Volume 43 Issue 6
Jun.  2022
Turn off MathJax
Article Contents
Fei BI, Weihua GUO. Advances in Research on Hertwig’s Epithelial Root Sheath Cells[J]. Journal of Kunming Medical University, 2022, 43(6): 159-166. doi: 10.12259/j.issn.2095-610X.S20220628
Citation: Fei BI, Weihua GUO. Advances in Research on Hertwig’s Epithelial Root Sheath Cells[J]. Journal of Kunming Medical University, 2022, 43(6): 159-166. doi: 10.12259/j.issn.2095-610X.S20220628

Advances in Research on Hertwig’s Epithelial Root Sheath Cells

doi: 10.12259/j.issn.2095-610X.S20220628
  • Received Date: 2022-03-28
    Available Online: 2022-06-08
  • Publish Date: 2022-06-30
  • Hertwig's epithelial root sheath (HERS) cells are a special group of cells that play important roles during root development and formation of periodontal tissues. This paper summarizes the origin and morphological structure of HERS cells, as well as the recent researches on their biological behaviors, participation in the regulatory process of tooth development, and potential application to tissue repair and regeneration. It provides a reference for the subsequent study on application strategies and mechanisms of HERS cells and their derivatives in periodontal tissue regeneration.
  • loading
  • [1]
    于世凤. 口腔组织病理学[M]. 北京: 人民卫生出版社, 2012: 40-44.
    [2]
    Slavkin H C,Bringas P J,Bessem C,et al. Hertwig’s epithelial root sheath differentiation and initial cementum and bone formation during long-term organ culture of mouse mandibular first molars using serumless,chemically-defined medium[J]. J Periodontal Res,1989,24(1):28-40. doi: 10.1111/j.1600-0765.1989.tb00854.x
    [3]
    Luan X,Ito Y,Diekwisch T G. Evolution and development of Hertwig’s epithelial root sheath[J]. Dev Dyn,2006,235(5):1167-1180. doi: 10.1002/dvdy.20674
    [4]
    Howes R J. Root formation in ectopically transplanted teeth of the frog,Rana pipiens I. Tooth morphogenesis[J]. Acta Anat (Basel),1977,97(2):151-165. doi: 10.1159/000144729
    [5]
    Suzuki M,Inoue T,Shimono M,et al. Behavior of epithelial root sheath during tooth root formation in porcine molars:TUNEL,TEM,and immunohistochemical studies[J]. Anat Embryol (Berl),2002,206(1-2):13-20. doi: 10.1007/s00429-002-0276-3
    [6]
    Hamamoto Y,Nakajima T,Ozawa H. Ultrastructural and histochemical study on the morphogenesis of epithelial rests of Malassez[J]. Arch Histol Cytol,1989,52(1):61-70. doi: 10.1679/aohc.52.61
    [7]
    Andujar M B,Magloire H,Hartmann D J,et al. Early mouse molar root development:cellular changes and distribution of fibronectin,laminin and type-IV collagen[J]. Differentiation,1985,30(2):111-122. doi: 10.1111/j.1432-0436.1985.tb00522.x
    [8]
    Mu H,Liu X,Geng S,et al. Epithelial Bone Morphogenic Protein 2 and 4 Are Indispensable for Tooth Development[J]. Front Physiol,2021,12:660644. doi: 10.3389/fphys.2021.660644
    [9]
    Yang S,Choi H,Kim T H,et al. Cell dynamics in Hertwig’s epithelial root sheath are regulated by beta-catenin activity during tooth root development[J]. J Cell Physiol,2021,236(7):5387-5398. doi: 10.1002/jcp.30243
    [10]
    Nemoto E,Sakisaka Y,Tsuchiya M,et al. Wnt3a signaling induces murine dental follicle cells to differentiate into cementoblastic/osteoblastic cells via an osterix-dependent pathway[J]. J Periodontal Res,2016,51(2):164-174. doi: 10.1111/jre.12294
    [11]
