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Vaccine Design, Nanoparticle Vaccines and Biomaterial Applications

  • Pragya Misra
  • Shailza Singh
Chapter
  • 74 Downloads

Abstract

Leishmaniasis is a neglected tropical disease subverting the immune system of the infected individual. Most of available treatment regimens are associated with various drawbacks such as drug resistance, toxicity, and cost. Development and implementation of vaccines seem to be the only rationale to eradicate the disease. However, various traditional approaches for vaccine development have been implicated against leishmaniasis, but till date, no vaccine is available for humans in the market. It has been observed that vaccination strategy including live or attenuated vaccines is mainly due to their ability to deliver the antigens to the appropriate immune cells for generating an immune response. This indicates that pan-Leishmania vaccine packaged into a suitable delivery system could not only increase the stability of the vaccine candidate but also lead to its targeted delivery which will mimic the natural infection and recognition of the antigen by the desired antigen-presenting cells. Various natural and synthetic polymers have been used as delivery vehicles encapsulating the vaccine components against leishmaniasis. Herein, we have tried to summarize such attempts, along with our insight on using synthetic circuits as delivery system, not only for targeted but also controlling the expression dynamics of antigen as needed.

Keywords

Leishmania Vaccine Synthetic circuit Biomaterials 

References

  1. 1.
    World Health Organisation (2017) WHO|Universal health coverage (UHC). WHO fact sheet 2017Google Scholar
  2. 2.
    Centlivre M, Combadière B (2015) New challenges in modern vaccinology. BMC Immunol.  https://doi.org/10.1186/s12865-015-0075-2
  3. 3.
    Delany I, Rappuoli R, De Gregorio E (2014) Vaccines for the 21st century. EMBO Mol Med.  https://doi.org/10.1002/emmm.201403876
  4. 4.
    Nabel GJ (2013) Designing tomorrow’s vaccines. N Engl J Med.  https://doi.org/10.1056/NEJMra1204186
  5. 5.
    Griffiths KL, Khader SA (2014) Novel vaccine approaches for protection against intracellular pathogens. Curr Opin Immunol.  https://doi.org/10.1016/j.coi.2014.02.003
  6. 6.
    Robinson HL, Amara RR (2005) T cell vaccines for microbial infections. Nat Med.  https://doi.org/10.1038/nm1212
  7. 7.
    Servín-Blanco R, Zamora-Alvarado R, Gevorkian G, Manoutcharian K (2016) Antigenic variability: obstacles on the road to vaccines against traditionally difficult targets. Hum Vaccines Immunother.  https://doi.org/10.1080/21645515.2016.1191718
  8. 8.
    World Health Organization Leishmaniasis (2015). http://www.who.int/mediacentre/factsheets/fs375/en/. Leishmaniasis Fact Sheet No375 2015
  9. 9.
    Molyneux DH, Savioli L, Engels D (2017) Neglected tropical diseases: progress towards addressing the chronic pandemic. Lancet.  https://doi.org/10.1016/S0140-6736(16)30171-4
  10. 10.
    Alvar J, Yactayo S, Bern C (2006) Leishmaniasis and poverty. Trends Parasitol.  https://doi.org/10.1016/j.pt.2006.09.004
  11. 11.
    Cameron MM, Acosta-Serrano A, Bern C, Boelaert M, Den Boer M, Burza S et al (2016) Understanding the transmission dynamics of Leishmania donovani to provide robust evidence for interventions to eliminate visceral leishmaniasis in Bihar, India. The LCNTDR collection: advances in scientific research for NTD control. Parasit Vectors.  https://doi.org/10.1186/s13071-016-1309-8
  12. 12.
    Alvar J, Croft SL, Kaye P, Khamesipour A, Sundar S, Reed SG (2013) Case study for a vaccine against leishmaniasis. Vaccine.  https://doi.org/10.1016/j.vaccine.2012.11.080
  13. 13.
    Vallur AC, Duthie MS, Reinhart C, Tutterrow Y, Hamano S, Bhaskar KRH et al (2014) Biomarkers for intracellular pathogens: establishing tools as vaccine and therapeutic endpoints for visceral leishmaniasis. Clin Microbiol Infect.  https://doi.org/10.1111/1469-0691.12421.
  14. 14.
    Noazin S, Modabber F, Khamesipour A, Smith PG, Moulton LH, Nasseri K et al (2008) First generation leishmaniasis vaccines: a review of field efficacy trials. Vaccine.  https://doi.org/10.1016/j.vaccine.2008.09.085
  15. 15.
    Srivastava S, Shankar P, Mishra J, Singh S (2016) Possibilities and challenges for developing a successful vaccine for leishmaniasis. Parasit Vectors 9:1–15.  https://doi.org/10.1186/s13071-016-1553-yCrossRefGoogle Scholar
  16. 16.
    Halstead SB, Mahalingam S, Marovich MA, Ubol S, Mosser DM (2010) Intrinsic antibody-dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes. Lancet Infect Dis.  https://doi.org/10.1016/S1473-3099(10)70166-3
  17. 17.
    Dube A, Rawat K, Yadav N, Joshi S, Ratnapriya S, Sahasrabuddhe A (2016) Management of visceral leishmaniasis with therapeutic vaccines. Vaccine Dev Ther.  https://doi.org/10.2147/vdt.s110654
  18. 18.
    Kamhawi S (2017) The yin and yang of leishmaniasis control. PLoS Negl Trop Dis.  https://doi.org/10.1371/journal.pntd.0005529
  19. 19.
    Nadim A, Javadian E, Tahvildar Bidruni G, Ghorbani M (1983) Effectiveness of leishmanization in the control of cutaneous leishmaniasis. Bull Soc Pathol Exot Filiales 76(4):377–383PubMedGoogle Scholar
  20. 20.
    Okwor I, Uzonna J (2016) Social and economic burden of human leishmaniasis. Am J Trop Med Hyg.  https://doi.org/10.4269/ajtmh.15-0408
  21. 21.
    Kellina OI (1981) Problem and current lines in investigations on the epidemiology of leishmaniasis and its control in the USSR. Bull Soc Pathol Exot Filiales 74(3):306–318PubMedGoogle Scholar
  22. 22.
    Khamesipour A, Rafati S, Davoudi N, Maboudi F, Modabber F (2006) Leishmaniasis vaccine candidates for development: a global overview. Indian J Med Res 123(3):423–438PubMedGoogle Scholar
  23. 23.
    Nadim A, Javadian E, Mohebali M (1997) The experience of leishmanization in the Islamic Republic of Iran. East Mediterr Heal JGoogle Scholar
  24. 24.
    Hosseini SMH, Hatam GR, Ardehali S (2005) Characterization of leishmania isolated from unhealed lesions caused by leishmanization. East Mediterr Heal J 11(1–2):240–243Google Scholar
  25. 25.
    Khamesipour A, Dowlati Y, Asilian A, Hashemi-Fesharki R, Javadi A, Noazin S et al (2005) Leishmanization: use of an old method for evaluation of candidate vaccines against leishmaniasis. Vaccine.  https://doi.org/10.1016/j.vaccine.2005.02.015
  26. 26.
    Khamesipour A, Abbasi A, Firooz A, Amin Mohammadi AM, Eskandari SE, Jaafari MR (2012) Treatment of cutaneous lesion of 20 years’ duration caused by leishmanization. Indian J Dermatol.  https://doi.org/10.4103/0019-5154.94280
  27. 27.
    Uzonna JE, Wei G, Yurkowski D, Bretscher P (2001) Immune elimination of Leishmania major in mice: implications for immune memory, vaccination, and reactivation disease. J Immunol.  https://doi.org/10.4049/jimmunol.167.12.6967
  28. 28.
    Zaph C, Uzonna J, Beverley SM, Scott P (2004) Central memory T cells mediate long-term immunity to Leishmania major in the absence of persistent parasites. Nat Med.  https://doi.org/10.1038/nm1108
  29. 29.
