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Cited by 60Hydrogels: synthesis, properties, applications3D Printing in Biomedical ResearchTissue Engineering and Regenerative Medicine

Bioprinting of a Blue Light-Cross-Linked Biodegradable Hydrogel Encapsulating Amniotic Mesenchymal Stem Cells for Intrauterine Adhesion Prevention

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Feng, Miao, Hu, Shengxue, Qin, Weibing, Tang, Yunge, Guo, Rui, Han, Liwei·2021·ACS Omega
DOI 10.1021/acsomega.1c02117PMC PMC8444209
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Abstract

Intrauterine adhesion (IUA) is a common and prevailing complication after uterine surgery, which can lead to clinical symptoms such as a low menstrual volume, amenorrhea, periodic lower abdominal pain, infertility, and so on. Placing a three-dimensional printing hydrogel between the injured site and the adjacent tissue is considered to be a physical barrier to prevent adhesion, which can isolate the damaged area during the healing process. In this work, a tissue hydrogel with various proportions of a methacrylated gelatin (GelMA) and methacrylated collagen (ColMA) composite hydrogel loaded with amniotic mesenchymal stem cells (AMSCs) was constructed by using three-dimensional biological printing technology. Compared with the single GelMA hydrogel, the composite antiadhesion hydrogel (GelMA/ColMA) showed an appropriate swelling ratio, enhanced mechanical properties, and impressive stability. Meanwhile, the microstructure of the GelMA/ColMA composite hydrogel showed a denser and interconnected microporous structure. In addition, the cytotoxicity study indicated that the GelMA/ColMA hydrogel has a cytocompatibility nature toward AMSCs. Finally, the fabrication of stem cell encapsulation hydrogels was studied, and the cells could be released continuously for more than 7 days with the normal cell function. The results of in vivo experiments indicated that the GelMA/ColMA/hAMSC (human amnion mesenchymal stem cell) hydrogel can prevent cavity adhesion in a rat IUA model. Therefore, bioprinting a biodegradable hydrogel cross-linked by blue light has satisfactory anticavity adhesion effects with excellent physical properties and biocompatibility, which could be used as a preventive barrier for intrauterine adhesion.

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  • A composite hydrogel of GelMA and collagen methacrylate bioprinted with encapsulated human amniotic mesenchymal stem cells and crosslinked by blue light successfully prevented uterine cavity adhesions in a rat model of intrauterine adhesions, demonstrating excellent biocompatibility and anti-adhesion efficacy.

    “For instance, a composite hydrogel of gelatin methacrylate (GelMA) and collagen methacrylate was bioprinted with encapsulated human amniotic mesenchymal stem cells (hAMSCs) and crosslinked by blue light. In a rat model of intrauterine adhesions, this cell-laden printed hydrogel successfully prevented uterine cavity adhesions, demonstrating excellent biocompatibility and anti-adhesion efficacy [275”

    From Biomaterials in Postoperative Adhesion Barriers and Uterine Tissue Engineering (2025) · cites this paper as [275]

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Research works printed but not linked: 41

