Skip to main content

Advertisement

SpringerLink
Log in

Development of printable nanoengineered composite hydrogels based on human amniotic membrane for wound healing application

  • Materials for life sciences
  • Published:
Journal of Materials Science Aims and scope Submit manuscript

Abstract

Recently, decellularized amniotic membranes (dAM) have attracted significant interest as a valuable source for the development of shear-thinning hydrogels and bioinks. However, the inferior rheological behavior and weak mechanical durability restrict the printability of the hydrogels and their stability after three-dimensional (3D) bioprinting. Therefore, a chemical or physical modification with biocompatible components is necessary to improve dAM-derived hydrogels’ properties. The present study proposes a strategy to fabricate printable dAM-derived hydrogels (DAMHs) supplemented with sodium alginate and Laponite nanoplatelets. Rheological experiments determined the key role of Laponite nanoplatelets in tailoring the shear-thinning behavior of the DAMHs. The dynamic mechanical modulus of the hydrogel was significantly enhanced (up to 16 folds, for example, storage modulus increased from ~ 0.5 to 8.4 kPa by adding 1% Laponite), which facilitated 3D printing of free-standing constructs without compromising biological properties. Meanwhile, excess agglomeration of the nanoplatelets in an ion-containing medium leading to nozzle clogging was observed at high Laponite concentrations (\(\ge\) 2%). Microstructural evaluations also revealed nanoplatelet-induced changes in the pore structures of the hydrogel, i.e., a finer pore structure was obtained. In vitro biological assays affirmed the biocompatibility of the nanoengineered hydrogels, while wound healing experiments revealed the positive effect of Laponite on fibroblast cell migration, as evidenced by ~ 30% enhancement in the wound healing rate after 36 h. Generally, the results obtained in this study demonstrate that the developed nanoengineered hydrogel provides suitable structural integrity and biocompatibility, highlighting its potential for therapeutic applications, particularly tissue engineering.

Graphical Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8

Similar content being viewed by others

Data availability

The raw/processed data required to reproduce these findings are available for sharing upon request.

References

  1. Smandri A, Nordin A, Hwei NM, Chin K-Y, Abd Aziz I, Fauzi MB (2020) Natural 3D-printed bioinks for skin regeneration and wound healing: a systematic review. Polymers 12:1782. https://doi.org/10.3390/polym12081782

    Article  CAS  Google Scholar 

  2. Wallace ER, Yue Z, Dottori M, Wood FM, Fear M, Wallace GG, Beirne S (2023) Point of care approaches to 3D bioprinting for wound healing applications. Progress in Biomedical Engineering 5:023002. https://doi.org/10.1088/2516-1091/acceeb

    Article  Google Scholar 

  3. He P, Zhao J, Zhang J, Li B, Gou Z, Gou M, Li X (2018) Bioprinting of skin constructs for wound healing. Burns Trauma 6:1–10. https://doi.org/10.1186/s41038-017-0104-x

    Article  Google Scholar 

  4. Kim H, Kang B, Cui X, Lee SH, Lee K, Cho DW, Hwang W, Woodfield TB, Lim KS, Jang J (2021) Light-activated decellularized extracellular matrix-based bioinks for volumetric tissue analogs at the centimeter scale. Adv Funct Mater 31:2011252. https://doi.org/10.1002/adfm.202011252

    Article  CAS  Google Scholar 

  5. Antezana PE, Municoy S, Álvarez-Echazú MI, Santo-Orihuela PL, Catalano PN, Al-Tel TH, Kadumudi FB, Dolatshahi-Pirouz A, Orive G, Desimone MF (2022) The 3D bioprinted scaffolds for wound healing. Pharmaceutics 14:464. https://doi.org/10.3390/pharmaceutics14020464

    Article  CAS  Google Scholar 

  6. Lian Q, Jiao T, Zhao T, Wang H, Yang S, Li D (2021) 3D bioprinted skin substitutes for accelerated wound healing and reduced scar. J Bionic Eng 18:900–914. https://doi.org/10.1007/s42235-021-0053-8

    Article  Google Scholar 

  7. Kim BS, Das S, Jang J, Cho D-W (2020) Decellularized extracellular matrix-based bioinks for engineering tissue-and organ-specific microenvironments. Chem Rev 120:10608–10661. https://doi.org/10.1021/acs.chemrev.9b00808

    Article  CAS  Google Scholar 

  8. Daikuara LY, Chen X, Yue Z, Skropeta D, Wood FM, Fear MW, Wallace GG (2022) 3D bioprinting constructs to facilitate skin regeneration. Adv Func Mater 32:2105080. https://doi.org/10.1002/adfm.202105080

    Article  CAS  Google Scholar 

  9. Gholipourmalekabadi M, Samadikuchaksaraei A, Seifalian AM, Urbanska AM, Ghanbarian H, Hardy JG, Omrani MD, Mozafari M, Reis RL, Kundu SC (2018) Silk fibroin/amniotic membrane 3D bi-layered artificial skin. Biomed Mater 13:035003. https://doi.org/10.1088/1748-605X/aa999b

    Article  Google Scholar 

  10. Niknejad H, Peirovi H, Jorjani M, Ahmadiani A, Ghanavi J, Seifalian AM (2008) Properties of the amniotic membrane for potential use in tissue engineering. Eur Cells Mater 15:88–99. https://doi.org/10.22203/ecm

    Article  CAS  Google Scholar 

  11. Nasiry D, Khalatbary AR, Abdollahifar M-A, Amini A, Bayat M, Noori A, Piryaei A (2021) Engraftment of bioengineered three-dimensional scaffold from human amniotic membrane-derived extracellular matrix accelerates ischemic diabetic wound healing. Arch Dermatol Res 313:567–582. https://doi.org/10.1007/s00403-020-02137-3

    Article  CAS  Google Scholar 

  12. Kafili G, Tamjid E, Niknejad H, Simchi A (2022) Development of injectable hydrogels based on human amniotic membrane and polyethyleneglycol-modified nanosilicates for tissue engineering applications. Eur Polym J 179:111566. https://doi.org/10.1016/j.eurpolymj.2022.111566

    Article  CAS  Google Scholar 

  13. Ryzhuk V, Zeng X-X, Wang X, Melnychuk V, Lankford L, Farmer D, Wang A (2018) Human amnion extracellular matrix derived bioactive hydrogel for cell delivery and tissue engineering. Mater Sci Eng C Mater Biol Appl 85:191. https://doi.org/10.1016/j.msec.2017.12.026

    Article  CAS  Google Scholar 

  14. Zhang Q, Chang C, Qian C, Xiao W, Zhu H, Guo J, Meng Z, Cui W, Ge Z (2021) Photo-crosslinkable amniotic membrane hydrogel for skin defect healing. Acta Biomater 125:197–207. https://doi.org/10.1016/j.actbio.2021.02.043

    Article  CAS  Google Scholar 

  15. Deus IA, Santos SC, Custódio CA, Mano JF (2022) Designing highly customizable human based platforms for cell culture using proteins from the amniotic membrane. Biomater Adv 134:112574. https://doi.org/10.1016/j.msec.2021.112574

    Article  CAS  Google Scholar 

  16. Lee JY, Kim H, Ha DH, Shin JC, Kim A, Ko HS, Cho DW (2018) Amnion-analogous medical device for fetal membrane healing: a preclinical long-term study. Adv Healthcare Mater 7:1800673. https://doi.org/10.1002/adhm.201800673

    Article  CAS  Google Scholar 

  17. Toniato TV, Stocco TD, Martins DDS, Santanna LB, Tim CR, Marciano FR, SilvaFilho EC, Campana-Filho SP, Lobo ADO (2020) Hybrid chitosan/amniotic membrane-based hydrogels for articular cartilage tissue engineering application. Int J Polym Mater Polym Biomater 69:961–970. https://doi.org/10.1080/00914037.2019.1636249

    Article  CAS  Google Scholar 

  18. Peng X, Wang X, Cheng C, Zhou X, Gu Z, Li L, Liu J, Yu X (2020) Bioinspired artificial, small-diameter vascular grafts with selective and rapid endothelialization based on an amniotic membrane-derived hydrogel. ACS Biomater Sci Eng 6:1603–1613. https://doi.org/10.1021/acsbiomaterials.9b01493

    Article  CAS  Google Scholar 

  19. Lei X, Wu Y, Peng X, Zhao Y, Zhou X, Yu X (2020) Research on alginate-polyacrylamide enhanced amnion hydrogel, a potential vascular substitute material. Mater Sci Eng C 115:111145. https://doi.org/10.1016/j.msec.2020.111145

    Article  CAS  Google Scholar 

  20. Lee J, Hong J, Kim W, Kim GH (2020) Bone-derived dECM/alginate bioink for fabricating a 3D cell-laden mesh structure for bone tissue engineering. Carbohyd Polym 250:116914. https://doi.org/10.1016/j.carbpol.2020.116914

    Article  CAS  Google Scholar 

  21. Rastogi P, Kandasubramanian B (2019) Review of alginate-based hydrogel bioprinting for application in tissue engineering. Biofabrication 11:042001. https://doi.org/10.1088/1758-5090/ab331e

    Article  CAS  Google Scholar 

  22. Yang X, Lu Z, Wu H, Li W, Zheng L, Zhao J (2018) Collagen-alginate as bioink for three-dimensional (3D) cell printing based cartilage tissue engineering. Mater Sci Eng, C 83:195–201. https://doi.org/10.1016/j.msec.2017.09.002

    Article  CAS  Google Scholar 

  23. Gao G, Lee JH, Jang J, Lee DH, Kong JS, Kim BS, Choi YJ, Jang WB, Hong YJ, Kwon SM (2017) Tissue engineered bio-blood-vessels constructed using a tissue-specific bioink and 3D coaxial cell printing technique: a novel therapy for ischemic disease. Adv Func Mater 27:1700798. https://doi.org/10.1002/adfm.201700798

    Article  CAS  Google Scholar 

  24. De Santis MM, Alsafadi HN, Tas S, Bölükbas DA, Prithiviraj S, Da Silva IA, Mittendorfer M, Ota C, Stegmayr J, Daoud F (2021) Extracellular-matrix-reinforced bioinks for 3D bioprinting human tissue. Adv Mater 33:2005476. https://doi.org/10.1002/adma.202005476

    Article  CAS  Google Scholar 

  25. Rathan S, Dejob L, Schipani R, Haffner B, Möbius ME, Kelly DJ (2019) Fiber reinforced cartilage ECM functionalized bioinks for functional cartilage tissue engineering. Adv Healthcare Mater 8:1801501. https://doi.org/10.1002/adhm.201801501

    Article  CAS  Google Scholar 

  26. Zandi N, Dolatyar B, Lotfi R, Shallageh Y, Shokrgozar MA, Tamjid E, Annabi N, Simchi A (2021) Biomimetic nanoengineered scaffold for enhanced full-thickness cutaneous wound healing. Acta Biomater 124:191–204. https://doi.org/10.1016/j.actbio.2021.01.029

    Article  CAS  Google Scholar 

  27. Sheikhi A, Afewerki S, Oklu R, Gaharwar AK, Khademhosseini A (2018) Effect of ionic strength on shear-thinning nanoclay–polymer composite hydrogels. Biomaterials science 6:2073–2083. https://doi.org/10.1039/C8BM00469B

    Article  CAS  Google Scholar 

  28. Dávila JL, d’Ávila MA (2017) Laponite as a rheology modifier of alginate solutions: Physical gelation and aging evolution. Carbohyd Polym 157:1–8. https://doi.org/10.1016/j.carbpol.2016.09.057

    Article  CAS  Google Scholar 

  29. Xue C, Xie H, Eichenbaum J, Chen Y, Wang Y, van den Dolder FW, Lee J, Lee K, Zhang S, Sun W (2020) Synthesis of injectable shear-thinning biomaterials of various compositions of gelatin and synthetic silicate nanoplatelet. Biotechnol J 15:1900456. https://doi.org/10.1002/biot.201900456

    Article  CAS  Google Scholar 

  30. Parchehbaf-Kashani M, Sepantafar M, Talkhabi M, Sayahpour FA, Baharvand H, Pahlavan S, Rajabi S (2020) Design and characterization of an electroconductive scaffold for cardiomyocytes based biomedical assays. Mater Sci Eng C 109:110603. https://doi.org/10.1016/j.msec.2019.110603

    Article  CAS  Google Scholar 

  31. Freeman FE, Kelly DJ (2017) Tuning alginate bioink stiffness and composition for controlled growth factor delivery and to spatially direct MSC fate within bioprinted tissues. Sci Rep 7:1–12. https://doi.org/10.1038/s41598-017-17286-1

    Article  CAS  Google Scholar 

  32. Li X, Deng Q, Wang S, Li Q, Zhao W, Lin B, Luo Y, Zhang X (2021) Hydroxyethyl cellulose as a rheological additive for tuning the extrusion printability and Scaffold properties. 3D Print Addit Manuf 8:87–98. https://doi.org/10.1089/3dp.2020.0167

    Article  Google Scholar 

  33. Zmejkoski DZ, Marković ZM, Budimir MD, Zdravković NM, Trišić DD, Bugárová N, Danko M, Kozyrovska NO, Špitalský Z, Kleinová A (2021) Photoactive and antioxidant nanochitosan dots/biocellulose hydrogels for wound healing treatment. Mater Sci Eng C 122:111925. https://doi.org/10.1016/j.msec.2021.111925

    Article  CAS  Google Scholar 

  34. Choudhury D, Tun HW, Wang T, Naing MW (2018) Organ-derived decellularized extracellular matrix: a game changer for bioink manufacturing? Trends Biotechnol 36:787–805. https://doi.org/10.1016/j.tibtech.2018.03.003

    Article  CAS  Google Scholar 

  35. Kim BS, Kim H, Gao G, Jang J, Cho D-W (2017) Decellularized extracellular matrix: a step towards the next generation source for bioink manufacturing. Biofabrication 9:034104. https://doi.org/10.1088/1758-5090/aa7e98

    Article  CAS  Google Scholar 

  36. Dávila JL, d’Ávila MA (2019) Rheological evaluation of Laponite/alginate inks for 3D extrusion-based printing. Int J Adv Manuf Technol 101:675–686. https://doi.org/10.1007/s00170-018-2876-y

    Article  Google Scholar 

  37. Shin YJ, Shafranek RT, Tsui JH, Walcott J, Nelson A, Kim D-H (2021) 3D bioprinting of mechanically tuned bioinks derived from cardiac decellularized extracellular matrix. Acta Biomater 119:75–88. https://doi.org/10.1016/j.actbio.2020.11.006

    Article  CAS  Google Scholar 

  38. Morariu S, Bercea M, Gradinaru LM, Rosca I, Avadanei M (2020) Versatile poly (vinyl alcohol)/clay physical hydrogels with tailorable structure as potential candidates for wound healing applications. Mater Sci Eng: C 109:110395. https://doi.org/10.1016/j.msec.2019.110395

    Article  CAS  Google Scholar 

  39. Tao L, Zhonglong L, Ming X, Zezheng Y, Zhiyuan L, Xiaojun Z, Jinwu W (2017) In vitro and in vivo studies of a gelatin/carboxymethyl chitosan/LAPONITE® composite scaffold for bone tissue engineering. RSC Adv 7:54100–54110. https://doi.org/10.1039/C7RA06913H

    Article  CAS  Google Scholar 

  40. Bhattacharjee M, Ivirico JLE, Kan H-M, Bordett R, Pandey R, Otsuka T, Nair LS, Laurencin CT (2020) Preparation and characterization of amnion hydrogel and its synergistic effect with adipose derived stem cells towards IL1β activated chondrocytes. Sci Rep 10:18751. https://doi.org/10.1038/s41598-020-75921-w

    Article  CAS  Google Scholar 

  41. Khoshnood N, Zamanian A (2022) Development of novel alginate-polyethyleneimine cell-laden bioink designed for 3D bioprinting of cutaneous wound healing scaffolds. J Appl Polym Sci 139:52227. https://doi.org/10.1002/app.52227

    Article  CAS  Google Scholar 

  42. Yang H, Hua S, Wang W, Wang A (2011) Composite hydrogel beads based on chitosan and laponite: preparation, swelling, and drug release behaviour. Iran Polym J 20(6):479–490

    CAS  Google Scholar 

  43. Wang G, Maciel D, Wu Y, Rodrigues J, Shi X, Yuan Y, Liu C, Tomás H, Li Y (2014) Amphiphilic polymer-mediated formation of laponite-based nanohybrids with robust stability and pH sensitivity for anticancer drug delivery. ACS Appl Mater Interfaces 6:16687–16695. https://doi.org/10.1021/am5032874

    Article  CAS  Google Scholar 

  44. Dong L, Bu Z, Xiong Y, Zhang H, Fang J, Hu H, Liu Z, Li X (2021) Facile extrusion 3D printing of gelatine methacrylate/Laponite nanocomposite hydrogel with high concentration nanoclay for bone tissue regeneration. Int J Biol Macromol 188:72–81. https://doi.org/10.1016/j.ijbiomac.2021.07.199

    Article  CAS  Google Scholar 

  45. Sousa I, Mendes A, Pereira RF, Bártolo PJ (2014) Collagen surface modified poly (ε-caprolactone) scaffolds with improved hydrophilicity and cell adhesion properties. Mater Lett 134:263–267. https://doi.org/10.1016/j.matlet.2014.06.132

    Article  CAS  Google Scholar 

  46. Gao T, Gillispie GJ, Copus JS, Pr AK, Seol Y-J, Atala A, Yoo JJ, Lee SJ (2018) Optimization of gelatin–alginate composite bioink printability using rheological parameters: a systematic approach. Biofabrication 10:034106. https://doi.org/10.1088/1758-5090/aacdc7

    Article  CAS  Google Scholar 

  47. Eslahi N, Simchi A, Mehrjoo M, Shokrgozar MA, Bonakdar S (2016) Hybrid cross-linked hydrogels based on fibrous protein/block copolymers and layered silicate nanoparticles: tunable thermosensitivity, biodegradability and mechanical durability. RSC Adv 6:62944–62957. https://doi.org/10.1039/C6RA08563F

    Article  CAS  Google Scholar 

  48. Ordikhani F, Dehghani M, Simchi A (2015) Antibiotic-loaded chitosan–Laponite films for local drug delivery by titanium implants: Cell proliferation and drug release studies. J Mater Sci - Mater Med 26:1–12. https://doi.org/10.1007/s10856-015-5606-0

    Article  CAS  Google Scholar 

  49. Lokhande G, Carrow JK, Thakur T, Xavier JR, Parani M, Bayless KJ, Gaharwar AK (2018) Nanoengineered injectable hydrogels for wound healing application. Acta Biomater 70:35–47. https://doi.org/10.1016/j.actbio.2018.01.045

