CD8 T-cell priming upon mRNA vaccination is restricted to bone-marrow-derived antigen-presenting cells and may involve antigen transfer from myocytes

Immunology

Volumn 146, Issue 2, 2015, Pages 312-326

  Lazzaro, Sandra ^a,c   Giovani, Cinzia ^a   Mangiavacchi, Simona ^a   Magini, Diletta ^a   Maione, Domenico ^a   Baudner, Barbara ^a   Geall, Andrew J ^b,d   De Gregorio, Ennio ^a   D'Oro, Ugo ^a   Buonsanti, Cecilia ^a  

^a NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^b GLAXOSMITHKLINE   (United States)

^c CureVac GmbH   (Germany)

^d Avidity NanoMedicines   (United States)

Author keywords

Antigen presenting cells; Cross presentation; Muscle cells; Nucleic acid based vaccines; Self amplifying mRNA

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; NUCLEOPROTEIN; RNA VACCINE; SELF AMPLIFYING MESSENGER RNA VACCINE; UNCLASSIFIED DRUG; CORE PROTEIN; HLA ANTIGEN CLASS 1; INFLUENZA VACCINE; NP PROTEIN, INFLUENZA A VIRUS; RNA BINDING PROTEIN; VIRUS RNA;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ARTICLE; BONE MARROW DERIVED ANTIGEN PRESENTING CELL; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CROSS PRESENTATION; FEMALE; IN VITRO GENE TRANSFER; IN VITRO STUDY; IN VIVO GENE TRANSFER; IN VIVO STUDY; MOUSE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; REPLICON; ANIMAL; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; C3H MOUSE; C57BL MOUSE; CELL COMMUNICATION; CELL LINE; GENETIC TRANSFECTION; GENETICS; HAMSTER; HISTOCOMPATIBILITY; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); SKELETAL MUSCLE CELL; TRANSGENIC MOUSE; VIROLOGY;

ANIMALS; ANTIGEN-PRESENTING CELLS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CD8-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; CELL LINE; CRICETINAE; CROSS-PRIMING; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE FIBERS, SKELETAL; RNA, MESSENGER; RNA, VIRAL; RNA-BINDING PROTEINS; TRANSFECTION; TRANSPLANTATION CHIMERA; VIRAL CORE PROTEINS;

EID: 84941746198     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12505     Document Type: Article

References (56)

1. Deering RP, Kommareddy S, Ulmer JB, Brito LA, Geall AJ. Nucleic acid vaccines: prospects for non-viral delivery of mRNA vaccines. Expert Opin Drug Deliv 2014; 11:885-99.
2. Delany I, Rappuoli R, De Gregorio E. Vaccines for the 21st century. EMBO Mol Med 2014; 6:708-20.
3. Koup RA, Douek DC. Vaccine design for CD8 T lymphocyte responses. Cold Spring Harb Perspect Med 2011; 1:a007252.
4. Ferraro B, Morrow MP, Hutnick NA, Shin TH, Lucke CE, Weiner DB. Clinical applications of DNA vaccines: current progress. Clin Infect Dis 2011; 53:296-302.
5. Liu MA. DNA vaccines: an historical perspective and view to the future. Immunol Rev 2011; 239:62-84.
6. Liu MA. Immunologic basis of vaccine vectors. Immunity 2010; 33:504-15.
7. Kutzler MA, Weiner DB. DNA vaccines: ready for prime time? Nat Rev Genet 2008; 9:776-88.
8. Ulmer JB, Donnelly JJ, Parker SE, Rhodes GH, Felgner PL, Dwarki VJ et al. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science 1993; 259:1745-9.
9. Davis BS, Chang GJ, Cropp B, Roehrig JT, Martin DA, Mitchell CJ et al. West Nile virus recombinant DNA vaccine protects mouse and horse from virus challenge and expresses in vitro a noninfectious recombinant antigen that can be used in enzyme-linked immunosorbent assays. J Virol 2001; 75:4040-7.
10. Garver KA, LaPatra SE, Kurath G. Efficacy of an infectious hematopoietic necrosis (IHN) virus DNA vaccine in Chinook Oncorhynchus tshawytscha and sockeye O. nerka salmon. Dis Aquat Organ 2005; 64:13-22.
11. Prinz DM, Smithson SL, Kieber-Emmons T, Westerink MA. Induction of a protective capsular polysaccharide antibody response to a multiepitope DNA vaccine encoding a peptide mimic of meningococcal serogroup C capsular polysaccharide. Immunology 2003; 110:242-9.
12. Bagarazzi ML, Yan J, Morrow MP, Shen X, Parker RL, Lee JC et al. Immunotherapy against HPV16/18 generates potent TH1 and cytotoxic cellular immune responses. Sci Transl Med 2012; 4:155ra38.
13. Van Lint S, Renmans D, Broos K, Dewitte H, Lentacker I, Heirman C et al. The ReNAissanCe of mRNA-based cancer therapy. Expert Rev Vaccines 2015; 14:235-51.
14. Pascolo S. Messenger RNA-based vaccines. Expert Opin Biol Ther 2004; 4:1285-94.
15. Ulmer JB, Mason PW, Geall A, Mandl CW. RNA-based vaccines. Vaccine 2012; 30:4414-8.
16. Geall AJ, Mandl CW, Ulmer JB. RNA: the new revolution in nucleic acid vaccines. Semin Immunol 2013; 25:152-9.
17. Luo D, Saltzman WM. Synthetic DNA delivery systems. Nat Biotechnol 2000; 18:33-7.
18. Mandl CW, Aberle JH, Aberle SW, Holzmann H, Allison SL, Heinz FX. In vitro-synthesized infectious RNA as an attenuated live vaccine in a flavivirus model. Nat Med 1998; 4:1438-40.
19. Petsch B, Schnee M, Vogel AB, Lange E, Hoffmann B, Voss D et al. Protective efficacy of in vitro synthesized, specific mRNA vaccines against influenza A virus infection. Nat Biotechnol 2012; 30:1210-6.
20. Martinon F, Krishnan S, Lenzen G, Magne R, Gomard E, Guillet JG et al. Induction of virus-specific cytotoxic T lymphocytes in vivo by liposome-entrapped mRNA. Eur J Immunol 1993; 23:1719-22.
21. Hoerr I, Obst R, Rammensee HG, Jung G. In vivo application of RNA leads to induction of specific cytotoxic T lymphocytes and antibodies. Eur J Immunol 2000; 30:1-7.
22. Kofler RM, Aberle JH, Aberle SW, Allison SL, Heinz FX, Mandl CW. Mimicking live flavivirus immunization with a noninfectious RNA vaccine. Proc Natl Acad Sci USA 2004; 101:1951-6.
23. Kreiter S, Selmi A, Diken M, Koslowski M, Britten CM, Huber C et al. Intranodal vaccination with naked antigen-encoding RNA elicits potent prophylactic and therapeutic antitumoral immunity. Cancer Res 2010; 70:9031-40.
24. Fotin-Mleczek M, Duchardt KM, Lorenz C, Pfeiffer R, Ojkic-Zrna S, Probst J et al. Messenger RNA-based vaccines with dual activity induce balanced TLR-7 dependent adaptive immune responses and provide antitumor activity. J Immunother 2011; 34:1-15.
25. Sebastian M, Papachristofilou A, Weiss C, Fruh M, Cathomas R, Hilbe W et al. Phase Ib study evaluating a self-adjuvanted mRNA cancer vaccine (RNActive®) combined with local radiation as consolidation and maintenance treatment for patients with stage IV non-small cell lung cancer. BMC Cancer 2014; 14:748.
26. Bonehill A, Van Nuffel AM, Corthals J, Tuyaerts S, Heirman C, Francois V et al. Single-step antigen loading and activation of dendritic cells by mRNA electroporation for the purpose of therapeutic vaccination in melanoma patients. Clin Cancer Res 2009; 15:3366-75.
27. Van Lint S, Goyvaerts C, Maenhout S, Goethals L, Disy A, Benteyn D et al. Preclinical evaluation of TriMix and antigen mRNA-based antitumor therapy. Cancer Res 2012; 72:1661-71.
28. Van Lint S, Wilgenhof S, Heirman C, Corthals J, Breckpot K, Bonehill A et al. Optimized dendritic cell-based immunotherapy for melanoma: the TriMix-formula. Cancer Immunol Immunother 2014; 63:959-67.
29. Geall AJ, Verma A, Otten GR, Shaw CA, Hekele A, Banerjee K et al. Nonviral delivery of self-amplifying RNA vaccines. Proc Natl Acad Sci USA 2012; 109:14604-9.
