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Article ; Online: mRNA-Loaded Lipid Nanoparticles Targeting Immune Cells in the Spleen for Use as Cancer Vaccines

Ryoya Shimosakai / Ikramy A. Khalil / Seigo Kimura / Hideyoshi Harashima

Pharmaceuticals, Vol 15, Iss 8, p

2022 Volume 1017

Abstract: mRNA delivery has recently gained substantial interest for possible use in vaccines. Recently approved mRNA vaccines are administered intramuscularly where they transfect antigen-presenting cells (APCs) near the site of administration, resulting in an ... ...

Abstract	mRNA delivery has recently gained substantial interest for possible use in vaccines. Recently approved mRNA vaccines are administered intramuscularly where they transfect antigen-presenting cells (APCs) near the site of administration, resulting in an immune response. The spleen contains high numbers of APCs, which are located near B and T lymphocytes. Therefore, transfecting APCs in the spleen would be expected to produce a more efficient immune response, but this is a challenging task due to the different biological barriers. Success requires the development of an efficient system that can transfect different immune cells in the spleen. In this study, we report on the development of mRNA-loaded lipid nanoparticles (LNPs) targeting immune cells in the spleen with the goal of eliciting an efficient immune response against the antigen encoded in the mRNA. The developed system is composed of mRNA loaded in LNPs whose lipid composition was optimized for maximum transfection into spleen cells. Dendritic cells, macrophages and B cells in the spleen were efficiently transfected. The optimized LNPs produced efficient dose-dependent cytotoxic T lymphocyte activities that were significantly higher than that produced after local administration. The optimized LNPs encapsulating tumor-antigen encoding mRNA showed both prophylactic and therapeutic antitumor effects in mice.
Keywords	mRNA ; spleen ; immune cell ; vaccine ; lipid nanoparticle ; Medicine ; R ; Pharmacy and materia medica ; RS1-441
Subject code	570
Language	English
Publishing date	2022-08-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article: mRNA-Loaded Lipid Nanoparticles Targeting Immune Cells in the Spleen for Use as Cancer Vaccines.

Shimosakai, Ryoya / Khalil, Ikramy A / Kimura, Seigo / Harashima, Hideyoshi

Pharmaceuticals (Basel, Switzerland)

2022 Volume 15, Issue 8

Abstract	mRNA delivery has recently gained substantial interest for possible use in vaccines. Recently approved mRNA vaccines are administered intramuscularly where they transfect antigen-presenting cells (APCs) near the site of administration, resulting in an immune response. The spleen contains high numbers of APCs, which are located near B and T lymphocytes. Therefore, transfecting APCs in the spleen would be expected to produce a more efficient immune response, but this is a challenging task due to the different biological barriers. Success requires the development of an efficient system that can transfect different immune cells in the spleen. In this study, we report on the development of mRNA-loaded lipid nanoparticles (LNPs) targeting immune cells in the spleen with the goal of eliciting an efficient immune response against the antigen encoded in the mRNA. The developed system is composed of mRNA loaded in LNPs whose lipid composition was optimized for maximum transfection into spleen cells. Dendritic cells, macrophages and B cells in the spleen were efficiently transfected. The optimized LNPs produced efficient dose-dependent cytotoxic T lymphocyte activities that were significantly higher than that produced after local administration. The optimized LNPs encapsulating tumor-antigen encoding mRNA showed both prophylactic and therapeutic antitumor effects in mice.
Language	English
Publishing date	2022-08-18
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2193542-7
ISSN	1424-8247
ISSN	1424-8247
DOI	10.3390/ph15081017
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Article ; Online: Recent advances in the targeting of systemically administered non-viral gene delivery systems.

Khalil, Ikramy A / Sato, Yusuke / Harashima, Hideyoshi

Expert opinion on drug delivery

2019 Volume 16, Issue 10, Page(s) 1037–1050

Abstract: ... ...

Abstract	Introduction
MeSH term(s)	Animals ; Endothelium/metabolism ; Gene Transfer Techniques ; Genetic Therapy/methods ; Humans ; Nanoparticles ; Neoplasms/therapy
Language	English
Publishing date	2019-08-21
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2167286-6
ISSN	1744-7593 ; 1742-5247
ISSN (online)	1744-7593
ISSN	1742-5247
DOI	10.1080/17425247.2019.1656196
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Article ; Online: Novel lipid combination for delivery of plasmid DNA to immune cells in the spleen.

