In vitro transfection of bone marrow-derived dendritic cells with TATp-liposomes

International Journal of Nanomedicine

Volumn 9, Issue 1, 2014, Pages 963-973

  Pappalardo, Juan Sebastián ^a,b,c   Langellotti, Cecilia A ^b   Di Giacomo, Sebastián ^a   Olivera, Valeria ^a   Quattrocchi, Valeria ^a,b   Zamorano, Patricia I ^b   Hartner, William C ^c   Levchenko, Tatyana S ^c   Torchilin, Vladimir P ^c  

^a Anguil Experimental Station   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Bovine herpes virus 1 glycoprotein D; Dendritic cell transfection; Green fluorescent protein; Interleukin 6; Liposomes; TAT peptide

Indexed keywords

DNA; ENHANCED GREEN FLUORESCENT PROTEIN; GLYCOPROTEIN D; GREEN FLUORESCENT PROTEIN; LIPOSOME; TRANSACTIVATOR PROTEIN; BOVINE HERPESVIRUS TYPE-1 GLYCOPROTEINS; INTERLEUKIN 6; PEPTIDE FRAGMENT; TAT PEPTIDE (47-57), HUMAN IMMUNODEFICIENCY VIRUS 1; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; FEMALE; HERPES SIMPLEX VIRUS 1; IMMUNOSTIMULATION; IN VIVO GENE TRANSFER; INTERNALIZATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN SYNTHESIS; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BOVINE; CHEMISTRY; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; IMMUNOLOGY; METABOLISM; NANOMEDICINE; PROCEDURES;

ANIMALS; CATTLE; DENDRITIC CELLS; FEMALE; GREEN FLUORESCENT PROTEINS; INTERLEUKIN-6; LIPOSOMES; MICE; MICE, INBRED BALB C; NANOMEDICINE; PEPTIDE FRAGMENTS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANSFECTION; VIRAL PROTEINS;

EID: 84896830779     PISSN: 11769114     EISSN: 11782013     Source Type: Journal    
DOI: 10.2147/IJN.S53432     Document Type: Article

References (67)

1. Howard CJ, Charleston B, Stephens SA, Sopp P, Hope JC. The role of dendritic cells in shaping the immune response. Anim Health Res Rev. 2004;5(2):191-195.
2. Kapsenberg ML. Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol. 2003;3(12):984-993.
3. Lowrie DB, Whalen RG. DNA Vaccines. Methods and Protocols. Vol 29, 1 ed. Totowa, NJ, USA: Humana Press; 2000.
4. Landi A, Babiuk LA, van Drunen L.H.S. High t{stroke}ransfection efficiency, gene expression, and viability of monocyte-derived human dendritic cells after nonviral gene transfer. J Leukoc Biol. 2007;82(4):849-860.
5. Cartier A, Masucci MG. Differential regulation of MHC class-I-restricted and unrestricted cytotoxicity by the Us3 protein kinase of herpes simplex virus-1. Scand J Immunol. Dec 2004;60(6): 592-599.
6. Decman V, Freeman ML, Kinchington PR, Hendricks RL. Immune control of HSV-1 latency. Viral Immunol. 2005;18(3):466-473.
7. Deng Y, Yang D, Chen X, Chen Y. Tc1/Tc2 imbalance in the peripheral blood of patients with recurrent genital herpes. J Huazhong Univ Sci Technolog Med Sci. 2006;26(1):145-147.
8. Divito S, Cherpes TL, Hendricks RL. A triple entente: virus, neurons, and CD8+ T cells maintain HSV-1 latency. Immunol Res. 2006;36(1/3): 119-126.
9. Hoshino Y, Pesnicak L, Cohen JI, Straus SE. Rates of reactivation of latent herpes simplex virus from mouse trigeminal ganglia ex vivo correlate directly with viral load and inversely with number of infiltrating CD8+ T cells. J Virol. 2007;81(15):8157-8164.
10. Khanna KM, Lepisto AJ, Decman V, Hendricks RL. Immune control of herpes simplex virus during latency. Curr Opin Immunol. 2004;16(4): 463-469.
11. Sheridan BS, Knickelbein JE, Hendricks RL. CD8 T cells and latent herpes simplex virus type 1: keeping the peace in sensory ganglia. Expert Opin Biol Ther. 2007;7(9):1323-1331.
12. Stuart PM, Summers B, Morris JE, Morrison LA, Leib DA. CD8(+) T cells control corneal disease following ocular infection with herpes simplex virus type 1. J Gen Virol. 2004;85(Part 7):2055-2063.
13. Verjans GM, Hintzen RQ, van Dun JM, et al. Selective retention of herpes simplex virus-specific T cells in latently infected human trigeminal ganglia. Proc Natl Acad Sci U S A. 2007;104(9):3496-3501.
14. Vider-Shalit T, Fishbain V, Raffaeli S, Louzoun Y. Phase-dependent immune evasion of herpesviruses. J Virol. 2007;81(17):9536-9545.
15. Fiammenghi L, Ancarani V, Rosales T, et al. FRET microscopy autologous tumor lysate processing in mature dendritic cell vaccine therapy. J Transl Med. 2010;8:52.
16. Gholamin M, Moaven O, Farshchian M, et al. Induction of cytotoxic T lymphocytes primed with tumor RNA-loaded dendritic cells in esophageal squamous cell carcinoma: preliminary step for DC vaccine design. BMC Cancer. 2010;10:261.
17. Ma F, Zhang J, Zhang J, Zhang C. The TLR7 agonists imiquimod and gardiquimod improve DC-based immunotherapy for melanoma in mice. Cell Mol Immunol. 2010;7(5):381-388.
18. Met O, Eriksen J, Svane IM. Studies on mRNA electroporation of immature and mature dendritic cells: effects on their immunogenic potential. Mol Biotechnol. 2008;40(2):151-160.
19. Michiels A, Tuyaerts S, Bonehill A, et al. Electroporation of immature and mature dendritic cells: implications for dendritic cell-based vaccines. Gene Ther. 2005;12(9):772-782.
20. Tan PH, Beutelspacher SC, Wang YH, et al. Immunolipoplexes: an efficient, nonviral alternative for transfection of human dendritic cells with potential for clinical vaccination. Mol Ther. 2005;11(5):790-800.
21. Serafini M, Naldini L, Introna M. Molecular evidence of inefficient transduction of proliferating human B lymphocytes by VSV-pseudotyped HIV-1-derived lentivectors. Virology. 2004;325(2):413-424.
22. Gitton Y, Tibaldi L, Dupont E, Levi G, Joliot A. Efficient CPP-mediated Cre protein delivery to developing and adult CNS tissues. BMC Biotechnol. 2009;9:40.
