The DOI matches its Crossref record; 28 of the 28 references it cites were found in a registry or an index.
Induction of virus‐specific cytotoxic T lymphocytes in vivo by liposome‐entrapped mRNA
Abstract
The induction of anti-influenza cytotoxic T lymphocytes (CTL) in vivo by immunizing mice with liposomes containing messenger RNA (mRNA) encoding the influenza virus nucleoprotein (NP) is described. NP mRNA, obtained by in vitro transcription, was encapsulated into simple cholesterol/phosphatidylcholine/phosphatidylserine liposomes by the detergent removal technique. The dependence of the route of mRNA-liposomes delivery on CTL induction was studied. The CTL induced were identical to those obtained in vivo with infectious virus in terms of specificity, lysing both peptide-sensitized and virus-infected targets. Furthermore, with the same mRNA-liposome preparation, virus-specific CTL responses could be also elicited in mice of three different haplotypes each of them known to present a distinct NP peptide in an MHC-restricted fashion. The relevance of these results in the context of vaccine development is discussed.
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In the citing paper
“Hence, mRNA vaccines have been formulated with synthetic delivery vehicles such as liposomes (16) and cationic polymers (17) to increase potency.”
From Nonviral delivery of self-amplifying RNA vaccines (2012) · cites this paper as [16]
In the citing paper
“It was not until 1993 that mRNA was used as a vaccine for the first time to elicit a specific immune response against the encoded pathogenic antigen in a preclinical setting using lipid-based delivery.22”
From COVID-19 mRNA vaccines: Platforms and current developments (2022) · cites this paper as [22]
In the citing paper
“The first mRNA vaccine was made of liposomes and mRNA encoding an influenza virus nucleoprotein184.”
From Lipid nanoparticles for mRNA delivery (2021) · cites this paper as [184]
In the citing paper
“This vaccine, designed in 1993, was able to induce virus-specific cytotoxic T cell responses in mice184.”
From Lipid nanoparticles for mRNA delivery (2021) · cites this paper as [184]
In the citing paper
“Lipid nanoparticle–mRNA vaccines are also being investigated as influenza vaccines29,41,156,157,159,184,189–191, with some formulations in clinical trials (Table 1).”
From Lipid nanoparticles for mRNA delivery (2021) · cites this paper as [184]
In the citing paper
“As pioneers, Martinon et al. showed that liposomes containing mRNA encoding the influenza virus nucleoprotein elicited virus-specific cytotoxic T lymphocytes (CTLs) [3].”
From Three decades of messenger RNA vaccine development (2019) · cites this paper as [3]
In the citing paper
“encapsulation of RNA in lipid carriers 72 , and their utility in vaccination 73 , was demonstrated.”
From Nanotechnology approaches for global infectious diseases (2021) · cites this paper as [73]
Citations
Cites
Direct Gene Transfer into Mouse Muscle in Vivo
Wolff, J. A., Malone, R. W., Williams, P., Chong, W., Acsadi, G., Jani, A., & Felgner, P. L. (1990) · Science · doi:10.1126/science.1690918 · Cited by 4,173
Cationic liposome-mediated RNA transfection.
Malone, R. W., Felgner, P. L., & Verma, I. M. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.16.6077 · Cited by 911
In vivo priming of virus-specific cytotoxic T lymphocytes with synthetic lipopeptide vaccine
Deres, K., Schild, H., Wiesmüller, K., Jung, G., & Rammensee, H. (1989) · Nature · doi:10.1038/342561a0 · Cited by 632
Morrison, L. A., Lukacher, A. E., Braciale, V. L., Fan, D. P., & Braciale, T. J. (1986) · The Journal of Experimental Medicine · doi:10.1084/jem.163.4.903 · Cited by 507
Induction of CD8+ cytotoxic T cells by immunization with purified HIV-1 envelope protein in ISCOMs
Takahashi, H., Takeshfta, T., Morein, B., Putney, S. D., Germain, R. N., & Berzofsky, J. A. (1990) · Nature · doi:10.1038/344873a0 · Cited by 473
A molecular model of MHC class-I-restricted antigen processing
Monaco, J. J. (1992) · Immunology Today · doi:10.1016/0167-5699(92)90122-n · Cited by 433
Kast, W. M., Roux, L., Curren, J., Blom, H., Voordouw, A. C., Meloen, R. H., Kolakofsky, D., & Melief, C. J. M. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.6.2283 · Cited by 326
Peptide-induced antiviral protection by cytotoxic T cells.
Schulz, M., Zinkernagel, R. M., & Hengartner, H. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.3.991 · Cited by 239
Antiviral cytotoxic T cell response induced by in vivo priming with a free synthetic peptide.
