Plant-produced anti-dengue virus monoclonal antibodies exhibit reduced antibody-dependent enhancement of infection activity

Journal of General Virology

Volumn 97, Issue 12, 2016, Pages 3280-3290

  Dent, Matthew ^a   Hurtado, Jonathan ^a   Paul, Amber M ^b   Sun, Haiyan ^a   Lai, Huafang ^a   Yang, Ming ^a   Esqueda, Adrian ^a   Bai, Fengwei ^b   Steinkellner, Herta ^c   Chen, Qiang ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b University of Southern Mississippi   (United States)

^c UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

Antibody dependent enhancement (ADE); Dengue virus; Fc receptors; Glycosylation; Monoclonal antibody; Plant made therapeutics

Indexed keywords

ANTIVIRUS AGENT; FC RECEPTOR; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY E60; NEUTRALIZING ANTIBODY; PLANT EXTRACT; UNCLASSIFIED DRUG; VIRUS ANTIBODY;

ANIMAL CELL; ANTIBODY DEPENDENT ENHANCEMENT; ANTIGEN BINDING; ANTIVIRAL ACTIVITY; ARTICLE; DENGUE; DISEASE ACTIVITY; DNA SEQUENCE; FEMALE; GLYCOSYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; NICOTIANA BENTHAMIANA; NONHUMAN; PATHOGENESIS; PLANT LEAF; PRIORITY JOURNAL; SEROTYPE; DENGUE VIRUS; GENE EXPRESSION; GENETICS; IMMUNOLOGY; METABOLISM; TOBACCO; VIROLOGY;

ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY-DEPENDENT ENHANCEMENT; DENGUE; DENGUE VIRUS; GENE EXPRESSION; HUMANS; TOBACCO;

EID: 85007256378     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000635     Document Type: Article

References (80)

