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Oral Administration of Hydrogel-Embedding Silk Sericin Alleviates Ulcerative Colitis through Wound Healing, Anti-Inflammation, and Anti-Oxidation

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    Oral Administration of Hydrogel-Embedding Silk Sericin Alleviates Ulcerative Colitis through Wound Healing, Anti-Inflammation, and Anti-Oxidation
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    • Ya Ma
      Ya Ma
      State Key Laboratory of Silkworm Genome Biology, School of Materials and Energy  and  Chongqing Key Laboratory of Soft-Matter Material Chemistry and Function Manufacturing, School of Materials and Energy, Southwest University, No. 2 Tiansheng Road, Beibei, Chongqing 400715, People’s Republic of China
      More by Ya Ma
    • Xiaoling Tong
      Xiaoling Tong
      State Key Laboratory of Silkworm Genome Biology, School of Materials and Energy  and  Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, College of Biotechnology, Southwest University, No. 2 Tiansheng Road, Beibei, Chongqing 400715, People’s Republic of China
      More by Xiaoling Tong
    • Yamei Huang
      Yamei Huang
      State Key Laboratory of Silkworm Genome Biology, School of Materials and Energy  and  Chongqing Key Laboratory of Soft-Matter Material Chemistry and Function Manufacturing, School of Materials and Energy, Southwest University, No. 2 Tiansheng Road, Beibei, Chongqing 400715, People’s Republic of China
      More by Yamei Huang
    • Xin Zhou
      Xin Zhou
      State Key Laboratory of Silkworm Genome Biology, School of Materials and Energy  and  Chongqing Key Laboratory of Soft-Matter Material Chemistry and Function Manufacturing, School of Materials and Energy, Southwest University, No. 2 Tiansheng Road, Beibei, Chongqing 400715, People’s Republic of China
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    • Chunhua Yang*
      Chunhua Yang
      Institute for Biomedical Sciences, Center for Diagnostics and Therapeutics, Georgia State University, 100 Piedmont Avenue SE, Atlanta, Georgia 30302, United States
      *Tel.: (404) 413-3597. Fax: (404) 413-3580. E-mail: [email protected]
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    • Jiucun Chen*
      Jiucun Chen
      Chongqing Key Laboratory of Soft-Matter Material Chemistry and Function Manufacturing, School of Materials and Energy, Southwest University, No. 2 Tiansheng Road, Beibei, Chongqing 400715, People’s Republic of China
      *Tel.: +86-23-6825-3204. Fax: +86-23-6825-4056. E-mail: [email protected]
      More by Jiucun Chen
      Orcidhttp://orcid.org/0000-0002-6677-2228
    • Fangyin Dai
      Fangyin Dai
      State Key Laboratory of Silkworm Genome Biology, School of Materials and Energy  and  Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, College of Biotechnology, Southwest University, No. 2 Tiansheng Road, Beibei, Chongqing 400715, People’s Republic of China
      More by Fangyin Dai
    • Bo Xiao*
      Bo Xiao
      State Key Laboratory of Silkworm Genome Biology, School of Materials and Energy  and  Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, College of Biotechnology, Southwest University, No. 2 Tiansheng Road, Beibei, Chongqing 400715, People’s Republic of China
      Institute for Biomedical Sciences, Center for Diagnostics and Therapeutics, Georgia State University, 100 Piedmont Avenue SE, Atlanta, Georgia 30302, United States
      *Tel.: +86-23-6825-3597. Fax: +86-23-6825-4056. E-mail: [email protected]
      More by Bo Xiao
      Orcidhttp://orcid.org/0000-0002-2992-6435
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    ACS Biomaterials Science & Engineering

    Cite this: ACS Biomater. Sci. Eng. 2019, 5, 11, 6231–6242
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsbiomaterials.9b00862
    Published October 8, 2019
    Copyright © 2019 American Chemical Society
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    Abstract

