Programmable Artificial Skins Accomplish Antiscar Healing with Multiple Appendage Regeneration.

DNA supramolecular hydrogel microenvironment scar skin appendage regeneration wound healing

Journal

Advanced materials (Deerfield Beach, Fla.)
ISSN: 1521-4095
Titre abrégé: Adv Mater
Pays: Germany
ID NLM: 9885358

Informations de publication

Date de publication:
25 Oct 2024
Historique:
revised: 21 08 2024
received: 22 05 2024
medline: 26 10 2024
pubmed: 26 10 2024
entrez: 26 10 2024
Statut: aheadofprint

Résumé

Functional appendage regeneration is essential for skin rehabilitation, but it has always failed by current existing healing approaches, owing to their inefficacy in preventing disfiguring scars. In this study, a novel regeneration-directing artificial skin (RDAS) system is presented, which is based on the rational design of multi-layered hydrogels that closely mimic natural skin matrices. By leveraging the programmability and architectural rigidity of DNA components, without the need for exogenous cell transplantation, such RDAS effectively minimizes tissue fibrosis by accurately guiding the regenerative process in wound fibroblasts, enabling rapid scarless wound repair, restoration of dermal function, and successful in situ regeneration of multiple appendages, such as hair follicles (HFs), sebaceous glands (SGs), and sweat glands (SwGs). Therefore, the RDAS offers a cell-free antiscarring therapeutic strategy for regenerative wound healing, resulting in improved outcomes. This innovative approach holds great potential for future clinical applications and burn rehabilitation.

Identifiants

pubmed: 39460410
doi: 10.1002/adma.202407322
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2407322

Subventions

Organisme : National Natural Science Foundation of China
ID : 92268206
Organisme : National Basic Research Plan of China
ID : 2023YFA0915201
Organisme : Beijing Municipal Science & Technology Commission and Zhongguancun Science Park Administrative Committee
ID : Z231100007223003
Organisme : CAMS Innovation Fund for Medical Sciences
ID : CIFMS 2019-I2M-5-059
Organisme : Military Medical Research Projects
ID : 2023-JSKY-SSQG-006
Organisme : Independent Research Project of State Key Laboratory of Trauma and Chemical Poisoning
Organisme : National Key Research and Development Program of China
ID : 2023YFC3011900
Organisme : Specific Research Fund of The Innovation Platform for Academicians of Hainan Province
ID : YSPTZX202317

Informations de copyright

© 2024 Wiley‐VCH GmbH.

