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

https://doi.org/10.1016/j.bios.2020.112845Get rights and content

Highlights

  • Red Blood Cells (RBC)-mediated delivery of in vivo nano-biosensors for applications of bio-imaging.

  • Analytical detection of biomolecules and cellular activities.

  • Technical framework of the state-of-the-art RBC-mediated delivery systems.

Abstract

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.

Introduction

A nanobiosensor is an analytical device in nanometer scales used to probe or measure biochemical substances, usually comprises a sensing element “bio-receptor” to interact with the targeted analyte and produce a detectable physical signal to be transformed by a transducer component, making it possible to convert and quantify the biological and biochemical signals through optical, electronic, thermal, or magnetic methods (Prasad, 2014). In recent years, together with the progress in the nano-technology, nanobiosensors that can be used in vivo are vigorously developing as they can provide real-time, rapid, and accurate analysis of physiological and pathological processes in living organisms, which has been a hot research topic in medical and ecological diagnostics (Sadovoy and Teh, 2015; Gurkov et al., 2016, 2017; Volkova et al., 2017).

In the emerging field of nanomedicine, novel nano-agents are intensively developed and manufactured for potential biomedical applications including nano-biosensing, nano-diagnostics, and personalized therapy while lacking comprehensive assessment of their potential health risks. In recent years, the application of smart drug delivery systems (DDSs) in the field of in vivo biosensing has attracted extensive attention and been widely studied to promote the clinical early diagnosis and therapy, especially early cancer screening and treatment (Argyo et al., 2014; Wang et al., 2019). Controllable, precise, and safe delivery of diagnostic nano devices and therapeutic agents to the target tissues, organs, or cells is an important determinant in every clinical approach. In recent years, inspired by the red blood cell (RBC)-mediated delivery methods, nanomaterial-based theragnostic platforms for bio-sensing applications including bio-imaging at the single-cell level, advanced medical diagnostics, and analytical detection of biomolecules and cellular activities are facing new development opportunities.

At present, there are many reviews on the medical applications based on the development of new sensing techniques capable of performing very sensitive detection and quantifying certain parameters, especially based on smart nanobiosensors (Ahmed et al., 2014; Attaallah et al., 2020; Chamorro-Garcia and Merkoçi, 2016; Ghorbani et al., 2019; Maxwell et al., 2002; Prasad, 2014). Numbers of reviews have summarized the cell-based DDSs in general (Glassman et al., 2020; Jahangirian et al., 2019; Kurapati et al., 2019; Sun et al., 2017). However, currently, there are only a few of reviews place emphasis on the RBC-mediated delivery for specific application areas and the adverse effects on human health induced by the interaction of delivered sensing devices and theranostic agents with blood components.

In this review, the emphasis is placed on the nanomaterial-based in vivo biosensing elements for applications of bio-imaging at the single-cell level, advanced medical diagnostics, and analytical detection of biomolecules and cellular activities that benefited from the RBC-mediated DDSs. Specifically, the technical framework of the state-of-the-art developments of RBC-mediated delivery of theragnostic nano devices/agents is presented. Finally, the advantages, challenges, and the development trends of nanobiosensors based on the RBC-mediated delivery are indicated to inspire the design and implementation of advanced nano-biosensing platforms taking advantage of RBC-delivery modalities.

Section snippets

The application of nanomaterials in biosensing

The revolutionary development of nanotechnology has encouraged tremendous progress in the design of in vivo/vitro diagnostic/therapeutic tools utilizing nanostructures with various types and materials (Anselmo and Mitragotri, 2016; Lucky et al., 2015; Wolfbeis, 2015; Zhou et al., 2015). To date, distinguished by different dimensions and geometry, diverse types of nanomaterials including nanoparticles (NPs), nanofiber, nanotubes, nanorods, and nanoribbon have been studied (Wolfbeis, 2015). Among

RBC-mediated delivery of nanobiosensors and nanoprobes for bio-imaging at the single-cell level

Biosensor systems are widely used in multi-modal bio-imaging at the single-cell level including imaging and tracking of single molecules and molecular interactions, visualizing and monitoring specific enzyme activities, and dynamic imaging of bio-fluids for clinical applications (Stawarski et al., 2014; Tran et al., 2018). With the support of nanomaterials, the design of this kind of biosensor imaging system is more diversified and the performance is further promoted. For example, organic

