Insights into skeletal stem cells

Qiwen Li , Ruoshi Xu , Kexin Lei , Quan Yuan

Bone Research ›› 2022, Vol. 10 ›› Issue (1) : 61

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Bone Research ›› 2022, Vol. 10 ›› Issue (1) : 61 DOI: 10.1038/s41413-022-00235-8
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Insights into skeletal stem cells

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Abstract

The tissue-resident skeletal stem cells (SSCs), which are self-renewal and multipotent, continuously provide cells (including chondrocytes, bone cells, marrow adipocytes, and stromal cells) for the development and homeostasis of the skeletal system. In recent decade, utilizing fluorescence-activated cell sorting, lineage tracing, and single-cell sequencing, studies have identified various types of SSCs, plotted the lineage commitment trajectory, and partially revealed their properties under physiological and pathological conditions. In this review, we retrospect to SSCs identification and functional studies. We discuss the principles and approaches to identify bona fide SSCs, highlighting pioneering findings that plot the lineage atlas of SSCs. The roles of SSCs and progenitors in long bone, craniofacial tissues, and periosteum are systematically discussed. We further focus on disputes and challenges in SSC research.

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Qiwen Li, Ruoshi Xu, Kexin Lei, Quan Yuan. Insights into skeletal stem cells. Bone Research, 2022, 10(1): 61 DOI:10.1038/s41413-022-00235-8

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References

[1]

Chande S, Bergwitz C. Role of phosphate sensing in bone and mineral metabolism. Nat. Rev. Endocrinol., 2018, 14: 637-655

[2]

Farr JN, Khosla S. Skeletal changes through the lifespan—from growth to senescence. Nat. Rev. Endocrinol., 2015, 11: 513-521

[3]

Morrison SJ, Scadden DT. The bone marrow niche for haematopoietic stem cells. Nature, 2014, 505: 327-334

[4]

van Gastel N, Carmeliet G. Metabolic regulation of skeletal cell fate and function in physiology and disease. Nat. Metab., 2021, 3: 11-20

[5]

Karsenty G, Khosla S. The crosstalk between bone remodeling and energy metabolism: a translational perspective. Cell Metab., 2022, 34: 805-817

[6]

Lu K et al. Defects in a liver-bone axis contribute to hepatic osteodystrophy disease progression. Cell Metab., 2022, 34: 441-457.e7

[7]

Berger JM et al. Mediation of the acute stress response by the skeleton. Cell Metab., 2019, 30: 890-902.e8

[8]

Whyte MP. Hypophosphatasia — aetiology, nosology, pathogenesis, diagnosis and treatment. Nat. Rev. Endocrinol., 2016, 12: 233-246

[9]

Sugisawa E et al. RNA sensing by gut Piezo1 is essential for systemic serotonin synthesis. Cell, 2020, 182: 609-624.e21

[10]

Han Y, You X, Xing W, Zhang Z, Zou W. Paracrine and endocrine actions of bone—the functions of secretory proteins from osteoblasts, osteocytes, and osteoclasts. Bone Res., 2018, 6: 16

[11]

Bianco P et al. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat. Med., 2013, 19: 35-42

[12]

Bianco P, Robey PG. Skeletal stem cells. Development, 2015, 142: 1023-1027

[13]

Marecic O et al. Identification and characterization of an injury-induced skeletal progenitor. Proc. Natl. Acad. Sci. USA, 2015, 112: 9920-9925

[14]

Ono N, Kronenberg HM. Bone repair and stem cells. Curr. Opin. Genet. Dev., 2016, 40: 103-107

[15]

Klingseisen A, Jackson AP. Mechanisms and pathways of growth failure in primordial dwarfism. Genes Dev., 2011, 25: 2011-2024

[16]

Shiang R et al. Mutations in the transmembrane domain of FGFR3 cause the most common genetic form of dwarfism, achondroplasia. Cell, 1994, 78: 335-342

[17]

Singer FR. Paget’s disease of bone—genetic and environmental factors. Nat. Rev. Endocrinol., 2015, 11: 662-671

[18]

Hendrickx G, Boudin E, Van Hul W. A look behind the scenes: the risk and pathogenesis of primary osteoporosis. Nat. Rev. Rheumatol., 2015, 11: 462-474

[19]