    McCall LI, Zhang WW, Ranasinghe S, Matlashewski G (2013) Leishmanization revisited: immunization with a naturally attenuated cutaneous Leishmania donovani isolate from Sri Lanka protects against visceral leishmaniasis. Vaccine.  https://doi.org/10.1016/j.vaccine.2012.11.065
  30. 30.
    Sundar S, Singh B (2014) Identifying vaccine targets for anti-leishmanial vaccine development. Expert Rev Vaccines.  https://doi.org/10.1586/14760584.2014.894467
  31. 31.
    Mitchell GF, Handman E, Spithill TW (1984) Vaccination against cutaneous Leishmaniasis in mice using nonpathogenic cloned promastigotes of leishmania major and importance of route of injection. Aust J Exp Biol Med Sci.  https://doi.org/10.1038/icb.1984.14
  32. 32.
    Kimsey PB, Theodos CM, Mitchen TK, Turco SJ, Titus RG (1993) An avirulent lipophosphoglycan-deficient Leishmania major clone induces CD4+ T cells which protect susceptible BALB/c mice against infection with virulent L. major. Infect Immun 61(12):5205–5213CrossRefGoogle Scholar
  33. 33.
    Rivier D, Shah R, Bovay P, Mauel J (1993) Vaccine development against cutaneous leishmaniasis. Subcutaneous administration of radioattenuated parasites protects CBA mice against virulent Leishmania major challenge. Parasite Immunol.  https://doi.org/10.1111/j.1365-3024.1993.tb00587.x
  34. 34.
    Daneshvar H, Coombs GH, Hagan P, Phillips RS (2003) Leishmania mexicana and Leishmania major: attenuation of wild-type parasites and vaccination with the attenuated lines. J Infect Dis.  https://doi.org/10.1086/374783
  35. 35.
    Das A, Ali N (2012) Vaccine prospects of killed but metabolically active leishmania against visceral leishmaniasis. Expert Rev Vaccines.  https://doi.org/10.1586/erv.12.50
  36. 36.
    Jain K, Jain NK (2015) Vaccines for visceral leishmaniasis: a review. J Immunol Methods.  https://doi.org/10.1016/j.jim.2015.03.017
  37. 37.
    Saljoughian N, Taheri T, Rafati S (2014) Live vaccination tactics: possible approaches for controlling visceral leishmaniasis. Front Immunol.  https://doi.org/10.3389/fimmu.2014.00134
  38. 38.
    Streit JA, Recker TJ, Filho FG, Beverley SM, Wilson ME (2001) Protective immunity against the protozoan Leishmania chagasi is induced by subclinical cutaneous infection with virulent but not avirulent organisms. J Immunol.  https://doi.org/10.4049/jimmunol.166.3.1921
  39. 39.
    Titus RG, Gueiros-Filho FJ, De Freitas LAR, Beverley SM (1995) Development of a safe live Leishmania vaccine line by gene replacement. Proc Natl Acad Sci U S A.  https://doi.org/10.1073/pnas.92.22.10267
  40. 40.
    Amaral VF, Teva A, Oliveira-Neto MP, Silva AJ, Pereira MS, Cupolillo E et al (2002) Study of the safety, immunogenicity and efficacy of attenuated and killed Leishmania (Leishmania) major vaccines in a rhesus monkey (Macaca mulatta) model of the human disease. Mem Inst Oswaldo Cruz.  https://doi.org/10.1590/S0074-02762002000700019
  41. 41.
    Anand S, Madhubala R (2015) Genetically engineered ascorbic acid-deficient live mutants of leishmania donovani induce long lasting protective immunity against visceral leishmaniasis. Sci Rep.  https://doi.org/10.1038/srep10706
  42. 42.
    Fiuza JA, Gannavaram S, da Costa Santiago H, Selvapandiyan A, Souza DM, Passos LSA et al (2015) Vaccination using live attenuated Leishmania donovani centrin deleted parasites induces protection in dogs against Leishmania infantum. Vaccine.  https://doi.org/10.1016/j.vaccine.2014.11.039
  43. 43.
    Joshi S, Rawat K, Yadav NK, Kumar V, Siddiqi MI, Dube A (2014) Visceral leishmaniasis: advancements in vaccine development via classical and molecular approaches. Front Immunol.  https://doi.org/10.3389/fimmu.2014.00380
  44. 44.
    Silvestre R, Cordeiro-Da-Silva A, Santarém N, Vergnes B, Sereno D, Ouaissi A (2007) SIR2-deficient Leishmania infantum induces a defined IFN-γ/IL-10 pattern that correlates with protection. J Immunol.  https://doi.org/10.4049/jimmunol.179.5.3161
  45. 45.
    Alexander J, Coombs GH, Mottram JC (1998) Leishmania mexicana cysteine proteinase-deficient mutants have attenuated virulence for mice and potentiate a Th1 response. J ImmunolGoogle Scholar
  46. 46.
    Carrión J, Folgueira C, Soto M, Fresno M, Requena JM (2011) Leishmania infantum HSP70-II null mutant as candidate vaccine against leishmaniasis: a preliminary evaluation. Parasit Vectors.  https://doi.org/10.1186/1756-3305-4-150
  47. 47.
    Dey R, Meneses C, Salotra P, Kamhawi S, Nakhasi HL, Duncan R (2010) Characterization of a Leishmania stage-specific mitochondrial membrane protein that enhances the activity of cytochrome c oxidase and its role in virulence. Mol Microbiol.  https://doi.org/10.1111/j.1365-2958.2010.07214.x
  48. 48.
    Dey R, Dagur PK, Selvapandiyan A, McCoy JP, Salotra P, Duncan R et al (2013) Live attenuated Leishmania donovani p27 gene knockout parasites are nonpathogenic and elicit long-term protective immunity in BALB/c mice. J Immunol.  https://doi.org/10.4049/jimmunol.1202801
  49. 49.
    Elikaee S, Mohebali M, Rezaei S, Eslami H, Khamesipour A, Keshavarz H et al (2018) Development of a new live attenuated Leishmania major p27 gene knockout: safety and immunogenicity evaluation in BALB/c mice. Cell Immunol.  https://doi.org/10.1016/j.cellimm.2018.07.002.
  50. 50.
    Elikaee S, Mohebali M, Rezaei S, Eslami H, Khamesipour A, Keshavarz H et al (2019) Leishmania major p27 gene knockout as a novel live attenuated vaccine candidate: protective immunity and efficacy evaluation against cutaneous and visceral leishmaniasis in BALB/c mice. Vaccine.  https://doi.org/10.1016/j.vaccine.2019.04.068
  51. 51.
    Davoudi N, Khamesipour A, Mahboudi F, McMaster WR (2014) A dual drug Sensitive L. major induces protection without lesion in C57BL/6 mice. PLoS Negl Trop Dis.  https://doi.org/10.1371/journal.pntd.0002785
  52. 52.
    Kumari S, Samani M, Khare P, Misra P, Dutta S, Kolli BK et al (2009) Photodynamic vaccination of hamsters with inducible suicidal mutants of Leishmania amazonensis elicits immunity against visceral leishmaniasis. Eur J Immunol.  https://doi.org/10.1002/eji.200838389
  53. 53.
    Raymond F, Boisvert S, Roy G, Ritt JF, Légaré D, Isnard A et al (2012) Genome sequencing of the lizard parasite Leishmania tarentolae reveals loss of genes associated to the intracellular stage of human pathogenic species. Nucleic Acids Res.  https://doi.org/10.1093/nar/gkr834
  54. 54.
    Pirdel L, Farajnia S (2017) A non-pathogenic recombinant Leishmania expressing lipophosphoglycan 3 against experimental infection with Leishmania infantum. Scand J Immunol.  https://doi.org/10.1111/sji.12557
  55. 55.
