Click-hydrogel delivered aggregation-induced emissive nanovesicles for simultaneous remodeling and antibiosis of deep burn wounds

  • Xu Chen 1 ,
  • Meijiao Zhao 2 ,
  • Qihu Xie 3 ,
  • Sitong Zhou 4 ,
  • Xiaoping Zhong 3 ,
  • Judun Zheng 2 ,
  • Ronghua Yang , 5 ,
  • Xianjin Du , 6 ,
  • Jinyu Xia , 1 ,
  • Yuhui Liao , 2
Expand
  • 1. Department of Infectious Diseases, The Fifth Affiliated Hospital, Sun Yat-sen University, Zhuhai, China
  • 2. Molecular Diagnosis and Treatment Center for Infectious Diseases, Dermatology Hospital, Southern Medical University, Guangzhou, China
  • 3. Department of Burns and Plastic Surgery, The Second Affiliated Hospital of Shantou University Medical College, Shantou, China
  • 4. Department of Dermatology, The, First People’s Hospital of Foshan, Foshan, China
  • 5. Department of Burn and Plastic Surgery, Guangzhou First People’s Hospital, South China University of Technology, Guangzhou, China
  • 6. Department of Critical Care Medicine, Renmin Hospital of Wuhan University, Wuhan, China
eyyangronghua@scut.edu.cn
duxianjin@whu.edu.cn
xiajinyu@mail.sysu.edu.cn
liaoyh8@mail.sysu.edu.cn

Received date: 27 Jul 2023

Accepted date: 08 Aug 2023

Copyright

2023 2023 The Authors. Aggregate published by SCUT, AIEI, and John Wiley & Sons Australia, Ltd.

Abstract

As a high-risk trauma, deep burns are always hindered in their repair process by decreased tissue regeneration capacity and persistent infections. In this study, we developed a simultaneous strategy for deep burn wounds treatment using functional nanovesicles with antibacterial and tissue remodeling properties, delivered via a click-chemistry hydrogel. An aggregation-induced emission photosensitizer of 4-(2-(5-(4-(diphenylamino)phenyl)thiophen-2-yl)vinyl)-1-(2-hydroxyethyl) pyridin-1-ium bromide (THB) with excellent photodynamic properties was first prepared, and then combined with readily accessible adipose stem cells-derived nanovesicles to generate the THB functionalized nanovesicles (THB@ANVs). The THB@ANVs showed strong antibacterial activity against Gram-positive bacteria (up to 100% killing rate), and also beneficial effects on tissue remodeling, including promoting cell migration, cell proliferation, and regulating immunity. In addition, we prepared a click-hydrogel of carboxymethyl chitosan for effective delivery of THB@ANVs on wounds. This hydrogel could be injected to conform to the wound morphology while responding to the acidic microenvironment. In vivo evaluations of wound healing revealed that the THB@ANVs hydrogel dressing efficiently accelerated the healing of second-degree burn wounds by reducing bacterial growth, regulating inflammation, promoting early angiogenesis, and collagen deposition. This study provides a promising candidate of wound dressing with diverse functions for deep burn wound repair.

Cite this article

Xu Chen , Meijiao Zhao , Qihu Xie , Sitong Zhou , Xiaoping Zhong , Judun Zheng , Ronghua Yang , Xianjin Du , Jinyu Xia , Yuhui Liao . Click-hydrogel delivered aggregation-induced emissive nanovesicles for simultaneous remodeling and antibiosis of deep burn wounds[J]. Aggregate, 2024 , 5(1) : 406 . DOI: 10.1002/agt2.406

1
V. Pavoni, L. Gianesello, L. Paparella, L. T. Buoninsegni, E. Barboni, Scand. J. Trauma Resusc. Emerg. Med. 2010, 18, 24.

2
Y. Yoshino, M. Ohtsuka, M. Kawaguchi, K. Sakai, A. Hashimoto, M. Hayashi, N. Madokoro, Y. Asano, M. Abe, T. Ishii, T. Isei, T. Ito, Y. Inoue, S. Imafuku, R. Irisawa, M. Ohtsuka, F. Ogawa, T. Kadono, T. Kawakami, R. Kukino, T. Kono, M. Kodera, M. Takahara, M. Tanioka, T. Nakanishi, Y. Nakamura, M. Hasegawa, M. Fujimoto, H. Fujiwara, T. Maekawa, K. Matsuo, O. Yamasaki, A. Le Pavoux, T. Tachibana, H. Ihn, J. Dermatol. 2016, 43, 989.

DOI

3
C. E. Salyer, C. Bomholt, N. Beckmann, C. B. Bergmann, C. A. Plattner, C. C. Caldwell, Surg. Infect. 2021, 22, 113.

DOI

4
M. P. Rowan, L. C. Cancio, E. A. Elster, D. M. Burmeister, L. F. Rose, S. Natesan, R. K. Chan, R. J. Christy, K. K. Chung, Crit. Care 2015, 19, 243.

5
L. Li, Z. Y. He, X. W. Wei, Y. Q. Wei, Regen. Biomater. 2016, 3, 99.

DOI

6
P. Everts, K. Onishi, P. Jayaram, J. F. Lana, K. Mautner, Int. J. Mol. Sci. 2020, 21, 7794.

DOI

7
Z. Li, P. Maitz, Burns Trauma 2018, 6, 13.

8
E. Coffin, A. Grangier, G. Perrod, M. Piffoux, I. Marangon, I. Boucenna, A. Berger, L. M’Harzi, J. Assouline, T. Lecomte, A. Chipont, C. Guérin, F. Gazeau, C. Wilhelm, C. Cellier, O. Clément, A. K. A. Silva, G. Rahmi, Nanoscale 2021, 13, 14866.

DOI

9
A. Shpichka, D. Butnaru, E. A. Bezrukov, R. B. Sukhanov, A. Atala, V. Burdukovskii, Y. Zhang, P. Timashev, Stem Cell Res. Ther. 2019, 10, 94.

10
R. Yang, F. Liu, J. Wang, X. Chen, J. Xie, K. Xiong, Stem Cell Res. Ther. 2019, 10, 229.

11
X. Sun, W. Song, L. Teng, Y. Huang, J. Liu, Y. Peng, X. Lu, J. Yuan, X. Zhao, Q. Zhao, Y. Xu, J. Shen, X. Peng, L. Ren, Bioact. Mater. 2022, 25, 640.

DOI

12
S. Rani, A. E. Ryan, M. D. Griffin, T. Ritter, Mol. Ther. 2015, 23, 812.

DOI

13
P. Hu, Q. Yang, Q. Wang, C. Shi, D. Wang, U. Armato, I. D. Pra, A. Chiarini, Burns Trauma 2019, 7, 38.

14
C. Liu, Y. Wang, L. Li, D. He, J. Chi, Q. Li, Y. Wu, Y. Zhao, S. Zhang, L. Wang, Z. Fan, Y. Liao. J. Control. Release 2022, 349, 679.

DOI

15
P. Guo, S. Busatto, J. Huang, G. Morad, M. A. Moses, Adv. Funct. Mater. 2021, 31, 2008326.

16
H. Wu, X. Jiang, Y. Li, Y. Zhou, T. Zhang, P. Zhi, J. Gao, Adv. Funct. Mater. 2020, 30, 2006169.

17
C. Hu, T. Lei, Y. Wang, J. Cao, X. Yang, L. Qin, R. Liu, Y. Zhou, F. Tong, C. S. Umeshappa, H. Gao, Biomaterials 2020, 255, 120159.

DOI

18
Y. Wen, Q. Fu, A. Soliwoda, S. Zhang, M. Zheng, W. Mao, Y. Wan, J. Extracell. Vesicles 2022, 1, 100004.

DOI

19
J. Li, H. Zhou, C. Liu, S. Zhang, R. Du, Y. Deng, X. Zou, Aggregate 2023, e359.

DOI

20
B. Li, W. Wang, L. Zhao, D. Yan, X. Li, Q. Gao, J. Zheng, S. Zhou, S. Lai, Y. Feng, J. Zhang, H. Jiang, C. Long, W. Gan, X. Chen, D. Wang, B. Z. Tang, Y. Liao, ACS Nano 2023, 17, 4601.

DOI

21
E. B. Souto, A. F. Ribeiro, M. I. Ferreira, M. C. Teixeira, A. A. M. Shimojo, J. L. Soriano, B. C. Naveros, A. Durazzo, M. Lucarini, S. B. Souto, A. Santini, Int. J. Mol. Sci. 2020, 21, 393.

DOI

22
G. Taubes, Science 2008, 321, 356.

DOI

23
J. Zhang, F. Zhou, Z. He, Y. Pan, S. Zhou, C. Yan, L. Luo, Y. Gao, ACS Appl. Mater. Interface 2022, 14, 30533.

DOI

24
J. Zheng, X. Long, H. Chen, Z. Ji, B. Shu, R. Yue, Y. Liao, S. Ma, K. Qiao, Y. Liu, Y. Liao, Front. Mol. Biosci. 2022, 9, 845179.

25
J. Sun, H. Li, X. Gu, B. Z. Tang, Adv. Healthc. Mater. 2021, 10, e2101177.

26
D. Zhu, Y. Duo, M. Suo, Y. Zhao, L. Xia, Z. Zheng, Y. Li, B. Z. Tang, Angew. Chem. Int. Ed. Engl 2020, 59, 13836.

DOI

27
K. Nuutila, E. Eriksson, Adv. Wound Care 2021, 10, 685.

DOI

28
C. Han, D. Jeong, B. Kim, W. Jo, H. Kang, S. Cho, K. H. Kim, J. Park, ACS Biomater. Sci. Eng. 2019, 5, 1534.

DOI

29
Y. Yao, A. Zhang, C. Yuan, X. Chen, Y. Liu, Biomater. Sci. 2021, 9, 4523.

DOI

30
H. Zhang, M. Song, C. Hu, Z. Zhang, S. Zhang, Y. Zhang, Y. Yang, P. Zhou, L. Zheng, L. Li, M. Mao, Y. S. Zhang, P. Ji, X. Zhang, Aggregate 2023, e332.

