AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Nano Research Article
Article Link
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article

Tannic acid assisted anti-TNF-α nanobody assembly modulating the epithelial barrier dysregulation of allergic rhinitis

Shuilian Fu1,§, Zhiting Cao3,§, Baolian Huang3,§, Te Yin3, Chujun Huang1, Zhiqian Bi1, Yingying Yao1, Xiaoyao Chang1, Hongqin Zhuang1( ), Zi-Chun Hua1,2,3( )
The State Key Laboratory of Pharmaceutical Biotechnology, College of Life Sciences, Nanjing University, Nanjing 210023, China
Changzhou High-Tech Research Institute of Nanjing University and Jiangsu TargetPharma Laboratories Inc., Changzhou 213164, China
School of Biopharmacy, China Pharmaceutical University, Nanjing 211198, China

§ Shuilian Fu, Zhiting Cao, and Baolian Huang contributed equally to this work.

Show Author Information

Graphical Abstract

Tannic acid (TA) assisted anti-tumor necrosis factor-alpha (TNF-α) nanobody assembly (V/TA) could regulate tight junction proteins expression and restore epithelial barrier function, which played an important role in allergic rhinitis treatment.

Abstract

The derailed nasal epithelial barrier is associated with the disorder of tight junctions (TJ) function or expression, leading to more penetration of allergens to the barrier, accompanied by the release of cytokines, which develop allergic rhinitis (AR). Considering the increasing AR disease incidence worldwide, there is still an urgent unmet medical need to develop new therapeutics. Tumor necrosis factor-alpha (TNF-α) inhibitors have been applied in treating autoimmune diseases. However, their roles in AR remain unclear. In this study, anti-TNF-α nanobody (V) was assembled with tannic acid (V/TA) as a functional antibody drug candidate which could inhibit the release of the cytokines in ovalbumin (OVA)-induced AR murine model. Upon receiving V/TA treatment, the infiltration level of inflammatory cells, and the number of mucus-secreting cells and mast cells in the nasal mucosa recovered to a relatively normal level. Preliminary mechanism of action research revealed that the efficacy of V/TA was accompanied by the restricted level of TJ molecules: zonula occluden-1 (ZO-1), occludin, claudin-1, and claudin-5. The therapeutic effect of the anti-TNF-α nanobody against AR was enhanced with the tannic acid assisted without any toxicity observed. This study supplied a promising delivery strategy of TNF-α inhibitor for the effective treatment of complicated allergic rhinitis disease, with an advantage in restoring effect on the AR-caused epithelial barrier defects than the commercial drug Infliximab.

Keywords

allergic rhinitistumor necrosis factor-alpha (TNF-α) nanobodynanoparticlesepithelial permeabilitytight junctions

Electronic Supplementary Material

Download File(s)
12274_2023_5646_MOESM1_ESM.pdf (1.2 MB)

References

[1]

Okubo, K.; Kurono, Y.; Ichimura, K.; Enomoto, T.; Okamoto, Y.; Kawauchi, H.; Suzaki, H.; Fujieda, S.; Masuyama, K. The Japanese Society of Allergology. Japanese guidelines for allergic rhinitis 2020. Allergol. Int. 2020, 69, 331–345.
Crossref Google Scholar
[2]

Wheatley, L. M.; Togias, A. Allergic rhinitis. N. Engl. J. Med. 2015, 372, 456–463.
Crossref Google Scholar
[3]

Kanagaratham, C.; El Ansari, Y. S.; Sallis, B. F.; Hollister, B. M. A.; Lewis, O. L.; Minnicozzi, S. C.; Oyoshi, M. K.; Rosen, R.; Nurko, S.; Fiebiger, E. et al. Omeprazole inhibits IgE-mediated mast cell activation and allergic inflammation induced by ingested allergen in mice. J. Allergy Clin. Immunol. 2020, 146, 884–893.e5.
Crossref Google Scholar
[4]

Meng, Y. F.; Wang, C. S.; Zhang, L. Advances and novel developments in allergic rhinitis. Allergy 2020, 75, 3069–3076.
Crossref Google Scholar
[5]

Zhang, Y.; Lan, F.; Zhang, L. Advances and highlights in allergic rhinitis. Allergy 2021, 76, 3383–3389.
Crossref Google Scholar
[6]

Steelant, B.; Farré, R.; Wawrzyniak, P.; Belmans, J.; Dekimpe, E.; Vanheel, H.; Van Gerven, L.; Kortekaas Krohn, I.; Bullens, D. M. A.; Ceuppens, J. L. et al. Impaired barrier function in patients with house dust mite-induced allergic rhinitis is accompanied by decreased occludin and zonula occludens-1 expression. J. Allergy Clin. Immunol. 2016, 137, 1043–1053.e5.
Crossref Google Scholar
[7]

Steelant, B.; Wawrzyniak, P.; Martens, K.; Jonckheere, A. C.; Pugin, B.; Schrijvers, R.; Bullens, D. M.; Vanoirbeek, J. A.; Krawczyk, K.; Dreher, A. et al. Blocking histone deacetylase activity as a novel target for epithelial barrier defects in patients with allergic rhinitis. J. Allergy Clin. Immunol. 2019, 144, 1242–1253.e7.
Crossref Google Scholar
[8]

Goleva, E.; Berdyshev, E.; Leung, D. Y. M. Epithelial barrier repair and prevention of allergy. J. Clin. Invest. 2019, 129, 1463–1474.
Crossref Google Scholar
[9]

Siti Sarah, C. O.; Md Shukri, N.; Mohd Ashari, N. S.; Wong, K. K. Zonula occludens and nasal epithelial barrier integrity in allergic rhinitis. PeerJ 2020, 8, e9834.
Crossref Google Scholar
[10]

Wawrzyniak, P.; Wawrzyniak, M.; Wanke, K.; Sokolowska, M.; Bendelja, K.; Rückert, B.; Globinska, A.; Jakiela, B.; Kast, J. I.; Idzko, M. et al. Regulation of bronchial epithelial barrier integrity by type 2 cytokines and histone deacetylases in asthmatic patients. J. Allergy Clin. Immunol. 2017, 139, 93–103.
Crossref Google Scholar
[11]

Celebi Sözener, Z.; Cevhertas, L.; Nadeau, K.; Akdis, M.; Akdis, C. A. Environmental factors in epithelial barrier dysfunction. J. Allergy Clin. Immunol. 2020, 145, 1517–1528.
Crossref Google Scholar
[12]

Sugita, K.; Steer, C. A.; Martinez-Gonzalez, I.; Altunbulakli, C.; Morita, H.; Castro-Giner, F.; Kubo, T.; Wawrzyniak, P.; Rückert, B.; Sudo, K. et al. Type 2 innate lymphoid cells disrupt bronchial epithelial barrier integrity by targeting tight junctions through IL-13 in asthmatic patients. J. Allergy Clin. Immunol. 2018, 141, 300–310.e11.
Crossref Google Scholar
[13]

Romanowska-Próchnicka, K.; Felis-Giemza, A.; Olesińska, M.; Wojdasiewicz, P.; Paradowska-Gorycka, A.; Szukiewicz, D. The role of TNF-α and anti-TNF-α agents during preconception, pregnancy, and breastfeeding. Int. J. Mol. Sci. 2021, 22, 2922.
Crossref Google Scholar
[14]

Iwasaki, M.; Saito, K.; Takemura, M.; Sekikawa, K.; Fujii, H.; Yamada, Y.; Wada, H.; Mizuta, K.; Seishima, M.; Ito, Y. TNF-α contributes to the development of allergic rhinitis in mice. J. Allergy Clin. Immunol. 2003, 112, 134–140.
Crossref Google Scholar
[15]

Jang, D. I.; Lee, A. H.; Shin, H. Y.; Song, H. R.; Park, J. H.; Kang, T. B.; Lee, S. R.; Yang, S. H. The role of tumor necrosis factor alpha (TNF-α) in autoimmune disease and current TNF-α inhibitors in therapeutics. Int. J. Mol. Sci. 2021, 22, 2719.
Crossref Google Scholar
[16]

Steelant, B.; Seys, S. F.; Van Gerven, L.; Van Woensel, M.; Farré, R.; Wawrzyniak, P.; Kortekaas Krohn, I.; Bullens, D. M.; Talavera, K.; Raap, U. et al. Histamine and T helper cytokine-driven epithelial barrier dysfunction in allergic rhinitis. J. Allergy Clin. Immunol. 2018, 141, 951–963.e8.
Crossref Google Scholar
[17]

