An Asymmetric Natural Nanofiber with Rapid Temperature Responsive Detachability Inspired by Andrias davidianus for Full-Thickness Skin Wound Healing

Zhe Huang, Heng An, Haitao Guo, Shen Ji, Qi Gu, Zhen Gu, Yongqiang Wen

Advanced Fiber Materials ›› 2024, Vol. 6 ›› Issue (2) : 473-488. DOI: 10.1007/s42765-023-00364-7
Research Article

An Asymmetric Natural Nanofiber with Rapid Temperature Responsive Detachability Inspired by Andrias davidianus for Full-Thickness Skin Wound Healing

Author information +
History +

Abstract

Wound dressing management is critical in healthcare, and frequent dressing changes for full-thickness skin wounds can hinder healing. Nanofiber dressings that resemble the extracellular matrix, have gained popularity in wound repair, however, it is challenging to explore how to frequently change it without affecting healing processing and avoiding secondary damage. Here, we developed a self-adhesive and detachable nanofiber dressing inspired by Andrias davidianus. Our asymmetric nanofiber dressing exhibits strong adhesion (26 kPa), to the wound at high temperature (approximately 25 °C) to the wound surface and can be easily detached (4 kPa) at low temperature (below 8 °C), enabling painless dressing changes that minimize secondary injuries. The dressing comprises an outer layer of polylactic acid which provides mechanical property, support, and pollution resistance, with an inner layer of nanofibrous membrane, composed of gelatin and Andrias davidianus skin secretions, which promotes cellular migration, enhances wound healing and possesses inherent antimicrobial properties. Furthermore, the all-natural nanofiber dressings can be prepared on a large scale and offer favorable biocompatibility to meet the basic requirements of wound dressings. These findings demonstrate the potential applicability of our multilayer nanofiber dressing for advancing wound healing practices.

Keywords

Natural / Rapid / Temperature Responsive Detachability / Asymmetric / Nanofibers / Bionic Wound Healing

Cite this article

Download citation ▾
Zhe Huang, Heng An, Haitao Guo, Shen Ji, Qi Gu, Zhen Gu, Yongqiang Wen. An Asymmetric Natural Nanofiber with Rapid Temperature Responsive Detachability Inspired by Andrias davidianus for Full-Thickness Skin Wound Healing. Advanced Fiber Materials, 2024, 6(2): 473‒488 https://doi.org/10.1007/s42765-023-00364-7

References

[1]
Zhang X, Lv R, Chen L, Sun R, Zhang Y, Sheng R, Du T, Li Y, Qi Y. A multifunctional janus electrospun nanofiber dressing with biofluid draining, monitoring, and antibacterial properties for wound healing. ACS Appl Mater Interfaces, 2022, 14: 12984,
CrossRef Google scholar
[2]
Dong Y, Cui M, Qu J, Wang X, Kwon SH, Barrera J, Elvassore N, Gurtner GC. Conformable hyaluronic acid hydrogel delivers adipose-derived stem cells and promotes regeneration of burn injury. Acta Biomater, 2020, 108: 56,
CrossRef Google scholar
[3]
Jayarama Reddy V, Radhakrishnan S, Ravichandran R, Mukherjee S, Balamurugan R, Sundarrajan S, Ramakrishna S. Nanofibrous structured biomimetic strategies for skin tissue regeneration. Wound Repair Regen, 2013, 21: 1,
CrossRef Google scholar
[4]
Feng JJ, See JL, Choke A, Ooi A, Chong SJ. Biobrane for burns of the pubic region: minimizing dressing changes. Mil Med Res, 2018, 5: 29
[5]
Yang M, Fei X, Tian J, Xu L, Wang Y, Li Y. A starch-regulated adhesive hydrogel dressing with controllable separation properties for painless dressing change. J Mater Chem B, 2022, 10: 6026,
CrossRef Google scholar
[6]
Li ZY, Zhang XJ, Gao YM, Song Y, Sands MX, Zhou SB, Li QF, Zhang J. Photo-responsive hydrogel for contactless dressing change to attenuate secondary damage and promote diabetic wound healing. Adv Healthc Mater., 2023, 1: e2202770,
CrossRef Google scholar
[7]
Blakeney BA, Tambralli A, Anderson JM, Andukuri A, Lim DJ, Dean DR, Jun HW. Cell infiltration and growth in a low density, uncompressed three-dimensional electrospun nanofibrous scaffold. Biomaterials, 2011, 32: 1583,
CrossRef Google scholar
[8]
Rahmati M, Mills DK, Urbanska AM, Saeb MR, Venugopal JR, Ramakrishna S, Mozafari M. Electrospinning for tissue engineering applications. Prog Mater Sci, 2021, 117,
CrossRef Google scholar
[9]
Huang C, Thomas NL. Fabrication of porous fibers via electrospinning: strategies and applications. Polym Rev, 2019, 60: 595,
CrossRef Google scholar
[10]
Jiang S, Deng J, Jin Y, Qian B, Lv W, Zhou Q, Mei E, Neisiany RE, Liu Y, You Z, Pan J. Breathable, antifreezing, mechanically skin-like hydrogel textile wound dressings with dual antibacterial mechanisms. Bioact Mater., 2023, 21: 313-323
[11]
Yue Y, Gong X, Jiao W, Li Y, Yin X, Si Y, Yu J, Ding B. In-situ electrospinning of thymol-loaded polyurethane fibrous membranes for waterproof, breathable, and antibacterial wound dressing application. J Colloid Interface Sci, 2021, 592: 310-318,
CrossRef Google scholar
[12]
Yang Y, Du Y, Zhang J, Zhang H, Guo B. Structural and functional design of electrospun nanofibers for hemostasis and wound healing. Adv Fiber Mater, 2022, 4: 1027-1057,
CrossRef Google scholar
[13]
Liu J, Ye L, Sun Y, Hu M, Chen F, Wegner S, Mailander V, Steffen W, Kappl M, Butt HJ. Elastic superhydrophobic and photocatalytic active films used as blood repellent dressing. Adv Mater, 2020, 32,
CrossRef Google scholar
[14]
Sun J, Chen T, Zhao B, Fan W, Shen Y, Wei H, Zhang M, Zheng W, Peng J, Wang J, Wang Y, Fan L, Chu Y, Chen L, Yang C. Acceleration of oral wound healing under diabetes mellitus conditions using bioadhesive hydrogel. ACS Appl Mater Interfaces, 2023, 15: 416,
CrossRef Google scholar
[15]
Chen T, Chen Y, Rehman HU, Chen Z, Yang Z, Wang M, Li H, Liu H. Ultratough, self-healing, and tissue-adhesive hydrogel for wound dressing. ACS Appl Mater Interfaces, 2018, 10: 33523,
CrossRef Google scholar
[16]
Azuma K, Nishihara M, Shimizu H, Itoh Y, Takashima O, Osaki T, Itoh N, Imagawa T, Murahata Y, Tsuka T, Izawa H, Ifuku S, Minami S, Saimoto H, Okamoto Y, Morimoto M. Biological adhesive based on carboxymethyl chitin derivatives and chitin nanofibers. Biomaterials, 2015, 42: 20,
CrossRef Google scholar
[17]
Song YH, Ji E, Joo KI, Seo JH. Development of mechanically reinforced bioadhesive electrospun nanofibers using cellulose acetate–levan complexes. Cellulose, 2022, 30: 1685,
CrossRef Google scholar
[18]
Kim S, Ko J, Choi JH, Kang JY, Lim C, Shin M, Lee DW, Kim JW. Antigen-antibody interaction-derived bioadhesion of bacterial cellulose nanofibers to promote topical wound healing. Adv Funct Mater, 2022, 32: 2110557,
CrossRef Google scholar
[19]
Ku SH, Park CB. Combined effect of mussel-inspired surface modification and topographical cues on the behavior of skeletal myoblasts. Adv Healthc Mater, 2013, 2: 1445,
CrossRef Google scholar
[20]
Ku SH, Park CB. Human endothelial cell growth on mussel-inspired nanofiber scaffold for vascular tissue engineering. Biomaterials, 2010, 31: 9431,
CrossRef Google scholar
[21]
Kim BJ, Choi YS, Cha HJ. Reinforced multifunctionalized nanofibrous scaffolds using mussel adhesive proteins. Angew Chem Int Ed, 2012, 51: 675,
CrossRef Google scholar
[22]
Li Q, Shen X, Liu C, Xing D. Facile wound dressing replacement: carbon dots for dissolving alginate hydrogels via competitive complexation. Int J Biol Macromol, 2023, 240,
CrossRef Google scholar
[23]
Zhang K, Bai X, Yuan Z, Cao X, Jiao X, Li Y, Qin Y, Wen Y, Zhang X. Layered nanofiber sponge with an improved capacity for promoting blood coagulation and wound healing. Biomaterials, 2019, 204: 70,
CrossRef Google scholar
[24]
An H, Zhang M, Zhou L, Huang Z, Duan Y, Wang C, Gu Z, Zhang P, Wen Y. Anti-dehydration and rapid trigger-detachable multifunctional hydrogels promote scarless therapeutics of deep burn. Adv Funct Mater, 2023, 33: 2211182,
CrossRef Google scholar
[25]
Deng J, Tang Y, Zhang Q, Wang C, Liao M, Ji P, Song J, Luo G, Chen L, Ran X, Wei Z, Zheng L, Dang R, Liu X, Zhang H, Zhang YS, Zhang X, Tan H. A Bioinspired medical adhesive derived from skin secretion of andrias davidianus for wound healing. Adv Funct Mater, 2019, 29: 1809110,
CrossRef Google scholar
[26]
Dang R, Chen L, Sefat F, Li X, Liu S, Yuan X, Ning X, Zhang YS, Ji P, Zhang X. A natural hydrogel with prohealing properties enhances tendon regeneration. Small, 2022, 1: e2105255,
CrossRef Google scholar
[27]
Zhang X, Jiang L, Li X, Zheng L, Dang R, Liu X, Wang X, Chen L, Zhang YS, Zhang J, Yang D. A bioinspired hemostatic powder derived from the skin secretion of andrias davidianus for rapid hemostasis and intraoral wound healing. Small, 2022, 18,
CrossRef Google scholar
[28]
Zheng L, Wang Q, Zhang YS, Zhang H, Tang Y, Zhang Y, Zhang W, Zhang X. A hemostatic sponge derived from skin secretion of Andrias davidianus and nanocellulose. Chem Eng J, 2021, 1: 416
[29]
Liu X, Mao X, Ye G, Wang M, Xue K, Zhang Y, Zhang H, Ning X, Zhao M, Song J, Zhang YS, Zhang X. Bioinspired Andrias davidianus-Derived wound dressings for localized drug-elution. Bioact Mater, 2022, 15: 482
[30]
Li T, Sun M, Wu S. State-of-the-art review of electrospun gelatin-based nanofiber dressings for wound healing applications. Nanomaterials, 2022, 12: 784,
CrossRef Google scholar
[31]
Dong Y, Rodrigues M, Li X, Kwon SH, Kosaric N, Khong S, Gao Y, Wang W, Gurtner GC. Injectable and tunable gelatin hydrogels enhance stem cell retention and improve cutaneous wound healing. Adv Funct Mater, 2017, 27: 1606619,
CrossRef Google scholar
[32]
Tao B, Lin C, Qin X, Yu Y, Guo A, Li K, Tian H, Yi W, Lei D, Chen Y, Chen L. Fabrication of gelatin-based and Zn(2+)-incorporated composite hydrogel for accelerated infected wound healing. Mater Today Bio, 2022, 13,
CrossRef Google scholar
[33]
Wang L, Mao L, Qi F, Li X, Wajid Ullah M, Zhao M, Shi Z, Yang G. Synergistic effect of highly aligned bacterial cellulose/gelatin membranes and electrical stimulation on directional cell migration for accelerated wound healing. Chem Eng J, 2021, 424,
CrossRef Google scholar
[34]
