Boosting in plantaproduction of antigens derived from the porcine reproductive and respiratory syndrome virus (PRRSV) and subsequent evaluation of their immunogenicity

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Piron, Robin ^a,b   De Koker, Stefaan ^b   De Paepe, Annelies ^a,b   Goossens, Julie ^c   Grooten, Johan ^b   Nauwynck, Hans ^b   Depicker, Ann ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G3; MANNOSE; MEMBRANE PROTEIN; PROTEIN GP3; PROTEIN GP4; PROTEIN GP5; SUBUNIT VACCINE; UNCLASSIFIED DRUG; VIRUS ANTIGEN; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN; BACTERIAL DNA; GLYCOPROTEIN; POLYSACCHARIDE; T-DNA;

ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ANTIGEN PURIFICATION; ARABIDOPSIS THALIANA; ARTERIVIRUS; ARTICLE; ENDOPLASMIC RETICULUM; FEMALE; HOMOZYGOSITY; IMMUNOGENICITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT SEED; PROTEIN DOMAIN; PROTEIN STABILITY; SWINE; VIRUS NEUTRALIZATION; AFFINITY CHROMATOGRAPHY; ANIMAL; ANIMAL MODEL; ARABIDOPSIS; BIOSYNTHESIS; C57BL MOUSE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; GLYCOSYLATION; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; PIG; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS; TRANSGENIC PLANT; VIROLOGY;

ANIMALS; ANTIGENS, VIRAL; ARABIDOPSIS; CHROMATOGRAPHY, AFFINITY; DNA, BACTERIAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GLYCOPROTEINS; GLYCOSYLATION; MICE, INBRED C57BL; MODELS, ANIMAL; MOLECULAR SEQUENCE DATA; PLANTS, GENETICALLY MODIFIED; POLYSACCHARIDES; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SEEDS; SWINE;

EID: 84897567941     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0091386     Document Type: Article

References (69)

1. Collins JE, Benfield DA, Christianson WT, Harris L, Hennings JC, et al. (1992) Isolation of swine infertility and respiratory syndrome virus (isolate ATCC VR-2332) in North America and experimental reproduction of the disease in gnotobiotic pigs. J Vet Diagn Invest 4: 117-126.
2. Wensvoort G, Terpstra C, Pol JMA, ter Laak EA, Bloemraad M, et al. (1991) Mystery swine disease in the Netherlands: The isolation of Lelystad virus. Vet Q 13: 121-130.
3. Neumann EJ, Kliebenstein JB, Johnson CD, Mabry JW, Bush EJ, et al. (2005) Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J Am Vet Med Assoc 227: 385-392. (Pubitemid 41098522)
4. Zhou L, Yang H (2010) Porcine reproductive and respiratory syndrome in China. Virus Res 154: 31-37.
5. Terpstra C, Wensvoort G, Pol JMA (1991) Experimental reproduction of porcine epidemic abortion and respiratory syndrome (mystery swine disease) by infection with Lelystad vims: Koch's postulates fulfilled. Vet Q 13: 131-136.
6. Karniychuk UU, Geldhof M, Vanhee M, Van Doorsselaere J, Saveleva TA, et al. (2010) Pathogenesis and antigenic characterization of a new East European subtype 3 porcine reproductive and respiratory syndrome virus isolate. BMC Vet Res 6: 30.
7. Meulenberg JJM, Hulst MM, de Meijer EJ, Moonen PLJM, den Besten A, et al. (1993) Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to LDV and EAV. Virology 192: 62-72.
8. Stadejek T, Oleksiewicz MB, Scherbakov AV, Timina AM, Krabbe JS, et al. (2008) Definition of subtypes in the European genotype of porcine reproductive and respiratory syndrome virus: nucleocapsid characteristics and geographical distribution in Europe. Arch Virol 153: 1479-1488.