Bovée JVMG, Hogendoorn PCW, Wunder JS, Alman BA. Cartilage tumours and bone development: molecular pathology and possible therapeutic targets. Nat. Rev. Cancer, 2010, 10: 481-488

[20]

Pignolo RJ, Ramaswamy G, Fong JT, Shore EM, Kaplan FS. Progressive osseous heteroplasia: diagnosis, treatment, and prognosis. Appl. Clin. Genet., 2015, 8: 37-48

[21]

Farrow E, Nicot R, Wiss A, Laborde A, Ferri J. Cleidocranial dysplasia: a review of clinical, radiological, genetic implications and a guidelines proposal. J. Craniofac. Surg., 2018, 29: 382-389

[22]

Deng P et al. Loss of KDM4B exacerbates bone-fat imbalance and mesenchymal stromal cell exhaustion in skeletal aging. Cell Stem Cell, 2021, 28: 1057-1073.e7

[23]

Wang Y et al. Alpha-ketoglutarate ameliorates age-related osteoporosis via regulating histone methylations. Nat. Commun., 2020, 11

[24]

Chai Y, Maxson RE. Recent advances in craniofacial morphogenesis. Dev. Dyn., 2006, 235: 2353-2375

[25]

Zeller R, López-Ríos J, Zuniga A. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat. Rev. Genet., 2009, 10: 845-858

[26]

Friedenstein AJ, Piatetzky-Shapiro II, Petrakova KV. Osteogenesis in transplants of bone marrow cells. J. Embryol. Exp. Morphol., 1966, 16: 381-390

[27]

Tavassoli M, Crosby WH. Transplantation of marrow to extramedullary sites. Science, 1968, 161: 54-56

[28]

Castro-Malaspina H et al. Characterization of human bone marrow fibroblast colony-forming cells (CFU-F) and their progeny. Blood, 1980, 56: 289-301

[29]

Owen M, Friedenstein AJ. Stromal stem cells: marrow-derived osteogenic precursors. Ciba Found. Symp., 1988, 136: 42-60

[30]

Caplan AI. Mesenchymal stem cells. J. Orthop. Res., 1991, 9: 641-650

[31]

Dominici M et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 2006, 8: 315-317

[32]

Prieto González EA. Heterogeneity in adipose stem cells. Adv. Exp. Med. Biol., 2019, 1123: 119-150

[33]

De Micheli AJ et al. Single-cell analysis of the muscle stem cell hierarchy identifies heterotypic communication signals involved in skeletal muscle regeneration. Cell Rep., 2020, 30: 3583-3595.e5

[34]

Campanella V. Dental stem cells: current research and future applications. Eur. J. Paediatr. Dent., 2018, 19: 257

[35]

Sacchetti B et al. No Identical ‘mesenchymal stem cells’ at different times and sites: human committed progenitors of distinct origin and differentiation potential are incorporated as adventitial cells in microvessels. Stem Cell Rep., 2016, 6: 897-913

[36]

Galipeau J, Sensébé L. Mesenchymal stromal cells: clinical challenges and therapeutic opportunities. Cell Stem Cell, 2018, 22: 824-833

[37]

Bianco P, Robey PG, Simmons PJ. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell, 2008, 2: 313-319

[38]

Chan CKF et al. Identification and specification of the mouse skeletal stem cell. Cell, 2015, 160: 285-298

[39]

Sacchetti B et al. Self-Renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell, 2007, 131: 324-336

[40]

Ambrosi TH, Longaker MT, Chan CKF. A revised perspective of skeletal stem cell biology. Front. Cell Dev. Biol., 2019, 7: 189

[41]

Mizuhashi K et al. Resting zone of the growth plate houses a unique class of skeletal stem cells. Nature, 2018, 563: 254-258

[42]

Newton PT et al. A radical switch in clonality reveals a stem cell niche in the epiphyseal growth plate. Nature, 2019, 567: 234-238

[43]

Kretzschmar K, Watt FM. Lineage tracing. Cell, 2012, 148: 33-45

[44]

Gulati GS et al. Isolation and functional assessment of mouse skeletal stem cell lineage. Nat. Protoc., 2018, 13: 1294-1309

[45]

Frisch BJ. Hematopoietic stem cell cultures and assays. Methods Mol. Biol., 2021, 2230: 467-477

[46]

Sun J et al. Clonal dynamics of native haematopoiesis. Nature, 2014, 514: 322-327

[47]

Han X et al. A suite of new Dre recombinase drivers markedly expands the ability to perform intersectional genetic targeting. Cell Stem Cell, 2021, 28: 1160-1176.e7

[48]

He L et al. Enhancing the precision of genetic lineage tracing using dual recombinases. Nat. Med., 2017, 23: 1488-1498

[49]

Theodosiou NA, Xu T. Use of FLP/FRT system to study Drosophila development. Methods, 1998, 14: 355-365

[50]

McLellan MA, Rosenthal NA, Pinto AR. Cre-loxP-mediated recombination: general principles and experimental considerations. Curr. Protoc. Mouse Biol., 2017, 7: 1-12

[51]

Feil S, Valtcheva N, Feil R. Inducible Cre mice. Methods Mol. Biol., 2009, 530: 343-363

[52]

Kalajzic Z et al. Directing the expression of a green fluorescent protein transgene in differentiated osteoblasts: comparison between rat type I collagen and rat osteocalcin promoters. Bone, 2002, 31: 654-660

[53]

Zhao H, Zhou B. Dual genetic approaches for deciphering cell fate plasticity in vivo: more than double. Curr. Opin. Cell Biol., 2019, 61: 101-109

[54]

He L et al. Genetic lineage tracing of resident stem cells by DeaLT. Nat. Protoc., 2018, 13: 2217-2246

[55]

Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet., 1999, 21: 70-71

[56]

Srinivas S et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol., 2001, 1: 4

[57]

Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis, 2007, 45: 593-605

[58]

Madisen L et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci., 2010, 13: 133-140

[59]

Abe T, Fujimori T. Reporter mouse lines for fluorescence imaging. Dev. Growth Differ., 2013, 55: 390-405

[60]

Ding L, Saunders TL, Enikolopov G, Morrison SJ. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature, 2012, 481: 457-462

[61]

Rivers LE et al. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat. Neurosci., 2008, 11: 1392-1401

[62]

Huang W, Olsen BR. Skeletal defects in Osterix-Cre transgenic mice. Transgenic Res., 2015, 24: 167-172

[63]

Livet J et al. Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature, 2007, 450: 56-62

[64]

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: 154-168

[65]

Morikawa S et al. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J. Exp. Med., 2009, 206: 2483-2496

[66]

Chan CKF et al. Identification of the human skeletal stem cell. Cell, 2018, 175: 43-56.e21

[67]

Ono N, Ono W, Nagasawa T, Kronenberg HM. A subset of chondrogenic cells provides early mesenchymal progenitors in growing bones. Nat. Cell Biol., 2014, 16: 1157-1167

[68]

Ono N et al. Vasculature-associated cells expressing nestin in developing bones encompass early cells in the osteoblast and endothelial lineage. Dev. Cell, 2014, 29: 330-339

[69]

Mizoguchi T et al. Osterix marks distinct waves of primitive and definitive stromal progenitors during bone marrow development. Dev. Cell, 2014, 29: 340-349

[70]

Nusspaumer G et al. Ontogenic identification and analysis of mesenchymal stromal cell populations during mouse limb and long bone development. Stem Cell Rep., 2017, 9: 1124-1138

[71]

Debnath S et al. Discovery of a periosteal stem cell mediating intramembranous bone formation. Nature, 2018, 562: 133-139

[72]

Ambrosi TH et al. Adipocyte accumulation in the bone marrow during obesity and aging impairs stem cell-based hematopoietic and bone regeneration. Cell Stem Cell, 2017, 20: 771-784.e6

[73]

Ambrosi TH et al. Distinct skeletal stem cell types orchestrate long bone skeletogenesis. eLife, 2021, 10: e66063

[74]

Hu X et al. Identification of a common mesenchymal stromal progenitor for the adult haematopoietic niche. Nat. Commun., 2016, 7

[75]

Nakashima K et al. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell, 2002, 108: 17-29

[76]

Liu Y et al. Osterix-cre labeled progenitor cells contribute to the formation and maintenance of the bone marrow stroma. PLoS One, 2013, 8: e71318

[77]

Shu HS et al. Tracing the skeletal progenitor transition during postnatal bone formation. Cell Stem Cell, 2021, 28: 2122-2136.e3

[78]

