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Current Stem Cell Research & Therapy

Editor-in-Chief

ISSN (Print): 1574-888X
ISSN (Online): 2212-3946

Mini-Review Article

Gli1+ Mesenchymal Stem Cells in Bone and Teeth

Author(s): Yange Wu, Xueman Zhou, Wenxiu Yuan, Jiaqi Liu, Wenke Yang, Yufan Zhu, Chengxinyue Ye, Xin Xiong, Qinlanhui Zhang, Jin Liu and Jun Wang*

Volume 17, Issue 6, 2022

Published on: 18 February, 2022

Page: [494 - 502] Pages: 9

DOI: 10.2174/1574888X17666220107102911

Price: $65

Abstract

Mesenchymal stem cells (MSCs) are remarkable and noteworthy. Identification of markers for MSCs enables the study of their niche in vivo. It has been identified that glioma-associated oncogene 1 positive (Gli1+) cells are mesenchymal stem cells supporting homeostasis and injury repair, especially in the skeletal system and teeth. This review outlines the role of Gli1+ cells as MSC subpopulation in both bones and teeth, suggesting the prospects of Gli1 an + cells in stem cell- based tissue engineering.

Keywords: Gli1, injury repair, mesenchymal stem cells, neurovascular bundle, suture, teeth.

Graphical Abstract
[1]
Friedenstein AJ, Petrakova KV, Kurolesova AI, Frolova GP. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 1968; 6(2): 230-47.
[http://dx.doi.org/10.1097/00007890-196803000-00009] [PMID: 5654088]
[2]
Caplan AI. Mesenchymal stem cells. J Orthop Res 1991; 9(5): 641-50.
[http://dx.doi.org/10.1002/jor.1100090504] [PMID: 1870029]
[3]
Ding DC, Shyu WC, Lin SZ. Mesenchymal stem cells. Cell Transplant 2011; 20(1): 5-14.
[http://dx.doi.org/10.3727/096368910X] [PMID: 21396235]
[4]
Zhao H, Chai Y. Stem cells in teeth and craniofacial bones. J Dent Res 2015; 94(11): 1495-501.
[http://dx.doi.org/10.1177/0022034515603972] [PMID: 26350960]
[5]
Levato R, Webb WR, Otto IA, et al. The bio in the ink: cartilage regeneration with bioprintable hydrogels and articular cartilage-derived progenitor cells. Acta Biomater 2017; 61: 41-53.
[http://dx.doi.org/10.1016/j.actbio.2017.08.005] [PMID: 28782725]
[6]
Abad V, Meyers JL, Weise M, et al. The role of the resting zone in growth plate chondrogenesis. Endocrinology 2002; 143(5): 1851-7.
[http://dx.doi.org/10.1210/endo.143.5.8776] [PMID: 11956168]
[7]
Haraguchi R, Kitazawa R, Imai Y, Kitazawa S. Growth plate-derived hedgehog-signal-responsive cells provide skeletal tissue components in growing bone. Histochem Cell Biol 2018; 149(4): 365-73.
[http://dx.doi.org/10.1007/s00418-018-1641-5] [PMID: 29356962]
[8]
Xiao H, Wang L, Zhang T, et al. Periosteum progenitors could stimulate bone regeneration in aged murine bone defect model. J Cell Mol Med 2020; 24(20): 12199-210.
[http://dx.doi.org/10.1111/jcmm.15891] [PMID: 32931157]
[9]
Maruyama T, Jeong J, Sheu TJ, Hsu W. Stem cells of the suture mesenchyme in craniofacial bone development, repair and regeneration. Nat Commun 2016; 7: 10526.
[http://dx.doi.org/10.1038/ncomms10526] [PMID: 26830436]
[10]
Kong L, Wang Y, Ji Y, Chen J, Cui J, Shen W. Isolation and characterization of human suture mesenchymal stem cells in vitro. Int J Stem Cells 2020; 13(3): 377-85.
[http://dx.doi.org/10.15283/ijsc20024] [PMID: 32587131]
[11]
Sharpe PT. Dental mesenchymal stem cells. Development 2016; 143(13): 2273-80.
[http://dx.doi.org/10.1242/dev.134189] [PMID: 27381225]
[12]