9. Meulenberg JJM, Petersen den Besten A, de Kluyver E, van Nieuwstadt A, Wensvoort G, et al. (1997) Molecular characterization of Lelystad virus. Vet Microbiol 55: 197-202. (Pubitemid 27286214)
10. Meulenberg JJM, Petersen-Den Besten A, De Kluyver EP, Moormann RJM, Schaaper WMM, et al. (1995) Characterization of proteins encoded by ORFs 2 to 7 of Lelystad virus. Virology 206: 155-163.
11. Wu W-H, Fang Y, Farwell R, Steffen-Bien M, Rowland RRR, et al. (2001) A 10-kDa structural protein of porcine reproductive and respiratory syndrome virus encoded by ORF2b. Virology 287: 183-191. (Pubitemid 32778250)
12. Wu W-H, Fang Y, Rowland RRR, Lawson SR, Christopher-Hennings J, et al. (2005) The 2b protein as a minor structural component of PRRSV. Virus Res 114: 177-181. (Pubitemid 41586614)
13. Mardassi H, Massie B, Dea S (1996) Intracellular synthesis, processing, and transport of proteins encoded by ORFs 5 to 7 of Porcine Reproductive and Respiratory Syndrome Virus. Virology 221: 98-112. (Pubitemid 26266546)
14. Lopez OJ, Osorio FA (2004) Role of neutralizing antibodies in PRRSV protective immunity. Vet Immunol Immunopathol 102: 155-163. (Pubitemid 39422641)
15. Kimman TG, Cornelissen LA, Moormann RJ, Rebel JMJ, Stochofe-Zurwieden N (2009) Challenges for porcine reproductive and respiratory syndrome virus (PRRSV) vaccinology. Vaccine 27: 3704-3718.
16. Geldhof MF, Vanhee M, Van Breedam W, Van Doorsselaere J, Karniychuk UU, et al. (2012) Comparison of the efficacy of autogenous inactivated Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) vaccines with that of commercial vaccines against homologous and heterologous challenges. BMC Vet Res 8: 182.
17. Zuckermann FA, Garcia EA, Luque ID, Christopher-Hennings J, Doster A, et al. (2007) Assessment of the efficacy of commercial porcine reproductive and respiratory syndrome virus (PRRSV) vaccines based on measurement of serologic response, frequency of gamma-IFN-producing cells and virological parameters of protection upon challenge. Vet Microbiol 123: 69-85. (Pubitemid 46898707)
18. D́iaz I, Darwich L, Pappaterra G, Pujols J, Mateu E (2006) Different European-type vaccines against porcine reproductive and respiratory syndrome virus have different immunological properties and confer different protection to pigs. Virology 351: 249-259. (Pubitemid 44108075)
19. Key KF, Guenette DK, Yoon K-J, Halbur PG, Toth TE, et al. (2003) Development of a heteroduplex mobility assay to identify field isolates of porcine reproductive and respiratory syndrome virus with nucleotide sequences closely related to those of modified live-attenuated vaccines. J Clin Microbiol 41: 2433-2439. (Pubitemid 36712447)
20. Nielsen HS, Oleksiewicz MB, Forsberg R, Stadejek T, Bøtner A, et al. (2001) Reversion of a live porcine reproductive and respiratory syndrome virus vaccine investigated by parallel mutations. J Gen Virol 82: 1263-1272. (Pubitemid 32519757)
21. Opriessnig T, Halbur PG, Yoon K-J, Pogranichniy RM, Harmon KM, et al. (2002) Comparison of molecular and biological characteristics of a modified live porcine reproductive and respiratory syndrome virus (PRRSV) vaccine (Ingelvac PRRS MLV), the parent strain of the vaccine (ATCC VR2332), ATCC-VR2385, and two recent field isolates of PRRSV. J Virol 76: 11837-11844. (Pubitemid 35304284)
22. De Jaeger G, Scheffer S, Jacobs A, Zambre M, Zobell O, et al. (2002) Boosting heterologous protein production in transgenic dicotyledonous seeds using Phaseolus vulgaris regulatory sequences. Nat Biotechnol 20: 1265-1268. (Pubitemid 35462494)
23. Van Droogenbroeck B, Cao J, Stadlmann J, Altmann F, Colanesi S, et al. (2007) Aberrant localization and underglycosylation of highly accumulating single-chain Fv-Fc antibodies in transgenic Arabidopsis seeds. Proc Natl Acad Sci USA 104: 1430-1435. (Pubitemid 46184021)
24. Goossens A, Dillen W, De Clercq J, Van Montagu M, Angenon G (1999) The arcelin-5 gene of Phaseolus vulgaris directs high seed-specific expression in transgenic Phaseolus acutifolius and Arabidopsis plants. Plant Physiol 120: 1095-1104. (Pubitemid 29411897)
25. Loos A, Van Droogenbroeck B, Hillmer S, Grass J, Kunert R, et al. (2011) Production of monoclonal antibodies with a controlled N-glycosylation pattern in seeds of Arabidopsis thaliana. Plant Biotechnol J 9: 179-192.