23. Ruzza P, Calderan A, Guiotto A, Osler A, Borin G. Tat cell-penetrating peptide has the characteristics of a poly(proline) II helix in aqueous solution and in SDS micelles. J Pept Sci. 2004;10(7):423-426.
24. Levchenko TS, Rammohan R, Volodina N, Torchilin VP. Tat peptide-mediated intracellular delivery of liposomes. Methods Enzymol. 2003;372:339-349.
25. Torchilin VP, Levchenko TS. TAT-liposomes: a novel intracellular drug carrier. Curr Protein Pept Sci. 2003;4(2):133-140.
26. Torchilin VP, Levchenko TS, Rammohan R, Volodina N, Papahadjopoulos-Sternberg B, D'Souza GG. Cell transfection in vitro and in vivo with nontoxic TAT peptide-liposome-DNA complexes. Proc Natl Acad Sci U S A. 2003;100(4):1972-1977.
27. Pappalardo JS, Quattrocchi V, Langellotti C, et al. Improved t{stroke}ransfection of spleen-derived antigen-presenting cells in culture using T{stroke}ATp-liposomes. J Control Release. 2009;134(1):41-46.
28. Zamorano P, Taboga O, Dominguez M, et al. BHV-1 DNA vaccination: effect of the adjuvant RN-205 on the modulation of the immune response in mice. Vaccine. 2002;20(21/22):2656-2664.
29. van Drunen L.H.S, van den Hurk JV, Gilchrist JE, Misra V, Babiuk LA. Interactions of monoclonal antibodies and bovine herpesvirus type 1 (BHV-1) glycoproteins: characterization of their biochemical and immunological properties. Virology. 1984;135(2):466-479.
30. Misra V, Gilchrist JE, Weinmaster G, Qualtiere L, Van den Hurk S, Babiuk LA. Herpesvirus-induced "early" glycoprotein: characterization and possible role in immune cytolysis. J Virol. 1982;43(3):1046-1054.
31. Inaba K, Inaba M, Romani N, et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med. 1992;176(6):1693-1702.
32. Torchilin VP, Levchenko TS, Lukyanov AN, et al. p-Nitrophenylcarbonyl-PEG-PE-liposomes: fast and simple attachment of specific ligands, including monoclonal antibodies, to distal ends of PEG chains via p-nitrophenylcarbonyl groups. Biochim Biophys Acta. 2001;1511(2): 397-411.
33. Buonerba C, Ferro M, Di Lorenzo G. Sipuleucel-T for prostate cancer: the immunotherapy era has commenced. Expert Rev Anticancer Ther. 2011;11(1):25-28.
34. Di Lorenzo G, Buonerba C, Kantoff PW. Immunotherapy for the treatment of prostate cancer. Nat Rev Clin Oncol. 2011;8(9):551-561.
35. Harada Y, Yonemitsu Y. Dramatic improvement of DC-based immunotherapy against various malignancies. Front Biosci (Landmark Ed). 2011;16:2233-2242.
36. Thara E, Dorff TB, Pinski JK, Quinn DI. Vaccine therapy with sipuleucel-T (Provenge) for prostate cancer. Maturitas. 2011;69(4): 296-303.
37. Turnis ME, Rooney CM. Enhancement of dendritic cells as vaccines for cancer. Immunotherapy. 2010;2(6):847-862.
38. Marty C, Meylan C, Schott H, Ballmer-Hofer K, Schwendener RA. Enhanced heparan sulfate proteoglycan-mediated uptake of cell-penetrating peptide-modified liposomes. Cell Mol Life Sci. 2004;61(14):1785-1794.
39. Torchilin VP, Rammohan R, Weissig V, Levchenko TS. TAT peptide on the surface of liposomes affords their efficient intracellular delivery even at low temperature and in the presence of metabolic inhibitors. Proc Natl Acad Sci U S A. 2001;98(15):8786-8791.
40. Tseng YL, Liu JJ, Hong RL. Translocation of liposomes into cancer cells by cell-penetrating peptides penetratin and tat: a kinetic and efficacy study. Mol Pharmacol. 2002;62(4):864-872.
41. Marshak-Rothstein A. Toll-like receptors in systemic autoimmune disease. Nat Rev Immunol. 2006;6(11):823-835.
42. Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol. 2001;1(2):135-145.
43. Sandor F, Buc M. Toll-like receptors. I. Structure, function and their ligands. Folia Biol (Praha). 2005;51(5):148-157.
44. Sandor F, Buc M. Toll-like receptors. III. Biological significance and impact for human medicine. Folia Biol (Praha). 2005;51(6): 198-203.
