Nanobiotechnologic approach to a promising vaccine prototype for immunisation against leishmaniasis: a fast and effective method to incorporate GPI-anchored proteins of Leishmania amazonensis into liposomes

References

• Afrin F, Rajesh R, Anam K, Gopinath M, Pal S, Ali N. Characterization of Leishmania donovani antigens encapsulated in liposomes that induce protective immunity in BALB/c mice. Infect Immun, 2002;70:6697–706
   PubMed Web of Science ®Google Scholar
• Ali N, Afrin F. Protection of mice against visceral leishmaniasis by immunization with promastigote antigen incorporated in liposomes. J Parasitol, 1997;83:70–5
   PubMed Web of Science ®Google Scholar
• Alvar J, Vélez ID, Bern C, Herrero M, Desjeux F, Cano J, Jannin J, Boer MD. Leishmaniasis worldwide and global estimates of its incidence. PLOS One, 2012;7:e35671
   PubMed Web of Science ®Google Scholar
• Badiee A, Jaafari MR, Khamesipour A. Leishmania major: Immune response in BALB/c mice immunized with stress-inducible protein 1 encapsulated in liposomes. Exp Parasitol, 2007;115:127–34
   PubMed Web of Science ®Google Scholar
• Barral A, Pedral-Sampaio D, Grimaldi G Jr, Momen H, McMahon-Pratt D, Ribeiro de Jesus A, Almeida R, Badaro R, Barral-Netto M, Carvalho EM, Johnson WD Jr. Leishmaniasis in Bahia, Brazil: Evidence that Leishmania amazonensis produces a wide spectrum of clinical disease. Am J Trop Med Hyg, 1991;44:536–46
   PubMed Web of Science ®Google Scholar
• Bhowmick S, Ravindram R, Ali N. Leishmanial antigens in liposomes promote protective immunity and provide immunotherapy against visceral leishmaniasis via polarized Th1 response. Vaccine, 2007;25:6544–56
   PubMed Web of Science ®Google Scholar
• Bhowmick S, Ravindran R, Ali N. Gp63 in stable cationic liposomes confers sustained vaccine immunity to susceptible BALB/c mice infected with Leishmania donovani. Infect Immun, 2008;76:1003–15
   PubMed Web of Science ®Google Scholar
• Bordier C. The promastigote surface of Leishmania. Parasitol Today, 1981;24:73–9
   Google Scholar
• Brewer JM, Tetley L, Richmond J, Liew FY, Alexander J. Cellular immunology and immune regulation: Lipid vesicle size determines the Th1 or Th2 response to entrapped antigen. J Immunol, 1998;161:4000–7
   PubMed Web of Science ®Google Scholar
• Cevc G, March D. 1987. Bilayer elasticity. In: Bittar EE, ed. Phospholipid bilayer, physical principles and models. Cell biology: A series of monographs. New York: Wiley, pp. 347–68
   Google Scholar
• Chen PS Jr, Toribara TY, Warner H. Microdetermination of phosphorus. Anal Chem, 1956;28:1756–8
   Web of Science ®Google Scholar
• Colhone MC, Nobre TM, Zaniquelli MED, Stabeli RG, Ciancaglini P. Incorporation of antigenic GPI-protein from Leishmania amazonensis to membrane mimetic systems: Influence of DPPC/cholesterol ratio. J Colloid Interface Sci, 2009;333:373–9
   PubMed Web of Science ®Google Scholar
• Daghastanli KR, Ferreira RB, Thedei G Jr, Maggio B, Ciancaglini P. Lipid composition-dependent incorporation of multiple membrane proteins into liposomes. Colloids Surf B Biointerfaces, 2004;36:127–37
   PubMed Web of Science ®Google Scholar
• de Oliveira CI, Nascimento IP, Barral A, Soto M, Barral-Netto M. Challenges and perspectives in vaccination against leishmaniasis. Parasitol Int, 2009;58:319–24
   PubMed Web of Science ®Google Scholar
• De Souza W. Structural organization of the cell surface of pathogenic protozoa. Micron, 1995;26:405–30
   PubMed Web of Science ®Google Scholar
• Doroud D, Zahedifard F, Vatanara A, Taslimi Y, Vahabpour R, Torkashvand F, Vaziri B, Rouholamini Najafabadi A, Rafati S. C-terminal domain deletion enhances the protective activity of cpa/cpb loaded solid lipid nanoparticles against Leishmania major in BALB/c mice. PLOS Neglected Trop Dis, 2011;5:e1236
   PubMed Web of Science ®Google Scholar
• Felnerova D, Viret JF, Gluck R, Moser C. Liposomes and virosomes as delivery systems for antigens, nucleic acids and drugs. Curr Opin Biotechnol, 2004;15:518–29