  1. Wei C.; Pan Y.; Zhang Y.; Dai Y.; Jiang L.; Shi L.; Yang W.; Xu S.; Zhang Y.; Xu W.; Zhang Y.; Lin X.; Zhang S. Overactivated sonic hedgehog signaling aggravates intrauterine adhesion via inhibiting autophagy in endometrial stromal cells. Cell Death Dis. 2020, 11, 755– 755. 10.1038/s41419-020-02956-2. 32934215 PMC7492405 · DOI
  2. Zhu X.; Ye H.; Fu Y. The effect of frozen-thawed embryo transfer performed concurrently with hysteroscopy on the reproductive outcomes during assisted reproductive treatments. Sci. Rep. 2017, 7, 11852– 11852. 10.1038/s41598-017-12068-1. 28928434 PMC5605495 · DOI
  3. Chen G.; Liu L.; Sun J.; Zeng L.; Cai H.; He Y. Foxf2 and Smad6 co-regulation of collagen 5A2 transcription is involved in the pathogenesis of intrauterine adhesion. J. Cell Mol. Med. 2020, 24, 2802– 2818. 10.1111/jcmm.14708. 32022446 PMC7077542 · DOI
  4. Guo L.-P.; Chen L.-M.; Chen F.; Jiang N.-H.; Sui L. Smad signaling coincides with epithelial-mesenchymal transition in a rat model of intrauterine adhesion. Am. J. Transl. Res. 2019, 11, 4726– 4737. 31497194 PMC6731410
  5. Sebbag L.; Even M.; Fay S.; Naoura I.; Revaux A.; Carbonnel M.; Pirtea P.; de Ziegler D.; Ayoubi J.-M. Early Second-Look Hysteroscopy: Prevention and Treatment of Intrauterine Post-surgical Adhesions. Front. Surg. 2019, 6, 50 10.3389/fsurg.2019.00050. 31475154 PMC6706867 · DOI
  6. Zhang S.-S.; Xia W.-T.; Xu J.; Xu H.-L.; Lu C.-T.; Zhao Y.-Z.; Wu X.-Q. Three-dimensional structure micelles of heparin-poloxamer improve the therapeutic effect of 17β-estradiol on endometrial regeneration for intrauterine adhesions in a rat model. Int. J. Nanomed. 2017, Volume 12, 5643– 5657. 10.2147/IJN.S137237. PMC5557621 28848344 · DOI
  7. Xin L.; Lin X.; Pan Y.; Zheng X.; Shi L.; Zhang Y.; Ma L.; Gao C.; Zhang S. A collagen scaffold loaded with human umbilical cord-derived mesenchymal stem cells facilitates endometrial regeneration and restores fertility. Acta Biomater. 2019, 92, 160– 171. 10.1016/j.actbio.2019.05.012. 31075515 · DOI · Paper page
  8. Gil-Sanchis C.; Cervelló I.; Khurana S.; Faus A.; Verfaillie C.; Simón C. Contribution of different bone marrow-derived cell types in endometrial regeneration using an irradiated murine model. Fertil. Steril. 2015, 103, 1596– 1605.e1. 10.1016/j.fertnstert.2015.02.030. 25813284 · DOI
  9. Santamaria X.; Mas A.; Cervelló I.; Taylor H.; Simon C. Uterine stem cells: from basic research to advanced cell therapies. Hum. Reprod. Update 2018, 24, 673– 693. 10.1093/humupd/dmy028. 30239705 · DOI
  10. Li H.; Yahaya B. H.; Ng W. H.; Yusoff N. M.; Lin J. Conditioned Medium of Human Menstrual Blood-Derived Endometrial Stem Cells Protects Against MPP-Induced Cytotoxicity in vitro. Front. Mol. Neurosci. 2019, 12, 80 10.3389/fnmol.2019.00080. 31024252 PMC6460823 · DOI
  11. Zhao S.; Qi W.; Zheng J.; Tian Y.; Qi X.; Kong D.; Zhang J.; Huang X. Exosomes Derived from Adipose Mesenchymal Stem Cells Restore Functional Endometrium in a Rat Model of Intrauterine Adhesions. Reprod. Sci. 2020, 27, 1266– 1275. 10.1007/s43032-019-00112-6. 31933162 · DOI
  12. Zheng J.-H.; Zhang J.-K.; Kong D.-S.; Song Y.-B.; Zhao S.-D.; Qi W.-B.; Li Y.-N.; Zhang M.-l.; Huang X.-H. Quantification of the CM-Dil-labeled human umbilical cord mesenchymal stem cells migrated to the dual injured uterus in SD rat. Stem Cell Res. Ther. 2020, 11, 280 10.1186/s13287-020-01806-4. 32660551 PMC7359016 · DOI
  13. Tang Z.; Wu X.; Hu L.; Xiao Y.; Tan J.; Zuo S.; Shen M.; Yuan X. Circ-100290 Positively Regulates Angiogenesis Induced by Conditioned Medium of Human Amnion-Derived Mesenchymal Stem Cells Through miR-449a/eNOS and miR-449a/VEGFA Axes. Inter. J. Biol. Sci. 2020, 16, 2131– 2144. 10.7150/ijbs.39895. PMC7294943 32549760 · DOI
  14. Li B.; Zhang Q.; Sun J.; Lai D. Human amniotic epithelial cells improve fertility in an intrauterine adhesion mouse model. Stem Cell Res. Ther. 2019, 10, 257 10.1186/s13287-019-1368-9. 31412924 PMC6694540 · DOI
