Cell-mediated and cell membrane-coated nanoparticles for drug delivery and cancer therapy

Abstract

Nanotechnology-based drug delivery platforms have been developed over the last two decades because of their favorable features in terms of improved drug bioavailability and stability. Despite recent advancement in nanotechnology platforms, this approach still falls short to meet the complexity of biological systems and diseases, such as avoiding systemic side effects, manipulating biological interactions and overcoming drug resistance, which hinders the therapeutic outcomes of the NP-based drug delivery systems. To address these issues, various strategies have been developed including the use of engineered cells and/or cell membrane-coated nanocarriers. Cell membrane receptor profiles and characteristics are vital in performing therapeutic functions, targeting, and homing of either engineered cells or cell membrane-coated nanocarriers to the sites of interest. In this context, we comprehensively discuss various cell- and cell membrane-based drug delivery approaches towards cancer therapy, the therapeutic potential of these strategies, and the limitations associated with engineered cells as drug carriers and cell membrane-associated drug nanocarriers. Finally, we review various cell types and cell membrane receptors for their potential in targeting, immunomodulation and overcoming drug resistance in cancer.

Keywords

Cell membrane-based drug delivery / cell-mediated drug delivery / membrane receptors / drug carriers / cancer drug resistance / nanoparticles

References

[1] Bray F,Soerjomataram I.Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries..CA Cancer J Clin2018;68:394-424

[2] Liang XJ,Zhao Y.Circumventing tumor resistance to chemotherapy by nanotechnology..Methods Mol Biol2010;596:467-88 PMCID:PMC3047496

[3] Barbero F,Vitali M.Formation of the protein corona: the interface between nanoparticles and the immune system..Semin Immunol2017;34:52-60

[4] Mout R,Rana S.Surface functionalization of nanoparticles for nanomedicine..Chem Soc Rev2012;41:2539-44 PMCID:PMC4102397

[5] Maeda H.Toward a full understanding of the EPR effect in primary and metastatic tumors as well as issues related to its heterogeneity..Adv Drug Deliv Rev2015;91:3-6

[6] Hua S,Metselaar JM.Current trends and challenges in the clinical translation of nanoparticulate nanomedicines: pathways for translational development and commercialization..Front Pharmacol2018;9:790 PMCID:PMC6056679

[7] Luk BT,Hu CMJ,Thamphiwatana S.Safe and immunocompatible nanocarriers cloaked in RBC membranes for drug delivery to treat solid tumors..Theranostics2016;6:1004-11 PMCID:PMC4876624

[8] Cao H,He X.Liposomes coated with isolated macrophage membrane can target lung metastasis of breast cancer..ACS Nano2016;10:7738-48

[9] Cao X,Luo S.Neutrophil-mimicking therapeutic nanoparticles for targeted chemotherapy of pancreatic carcinoma..Acta pharmaceutica Sinica B2019;9:575-89 PMCID:PMC6543032

[10] Gao C,Jurado-Sánchez B.Stem cell membrane-coated nanogels for highly efficient in vivo tumor targeted drug delivery..Small2016;12:4056-62

[11] Kang T,Wei D.Nanoparticles coated with neutrophil membranes can effectively treat cancer metastasis..ACS Nano2017;11:1397-411

[12] Mitchell MJ,Rana K,King MR.TRAIL-coated leukocytes that kill cancer cells in the circulation..Proc Natl Acad Sci U S A2014;111:930-5 PMCID:PMC3903223

[13] Gao W,Fang RH.Surface functionalization of gold nanoparticles with red blood cell membranes..Adv Mater2013;25:3549-53 PMCID:PMC4138311

[14] Tian W,Jiao D.Stem cell membrane vesicle-coated nanoparticles for efficient tumor-targeted therapy of orthotopic breast cancer..Polym Adv Technol2019;30:1051-60

[15] Yaman S,Oter G.Melanoma peptide MHC specific TCR expressing T-Cell membrane camouflaged PLGA nanoparticles for treatment of melanoma skin cancer..Front Bioeng Biotechnol2020;8:943 PMCID:PMC7431670

[16] Schmid D,Hartl CA.T cell-targeting nanoparticles focus delivery of immunotherapy to improve antitumor immunity..Nat Commun2017;8:1747 PMCID:PMC5700944