Gronthos S, Mankani M, Brahim J, Robey PG, Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA 2000; 97(25): 13625-30.
[http://dx.doi.org/10.1073/pnas.240309797] [PMID: 11087820]
[13]
Miura M, Gronthos S, Zhao M, et al. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA 2003; 100(10): 5807-12.
[http://dx.doi.org/10.1073/pnas.0937635100] [PMID: 12716973]
[14]
Seo BM, Miura M, Gronthos S, et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004; 364(9429): 149-55.
[http://dx.doi.org/10.1016/S0140-6736(04)16627-0] [PMID: 15246727]
[15]
Morsczeck C, Götz W, Schierholz J, et al. Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol 2005; 24(2): 155-65.
[http://dx.doi.org/10.1016/j.matbio.2004.12.004] [PMID: 15890265]
[16]
Sonoyama W, Liu Y, Fang D, et al. Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS One 2006; 1: e79.
[http://dx.doi.org/10.1371/journal.pone.0000079] [PMID: 17183711]
[17]
Sonoyama W, Liu Y, Yamaza T, et al. Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod 2008; 34(2): 166-71.
[http://dx.doi.org/10.1016/j.joen.2007.11.021] [PMID: 18215674]
[18]
Boregowda SV, Krishnappa V, Chambers JW, et al. Atmospheric oxygen inhibits growth and differentiation of marrow-derived mouse mesenchymal stem cells via a p53-dependent mechanism: implications for long-term culture expansion. Stem Cells 2012; 30(5): 975-87.
[http://dx.doi.org/10.1002/stem.1069] [PMID: 22367737]
[19]
Kfoury Y, Scadden DT. Mesenchymal cell contributions to the stem cell niche. Cell Stem Cell 2015; 16(3): 239-53.
[http://dx.doi.org/10.1016/j.stem.2015.02.019] [PMID: 25748931]
[20]
Méndez-Ferrer S, Michurina TV, Ferraro F, et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010; 466(7308): 829-34.
[http://dx.doi.org/10.1038/nature09262] [PMID: 20703299]
[21]
Zhu X, Hill RA, Dietrich D, Komitova M, Suzuki R, Nishiyama A. Age-dependent fate and lineage restriction of single NG2 cells. Development 2011; 138(4): 745-53.
[http://dx.doi.org/10.1242/dev.047951] [PMID: 21266410]
[22]
Park D, Spencer JA, Koh BI, et al. Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell 2012; 10(3): 259-72.
[http://dx.doi.org/10.1016/j.stem.2012.02.003] [PMID: 22385654]
[23]
Roguljic H, Matthews BG, Yang W, Cvija H, Mina M, Kalajzic I. In vivo identification of periodontal progenitor cells. J Dent Res 2013; 92(8): 709-15.
[http://dx.doi.org/10.1177/0022034513493434] [PMID: 23735585]
[24]
Zhou BO, Yue R, Murphy MM, Peyer JG, Morrison SJ. Leptin-receptor-expressing mesenchymal stromal cells represent the main source of bone formed by adult bone marrow. Cell Stem Cell 2014; 15(2): 154-68.
[http://dx.doi.org/10.1016/j.stem.2014.06.008] [PMID: 24953181]
[25]
Worthley DL, Churchill M, Compton JT, et al. Gremlin 1 identifies a skeletal stem cell with bone, cartilage, and reticular stromal potential. Cell 2015; 160(1-2): 269-84.
[http://dx.doi.org/10.1016/j.cell.2014.11.042] [PMID: 25594183]
[26]
Kramann R, Schneider RK, DiRocco DP, et al. Perivascular Gli1+ progenitors are key contributors to injury-induced organ fibrosis. Cell Stem Cell 2015; 16(1): 51-66.
[http://dx.doi.org/10.1016/j.stem.2014.11.004] [PMID: 25465115]
[27]
Yue R, Zhou BO, Shimada IS, Zhao Z, Morrison SJ. Leptin receptor promotes adipogenesis and reduces osteogenesis by regulating mesenchymal stromal cells in adult bone marrow. Cell Stem Cell 2016; 18(6): 782-96.
[http://dx.doi.org/10.1016/j.stem.2016.02.015] [PMID: 27053299]
[28]