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    Silk sericin (SS) is abundant in silk industry wastewater, and it has emerged as a promising natural protein for biomedical research. However, its therapeutic potential against ulcerative colitis (UC) has not been exploited. The objective of this study is to investigate the therapeutic effects of SS in a dextran sulfate sodium-induced UC mouse model, and further discover its underlying mechanisms. The purified SS molecules showed negative cytotoxicity, and could be efficiently internalized by colonic epithelial cells and macrophages. In vitro experiments revealed that it could accelerate the mucosal healing, down-regulate the production of pro-inflammatory factors, increase the secretion of anti-inflammatory cytokines, and eliminate the intracellular reactive oxygen species. Finally, animal experiments confirmed that oral administration of hydrogel (chitosan/alginate)-embedding SS molecules attenuated UC-induced symptoms (e.g., body weight loss, colon shortening, increase of spleen weight, and histopathological appearance), which was supported by signs of mucosal healing, anti-inflammation, and elevation of the amounts of tight junction proteins (occludin and zonula occludens-1) and mucin protein (MUC2). Taken together, our results demonstrate that SS can be exploited as a promising oral natural therapeutic for UC treatment with the aid of hydrogel.

    Copyright © 2019 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsbiomaterials.9b00862.

    • Experimental description, fluorescence images of SS solutions, FTIR and UV–vis absorbance spectra, standard curve for the fluorescence intensity of FITC solution, standard curve for the fluorescence intensity of Cy7 solution, in vitro cytotoxicity, antioxidant activity of SS, fluorescence images of GIT and five major organs, in vivo biodistribution, and hemocompatibility of SS (PDF)

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    Cited By

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    This article is cited by 28 publications.

    1. Dona Deb, Bably Khatun, Bidyarani Devi M, Mojibur R. Khan, Neelotpal Sen Sarma, Kamatchi Sankaranarayanan. Utilizing Silk Sericin as a Biomaterial for Drug Encapsulation in a Hydrogel Matrix with Polycaprolactone: Formulation and Evaluation of Antibacterial Activity. ACS Omega 2024, 9 (30) , 32706-32716. https://doi.org/10.1021/acsomega.4c02453
    2. Ma Yu, Pengfei Tang, Youhong Tang, Cheng Wei, Zhenming Wang, Hongping Zhang. Breathable, Moisturizing, Anti-Oxidation SSD-PG-PVA/KGM Fibrous Membranes for Accelerating Diabetic Wound Tissue Regeneration. ACS Applied Bio Materials 2022, 5 (6) , 2894-2901. https://doi.org/10.1021/acsabm.2c00255
    3. Ya Ma, Lei Zhou, Chunhua Yang, Lingshuang Wang, Sixiong Yi, Xiaoling Tong, Bo Xiao, Jiucun Chen. Comparison of Sericins from Different Sources as Natural Therapeutics against Ulcerative Colitis. ACS Biomaterials Science & Engineering 2021, 7 (9) , 4626-4636. https://doi.org/10.1021/acsbiomaterials.1c00256
    4. Yongping Liang, Jiahui He, Baolin Guo. Functional Hydrogels as Wound Dressing to Enhance Wound Healing. ACS Nano 2021, 15 (8) , 12687-12722. https://doi.org/10.1021/acsnano.1c04206
    5. Jayavardhini Bhoopathy, Weslen Vedakumari Sathyaraj, Beryl Vedha Yesudhason, Selvarajan Rajendran, Sankari Dharmalingam, Jayashri Seetharaman, Ranjitha Muthu, Ramachandran Murugesan, Subramanian Raghunandhakumar, Suresh Kumar Anandasadagopan. Haemostatic potency of sodium alginate/aloe vera/sericin composite scaffolds – preparation, characterisation, and evaluation. Artificial Cells, Nanomedicine, and Biotechnology 2024, 52 (1) , 35-45. https://doi.org/10.1080/21691401.2023.2293784
    6. Yunong Yuan, Mohammad Nasri, Azadeh Manayi, Junying Zhang, Chunyong Wu, Tae-Joon Jeon, Lifeng Kang. Sericin coats of silk fibres, a degumming waste or future material?. Materials Today Bio 2024, 29 , 101306. https://doi.org/10.1016/j.mtbio.2024.101306
    7. Hongtao Zhu, Zhi-Jing Ni, Qian Zhong, Wei Wang, Ya-Jing An, Kiran Thakur, Jian-Guo Zhang, Zhong-Li Chen, Zhao-Jun Wei. Sericin peptides alleviate dextran sulfate-induced ulcerative colitis symptoms by modulating the Th17 cell differentiation pathway in C57BL/6 mice. Food Bioscience 2024, 62 , 105555. https://doi.org/10.1016/j.fbio.2024.105555
    8. Monika Prakash, Chandraprabha Mathikere Naganna, Vivek Radhakrishnan, Prathik Somayaji, Leah Sabu. Therapeutic potential of silkworm sericin in wound healing applications. Wound Repair and Regeneration 2024, 32 (6) , 916-940. https://doi.org/10.1111/wrr.13216
    9. Lan Jiang, Jia Li, Runkun Yang, Shunpeng Chen, Yongjun Wu, Yuanyuan Jin, Jiajia Wang, Qinjie Weng, Jincheng Wang. Effect of hydrogel drug delivery system for treating ulcerative colitis: A preclinical meta-analysis. International Journal of Pharmaceutics 2024, 659 , 124281. https://doi.org/10.1016/j.ijpharm.2024.124281
    10. Zicheng Yang, Rongyu Li, Ruonan Wang, Senhe Qian. Enhancing Healing of Infected Wounds with Glycerin‐Modified Sodium Alginate/Silk Sericin Composite Film Functionalized with Polygonatum sibiricum Polysaccharide‐Capped Silver Nanoparticles. ChemistrySelect 2024, 9 (14) https://doi.org/10.1002/slct.202400566
    11. Chunru Wang, Yingjie Xiang, Wenjie Ma, Chuanlong Guo, Xiaochen Wu. Therapeutic Potential Evaluation of Silk Sericin Stabilized Fisetin to Ulcerative Colitis. Macromolecular Bioscience 2024, 24 (2) https://doi.org/10.1002/mabi.202300277
    12. Yeshun Zhang, Susu Wang, Yurong Li, Xiang Li, Zhanyan Du, Siyu Liu, Yushuo Song, Yanyan Li, Guozheng Zhang. A Sterile, Injectable, and Robust Sericin Hydrogel Prepared by Degraded Sericin. Gels 2023, 9 (12) , 948. https://doi.org/10.3390/gels9120948
    13. Dinakar Swastha, Nambolan Varsha, Suresh Aravind, Kavassery Balasubramanian Samyuktha, Muruganandam Mohaneswari Yokesh, Akshad Balde, Bakthavatchalam Loganathan Ayilya, Soottawat Benjakul, Se-Kwon Kim, Rasool Abdul Nazeer. Alginate-based drug carrier systems to target inflammatory bowel disease: A review. International Journal of Biological Macromolecules 2023, 244 , 125472. https://doi.org/10.1016/j.ijbiomac.2023.125472