Méndez-Ferrer S et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature, 2010, 466: 829-834

[79]

Rauch A et al. Osteogenesis depends on commissioning of a network of stem cell transcription factors that act as repressors of adipogenesis. Nat. Genet., 2019, 51: 716-727

[80]

Baccin C et al. Combined single-cell and spatial transcriptomics reveal the molecular, cellular and spatial bone marrow niche organization. Nat. Cell Biol., 2020, 22: 38-48

[81]

Lanske B et al. PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science, 1996, 273: 663-666

[82]

Hallett SA et al. Chondrocytes in the resting zone of the growth plate are maintained in a Wnt-inhibitory environment. eLife, 2021, 10: e64513

[83]

Vortkamp A et al. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science, 1996, 273: 613-622

[84]

Ornitz DM, Marie PJ. Fibroblast growth factor signaling in skeletal development and disease. Genes Dev., 2015, 29: 1463-1486

[85]

Salazar VS, Gamer LW, Rosen V. BMP signalling in skeletal development, disease and repair. Nat. Rev. Endocrinol., 2016, 12: 203-221

[86]

Song L et al. Loss of wnt/β-catenin signaling causes cell fate shift of preosteoblasts from osteoblasts to adipocytes. J. Bone Miner. Res., 2012, 27: 2344-2358

[87]

Shi S, Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J. Bone Miner. Res., 2003, 18: 696-704

[88]

Pinho S et al. PDGFRα and CD51 mark human nestin+ sphere-forming mesenchymal stem cells capable of hematopoietic progenitor cell expansion. J. Exp. Med., 2013, 210: 1351-1367

[89]

Tormin A et al. CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood, 2011, 117: 5067-5077

[90]

He J et al. Dissecting human embryonic skeletal stem cell ontogeny by single-cell transcriptomic and functional analyses. Cell Res., 2021, 31: 742-757

[91]

Chan CKF et al. Clonal precursor of bone, cartilage, and hematopoietic niche stromal cells. Proc. Natl. Acad. Sci. USA, 2013, 110: 12643-12648

[92]

Crisan M et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell, 2008, 3: 301-313

[93]

Seike M, Omatsu Y, Watanabe H, Kondoh G, Nagasawa T. Stem cell niche-specific Ebf3 maintains the bone marrow cavity. Genes Dev., 2018, 32: 359-372

[94]

Greenbaum A et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature, 2013, 495: 227-230

[95]

Matthews BG et al. Analysis of αSMA-labeled progenitor cell commitment identifies notch signaling as an important pathway in fracture healing. J. Bone Miner. Res., 2014, 29: 1283-1294

[96]

Isern J et al. Self-renewing human bone marrow mesenspheres promote hematopoietic stem cell expansion. Cell Rep., 2013, 3: 1714-1724

[97]

Worthley DL et al. Gremlin 1 identifies a skeletal stem cell with bone, cartilage, and reticular stromal potential. Cell, 2015, 160: 269-284

[98]

Shi Y et al. Gli1 identifies osteogenic progenitors for bone formation and fracture repair. Nat. Commun., 2017, 8

[99]

Ortinau LC et al. Identification of functionally distinct Mx1+αSMA+ periosteal skeletal stem cells. Cell Stem Cell, 2019, 25: 784-796.e5

[100]

Petit F, Sears KE, Ahituv N. Limb development: a paradigm of gene regulation. Nat. Rev. Genet., 2017, 18: 245-258

[101]

Zhulyn O et al. A switch from low to high Shh activity regulates establishment of limb progenitors and signaling centers. Dev. Cell, 2014, 29: 241-249

[102]

Cooper KL et al. Initiation of proximal-distal patterning in the vertebrate limb by signals and growth. Science, 2011, 332: 1083-1086

[103]

Roselló-Díez A, Ros MA, Torres M. Diffusible signals, not autonomous mechanisms, determine the main proximodistal limb subdivision. Science, 2011, 332: 1086-1088

[104]

Kronenberg HM. Developmental regulation of the growth plate. Nature, 2003, 423: 332-336

[105]

Li Y et al. Dynamic imaging of the growth plate cartilage reveals multiple contributors to skeletal morphogenesis. Nat. Commun., 2015, 6

[106]

Cooper KL et al. Multiple phases of chondrocyte enlargement underlie differences in skeletal proportions. Nature, 2013, 495: 375-378

