The role of nanoliposome bilayer composition containing soluble leishmania antigen on maturation and activation of dendritic cells

Document Type: Original Article

Authors

1 Nanotechnology Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran

2 Department of Pharmaceutical Nanotechnology, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran

3 Department of Immunology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

4 Department of Immunology, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

5 Biotechnology Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran

Abstract

Objective(s): Dendritic cells (DCs) play a critical role in activation of T cell responses. Induction of type1 T helper (Th1) immune response is essential to generate protective immunity against cutaneous leishmaniasis. The intrinsic tendency of liposomes to have interaction with antigen-presenting cells is the main rationale to utilize liposomes as antigen carriers. In the present study, the effect of lipid phase transition temperature on DCs maturation and liposome uptake by murine bone marrow derived dendritic cells and human monocyte derived dendritic cells was investigated.
Materials and Methods: Two cationic liposomal formulations consisting of DOTAP and DSPC/DOTAP were prepared and contained soluble leishmania antigen. Liposomes were incubated with immature or mature DCs derived from bone marrow (BMDCs) of C57BL/6 (which are resistant to cutaneous leishmaniasis), BALB/c mice (susceptible to cutaneous leishmaniasis) or DCs derived from human monocytes (MoDCs). The expression of DCs co-stimulatory markers and liposomal uptake were evaluated by flow cytometry method.
Results: DCs which were encountered to liposomes consisting of DSPC showed significantly more expression of co-stimulatory molecules in cells from both human and C57BL/6 mice but not in cells from BALB/c mice.
Conclusion: It is concluded that cationic liposomes consisting of DSPC are an effective adjuvant for antigen delivery in case of MoDCs and BMDCs from C57BL/6 mice. Moreover, DCs from different origins act differently in uptake of liposomes.

