Linkage between endosomal escape of LNP-mRNA and loading into EVs for transport to other cells.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
24 09 2019
Historique:
received: 13 09 2018
accepted: 23 08 2019
entrez: 26 9 2019
pubmed: 26 9 2019
medline: 14 1 2020
Statut: epublish

Résumé

RNA-based therapeutics hold great promise for treating diseases and lipid nanoparticles (LNPs) represent the most advanced platform for RNA delivery. However, the fate of the LNP-mRNA after endosome-engulfing and escape from the autophagy-lysosomal pathway remains unclear. To investigate this, mRNA (encoding human erythropoietin) was delivered to cells using LNPs, which shows, for the first time, a link between LNP-mRNA endocytosis and its packaging into extracellular vesicles (endo-EVs: secreted after the endocytosis of LNP-mRNA). Endosomal escape of LNP-mRNA is dependent on the molar ratio between ionizable lipids and mRNA nucleotides. Our results show that fractions of ionizable lipids and mRNA (1:1 molar ratio of hEPO mRNA nucleotides:ionizable lipids) of endocytosed LNPs were detected in endo-EVs. Importantly, these EVs can protect the exogenous mRNA during in vivo delivery to produce human protein in mice, detected in plasma and organs. Compared to LNPs, endo-EVs cause lower expression of inflammatory cytokines.

Identifiants

pubmed: 31551417
doi: 10.1038/s41467-019-12275-6
pii: 10.1038/s41467-019-12275-6
pmc: PMC6760118
doi:

Substances chimiques

EPO protein, human 0
Lipids 0
RNA, Messenger 0
Erythropoietin 11096-26-7

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4333

Références

PLoS Biol. 2014 Jun 03;12(6):e1001874
pubmed: 24893313
Cell. 2017 Mar 9;168(6):1114-1125.e10
pubmed: 28222903
Nat Commun. 2018 Jun 15;9(1):2359
pubmed: 29907766
Immunity. 2013 Aug 22;39(2):211-27
pubmed: 23973220
Nat Biotechnol. 2011 Apr;29(4):325-6
pubmed: 21478846
Mol Ther. 2000 Sep;2(3):204-10
pubmed: 10985950
Hum Gene Ther Clin Dev. 2015 Dec;26(4):216-27
pubmed: 26684446
Autophagy. 2018;14(2):243-251
pubmed: 29165043
Nat Biotechnol. 2013 Jul;31(7):653-8
pubmed: 23792629
Am J Hum Genet. 2019 Apr 4;104(4):625-637
pubmed: 30879639
Mol Ther. 2018 Jun 6;26(6):1520-1528
pubmed: 29699940
Adv Sci (Weinh). 2018 Jan 30;5(4):1700611
pubmed: 29721412
Nature. 2017 Feb 23;542(7642):450-455
pubmed: 28199304
Nat Biotechnol. 2017 Mar;35(3):238-248
pubmed: 28244990
J Extracell Vesicles. 2014 Aug 04;3:
pubmed: 25143819
Nucleic Acids Res. 2012 Sep 1;40(17):e130
pubmed: 22618874
Front Physiol. 2017 Aug 02;8:545
pubmed: 28824444
Eur J Pharm Biopharm. 2011 Sep;79(1):150-61
pubmed: 21458564
Nat Biotechnol. 2015 Aug;33(8):870-6
pubmed: 26192320
Curr Opin Cell Biol. 2004 Aug;16(4):415-21
pubmed: 15261674
Nucleic Acid Ther. 2018 Jun;28(3):146-157
pubmed: 29683383
J Extracell Vesicles. 2017 Mar 7;6(1):1286095
pubmed: 28326170
Nanotechnol Sci Appl. 2012 Sep 07;5:87-100
pubmed: 24198499
Nanoscale. 2018 Jan 18;10(3):881-906
pubmed: 29265147
Science. 2018 Jan 12;359(6372):
pubmed: 29326244
Angew Chem Int Ed Engl. 2012 Aug 20;51(34):8529-33
pubmed: 22782619
Cell Rep. 2017 Dec 19;21(12):3548-3558
pubmed: 29262333
Semin Cell Dev Biol. 2017 Jul;67:48-55
pubmed: 28104520
Nat Biotechnol. 2011 Apr;29(4):341-5
pubmed: 21423189
Nat Biotechnol. 2013 Jul;31(7):638-46
pubmed: 23792630
Cell Commun Signal. 2012 Nov 28;10(1):37
pubmed: 23190502
Nature. 2017 Jun 22;546(7659):498-503
pubmed: 28607485
Curr Protoc Cell Biol. 2006 Apr;Chapter 3:Unit 3.22
pubmed: 18228490
Mol Ther. 2018 Jun 6;26(6):1509-1519
pubmed: 29653760
Nature. 2015 Nov 19;527(7578):329-35
pubmed: 26524530
Annu Rev Immunol. 2012;30:611-46
pubmed: 22449030
Vet Pathol. 2018 Mar;55(2):341-354
pubmed: 29191134
Nat Commun. 2015 May 13;6:7029
pubmed: 25967391
Nat Biotechnol. 2013 Jul;31(7):611-2
pubmed: 23839146
Nat Rev Mol Cell Biol. 2018 Apr;19(4):213-228
pubmed: 29339798
Biochem J. 2012 Feb 1;441(3):813-21
pubmed: 22026563
Nat Biotechnol. 2010 Feb;28(2):172-6
pubmed: 20081866
Nat Cell Biol. 2007 Jun;9(6):654-9
pubmed: 17486113
Proc Natl Acad Sci U S A. 2014 Oct 14;111(41):14888-93
pubmed: 25267620
Proc Natl Acad Sci U S A. 2018 Apr 10;115(15):E3351-E3360
pubmed: 29588418
Nat Rev Drug Discov. 2018 Apr;17(4):261-279
pubmed: 29326426
Autophagy. 2007 May-Jun;3(3):278-81
pubmed: 17351332
ACS Nano. 2017 Aug 22;11(8):7572-7586
pubmed: 28727419
J Drug Target. 2016 Nov;24(9):780-786
pubmed: 27030014
Nat Commun. 2017 Oct 26;8(1):1145
pubmed: 29074968
Mol Ther. 2017 Jun 7;25(6):1316-1327
pubmed: 28457665
J Extracell Vesicles. 2018 Nov 23;7(1):1535750
pubmed: 30637094
Cell Commun Signal. 2013 Nov 18;11:88
pubmed: 24245560
Nat Mater. 2013 Nov;12(11):967-77
pubmed: 24150415
Nano Lett. 2017 Sep 13;17(9):5711-5718
pubmed: 28836442
Sci Rep. 2016 Feb 17;6:20019
pubmed: 26883577
Mol Ther. 2019 Jul 3;27(7):1242-1251
pubmed: 31056400
Nano Lett. 2018 Jun 13;18(6):3814-3822
pubmed: 29694050
Mol Ther. 2013 Jan;21(1):185-91
pubmed: 23032975
Nat Rev Urol. 2014 Dec;11(12):688-701
pubmed: 25403245
Silence. 2010 Jul 08;1(1):14
pubmed: 20615220

Auteurs

Marco Maugeri (M)

Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, 413 46, Gothenburg, Sweden.

Muhammad Nawaz (M)

Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, 413 46, Gothenburg, Sweden.

Alexandros Papadimitriou (A)

Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, 413 46, Gothenburg, Sweden.

Annelie Angerfors (A)

Advanced Drug Delivery, Pharmaceutical Sciences, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, 431 83, Mölndal, Sweden.

Alessandro Camponeschi (A)

Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, 413 46, Gothenburg, Sweden.

Manli Na (M)

Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, 413 46, Gothenburg, Sweden.

Mikko Hölttä (M)

Translational Biomarkers and Bioanalysis, Clinical Pharmacology & Safety Sciences, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, 431 83, Mölndal, Sweden.

Pia Skantze (P)

Advanced Drug Delivery, Pharmaceutical Sciences, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, 431 83, Mölndal, Sweden.

Svante Johansson (S)

Advanced Drug Delivery, Pharmaceutical Sciences, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, 431 83, Mölndal, Sweden.

Martina Sundqvist (M)

Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, 413 46, Gothenburg, Sweden.

Johnny Lindquist (J)

Translational Biomarkers and Bioanalysis, Clinical Pharmacology & Safety Sciences, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, 431 83, Mölndal, Sweden.

Tomas Kjellman (T)

Advanced Drug Delivery, Pharmaceutical Sciences, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, 431 83, Mölndal, Sweden.

Inga-Lill Mårtensson (IL)

Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, 413 46, Gothenburg, Sweden.

Tao Jin (T)

Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, 413 46, Gothenburg, Sweden.

Per Sunnerhagen (P)

Department of Chemistry and Molecular Biology, University of Gothenburg, Box 462, 405 30, Gothenburg, Sweden.

Sofia Östman (S)

Animal Sciences and Technologies, Clinical Pharmacology & Safety Sciences, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, 431 83, Mölndal, Sweden.

Lennart Lindfors (L)

Advanced Drug Delivery, Pharmaceutical Sciences, BioPharmaceuticals R&D, AstraZeneca, Gothenburg, 431 83, Mölndal, Sweden.

Hadi Valadi (H)

Department of Rheumatology and Inflammation Research, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, 413 46, Gothenburg, Sweden. hadi.valadi@gu.se.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH