Recombinant protein subunit vaccine synthesis in microbes: A role for yeast?

Journal of Pharmacy and Pharmacology

Volumn 67, Issue 3, 2015, Pages 319-328

  Bill, Roslyn M ^a  

^a ASTON UNIVERSITY   (United Kingdom)

Author keywords

Pichia pastoris; recombinant antigen; Saccharomyces cerevisiae; yeast

Indexed keywords

RECOMBINANT ANTIGEN; RECOMBINANT PROTEIN; RECOMBINANT VACCINE; ANTIGEN; SUBUNIT VACCINE;

ARTICLE; BACTERIUM IDENTIFICATION; DRUG APPROVAL; DRUG DESIGN; DRUG DETERMINATION; DRUG RESPONSE; DRUG SYNTHESIS; ESCHERICHIA COLI; FUNGUS IDENTIFICATION; HOST CELL; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; KOMAGATAELLA PASTORIS; NONHUMAN; SACCHAROMYCES CEREVISIAE; VACCINATION; VACCINE PRODUCTION; VIRUS LIKE AGENT; BACTERIAL INFECTIONS; BIOSYNTHESIS; METABOLISM; PICHIA; PROTEIN SYNTHESIS; VIRUS DISEASES; YEAST;

ANTIGENS; BACTERIAL INFECTIONS; HUMANS; PICHIA; PROTEIN BIOSYNTHESIS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; VACCINES, SUBUNIT; VIRUS DISEASES; YEASTS;

EID: 84925743410     PISSN: 00223573     EISSN: 20427158     Source Type: Journal    
DOI: 10.1111/jphp.12353     Document Type: Article

References (106)

1. Kao CM, et al. Child and adolescent immunizations: selected review of recent US recommendations and literature. Curr Opin Pediatr 2014; 26: 383-395.
2. Liljeqvist S, Stahl S,. Production of recombinant subunit vaccines: protein immunogens, live delivery systems and nucleic acid vaccines. J Biotechnol 1999; 73: 1-33.
3. Coffman RL, et al. Vaccine adjuvants: putting innate immunity to work. Immunity 2010; 33: 492-503.
4. Plotkin SA,. Vaccines: past, present and future. Nat Med 2005; 11: S5-S11.
5. Bill RM,. Playing catch-up with Escherichia coli: using yeast to increase success rates in recombinant protein production experiments. Front Microbiol 2014; 5: 85.
6. Spring MD, et al. Phase 1/2a study of the malaria vaccine candidate apical membrane antigen-1 (AMA-1) administered in adjuvant system AS01B or AS02A. PLoS ONE 2009; 4: e5254.
7. Roldao A, et al. Virus-like particles in vaccine development. Expert Rev Vaccines 2010; 9: 1149-1176.
8. Cohen SN, et al. Construction of biologically functional bacterial plasmids in vitro. Proc Natl Acad Sci U S A 1973; 70: 3240-3244.
9. Itakura K, et al. Expression in Escherichia coli of a chemically synthesized gene for the hormone somatostatin. Science 1977; 198: 1056-1063.
10. Goeddel DV, et al. Expression in Escherichia coli of chemically synthesized genes for human insulin. Proc Natl Acad Sci U S A 1979; 76: 106-110.
11. Goodman M,. Market watch: sales of biologics to show robust growth through to 2013. Nat Rev Drug Discov 2009; 8: 837.
12. Ferrer-Miralles N, et al. Microbial factories for recombinant pharmaceuticals. Microb Cell Fact 2009; 8: 17.
13. Zhu J,. Mammalian cell protein expression for biopharmaceutical production. Biotechnol Adv 2012; 30: 1158-1170.
14. Mattanovich D, et al. Recombinant protein production in yeasts. Methods Mol Biol 2012; 824: 329-358.
15. Valenzuela P, et al. Synthesis and assembly of hepatitis B virus surface antigen particles in yeast. Nature 1982; 298: 347-350.
16. Nigrovic LE, Thompson KM,. The Lyme vaccine: a cautionary tale. Epidemiol Infect 2007; 135: 1-8.
17. Meltzer MI, et al. The cost effectiveness of vaccinating against Lyme disease. Emerg Infect Dis 1999; 5: 321-328.
18. Soliakov A, et al. Anthrax sub-unit vaccine: the structural consequences of binding rPA83 to Alhydrogel(R). Eur J Pharm Biopharm 2012; 80: 25-32.
19. Jones SM, et al. Protection conferred by a fully recombinant sub-unit vaccine against Yersinia pestis in male and female mice of four inbred strains. Vaccine 2000; 19: 358-366.
20. Holley JL, et al. Cloning, expression and evaluation of a recombinant sub-unit vaccine against Clostridium botulinum type F toxin. Vaccine 2000; 19: 288-297.
21. Kleanthous H, et al. Vaccine development against infection with Helicobacter pylori. Br Med Bull 1998; 54: 229-241.
22. Colonna C, et al. Sub-unit vaccine against S. aureus-mediated infections: set-up of nano-sized polymeric adjuvant. Int J Pharm 2013; 452: 390-401.
23. Duthie MS, et al. Development and pre-clinical assessment of a 73 kD chimeric fusion protein as a defined sub-unit vaccine for leprosy. Vaccine 2013; 31: 813-819.
24. Mufalo BC, et al. Plasmodium vivax apical membrane antigen-1: comparative recognition of different domains by antibodies induced during natural human infection. Microbes Infect 2008; 10: 1266-1273.
25. Vanloubbeeck Y, et al. Comparison of the immune responses induced by soluble and particulate Plasmodium vivax circumsporozoite vaccine candidates formulated in AS01 in rhesus macaques. Vaccine 2013; 31: 6216-6224.
26. Weinrich Olsen A, et al. Protection of mice with a tuberculosis subunit vaccine based on a fusion protein of antigen 85b and esat-6. Infect Immun 2001; 69: 2773-2778.
27. Ramirez R, et al. Recombinant dengue 2 virus NS3 protein conserves structural antigenic and immunological properties relevant for dengue vaccine design. Virus Genes 2014; 49: 185-195.
28. Jang KO, et al. Expression and immunogenic analysis of recombinant polypeptides derived from capsid protein VP1 for developing subunit vaccine material against hepatitis A virus. Protein Expr Purif 2014; 100C: 1-9.
29. Wu K, et al. High level expression, purification and characterization of recombinant CCR5 as a vaccine candidate against HIV. Protein Expr Purif 2013; 89: 124-130.
30. Wen X, et al. Construction and characterization of human rotavirus recombinant VP8∗ subunit parenteral vaccine candidates. Vaccine 2012; 30: 6121-6126.
31. Dagouassat N, et al. A novel bipolar mode of attachment to aluminium-containing adjuvants by BBG2Na, a recombinant subunit hRSV vaccine. Vaccine 2001; 19: 4143-4152.
32. Treanor JJ, et al. Safety and immunogenicity of a recombinant hemagglutinin influenza-flagellin fusion vaccine (VAX125) in healthy young adults. Vaccine 2010; 28: 8268-8274.
33. Tanomand A, et al. Cloning, expression and characterization of recombinant exotoxin A-flagellin fusion protein as a new vaccine candidate against Pseudomonas aeruginosa infections. Iran Biomed J 2013; 17: 1-7.
34. Chura-Chambi RM, et al. Refolding of the recombinant protein Sm29, a step toward the production of the vaccine candidate against schistosomiasis. J Biotechnol 2013; 168: 511-519.
35. Sørensen HP,. Towards universal systems for recombinant gene expression. Microb Cell Fact 2010; 9: 27.
36. Bandaranayake AD, Almo SC,. Recent advances in mammalian protein production. FEBS Lett 2013; 588: 253-260.
37. Kunert R, Casanova E,. Recent advances in recombinant protein production: BAC-based expression vectors, the bigger the better. Bioengineered 2013; 4: 258-261.
38. Widmann M, Christen P,. Comparison of folding rates of homologous prokaryotic and eukaryotic proteins. J Biol Chem 2000; 275: 18619-18622.
39. Null D Jr, et al. Safety and immunogenicity of palivizumab (Synagis) administered for two seasons. Pediatr Infect Dis J 2005; 24: 1021-1023.
40. Stanberry LR, et al. Glycoprotein-D-adjuvant vaccine to prevent genital herpes. N Engl J Med 2002; 347: 1652-1661.
41. Villaflores OB, et al. Easy expression of the C-terminal heavy chain domain of botulinum neurotoxin serotype A as a vaccine candidate using a bi-cistronic baculovirus system. J Virol Methods 2013; 189: 58-64.
42. Arnot DE, et al. Comparative testing of six antigen-based malaria vaccine candidates directed toward merozoite-stage Plasmodium falciparum. Clin Vaccine Immunol 2008; 15: 1345-1355.
43. Venkateswarlu CH, Arankalle VA,. Recombinant glycoprotein based vaccine for Chandipura virus infection. Vaccine 2009; 27: 2845-2850.
44. McAtee CP, et al. Purification and characterization of a recombinant hepatitis E protein vaccine candidate by liquid chromatography-mass spectrometry. J Chromatogr B Biomed Appl 1996; 685: 91-104.
45. Shi YP, et al. Immunogenicity and in vitro protective efficacy of a recombinant multistage Plasmodium falciparum candidate vaccine. Proc Natl Acad Sci U S A 1999; 96: 1615-1620.
46. Zhou Z, et al. A recombinant baculovirus-expressed S glycoprotein vaccine elicits high titers of SARS-associated coronavirus (SARS-CoV) neutralizing antibodies in mice. Vaccine 2006; 24: 3624-3631.
47. Bonafe N, et al. A recombinant West Nile virus envelope protein vaccine candidate produced in Spodoptera frugiperda expresSF + cells. Vaccine 2009; 27: 213-222.
48. Ma JK, et al. The production of recombinant pharmaceutical proteins in plants. Nat Rev Genet 2003; 4: 794-805.
49. Streatfield SJ, Howard JA,. Plant-based vaccines. Int J Parasitol 2003; 33: 479-493.
50. Huang Z, et al. Plant-derived measles virus hemagglutinin protein induces neutralizing antibodies in mice. Vaccine 2001; 19: 2163-2171.
51. De Schutter K, et al. Genome sequence of the recombinant protein production host Pichia pastoris. Nat Biotechnol 2009; 27: 561-566.
52. Goffeau A, et al. Life with 6000 genes. Science 1996; 274: 546-567.
53. Porro D, et al. Production of recombinant proteins and metabolites in yeasts: when are these systems better than bacterial production systems? Appl Microbiol Biotechnol 2011; 89: 939-948.
54. Hepler RW, et al. A recombinant 63-kDa form of Bacillus anthracis protective antigen produced in the yeast Saccharomyces cerevisiae provides protection in rabbit and primate inhalational challenge models of anthrax infection. Vaccine 2006; 24: 1501-1514.
55. Romanos MA, et al. Expression of tetanus toxin fragment C in yeast: gene synthesis is required to eliminate fortuitous polyadenylation sites in AT-rich DNA. Nucleic Acids Res 1991; 19: 1461-1467.
56. Nguyen NL, et al. Expression and purification of an immunogenic dengue virus epitope using a synthetic consensus sequence of envelope domain III and Saccharomyces cerevisiae. Protein Expr Purif 2013; 88: 235-242.
57. Antoniukas L, et al. Production of hantavirus Puumala nucleocapsid protein in Saccharomyces cerevisiae for vaccine and diagnostics. J Biotechnol 2006; 124: 347-362.
58. Tomo N, et al. Trans-packaging of human immunodeficiency virus type 1 genome into Gag virus-like particles in Saccharomyces cerevisiae. Microb Cell Fact 2013; 12: 28.
59. Mendoza-Vega O, et al. Recombinant outer-surface protein A (des-Cys1-OspA) from the Lyme disease spirochete Borrelia burgdorferi: high production levels in Saccharomyces cerevisiae yeast cultures. Appl Microbiol Biotechnol 1996; 44: 624-628.
60. Schuldt NJ, Amalfitano A,. Malaria vaccines: focus on adenovirus based vectors. Vaccine 2012; 30: 5191-5198.
61. Gozar MM, et al. Saccharomyces cerevisiae-secreted fusion proteins Pfs25 and Pfs28 elicit potent Plasmodium falciparum transmission-blocking antibodies in mice. Infect Immun 1998; 66: 59-64.
62. Rombaut B, Jore JP,. Immunogenic, non-infectious polio subviral particles synthesized in Saccharomyces cerevisiae. J Gen Virol 1997; 78 (Pt 8): 1829-1832.
63. Klepfer SR, et al. Characterization of rabies glycoprotein expressed in yeast. Arch Virol 1993; 128: 269-286.
64. Rodriguez-Limas WA, et al. Molecular and process design for rotavirus-like particle production in Saccharomyces cerevisiae. Microb Cell Fact 2011; 10: 33.
65. Tan L, et al. Yeast expressed foldable quadrivalent Abeta15 elicited strong immune response against Abeta without Abeta-specific T cell response in wild C57BL/6 mice. Hum Vaccin Immunother. 2012; 8: 1090-1098.
66. Fontanella GH, et al. Immunization with an engineered mutant trans-sialidase highly protects mice from experimental Trypanosoma cruzi infection: a vaccine candidate. Vaccine 2008; 26: 2322-2334.
67. Batra G, et al. Optimization of conditions for secretion of dengue virus type 2 envelope domain III using Pichia pastoris. J Biosci Bioeng 2010; 110: 408-414.
68. Wang M, et al. Expression, purification, and immunogenic characterization of Epstein-Barr virus recombinant EBNA1 protein in Pichia pastoris. Appl Microbiol Biotechnol 2013; 97: 6251-6262.
69. Wang M, et al. Recombinant VP1 protein expressed in Pichia pastoris induces protective immune responses against EV71 in mice. Biochem Biophys Res Commun 2013; 430: 387-393.
70. Riordan AAO, et al. Alkyl hydroperoxide reductase: a candidate Helicobacter pylori vaccine. Vaccine 2012; 30: 3876-3884.
71. Gurramkonda C, et al. Purification of hepatitis B surface antigen virus-like particles from recombinant Pichia pastoris and in vivo analysis of their immunogenic properties. J Chromatogr B Analyt Technol Biomed Life Sci 2013; 940: 104-111.
72. Cai W, et al. Expression, purification and immunogenic characterization of hepatitis C virus recombinant E1E2 protein expressed by Pichia pastoris yeast. Antiviral Res 2010; 88: 80-85.
73. Curti E, et al. Optimization and revisions of the production process of the Necator americanus glutathione S-transferase 1 (Na-GST-1), the lead hookworm vaccine recombinant protein candidate. Hum Vaccin Immunother 2014; 10: 1914-1925.
74. Jiang WZ, et al. Expression and characterization of Gag protein of HIV-1(CN) in Pichia pastoris. J Virol Methods 2005; 123: 35-40.
75. Coimbra EC, et al. Production of L1 protein from different types of HPV in Pichia pastoris using an integrative vector. Braz J Med Biol Res 2011; 44: 1209-1214.
76. Curti E, et al. Expression at a 20L scale and purification of the extracellular domain of the Schistosoma mansoni TSP-2 recombinant protein: a vaccine candidate for human intestinal schistosomiasis. Hum Vaccin Immunother 2013; 9: 2342-2350.
77. Subathra M, et al. Evaluation of antibody response in mice against avian influenza A (H5N1) strain neuraminidase expressed in yeast Pichia pastoris. J Biosci 2014; 39: 443-451.
78. Athmaram TN, et al. A simple Pichia pastoris fermentation and downstream processing strategy for making recombinant pandemic Swine Origin Influenza a virus Hemagglutinin protein. J Ind Microbiol Biotechnol 2013; 40: 245-255.
79. Kwon WT, et al. Protective immunity of Pichia pastoris-expressed recombinant envelope protein of Japanese encephalitis virus. J Microbiol Biotechnol 2012; 22: 1580-1587.
80. Lau YL, et al. Immunogenic characterization of the chimeric surface antigen 1 and 2 (SAG1/2) of Toxoplasma gondii expressed in the yeast Pichia pastoris. Parasitol Res 2011; 109: 871-878.