[107]

Logan M et al. Expression of Cre Recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis, 2002, 33: 77-80

[108]

Akiyama‡ H et al. Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc. Natl. Acad. Sci. USA, 2005, 102: 14665-14670

[109]

Kronenberg HM. The role of the perichondrium in fetal bone development. Ann. N. Y. Acad. Sci., 2007, 1116: 59-64

[110]

Gerber HP et al. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat. Med., 1999, 5: 623-628

[111]

Maes C et al. Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev. Cell, 2010, 19: 329-344

[112]

Zhou X et al. Chondrocytes transdifferentiate into osteoblasts in endochondral bone during development, postnatal growth and fracture healing in mice. PLoS Genet., 2014, 10: e1004820

[113]

Yang L, Tsang KY, Tang HC, Chan D, Cheah KSE. Hypertrophic chondrocytes can become osteoblasts and osteocytes in endochondral bone formation. Proc. Natl. Acad. Sci. USA, 2014, 111: 12097-12102

[114]

Yang G et al. Osteogenic fate of hypertrophic chondrocytes. Cell Res., 2014, 24: 1266-1269

[115]

Ding L, Morrison SJ. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature, 2013, 495: 231-235

[116]

Zhang D et al. LepR-expressing stem cells are essential for alveolar bone regeneration. J. Dent. Res., 2020, 99: 1279-1286

[117]

Dzierzak E, Speck NA. Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat. Immunol., 2008, 9: 129-136

[118]

He DD et al. C-KIT expression distinguishes fetal from postnatal skeletal progenitors. Stem Cell Rep., 2020, 14: 614-630

[119]

Muruganandan S et al. A FoxA2+ long-term stem cell population is necessary for growth plate cartilage regeneration after injury. Nat. Commun., 2022, 13

[120]

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

[121]

Rux DR et al. Regionally restricted hox function in adult bone marrow multipotent mesenchymal stem/stromal cells. Dev. Cell, 2016, 39: 653-666

[122]

Long JT et al. Hypertrophic chondrocytes serve as a reservoir for marrow-associated skeletal stem and progenitor cells, osteoblasts, and adipocytes during skeletal development. eLife, 2022, 11: e76932

[123]

Matsushita Y et al. A Wnt-mediated transformation of the bone marrow stromal cell identity orchestrates skeletal regeneration. Nat. Commun., 2020, 11

[124]

Kunisaki Y et al. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature, 2013, 502: 637-643

[125]

Omatsu Y et al. The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity, 2010, 33: 387-399

[126]

Comazzetto S et al. Restricted hematopoietic progenitors and erythropoiesis require SCF from leptin receptor+ niche cells in the bone marrow. Cell Stem Cell, 2019, 24: 477-486.e6

[127]

Park D et al. Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell, 2012, 10: 259-272

[128]

Shen B et al. A mechanosensitive peri-arteriolar niche for osteogenesis and lymphopoiesis. Nature, 2021, 591: 438-444

[129]

Li Q, Wu Y, Kang N. Marrow adipose tissue: its origin, function, and regulation in bone remodeling and regeneration. Stem Cells Int., 2018, 2018: 1-11

[130]

Wu Y et al. Mettl3-mediated m6A RNA methylation regulates the fate of bone marrow mesenchymal stem cells and osteoporosis. Nat. Commun., 2018, 9

[131]

Fan Y et al. Parathyroid hormone directs bone marrow mesenchymal cell fate. Cell Metab., 2017, 25: 661-672

[132]

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: 782-796

[133]

Zhou BO et al. Bone marrow adipocytes promote the regeneration of stem cells and haematopoiesis by secreting SCF. Nat. Cell Biol., 2017, 19: 891-903

[134]

Zhong L et al. Single cell transcriptomics identifies a unique adipose lineage cell population that regulates bone marrow environment. eLife, 2020, 9: e54695

[135]

Yu W et al. Bone marrow adipogenic lineage precursors promote osteoclastogenesis in bone remodeling and pathologic bone loss. J. Clin. Investig, 2021, 131: 140214

[136]

Palmisano B et al. GsαR201C and estrogen reveal different subsets of bone marrow adiponectin expressing osteogenic cells. Bone Res., 2022, 10: 50

[137]

