In vivo nano-biosensing element of red blood cell-mediated delivery.

Biosensors based on nanotechnology are developing rapidly and are widely applied in many fields including biomedicine, environmental monitoring, national defense and analytical chemistry, and have achieved vital positions in these fields. Novel nano-materials are intensively developed and manufactured for potential biosensing and theranostic applications while lacking comprehensive assessment of their potential health risks. The integration of diagnostic in vivo biosensors and the DDSs for delivery of therapeutic drugs holds an enormous potential in next-generation theranostic platforms. Controllable, precise, and safe delivery of diagnostic biosensing devices and therapeutic agents to the target tissues, organs, or cells is an important determinant in developing advanced nanobiosensor-based theranostic platforms. Particularly, inspired by the comprehensive biological investigations on the red blood cells (RBCs), advanced strategies of RBC-mediated in vivo delivery have been developed rapidly and are currently in different stages of transforming from research and design to pre-clinical and clinical investigations. In this review, the RBC-mediated delivery of in vivo nanobiosensors for applications of bio-imaging at the single-cell level, advanced medical diagnostics, and analytical detection of biomolecules and cellular activities are presented. A comprehensive perspective of the technical framework of the state-of-the-art RBC-mediated delivery systems is explained in detail to inspire the design and implementation of advanced nanobiosensor-based theranostic platforms taking advantage of RBC-delivery modalities.

[1]  Dennis H. Robinson,et al.  Drug delivery systems , 1991 .

[2]  S. Nie,et al.  Self-assembled nanoparticle probes for recognition and detection of biomolecules. , 2002, Journal of the American Chemical Society.

[3]  R. Tiwari,et al.  Drug delivery systems: An updated review , 2012, International journal of pharmaceutical investigation.

[4]  Jie Chao,et al.  Single-Molecule Analysis of MicroRNA and Logic Operations Using a Smart Plasmonic Nanobiosensor. , 2018, Journal of the American Chemical Society.

[5]  Peter Wipf,et al.  Nanoparticles in cellular drug delivery. , 2009, Bioorganic & medicinal chemistry.

[6]  Bernhard Gleich,et al.  Red blood cells as carriers in magnetic particle imaging , 2013, Biomedizinische Technik. Biomedical engineering.

[7]  Michael R Hamblin,et al.  Smart micro/nanoparticles in stimulus-responsive drug/gene delivery systems. , 2016, Chemical Society reviews.

[8]  C. Cinti,et al.  Newly Engineered Magnetic Erythrocytes for Sustained and Targeted Delivery of Anti-Cancer Therapeutic Compounds , 2011, PloS one.

[9]  K. Soo,et al.  Nanoparticles in photodynamic therapy. , 2015, Chemical reviews.

[10]  Yury V. Ryabchikov,et al.  Facile laser synthesis of multimodal composite silicon/gold nanoparticles with variable chemical composition , 2019, Journal of Nanoparticle Research.

[11]  Arben Merkoçi,et al.  Nanobiosensors in diagnostics , 2016, Nanobiomedicine.

[12]  H. Tajerzadeh,et al.  Evaluation of Hypotonic Preswelling Method for Encapsulation of Enalaprilat in Intact Human Erythrocytes , 2000, Drug development and industrial pharmacy.

[13]  Igor Meglinski,et al.  Influence of interaction time on the red blood cell (dis)aggregation dynamics in vitro studied by optical tweezers , 2019, European Conference on Biomedical Optics.

[14]  J. Paul Robinson,et al.  A novel and simple cell-based detection system with a collagen-encapsulated B-lymphocyte cell line as a biosensor for rapid detection of pathogens and toxins , 2008, Laboratory Investigation.

[15]  Igor Meglinski,et al.  Remote in vivo stress assessment of aquatic animals with microencapsulated biomarkers for environmental monitoring , 2016, Scientific Reports.

[16]  A. Hasan,et al.  Development of point-of-care nanobiosensors for breast cancers diagnosis. , 2020, Talanta.