81. Jacob D, et al. Whole Pichia pastoris yeast expressing measles virus nucleoprotein as a production and delivery system to multimerize Plasmodium antigens. PLoS ONE 2014; 9: e86658.
82. Vicentin EC, et al. Invasion-inhibitory antibodies elicited by immunization with Plasmodium vivax apical membrane antigen-1 expressed in Pichia pastoris yeast. Infect Immun 2014; 82: 1296-1307.
83. Xia M, et al. Norovirus capsid protein expressed in yeast forms virus-like particles and stimulates systemic and mucosal immunity in mice following an oral administration of raw yeast extracts. J Med Virol 2007; 79: 74-83.
84. Cregg JM, et al. Pichia pastoris as a host system for transformations. Mol Cell Biol 1985; 5: 3376-3385.
85. Habersetzer F, et al. GI-5005, a yeast vector vaccine expressing an NS3-core fusion protein for chronic HCV infection. Curr Opin Mol Ther 2009; 11: 456-462.
86. Upadhyaya B, Manjunath R,. Baker's yeast expressing the Japanese encephalitis virus envelope protein on its cell surface: induction of an antigen-specific but non-neutralizing antibody response. Yeast 2009; 26: 383-397.
87. Scott DJ, et al. Stabilizing membrane proteins through protein engineering. Curr Opin Chem Biol 2013; 17: 427-435.
88. Traxlmayr MW, Obinger C,. Directed evolution of proteins for increased stability and expression using yeast display. Arch Biochem Biophys 2012; 526: 174-180.
89. Oberg F, et al. Improving recombinant eukaryotic membrane protein yields in Pichia pastoris: the importance of codon optimization and clone selection. Mol Membr Biol 2011; 28: 398-411.
90. Halliday M, Mallucci GR,. Targeting the unfolded protein response in neurodegeneration: a new approach to therapy. Neuropharmacology 2014; 76 (Pt A): 169-174.
91. Rebnegger C, et al. In Pichia pastoris, growth rate regulates protein synthesis and secretion, mating and stress response. Biotechnol J 2013; 9: 511-525.
92. Spadiut O, et al. Quantitative comparison of dynamic physiological feeding profiles for recombinant protein production with Pichia pastoris. Bioprocess Biosyst Eng 2013; 36: 1571-1577.
93. Jazini M, Herwig C,. Effects of temperature shifts and oscillations on recombinant protein production expressed in Escherichia coli. Bioprocess Biosyst Eng 2013; 36: 1571-1577.
94. Bora N, et al. The implementation of a design of experiments strategy to increase recombinant protein yields in yeast (review). Methods Mol Biol 2012; 866: 115-127.
95. Holmes WJ, et al. Developing a scalable model of recombinant protein yield from Pichia pastoris: the influence of culture conditions, biomass and induction regime. Microb Cell Fact 2009; 8: 35.
96. Dietzsch C, et al. A dynamic method based on the specific substrate uptake rate to set up a feeding strategy for Pichia pastoris. Microb Cell Fact 2011; 10: 14.
97. Drew D, et al. GFP-based optimization scheme for the overexpression and purification of eukaryotic membrane proteins in Saccharomyces cerevisiae. Nat Protoc 2008; 3: 784-798.
98. Ashe MP, Bill RM,. Mapping the yeast host cell response to recombinant membrane protein production: relieving the biological bottlenecks. Biotechnol J 2011; 6: 707-714.
99. De Pourcq K, et al. Engineering of glycosylation in yeast and other fungi: current state and perspectives. Appl Microbiol Biotechnol 2010; 87: 1617-1631.
100. Kitson SM, et al. GPCR production in a novel yeast strain that makes cholesterol-like sterols. Methods 2011; 55: 287-292.
101. Guerfal M, et al. Enhanced membrane protein expression by engineering increased intracellular membrane production. Microb Cell Fact 2013; 12: 122.
102. Bonander N, Bill RM,. Relieving the first bottleneck in the drug discovery pipeline: using array technologies to rationalize membrane protein production. Expert Rev Proteomics 2009; 6: 501-505.
103. Bonander N, et al. Design of improved membrane protein production experiments: quantitation of the host response. Protein Sci 2005; 14: 1729-1740.
104. Baumann K, et al. Protein trafficking, ergosterol biosynthesis and membrane physics impact recombinant protein secretion in Pichia pastoris. Microb Cell Fact 2011; 10: 93.
105. Bonander N, et al. Altering the ribosomal subunit ratio in yeast maximizes recombinant protein yield. Microb Cell Fact 2009; 8: 10.
106. Norden K, et al. Increasing gene dosage greatly enhances recombinant expression of aquaporins in Pichia pastoris. BMC Biotechnol 2011; 11: 47.