Yang X, Li L, Yang D, Nie J, Ma G. Electrospun core-shell fibrous 2D scaffold with biocompatible poly(glycerol sebacate) and poly-l-lactic acid for wound healing. Adv Fiber Mater, 2020, 2: 105-117,
CrossRef Google scholar
[35]
Ren Y, Huang L, Wang Y, Mei L, Fan R, He M, Wang C, Tong A, Chen H, Guo G. Stereocomplexed electrospun nanofibers containing poly (lactic acid) modified quaternized chitosan for wound healing. Carbohydr Polym, 2020, 247,
CrossRef Google scholar
[36]
Jiang Y, Zhang X, Zhang W, Wang M, Yan L, Wang K, et al.. Infant skin friendly adhesive hydrogel patch activated at body temperature for bioelectronics securing and diabetic wound healing. ACS Nano, 2022, 16: 8662-8676,
CrossRef Google scholar
[37]
Zhang L, Wang S, Wang Z, Liu Z, Xu X, Liu H, Wang D, Tian Z. Temperature-mediated phase separation enables strong yet reversible mechanical and adhesive hydrogels. ACS Nano, 2023, 14: 13948-13960,
CrossRef Google scholar
[38]
Lv Y, Xu Y, Sang X, Li C, Liu Y, Guo Q, et al.. PLLA-gelatin composite fiber membranes incorporated with functionalized CeNPs as a sustainable wound dressing substitute promoting skin regeneration and scar remodeling. J Mater Chem B, 2022, 10: 1116-1127,
CrossRef Google scholar
[39]
Dias JR, Baptista-Silva S, Oliveira CM, Sousa A, Oliveira AL, Bártolo PJ, et al.. In situ crosslinked electrospun gelatin nanofibers for skin regeneration. Eur Polym J, 2017, 95: 161-173,
CrossRef Google scholar
[40]
Rodrigo-Navarro A, Sankaran S, Dalby MJ, del Campo A, Salmeron-Sanchez M. . Engineered living biomaterials Nat Rev Mater, 2021, 6: 1175,
CrossRef Google scholar
[41]
Xue J, Wu T, Dai Y, Xia Y. Electrospinning and electrospun nanofibers: methods, materials, and applications. Chem Rev, 2019, 119: 5298,
CrossRef Google scholar
[42]
Zhang YZ, Venugopal J, Huang ZM, Lim CT, Ramakrishna S. Crosslinking of the electrospun gelatin nanofibers. Polymer, 2006, 47: 2911,
CrossRef Google scholar
[43]
Bahrami S, Solouk A, Mirzadeh H, Seifalian AM. Electroconductive polyurethane/graphene nanocomposite for biomedical applications. Compos B Eng, 2019, 168: 421,
CrossRef Google scholar
[44]
Li M, Dong Y, Wang M, Lu X, Li X, Yu J, Ding B. Hydrogel/nanofibrous membrane composites with enhanced water retention, stretchability and self-healing capability for wound healing. Compos B Eng, 2023, 257,
CrossRef Google scholar
[45]
Dias JR, Granja PL, Bártolo PJ. Advances in electrospun skin substitutes. Prog Mater Sci, 2016, 84: 314,
CrossRef Google scholar
[46]
Liu W, Xie R, Zhu J, Wu J, Hui J, Zheng X, Huo F. A temperature responsive adhesive hydrogel for fabrication of flexible electronic sensors. Npj Flex Electron., 2022, 6: 68,
CrossRef Google scholar
[47]
Zhou L, Zeng Z, Liu S, Min T, Zhang W, Bian X, Du H, Zhang P, Wen Y. Multifunctional DNA hydrogel enhances stemness of adipose-derived stem cells to activate immune pathways for guidance burn wound regeneration. Adv Funct Mater, 2022, 32: 2207466,
CrossRef Google scholar
[48]
Shi S, Si Y, Han Y, Wu T, Iqbal MI, Fei B, Li R, Hu J, Qu J. Recent progress in protective membranes fabricated via electrospinning: advanced materials, biomimetic structures, and functional applications. Adv Mater, 2022, 34,
CrossRef Google scholar
[49]
Wu Y, Liu H, Li B, Jokisalo J, Kosonen R, Cheng Y, Zhao W, Yuan X. Evaluation and modification of the weighting formulas for mean skin temperature of human body in winter conditions. Energy Build, 2020, 229,
CrossRef Google scholar
[50]
Daelemans L, van Paepegem W, Hooge DR, Clerck KD. Excellent nanofiber adhesion for hybrid polymer materials with high toughness based on matrix interdiffusion during chemical conversion. Adv Funct Mater, 2019, 29: 1807434,
CrossRef Google scholar
[51]
Kimna C, Bauer MG, Lutz TM, Mansi S, Akyuz E, Doganyigit Z, et al.. Multifunctional “Janus-Type” bilayer films combine broad-range tissue adhesion with guided drug release. Adv Funct Mater, 2022, 32: 2105721,
CrossRef Google scholar
[52]
Gregory DA, Tripathi L, Fricker ATR, Asare E, Orlando I, Raghavendran V, Roy I. Bacterial cellulose: a smart biomaterial with diverse applications. Mater Sci Eng R Rep, 2021, 145,
CrossRef Google scholar
[53]
Chen S, John JV, Carthy AM, Carlson MA, Li X, Xie J. Fast transformation of 2D nanofiber membranes into pre-molded 3D scaffolds with biomimetic and oriented porous structure for biomedical applications. Appl Phys Rev, 2020, 7: 021406,
CrossRef Google scholar
[54]
Carvalho T, Ezazi NZ, Correia A, Vilela C, Santos HA, Freire CSR. Gelatin-lysozyme nanofibrils electrospun patches with improved mechanical, antioxidant, and bioresorbability properties for myocardial regeneration applications. Adv Funct Mater, 2022, 32: 2113390,
CrossRef Google scholar
[55]
Liu X, Wu M, Wang M, Hu Q, Liu J, Duan Y, Liu B. Direct synthesis of photosensitizable bacterial cellulose as engineered living material for skin wound repair. Adv Mater, 2022, 34: e2109010,
CrossRef Google scholar
[56]
Du XY, Li Q, Wu G, Chen S. Multifunctional micro/nanoscale fibers based on microfluidic spinning technology. Adv Mater, 2019, 31: e1903733,
CrossRef Google scholar
[57]
Xia Y, Yang H, Li S, Zhou S, Wang L, Tang Y, Cheng C, Haag R. Multivalent polyanionic 2D nanosheets functionalized nanofibrous stem cell-based neural scaffolds. Adv Funct Mater, 2021, 31: 2010145,
CrossRef Google scholar
[58]
Luo Z, Cui H, Guo J, Yao J, Fang X, Yan F, Wang B, Mao H. Poly(ionic liquid)/Ce-based antimicrobial nanofibrous membrane for blocking drug-resistance dissemination from MRSA-infected wounds. Adv Funct Mater, 2021, 31: 2100336,
CrossRef Google scholar
[59]
Wang Q, Feng Y, He M, Zhao W, Qiu L, Zhao C. A hierarchical janus nanofibrous membrane combining direct osteogenesis and osteoimmunomodulatory functions for advanced bone regeneration. Adv Funct Mater, 2020, 31: 2008906,
CrossRef Google scholar
[60]
Du J, Yao Y, Wang M, Su R, Li X, Yu J, Ding B. Programmable building of radially gradient nanofibrous patches enables deployment, bursting bearing capability, and stem cell recruitment. Adv Funct Mater, 2022, 32: 2109833,
CrossRef Google scholar
[61]
Roshanbinfar K, Vogt L, Ruther F, Roether JA, Boccaccini AR, Engel FB. Nanofibrous composite with tailorable electrical and mechanical properties for cardiac tissue engineering. Adv Funct Mater, 2020, 30: 1908612,
CrossRef Google scholar
[62]
Ceylan H, Urel M, Erkal TS, Tekinay AB, Dana A, Guler MO. Mussel inspired dynamic cross-linking of self-healing peptide nanofiber network. Adv Funct Mater, 2013, 23: 2081,
CrossRef Google scholar
[63]
Liu C, Wang S, Wang N, Yu J, Liu YT, Ding B. From 1D nanofibers to 3D nanofibrous aerogels: a marvellous evolution of electrospun SiO(2) nanofibers for emerging applications. Nano Lett, 2022, 14: 194,
CrossRef Google scholar
[64]
Xu B, Li A, Wang R, Zhang J, Ding Y, Pan D, Shen Z. Elastic janus film for wound dressings: unidirectional biofluid transport and effectively promoting wound healing. Adv Funct Mater, 2021, 31: 2105265,
CrossRef Google scholar
Funding
National Natural Science Foundation of China(T2222029 U21A20396); CAS Project for Young Scientists in Basic Research(YSBR-012); Incubation Foundation of Beijing Institute for Stem Cell and Regenerative Medicine(2023FH122); The Strategic Priority Research Program of the Chinese Academy of Sciences(XDA16020802); the China Scholarship Council(202206465017); the Fundamental Research Funds for the Central Universities(FRFTP-20-019A2 FRF-BR-20-03B); Science Fund of Shandong Laboratory of Advanced Materials and Green Manufacturing (Yantai)(AMGM2023F04)

Accesses

Citations

Detail

Sections
Recommended

/