    Giunchetti RC, Corrêa-Oliveira R, Martins-Filho OA, Teixeira-Carvalho A, Roatt BM, de Oliveira Aguiar-Soares RD et al (2008) A killed Leishmania vaccine with sand fly saliva extract and saponin adjuvant displays immunogenicity in dogs. Vaccine.  https://doi.org/10.1016/j.vaccine.2007.11.057.
  56. 56.
    Petrovsky N, Aguilar JC (2004) Vaccine adjuvants: current state and future trends. Immunol Cell Biol.  https://doi.org/10.1111/j.0818-9641.2004.01272.x
  57. 57.
    Raman VS, Duthie MS, Fox CB, Matlashewski G, Reed SG (2012) Adjuvants for Leishmania vaccines: from models to clinical application. Front Immunol.  https://doi.org/10.3389/fimmu.2012.00144
  58. 58.
    Teixeira MCA, de Sá Oliveira GG, Santos POM, Bahiense TC, da Silva VMG, Rodrigues MS et al (2011) An experimental protocol for the establishment of dogs with long-term cellular immune reactions to Leishmania antigens. Mem Inst Oswaldo Cruz.  https://doi.org/10.1590/S0074-02762011000200011
  59. 59.
    Bruhn KW, Birnbaum R, Haskell J, Vanchinathan V, Greger S, Narayan R et al (2012) Killed but metabolically active Leishmania infantum as a novel whole-cell vaccine for visceral leishmaniasis. Clin Vaccine Immunol.  https://doi.org/10.1128/CVI.05660-11
  60. 60.
    Khamesipour A (2014) Therapeutic vaccines for leishmaniasis. Expert Opin Biol Ther.  https://doi.org/10.1517/14712598.2014.945415
  61. 61.
    Sharifi I, Aflatoonian MR, Fekri AR, Hakimi Parizi M, Aghaei Afshar A, Khosravi A et al (2015) A comprehensive review of cutaneous leishmaniasis in Kerman province, Southeastern Iran- narrative review article. Iran J Public HealthGoogle Scholar
  62. 62.
    Nagill R, Mahajan R, Sharma M, Kaur S (2009) Induction of cellular and humoral responses by autoclaved and heat-killed antigen of Leishmania donovani in experimental visceral leishmaniasis. Parasitol Int.  https://doi.org/10.1016/j.parint.2009.07.008
  63. 63.
    Kumar R, Engwerda C (2014) Vaccines to prevent leishmaniasis. Clin Transl Immunol.  https://doi.org/10.1038/cti.2014.4
  64. 64.
    Gholami E, Zahedifard F, Rafati S (2016) Delivery systems for Leishmania vaccine development. Expert Rev Vaccines.  https://doi.org/10.1586/14760584.2016.1157478
  65. 65.
    Ravindran R, Bhowmick S, Das A, Ali N (2010) Comparison of BCG, MPL and cationic liposome adjuvant systems in leishmanial antigen vaccine formulations against murine visceral leishmaniasis. BMC Microbiol.  https://doi.org/10.1186/1471-2180-10-181
  66. 66.
    Kumari S, Samant M, Khare P, Sundar S, Sinha S, Dube A (2008) Induction of Th1-type cellular responses in cured/exposed Leishmania-infected patients and hamsters against polyproteins of soluble Leishmania donovani promastigotes ranging from 89.9 to 97.1 kDa. Vaccine.  https://doi.org/10.1016/j.vaccine.2008.06.102
  67. 67.
    Kumari S, Samant M, Misra P, Khare P, Sisodia B, Shasany AK et al (2008) Th1-stimulatory polyproteins of soluble Leishmania donovani promastigotes ranging from 89.9 to 97.1 kDa offers long-lasting protection against experimental visceral leishmaniasis. Vaccine.  https://doi.org/10.1016/j.vaccine.2008.08.021
  68. 68.
    Lemesre JL, Holzmuller P, Gonçalves RB, Bourdoiseau G, Hugnet C, Cavaleyra M et al (2007) Long-lasting protection against canine visceral leishmaniasis using the LiESAp-MDP vaccine in endemic areas of France: double-blind randomised efficacy field trial. Vaccine.  https://doi.org/10.1016/j.vaccine.2007.02.083
  69. 69.
    Reed SG, Bertholet S, Coler RN, Friede M (2009) New horizons in adjuvants for vaccine development. Trends Immunol.  https://doi.org/10.1016/j.it.2008.09.006
  70. 70.
    Duthie MS, Windish HP, Fox CB, Reed SG (2011) Use of defined TLR ligands as adjuvants within human vaccines. Immunol Rev.  https://doi.org/10.1111/j.1600-065X.2010.00978.x
  71. 71.
    Stäger S, Smith DF, Kaye PM (2000) Immunization with a recombinant stage-regulated surface protein from Leishmania donovani induces protection against visceral leishmaniasis. J Immunol.  https://doi.org/10.4049/jimmunol.165.12.7064
  72. 72.
    Soong L, Duboise SM, Kima P, McMahon-Pratt D (1995) Leishmania pifanoi amastigote antigens protect mice against cutaneous leishmaniasis. Infect Immun 63(9):3559CrossRefGoogle Scholar
  73. 73.
    Martins VT, Chávez-Fumagalli MA, Costa LE, Martins AMCC, Lage PS, Lage DP et al (2013) Antigenicity and protective efficacy of a Leishmania amastigote-specific protein, member of the super-oxygenase family, against visceral leishmaniasis. PLoS Negl Trop Dis.  https://doi.org/10.1371/journal.pntd.0002148
  74. 74.
    Basu R, Bhaumik S, Basu JM, Naskar K, De T, Roy S (2005) Kinetoplastid membrane protein-11 DNA vaccination induces complete protection against both pentavalent antimonial-sensitive and -resistant strains of Leishmania donovani that correlates with inducible nitric oxide synthase activity and IL-4 generation: E. J Immunol.  https://doi.org/10.4049/jimmunol.174.11.7160
  75. 75.
    Streit JA, Recker TJ, Donelson JE, Wilson ME (2000) BCG expressing LCR1 of Leishmania chagasi induces protective immunity in susceptible mice. Exp Parasitol.  https://doi.org/10.1006/expr.1999.4459
  76. 76.
    Abdelhak S, Louzir H, Timm J, Blel L, Benlasfar Z, Lagranderie M et al (1995) Recombinant BCG expressing the leishmania surface antigen gp63 induces protective immunity against Leishmania major infection in BALB/c mice. Microbiology.  https://doi.org/10.1099/13500872-141-7-1585
  77. 77.
    Grimaldi G, Teva A, Porrozzi R, Pinto MA, Marchevsky RS, Rocha MGL et al (2014) Clinical and parasitological protection in a Leishmania infantum-macaque model vaccinated with adenovirus and the recombinant A2 antigen. PLoS Negl Trop Dis.  https://doi.org/10.1371/journal.pntd.0002853
  78. 78.
    Kushawaha PK, Gupta R, Sundar S, Sahasrabuddhe AA, Dube A (2011) Elongation Factor-2, a Th1 stimulatory protein of Leishmania donovani, generates strong IFN-γ and IL-12 response in cured Leishmania -infected patients/hamsters and protects hamsters against leishmania challenge. J Immunol.  https://doi.org/10.4049/jimmunol.1102081
  79. 79.
    Moreno J, Nieto J, Masina S, Cañavate C, Cruz I, Chicharro C et al (2007) Immunization with H1, HASPB1 and MML leishmania proteins in a vaccine trial against experimental canine leishmaniasis. Vaccine.  https://doi.org/10.1016/j.vaccine.2007.05.010
  80. 80.
    Solioz N, Blum-Tirouvanziam U, Jacquet R, Rafati S, Corradin G, Mauël J et al (1999) The protective capacities of histone H1 against experimental murine cutaneous leishmaniasis. Vaccine.  https://doi.org/10.1016/S0264-410X(99)00340-0
  81. 81.
