mRNA mediates passive vaccination against infectious agents, toxins, and tumors

EMBO Molecular Medicine

Volumn 9, Issue 10, 2017, Pages 1434-1447

  Thran, Moritz ^a   Mukherjee, Jean ^b   Pönisch, Marion ^a   Fiedler, Katja ^a   Thess, Andreas ^a   Mui, Barbara L ^c   Hope, Michael J ^c   Tam, Ying K ^c   Horscroft, Nigel ^a   Heidenreich, Regina ^a   Fotin Mleczek, Mariola ^a   Shoemaker, Charles B ^b   Schlake, Thomas ^a  

^a CureVac GmbH   (Germany)

^b TUFTS UNIVERSITY   (United States)

^c Acuitas Therapeutics   (Canada)

Author keywords

antibody; lipid nanoparticle; messenger RNA; mouse; passive immunization

Indexed keywords

INFLUENZA VACCINE; MESSENGER RNA; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY S057; NANOPARTICLE; RABIES VACCINE; RITUXIMAB; UNCLASSIFIED DRUG; BOTULINUM ANTISERUM; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ANTIGEN EXPRESSION; ARTICLE; BOTULISM; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENETIC TRANSFECTION; HALF LIFE TIME; MOUSE; NONHUMAN; PASSIVE IMMUNIZATION; PRIORITY JOURNAL; RABIES VIRUS; RAJI CELL LINE; VIRUS NEUTRALIZATION; ANIMAL; BAGG ALBINO MOUSE; BLOOD; DOSE RESPONSE; GENETICS; HUMAN; IMMUNOLOGY; POST EXPOSURE PROPHYLAXIS; PROCEDURES; RABIES;

ANIMALS; ANTIBODIES, VIRAL; BOTULINUM ANTITOXIN; BOTULISM; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; FEMALE; HUMANS; IMMUNIZATION, PASSIVE; MICE; MICE, INBRED BALB C; NANOPARTICLES; POST-EXPOSURE PROPHYLAXIS; RABIES; RABIES VACCINES; RABIES VIRUS; RNA, MESSENGER;

EID: 85030264484     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201707678     Document Type: Article

References (54)

