Immune responses of therapeutic lipid nanoparticles

Nanotechnology Reviews

Volumn 2, Issue 2, 2013, Pages 201-213

  Chen, Weihsu Claire ^a   May, Jonathan P ^a   Li, Shyh Dar ^a,b  

^a ONTARIO INSTITUTE FOR CANCER RESEARCH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Immune response; Lipid nanoparticle; Nanomedicine

Indexed keywords

IMMUNE SYSTEM; MEDICAL NANOTECHNOLOGY; NANOPARTICLES; PHARMACOKINETICS; TOXICITY;

BIODISTRIBUTIONS; EMERGING TECHNOLOGIES; IMMUNE RESPONSE; LIPID NANOPARTICLES; MECHANISTIC STUDIES; PHARMACEUTICAL PRODUCTS; REDUCED TOXICITY; THERAPEUTIC EFFECTS;

DRUG DELIVERY;

EID: 84887614037     PISSN: 21919089     EISSN: 21919097     Source Type: Journal    
DOI: 10.1515/ntrev-2012-0040     Document Type: Review

References (66)

1. Dobrovolskaia MA, McNeil SE. Immunological properties of engineered nanomaterials. Nat. Nanotechnol. 2007, 2, 469-478.
2. Gabizon A, Isacson R, Rosengarten O, Tzemach D, Shmeeda H, Sapir R. An open-label study to evaluate dose and cycle dependence of the pharmacokinetics of pegylated liposomal doxorubicin. Cancer Chemother. Pharmacol. 2008, 61, 695-702.
3. Hussain S, Vanoirbeek JA, Hoet PH. Interactions of nanomaterials with the immune system. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2012, 4, 169-183.
4. Zolnik BS, Gonzalez-Fernandez A, Sadrieh N, Dobrovolskaia MA. Nanoparticles and the immune system. Endocrinology 2010, 151, 458-465.
5. Szebeni J, Alving CR, Savay S, Barenholz Y, Priev A, Danino D, Talmon Y. Formation of complement-activating particles in aqueous solutions of Taxol: possible role in hypersensitivity reactions. Int Immunopharmacol. 2001, 1, 721-735.
6. Kloover JS, den Bakker MA, Gelderblom H, van Meerbeeck JP. Fatal outcome of a hypersensitivity reaction to paclitaxel: a critical review of premedication regimens. Br. J. Cancer 2004, 90, 304-305.
7. Chanan-Khan A, Szebeni J, Savay S, Liebes L, Rafique NM, Alving CR, Muggia FM. Complement activation following first exposure to pegylated liposomal doxorubicin (Doxil): possible role in hypersensitivity reactions. Ann. Oncol. 2003, 14, 1430-1437.
8. Lonez C, Vandenbranden M, Ruysschaert JM. Cationic lipids activate intracellular signaling pathways. Adv. Drug Deliv. Rev. 2012, 64, 1749-1758.
9. Chen W, Huang L. Induction of cytotoxic T-lymphocytes and antitumor activity by a liposomal lipopeptide vaccine. Mol. Pharm. 2008, 5, 464-471.
10. 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.
11. Vangasseri DP, Cui Z, Chen W, Hokey DA, Falo LD Jr., Huang L. Immunostimulation of dendritic cells by cationic liposomes. Mol. Membr. Biol. 2006, 23, 385-395.
12. Vasievich EA, Chen W, Huang L. Enantiospecific adjuvant activity of cationic lipid DOTAP in cancer vaccine. Cancer Immunol. Immunother. 2011, 60, 629-638.
13. 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.
14. Tanaka T, Legat A, Adam E, Steuve J, Gatot JS, Vandenbranden M, Ulianov L, Lonez C, Ruysschaert JM, 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.
15. Zanoni I, Ostuni R, Marek LR, Barresi S, Barbalat R, Barton GM, Granucci F, Kagan JC. CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 2011, 147, 868-880.
16. 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.
17. Zhang JS, Liu F, Huang L. Implications of pharmacokinetic behavior of lipoplex for its inflammatory toxicity. Adv. Drug Deliv. Rev. 2005, 57, 689-698.
18. Conwell CC, Liu F, Huang L. Several serum proteins significantly decrease inflammatory response to lipid-based non-viral vectors. Mol. Ther. 2008, 16, 370-377.
19. Li SD, Huang L. Gene therapy progress and prospects: non-viral gene therapy by systemic delivery. Gene Ther. 2006, 13, 1313-1319.
20. Sellins K, Fradkin L, Liggitt D, Dow S. Type I interferons potently suppress gene expression following gene delivery using liposome(-)DNA complexes. Mol. Ther. 2005, 12, 451-459.
21. Baatz JE, Zou Y, Korfhagen TR. Inhibitory effects of tumor necrosis factor-a on cationic lipid-mediated gene delivery to airway cells in vitro. Biochim. Biophys. Acta 2001, 41535, 100-109.
22. Elouahabi A, Flamand V, Ozkan S, Paulart F, Vandenbranden M, Goldman M, Ruysschaert JM. Free cationic liposomes inhibit the inflammatory response to cationic lipid-DNA complex injected intravenously and enhance its transfection efficiency. Mol. Ther. 2003, 7, 81-88.
23. Qin L, Ding Y, Pahud DR, Chang E, Imperiale MJ, Bromberg JS. Promoter attenuation in gene therapy: interferon-? and tumor necrosis factor-a inhibit transgene expression. Hum. Gene Ther. 1997, 8, 2019-2029.
24. Sakurai H, Sakurai F, Kawabata K, Sasaki T, Koizumi N, Huang H, Tashiro K, Kurachi S, Nakagawa S, Mizuguchi H. Comparison of gene expression efficiency and innate immune response induced by Ad vector and lipoplex. J. Control. Release 2007, 117, 430-437.
25. Gao X, Kim KS, Liu D. Nonviral gene delivery: what we know and what is next. AAPS J. 2007, 9, E92-E104.
26. Liu F, Conwell CC, Yuan X, Shollenberger LM, Huang L. Novel nonviral vectors target cellular signaling pathways: regulated gene expression and reduced toxicity. J. Pharmacol. Exp. Ther. 2007, 321, 777-783.
27. Liu F, Shollenberger LM, Huang L. Non-immunostimulatory nonviral vectors. FASEB J. 2004, 18, 1779-1781.
28. Uchida S, Itaka K, Chen Q, Osada K, Ishii T, Shibata MA, Harada-Shiba M, Kataoka K. PEGylated polyplex with optimized PEG shielding enhances gene introduction in lungs by minimizing inflammatory responses. Mol. Ther. 2012, 20, 1196-1203.
29. Morrissey DV, Lockridge JA, Shaw L, Blanchard K, Jensen K, Breen W, Hartsough K, Machemer L, Radka S, Jadhav V, Vaish N, Zinnen S, Vargeese C, Bowman K, Shaffer CS, Jeffs LB, Judge A, MacLachlan I, Polisky B. Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs. Nat. Biotechnol. 2005, 23, 1002-1007.
30. Zimmermann TS, Lee ACH, Akinc A, Bramlage B, Bumcrot D, Fedoruk MN, Harborth J, Heyes JA, Jeffs LB, John M, Judge AD, Lam K, McClintock K, Nechev LV, Palmer LR, Racie T, R o hl I, Seiffert S, Shanmugam S, Sood V, Soutschek J, Toudjarska I, Wheat AJ, Yaworski E, Zedalis W, Koteliansky V, Manoharan M, Vornlocher HP, MacLachlan I. RNAi-mediated gene silencing in non-human primates. Nature 2006, 441, 111-114.
31. Akinc A, Querbes W, De S, Qin J, Frank-Kamenetsky M, Jayaprakash KN, Jayaraman M, Rajeev KG, Cantley WL, Dorkin JR, Butler JS, Qin L, Racie T, Sprague A, Fava E, Zeigerer A, Hope MJ, Zerial M, Sah DW, Fitzgerald K, Tracy MA, Manoharan M, Koteliansky V, Fougerolles Ad, Maier MA. Targeted delivery of RNAi therapeutics with endogenous and exogenous ligand-based mechanisms. Mol. Ther. 2010, 18, 1357-1364.
32. Judge AD, Bola G, Lee AC, MacLachlan I. Design of noninflammatory synthetic siRNA mediating potent gene silencing in vivo. Mol. Ther. 2006, 13, 494-505.