Aichele, P., Hengartner, H., Zinkernagel, R. M., & Schulz, M. (1990) · The Journal of Experimental Medicine · doi:10.1084/jem.171.5.1815 · Cited by 198
Townsend, A., & Skehel, J. J. (1984) · The Journal of Experimental Medicine · doi:10.1084/jem.160.2.552 · Cited by 182
MHC interaction and T cell recognition of carbohydrates and glycopeptides
Ishioka, G. Y., Lamont, A. G., Thomson, D., Bulbow, N., Gaeta, F. C., Sette, A., & Grey, H. M. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.148.8.2446 · Cited by 168
OSTRO, M. J., GIACOMONI, D., LAVELLE, D., PAXTON, W., & DRAY, S. (1978) · Nature · doi:10.1038/274921a0 · Cited by 154
Bastin, J., Rothbard, J. B., Davey, J. F., Jones, I. M., & Townsend, A. (1987) · The Journal of Experimental Medicine · doi:10.1084/jem.165.6.1508 · Cited by 154
Macrophages as accessory cells for class I MHC-restricted immune responses
Debrick, J. E., Campbell, P., & Staerz, U. D. (1991) · The Journal of Immunology · doi:10.4049/jimmunol.147.9.2846 · Cited by 148
Efficiency of peptides and lipopeptides for in vivo priming of virus‐specific cytotoxic T cells
Schild, H., Deres, K., Wiesmüller, K., Jung, G., & Rammensee, H. (1991) · European Journal of Immunology · doi:10.1002/eji.1830211102 · Cited by 140
In vivo cytotoxic T lymphocyte induction with soluble proteins administered in liposomes
Reddy, R., Zhou, F., Nair, S. K., Huang, L., & Rouse, B. T. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.148.5.1585 · Cited by 129
Martinon, F., Gras‐Masse, H., Boutillon, C., Chirat, F., Deprez, B. P., Guillet, J., GOMARD, E., Tartar, A. L., & Lévy, J. P. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.149.10.3416 · Cited by 104
Heeg, K. M., Kuon, W., & Wagner, H. (1991) · European Journal of Immunology · doi:10.1002/eji.1830210628 · Cited by 94
Priming of influenza virus-specific cytotoxic T lymphocytes vivo by short synthetic peptides
Gao, X. M., Zheng, B. Q., Liew, F. Y., Brett, S. J., & Tite, J. P. (1991) · The Journal of Immunology · doi:10.4049/jimmunol.147.10.3268 · Cited by 87
Hart, M. K., Weinhold, K. J., Scearce, R. M., Washburn, E., Clark, C. A., Palker, T. J., & Haynes, B. F. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.21.9448 · Cited by 85
Robertson, M. N., Spangrude, G. J., Hasenkrug, K. J., Perry, L., Nishio, J., Wehrly, K., & Chesebro, B. W. (1992) · Journal of Virology · doi:10.1128/jvi.66.6.3271-3277.1992 · Cited by 83
Philippot, J. R., Mutaftschiev, S., & Liautard, J. (1983) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(83)90111-6 · Cited by 80
Schild, H., Norda, M., Deres, K., Falk, K., Rötzschke, O., Wiesmüller, K., Jung, G., & Rammensee, H. (1991) · The Journal of Experimental Medicine · doi:10.1084/jem.174.6.1665 · Cited by 71
Noguchi, Y., Noguchi, T., Sato, T., Yokoo, Y., Itoh, S., Yoshida, M., Yoshiki, T., Akiyoshi, K., Sunamoto, J., & Nakayama, E. (1991) · The Journal of Immunology · doi:10.4049/jimmunol.146.10.3599 · Cited by 49
The macrophage as the principal antigen-presenting cell for liposome-encapsulated antigen
Szoka, F. C. (1992) · Research in Immunology · doi:10.1016/s0923-2494(92)80162-e · Cited by 29
Martinon, F., GOMARD, E., HANNOUN, C., & Lévy, J. P. (1990) · European Journal of Immunology · doi:10.1002/eji.1830201004 · Cited by 19
Recruitment of alloreactive cytotoxic T lymphocytes by an antigenic peptide
Staerz, U. D., Zepp, F., Schmid, R., Hill, M., & Rothbard, J. B. (1989) · European Journal of Immunology · doi:10.1002/eji.1830191203 · Cited by 16
Two epitopes and one agretope map to a single HLA-A2 peptide recognized by H-2-restricted T cells.
Martinon, F., Cornille, F., GOMARD, E., Fournié‐Zaluski, M., Abastado, J., Roques, B. P., & Lévy, J. P. (1989) · The Journal of Immunology · doi:10.4049/jimmunol.142.10.3489 · Cited by 8
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Boczkowski, D., Nair, S. K., Snyder, D., & Gilboa, E. (1996) · The Journal of experimental medicine · doi:10.1084/jem.184.2.465 · Cited by 915
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Metadata
- Authors
- Martinon, F., Krishnan, S., Lenzen, G., Magné, R., Gomard, E., Guillet, J., Lévy, J., & Meulien, P.
- Affiliations
- Inserm (FR)
- Institut Cochin (FR)
- Corresponding author
- Meulien, Pierre
- ORCID
- Martinon, Frédéric
- Venue
- European Journal of Immunology
- Publisher
- Wiley
- Published
- 1993-07
- Volume
- 23
- Issue
- 7
- Pages
- 1719-1722
- ISSN
- 0014-2980 (ISSN-L)
- 1521-4141
- OpenAlex
- W2083958143
- Cited by
- 473
- References
- 28
- Citations by year
- 2026: 18 · 2025: 42 · 2024: 51 · 2023: 59 · 2022: 58 · 2021: 64 · 2020: 18 · 2019: 10 · 2018: 12 · 2017: 8 · 2016: 12 · 2015: 13 · 2014: 12 · 2013: 9 · 2012: 10
- FWCI
- 2.87
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
- Keywords
- cytotoxic T lymphocytes, influenza virus, nucleocapsid protein, mRNA vaccines, MHC restriction, peptide presentation, vaccine development, in vitro transcription
- MeSH terms
- Animals, Antigens, Viral, Cytotoxicity, Immunologic, Immunity, Cellular, Liposomes, Mice, Inbred Strains, Nucleoproteins, Influenza A virus, RNA, Messenger, T-Lymphocytes, Cytotoxic, Vaccines, Synthetic, Viral Core Proteins, Viral Vaccines, Nucleocapsid Proteins, Mice
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