Keywords

Main Subjects


1. Labeur MS, Roters B, Pers B, Mehling A, Luger TA, Schwarz T, et al 1999. Generation of tumor immunity by bone marrow-derived dendritic cells correlates with dendritic cell maturation stage. J Immunol 162:168-175.
2. Sozzani S, Allavena P, D’Amico G, Luini W, Bianchi G, Kataura M, et al 1998. Cutting edge: differential regulation of chemokine receptors during dendritic cell maturation: a model for their trafficking properties. J Immunol 161:1083-1086.
3. Mellman I, Steinman RM 2001. Dendritic cells: specialized and regulated antigen processing machines. Cell  106:255-258.
4. Copland MJ, Baird MA, Rades T, McKenzie JL, Becker B, Reck F, et al 2003. Liposomal delivery of antigen to human dendritic cells. Vaccine  21:883-890.
5. Alving CR 1991. Liposomes as carriers of antigens and adjuvants. J Immunol Methods 140:1-13.
6. Schwendener RA 2014. Liposomes as vaccine delivery systems: a review of the recent advances. Ther Adv Vaccines  2:159-182.
7. Watson DS, Endsley AN, Huang L 2012. Design considerations for liposomal vaccines: influence of formulation parameters on antibody and cell-mediated immune responses to liposome associated antigens. Vaccine  30:2256-2272.
8. Ravindran R, Maji M, Ali N 2011. Vaccination with liposomal leishmanial antigens adjuvanted with monophosphoryl lipid–trehalose dicorynomycolate (MPL-TDM) confers long-term protection against visceral leishmaniasis through a human administrable route. Mol Pharm 9:59-70.
9. Brewer JM, Tetley L, Richmond J, Liew FY, Alexander J 1998. Lipid vesicle size determines the Th1 or Th2 response to entrapped antigen. J Immunol 161:4000-4007.
10. Christensen D, Korsholm KS, Rosenkrands I, Lindenstrøm T, Andersen P, Agger EM 2007. Cationic liposomes as vaccine adjuvants. Expert Rev Vaccines 6:785-796.
11. Soema PC, Willems G-J, Jiskoot W, Amorij J-P, Kersten GF 2015. Predicting the influence of liposomal lipid composition on liposome size, zeta potential and liposome-induced dendritic cell maturation using a design of experiments approach. Eur J Pharm Biopharm 94:427-435.
12. Vangasseri DP, Cui Z, Chen W, Hokey DA, Falo Jr LD, Huang L 2006. Immunostimulation of dendritic cells by cationic liposomes. Mol Membr Biol 23:385-395.
13. Cunningham AC 2002. Parasitic adaptive mechanisms in infection by Leishmania. Exp Mol Pathol 72:132-141.
14. Sacks D, Noben-Trauth N 2002. The immunology of susceptibility and resistance to Leishmania major in mice. Nat Rev Immunol 2:845-858.
15. Silvestre R, Cordeiro-da-Silva A, Ouaissi A 2008. Live attenuated Leishmania vaccines: a potential strategic alternative. Arch Immunol Ther Exp (Warsz)  56:123-126.
16. Rafati seyedi yazdi s, Couty-jouve s, Alimohamadian mh, Dowlati y 1997. Evaluation of cellular immune responses to amastigote soluble leishmania major antigens in recovered cases of cutaneous leishmaniasis. Med J Islam Repub Iran 11:33-38.
17. Firouzmand H, Badiee A, Khamesipour A, Shargh VH, Alavizadeh SH, Abbasi A, et al 2013. Induction of protection against leishmaniasis in susceptible BALB/c mice using simple DOTAP cationic nanoliposomes containing soluble Leishmania antigen (SLA). Acta Trop 128:528-535.
18. Barbi J, Brombacher F, Satoskar AR 2008. T cells from Leishmania major-susceptible BALB/c mice have a defect in efficiently up-regulating CXCR3 upon activation. J Immunol 181:4613-4620.
19. Scott P 1991. IFN-gamma modulates the early development of Th1 and Th2 responses in a murine model of cutaneous leishmaniasis. J Immunol 147:3149-3155.
20. Lohoff M, Sommer F, Solbach W, Röllinghoff M 1989. Coexistence of Antigen-Specific T H 1 and T H 2 Cells in Genetically Susceptible BALB/c Mice Infected with Leishmania major. Immunobiology  179:412-421.
21. Scott P, Novais FO 2016. Cutaneous leishmaniasis: immune responses in protection and pathogenesis. Nat Rev Immunol 16:581-592.
22. Stamatatos L, Leventis R, Zuckermann MJ, Silvius JR 1988. Interactions of cationic lipid vesicles with negatively charged phospholipid vesicles and biological membranes. Biochemistry  27:3917-3925.
23. Maji M, Mazumder S, Bhattacharya S, Choudhury ST, Sabur A, Shadab M, et al 2016. A lipid based antigen delivery system efficiently facilitates MHC class-I antigen presentation in dendritic cells to stimulate CD8+ T cells. Sci Rep 6:27206.
24. Scott P, Pearce E, Natovitz P, Sher A 1987. Vaccination against cutaneous leishmaniasis in a murine model. I. Induction of protective immunity with a soluble extract of promastigotes. J Immunol 139:221-227.