[17] Gao M,Song X.Erythrocyte-membrane-enveloped perfluorocarbon as nanoscale artificial red blood cells to relieve tumor hypoxia and enhance cancer radiotherapy..Adv Mater2017;29:1701429

[18] Rao L,Cai B.Cancer cell membrane-coated upconversion nanoprobes for highly specific tumor imaging..Adv Mater2016;28:3460-6

[19] Gos M,Fau-Przybyszewska M.Epithelial-mesenchymal transition in cancer progression..Postepy Biochem2009;55:121-8

[20] Beatty GL.Immune escape mechanisms as a guide for cancer immunotherapy..Clin Cancer Res2015;21:687-92 PMCID:PMC4334715

[21] Pandya PH,Pollok KE.The immune system in cancer pathogenesis: potential therapeutic approaches..J Immunol Res2016;2016:4273943 PMCID:PMC5220497

[22] Kroll AV,Zhang L.Biointerfacing and applications of cell membrane-coated nanoparticles..Bioconjug Chem2017;28:23-32 PMCID:PMC5471317

[23] Kroll AV,Jiang Y.Nanoparticulate delivery of cancer cell membrane elicits multiantigenic antitumor immunity..Adv Mater2017;29:10.1002/adma.201703969 PMCID:PMC5794340

[24] Angsantikul P,Gao W.Cell membrane-coated nanoparticles as an emerging antibacterial vaccine platform..Vaccines2015;3:814-28 PMCID:PMC4693220

[25] Fontana F,Liu D.Multistaged nanovaccines based on porous silicon@acetalated dextran@cancer cell membrane for cancer immunotherapy..Adv Mater2017;29:1603239

[26] Yang Y.Cancer immunotherapy: harnessing the immune system to battle cancer..J Clin Invest2015;125:3335-7 PMCID:PMC4588312

[27] Gajewski TF,Fu YX.Innate and adaptive immune cells in the tumor microenvironment..Nat Immunol2013;14:1014-22 PMCID:PMC4118725

[28] Roybal KT,Morsut L.Engineering T cells with customized therapeutic response programs using synthetic notch receptors..Cell2016;167:419-32.e16 PMCID:PMC5072533

[29] Schwarz KA.Engineering cell-based therapies to interface robustly with host physiology..Adv Drug Deliv Rev2016;105:55-65 PMCID:PMC5084532

[30] Roybal KT,Morsut L.Engineering T cells with customized therapeutic response programs using synthetic notch receptors..Cell2016;167:419-32.e16 PMCID:PMC5072533

[31] Baeumler TA,Fulga TA.Engineering synthetic signaling pathways with programmable dCas9-based chimeric receptors..Cell Rep2017;20:2639-53 PMCID:PMC5608971

[32] Östman A.The tumor microenvironment controls drug sensitivity..Nature medicine2012;18:1332-4

[33] Son B,Youn H.The role of tumor microenvironment in therapeutic resistance..Oncotarget2017;8:3933 PMCID:PMC5354804

[34] Paulitschke M,Anstee D,Gratzer W.Pertubation of red blood cell membrane rigidity by extracellular ligands..Blood1995;86:342-8

[35] Orbach A,Yedgar S.Biophysical and biochemical markers of red blood cell fragility..Transfus Med Hemother2017;44:183-7 PMCID:PMC5473068

[36] Morera D.Is there a direct role for erythrocytes in the immune response?.Vet Res2011;42:89 PMCID:PMC3199785

[37] Forbes NS.Engineering the perfect (bacterial) cancer therapy..Nat Rev Cancer2010;10:785-94 PMCID:PMC3756932

[38] Mohr A.The future of mesenchymal stem cell-based therapeutic approaches for cancer - from cells to ghosts..Cancer Lett2018;414:239-49

[39] Thanuja MY,Ranganath SH.Bioengineered cellular and cell membrane-derived vehicles for actively targeted drug delivery: So near and yet so far..Adv Drug Deliv Rev2018;132:57-80

[40] von Roemeling C,Chan CK,Kim BYS.Breaking down the barriers to precision cancer nanomedicine..Trends Biotechnol2017;35:159-71

[41] Hu CMJ,Aryal S.Erythrocyte membrane-camouflaged polymeric nanoparticles as a biomimetic delivery platform..Proc Natl Acad Sci U S A2011;108:10980-5 PMCID:PMC3131364