Références

P. D'Arpa, K. P. Leung, Adv. Wound Care 2022, 11, 428.
C. Zhang, D. Yang, T.‐B. Wang, X. Nie, G. Chen, L.‐H. Wang, Y.‐Z. You, Q. Wang, Biomater. Sci. 2023, 11, 288.
L. B. Baker, Temp 2019, 6, 211.
W. H. G. Lv, M. Wu, Y. P. G. Ren, X. Luo, W. J. Hu, Q. Zhang, Y. P. G. Wu, Mol. Med. Rep. 2021, 23, 1.
L. R. Jones, W. Young, G. Divine, I. Datta, K. M. Chen, D. Ozog, M. J. Worsham, Dis. Markers 2015, 2015, 943176.
C. C. Finnerty, M. G. Jeschke, L. K. Branski, J. P. Barret, P. Dziewulski, D. N. Herndon, Lancet 2016, 388, 1427.
D. Parry, K. Allison, Scars, Burn. Heal. 2022, 8, 205951312210953.
H. S. Kim, X. Sun, J.‐H. Lee, H.‐W. Kim, X. Fu, K. W. Leong, Adv. Drug Deliv. Rev. 2019, 146, 209.
F. Berthiaume, H. C. Hsia, Annu. Rev. Biomed. Eng. 2022, 24, 61.
S. Hinderer, S. L. Layland, K. Schenke‐Layland, Adv. Drug Deliv. Rev. 2016, 97, 260.
M. Hosseini, K. R. Koehler, A. Shafiee, Adv. Healthcare Mater. 2022, 11, 2201626.
K. M. Yamada, M. Sixt, Nat. Rev. Mol. Cell Biol. 2019, 20, 738.
V. Ajeti, A. P. Tabatabai, A. J. Fleszar, M. F. Staddon, D. S. Seara, C. Suarez, M. S. Yousafzai, D. Bi, D. R. Kovar, S. Banerjee, M. P. Murrell, Nat. Phys. 2019, 15, 696.
M. Zhao, L. Wang, M. Wang, S. Zhou, Y. Lu, H. Cui, A. C. Racanelli, L. Zhang, T. Ye, B. Ding, B. Zhang, J. Yang, Y. Yao, Signal Transduct. Target. Ther. 2022, 7, 206.
M. D'Urso, N. A. Kurniawan, Front. Bioeng. Biotechnol. 2020, 8, 609653.
A. Desmouliere, I. A. Darby, B. Laverdet, F. Bonté, Clin. Cosmet. Investig. Dermatol. 2014, 7, 301.
G. S. Schultz, J. M. Davidson, R. S. Kirsner, P. Bornstein, I. M. Herman, Wound Repair Regen. 2011, 19, 134.
T. Kageyama, A. Shimizu, R. Anakama, R. Nakajima, K. Suzuki, Y. Okubo, J. Fukuda, Sci. Adv. 2022, 8, eadd4603.
S. Yui, L. Azzolin, M. Maimets, M. T. Pedersen, R. P. Fordham, S. L. Hansen, H. L. Larsen, J. Guiu, M. R. P. Alves, C. F. Rundsten, J. V. Johansen, Y. Li, C. D. Madsen, T. Nakamura, M. Watanabe, O. H. Nielsen, P. J. Schweiger, S. Piccolo, K. B. Jensen, Cell Stem Cell 2018, 22, 35.
D. Jiang, D. Correa‐Gallegos, S. Christ, A. Stefanska, J. Liu, P. Ramesh, V. Rajendran, M. M. De Santis, D. E. Wagner, Y. Rinkevich, Nat. Cell Biol. 2018, 20, 422.
O. Maller, C. C. DuFort, V. M. Weaver, Nat. Cell Biol. 2013, 15, 570.
S. Mascharak, H. E. des Jardins‐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, 2374.
S. Liu, Z. Luan, T. Wang, K. Xu, Q. Luo, S. Ye, W. Wang, R. Dan, Z. Shu, Y. Huang, K. Mequanint, C. Fan, M. Xing, S. Yang, ACS Nano 2023, 17, 111.
Z. Wang, W. Li, L. Gou, Y. Zhou, G. Peng, J. Zhang, J. Liu, R. Li, H. Ni, W. Zhang, T. Cao, Q. Cao, H. Su, Y. Han, N. Tong, X. Fu, E. Ilegems, Y. Lu, P. Berggren, X. Zheng, C. Wang, Adv. Healthcare Mater. 2022, 11, 2200782.
F. Mo, K. Jiang, D. Zhao, Y. Wang, J. Song, W. Tan, Adv. Drug Delivery Rev. 2021, 168, 79.
L. Zhou, W. Pi, S. Cheng, Z. Gu, K. Zhang, T. Min, W. Zhang, H. Du, P. Zhang, Y. Wen, Adv. Funct. Mater. 2021, 31, 2106167.
J. Wu, B. R. Liyarita, H. Zhu, M. Liu, X. Hu, F. Shao, ACS Appl. Mater. Interfaces 2021, 13, 49705.
T. Yuan, Y. Shao, X. Zhou, Q. Liu, Z. Zhu, B. Zhou, Y. Dong, N. Stephanopoulos, S. Gui, H. Yan, D. Liu, Adv. Mater. 2021, 33, 2102428.