Kimura, Seigo / Khalil, Ikramy A / Elewa, Yaser H A / Harashima, Hideyoshi

Journal of controlled release : official journal of the Controlled Release Society

2021 Volume 330, Page(s) 753–764

Abstract: This study reports on the development of a novel lipid combination that permits the efficient and highly selective delivery of plasmid DNA (pDNA) to immune cells in the spleen. Using DODAP, an ionizable lipid that was previously thought to be inefficient ...

Abstract	This study reports on the development of a novel lipid combination that permits the efficient and highly selective delivery of plasmid DNA (pDNA) to immune cells in the spleen. Using DODAP, an ionizable lipid that was previously thought to be inefficient for gene delivery, we show for the first time, that this ignored lipid can be successfully used for efficient and targeted gene delivery in vivo, but only when combined with DOPE, a specific helper lipid. Using certain DODAP and DOPE ratios resulted in the formation of lipid nanoparticles (LNPs) with a ~ 1000-fold higher gene expression, and this expression was specific for the spleen, making it the most spleen-selective system for transfection using pDNA. The developed DODAP/DOPE-LNPs target immune cells in the spleen via receptors for complement C3 and this pathway is critical for efficient gene expression. We hypothesize that the high spleen transfection activity of DODAP/DOPE-LNPs is caused by the promotion of gene expression associated with B cell activation via complement receptors. LNPs encapsulating tumor-antigen encoding pDNA showed both prophylactic and therapeutic anti-tumor effects. The optimized LNPs resulted in the production of different cytokines and antigen-specific antibodies as well as exerting antigen-specific cytotoxic effects. This study revives the use of DODAP in gene delivery and highlights the importance of using appropriate lipid combinations for delivering genes to specific cells.
MeSH term(s)	DNA ; Lipids ; Nanoparticles ; Plasmids ; Spleen ; Transfection
Chemical Substances	Lipids ; DNA (9007-49-2)
Language	English
Publishing date	2021-01-08
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	632533-6
ISSN	1873-4995 ; 0168-3659
ISSN (online)	1873-4995
ISSN	0168-3659
DOI	10.1016/j.jconrel.2021.01.005
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Article ; Online: An efficient PEGylated gene delivery system with improved targeting: Synergism between octaarginine and a fusogenic peptide.

Khalil, Ikramy A / Harashima, Hideyoshi

International journal of pharmaceutics

2018 Volume 538, Issue 1-2, Page(s) 179–187

Abstract: Because of their ability to translocate different cargos into cells, arginine-rich cell penetrating peptides (CPPs) are promising vehicles for drug and gene delivery. The use of CPP-based carriers, however, is hampered by the lack of specificity and by ... ...

Abstract	Because of their ability to translocate different cargos into cells, arginine-rich cell penetrating peptides (CPPs) are promising vehicles for drug and gene delivery. The use of CPP-based carriers, however, is hampered by the lack of specificity and by interactions with negative serum components. Polyethylene glycol (PEG) is used to decrease such non-specific interactions, albeit its use is associated with reduced transfection efficiency. In this study, we describe the development of PEGylated CPP-based gene carrier with an improved targeting and a high transfection activity. The system was prepared by condensing DNA with a polycation followed by coating with a lipid envelope containing the octaarginine (R8) peptide as a model CPP. R8-modified nanoparticles produced high transfection activities, but the efficiency was reduced by PEG shielding. The reduced activity could be fully restored by the addition of a targeting ligand and a pH-sensitive fusogenic peptide. The efficiency of the proposed system is quite high, even in the presence of serum, and shows improved targeting and selectivity. Surprisingly, the effect of the fusogenic peptide was dramatically reduced in the absence of R8. Although shielded, R8 augmented the activity of the fusogenic peptide, suggesting a synergistic effect between the two peptides at the intracellular level.
MeSH term(s)	Cell-Penetrating Peptides/administration & dosage ; Cell-Penetrating Peptides/chemistry ; Gene Targeting ; Gene Transfer Techniques ; HeLa Cells ; Humans ; Hydrogen-Ion Concentration ; Ligands ; Nanoparticles ; Oligopeptides/administration & dosage ; Oligopeptides/chemistry ; Peptides/chemistry ; Polyethylene Glycols/chemistry ; Transfection
Chemical Substances	Cell-Penetrating Peptides ; Ligands ; Oligopeptides ; Peptides ; octaarginine ; Polyethylene Glycols (30IQX730WE)
Language	English
Publishing date	2018-01-16
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	428962-6
ISSN	1873-3476 ; 0378-5173
ISSN (online)	1873-3476
ISSN	0378-5173
DOI	10.1016/j.ijpharm.2018.01.007
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Article ; Online: Lipid Nanoparticles for Cell-Specific in Vivo Targeted Delivery of Nucleic Acids.

