Extracellular vesicles in skin health, diseases, and aging

Juan Wang , Siqi Yuan , Yidong Tu , Zhi Lv , Hua Cheng , Xiaolei Ding

Interdisciplinary Medicine ›› 2024, Vol. 2 ›› Issue (3) : e20240011

PDF
Interdisciplinary Medicine ›› 2024, Vol. 2 ›› Issue (3) : e20240011 DOI: 10.1002/inmd.20240011
REVIEW

Extracellular vesicles in skin health, diseases, and aging

Author information +
History +
PDF

Abstract

The skin interfaces with the external environment, acting as both a physical barrier and an immunologic defense. The dynamic interactions between various cell types are essential for skin homeostasis and function. Emerging research has unveiled the significant role of extracellular vesicles (EVs) as key mediators of cell communication in regulating many aspects of skin physiological and pathological processes. In this review, we provide an overview of recent advances in understanding the physiological and pathological roles of EVs in skin health, aging, and diseases, and discuss natural and engineered EVs in skin disease treatment along with the potential challenges. The burgeoning area of EVs may expand new therapeutic approaches for various skin disorders and open new avenues for personalized skincare treatments.

Keywords

aging / extracellular vesicles / skin diseases / therapeutic agents / tissue regeneration

Cite this article

Download citation ▾
Juan Wang, Siqi Yuan, Yidong Tu, Zhi Lv, Hua Cheng, Xiaolei Ding. Extracellular vesicles in skin health, diseases, and aging. Interdisciplinary Medicine, 2024, 2(3): e20240011 DOI:10.1002/inmd.20240011

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

E.Fuchs, Nature 2007, 445, 834.

[2]

E.Rognoni, F. M.Watt, Trends Cell Biol. 2018, 28, 709.

[3]

K.Urban, S.Chu, R. L.Giesey, S. Mehrmal, P.Uppal, M. E.Delost, G. R.Delost, JAAD Int. 2021, 2, 40.

[4]

K. W.Witwer, D. C.Goberdhan, L.O’Driscoll, C.Théry, J. A.Welsh, C.Blenkiron, E. I. Buzás, D.Di Vizio, U.Erdbrügger, J. M.Falcón-Pérez, Q. L.Fu, A. F.Hill, M.Lenassi, J. Lötvall, R.Nieuwland, T.Ochiya, S.Rome, S.Sahoo, L.Zheng, J. Extracell. Vesicles 2021, 10, e12182.

[5]

R.Kalluri, V. S.LeBleu, Science 2020, 367, eaau6977.

[6]

M.Xiong, Q.Zhang, W.Hu, C.Zhao, W.Lv, Y.Yi, Y.Wang, H. Tang, M.Wu, Y.Wu, Pharmacol. Res. 2021, 166, 105490.

[7]

C. L.Simpson, D. M.Patel, K. J.Green, Nat. Rev. Mol. Cell Biol. 2011, 12, 565.

[8]

L.Eckhart, S.Lippens, E.Tschachler, W.Declercq, Biochim. Biophys. Acta 2013, 1833, 3471.

[9]

T.Kobayashi, S.Naik, K.Nagao, Immunity 2019, 50, 552.

[10]

A.Nyström, L.Bruckner-Tuderman, Semin. Cell Dev. Biol. 2019, 89, 136.

[11]

C. FGuerrero-Juarez, M. V. Plikus, Nat. Rev. Endocrinol. 2018, 14, 163.

[12]

M.Chinnappan, T. AHarris-Tryon, Exp. Dermatol. 2021, 30, 1484.

[13]

P.Wolf, Br. J. Haematol. 1967, 13, 269.

[14]

L.Mashouri, H.Yousefi, A. R.Aref, A. M.Ahadi, F.Molaei, S. K.Alahari, Mol. Cancer 2019, 18, 75.

[15]

J. A.Welsh, D. C. I. Goberdhan, L.O’Driscoll, E. I.Buzas, C.Blenkiron, B.Bussolati, H.Cai, D.Di Vizio, T. A. P.Driedonks, U.Erdbrügger, J. M Falcon-Perez, Q. L.Fu, A. F.Hill, M. Lenassi, S. K.Lim, M. G.Mahoney, S.Mohanty, A.Möller, R.Nieuwland, T.Ochiya, S.Sahoo, A. C.Torrecilhas, L. Zheng, A.Zijlstra, S.Abuelreich, R.Bagabas, P.Bergese, E. M.Bridges, M.Brucale, D.Burger, R. P.Carney, E.Cocucci, R.Crescitelli, E.Hanser, A. L.Harris, N. J.Haughey, A.Hendrix, A. R.Ivanov, T.Jovanovic-Talisman, N. AKruh-Garcia, V. Ku’ulei-Lyn Faustino, D.Kyburz, C.Lässer, K. M.Lennon, J.Lötvall, A. L.Maddox, E. SMartens-Uzunova, R. R. Mizenko, L. A.Newman, A.Ridolfi, E.Rohde, T.Rojalin, A. Rowland, A.Saftics, U. S.Sandau, J. A.Saugstad, F.Shekari, S.Swift, D.Ter-Ovanesyan, J. P.Tosar, Z.Useckaite, F.Valle, Z.Varga, E. van der Pol, M. J. C.van Herwijnen, M. H. M.Wauben, A. M.Wehman, S.Williams, A.Zendrini, A. J.Zimmerman, C.Théry, K. W.Witwer, J. Extracell. Vesicles 2024, 13, e12404.

