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Research Articles

Effective blocking of neuropilin-1activity using oligoclonal nanobodies targeting different epitopes

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References

  • Naderi, S.; Roshan, R.; Ghaderi, H.; Behdani, M.; Mahmoudi, S.; Habibi-Anbouhi, M.; Shokrgozar, M. A.; Kazemi-Lomedasht, F. Selection and Characterization of Specific Nanobody against Neuropilin-1 for Inhibition of Angiogenesis. Mol. Immunol. 2020, 128, 56–63. DOI: 10.1016/j.molimm.2020.10.004.
  • Guo, H.-F.; Vander Kooi, C. W. Neuropilin Functions as an Essential Cell Surface Receptor. J. Biol. Chem. 2015, 290, 29120–29126. DOI: 10.1074/jbc.R115.687327.
  • Leng, Q.; Woodle, M. C.; Mixson, A. J. NRP1 Transport of Cancer Therapeutics Mediated by Tumor-Penetrating Peptides. Drugs Future 2017, 42, 95–104. DOI: 10.1358/dof.2017.042.02.2564106.
  • Koch, S.; van Meeteren, L. A.; Morin, E.; Testini, C.; Weström, S.; Björkelund, H.; Le Jan, S.; Adler, J.; Berger, P.; Claesson-Welsh, L.; et al. NRP1 Presented in Trans to the Endothelium Arrests VEGFR2 Endocytosis, Preventing Angiogenic Signaling and Tumor Initiation. Dev. Cell. 2014, 28, 633–646. DOI: 10.1016/j.devcel.2014.02.010.
  • Tymecka, D.; Lipiński, P. F. J.; Fedorczyk, B.; Puszko, A.; Wileńska, B.; Perret, G. Y.; Misicka, A. Structure-Activity Relationship Study of Tetrapeptide Inhibitors of the Vascular Endothelial Growth Factor a Binding to Neuropilin-1. Peptides 2017, 94, 25–32. DOI: 10.1016/j.peptides.2017.06.003.
  • Jia, H.; Cheng, L.; Tickner, M.; Bagherzadeh, A.; Selwood, D.; Zachary, I. Neuropilin-1 Antagonism in Human Carcinoma Cells Inhibits Migration and Enhances Chemosensitivity. Br. J. Cancer. 2010, 102, 541–552. DOI: 10.1038/sj.bjc.6605539.
  • Raskopf, E.; Vogt, A.; Standop, J.; Sauerbruch, T.; Schmitz, V. Inhibition of Neuropilin-1 by RNA-Interference and Its Angiostatic Potential in the Treatment of Hepatocellular Carcinoma. Z Gastroenterol. 2010, 48, 21–27. DOI: 10.1055/s-0028-1109907.
  • Jarvis, A.; Allerston, C. K.; Jia, H.; Herzog, B.; Garza-Garcia, A.; Winfield, N.; Ellard, K.; Aqil, R.; Lynch, R.; Chapman, C.; et al. Small Molecule Inhibitors of the Neuropilin-1 Vascular Endothelial Growth Factor A (VEGF-A) Interaction. J. Med. Chem. 2010, 53, 2215–2226. DOI: 10.1021/jm901755g.
  • Pan, Q.; Chanthery, Y.; Liang, W.-C.; Stawicki, S.; Mak, J.; Rathore, N.; Tong, R. K.; Kowalski, J.; Yee, S. F.; Pacheco, G.; et al. Blocking Neuropilin-1 Function Has an Additive Effect with anti-VEGF to Inhibit Tumor Growth. Cancer Cell. 2007, 11, 53–67. DOI: 10.1016/j.ccr.2006.10.018.
  • Khodabakhsh, F.; Behdani, M.; Rami, A.; Kazemi-Lomedasht, F. Single-Domain Antibodies or Nanobodies: A Class of Next-Generation Antibodies. Int. Rev. Immunol. 2018, 37, 316–322. DOI: 10.1080/08830185.2018.1526932.
  • Schumacher, D.; Helma, J.; Schneider, A. F.; Leonhardt, H.; Hackenberger, C. P. Nanobodies: chemical Functionalization Strategies and Intracellular Applications. Angew. Chem. Int. Ed. Engl. 2018, 57, 2314–2333. DOI: 10.1002/anie.201708459.
  • Karami, E.; Sabatier, J.-M.; Behdani, M.; Irani, S.; Kazemi-Lomedasht, F. A Nanobody-Derived Mimotope against VEGF Inhibits Cancer Angiogenesis. J. Enzyme Inhib. Med. Chem. 2020, 35, 1233–1239. DOI: 10.1080/14756366.2020.1758690.
  • Jovčevska, I.; Muyldermans, S. The Therapeutic Potential of Nanobodies. BioDrugs 2020, 34, 11–26. DOI: 10.1007/s40259-019-00392-z.