[42] Tsai RK,Discher DE.Self inhibition of phagocytosis: the affinity of ‘marker of self’ CD47 for SIRPalpha dictates potency of inhibition but only at low expression levels..Blood Cells Mol Dis2010;45:67-74 PMCID:PMC2878922

[43] Dehaini D,Fang RH.Erythrocyte-platelet hybrid membrane coating for enhanced nanoparticle functionalization..Adv Mater2017;29:10.1002/adma.201606209 PMCID:PMC5469720

[44] Ma YQ,Plow EF.Platelet integrin αIIbβ3: activation mechanisms..J Thromb Haemost2007;5:1345-52

[45] Fang RH,Luk BT.Cancer cell membrane-coated nanoparticles for anticancer vaccination and drug delivery..Nano Lett2014;14:2181-8 PMCID:PMC3985711

[46] Zhang L,Chen H.Human cytotoxic T-lymphocyte membrane-camouflaged nanoparticles combined with low-dose irradiation: a new approach to enhance drug targeting in gastric cancer..Int J Nanomedicine2017;12:2129-42 PMCID:PMC5364008

[47] Bu LL,Yu GT.Cancer stem cell-platelet hybrid membrane-coated magnetic nanoparticles for enhanced photothermal therapy of head and neck squamous cell carcinoma..Adv Funct Mater2019;29:1807733

[48] Zhang Y,Li C.Macrophage-membrane-coated nanoparticles for tumor-targeted chemotherapy..Nano Lett2018;18:1908-15 PMCID:PMC7470025

[49] Jin J,Barnett JD.Human cancer cell membrane-coated biomimetic nanoparticles reduce fibroblast-mediated invasion and metastasis and induce T-cells..ACS Appl Mater Interfaces2019;11:7850-61 PMCID:PMC6628902

[50] Felgner S,Frahm M.Engineered Salmonella enterica serovar Typhimurium overcomes limitations of anti-bacterial immunity in bacteria-mediated tumor therapy..Oncoimmunology2017;7:e1382791 PMCID:PMC5749626

[51] Gujrati V,Kim SH.Bioengineered bacterial outer membrane vesicles as cell-specific drug-delivery vehicles for cancer therapy..ACS Nano2014;8:1525-37

[52] Wang D,Li M.Erythrocyte-cancer hybrid membrane camouflaged hollow copper sulfide nanoparticles for prolonged circulation life and homotypic-targeting photothermal/chemotherapy of melanoma..ACS Nano2018;12:5241-52

[53] Zhang D,Xu D.Cell-penetrating peptides as noninvasive transmembrane vectors for the development of novel multifunctional drug-delivery systems..J Control Release2016;229:130-9

[54] Hu CMJ,Copp J,Zhang L.A biomimetic nanosponge that absorbs pore-forming toxins..Nat nanotechnol2013;8:336-40 PMCID:PMC3648601

[55] Zhu JY,Zhang MK.Preferential cancer cell self-recognition and tumor self-targeting by coating nanoparticles with homotypic cancer cell membranes..Nano Letters2016;16:5895-901

[56] Spicer JD,Cools-Lartigue JJ.Neutrophils promote liver metastasis via Mac-1-mediated interactions with circulating tumor cells..Cancer Res2012;72:3919

[57] Strell C,Niggemann B,Entschladen F.Surface molecules regulating rolling and adhesion to endothelium of neutrophil granulocytes and MDA-MB-468 breast carcinoma cells and their interaction..Cell Mol Life Sci2007;64:3306-16

[58] Parodi A,van de Ven AL.Synthetic nanoparticles functionalized with biomimetic leukocyte membranes possess cell-like functions..Nat Nanotechnol2013;8:61-8 PMCID:PMC3751189

[59] Stephan MT,Um SH,Irvine DJ.Therapeutic cell engineering with surface-conjugated synthetic nanoparticles..Nat Med2010;16:1035-41 PMCID:PMC2935928

[60] Van Deun J,Deville S.Feasibility of mechanical extrusion to coat nanoparticles with extracellular vesicle membranes..Cells2020;9:1797 PMCID:PMC7464356

[61] Milne JL,Bartesaghi A.Cryo-electron microscopy-a primer for the non-microscopist..FEBS J2013;280:28-45 PMCID:PMC3537914