    Huang H,Wang J,Zhang Y,et al. Bone resorption deficiency affects tooth root development in RANKL mutant mice due to attenuated IGF-1 signaling in radicular odontoblasts[J]. Bone,2018,114:161-171. doi: 10.1016/j.bone.2017.12.026
    [12]
    Nakatomi M,Morita I,Eto K,et al. Sonic hedgehog signaling is important in tooth root development[J]. J Dent Res,2006,85(5):427-431. doi: 10.1177/154405910608500506
    [13]
    Yokohama-tamaki T,Ohshima H,Fujiwara N,et al. Cessation of Fgf10 signaling,resulting in a defective dental epithelial stem cell compartment,leads to the transition from crown to root formation[J]. Development,2006,133(7):1359-1366. doi: 10.1242/dev.02307
    [14]
    Wang J,Feng J Q. Signaling Pathways Critical for Tooth Root Formation[J]. J Dent Res,2017,96(11):1221-1228. doi: 10.1177/0022034517717478
    [15]
    Li J,Parada C,Chai Y. Cellular and molecular mechanisms of tooth root development[J]. Development,2017,144(3):374-384. doi: 10.1242/dev.137216
    [16]
    Huang X,Xu X,Bringas P J,et al. Smad4-Shh-Nfic signaling cascade-mediated epithelial-mesenchymal interaction is crucial in regulating tooth root development[J]. J Bone Miner Res,2010,25(5):1167-1178.
    [17]
    Tian Q,Wang Y Y,Li Q,et al. Expressions of cytokeratin 14 and proliferating cell nuclear antigen in the Hertwig’s epithelial root sheath of a Vps4b knockout mouse[J]. Hua Xi Kou Qiang Yi Xue Za Zhi,2021,39(3):274-278.
    [18]
    Date Y,Kondo H,Yamashita A,et al. Combined in silico analysis identified a putative tooth root formation-related gene,Chd3,which regulates DNA synthesis in HERS01a cells[J]. Odontology,2020,108(3):386-395. doi: 10.1007/s10266-020-00489-w
    [19]
    Date Y,Yokoyama Y,Kondo H,et al. Restricted expression of chromatin remodeling associated factor Chd3 during tooth root development[J]. J Periodontal Res,2012,47(2):180-187. doi: 10.1111/j.1600-0765.2011.01419.x
    [20]
    Xu J,Kawashima N,Fujiwara N,et al. Promotional effects of vasoactive intestinal peptide on the development of rodent Hertwig’s epithelial root sheath[J]. Congenit Anom (Kyoto),2012,52(3):162-167. doi: 10.1111/j.1741-4520.2012.00371.x
    [21]
    Ida-yonemochi H,Satokata I,Ohshima H,et al. Morphogenetic roles of perlecan in the tooth enamel organ:an analysis of overexpression using transgenic mice[J]. Matrix Biol,2011,30(7-8):379-388. doi: 10.1016/j.matbio.2011.08.001
    [22]
    Sakuraba H,Fujiwara N,Sasaki-oikawa A,et al. Hepatocyte growth factor stimulates root growth during the development of mouse molar teeth[J]. J Periodontal Res,2012,47(1):81-88. doi: 10.1111/j.1600-0765.2011.01407.x
    [23]
    Fujiwara N,Lee J W,Kumakami-sakano M,et al. Harmine promotes molar root development via SMAD1/5/8 phosphorylation[J]. Biochem Biophys Res Commun,2018,497(3):924-929. doi: 10.1016/j.bbrc.2017.12.062
    [24]
    Fujiwara N,Akimoto T,Otsu K,et al. Reduction of Egf signaling decides transition from crown to root in the development of mouse molars[J]. J Exp Zool B Mol Dev Evol,2009,312B(5):486-494. doi: 10.1002/jez.b.21268
    [25]
    Fujiwara N,Tabata M J,Endoh M,et al. Insulin-like growth factor-I stimulates cell proliferation in the outer layer of Hertwig’s epithelial root sheath and elongation of the tooth root in mouse molars in vitro[J]. Cell Tissue Res,2005,320(1):69-75. doi: 10.1007/s00441-004-1065-5
    [26]
