Cell-Based Drug Delivery Systems with Innate Homing Capability as a Novel Nanocarrier Platform

Abstract Nanoparticle-based drug delivery systems have been designed to treat various diseases. However, many problems remain, such as inadequate tumor targeting and poor therapeutic outcomes. To overcome these obstacles, cell-based drug delivery systems have been developed. Candidates for cell-mediated drug delivery include blood cells, immune cells, and stem cells with innate tumor tropism and low immunogenicity; they act as a disguise to deliver the therapeutic payload. In drug delivery systems, therapeutic agents are encapsulated intracellularly or attached to the surface of the plasma membrane and transported to the desired site. Here, we review the pros and cons of cell-based therapies and discuss their homing mechanisms in the tumor microenvironment. In addition, different strategies to load therapeutic agents inside or on the surface of circulating cells and the current applications for a wide range of disease treatments are summarized.

[1]  J. Bhattacharya,et al.  Antibiotic-Loaded Smart Platelet: A Highly Effective Invisible Mode of Killing Both Antibiotic-Sensitive and -Resistant Bacteria , 2022, ACS omega.

[2]  Weien Yuan,et al.  Clinical progress and advanced research of red blood cells based drug delivery system. , 2021, Biomaterials.

[3]  Nikola A. Ivica,et al.  Tracking the CAR-T Revolution: Analysis of Clinical Trials of CAR-T and TCR-T Therapies for the Treatment of Cancer (1997–2020) , 2021, Healthcare.

[4]  Rosalie M Sterner,et al.  CAR-T cell therapy: current limitations and potential strategies , 2021, Blood Cancer Journal.

[5]  S. Mitragotri,et al.  The evolution of commercial drug delivery technologies , 2021, Nature Biomedical Engineering.

[6]  Yu Su,et al.  Current Advances and Challenges of Mesenchymal Stem Cells-Based Drug Delivery System and Their Improvements. , 2021, International journal of pharmaceutics.

[7]  B. Engelhardt,et al.  Biotin-NeutrAvidin Mediated Immobilization of Polymer Micro- and Nanoparticles on T Lymphocytes. , 2021, Bioconjugate chemistry.

[8]  H. Klok,et al.  Chemical Cell Surface Modification and Analysis of Nanoparticle-Modified Living Cells. , 2021, ACS applied bio materials.

[9]  Hongwei Fu,et al.  Stem cell and its derivatives as drug delivery vehicles: an effective new strategy of drug delivery system , 2021, All Life.

[10]  Jeffrey S. Miller,et al.  Exploring the NK cell platform for cancer immunotherapy , 2020, Nature Reviews Clinical Oncology.

[11]  M. Smyth,et al.  The NK cell–cancer cycle: advances and new challenges in NK cell–based immunotherapies , 2020, Nature Immunology.

[12]  J. Liesveld,et al.  Stem cell homing: From physiology to therapeutics , 2020, Stem cells.

[13]  G. Opdenakker,et al.  Neutrophils: Underestimated Players in the Pathogenesis of Multiple Sclerosis (MS) , 2020, International journal of molecular sciences.

[14]  Xinyu Wang,et al.  Microfluidic-mediated nano-drug delivery systems: from fundamentals to fabrication for advanced therapeutic applications. , 2020, Nanoscale.

[15]  J. Bueren,et al.  Cell Therapy With Mesenchymal Stem Cells Induces an Innate Immune Memory Response That Attenuates Experimental Colitis in the Long Term , 2020, Journal of Crohn's & colitis.

[16]  Kai Wang,et al.  Targeted Repair of Vascular Injury by Adipose‐Derived Stem Cells Modified with P‐Selectin Binding Peptide , 2020, Advanced science.

[17]  Jie Cao,et al.  Targeted nanocarriers based on iodinated-cyanine dyes as immunomodulators for synergistic phototherapy. , 2020, Nanoscale.

[18]  C. Fu,et al.  Nanoparticle Drug Delivery System for Glioma and Its Efficacy Improvement Strategies: A Comprehensive Review , 2020, International journal of nanomedicine.

[19]  F. Ataullakhanov,et al.  Erythrocytes as Carriers: From Drug Delivery to Biosensors , 2020, Pharmaceutics.

[20]  Yong Gu Lee,et al.  Impaired death receptor signaling in leukemia causes antigen-independent resistance by inducing CAR T cell dysfunction. , 2020, Cancer discovery.

[21]  Zhihong Yang,et al.  Cell-mediated targeting drugs delivery systems , 2020, Drug delivery.

[22]  June Tracking the CAR-T revolution: Analysis of clinical trials of CAR-T and TCR therapies for the treatment of cancer , 2020 .

[23]  B. Baradaran,et al.  The effect of Yarrowia lipolytica L-asparaginase on apoptosis induction and inhibition of growth in Burkitt's lymphoma Raji and acute lymphoblastic leukemia MOLT-4 cells. , 2019, International journal of biological macromolecules.

[24]  Behnaz Valipour,et al.  NK cells: An attractive candidate for cancer therapy , 2019, Journal of cellular physiology.

[25]  G. Bardi,et al.  Natural Polysaccharide Nanomaterials: An Overview of Their Immunological Properties , 2019, International journal of molecular sciences.

[26]  Yanbo Zhang,et al.  Mesenchymal Stem Cells for Regenerative Medicine , 2019, Cells.

[27]  Yajing Wang,et al.  Mesenchymal stem cells-curcumin loaded chitosan nanoparticles hybrid vectors for tumor-tropic therapy. , 2019, International journal of biological macromolecules.

[28]  T. Ma,et al.  Development of a microdevice-based human mesenchymal stem cell-mediated drug delivery system. , 2019, Biomaterials science.

[29]  Gareth R. Williams,et al.  Platelet-membrane-biomimetic nanoparticles for targeted antitumor drug delivery , 2019, Journal of Nanobiotechnology.

[30]  G. Basturea,et al.  Endocytosis , 1985, Springer US.

[31]  H. Mandel,et al.  Safety and Efficacy of Erythrocyte Encapsulated Thymidine Phosphorylase in Mitochondrial Neurogastrointestinal Encephalomyopathy , 2019, Journal of clinical medicine.

[32]  Lin Mei,et al.  Efficient lung cancer-targeted drug delivery via a nanoparticle/MSC system , 2018, Acta pharmaceutica Sinica. B.

[33]  Byung‐Hyun Cha,et al.  Cell surface engineering and application in cell delivery to heart diseases , 2018, Journal of biological engineering.

[34]  Ping Gong,et al.  Cell-Membrane Immunotherapy Based on Natural Killer Cell Membrane Coated Nanoparticles for the Effective Inhibition of Primary and Abscopal Tumor Growth. , 2018, ACS nano.

[35]  Zhen Gu,et al.  Cardiac cell–integrated microneedle patch for treating myocardial infarction , 2018, Science Advances.

[36]  Quanyin Hu,et al.  Conjugation of haematopoietic stem cells and platelets decorated with anti-PD-1 antibodies augments anti-leukaemia efficacy , 2018, Nature Biomedical Engineering.

[37]  M. Chapman,et al.  Nanoparticle‐Laden Macrophages for Tumor‐Tropic Drug Delivery , 2018, Advanced materials.

[38]  Xiaoyi Sun,et al.  Mesenchymal stem cells loaded with paclitaxel-poly(lactic-co-glycolic acid) nanoparticles for glioma-targeting therapy , 2018, International journal of nanomedicine.

[39]  J. Isaacs,et al.  Concise Review: Mesenchymal Stem Cell‐Based Drug Delivery: The Good, the Bad, the Ugly, and the Promise , 2018, Stem cells translational medicine.

[40]  M. Y. Thanuja,et al.  Bioengineered cellular and cell membrane‐derived vehicles for actively targeted drug delivery: So near and yet so far , 2018, Advanced drug delivery reviews.

[41]  L. Jeng,et al.  Role of Insulin-like Growth Factor 1 Receptor Signaling in Stem Cell Stemness and Therapeutic Efficacy , 2018, Cell transplantation.

[42]  Jennifer A. Rohrs,et al.  CAR-T Cells Surface-Engineered with Drug-Encapsulated Nanoparticles Can Ameliorate Intratumoral T-cell Hypofunction , 2018, Cancer Immunology Research.

[43]  F. Cuisinier,et al.  Dental pulp stem cells used to deliver the anticancer drug paclitaxel , 2018, Stem Cell Research & Therapy.

[44]  Ö. Met,et al.  Chemokine receptor engineering of T cells with CXCR2 improves homing towards subcutaneous human melanomas in xenograft mouse model , 2018, Oncoimmunology.

[45]  M. Sarazin,et al.  Neutrophil hyperactivation correlates with Alzheimer's disease progression , 2018, Annals of neurology.

[46]  T. Hyeon,et al.  General and Facile Coating of Single Cells via Mild Reduction. , 2018, Journal of the American Chemical Society.

[47]  G. Golomb,et al.  Monocyte-mediated drug delivery systems for the treatment of cardiovascular diseases , 2018, Drug Delivery and Translational Research.

[48]  T. Iida,et al.  The Phagocytic Function of Macrophage-Enforcing Innate Immunity and Tissue Homeostasis , 2017, International journal of molecular sciences.

[49]  J. Berlin,et al.  Exploiting homing abilities of cell carriers: Targeted delivery of nanoparticles for cancer therapy , 2017, Biochemical pharmacology.

[50]  Shukry J. Habib,et al.  Wnt ligand presentation and reception: from the stem cell niche to tissue engineering , 2017, Open Biology.

[51]  Tithi Ghosh,et al.  Tumor promoting role of anti-tumor macrophages in tumor microenvironment. , 2017, Cellular immunology.

[52]  Peipei Xu,et al.  Doxorubicin-loaded platelets conjugated with anti-CD22 mAbs: a novel targeted delivery system for lymphoma treatment with cardiopulmonary avoidance , 2017, Oncotarget.

[53]  H. Lodish,et al.  Engineered erythrocytes covalently linked to antigenic peptides can protect against autoimmune disease , 2017, Proceedings of the National Academy of Sciences.

[54]  C. Dong,et al.  Immune Cell-Mediated Biodegradable Theranostic Nanoparticles for Melanoma Targeting and Drug Delivery. , 2017, Small.

[55]  S. Geary,et al.  Surface engineering tumor cells with adjuvant‐loaded particles for use as cancer vaccines , 2017, Journal of controlled release : official journal of the Controlled Release Society.

[56]  Yi Zhang,et al.  Tumor-associated macrophages: from basic research to clinical application , 2017, Journal of Hematology & Oncology.

[57]  Xunbin Wei,et al.  Systemically Infused Mesenchymal Stem Cells Show Different Homing Profiles in Healthy and Tumor Mouse Models , 2017, Stem cells translational medicine.

[58]  Liangzhu Feng,et al.  Photosensitizer Decorated Red Blood Cells as an Ultrasensitive Light-Responsive Drug Delivery System. , 2017, ACS applied materials & interfaces.

[59]  I. Galea,et al.  The blood-brain barrier in systemic inflammation , 2017, Brain, Behavior, and Immunity.

[60]  Todd M. Allen,et al.  Antigen recognition-triggered drug delivery mediated by nanocapsule-functionalized cytotoxic T-cells. , 2017, Biomaterials.

[61]  R. Sackstein,et al.  T-Lymphocyte Homing: An Underappreciated yet Critical Hurdle for Successful Cancer Immunotherapy , 2017, Laboratory investigation; a journal of technical methods and pathology.

[62]  Zhenjia Wang,et al.  Leukocyte-mediated Delivery of Nanotherapeutics in Inflammatory and Tumor Sites , 2017, Theranostics.

[63]  Yanyan Jiang,et al.  Maximized nanodrug-loaded mesenchymal stem cells by a dual drug-loaded mode for the systemic treatment of metastatic lung cancer , 2017, Drug delivery.

[64]  Sandra C Bustamante López,et al.  Characterization of carrier erythrocytes for biosensing applications , 2017, Journal of biomedical optics.

[65]  P. Frankel,et al.  Neural Stem Cell–Based Anticancer Gene Therapy: A First-in-Human Study in Recurrent High-Grade Glioma Patients , 2016, Clinical Cancer Research.

[66]  Samir Mitragotri,et al.  Red blood cells: Supercarriers for drugs, biologicals, and nanoparticles and inspiration for advanced delivery systems. , 2016, Advanced drug delivery reviews.

[67]  M. Sitti,et al.  Bioengineered and biohybrid bacteria-based systems for drug delivery. , 2016, Advanced drug delivery reviews.

[68]  D. Greaves,et al.  A novel real time imaging platform to quantify macrophage phagocytosis , 2016, Biochemical pharmacology.

[69]  M. Essand,et al.  Safe engineering of CAR T cells for adoptive cell therapy of cancer using long‐term episomal gene transfer , 2016, EMBO molecular medicine.

[70]  E. Hattingen,et al.  ErbB2/HER2-Specific NK Cells for Targeted Therapy of Glioblastoma. , 2016, Journal of the National Cancer Institute.

[71]  A. de Becker,et al.  Homing and migration of mesenchymal stromal cells: How to improve the efficacy of cell therapy? , 2016, World journal of stem cells.

[72]  S. Gordon Phagocytosis: An Immunobiologic Process. , 2016, Immunity.

[73]  Jin Gao,et al.  Neutrophil-Mediated Delivery of Therapeutic Nanoparticles across Blood Vessel Barrier for Treatment of Inflammation and Infection. , 2015, ACS nano.

[74]  Wei Wang,et al.  NK Cell-Mediated Antibody-Dependent Cellular Cytotoxicity in Cancer Immunotherapy , 2015, Front. Immunol..

[75]  F. Sharp,et al.  Targeting Neutrophils in Ischemic Stroke: Translational Insights from Experimental Studies , 2015, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[76]  Cheng Dong,et al.  Design strategies and applications of circulating cell-mediated drug delivery systems. , 2015, ACS biomaterials science & engineering.

[77]  M. Smyth,et al.  Balancing natural killer cell activation through paired receptors , 2015, Nature Reviews Immunology.

[78]  J. Pollard,et al.  Immune cell promotion of metastasis , 2015, Nature Reviews Immunology.

[79]  Ashutosh Chilkoti,et al.  Co‐opting biology to deliver drugs , 2014, Biotechnology and bioengineering.

[80]  Samir Mitragotri,et al.  Overcoming the challenges in administering biopharmaceuticals: formulation and delivery strategies , 2014, Nature Reviews Drug Discovery.

[81]  Rajbir Singh,et al.  Erythrocytes-based synthetic delivery systems: transition from conventional to novel engineering strategies , 2014, Expert opinion on drug delivery.

[82]  P. Rameshwar,et al.  Stem cell delivery of therapies for brain disorders , 2014, Clinical and Translational Medicine.

[83]  Jeffrey W Pollard,et al.  Tumor-associated macrophages: from mechanisms to therapy. , 2014, Immunity.

[84]  R. Weinberg,et al.  Tackling the cancer stem cells — what challenges do they pose? , 2014, Nature Reviews Drug Discovery.

[85]  Kam W. Leong,et al.  Whole Blood Cells Loaded with Messenger RNA as an Anti‐Tumor Vaccine , 2014, Advanced healthcare materials.

[86]  L. Moretta,et al.  Effect of tumor cells and tumor microenvironment on NK‐cell function , 2014, European journal of immunology.

[87]  Jennifer A. Prescher,et al.  Selective uptake of single walled carbon nanotubes by circulating monocytes for enhanced tumour delivery , 2014, Nature nanotechnology.

[88]  QUAN LIU,et al.  Cell-penetrating peptides meditated encapsulation of protein therapeutics into intact red blood cells and its application. , 2014, Journal of controlled release : official journal of the Controlled Release Society.

[89]  J. Berlin,et al.  Neural stem cells improve intracranial nanoparticle retention and tumor-selective distribution. , 2014, Future oncology.

[90]  J. Kurtzberg,et al.  Allogeneic human mesenchymal stem cell therapy (remestemcel-L, Prochymal) as a rescue agent for severe refractory acute graft-versus-host disease in pediatric patients. , 2014, Biology of blood and marrow transplantation : journal of the American Society for Blood and Marrow Transplantation.

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

[92]  W. Prasongchean Introduction to Stem cells and Regenerative Medicine , 2013 .

[93]  A. Caplan,et al.  MSCs: Delivery Routes and Engraftment, Cell-Targeting Strategies, and Immune Modulation , 2013, Stem cells international.

[94]  G. Damonte,et al.  Erythrocytes-mediated Delivery of Dexamethasone 21-phosphate in Steroid-dependent Ulcerative Colitis: A Randomized, Double-blind Sham-controlled Study , 2013, Inflammatory bowel diseases.

[95]  R. Casaburi,et al.  A placebo-controlled, randomized trial of mesenchymal stem cells in COPD. , 2013, Chest.

[96]  J. Frank,et al.  A first-in-human study of neural stem cells (NSCs) expressing cytosine deaminase (CD) in combination with 5-fluorocytosine (5-FC) in patients with recurrent high-grade glioma. , 2013 .

[97]  P. Kubes,et al.  Neutrophil recruitment and function in health and inflammation , 2013, Nature Reviews Immunology.

[98]  S. H. A. Rizvi,et al.  Formulation development of albumin based theragnostic nanoparticles as a potential delivery system for tumor targeting , 2013, Journal of drug targeting.

[99]  E. D. de Vries,et al.  A review on CXCR4/CXCL12 axis in oncology: no place to hide. , 2013, European journal of cancer.

[100]  J. Burns,et al.  MSC and Tumors: Homing, Differentiation, and Secretion Influence Therapeutic Potential. , 2013, Advances in biochemical engineering/biotechnology.

[101]  J. Hubbell,et al.  Engineering antigens for in situ erythrocyte binding induces T-cell deletion , 2012, Proceedings of the National Academy of Sciences.

[102]  George Kolios,et al.  Introduction to Stem Cells and Regenerative Medicine , 2012, Respiration.

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

[104]  D. Irvine,et al.  Synapse-directed delivery of immunomodulators using T-cell-conjugated nanoparticles. , 2012, Biomaterials.

[105]  Yujie Ma,et al.  Virus-based nanocarriers for drug delivery. , 2012, Advanced drug delivery reviews.

[106]  F. Wenz,et al.  Tumor–platelet interaction in solid tumors , 2012, International journal of cancer.

[107]  E. Choi,et al.  Use of macrophages to deliver therapeutic and imaging contrast agents to tumors. , 2012, Biomaterials.

[108]  James J Moon,et al.  Engineering Nano‐ and Microparticles to Tune Immunity , 2012, Advanced materials.

[109]  S. Kiriakidis,et al.  Hypoxia—a key regulator of angiogenesis and inflammation in rheumatoid arthritis , 2012, Nature Reviews Rheumatology.

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

[111]  L. Zitvogel,et al.  Trial watch , 2012, Oncoimmunology.

[112]  K. Ley,et al.  Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. , 2011, Blood.

[113]  C. Larochelle,et al.  How do immune cells overcome the blood–brain barrier in multiple sclerosis? , 2011, FEBS letters.

[114]  S. Rosenberg,et al.  Treating cancer with genetically engineered T cells. , 2011, Trends in biotechnology.

[115]  P. Kubes,et al.  The neutrophil in vascular inflammation , 2011, Nature Medicine.

[116]  H. Gendelman,et al.  Active Targeted Macrophage-mediated Delivery of Catalase to Affected Brain Regions in Models of Parkinson's Disease. , 2011, Journal of nanomedicine & nanotechnology.

[117]  Wei-Hsin Hsu,et al.  Novel geometry type of nanocarriers mitigated the phagocytosis for drug delivery. , 2011, Journal of controlled release : official journal of the Controlled Release Society.

[118]  Albert Zlotnik,et al.  Homeostatic chemokine receptors and organ-specific metastasis , 2011, Nature Reviews Immunology.

[119]  Dong Chen,et al.  Silica nanorattle-doxorubicin-anchored mesenchymal stem cells for tumor-tropic therapy. , 2011, ACS nano.

[120]  D. Irvine,et al.  Bio-inspired, bioengineered and biomimetic drug delivery carriers , 2011, Nature Reviews Drug Discovery.

[121]  J. Freedman,et al.  Platelets and the immune continuum , 2011, Nature Reviews Immunology.

[122]  U. A. Ndefo,et al.  Sipuleucel-T (provenge) injection: the first immunotherapy agent (vaccine) for hormone-refractory prostate cancer. , 2011, P & T : a peer-reviewed journal for formulary management.

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

[124]  L. Ciaccia Fundamentals of Inflammation , 2011, The Yale Journal of Biology and Medicine.

[125]  A. Hoffman,et al.  Efficient Intracellular Delivery of a Pro-Apoptotic Peptide With A pH-Responsive Carrier. , 2011, Reactive & functional polymers.

[126]  B Gleich,et al.  Human erythrocytes as nanoparticle carriers for magnetic particle imaging , 2010, Physics in medicine and biology.

[127]  P. Schiller,et al.  Mesenchymal stem cells as cellular vehicles for delivery of nanoparticles to brain tumors. , 2010, Biomaterials.

[128]  P. Kubes,et al.  Intravascular Danger Signals Guide Neutrophils to Sites of Sterile Inflammation , 2010, Science.

[129]  G. Almeida-Porada,et al.  Mesenchymal stem cells as therapeutics and vehicles for gene and drug delivery. , 2010, Advanced drug delivery reviews.

[130]  C. Rolny,et al.  A chemotactic gradient sequestered on endothelial heparan sulfate induces directional intraluminal crawling of neutrophils. , 2010, Blood.

[131]  S. Rankin,et al.  Neutrophil kinetics in health and disease , 2010, Trends in immunology.

[132]  Soong Ho Um,et al.  Therapeutic cell engineering using surface-conjugated synthetic nanoparticles , 2010, Nature Medicine.

[133]  D. Brooks,et al.  Red blood cell membrane grafting of multi-functional hyperbranched polyglycerols. , 2010, Biomaterials.

[134]  A. Giaccia,et al.  Hypoxia, inflammation, and the tumor microenvironment in metastatic disease , 2010, Cancer and Metastasis Reviews.

[135]  Markus G. Manz,et al.  Development of Monocytes, Macrophages, and Dendritic Cells , 2010, Science.

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

[137]  P. Couvreur,et al.  Nanocarriers’ entry into the cell: relevance to drug delivery , 2009, Cellular and Molecular Life Sciences.

[138]  H. McMahon,et al.  Mechanisms of endocytosis. , 2009, Annual review of biochemistry.

[139]  J. Ghersi-Egea,et al.  The Role of the Choroid Plexus in Neutrophil Invasion after Traumatic Brain Injury , 2009, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[140]  Alexander Kabanov,et al.  Facilitated Monocyte-Macrophage Uptake and Tissue Distribution of Superparmagnetic Iron-Oxide Nanoparticles , 2009, PloS one.

[141]  Y. Oh,et al.  Opsonized erythrocyte ghosts for liver-targeted delivery of antisense oligodeoxynucleotides. , 2009, Biomaterials.

[142]  Soong Ho Um,et al.  Surface functionalization of living cells with multilayer patches. , 2008, Nano letters.

[143]  L. Borsig The role of platelet activation in tumor metastasis , 2008, Expert review of anticancer therapy.

[144]  M. Andreeff,et al.  Inflammation and tumor microenvironments: defining the migratory itinerary of mesenchymal stem cells , 2008, Gene Therapy.

[145]  M. Cybulsky,et al.  Getting to the site of inflammation: the leukocyte adhesion cascade updated , 2007, Nature Reviews Immunology.

[146]  S. Mitragotri,et al.  Making polymeric micro- and nanoparticles of complex shapes , 2007, Proceedings of the National Academy of Sciences.

[147]  D. Hackam,et al.  Toll-like receptor 4 plays a role in macrophage phagocytosis during peritoneal sepsis. , 2007, Journal of pediatric surgery.

[148]  A. Koong,et al.  Amplification of tumor hypoxic responses by macrophage migration inhibitory factor-dependent hypoxia-inducible factor stabilization. , 2007, Cancer research.

[149]  Julia L. Gregory,et al.  Macrophage Migration Inhibitory Factor Induces Macrophage Recruitment via CC Chemokine Ligand 21 , 2006, The Journal of Immunology.

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

[151]  A. Steinkasserer,et al.  Small interfering RNA (siRNA) delivery into monocyte-derived dendritic cells by electroporation. , 2006, Journal of immunological methods.