[62] Parrow NL,Tu H.Measuring deformability and red cell heterogeneity in blood by ektacytometry..J Vis Exp2018;e56910 PMCID:PMC5908551

[63] Kuo YC,Hoang D.Colloidal properties of nanoerythrosomes derived from bovine red blood cells..Langmuir2016;32:171-9

[64] Deák R,Szigyártó IC.Physicochemical characterization of artificial nanoerythrosomes derived from erythrocyte ghost membranes..Colloids Surf B Biointerfaces2015;135:225-34

[65] Evangelopoulos M,Martinez JO.Cell source determines the immunological impact of biomimetic nanoparticles..Biomaterials2016;82:168-77 PMCID:PMC4916497

[66] Kaneti L,Malkah Dayan N.Nanoghosts as a novel natural nonviral gene delivery platform safely targeting multiple cancers..Nano letters2016;16:1574-82

[67] Sohni A.Mesenchymal stem cells migration homing and tracking..Stem Cells Int2013;2013:130763 PMCID:PMC3806396

[68] Turinetto V,Giachino C.Senescence in human mesenchymal stem cells: functional changes and implications in stem cell-based therapy..Int J Mol Sci2016;17:1164 PMCID:PMC4964536

[69] Geißler S,Kühnisch J.Functional comparison of chronological and in vitro aging: differential role of the cytoskeleton and mitochondria in mesenchymal stromal cells..PLoS One2012;7:e52700 PMCID:PMC3532360

[70] Li Q,Tao C,Jin P.The role of SDF-1-CXCR4/CXCR7 axis in biological behaviors of adipose tissue-derived mesenchymal stem cells in vitro..Biochem Biophys Res Commun2013;441:675-80

[71] Kim DS,Ko YJ.Effect of ex vivo culture density on CXCR7 expression in human mesenchymal stem cells..Int J Clin Exp Med2016;9:10802-10

[72] Murray PJ.Protective and pathogenic functions of macrophage subsets..Nat Rev Immunol2011;11:723-37 PMCID:PMC3422549

[73] Mantovani A,Locati M,Sica A.Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes..Trends Immunol2002;23:549-55

[74] Park JS,Lao YH.Engineering mesenchymal stem cells for regenerative medicine and drug delivery..Methods2015;84:3-16 PMCID:PMC4526354

[75] Muzykantov VR,Taylor RP,Herraez A.Regulation of the complement-mediated elimination of red blood cells modified with biotin and streptavidin..Analytical biochemistry1996;241:109-19

[76] Muzykantov VR,Samokhin GP.Avidin attachment to biotinylated erythrocytes induces homologous lysis via the alternative pathway of complement..Blood1991;78:2611-8

[77] Zaltzman A,Muzykantov V.Enhanced complement susceptibility of avidin-biotin-treated human erythrocytes is a consequence of neutralization of the complement regulators CD59 and decay accelerating factor..Biochem J1995;307:651-6 PMCID:PMC1136700

[78] Rennerfeldt DA.Concise review: when colonies are not clones: evidence and implications of intracolony heterogeneity in mesenchymal stem cells..Stem Cells2016;34:1135-41

[79] Klimentová J.Methods of isolation and purification of outer membrane vesicles from gram-negative bacteria..Microbiol Res2015;170:1-9

[80] Anselmo AC.Nanoparticles in the clinic: an update..Bioeng Transl Med2019;4:e10143 PMCID:PMC6764803

[81] Trinidad AJ,Peng Q,Hirschberg H.Combined concurrent photodynamic and gold nanoshell loaded macrophage-mediated photothermal therapies: an in vitro study on squamous cell head and neck carcinoma..Lasers Surg Med2014;46:310-8 PMCID:PMC4142684

[82] Bahmani B,Anvari B.Erythrocyte-derived photo-theranostic agents: hybrid nano-vesicles containing indocyanine green for near infrared imaging and therapeutic applications..Sci Rep2013;3:2180 PMCID:PMC3709166

[83] Baek SK,Krasieva T.Photothermal treatment of glioma; an in vitro study of macrophage-mediated delivery of gold nanoshells..J Neurooncol2011;104:439-48 PMCID:PMC3161184

[84] Prabhakar U,Jain RK.Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology..Cancer Res2013;73:2412-7 PMCID:PMC3916009

