang D, Liu Z, Guo X, Zhong H. Synergistic effect of chemo-photothermal therapy using PEGylated graphene oxide. Biomaterials. 2011;32(33):8555\u201361.","journal-title":"Biomaterials"},{"issue":"1","key":"831_CR34","doi-asserted-by":"publisher","first-page":"516","DOI":"10.1021\/nn1024303","volume":"5","author":"K Yang","year":"2011","unstructured":"Yang K, Wan J, Zhang S, Zhang Y, Lee ST, Liu Z. In vivo pharmacokinetics, long-term biodistribution, and toxicology of PEGylated graphene in mice. ACS Nano. 2011;5(1):516\u201322.","journal-title":"ACS Nano"},{"issue":"21","key":"831_CR35","doi-asserted-by":"publisher","first-page":"17617","DOI":"10.1021\/acsami.8b03185","volume":"10","author":"R Zhao","year":"2018","unstructured":"Zhao R, Kong W, Sun M, Yang Y, Liu W, Lv M, Song S, Wang L, Song H, Hao R. Highly stable graphene-based nanocomposite (GO-PEI-Ag) with broad-spectrum, long-term antimicrobial activity and antibiofilm effects. ACS Appl Mater Interfaces. 2018;10(21):17617\u201329.","journal-title":"ACS Appl Mater Interfaces"},{"issue":"2","key":"831_CR36","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1016\/j.cmet.2015.11.014","volume":"23","author":"A Logan","year":"2016","unstructured":"Logan A, Pell VR, Shaffer KJ, Evans C, Stanley NJ, Robb EL, Prime TA, Chouchani ET, Cocheme HM, Fearnley IM, Vidoni S, James AM, Porteous CM, Partridge L, Krieg T, Smith RA, Murphy MP. Assessing the mitochondrial membrane potential in cells and in vivo using targeted click chemistry and mass spectrometry. Cell Metab. 2016;23(2):379\u201385.","journal-title":"Cell Metab"},{"issue":"8","key":"831_CR37","doi-asserted-by":"publisher","first-page":"4806","DOI":"10.1021\/nn1006368","volume":"4","author":"DC Marcano","year":"2010","unstructured":"Marcano DC, Kosynkin DV, Berlin JM, Sinitskii A, Sun Z, Slesarev A, Alemany LB, Lu W, Tour JM. Improved synthesis of graphene oxide. ACS Nano. 2010;4(8):4806\u201314.","journal-title":"ACS Nano"},{"issue":"25","key":"831_CR38","doi-asserted-by":"publisher","first-page":"6612","DOI":"10.1016\/j.biomaterials.2010.05.007","volume":"31","author":"C Zhang","year":"2010","unstructured":"Zhang C, Liu T, Su Y, Luo S, Zhu Y, Tan X, Fan S, Zhang L, Zhou Y, Cheng T, Shi C. A near-infrared fluorescent heptamethine indocyanine dye with preferential tumor accumulation for in vivo imaging. Biomaterials. 2010;31(25):6612\u20137.","journal-title":"Biomaterials"},{"issue":"9","key":"831_CR39","doi-asserted-by":"publisher","first-page":"2314","DOI":"10.1021\/acs.accounts.8b00307","volume":"51","author":"C Feng","year":"2018","unstructured":"Feng C, Huang X. Polymer brushes: efficient synthesis and applications. Acc Chem Res. 2018;51(9):2314\u201323.","journal-title":"Acc Chem Res"},{"issue":"19","key":"831_CR40","doi-asserted-by":"publisher","first-page":"17268","DOI":"10.1021\/am505308f","volume":"6","author":"Z Xu","year":"2014","unstructured":"Xu Z, Wang S, Li Y, Wang M, Shi P, Huang X. Covalent functionalization of graphene oxide with biocompatible poly (ethylene glycol) for delivery of paclitaxel. ACS Appl Mater Interfaces. 2014;6(19):17268\u201376.","journal-title":"ACS Appl Mater Interfaces"},{"issue":"2","key":"831_CR41","doi-asserted-by":"publisher","first-page":"1355","DOI":"10.1021\/am507798d","volume":"7","author":"Z Xu","year":"2015","unstructured":"Xu Z, Zhu S, Wang M, Li Y, Shi P, Huang X. Delivery of paclitaxel using PEGylated graphene oxide as a nanocarrier. ACS Appl Mater Interfaces. 2015;7(2):1355\u201363.","journal-title":"ACS Appl Mater Interfaces"},{"issue":"27","key":"831_CR42","doi-asserted-by":"publisher","first-page":"17352","DOI":"10.1021\/acsami.6b05271","volume":"8","author":"Y Li","year":"2016","unstructured":"Li Y, Jian Z, Lang M, Zhang C, Huang X. Covalently functionalized graphene by radical polymers for graphene-based high-performance cathode materials. ACS Appl Mater Interfaces. 2016;8(27):17352\u20139.","journal-title":"ACS Appl Mater Interfaces"},{"issue":"17","key":"831_CR43","doi-asserted-by":"publisher","first-page":"14647","DOI":"10.1021\/acsami.7b01452","volume":"9","author":"Y Que","year":"2017","unstructured":"Que Y, Feng C, Lu G, Huang X. Polymer-coated ultrastable and biofunctionalizable lanthanide nanoparticle. ACS Appl Mater Interfaces. 2017;9(17):14647\u201355.","journal-title":"ACS Appl Mater Interfaces"},{"key":"831_CR44","doi-asserted-by":"publisher","first-page":"119569","DOI":"10.1016\/j.biomaterials.2019.119569","volume":"228","author":"Z Wang","year":"2020","unstructured":"Wang Z, Jia T, Sun Q, Kuang Y, Liu B, Xu M, Zhu H, He F, Gai S, Yang P. Construction of Bi\/phthalocyanine manganese nanocomposite for trimodal imaging directed photodynamic and photothermal therapy mediated by 808 nm light. Biomaterials. 2020;228:119569.","journal-title":"Biomaterials"},{"key":"831_CR45","doi-asserted-by":"publisher","first-page":"5381","DOI":"10.1039\/C9CS00309F","volume":"48","author":"JK Tee","year":"2019","unstructured":"Tee JK, Yip LX, Tan ES, Santitewagun S, Prasath A, Ke PC, Ho HK, Leong DT. Nanoparticles\u2019 interactions with vasculature in diseases. Chem Soc Rev. 2019;48:5381\u2013407.","journal-title":"Chem Soc Rev"},{"issue":"29","key":"831_CR46","doi-asserted-by":"publisher","first-page":"e1801216","DOI":"10.1002\/adma.201801216","volume":"30","author":"S Ye","year":"2018","unstructured":"Ye S, Rao J, Qiu S, Zhao J, He H, Yan Z, Yang T, Deng Y, Ke H, Yang H, Zhao Y, Guo Z, Chen H. Rational design of conjugated photosensitizers with controllable photoconversion for dually cooperative phototherapy. Adv Mater. 2018;30(29):e1801216.","journal-title":"Adv Mater"},{"issue":"2","key":"831_CR47","doi-asserted-by":"publisher","first-page":"954","DOI":"10.1016\/j.tiv.2013.01.016","volume":"27","author":"A Aranda","year":"2013","unstructured":"Aranda A, Sequedo L, Tolosa L, Quint\u00e1s G, Gombau L. Dichloro-dihydro-fluorescein diacetate (DCFH-DA) assay: a quantitative method for oxidative stress assessment of nanoparticle-treated cells. Toxicol In Vitro. 2013;27(2):954\u201363.","journal-title":"Toxicol In Vitro"},{"key":"831_CR48","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1007\/s10689-014-9757-9","volume":"14","author":"BB Zhang","year":"2015","unstructured":"Zhang BB, Wang DG, Guo FF, Xuan C. Mitochondrial membrane potential and reactive oxygen species in cancer stem cells. Fam Cancer. 2015;14:19\u201323.","journal-title":"Fam Cancer"},{"issue":"1","key":"831_CR49","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/j.toxlet.2007.02.013","volume":"170","author":"M Yu","year":"2007","unstructured":"Yu M, Shi Y, Wei X, Yang Y, Zhou Y, Hao X, Zhang N, Niu R. Depletion of mitochondrial DNA by ethidium bromide treatment inhibits the proliferation and tumorigenesis of T47D human breast cancer cells. Toxicol Lett. 2007;170(1):83\u201393.","journal-title":"Toxicol Lett"},{"issue":"1","key":"831_CR50","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1016\/j.ab.2017.07.009","volume":"552","author":"LD Zorova","year":"2018","unstructured":"Zorova LD, Popkov VA, Plotnikov EY, Silachev DN, Pevzner IB, Jankauskas SS, Babenko VA, Zorov SD, Balakireva AV, Juhaszova M, Sollott SJ, Zorov DB. Mitochondrial membrane potential. Anal Biochem. 2018;552(1):50\u20139.","journal-title":"Anal Biochem"},{"issue":"38","key":"831_CR51","doi-asserted-by":"publisher","first-page":"25060","DOI":"10.1021\/acsami.6b06522","volume":"8","author":"K Han","year":"2016","unstructured":"Han K, Zhu JY, Jia HZ, Wang SB, Li SY, Zhang XZ, Han HY. Mitochondria-targeted chimeric peptide for trinitarian overcoming of drug resistance. ACS Appl Mater Interfaces. 2016;8(38):25060\u20138.","journal-title":"ACS Appl Mater Interfaces"},{"issue":"3","key":"831_CR52","doi-asserted-by":"publisher","first-page":"523","DOI":"10.1016\/S0950-351X(05)80067-9","volume":"4","author":"HS Sherratt","year":"1990","unstructured":"Sherratt HS, Turnbull DM. Mitochondrial oxidations and ATP synthesis in muscle. Baillieres Clin Endocrinol Metab. 1990;4(3):523\u201360.","journal-title":"Baillieres Clin Endocrinol Metab"}],"container-title":["Journal of Nanobiotechnology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12951-021-00831-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/s12951-021-00831-6\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12951-021-00831-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,3,19]],"date-time":"2021-03-19T16:14:11Z","timestamp":1616170451000},"score":1,"resource":{"primary":{"URL":"https:\/\/jnanobiotechnology.biomedcentral.com\/articles\/10.1186\/s12951-021-00831-6"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,3,19]]},"references-count":52,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2021,12]]}},"alternative-id":["831"],"URL":"https:\/\/doi.org\/10.1186\/s12951-021-00831-6","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-142918\/v1","asserted-by":"object"}]},"ISSN":["1477-3155"],"issn-type":[{"value":"1477-3155","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,19]]},"assertion":[{"value":"4 January 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 March 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"19 March 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"All animal experiments were approved by the Ethics Committee of the Chongqing General Hospital in accordance with the guidelines on animal care and use.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate."}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"79"}}