[16]

Q.Li, B.Li, T.Ye, W.Xu, H.Yin, Z. Deng, H.Li, X.Yan, X.Hao, L.Li, Z.Tao, B.Liu, Z. Chen, L.Luo, H.Qian, Q.-L.Fu, Q.Wang, L. Zheng, Y.Wang, Interdiscip. Med. 2023, 1, e20220015.

[17]

M.Mohammadi, H.Zargartalebi, R.Salahandish, R.Aburashed, K.Wey Yong, A.Sanati-Nezhad, Biosens. Bioelectron. 2021, 183, 113176.

[18]

R. A.Dragovic, C.Gardiner, A. S.Brooks, D. S.Tannetta, D. J.Ferguson, P.Hole, B.Carr, C. W.Redman, A. L.Harris, P. J.Dobson, P.Harrison, I. L.Sargent, Nanomed. Nanotech. Biol. Med. 2011, 7, 780.

[19]

G.van Niel, G.D’Angelo, G.Raposo, Nat. Rev. Mol. Cell Biol. 2018, 19, 213.

[20]

A. C.Dixson, T. R.Dawson, D.Di Vizio, A. M.Weaver, Nat. Rev. Mol. Cell Biol. 2023, 24, 454.

[21]

R.Isaac, F. C. G. Reis, W.Ying, J. M.Olefsky, Cell Metab. 2021, 33, 1744.

[22]

L.Blanc, M.Vidal, Small GTPases 2018, 9, 95.

[23]

F.Fabbiano, J.Corsi, E.Gurrieri, C. Trevisan, M.Notarangelo, V. G.D’Agostino, J. Extracell. Vesicles 2020, 10, e12043.

[24]

J.Johnson, S. Q. K. Law, M.Shojaee, A. S.Hall, S.Bhuiyan, M. B. L.Lim, A.Silva, K. J. W. Kong, M.Schoppet, C.Blyth, H. N.Ranasinghe, N.Sejic, M. J.Chuei, O. C.Tatford, A.Cifuentes-Rius, P. F.James, A.Tester, I.Dixon, G.Lichtfuss, J. Extracell. Vesicles 2023, 12, e12332.

[25]

T.Skotland, K.Sagini, K.Sandvig, A.Llorente, Adv. Drug Deliv. Rev. 2020, 159, 308.

[26]

H.Liu, Q.Zhang, S.Wang, W. Weng, Y.Jing, J.Su, Bioact. Mater. 2022, 14, 169.

[27]

M.Toyofuku, S.Schild, M.Kaparakis-Liaskos, L.Eberl, Nat. Rev. Microbiol. 2023, 21, 415.

[28]

M.Cao, N.Diao, X.Cai, X. Chen, Y.Xiao, C.Guo, D.Chen, X.Zhang, Mater. Horiz. 2023, 10, 3879.

[29]

Q.Yi, Z.Xu, A.Thakur, K. Zhang, Q.Liang, Y.Liu, Y.Yan, Pharmacol. Res. 2023, 190, 106733.

[30]

H.Liu, H.Zhang, S. C.Wang, J. Cui, W. Z.Weng, X. R.Liu, H.Tang, Y.Hu, X. Q.Li, K.Zhang, F. J. Zhou, Y. Y.Jing, J. C.Su, Compos. B Eng. 2023, 255, 110610.

[31]

H.Liu, Y.Wu, F.Wang, S. Wang, N.Ji, M.Wang, G.Zhou, R.Han, X. Liu, W.Weng, H.Tan, Y.Jing, W.Zhang, H. Zhang, Z.Shi, J.Su, Compos. B Eng. 2023, 267, 111047.

[32]

M.Wen, J.Wang, Z.Ou, G.Nie, Y.Chen, M. Li, Z.Wu, S.Xiong, H.Zhou, Z.Yang, G. Long, J.Su, H.Liu, Y.Jing, Z.Wen, Y. Fu, T.Zhou, H.Xie, W.Guan, X.Sun, Z. Wang, J.Wang, X.Chen, L.Jiang, X.Qin, Y. Xue, M.Huang, X.Huang, R.Pan, H.Zhen, Y. Du, Q.Li, X.Huang, Y.Wu, P.Wang, K. Zhao, B.Situ, X.Hu, L.Zheng, Interdiscip. Med. 2023, 1, e20230017.

[33]

J.Xie, Q.Li, F.Haesebrouck, L.Van Hoecke, R. E.Vandenbroucke, Trends Biotechnol. 2022, 40, 1173.

[34]

Z.Xu, Y.Xu, K.Zhang, Y. Liu, Q.Liang, A.Thakur, W.Liu, Y.Yan, J. Nanobiotechnol. 2023, 21, 114.

[35]

H.Liu, H.Zhang, Y.Han, Y. Hu, Z.Geng, J.Su, Theranostics 2022, 12, 6576.

[36]

J.Feng, Q.Xiu, Y.Huang, Z. Troyer, B.Li, L.Zheng, Adv. Mater. 2023, 35, 2207826.