[17]  Chunhai Fan,et al.  Biomolecular sensing via coupling DNA-based recognition with gold nanoparticles , 2009 .

[18]  Yuan Wang,et al.  Advances in refunctionalization of erythrocyte-based nanomedicine for enhancing cancer-targeted drug delivery , 2019, Theranostics.

[19]  Tuan Vo-Dinh,et al.  Nanoprobes and nanobiosensors for monitoring and imaging individual living cells. , 2006, Nanomedicine : nanotechnology, biology, and medicine.

[20]  H. Gendelman,et al.  Cell-mediated drug delivery , 2011, Expert opinion on drug delivery.

[21]  Yongtai Zhang,et al.  Red blood cell membrane-camouflaged nanoparticles: a novel drug delivery system for antitumor application , 2019, Acta pharmaceutica Sinica. B.

[22]  Brian D Ross,et al.  In vivo targeting of metastatic breast cancer via tumor vasculature-specific nano-graphene oxide. , 2016, Biomaterials.

[23]  Silke Krol,et al.  Nanosensors for early cancer detection and for therapeutic drug monitoring. , 2015, Nanomedicine.

[24]  Antony Thomas,et al.  Influence of Red Blood Cells on Nanoparticle Targeted Delivery in Microcirculation. , 2011, Soft matter.

[25]  Tullio Pozzan,et al.  Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells , 1995, Current Biology.

[26]  Vladimir R Muzykantov,et al.  Drug delivery by red blood cells: vascular carriers designed by mother nature , 2010, Expert opinion on drug delivery.

[27]  Shalini Prasad,et al.  Nanobiosensors: the future for diagnosis of disease? , 2014 .

[28]  Ralph Weissleder,et al.  Peroxidase Substrate Nanosensors for MR Imaging , 2004 .

[29]  T. Groth,et al.  Recent Developments in Layer-by-Layer Technique for Drug Delivery Applications. , 2019, ACS applied bio materials.

[30]  J Szebeni,et al.  Stealth liposomes and long circulating nanoparticles: critical issues in pharmacokinetics, opsonization and protein-binding properties. , 2003, Progress in lipid research.

[31]  Igor Meglinski,et al.  Optical Tweezers in Studies of Red Blood Cells , 2020, Cells.

[32]  O. Wolfbeis An overview of nanoparticles commonly used in fluorescent bioimaging. , 2015, Chemical Society reviews.

[33]  Antonella Antonelli,et al.  Intravascular contrast agents in diagnostic applications: Use of red blood cells to improve the lifespan and efficacy of blood pool contrast agents , 2017, Nano Research.

[34]  A. Evlyukhin,et al.  The Synthesis of Hybrid Gold-Silicon Nano Particles in a Liquid , 2017, Scientific Reports.

[35]  Haiying Gu,et al.  Cellular biosensor based on red blood cells immobilized on Fe3O4 Core/Au Shell nanoparticles for hydrogen peroxide electroanalysis , 2010 .

[36]  Igor Meglinski,et al.  Mutual interaction of red blood cells assessed by optical tweezers and scanning electron microscopy imaging. , 2018, Optics letters.

[37]  C. Murphy,et al.  Recent Progress in Cancer Thermal Therapy Using Gold Nanoparticles , 2016 .

[38]  Koen Raemdonck,et al.  Hitchhiking nanoparticles: Reversible coupling of lipid-based nanoparticles to cytotoxic T lymphocytes. , 2016, Biomaterials.

[39]  Samir Mitragotri,et al.  Red blood cell-mimicking synthetic biomaterial particles , 2009, Proceedings of the National Academy of Sciences.

[40]  U Teichgräber,et al.  Magnetite-loaded carrier erythrocytes as contrast agents for magnetic resonance imaging. , 2006, Nano letters.

[41]  P. Nikitin,et al.  Nanoparticle-based drug delivery via RBC-hitchhiking for the inhibition of lung metastases growth. , 2019, Nanoscale.