B. Zhou, B. Yang, Q. Liu, L. Jin, Y. Shao, T. Yuan, Y. N. Zhang, C. Wang, Z. Shi, X. Li, Y. Pan, N. Qiao, J. F. Xu, Y. R. Yang, Y. Dong, L. Xu, S. Gui, D. Liu, J. Am. Chem. Soc. 2023, 145, 8954.
L. Zhou, X. Jiao, S. Liu, M. Hao, S. Cheng, P. Zhang, Y. Wen, J. Mater. Chem. B 2020, 8, 1991.
Y. Wei, K. Wang, S. Luo, F. Li, X. Zuo, C. Fan, Q. Li, Small 2022, 18, 2107640.
S. Mascharak, H. E. Talbott, M. Januszyk, M. Griffin, K. Chen, M. F. Davitt, J. Demeter, D. Henn, C. A. Bonham, D. S. Foster, N. Mooney, R. Cheng, P. K. Jackson, D. C. Wan, G. C. Gurtner, M. T. Longaker, Cell Stem Cell 2022, 29, 315.
M. Hosseini, A. Shafiee, Small 2021, 17, 2101384.
V. S. Meli, H. Atcha, P. K. Veerasubramanian, R. R. Nagalla, T. U. Luu, E. Y. Chen, C. F. Guerrero‐Juarez, K. Yamaga, W. Pandori, J. Y. Hsieh, T. L. Downing, D. A. Fruman, M. B. Lodoen, M. V. Plikus, W. Wang, W. F. Liu, Sci. Adv. 2020, 6, 8471.
K. Yang, J. Xu, M. Fan, F. Tu, X. Wang, T. Ha, D. L. Williams, C. Li, Front. Immunol. 2020, 11, 587913.
J. Y. Hsieh, T. D. Smith, V. S. Meli, T. N. Tran, E. L. Botvinick, W. F. Liu, Acta Biomater. 2017, 47, 14.
L. He, J.‐H. Jhong, Q. Chen, K.‐Y. Huang, K. Strittmatter, J. Kreuzer, M. DeRan, X. Wu, T.‐Y. Lee, N. Slavov, W. Haas, A. G. Marneros, Cell Rep. 2021, 37, 109955.
D. Y. Shu, F. J. Lovicu, Prog. Retinal Eye Res. 2017, 60, 44.
T. Panciera, L. Azzolin, M. Cordenonsi, S. Piccolo, Nat. Rev. Mol. Cell Biol. 2017, 18, 758.
H. E. Talbott, S. Mascharak, M. Griffin, D. C. Wan, M. T. Longaker, Cell Stem Cell 2022, 29, 1161.
T. Zhu, Z. Ma, H. Wang, X. Jia, Y. Wu, L. Fu, Z. Li, C. Zhang, G. Yu, Mol. Cell. Biochem. 2020, 475, 137.
K. L. Spiller, S. Nassiri, C. E. Witherel, R. R. Anfang, J. Ng, K. R. Nakazawa, T. Yu, G. Vunjak‐Novakovic, Biomaterials 2015, 37, 194.
Y. Cai, K. Chen, C. Liu, X. Qu, Bioact. Mater. 2023, 28, 243.
N. Gao, L. Lu, X. Ma, Z. Liu, S. Yang, G. Han, Exp. Dermatol. 2022, 31, 320.
Y. Zhang, S. Wang, Y. Yang, S. Zhao, J. You, J. Wang, J. Cai, H. Wang, J. Wang, W. Zhang, J. Yu, C. Han, Y. Zhang, Z. Gu, Nat. Commun. 2023, 14, 3431.
Y. G. Kamberov, E. K. Karlsson, G. L. Kamberova, D. E. Lieberman, P. C. Sabeti, B. A. Morgan, C. J. Tabin, Proc. Natl. Acad. Sci. 2015, 112, 9932.
Z. Chen, J. Zhao, Y. Yan, L. Zhang, L. Du, X. Liu, M. Cao, C. Wang, Y. Tang, H. Li, BMC Vet. Res. 2022, 18, 316.
Z. Liu, J. Huang, D. Kang, Y. Zhou, L. Du, Q. Qu, J. Wang, L. Wen, D. Fu, Z. Hu, Y. Miao, Acta Biomater. 2023, 165, 31.
C. Lu, E. Fuchs, Cold Spring Harb. Perspect. Med. 2014, 4, a015222.
C. P. Lu, L. Polak, B. E. Keyes, E. Fuchs, Science 2016, 354, 6102.
H. L. Dingwall, R. R. Tomizawa, A. Aharoni, P. Hu, Q. Qiu, B. Kokalari, S. M. Martinez, J. C. Donahue, D. Aldea, M. Mendoza, I. A. Glass, H. Wu, Y. G. Kamberov, Dev. Cell 2023, 59, p20.
C. P. Lu, L. Polak, A. S. Rocha, H. A. Pasolli, S. Chen, N. Sharma, C. Blanpain, E. Fuchs, Cell 2012, 150, 136.
X. Sun, J. Xiang, R. Chen, Z. Geng, L. Wang, Y. Liu, S. Ji, H. Chen, Y. Li, C. Zhang, P. Liu, T. Yue, L. Dong, X. Fu, Adv. Sci. 2021, 8, e2103079.
H. Gao, Y. Liu, Z. Shi, H. Zhang, M. Wang, H. Chen, Y. Li, S. Ji, J. Xiang, W. Pi, L. Zhou, Y. Hong, L. Wu, A. Cai, X. Fu, X. Sun, Burn. Trauma 2023, 11, tkad027.

