Cationic lipids activate intracellular signaling pathways

Advanced Drug Delivery Reviews

Volumn 64, Issue 15, 2012, Pages 1749-1758

  Lonez, Caroline ^a   Vandenbranden, Michel ^a   Ruysschaert, Jean Marie ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Apoptosis; Cationic lipids; CD14; Immunostimulatory; MAPK; Signaling

Indexed keywords

CATIONIC COMPOUNDS; CATIONIC LIPIDS; CATIONIC LIPOSOMES; CD14; CELL SURFACES; CELLULAR PATHWAY; GENE TRANSPORT; HIGH DENSITY; HYDROCARBON TAIL; HYDROPHILIC MOIETIES; IMMUNOSTIMULATORY; INTRACELLULAR SIGNALING PATHWAYS; MAPK; POSITIVE CHARGES; TRANSFECTION REAGENTS;

CELL DEATH; CELL MEMBRANES; HYDROCARBONS; RNA; SIGNALING;

LIPIDS;

B7 ANTIGEN; BETA INTERFERON; CALCIUM; CASPASE; CATIONIC LIPOSOME; CD86 ANTIGEN; CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERLEUKIN 12P40; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOSOME; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; APOPTOSIS; CALCIUM TRANSPORT; CELL INTERACTION; CELL MATURATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EXPERIMENTAL DESIGN; HUMAN; HYDROPHILICITY; IMMUNOSTIMULATION; INTRACELLULAR SIGNALING; LIPID PEROXIDATION; MOLECULAR DYNAMICS; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REACTOR CASCADE; REVIEW;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGENS; APOPTOSIS; CATIONS; DRUG DESIGN; HUMANS; INFLAMMATION; LIPIDS; LIPOSOMES; SIGNAL TRANSDUCTION; TRANSFECTION; VACCINES;

EID: 84869201879     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2012.05.009     Document Type: Review

References (92)

