AccScience Publishing / IJB / Volume 8 / Issue 3 / DOI: 10.18063/ijb.v8i3.512
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RESEARCH ARTICLE

3D-bioprinted Recombination Structure of Hertwig’s Epithelial Root Sheath Cells and Dental Papilla Cells for Alveolar Bone Regeneration

Huilin Tang1,2,3 Fei Bi1,2,3 Guoqing Chen4 Shuning Zhang1,2,3 Yibing Huang1,2,3 Jiahao Chen1,2,3 Li Xie5,6 Xiangchen Qiao7 Weihua Guo1,2,3*
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1 State Key Laboratory of Oral Disease, West China Hospital of Stomatology, Sichuan University, Chengdu, China
2 National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
3 Department of Pediatric Dentistry, West China School of Stomatology, Sichuan University, Chengdu, China
4 Department of Human Anatomy, School of Medicine, University of Electronic Science and Technology of China, Chengdu, China
5 National Engineering Laboratory for Oral Regenerative Medicine, West China Hospital of Stomatology, Sichuan University, Chengdu, China
6 Engineering Research Center of Oral Translational Medicine, Ministry of Education, State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, China
7 Chengdu Renjitiancheng Biotechnology Limited Corporation, Chengdu, China
Submitted: 1 February 2022 | Accepted: 20 April 2022 | Published: 10 June 2022
(This article belongs to the Special Issue 3D Bioprinting with Photocurable Bioinks--Call for Papers )
© 2022 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Abstract

Three-dimensional (3D) bioprinting is an emerging method for tissue regeneration. However, promoting the epithelial-mesenchymal interaction (EMI), while maintaining the characteristics of epithelial cells has always been a challenge in tissue engineering. Since EMI acts as a critical factor in bone regeneration, this study aims to promote EMI by recombining epithelial and mesenchymal cells through 3D bioprinting. Hertwig’s epithelial root sheath (HERS) is a transient structure appeared in the process of tooth root formation. Its epithelial characteristics are easy to attenuate under appropriate culture environment. We recombined HERS cells and dental papilla cells (DPCs) through 3D bioprinting to simulate the microenvironment of cell-cell interaction in vivo. HERS cells and DPCs were mixed with gelatin methacrylate (GelMA) separately to prepare bio-inks for bioprinting. The cells/GelMA constructs were transplanted into the alveolar socket of Sprague-Dawley rats and then observed for 8 weeks. Hematoxylin and eosin staining, Masson staining, and immunohistochemical analysis showed that dimensional cultural pattern provided ideal environment for HERS cells and DPCs to generate mineralization texture and promote alveolar bone regeneration through their interactions. 3D bioprinting technology provides a new way for the co-culture of HERS cells and DPCs and this study is inspiring for future research on EMI model.

Keywords
Epithelial-mesenchymal interaction
3D bioprinting
Hertwig’s epithelial root sheath cell
Alveolar bone regeneration
References

1. Nanci A, editor, 2013, Development of the Tooth and its Supporting Tissues. In: Ten Cate’s Oral Histology: Development, Structure, and Function. St. Louis, Missouri: Elsevier, Mosby. p70–71. https://doi.org/10.1016/B978-0-323-07846-7.00005-7

2. Zhang YD, Chen Z, Song YQ, et al., 2005, Making a Tooth: Growth Factors, Transcription Factors, and Stem Cells. Cell Res, 15:301–16. http://doi.org/10.1038/sj.cr.7290299

3. De Luca M, Aiuti A, Cossu G, et al., 2019, Advances in Stem Cell Research and Therapeutic Development. Nat Cell Biol, 21:801–11. http://doi.org/10.1038/s41556-019-0344-z

4. Ikeda E, Morita R, Nakao K, et al., 2009, Fully Functional Bioengineered Tooth Replacement as an Organ Replacement Therapy. Proc Natl Acad Sci U S A, 106:13475–80. http://doi.org/10.1073/pnas.0902944106

5. Nakao K, Morita R, Saji Y, et al., 2007, The Development of a Bioengineered Organ Germ Method. Nat Methods, 4:227–30. http://doi.org/10.1038/nmeth1012

6. Monteiro N, Smith EE, Angstadt S, et al., 2016, Dental Cell Sheet Biomimetic Tooth Bud Model. Biomaterials, 106:167–79. http://doi.org/10.1016/j.biomaterials.2016.08.024

7. Smith EE, Angstadt S, Monteiro N, et al., 2018, Bioengineered Tooth Buds Exhibit Features of Natural Tooth Buds. J Dent Res, 97:1144–51. http://doi.org/10.1177/0022034518779075

8. Nanci A, editor, 2013, Development of the Tooth and its Supporting Tissues. In: Ten Cate’s Oral Histology: Development, Structure, and Function. St. Louis, Missouri: Elsevier, Mosby. p89–90. https://doi.org/10.1016/B978-0-323-07846-7.00005-7

9. Nanci A, editor, 2013, Periodontium. In: Ten Cate’s Oral Histology: Development, Structure, and Function. St. Louis, Missouri: Elsevier, Mosby. p207. https://doi.org/10.1016/B978-0-323-07846-7.00009-4