33. Judge AD, Sood V, Shaw JR, Fang D, McClintock K, MacLachlan I. Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat. Biotechnol. 2005, 23, 457-462.
34. Robbins M, Judge A, Ambegia E, Choi C, Yaworski E, Palmer L, McClintock K, MacLachlan I. Misinterpreting the therapeutic effects of small interfering RNA caused by immune stimulation. Hum. Gene Ther. 2008, 19, 991-999.
35. Robbins M, Judge A, Liang L, McClintock K, Yaworski E, MacLachlan I. 2 '-O-Methyl-modified RNAs act as TLR7 antagonists. Mol. Ther. 2007, 15, 1663-1669.
36. Huang L, Liu Y. In vivo delivery of RNAi with lipid-based nanoparticles. Annu. Rev. Biomed. Eng. 2011, 13, 507-530.
37. Dams ET, Laverman P, Oyen WJ, Storm G, Scherphof GL, van Der Meer JW, Corstens FH, Boerman OC. Accelerated blood clearance and altered biodistribution of repeated injections of sterically stabilized liposomes. J. Pharmacol. Exp. Ther. 2000, 292, 1071-1079.
38. Ishida T, Maeda R, Ichihara M, Mukai Y, Motoki Y, Manabe Y, Irimura K, Kiwada H. The accelerated clearance on repeated injection of pegylated liposomes in rats: laboratory and histopathological study. Cell. Mol. Biol. Lett. 2002, 7, 286.
39. Laverman P, Carstens MG, Boerman OC, Dams ET, Oyen WJ, van Rooijen N, Corstens FH, Storm G. Factors affecting the accelerated blood clearance of polyethylene glycol-liposomes upon repeated injection. J. Pharmacol. Exp. Ther. 2001, 298, 607-612.
40. Ishida T, Kiwada H. Accelerated blood clearance (ABC) phenomenon upon repeated injection of PEGylated liposomes. Int. J. Pharm. 2008, 354, 56-62.
41. Shimizu T, Ishida T, Kiwada H. Transport of PEGylated liposomes from the splenic marginal zone to the follicle in the induction phase of the accelerated blood clearance phenomenon. Immunobiology 2012, http://dx.doi. org/10.1016/j.imbio.2012.08.274.
42. Ishida T, Harada M, Wang XY, Ichihara M, Irimura K, Kiwada H. Accelerated blood clearance of PEGylated liposomes following preceding liposome injection: effects of lipid dose and PEG surface-density and chain length of the first-dose liposomes. J. Control. Release 2005, 105, 305-317.
43. Koide H, Asai T, Hatanaka K, Urakami T, Ishii T, Kenjo E, Nishihara M, Yokoyama M, Ishida T, Kiwada H, Oku N. Particle size-dependent triggering of accelerated blood clearance phenomenon. Int. J. Pharm. 2008, 362, 197-200.
44. Ishida T, Ichihara M, Wang X, Yamamoto K, Kimura J, Majima E, Kiwada H. Injection of PEGylated liposomes in rats elicits PEG-specific IgM, which is responsible for rapid elimination of a second dose of PEGylated liposomes. J. Control. Release 2006, 112, 15-25.
45. Suzuki T, Ichihara M, Hyodo K, Yamamoto E, Ishida T, Kiwada H, Ishihara H, Kikuchi H. Accelerated blood clearance of PEGylated liposomes containing doxorubicin upon repeated administration to dogs. Int. J. Pharm. 2012, 436, 636-643.
46. La-Beck NM, Zamboni BA, Gabizon A, Schmeeda H, Amantea M, Gehrig PA, Zamboni WC. Factors affecting the pharmacokinetics of PEGylated liposomal doxorubicin in patients. Cancer Chemother. Pharmacol. 2012, 69, 43-50.
47. Tagami T, Nakamura K, Shimizu T, Yamazaki N, Ishida T, Kiwada H. CpG motifs in pDNA-sequences increase anti-PEG IgM production induced by PEG-coated pDNA-lipoplexes. J. Control. Release 2010, 142, 160-166.
48. Tagami T, Uehara Y, Moriyoshi N, Ishida T, Kiwada H. Anti-PEG IgM production by siRNA encapsulated in a PEGylated lipid nanocarrier is dependent on the sequence of the siRNA. J. Control. Release 2011, 151, 149-154.
49. Judge A, McClintock K, Phelps JR, Maclachlan I. Hypersensitivity and loss of disease site targeting caused by antibody responses to PEGylated liposomes. Mol. Ther. 2006, 13, 328-337.
50. Cheng WW, Allen TM. The use of single chain Fv as targeting agents for immunoliposomes: an update on immunoliposomal drugs for cancer treatment. Expert Opin. Drug Deliv. 2010, 7, 461-478.
51. Harding JA, Engbers CM, Newman MS, Goldstein NI, Zalipsky S. Immunogenicity and pharmacokinetic attributes of poly(ethylene glycol)-grafted immunoliposomes. Biochim. Biophys. Acta 1997, 1327, 181-192.
52. Banerji B, Alving CR. Anti-liposome antibodies induced by lipid A. I. Influence of ceramide, glycosphingolipids, and phosphocholine on complement damage. J. Immunol. 1981, 126, 1080-1084.
53. Banerji B, Lyon JA, Alving CR. Membrane lipid composition modulates the binding specificity of a monoclonal antibody against liposomes. Biochim. Biophys. Acta 1982, 689, 319-326.
54. Schuster BG, Neidig M, Alving BM, Alving CR. Production of antibodies against phosphocholine, phosphatidylcholine, sphingomyelin, and lipid A by injection of liposomes containing lipid A. J. Immunol. 1979, 122, 900-905.
55. Wassef NM, Roerdink F, Swartz GM Jr, Lyon JA, Berson BJ, Alving CR. Phosphate-binding specificities of monoclonal antibodies against phosphoinositides in liposomes. Mol. Immunol. 1984, 21, 863-868.
56. Wassef NM, Swartz GM Jr, Alving CR, Kates M. Antibodies to liposomal phosphatidylcholine and phosphatidylsulfocholine. Biochem. Cell Biol. 1990, 68, 54-58.
57. Gluck R, Walti E. Are anti-phospholipid antibodies to be expected after proteoliposomal hepatitis A vaccination ? J. Liposome Res. 1996, 6, 415-439.
58. Rauch J, Janoff AS. Phospholipid in the hexagonal II phase is immunogenic: evidence for immunorecognition of nonbilayer lipid phases in vivo. Proc. Natl. Acad. Sci. USA. 1990, 87, 4112-4114.
59. Di Gioacchino M, Petrarca C, Lazzarin F, Di Giampaolo L, Sabbioni E, Boscolo P, Mariani-Costantini R, Bernardini G. Immunotoxicity of nanoparticles. Int. J. Immunopathol. Pharmacol. 2011, 24 (Suppl. 1), 65S-71S.
60. Landesman-Milo D, Peer D. Altering the immune response with lipid-based nanoparticles. J. Control. Release 2012, 161, 600-608.
61. Lonez C, Vandenbranden M, Ruysschaert JM. Cationic liposomal lipids: from gene carriers to cell signaling. Prog. Lipid Res. 2008, 47, 340-347.
62. Moyano DF, Goldsmith M, Solfiell DJ, Landesman-Milo D, Miranda OR, Peer D, Rotello VM. Nanoparticle hydrophobicity dictates immune response. J. Am. Chem. Soc. 2012, 134, 3965-3967.
63. Peer D. Immunotoxicity derived from manipulating leukocytes with lipid-based nanoparticles. Adv. Drug Deliv. Rev. 2012, 64, 1738-1748.
64. Christensen D, Korsholm KS, Andersen P, Agger EM. Cationic liposomes as vaccine adjuvants. Expert Rev. Vaccines 2011, 10, 513-521.
65. Christensen D, Korsholm KS, Rosenkrands I, Lindenstrom T, Andersen P, Agger EM. Cationic liposomes as vaccine adjuvants. Expert Rev. Vaccines 2007, 6, 785-796.
66. Chono S, Li SD, Conwell CC, Huang L. An efficient and low immunostimulatory nanoparticle formulation for systemic siRNA delivery to the tumor. J. Control. Release 2008, 131, 64-69.