    Kawakami T,Nakamura Y,Karibe H. Cyclophosphamide inhibits root development of molar teeth in growing mice[J]. Odontology,2015,103(2):143-151. doi: 10.1007/s10266-014-0158-1
    [27]
    Hirose N,Shimazu A,Watanabe M,et al. Ameloblastin in Hertwig’s epithelial root sheath regulates tooth root formation and development[J]. PLoS One,2013,8(1):e54449. doi: 10.1371/journal.pone.0054449
    [28]
    Ide Y,Nakahara T,Nasu M,et al. Cell dynamics in Hertwig’s epithelial root sheath and surrounding mesenchyme in mice irradiated to the head[J]. Oral Dis,2015,21(2):232-239. doi: 10.1111/odi.12253
    [29]
    Nakasone N,Yoshie H. Occlusion regulates tooth-root elongation during root development in rat molars[J]. Eur J Oral Sci,2011,119(6):418-426. doi: 10.1111/j.1600-0722.2011.00856.x
    [30]
    Hodgson B D,Pyszka B,Henry M M,et al. Effect of photobiomodulation on vinblastine-poisoned murine HERS cells[J]. Photomed Laser Surg,2011,29(4):233-237. doi: 10.1089/pho.2010.2794
    [31]
    Jiang X,Liu H. An uncommon type of segmental root development after revitalization[J]. Int Endod J,2020,53(12):1728-1741. doi: 10.1111/iej.13387
    [32]
    Jung I Y,Kim E S,Lee C Y,et al. Continued development of the root separated from the main root[J]. J Endod,2011,37(5):711-714. doi: 10.1016/j.joen.2011.01.015
    [33]
    Andreasen J O,Kristerson L,Andreasen F M. Damage of the Hertwig’s epithelial root sheath:effect upon root growth after autotransplantation of teeth in monkeys[J]. Endod Dent Traumatol,1988,4(4):145-151. doi: 10.1111/j.1600-9657.1988.tb00313.x
    [34]
    Andreasen J O,Paulsen H U,Yu Z,et al. A long-term study of 370 autotransplanted premolars. Part IV. Root development subsequent to transplantation[J]. Eur J Orthod,1990,12(1):38-50. doi: 10.1093/ejo/12.1.38
    [35]
    He M,Wang P,Li B,et al. Rodent incisor and molar dental follicles show distinct characteristics in tooth eruption[J]. Arch Oral Biol,2021,126:105117. doi: 10.1016/j.archoralbio.2021.105117
    [36]
    Yang Y,Ge Y,Chen G,et al. Hertwig's epithelial root sheath cells regulate osteogenic differentiation of dental follicle cells through the Wnt pathway[J]. Bone,2014,63:158-165. doi: 10.1016/j.bone.2014.03.006
    [37]
    Guo Y,Guo W,Chen J,et al. Are Hertwig's epithelial root sheath cells necessary for periodontal formation by dental follicle cells?[J]. Arch Oral Biol,2018,94:1-9. doi: 10.1016/j.archoralbio.2018.06.014
    [38]
    Guo Y,Guo W,Chen J,et al. Comparative study on differentiation of cervical-loop cells and Hertwig’s epithelial root sheath cells under the induction of dental follicle cells in rat[J]. Sci Rep,2018,8(1):6546. doi: 10.1038/s41598-018-24973-0
    [39]
    Jung H S,Lee D S,Lee J H,et al. Directing the differentiation of human dental follicle cells into cementoblasts and/or osteoblasts by a combination of HERS and pulp cells[J]. J Mol Histol,2011,42(3):227-235. doi: 10.1007/s10735-011-9327-5
    [40]
    Bai Y,Bai Y,Matsuzaka K,et al. Cementum- and periodontal ligament-like tissue formation by dental follicle cell sheets co-cultured with Hertwig’s epithelial root sheath cells[J]. Bone,2011,48(6):1417-1426. doi: 10.1016/j.bone.2011.02.016
    [41]
    Duan Y,Li X,Zhang S,et al. Therapeutic potential of HERS spheroids in tooth regeneration[J]. Theranostics,2020,10(16):7409-7421. doi: 10.7150/thno.44782
    [42]