  15. Gan L.; Duan H.; Xu Q.; Tang Y.-Q.; Li J.-J.; Sun F.-Q.; Wang S. Human amniotic mesenchymal stromal cell transplantation improves endometrial regeneration in rodent models of intrauterine adhesions. Cytotherapy 2017, 19, 603– 616. 10.1016/j.jcyt.2017.02.003. 28285950 · DOI
  16. Yang Y.; Zhao X.; Yu J.; Chen X.; Chen X.; Cui C.; Zhang J.; Zhang Q.; Zhang Y.; Wang S.; Cheng Y. H-Bonding Supramolecular Hydrogels with Promising Mechanical Strength and Shape Memory Properties for Postoperative Antiadhesion Application. ACS Appl. Mater. Interfaces 2020, 12, 34161– 34169. 10.1021/acsami.0c07753. 32631044 · DOI
  17. Ohta S.; Toda T.; Inagaki F.; Omichi K.; Shimizu A.; Kokudo N.; Hasegawa K.; Ito T. The Prevention of Hepatectomy-Induced Adhesions by Bilayer Sponge Composed of Ultrapure Alginate. J. Surg. Res. 2019, 242, 286– 295. 10.1016/j.jss.2019.04.063. 31125842 · DOI
  18. Potyondy T.; Uquillas J.; Tebon P.; Byambaa B.; Hasan A.; Tavafoghi M.; Mary H.; Aninwene Ii G.; Pountos I.; Khademhosseini A.; Ashammakhi N. Recent advances in 3D bioprinting of musculoskeletal tissues. Biofabrication 2021, 022001 10.1088/1758-5090/abc8de. PMC8312688 33166949 · DOI
  19. Zhang P.; Wang H.; Wang P.; Zheng Y.; Liu L.; Hu J.; Liu Y.; Gao Q.; He Y. Lightweight 3D bioprinting with point by point photocuring. Bioact. Mater. 2021, 6, 1402– 1412. 10.1016/j.bioactmat.2020.10.023. 33210032 PMC7658498 · DOI
  20. Cheng F.; Wu Y.; Li H.; Yan T.; Wei X.; Wu G.; He J.; Huang Y. Biodegradable N, O-carboxymethyl chitosan/oxidized regenerated cellulose composite gauze as a barrier for preventing postoperative adhesion. Carbohydr. Polym. 2019, 207, 180– 190. 10.1016/j.carbpol.2018.10.077. 30599998 · DOI
  21. Feng B.; Wang S.; Hu D.; Fu W.; Wu J.; Hong H.; Domian I. J.; Li F.; Liu J. Bioresorbable electrospun gelatin/polycaprolactone nanofibrous membrane as a barrier to prevent cardiac postoperative adhesion. Acta Biomater. 2019, 83, 211– 220. 10.1016/j.actbio.2018.10.022. 30352286 · DOI
  22. Cheng M.; Chang W.-H.; Yang S.-T.; Huang H.-Y.; Tsui K.-H.; Chang C.-P.; Lee W.-L.; Wang P.-H. Efficacy of Applying Hyaluronic Acid Gels in the Primary Prevention of Intrauterine Adhesion after Hysteroscopic Myomectomy: A Meta-Analysis of Randomized Controlled Trials. Life 2020, 10, 285 10.3390/life10110285. PMC7697815 33203159 · DOI
  23. Fierke C. A.; Hammes G. G. Transient kinetic approaches to enzyme mechanisms. In Contemporary Enzyme Kinetics and Mechanism; 2nd Ed.; Purich D. Ed.; Academic Press: New York, 1996; pp. 1– 35.
  24. Doe J. S.; Smith J.; Roe P. Syntheses and biological activities of rebeccamycin analogues. Introduction of a halogenoacetyl substituent. J. Am. Chem. Soc. 1968, 90, 8234– 8241. 10052965
  25. Cai X.; Hu S.; Yu B.; Cai Y.; Yang J.; Li F.; Zheng Y.; Shi X. Transglutaminase-catalyzed preparation of crosslinked carboxymethyl chitosan/carboxymethyl cellulose/collagen composite membrane for postsurgical peritoneal adhesion prevention. Carbohydr. Polym. 2018, 201, 201– 210. 10.1016/j.carbpol.2018.08.065. 30241812 · DOI
  26. Hu S.; Cai X.; Qu X.; Yu B.; Yan C.; Yang J.; Li F.; Zheng Y.; Shi X. Preparation of biocompatible wound dressings with long-term antimicrobial activity through covalent bonding of antibiotic agents to natural polymers. Int. J. Biol. Macromol. 2019, 123, 1320– 1330. 10.1016/j.ijbiomac.2018.09.122. 30248428 · DOI
  27. Kurzyński M. Protein machine model of enzymatic reactions gated by enzyme internal dynamics. Biophys. Chem. 1997, 65, 1– 28. 10.1016/S0301-4622(96)02209-0. 17029837 · DOI
  28. Chen J.; Cai Z.; Wei Q.; Wang D.; Wu J.; Tan Y.; Lu J.; Ai H. Proanthocyanidin-crosslinked collagen/konjac glucomannan hydrogel with improved mechanical properties and MRI trackable biodegradation for potential tissue engineering scaffolds. J. Mater. Chem. B 2020, 8, 316– 331. 10.1039/C9TB02053E. 31819938 · DOI