    Baharia RK, Tandon R, Sahasrabuddhe AA, Sundar S, Dube A (2014) Nucleosomal histone proteins of L. donovani: a combination of recombinant H2A, H2B, H3 and H4 proteins were highly immunogenic and offered optimum prophylactic efficacy against Leishmania challenge in hamsters. PLoS One.  https://doi.org/10.1371/journal.pone.0097911
  82. 82.
    Hugentobler F, Yam KK, Gillard J, Mahbuba R, Olivier M, Cousineau B (2012) Immunization against Leishmania major infection using LACK- and IL-12-expressing lactococcus lactis induces delay in footpad swelling. PLoS One.  https://doi.org/10.1371/journal.pone.0030945
  83. 83.
    Tandon R, Chandra S, Baharia RK, Misra P, Das S, Rawat K et al (2018) Molecular, biochemical characterization and assessment of immunogenic potential of cofactor-independent phosphoglycerate mutase against Leishmania donovani: a step towards exploring novel vaccine candidate. Parasitology.  https://doi.org/10.1017/S0031182017001160
  84. 84.
    Mizbani A, Taheri T, Zahedifard F, Taslimi Y, Azizi H, Azadmanesh K et al (2009) Recombinant Leishmania tarentolae expressing the A2 virulence gene as a novel candidate vaccine against visceral leishmaniasis. Vaccine.  https://doi.org/10.1016/j.vaccine.2009.09.114
  85. 85.
    Shahbazi M, Zahedifard F, Taheri T, Taslimi Y, Jamshidi S, Shirian S et al (2015) Evaluation of live recombinant nonpathogenic leishmania tarentolae expressing cysteine proteinase and A2 genes as a candidate vaccine against experimental canine visceral leishmaniasis. PLoS One.  https://doi.org/10.1371/journal.pone.0132794
  86. 86.
    Yam KK, Hugentobler F, Pouliot P, Stern AM, Lalande JD, Matlashewski G et al (2011) Generation and evaluation of A2-expressing Lactococcus lactis live vaccines against Leishmania donovani in BALB/c mice. J Med Microbiol.  https://doi.org/10.1099/jmm.0.029959-0
  87. 87.
    Grimaldi G, Teva A, Dos-Santos CB, Santos FN, Pinto IDS, Fux B et al (2017) Field trial of efficacy of the Leish-tec® vaccine against canine leishmaniasis caused by Leishmania infantum in an endemic area with high transmission rates. PLoS One.  https://doi.org/10.1371/journal.pone.0185438
  88. 88.
    Spitzer N, Jardim A, Lippert D, Olafson RW (1999) Long-term protection of mice against Leishmania major with a synthetic peptide vaccine. Vaccine.  https://doi.org/10.1016/S0264-410X(98)00363-6
  89. 89.
    Tsagozis P, Karagouni E, Dotsika E (2004) Dendritic cells pulsed with peptides of gp63 induce differential protection against experimental cutaneous leishmaniasis. Int J Immunopathol Pharmacol.  https://doi.org/10.1177/039463200401700314
  90. 90.
    Rezvan H (2013) Immunogenicity of HLA-DR1 restricted peptides derived from Leishmania major gp63 using FVB/N-DR1 transgenic mouse model. Iran J Parasitol 8(2):273–279PubMedPubMedCentralGoogle Scholar
  91. 91.
    Delgado G, Parra-López CA, Vargas LE, Hoya R, Estupiñán M, Guzmán F et al (2003) Characterizing cellular immune response to kinetoplastid membrane protein-11 (KMP-11) during Leishmania (Viannia) panamensis infection using dendritic cells (DCs) as antigen presenting cells (APCs). Parasite Immunol.  https://doi.org/10.1046/j.1365-3024.2003.00626.x
  92. 92.
    Herrera-Najera C, Piña-Aguilar R, Xacur-Garcia F, Ramirez-Sierra MJ, Dumonteil E (2009) Mining the leishmania genome for novel antigens and vaccine candidates. Proteomics.  https://doi.org/10.1002/pmic.200800533
  93. 93.
    Naouar I, Boussoffara T, Chenik M, Gritli S, Ben Ahmed M, Belhadj Hmida N et al (2016) Prediction of T cell epitopes from Leishmania major potentially excreted/secreted proteins inducing granzyme B production. PLoS One.  https://doi.org/10.1371/journal.pone.0147076
  94. 94.
    Costa LE, Chávez-Fumagalli MA, Martins VT, Duarte MC, Lage DP, Lima MIS et al (2015) Phage-fused epitopes from Leishmania infantum used as immunogenic vaccines confer partial protection against Leishmania amazonensis infection. Parasitology.  https://doi.org/10.1017/S0031182015000724
  95. 95.
    Gillespie PM, Beaumier CM, Strych U, Hayward T, Hotez PJ, Bottazzi ME (2016) Status of vaccine research and development of vaccines for leishmaniasis. Vaccine.  https://doi.org/10.1016/j.vaccine.2015.12.071
  96. 96.
    Chakravarty J, Kumar S, Trivedi S, Rai VK, Singh A, Ashman JA et al (2011) A clinical trial to evaluate the safety and immunogenicity of the LEISH-F1+MPL-SE vaccine for use in the prevention of visceral leishmaniasis. Vaccine.  https://doi.org/10.1016/j.vaccine.2011.02.096
  97. 97.
    Llanos-Cuentas A, Calderón W, Cruz M, Ashman JA, Alves FP, Coler RN et al (2010) A clinical trial to evaluate the safety and immunogenicity of the LEISH-F1+MPL-SE vaccine when used in combination with sodium stibogluconate for the treatment of mucosal leishmaniasis. Vaccine.  https://doi.org/10.1016/j.vaccine.2010.08.092
  98. 98.
    Christiaansen AF, Dixit UG, Coler RN, Marie Beckmann A, Reed SG, Winokur PL et al (2017) CD11a and CD49d enhance the detection of antigen-specific T cells following human vaccination. Vaccine.  https://doi.org/10.1016/j.vaccine.2017.06.013
  99. 99.
    Coler RN, Duthie MS, Hofmeyer KA, Guderian J, Jayashankar L, Vergara J et al (2015) From mouse to man: safety, immunogenicity and efficacy of a candidate leishmaniasis vaccine LEISH-F3+GLA-SE. Clin Transl Immunol.  https://doi.org/10.1038/cti.2015.6
  100. 100.
    Parody N, Soto M, Requena JM, Álonso C (2004) Adjuvant guided polarization of the immune humoral response against a protective multicomponent antigenic protein (Q) from Leishmania infantum. A CpG + Q mix protects Balb/c mice from infection. Parasite Immunol.  https://doi.org/10.1111/j.0141-9838.2004.00711.x
  101. 101.
    Ferraro B, Morrow MP, Hutnick NA, Shin TH, Lucke CE, Weiner DB (2011) Clinical applications of DNA vaccines: current progress. Clin Infect Dis.  https://doi.org/10.1093/cid/cir334
  102. 102.
    Maspi N, Ghaffarifar F, Sharifi Z, Dalimi A, Khademi SZ (2017) DNA vaccination with a plasmid encoding LACK-TSA fusion against leishmania major infection in BALB/c mice. Malays J Pathol 39(3):267–275PubMedGoogle Scholar
  103. 103.
    Louis L, Clark M, Wise MC, Glennie N, Wong A, Broderick K et al (2019) Intradermal synthetic DNA vaccination generates leishmania -specific T cells in the skin and protection against Leishmania major. Infect Immun.  https://doi.org/10.1128/iai.00227-19
  104. 104.
    Guha R, Gupta D, Rastogi R, Vikram R, Krishnamurthy G, Bimal S et al (2013) Vaccination with leishmania hemoglobin receptor-encoding DNA protects against visceral leishmaniasis. Sci Transl Med.  https://doi.org/10.1126/scitranslmed.3006406
  105. 105.