45. Sandor F, Buc M. Toll-like receptors. II. Distribution and pathways involved in TLR signalling. Folia Biol (Praha). 2005;51(6):188-197.
46. Yoshikawa T, Imazu S, Gao JQ, et al. Non-methylated CpG motif packaged into fusogenic liposomes enhance antigen-specific immunity in mice. Biol Pharm Bull. 2006;29(1):105-109.
47. Williams RL, Urbé S. The emerging shape of the ESCRT machinery. Nat Rev Mol Cell Biol. 2007;8(5):355-368.
48. Futaki S, Nakase I, Tadokoro A, Takeuchi T, Jones AT. Arginine-rich peptides and their internalization mechanisms. Biochem Soc Trans. 2007;35(Part 4):784-787.
49. Wadia JS, Stan RV, Dowdy SF. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med. 2004;10(3):310-315.
50. Torchilin VP. TAT peptide-modified liposomes for intracellular delivery of drugs and DNA. Cell Mol Biol Lett. 2002;7(2):265-267.
51. Torchilin VP. Tat peptide-mediated intracellular delivery of pharmaceutical nanocarriers. Adv Drug Deliv Rev. 2008;60(4/5):548-558.
52. Ruan G, Agrawal A, Marcus AI, Nie S. Imaging and tracking of tat peptide-conjugated quantum dots in living cells: new insights into nanoparticle uptake, intracellular transport, and vesicle shedding. J Am Chem Soc. 2007;129(47):14759-14766.
53. Torchilin V. Multifunctional Pharmaceutical Nanocarriers. Volume 4 of Fundamental Biomedical Technologies. New York: Springer; 2008.
54. Lundberg P, El-Andaloussi S, Sütlü T, Johansson H, Langel U. Delivery of short interfering RNA using endosomolytic cell-penetrating peptides. FASEB J. 2007;21(11):2664-2671.
55. Kishimoto T. Interleukin-6: from basic science to medicine - 40 years in immunology. Annu Rev Immunol. 2005;23:1-21.
56. Kishimoto T. IL-6: from its discovery to clinical applications. Int Immunol. 2010;22(5):347-352.
57. Baker M, Noisakran S, Gebhardt BM, Kriesel JD, Carr DJ. The relationship between interleukin-6 and herpes simplex virus type 1: implications for behavior and immunopathology. Brain Behav Immun. 1999;13(3): 201-211.
58. Geisel J, Kahl F, Müller M, et al. IL-6 and maturation govern TLR2 and TLR4 induced TLR agonist tolerance and cross-tolerance in dendritic cells. J Immunol. 2007;179(9):5811-5818.
59. Jang S, Uematsu S, Akira S, Salgame P. IL-6 and IL-10 induction from dendritic cells in response to Mycobacterium tuberculosis is predominantly dependent on TLR2-mediated recognition. J Immunol. 2004;173(5):3392-3397.
60. Loures FV, Pina A, Felonato M, Calich VL. TLR2 is a negative regulator of Th17 cells and tissue pathology in a pulmonary model of fungal infection. J Immunol. 2009;183(2):1279-1290.
61. Salio M, Cella M, Suter M, Lanzavecchia A. Inhibition of dendritic cell maturation by herpes simplex virus. Eur J Immunol. 1999;29(10): 3245-3253.
62. Sato A, Linehan MM, Iwasaki A. Dual recognition of herpes simplex viruses by TLR2 and TLR9 in dendritic cells. Proc Natl Acad Sci U S A. 2006;103(46):17343-17348.
63. Irvine AS, Trinder PK, Laughton DL, et al. Eff icient nonviral t{stroke}ransfection of dendritic cells and their use for in vivo immunization. Nat Biotechnol. 2000;18(12):1273-1278.
64. Tan PH, Beutelspacher SC, Xue SA, et al. Modulation of human dendritic-cell function following transduction with viral vectors: implications for gene therapy. Blood. 2005;105(10):3824-3832.
65. Tan PH, Yates JB, Xue SA, et al. Creation of tolerogenic human dendritic cells via intracellular CTLA4: a novel strategy with potential in clinical immunosuppression. Blood. 2005;106(9):2936-2943.
66. Jonuleit H, Tüting T, Steitz J, et al. Efficient transduction of mature CD83+ dendritic cells using recombinant adenovirus suppressed T cell stimulatory capacity. Gene Ther. 2000;7(3):249-254.
67. Parker AL, Newman C, Briggs S, Seymour L, Sheridan PJ. Nonviral gene delivery: techniques and implications for molecular medicine. Expert Rev Mol Med. 2003;5(22):1-15.