    Article  CAS  Google Scholar 

  50. Pettinelli N, Rodriguez-Llamazares S, Bouza R, Barral L, Feijoo-Bandin S, Lago F (2020) Carrageenan-based physically crosslinked injectable hydrogel for wound healing and tissue repairing applications. Int J Pharm 589:119828. https://doi.org/10.1016/j.ijpharm.2020.119828

    Article  CAS  Google Scholar 

  51. Kiaee G, Mostafalu P, Samandari M, Sonkusale S (2018) A pH-mediated electronic wound dressing for controlled drug delivery. Adv Healthcare Mater 7:1800396. https://doi.org/10.1002/adhm.201800396

    Article  CAS  Google Scholar 

  52. Pati F, Jang J, Ha D-H, Won Kim S, Rhie J-W, Shim J-H, Kim D-H, Cho D-W (2014) Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat Commun 5:1–11. https://doi.org/10.1038/ncomms4935

    Article  CAS  Google Scholar 

  53. Golafshan N, Rezahasani R, Esfahani MT, Kharaziha M, Khorasani S (2017) Nanohybrid hydrogels of laponite: PVA-Alginate as a potential wound healing material. Carbohyd Polym 176:392–401. https://doi.org/10.1016/j.carbpol.2017.08.070

    Article  CAS  Google Scholar 

  54. Li H, Liu S, Lin L (2016) Rheological study on 3D printability of alginate hydrogel and effect of graphene oxide. Int J Bioprint 2:54–66. https://doi.org/10.18063/IJB.2016.02.007

    Article  CAS  Google Scholar 

  55. Chen Y, Xiong X, Liu X, Cui R, Wang C, Zhao G, Zhi W, Lu M, Duan K, Weng J (2020) 3D Bioprinting of shear-thinning hybrid bioinks with excellent bioactivity derived from gellan/alginate and thixotropic magnesium phosphate-based gels. J Mater Chem B 8:5500–5514. https://doi.org/10.1039/D0TB00060D

    Article  CAS  Google Scholar 

  56. Choi D, Heo J, Milan JA, Oreffo RO, Dawson JI, Hong J, Kim Y-H (2021) Structured nanofilms comprising Laponite® and bone extracellular matrix for osteogenic differentiation of skeletal progenitor cells. Mater Sci Eng: C 118:111440. https://doi.org/10.1016/j.msec.2020.111440

    Article  CAS  Google Scholar 

  57. Paxton N, Smolan W, Böck T, Melchels F, Groll J, Jungst T (2017) Proposal to assess printability of bioinks for extrusion-based bioprinting and evaluation of rheological properties governing bioprintability. Biofabrication 9:044107. https://doi.org/10.1088/1758-5090/aa8dd8

    Article  CAS  Google Scholar 

  58. Ribeiro A, Blokzijl MM, Levato R, Visser CW, Castilho M, Hennink WE, Vermonden T, Malda J (2017) Assessing bioink shape fidelity to aid material development in 3D bioprinting. Biofabrication 10:014102. https://doi.org/10.1088/1758-5090/aa90e2

    Article  CAS  Google Scholar 

  59. Wang Y, Yuan X, Yao B, Zhu S, Zhu P, Huang S (2022) Tailoring bioinks of extrusion-based bioprinting for cutaneous wound healing. Bioact Mater 17:178–194. https://doi.org/10.1016/j.bioactmat.2022.01.024

    Article  CAS  Google Scholar 

  60. Alsharif SB, Wali R, Vanyo ST, Andreana S, Chen K, Sheth B, Swihart MT, Dziak R, Visser MB (2022) Strontium-loaded hydrogel scaffolds to promote gingival fibroblast function. J Biomed Mater Res, Part A 111:6–14. https://doi.org/10.1002/jbm.a.37439

    Article  CAS  Google Scholar 

  61. Ghadiri M, Chrzanowski W, Lee W, Rohanizadeh R (2014) Layered silicate clay functionalized with amino acids: wound healing application. RSC Adv 4:35332–35343. https://doi.org/10.1039/C4RA05216A