[37]

I.Barák, K.Muchová, Int. J. Mol. Sci. 2013, 14, 4050.

[38]

J.Huang, X.Wang, Z.Wang, L. Deng, Y.Wang, Y.Tang, L.Luo, E. L. H.Leung, Cytokine Growth Factor Rev. 2023, 73, 173.

[39]

M.De Palma, A.Ambrosone, A.Leone, P.Del Gaudio, M.Ruocco, L.Turiák, R.Bokka, I.Fiume, M.Tucci, G. Pocsfalvi, Plants 2020, 9, 1777.

[40]

J.Mondal, S.Pillarisetti, V.Junnuthula, M.Saha, S. R.Hwang, I. K.Park, Y. K. Lee, J. Control. Release 2023, 353, 1127.

[41]

P.Wu, B.Zhang, D. K. W.Ocansey, W.Xu, H.Qian, Biomaterials 2021, 269, 120467.

[42]

X.Liu, Q.Wei, Z.Sun, S. Cui, X.Wan, Z.Chu, Y.Zhang, W.Zhong, L. Lu, L.Shi, X.Fu, C.Zhang, S.Wang, Interdiscip. Med. 2023, 1, e20230019.

[43]

Y.Liang, L.Duan, J.Lu, J.Xia, Theranostics 2021, 11, 3183.

[44]

X.Li, X.Xie, W.Lian, R. Shi, S.Han, H.Zhang, L.Lu, M.Li, Exp. Mol. Med. 2018, 50, 1.

[45]

J.Huang, M.Yu, W.Yin, B. Liang, A.Li, J.Li, X.Li, S.Zhao, F. Liu, Bioact. Mater. 2021, 6, 2841.

[46]

Q.Wei, J.Su, S.Meng, Y. Wang, K.Ma, B.Li, Z.Chu, Q.Huang, W. Hu, Z.Wang, L.Tian, X.Liu, T.Li, X.Fu, C.Zhang, Adv. Sci. 2024, 11, 2307761.

[47]

Z.Pan, W.Sun, Y.Chen, H. Tang, W.Lin, J.Chen, C.Chen, Adv. Healthcare Mater. 2022, 11, 2201384.

[48]

C.Yang, Y.Xue, Y.Duan, C. Mao, M.Wan, J. Control. Release 2024, 365, 1089.

[49]

S.Shao, H.Fang, Q.Li, G.Wang, Theranostics 2020, 10, 9937.

[50]

Y.Liao, Z.Zhang, L.Ouyang, B. Mi, G.Liu, Small 2024, 20, 2307058.

[51]

E. J.Choi, I. S.Kil, E. G.Cho, Int. J. Mol. Sci. 2020, 21, 1022.

[52]

L.Terlecki-Zaniewicz, I. Lämmermann, J.Latreille, M. R.Bobbili, V.Pils, M.Schosserer, R.Weinmüllner, H.Dellago, S.Skalicky, D.Pum, J. C. H.Almaraz, M. Scheideler, F.Morizot, M.Hackl, F.Gruber, J.Grillari, Aging (Albany NY) 2018, 10, 1103.

[53]

L.Terlecki-Zaniewicz, V. Pils, M. R.Bobbili, I.Lämmermann, I. Perrotta, T.Grillenberger, J.Schwestka, K.Weiß, D.Pum, E.Arcalis, S.Schwingenschuh, T.Birngruber, M.Brandstetter, T.Heuser, M.Schosserer, F.Morizot, M.Mildner, E.Stöger, E.Tschachler, R.Weinmüllner, F.Gruber, J.Grillari, J. Invest. Dermatol. 2019, 139, 2425.

[54]

M.Borghesan, J.Fafián-Labora, O.Eleftheriadou, P.Carpintero-Fernández, M.Paez-Ribes, G.Vizcay-Barrena, A.Swisa, D.Kolodkin-Gal, P.Ximénez-Embún, R.Lowe, B.Martín-Martín, H.Peinado, J.Muñoz, R. A.Fleck, Y.Dor, I.Ben-Porath, A.Vossenkamper, D.Muñoz-Espin, A. O’Loghlen, Cell Rep. 2019, 27, 3956.

[55]

T.Nedachi, C.Bonod, J.Rorteau, W. Chinoune, Y.Ishiuchi, S.Hughes, B.Gillet, N.Bechetoille, D.Sigaudo-Roussel, J. Lamartine, Aging (Albany NY) 2023, 15, 12702.

[56]

M.Sinha, C. K.Sen, K.Singh, A. Das, S.Ghatak, B.Rhea, B.Blackstone, H. M.Powell, S.Khanna, S.Roy, Nat. Commun. 2018, 9, 936.

[57]

Y.Wu, X.Wu, J.Wang, S. Chen, H.Chen, J.Liu, T.Zeng, M.Hu, Y.Liang, K.Sun, C. Yang, L.Yan, M.Ren, Lab. Invest. 2023, 103, 100019.

[58]

L.Li, X.Zuo, D.Liu, H. Luo, H.Zhu, J. Dermatol. Sci. 2020, 98, 88.