Miwa H, Era T. Tracing the destiny of mesenchymal stem cells from embryo to adult bone marrow and white adipose tissue via Pdgfrα expression. Development 2018; 145(2): dev155879.
[http://dx.doi.org/10.1242/dev.155879] [PMID: 29378823]
[29]
Mizuhashi K, Ono W, Matsushita Y, et al. Resting zone of the growth plate houses a unique class of skeletal stem cells. Nature 2018; 563(7730): 254-8.
[http://dx.doi.org/10.1038/s41586-018-0662-5] [PMID: 30401834]
[30]
Kuwahara ST, Serowoky MA, Vakhshori V, et al. Sox9+ messenger cells orchestrate large-scale skeletal regeneration in the mammalian rib. eLife 2019; 8: e40715.
[http://dx.doi.org/10.7554/eLife.40715] [PMID: 30983567]
[31]
Pineault KM, Song JY, Kozloff KM, Lucas D, Wellik DM. Hox11 expressing regional skeletal stem cells are progenitors for osteoblasts, chondrocytes and adipocytes throughout life. Nat Commun 2019; 10(1): 3168.
[http://dx.doi.org/10.1038/s41467-019-11100-4] [PMID: 31320650]
[32]
Feng H, Xing W, Han Y, et al. Tendon-derived cathepsin K-expressing progenitor cells activate Hedgehog signaling to drive heterotopic ossification. J Clin Invest 2020; 130(12): 6354-65.
[http://dx.doi.org/10.1172/JCI132518] [PMID: 32853181]
[33]
Lei T, Wang J, Liu Y, et al. Calreticulin as a special marker to distinguish dental pulp stem cells from gingival mesenchymal stem cells. Int J Biol Macromol 2021; 178: 229-39.
[http://dx.doi.org/10.1016/j.ijbiomac.2021.02.126] [PMID: 33647340]
[34]
Briscoe J, Thérond PP. The mechanisms of Hedgehog signalling and its roles in development and disease. Nat Rev Mol Cell Biol 2013; 14(7): 416-29.
[http://dx.doi.org/10.1038/nrm3598] [PMID: 23719536]
[35]
Nüsslein-Volhard C, Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature 1980; 287(5785): 795-801.
[http://dx.doi.org/10.1038/287795a0] [PMID: 6776413]
[36]
Kinzler KW, Bigner SH, Bigner DD, et al. Identification of an amplified, highly expressed gene in a human glioma. Science 1987; 236(4797): 70-3.
[http://dx.doi.org/10.1126/science.3563490] [PMID: 3563490]
[37]
McMahon AP, Ingham PW, Tabin CJ. Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol 2003; 53: 1-114.
[http://dx.doi.org/10.1016/S0070-2153(03)53002-2] [PMID: 12509125]
[38]
Hojo H, Ohba S, Yano F, et al. Gli1 protein participates in Hedgehog-mediated specification of osteoblast lineage during endochondral ossification. J Biol Chem 2012; 287(21): 17860-9.
[http://dx.doi.org/10.1074/jbc.M112.347716] [PMID: 22493482]
[39]
Zhao H, Feng J, Ho TV, Grimes W, Urata M, Chai Y. The suture provides a niche for mesenchymal stem cells of craniofacial bones. Nat Cell Biol 2015; 17(4): 386-96.
[http://dx.doi.org/10.1038/ncb3139] [PMID: 25799059]
[40]
Men Y, Wang Y, Yi Y, et al. Gli1+ periodontium stem cells are regulated by osteocytes and occlusal force. Dev Cell 2020; 54(5): 639-654.e6.
[http://dx.doi.org/10.1016/j.devcel.2020.06.006] [PMID: 32652075]
[41]
Shi Y, He G, Lee WC, McKenzie JA, Silva MJ, Long F. Gli1 identifies osteogenic progenitors for bone formation and fracture repair. Nat Commun 2017; 8(1): 2043.
[http://dx.doi.org/10.1038/s41467-017-02171-2] [PMID: 29230039]
[42]
Xia C, Ge Q, Fang L, et al. TGF-β/Smad2 signalling regulates enchondral bone formation of Gli1+ periosteal cells during fracture healing. Cell Prolif 2020; 53(11): e12904.
[http://dx.doi.org/10.1111/cpr.12904] [PMID: 32997394]
[43]