    Osman M, Mistry A, Keding A, Gabe R, Cook E, Forrester S et al (2017) A third generation vaccine for human visceral leishmaniasis and post kala azar dermal leishmaniasis: first-in-human trial of ChAd63-KH. PLoS Negl Trop Dis.  https://doi.org/10.1371/journal.pntd.0005527
  106. 106.
    Ada GL (1991) The ideal vaccine. World J Microbiol Biotechnol.  https://doi.org/10.1007/BF00328978
  107. 107.
    Beverley PCL (2002) Immunology of vaccination. Br Med Bull.  https://doi.org/10.1093/bmb/62.1.15
  108. 108.
    Deye N, Vincent F, Michel P, Ehrmann S, Da Silva D, Piagnerelli M et al (2016) Changes in cardiac arrest patients’ TM temperature management after the 2013 “TTM” trial: results from an international survey. Ann Intensive 6(1).  https://doi.org/10.1186/s13613-015-0104-6; Al-Hussaini M, Mustafa S (2016) Adolescents’ TM knowledge and awareness of diabetes mellitus in Kuwait. Alexandria J Med 52(1):61–66.  https://doi.org/10.1016/j.ajme.2015.04.001; Pollach G, Brunkhorst F, Mipando M, Namboya F, Mndolo S, Luiz T (2016) The “first digit law” – a hypothesis on its possible impact on medicine and development aid. Med Hypotheses 97:102–106.  https://doi.org/10.1016/j.mehy.2016.10.021; Asiedu K, Kyei S, Ayobi B, Agyemang FO, Ablordeppey RK (2016) Survey of eye practitioners’ preference of diagnostic tests and treatment modalities for dry eye in Ghana. Contact Lens Anterior Eye 39(6):411–415.  https://doi.org/10.1016/j.clae.2016.08.001; Barakat KH, Gajewski MM, Tuszynski JA (2012) DNA polymerase beta (pol β) inhibitors: a comprehensive overview. Drug Discov Today 17(15–16):913–920.  https://doi.org/10.1016/j.drudis.2012.04.008; Mocan O, Dumitraşcu DL (2016) The broad spectrum of celiac disease and gluten sensitive enteropathy. Clujul Med 89(3):335–342.  https://doi.org/10.15386/cjmed-698; et al. Incorporating evidenced based practice into an international mentorship model: a pilot burn nursing experience. J Burn Care Res 2015.  https://doi.org/10.1097/BCR.0000000000000251
  109. 109.
    Nascimento IP, Leite LCC (2012) Recombinant vaccines and the development of new vaccine strategies. Braz J Med Biol Res.  https://doi.org/10.1590/S0100-879X2012007500142
  110. 110.
    Donnelly JJ, Wahren B, Liu MA (2005) DNA vaccines: progress and challenges. J Immunol.  https://doi.org/10.4049/jimmunol.175.2.633
  111. 111.
    Skibinski DAG, Baudner BC, Singh M, O’hagan DT (2011) Combination vaccines. J Glob Infect Dis.  https://doi.org/10.4103/0974-777X.77298
  112. 112.
    Huber VC (2014) Influenza vaccines: from whole virus preparations to recombinant protein technology. Expert Rev Vaccines.  https://doi.org/10.1586/14760584.2014.852476
  113. 113.
    Sahdev P, Ochyl LJ, Moon JJ (2014) Biomaterials for nanoparticle vaccine delivery systems. Pharm Res.  https://doi.org/10.1007/s11095-014-1419-y
  114. 114.
    Shao K, Singha S, Clemente-Casares X, Tsai S, Yang Y, Santamaria P (2015) Nanoparticle-based immunotherapy for cancer. ACS Nano.  https://doi.org/10.1021/nn5062029
  115. 115.
    Singh A, Peppas NA (2014) Hydrogels and scaffolds for immunomodulation. Adv Mater.  https://doi.org/10.1002/adma.201402105
  116. 116.
    Quinn HL, Kearney MC, Courtenay AJ, McCrudden MT, Donnelly RF (2014) The role of microneedles for drug and vaccine delivery. Expert Opin Drug Deliv.  https://doi.org/10.1517/17425247.2014.938635
  117. 117.
    Indermun S, Luttge R, Choonara YE, Kumar P, Du Toit LC, Modi G et al (2014) Current advances in the fabrication of microneedles for transdermal delivery. J Control Release.  https://doi.org/10.1016/j.jconrel.2014.04.052.
  118. 118.
    Tsoras AN, Champion JA (2019) Protein and peptide biomaterials for engineered subunit vaccines and immunotherapeutic applications. Annu Rev Chem Biomol Eng.  https://doi.org/10.1146/annurev-chembioeng-060718-030347
  119. 119.
    Bookstaver ML, Tsai SJ, Bromberg JS, Jewell CM (2018) Improving vaccine and immunotherapy design using biomaterials. Trends Immunol.  https://doi.org/10.1016/j.it.2017.10.002
  120. 120.
    Oelke M, Maus MV, Didiano D, June CH, Mackensen A, Schneck JP (2003) Ex vivo induction and expansion of antigen-specific cytotoxic T cells by HLA-Ig-coated artificial antigen-presenting cells. Nat Med.  https://doi.org/10.1038/nm869
  121. 121.
    Sunshine JC, Perica K, Schneck JP, Green JJ (2014) Particle shape dependence of CD8+ T cell activation by artificial antigen presenting cells. Biomaterials.  https://doi.org/10.1016/j.biomaterials.2013.09.050
  122. 122.
    Kumar S, Anselmo AC, Banerjee A, Zakrewsky M, Mitragotri S (2015) Shape and size-dependent immune response to antigen-carrying nanoparticles. J Control Release.  https://doi.org/10.1016/j.jconrel.2015.09.069.
  123. 123.
    Hardy CL, LeMasurier JS, Mohamud R, Yao J, Xiang SD, Rolland JM et al (2013) Differential uptake of nanoparticles and microparticles by pulmonary APC subsets induces discrete immunological imprints. J Immunol.  https://doi.org/10.4049/jimmunol.1203131
  124. 124.
    Shahbazi MA, Fernández TD, Mäkilä EM, Le Guével X, Mayorga C, Kaasalainen MH et al (2014) Surface chemistry dependent immunostimulative potential of porous silicon nanoplatforms. Biomaterials.  https://doi.org/10.1016/j.biomaterials.2014.07.050
  125. 125.
    Moyano DF, Goldsmith M, Solfiell DJ, Landesman-Milo D, Miranda OR, Peer D et al (2012) Nanoparticle hydrophobicity dictates immune response. J Am Chem Soc.  https://doi.org/10.1021/ja2108905.
  126. 126.
    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.  https://doi.org/10.1016/j.vaccine.2012.01.070
  127. 127.
    Sharma A, Sharma US (1997) Liposomes in drug delivery: progress and limitations. Int J Pharm.  https://doi.org/10.1016/S0378-5173(97)00135-X.
  128. 128.
    Rao M, Alving CR (2000) Delivery of lipids and liposomal proteins to the cytoplasm and Golgi of antigen-presenting cells. Adv Drug Deliv Rev.  https://doi.org/10.1016/S0169-409X(99)00064-2
  129. 129.
    Kersten GFA, Crommelin DJA (1995) Liposomes and ISCOMS as vaccine formulations. BBA Rev Biomembr.  https://doi.org/10.1016/0304-4157(95)00002-9
  130. 130.
    Schmidt ST, Foged C, Korsholm KS, Rades T, Christensen D (2016) Liposome-based adjuvants for subunit vaccines: formulation strategies for subunit antigens and immunostimulators. Pharmaceutics.  https://doi.org/10.3390/pharmaceutics8010007
  131. 131.
    Carstens MG, Camps MGM, Henriksen-Lacey M, Franken K, Ottenhoff THM, Perrie Y et al (2011) Effect of vesicle size on tissue localization and immunogenicity of liposomal DNA vaccines. Vaccine.  https://doi.org/10.1016/j.vaccine.2011.04.081
  132. 132.
