Whole Pichia pastoris yeast expressing measles virus nucleoprotein as a production and delivery system to multimerize Plasmodium antigens

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Jacob, Daria ^a,b   Ruffie, Claude ^a,b   Dubois, Myriam ^a,b   Combredet, Chantal ^a,b   Amino, Rogerio ^a   Formaglio, Pauline ^a   Gorgette, Olivier ^a,b   Pehau Arnaudet, Gérard ^a,b   Guery, Charline ^a,b   Puijalon, Odile ^a,b   Barale, Jean Christophe ^a,b   Ménard, Robert ^a   Tangy, Frédéric ^a,b   Sala, Monica ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCUMSPOROZOITE PROTEIN; RIBONUCLEOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INCLUSION; CONTROLLED STUDY; DRUG EFFICACY; DRUG MIXTURE; FEMALE; GENE EXPRESSION SYSTEM; IN VIVO STUDY; LONG TERM SURVIVAL; MEASLES VIRUS; MOUSE; NONHUMAN; PARASITEMIA; PICHIA PASTORIS; PLASMODIUM BERGHEI; PLASMODIUM BERGHEI INFECTION; PROTEIN LOCALIZATION; PROTEIN MULTIMERIZATION; SPOROZOITE; SURVIVAL TIME; VACCINE PRODUCTION; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; BIOREACTORS; DRUG DELIVERY SYSTEMS; DRUG DISCOVERY; FLUORESCENT ANTIBODY TECHNIQUE; MALARIA VACCINES; MEASLES VIRUS; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON; NUCLEOPROTEINS; PICHIA; PLASMODIUM BERGHEI; PROTOZOAN PROTEINS; RIBONUCLEOPROTEINS;

EID: 84900315543     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086658     Document Type: Article

References (69)

1. FDA website. Common Ingredients in U.S. Licensed Vaccines. Vaccines, Blood & Biologics. Available:http://www.fda.gov/BiologicsBloodVaccines/ SafetyAvailability/VaccineSafety/ucm187810.htm. Accessed 2013 December 13.
2. Ribeiro CM, Schijns VE (2010) Immunology of vaccine adjuvants. Methods Mol Biol 626: 1-14.
3. Bagnoli F, Baudner B, Mishra RP, Bartolini E, Fiaschi L, et al. (2011) Designing the next generation of vaccines for global public health. OMICS 15: 545-566.
4. Tomljenovic L (2011) Aluminum and Alzheimer's disease: after a century of controversy, is there a plausible link? J Alzheimers Dis 23: 567-598.
5. Francois G, Duclos P, Margolis H, Lavanchy D, Siegrist CA, et al. (2005) Vaccine safety controversies and the future of vaccination programs. Pediatr Infect Dis J 24: 953-961. (Pubitemid 41689596)
6. Piyasirisilp S, Hemachudha T (2002) Neurological adverse events associated with vaccination. Curr Opin Neurol 15: 333-338. (Pubitemid 34596899)
7. Miller E, Andrews N, Stellitano L, Stowe J, Winstone AM, et al. (2013) Risk of narcolepsy in children and young people receiving AS03 adjuvanted pandemic A/H1N1 2009 influenza vaccine: retrospective analysis. BMJ 346: f794.
8. Lacerda CM, Martins EM, de Resende MA, de Andrade AS (2011) Gamma radiation effects on Sporothrix schenckii yeast cells. Mycopathologia 171: 395-401.
9. Stubbs AC, Martin KS, Coeshott C, Skaates SV, Kuritzkes DR, et al. (2001) Whole recombinant yeast vaccine activates dendritic cells and elicits protective cell-mediated immunity. Nat Med 7: 625-629. (Pubitemid 32448332)
10. Roohvand F, Kossari N (2012) Advances in hepatitis C virus vaccines, part two: advances in hepatitis C virus vaccine formulations and modalities. Expert Opin Ther Pat 22: 391-415.
11. Bian G, Cheng Y, Wang Z, Hu Y, Zhang X, et al. (2009) Whole recombinant Hansenula polymorpha expressing hepatitis B virus surface antigen (yeast-HBsAg) induces potent HBsAg-specific Th1 and Th2 immune responses. Vaccine 28: 187-194.