1. Martin B., Sainlos M., Aissaoui A., Oudrhiri N., Hauchecorne M., Vigneron J.P., Lehn J.M., Lehn P. The design of cationic lipids for gene delivery. Curr. Pharm. Des. 2005, 11:375-394.
2. Karmali P.P., Chaudhuri A. Cationic liposomes as non-viral carriers of gene medicines: resolved issues, open questions, and future promises. Med. Res. Rev. 2007, 27:696-722.
3. Montier T., Benvegnu T., Jaffres P.A., Yaouanc J.J., Lehn P. Progress in cationic lipid-mediated gene transfection: a series of bio-inspired lipids as an example. Curr. Gene Ther. 2008, 8:296-312.
4. Zhang S., Xu Y., Wang B., Qiao W., Liu D., Li Z. Cationic compounds used in lipoplexes and polyplexes for gene delivery. J. Control. Release 2004, 100:165-180.
5. Arima H., Aramaki Y., Tsuchiya S. Contribution of trypsin-sensitive proteins to binding of cationic liposomes to the mouse macrophage-like cell line RAW264.7. J. Pharm. Sci. 1997, 86:786-790.
6. Chenevier P., Veyret B., Roux D., Henry-Toulme N. Interaction of cationic colloids at the surface of J774 cells: a kinetic analysis. Biophys. J. 2000, 79:1298-1309.
7. Wasungu L., Hoekstra D. Cationic lipids, lipoplexes and intracellular delivery of genes. J. Control. Release 2006, 116:255-264.
8. Zhang S., Zhao B., Jiang H., Wang B., Ma B. Cationic lipids and polymers mediated vectors for delivery of siRNA. J. Control. Release 2007, 123:1-10.
9. Rao N.M. Cationic lipid-mediated nucleic acid delivery: beyond being cationic. Chem. Phys. Lipids 2010, 163:245-252.
10. Guo X., Huang L. Recent advances in nonviral vectors for gene delivery. Acc. Chem. Res. 2011, (Epub ahead of print). 10.1021/ar200151m.
11. Zelphati O., Wang Y., Kitada S., Reed J.C., Felgner P.L., Corbeil J. Intracellular delivery of proteins with a new lipid-mediated delivery system. J. Biol. Chem. 2001, 276:35103-35110.
12. Dalkara D., Chandrashekhar C., Zuber G. Intracellular protein delivery with a dimerizable amphiphile for improved complex stability and prolonged protein release in the cytoplasm of adherent cell lines. J. Control. Release 2006, 116:353-359.
13. Yamaguchi K., Inoue M., Goshima N. Efficient protein transduction method using cationic peptides and lipids. J. Biomed. Biotechnol. 2011, (Article ID 872065). 10.1155/2011/872065.
14. Christensen D., Korsholm K.S., Rosenkrands I., Lindenstrom T., Andersen P., Agger E.M. Cationic liposomes as vaccine adjuvants. Expert Rev. Vaccines 2007, 6:785-796.
15. Christensen D., Korsholm K.S., Andersen P., Agger E.M. Cationic liposomes as vaccine adjuvants. Expert Rev. Vaccines 2011, 10:513-521.
16. Elouahabi A., Ruysschaert J.M. Formation and intracellular trafficking of lipoplexes and polyplexes. Mol. Ther. 2005, 11:336-347.
17. Hoekstra D., Rejman J., Wasungu L., Shi F., Zuhorn I. Gene delivery by cationic lipids: in and out of an endosome. Biochem. Soc. Trans. 2007, 35:68-71.
18. Khalil I.A., Kogure K., Akita H., Harashima H. Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery. Pharmacol. Rev. 2006, 58:32-45.
19. Boussif O., Lezoualc'h F., Zanta M.A., Mergny M.D., Scherman D., Demeneix B., Behr J.P. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:7297-7301.
20. Xu Y., Szoka F.C. Mechanism of DNA release from cationic liposome/DNA complexes used in cell transfection. Biochemistry 1996, 35:5616-5623.
21. Zuhorn I.S., Hoekstra D. On the mechanism of cationic amphiphile-mediated transfection. To fuse or not to fuse: is that the question?. J. Membr. Biol. 2002, 189:167-179.
22. Coburn R.F. Polyamine effects on cell function: Possible central role of plasma membrane PI(4,5)P2. J. Cell. Physiol. 2009, 221:544-551.
23. von Deutsch A.W., Mitchell C.D., Williams C.E., Dutt K., Silvestrov N.A., Klement B.J., Abukhalaf I.K., von Deutsch D.A. Polyamines protect against radiation-induced oxidative stress. Gravit. Space Biol. Bull. 2005, 18:109-110.
24. Loscalzo J. L-arginine and atherothrombosis. J. Nutr. 2004, 134:2798S-2800S.
25. Verzola D., Fama A., Villaggio B., Di Rocco M., Simonato A., D'Amato E., Gianiorio F., Garibotto G. Lysine triggers apoptosis through a NADPH oxidase-dependent mechanism in human renal tubular cells. J. Inherit. Metab. Dis. 2012, (Epub ahead of print). 10.1007/s10545-012-9468-z.
26. Ray R.M., Li C., Bhattacharya S., Naren A.P., Johnson L.R. Spermine, a molecular switch regulating EGFR, integrin beta3, Src, and FAK scaffolding. Cell. Signal. 2012, 24:931-942.
27. Carmona-Ribeiro A.M., Ortis F., Schumacher R.I., Armelin M.C.S. Interactions between cationic vesicles and cultured mammalian cells. Langmuir 1997, 13:2215-2218.
28. Dymond M.K., Attard G.S. Cationic type I amphiphiles as modulators of membrane curvature elastic stress in vivo. Langmuir 2008, 24:11743-11751.
29. Lonez C., Vandenbranden M., Ruysschaert J.M. Cationic liposomal lipids: from gene carriers to cell signaling. Prog. Lipid Res. 2008, 47:340-347.
30. Lonez C., Lensink M.F., Vandenbranden M., Ruysschaert J.M. Cationic lipids activate cellular cascades. Which receptors are involved?. Biochim. Biophys. Acta 2009, 1790:425-430.
31. Aramaki Y., Takano S., Tsuchiya S. Induction of apoptosis in macrophages by cationic liposomes. FEBS Lett. 1999, 460:472-476.
32. Aramaki Y., Takano S., Arima H., Tsuchiya S. Induction of apoptosis in WEHI 231 cells by cationic liposomes. Pharm. Res. 2000, 17:515-520.
33. Aramaki Y., Takano S., Tsuchiya S. Cationic liposomes induce macrophage apoptosis through mitochondrial pathway. Arch. Biochem. Biophys. 2001, 392:245-250.
34. Takano S., Aramaki Y., Tsuchiya S. Lipoxygenase may be involved in cationic liposome-induced macrophage apoptosis. Biochem. Biophys. Res. Commun. 2001, 288:116-120.
35. Takano S., Aramaki Y., Tsuchiya S. Physicochemical properties of liposomes affecting apoptosis induced by cationic liposomes in macrophages. Pharm. Res. 2003, 20:962-968.
36. Iwaoka S., Nakamura T., Takano S., Tsuchiya S., Aramaki Y. Cationic liposomes induce apoptosis through p38 MAP kinase-caspase-8-Bid pathway in macrophage-like RAW264.7 cells. J. Leukoc. Biol. 2006, 79:184-191.
37. Arisaka M., Nakamura T., Yamada A., Negishi Y., Aramaki Y. Involvement of protein kinase Cdelta in induction of apoptosis by cationic liposomes in macrophage-like RAW264.7 cells. FEBS Lett. 2010, 584:1016-1020.
38. Arisaka M., Takano K., Negishi Y., Arima H., Aramaki Y. Involvement of lipid rafts in macrophage apoptosis induced by cationic liposomes. Arch. Biochem. Biophys. 2011, 508:72-77.
39. Takano K., Sato K., Negishi Y., Aramaki Y. Involvement of actin cytoskeleton in macrophage apoptosis induced by cationic liposomes. Arch. Biochem. Biophys. 2012, 518:89-94.
40. Kongkaneramit L., Sarisuta N., Azad N., Lu Y., Iyer A.K., Wang L., Rojanasakul Y. Dependence of reactive oxygen species and FLICE inhibitory protein on lipofectamine-induced apoptosis in human lung epithelial cells. J. Pharmacol. Exp. Ther. 2008, 325:969-977.
41. Yan W., Chen W., Huang L. Reactive oxygen species play a central role in the activity of cationic liposome based cancer vaccine. J. Control. Release 2008, 130:22-28.
42. Ouali M., Ruysschaert J.M., Lonez C., Vandenbranden M. Cationic lipids involved in gene transfer mobilize intracellular calcium. Mol. Membr. Biol. 2007, 24:225-232.
43. Adam-Vizi V., Starkov A.A. Calcium and mitochondrial reactive oxygen species generation: how to read the facts. J. Alzheimers Dis. 2010, 20(Suppl. 2):S413-S426.
44. Bogeski I., Kappl R., Kummerow C., Gulaboski R., Hoth M., Niemeyer B.A. Redox regulation of calcium ion channels: chemical and physiological aspects. Cell Calcium 2011, 50:407-423.
45. Yan W., Chen W., Huang L. Mechanism of adjuvant activity of cationic liposome: phosphorylation of a MAP kinase, ERK and induction of chemokines. Mol. Immunol. 2007, 44:3672-3681.
46. Tagami T., Hirose K., Barichello J.M., Ishida T., Kiwada H. Global gene expression profiling in cultured cells is strongly influenced by treatment with siRNA-cationic liposome complexes. Pharm. Res. 2008, 25:2497-2504.
47. Omidi Y., Kafil V., Barar J. Toxicogenomics of Nonviral Cationic Gene Delivery Nanosystems. Non-Viral Gene Therapy, InTech 2011, 547-576. X.-B. Yuan (Ed.).
48. Tanaka T., Legat A., Adam E., Steuve J., Gatot J.S., Vandenbranden M., Ulianov L., Lonez C., Ruysschaert J.M., Muraille E., Tuynder M., Goldman M., Jacquet A. DiC14-amidine cationic liposomes stimulate myeloid dendritic cells through Toll-like receptor 4. Eur. J. Immunol. 2008, 38:1351-1357.