Sivaraj KK et al. Regional specialization and fate specification of bone stromal cells in skeletal development. Cell Rep., 2021, 36: 109352

[138]

Ferguson JW, Atit RP. A tale of two cities: the genetic mechanisms governing calvarial bone development. Genesis, 2019, 57: e23248

[139]

Shah HN et al. Craniofacial and long bone development in the context of distraction osteogenesis. Plast. Reconstr. Surg., 2021, 147: 54e-65e

[140]

Soldatov R et al. Spatiotemporal structure of cell fate decisions in murine neural crest. Science, 2019, 364: eaas9536

[141]

Xie M et al. Schwann cell precursors contribute to skeletal formation during embryonic development in mice and zebrafish. Proc. Natl. Acad. Sci. USA, 2019, 116: 15068-15073

[142]

Kaucka M et al. Analysis of neural crest-derived clones reveals novel aspects of facial development. Sci. Adv., 2016, 2: e1600060

[143]

Lin W et al. Mapping the immune microenvironment for mandibular alveolar bone homeostasis at single-cell resolution. Bone Res., 2021, 9: 17

[144]

Zhou X et al. SM22alpha-lineage niche cells regulate intramembranous bone regeneration via PDGFRbeta-triggered hydrogen sulfide production. Cell Rep., 2022, 39: 110750

[145]

Zhao H et al. The suture provides a niche for mesenchymal stem cells of craniofacial bones. Nat. Cell Biol., 2015, 17: 386-396

[146]

Park S, Zhao H, Urata M, Chai Y. Sutures possess strong regenerative capacity for calvarial bone injury. Stem Cells Dev., 2016, 25: 1801-1807

[147]

Yu M et al. Cranial suture regeneration mitigates skull and neurocognitive defects in craniosynostosis. Cell, 2021, 184: 243-256.e18

[148]

Jing D et al. Response of Gli1+ suture stem cells to mechanical force upon suture expansion. J. Bone Miner. Res., 2022, 37: 1307-1320

[149]

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

[150]

Menon S et al. Skeletal stem and progenitor cells maintain cranial suture patency and prevent craniosynostosis. Nat. Commun., 2021, 12

[151]

Ouyang Z et al. Prx1 and 3.2kb Col1a1 promoters target distinct bone cell populations in transgenic mice. Bone, 2014, 58: 136-145

[152]

Wilk K et al. Postnatal calvarial skeletal stem cells expressing PRX1 reside exclusively in the calvarial sutures and are required for bone regeneration. Stem Cell Rep., 2017, 8: 933-946

[153]

Seo B-M et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet, 2004, 364: 149-155

[154]

Liang JF et al. Identification of dental stem cells similar to skeletal stem cells. J. Dent. Res., 2022, 101: 1092-1100

[155]

Men Y et al. Gli1+ periodontium stem cells are regulated by osteocytes and occlusal force. Dev. Cell, 2020, 54: 639-654

[156]

Liu AQ et al. Mechanosensing by Gli1(+) cells contributes to the orthodontic force-induced bone remodelling. Cell Prolif., 2020, 53: e12810

[157]

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: 1289-1298

[158]

Lim WH et al. Wnt signaling regulates homeostasis of the periodontal ligament. J. Periodontal Res, 2014, 49: 751-759

[159]

Wang K et al. Axin2+ PDL cells directly contribute to new alveolar bone formation in response to orthodontic tension force. J. Dent. Res., 2022, 101: 695-703

[160]

Yuan X et al. A Wnt-responsive PDL population effectuates extraction socket healing. J. Dent. Res., 2018, 97: 803-809

[161]

Xie X et al. Axin2(+)-mesenchymal PDL cells, instead of K14(+) epithelial cells, play a key role in rapid cementum growth. J. Dent. Res., 2019, 98: 1262-1270

[162]

Zhao J, Faure L, Adameyko I, Sharpe PT. Stem cell contributions to cementoblast differentiation in healthy periodontal ligament and periodontitis. Stem Cells, 2021, 39: 92-102

[163]

Bassir SH et al. Prx1 expressing cells are required for periodontal regeneration of the mouse incisor. Front. Physiol., 2019, 10: 591

[164]

Cui C et al. Role of PTH1R signaling in Prx1+ mesenchymal progenitors during eruption. J. Dent. Res., 2020, 99: 1296-1305