1. Amanna IJ, Slifka MK (2011) Contributions of humoral and cellular immunity to vaccine-induced protection in humans. Virology 411: 206–215
2. Balazs AB, Chen J, Hong CM, Rao DS, Yang L, Baltimore D (2011) Antibody-based protection against HIV infection by vectored immunoprophylaxis. Nature 481: 81–84
3. Balmayor ER, Geiger JP, Aneja MK, Berezhanskyy T, Utzinger M, Mykhaylyk O, Rudolph C, Plank C (2016) Chemically modified RNA induces osteogenesis of stem cells and human tissue explants as well as accelerates bone healing in rats. Biomaterials 87: 131–146
4. Both L, Banyard AC, van Dolleweerd C, Wright E, Ma JK, Fooks AR (2013) Monoclonal antibodies for prophylactic and therapeutic use against viral infections. Vaccine 31: 1553–1559
5. Bugli F, Cacaci M, Martini C, Torelli R, Posteraro B, Sanguinetti M, Paroni Sterbini F (2013) Human monoclonal antibody-based therapy in the treatment of invasive candidiasis. Clin Dev Immunol 2013: 403121
6. Burton DR, Poignard P, Stanfield RL, Wilson IA (2012) Broadly neutralizing antibodies present new prospects to counter highly antigenically diverse viruses. Science 337: 183–186
7. Casadevall A, Scharff MD (1994) Serum therapy revisited: animal models of infection and development of passive antibody therapy. Antimicrob Agents Chemother 38: 1695–1702
8. Chames P, Van Regenmortel M, Weiss E, Baty D (2009) Therapeutic antibodies: successes, limitations and hopes for the future. Br J Pharmacol 157: 220–233
9. De Benedictis P, Minola A, Rota Nodari E, Aiello R, Zecchin B, Salomoni A, Foglierini M, Agatic G, Vanzetta F, Lavenir R et al (2016) Development of broad-spectrum human monoclonal antibodies for rabies post-exposure prophylaxis. EMBO Mol Med 8: 407–421
10. Deal CE, Balazs AB (2015) Engineering humoral immunity as prophylaxis or therapy. Curr Opin Immunol 35: 113–122
11. Dennis MS, Zhang M, Meng YG, Kadkhodayan M, Kirchhofer D, Combs D, Damico LA (2002) Albumin binding as a general strategy for improving the pharmacokinetics of proteins. J Biol Chem 277: 35035–35043
12. Dietzschold B, Wiktor TJ, Trojanowski JQ, Macfarlan RI, Wunner WH, Torres-Anjel MJ, Koprowski H (1985) Differences in cell-to-cell spread of pathogenic and apathogenic rabies virus in vivo and in vitro. J Virol 56: 12–18
13. Dreyfus C, Laursen NS, Kwaks T, Zuijdgeest D, Khayat R, Ekiert DC, Lee JH, Metlagel Z, Bujny MV, Jongeneelen M et al (2012) Highly conserved protective epitopes on influenza B viruses. Science 337: 1343–1348
14. Fotin-Mleczek M, Duchardt KM, Lorenz C, Pfeiffer R, Ojkic-Zrna S, Probst J, Kallen KJ (2011) Messenger RNA-based vaccines with dual activity induce balanced TLR-7 dependent adaptive immune responses and provide antitumor activity. J Immunother 34: 1–15
15. Hamers-Casterman C, Atarhouch T, Muyldermans S, Robinson G, Hamers C, Songa EB, Bendahman N, Hamers R (1993) Naturally occurring antibodies devoid of light chains. Nature 363: 446–448
16. Hammon WM, Coriell LL, Wehrle PF, Stokes J Jr (1953) Evaluation of Red Cross gamma globulin as a prophylactic agent for poliomyelitis. IV. Final report of results based on clinical diagnoses. J Am Med Assoc 151: 1272–1285
17. Hendershot L, Bole D, Kohler G, Kearney JF (1987) Assembly and secretion of heavy chains that do not associate posttranslationally with immunoglobulin heavy chain-binding protein. J Cell Biol 104: 761–767
18. Hoerr I, Obst R, Rammensee HG, Jung G (2000) In vivo application of RNA leads to induction of specific cytotoxic T lymphocytes and antibodies. Eur J Immunol 30: 1–7
19. Janeway CA (1945) Use of concentrated human serum gamma-globulin in the prevention and attenuation of measles. Bull N Y Acad Med 21: 202–222