Hu, G. Z.; Zhu, X. L.; Wen, Z.; Wu, L. H.; He, D.; Wu, X. M.; Zhou, W. Y.; Hu, W. X. Therapeutic potential of combined anti-IL-1β IgY and anti-TNF-α IgY in guinea pigs with allergic rhinitis induced by ovalbumin. Int. Immunopharmacol. 2015, 25, 155–161.
Crossref Google Scholar
[18]

Hu, W. X.; Zhou, W. Y.; Zhu, X. L.; Wen, Z.; Wu, L. H.; Wu, X. M.; Wei, H. P.; Wang, W. D.; He, D.; Xiang, Q. et al. Anti-interleukin-1 beta/tumor necrosis factor-alpha IgY antibodies reduce pathological allergic responses in guinea pigs with allergic rhinitis. Mediators Inflamm. 2016, 2016, 3128182.
Crossref Google Scholar
[19]

Mo, J. H.; Kang, E. K.; Quan, S. H.; Rhee, C. S.; Lee, C. H.; Kim, D. Y. Anti-tumor necrosis factor-alpha treatment reduces allergic responses in an allergic rhinitis mouse model. Allergy 2011, 66, 279–286.
Crossref Google Scholar
[20]

Syversen, S. W.; Goll, G. L.; Jørgensen, K. K.; Sandanger, Ø.; Sexton, J.; Olsen, I. C.; Gehin, J. E.; Warren, D. J.; Brun, M. K.; Klaasen, R. A. et al. Effect of therapeutic drug monitoring vs standard therapy during infliximab induction on disease remission in patients with chronic immune-mediated inflammatory diseases: A randomized clinical trial. JAMA 2021, 325, 1744–1754.
Crossref Google Scholar
[21]

Nencini, F.; Vultaggio, A.; Pratesi, S.; Cammelli, D.; Milla, M.; Fiori, G.; Bagnoli, S.; Prignano, F.; Romagnani, S.; Maggi, E. et al. The kinetics of antidrug antibodies, drug levels, and clinical outcomes in infliximab-exposed patients with immune-mediated disorders. J. Allergy Clin. Immunol. Pract. 2018, 6, 2065–2072.e2.
Crossref Google Scholar
[22]

Li, R. Y.; Dai, T. T.; Tan, Y. B.; Fu, G. M.; Wan, Y.; Liu, C. M.; McClements, D. J. Fabrication of pea protein-tannic acid complexes: Impact on formation, stability, and digestion of flaxseed oil emulsions. Food Chem. 2020, 310, 125828.
Crossref Google Scholar
[23]

Wang, X. Y.; Yan, J. J.; Wang, L. Z.; Pan, D. H.; Xu, Y. P.; Wang, F.; Sheng, J.; Li, X. X.; Yang, M. Oral delivery of anti-TNF antibody shielded by natural polyphenol-mediated supramolecular assembly for inflammatory bowel disease therapy. Theranostics 2020, 10, 10808–10822.
Crossref Google Scholar
[24]

Xiong, H.; Wang, Z. H.; Wang, C.; Yao, J. Transforming complexity to simplicity: Protein-like nanotransformer for improving tumor drug delivery programmatically. Nano Lett. 2020, 20, 1781–1790.
Crossref Google Scholar
[25]

Shin, M.; Lee, H. A.; Lee, M.; Shin, Y.; Song, J. J.; Kang, S. W.; Nam, D. H.; Jeon, E. J.; Cho, M.; Do, M. et al. Targeting protein and peptide therapeutics to the heart via tannic acid modification. Nat. Biomed. Eng. 2018, 2, 304–317.
Crossref Google Scholar
[26]

Zheng, X.; Sun, C.; Yu, R. L.; Chu, X.; Xu, J. H.; Liu, C. C.; Zhao, M. Q.; Xu, X. L.; Xia, M.; Wang, C. CD13-specific ligand facilitates Xanthatin nanomedicine targeting dendritic cells for therapy of refractory allergic rhinitis. Int. J. Pharm. 2020, 577, 119034.
Crossref Google Scholar
[27]

Liang, X.; Cao, K. X.; Li, W.; Li, X. Q.; McClements, D. J.; Hu, K. Tannic acid-fortified zein-pectin nanoparticles: Stability, properties, antioxidant activity, and in vitro digestion. Food Res. Int. 2021, 145, 110425.
Crossref Google Scholar
[28]

Honda, Y.; Nomoto, T.; Matsui, M.; Takemoto, H.; Kaihara, Y.; Miura, Y.; Nishiyama, N. Sequential self-assembly using tannic acid and phenylboronic acid-modified copolymers for potential protein delivery. Biomacromolecules 2020, 21, 3826–3835.
Crossref Google Scholar
[29]

Zhang, W. C.; Zhang, Y. X.; Luo, Y. L.; Chen, S. B.; Huang, Q. Y.; Cao, Z. T.; Liang, M.; Yang, X. Z. A nanoconfined loading strategy for highly efficient siRNA delivery and cancer therapy. Nano Today 2022, 43, 101418.
Crossref Google Scholar
[30]

Cao, Z. Y.; Li, D. D.; Zhao, L.; Liu, M. T.; Ma, P. Y.; Luo, Y. L.; Yang, X. Z. Bioorthogonal in situ assembly of nanomedicines as drug depots for extracellular drug delivery. Nat. Commun. 2022, 13, 2038.
Crossref Google Scholar
[31]

Richter, F.; Zettlitz, K. A.; Seifert, O.; Herrmann, A.; Scheurich, P.; Pfizenmaier, K.; Kontermann, R. E. Monovalent TNF receptor 1-selective antibody with improved affinity and neutralizing activity. mAbs 2019, 11, 166–177.
Crossref Google Scholar
[32]

Thapa, R. K.; Choi, H. G.; Kim, J. O.; Yong, C. S. Analysis and optimization of drug solubility to improve pharmacokinetics. J. Pharm. Investig. 2017, 47, 95–110.
Crossref Google Scholar
[33]

Mendez-Barbero, N.; Yuste-Montalvo, A.; Nuñez-Borque, E.; Jensen, B. M.; Gutiérrez-Muñoz, C.; Tome-Amat, J.; Garrido-Arandia, M.; Díaz-Perales, A.; Ballesteros-Martinez, C.; Laguna, J. J. et al. The TNF-like weak inducer of the apoptosis/fibroblast growth factor-inducible molecule 14 axis mediates histamine and platelet-activating factor-induced subcutaneous vascular leakage and anaphylactic shock. J. Allergy Clin. Immunol. 2020, 145, 583–596.e6.
Crossref Google Scholar
[34]

Park, J. Y.; Choi, J. H.; Lee, S. N.; Cho, H. J.; Ahn, J. S.; Kim, Y. B.; Park, D. Y.; Park, S. C.; Kim, S. I.; Kang, M. J. et al. Protein arginine methyltransferase 1 contributes to the development of allergic rhinitis by promoting the production of epithelial-derived cytokines. J. Allergy Clin. Immunol. 2021, 147, 1720–1731.
Crossref Google Scholar
[35]

Eifan, A. O.; Durham, S. R. Pathogenesis of rhinitis. Clin. Exp. Allergy 2016, 46, 1139–1151.
Crossref Google Scholar
[36]

Shamji, M. H.; Sharif, H.; Layhadi, J. A.; Zhu, R. F.; Kishore, U.; Renz, H. Diverse immune mechanisms of allergen immunotherapy for allergic rhinitis with and without asthma. J. Allergy Clin. Immunol. 2022, 149, 791–801.
Crossref Google Scholar
[37]

Pothoven, K. L.; Schleimer, R. P. The barrier hypothesis and Oncostatin M: Restoration of epithelial barrier function as a novel therapeutic strategy for the treatment of type 2 inflammatory disease. Tissue Barriers 2017, 5, e1341367.
Crossref Google Scholar
[38]

Akdis, C. A. Does the epithelial barrier hypothesis explain the increase in allergy, autoimmunity and other chronic conditions. Nat. Rev. Immunol. 2021, 21, 739–751.
Crossref Google Scholar
[39]

Lee, H. J.; Kim, B.; Im, N. R.; Lee, D. Y.; Kim, H. K.; Lee, S. H.; Lee, H. M.; Lee, S. H.; Baek, S. K.; Kim, T. H. Decreased expression of E-cadherin and ZO-1 in the nasal mucosa of patients with allergic rhinitis: Altered regulation of E-cadherin by IL-4, IL-5, and TNF-alpha. Am. J. Rhinol. Allergy 2016, 30, 173–178.
Crossref Google Scholar
[40]

Hammad, H.; Lambrecht, B. N. Barrier epithelial cells and the control of type 2 immunity. Immunity 2015, 43, 29–40.
Crossref Google Scholar
[41]

Yazici, D.; Ogulur, I.; Kucukkase, O.; Li, M. R.; Rinaldi, A. O.; Pat, Y.; Wallimann, A.; Wawrocki, S.; Celebi Sozener, Z.; Buyuktiryaki, B. et al. Epithelial barrier hypothesis and the development of allergic and autoimmune diseases. Allergo J. Int. 2022, 31, 91–102.
Crossref Google Scholar
[42]

Huang, Z. Q.; Liu, J.; Ong, H. H.; Yuan, T.; Zhou, X. M.; Wang, J.; Tan, K. S.; Chow, V. T.; Yang, Q. T.; Shi, L. et al. Interleukin-13 alters tight junction proteins expression thereby compromising barrier function and dampens rhinovirus induced immune responses in nasal epithelium. Front. Cell Dev. Biol. 2020, 8, 572749.
Crossref Google Scholar
[43]

Saatian, B.; Rezaee, F.; Desando, S.; Emo, J.; Chapman, T.; Knowlden, S.; Georas, S. N. Interleukin-4 and interleukin-13 cause barrier dysfunction in human airway epithelial cells. Tissue Barriers 2013, 1, e24333.
Crossref Google Scholar
[44]

Tokumasu, R.; Yamaga, K.; Yamazaki, Y.; Murota, H.; Suzuki, K.; Tamura, A.; Bando, K.; Furuta, Y.; Katayama, I.; Tsukita, S. Dose-dependent role of claudin-1 in vivo in orchestrating features of atopic dermatitis. Proc. Natl. Acad. Sci. USA 2016, 113, E4061–E4068.
Crossref Google Scholar
[45]

Wang, J.; Kang, X.; Huang, Z. Q.; Shen, L.; Luo, Q.; Li, M. Y.; Luo, L. P.; Tu, J. H.; Han, M.; Ye, J. Protease-activated receptor-2 decreased zonula occlidens-1 and claudin-1 expression and induced epithelial barrier dysfunction in allergic rhinitis. Am. J. Rhinol. Allergy 2021, 35, 26–35.
Crossref Google Scholar
[46]

Nur Husna, S. M.; Tan, H. T. T.; Md Shukri, N.; Mohd Ashari, N. S.; Wong, K. K. Nasal epithelial barrier integrity and tight junctions disruption in allergic rhinitis: Overview and pathogenic insights. Front. Immunol. 2021, 12, 663626.
Crossref Google Scholar
[47]

Nitta, T.; Hata, M.; Gotoh, S.; Seo, Y.; Sasaki, H.; Hashimoto, N.; Furuse, M.; Tsukita, S. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J. Cell Biol. 2003, 161, 653–660.
Crossref Google Scholar
[48]

Markov, A. G.; Aschenbach, J. R.; Amasheh, S. Claudin clusters as determinants of epithelial barrier function. IUBMB Life 2015, 67, 29–35.
Crossref Google Scholar
Nano Research
Volume 16 Issue 7,
July 2023
Pages 9781-9791
DOI: 10.1007/s12274-023-5646-6
Cite this article:
Fu S, Cao Z, Huang B, et al. Tannic acid assisted anti-TNF-α nanobody assembly modulating the epithelial barrier dysregulation of allergic rhinitis. Nano Research, 2023, 16(7): 9781-9791. https://doi.org/10.1007/s12274-023-5646-6
Topics:
Drug deliveryDrug therapy

905

Views

4

Crossref

3

Web of Science

4

Scopus

0

CSCD

Altmetrics
Received: 15 December 2022
Revised: 27 February 2023
Accepted: 07 March 2023
Published: 14 April 2023
© Tsinghua University Press 2023
Return