10. Duan Y, Li X, Zhang S, et al., 2020, Therapeutic Potential of HERS Spheroids in Tooth Regeneration. Theranostics, 10:7409–21. http://doi.org/10.7150/thno.44782

11. Vijayavenkataraman S, Yan W, Lu WF, et al., 2018, 3D Bioprinting of Tissues and Organs for Regenerative Medicine. Adv Drug Deliver Rev, 132:296–332. http://doi.org/10.1016/j.addr.2018.07.004

12. Ji Y, Yang Q, Huang G, et al., 2019, Improved Resolution and Fidelity of Droplet-Based Bioprinting by Upward Ejection. ACS Biomater Sci Eng, 5:4112–21. http://doi.org/10.1021/acsbiomaterials.9b00400

13. Yang Q, Lian Q, Xu F, 2017, Perspective: Fabrication of integrated organ-on-a-chip via bioprinting. Biomicrofluidics, 11:31301. http://doi.org/10.1063/1.4982945

14. Qing H, Ji Y, Li W, et al., 2020, Microfluidic Printing of Three-Dimensional Graphene Electroactive Microfibrous Scaffolds. ACS Appl Mater Interfaces, 12:2049–58. http://doi.org/10.1021/acsami.9b17948

15. Yang Q, Gao B, Xu F, 2019, Recent Advances in 4D Bioprinting. Biotechnol J, 15:1900086. http://doi.org/10.1002/biot.201900086

16. Bordas SP, Balint DS, editors, 2021, Mechanics of Hydrogel based Bioprinting: From 3D to 4D. In: Advances in Applied Mechanics. San Diego, CA: Elsevier. p285–318. https://doi.org/10.1016/bs.aams.2021.03.001

17. Gao B, Yang Q, Zhao X, et al., 2016, 4D Bioprinting for Biomedical Applications. Trends Biotechnol, 34:746–56. http://doi.org/10.1016/j.tibtech.2016.03.004

18. Zhou M, Lee BH, Tan LP, 2017, A Dual Crosslinking Strategy to Tailor Rheological Properties of Gelatin Methacryloyl. Int J Bioprinting, 3:3. http://doi.org/10.18063/IJB.2017.02.003

19. Ma Y, Xie L, Yang B, et al., 2018, Three‐Dimensional Printing Biotechnology for the Regeneration of the Tooth and Tooth‐supporting Tissues. Biotechnol Bioeng, 116:452–68. http://doi.org/10.1002/bit.26882

20. Yang T, Zhang Q, Xie L, et al., 2021, hDPSC-laden GelMA Microspheres Fabricated Using Electrostatic Microdroplet Method for Endodontic Regeneration. Mater Sci Eng C, 121:111850. http://doi.org/10.1016/j.msec.2020.111850

21. Smith EE, Zhang W, Schiele NR, et al., 2017, Developing a Biomimetic Tooth Bud Model. J Tissue Eng Regen Med, 11:3326–36. http://doi.org/10.1002/term.2246

22. Khayat A, Monteiro N, Smith EE, et al., 2016, GelMA Encapsulated hDPSCs and HUVECs for Dental Pulp Regeneration. J Dent Res, 96:192–9. http://doi.org/10.1177/0022034516682005

23. Murphy C, Kolan K, Li W, et al., 2017, 3D Bioprinting of Stem Cells and Polymer/Bioactive Glass Composite Scaffolds for Tissue Engineering. Int J Bioprint, 3:5. http://doi.org/10.18063/IJB.2017.01.005

24. Ma Y, Ji Y, Zhong T, et al., 2017, Bioprinting-Based PDLSCECM Screening for in Vivo Repair of Alveolar Bone Defect Using Cell-Laden, Injectable and Photo crosslinkable Hydrogels. ACS Biomater Sci Eng, 3:3534–45. http://doi.org/10.1021/acsbiomaterials.7b00601

25. Barros NR, Kim H, Gouidie MJ, et al., 2021, Biofabrication of Endothelial Cell, Dermal Fibroblast, and Multilayered Keratinocyte Layers for Skin Tissue Engineering. Biofabrication, 13:35030. http://doi.org/10.1088/1758-5090/aba503

26. Chen J, Chen G, Yan Z, et al., 2014, TGF-β1 and FGF2 Stimulate the Epithelial-Mesenchymal Transition of HERS Cells Through a MEK-Dependent Mechanism, J Cell Physiol, 229:1647–59. http://doi.org/10.1002/jcp.24610

27. Chen G, Sun W, Liang Y, et al., 2017, Maternal Diabetes Modulates Offspring Cell Proliferation and Apoptosis During Odontogenesis via the TLR4/NF-κB Signalling Pathway. Cell Prolif, 50:e12324. http://doi.org/10.1111/cpr.12324

28. Chen T, Liu Z, Sun W, et al., 2015, Inhibition of Ape1 Redox Activity Promotes Odonto/osteogenic Differentiation of Dental Papilla Cells. Sci Rep, 5:17483. http://doi.org/10.1038/srep17483