20. Jirikowski GF, Sanna PP, Maciejewski-Lenoir D, Bloom FE (1992) Reversal of diabetes insipidus in Brattleboro rats: intrahypothalamic injection of vasopressin mRNA. Science 255: 996–998
21. Kariko K, Muramatsu H, Keller JM, Weissman D (2012) Increased erythropoiesis in mice injected with submicrogram quantities of pseudouridine-containing mRNA encoding erythropoietin. Mol Ther 20: 948–953
22. Keizer RJ, Huitema AD, Schellens JH, Beijnen JH (2010) Clinical pharmacokinetics of therapeutic monoclonal antibodies. Clin Pharmacokinet 49: 493–507
23. Kohler G, Milstein C (1975) Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256: 495–497
24. Kormann MS, Hasenpusch G, Aneja MK, Nica G, Flemmer AW, Herber-Jonat S, Huppmann M, Mays LE, Illenyi M, Schams A et al (2011) Expression of therapeutic proteins after delivery of chemically modified mRNA in mice. Nat Biotechnol 29: 154–157
25. Kranz LM, Diken M, Haas H, Kreiter S, Loquai C, Reuter KC, Meng M, Fritz D, Vascotto F, Hefesha H et al (2016) Systemic RNA delivery to dendritic cells exploits antiviral defence for cancer immunotherapy. Nature 534: 396–401
26. Kreiter S, Selmi A, Diken M, Koslowski M, Britten CM, Huber C, Tureci O, Sahin U (2010) Intranodal vaccination with naked antigen-encoding RNA elicits potent prophylactic and therapeutic antitumoral immunity. Can Res 70: 9031–9040
27. Kubler H, Scheel B, Gnad-Vogt U, Miller K, Schultze-Seemann W, Vom Dorp F, Parmiani G, Hampel C, Wedel S, Trojan L et al (2015) Self-adjuvanted mRNA vaccination in advanced prostate cancer patients: a first-in-man phase I/IIa study. J Immunother Cancer 3: 26
28. Lackman-Smith C, Osterling C, Luckenbaugh K, Mankowski M, Snyder B, Lewis G, Paull J, Profy A, Ptak RG, Buckheit RW Jr et al (2008) Development of a comprehensive human immunodeficiency virus type 1 screening algorithm for discovery and preclinical testing of topical microbicides. Antimicrob Agents Chemother 52: 1768–1781
29. Lewis AD, Chen R, Montefiori DC, Johnson PR, Clark KR (2002) Generation of neutralizing activity against human immunodeficiency virus type 1 in serum by antibody gene transfer. J Virol 76: 8769–8775
30. van der Linden RH, Frenken LG, de Geus B, Harmsen MM, Ruuls RC, Stok W, de Ron L, Wilson S, Davis P, Verrips CT (1999) Comparison of physical chemical properties of llama VHH antibody fragments and mouse monoclonal antibodies. Biochim Biophys Acta 1431: 37–46
31. Mukherjee J, Tremblay JM, Leysath CE, Ofori K, Baldwin K, Feng X, Bedenice D, Webb RP, Wright PM, Smith LA et al (2012) A novel strategy for development of recombinant antitoxin therapeutics tested in a mouse botulism model. PLoS One 7: e29941
32. Mukherjee J, Dmitriev I, Debatis M, Tremblay JM, Beamer G, Kashentseva EA, Curiel DT, Shoemaker CB (2014) Prolonged prophylactic protection from botulism with a single adenovirus treatment promoting serum expression of a VHH-based antitoxin protein. PLoS One 9: e106422
33. Nagarajan T, Marissen WE, Rupprecht CE (2014) Monoclonal antibodies for the prevention of rabies: theory and clinical practice. Antibody Technol J 4: 1–12
34. Nebija D, Kopelent-Frank H, Urban E, Noe CR, Lachmann B (2011) Comparison of two-dimensional gel electrophoresis patterns and MALDI-TOF MS analysis of therapeutic recombinant monoclonal antibodies trastuzumab and rituximab. J Pharm Biomed Anal 56: 684–691
35. Nosanchuk JD, Steenbergen JN, Shi L, Deepe GS Jr, Casadevall A (2003) Antibodies to a cell surface histone-like protein protect against Histoplasma capsulatum. J Clin Investig 112: 1164–1175
36. Pardi N, Tuyishime S, Muramatsu H, Kariko K, Mui BL, Tam YK, Madden TD, Hope MJ, Weissman D (2015) Expression kinetics of nucleoside-modified mRNA delivered in lipid nanoparticles to mice by various routes. J Control Release 217: 345–351