[59]

P. J.Wermuth, S.Piera-Velazquez, S. A.Jimenez, Clin. Exp. Rheumatol. 2017, 35, 21.

[60]

R.Bhandari, H.Yang, N. N.Kosarek, A. E.Smith, J. A.Garlick, M.Hinchcliff, M. L.Whitfield, P. A.Pioli, Rheumatology 2023, 62, SI114.

[61]

S. W.Hong, M. R.Kim, E. Y.Lee, J. H. Kim, Y. S.Kim, S. G.Jeon, J. M.Yang, B. J.Lee, B. Y. Pyun, Y. S.Gho, Y. K.Kim, Allergy 2011, 66, 351.

[62]

S. H.Jun, J. H.Lee, S. I.Kim, C. W. Choi, T. I.Park, H. R.Jung, J. W.Cho, S. H.Kim, J. C. Lee, Clin. Exp. Allergy 2017, 47, 85.

[63]

J.Kim, B. H.Bin, E. J.Choi, H. G. Lee, T. R.Lee, E. G.Cho, Clin. Exp. Allergy 2019, 49, 68.

[64]

S. W.Hong, E. B.Choi, T. K.Min, J. H. Kim, M. H.Kim, S. G.Jeon, B. J.Lee, Y. S.Gho, Y. K. Jee, B. Y.Pun, Y. K.Kim, PloS One 2014, 9, e100499.

[65]

M.Jiang, H.Fang, S.Shao, E. Dang, J.Zhang, P.Qiao, A.Yang, G.Wang, FASEB J. 2019, 33, 13241.

[66]

M.Jiang, H.Fang, E.Dang, J. Zhang, P.Qiao, C.Yu, A.Yang, G.Wang, J. Invest. Dermatol. 2021, 141, 563.

[67]

S.Shao, H.Fang, J.Zhang, M. Jiang, K.Xue, J.Ma, J.Zhang, J.Lei, Y. Zhang, B.Li, X.Yuan, E.Dang, G.Wang, FASEB J. 2019, 33, 6813.

[68]

J.Yan, K.Zhang, T.Guo, S. Yang, H.Jia, Cell. Immunol. 2022, 373, 104496.

[69]

E. J.Choi, H. G.Lee, I. H.Bae, W. Kim, J.Park, T. R.Lee, E. G.Cho, J. Invest. Dermatol. 2018, 138, 1371.

[70]

M.Oh, J.Lee, Y. J.Kim, W. J. Rhee, J. H.Park, Int. J. Mol. Sci. 2018, 19, 1715.

[71]

H. Z.Shi, J. C.Zeng, S. H.Shi, H. Giannakopoulos, Q. Z.Zhang, A. D.Le, J. Dent. Res. 2021, 100, 283.

[72]

J. S.Choi, W. L.Cho, Y. J.Choi, J. D. Kim, H. A.Park, S. Y.Kim, J. H.Park, D. G.Jo, Y. W. Cho, J. Extracell. Vesicles 2019, 8, 1565885.

[73]

V. C.Khanh, T.Yamashita, K.Ohneda, C.Tokunaga, H.Kato, M.Osaka, Y. Hiramatsu, O.Ohneda, Sci. Rep. 2020, 10, 17315.

[74]

X.Zhao, Y.Liu, P.Jia, H. Cheng, C.Wang, S.Chen, H.Huang, Z.Han, Z. C. Han, K.Marycz, X.Chen, Z.Li, Stem Cell Res. Ther. 2021, 12, 196.

[75]

K.Zhang, L.Yu, F. R.Li, X. Li, Z.Wang, X.Zou, C.Zhang, K.Lv, B.Zhou, S.Mitragotri, M.Chen, Int. J. Nanomed. 2020, 15, 2859.

[76]

C. S.Jo, C. H.Myung, Y. C.Yoon, B. H. Ahn, J. W.Min, W. S.Seo, D. H.Lee, H. C.Kang, Y. H. Heo, H.Choi, I. K.Hong, J. S.Hwang, Curr. Issues Mol. Biol. 2022, 44, 526.

[77]

E. G.Cho, S. Y.Choi, H.Kim, E. J. Choi, E. J.Lee, P. J.Park, J.Ko, K. P.Kim, H. S. Baek, Cells 2021, 10, 486.

[78]

J.Han, T.Wu, J.Jin, Z. Li, W.Cheng, X.Dai, K.Yang, H.Zhang, Z. Zhang, H.Zhang, R.Fan, S.Zheng, H.Liu, Y. Li, H.Zhao, C.Yao, T.Lin, C.Zhu, H. Liu, J. Nanobiotechnol. 2022, 20, 455.

[79]

Y.You, Y.Tian, Z.Yang, J. Shi, K. J.Kwak, Y.Tong, A. P.Estania, J.Cao, W. H.Hsu, Y.Liu, C. L.Chiang, B. R. Schrank, K.Huntoon, D.Lee, Z.Li, Y.Zhao, H. Zhang, T. D.Gallup, J.Ha, S.Dong, X.Li, Y.Wang, W. J.Lu, E. Bahrani, L. J.Lee, L.Teng, W.Jiang, F.Lan, B. Y. S. Kim, A. S.Lee, Nat. Biomed. Eng. 2023, 7, 887.