Yang M, Zhang H, Gangolli R. Advances of mesenchymal stem cells derived from bone marrow and dental tissue in craniofacial tissue engineering. Curr Stem Cell Res Ther 2014; 9(3): 150-61.
[http://dx.doi.org/10.2174/1574888X09666140213142258] [PMID: 24524798]
[44]
Chai Y, Maxson RE Jr. Recent advances in craniofacial morphogenesis. Dev Dyn 2006; 235(9): 2353-75.
[http://dx.doi.org/10.1002/dvdy.20833] [PMID: 16680722]
[45]
Di Pietro L, Barba M, Prampolini C, et al. GLI1 and AXIN2 are distinctive markers of human calvarial mesenchymal stromal cells in nonsyndromic craniosynostosis. Int J Mol Sci 2020; 21(12): E4356.
[http://dx.doi.org/10.3390/ijms21124356] [PMID: 32575385]
[46]
Seidel K, Ahn CP, Lyons D, et al. Hedgehog signaling regulates the generation of ameloblast progenitors in the continuously growing mouse incisor. Development 2010; 137(22): 3753-61.
[http://dx.doi.org/10.1242/dev.056358] [PMID: 20978073]
[47]
Zhao H, Feng J, Seidel K, et al. Secretion of shh by a neurovascular bundle niche supports mesenchymal stem cell homeostasis in the adult mouse incisor. Cell Stem Cell 2014; 14(2): 160-73.
[http://dx.doi.org/10.1016/j.stem.2013.12.013] [PMID: 24506883]
[48]
Chen S, Jing J, Yuan Y, et al. Runx2+ niche cells maintain incisor mesenchymal tissue homeostasis through IGF signaling. Cell Rep 2020; 32(6): 108007.
[http://dx.doi.org/10.1016/j.celrep.2020.108007] [PMID: 32783935]
[49]
Xie X, Xu C, Zhao H, Wang J, Feng JQ. A biphasic feature of Gli1+-mesenchymal progenitors during cementogenesis that is positively controlled by Wnt/β-Catenin Signaling. J Dent Res 2021; 100(11): 1289-98.
[http://dx.doi.org/10.1177/00220345211007429] [PMID: 33853427]
[50]
Horwitz EM, Le Blanc K, Dominici M, et al. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 2005; 7(5): 393-5.
[http://dx.doi.org/10.1080/14653240500319234] [PMID: 16236628]
[51]
Lv FJ, Tuan RS, Cheung KM, Leung VY. Concise review: the surface markers and identity of human mesenchymal stem cells. Stem Cells 2014; 32(6): 1408-19.
[http://dx.doi.org/10.1002/stem.1681] [PMID: 24578244]
[52]
Mabuchi Y, Morikawa S, Harada S, et al. LNGFR(+)THY-1(+)VCAM-1(hi+) cells reveal functionally distinct subpopulations in mesenchymal stem cells. Stem Cell Reports 2013; 1(2): 152-65.
[http://dx.doi.org/10.1016/j.stemcr.2013.06.001] [PMID: 24052950]
[53]
Tormin A, Li O, Brune JC, et al. CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood 2011; 117(19): 5067-77.
[http://dx.doi.org/10.1182/blood-2010-08-304287] [PMID: 21415267]
[54]
Boxall SA, Jones E. Markers for characterization of bone marrow multipotential stromal cells. Stem Cells Int 2012; 2012: 975871.
[http://dx.doi.org/10.1155/2012/975871] [PMID: 22666272]
[55]
Yi Y, Stenberg W, Luo W, Feng JQ, Zhao H. Alveolar bone marrow Gli1+ stem cells support implant osseointegration. J Dent Res 2021; 220345211013722.
[http://dx.doi.org/10.1177/00220345211013722] [PMID: 34009063]
[56]
Howard TD, Paznekas WA, Green ED, et al. Mutations in TWIST, a basic helix-loop-helix transcription factor, in Saethre- Chotzen syndrome. Nat Genet 1997; 15(1): 36-41.
[http://dx.doi.org/10.1038/ng0197-36] [PMID: 8988166]
[57]
Behr B, Longaker MT, Quarto N. Craniosynostosis of coronal suture in twist1 mice occurs through endochondral ossification recapitulating the physiological closure of posterior frontal suture. Front Physiol 2011; 2: 37.
[http://dx.doi.org/10.3389/fphys.2011.00037] [PMID: 21811467]