29. Li X, Zhang S, Zhang Z, et al., 2019, Development of Immortalized Hertwig’s Epithelial Root Sheath Cell Lines for Cementum and Dentin Regeneration. Stem Cell Res Ther, 10:3. http://doi.org/10.1186/s13287-018-1106-8

30. Billiet T, Gevaert E, De Schryver T, et al., 2014, The 3D Printing of Gelatin Methacrylamide Cell-laden Tissue engineered Constructs with High Cell Viability. Biomaterials, 35:49–62. http://doi.org/10.1016/j.biomaterials.2013.09.078

31. Laronda MM, Rutz AL, Xiao S, et al., 2017, A Bioprosthetic Ovary Created Using 3D Printed Microporous Scaffolds Restores Ovarian Function in Sterilized Mice. Nat Commun, 8:15261. http://doi.org/10.1038/ncomms15261

32. Jiang G, Li S, Yu K, et al., 2021, A 3D-printed PRP-GelMA Hydrogel Promotes Osteochondral Regeneration through M2 Macrophage Polarization in a Rabbit Model. Acta Biomater, 128:150–62. http://doi.org/10.1016/j.actbio.2021.04.010

33. Ren J, Wang H, Tran K, et al., 2015, Human Bone Marrow Stromal Cell Confluence: Effects on Cell Characteristics and Methods of Assessment. Cytotherapy, 17:897–911. http://doi.org/10.1016/j.jcyt.2015.03.607

34. Odeleye AO, Castillo-Avila S, Boon M, et al., 2017, Development of an Optical System for the Non-invasive Tracking of Stem Cell Growth on Microcarriers. Biotechnol Bioeng, 114:2032–42. http://doi.org/10.1002/bit.26328

35. Honda MJ, Tsuchiya S, Sumita Y, et al., 2007, The Sequential Seeding of Epithelial and Mesenchymal Cells for Tissue engineered Tooth Regeneration. Biomaterials, 28:680–9. http://doi.org/10.1016/j.biomaterials.2006.09.039

36. Thesleff I, Hurmerinta K, 1981, Tissue Interactions in Tooth Development. Differentiation (London), 18:75. https://doi.org/10.1111/j.1432-0436.1981.tb01107.x

37. Slavkin HC, Snead ML, Zeichner-David M, et al., 1984, Concepts of Epithelial-mesenchymal Interactions during Development: Tooth and Lung Organogenesis. J Cell Biochem, 26:117–25. http://doi.org/10.1002/jcb.240260207

38. Thesleff I, Lehtonen E, Saxen L, 1978, Basement Membrane Formation in Transfilter Tooth Culture and its Relation to Odontoblast Differentiation. Differentiation, 10:71–9. http://doi.org/10.1111/j.1432-0436.1978.tb00948.x

39. Zeichner-David M, Oishi K, Su Z, et al., 2003, Role of Hertwig’s Epithelial Root Sheath Cells in Tooth Root Development. Dev Dyn, 228:651–63. http://doi.org/10.1002/dvdy.10404

40. Sonoyama W, Seo BM, Yamaza T, et al., 2007, Human Hertwig’s Epithelial Root Sheath Cells Play Crucial Roles in Cementum Formation. J Dent Res, 86:594–9. http://doi.org/10.1177/154405910708600703

41. Xie M, Zheng Y, Gao Q, et al., 2021, Facile 3D Cell Culture Protocol Based on Photocurable Hydrogels. Biodes Manuf, 4:149–53. http://doi.org/10.1007/s42242-020-00096-2

42. Yelick PC, Sharpe PT, 2019, Tooth Bioengineering and Regenerative Dentistry. J Dent Res, 98:1173–82.  http://doi.org/10.1177/0022034519861903

43. Ono M, Oshima M, Ogawa M, et al., 2017, Practical Whole tooth Restoration Utilizing Autologous Bioengineered Tooth Germ Transplantation in a Postnatal Canine Model. Sci Rep, 7:44522. http://doi.org/10.1038/srep44522

44. Li J, Parada C, Chai Y, 2017, Cellular and Molecular Mechanisms of Tooth Root Development. Development, 144:374–84. http://doi.org/10.1242/dev.137216

45. Aubin JE, Liu F, Malaval L, et al., 1995, Osteoblast and Chondroblast Differentiation. Bone, 17 Suppl2:77S–83. http://doi.org/10.1016/8756-3282(95)00183-e

46. Kim S, Turnbull J, Guimond S, 2011, Extracellular Matrix and Cell Signalling: The Dynamic Cooperation of Integrin, Proteoglycan and Growth Factor Receptor. J Endocrinol, 209:139–51. http://doi.org/10.1530/JOE-10-0377

47. Li W, Chen L, Chen Z, et al., 2017, Dentin Sialoprotein Facilitates Dental Mesenchymal Cell Differentiation and Dentin Formation. Sci Rep, 7:300. http://doi.org/10.1038/s41598-017-00339-w

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International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing