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Title: Mesoporous Silica Nanoparticle-Supported Lipid Bilayers (Protocells) for Active Targeting and Delivery to Individual Leukemia Cells

Abstract

Many nanocarrier cancer therapeutics currently under development, as well as those used in the clinical setting, rely upon the enhanced permeability and retention (EPR) effect to passively accumulate in the tumor microenvironment and kill cancer cells. In leukemia, where leukemogenic stem cells and their progeny circulate within the peripheral blood or bone marrow, the EPR effect may not be operative. Thus, for leukemia therapeutics, it is essential to target and bind individual circulating cells. Here in this research, we investigate mesoporous silica nanoparticle (MSN)-supported lipid bilayers (protocells), an emerging class of nanocarriers, and establish the synthesis conditions and lipid bilayer composition needed to achieve highly monodisperse protocells that remain stable in complex media as assessed in vitro by dynamic light scattering and cryo-electron microscopy and ex ovo by direct imaging within a chick chorioallantoic membrane (CAM) model. We show that for vesicle fusion conditions where the lipid surface area exceeds the external surface area of the MSN and the ionic strength exceeds 20 mM, we form monosized protocells (polydispersity index <0.1) on MSN cores with varying size, shape, and pore size, whose conformal zwitterionic supported lipid bilayer confers excellent stability as judged by circulation in the CAM and minimal opsonizationmore » in vivo in a mouse model. Having established protocell formulations that are stable colloids, we further modified them with anti-EGFR antibodies as targeting agents and reverified their monodispersity and stability. Then, using intravital imaging in the CAM, we directly observed in real time the progression of selective targeting of individual leukemia cells (using the established REH leukemia cell line transduced with EGFR) and delivery of a model cargo. In conclusion, overall we have established the effectiveness of the protocell platform for individual cell targeting and delivery needed for leukemia and other disseminated disease.« less

Authors:
 [1];  [2];  [3];  [4];  [3];  [5];  [4];  [3];  [6];  [7];  [8];  [2];  [8];  [9]
+ Show Author Affiliations
  1. Univ. of New Mexico, Albuquerque, NM (United States). Dept. of Chemical and Biological Engineering; Univ. of New Mexico, Albuquerque, NM (United States). Center for Micro-Engineered Materials, Advanced Materials Lab.
  2. Univ. of New Mexico, Albuquerque, NM (United States). Internal Medicine; Oncothyreon, Inc., Seattle, WA (United States)
  3. Univ. of New Mexico, Albuquerque, NM (United States). Center for Micro-Engineered Materials, Advanced Materials Lab.
  4. Univ. of New Mexico, Albuquerque, NM (United States). Health Sciences Center, Biochemistry and Molecular Biology
  5. Vanderbilt Univ., Nashville, TN (United States). Dept. of Biomolecular Engineering
  6. Sandia National Lab. (SNL-CA), Livermore, CA (United States). Advanced Materials Lab.
  7. Univ. of New Mexico, Albuquerque, NM (United States). Dept. of Pathology; Univ. of New Mexico, Albuquerque, NM (United States). Comprehensive Cancer Center
  8. Univ. of New Mexico, Albuquerque, NM (United States). Dept. of Pathology; Univ. of New Mexico, Albuquerque, NM (United States). Comprehensive Cancer Center
  9. Univ. of New Mexico, Albuquerque, NM (United States). Dept. of Chemical and Biological Engineering; Univ. of New Mexico, Albuquerque, NM (United States). Center for Micro-Engineered Materials, Advanced Materials Lab.; Sandia National Lab. (SNL-NM), Albuquerque, NM (United States). Advanced Materials Lab.; Univ. of New Mexico, Albuquerque, NM (United States). Comprehensive Cancer Center
Publication Date:
Research Org.:
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); National Science Foundation (NSF); US Air Force Office of Scientific Research (AFOSR)
OSTI Identifier:
1340264
Report Number(s):
SAND-2016-12522J
Journal ID: ISSN 1936-0851; 649845
Grant/Contract Number:  
AC04-94AL85000; FA 9550-1-14-066; 1344298; DBI-1266377; UO1 CA151792-01
Resource Type:
Accepted Manuscript
Journal Name:
ACS Nano
Additional Journal Information:
Journal Volume: 10; Journal Issue: 9; Journal ID: ISSN 1936-0851
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; chorioallantoic membrane; colloidal stability; leukemia cell targeting; mesoporous silica nanoparticle; supported lipid bilayer