[80]

S. C.Guo, S. C.Tao, W. J.Yin, X. Qi, T.Yuan, C. Q.Zhang, Theranostics 2017, 7, 81.

[81]

T.Nielsen, A. F.Kristensen, S.Pedersen, G.Christiansen, S. R.Kristensen, J. Extracell. Vesicles 2018, 7, 1454777.

[82]

T. C.Chance, C. R.Rathbone, R. M.Kamucheka, G. C.Peltier, A. P.Cap, J. A.Bynum, J. Trauma Acute Care Surg. 2019, 87, S74.

[83]

E. M.Guerreiro, S. G.Kruglik, S.Swamy, N.Latysheva, B.Østerud, J. M.Guigner, F.Sureau, S.Bonneau, A. N.Kuzmin, P. N.Prasad, J. B.Hansen, O. G.Hellesø, O.Snir, J. Thromb. Haemost. 2024, 22, 1463.

[84]

X.Li, L.Liu, J.Yang, Y. Yu, J.Chai, L.Wang, L.Ma, H.Yin, EBioMedicine 2016, 8, 72.

[85]

B.Zhang, X.Wu, X.Zhang, Y. Sun, Y.Yan, H.Shi, Y.Zhu, L.Wu, Z.Pan, W.Zhu, H. Qian, W.Xu, Stem Cells Transl. Med. 2015, 4, 513.

[86]

X.He, Z.Dong, Y.Cao, H. Wang, S.Liu, L.Liao, Y.Jin, L.Yuan, B. Li, Stem Cells Int. 2019, 2019, 7132708.

[87]

X.Xiao, M.Xu, H.Yu, L.Wang, X.Li, J.Rak, S.Wang, R. C. Zhao, Signal. Transduct. Target. Ther. 2021, 6, 354.

[88]

J.Yang, X.Zhang, G.Wang, S. Ma, Y.Yu, C.Liao, Z.Wang, C.Liang, M. Li, W.Tian, L.Liao, Int. J. Nanomed. 2023, 18, 6955.

[89]

M.Pomatto, C.Gai, F.Negro, M. Cedrino, C.Grange, E.Ceccotti, G.Togliatto, F.Collino, M.Tapparo, F.Figliolini, T.Lopatina, M. F.Brizzi, G.Camussi, Int. J. Mol. Sci. 2021, 22, 3851.

[90]

P.Wang, G.Theocharidis, I. S.Vlachos, K.Kounas, A.Lobao, B.Shu, B. Wu, J.Xie, Z.Hu, S.Qi, B.Tang, J. Zhu, A.Veves, J. Invest. Dermatol. 2022, 142, 2508.

[91]

S.Cui, X.Liu, Y.Liu, W. Hu, K.Ma, Q.Huang, Z.Chu, L.Tian, S. Meng, J.Su, W.Zhang, H.Li, X.Fu, C.Zhang, Adv. Sci. 2023, 10, 2300414.

[92]

J.Zhang, J.Guan, X.Niu, G. Hu, S.Guo, Q.Li, Z.Xie, C.Zhang, Y. Wang, J. Transl. Med. 2015, 13, 49.

[93]

J.Zhang, C.Chen, B.Hu, X.Niu, X.Liu, G. Zhang, C.Zhang, Q.Li, Y.Wang, Int. J. Biol. Sci. 2016, 12, 1472.

[94]

Q.Liao, L.Su, L.Pang, J. Li, H.Li, J.Li, Y.Liu, J.Zhang, J. Nanobiotechnol. 2023, 21, 169.

[95]

Q.Lv, J.Deng, Y.Chen, Y. Wang, B.Liu, J.Liu, Mol. Pharm. 2020, 17, 1723.

[96]

W.Li, S.Wu, L.Ren, B. Feng, Z.Chen, Z.Li, B.Cheng, J.Xia, ACS Nano 2023, 17, 22106.

[97]

Q.Li, W.Hu, Q.Huang, J. Yang, B.Li, K.Ma, Q.Wei, Y.Wang, J. Su, M.Sun, S.Cui, R.Yang, H.Li, X.Fu, C.Zhang, Signal Transduct. Target. Ther. 2023, 8, 62.

[98]

L.Hu, J.Wang, X.Zhou, Z. Xiong, J.Zhao, R.Yu, F.Huang, H.Zhang, L. Chen, Sci. Rep. 2016, 6, 32993.

[99]

Y.Li, J.Zhang, J.Shi, K. Liu, X.Wang, Y.Jia, T.He, K.Shen, Y. Wang, J.Liu, W.Zhang, H.Wang, Z.Zheng, D. Hu, Stem Cell Res. Ther. 2021, 12, 221.

[100]

P.Rozier, M.Maumus, A. T. J.Maria, K.Toupet, J.Lai-Kee-Him, C.Jorgensen, P.Guilpain, D.Noël, J. Autoimmun. 2021, 121, 102660.

[101]

F.Han, K.Wang, K.Shen, J. Wang, S.Han, D.Hu, G.Wu, J. Nanobiotechnol. 2023, 21, 113.

[102]

J.Jin, Q.Ou, Z.Wang, H. Tian, J. Y.Xu, F.Gao, S.Hu, J.Chen, J. Wang, J.Zhang, L.Lu, C.Jin, G. T.Xu, J. Zhao, Stem Cell Res. Ther. 2021, 12, 327.

