Why nanodiamond carriers manage to overcome drug resistance in cancer

Abstract

Nanodiamonds represent an attractive potential carrier for anticancer drugs. The main advantages of nanodiamond particles with respect to medical applications are their high compatibility with non-cancerous cells, feasible surface decoration with therapeutic and cancer-cell targeting molecules, and their relatively low manufacturing cost. Additionally, nanodiamond carriers significantly increase treatment efficacy of the loaded drug, so anticancer drugs execute more effectively at a lower dose. Subsequently, lower drug dose results in less extensive side effects. The carriers decorated with a targeting molecule accumulate primarily in the tumor tissue, and those nanodiamond particles impair efflux of the drug from cancer cells. Therapeutic approaches considering nanodiamond carriers were already tested in vitro, as well as in vivo. Now, researchers focus particularly on the possible side effects of nanodiamond carriers applied systemically in vivo. The behavior of nanodiamond carriers depends heavily on their surface coatings, so each therapeutic complex must be evaluated separately. Generally, it seems that site-specific application of nanodiamond carriers is a rather safe therapeutic approach, but intravenous application needs further study. The benefits of nanodiamond carriers are remarkable and represent a potent approach to overcome the drug resistance of many cancers.

Keywords

Nanodiamond / drug carrier / drug resistance / cancer therapy / nanoparticles

References

[1] Alavi M.Passive and active targeting in cancer therapy by liposomes and lipid nanoparticles..Drug Metab Pers Ther2019;34:20180032

[2] Vladimis Y.Bringing again noble metal nanoparticles to the forefront of cancer therapy..Front Bioeng Biotechnol2018;6:143 PMCID:PMC6186777

[3] Marchesan S,Bianco A.The winding road for carbon nanotubes in nanomedicine..Mat Today2015;18:12-9

[4] Tsai LW,Perevedentseva E,Priezzhev A.Nanodiamonds for medical applications: interaction with blood in vitro and in vivo..Int J Mol Sci2016;17:1111 PMCID:PMC4964486

[5] Křivohlavá R,Jakobsen KQ.Knockdown of microRNA-135b in mammary carcinoma by targeted nanodiamonds: potentials and pitfalls of in vivo applications..Nanomaterials (Basel)2019;9:866 PMCID:PMC6632128

[6] Suarez-Kelly LP,Rampersaud IV,Wang MS.Fluorescent nanodiamonds engage innate immune effector cells: a potential vehicle for targeted anti-tumor immunotherapy..Nanomedicine2017;13:909-20 PMCID:PMC5405740

[7] Barnard AS.Diamond standard in diagnostics: nanodiamond biolabels make their mark..Analyst2009;134:1751-64

[8] Faklaris O,Irinopoulou T,Sennour M.Photoluminescent diamond nanoparticles for cell labeling: study of the uptake mechanism in mammalian cells..ACS Nano2009;3:3955-62

[9] Hui YY,Chang HC.Nanodiamonds for optical bioimaging..J Phys D Appl Phys2010;43:374021

[10] Lukowski S,Kinderman M,Mineva A.Fluorescent nanodiamonds are efficient, easy-to-use cyto-compatible vehicles for monitored delivery of non-coding regulatory RNAs..J Biomed Nanotechnol2018;14:946-58

[11] McGuinness LP,Stacey A,Hall LT.Quantum measurement and orientation tracking of fluorescent nanodiamonds inside living cells..Nat Nanotechnol2011;6:358-63

[12] Mochalin VN,Ho D.The properties and applications of nanodiamonds..Nat Nanotechnol2011;7:11-23

[13] Petrakova V,Buncek M,Ledvina M.Imaging of transfection and intracellular release of intact, non-labeled DNA using fluorescent nanodiamonds..Nanoscale2016;8:12002-12

[14] Kaur R.Nanodiamonds as novel nanomaterials for biomedical applications: drug delivery and imaging systems..Int J Nanomedicine2013;8:203-20 PMCID:PMC3544342

[15] Turcheniuk K.Biomedical applications of nanodiamond (Review)..Nanotechnology2017;28:252001

[16] Chang YR,Chen K,Tsai DS.Mass production and dynamic imaging of fluorescent nanodiamonds..Nat Nanotechnol2008;3:284-8

[17] Longmire M,Kobayashi H.Clearance properties of nano-sized particles and molecules as imaging agents: considerations and caveats..Nanomedicine (Lond)2008;3:703-17 PMCID:PMC3407669

[18] Fang J,Maeda H.The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect..Adv Drug Deliv Rev2011;63:136-51

[19] Yu M.Clearance pathways and tumor targeting of imaging nanoparticles..ACS Nano2015;9:6655-74 PMCID:PMC4955575

[20] Mohan N,Hsieh HH,Chang HC.In vivo imaging and toxicity assessments of fluorescent nanodiamonds in Caenorhabditis elegans..Nano Lett2010;10:3692-9

[21] Vaijayanthimala V,Yeh SH,Hsiao CH.The long-term stability and biocompatibility of fluorescent nanodiamond as an in vivo contrast agent..Biomaterials2012;33:7794-802

[22] Zheng T,Storm IM,Sprakel J.Recombinant protein polymers for colloidal stabilization and improvement of cellular uptake of diamond nanosensors..Anal Chem2017;89:12812-20

[23] Hemelaar SR,Bigot F,de Vries MP.The interaction of fluorescent nanodiamond probes with cellular media..Mikrochim Acta2017;184:1001-9 PMCID:PMC5346409

[24] Daniels TR,Rodríguez JA,Kozman M.The transferrin receptor and the targeted delivery of therapeutic agents against cancer..Biochim Biophys Acta2012;1820:291-317 PMCID:PMC3500658

[25] Chang LY,Barnard AS.Confirmation of the electrostatic self-assembly of nanodiamonds.Nanoscale.2011;3:958-62

[26] Chow EK.Implication of cancer stem cells in cancer drug development and drug delivery..J Lab Autom2013;18:6-11

[27] Chu Z,Zhang B,Fang CY.Unambiguous observation of shape effects on cellular fate of nanoparticles..Sci Rep2014;4:4495 PMCID:PMC3968459

[28] Puzyr A,Purtov K,Skobelev N.Nanodiamonds with novel properties: a biological study..Diam Relat Mater2007;16:5

[29] van der Laan K,Zheng T.Nanodiamonds for in vivo applications..Small2018;14:e1703838

[30] Hsiao WW,Tsai PC.Fluorescent nanodiamond: a versatile tool for long-term cell tracking, super-resolution imaging, and nanoscale temperature sensing..Acc Chem Res2016;49:400-7

[31] Gulka M,Varga B,Pall O.Simultaneous label-free live imaging of cell nucleus and luminescent nanodiamonds..Sci Rep2020;10:9791 PMCID:PMC7299945

[32] Gismondi A,Orlanducci S,Gay S.Nanodiamonds coupled with plant bioactive metabolites: a nanotech approach for cancer therapy..Biomaterials2015;38:22-35

[33] Martín R,Herance JR.Fenton-treated functionalized diamond nanoparticles as gene delivery system..ACS Nano2010;4:65-74

[34] Chen M,Man HB,Chow EK.Nanodiamond vectors functionalized with polyethylenimine for siRNA delivery..J Phys Chem Lett2010;1:3167-71

[35] Ho D,Chow EK.Nanodiamonds: the intersection of nanotechnology, drug development, and personalized medicine..Sci Adv2015;1:e1500439 PMCID:PMC4643796

[36] Lee DK,Liang Z,Miya D.Clinical validation of a nanodiamond-embedded thermoplastic biomaterial..Proc Natl Acad Sci U S A2017;114:E9445-54 PMCID:PMC5692571

[37] Nakamura Y,Choyke PL.Nanodrug delivery: is the enhanced permeability and retention effect sufficient for curing cancer?.Bioconjug Chem2016;27:2225-38 PMCID:PMC7397928