[85] Pasto A,Evangelopoulos M,Tasciotti E.Cell membrane protein functionalization of nanoparticles as a new tumor-targeting strategy..Clin Transl Med2019;8:8 PMCID:PMC6420595

[86] Munich S,Buchser WJ,Vujanovic NL.Dendritic cell exosomes directly kill tumor cells and activate natural killer cells via TNF superfamily ligands..Oncoimmunology2012;1:1074-83 PMCID:PMC3494621

[87] Xuan M,Dai L,Li J.Macrophage cell membrane camouflaged mesoporous silica nanocapsules for in vivo cancer therapy..Adv Healthc Mater2015;4:1645-52

[88] Thamphiwatana S,Escajadillo T.Macrophage-like nanoparticles concurrently absorbing endotoxins and proinflammatory cytokines for sepsis management..Proc Natl Acad Sci U S A2017;114:11488-93 PMCID:PMC5664555

[89] Krishnamurthy S,Xie C.Monocyte cell membrane-derived nanoghosts for targeted cancer therapy..Nanoscale2016;8:6981-5

[90] Xue J,Zhang L.Neutrophil-mediated anticancer drug delivery for suppression of postoperative malignant glioma recurrence..Nat Nanotechnol2017;12:692-700

[91] Wang F,Luk BT.Nanoparticle-based antivirulence vaccine for the management of methicillin-resistant staphylococcus aureus skin infection..Adv Mater2016;26:1628-35 PMCID:PMC4912041

[92] Wang C,Ye Y.In situ activation of platelets with checkpoint inhibitors for post-surgical cancer immunotherapy..Nat Biomed Eng2017;1:11

[93] Li J,Wun B,King MR.Genetic engineering of platelets to neutralize circulating tumor cells..J Control Release2016;228:38-47 PMCID:PMC4828270

[94] Hu Q,Sun W.Engineered nanoplatelets for enhanced treatment of multiple myeloma and thrombus..Adv Mater2016;28:9573-80 PMCID:PMC5283718

[95] Sadhukha T,Prabha S.Nano-engineered mesenchymal stem cells as targeted therapeutic carriers..J Control Release2014;196:243-51

[96] Wang X,Ouyang X.Mesenchymal stem cells loaded with paclitaxel-poly(lactic-co-glycolic acid) nanoparticles for glioma-targeting therapy..Int J Nanomedicine2018;13:5231-48 PMCID:PMC6136913

[97] Sun H,Meng Q.Cancer cell membrane-coated gold nanocages with hyperthermia-triggered drug release and homotypic target inhibit growth and metastasis of breast cancer..Adv Funct Mater2017;27:1604300

[98] Kim OY,Dinh NTH.Bacterial outer membrane vesicles suppress tumor by interferon-γ-mediated antitumor response..Nat Commun2017;8:626 PMCID:PMC5606984

[99] Fantappiè L,Chiarot E.Antibody-mediated immunity induced by engineered Escherichia coli OMVs carrying heterologous antigens in their lumen..J Extracell Vesicles2014;3:10.3402/jev.v3.24015 PMCID:PMC4131003

[100] Stephan MT,Bak P,Irvine DJ.Synapse-directed delivery of immunomodulators using T-cell-conjugated nanoparticles..Biomaterials2012;33:5776-87 PMCID:PMC3395588

[101] Xie Z,Kim GB.Immune cell-mediated biodegradable theranostic nanoparticles for melanoma targeting and drug delivery..Small2017;13:1603121 PMCID:PMC5342926

[102] Guilliams M,Jakubzick C.Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny..Nat Rev Immunol2014;14:571-8 PMCID:PMC4638219

[103] Fossati G,Edwards SW.Neutrophil infiltration into human gliomas..Acta Neuropathol1999;98:349-54

[104] Fang RH,Gao W.Cell membrane coating nanotechnology..Adv Mater2018;30:1706759 PMCID:PMC5984176

[105] Danesh A,Jackman RP.Exosomes from red blood cell units bind to monocytes and induce proinflammatory cytokines, boosting T-cell responses in vitro..Blood2014;123:687-96 PMCID:PMC3907755

[106] Harrison P.Platelet function analysis..Blood Rev2005;19:111-23

[107] Haemmerle M,Menter DG,Sood AK.The platelet lifeline to cancer: challenges and opportunities..Cancer Cell2018;33:965-83 PMCID:PMC5997503