[58]
Jezela-Stanek A, Krajewska-Walasek M. Genetic causes of syndromic craniosynostoses. Eur J Paediatr Neurol 2013; 17(3): 221-4.
[http://dx.doi.org/10.1016/j.ejpn.2012.09.009] [PMID: 23062756]
[59]
Luo W, Yi Y, Jing D, et al. Investigation of postnatal craniofacial bone development with tissue clearing-based three-dimensional imaging. Stem Cells Dev 2019; 28(19): 1310-21.
[http://dx.doi.org/10.1089/scd.2019.0104] [PMID: 31392933]
[60]
Kusumbe AP, Ramasamy SK, Adams RH. Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature 2014; 507(7492): 323-8.
[http://dx.doi.org/10.1038/nature13145] [PMID: 24646994]
[61]
Chen J, Li M, Liu AQ, et al. Gli1+ cells couple with type H vessels and are required for type H vessel formation. Stem Cell Reports 2020; 15(1): 110-24.
[http://dx.doi.org/10.1016/j.stemcr.2020.06.007] [PMID: 32668219]
[62]
Nakamura T, Naruse M, Chiba Y, et al. Novel hedgehog agonists promote osteoblast differentiation in mesenchymal stem cells. J Cell Physiol 2015; 230(4): 922-9.
[http://dx.doi.org/10.1002/jcp.24823] [PMID: 25215620]
[63]
Liu AQ, Zhang LS, Chen J, et al. Mechanosensing by Gli1+ cells contributes to the orthodontic force-induced bone remodelling. Cell Prolif 2020; 53(5): e12810.
[http://dx.doi.org/10.1111/cpr.12810] [PMID: 32472648]
[64]
Kitaura Y, Hojo H, Komiyama Y, Takato T, Chung UI, Ohba S. Gli1 haploinsufficiency leads to decreased bone mass with an uncoupling of bone metabolism in adult mice. PLoS One 2014; 9(10): e109597.
[http://dx.doi.org/10.1371/journal.pone.0109597] [PMID: 25313900]
[65]
Plikus MV, Zeichner-David M, Mayer JA, et al. Morphoregulation of teeth: modulating the number, size, shape and differentiation by tuning Bmp activity. Evol Dev 2005; 7(5): 440-57.
[http://dx.doi.org/10.1111/j.1525-142X.2005.05048.x] [PMID: 16174037]
[66]
Shi C, Yuan Y, Guo Y, et al. BMP signaling in regulating mesenchymal stem cells in incisor homeostasis. J Dent Res 2019; 98(8): 904-11.
[http://dx.doi.org/10.1177/0022034519850812] [PMID: 31136721]
[67]
Feng J, Jing J, Li J, et al. BMP signaling orchestrates a transcriptional network to control the fate of mesenchymal stem cells in mice. Development 2017; 144(14): 2560-9.
[http://dx.doi.org/10.1242/dev.150136] [PMID: 28576771]
[68]
Guo Y, Yuan Y, Wu L, et al. BMP-IHH-mediated interplay between mesenchymal stem cells and osteoclasts supports calvarial bone homeostasis and repair. Bone Res 2018; 6: 30.
[http://dx.doi.org/10.1038/s41413-018-0031-x] [PMID: 30345151]
[69]
Clevers H, Loh KM, Nusse R. Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 2014; 346(6205): 1248012.
[http://dx.doi.org/10.1126/science.1248012] [PMID: 25278615]
[70]
Degirmenci B, Valenta T, Dimitrieva S, Hausmann G, Basler K. GLI1-expressing mesenchymal cells form the essential Wnt-secreting niche for colon stem cells. Nature 2018; 558(7710): 449-53.
[http://dx.doi.org/10.1038/s41586-018-0190-3] [PMID: 29875413]
[71]
Keating A. Mesenchymal stromal cells: new directions. Cell Stem Cell 2012; 10(6): 709-16.
[http://dx.doi.org/10.1016/j.stem.2012.05.015] [PMID: 22704511]
[72]
Yu M, Ma L, Yuan Y, et al. Cranial suture regeneration mitigates skull and neurocognitive defects in craniosynostosis. Cell 2021; 184(1): 243-256.e18.
[http://dx.doi.org/10.1016/j.cell.2020.11.037] [PMID: 33417861]

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