26. Loos A, Van Droogenbroeck B, Hillmer S, Grass J, Pabst M, et al. (2011) Expression of antibody fragments with a controlled N-glycosylation pattern and induction of endoplasmic reticulum-derived vesicles in seeds of Arabidopsis. Plant Physiol 155: 2036-2048.
27. Paul M, Ma JK-C (2010) Plant-made immunogens and effective delivery strategies. Expert Rev Vaccines 9: 821-833.
28. Rybicki EP (2010) Plant-made vaccines for humans and animals. Plant Biotechnol J 8: 620-637.
29. Nagels B, Weterings K, Callewaert N, Van Damme EJM (2012) Production of plant made pharmaceuticals: from plant host to functional protein. Crit Rev Plant Sci 31: 148-180.
30. Yusibov V, Streatfield SJ, Kushnir N (2011) Clinical development of plant-produced recombinant pharmaceuticals: Vaccines, antibodies and beyond. Hum Vaccin 7: 313-321.
31. Chan HT, Chia MY, Pang VF, Jeng CR, Do YY, et al. (2013) Oral immunogenicity of porcine reproductive and respiratory syndrome virus antigen expressed in transgenic banana. Plant Biotechnol J 11: 315-324.
32. Chen X, Liu J (2011) Generation and immunogenicity of transgenic potato expressing the GP5 protein of porcine reproductive and respiratory syndrome virus. J Virol Methods 173: 153-158.
33. Chia M-Y, Hsiao S-H, Chan H-T, Do Y-Y, Huang P-L, et al. (2011) Evaluation of the immunogenicity of a transgenic tobacco plant expressing the recombinant fusion protein of GP5 of porcine reproductive and respiratory syndrome virus and B subunit of Escherichia coli heat-labile enterotoxin in pigs. Vet Immunol Immunopathol 140: 215-225.
34. Chia M-Y, Hsiao S-H, Chan H-T, Do Y-Y, Huang PL, et al. (2010) Immunogenicity of recombinant GP5 protein of porcine reproductive and respiratory syndrome virus expressed in tobacco plant. Vet Immunol Immunopathol 135: 234-242.
35. Hu J, Ni Y, Dryman BA, Meng XJ, Zhang C (2012) Immunogenicity study of plant-made oral subunit vaccine against porcine reproductive and respiratory syndrome virus (PRRSV). Vaccine 30: 2068-2074.
36. Vimolmangkang S, Gasic K, Soria-Guerra R, Rosales-Mendoza S, Moreno-Fierros L, et al. (2012) Expression of the nucleocapsid protein of porcine reproductive and respiratory syndrome virus in soybean seed yields an immunogenic antigenic protein. Planta 235: 513-522.
37. Morandini F, Avesani L, Bortesi L, Van Droogenbroeck B, De Wilde K, et al. (2011) Non-food/feed seeds as biofactories for the high-yield production of recombinant pharmaceuticals. Plant Biotechnol J 9: 911-921.