30. Hekele A, Bertholet S, Archer J, Gibson DG, Palladino G, Brito LA et al. Rapidly produced SAM® vaccine against H7N9 influenza is immunogenic in mice. Emerg Microbes Infect 2013; 2:e52.
31. Ulmer JB, Mansoura MK, Geall AJ. Vaccines 'on demand': science fiction or a future reality. Expert Opin Drug Discov 2015; 10:101-6.
32. Semple SC, Akinc A, Chen J, Sandhu AP, Mui BL, Cho CK et al. Rational design of cationic lipids for siRNA delivery. Nat Biotechnol 2010; 28:172-6.
33. Whitehead KA, Langer R, Anderson DG. Knocking down barriers: advances in siRNA delivery. Nat Rev Drug Discov 2009; 8:129-38.
34. Lundstrom K. Alphavirus-based vaccines. Viruses 2014; 6:2392-415.
35. Atkins GJ, Fleeton MN, Sheahan BJ. Therapeutic and prophylactic applications of alphavirus vectors. Expert Rev Mol Med 2008; 10:e33.
36. Perri S, Greer CE, Thudium K, Doe B, Legg H, Liu H et al. An alphavirus replicon particle chimera derived from Venezuelan equine encephalitis and sindbis viruses is a potent gene-based vaccine delivery vector. J Virol 2003; 77:10394-403.
37. Jin B, Wang RY, Qiu Q, Sugauchi F, Grandinetti T, Alter HJ et al. Induction of potent cellular immune response in mice by hepatitis C virus NS3 protein with double-stranded RNA. Immunology 2007; 122:15-27.
38. Jin B, Sun T, Yu XH, Liu CQ, Yang YX, Lu P et al. Immunomodulatory effects of dsRNA and its potential as vaccine adjuvant. J Biomed Biotechnol 2010; 2010:690438.
39. Caskey M, Lefebvre F, Filali-Mouhim A, Cameron MJ, Goulet JP, Haddad EK et al. Synthetic double-stranded RNA induces innate immune responses similar to a live viral vaccine in humans. J Exp Med 2011; 208:2357-66.
40. Bogers WM, Oostermeijer H, Mooij P, Koopman G, Verschoor EJ, Davis D et al. Potent immune responses in rhesus macaques induced by nonviral delivery of a self-amplifying RNA vaccine expressing HIV type 1 envelope with a cationic nanoemulsion. J Infect Dis 2015; 211:947-55.
41. Brito LA, Chan M, Shaw CA, Hekele A, Carsillo T, Schaefer M et al. A cationic nanoemulsion for the delivery of next-generation RNA vaccines. Mol Ther 2014; 22:2118-29.
42. Lorenz C, Fotin-Mleczek M, Roth G, Becker C, Dam TC, Verdurmen WP et al. Protein expression from exogenous mRNA: uptake by receptor-mediated endocytosis and trafficking via the lysosomal pathway. RNA Biol 2011; 8:627-36.
43. Probst J, Weide B, Scheel B, Pichler BJ, Hoerr I, Rammensee HG et al. Spontaneous cellular uptake of exogenous messenger RNA in vivo is nucleic acid-specific, saturable and ion dependent. Gene Ther 2007; 14:1175-80.
44. Diken M, Kreiter S, Selmi A, Britten CM, Huber C, Tureci O et al. Selective uptake of naked vaccine RNA by dendritic cells is driven by macropinocytosis and abrogated upon DC maturation. Gene Ther 2011; 18:702-8.
45. Kormann MS, Hasenpusch G, Aneja MK, Nica G, Flemmer AW, Herber-Jonat S et al. Expression of therapeutic proteins after delivery of chemically modified mRNA in mice. Nat Biotechnol 2011; 29:154-7.
46. Wolff JA, Malone RW, Williams P, Chong W, Acsadi G, Jani A et al. Direct gene transfer into mouse muscle in vivo. Science 1990; 247:1465-8.
47. Johanning FW, Conry RM, LoBuglio AF, Wright M, Sumerel LA, Pike MJ et al. A Sindbis virus mRNA polynucleotide vector achieves prolonged and high level heterologous gene expression in vivo. Nucleic Acids Res 1995; 23:1495-501.
48. Piggott JM, Sheahan BJ, Soden DM, O'Sullivan GC, Atkins GJ. Electroporation of RNA stimulates immunity to an encoded reporter gene in mice. Mol Med Rep 2009; 2:753-6.
49. Conry RM, LoBuglio AF, Wright M, Sumerel L, Pike MJ, Johanning F et al. Characterization of a messenger RNA polynucleotide vaccine vector. Cancer Res 1995; 55:1397-400.
50. Hochweller K, Striegler J, Hammerling GJ, Garbi N. A novel CD11c.DTR transgenic mouse for depletion of dendritic cells reveals their requirement for homeostatic proliferation of natural killer cells. Eur J Immunol 2008; 38:2776-83.
51. Heyes J, Palmer L, Bremner K, MacLachlan I. Cationic lipid saturation influences intracellular delivery of encapsulated nucleic acids. J Control Release 2005; 107:276-87.
52. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, Romani N et al. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 1999; 223:77-92.
53. Fu TM, Ulmer JB, Caulfield MJ, Deck RR, Friedman A, Wang S et al. Priming of cytotoxic T lymphocytes by DNA vaccines: requirement for professional antigen presenting cells and evidence for antigen transfer from myocytes. Mol Med 1997; 3:362-71.
54. Donnelly JJ, Liu MA, Ulmer JB. Antigen presentation and DNA vaccines. Am J Respir Crit Care Med 2000; 162:S190-3.
55. Abdulhaqq SA, Weiner DB. DNA vaccines: developing new strategies to enhance immune responses. Immunol Res 2008; 42:219-32.
56. Ishii T, Ishii M. Intravital two-photon imaging: a versatile tool for dissecting the immune system. Ann Rheum Dis 2011; 70(Suppl. 1):i113-5.