37. Pardi N, Secreto AJ, Shan X, Debonera F, Glover J, Yi Y, Muramatsu H, Ni H, Mui BL, Tam YK et al (2017) Administration of nucleoside-modified mRNA encoding broadly neutralizing antibody protects humanized mice from HIV-1 challenge. Nat Commun 8: 14630
38. Pediatrics AAo (1997) Clostridial infections. In Red book. Report of the committee on infectious diseases, Peter G (ed.), pp 174–178. Elk Grove Village, Ill.: American Academy of Pediatrics
39. Petsch B, Schnee M, Vogel AB, Lange E, Hoffmann B, Voss D, Schlake T, Thess A, Kallen KJ, Stitz L et al (2012) Protective efficacy of in vitro synthesized, specific mRNA vaccines against influenza A virus infection. Nat Biotechnol 30: 1210–1216
40. Plotkin SA (2010) Correlates of protection induced by vaccination. Clin Vaccine Immunol 17: 1055–1065
41. Prosniak M, Faber M, Hanlon CA, Rupprecht CE, Hooper DC, Dietzschold B (2003) Development of a cocktail of recombinant-expressed human rabies virus-neutralizing monoclonal antibodies for postexposure prophylaxis of rabies. J Infect Dis 188: 53–56
42. Ramaswamy S, Tonnu N, Tachikawa K, Limphong P, Vega JB, Karmali PP, Chivukula P, Verma IM (2017) Systemic delivery of factor IX messenger RNA for protein replacement therapy. Proc Natl Acad Sci USA 114: E1941–E1950
43. Schlake T, Thess A, Fotin-Mleczek M, Kallen KJ (2012) Developing mRNA-vaccine technologies. RNA Biol 9: 1319–1330
44. Schnee M, Vogel AB, Voss D, Petsch B, Baumhof P, Kramps T, Stitz L (2016) An mRNA vaccine encoding rabies virus glycoprotein induces protection against lethal infection in mice and correlates of protection in adult and newborn pigs. PLoS Negl Trop Dis 10: e0004746
45. Sheoran AS, Dmitriev IP, Kashentseva EA, Cohen O, Mukherjee J, Debatis M, Shearer J, Tremblay JM, Beamer G, Curiel DT et al (2015) Adenovirus vector expressing Stx1/Stx2-neutralizing agent protects piglets infected with Escherichia coli O157:H7 against fatal systemic intoxication. Infect Immun 83: 286–291
46. Skaricic D, Traube C, De B, Joh J, Boyer J, Crystal RG, Worgall S (2008) Genetic delivery of an anti-RSV antibody to protect against pulmonary infection with RSV. Virology 378: 79–85
47. Steele JH (1988) Rabies in the Americas and remarks on global aspects. Rev Infect Dis 10(Suppl 4): S585–S597
48. Teitelbaum R, Glatman-Freedman A, Chen B, Robbins JB, Unanue E, Casadevall A, Bloom BR (1998) A mAb recognizing a surface antigen of Mycobacterium tuberculosis enhances host survival. Proc Natl Acad Sci USA 95: 15688–15693
49. Thess A, Grund S, Mui BL, Hope MJ, Baumhof P, Fotin-Mleczek M, Schlake T (2015) Sequence-engineered mRNA without chemical nucleoside modifications enables an effective protein therapy in large animals. Mol Ther 23: 1456–1464
50. Tillib SV, Ivanova TI, Vasilev LA, Rutovskaya MV, Saakyan SA, Gribova IY, Tutykhina IL, Sedova ES, Lysenko AA, Shmarov MM et al (2013) Formatted single-domain antibodies can protect mice against infection with influenza virus (H5N2). Antiviral Res 97: 245–254
51. Tremblay JM, Mukherjee J, Leysath CE, Debatis M, Ofori K, Baldwin K, Boucher C, Peters R, Beamer G, Sheoran A et al (2013) A single VHH-based toxin-neutralizing agent and an effector antibody protect mice against challenge with Shiga toxins 1 and 2. Infect Immun 81: 4592–4603
52. Wolff JA, Malone RW, Williams P, Chong W, Acsadi G, Jani A, Felgner PL (1990) Direct gene transfer into mouse muscle in vivo. Science 247: 1465–1468
53. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, Seaman MS, Zhou T, Schmidt SD, Wu L, Xu L et al (2010) Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329: 856–861
54. Zangi L, Lui KO, von Gise A, Ma Q, Ebina W, Ptaszek LM, Spater D, Xu H, Tabebordbar M, Gorbatov R et al (2013) Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat Biotechnol 31: 898–907