  29. Abbas Y.; Brunel L. G.; Hollinshead M. S.; Fernando R. C.; Gardner L.; Duncan I.; Moffett A.; Best S.; Turco M. Y.; Burton G. J.; Cameron R. E. Generation of a three-dimensional collagen scaffold-based model of the human endometrium. Interface Focus 2020, 10, 20190079 10.1098/rsfs.2019.0079. 32194932 PMC7061944 · DOI
  30. Su K.; Edwards S. L.; Tan K. S.; White J. F.; Kandel S.; Ramshaw J. A. M.; Gargett C. E.; Werkmeister J. A. Induction of endometrial mesenchymal stem cells into tissue-forming cells suitable for fascial repair. Acta Biomater. 2014, 10, 5012– 5020. 10.1016/j.actbio.2014.08.031. 25194931 · DOI
  31. Xiao B.; Yang W.; Lei D.; Huang J.; Yin Y.; Zhu Y.; You Z.; Wang F.; Sun S. PGS Scaffolds Promote the In Vivo Survival and Directional Differentiation of Bone Marrow Mesenchymal Stem Cells Restoring the Morphology and Function of Wounded Rat Uterus. Adv. Healthcare Mater. 2019, 8, e1801455 10.1002/adhm.201801455. 30734535 · DOI
  32. Menzies D.; Ellis H. Intestinal obstruction from adhesions--how big is the problem?. Ann. R. Coll. Surg. Engl. 1990, 72, 60– 63. 2301905 PMC2499092
  33. Wu W.; Ni Q.; Xiang Y.; Dai Y.; Jiang S.; Wan L.; Liu X.; Cui W. Fabrication of photo-crosslinked gelatin hydrogel for preventing abdominal adhesion. RSC Adv. 2016, 6, 92449– 92453. 10.1039/C6RA21435E. · DOI
  34. Jin X.; Shang Y.; Zou Y.; Xiao M.; Huang H.; Zhu S.; Liu N.; Li J.; Wang W.; Zhu P. Injectable Hypoxia-Induced Conductive Hydrogel to Promote Diabetic Wound Healing. ACS Appl. Mater. Interfaces 2020, 12, 56681– 56691. 10.1021/acsami.0c13197. 33274927 · DOI
  35. Ucar B.; Kajtez J.; Foidl B. M.; Eigel D.; Werner C.; Long K. R.; Emnéus J.; Bizeau J.; Lomora M.; Pandit A.; Newland B.; Humpel C. Biomaterial based strategies to reconstruct the nigrostriatal pathway in organotypic slice co-cultures. Acta Biomater. 2021, 121, 56681– 56262. 10.1016/j.actbio.2020.11.035. 33242639 · DOI
  36. Dutta S. D.; Hexiu J.; Patel D. K.; Ganguly K.; Lim K.-T. 3D-printed bioactive and biodegradable hydrogel scaffolds of alginate/gelatin/cellulose nanocrystals for tissue engineering. Int. J. Biol. Macromol. 2021, 167, 644– 658. 10.1016/j.ijbiomac.2020.12.011. 33285198 · DOI
  37. Yang Y.; Mao Y.; Wang J.; Sun C.; Zhang Y.; Chen X. In vivo tracing of human amniotic mesenchymal stem cells labeled with PKH26 in rat intrauterine adhesions model. Shengwu Gongcheng Xuebao Chin. J. Biotechnol. 2018, 34, 1660– 1667. 10.13345/j.cjb.180018. 30394033 · DOI
  38. Cho H.; Jammalamadaka U.; Tappa K.; Egbulefu C.; Prior J.; Tang R.; Achilefu S. 3D Printing of Poloxamer 407 Nanogel Discs and Their Applications in Adjuvant Ovarian Cancer Therapy. Mol. Pharmaceutics 2019, 16, 552– 560. 10.1021/acs.molpharmaceut.8b00836. PMC7357236 30608705 · DOI
  39. Zhou F.; Hong Y.; Zhang X.; Yang L.; Li J.; Jiang D.; Bunpetch V.; Hu Y.; Ouyang H.; Zhang S. Tough hydrogel with enhanced tissue integration and in situ forming capability for osteochondral defect repair. Appl. Mater. Today 2018, 13, 32– 44. 10.1016/j.apmt.2018.08.005. · DOI
  40. Eke G.; Mangir N.; Hasirci N.; MacNeil S.; Hasirci V. Development of a UV crosslinked biodegradable hydrogel containing adipose derived stem cells to promote vascularization for skin wounds and tissue engineering. Biomaterials 2017, 129, 188– 198. 10.1016/j.biomaterials.2017.03.021. 28343005 · DOI
  41. Zhao Y.-x.; Chen S.-r.; Huang Q.-y.; Chen W.-c.; Xia T.; Shi Y.-c.; Gao H.-z.; Shi Q.-y.; Lin S. Repair abilities of mouse autologous adipose-derived stem cells and ShakeGelTM3D complex local injection with intrauterine adhesion by BMP7-Smad5 signaling pathway activation. Stem Cell Res. Ther. 2021, 12, 191 10.1186/s13287-021-02258-0. 33736694 PMC7977602 · DOI