[103]

P.Lai, X.Chen, L.Guo, Y. Wang, X.Liu, Y.Liu, T.Zhou, T.Huang, S. Geng, C.Luo, X.Huang, S.Wu, W.Ling, X. Du, C.He, J.Weng, J. Hematol. Oncol. 2018, 11, 135.

[104]

H.Zhang, C.Zang, W.Zhao, L. Zhang, R.Liu, Z.Feng, J.Wu, R.Cui, Int. J. Nanomed. 2023, 18, 7047.

[105]

L.Guo, P.Lai, Y.Wang, T. Huang, X.Chen, S.Geng, X.Huang, C.Luo, S. Wu, W.Ling, L.Huang, X.Du, J.Weng, Int. Immunopharmacol. 2020, 84, 106541.

[106]

S.Fang, C.Xu, Y.Zhang, C. Xue, C.Yang, H.Bi, X.Qian, M.Wu, K.Ji, Y.Zhao, Y. Wang, H.Liu, X.Xing, Stem Cells Transl. Med. 2016, 5, 1425.

[107]

M.Suárez-Fariñas, N.Dhingra, J.Gittler, A.Shemer, I.Cardinale, C.de Guzman Strong, J. G.Krueger, E.Guttman-Yassky, J. Allergy Clin. Immunol. 2013, 132, 361.

[108]

B. S.Cho, J. O.Kim, D. H.Ha, Y. W. Yi, Stem Cell Res. Ther. 2018, 9, 187.

[109]

J.Guan, Y.Li, F.Lu, J.Feng, Stem Cell Res. Ther. 2022, 13, 98.

[110]

K. O.Shin, D. H.Ha, J. O.Kim, D. A. Crumrine, J. M.Meyer, J. S.Wakefield, Y.Lee, B.Kim, S. Kim, H. K.Kim, J.Lee, H. H.Kwon, G. H.Park, J. H. Lee, J.Lim, S.Park, P. M.Elias, K.Park, Y. W. Yi, B. S.Cho, Cells 2020, 9, 680.

[111]

M. H.Kim, S. J.Choi, H. I.Choi, J. P. Choi, H. K.Park, E. K.Kim, M. J.Kim, B. S.Moon, T. K. Min, M.Rho, Y. J.Cho, S.Yang, Y. K.Kim, Y. Y. Kim, B. Y.Pyun, Allergy Asthma Immunol. Res. 2018, 10, 516.

[112]

W.Zhang, J.Lin, P.Shi, D. Su, X.Cheng, W.Yi, J.Yan, H.Chen, F. Cheng, Front. Cell Dev. Biol. 2022, 10, 842813.

[113]

R.Huang, B.Jia, D.Su, M.Li, Z.Xu, C.He, Y.Huang, H. Fan, H.Chen, F.Cheng, J. Extracell. Vesicles 2023, 12, e12361.

[114]

F.Gómez-Chávez, C.Cedillo-Peláez, L. A.Zapi-Colín, G.Gutiérrez-González, I.Martínez-Torres, H.Peralta, L.Chavez-Galan, E. D.Avila-Calderón, A.Contreras-Rodríguez, Y.Bartolo-Aguilar, S. Rodríguez-Martínez, M. E Cancino-Diaz, J. C.Cancino-Diaz, Int. J. Mol. Sci. 2021, 22, 13029.

[115]

X.Ding, P.Kakanj, M.Leptin, S. A.Eming, J. Invest. Dermatol. 2021, 141, 1063.

[116]

E.Low, G.Alimohammadiha, L. A.Smith, L. F.Costello, S. A.Przyborski, T.von Zglinicki, S.Miwa, Ageing Res. Rev. 2021, 71, 101456.

[117]

C.López-Otín, M. A.Blasco, L.Partridge, M.Serrano, G.Kroemer, Cell 2023, 186, 243.

[118]

S.Jin, K.Li, X.Zong, S. Eun, N.Morimoto, S.Guo, Aging Dis. 2023, 14, 2167.

[119]

F. P.Chevalier, J.Rorteau, S.Ferraro, L. S.Martin, A.Gonzalez-Torres, A.Berthier, N.El Kholti, J.Lamartine, Cells 2022, 11, 836.

[120]

H. A.Rather, S.Almousa, S.Craft, G.Deep, Ageing Res. Rev. 2023, 92, 102088.

[121]

F.Li, G.Huang, F.Tan, R. Yi, X.Zhou, J.Mu, X.Zhao, Food Sci. Nutr. 2020, 8, 379.

[122]

K.Lee, H. J.Kim, S. A.Kim, S. D. Park, J. J.Shim, J. L.Lee, Molecules 2021, 26, 1651.

[123]

S.Shahid, G.Kim, N. R.Johnson, E.Wafula, F.Wang, C.Coruh, V. Bernal-Galeano, T.Phifer, C. W.dePamphilis, J. H.Westwood, M. J.Axtell, Nature 2018, 553, 82.

[124]

Q.Cai, B.He, A.Weiberg, A. H. Buck, H.Jin, PLoS Pathog. 2019, 15, e1008090.

[125]

C.Cui, Y.Wang, J.Liu, J. Zhao, P.Sun, S.Wang, Nat. Commun. 2019, 10, 4298.