Principles of cargo loading onto RBCs

Various procedures have been proposed to deliver and transport therapeutic and diagnostic nano-agents through human RBCs so that they can circulate with natural RBCs in the bloodstream for a long time, reach the target position, and be released and accumulated in certain tissues or organs to achieve excellent therapeutic or diagnostic performances (Hu et al., 2012). Numerous therapeutic agents including proteins, nucleic acid, viral agents, and novel nano-drugs have been explored to be carried

Advantages of RBC-mediated delivery of biosensing nano-agents

Circulation prolongation is one of the main advantages of RBC-delivered biosensing nano-agents. For intravenous injection of free NPs, the particle uptake in liver and spleen is the most significant and shows particle size-dependent organ distribution. Among different sized (10–250 nm) spherical-shaped gold NPs (Au-NPs), large NPs mainly distributed in blood, liver, and spleen, whereas smaller (10 nm) Au-NPs were found in various organs including blood, liver, spleen, kidney, testis, heart,

Conclusions and perspectives

In conclusion, with the rapid development in the emerging field of nanomedicine, novel NPs have been investigated in preclinical studies and are being transformed to a great variety of clinical applications including cancer imaging (e.g., with silica NPs) and thermal ablation of tumors (e.g., with gold and iron-oxide NPs). Currently, transport and delivery of NP-based theranostic agents via their covalent or physical interactions with RBCs have been developed rapidly and are currently in

Funding

This work was partially funded by the China Scholarship Council (CSC No. 201706410089, R.Z.), STSM Grant from COST Action CA 17,140 ″Cancer Nanomedicine from the Bench to the Bedside” supported by COST (European Cooperation in Science and Technology) (grant No. ECOST-STSM-CA17140-230,919-113049, R.Z.). EDUFI Fellowship (TM-17-10,370, TM-18-10,820, T.A.) and Suomen Kulttuurirahasto (grant No. 00190188, T.A.). The authors also acknowledge the contribution of Russian Science Foundation (Projects:

Author contributions

R.Z; Writing – original draft preparation, Writing – review & editing, T.A; Writing – review & editing, A.P; Supervision, A.B; Supervision, I.M; Writing – review & editing, Supervision, Funding acquisition, All authors have read and agreed to the published version of the manuscript.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References (138)

  • S. Kumar et al.

    Graphene, carbon nanotubes, zinc oxide and gold as elite nanomaterials for fabrication of biosensors for healthcare

    Biosens. Bioelectron.

    (2015)
  • J.-M. Liu et al.

    Erythrocyte membrane bioinspired near-infrared persistent luminescence nanocarriers for in vivo long-circulating bioimaging and drug delivery

    Biomaterials

    (2018)
  • C. Lizano et al.

    In vitro study of alcohol dehydrogenase and acetaldehyde dehydrogenase encapsulated into human erythrocytes by an electroporation procedure

    Biochim. Biophys. Acta Gen. Subj.

    (1998)
  • S.M. Moghimi et al.

    Stealth liposomes and long circulating nanoparticles: critical issues in pharmacokinetics, opsonization and protein-binding properties

    Prog. Lipid Res.

    (2003)
  • V.R. Muzykantov et al.

    Targeting of enzyme immobilized on erythrocyte membrane to collagen-coated surface

    FEBS Lett.

    (1985)
  • V.R. Muzykantov et al.

    Target-sensitive immunoerythrocytes: interaction of biotinylated red blood cells with immobilized avidin induces their lysis by complement

    Biochim. Biophys. Acta Biomembr.

    (1996)
  • I. Nobiron

    DNA vaccination against bovine viral diarrhoea virus induces humoral and cellular responses in cattle with evidence for protection against viral challenge

    Vaccine

    (2003)
  • R. Oppenheim

    Solid colloidal drug delivery systems: Nanoparticles

    Int. J. Pharm.

    (1981)
  • M. Pacheco-Jerez et al.

    Biomimetic nanoparticles and self-propelled micromotors for biomedical applications

  • K. Park

    Controlled drug delivery systems: past forward and future back

    J. Contr. Release

    (2014)
  • F. Pierigè et al.

    Cell-based drug delivery

    Adv. Drug Deliv. Rev.