[152]  Samir Mitragotri,et al.  Role of target geometry in phagocytosis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[153]  R. Alon,et al.  Immune cell migration in inflammation: present and future therapeutic targets , 2005, Nature Immunology.

[154]  C. Lewis,et al.  Macrophage responses to hypoxia: implications for tumor progression and anti-cancer therapies. , 2005, The American journal of pathology.

[155]  F. Chen,et al.  Analysis of amino acids in individual wheat embryonic protoplast , 2005, Amino Acids.

[156]  M. Smyth,et al.  Activation of NK cell cytotoxicity. , 2005, Molecular immunology.

[157]  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.

[158]  R. Barber,et al.  Cerebral Neutrophil Recruitment, Histology, and Outcome in Acute Ischemic Stroke: An Imaging-Based Study , 2004, Stroke.

[159]  P. Cullis,et al.  Drug Delivery Systems: Entering the Mainstream , 2004, Science.

[160]  A. Palamara,et al.  Erythrocytes as carriers of reduced glutathione (GSH) in the treatment of retroviral infections. , 2003, The Journal of antimicrobial chemotherapy.

[161]  M. Barry,et al.  Metabolically biotinylated adenovirus for cell targeting, ligand screening, and vector purification. , 2003, Molecular therapy : the journal of the American Society of Gene Therapy.

[162]  J. Gehl,et al.  Electroporation: theory and methods, perspectives for drug delivery, gene therapy and research. , 2003, Acta physiologica Scandinavica.

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

[164]  E. de Vries,et al.  A potential role of macrophage activation in the treatment of cancer. , 2002, Critical reviews in oncology/hematology.

[165]  C. van Broeckhoven,et al.  Messenger RNA Electroporation of Human Monocytes, Followed by Rapid In Vitro Differentiation, Leads to Highly Stimulatory Antigen-Loaded Mature Dendritic Cells1 , 2002, The Journal of Immunology.

[166]  L Bigi,et al.  Erythrocyte‐mediated delivery of dexamethasone in patients with chronic obstructive pulmonary disease , 2001, Biotechnology and applied biochemistry.

[167]  M. Pinilla,et al.  Mouse erythrocytes as carriers for coencapsulated alcohol and aldehyde dehydrogenase obtained by electroporation in vivo survival rate in circulation, organ distribution and ethanol degradation. , 2001, Life sciences.

[168]  P. Vaupel,et al.  Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. , 2001, Journal of the National Cancer Institute.

[169]  M. Pinilla,et al.  In vitro and in vivo study of glutamate dehydrogenase encapsulated into mouse erythrocytes by a hypotonic dialysis procedure. , 1999, Life sciences.

[170]  H. Sakahara,et al.  Avidin-biotin system for delivery of diagnostic agents. , 1999, Advanced drug delivery reviews.

[171]  A. Lanzavecchia,et al.  From TCR Engagement to T Cell Activation A Kinetic View of T Cell Behavior , 1999, Cell.

[172]  A. Aderem,et al.  Mechanisms of phagocytosis in macrophages. , 1999, Annual review of immunology.

[173]  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.

[174]  M. Cremonesi,et al.  Biochemical modifications of avidin improve pharmacokinetics and biodistribution, and reduce immunogenicity. , 1998, British Journal of Cancer.

[175]  John A. Smith Neutrophils, host defense, and inflammation: a double‐edged sword , 1994, Journal of leukocyte biology.

[176]  P. Kochanek,et al.  Neutrophil accumulation after traumatic brain injury in rats: comparison of weight drop and controlled cortical impact models. , 1994, Journal of neurotrauma.

[177]  T. Carlos,et al.  Leukocyte-endothelial adhesion molecules. , 1994, Blood.

[178]  T. Standiford,et al.  Cytokines. 2. Cytokines and lung inflammation: mechanisms of neutrophil recruitment to the lung. , 1993, Thorax.

[179]  A. Chait,et al.  Phagocytosis of aggregated lipoprotein by macrophages: low density lipoprotein receptor-dependent foam-cell formation. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[180]  R H Glew,et al.  Enzyme loading of erythrocytes. , 1973, Proceedings of the National Academy of Sciences of the United States of America.