Cloning and characterisation of nanobodies against the coat protein of Zucchini yellow mosaic virus

https://doi.org/10.17221/158/2017-PPSCitation:Zakri A.M., AL-Doss A.A., Sack M., Ali A.A., Samara E.M., Ahmed B.S., Amer M.A., Abdalla O.A., Al-Saleh M.A. (2018): Cloning and characterisation of nanobodies against the coat protein of Zucchini yellow mosaic virus. Plant Protect. Sci., 54: 215-221.
download PDF

Zucchini yellow mosaic virus (ZYMV), in the family Potyviridae, causes an economically important disease. Antibodies are valuable reagents for diagnostic assays to rapidly detect viral infection. Here, we report the isolation of camel-derived variable domains of the heavy chain antibody (VHH, also called nanobodies) directed against the coat protein (CP) of ZYMV. Several nanobodies that specifically recognise ZYMV-CP were identified. The isolated nanobodies showed binding not only to recombinant ZYMV-CP but also to native ZYMV, indicating that these nanobodies can be used in diagnostic tools to detect viral infections.

References:
Abbady A.Q., Al-Mariri A., Zarkawi M., Al-Assad A., Muyldermans S. (2011): Evaluation of a nanobody phage display library constructed from a Brucella-immunised camel. Veterinary Immunology and Immunopathology, 142, 49-56  https://doi.org/10.1016/j.vetimm.2011.04.004
 
Al-Saleh M.A. (1994): Identification of viruses infecting cucurbits in the central region of Saudi Arabia and evaluation of different cucurbits sp. to the most important ones. [MSc Thesis.] King Saud University, Saudi Arabia.
 
Mohammed A. Al-Saleh, Mahmoud A. Amer, Ibrahim M. AL-Shahwan, Omer A. Abdalla, Mohammed A. Zakri (2014): Characterization of different isolates of Zucchini yellow mosaic virus from cucurbits in Saudi Arabia. African Journal of Microbiology Research, 8, 1987-1994  https://doi.org/10.5897/AJMR2014.6673
 
Shahwan I. M.Al- (1995): Response of Greenhouse-Grown Cucumber Cultivars to an Isolate of Zucchini Yellow Mosaic Virus (ZYMV). Plant Disease, 79, 898-  https://doi.org/10.1094/PD-79-0898
 
Blua Matthew J. (1989): Effect of Zucchini Yellow Mosaic Virus on Development and Yield of Cantaloupe (Cucumis melo). Plant Disease, 73, 317-  https://doi.org/10.1094/PD-73-0317
 
Cervera Magdalena, Esteban Olga, Gil Maite, Gorris M. Teresa, Martínez M. Carmen, Peña Leandro, Cambra Mariano (2010): Transgenic expression in citrus of single-chain antibody fragments specific to Citrus tristeza virus confers virus resistance. Transgenic Research, 19, 1001-1015  https://doi.org/10.1007/s11248-010-9378-5
 
Chung Wen Yuan, Sack Markus, Carter Rachel, Spiegel Holger, Fischer Rainer, Hirst Timothy R., Williams Neil A., James Roger F.L. (2008): Phage-display derived single-chain fragment variable (scFv) antibodies recognizing conformational epitopes of Escherichia coli heat-labile enterotoxin B-subunit. Journal of Immunological Methods, 339, 115-123  https://doi.org/10.1016/j.jim.2008.08.005
 
Cortez-Retamozo V. (2004): Efficient Cancer Therapy with a Nanobody-Based Conjugate. Cancer Research, 64, 2853-2857  https://doi.org/10.1158/0008-5472.CAN-03-3935
 
De Buck Sylvie, Nolf Jonah, De Meyer Thomas, Virdi Vikram, De Wilde Kirsten, Van Lerberge Els, Van Droogenbroeck Bart, Depicker Ann (2013): Fusion of an Fc chain to a VHH boosts the accumulation levels in Arabidopsis seeds. Plant Biotechnology Journal, 11, 1006-1016  https://doi.org/10.1111/pbi.12094
 
Desbiez C., Wipf-Scheibel C., Lecoq H. (2002): Biological and serological variability, evolution and molecular epidemiology of Zucchini yellow mosaic virus (ZYMV, Potyvirus) with special reference to Caribbean islands. Virus Research, 85, 5-16  https://doi.org/10.1016/S0168-1702(02)00013-8
 
Dietzgen R. G., Sander Evamarie (1982): Monoclonal antibodies against a plant virus. Archives of Virology, 74, 197-204  https://doi.org/10.1007/BF01314712
 
Flajnik Martin F., Deschacht Nick, Muyldermans Serge (2011): A Case Of Convergence: Why Did a Simple Alternative to Canonical Antibodies Arise in Sharks and Camels?. PLoS Biology, 9, e1001120-  https://doi.org/10.1371/journal.pbio.1001120
 
GAL-ON AMIT (2007): Zucchini yellow mosaic virus: insect transmission and pathogenicity ?the tails of two proteins. Molecular Plant Pathology, 8, 139-150  https://doi.org/10.1111/j.1364-3703.2007.00381.x
 
Ghannam Ahmed, Kumari Safa, Muyldermans Serge, Abbady Abdul Qader (2015): Camelid nanobodies with high affinity for broad bean mottle virus: a possible promising tool to immunomodulate plant resistance against viruses. Plant Molecular Biology, 87, 355-369  https://doi.org/10.1007/s11103-015-0282-5
 
Grafton-Cardwell Elizabeth E. (1996): Occurrence of Mosaic Viruses in Melons in the Central Valley of California. Plant Disease, 80, 1092-  https://doi.org/10.1094/PD-80-1092
 
Hamers-Casterman C., Atarhouch T., Muyldermans S., Robinson G., Hammers C., Songa E. Bajyana, Bendahman N., Hammers R. (1993): Naturally occurring antibodies devoid of light chains. Nature, 363, 446-448  https://doi.org/10.1038/363446a0
 
Harper K., Kerschbaumer R.J., Ziegler A., Macintosh S.M., Cowan G.H., Himmler G., Mayo M.A., Torrance L. (1997): A scFv-alkaline phosphatase fusion protein which detects potato leafroll luteovirus in plant extracts by ELISA. Journal of Virological Methods, 63, 237-242  https://doi.org/10.1016/S0166-0934(96)02133-7
 
Harries Phillip, Ding Biao (2011): Cellular factors in plant virus movement: At the leading edge of macromolecular trafficking in plants. Virology, 411, 237-243  https://doi.org/10.1016/j.virol.2010.12.021
 
Hassanzadeh-Ghassabeh Gholamreza, Devoogdt Nick, De Pauw Pieter, Vincke Cécile, Muyldermans Serge (2013): Nanobodies and their potential applications. Nanomedicine, 8, 1013-1026  https://doi.org/10.2217/nnm.13.86
 
Head Graham P, Carroll Matthew W, Evans Sean P, Rule Dwain M, Willse Alan R, Clark Thomas L, Storer Nicholas P, Flannagan Ronald D, Samuel Luke W, Meinke Lance J (2017): Evaluation of SmartStax and SmartStax PRO maize against western corn rootworm and northern corn rootworm: efficacy and resistance management. Pest Management Science, 73, 1883-1899  https://doi.org/10.1002/ps.4554
 
Heinlein Manfred (2015): Plant virus replication and movement. Virology, 479-480, 657-671  https://doi.org/10.1016/j.virol.2015.01.025
 
Kihara T. (1985): Self-crystallizing molecular models. VII. Plant-virus coat protein. Acta Crystallographica Section A Foundations of Crystallography, 41, 556-559  https://doi.org/10.1107/S0108767385001210
 
Koide Akiko, Tereshko Valentina, Uysal Serdar, Margalef Katrina, Kossiakoff Anthony A., Koide Shohei (2007): Exploring the Capacity of Minimalist Protein Interfaces: Interface Energetics and Affinity Maturation to Picomolar KD of a Single-domain Antibody with a Flat Paratope. Journal of Molecular Biology, 373, 941-953  https://doi.org/10.1016/j.jmb.2007.08.027
 
Laliberté Jean-François, Sanfaçon Hélène (2010): Cellular Remodeling During Plant Virus Infection. Annual Review of Phytopathology, 48, 69-91  https://doi.org/10.1146/annurev-phyto-073009-114239
 
Lucas William J. (2006): Plant viral movement proteins: Agents for cell-to-cell trafficking of viral genomes. Virology, 344, 169-184  https://doi.org/10.1016/j.virol.2005.09.026
 
Magnus Carsten, Reh Lucia, Trkola Alexandra (2016): HIV-1 resistance to neutralizing antibodies: Determination of antibody concentrations leading to escape mutant evolution. Virus Research, 218, 57-70  https://doi.org/10.1016/j.virusres.2015.10.009
 
Monegal A., Ami D., Martinelli C., Huang H., Aliprandi M., Capasso P., Francavilla C., Ossolengo G., de Marco A. (2009): Immunological applications of single-domain llama recombinant antibodies isolated from a naive library. Protein Engineering, Design & Selection, 22: 273–280.
 
Muyldermans Serge (2013): Nanobodies: Natural Single-Domain Antibodies. Annual Review of Biochemistry, 82, 775-797  https://doi.org/10.1146/annurev-biochem-063011-092449
 
Muyldermans Serge, Lauwereys Marc (1999): Unique single-domain antigen binding fragments derived from naturally occurring camel heavy-chain antibodies. Journal of Molecular Recognition, 12, 131-140  https://doi.org/10.1002/(SICI)1099-1352(199903/04)12:2<131::AID-JMR454>3.0.CO;2-M
 
Nickel Holger, Kawchuk Lawrence, Twyman Richard M., Zimmermann Sabine, Junghans Holger, Winter Stephan, Fischer Rainer, Prüfer Dirk (2008): Plantibody-mediated inhibition of the Potato leafroll virus P1 protein reduces virus accumulation. Virus Research, 136, 140-145  https://doi.org/10.1016/j.virusres.2008.05.001
 
Niehl Annette, Heinlein Manfred (2011): Cellular pathways for viral transport through plasmodesmata. Protoplasma, 248, 75-99  https://doi.org/10.1007/s00709-010-0246-1
 
Orecchia Martin, Nölke Greta, Saldarelli Pasquale, Dell’Orco Mariangela, Uhde-Holzem Kerstin, Sack Markus, Martelli Giovanni, Fischer Rainer, Schillberg Stefan (2008): Generation and characterization of a recombinant antibody fragment that binds to the coat protein of grapevine leafroll-associated virus 3. Archives of Virology, 153, 1075-1084  https://doi.org/10.1007/s00705-008-0100-3
 
Revets Hilde, De Baetselier Patrick, Muyldermans Serge (2005): Nanobodies as novel agents for cancer therapy. Expert Opinion on Biological Therapy, 5, 111-124  https://doi.org/10.1517/14712598.5.1.111
 
Schoelz James E., Harries Phillip A., Nelson Richard S. (2011): Intracellular Transport of Plant Viruses: Finding the Door out of the Cell. Molecular Plant, 4, 813-831  https://doi.org/10.1093/mp/ssr070
 
Shukla D.D., Ward C.W. (1989): Structure of potyvirus coat proteins and its application in the taxonomy of the potyvirus group. In: Maramorosch K., Murphy F.A., Aaron J.S.: Advances in Virus Research. Vol. 36. Academic Press: 273–314.
 
Simmons H.E., Dunham J.P., Zinn K.E., Munkvold G.P., Holmes E.C., Stephenson A.G. (2013): Zucchini yellow mosaic virus (ZYMV, Potyvirus): Vertical transmission, seed infection and cryptic infections. Virus Research, 176, 259-264  https://doi.org/10.1016/j.virusres.2013.06.016
 
Stijlemans Benoît, Caljon Guy, Natesan Senthil Kumar A., Saerens Dirk, Conrath Katja, Pérez-Morga David, Skepper Jeremy N., Nikolaou Alexandros, Brys Lea, Pays Etienne, Magez Stefan, Field Mark C., De Baetselier Patrick, Muyldermans Serge, Parsons Marilyn (2011): High Affinity Nanobodies against the Trypanosome brucei VSG Are Potent Trypanolytic Agents that Block Endocytosis. PLoS Pathogens, 7, e1002072-  https://doi.org/10.1371/journal.ppat.1002072
 
Teh Yi-Hui Audrey, Kavanagh Tony A. (2010): High-level expression of Camelid nanobodies in Nicotiana benthamiana. Transgenic Research, 19, 575-586  https://doi.org/10.1007/s11248-009-9338-0
 
Tilsner Jens, Oparka Karl J (2012): Missing links? — The connection between replication and movement of plant RNA viruses. Current Opinion in Virology, 2, 705-711  https://doi.org/10.1016/j.coviro.2012.09.007
 
Tobias H., Kulhmann, Gullner G. (2012): Recovery-type resistance to Zucchini yellow mosaic virus in oilseed pumpkin. In: Proceedings Xth EUCARPIA Meeting on Genetics and Breeding of Cucurbitaceae, Oct 15–18, 2012, Antalya, Turkey: 222–229.
 
Ueki Shoko, Spektor Roman, Natale Danielle M., Citovsky Vitaly, Ding Biao (2010): ANK, a Host Cytoplasmic Receptor for the Tobacco mosaic virus Cell-to-Cell Movement Protein, Facilitates Intercellular Transport through Plasmodesmata. PLoS Pathogens, 6, e1001201-  https://doi.org/10.1371/journal.ppat.1001201
 
Verheesen P, ten Haaft M.R, Lindner N, Verrips C.T, de Haard J.J.W (2003): Beneficial properties of single-domain antibody fragments for application in immunoaffinity purification and immuno-perfusion chromatography. Biochimica et Biophysica Acta (BBA) - General Subjects, 1624, 21-28  https://doi.org/10.1016/j.bbagen.2003.09.006
 
Vincke C., Gutierrez C., Wernery U., Devoogdt N., Hassanzadeh-Ghassabeh G., Muyldermans S. (2012): Generation of single domain antibody fragments derived from camelids and generation of manifold constructs. Methods in Molecular Biology, 907: 145–176.
 
Wesolowski Janusz, Alzogaray Vanina, Reyelt Jan, Unger Mandy, Juarez Karla, Urrutia Mariela, Cauerhff Ana, Danquah Welbeck, Rissiek Björn, Scheuplein Felix, Schwarz Nicole, Adriouch Sahil, Boyer Olivier, Seman Michel, Licea Alexei, Serreze David V., Goldbaum Fernando A., Haag Friedrich, Koch-Nolte Friedrich (2009): Single domain antibodies: promising experimental and therapeutic tools in infection and immunity. Medical Microbiology and Immunology, 198, 157-174  https://doi.org/10.1007/s00430-009-0116-7
 
Winichayakul Somrutai, Pernthaner Anton, Scott Richard, Vlaming Ruth, Roberts Nick (2009): Head-to-tail fusions of camelid antibodies can be expressed in planta and bind in rumen fluid. Biotechnology and Applied Biochemistry, 53, 111-  https://doi.org/10.1042/BA20080076
 
Zakri Adel M., Ziegler Angelika, Torrance Lesley, Fischer Rainer, Commandeur Ulrich (2010): Generation and characterization of a scFv against recombinant coat protein of the geminivirus tomato leaf curl New Delhi virus. Archives of Virology, 155, 335-342  https://doi.org/10.1007/s00705-010-0591-6
 
Zell R., Fritz H.J. (1987): DNA mismatch-repair in Escherichia coli counteracting the hydrolytic deamination of 5-methyl-cytosine residues. The EMBO Journal, 6: 1809–1815.
 
Ziegler Angelika, Torrance Lesley (2002): Applications of recombinant antibodies in plant pathology. Molecular Plant Pathology, 3, 401-407  https://doi.org/10.1046/j.1364-3703.2002.00130.x
 
ZIEGLER A., TORRANCE L., MACINTOSH S.M., COWAN G.H., MAYO M.A. (1995): Cucumber Mosaic Cucumovirus Antibodies from a Synthetic Phage Display Library. Virology, 214, 235-238  https://doi.org/10.1006/viro.1995.9935
 
download PDF

© 2020 Czech Academy of Agricultural Sciences