[42]  Samir Mitragotri,et al.  Nanoparticle Properties Modulate Their Attachment and Effect on Carrier Red Blood Cells , 2018, Scientific Reports.

[43]  Xingyu Chen,et al.  Bioinspired by cell membranes: functional polymeric materials for biomedical applications , 2020, Materials Chemistry Frontiers.

[44]  Hong Yu Yang,et al.  Polymer-Based and pH-Sensitive Nanobiosensors for Imaging and Therapy of Acidic Pathological Areas , 2016, Pharmaceutical Research.

[45]  Mehrdad Hamidi,et al.  Carrier Erythrocytes: An Overview , 2003, Drug delivery.

[46]  Junyoung Kwon,et al.  Magnetoplasmonic Nanomaterials for Biosensing/Imaging and in Vitro/in Vivo Biousability. , 2018, Analytical chemistry.

[47]  G P Samokhin,et al.  Target-sensitive immunoerythrocytes: interaction of biotinylated red blood cells with immobilized avidin induces their lysis by complement. , 1996, Biochimica et biophysica acta.

[48]  Xiaoyuan Ji,et al.  Doxorubicin-loaded silicon nanoparticles impregnated into red blood cells featuring bright fluorescence, strong photostability, and lengthened blood residency , 2018, Nano Research.

[49]  Igor Meglinski,et al.  Microencapsulated fluorescent pH probe as implantable sensor for monitoring the physiological state of fish embryos , 2017, PloS one.

[50]  P. Couvreur,et al.  Nanoparticles in cancer therapy and diagnosis. , 2002, Advanced drug delivery reviews.

[51]  Halahakoon Mudiyanselge Amila Jeewantha,et al.  The terpene-indole alkaloids loaded erythrocytes as a drug carrier: design and assessment , 2018, Russian Open Medical Journal.

[52]  Antonella Antonelli,et al.  Red blood cells as carriers of iron oxide-based contrast agents for diagnostic applications. , 2014, Journal of biomedical nanotechnology.

[53]  Inho Kim,et al.  Silver nanoparticles promote procoagulant activity of red blood cells: a potential risk of thrombosis in susceptible population , 2019, Particle and Fibre Toxicology.

[54]  Alke Petri-Fink,et al.  Nanoparticle–Cell Interaction: A Cell Mechanics Perspective , 2018, Advanced materials.

[55]  Yahya E Choonara,et al.  The Hemocompatibility of Nanoparticles: A Review of Cell–Nanoparticle Interactions and Hemostasis , 2019, Cells.

[56]  Joe Brownlie,et al.  DNA vaccination against bovine viral diarrhoea virus induces humoral and cellular responses in cattle with evidence for protection against viral challenge. , 2003, Vaccine.

[57]  J. M. Lanao,et al.  Factors associated with the performance of carrier erythrocytes obtained by hypotonic dialysis. , 2004, Blood cells, molecules & diseases.

[58]  Samir Mitragotri,et al.  Vascular Drug Delivery Using Carrier Red Blood Cells: Focus on RBC Surface Loading and Pharmacokinetics , 2020, Pharmaceutics.

[59]  Samir Mitragotri,et al.  Delivering nanoparticles to lungs while avoiding liver and spleen through adsorption on red blood cells. , 2013, ACS nano.

[60]  Mauro Magnani,et al.  Erythrocytes as carriers for drugs: the transition from the laboratory to the clinic is approaching , 2012, Expert opinion on biological therapy.

[61]  Majid Sharifi,et al.  Cancer diagnosis using nanomaterials based electrochemical nanobiosensors. , 2019, Biosensors & bioelectronics.

[62]  Farzaneh Ghorbani,et al.  Biosensors and nanobiosensors for rapid detection of autoimmune diseases: a review , 2019, Microchimica Acta.

[63]  Amir Sanati-Nezhad,et al.  Nano-biosensor for highly sensitive detection of HER2 positive breast cancer. , 2018, Biosensors & bioelectronics.

[64]  V R Muzykantov,et al.  Enhanced complement susceptibility of avidin-biotin-treated human erythrocytes is a consequence of neutralization of the complement regulators CD59 and decay accelerating factor. , 1995, The Biochemical journal.

[65]  Yi Wang,et al.  A label-free biosensor based on gold nanoshell monolayers for monitoring biomolecular interactions in diluted whole blood. , 2008, Biosensors & bioelectronics.

[66]  Richard C. Oppenheim,et al.  Solid colloidal drug delivery systems: Nanoparticles , 1981 .

[67]  Ronnie H. Fang,et al.  Surface Functionalization of Gold Nanoparticles with Red Blood Cell Membranes , 2013, Advanced materials.

[68]  Woo-Sik Kim,et al.  Interpretation of protein adsorption phenomena onto functional microspheres , 1998 .

[69]  Ronnie H. Fang,et al.  Interfacial interactions between natural RBC membranes and synthetic polymeric nanoparticles. , 2013, Nanoscale.

[70]  Pae C. Wu,et al.  Personalized diagnostics and biosensors: a review of the biology and technology needed for personalized medicine , 2014, Critical reviews in biotechnology.

[71]  Sang Joon Lee,et al.  Gold nanoparticle-incorporated human red blood cells (RBCs) for X-ray dynamic imaging. , 2011, Biomaterials.

[72]  T. Bein,et al.  Multifunctional Mesoporous Silica Nanoparticles as a Universal Platform for Drug Delivery , 2014 .

[73]  Robert J. Flatt,et al.  Nanoparticle decoration with surfactants: Molecular interactions, assembly, and applications , 2017 .

[74]  Per Stoltze Microkinetic simulation of catalytic reactions , 2000 .

[75]  Zhiping Zhang,et al.  Cell or Cell Membrane-Based Drug Delivery Systems , 2015, Theranostics.

[76]  Kinam Park Controlled drug delivery systems: past forward and future back. , 2014, Journal of controlled release : official journal of the Controlled Release Society.

[77]  Robert Langer,et al.  Nanoparticulate cellular patches for cell-mediated tumoritropic delivery. , 2010, ACS nano.

[78]  Eric Pridgen,et al.  Factors Affecting the Clearance and Biodistribution of Polymeric Nanoparticles , 2008, Molecular pharmaceutics.

[79]  Longyi Chen,et al.  Fluorescent Nanobiosensors for Sensing Glucose , 2018, Sensors.

[80]  Huimin Zhao,et al.  In vivo biosensors: mechanisms, development, and applications , 2018, Journal of Industrial Microbiology & Biotechnology.

[81]  C. Teh,et al.  Encapsulated biosensors for advanced tissue diagnostics , 2015 .

[82]  Yang Li,et al.  Recent Advances of Persistent Luminescence Nanoparticles in Bioapplications , 2020, Nano-micro letters.

[83]  Xiaoyuan Chen,et al.  Gold Nanoparticles for In Vitro Diagnostics. , 2015, Chemical reviews.

[84]  Ronnie H. Fang,et al.  Erythrocyte membrane-camouflaged polymeric nanoparticles as a biomimetic delivery platform , 2011, Proceedings of the National Academy of Sciences.

[85]  Igor Meglinski,et al.  Ecophotonics: assessment of temperature gradient in aquatic organisms using up-conversion luminescent particles , 2017 .

[86]  Xiaoqi Sun,et al.  Remotely Controlled Red Blood Cell Carriers for Cancer Targeting and Near‐Infrared Light‐Triggered Drug Release in Combined Photothermal–Chemotherapy , 2015 .

[87]  Arnan Mitchell,et al.  Label-Free Optofluidic Nanobiosensor Enables Real-Time Analysis of Single-Cell Cytokine Secretion. , 2018, Small.

[88]  Jun Gao,et al.  A fullerene-based multi-functional nanoplatform for cancer theranostic applications. , 2014, Biomaterials.

[89]  S M Moghimi,et al.  Long-circulating and target-specific nanoparticles: theory to practice. , 2001, Pharmacological reviews.

[90]  Zhen Gu,et al.  Red Blood Cells for Drug Delivery , 2017 .

[91]  E. Wang,et al.  Nanomaterials with enzyme-like characteristics (nanozymes): next-generation artificial enzymes. , 2013, Chemical Society reviews.

[92]  Mehrdad Hamidi,et al.  Carrier erythrocytes: recent advances, present status, current trends and future horizons , 2014, Expert opinion on drug delivery.

[93]  Michel Meunier,et al.  Femtosecond laser ablation in aqueous solutions: a novel method to synthesize non-toxic metal colloids with controllable size , 2007 .

[94]  G P Samokhin,et al.  Targeting of enzyme immobilized on erythrocyte membrane to collagen‐coated surface , 1985, FEBS letters.

[95]  Robert Franco,et al.  International seminar on the red blood cells as vehicles for drugs , 2012, Expert opinion on biological therapy.

[96]  Meral Yüce,et al.  How to make nanobiosensors: surface modification and characterisation of nanomaterials for biosensing applications , 2017 .

[97]  Samir Mitragotri,et al.  Red blood cell-hitchhiking boosts delivery of nanocarriers to chosen organs by orders of magnitude , 2018, Nature Communications.

[98]  Igor Meglinski,et al.  Probing the Red Blood Cell Interaction in Individual Cell Pairs by Optical Tweezers , 2020, 2020 Conference on Lasers and Electro-Optics (CLEO).

[99]  S. Mitragotri,et al.  Nanoparticles in the clinic , 2016, Bioengineering & translational medicine.

[100]  Bahman Anvari,et al.  Erythrocyte-derived photo-theranostic agents: hybrid nano-vesicles containing indocyanine green for near infrared imaging and therapeutic applications , 2013, Scientific Reports.

[101]  S. Oancea,et al.  Magnetic nanoparticle effects on the red blood cells , 2009 .

[102]  Yuchao Li,et al.  Red‐Blood‐Cell Waveguide as a Living Biosensor and Micromotor , 2019, Advanced Functional Materials.

[103]  G Monserratt Lopez-Ayon,et al.  Reversing adhesion with light: a general method for functionalized bead release from cells. , 2016, Biomaterials science.

[104]  Lutz Heinemann,et al.  Options for the Development of Noninvasive Glucose Monitoring , 2016, Journal of diabetes science and technology.

[105]  Joseph M. DeSimone,et al.  Strategies in the design of nanoparticles for therapeutic applications , 2010, Nature Reviews Drug Discovery.

[106]  Mostafa Azimzadeh,et al.  An electrochemical nanobiosensor for plasma miRNA-155, based on graphene oxide and gold nanorod, for early detection of breast cancer. , 2016, Biosensors & bioelectronics.

[107]  Mingfeng Qiu,et al.  Advances of blood cell‐based drug delivery systems , 2017, European journal of pharmaceutical sciences : official journal of the European Federation for Pharmaceutical Sciences.

[108]  M. Ozkan,et al.  Nano-oncology: drug delivery, imaging, and sensing , 2006, Analytical and bioanalytical chemistry.

[109]  Igor Meglinski,et al.  Influence of Pulsed He–Ne Laser Irradiation on the Red Blood Cell Interaction Studied by Optical Tweezers , 2019, Micromachines.

[110]  Jakub Wlodarczyk,et al.  Genetically encoded FRET-based biosensor for imaging MMP-9 activity. , 2014, Biomaterials.

[111]  R. Kumar,et al.  Graphene, carbon nanotubes, zinc oxide and gold as elite nanomaterials for fabrication of biosensors for healthcare. , 2015, Biosensors & bioelectronics.