    Oussoren C, Zuidema J, Crommelin DJA, Storm G (1997) Lymphatic uptake and biodistribution of liposomes after subcutaneous injection. II. Influence of liposomal size, lipid composition and lipid dose. Biochim Biophys Acta Biomembr.  https://doi.org/10.1016/S0005-2736(97)00122-3
  133. 133.
    McLennan DN, Porter CJH, Charman SA (2005) Subcutaneous drug delivery and the role of the lymphatics. Drug Discov Today Technol.  https://doi.org/10.1016/j.ddtec.2005.05.006
  134. 134.
    Bachmann MF, Jennings GT (2010) Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol.  https://doi.org/10.1038/nri2868
  135. 135.
    Sharma SK, Dube A, Nadeem A, Khan S, Saleem I, Garg R et al (2006) Non PC liposome entrapped promastigote antigens elicit parasite specific CD8+ and CD4+ T-cell immune response and protect hamsters against visceral leishmaniasis. Vaccine.  https://doi.org/10.1016/j.vaccine.2005.10.025
  136. 136.
    Bhowmick S, Ravindran R, Ali N (2008) Gp63 in stable cationic liposomes confers sustained vaccine immunity to susceptible BALB/c mice infected with Leishmania donovani. Infect Immun.  https://doi.org/10.1128/IAI.00611-07
  137. 137.
    Mazumder S, Maji M, Ali N (2011) Potentiating effects of MPL on DSPC bearing cationic liposomes promote recombinant GP63 vaccine efficacy: high immunogenicity and protection. PLoS Negl Trop Dis.  https://doi.org/10.1371/journal.pntd.0001429
  138. 138.
    Badiee A, Jaafari MR, Khamesipour A, Samiei A, Soroush D, Kheiri MT et al (2009) Enhancement of immune response and protection in BALB/c mice immunized with liposomal recombinant major surface glycoprotein of Leishmania (rgp63): the role of bilayer composition. Colloids Surfaces B Biointerfaces.  https://doi.org/10.1016/j.colsurfb.2009.06.025
  139. 139.
    Badiee A, Khamesipour A, Samiei A, Soroush D, Shargh VH, Kheiri MT et al (2012) The role of liposome size on the type of immune response induced in BALB/c mice against leishmaniasis: rgp63 as a model antigen. Exp Parasitol.  https://doi.org/10.1016/j.exppara.2012.09.001
  140. 140.
    Afrin F, Ali N (1997) Adjuvanticity and protective immunity elicited by Leishmania donovani antigens encapsulated in positively charged liposomes. Infect ImmunGoogle Scholar
  141. 141.
    Afrin F, Anam K, Ali N (2000) Induction of partial protection against Leishmania donovani by promastigote antigens in negatively charged liposomes. J Parasitol.  https://doi.org/10.2307/3284956
  142. 142.
    Afrin F, Rajesh R, Anam K, Gopinath M, Pal S, Ali N (2002) Characterization of Leishmania donovani antigens encapsulated in liposomes that induce protective immunity in BALB/c mice. Infect Immun.  https://doi.org/10.1128/IAI.70.12.6697-6706.2002
  143. 143.
    Badiee A, Jaafari MR, Khamesipour A, Samiei A, Soroush D, Kheiri MT et al (2009) The role of liposome charge on immune response generated in BALB/c mice immunized with recombinant major surface glycoprotein of Leishmania (rgp63). Exp Parasitol.  https://doi.org/10.1016/j.exppara.2008.12.015
  144. 144.
    Badiee A, Jaafari MR, Khamesipour A (2007) Leishmania major: immune response in BALB/c mice immunized with stress-inducible protein 1 encapsulated in liposomes. Exp Parasitol.  https://doi.org/10.1016/j.exppara.2006.07.002
  145. 145.
    Badiee A, Jaafari MR, Samiei A, Soroush D, Khamesipour A (2008) Coencapsulation of CpG oligodeoxynucleotides with recombinant Leishmania major stress-inducible protein 1 in liposome enhances immune response and protection against leishmaniasis in immunized BALB/c mice. Clin Vaccine Immunol.  https://doi.org/10.1128/CVI.00413-07
  146. 146.
    Heravi Shargh V, Jaafari MR, Khamesipour A, Jalali SA, Firouzmand H, Abbasi A et al (2012) Cationic liposomes containing soluble leishmania antigens (SLA) plus CpG ODNs induce protection against murine model of leishmaniasis. Parasitol Res.  https://doi.org/10.1007/s00436-011-2806-5
  147. 147.
    Sabur A, Bhowmick S, Chhajer R, Ejazi SA, Didwania N, Asad M et al (2018) Liposomal elongation factor-1α triggers effector CD4 and CD8 T cells for induction of long-lasting protective immunity against visceral leishmaniasis. Front Immunol.  https://doi.org/10.3389/fimmu.2018.00018
  148. 148.
    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.  https://doi.org/10.1645/ge-356r1
  149. 149.
    Antimisiaris SG, Jayasekera P, Gregoriadis G (1993) Liposomes as vaccine carriers. Incorporation of soluble and particulate antigens in giant vesicles. J Immunol Methods.  https://doi.org/10.1016/0022-1759(93)90368-H
  150. 150.
    Moghimi SM, Patel HM (1988) Tissue specific opsonins for phagocytic cells and their different affinity for cholesterol-rich liposomes. FEBS Lett.  https://doi.org/10.1016/0014-5793(88)81372-3
  151. 151.
    Kojima N, Ishii M, Kawauchi Y, Takagi H (2013) Oligomannose-coated liposome as a novel adjuvant for the induction of cellular immune responses to control disease status. Biomed Res Int.  https://doi.org/10.1155/2013/562924
  152. 152.
    Shimizu Y, Takagi H, Nakayama T, Yamakami K, Tadakuma T, Yokoyama N et al (2007) Intraperitoneal immunization with oligomannose-coated liposome-entrapped soluble leishmanial antigen induces antigen-specific T-helper type immune response in BALB/c mice through uptake by peritoneal macrophages. Parasite Immunol.  https://doi.org/10.1111/j.1365-3024.2007.00937.x
  153. 153.
    Almeida JD, Edwards DC, Brand CM, Heath TD (1975) Formation of virosomes from influenza subunits and liposomes. Lancet.  https://doi.org/10.1016/S0140-6736(75)92130-3
  154. 154.
    Stegmann T, Morselt HW, Booy FP, van Breemen JF, Scherphof G, Wilschut J (1987) Functional reconstitution of influenza virus envelopes. EMBO J.  https://doi.org/10.1002/j.1460-2075.1987.tb02556.x
  155. 155.
    Bron R, Wahlberg JM, Garoff H, Wilschut J (1993) Membrane fusion of Semliki Forest virus in a model system: correlation between fusion kinetics and structural changes in the envelope glycoprotein. EMBO J.  https://doi.org/10.1002/j.1460-2075.1993.tb05703.x
  156. 156.
    Bron R, Ortiz A, Dijkstra J, Stegmann T, Wilschut J (1993) [23] Preparation, properties, and applications of reconstituted influenza virus envelopes (virosomes). Methods Enzymol.  https://doi.org/10.1016/0076-6879(93)20091-G
  157. 157.
    Gunther-Ausborn S, Schoen P, Bartoldus I, Wilschut J, Stegmann T (2000) Role of hemagglutinin surface density in the initial stages of influenza virus fusion: lack of evidence for cooperativity. J Virol.  https://doi.org/10.1128/jvi.74.6.2714-2720.2000
  158. 158.
    Homhuan A, Prakongpan S, Poomvises P, Maas RA, Crommelin DJA, Kersten GFA et al (2004) Virosome and ISCOM vaccines against Newcastle disease: preparation, characterization and immunogenicity. Eur J Pharm Sci.  https://doi.org/10.1016/j.ejps.2004.05.005
  159. 159.
    Cecílio P, Pérez-Cabezas B, Fernández L, Moreno J, Carrillo E, Requena JM et al (2017) Pre-clinical antigenicity studies of an innovative multivalent vaccine for human visceral leishmaniasis. PLoS Negl Trop Dis.  https://doi.org/10.1371/journal.pntd.0005951
  160. 160.
    Liu X, Siegrist S, Amacker M, Zurbriggen R, Pluschke G, Seeberger PH (2006) Enhancement of the immunogenicity of synthetic carbohydrates by conjugation to virosomes: a leishmaniasis vaccine candidate. ACS Chem Biol.  https://doi.org/10.1021/cb600086b
  161. 161.
    Yoshida H, Lehr CM, Kok W, Junginger HE, Verhoef JC, Bouwstra JA (1992) Niosomes for oral delivery of peptide drugs. J Control Release.  https://doi.org/10.1016/0168-3659(92)90016-K
  162. 162.
    Pardakhty A, Shakibaie M, Daneshvar H, Khamesipour A, Mohammadi-Khorsand T, Forootanfar H (2012) Preparation and evaluation of niosomes containing autoclaved Leishmania major: a preliminary study. J Microencapsul.  https://doi.org/10.3109/02652048.2011.642016
  163. 163.
    Lezama-Dávila CM (1999) Vaccination of C57BL/10 mice against cutaneous leishmaniasis. Use of purified gp63 encapsulated into niosomes surfactants vesicles: a novel approach. Mem Inst Oswaldo Cruz.  https://doi.org/10.1590/S0074-02761999000100014
  164. 164.
    Mehnert W, Mäder K (2012) Solid lipid nanoparticles: production, characterization and applications. Adv Drug Deliv Rev.  https://doi.org/10.1016/j.addr.2012.09.021.
  165. 165.
    Souto EB, Doktorovova S, Boonme P (2011) Lipid-based colloidal systems (nanoparticles, microemulsions) for drug delivery to the skin: materials and end-product formulations. J Drug Deliv Sci Technol.  https://doi.org/10.1016/S1773-2247(11)50005-X
  166. 166.
    Bond ML, Craparo EF (2010) Solid lipid nanoparticles for applications in gene therapy: a review of the state of the art. Expert Opin Drug Deliv.  https://doi.org/10.1517/17425240903362410
  167. 167.
    Vighi E, Ruozi B, Montanari M, Battini R, Leo E (2007) Re-dispersible cationic solid lipid nanoparticles (SLNs) freeze-dried without cryoprotectors: characterization and ability to bind the pEGFP-plasmid. Eur J Pharm Biopharm.  https://doi.org/10.1016/j.ejpb.2007.02.006
  168. 168.
    Xue HY, Wong HL (2011) Tailoring nanostructured solid-lipid carriers for time-controlled intracellular siRNA kinetics to sustain RNAi-mediated chemosensitization. Biomaterials.  https://doi.org/10.1016/j.biomaterials.2010.12.029
  169. 169.
    del Pozo-Rodríguez A, Delgado D, Solinís MÁ, Pedraz JL, Echevarría E, Rodríguez JM et al (2010) Solid lipid nanoparticles as potential tools for gene therapy: in vivo protein expression after intravenous administration. Int J Pharm.  https://doi.org/10.1016/j.ijpharm.2009.10.020
  170. 170.
    Doroud D, Vatanara AV, Zahedifard F, Gholami E, Vahabpour R, Najafabadi AR et al (2010) Cationic solid lipid nanoparticles loaded by cysteine proteinase genes as a novel anti-leishmaniasis DNA vaccine delivery system: characterization and in vitro evaluations. J Pharm Pharm Sci.  https://doi.org/10.18433/j3r30t
  171. 171.
    Doroud D, Zahedifard F, Vatanara A, Najafabadi AR, Taslimi Y, Vahabpour R et al (2011) Delivery of a cocktail DNA vaccine encoding cysteine proteinases type I, II and III with solid lipid nanoparticles potentiate protective immunity against Leishmania major infection. J Control Release.  https://doi.org/10.1016/j.jconrel.2011.04.011
  172. 172.
    Saljoughian N, Zahedifard F, Doroud D, Doustdari F, Vasei M, Papadopoulou B et al (2013) Cationic solid-lipid nanoparticles are as efficient as electroporation in DNA vaccination against visceral leishmaniasis in mice. Parasite Immunol.  https://doi.org/10.1111/pim.12042
  173. 173.
    Shahbazi M, Zahedifard F, Saljoughian N, Doroud D, Jamshidi S, Mahdavi N et al (2015) Immunological comparison of DNA vaccination using two delivery systems against canine leishmaniasis. Vet Parasitol.  https://doi.org/10.1016/j.vetpar.2015.07.005
  174. 174.
    Danhier F, Ansorena E, Silva JM, Coco R, Le Breton A, Préat V (2012) PLGA-based nanoparticles: an overview of biomedical applications. J Control Release.  https://doi.org/10.1016/j.jconrel.2012.01.043
  175. 175.
    Margaroni M, Agallou M, Athanasiou E, Kammona O, Kiparissides C, Gaitanaki C et al (2017) Vaccination with poly(D,L-lactide-co-glycolide) nanoparticles loaded with soluble leishmania antigens and modified with a TNFα-mimicking peptide or monophosphoryl lipid aconfers protection against experimental visceral leishmaniasis. Int J Nanomedicine.  https://doi.org/10.2147/IJN.S141069
  176. 176.
    Abamor E, Allahverdiyev A, Tosyali O, Bagirova M, Acar T, Mustafaeva Z et al (2019) Evaluation of in vitro and in vivo immunostimulatory activities of poly (lactic-co-glycolic acid) nanoparticles loaded with soluble and autoclaved Leishmania infantum antigens: a novel vaccine candidate against visceral leishmaniasis. Asian Pac J Trop Med.  https://doi.org/10.4103/1995-7645.262564
  177. 177.
    Tafaghodi M, Eskandari M, Kharazizadeh M, Khamesipour A, Jaafari MR (2010) Immunization against leishmaniasis by PLGA nanospheres loaded with an experimental autoclaved Leishmania major (ALM) and Quillaja saponins. Trop BiomedGoogle Scholar
  178. 178.
    Agallou M, Margaroni M, Athanasiou E, Toubanaki DK, Kontonikola K, Karidi K et al (2017) Identification of BALB/c immune markers correlated with a partial protection to Leishmania infantum after vaccination with a rationally designed multi-epitope cysteine protease a peptide-based nanovaccine. PLoS Negl Trop Dis.  https://doi.org/10.1371/journal.pntd.0005311
  179. 179.
    Athanasiou E, Agallou M, Tastsoglou S, Kammona O, Hatzigeorgiou A, Kiparissides C et al (2017) A poly(lactic-co-glycolic) acid nanovaccine based on chimeric peptides from different Leishmania infantum proteins induces dendritic cells maturation and promotes peptide-specific IFNγ-producing CD8+ T cells essential for the protection against experiment. Front Immunol.  https://doi.org/10.3389/fimmu.2017.00684.
  180. 180.
    Lövgren Bengtsson K, Morein B, Osterhaus AD (2011) ISCOM technology-based matrix M™ adjuvant: success in future vaccines relies on formulation. Expert Rev Vaccines.  https://doi.org/10.1586/erv.11.25
  181. 181.
    Morelli AB, Becher D, Koernig S, Silva A, Drane D, Maraskovsky E (2012) ISCOMATRIX: a novel adjuvant for use in prophylactic and therapeutic vaccines against infectious diseases. J Med Microbiol.  https://doi.org/10.1099/jmm.0.040857-0
  182. 182.
    Papadopoulou G, Karagouni E, Dotsika E (1998) ISCOMs vaccine against experimental leishmaniasis. Vaccine.  https://doi.org/10.1016/S0264-410X(97)00308-3
  183. 183.
