Engineering soya bean seeds as a scalable platform to produce cyanovirin-N, a non-ARV microbicide against HIV

Plant Biotechnology Journal

Volumn 13, Issue 7, 2015, Pages 884-892

  O'Keefe, Barry R ^a   Murad, André M ^b   Vianna, Giovanni R ^b   Ramessar, Koreen ^a   Saucedo, Carrie J ^a,c   Wilson, Jennifer ^a   Buckheit, Karen W ^d   da Cunha, Nicolau B ^b   Araújo, Ana Claudia G ^b   Lacorte, Cristiano C ^b   Madeira, Luisa ^b,e   Mcmahon, James B ^a   Rech, Elibio L ^b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b EMBRAPA RECURSOS GENÉTICOS E BIOTECNOLOGIA   (Brazil)

^c FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^d ImQuest Biosciences   (United States)

^e ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Anti HIV; Cyanovirin N; Soya bean

Indexed keywords

ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; BACTERIAL PROTEIN; CARRIER PROTEIN; CYANOVIRIN N;

BIOSYNTHESIS; GENETICS; METABOLISM; PLANT SEED; PROTEIN ENGINEERING; SOYBEAN;

ANTI-HIV AGENTS; BACTERIAL PROTEINS; CARRIER PROTEINS; PROTEIN ENGINEERING; SEEDS; SOYBEANS;

EID: 84939566084     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12309     Document Type: Article

References (46)

1. American Oil Chemists Society (1980a) Urease Activity. Official Method Ba 9-58. Champagne, IL, USA: American Oil Chemists Society.
2. Aragão, F.J.L., Sarokin, L., Vianna, G.R. and Rech, E.L. (2000) Selection of transgenic meristematic cells utilizing a herbicidal molecule results in the recovery of fertile transgenic soybean [Glycine max (L.) Merril] plants at a high frequency. Theor. Appl. Genet. 101, 1-6.
3. Boyd, M.R., Gustafson, K.R., McMahon, J.B., Shoemaker, R.H., O'Keefe, B.R., Mori, T., Gulakowski, T.R.J., Wu, L., Rivera, M.I., Laurencot, C.M., Currens, M.J., Cardellina, J.H. II, Buckheit, R.W. Jr, Nara, P.L., Pannell, L.K., Sowder, R.C. and Henderson, L.E. (1997) Discovery of cyanovirin-N, a novel human immunodeficiency virus-inactivating protein that binds viral surface envelope glycoprotein gp120; potential applications to microbicide development. Antimicrob. Agents Chemother. 41, 1521-1530.
4. Brichacek, B., Lagenaur, L.A., Lee, P.P., Venzon, D. and Hamer, D.H. (2013) In vivo evaluation of safety and toxicity of a Lactobacillus jensenii producing modified Cyanovirin-N in a rhesus macaque vaginal challenge model. PLoS ONE, 8, e78817.
5. Buffa, V., Stieh, D., Mamhood, N., Hu, Q., Fletcher, P. and Shattock, R.J. (2009) Cyanovirin-N potently inhibits human immunodeficiency virus type 1 infection in cellular and cervical explant models. J. Gen. Virol. 90, 234-243.
6. Cavazzoni, J., Volk, T., Bugbee, B. and Dougher, T. (1999) Phasic temperature and photoperiod control for soybean using a modified CROPGRO model. Life Support Biosph Sci. 6, 273-278.
7. Cunha, N.B., Murad, A.M., Cipriano, T.M., Araújo, A.C.G., Aragão, F.J.L., Leite, A., Vianna, G.R., McPhee, T.R., Souza, G.H.M.F., Waters, M.J. and Rech, E.L. (2011a) Expression of functional recombinant human growth hormone in transgenic soybean seeds. Transgenic Res. 20, 811-826.
8. Cunha, N.B., Murad, A.M., Ramos, G.L., Maranhão, A.Q., Brígido, M.M., Araújo, A.C.G., Lacorte, C., Aragão, F.J.L., Covas, D.T., Fontes, A.M., Souza, G.H.M.F., Vianna, G.R. and Rech, E.L. (2011b) Accumulation of functional recombinant human coagulation factor IX in transgenic soybean seeds. Transgenic Res. 20, 841-855.
9. Dashiell, G.L. (1989) Lecithin and food processing applications. In ACOS Monograph (Szuhaj, B.F., ed.), pp. 16. Champaign, IL: American Oil Chemists Society.
10. Doyle, J.J. and Doyle, J.L. (1987) A rapid DNA isolation procedure from small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11-15.
11. Drake, P.M.W., Madeira, L.D., Szeto, T.H. and Ma, J.K.C. (2013) Transformation of Althaea officinalis L. by Agrobacterium rhizogenes for the production of transgenic roots expressing the anti-HIV microbicide cyanovirin-N. Transgenic Res. 22, 1225-1229.
12. Elghabi, Z., Karcher, D., Zhou, F., Ruf, S. and Bock, R. (2011) Optimization of the expression of the HIV fusion inhibitor cyanovirin-N from the tobacco plastid genome. Plant Biotechnol. J. 9, 599-608.
13. Erickson, D.R. (1995) Overview of modern soybean processing and links between processes. Chapter 5. Practical Handbook of Soybean Processing and Utilization. Amer Oil Chemists Society (AOCS), 6th edn (Erickson, D.R., ed.), pp. 56-64. AOCS, 2710 S. Boulder, Urbana, IL 61802?6996, USA.
14. Essex, M. (1996) Retroviral vaccines: challenges for the developing world. AIDS Res. Hum. Retroviruses 12, 361-363.
15. Friend, D.R. and Kiser, P.F. (2013) Assessment of topical microbicides to prevent HIV-1 transmission: concepts, testing, lessons learned. Antiviral Res. 99, 391-400.
16. Gartner, S.P., Markovits, D.M., Kaplan, M.H., Gallor, R.C. and Popovic, M. (1986) The role of mononuclear phagocytes in HTLV-III/LAV infection. Science, 233, 215-219.
17. Gulakowski, R.J., McMahon, J.B., Staley, P.G., Moran, R.A. and Boyd, M.R. (1991) A semiautomated multiparameter approach for anti-HIV drug screening. J. Virol. Methods, 33, 87-100.
18. Hohl, I., Robinson, D.G., Chrispeels, M.J. and Hinz, G. (1996) Transport of storage proteins to the vacuole is mediated by vesicles without a clathrin coat. J. Cell Sci. 109, 2539-2550.
19. Imoto, Y., Yamada, T., Kitamura, K. and Kanazawa, A. (2008) Spatial and temporal control of transcription of the soybean beta-conglycinin alpha subunit gene is conferred by its proximal promoter region and accounts for the unequal distribution of the protein during embryogenesis. Genes Genet Syst. 83, 469-476.
20. Kantolic, A.G. and Slafer, G.A. (2007) Development and seed number in indeterminate soybean as affected by timing and duration of exposure to long photoperiods after flowering. Ann. Bot. 99, 925-933.
21. Kim, W.S. and Krishnan, H.B. (2004) Expression of an 11 kDa methionine-rich delta-zein in transgenic soybean results in the formation of two types of novel protein bodies in transitional cells situated between the vascular tissue and storage parenchyma cells. Plant Biotechnol. J. 2, 199-210.
22. Kouokam, J.C., Huskens, D., Schols, D., Johannemann, A., Riedell, S.K., Walter, W., Walker, J.M., Matoba, N., O'Keefe, B.R. and Palmer, K.E. (2011) Investigation of griffithsin's interactions with human cells confirms its outstanding safety and efficacy profile as a microbicide candidate. PLoS ONE, 6, e22635.
23. Ladin, B.F., Tierney, M.L., Meinke, D.W., Hosangadi, P., Veith, M. and Beachy, R.N. (1987) Developmental regulation of β-conglycinin in soybean axes and cotyledons. Plant Physiol. 84, 35-41.
24. Lagenaur, L.A., Sanders-Beer, B.E., Brichacek, B., Pal, R., Liu, X., Liu, Y., Yu, R., Venzon, D., Lee, P.P. and Hamer, D.H. (2011) Prevention of vaginal SHIV transmission in macaques by a live recombinant Lactobacillus. Mucosal Immunol. 4, 648-657.
25. Li, D., O'Leary, J.J., Huang, Y., Huner, N.A., Jevnikar, A. and Ma, S. (2006) Expression of cholera toxin B subunit and the B chain of human insulin as a fusion protein in transgenic tobacco plants. Plant Cell Rep. 25, 417-424.
26. Li, M., Patton, D.L., Cosgrove-Sweeney, Y., Ratner, D., Rohan, L.C., Cole, A.M., Tarwater, P.M., Gupta, P. and Ramratnam, B. (2011) Incorporation of the HIV-1 microbicide cyanovirin-N in a food product. J. Acquir. Immune Defic. Syndr. 58, 379-384.
27. Mori, T., Pannell, L.K., Shoemaker, R.H., Wu, L., McMahon, J.B. and Boyd, M.R. (1998) Recombinant production of cyanovirin-N, a potent HIV (human immunodeficiency virus)-inactivating protein derived from a cultured cyanobacterium. Protein Expr. Purif. 12, 151-158.
28. Mori, T., Barrientos, L.G., Han, Z., Gronenborn, A.M., Turpin, J.A. and Boyd, M.R. (2002) Functional homologs of cyanovirin-N amenable to mass production in prokaryotic and eukaryotic hosts. Protein Expr. Purif. 26, 42-49.
29. Mori, T., Saruta, Y., Fukuda, T., Prak, K., Ishimoto, M., Maruyama, N. and Utsumi, S. (2009) Vacuolar sorting behaviors of 11S globulins in plant cells. Biosci. Biotechnol. Biochem. 73, 53-60.
30. Muntz, K. (1998) Deposition of storage proteins. Plant Mol. Biol. 38, 77-99.
31. O'Keefe, B., Vojdani, F., Buffa, V., Shattock, R.J., Montefiori, D.C., Bakke, J., Mirsalise, J., d'Andreae, A.-L., Hume, S.D., Bratcherf, B., Saucedo, C.J., McMahon, J.B., Pogue, G.P. and Palmer, K.E. (2009) Scaleable manufacture of HIV-1 entry inhibitor griffithsin and validation of its safety and efficacy as a topical microbicide component. Proc. Natl Acad. Sci. USA, 106, 6099-6104.
32. Rech, E.L., Vianna, G.R. and Aragao, F.J. (2008) High-efficiency transformation by biolistics of soybean, common bean and cotton transgenic plants. Nat. Protoc. 3, 410-418.
33. Robinson, D.G., Oliviusson, P. and Hinz, G. (2005) Protein sorting to the storage vacuoles of plants: a critical appraisal. Traffic, 6, 615-625.
34. Sexton, A., Drake, P.M., Mahmood, N., Harman, S.J., Shattock, R.J. and Ma, J.K.C. (2006) Transgenic plant production of cyanovirin-N, an HIV microbicide. FASEB J. 20, 356-358.
35. Shattock, R.J. and Rosenberg, Z. (2012) Microbicides: topical prevention against HIV. Cold Spring Harb. Perspect Med. 2, a007385.
36. Takaiwa, F., Takagi, H., Hirose, S. and Wakasa, Y. (2007) Endosperm tissue is good production platform for artificial recombinant proteins in transgenic rice. Plant Biotechnol. J. 5, 84-92.
37. Tsai, C.-C., Emau, P., Jinag, Y., Tian, B., Morton, W.R., Gustafson, K.R. and Boyd, M.R. (2003) Cyanovirin-N Gel as a Topical Microbicide Prevents Rectal Transmission of SHIV89.6P in Macaques. AIDS Res. Hum. Retroviruses, 19, 535-541.
38. Tsai, C.C., Emau, P., Jiang, Y., Agy, M.B., Shattock, R.J., Schmidt, A., Morton, W.R., Gustafson, K.R. and Boyd, M.R. (2004) Cyanovirin-N inhibits AIDS virus infections in vaginal transmission models. AIDS Res. Hum. Retroviruses, 20, 11-18.
39. UNAIDS. (2013) Joint United Nations Programme on HIV/AIDS. UNAIDS report on the global AIDS epidemic 2013. UNAIDS/JC2502/1/E.
40. Vitale, A. and Raikhel, N.V. (1999) What do proteins need to reach different vacuoles? Trends Plant Sci. 4, 149-155.
41. Watanabe, S., Hideshima, R., Xia, Z., Tsubokura, Y., Sato, S., Nakamoto, Y., Yamanaka, N., Takahashi, R., Ishimoto, M., Anai, T., Tabata, S. and Harada, K. (2009) Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics, 182, 1251-1262.
42. Wilson, K.A., Rightmire, B.R., Chen, J.C. and Tanwilson, A.L. (1986) Differential proteolysis of glycinin and beta-conglycinin polypeptides during soybean germination and seedling growth. Plant Physiol. 82, 71-76.
43. Wu, F.Q., Fan, C.M., Zhang, X.M. and Fu, Y.F. (2013) The phytochrome gene family in soybean and a dominant negative effect of a soybean PHYA transgene on endogenous Arabidopsis PHYA. Plant Cell Rep. 32, 1879-1890.
44. Xiong, S., Fan, J. and Kitazato, K. (2010) The antiviral protein cyanovirin-N: the current state of its production and applications. Appl Microbiol Biot. 86, 805-812.
45. Yamada, Y., Nishizawa, K., Yokoo, M., Zhao, H., Onishi, K., Teraishi, M., Utsumi, S., Ishimoto, M. and Yoshikawa, M. (2008) Anti-hypertensive activity of genetically modified soybean seeds accumulating novokinin. Peptides, 29, 331-337.
46. Yoo, B.Y. and Chrispeels, M.J. (1980) The origin of protein bodies in developing soybean cotyledons - a proposal. Protoplasma, 103, 201-204.