   PubMed Web of Science ®Google Scholar
• Grenfell RF, Marques-da-Silva EA, Souza-Testasicca MC, Coelho EA, Fernandes AP, Afonso LC, Rezende SA. Antigenic extracts of Leishmania braziliensis and Leishmania amazonensis associated with saponin partially protects BALB/c mice against Leishmania chagasi infection by suppressing IL-10 and IL-4 prodution. Mem Instit Oswaldo Cruz, 2010;105:818–22
   PubMed Web of Science ®Google Scholar
• Handman E. Leishmaniasis: Current status of vaccine development. Clin Microbiol Rev, 2001;14:229–43
   PubMed Web of Science ®Google Scholar
• Hartree EF. Determination of protein: A modification of the Lowry method that gives a linear photometric response. Anal Biochem, 1972;48:422–7
   PubMed Web of Science ®Google Scholar
• Higgins G. 1987. Separation and analysis of membrane lipid components. In: Findlay JBC, Evans WH, eds. Biological membranes. Practical approach series. Oxford-Washington DC: IRL Press, pp. 104–37
   Google Scholar
• Jaafari MR, Badiee A, Khamesipour A, Samiei A, Soroush D, Kheiri MT, Barkhordari F, McMaster WR, Mahboudi F. The role of CpG ODN in enhancement of immune response and protection in BALB/c mice immunized with recombinant major surface glycoprotein of Leishmania (rgp63) encapsulated in cationic liposome. Vaccine, 2007;25:6107–17
   PubMed Web of Science ®Google Scholar
• Jaafari MR, Ghafarian A, Farrokh-Gisour A, Samiei A, Kheiri MT, Mahboudi F, Barkhordari F, Khamesipour A, McMaster WR. Immune response and protection assay of recombinant major surface glycoprotein of Leishmania (rgp63) reconstituted with liposomes in BALB/c mice. Vaccine, 2006;24:5708–17
   PubMed Web of Science ®Google Scholar
• Janssen R, Wauben MH, Tommassen J. Quaternary structure of a carrier protein influences antigenicity and immunogenicity of an inserted T cell determinant. Int Immunol, 1996;8:829–36
   PubMed Web of Science ®Google Scholar
• Kawamura K, Kadowaki N, Suzuki R, Udagawa S, Kasaoka S, Utoguchi N, Kitawaki T, Sugimoto N, Okada N, Maruyama K, Uchiyama T. Dendritic cells that endocytosed antigen-containing IgG-liposomes elicit effective antitumor immunity. J Immunother, 2006;29:165–74
   PubMed Web of Science ®Google Scholar
• Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 1970;227:680–5
   PubMed Web of Science ®Google Scholar
• Laing P, Bacon A, McCormack B, Gregoriadis G, Frisch B, Schuber F. The co-delivery approach to liposomal vaccines: Application to the development of influenza-A and hepatitis-B vaccine candidates. J Liposome Res, 2006;16:229–35
   PubMed Web of Science ®Google Scholar
• Leserman L. Liposomes as protein carriers in immunology. J Liposome Res, 2004;14:175–89
   PubMed Web of Science ®Google Scholar
• Mazumdar T, Anam K, Ali N. A mixed Th1/Th2 response elicited by a liposomal formulation of Leishmania vaccine instructs Th1 responses and resistance to Leishmania donovani in susceptible BALB/c mice. Vaccine, 2004;22:1162–71
   PubMed Web of Science ®Google Scholar
• Mazumder S, Maji M, Ali N. Potentiating effects of MPL on DSPC bearing cationic liposomes promote recombinant gp63 vaccine efficacy: High immunogenicity and protection. PLoS Neglected Trop Dis, 2011;5:e1429
   PubMed Web of Science ®Google Scholar
• Mutwiri GK, Nichani AK, Baiuk S, Baiuk LA. Strategies for enhancing the immunostimulatory effects of CpG oligodeoxynucleotides. J Control Release, 2004;97:1–17
   PubMed Web of Science ®Google Scholar
• Nagill R, Kaur S. Enhanced efficacy and immunogenicity of 78 kDa antigen formulated in various adjuvants against murine visceral leishmaniasis. Vaccine, 2010;28:4002–12
   PubMed Web of Science ®Google Scholar
• Nguyen DN, Green JJ, Chan JM, Langer R, Anderson DG. Polymeric materials for gene delivery and DNA vaccination. Adv Mater, 2009;21:847–67
   PubMed Web of Science ®Google Scholar