38. Rybicki ER (2009) Plant-produced vaccines: promise and reality. Drug Discov Today 14: 16-24.
39. Wissink EHJ, Kroese MV, van Wijk HAR, Rijsewijk FAM, Meulenberg JJM, et al. (2005) Envelope protein requirements for the assembly of infectious virions of porcine reproductive and respiratory syndrome virus. J Virol 79: 12495-12506. (Pubitemid 41346112)
40. Meulenberg JJ, van Nieuwstadt AP, van Essen-Zandbergen A, Langeveld JP (1997) Posttranslational processing and identification of a neutralization domain of the GP4 protein encoded by ORF4 of Lelystad virus. J Virol 71: 6061-6067. (Pubitemid 27304946)
41. Van Breedam W, Costers S, Vanhee M, Gagnon CA, Rodŕiguez- Gómez IM, et al. (2011) Porcine reproductive and respiratory syndrome virus (PRRSV)-specific mAbs: supporting diagnostics and providing new insights into the antigenic properties of the virus. Vet Immunol Immunopathol 141: 246-257.
42. Costers S, Lefebvre DJ, Van Doorsselaere J, Vanhee M, Delputte PL, et al. (2010) GP4 of porcine reproductive and respiratory syndrome virus contains a neutralizing epitope that is susceptible to immunoselection in vitro. Arch Virol 155: 371-378.
43. Krebbers E, Herdies L, De Clercq A, Seurinck J, Leemans J, et al. (1988) Determination of the processing sites of an Arabidopsis 2S albumin and characterization of the complete gene family. Plant Physiol 87: 859-866.
44. Gomord V, Denmat L-A, Fitchette-Lainé A-C, Satiat-Jeunemaitre B, Hawes C, et al. (1997) The C-terminal HDEL sequence is sufficient for retention of secretory proteins in the endoplasmic reticulum (ER) but promotes vacuolar targeting of proteins that escape the ER. Plant J 11: 313-325. (Pubitemid 27147977)
45. Pearse BR, Hebert DN (2010) Lectin chaperones help direct the maturation of glycoproteins in the endoplasmic reticulum. Biochim Biophys Acta 1803: 684-693.
46. Maley F, Trimble RB, Tarentino AL, Plummer TH Jr (1989) Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases. Anal Biochem 180: 195-204. (Pubitemid 19198046)
47. Gomord V, Fitchette AC, Menu-Bouaouiche L, Saint-Jore-Dupas C, Plasson C, et al. (2010) Plant-specific glycosylation patterns in the context of therapeutic protein production. Plant Biotechnol J 8: 564-587.
48. He X, Haselhorst T, von Itzstein M, Kolarich D, Packer NH, et al. (2012) Influence of an ER-retention signal on the N-glycosylation of recombinant human alpha-L-iduronidase generated in seeds of Arabidopsis. Plant Mol Biol 79: 157-169.
49. De Buck S, Nolf J, De Meyer T, Virdi V, De Wilde K, et al. (2013) Fusion of an Fc chain to a VHH boosts the accumulation levels in Arabidopsis seeds. Plant Biotechnol J 11: 1006-1016.
50. Goding JW (1978) Use of staphylococcal protein A as an immunological reagent. J Immunol Methods 20: 241-253. (Pubitemid 8329659)
51. Obregon P, Chargelegue D, Drake PMW, Prada A, Nuttall J, et al. (2006) HIV-1 p24-immunoglobulin fusion molecule: a new strategy for plant-based protein production. Plant Biotechnol J 4: 195-207.
52. Cubitt AB, Heim R, Adams SR, Boyd AE, Gross LA, et al. (1995) Understanding, improving and using green fluorescent proteins. Trends Biochem Sci 20: 448-455.