Auteurs

Mingchen Xiong (M)

Research Center for Tissue Repair and Regeneration affiliated to the Medical Innovation Research Department, PLA General Hospital and PLA Medical College, Beijing, 100048, P. R. China.
State Key Laboratory of Trauma and Chemical Poisoning, Beijing, 100048, P. R. China.
PLA Key Laboratory of Tissue Repair and Regenerative Medicine and Beijing Key Research Laboratory of Skin Injury, Repair and Regeneration, Beijing, 100048, P. R. China.
Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU051, Beijing, 100048, P. R. China.

Xinling Yang (X)

Research Center for Tissue Repair and Regeneration affiliated to the Medical Innovation Research Department, PLA General Hospital and PLA Medical College, Beijing, 100048, P. R. China.
State Key Laboratory of Trauma and Chemical Poisoning, Beijing, 100048, P. R. China.
PLA Key Laboratory of Tissue Repair and Regenerative Medicine and Beijing Key Research Laboratory of Skin Injury, Repair and Regeneration, Beijing, 100048, P. R. China.
Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU051, Beijing, 100048, P. R. China.

Ziwei Shi (Z)

CAS Key Laboratory of Colloid, Interface and Chemical Thermodynamics, Institute of Chemistry, Chinese Academy of Sciences, Beijing, 100190, P. R. China.
University of Chinese Academy of Sciences, Beijing, 100049, P. R. China.

Jiangbing Xiang (J)

State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, Jiangsu, 210023, P. R. China.

Huanhuan Gao (H)

Research Center for Tissue Repair and Regeneration affiliated to the Medical Innovation Research Department, PLA General Hospital and PLA Medical College, Beijing, 100048, P. R. China.
State Key Laboratory of Trauma and Chemical Poisoning, Beijing, 100048, P. R. China.
PLA Key Laboratory of Tissue Repair and Regenerative Medicine and Beijing Key Research Laboratory of Skin Injury, Repair and Regeneration, Beijing, 100048, P. R. China.
Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU051, Beijing, 100048, P. R. China.

Shuaifei Ji (S)

Research Center for Tissue Repair and Regeneration affiliated to the Medical Innovation Research Department, PLA General Hospital and PLA Medical College, Beijing, 100048, P. R. China.
State Key Laboratory of Trauma and Chemical Poisoning, Beijing, 100048, P. R. China.
PLA Key Laboratory of Tissue Repair and Regenerative Medicine and Beijing Key Research Laboratory of Skin Injury, Repair and Regeneration, Beijing, 100048, P. R. China.
Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU051, Beijing, 100048, P. R. China.

Yingying Li (Y)

Research Center for Tissue Repair and Regeneration affiliated to the Medical Innovation Research Department, PLA General Hospital and PLA Medical College, Beijing, 100048, P. R. China.
State Key Laboratory of Trauma and Chemical Poisoning, Beijing, 100048, P. R. China.
PLA Key Laboratory of Tissue Repair and Regenerative Medicine and Beijing Key Research Laboratory of Skin Injury, Repair and Regeneration, Beijing, 100048, P. R. China.
Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU051, Beijing, 100048, P. R. China.