[112]  Joseph C Liao,et al.  Advances and challenges in biosensor-based diagnosis of infectious diseases , 2014, Expert review of molecular diagnostics.

[113]  Liangfang Zhang,et al.  Erythrocyte‐Inspired Delivery Systems , 2012, Advanced healthcare materials.

[114]  Yuyan Shao,et al.  Graphene Based Electrochemical Sensors and Biosensors: A Review , 2010 .

[115]  Yanglong Hou,et al.  Near-infrared light and tumor microenvironment dual responsive size-switchable nanocapsules for multimodal tumor theranostics , 2019, Nature Communications.

[116]  Dong-Dong Zhang,et al.  Erythrocyte membrane bioinspired near-infrared persistent luminescence nanocarriers for in vivo long-circulating bioimaging and drug delivery. , 2018, Biomaterials.

[117]  Igor Meglinski,et al.  The advancement of blood cell research by optical tweezers , 2020, Reviews in Physics.

[118]  Jeffrey A. Chao,et al.  An RNA biosensor for imaging the first round of translation from single cells to living animals , 2015, Science.

[119]  Petra Krystek,et al.  Particle size-dependent organ distribution of gold nanoparticles after intravenous administration. , 2008, Biomaterials.

[120]  Samir Mitragotri,et al.  Prolonged circulation of large polymeric nanoparticles by non-covalent adsorption on erythrocytes. , 2004, Journal of controlled release : official journal of the Controlled Release Society.

[121]  Ralph Weissleder,et al.  Magnetic relaxation switches capable of sensing molecular interactions , 2002, Nature Biotechnology.

[122]  Huang-Hao Yang,et al.  A graphene platform for sensing biomolecules. , 2009, Angewandte Chemie.

[123]  Rakesh Patel,et al.  An Overview of Resealed Erythrocyte Drug Delivery , 2009 .

[124]  David E Benson,et al.  Protein design provides lead(II) ion biosensors for imaging molecular fluxes around red blood cells. , 2009, Biochemistry.

[125]  Beatriz Jurado-Sánchez,et al.  Biomimetic nanoparticles and self-propelled micromotors for biomedical applications , 2019, Materials for Biomedical Engineering.

[126]  Amina Antonacci,et al.  Nanobiosensors for Bioclinical Applications: Pros and Cons , 2020 .

[127]  Klaus Gersonde,et al.  Incorporation of inositol hexaphosphate into intact red blood cells , 2004, Naturwissenschaften.

[128]  R L Juliano,et al.  Drug delivery systems: a brief review. , 1978, Canadian journal of physiology and pharmacology.

[129]  Thomas J Webster,et al.  A review of small molecules and drug delivery applications using gold and iron nanoparticles , 2019, International journal of nanomedicine.

[130]  Igor Meglinski,et al.  Mutual interaction of red blood cells influenced by nanoparticles , 2019, Scientific Reports.

[131]  M. Magnani,et al.  Cell-based drug delivery. , 2008, Advanced drug delivery reviews.

[132]  C Lizano,et al.  In vitro study of alcohol dehydrogenase and acetaldehyde dehydrogenase encapsulated into human erythrocytes by an electroporation procedure. , 1998, Biochimica et biophysica acta.

[133]  Igor Meglinski,et al.  Impact of Nanocapsules on Red Blood Cells Interplay Jointly Assessed by Optical Tweezers and Microscopy , 2019, Micromachines.

[134]  S. Schrier,et al.  Drug-induced erythrocyte membrane internalization. , 1972, The Journal of clinical investigation.

[135]  M. Magnani,et al.  Erythrocyte-mediated delivery of drugs, peptides and modified oligonucleotides , 2002, Gene Therapy.

[136]  Khalid Saeed,et al.  Nanoparticles: Properties, applications and toxicities , 2017, Arabian Journal of Chemistry.

[137]  Mary E Napier,et al.  More effective nanomedicines through particle design. , 2011, Small.