Khalil, Ikramy A / Younis, Mahmoud A / Kimura, Seigo / Harashima, Hideyoshi

Biological & pharmaceutical bulletin

2020 Volume 43, Issue 4, Page(s) 584–595

Abstract: The last few years have witnessed a great advance in the development of nonviral systems for in vivo targeted delivery of nucleic acids. Lipid nanoparticles (LNPs) are the most promising carriers for producing clinically approved products in the future. ... ...

Abstract	The last few years have witnessed a great advance in the development of nonviral systems for in vivo targeted delivery of nucleic acids. Lipid nanoparticles (LNPs) are the most promising carriers for producing clinically approved products in the future. Compared with other systems used for nonviral gene delivery, LNPs provide several advantages including higher stability, low toxicity, and greater efficiency. Additionally, systems based on LNPs can be modified with ligands and devices for controlled biodistribution and internalization into specific cells. Efforts are ongoing to improve the efficiency of lipid-based gene vectors. These efforts depend on the appropriate design of nanocarriers as well as the development of new lipids with improved gene delivery ability. Several ionizable lipids have recently been developed and have shown dramatically improved efficiency. However, enhancing the ability of nanocarriers to target specific cells in the body remains the most difficult challenge. Systemically administered LNPs can access organs in which the capillaries are characterized by the presence of fenestrations, such as the liver and spleen. The liver has received the most attention to date, although targeted delivery to the spleen has recently emerged as a promising tool for modulating the immune system. In this review, we discuss recent advances in the use of LNPs for cell-specific targeted delivery of nucleic acids. We focus mainly on targeting liver hepatocytes and spleen immune cells as excellent targets for gene therapy. We also discuss the potential of endothelial cells as an alternate approach for targeting organs with a continuous endothelium.
MeSH term(s)	Animals ; Endothelial Cells/metabolism ; Gene Transfer Techniques ; Hepatocytes/metabolism ; Humans ; Lipids/administration & dosage ; Nanoparticles/administration & dosage ; Nucleic Acids/administration & dosage ; Spleen/metabolism
Chemical Substances	Lipids ; Nucleic Acids
Language	English
Publishing date	2020-03-31
Publishing country	Japan
Document type	Journal Article ; Review
ZDB-ID	1150271-x
ISSN	1347-5215 ; 0918-6158
ISSN (online)	1347-5215
ISSN	0918-6158
DOI	10.1248/bpb.b19-00743
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Article ; Online: Ultra-small lipid nanoparticles encapsulating sorafenib and midkine-siRNA selectively-eradicate sorafenib-resistant hepatocellular carcinoma in vivo.

Younis, Mahmoud A / Khalil, Ikramy A / Elewa, Yaser H A / Kon, Yasuhiro / Harashima, Hideyoshi

Journal of controlled release : official journal of the Controlled Release Society

2021 Volume 331, Page(s) 335–349

Abstract: Hepatocellular carcinoma (HCC) is a fatal disease with limited therapeutic choices. The stroma-rich tumor microenvironment hinders the in vivo delivery of most nanomedicines. Ultra-small lipid nanoparticles (usLNPs) were designed for the selective co- ... ...