    14. Dongdong Liu, Meng Wei, Wenrui Yan, Hua Xie, Yingbao Sun, Bochuan Yuan, Yiguang Jin. Potential applications of drug delivery technologies against radiation enteritis. Expert Opinion on Drug Delivery 2023, 20 (4) , 435-455. https://doi.org/10.1080/17425247.2023.2183948
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    16. Sina Rahimpour, Hadi Jabbari, Hajar Yousofi, Arian Fathi, Shiva Mahmoodi, Mohammad Javad Jafarian, Navid Shomali, Siamak Sandoghchian Shotorbani. Regulatory effect of sericin protein in inflammatory pathways; A comprehensive review. Pathology - Research and Practice 2023, 243 , 154369. https://doi.org/10.1016/j.prp.2023.154369
    17. Yongliang Ouyang, Jiulong Zhao, Shige Wang. Multifunctional hydrogels based on chitosan, hyaluronic acid and other biological macromolecules for the treatment of inflammatory bowel disease: A review. International Journal of Biological Macromolecules 2023, 227 , 505-523. https://doi.org/10.1016/j.ijbiomac.2022.12.032
    18. Sehrish Ashraaf, Hafiz Muhammad Tahir, Chand Raza, Ezzat M Awad, Shaukat Ali, Shafaat Yar Khan, Talin Barisani-Asenbauer. Synergistic Effect of Silk Sericin and Curcumin to Treat an Inflammatory Condition. Journal of Burn Care & Research 2023, 44 (1) , 106-113. https://doi.org/10.1093/jbcr/irac157
    19. Doudou Hu, Tiandong Li, Wen’an Liang, Yeyuan Wang, Min Feng, Jingchen Sun. Silk sericin as building blocks of bioactive materials for advanced therapeutics. Journal of Controlled Release 2023, 353 , 303-316. https://doi.org/10.1016/j.jconrel.2022.11.019
    20. Chunru Wang, Junyao Li, Xiangsheng Han, Shuai Liu, Xintao Gao, Chuanlong Guo, Xiaochen Wu. Silk sericin stabilized proanthocyanidins for synergetic alleviation of ulcerative colitis. International Journal of Biological Macromolecules 2022, 220 , 1021-1030. https://doi.org/10.1016/j.ijbiomac.2022.08.134
    21. Chuanjin Yin, Xueju Qi, Shuhan Zhao, Xiangsheng Han, Chuanlong Guo, Xiaochen Wu. Natural silk fibers incorporated aramid nanofibers sponges for efficient oil/water separation. Colloids and Surfaces A: Physicochemical and Engineering Aspects 2022, 648 , 129323. https://doi.org/10.1016/j.colsurfa.2022.129323
    22. Sheng Xu, Qianqian Yang, Riyuan Wang, Chi Tian, Yanting Ji, Huanhuan Tan, Ping Zhao, David L. Kaplan, Feng Wang, Qingyou Xia. Genetically engineered pH-responsive silk sericin nanospheres with efficient therapeutic effect on ulcerative colitis. Acta Biomaterialia 2022, 144 , 81-95. https://doi.org/10.1016/j.actbio.2022.03.012
    23. Fayaz Ali, Imran Khan, Jianmin Chen, Kalsoom Akhtar, Esraa M. Bakhsh, Sher Bahadar Khan. Emerging Fabrication Strategies of Hydrogels and Its Applications. Gels 2022, 8 (4) , 205. https://doi.org/10.3390/gels8040205
    24. Ying Bai, Xing Chen, Hang Qi. Characterization and bioactivity of phlorotannin loaded protein-polysaccharide nanocomplexes. LWT 2022, 155 , 112998. https://doi.org/10.1016/j.lwt.2021.112998
    25. Ji-Xin Li, Shu-Xiang Zhao, Yu-Qing Zhang. Silk Protein Composite Bioinks and Their 3D Scaffolds and In Vitro Characterization. International Journal of Molecular Sciences 2022, 23 (2) , 910. https://doi.org/10.3390/ijms23020910
    26. Payal Kesharwani, Akansha Bisht, Amit Alexander, Vivek Dave, Swapnil Sharma. Biomedical applications of hydrogels in drug delivery system: An update. Journal of Drug Delivery Science and Technology 2021, 66 , 102914. https://doi.org/10.1016/j.jddst.2021.102914
    27. Yongkui Li, Ying Huang, Pan Pan, Xu Che, Yaru Zhang, Yeshun Zhang, Algahtany Amal, Xin Li, Wenjing Niu, Nachuan Luo, Wen Zhang, Daolong Gao, Qiuping Tan, Qiwei Zhang, Xiwen Xing, Zhen Luo, Jianguo Wu. Sericin and sericin-derived peptide alleviate viral pathogenesis in mice though inhibiting lactate production and facilitating antiviral response. Applied Materials Today 2021, 25 , 101256. https://doi.org/10.1016/j.apmt.2021.101256
    28. . Applications of Sericin. 2021, 101-130. https://doi.org/10.1002/9783527828760.ch3
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    ACS Biomaterials Science & Engineering

    Cite this: ACS Biomater. Sci. Eng. 2019, 5, 11, 6231–6242
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsbiomaterials.9b00862
    Published October 8, 2019
    Copyright © 2019 American Chemical Society
    Request reuse permissions

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