[108] Li J,Wang L.Targeted drug delivery to circulating tumor cells via platelet membrane-functionalized particles..Biomaterials2016;76:52-65 PMCID:PMC4662903

[109] Wu HH,Tabata Y.Mesenchymal stem cell-based drug delivery strategy: from cells to biomimetic..J Control Release2019;294:102-13

[110] Kuriakose AE,Noukeu LC.Stem cells as drug delivery vehicles. Encyclopedia of tissue engineering and regenerative medicine.2019;OxfordAcademic Press197-210

[111] Poetsch A.Bacterial membrane proteomics..Proteomics2008;8:4100-22

[112] Lee EY,Park GW.Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli..Proteomics2007;7:3143-53

[113] Kuehn MJ.Bacterial outer membrane vesicles and the host-pathogen interaction..Genes Dev2005;19:2645-55

[114] Gao W,Thamphiwatana S.Modulating antibacterial immunity via bacterial membrane-coated nanoparticles..Nano letters2015;15:1403-9 PMCID:PMC4399974

[115] Muralinath M,Roland KL.Immunization with Salmonella enterica serovar Typhimurium-derived outer membrane vesicles delivering the pneumococcal protein PspA confers protection against challenge with Streptococcus pneumoniae..Infect Immun2011;79:887-94 PMCID:PMC3028854

[116] Sick E,Schneider C.CD47 update: a multifaceted actor in the tumour microenvironment of potential therapeutic interest..Br J Pharmacol2012;167:1415-30 PMCID:PMC3514757

[117] Lee JY,Kim GG.Red blood cell membrane bioengineered Zr-89 labelled hollow mesoporous silica nanosphere for overcoming phagocytosis..Sci Rep2019;9:7419 PMCID:PMC6520393

[118] Othman M.Gene of the issue: GP1BA gene mutations associated with bleeding..Platelets2017;28:832-6

[119] Li R.The organizing principle of the platelet glycoprotein Ib-IX-V complex..J Thromb Haemost2013;11:605-14 PMCID:PMC3696474

[120] Erpenbeck L,Schön M,Schön MP.Inhibition of platelet GPIbα and promotion of melanoma metastasis..J Investig Dermatol2010;130:576-86

[121] Malehmir M,Gallage S.Platelet GPIbalpha is a mediator and potential interventional target for NASH and subsequent liver cancer..Nat Med2019;25:641-55

[122] Hong W.Tethering the assembly of SNARE complexes..Trends Cell Biol2014;24:35-43

[123] Sutton RB,Jahn R.Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution..Nature1998;395:347-53

[124] Scales SJ,Masuda ES.Amisyn, a novel syntaxin-binding protein that may regulate SNARE complex assembly..J Biol Chem2002;277:28271-9

[125] Sheridan JP,Pitti RM.Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors..Science1997;277:818

[126] Kube S,Naumovska E.Fusogenic liposomes as nano carriers for delivery of intracellular proteins..Langmuir2017;33:1051-9

[127] Han J,Böckmann RA.The multifaceted role of SNARE proteins in membrane fusion..Front Physiol2017;8:5 PMCID:PMC5247469

[128] East L.The mannose receptor family..Biochim Biophys Acta Gen Subj2002;1572:364-86

[129] Martinez-Pomares L.The mannose receptor..J Leukoc Biol2012;92:1177-86

[130] Sallusto F,Danieli C.Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products..J Exp Med1995;182:389-400 PMCID:PMC2192110

[131] Miller JL,Martinez-Pomares L.The mannose receptor mediates dengue virus infection of macrophages..PLOS Pathogens2008;4:e17 PMCID:PMC2233670

[132] Sukegawa S,Bouamr F,Strebel K.Mannose receptor 1 restricts HIV particle release from infected macrophages..Cell Rep2018;22:786-95 PMCID:PMC5792083

[133] Springer TA.Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm..Cell1994;76:301-14

[134] Baggiolini M.Chemokines and leukocyte traffic..Nature1998;392:565-8

[135] Panés J,Granger DN.Leukocyte-endothelial cell adhesion: avenues for therapeutic intervention..Br J Pharmacol1999;126:537-50 PMCID:PMC1565837