[126]

S.Cosenza, K.Toupet, M.Maumus, P.Luz-Crawford, O.Blanc-Brude, C.Jorgensen, D.Noël, Theranostics 2018, 8, 1399.

[127]

G. C.Gurtner, S.Werner, Y.Barrandon, M. T.Longaker, Nature 2008, 453, 314.

[128]

M.Rodrigues, N.Kosaric, C. A.Bonham, G. C.Gurtner, Physiol. Rev. 2019, 99, 665.

[129]

S. A.Eming, P. J.Murray, E. J.Pearce, Cell Metab. 2021, 33, 1726.

[130]

K. A. UGonzales, E. Fuchs, Dev. Cell 2017, 43, 387.

[131]

I.Pastar, N. C.Balukoff, J.Marjanovic, V. Y.Chen, R. C.Stone, M.Tomic-Canic, Cold Spring Harb. Perspect. Biol. 2023, 15, a041243.

[132]

N.Graves, C. J.Phillips, K.Harding, Br. J. Dermatol. 2022, 187, 141.

[133]

X.Zhou, B. A.Brown, A. P.Siegel, M. S. El Masry, X.Zeng, W.Song, A.Das, P.Khandelwal, A.Clark, K.Singh, P. R.Guda, M. Gorain, L.Timsina, Y.Xuan, S. C.Jacobson, M. V.Novotny, S.Roy, M.Agarwal, R. J.Lee, C. K.Sen, D. E.Clemmer, S.Ghatak, ACS Nano 2020, 14, 12732.

[134]

Z.Cao, X.Sun, B.Icli, A. K. Wara, M. W.Feinberg, Blood 2010, 116, 4404.

[135]

E.Sahin, S.Haubenwallner, M.Kuttke, I.Kollmann, A.Halfmann, A. M.Dohnal, L.Chen, P.Cheng, B.Hoesel, E. Einwallner, J.Brunner, J. B.Kral, W. C.Schrottmaier, K.Thell, V.Saferding, S.Blüml, G.Schabbauer, J. Immunol. 2014, 193, 1717.

[136]

M. EAl-Masawa, M. A.Alshawsh, C. Y.Ng, A. M. H.Ng, J. B.Foo, U.Vijakumaran, R.Subramaniam, N. A. A. Ghani, K. W.Witwer, J. X.Law, Theranostics 2022, 12, 6455.

[137]

D. Y.Matar, B.Ng, O.Darwish, M. Wu, D. P.Orgill, A. C.Panayi, Adv. Wound Care 2023, 12, 269.

[138]

F.Al-Rashed, S.Sindhu, H.Arefanian, A.Al Madhoun, S.Kochumon, R.Thomas, S.Al-Kandari, A.Alghaith, T.Jacob, F.Al-Mulla, R.Ahmad, Cells 2020, 9, 1892.

[139]

X.Liu, Q.Wei, L.Lu, S.Cui, K.Ma, W.Zhang, F.Ma, H.Li, X.Fu, C.Zhang, Front. Immunol. 2023, 14, 1094685.

[140]

M. D.Hade, C. N.Suire, J.Mossell, Z. Suo, Med. Res. Rev. 2022, 42, 2102.

[141]

R. C.Lai, S. S.Tan, B. J.Teh, S. K. Sze, F.Arslan, D. P.de Kleijn, A.Choo, S. K.Lim, Int. J. Proteomics 2012, 2012, 971907.

[142]

X.Jiang, B. R.Stockwell, M.Conrad, Nat. Rev. Mol. Cell Biol. 2021, 22, 266.

[143]

J.Song, K.Zhu, H.Wang, M. Wu, Y.Wu, Q.Zhang, Int. J. Biol. Sci. 2023, 19, 4989.

[144]

S.Li, Y.Li, Z.Wu, Z.Wu, H.Fang, Am. J. Physiol. Endocrinol. Metab. 2021, 321, E509.

[145]

E.Shaabani, M.Sharifiaghdam, R.Faridi-Majidi, S. C.De Smedt, K.Braeckmans, J. C.Fraire, Mol. Ther. Nucleic Acids 2022, 29, 871.

[146]

Y.Liao, Z.Zhang, L.Ouyang, B. Mi, G.Liu, Small 2023, 20, 2307058.

[147]

M.Li, F.Fang, M.Sun, Y. Zhang, M.Hu, J.Zhang, Theranostics 2022, 12, 4879.

[148]

P.Lou, S.Liu, X.Xu, C.Pan, Y.Lu, J.Liu, Acta Biomater. 2021, 119, 42.

[149]

Y.Wang, Z.Cao, Q.Wei, K. Ma, W.Hu, Q.Huang, J.Su, H.Li, C.Zhang, X.Fu, Acta Biomater. 2022, 147, 342.

[150]

G.Wang, Z.Lin, Y.Li, L.Chen, S. K.Reddy, Z. Hu, L. A.Garza, Adv. Drug Deliv. Rev. 2023, 194, 114727.

[151]

H. E.Talbott, S.Mascharak, M.Griffin, D. C.Wan, M. T.Longaker, Cell Stem Cell 2022, 29, 1161.

[152]

N. N.Do, S. A.Eming, Curr. Res. Transl. Med. 2016, 64, 185.

[153]

C. P.Denton, D.Khanna, Lancet 2017, 390, 1685.

[154]

M. B.Buechler, W.Fu, S. J.Turley, Immunity 2021, 54, 903.

[155]

Y.Wang, Y.Zhang, T.Li, K.Shen, K. J.Wang, C. Tian, D.Hu, Adv. Mater. 2023, 35, 2303642.

[156]

J.Dong, B.Wu, W.Tian, Int. J. Nanomed. 2023, 18, 2923.

[157]

C. F. tSchuler, A. C.Billi, E.Maverakis, L. C. Tsoi, J. E.Gudjonsson, J. Allergy Clin. Immunol. 2023, 151, 1145.

[158]

T.Dainichi, A.Kitoh, A.Otsuka, S. Nakajima, T.Nomura, D. H.Kaplan, K.Kabashima, Nat. Immunol. 2018, 19, 1286.

[159]

T.Bieber, Nat. Rev. Drug Discov. 2022, 21, 21.

[160]

H. I.Kwon, N. H.Jeong, S. H.Jun, J. H. Son, S.Kim, H.Jeon, S. C.Kang, S. H.Kim, J. C. Lee, Int. Immunopharmacol. 2018, 59, 301.

[161]

J.Qiu, D.Wang, H.Xiang, H. Feng, Y.Jiang, L.Xia, J.Dong, J.Lu, L.Yu, X.Deng, PLoS One 2010, 5, e9736.

[162]

T. H.Shin, H. S.Kim, S. W.Choi, K. S. Kang, Int. J. Mol. Sci. 2017, 18, 244.

[163]

C. E. MGriffiths, A. W. Armstrong, J. E.Gudjonsson, J.Barker, Lancet 2021, 397, 1301.

[164]

A. W.Armstrong, C.Read, JAMA 2020, 323, 1945.

[165]

C.Wu, Z.Chen, V. K.Kuchroo, Cell Res. 2015, 25, 273.

[166]

A.Lainé, B.Martin, M.Luka, L.Mir, C.Auffray, B.Lucas, G.Bismuth, C.Charvet, J. Immunol. 2015, 195, 1791.

[167]

B.Zhang, R. C.Lai, W. K.Sim, A. B. H. Choo, E. B.Lane, S. K.Lim, Int. J. Mol. Sci. 2021, 22, 720.

[168]

K.Aquilano, V.Ceci, A.Gismondi, S. De Stefano, F.Iacovelli, R.Faraonio, G.Di Marco, N.Poerio, A.Minutolo, G.Minopoli, A.Marcone, M.Fraziano, F.Tortolici, S.Sennato, S.Casciardi, M.Potestà, R.Bernardini, M.Mattei, M.Falconi, C.Montesano, S.Rufini, A.Canini, D.Lettieri-Barbato, Commun. Biol. 2019, 2, 317.

[169]

Y.Wang, S.Kuo, M.Shu, J. Yu, S.Huang, A.Dai, A.Two, R. L.Gallo, C. M. Huang, Appl. Microbiol. Biotechnol. 2014, 98, 411.

[170]

A. M.Layton, J.Ravenscroft, Lancet Child. Adolesc. Health 2023, 7, 136.

[171]

A. L.Zaenglein, N. Engl. J. Med. 2018, 379, 1343.

[172]

A.Chudzik, P.Migdał, M.Paściak, Int. J. Mol. Sci. 2022, 23, 5797.

[173]

M. P.Cros, J.Mir-Pedrol, L.Toloza, N.Knödlseder, J. Maruotti, C. C.Zouboulis, M.Güell, M. J.Fábrega, Sci. Rep. 2023, 13, 16058.

[174]

M. J.Kim, K. P.Kim, E.Choi, J. H. Yim, C.Choi, H. S.Yun, H. Y.Ahn, J. Y.Oh, Y. Cho, Nutrients 2021, 13, 1368.

[175]

D. R.Wang, J.Pan, World J. Stem Cell 2023, 15, 165.

[176]

W. K.Rhim, J. Y.Kim, S. Y.Lee, S. G. Cha, J. M.Park, H. J.Park, C. G.Park, D. K.Han, Biomater. Res. 2023, 27, 130.

[177]

E.Willms, C.Cabañas, I.Mäger, M. J. A.Wood, P.Vader, Front. Immunol. 2018, 9, 738.

[178]

S. I.van de Wakker, F. M. Meijers, J. P. G.Sluijter, P.Vader, Pharmacol. Rev. 2023, 75, 1043.

[179]

G.Bordanaba-Florit, F. Royo, S. G.Kruglik, J. M.Falcón-Pérez, Nat. Protoc. 2021, 16, 3163.

[180]

H.Liu, P.Song, H.Zhang, F. Zhou, N.Ji, M.Wang, G.Zhou, R.Han, X. Liu, W.Weng, H.Tan, S.Wang, L.Zheng, Y. Jing, J.Su, J. Extracell. Vesicles 2024, 13, e12429.

RIGHTS & PERMISSIONS

2024 The Authors. Interdisciplinary Medicine published by Wiley-VCH GmbH on behalf of Nanfang Hospital, Southern Medical University.

AI Summary AI Mindmap
PDF

225

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/