  • Alirahimi, E.; Kazemi-Lomedasht, F.; Shahbazzadeh, D.; Habibi-Anbouhi, M.; Hosseininejad Chafi, M.; Sotoudeh, N.; Ghaderi, H.; Muyldermans, S.; Behdani, M. Nanobodies as Novel Therapeutic Agents in Envenomation. Biochim. Biophys. Acta. Gen. Subj. 2018, 1862, 2955–2965. DOI: 10.1016/j.bbagen.2018.08.019.
  • Muyldermans, S. Applications of Nanobodies. Annu. Rev. Anim. Biosci. 2021, 9, 401–421. DOI: 10.1146/annurev-animal-021419-083831.
  • Ahadi, M.; Ghasemian, H.; Behdani, M.; Kazemi-Lomedasht, F. Oligoclonal Selection of Nanobodies Targeting Vascular Endothelial Growth Factor. J. Immunotoxicol. 2019, 16, 34–42. DOI: 10.1080/1547691X.2018.1526234.
  • Stills, H. F. Polyclonal Antibody Production. The Laboratory Rabbit, Guinea Pig, Hamster, and Other Rodents. Elsevier: Amsterdam, 2012; pp. 259–274.
  • Farasat, A.; Rahbarizadeh, F.; Ahmadvand, D.; Ranjbar, S.; Khoshtinat Nikkhoi, S. Effective Suppression of Tumour Cells by Oligoclonal HER2-Targeted Delivery of Liposomal Doxorubicin. J. Liposome Res. 2019, 29, 53–65. DOI: 10.1080/08982104.2018.1430829.
  • Nikkhoi, S. K.; Rahbarizadeh, F.; Ahmadvand, D. Oligo-Clonal Nanobodies as an Innovative Targeting Agent for Cancer Therapy: New Biology and Novel Targeting Systems. Protein Expr. Purif. 2017, 129, 115–121. DOI: 10.1016/j.pep.2016.09.012.
  • Jamnani, F. R.; Rahbarizadeh, F.; Shokrgozar, M. A.; Ahmadvand, D.; Mahboudi, F.; Sharifzadeh, Z. Targeting High Affinity and Epitope-Distinct Oligoclonal Nanobodies to HER2 over-Expressing Tumor Cells. Exp. Cell Res. 2012, 318, 1112–1124. DOI: 10.1016/j.yexcr.2012.03.004.
  • Asadpour, O.; Rahbarizadeh, F. Phospholipase-Cγ1 Signaling Protein down-Regulation by Oligoclonal-VHHs Based Immuno-Liposome: A Potent Metastasis Deterrent in HER2 Positive Breast Cancer Cells. Cell J. 2020, 22, 30.
  • Ascoli, C. A.; Aggeler, B. Overlooked Benefits of Using Polyclonal Antibodies. Biotechniques. 2018, 65, 127–136. DOI: 10.2144/btn-2018-0065.
  • Newcombe, C.; Newcombe, A. R. Antibody Production: Polyclonal-Derived Biotherapeutics. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2007, 848, 2–7. DOI: 10.1016/j.jchromb.2006.07.004.
  • Kazemi-Lomedasht, F.; Behdani, M.; Pooshang Bagheri, K.; Habibi Anbouhi, M.; Abolhassani, M.; Khanahmad, H.; Shahbazzadeh, D.; Mirzahoseini, H. Expression and Purification of Functional Human Vascular Endothelial Growth Factor-a121; the Most Important Angiogenesis Factor. Adv. Pharm. Bull. 2014, 4, 323–328.
  • Kazemi-Lomedasht, F.; Behdani, M.; Bagheri, K. P.; Habibi-Anbouhi, M.; Abolhassani, M.; Arezumand, R.; Shahbazzadeh, D.; Mirzahoseini, H. Inhibition of Angiogenesis in Human Endothelial Cell Using VEGF Specific Nanobody. Mol. Immunol. 2015, 65, 58–67. DOI: 10.1016/j.molimm.2015.01.010.
  • Baharlou, R.; Tajik, N.; Behdani, M.; Shokrgozar, M. A.; Tavana, V.; Kazemi-Lomedasht, F.; Faraji, F.; Habibi-Anbouhi, M. An Antibody Fragment against Human Delta-like Ligand-4 for Inhibition of Cell Proliferation and Neovascularization. Immunopharmacol. Immunotoxicol. 2018, 40, 368–374. DOI: 10.1080/08923973.2018.1505907.
  • Sotoudeh, N.; Noormohammadi, Z.; Habibi-Anbouhi, M.; Kazemi-Lomedasht, F.; Behdani, M. Developing and Characterizing a Single-Domain Antibody (Nanobody) against Human Cytotoxic T-Lymphocyte-Associated Protein 4 (hCTLA-4). Iran. J. Basic Med. Sci. 2021, 24, 1264–1271.
  • Oghalaie, A.; Mahboudi, F.; Rahimi-Jamnani, F.; Piri-Gavgani, S.; Kazemi-Lomedasht, F.; Hassanzadeh Eskafi, A.; Shahbazzadeh, D.; Adeli, A.; Talebkhan, Y.; Behdani, M.; et al. Development and Characterization of Single Domain Monoclonal Antibody against Programmed Cell Death Ligand-1; as a Cancer Inhibitor Candidate. Iran. J. Basic Med. Sci. 2022, 25, 313–319.
  • Ghaderi, H.; Noormohammadi, Z.; Habibi-Anbouhi, M.; Kazemi-Lomedasht, F.; Behdani, M. Development of Camelid Monoclonal Nanobody against SLC39A6 Zinc Transporter Protein. Iran. J. Basic Med. Sci. 2021, 24, 1726–1733.
  • Faraji, F.; Habibi-Anbouhi, M.; Behdani, M.; Kazemi-Lomedasht, F.; Shokrgozar, M. A.; Zarnani, A.-H.; Tajik, N. Functional Study of a Camelid Single Domain Anti-CD22 Antibody. Int. J. Pept. Res. Ther. 2020, 26, 633–639. DOI: 10.1007/s10989-019-09870-y.
  • Hosseininejad-Chafi, M.; Alirahimi, E.; Ramezani, B.; Oghalaie, A.; Sotoudeh, N.; Ghaderi, H.; Kazemi-Lomedasht, F.; Habibi-Anbouhi, M.; Moazzami, R.; Behdani, M.; et al. In Vivo Solid Tumor Targeting with Recombinant VEGF-Diphtheria Immunotoxin. Iran. J. Basic Med. Sci. 2022, 25, 27–31. DOI: 10.22038/IJBMS.2021.54293.12195.
  • Alirahimi, E.; Ashkiyan, A.; Kazemi-Lomedasht, F.; Azadmanesh, K.; Hosseininejad-Chafi, M.; Habibi-Anbouhi, M.; Moazami, R.; Behdani, M. Intrabody Targeting Vascular Endothelial Growth Factor Receptor-2 Mediates Downregulation of Surface Localization. Cancer Gene Ther. 2017, 24, 33–37. DOI: 10.1038/cgt.2016.76.
  • Bagheri, M.; Babaei, E.; Shahbazzadeh, D.; Habibi-Anbouhi, M.; Alirahimi, E.; Kazemi-Lomedasht, F.; Behdani, M. Development of a Recombinant Camelid Specific Diabody against the Heminecrolysin Fraction of Hemiscorpius lepturus Scorpion. Toxin Rev. 2017, 36, 7–11. DOI: 10.1080/15569543.2016.1244552.
  • Beatty, J. D.; Beatty, B. G.; Vlahos, W. G. Measurement of Monoclonal Antibody Affinity by Non-Competitive Enzyme Immunoassay. J. Immunol. Methods. 1987, 100, 173–179. DOI: 10.1016/0022-1759(87)90187-6.
  • Karami, E.; Naderi, S.; Roshan, R.; Behdani, M.; Kazemi-Lomedasht, F. Targeted Therapy of Angiogenesis Using Anti-VEGFR2 and anti-NRP-1 Nanobodies. Cancer Chemother. Pharmacol. 2022, 89, 165–168. DOI: 10.1007/s00280-021-04372-5.
  • Sotoudeh, N.; Noormohammadi, Z.; Habibi-Anbouhi, M.; Kazemi-Lomedasht, F.; Behdani, M. Evaluation of Laboratory Application of Camelid Sera Containing Heavy-Chain Polyclonal Antibody against Recombinant Cytotoxic T-Lymphocyte-Associated Protein-4. Monoclon. Antib. Immunodiagn. Immunother. 2019, 38, 235–241. DOI: 10.1089/mab.2019.0031.
  • Naderi, S.; Roshan, R.; Behdani, M.; Kazemi-Lomedasht, F. Inhibition of Neovascularisation in Human Endothelial Cells Using anti NRP-1 Nanobody Fused to Truncated Form of Diphtheria Toxin as a Novel Immunotoxin. Immunopharmacol. Immunotoxicol. 2021, 43, 230–238. DOI: 10.1080/08923973.2021.1888114.
  • Mohseni, N.; Roshan, R.; Naderi, S.; Behdani, M.; Kazemi-Lomedasht, F. In Vitro Combination Therapy of Pathologic Angiogenesis Using Anti-Vascular Endothelial Growth Factor and anti-Neuropilin-1 Nanobodies. Iran. J. Basic Med. Sci. 2020, 23, 1335–1339.