[136] Ley K.Molecular mechanisms of leukocyte recruitment in the inflammatory process..Cardiovasc Res1996;32:733-42

[137] Huang Y,Chen J.Leukocyte-derived biomimetic nanoparticulate drug delivery systems for cancer therapy..Acta pharmaceutica Sinica B2018;8:4-13 PMCID:PMC5985693

[138] Mitchell MJ.Leukocytes as carriers for targeted cancer drug delivery..Expert Opin Drug Deliv2015;12:375-92 PMCID:PMC5658012

[139] Huang R,He Y.Recent advances in CAR-T cell engineering..J Hematol Oncol2020;13:86 PMCID:PMC7333410

[140] Crittenden M,Chester J.Pharmacologically regulated production of targeted retrovirus from T cells for systemic antitumor gene therapy..Cancer Res2003;63:3173-80

[141] Ma W,Li J.Coating biomimetic nanoparticles with chimeric antigen receptor T cell-membrane provides high specificity for hepatocellular carcinoma photothermal therapy treatment..Theranostics2020;10:1281-95 PMCID:PMC6956810

[142] Atsuhiro M,Hideyuki S.Role of Fc receptors as a therapeutic target..Inflamm Allergy Drug Targets2009;8:80-6 PMCID:PMC3990358

[143] Clynes R,Moroi Y,Ravetch JV.Fc receptors are required in passive and active immunity to melanoma..Proc Natl Acad Sci U S A1998;95:652-6 PMCID:PMC18475

[144] Tan Sardjono C,Hogarth PM.The role of FcgammaRIIa as an inflammatory mediator in rheumatoid arthritis and systemic lupus erythematosus..Immunol Cell Biol2003;81:374-81

[145] Patten DA.SCARF1: a multifaceted, yet largely understudied, scavenger receptor..Inflamm Res2018;67:627-32 PMCID:PMC6028831

[146] Païdassi H,Garlatti V.C1q binds phosphatidylserine and likely acts as a multiligand-bridging molecule in apoptotic cell recognition..J Immunol2008;180:2329-38 PMCID:PMC2632962

[147] Wiley SR,Smolak PJ.Identification and characterization of a new member of the TNF family that induces apoptosis..Immunity1995;3:673-82

[148] Pitti RM,Ruppert S.Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family..J Biol Chem1996;271:12687-90

[149] LeBlanc HN.Apo2L/TRAIL and its death and decoy receptors..Cell Death Differ2003;10:66-75

[150] Degli-Esposti MA,Smolak PJ.The novel receptor TRAIL-R4 induces NF-kappaB and protects against TRAIL-mediated apoptosis, yet retains an incomplete death domain..Immunity1997;7:813-20

[151] Pan G,Wei YF.An antagonist decoy receptor and a death domain-containing receptor for TRAIL..Science1997;277:815

[152] Jo M,Seol DW.Apoptosis induced in normal human hepatocytes by tumor necrosis factor-related apoptosis-inducing ligand..Nat Med2000;6:564-7

[153] Korsmeyer SJ,Saito M.Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c..Cell Death Differ2000;7:1166-73

[154] Jiang X,Wang C.Nanoparticle engineered TRAIL-overexpressing adipose-derived stem cells target and eradicate glioblastoma via intracranial delivery..Proc Natl Acad Sci U S A2016;113:13857-62 PMCID:PMC5137687

[155] Agata Y,Nishimura H.Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes..Int Immunol1996;8:765-72

[156] Yamazaki T,Iwai H.Expression of programmed death 1 ligands by murine T cells and APC..J Immunol2002;169:5538

[157] Blank C.Contribution of the PD-L1/PD-1 pathway to T-cell exhaustion: an update on implications for chronic infections and tumor evasion..Cancer Immunol Immunother2007;56:739-45

[158] Iwai Y,Tanaka Y.Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade..Proc Natl Acad Sci U S A2002;99:12293-7 PMCID:PMC129438

[159] Akbay EA,Carretero J,Tchaicha JH.Activation of the PD-1 pathway contributes to immune escape in EGFR-driven lung tumors..Cancer discovery2013;3:1355-63 PMCID:PMC3864135

[160] Sheng Z,Sun Y.The efficacy of anti-PD-1/PD-L1 therapy and its comparison with EGFR-TKIs for advanced non-small-cell lung cancer..Oncotarget2017;8:57826-35 PMCID:PMC5593686