    Thomas H F,Kollar E J. Differentiation of odontoblasts in grafted recombinants of murine epithelial root sheath and dental mesenchyme[J]. Arch Oral Biol,1989,34(1):27-35. doi: 10.1016/0003-9969(89)90043-5
    [43]
    Oh J E,Yi J K. Isolation and characterization of dental follicle-derived Hertwig’s epithelial root sheath cells[J]. Clin Oral Investig,2021,25(4):1787-1796. doi: 10.1007/s00784-020-03481-4
    [44]
    Chen J,Chen G,Yan Z,et al. TGF-beta1 and FGF2 stimulate the epithelial-mesenchymal transition of HERS cells through a MEK-dependent mechanism[J]. J Cell Physiol,2014,229(11):1647-1659. doi: 10.1002/jcp.24610
    [45]
    Li Y,Liu A,Zhang L,et al. Epithelial Cell Rests of Malassez Provide a Favorable Microenvironment for Ameliorating the Impaired Osteogenic Potential of Human Periodontal Ligament Stem Cells[J]. Front Physiol,2021,12:735234. doi: 10.3389/fphys.2021.735234
    [46]
    Bosshardt D D,Stadlinger B,Terheyden H. Cell-to-cell communication-periodontal regeneration[J]. Clin Oral Implants Res,2015,26(3):229-239. doi: 10.1111/clr.12543
    [47]
    Huang X,Bringas P J,Slavkin H C,et al. Fate of HERS during tooth root development[J]. Dev Biol,2009,334(1):22-30. doi: 10.1016/j.ydbio.2009.06.034
    [48]
    Xiong J,Gronthos S,Bartold P M. Role of the epithelial cell rests of Malassez in the development,maintenance and regeneration of periodontal ligament tissues[J]. Periodontol,2013,63(1):217-233.
    [49]
    Kim G H, Yang J, Jeon D H, et al. Differentiation and Establishment of Dental Epithelial-Like Stem Cells Derived from Human ESCs and iPSCs[J]. Int J Mol Sci, 2020, 21(12): 220-226.
    [50]
    Li X,Zhang S,Zhang Z,et al. Development of immortalized Hertwig’s epithelial root sheath cell lines for cementum and dentin regeneration[J]. Stem Cell Res Ther,2019,10(1):3. doi: 10.1186/s13287-018-1106-8
    [51]
    Zhang S,Li X,Wang S,et al. Immortalized Hertwig’s epithelial root sheath cell line works as model for epithelial-mesenchymal interaction during tooth root formation[J]. J Cell Physiol,2020,235(3):2698-2709. doi: 10.1002/jcp.29174
    [52]
    Tsunematsu T,Fujiwara N,Yoshida M,et al. Human odontogenic epithelial cells derived from epithelial rests of Malassez possess stem cell properties[J]. Lab Invest,2016,96(10):1063-1075. doi: 10.1038/labinvest.2016.85
    [53]
    Nam H,Kim J,Park J,et al. Expression profile of the stem cell markers in human Hertwig’s epithelial root sheath/Epithelial rests of Malassez cells[J]. Mol Cells,2011,31(4):355-360. doi: 10.1007/s10059-011-0045-3
    [54]
    Nam H,Kim J H,Kim J W,et al. Establishment of Hertwig’s epithelial root sheath/epithelial rests of Malassez cell line from human periodontium[J]. Mol Cells,2014,37(7):562-567. doi: 10.14348/molcells.2014.0161
    [55]
    Akimoto T,Fujiwara N,Kagiya T,et al. Establishment of Hertwig’s epithelial root sheath cell line from cells involved in epithelial-mesenchymal transition[J]. Biochem Biophys Res Commun,2011,404(1):308-312. doi: 10.1016/j.bbrc.2010.11.112
    [56]
    Zhang S,Yang Y,Jia S,et al. Exosome-like vesicles derived from Hertwig’s epithelial root sheath cells promote the regeneration of dentin-pulp tissue[J]. Theranostics,2020,10(13):5914-5931. doi: 10.7150/thno.43156
    [57]
    Diekwisch T G. The developmental biology of cementum[J]. Int J Dev Biol,2001,45(5-6):695-706.
    [58]
    Yamamoto T,Yamada T,Yamamoto T,et al. Hertwig’s Epithelial Root Sheath Fate during Initial Cellular Cementogenesis in Rat Molars[J]. Acta Histochem Cytochem,2015,48(3):95-101. doi: 10.1267/ahc.15006
    [59]
    Yamamoto T,Yamamoto T,Yamada T,et al. Hertwig’s epithelial root sheath cell behavior during initial acellular cementogenesis in rat molars[J]. Histochem Cell Biol,2014,142(5):489-496. doi: 10.1007/s00418-014-1230-1
    [60]
    Yamamoto T,Takahashi S. Hertwig’s epithelial root sheath cells do not transform into cementoblasts in rat molar cementogenesis[J]. Ann Anat,2009,191(6):547-555. doi: 10.1016/j.aanat.2009.07.004
    [61]
    Bosshardt D D,Nanci A. Immunodetection of enamel- and cementum-related (bone) proteins at the enamel-free area and cervical portion of the tooth in rat molars[J]. J Bone Miner Res,1997,12(3):367-379. doi: 10.1359/jbmr.1997.12.3.367
    [62]
    Bosshardt D D. Are cementoblasts a subpopulation of osteoblasts or a unique phenotype?[J]. J Dent Res,2005,84(5):390-406. doi: 10.1177/154405910508400501
    [63]
    Bosshardt D D,Nanci A. Immunolocalization of epithelial and mesenchymal matrix constituents in association with inner enamel epithelial cells[J]. J Histochem Cytochem,1998,46(2):135-142. doi: 10.1177/002215549804600201
    [64]
    Bosshardt D D,Nanci A. Hertwig’s epithelial root sheath,enamel matrix proteins,and initiation of cementogenesis in porcine teeth[J]. J Clin Periodontol,2004,31(3):184-192. doi: 10.1111/j.0303-6979.2004.00473.x
    [65]
    Hammarstrom L,Alatli I,Fong C D. Origins of cementum[J]. Oral Dis,1996,2(1):63-69.