53. Peckham GD, Bugos RC, Su WW (2006) Purification of GFP fusion proteins from transgenic plant cell cultures. Protein Expr Purif 49: 183-189. (Pubitemid 44419596)
54. Rothbauer U, Zolghadr K, Muyldermans S, Schepers A, Cardoso MC, et al. (2008) A versatile nanotrap for biochemical and functional studies with fluorescent fusion proteins. Mol Cell Proteomics 7: 282-289. (Pubitemid 351298442)
55. Prieto C, Mart́inez-Lobo FJ, D́iez-Fuertes F, Aguilar-Calvo P, Simarro I, et al. (2011) Immunisation of pigs with a major envelope protein sub-unit vaccine against porcine reproductive and respiratory syndrome virus (PRRSV) results in enhanced clinical disease following experimental challenge. Vet J 189: 323-329.
56. Duran JP, Climent I, Sarraseca J, Urniza A, Cortés E, et al. (1997) Baculovirus expression of proteins of porcine reproductive and respiratory syndrome virus strain Olot/91. Involvement of ORF3 and ORF5 proteins in protection. Virus Genes 14: 19-29. (Pubitemid 27267513)
57. Nam H-M, Chae K-S, Song Y-J, Lee N-H, Lee J-B, et al. (2013) Immune responses in mice vaccinated with virus-like particles composed of the GP5 and M proteins of porcine reproductive and respiratory syndrome virus. Arch Virol 158: 1275-1285.
58. Wang W, Chen X, Xue C, Du Y, Lv L, et al. (2012) Production and immunogenicity of chimeric virus-like particles containing porcine reproductive and respiratory syndrome virus GP5 protein. Vaccine 30: 7072-7077.
59. Czajkowsky DM, Hu J, Shao Z, Pleass RJ (2012) Fc-fusion proteins: new developments and future perspectives. EMBO Mol Med 4: 1015-1028.
60. Ye L, Zeng R, Bai Y, Roopenian DC, Zhu X (2011) Efficient mucosal vaccination mediated by the neonatal Fc receptor. Nat Biotechnol 29: 158-163.
61. Engering AJ, Cella M, Fluitsma D, Brockhaus M, Hoefsmit ECM, et al. (1997) The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells. Eur J Immunol 27: 2417-2425. (Pubitemid 27404329)
62. Tan MCAA, Mommaas AM, Drijfhout JW, Jordens R, Onderwater JJM, et al. (1997) Mannose receptor-mediated uptake of antigens strongly enhances HLA class II-restricted antigen presentation by cultured dendritic cells. Eur J Immunol 27: 2426-2435. (Pubitemid 27404330)
63. Plana-Durán J, Bastons M, Urniza A, Vayreda M, Vilà X, et al. (1997) Efficacy of an inactivated vaccine for prevention of reproductive failure induced by porcine reproductive and respiratory syndrome virus. Vet Microbiol 55: 361-370. (Pubitemid 27286233)
64. Vanhee M, Delputte PL, Delrue I, Geldhof MF, Nauwynck HJ (2009) Development of an experimental inactivated PRRSV vaccine that induces virus-neutralizing antibodies. Vet Res 40: 63.
65. Virdi V, Coddens A, De Buck S, Millet S, Goddeeris BM, et al. (2013) Orally fed seeds producing designer IgAs protect weaned piglets against enterotoxigenic Escherichia coli infection. Proc Natl Acad Sci USA 110: 11809-11814.
66. TM vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193-195. (Pubitemid 36725938)
67. L-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204: 383-396.
68. De Buck S, Virdi V, De Meyer T, De Wilde K, Piron R, et al. (2012) Production of camel-like antibodies in plants. Methods Mol Biol 911: 305-324.
69. Labarque GG, Nauwynck HJ, Van Reeth K, Pensaert MB (2000) Effect of cellular changes and onset of humoral immunity on the replication of porcine reproductive and respiratory syndrome virus in the lungs of pigs. J Gen Virol 81: 1327-1334. (Pubitemid 30232719)