25. Torchilin V, Weissig V. 2003. Liposomes: a practical approach. ed.: Oxford University Press.
26. Torchilin VP 2005. Recent advances with liposomes as pharmaceutical carriers. Nat Rev Drug Discov 4:145-160.
27. Nobs L, Buchegger F, Gurny R, Allémann E 2004. Current methods for attaching targeting ligands to liposomes and nanoparticles. J Pharm Sci 93:1980-1992.
28. Quer CB, Elsharkawy A, Romeijn S, Kros A, Jiskoot W 2012. Cationic liposomes as adjuvants for influenza hemagglutinin: more than charge alone. Eur J Pharm Biopharm 81:294-302.
29. Henriksen-Lacey M, Bramwell VW, Christensen D, Agger E-M, Andersen P, Perrie Y 2010. Liposomes based on dimethyldioctadecylammonium promote a depot effect and enhance immunogenicity of soluble antigen. J Control Release 142:180-186.
30. Brgles M, Habjanec L, Halassy B, Tomašić J 2009. Liposome fusogenicity and entrapment efficiency of antigen determine the Th1/Th2 bias of antigen-specific immune response. Vaccine 27:5435-5442.
31. Copland MJ, Rades T, Davies NM, Baird MA 2005. Lipid based particulate formulations for the delivery of antigen. Immunol Cell Biol 83:97-105.
32. Heravi Shargh V, Jaafari MR, Khamesipour A, Jaafari I, Jalali SA, Abbasi A, et al. 2012. Liposomal SLA co-incorporated with PO CpG ODNs or PS CpG ODNs induce the same protection against the murine model of leishmaniasis. Vaccine  30:3957-3964.
33. Antimisiaris SG, Jayasekera P, Gregoriadis G 1993. Liposomes as vaccine carriers: incorporation of soluble and particulate antigens in giant vesicles. J Immunol Methods 166:271-280.
34. Moghimi SM, Patel HM 1988. Tissue specific opsonins for phagocytic cells and their different affinity for cholesterol‐rich liposomes. FEBS lett 233:143-147.
35. Kersten GF, Crommelin DJ 1995. Liposomes and ISCOMS as vaccine formulations. Biochim Biophys Acta 1241:117-138.
36. Mazumdar T, Anam K, Ali N 2005. Influence of phospholipid composition on the adjuvanticity and protective efficacy of liposome-encapsulated Leishmania donovani antigens. J Parasitol 91:269-274.
37. Foged C, Arigita C, Sundblad A, Jiskoot W, Storm G, Frokjaer S 2004. Interaction of dendritic cells with antigen-containing liposomes: effect of bilayer composition. Vaccine  22:1903-1913.
38. Noben-Trauth N, Kropf P, Muller I 1996. Susceptibility to Leishmania major infection in interleukin-4-deficient mice. Science 271:987.
39. Scharton-Kersten T, Scott P 1995. The role of the innate immune response in Th1 cell development following Leishmania major infection. J Leukoc Biol 57:515-522.
40. Ma Y, Zhuang Y, Xie X, Wang C, Wang F, Zhou D et al 2011. The role of surface charge density in cationic liposome-promoted dendritic cell maturation and vaccine-induced immune responses. Nanoscale  3:2307-2314.
41. Banchereau J, Steinman RM 1998. Dendritic cells and the control of immunity. Nature  392:245-252.
42. Lutz MB, Schuler G 2002. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol 23:445-449.
43. Mahnke K, Qian Y, Knop J, Enk AH 2003. Induction of CD4+/CD25+ regulatory T cells by targeting of antigens to immature dendritic cells. Blood  101:4862-4869.
44. Dieu M-C, Vanbervliet B, Vicari A, Bridon J-M, Oldham E, Aït-Yahia S, et al. 1998. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J Exp Med 188:373-386.
45. McLellan AD, Starling GC, Williams LA, Hock BD, Hart DN 1995. Activation of human peripheral blood dendritic cells induces the CD86 co‐stimulatory molecule. Eur J Immunol 25:2064-2068.
46. Dzionek A, Fuchs A, Schmidt P, Cremer S, Zysk M, Miltenyi S, et al. 2000. BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J Immunol 165:6037-6046.
47. Tsuji S, Matsumoto M, Takeuchi O, Akira S, Azuma I, Hayashi A, et al. 2000. Maturation of human dendritic cells by cell wall skeleton of Mycobacterium bovis bacillus Calmette-Guerin: involvement of toll-like receptors. Infect Immun 68:6883-6890.
48. Shortman K, Liu Y-J 2002. Mouse and human dendritic cell subtypes. Nat Rev Immunol 2:151-161.
49. Singh-Jasuja H, Thiolat A, Ribon M, Boissier M-C, Bessis N, Rammensee H-G, et al. 2013. The mouse dendritic cell marker CD11c is down-regulated upon cell activation through Toll-like receptor triggering. Immunobiology  218:28-39.
50. Lonez C, Vandenbranden M, Ruysschaert J-M 2008. Cationic liposomal lipids: from gene carriers to cell signaling. Prog Lipid Res 47:340-347.
51. Tanaka T, Legat A, Adam E, Steuve J, Gatot JS, Vandenbranden M, et al. 2008. DiC14‐amidine cationic liposomes stimulate myeloid dendritic cells through toll‐like receptor 4. Eur J Immunol 38:1351-1357.