    Mehravaran A, Jaafari MR, Jalali SA, Khamesipour A, Ranjbar R, Hojatizade M et al (2016) The role of ISCOMATRIX bilayer composition to induce a cell mediated immunity and protection against leishmaniasis in BALB/c mice. Iran J Basic Med Sci.  https://doi.org/10.22038/ijbms.2016.6542.
  184. 184.
    Draget KI, Taylor C (2011) Chemical, physical and biological properties of alginates and their biomedical implications. Food Hydrocoll.  https://doi.org/10.1016/j.foodhyd.2009.10.007
  185. 185.
    Downs EC, Robertson NE, Riss TL, Plunkett ML (1992) Calcium alginate beads as a slow-release system for delivering angiogenic molecules in vivo and in vitro. J Cell Physiol.  https://doi.org/10.1002/jcp.1041520225
  186. 186.
    Tafaghodi M, Eskandari M, Khamesipour A, Jaafaric MR (2016) Immunization against cutaneous Leishmaniasis by alginate microspheres loaded with autoclaved Leishmania major (ALM) and Quillaja saponins. Iran J Pharm Res.  https://doi.org/10.22037/ijpr.2016.1832.
  187. 187.
    Tafaghodi M, Eskandari M, Khamesipour A, Jaafari MR (2011) Alginate microspheres encapsulated with autoclaved Leishmania major (ALM) and CpG-ODN induced partial protection and enhanced immune response against murine model of leishmaniasis. Exp Parasitol.  https://doi.org/10.1016/j.exppara.2011.07.007
  188. 188.
    Beaumier CM, Gillespie PM, Strych U, Hayward T, Hotez PJ, Bottazzi ME (2016) Status of vaccine research and development of vaccines for Chagas disease. Vaccine.  https://doi.org/10.1016/j.vaccine.2016.03.074
  189. 189.
    Ye Z, Li Z, Jin H, Qian Q (2016) Therapeutic cancer vaccines. Adv Exp Med Biol.  https://doi.org/10.1007/978-94-017-7555-7_3
  190. 190.
    Bachmann MF, Dyer MR (2004) Therapeutic vaccination for chronic diseases: a new class of drugs in sight. Nat Rev Drug Discov.  https://doi.org/10.1038/nrd1284
  191. 191.
    Gröschel MI, Prabowo SA, Cardona PJ, Stanford JL, Van der Werf TS (2014) Therapeutic vaccines for tuberculosis-a systematic review. Vaccine.  https://doi.org/10.1016/j.vaccine.2014.03.047
  192. 192.
    Kim TJ, Jin HT, Hur SY, Yang HG, Seo YB, Hong SR et al (2014) Clearance of persistent HPV infection and cervical lesion by therapeutic DNA vaccine in CIN3 patients. Nat Commun.  https://doi.org/10.1038/ncomms6317
  193. 193.
    Mukhopadhyay S, Bhattacharyya S, Majhi R, De T, Naskar K, Majumdar S et al (2000) Use of an attenuated leishmanial parasite as an immunoprophylactic and immunotherapeutic agent against murine visceral leishmaniasis. Clin Diagn Lab Immunol.  https://doi.org/10.1128/CDLI.7.2.233-240.2000
  194. 194.
    Datta S, Roy S, Manna M (2015) Therapy with radio-attenuated vaccine in experimental murine visceral leishmaniasis showed enhanced T cell and inducible nitric oxide synthase levels, suppressed tumor growth factor-beta production with higher expression of some signaling molecules. Braz J Infect Dis.  https://doi.org/10.1016/j.bjid.2014.10.009
  195. 195.
    Borja-Cabrera GP, Mendes AC, Paraguai De Souza E, Okada LYH, Trivellato FADA, Kawasaki JKA et al (2004) Effective immunotherapy against canine visceral leishmaniasis with the FML-vaccine. Vaccine.  https://doi.org/10.1016/j.vaccine.2003.11.039
  196. 196.
    Musa AM, Khalil EAG, Mahgoub FAE, Elgawi SHH, Modabber F, Elkadaru AEMY et al (2008) Immunochemotherapy of persistent post-kala-azar dermal leishmaniasis: a novel approach to treatment. Trans R Soc Trop Med Hyg.  https://doi.org/10.1016/j.trstmh.2007.08.006
  197. 197.
    Ghosh M, Pal C, Ray M, Maitra S, Mandal L, Bandyopadhyay S (2003) Dendritic cell-based immunotherapy combined with antimony-based chemotherapy cures established murine visceral leishmaniasis. J Immunol.  https://doi.org/10.4049/jimmunol.170.11.5625
  198. 198.
    Miret J, Nascimento E, Sampaio W, França JC, Fujiwara RT, Vale A et al (2008) Evaluation of an immunochemotherapeutic protocol constituted of N-methyl meglumine antimoniate (Glucantime®) and the recombinant Leish-110f® + MPL-SE® vaccine to treat canine visceral leishmaniasis. Vaccine.  https://doi.org/10.1016/j.vaccine.2008.01.026
  199. 199.
    Trigo J, Abbehusen M, Netto EM, Nakatani M, Pedral-Sampaio G, de Jesus RS et al (2010) Treatment of canine visceral leishmaniasis by the vaccine Leish-111f + MPL-SE. Vaccine.  https://doi.org/10.1016/j.vaccine.2010.02.089
  200. 200.
    Seifert K, Juhls C, Salguero FJ, Croft SL (2015) Sequential chemoimmunotherapy of experimental visceral leishmaniasis using a single low dose of liposomal amphotericin B and a novel DNA vaccine candidate. Antimicrob Agents Chemother.  https://doi.org/10.1128/AAC.00273-15
  201. 201.
    Bhowmick S, Ravindran R, Ali N (2007) Leishmanial antigens in liposomes promote protective immunity and provide immunotherapy against visceral leishmaniasis via polarized Th1 response. Vaccine.  https://doi.org/10.1016/j.vaccine.2007.05.042
  202. 202.
    Maroof A, Brown N, Smith B, Hodgkinson MR, Maxwell A, Losch FO et al (2012) Therapeutic vaccination with recombinant adenovirus reduces splenic parasite burden in experimental visceral leishmaniasis. J Infect Dis.  https://doi.org/10.1093/infdis/jir842
  203. 203.
    Xie Z, Wroblewska L, Prochazka L, Weiss R, Benenson Y (2011) Multi-input RNAi-based logic circuit for identification of specific cancer cells. Science 80.  https://doi.org/10.1126/science.1205527
  204. 204.
    Kemmer C, Gitzinger M, Daoud-El Baba M, Djonov V, Stelling J, Fussenegger M (2010) Self-sufficient control of urate homeostasis in mice by a synthetic circuit. Nat Biotechnol.  https://doi.org/10.1038/nbt.1617
  205. 205.
    Ye H, Daoud-El Baba M, Peng RW, Fussenegger M (2011) A synthetic optogenetic transcription device enhances blood-glucose homeostasis in mice. Science 80.  https://doi.org/10.1126/science.1203535
  206. 206.
    Ye H, Charpin-El Hamri G, Zwicky K, Christen M, Folcher M, Fussenegger M (2013) Pharmaceutically controlled designer circuit for the treatment of the metabolic syndrome. Proc Natl Acad Sci U S A.  https://doi.org/10.1073/pnas.1216801110
  207. 207.
    Rössger K, El Hamri GC, Fussenegger M (2013) Reward-based hypertension control by a synthetic brain-dopamine interface. Proc Natl Acad Sci U S A.  https://doi.org/10.1073/pnas.1312414110
  208. 208.
    Ausländer D, Eggerschwiler B, Kemmer C, Geering B, Ausländer S, Fussenegger M (2014) A designer cell-based histamine-specific human allergy profiler. Nat Commun.  https://doi.org/10.1038/ncomms5408

Copyright information

© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  • Pragya Misra
    • 1
  • Shailza Singh
    • 1
  1. 1.National Centre for Cell SciencePuneIndia

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