Effects of immune responses mediated by topological structures of three-dimensional bioprinted scaffolds on hair follicle cycle in mice

Liu Qinghua; Li Zhao; Enhejirigala; Zhang Chao; Song Wei; Wang Yuzhen; Liang Liting; Zhang Mengde; Huang Yuyan; Li Xiaohe; Huang Sha

doi:10.3760/cma.j.cn501225-20231020-00125

Volume 40 Issue 1

Jan. 2024

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Article Navigation > CHINESE JOURNAL OF BURNS AND WOUNDS > 2024 > 40(1): 43-49

Liu QH,Li Z,Enhejirigala,et al.Effects of immune responses mediated by topological structures of three-dimensional bioprinted scaffolds on hair follicle cycle in mice[J].Chin J Burns Wounds,2024,40(1):43-49.DOI: 10.3760/cma.j.cn501225-20231020-00125.

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Effects of immune responses mediated by topological structures of three-dimensional bioprinted scaffolds on hair follicle cycle in mice

doi: 10.3760/cma.j.cn501225-20231020-00125

1.
School of Basic Medical Sciences, Inner Mongolia Medical University, Hohhot 010110, China
2.
Research Center for Wound Repair and Tissue Regeneration, Medical Innovation Research Department, the PLA General Hospital, Beijing 100048, China
3.
Department of Human Anatomy, Basic Medical School, Inner Mongolia Medical University, Hohhot 010110, China

Funds:

National Key Research and Development Program of China 2022YFA1104600, 2022YFA1104604, 2017YFC1103303

Science Fund for National Defense Distinguished Young Scholars 2022-JCJQ-ZQ-016

National Defense Science and Technology Basic Enhancement Program 2022-JCJQ-ZD-096-00, 2023-JCJQ-ZD-117-12

General Program of National Natural Science Foundation of China 82274362

Youth Science Foundation Project of National Natural Science Foundation of China 32000969

Scientific Research Project of the Key Laboratory for Military Research 2023-JSKY-SSQG-008

Natural Science Foundation of Inner Mongolia Autonomous Region of China 2021LHMS08050

Inner Mongolia Autonomous Region Higher Education Innovation Team Development Plan NMGIRT2227

Key Project of Inner Mongolia Medical University YKD2021ZD001

More Information

Corresponding author: Li Xiaohe, Email: 798242742@qq.com; Huang Sha, Email: stellarahuang@sina.com
Received Date: 2023-10-20

Abstract

Abstract

Objective To explore the effects of the immune responses mediated by topological structures of three-dimensional bioprinted scaffolds on hair follicle cycle in mice. Methods The study was an experimental research. The alginate-gelatin composite hydrogels were printed into scaffolds using a three-dimensional bioprinter and named T45 scaffolds, T60 scaffolds, and T90 scaffolds according to the 3 topological structures of the scaffolds (the rotation angles of the printhead during printing were 45°, 60°, and 90°, respectively), and the morphology of the three scaffolds was observed after cross-linking by naked eyes. Nine 8-week-old female C57BL/6J mice were divided into T45 group, T60 group, and T90 group, according to the random number table, with three mice in each group, and the T45, T60, and T90 scaffolds were subcutaneously implanted on the back of mice, respectively. On post implantation day (PID) 7, the hair growth in the dorsal depilated area of mice was observed, the thickness of the fiber capsule around the scaffolds was observed by hematoxylin-eosin staining, and the expression levels of CD68, bone morphogenetic protein-2 (BMP-2), and tumor necrosis factor (TNF) protein in the tissue surrounding the scaffolds were observed by immunofluorescence staining. The samples of the above experiments were all 3. Results The topological structures of the three scaffolds were all clear with high fidelity after cross-linking. On PID 7, the hair growth was obvious in the dorsal depilated area of mice in T45 group and T90 group, while hair growth was slow in the scaffold implantation area of mice in T60 group, which was significantly different from that of the unimplanted area. On PID 7, compared with (18±4) μm in T90 group, the thickness of both the fiber capsule around the scaffolds ((39±4) and (55±8) μm) of mice in T45 group and T60 group was significantly increased ( P<0.05); the thickness of the fiber capsule around the scaffolds of mice in T60 group was also significantly increased compared with that in T45 group ( P<0.05). On PID 7, the expression level of CD68 protein in the tissue surrounding the scaffolds of mice in T60 group was significantly higher than the levels in T45 group and T90 group (with both P values <0.05). The expression level of BMP-2 protein in the tissue surrounding the scaffolds of mice in T60 group was significantly higher than the levels in T45 group and T90 group (with both P values <0.05), and the expression level of BMP-2 protein in the tissue surrounding the scaffolds of mice in T45 group was significantly higher than that in T90 group ( P<0.05). The expression level of TNF protein in the tissue surrounding the scaffolds of mice in T60 group was significantly lower than the levels in T45 group and T90 group (with both P values <0.05). Conclusions Three-dimensional bioprinted scaffolds with different topological structures mediate different degrees of immune responses after being implanted in mice. A moderate immune response promotes hair growth in depilated area of mice, while an excessive immune response results inhibits the hair follicle entering into the anagen phase.
- Tissue engineering,
- Printing, three-dimensional,
- Immunity,
- Tissue scaffolds,
- Hair follicle,
- Topology