Citation Formats

Durfee, Paul N., Lin, Yu-Shen, Dunphy, Darren R., Muñiz, Ayşe J., Butler, Kimberly S., Humphrey, Kevin R., Lokke, Amanda J., Agola, Jacob O., Chou, Stanley S., Chen, I-Ming, Wharton, Walker, Townson, Jason L., Willman, Cheryl L., and Brinker, C. Jeffrey. Mesoporous Silica Nanoparticle-Supported Lipid Bilayers (Protocells) for Active Targeting and Delivery to Individual Leukemia Cells. United States: N. p., 2016. Web. doi:10.1021/acsnano.6b02819.
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Durfee, Paul N., Lin, Yu-Shen, Dunphy, Darren R., Muñiz, Ayşe J., Butler, Kimberly S., Humphrey, Kevin R., Lokke, Amanda J., Agola, Jacob O., Chou, Stanley S., Chen, I-Ming, Wharton, Walker, Townson, Jason L., Willman, Cheryl L., & Brinker, C. Jeffrey. Mesoporous Silica Nanoparticle-Supported Lipid Bilayers (Protocells) for Active Targeting and Delivery to Individual Leukemia Cells. United States. https://doi.org/10.1021/acsnano.6b02819
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Durfee, Paul N., Lin, Yu-Shen, Dunphy, Darren R., Muñiz, Ayşe J., Butler, Kimberly S., Humphrey, Kevin R., Lokke, Amanda J., Agola, Jacob O., Chou, Stanley S., Chen, I-Ming, Wharton, Walker, Townson, Jason L., Willman, Cheryl L., and Brinker, C. Jeffrey. Fri . "Mesoporous Silica Nanoparticle-Supported Lipid Bilayers (Protocells) for Active Targeting and Delivery to Individual Leukemia Cells". United States. https://doi.org/10.1021/acsnano.6b02819. https://www.osti.gov/servlets/purl/1340264.
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@article{osti_1340264,
title = {Mesoporous Silica Nanoparticle-Supported Lipid Bilayers (Protocells) for Active Targeting and Delivery to Individual Leukemia Cells},
author = {Durfee, Paul N. and Lin, Yu-Shen and Dunphy, Darren R. and Muñiz, Ayşe J. and Butler, Kimberly S. and Humphrey, Kevin R. and Lokke, Amanda J. and Agola, Jacob O. and Chou, Stanley S. and Chen, I-Ming and Wharton, Walker and Townson, Jason L. and Willman, Cheryl L. and Brinker, C. Jeffrey},
abstractNote = {Many nanocarrier cancer therapeutics currently under development, as well as those used in the clinical setting, rely upon the enhanced permeability and retention (EPR) effect to passively accumulate in the tumor microenvironment and kill cancer cells. In leukemia, where leukemogenic stem cells and their progeny circulate within the peripheral blood or bone marrow, the EPR effect may not be operative. Thus, for leukemia therapeutics, it is essential to target and bind individual circulating cells. Here in this research, we investigate mesoporous silica nanoparticle (MSN)-supported lipid bilayers (protocells), an emerging class of nanocarriers, and establish the synthesis conditions and lipid bilayer composition needed to achieve highly monodisperse protocells that remain stable in complex media as assessed in vitro by dynamic light scattering and cryo-electron microscopy and ex ovo by direct imaging within a chick chorioallantoic membrane (CAM) model. We show that for vesicle fusion conditions where the lipid surface area exceeds the external surface area of the MSN and the ionic strength exceeds 20 mM, we form monosized protocells (polydispersity index <0.1) on MSN cores with varying size, shape, and pore size, whose conformal zwitterionic supported lipid bilayer confers excellent stability as judged by circulation in the CAM and minimal opsonization in vivo in a mouse model. Having established protocell formulations that are stable colloids, we further modified them with anti-EGFR antibodies as targeting agents and reverified their monodispersity and stability. Then, using intravital imaging in the CAM, we directly observed in real time the progression of selective targeting of individual leukemia cells (using the established REH leukemia cell line transduced with EGFR) and delivery of a model cargo. In conclusion, overall we have established the effectiveness of the protocell platform for individual cell targeting and delivery needed for leukemia and other disseminated disease.},
doi = {10.1021/acsnano.6b02819},
journal = {ACS Nano},
number = 9,
volume = 10,
place = {United States},
year = {Fri Jul 15 00:00:00 EDT 2016},
month = {Fri Jul 15 00:00:00 EDT 2016}
}
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    Establishing the effects of mesoporous silica nanoparticle properties on in vivo disposition using imaging-based pharmacokinetics
    journal, October 2018