Cited by

Sorted by citations

Authors
Feng, M., Hu, S., Qin, W., Tang, Y., Guo, R., & Han, L.
Affiliations
  • Guangdong Provincial Family Planning Hospital (CN)
  • Beogene Biotech (Guangzhou) Co., Ltd., Guangzhou 510663, P. R. China
  • Jinan University (CN)
Corresponding author
  • Guo, Rui
  • Han, Liwei
ORCID
Venue
ACS Omega
Publisher
American Chemical Society (ACS)
Published
2021-09-03
Volume
6
Issue
36
Pages
23067-23075
ISSN
2470-1343 (ISSN-L)
DOI
10.1021/acsomega.1c02117
PMC
PMC8444209
OpenAlex
W3197527587
Cited by
60
References
0
Citations by year
2026: 15 · 2025: 15 · 2024: 12 · 2023: 8 · 2022: 10
FWCI
2.32
Type
journal article
Language
en
Open access
Licence
Locations
  • ACS Omega (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
NHC Key Laboratory of Male Reproduction and Genetics, Family Planning Research Institute of Guangdong Province (KF201705)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
  • Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
Keywords
intrauterine adhesions, bioprinting, biodegradable hydrogels, amniotic mesenchymal stem cells, anti-adhesion barrier, stem cell encapsulation, hydrogel mechanical properties, microporous structure, cytocompatibility, rat model

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