49. Wilmar A., Lonez C., Vermeersch M., Andrianne M., Perez-Morga D., Ruysschaert J.M., Vandenbranden M., Leo O., Temmerman S.T. The cationic lipid, diC14 amidine, extends the adjuvant properties of aluminum salts through a TLR-4- and caspase-1-independent mechanism. Vaccine 2012, 30:414-424.
50. Vangasseri D.P., Cui Z., Chen W., Hokey D.A., Falo L.D., Huang L. Immunostimulation of dendritic cells by cationic liposomes. Mol. Membr. Biol. 2006, 23:385-395.
51. Kusumoto K., Ishikawa T. Didodecyldimethylammonium bromide (DDAB) induces caspase-mediated apoptosis in human leukemia HL-60 cells. J. Control. Release 2010, 147:246-252.
52. Ostuni R., Zanoni I., Granucci F. Deciphering the complexity of Toll-like receptor signaling. Cell Mol. Life Sci. 2010, 67:4109-4134.
53. Mata-Haro V., Cekic C., Martin M., Chilton P.M., Casella C.R., Mitchell T.C. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 2007, 316:1628-1632.
54. Jiang Z., Georgel P., Du X., Shamel L., Sovath S., Mudd S., Huber M., Kalis C., Keck S., Galanos C., Freudenberg M., Beutler B. CD14 is required for MyD88-independent LPS signaling. Nat. Immunol. 2005, 6:565-570.
55. Regen T., van Rossum D., Scheffel J., Kastriti M.E., Revelo N.H., Prinz M., Bruck W., Hanisch U.K. CD14 and TRIF govern distinct responsiveness and responses in mouse microglial TLR4 challenges by structural variants of LPS. Brain Behav. Immun. 2011, 25:957-970.
56. Zanoni I., Ostuni R., Marek L.R., Barresi S., Barbalat R., Barton G.M., Granucci F., Kagan J.C. CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 2011, 147:868-880.
57. Kedmi R., Ben Arie N., Peer D. The systemic toxicity of positively charged lipid nanoparticles and the role of Toll-like receptor 4 in immune activation. Biomaterials 2010, 31:6867-6875.
58. O'Toole T., Peppelenbosch M.P. Phosphatidyl inositol-3-phosphate kinase mediates CD14 dependent signaling. Mol. Immunol. 2007, 44:2362-2369.
59. Zanoni I., Ostuni R., Capuano G., Collini M., Caccia M., Ronchi A.E., Rocchetti M., Mingozzi F., Foti M., Chirico G., Costa B., Zaza A., Ricciardi-Castagnoli P., Granucci F. CD14 regulates the dendritic cell life cycle after LPS exposure through NFAT activation. Nature 2009, 460:264-268.
60. Kim J.I., Lee C.J., Jin M.S., Lee C.H., Paik S.G., Lee H., Lee J.O. Crystal structure of CD14 and its implications for lipopolysaccharide signaling. J. Biol. Chem. 2005, 280:11347-11351.
61. Baumann C.L., Aspalter I.M., Sharif O., Pichlmair A., Bluml S., Grebien F., Bruckner M., Pasierbek P., Aumayr K., Planyavsky M., Bennett K.L., Colinge J., Knapp S., Superti-Furga G. CD14 is a coreceptor of Toll-like receptors 7 and 9. J. Exp. Med. 2010, 207:2689-2701.
62. Cros J., Cagnard N., Woollard K., Patey N., Zhang S.Y., Senechal B., Puel A., Biswas S.K., Moshous D., Picard C., Jais J.P., D'Cruz D., Casanova J.L., Trouillet C., Geissmann F. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 2010, 33:375-386.
63. Chun K.H., Seong S.Y. CD14 but not MD2 transmit signals from DAMP. Int. Immunopharmacol. 2010, 10:98-106.
64. Weber C., Muller C., Podszuweit A., Montino C., Vollmer J., Forsbach A. TLR3 immune modulation by unformulated siRNA or DNA and the role of CD14 (in TLR mediated effects). Immunology 2012, (Epub ahead of print). 10.1111/j.1365-2567.2012.03559.x.
65. Asai Y., Makimura Y., Kawabata A., Ogawa T. Soluble CD14 discriminates slight structural differences between lipid as that lead to distinct host cell activation. J. Immunol. 2007, 179:7674-7683.
66. Erridge C., Kennedy S., Spickett C.M., Webb D.J. Oxidized phospholipid inhibition of toll-like receptor (TLR) signaling is restricted to TLR2 and TLR4: roles for CD14, LPS-binding protein, and MD2 as targets for specificity of inhibition. J. Biol. Chem. 2008, 283:24748-24759.
67. Yu B., Hailman E., Wright S.D. Lipopolysaccharide binding protein and soluble CD14 catalyze exchange of phospholipids. J. Clin. Invest. 1997, 99:315-324.
68. Leon-Ponte M., Kirchhof M.G., Sun T., Stephens T., Singh B., Sandhu S., Madrenas J. Polycationic lipids inhibit the pro-inflammatory response to LPS. Immunol. Lett. 2005, 96:73-83.