12. Saiki M, Sakai K, Saiki S, Kitagawa Y, Nakanishi M, et al. (2005) Induction of humoral responses specific for paraneoplastic cerebellar degeneration-associated antigen by whole recombinant yeast immunization. J Autoimmun 24: 203-208. (Pubitemid 40545882)
13. Liu M, Clemons KV, Bigos M, Medovarska I, Brummer E, et al. (2011) Immune responses induced by heat killed Saccharomyces cerevisiae: a vaccine against fungal infection. Vaccine 29: 1745-1753.
14. Arnold M, Durairaj V, Mundt E, Schulze K, Breunig KD, et al. (2012) Protective vaccination against infectious bursal disease virus with whole recombinant Kluyveromyces lactis yeast expressing the viral VP2 subunit. PLoS One 7: e42870.
15. Haller AA, Lauer GM, King TH, Kemmler C, Fiolkoski V, et al. (2007) Whole recombinant yeast-based immunotherapy induces potent T cell responses targeting HCV NS3 and Core proteins. Vaccine 25: 1452-1463. (Pubitemid 46074294)
16. Bui MR, Hodson V, King T, Leopold D, Dai S, et al. (2010) Mutation-specific control of BCR-ABL T315I positive leukemia with a recombinant yeast-based therapeutic vaccine in a murine model. Vaccine 28: 6028-6035.
17. Neumann AK, Jacobson K (2010) A novel pseudopodial component of the dendritic cell anti-fungal response: the fungipod. PLoS Pathog 6: e1000760.
18. Goodridge HS, Reyes CN, Becker CA, Katsumoto TR, Ma J, et al. (2011) Activation of the innate immune receptor Dectin-1 upon formation of a 'phagocytic synapse'. Nature 472: 471-475.
19. Bazan SB, Geginat G, Breinig T, Schmitt MJ, Breinig F (2011) Uptake of various yeast genera by antigen-presenting cells and influence of subcellular antigen localization on the activation of ovalbumin-specific CD8 T lymphocytes. Vaccine 29: 8165-8173.
20. Arias MA, Loxley A, Eatmon C, Van Roey G, Fairhurst D, et al. (2011) Carnauba wax nanoparticles enhance strong systemic and mucosal cellular and humoral immune responses to HIV-gp140 antigen. Vaccine 29: 1258-1269.
21. Singh M, Chakrapani A, O'Hagan D (2007) Nanoparticles and microparticles as vaccine-delivery systems. Expert Rev Vaccines 6: 797-808. (Pubitemid 47607854)
22. Xiang SD, Scholzen A, Minigo G, David C, Apostolopoulos V, et al. (2006) Pathogen recognition and development of particulate vaccines: does size matter? Methods 40: 1-9. (Pubitemid 44415493)
23. Storni T, Kundig TM, Senti G, Johansen P (2005) Immunity in response to particulate antigen-delivery systems. Adv Drug Deliv Rev 57: 333-355. (Pubitemid 39555501)
24. Casares S, Brumeanu TD, Richie TL (2010) The RTS,S malaria vaccine. Vaccine 28: 4880-4894.
25. Gonzalez MC, Kostrzak A, Guetard D, Pniewski T, Sala M (2009) HIV-1 derived peptides fused to HBsAg affect its immunogenicity. Virus Res 146: 107-114.
26. Vietheer PT, Boo I, Drummer HE, Netter HJ (2007) Immunizations with chimeric hepatitis B virus-like particles to induce potential anti-hepatitis C virus neutralizing antibodies. Antivir Ther 12: 477-487. (Pubitemid 47041146)
27. Jariyapong P, Xing L, van Houten NE, Li TC, Weerachatyanukul W, et al. (2013) Chimeric hepatitis E virus-like particle as a carrier for oral-delivery. Vaccine 31: 417-424.
28. Griffin DE, Lin WH, Pan CH (2012) Measles virus, immune control, and persistence. FEMS Microbiol Rev 36: 649-662.
29. Griffin DE (2001) Measles virus. In: Knipe DM, Howley, P.M., editor. Fields Virology. Philadelphia: Lippincott Williams & Wilkins Publications. 1401-1441.
30. Bourhis JM, Canard B, Longhi S (2006) Structural disorder within the replicative complex of measles virus: functional implications. Virology 344: 94-110. (Pubitemid 41818949)
31. Warnes A, Fooks AR, Dowsett AB, Wilkinson GW, Stephenson JR (1995) Expression of the measles virus nucleoprotein gene in Escherichia coli and assembly of nucleocapsid-like structures. Gene 160: 173-178.
32. Slibinskas R, Samuel D, Gedvilaite A, Staniulis J, Sasnauskas K (2004) Synthesis of the measles virus nucleoprotein in yeast Pichia pastoris and Saccharomyces cerevisiae. J Biotechnol 107: 115-124. (Pubitemid 38058673)
33. Jensen MR, Communie G, Ribeiro EA, Jr., Martinez N, Desfosses A, et al. (2011) Intrinsic disorder in measles virus nucleocapsids. Proc Natl Acad Sci U S A 108: 9839-9844.
34. De Schutter K, Lin YC, Tiels P, Van Hecke A, Glinka S, et al. (2009) Genome sequence of the recombinant protein production host Pichia pastoris. Nat Biotechnol 27: 561-566.
35. Cregg JM, Vedvick TS, Raschke WC (1993) Recent advances in the expression of foreign genes in Pichia pastoris. Biotechnology (N Y) 11: 905-910. (Pubitemid 23218978)
36. Daily JP (2012) Malaria vaccine trials-beyond efficacy end points. N Engl J Med 367: 2349-2351.
37. Miller LH, Ackerman HC, Su XZ, Wellems TE (2013) Malaria biology and disease pathogenesis: insights for new treatments. Nat Med 19: 156-167.
38. Doud MB, Koksal AC, Mi LZ, Song G, Lu C, et al. (2012) Unexpected fold in the circumsporozoite protein target of malaria vaccines. Proc Natl Acad Sci U S A 109: 7817-7822.
39. Plassmeyer ML, Reiter K, Shimp RL, Jr., Kotova S, Smith PD, et al. (2009) Structure of the Plasmodium falciparum circumsporozoite protein, a leading malaria vaccine candidate. J Biol Chem 284: 26951-26963.
40. Kester KE, Cummings JF, Ofori-Anyinam O, Ockenhouse CF, Krzych U, et al. (2009) Randomized, double-blind, phase 2a trial of falciparum malaria vaccines RTS,S/AS01B and RTS,S/AS02A in malaria-naive adults: safety, efficacy, and immunologic associates of protection. J Infect Dis 200: 337-346.
41. John CC, Moormann AM, Pregibon DC, Sumba PO, McHugh MM, et al. (2005) Correlation of high levels of antibodies to multiple pre-erythrocytic Plasmodium falciparum antigens and protection from infection. Am J Trop Med Hyg 73: 222-228. (Pubitemid 41278777)
42. Schofield L, Villaquiran J, Ferreira A, Schellekens H, Nussenzweig R, et al. (1987) Gamma interferon, CD8+ T cells and antibodies required for immunity to malaria sporozoites. Nature 330: 664-666. (Pubitemid 18005584)
43. Weiss WR, Sedegah M, Beaudoin RL, Miller LH, Good MF (1988) CD8+ T cells (cytotoxic/suppressors) are required for protection in mice immunized with malaria sporozoites. Proc Natl Acad Sci U S A 85: 573-576. (Pubitemid 18059317)
44. Radosevic K, Rodriguez A, Lemckert AA, van der Meer M, Gillissen G, et al. (2010) The Th1 immune response to Plasmodium falciparum circumsporozoite protein is boosted by adenovirus vectors 35 and 26 with a homologous insert. Clin Vaccine Immunol 17: 1687-1694.
45. Agnandji ST, Lell B, Soulanoudjingar SS, Fernandes JF, Abossolo BP, et al. (2011) First results of phase 3 trial of RTS,S/AS01 malaria vaccine in African children. N Engl J Med 365: 1863-1875.
46. Scheller LF, Wirtz RA, Azad AF (1994) Susceptibility of different strains of mice to hepatic infection with Plasmodium berghei. Infect Immun 62: 4844-4847. (Pubitemid 24332785)
47. Craig AG, Grau GE, Janse C, Kazura JW, Milner D, et al. (2012) The role of animal models for research on severe malaria. PLoS Pathog 8: e1002401.