    Article  CAS  Google Scholar 

  62. Tomás H, Alves CS, Rodrigues J (2018) Laponite®: A key nanoplatform for biomedical applications?, Nanomedicine: Nanotechnology. Biol Med 14:2407–2420. https://doi.org/10.1016/j.nano.2017.04.016

    Article  CAS  Google Scholar 

  63. Reffitt D, Ogston N, Jugdaohsingh R, Cheung H, Evans BAJ, Thompson R, Powell J, Hampson G (2003) Orthosilicic acid stimulates collagen type 1 synthesis and osteoblastic differentiation in human osteoblast-like cells in vitro. Bone 32:127–135. https://doi.org/10.1016/S8756-3282(02)00950-X

    Article  CAS  Google Scholar 

  64. Orlando I, Basnett P, Nigmatullin R, Wang W, Knowles JC, Roy I (2020) Chemical modification of bacterial cellulose for the development of an antibacterial wound dressing. Frontiers in Bioengineering and Biotechnology 8:557885. https://doi.org/10.3389/fbioe.2020.557885

    Article  Google Scholar 

  65. Shi Z, Xu Y, Mulatibieke R, Zhong Q, Pan X, Chen Y, Lian Q, Luo X, Shi Z, Zhu Q (2020) Nanosilicate-reinforced and SDF-1α-loaded gelatin-methacryloyl hydrogel for bone tissue engineering. Int J Nanomed 15:9337. https://doi.org/10.2147/IJN.S270681

    Article  CAS  Google Scholar 

  66. Su D, Jiang L, Chen X, Dong J, Shao Z (2016) Enhancing the gelation and bioactivity of injectable silk fibroin hydrogel with laponite nanoplatelets. ACS Appl Mater Interfaces 8:9619–9628. https://doi.org/10.1021/acsami.6b00891

    Article  CAS  Google Scholar 

  67. Gaharwar AK, Mihaila SM, Swami A, Patel A, Sant S, Reis RL, Marques AP, Gomes ME, Khademhosseini A (2013) Bioactive silicate nanoplatelets for osteogenic differentiation of human mesenchymal stem cells. Adv Mater 25:3329–3336. https://doi.org/10.1002/adma.201300584

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the Sharif University of Technology (SUT) [Grant No. QA970816] and Iran National Science Foundation [Grant No. 95-S-48740].

Author information

Authors and Affiliations

  1. Institute for Nanoscience and Nanotechnology, Sharif University of Technology, P.O. Box 11365-8639, Tehran, Iran

    Golara Kafili & Abdolreza Simchi

  2. Department of Nanobiotechnology, Faculty of Biological Sciences, Tarbiat Modares University, P.O. Box 14115-175, Tehran, Iran

    Elnaz Tamjid

  3. Department of Pharmacology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Hassan Niknejad

  4. Department of Materials Science and Engineering, Sharif University of Technology, Azadi Avenue, P.O. Box 11365-11155, Tehran, Iran

    Abdolreza Simchi

Authors
  1. Golara Kafili
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elnaz Tamjid
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hassan Niknejad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abdolreza Simchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

GK was involved in conceptualization, data curation, methodology, investigation, validation, and writing—an original draft. ET and HN were involved in supervision and writing—review and editing. AS was involved in conceptualization, supervision, data curation, project administration, funding acquisition, resources, and writing—review and editing.

Corresponding author

Correspondence to Abdolreza Simchi.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Handling Editor:  Annela M. Seddon.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kafili, G., Tamjid, E., Niknejad, H. et al. Development of printable nanoengineered composite hydrogels based on human amniotic membrane for wound healing application. J Mater Sci 58, 12351–12372 (2023). https://doi.org/10.1007/s10853-023-08783-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10853-023-08783-y

Search

Navigation