1. Arntzen, C. (2015). Plant-made pharmaceuticals: from ‘Edible Vaccines’ to Ebola therapeutics. Plant Biotechnol J 13, 1013-1016.
2. Balsitis, S. J., Williams, K. L., Lachica, R., Flores, D., Kyle, J. L., Mehlhop, E., Johnson, S., Diamond, M. S., Beatty, P. R. & Harris, E. (2010). Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 6, e1000790.
3. Beltramello, M., Williams, K. L., Simmons, C. P., Macagno, A., Simonelli, L., Quyen, N. T., Sukupolvi-Petty, S., Navarro-Sanchez, E., Young, P. R. & other authors (2010). The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe 8, 271-283.
4. Bendandi, M., Marillonnet, S., Kandzia, R., Thieme, F., Nickstadt, A., Herz, S., Fröde, R., Inoges, S., Lòpez-Dìaz de Cerio, A. & other authors (2010). Rapid, high-yield production in plants of individualized idiotype vaccines for non-Hodgkin’s lymphoma. Ann Oncol 21, 2420-2427
5. Boonnak, K., Dambach, K. M., Donofrio, G. C., Tassaneetrithep, B. & Marovich, M. A. (2011). Cell type specificity and host genetic polymorphisms influence antibody-dependent enhancement of dengue virus infection. J Virol 85, 1671-1683.
6. Boonnak, K., Slike, B. M., Donofrio, G. C. & Marovich, M. A. (2013). Human FcgRII cytoplasmic domains differentially influence antibodymediated dengue virus infection. J Immunol 190, 5659-5665.
7. Brown, M. G., King, C. A., Sherren, C., Marshall, J. S. & Anderson, R. (2006). A dominant role for FcgammaRII in antibody-enhanced dengue virus infection of human mast cells and associated CCL5 release. J Leukoc Biol 80, 1242-1250.
8. Burke, D. S. & Monath, T. P. (2001). Flaviviruses. In Fields Virology, 4th edn, pp. 1043-1125. Edited by D. M. Knipe & P. M. Howley. Philadelphia: Lippincott Williams & Wilkins.
9. Chan, K. R., Zhang, S. L., Tan, H. C., Chan, Y. K., Chow, A., Lim, A. P., Vasudevan, S. G., Hanson, B. J. & Ooi, E. E. (2011). Ligation of Fc gamma receptor IIB inhibits antibody-dependent enhancement of dengue virus infection. Proc Natl Acad Sci U S A 108, 12479-12484.
10. Chawla, T., Chan, K. R., Zhang, S. L., Tan, H. C., Lim, A. P., Hanson, B. J. & Ooi, E. E. (2013). Dengue virus neutralization in cells expressing Fc gamma receptors. PLoS One 8, e65231
11. Check Hayden, E. E. & Reardon, S. (2014). Should experimental drugs be used in the Ebola outbreak? Nature http://dx.doi.org/10.1038/nature.2014.15698.
12. Chen, Q. (2011). Expression and manufacture of pharmaceutical proteins in genetically engineered horticultural plants. In Transgenic Horticultural Crops: Challenges and Opportunities Essays by Experts, pp. 83-124. Edited by B. Mou & R. Scorza. Boca Raton: Taylor & Francis.
13. Chen, Q. (2016). Glycoengineering of plants yields glycoproteins with polysialylation and other defined N-glycoforms. Proc Natl Acad Sci U S A 113, 9404-9406.
14. Chen, Q. & Davis, K. R. (2016). The potential of plants as a system for the development and production of human biologics. F1000Res 5, 912-920.
15. Chen, Q. & Lai, H. (2014a). Gene delivery into plant cells for recombinant protein production. Biomed Res Int 2015, 1-10.
16. Chen, Q. & Lai, H. (2014b). Plant-derived monoclonal antibodies as human biologics for infectious disease and cancer. In Plant-Derived Pharmaceuticals: Principles and Applications for Developing Countries, pp. 42-75. Edited by K. L. Hefferon. Croydon, UK: CABI.
17. Chen, Q. & Lai, H. (2015). The growing potential of plant-made monoclonal antibodies. Drug Target Review 2, 41-44.
18. Chen, Q., He, J., Phoolcharoen, W. & Mason, H. S. (2011). Geminiviral vectors based on bean yellow dwarf virus for production of vaccine antigens and monoclonal antibodies in plants. Hum Vaccin 7, 331-338.
19. Chen, Q., Lai, H., Hurtado, J., Stahnke, J., Leuzinger, K. & Dent, M. (2013). Agroinfiltration as an effective and scalable strategy of gene delivery for production of pharmaceutical proteins. Adv Tech Biol Med 1, 103-112.
20. Chung, K. M., Thompson, B. S., Fremont, D. H. & Diamond, M. S. (2007). Antibody recognition of cell surface-associated NS1 triggers Fcgamma receptor-mediated phagocytosis and clearance of West Nile Virusinfected cells. J Virol 81, 9551-9555.
21. de Alwis, R., Beltramello, M., Messer, W. B., Sukupolvi-Petty, S., Wahala, W. M., Kraus, A., Olivarez, N. P., Pham, Q., Brien, J. D. & other authors (2011). In-depth analysis of the antibody response of individuals exposed to primary dengue virus infection. PLoS Negl Trop Dis 5, e1188.
22. de Alwis, R., Smith, S. A., Olivarez, N. P., Messer, W. B., Huynh, J. P., Wahala, W. M. P. B., White, L. J., Diamond, M. S., Baric, R. S. & other authors (2012). Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. Proc Natl Acad Sci U S A 109, 7439-7444.
23. De Muynck, B., Navarre, C. & Boutry, M. (2010). Production of antibodies in plants: status after twenty years. Plant Biotechnol J 8, 529-563.
24. Dejnirattisai, W., Wongwiwat, W., Supasa, S., Zhang, X., Dai, X., Rouvinski, A., Rouvinsky, A., Jumnainsong, A., Edwards, C. & other authors (2015). A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat Immunol 16, 170-177.
25. Dejnirattisai, W., Supasa, P., Wongwiwat, W., Rouvinski, A., BarbaSpaeth, G., Duangchinda, T., Sakuntabhai, A., Cao-Lormeau, V. M., Malasit, P. & other authors (2016). Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with zika virus. Nat Immunol 17, 1102-1108.
26. Deng, Y. Q., Dai, J. X., Ji, G. H., Jiang, T., Wang, H. J., Yang, H. O., Tan, W. L., Liu, R., Yu, M. & other authors (2011). A broadly flavivirus cross-neutralizing monoclonal antibody that recognizes a novel epitope within the fusion loop of E protein. PLoS One 6, e16059.
27. García, G., Arango, M., Perez, A. B., Fonte, L., Sierra, B., RodríguezRoche, R., Aguirre, E., Fiterre, I. & Guzman, M. G. (2006). Antibodies from patients with dengue viral infection mediate cellular cytotoxicity. J Clin Virol 37, 53-57.
28. Giritch, A., Marillonnet, S., Engler, C., van Eldik, G., Botterman, J., Klimyuk, V. & Gleba, Y. (2006). Rapid high-yield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors. Proc Natl Acad Sci U S A 103, 14701-14706.
29. Halstead, S. B. (2007). Dengue. Lancet 370, 1644-1652
30. Halstead, S. B., Mahalingam, S., Marovich, M. A., Ubol, S. & Mosser, D. M. (2010). Intrinsic antibody-dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes. Lancet Infect Dis 10, 712-722.
31. He, J., Lai, H., Brock, C. & Chen, Q. (2012). A novel system for rapid and cost-effective production of detection and diagnostic reagents of West Nile virus in plants. J Biomed Biotechnol 2012, 1-10.
32. He, J., Lai, H., Engle, M., Gorlatov, S., Gruber, C., Steinkellner, H., Diamond, M. S. & Chen, Q. (2014). Generation and analysis of novel plant-derived antibody-based therapeutic molecules against West Nile virus. PLoS One 9, e93541.
33. Houde, D., Peng, Y., Berkowitz, S. A. & Engen, J. R. (2010). Post-translational modifications differentially affect IgG1 conformation and receptor binding. Mol Cell Proteomics 9, 1716-1728.
34. Huang, Z., Phoolcharoen, W., Lai, H., Piensook, K., Cardineau, G., Zeitlin, L., Whaley, K. J., Arntzen, C. J., Mason, H. S. & Chen, Q. (2010). High-level rapid production of full-size monoclonal antibodies in plants by a single-vector DNA replicon system. Biotechnol Bioeng 106, 9-17.
35. Huang, X., Yue, Y., Li, D., Zhao, Y., Qiu, L., Chen, J., Pan, Y., Xi, J., Wang, X. & other authors (2016). Antibody-dependent enhancement of dengue virus infection inhibits RLR-mediated Type-I IFN-independent signalling through upregulation of cellular autophagy. Sci Rep 6, 22303.
36. Huisman, W., Martina, B. E., Rimmelzwaan, G. F., Gruters, R. A. & Osterhaus, A. D. (2009). Vaccine-induced enhancement of viral infections. Vaccine 27, 505-512.
37. Jefferis, R. (2005). Glycosylation of recombinant antibody therapeutics. Biotechnol Prog 21, 11-16.
38. Kaneko, Y., Nimmerjahn, F. & Ravetch, J. V. (2006). Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 313, 670-673.
39. Kayser, V., Chennamsetty, N., Voynov, V., Forrer, K., Helk, B. & Trout, B. L. (2011). Glycosylation influences on the aggregation propensity of therapeutic monoclonal antibodies. Biotechnol J 6, 38-44.
40. Kuhn, R. J., Zhang, W., Rossmann, M. G., Pletnev, S. V., Corver, J., Lenches, E., Jones, C. T., Mukhopadhyay, S., Chipman, P. R. & other authors (2002). Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108, 717-725.
41. Kyle, J. L. & Harris, E. (2008). Global spread and persistence of dengue. Annu Rev Microbiol 62, 71-92.
42. Lai, H. & Chen, Q. (2012). Bioprocessing of plant-derived virus-like particles of Norwalk virus capsid protein under current Good Manufacture Practice regulations. Plant Cell Rep 31, 573-584.
43. Lai, H., Engle, M., Fuchs, A., Keller, T., Johnson, S., Gorlatov, S., Diamond, M. S. & Chen, Q. (2010). Monoclonal antibody produced in plants efficiently treats West Nile virus infection in mice. Proc Natl Acad Sci USA107,2419-2424.
44. Lai, H., He, J., Engle, M., Diamond, M. S. & Chen, Q. (2012). Robust production of virus-like particles and monoclonal antibodies with geminiviral replicon vectors in lettuce. Plant Biotechnol J 10, 95-104.
45. Lai, H., He, J., Hurtado, J., Stahnke, J., Fuchs, A., Mehlhop, E., Gorlatov, S., Loos, A., Diamond, M. S. & Chen, Q. (2014). Structural and functional characterization of an anti-West Nile virus monoclonal antibody and its single-chain variant produced in glycoengineered plants. Plant Biotechnol J 12, 1098-1107.
46. Laoprasopwattana, K., Libraty, D. H., Endy, T. P., Nisalak, A., Chunsuttiwat, S., Ennis, F. A., Rothman, A. L. & Green, S. (2007). Antibody-dependent cellular cytotoxicity mediated by plasma obtained before secondary dengue virus infections: potential involvement in early control of viral replication. J Infect Dis 195, 1108-1116.
47. Leuzinger, K., Dent, M., Hurtado, J., Stahnke, J., Lai, H., Zhou, X. & Chen, Q. (2013). Efficient agroinfiltration of plants for high-level transient expression of recombinant proteins. J Vis Exp 77, e50521.
48. Loos, A. & Steinkellner, H. (2012). IgG-Fc glycoengineering in nonmammalian expression hosts. Arch Biochem Biophys 526, 167-173.
49. Loos, A. & Steinkellner, H. (2014). Plant glyco-biotechnology on the way to synthetic biology. Front Plant Sci 5, 523.
50. Loos, A., Gruber, C., Altmann, F., Mehofer, U., Hensel, F., Grandits, M., Oostenbrink, C., Stadlmayr, G., Furtmüller, P. G. & Steinkellner, H. (2014). Expression and glycoengineering of functionally active heteromultimeric IgM in plants. Proc Natl Acad Sci U S A 111, 6263-6268.
51. Mehlhop, E., Ansarah-Sobrinho, C., Johnson, S., Engle, M., Fremont, D. H., Pierson, T. C. & Diamond, M. S. (2007). Complement protein C1q inhibits antibody-dependent enhancement of flavivirus infection in an IgG subclass-specific manner. Cell Host Microbe 2, 417-426.
52. Mehlhop, E., Nelson, S., Jost, C. A., Gorlatov, S., Johnson, S., Fremont, D. H., Diamond, M. S. & Pierson, T. C. (2009). Complement protein C1q reduces the stoichiometric threshold for antibody-mediated neutralization of West Nile virus. Cell Host Microbe 6, 381-391.
53. Mohamad Zamberi, Z., Zakaria, Z., Abdul Aziz, A. T., Heng, B. S., Zaid, M., Chong, C. L., Noor, F. M., Abu Bakar, S. & Boon Peng, H. (2015). The high-affinity human IgG receptor Fc gamma receptor I (FcgRI) is not associated with vascular leakage of dengue. J Negat Results Biomed 14, 1.
54. Morens, D. M. (1994). Antibody-dependent enhancement of infection and the pathogenesis of viral disease. Clin Infect Dis 19, 500-512.
55. Mukhopadhyay, S., Kuhn, R. J. & Rossmann, M. G. (2005). A structural perspective of the flavivirus life cycle. Nat Rev Microbiol 3, 13-22.
56. Murphy, B. R. & Whitehead, S. S. (2011). Immune response to dengue virus and prospects for a vaccine. Annu Rev Immunol 29, 587-619.
57. Murray, N. E., Quam, M. B. & Wilder-Smith, A. (2013). Epidemiology of dengue: past, present and future prospects. Clin Epidemiol 5, 299-309.
58. Olinger, G. G., Pettitt, J., Kim, D., Working, C., Bohorov, O., Bratcher, B., Hiatt, E., Hume, S. D., Johnson, A. K. & other authors (2012). Delayed treatment of Ebola virus infection with plant-derived monoclonal antibodies provides protection in rhesus macaques. Proc Natl Acad Sci U S A 109, 18030-18035.
59. Oliphant, T., Engle, M., Nybakken, G. E., Doane, C., Johnson, S., Huang, L., Gorlatov, S., Mehlhop, E., Marri, A. & other authors (2005). Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nat Med 11, 522-530.
60. Oliphant, T., Nybakken, G. E., Engle, M., Xu, Q., Nelson, C. A., Sukupolvi-Petty, S., Marri, A., Lachmi, B. E., Olshevsky, U. & other authors (2006). Antibody recognition and neutralization determinants on domains I and II of West Nile Virus envelope protein. J Virol 80, 12149-12159.
61. Pang, T. (2016). SAGE committee advice on dengue vaccine. Lancet Infect Dis 16, 880-882.
62. Paul, A. M., Shi, Y., Acharya, D., Douglas, J. R., Cooley, A., Anderson, J. F., Huang, F. & Bai, F. (2014). Delivery of antiviral small interfering RNA with gold nanoparticles inhibits dengue virus infection in vitro. J Gen Virol 95, 1712-1722.
63. Pierson, T. C., Xu, Q., Nelson, S., Oliphant, T., Nybakken, G. E., Fremont, D. H. & Diamond, M. S. (2007). The stoichiometry of antibodymediated neutralization and enhancement of West Nile virus infection. Cell Host Microbe 1, 135-145.
64. Rico-Hesse, R., Harrison, L. M., Salas, R. A., Tovar, D., Nisalak, A., Ramos, C., Boshell, J., de Mesa, M. T., Nogueira, R. M. & da Rosa, A. T. (1997). Origins of dengue type 2 viruses associated with increased pathogenicity in the Americas. Virology 230, 244-251.
65. Rodrigo, W. W., Jin, X., Blackley, S. D., Rose, R. C. & Schlesinger, J. J. (2006). Differential enhancement of dengue virus immune complex infectivity mediated by signaling-competent and signaling-incompetent human Fcgamma RIA (CD64) or FcgammaRIIA (CD32). J Virol 80, 10128-10138
66. Rodrigo, W. W., Block, O. K., Lane, C., Sukupolvi-Petty, S., Goncalvez, A. P., Johnson, S., Diamond, M. S., Lai, C. J., Rose, R. C. & other authors (2009). Dengue virus neutralization is modulated by IgG antibody subclass and Fcgamma receptor subtype. Virology 394, 175-182
67. Rothman, A. L. (2004). Dengue: defining protective versus pathologic immunity. J Clin Invest 113, 946-951.
68. Schlesinger, J. J., Brandriss, M. W. & Walsh, E. E. (1987). Protection of mice against dengue 2 virus encephalitis by immunization with the dengue 2 virus non-structural glycoprotein NS1. J Gen Virol 68, 853-857
69. Shaaltiel, Y. & Tekoah, Y. (2016). Plant specific N-glycans do not have proven adverse effects in humans. Nat Biotechnol 34, 706-708
70. Shevitz, J., Bonham-Carter, J., Lim, J. & Sinclair, A. (2011). An economic comparison of three cell culture techniques. BioPharm Int 24, 54-60
71. Stadlmann, J., Pabst, M., Kolarich, D., Kunert, R. & Altmann, F. (2008). Analysis of immunoglobulin glycosylation by LC-ESI-MS of glycopeptides and oligosaccharides. Proteomics 8, 2858-2871.
72. Strasser, R., Stadlmann, J., Schahs, M., Stiegler, G., Quendler, H., Mach, L., Glössl, J., Weterings, K., Pabst, M. & Steinkellner, H. (2008). Generation of glyco-engineered Nicotiana benthamiana for the production of monoclonal antibodies with a homogeneous human-like N-glycan structure. Plant Biotechnol J 6, 392-402.
73. Strasser, R., Altmann, F. & Steinkellner, H. (2014). Controlled glycosylation of plant-produced recombinant proteins. Curr Opin Biotechnol 30, 95-100.
74. Taylor, A., Foo, S. S., Bruzzone, R., Dinh, L. V., King, N. J. & Mahalingam, S. & Vu Dinh, L. (2015). Fc receptors in antibody-dependent enhancement of viral infections. Immunol Rev 268, 340-364.
75. Tirado, S. M. & Yoon, K. J. (2003). Antibody-dependent enhancement of virus infection and disease. Viral Immunol 16, 69-86.
76. Tuse, D., Tu, T. & McDonald, K. A. (2014). Manufacturing economics of plant-made biologics: case studies in therapeutic and industrial enzymes. Biomed Res Int 2014, 1-16.
77. Wilder-Smith, A. & Gubler, D. J. (2008). Geographic expansion of dengue: the impact of international travel. Med Clin North Am 92, 1377-1390.
78. Williams, K. L., Sukupolvi-Petty, S., Beltramello, M., Johnson, S., Sallusto, F., Lanzavecchia, A., Diamond, M. S. & Harris, E. (2013). Therapeutic efficacy of antibodies lacking Fcg receptor binding against lethal dengue virus infection is due to neutralizing potency and blocking of enhancing antibodies [corrected]. PLoS Pathog 9, e1003157.
79. Zeitlin, L., Pettitt, J., Scully, C., Bohorova, N., Kim, D., Pauly, M., Hiatt, A., Ngo, L., Steinkellner, H. & other authors (2011). Enhanced potency of a fucose-free monoclonal antibody being developed as an Ebola virus immunoprotectant. Proc Natl Acad Sci U S A 108, 20690-20694.
80. Zheng, K., Bantog, C. & Bayer, R. (2011). The impact of glycosylation on monoclonal antibody conformation and stability. MAbs 3, 568-576