48. Combredet C, Labrousse V, Mollet L, Lorin C, Delebecque F, et al. (2003) A molecularly cloned Schwarz strain of measles virus vaccine induces strong immune responses in macaques and transgenic mice. J Virol 77: 11546-11554. (Pubitemid 37271653)
49. Nussenzweig V, Nussenzweig RS (1985) Circumsporozoite proteins of malaria parasites. Cell 42: 401-403.
50. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105-132.
51. Jackson DA, Pombo A, Iborra F (2000) The balance sheet for transcription: an analysis of nuclear RNA metabolism in mammalian cells. FASEB J 14: 242-254. (Pubitemid 30086061)
52. Ishino T, Orito Y, Chinzei Y, Yuda M (2006) A calcium-dependent protein kinase regulates Plasmodium ookinete access to the midgut epithelial cell. Mol Microbiol 59: 1175-1184.
53. Nimmerjahn F, Ravetch JV (2008) Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 8: 34-47.
54. Liu R, Lin Q, Sun Y, Lu X, Qiu Y, et al. (2009) Expression, purification, and characterization of hepatitis B virus surface antigens (HBsAg) in yeast Pichia Pastoris. Appl Biochem Biotechnol 158: 432-444.
55. Kumar S, Zheng H, Sangweme DT, Mahajan B, Kozakai Y, et al. (2013) A chemiluminescent-western blot assay for quantitative detection of Plasmodium falciparum circumsporozoite protein. J Immunol Methods 390: 99-105.
56. Gueirard P, Tavares J, Thiberge S, Bernex F, Ishino T, et al. (2010) Development of the malaria parasite in the skin of the mammalian host. Proc Natl Acad Sci U S A 107: 18640-18645.
57. Regules JA, Cummings JF, Ockenhouse CF (2011) The RTS,S vaccine candidate for malaria. Expert Rev Vaccines 10: 589-599.
58. Agnandji ST, Lell B, Fernandes JF, Abossolo BP, Methogo BG, et al. (2012) A phase 3 trial of RTS,S/AS01 malaria vaccine in African infants. N Engl J Med 367: 2284-2295.
59. Bejon P, White MT, Olotu A, Bojang K, Lusingu JP, et al. (2013) Efficacy of RTS,S malaria vaccines: individual-participant pooled analysis of phase 2 data. Lancet Infect Dis.
60. Hafalla JC, Bauza K, Friesen J, Gonzalez-Aseguinolaza G, Hill AV, et al. (2013) Identification of targets of CD8(+) T cell responses to malaria liver stages by genome-wide epitope profiling. PLoS Pathog 9: e1003303.
61. Zhang T, Yang H, Wang R, Xu K, Xin Y, et al. (2011) Oral administration of myostatin-specific whole recombinant yeast Saccharomyces cerevisiae vaccine increases body weight and muscle composition in mice. Vaccine 29: 8412-8416.
62. Lu Y, Bellgrau D, Dwyer-Nield LD, Malkinson AM, Duke RC, et al. (2004) Mutation-selective tumor remission with Ras-targeted, whole yeast-based immunotherapy. Cancer Res 64: 5084-5088. (Pubitemid 39006523)
63. Salvador A, Hernandez RM, Pedraz JL, Igartua M (2012) Plasmodium falciparum malaria vaccines: current status, pitfalls and future directions. Expert Rev Vaccines 11: 1071-1086.
64. Buckland R, Giraudon P, Wild F (1989) Expression of measles virus nucleoprotein in Escherichia coli: use of deletion mutants to locate the antigenic sites. J Gen Virol 70 (Pt 2): 435-441. (Pubitemid 19051673)
65. Desfosses A, Goret G, Farias Estrozi L, Ruigrok RW, Gutsche I (2011) Nucleoprotein-RNA orientation in the measles virus nucleocapsid by three-dimensional electron microscopy. J Virol 85: 1391-1395.
66. Keeling JW, Miller RK (2011) Indirect immunofluorescence for monitoring spindle assembly and disassembly in yeast. Methods Mol Biol 782: 231-244.
67. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
68. Frachon E, Bondet V, Munier-Lehmann H, Bellalou J (2006) Multiple microfermentor battery: a versatile tool for use with automated parallel cultures of microorganisms producing recombinant proteins and for optimization of cultivation protocols. Appl Environ Microbiol 72: 5225-5231.
69. Longhi S (2012) The measles virus N(TAIL)-XD complex: an illustrative example of fuzziness. Adv Exp Med Biol 725: 126-141.