[38] Ramzy L,Metwally AA.Cancer nanotheranostics: a review of the role of conjugated ligands for overexpressed receptors..Eur J Pharm Sci2017;104:273-92

[39] Cersosimo RJ.Epirubicin: a review of the pharmacology, clinical activity, and adverse effects of an adriamycin analogue..J Clin Oncol1986;4:425-39

[40] Chow EK,Chen M,Robinson E.Nanodiamond therapeutic delivery agents mediate enhanced chemoresistant tumor treatment..Sci Transl Med2011;3:73ra21

[41] Lin YW,Liao WS,Liu KK.Co-delivery of paclitaxel and cetuximab by nanodiamond enhances mitotic catastrophe and tumor inhibition..Sci Rep2017;7:9814 PMCID:PMC5575327

[42] Moore LK,Osawa E,Ho D.Diamond-lipid hybrids enhance chemotherapeutic tolerance and mediate tumor regression..Adv Mater2013;25:3532-41 PMCID:PMC3872062

[43] Wang X,Hou W,Toh TB.Epirubicin-adsorbed nanodiamonds kill chemoresistant hepatic cancer stem cells..ACS Nano2014;8:12151-66 PMCID:PMC4334265

[44] Yuan SJ,Wang C,Xu HZ.Doxorubicin-polyglycerol-nanodiamond conjugate is a cytostatic agent that evades chemoresistance and reverses cancer-induced immunosuppression in triple-negative breast cancer..J Nanobiotechnology2019;17:110 PMCID:PMC6798483

[45] Huang H,Osawa E.Active nanodiamond hydrogels for chemotherapeutic delivery..Nano Lett2007;7:3305-14

[46] Lam R,Pierstorff E,Osawa E.Nanodiamond-embedded microfilm devices for localized chemotherapeutic elution..ACS Nano2008;2:2095-102

[47] Zhang XQ,Xu X,Kim HJ.Multimodal nanodiamond drug delivery carriers for selective targeting, imaging, and enhanced chemotherapeutic efficacy..Adv Mater2011;23:4770-5

[48] Madamsetty VS,Toma M,Gallud A.Tumor selective uptake of drug-nanodiamond complexes improves therapeutic outcome in pancreatic cancer..Nanomedicine2019;18:112-21 PMCID:PMC6588439

[49] Hoang Thi TT,Nguyen DH,Park KD.The importance of Poly(ethylene glycol) alternatives for overcoming PEG immunogenicity in drug delivery and bioconjugation..Polymers (Basel)2020;12:298 PMCID:PMC7077443

[50] Suliman S,Wu X,Pedersen TO.Release and bioactivity of bone morphogenetic protein-2 are affected by scaffold binding techniques in vitro and in vivo..J Control Release2015;197:148-57

[51] Manus LM,Waters EA,Schultz-Sikma EA.Gd(III)-nanodiamond conjugates for MRI contrast enhancement..Nano Lett2010;10:484-9 PMCID:PMC2829273

[52] Wu TJ,Chang WW,Kuo Y.Tracking the engraftment and regenerative capabilities of transplanted lung stem cells using fluorescent nanodiamonds..Nat Nanotechnol2013;8:682-9 PMCID:PMC7097076

[53] Lyakhovich A.Bypassing mechanisms of mitochondria-mediated cancer stem cells resistance to chemo- and radiotherapy..Oxid Med Cell Longev2016;2016:1716341 PMCID:PMC4677234

[54] Li L.Stem cell quiescence..Clin Cancer Res2011;17:4936-41 PMCID:PMC3410675

[55] Saha S,Bhattacharyya P,Sa G.Death by design: where curcumin sensitizes drug-resistant tumours..Anticancer Res2012;32:2567-84

[56] Sotiropoulou PA,Silvani A,Passarella D.Chemical approaches to targeting drug resistance in cancer stem cells..Drug Discov Today2014;19:1547-62

[57] Vinogradov S.Cancer stem cells and drug resistance: the potential of nanomedicine..Nanomedicine (Lond)2012;7:597-615 PMCID:PMC3376090

[58] Hill C.The importance of epithelial-mesenchymal transition and autophagy in cancer drug resistance..Cancer Drug Resist2020;3:38-47 PMCID:PMC7100899

[59] Wang Y,Rama M.Cell-mediated immune resistance in cancer..Cancer Drug Resist2020;3:232-51

[60] Sun Z,Li G,Huang Z.Relevance of two genes in the multidrug resistance of hepatocellular carcinoma: in vivo and clinical studies..Tumori2010;96:90-6

[61] Qin W,Chen Z.Nanomaterials in targeting cancer stem cells for cancer therapy..Front Pharmacol2017;8:1 PMCID:PMC5241315

[62] Stupp R.Targeting brain-tumor stem cells..Nat Biotechnol2007;25:193-4

[63] Hong IS,Lee HY.Targeting cancer stem cells by using the nanoparticles..Int J Nanomedicine2015;10:251-60 PMCID:PMC4583536

[64] Ali MS,Fahmy RH.Nanodiamonds: minuscule gems that ferry antineoplastic drugs to resistant tumors..Int J Pharm2019;558:165-76

[65] Chan MS,Leung HM.Cancer-cell-specific mitochondria-targeted drug delivery by dual-ligand-functionalized nanodiamonds circumvent drug resistance..ACS Appl Mater Interfaces2017;9:11780-9

[66] Batist G,Rao CS,Gutheil J.Reduced cardiotoxicity and preserved antitumor efficacy of liposome-encapsulated doxorubicin and cyclophosphamide compared with conventional doxorubicin and cyclophosphamide in a randomized, multicenter trial of metastatic breast cancer..J Clin Oncol2001;19:1444-54

[67] Toh TB,Hou W,Nguyen J.Nanodiamond-mitoxantrone complexes enhance drug retention in chemoresistant breast cancer cells..Mol Pharm2014;11:2683-91 PMCID:PMC4216229

[68] Setyawati MI,Leong DT.Tuning endothelial permeability with functionalized nanodiamonds..ACS Nano2016;10:1170-81

[69] Hoo CM,West P.A comparison of atomic force microscopy (AFM) and dynamic light scattering (DLS) methods to characterize nanoparticle size distributions..J Nanopart Res2008;10:89-96

[70] Fiorillo M,Iliut M,Ozsvari B.Graphene oxide selectively targets cancer stem cells, across multiple tumor types: implications for non-toxic cancer treatment, via “differentiation-based nano-therapy”..Oncotarget2015;6:3553-62 PMCID:PMC4414136

[71] Alshehri R,Hasan A,Ahmed F.Carbon nanotubes in biomedical applications: factors, mechanisms, and remedies of toxicity..J Med Chem2016;59:8149-67

[72] Burke AR,Carroll DL,Torti SV.Targeting cancer stem cells with nanoparticle-enabled therapies..J Mol Biomark Diagn2012;doi: 10.4172/2155-9929.S8-003 PMCID:PMC3875221

[73] Yao HJ,Sun L.The effect of hyaluronic acid functionalized carbon nanotubes loaded with salinomycin on gastric cancer stem cells..Biomaterials2014;35:9208-23

[74] Man HB,Kim HJ,Liu WK.Synthesis of nanodiamond-daunorubicin conjugates to overcome multidrug chemoresistance in leukemia..Nanomedicine2014;10:359-69 PMCID:PMC3912225

[75] Zhang Z,Chen J,Bao X.The use of lipid-coated nanodiamond to improve bioavailability and efficacy of sorafenib in resisting metastasis of gastric cancer..Biomaterials2014;35:4565-72

[76] Du X,Wei S,Li Y.A tumor-targeted, intracellular activatable and theranostic nanodiamond drug platform for strongly enhanced in vivo antitumor therapy..J Mater Chem B2020;8:1660