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References

[1]	ShafieeA, AtalaA. Tissue engineering: toward a new era of medicine[J]. Annu Rev Med, 2017, 68:29-40. DOI: 10.1146/annurev-med-102715-092331.
[2]	NairA, TangLP. Influence of scaffold design on host immune and stem cell responses[J]. Semin Immunol, 2017,29:62-71. DOI: 10.1016/j.smim.2017.03.001.
[3]	李洋, 惠涛涛, 郑东梅, 等. 基于三维生物打印技术的皮肤组织工程研究进展[J].中华烧伤与创面修复杂志,2023,39(11):1096-1100. DOI: 10.3760/cma.j.cn501225-20230131-00029.
[4]	DhaniaS, BernelaM, RaniR, et al. Scaffolds the backbone of tissue engineering: advancements in use of polyhydroxyalkanoates (PHA)[J]. Int J Biol Macromol, 2022, 208: 243-259. DOI: 10.1016/j.ijbiomac.2022.03.030.
[5]	AbnaveP, GhigoE. Role of the immune system in regeneration and its dynamic interplay with adult stem cells[J]. Semin Cell Dev Biol, 2019,87:160-168. DOI: 10.1016/j.semcdb.2018.04.002.
[6]	ZhangB, SuYC, ZhouJC, et al. Toward a better regeneration through implant-mediated immunomodulation: harnessing the immune responses[J]. Adv Sci (Weinh), 2021, 8(16): e2100446. DOI: 10.1002/advs.202100446.
[7]	JiangZW, FuMD, ZhuDJ, et al. Genetically modified immunomodulatory cell-based biomaterials in tissue regeneration and engineering[J]. Cytokine Growth Factor Rev, 2022,66:53-73. DOI: 10.1016/j.cytogfr.2022.05.003.
[8]	AntmenE, VranaNE, HasirciV. The role of biomaterials and scaffolds in immune responses in regenerative medicine: macrophage phenotype modulation by biomaterial properties and scaffold architectures[J]. Biomater Sci, 2021,9(24):8090-8110. DOI: 10.1039/d1bm00840d.
[9]	HeinrichMA, LiuWJ, JimenezA, et al. 3D bioprinting: from benches to translational applications[J]. Small, 2019, 15(23): e1805510. DOI: 10.1002/smll.201805510.
[10]	恩和吉日嘎拉, 张熠杰, 李建军, 等. 生物三维打印类细胞外基质硬度对骨髓间充质干细胞向皮肤附属器细胞分化的影响[J].中华烧伤杂志,2020,36(11):1013-1023. DOI: 10.3760/cma.j.cn501120-20200811-00375.
[11]	ZhangYS, YueK, AlemanJ, et al. 3D bioprinting for tissue and organ fabrication[J]. Ann Biomed Eng, 2017, 45(1): 148-163. DOI: 10.1007/s10439-016-1612-8.
[12]	JinS, YangRL, ChuCY, et al. Topological structure of electrospun membrane regulates immune response, angiogenesis and bone regeneration[J]. Acta Biomater, 2021,129:148-158. DOI: 10.1016/j.actbio.2021.05.042.
[13]	WangPJ, SunYZ, ShiXQ, et al. Bioscaffolds embedded with regulatory modules for cell growth and tissue formation: a review[J]. Bioact Mater, 2020, 6(5): 1283-1307. DOI: 10.1016/j.bioactmat.2020.10.014.
[14]	LiJJ, LiuYF, ZhangYJ, et al. Biophysical and biochemical cues of biomaterials guide mesenchymal stem cell behaviors[J]. Front Cell Dev Biol, 2021, 9: 640388. DOI: 10.3389/fcell.2021.640388.
[15]	WeiQH, ZhouJY, AnYL, et al. Modification, 3D printing process and application of sodium alginate based hydrogels in soft tissue engineering: a review[J]. Int J Biol Macromol, 2023, 232: 123450. DOI: 10.1016/j.ijbiomac.2023.123450.
[16]	MohantoS, NarayanaS, MeraiKP, et al. Advancements in gelatin-based hydrogel systems for biomedical applications: a state-of-the-art review[J]. Int J Biol Macromol, 2023,253(Pt 5):127143. DOI: 10.1016/j.ijbiomac.2023.127143.
[17]	LiJJ, ZhangYJ, EnheJ, et al. Bioactive nanoparticle reinforced alginate/gelatin bioink for the maintenance of stem cell stemness[J]. Mater Sci Eng C Mater Biol Appl, 2021,126:112193. DOI: 10.1016/j.msec.2021.112193.
[18]	YuXP, WangYF, ZhangM, et al. 3D printing of gear-inspired biomaterials: immunomodulation and bone regeneration[J]. Acta Biomater, 2023,156:222-233. DOI: 10.1016/j.actbio.2022.09.008.
[19]	WangYZ, ZhangFL, YaoB, et al. Notch4 participates in mesenchymal stem cell-induced differentiation in 3D-printed matrix and is implicated in eccrine sweat gland morphogenesis[J/OL]. Burns Trauma, 2023,11:tkad032[2023-10-20]. http://www.ncbi.nlm.nih.gov/pubmed/37397510. DOI: 10.1093/burnst/tkad032.
[20]	SchneiderMR, Schmidt-UllrichR, PausR. The hair follicle as a dynamic miniorgan[J]. Curr Biol, 2009,19(3):R132-142. DOI: 10.1016/j.cub.2008.12.005.
[21]	WangXS, ChenHY, TianRY, et al. Macrophages induce AKT/β-catenin-dependent Lgr5 ⁺ stem cell activation and hair follicle regeneration through TNF[J]. Nat Commun, 2017,8:14091. DOI: 10.1038/ncomms14091.
[22]	BuWH, WuYH, GhaemmaghamiAM, et al. Rational design of hydrogels for immunomodulation[J]. Regen Biomater, 2022,9:rbac009. DOI: 10.1093/rb/rbac009.
[23]	PlikusMV, ChuongCM. Complex hair cycle domain patterns and regenerative hair waves in living rodents[J]. J Invest Dermatol, 2008,128(5):1071-1080. DOI: 10.1038/sj.jid.5701180.