[161] Xu S,Huang D.PD-L1 monoclonal antibody-conjugated nanoparticles enhance drug delivery level and chemotherapy efficacy in gastric cancer cells..Int J Nanomedicine2018;14:17-32 PMCID:PMC6302817

[162] Zhang X,Wang J.PD-1 blockade cellular vesicles for cancer immunotherapy..Adv Mater2018;30:1707112

[163] Wieczorek M,Sticht J.Major histocompatibility complex (MHC) class I and MHC class II proteins: conformational plasticity in antigen presentation..Front Immunol2017;8:292 PMCID:PMC5355494

[164] Alberts B,Lewis J.T cells and MHC proteins. Molecular Biology of the Cell.2002;4th editionNew YorkGarland Science

[165] Fernando MMA,Walsh EC.Defining the role of the MHC in autoimmunity: a review and pooled analysis..PLoS Genet2008;4:e1000024 PMCID:PMC2291482

[166] Espel E,Aubert V.Transcriptional and translational control of TNF-α gene expression in human monocytes by major histocompatibility complex class II ligands..Eur J Immunol1996;26:2417-24

[167] Donati B,Ciarrocchi A.BRD4 and cancer: going beyond transcriptional regulation..Mol Cancer2018;17:164 PMCID:PMC6251205

[168] Da Costa D,Perry T.BET inhibition as a single or combined therapeutic approach in primary paediatric B-precursor acute lymphoblastic leukaemia..Blood Cancer J2013;3:e126 PMCID:PMC3730202

[169] Delmore JE,Lemieux ME.BET bromodomain inhibition as a therapeutic strategy to target c-Myc..Cell2011;146:904-17 PMCID:PMC3187920

[170] Crawford NPS,Lukes L.Bromodomain 4 activation predicts breast cancer survival..Proc Natl Acad Sci2008;105:6380 PMCID:PMC2359777

[171] Ding N,Yu RT.BRD4 is a novel therapeutic target for liver fibrosis..Proc Natl Acad Sci2015;112:15713 PMCID:PMC4697417

[172] Tang X,Ren Y.BET bromodomain proteins mediate downstream signaling events following growth factor stimulation in human lung fibroblasts and are involved in bleomycin-induced pulmonary fibrosis..Mol Pharmacol2012;83:mol.112.081661

[173] Zhou B,Gong Y.Brd4 inhibition attenuates unilateral ureteral obstruction-induced fibrosis by blocking TGF-β-mediated Nox4 expression..Redox biol2017;11:390-402 PMCID:PMC5219604

[174] Ai X,Duan Y.Emerging approaches to functionalizing cell membrane-coated nanoparticles..Biochemistry2020;doi: 10.1021/acs.biochem.0c00343

[175] Fang RH,Chen KNH.Lipid-insertion enables targeting functionalization of erythrocyte membrane-cloaked nanoparticles..Nanoscale2013;5:8884-8 PMCID:PMC3831007

[176] Zhang Z,Huang J.Anti-EGFR-iRGD recombinant protein modified biomimetic nanoparticles loaded with gambogic acid to enhance targeting and antitumor ability in colorectal cancer treatment..Int J Nanomedicine2018;13:4961-75 PMCID:PMC6124475

[177] Chen H,Zhang L.Lipid insertion enables targeted functionalization of paclitaxel-loaded erythrocyte membrane nanosystem by tumor-penetrating bispecific recombinant protein..Int J Nanomedicine2018;13:5347-59 PMCID:PMC6141126

[178] Liu L,Liu J.Advances on non-genetic cell membrane engineering for biomedical applications..Polymers2019;11:2017 PMCID:PMC6961000

[179] Krishnamurthy S,Jayakumar MKG.Surface protein engineering increases the circulation time of a cell membrane-based nanotherapeutic..Nanomedicine2019;18:169-78

[180] Leth-Larsen R,Ditzel HJ.Plasma membrane proteomics and its application in clinical cancer biomarker discovery..Mol Cell Proteomics2010;9:1369-82 PMCID:PMC2938092

[181] Saeui CT,Liu L,Yarema KJ.Cell surface and membrane engineering: emerging technologies and applications..J Funct Biomater2015;6:454-85 PMCID:PMC4493524

[182] 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