Abstract	Hepatocellular carcinoma (HCC) is a fatal disease with limited therapeutic choices. The stroma-rich tumor microenvironment hinders the in vivo delivery of most nanomedicines. Ultra-small lipid nanoparticles (usLNPs) were designed for the selective co-delivery of the cytotoxic drug, sorafenib (SOR), and siRNA against the Midkine gene (MK-siRNA) to HCC in mice. The usLNPs composed of a novel pH-sensitive lipid, a diversity of phospholipids and a highly-selective targeting peptide. A microfluidic device, iLiNP, was used and a variety of factors were controlled to tune particle size aiming at maximizing tumor penetration efficiency. Optimizing the composition and physico-chemical properties of the usLNPs resulted in an enhanced tumor accumulation, selectivity and in vivo gene silencing. The optimized usLNPs exerted potent gene silencing in the tumor (median effective dose, ED
MeSH term(s)	Animals ; Antineoplastic Agents/therapeutic use ; Carcinoma, Hepatocellular/drug therapy ; Cell Line, Tumor ; Hep G2 Cells ; Humans ; Lipids/therapeutic use ; Liver Neoplasms/drug therapy ; Mice ; Midkine ; Nanoparticles ; RNA, Small Interfering/therapeutic use ; Sorafenib ; Tumor Microenvironment
Chemical Substances	Antineoplastic Agents ; Lipids ; RNA, Small Interfering ; Midkine (137497-38-2) ; Sorafenib (9ZOQ3TZI87)
Language	English
Publishing date	2021-01-21
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	632533-6
ISSN	1873-4995 ; 0168-3659
ISSN (online)	1873-4995
ISSN	0168-3659
DOI	10.1016/j.jconrel.2021.01.021
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Article ; Online: GALA-Modified Lipid Nanoparticles for the Targeted Delivery of Plasmid DNA to the Lungs.

Hagino, Yuta / Khalil, Ikramy A / Kimura, Seigo / Kusumoto, Kenji / Harashima, Hideyoshi

Molecular pharmaceutics

2021 Volume 18, Issue 3, Page(s) 878–888

Abstract: This study describes the development of lipid nanoparticles (LNPs) for the efficient and selective delivery of plasmid DNA (pDNA) to the lungs. The GALA peptide was used as a ligand to target the lung endothelium and as an endosomal escape device. ... ...

Abstract	This study describes the development of lipid nanoparticles (LNPs) for the efficient and selective delivery of plasmid DNA (pDNA) to the lungs. The GALA peptide was used as a ligand to target the lung endothelium and as an endosomal escape device. Transfection activity in the lungs was significantly improved when pDNA was encapsulated in double-coated LNPs. The inner coat was composed of dioleoylphsophoethanolamine and a stearylated octaarginine (STR-R8) peptide, while the outer coat was largely a cationic lipid, di-octadecenyl-trimethylammonium propane, mixed with YSK05, a pH-sensitive lipid, and cholesterol. Optimized amounts of YSK05 and GALA were used to achieve an efficient and lung-selective system. The optimized system produced a high gene expression level in the lungs (>10
MeSH term(s)	Animals ; Cell Line ; DNA/administration & dosage ; Female ; Gene Expression/drug effects ; Gene Transfer Techniques ; Humans ; Hydrogen-Ion Concentration ; Lipids/chemistry ; Liver/drug effects ; Lung/drug effects ; Mice ; Mice, Inbred ICR ; Nanoparticles/chemistry ; Oligopeptides/administration & dosage ; Peptides/chemistry ; Plasmids/administration & dosage ; Transfection/methods
Chemical Substances	Lipids ; Oligopeptides ; Peptides ; octaarginine ; GALA peptide (107658-43-5) ; DNA (9007-49-2)
Language	English
Publishing date	2021-01-25
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2138405-8
ISSN	1543-8392 ; 1543-8384
ISSN (online)	1543-8392
ISSN	1543-8384
DOI	10.1021/acs.molpharmaceut.0c00854
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Article: Novel lipid combination for delivery of plasmid DNA to immune cells in the spleen

Kimura, Seigo / Khalil, Ikramy A / Elewa, Yaser H.A / Harashima, Hideyoshi

Journal of controlled release. 2021 Feb. 10, v. 330

2021

Abstract	This study reports on the development of a novel lipid combination that permits the efficient and highly selective delivery of plasmid DNA (pDNA) to immune cells in the spleen. Using DODAP, an ionizable lipid that was previously thought to be inefficient for gene delivery, we show for the first time, that this ignored lipid can be successfully used for efficient and targeted gene delivery in vivo, but only when combined with DOPE, a specific helper lipid. Using certain DODAP and DOPE ratios resulted in the formation of lipid nanoparticles (LNPs) with a ~ 1000-fold higher gene expression, and this expression was specific for the spleen, making it the most spleen-selective system for transfection using pDNA. The developed DODAP/DOPE-LNPs target immune cells in the spleen via receptors for complement C3 and this pathway is critical for efficient gene expression. We hypothesize that the high spleen transfection activity of DODAP/DOPE-LNPs is caused by the promotion of gene expression associated with B cell activation via complement receptors. LNPs encapsulating tumor-antigen encoding pDNA showed both prophylactic and therapeutic anti-tumor effects. The optimized LNPs resulted in the production of different cytokines and antigen-specific antibodies as well as exerting antigen-specific cytotoxic effects. This study revives the use of DODAP in gene delivery and highlights the importance of using appropriate lipid combinations for delivering genes to specific cells.
Keywords	B-lymphocytes ; antibodies ; antineoplastic activity ; complement ; cytokines ; cytotoxicity ; encapsulation ; gene expression ; genes ; lipids ; nanoparticles ; plasmids ; receptors ; spleen ; therapeutics ; transfection
Language	English
Dates of publication	2021-0210
Size	p. 753-764.
Publishing place	Elsevier B.V.
Document type	Article
ZDB-ID	632533-6
ISSN	1873-4995 ; 0168-3659
ISSN (online)	1873-4995
ISSN	0168-3659
DOI	10.1016/j.jconrel.2021.01.005
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Article: A novel dual-targeted rosiglitazone-loaded nanoparticle for the prevention of diet-induced obesity via the browning of white adipose tissue

Hiradate, Ryu / Khalil, Ikramy A / Matsuda, Aya / Sasaki, Mika / Hida, Kyoko / Harashima, Hideyoshi

Journal of controlled release. 2021 Jan. 10, v. 329

2021

Abstract: Adipose tissue in the body is classified as white adipose tissue (WAT); a fat-accumulating tissue, or brown adipose tissue (BAT); an energy-dissipating tissue. Transforming WAT-to-BAT (browning) is a promising strategy for the treatment of obesity, since ...

Abstract	Adipose tissue in the body is classified as white adipose tissue (WAT); a fat-accumulating tissue, or brown adipose tissue (BAT); an energy-dissipating tissue. Transforming WAT-to-BAT (browning) is a promising strategy for the treatment of obesity, since it would lead to an increase in energy expenditure. Rosiglitazone (Rosi), an agonist of the peroxisome proliferator-activated receptor γ (PPARγ), is known to be a potent browning inducer in subcutaneous WAT. However, the effectiveness of Rosi has been quite limited because of several off-target effects. The objective of this study was to develop locally administered Rosi-loaded nanoparticles (Rs-NPs) with the ability to target adipocytes to achieve the adipose tissue-specific activation of PPARγ, thus causing the browning of WAT. We prepared dual targeted Rs-NPs that were modified with a specific peptide that targets prohibitin that are expressed in adipocytes, and a cell penetrating peptide for enhancing cellular uptake and controlling intracellular trafficking. The Rs-NPs modified with a single ligand were internalized into mature adipocytes and induced browning activity in vitro but they failed to significantly affect the body weight of the diet-induced obese mice model. The dual-targeted Rs-NPs induced a strong browning activity, both in vitro and in vivo, and successfully inhibited the progression of obesity, as evidenced by the shrinkage of hypertrophied adipocytes without any detectable systemic adverse effects. Meanwhile, free Rosi aggravated hepatic steatosis and did not cause adipose tissue browning nor the inhibition of body weight gain. We conclude that the increased energy expenditure via adipose tissue browning using dual-targeted Rs-NP is a promising strategy for the treatment of obesity and its related metabolic syndrome.
Keywords	adipocytes ; adverse effects ; agonists ; animal disease models ; body weight changes ; brown adipose tissue ; energy expenditure ; fatty liver ; ligands ; metabolic syndrome ; mice ; nanoparticles ; obesity ; peptides ; peroxisome proliferator-activated receptor gamma ; physiological transport ; shrinkage ; white adipose tissue
Language	English
Dates of publication	2021-0110
Size	p. 665-675.
Publishing place	Elsevier B.V.
Document type	Article
ZDB-ID	632533-6
ISSN	1873-4995 ; 0168-3659
ISSN (online)	1873-4995
ISSN	0168-3659
DOI	10.1016/j.jconrel.2020.10.002
Database	NAL-Catalogue (AGRICOLA)

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