    [66]
    Alatli I,Lundmark C,Hammarstrom L. The localization of epithelial root sheath cells during cementum formation in rat molars[J]. J Periodontal Res,1996,31(6):433-440. doi: 10.1111/j.1600-0765.1996.tb00512.x
    [67]
    Zeichner-david M,Oishi K,Su Z,et al. Role of Hertwig’s epithelial root sheath cells in tooth root development[J]. Dev Dyn,2003,228(4):651-663. doi: 10.1002/dvdy.10404
    [68]
    Sonoyama W,Seo B M,Yamaza T,et al. Human Hertwig’s epithelial root sheath cells play crucial roles in cementum formation[J]. J Dent Res,2007,86(7):594-599. doi: 10.1177/154405910708600703
    [69]
    Itaya S,Oka K,Ogata K,et al. Hertwig’s epithelial root sheath cells contribute to formation of periodontal ligament through epithelial-mesenchymal transition by TGF-beta[J]. Biomed Res,2017,38(1):61-69. doi: 10.2220/biomedres.38.61
  • Relative Articles

    [1] Xiaobing GUO, Xiaowen LI, Hengxi LI, Yan CAO, Ping LI. miR-212-3p Targeted Regulation of NAP1L1 Inhibits Glioma Cell Proliferation,Migration and EMT. Journal of Kunming Medical University, 2024, 45(11): 22-30.  doi: 10.12259/j.issn.2095-610X.S20241104
    [2] Peng LI, Renchao ZOU, Longao DAI, Songzhou FU, Dong WEI, Bo TANG. The Effect of HIF-1α on Invasion and Metastasis of Gallbladder Cancer by Regulating the Epithelial-Mesenchymal Transformation. Journal of Kunming Medical University, 2024, 45(5): 44-48.  doi: 10.12259/j.issn.2095-610X.S20240507
    [3] Rongyu YANG, Fei SONG, Hao HUANG, Kaiwen DUAN, Yingying XIANG. Application of Bone Marrow Mesenchymal Stem Cells in Stomatology. Journal of Kunming Medical University, 2023, 44(3): 155-159.  doi: 10.12259/j.issn.2095-610X.S20230323
    [4] Li-ya MA, Nan-quan RAO, He-feng YANG. Research Progress of Mesenchymal Stem Cell Exosomes in Oral Tissue Regeneration. Journal of Kunming Medical University, 2021, 42(5): 147-153.  doi: 10.12259/j.issn.2095-610X.S20210527
    [5] Jing-hui LI, Ming ZHU, Hai QU, Qiu-yu LI, Yu-juan WU, He-ying YANG, Yu-zhu WANG, Yan-ping LI. miR-490-3p Suppresses EMT of SW1990 Pancreatic Cancer Cells. Journal of Kunming Medical University, 2021, 42(3): 10-17.  doi: 10.12259/j.issn.2095-610X.S20210305
    [6] Wei Han Xiao , Zhang Ai Jun , Li Qiang , Jin Pei Sheng . . Journal of Kunming Medical University, 2020, 41(09): 50-55.
    [7] Hu Zheng Xiong . Effect of TGF-β2 and geneX on the Proliferation and Osteogenic Differentiation of BrdU-labeled Bone Mesenchymal Stem Cells. Journal of Kunming Medical University,
    [8] Tang Bang Li . Therapeutic Effects and Mechanism of Umbilical Cord Derived Mesenchymal Stem Cell Transplantation for Lupus Nephritis. Journal of Kunming Medical University,
    [9] Yang Dan . Effect of Paracrine Function of Mesenchymal Stem Cells on Diabetic Nephropathy. Journal of Kunming Medical University,
    [10] Kang Qiang . Expression of E-cadherin and Vimentin and Clinic Significance in Intrahepatic Cholangiocarcinoma. Journal of Kunming Medical University,
    [11] Yi Min . . Journal of Kunming Medical University,
    [12] Tai Wen Lin . . Journal of Kunming Medical University,
    [13] Qi Zong Ze . . Journal of Kunming Medical University,
    [14] Wang Dian Hua . . Journal of Kunming Medical University,
    [15] Wang Tao . . Journal of Kunming Medical University,
    [16] Mao Xi Hong . Pathological Study of PNS in Regulating Cathepsin B Expression in Rabbits with Pulmonary Fibrosis of Pulmonary Heart Disease. Journal of Kunming Medical University,
    [17] Tai Wen Lin . Anti-inflammatory,Analgesic and Choleretic Effect of Lidan Zhitong Capsulen Mice. Journal of Kunming Medical University,
    [18] Huang Ying . The Research of Mouse Bone Marrow-derived Mesenchymal Stem Cells Culture Condition in vitro. Journal of Kunming Medical University,
    [19] . Inducing Differentiation of Pig's Bone Mesenchymal Stem Cell(BMSC) to Urothelial Epithelia in Vitro. Journal of Kunming Medical University,
    [20] Yang Feng . . Journal of Kunming Medical University,
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (2453) PDF downloads(50) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return