  • Papetti, M.; Herman, I. M. Mechanisms of Normal and Tumor-Derived Angiogenesis. Am. J. Physiol. Cell Physiol. 2002, 282, C947–C70. DOI: 10.1152/ajpcell.00389.2001.
  • Raimondi, C.; Brash, J. T.; Fantin, A.; Ruhrberg, C. NRP1 Function and Targeting in Neurovascular Development and Eye Disease. Prog. Retin. Eye Res. 2016, 52, 64–83. DOI: 10.1016/j.preteyeres.2016.02.003.
  • Gagnon, M. L.; Bielenberg, D. R.; Gechtman, Z.; Miao, H. Q.; Takashima, S.; Soker, S.; Klagsbrun, M. Identification of a Natural Soluble Neuropilin-1 That Binds Vascular Endothelial Growth Factor: In Vivo Expression and Antitumor Activity. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 2573–2578. DOI: 10.1073/pnas.040337597.
  • Kawasaki, T.; Kitsukawa, T.; Bekku, Y.; Matsuda, Y.; Sanbo, M.; Yagi, T.; Fujisawa, H. A Requirement for Neuropilin-1 in Embryonic Vessel Formation. Development 1999, 126, 4895–4902. DOI: 10.1242/dev.126.21.4895.
  • Rizzolio, S.; Cagnoni, G.; Battistini, C.; Bonelli, S.; Isella, C.; Van Ginderachter, J. A.; Bernards, R.; Di Nicolantonio, F.; Giordano, S.; Tamagnone, L.; et al. Neuropilin-1 Upregulation Elicits Adaptive Resistance to Oncogene-Targeted Therapies. J. Clin. Invest. 2018, 128, 3976–3990. DOI: 10.1172/JCI99257.
  • Abulrob, A.; Sprong, H.; En Henegouwen, P. V. B.; Stanimirovic, D. The Blood–Brain Barrier Transmigrating Single Domain Antibody: Mechanisms of Transport and Antigenic Epitopes in Human Brain Endothelial Cells. J. Neurochem. 2005, 95, 1201–1214. DOI: 10.1111/j.1471-4159.2005.03463.x.
  • Nguyen, V.; Su, C.; Muyldermans, S.; Van Der Loo, W. Heavy-Chain Antibodies in Camelidae; A Case of Evolutionary Innovation. Immunogenetics 2002, 54, 39–47. DOI: 10.1007/s00251-002-0433-0.
  • Roshan, R.; Naderi, S.; Behdani, M.; Cohan, R. A.; Ghaderi, H.; Shokrgozar, M. A.; Golkar, M.; Kazemi-Lomedasht, F. Isolation and Characterization of Nanobodies against Epithelial Cell Adhesion Molecule as Novel Theranostic Agents for Cancer Therapy. Mol. Immunol. 2021, 129, 70–77. DOI: 10.1016/j.molimm.2020.10.021.
  • Haurum, J. S. Recombinant Polyclonal Antibodies: The Next Generation of Antibody Therapeutics? Drug Discov. Today 2006, 11, 655–660. DOI: 10.1016/j.drudis.2006.05.009.
  • Kheddo, P.; Tracka, M.; Armer, J.; Dearman, R. J.; Uddin, S.; van der Walle, C. F.; Golovanov, A. P. The Effect of Arginine Glutamate on the Stability of Monoclonal Antibodies in Solution. Int. J. Pharm. 2014, 473, 126–133. DOI: 10.1016/j.ijpharm.2014.06.053.
  • Carter, P. J.; Lazar, G. A. Next Generation Antibody Drugs: Pursuit of the “High-Hanging Fruit.” Nat. Rev. Drug Discov. 2018, 17, 197–223. DOI: 10.1038/nrd.2017.227.
  • Shapiro, H. M. Practical Flow Cytometry. John Wiley & Sons: New York, 2005.
  • Auerbach, R.; Lewis, R.; Shinners, B.; Kubai, L.; Akhtar, N. Angiogenesis Assays: A Critical Overview. Clin. Chem. 2003, 49, 32–40. DOI: 10.1373/49.1.32.
  • Arnaoutova, I.; Kleinman, H. K. In Vitro Angiogenesis: endothelial Cell Tube Formation on Gelled Basement Membrane Extract. Nat. Protoc. 2010, 5, 628–635. DOI: 10.1038/nprot.2010.6.
  • Sadeghi, A.; Behdani, M.; Muyldermans, S.; Habibi‐Anbouhi, M.; Kazemi‐Lomedasht, F. Development of a Mono‐Specific anti‐VEGF Bivalent Nanobody with Extended Plasma Half‐Life for Treatment of Pathologic Neovascularization. Drug Test. Anal. 2020, 12, 92–100. DOI: 10.1002/dta.2693.

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