Wei Pi (W)

Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU051, Beijing, 100048, P. R. China.

Huating Chen (H)

Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU051, Beijing, 100048, P. R. China.

Hongliang Zhang (H)

Research Center for Tissue Repair and Regeneration affiliated to the Medical Innovation Research Department, PLA General Hospital and PLA Medical College, Beijing, 100048, P. R. China.
State Key Laboratory of Trauma and Chemical Poisoning, Beijing, 100048, P. R. China.
PLA Key Laboratory of Tissue Repair and Regenerative Medicine and Beijing Key Research Laboratory of Skin Injury, Repair and Regeneration, Beijing, 100048, P. R. China.
Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU051, Beijing, 100048, P. R. China.

Mengyang Wang (M)

Research Center for Tissue Repair and Regeneration affiliated to the Medical Innovation Research Department, PLA General Hospital and PLA Medical College, Beijing, 100048, P. R. China.
State Key Laboratory of Trauma and Chemical Poisoning, Beijing, 100048, P. R. China.
PLA Key Laboratory of Tissue Repair and Regenerative Medicine and Beijing Key Research Laboratory of Skin Injury, Repair and Regeneration, Beijing, 100048, P. R. China.
Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU051, Beijing, 100048, P. R. China.

Yan Li (Y)

Research Center for Tissue Repair and Regeneration affiliated to the Medical Innovation Research Department, PLA General Hospital and PLA Medical College, Beijing, 100048, P. R. China.
State Key Laboratory of Trauma and Chemical Poisoning, Beijing, 100048, P. R. China.
PLA Key Laboratory of Tissue Repair and Regenerative Medicine and Beijing Key Research Laboratory of Skin Injury, Repair and Regeneration, Beijing, 100048, P. R. China.
Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU051, Beijing, 100048, P. R. China.

Yiyue Hong (Y)

Research Center for Tissue Repair and Regeneration affiliated to the Medical Innovation Research Department, PLA General Hospital and PLA Medical College, Beijing, 100048, P. R. China.
State Key Laboratory of Trauma and Chemical Poisoning, Beijing, 100048, P. R. China.
PLA Key Laboratory of Tissue Repair and Regenerative Medicine and Beijing Key Research Laboratory of Skin Injury, Repair and Regeneration, Beijing, 100048, P. R. China.
Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU051, Beijing, 100048, P. R. China.

Dongsheng Liu (D)

Key Laboratory of Organic Optoelectronics & Molecular Engineering of the Ministry of Education, Department of Chemistry, Tsinghua University, Beijing, 100084, P. R. China.

Xiaobing Fu (X)

Research Center for Tissue Repair and Regeneration affiliated to the Medical Innovation Research Department, PLA General Hospital and PLA Medical College, Beijing, 100048, P. R. China.
State Key Laboratory of Trauma and Chemical Poisoning, Beijing, 100048, P. R. China.
PLA Key Laboratory of Tissue Repair and Regenerative Medicine and Beijing Key Research Laboratory of Skin Injury, Repair and Regeneration, Beijing, 100048, P. R. China.
Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU051, Beijing, 100048, P. R. China.

Yuanchen Dong (Y)

CAS Key Laboratory of Colloid, Interface and Chemical Thermodynamics, Institute of Chemistry, Chinese Academy of Sciences, Beijing, 100190, P. R. China.
University of Chinese Academy of Sciences, Beijing, 100049, P. R. China.

Xiaoyan Sun (X)

Research Center for Tissue Repair and Regeneration affiliated to the Medical Innovation Research Department, PLA General Hospital and PLA Medical College, Beijing, 100048, P. R. China.
State Key Laboratory of Trauma and Chemical Poisoning, Beijing, 100048, P. R. China.
PLA Key Laboratory of Tissue Repair and Regenerative Medicine and Beijing Key Research Laboratory of Skin Injury, Repair and Regeneration, Beijing, 100048, P. R. China.
Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU051, Beijing, 100048, P. R. China.

Classifications MeSH