DOI

31
C. Owh, V. Ow, Q. Lin, J. H. M. Wong, D. Ho, X. J. Loh, K. Xue, Biomater. Adv. 2022, 141, 213100.

DOI

32
E. Coffin, A. Grangier, G. Perrod, M. Piffoux, I. Marangon, I. Boucenna, A. Berger, L. M’Harzi, J. Assouline, T. Lecomte, A. Chipont, C. Guerin, F. Gazeau, C. Wilhelm, C. Cellier, O. Clement, A. K. A. Silva, G. Rahmi, Nanoscale 2021, 13, 14866.

DOI

33
J. Huang, X. Jiang, ACS Appl. Mater. Inter. 2018, 10, 361.

DOI

34
C. Théry, S. Amigorena, G. Raposo, A. Clayton, Curr. Protoc. Cell Biol. 2006, Chapter 3:Unit 3.22, 1.

35
M. Kang, C. Zhou, S. Wu, B. Yu, Z. Zhang, N. Song, M. M. S. Lee, W. Xu, F. J. Xu, D. Wang, L. Wang, B. Z. Tang, J. Am. Chem. Soc. 2019, 141, 16781.

DOI

36
D. Wang, H. Su, R. T. K. Kwok, X. Hu, H. Zou, Q. Luo, M. M. S. Lee, W. Xu, J. W. Y. Lam, B. Z. Tang, Chem. Sci. 2018, 9, 3685.

DOI

37
J. Sun, Y. Bai, E. Y. Yu, G. Ding, H. Zhang, M. Duan, P. Huang, M. Zhang, H. Jin, R. T. Kwok, Y. Li, G. G. Shan, B. Z. Tang, H. Wang, Biomaterials 2022, 291, 121898.

DOI

38
M. S. Kim, M. J. Haney, Y. Zhao, V. Mahajan, I. Deygen, N. L. Klyachko, E. Inskoe, A. Piroyan, M. Sokolsky, O. Okolie, S. D. Hingtgen, A. V. Kabanov, E. V. Batrakova, Nanomedicine 2016, 12, 655.

DOI

39
Y. Xiong, Y. Xu, F. Zhou, Y. Hu, J. Zhao, Z. Liu, Q. Zhai, S. Qi, Z. Zhang, L. Chen, Bioeng. Transl. Med. 2023, 8, e10373.

40
H. Zhao, Q. Shang, Z. Pan, Y. Bai, Z. Li, H. Zhang, Q. Zhang, C. Guo, L. Zhang, Q. Wang, J. Diabetes 2018, 67, 235.

DOI

41
X. Bai, J. Li, L. Li, M. Liu, Y. Liu, M. Cao, K. Tao, S. Xie, D. Hu, Front. Immunol. 2020, 11, 1391.

42
C. Li, S. Wei, Q. Xu, Y. Sun, X. Ning, Z. Wang, Stem Cell Rev. Rep. 2022, 18, 952.

DOI

43
Y. An, S. Lin, X. Tan, S. Zhu, F. Nie, Y. Zhen, L. Gu, C. Zhang, B. Wang, W. Wei, D. Li, J. Wu, Cell Prolif. 2021, 54, e12993.

44
B. He, J. Zhang, J. Wang, Y. Wu, A. Qin, B. Z. Tang, Macromolecules 2020, 53, 5248.

DOI

45
X. Chen, T. Bai, R. Hu, B. Song, L. Lu, J. Ling, A. Qin, B. Z. Tang, Macromolecules 2020, 53, 2516.

DOI

46
M. He, L. Shi, G. Wang, Z. Cheng, L. Han, X. Zhang, C. Wang, J. Wang, P. Zhou, G. Wang, Int. J. Biol. Macromol. 2020, 155, 1245.

DOI

47
W. Denissen, G. Rivero, R. Nicolaÿ, L. Leibler, J. M. Winne, F. E. D. Prez, Adv. Funct. Mater. 2015, 25, 2451.

DOI

48
Z. Shariatinia, Int. J. Biol. Macromol. 2018, 120, 1406.

DOI

49
S. Mascharak, H. E desJardins-Park, M. F. Davitt, M. Griffin, M. R. Borrelli, A. L. Moore, K. Chen, B. Duoto, M. Chinta, D. S. Foster, A. H. Shen, M. Januszyk, S. H. Kwon, G. Wernig, D. C. Wan, H. P. Lorenz, G. C. Gurtner, M. T. Longaker, Science 2021, 372, eaba2374.

Options
Outlines

/