    (2008)
  • R. Rizzuto et al.

    Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells

    Curr. Biol.

    (1995)
  • A. Sadovoy et al.

    Encapsulated biosensors for advanced tissue diagnostics

  • R. Salahandish et al.

    Nano-biosensor for highly sensitive detection of HER2 positive breast cancer

    Biosens. Bioelectron.

    (2018)
  • M. Sharifi et al.

    Cancer diagnosis using nanomaterials based electrochemical nanobiosensors

    Biosens. Bioelectron.

    (2019)
  • M. Sharifi et al.

    Development of point-of-care nanobiosensors for breast cancers diagnosis

    Talanta

    (2020)
  • J. Shi et al.

    A fullerene-based multi-functional nanoplatform for cancer theranostic applications

    Biomaterials

    (2014)
  • N.S. Abadeer et al.

    Recent progress in cancer thermal therapy using gold nanoparticles

    J. Phys. Chem. C

    (2016)
  • M.U. Ahmed et al.

    Personalized diagnostics and biosensors: a review of the biology and technology needed for personalized medicine

    Crit. Rev. Biotechnol.

    (2014)
  • F. Alexis et al.

    Factors affecting the clearance and biodistribution of polymeric nanoparticles

    Mol. Pharm.

    (2008)
  • A.C. Anselmo et al.

    Delivering nanoparticles to lungs while avoiding liver and spleen through adsorption on red blood cells

    ACS Nano

    (2013)
  • A.C. Anselmo et al.

    Nanoparticles in the clinic

    Bioeng. Transl. Med.

    (2016)
  • A. Antonelli et al.

    Red blood cells as carriers of iron oxide-based contrast agents for diagnostic applications

    J. Biomed. Nanotechnol.

    (2014)
  • A. 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

    Nano Res

    (2017)
  • A. Antonelli et al.

    Red blood cells as carriers in magnetic particle imaging

    Biomed. Tech. Eng.

    (2013)
  • C. Argyo et al.

    Multifunctional mesoporous silica nanoparticles as a universal platform for drug delivery

    Chem. Mater.

    (2014)
  • R. Attaallah et al.

    Nanobiosensors for bioclinical applications: pros and cons

  • T. Avsievich et al.

    Mutual interaction of red blood cells influenced by nanoparticles

    Sci. Rep.

    (2019)
  • T. Avsievich et al.

    Mutual interaction of red blood cells assessed by optical tweezers and scanning electron microscopy imaging

    Opt. Lett.

    (2018)
  • T. Avsievich et al.

    Impact of nanocapsules on red blood cells interplay jointly assessed by optical tweezers and microscopy

    Micromachines

    (2020)
  • B. Bahmani et al.

    Erythrocyte-derived photo-theranostic agents: hybrid nano-vesicles containing indocyanine green for near infrared imaging and therapeutic applications

    Sci. Rep.

    (2013)
  • E.V. Batrakova et al.

    Cell-mediated drug delivery

    Expet Opin. Drug Deliv.

    (2011)
  • I. Ben-Bassat et al.

    Drug-induced erythrocyte membrane internalization

    J. Clin. Invest.

    (1972)
  • Y. Bian et al.

    Silver nanoparticles promote procoagulant activity of red blood cells: a potential risk of thrombosis in susceptible population. Part

    Fibre Toxicol

    (2019)
  • M. Brähler et al.

    Magnetite-loaded carrier erythrocytes as contrast agents for magnetic resonance imaging

    Nano Lett.

    (2006)
  • J.S. Brenner et al.

    Red blood cell-hitchhiking boosts delivery of nanocarriers to chosen organs by orders of magnitude

    Nat. Commun.

    (2018)
  • I. Brigger et al.

    Nanoparticles in cancer therapy and diagnosis

    Adv. Drug Deliv. Rev.

    (2012)
  • A. Chamorro-Garcia et al.

    Nanobiosensors in diagnostics

    Nanobiomedicine

    (2016)
  • C. Chen et al.

    Cellular biosensor based on red blood cells immobilized on Fe3O4 Core/Au Shell nanoparticles for hydrogen peroxide electroanalysis

    Microchim. Acta

    (2010)
  • L. Chen et al.

    Fluorescent nanobiosensors for sensing glucose

    Sensors

    (2018)
  • Cited by (0)

    View full text