69. David S.A., Bechtel B., Annaiah C., Mathan V.I., Balaram P. Interaction of cationic amphiphilic drugs with lipid A: implications for development of endotoxin antagonists. Biochim. Biophys. Acta 1994, 1212:167-175.
70. Piazza M., Yu L., Teghanemt A., Gioannini T., Weiss J., Peri F. Evidence of a specific interaction between new synthetic antisepsis agents and CD14. Biochemistry 2009, 48:12337-12344.
71. Piazza M., Calabrese V., Baruffa C., Gioannini T., Weiss J., Peri F. The cationic amphiphile 3,4-bis(tetradecyloxy)benzylamine inhibits LPS signaling by competing with endotoxin for CD14 binding. Biochem. Pharmacol. 2010, 80:2050-2056.
72. Peri F., Piazza M. Therapeutic targeting of innate immunity with Toll-like receptor 4 (TLR4) antagonists. Biotechnol. Adv. 2012, 30:251-260.
73. Piazza M., Rossini C., Della F.S., Pozzi C., Comelli F., Bettoni I., Fusi P., Costa B., Peri F. Glycolipids and benzylammonium lipids as novel antisepsis agents: synthesis and biological characterization. J. Med. Chem. 2009, 52:1209-1213.
74. Zuhorn I.S., Kalicharan D., Robillard G.T., Hoekstra D. Adhesion receptors mediate efficient non-viral gene delivery. Mol. Ther. 2007, 15:946-953.
75. Carmona-Ribeiro A.M. Interactions between cationic liposomes and drugs or biomolecules. An. Acad. Bras. Cienc. 2000, 72:39-43.
76. Filion M.C., Phillips N.C. Toxicity and immunomodulatory activity of liposomal vectors formulated with cationic lipids toward immune effector cells. Biochim. Biophys. Acta 1997, 1329:345-356.
77. Filion M.C., Phillips N.C. Major limitations in the use of cationic liposomes for DNA delivery. Int. J. Pharm. 1998, 162:159-170.
78. Basu A., Pal D. Two faces of protein kinase Cdelta: the contrasting roles of PKCdelta in cell survival and cell death. ScientificWorldJournal 2010, 10:2272-2284.
79. Gregory C.D., Devitt A. CD14 and apoptosis. Apoptosis 1999, 4:11-20.
80. Kaiser W.J., Offermann M.K. Apoptosis induced by the toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif. J. Immunol. 2005, 174:4942-4952.
81. Gross O., Thomas C.J., Guarda G., Tschopp J. The inflammasome: an integrated view. Immunol. Rev. 2011, 243:136-151.
82. Sorbara M.T., Girardin S.E. Mitochondrial ROS fuel the inflammasome. Cell Res. 2011, 21:558-560.
83. Maelfait J., Vercammen E., Janssens S., Schotte P., Haegman M., Magez S., Beyaert R. Stimulation of Toll-like receptor 3 and 4 induces interleukin-1beta maturation by caspase-8. J. Exp. Med. 2008, 205:1967-1973.
84. Gringhuis S.I., Kaptein T.M., Wevers B.A., Theelen B., van der Vlist M., Boekhout T., Geijtenbeek T.B. Dectin-1 is an extracellular pathogen sensor for the induction and processing of IL-1beta via a noncanonical caspase-8 inflammasome. Nat. Immunol. 2012, 13:246-254.
85. Leemans J.C., Cassel S.L., Sutterwala F.S. Sensing damage by the NLRP3 inflammasome. Immunol. Rev. 2011, 243:152-162.
86. Festjens N., Cornelis S., Lamkanfi M., Vandenabeele P. Caspase-containing complexes in the regulation of cell death and inflammation. Biol. Chem. 2006, 387:1005-1016.
87. Nguyen L.T., Atobe K., Barichello J.M., Ishida T., Kiwada H. Complex formation with plasmid DNA increases the cytotoxicity of cationic liposomes. Biol. Pharm. Bull. 2007, 30:751-757.
88. Chen W., Yan W., Huang L. A simple but effective cancer vaccine consisting of an antigen and a cationic lipid. Cancer Immunol. Immunother. 2008, 57:517-530.
89. Jacquet A., Vanderschrick J.F., Vandenbranden M., Elouahabi A., Magi M., Garcia L., Ruysschaert J.M. Vaccination with the recombinant allergen ProDer p 1 complexed with the cationic lipid DiC14-amidine prevents allergic responses to house dust mite. Mol. Ther. 2005, 11:960-968.
90. Korsholm K.S., Agger E.M., Foged C., Christensen D., Dietrich J., Andersen C.S., Geisler C., Andersen P. The adjuvant mechanism of cationic dimethyldioctadecylammonium liposomes. Immunology 2007, 121:216-226.
91. Morille M., Passirani C., Vonarbourg A., Clavreul A., Benoit J.P. Progress in developing cationic vectors for non-viral systemic gene therapy against cancer. Biomaterials 2008, 29:3477-3496.
92. Landesman-Milo D., Peer D. Altering the immune response with lipid-based nanoparticles. J. Control. Release 2011, (Epub ahead of print). 10.1016/j.jconrel.2011.12.034.