    Cell membrane biomimetic nanoparticles for inflammation and cancer targeting in drug delivery
    journal, January 2020

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    On the issue of transparency and reproducibility in nanomedicine
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    • Leong, Hon S.; Butler, Kimberly S.; Brinker, C. Jeffrey
    • Nature Nanotechnology, Vol. 14, Issue 7
    • DOI: 10.1038/s41565-019-0496-9

    Mesoporous Silica Nanoparticles as Drug Delivery Vehicles in Cancer
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    • Watermann, Anna; Brieger, Juergen
    • Nanomaterials, Vol. 7, Issue 7, p. 189
    • DOI: 10.3390/nano7070189

    Approaches to improve the biocompatibility and systemic circulation of inorganic porous nanoparticles
    journal, January 2018

    • Tamarov, K.; Näkki, S.; Xu, W.
    • Journal of Materials Chemistry B, Vol. 6, Issue 22
    • DOI: 10.1039/c8tb00462e

    Large-Pore Functionalized Mesoporous Silica Nanoparticles as Drug Delivery Vector for a Highly Cytotoxic Hybrid Platinum-Acridine Anticancer Agent
    journal, February 2017

    • Zheng, Ye; Fahrenholtz, Cale D.; Hackett, Christopher L.
    • Chemistry - A European Journal, Vol. 23, Issue 14
    • DOI: 10.1002/chem.201604868

    Toxicological Evaluation of SiO2 Nanoparticles by Zebrafish Embryo Toxicity Test
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    • Vranic, Sandra; Shimada, Yasuhito; Ichihara, Sahoko
    • International Journal of Molecular Sciences, Vol. 20, Issue 4
    • DOI: 10.3390/ijms20040882

    Mesoporous Silica and Organosilica Nanoparticles: Physical Chemistry, Biosafety, Delivery Strategies, and Biomedical Applications
    journal, November 2017

    • Croissant, Jonas G.; Fatieiev, Yevhen; Almalik, Abdulaziz
    • Advanced Healthcare Materials, Vol. 7, Issue 4
    • DOI: 10.1002/adhm.201700831

    The role of surface charge in the interaction of nanoparticles with model pulmonary surfactants
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    Functionalization of carboxylated lignin nanoparticles for targeted and pH-responsive delivery of anticancer drugs
    journal, November 2017

    • Figueiredo, Patrícia; Ferro, Cláudio; Kemell, Marianna
    • Nanomedicine, Vol. 12, Issue 21
    • DOI: 10.2217/nnm-2017-0219

    Versatile Surface Functionalization of Metal-Organic Frameworks through Direct Metal Coordination with a Phenolic Lipid Enables Diverse Applications
    journal, February 2018

    • Zhu, Wei; Xiang, Guolei; Shang, Jin
    • Advanced Functional Materials, Vol. 28, Issue 16
    • DOI: 10.1002/adfm.201705274

    Cell‐Templated Silica Microparticles with Supported Lipid Bilayers as Artificial Antigen‐Presenting Cells for T Cell Activation
    journal, December 2018

    • Olden, Brynn R.; Perez, Caleb R.; Wilson, Ashley L.
    • Advanced Healthcare Materials
    • DOI: 10.1002/adhm.201801188

    Synchronized Ratiometric Codelivery of Metformin and Topotecan through Engineered Nanocarrier Facilitates In Vivo Synergistic Precision Levels at Tumor Site
    journal, August 2018

    • Banala, Venkatesh Teja; Sharma, Shweta; Barnwal, Puja
    • Advanced Healthcare Materials, Vol. 7, Issue 19
    • DOI: 10.1002/adhm.201800300

    Adsorption and fusion of hybrid lipid/polymer vesicles onto 2D and 3D surfaces
    journal, January 2018

    • Paxton, Walter F.; McAninch, Patrick T.; Shin, Sun Hae Ra
    • Soft Matter, Vol. 14, Issue 40
    • DOI: 10.1039/c8sm00343b

    Delivering CRISPR: a review of the challenges and approaches
    journal, January 2018

    Establishing the effects of mesoporous silica nanoparticle properties on in vivo disposition using imaging-based pharmacokinetics
    journal, October 2018

    Understanding the Connection between Nanoparticle Uptake and Cancer Treatment Efficacy using Mathematical Modeling
    journal, May 2018

    Biosafety of Mesoporous Silica Nanoparticles
    journal, August 2018

    Smart Mesoporous Silica Nanoparticles for Protein Delivery
    journal, April 2019

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