• Noronha FS, Nunes AC, Souza KT, Melo MN, Ramalho-Pinto FJ. Differential sensitivity of New World Leishmania spp. promastigotes to complement-mediated lysis: Correlation with the expression of three parasite polypeptides. Acta Trop, 1998;69:17–29
   PubMed Web of Science ®Google Scholar
• Noronha FS, Ramalho-Pinto FJ, Horta MF. Cytolytic activity in the genus Leishmania: Involvement of a putative pore-forming protein. Infect Immun, 1996;64:3975–82
   PubMed Web of Science ®Google Scholar
• Nunes AC, Almeida-Campos FR, Horta MF, Ramalho-Pinto FJ. Leishmania amazonensis promastigotes evade complement killing by interfering with the late steps of the cascade. Parasitology, 1997;115:601–9
   PubMed Web of Science ®Google Scholar
• Nylén S, Khamesipour A, Mohammadi A, Jafari-Shakib R, Eidsmo L, Noazin S, Modabber F, Akuffo H. Surrogate markers of immunity to Leishmania major in leishmanin skin test negative individuals from an endemic area re-visited. Vaccine, 2006;24:6944–54
   PubMed Web of Science ®Google Scholar
• O'Hagan DT, MacKichan ML, Singh M. Recent developments in adjuvants for vaccines against infectious diseases. Biomol Eng, 2001;18:69–85
   PubMedGoogle Scholar
• Perrie Y, Kastner E, Kaur R, Wilkinson A, Ingham AJ. A case-study investigating the physicochemical characteristics that dictate the function of a liposomal adjuvant. Hum Vaccines Immunother, 2013;9:1374–81
   PubMed Web of Science ®Google Scholar
• Rao M, Alving CR. Delivery of lipids and liposomal proteins to the cytoplasm and Golgi of antigen-presenting cells. Adv Drug Deliv Rev, 2000;41:171–88
   PubMed Web of Science ®Google Scholar
• Santos FR, Ferraz DB, Daghastanli KRP, Ramalho-Pinto FJ, Ciancaglini P. Mimetic membrane system to carry multiple antigenic proteins from Leishmania amazonensis. J Membr Biol, 2006;210:173–81
   PubMed Web of Science ®Google Scholar
• Shargh VH, Jaafari MR, Khamesipour A, Jalali SA, Firouzmand H, Abbasi A, Badiee A. Cationic liposomes containing soluble Leishmania antigens (SLA) plus CpG ODNs induce protection against murine model of leishmaniasis. Parasitol Res, 2012;111:105–14
   PubMed Web of Science ®Google Scholar
• Silveira FT, Lainson R, Corbett CEP. Clinical and immunopathological spectrum of American cutaneous leishmaniasis with special reference to the disease in Amazonian Brazil – A review. Mem Instit Oswaldo Cruz, 2004;99:239–51
   PubMed Web of Science ®Google Scholar
• Streit JA, Recker TJ, Filho FG, Beverley SM, Wilson ME. Protective immunity against the protozoan Leishmania chagasi is induced by subclinical cutaneous infection with virulent but not avirulent organisms. J Immunol, 2001;166:1921–9
   PubMed Web of Science ®Google Scholar
• Titus RG, Gueiros-Filho FJ, de Freitas LA, Beverley SM. Development of a safe live Leishmania vaccine line by gene replacement. Proc Natl Acad Sci USA, 1995;92:10267–71
   PubMed Web of Science ®Google Scholar
• Tolezano JE, Uliana SR, Taniguchi HH, Araújo MF, Barbosa JA, Barbosa JE, Floeter-Winter LM, Shaw JJ. The first records of Leishmania (Leishmania) amazonensis in dogs (Canis familiaris) diagnosed clinically as having canine visceral leishmaniasis from Araçatuba County. Vet Parasitol, 2007;149:280–4
   PubMed Web of Science ®Google Scholar
• Uemura A, Watarai S, Iwasaki T, Kodama H. Induction of immune responses against glycosphingolipid antigens: Comparison of antibody responses in mice immunized with antigen associated with liposomes prepared from various phospholipids. J Vet Med Sci, 2005;67:1197–201
   PubMed Web of Science ®Google Scholar
• WHO. 2013. Sustaining the Drive to Overcome the Global Impact of Neglected Tropical Diseases: Second WHO Report on Neglected Diseases. Available at: http://www.who.int/leishmaniasis/en/. Accessed 23 June 2014
   Google Scholar
• Yuba E, Kojima C, Harada A, Tana Watarai S, Kono K. pH-Sensitive fusogenic polymer-modified liposomes as a carrier of antigenic proteins for activation of cellular immunity. Biomaterials, 2010;31:943–51
   PubMed Web of Science ®Google Scholar