[165]

Gong X et al. Tracing PRX1(+) cells during molar formation and periodontal ligament reconstruction. Int J. Oral. Sci., 2022, 14: 5

[166]

Dragonas P, Katsaros T, Schiavo J, Galindo-Moreno P, Avila-Ortiz G. Osteogenic capacity of the sinus membrane following maxillary sinus augmentation procedures: a systematic review. Int. J. Oral. Implantol. Berl. Ger., 2020, 13: 213-232

[167]

Coyac BR, Wu M, Bahat DJ, Wolf BJ, Helms JA. Biology of sinus floor augmentation with an autograft versus a bone graft substitute in a preclinical in vivo experimental model. Clin. Oral. Implants Res., 2021, 32: 916-927

[168]

Weng Y et al. A novel lineage of osteoprogenitor cells with dual epithelial and mesenchymal properties govern maxillofacial bone homeostasis and regeneration after MSFL. Cell Res., 2022, 32: 814-830

[169]

Sharpe PT. Dental mesenchymal stem cells. Development, 2016, 143: 2273-2280

[170]

Miura M et al. SHED: stem cells from human exfoliated deciduous teeth. Proc. Natl. Acad. Sci. USA, 2003, 100: 5807-5812

[171]

Sloan AJ, Smith AJ. Stem cells and the dental pulp: potential roles in dentine regeneration and repair. Oral. Dis., 2007, 13: 151-157

[172]

Zhang QZ, Nguyen AL, Yu WH, Le AD. Human oral mucosa and gingiva: a unique reservoir for mesenchymal stem cells. J. Dent. Res., 2012, 91: 1011-1018

[173]

Feng J, Mantesso A, De Bari C, Nishiyama A, Sharpe PT. Dual origin of mesenchymal stem cells contributing to organ growth and repair. Proc. Natl. Acad. Sci. USA, 2011, 108: 6503-6508

[174]

Zhao H et al. Secretion of Shh by a neurovascular bundle niche supports mesenchymal stem cell homeostasis in the adult mouse incisor. Cell Stem Cell, 2018, 23: 147

[175]

Kaukua N et al. Glial origin of mesenchymal stem cells in a tooth model system. Nature, 2014, 513: 551-554

[176]

Gong S, Emperumal CP, Al-Eryani K, Enciso R. Regeneration of temporomandibular joint using in vitro human stem cells: a review. J. Tissue Eng. Regen. Med., 2022, 16: 591-604

[177]

Matheus HR, Özdemir ŞD, Guastaldi FPS. Stem cell-based therapies for temporomandibular joint osteoarthritis and regeneration of cartilage/osteochondral defects: a systematic review of preclinical experiments. Osteoarthr. Cartil., 2022, 30: 1174-1185

[178]

Van Bellinghen X et al. Temporomandibular joint regenerative medicine. Int. J. Mol. Sci., 2018, 19 2 446

[179]

Embree MC et al. Exploiting endogenous fibrocartilage stem cells to regenerate cartilage and repair joint injury. Nat. Commun., 2016, 7

[180]

Bi R et al. Identification of human temporomandibular joint fibrocartilage stem cells with distinct chondrogenic capacity. Osteoarthr. Cartil., 2020, 28: 842-852

[181]

Fan Y et al. Fibrocartilage stem cells in the temporomandibular joint: insights from animal and human studies. Front. Cell Dev. Biol., 2021, 9: 665995

[182]

Colnot C. Skeletal cell fate decisions within periosteum and bone marrow during bone regeneration. J. Bone Miner. Res., 2009, 24: 274-282

[183]

Colnot C, Zhang X, Knothe Tate ML. Current insights on the regenerative potential of the periosteum: molecular, cellular, and endogenous engineering approaches. J. Orthop. Res., 2012, 30: 1869-1878

[184]

Xu J et al. PDGFRα reporter activity identifies periosteal progenitor cells critical for bone formation and fracture repair. Bone Res., 2022, 10: 7

[185]

He X et al. Sox9 positive periosteal cells in fracture repair of the adult mammalian long bone. Bone, 2017, 103: 12-19

[186]

Kawanami A, Matsushita T, Chan YY, Murakami S. Mice expressing GFP and CreER in osteochondro progenitor cells in the periosteum. Biochem. Biophys. Res. Commun., 2009, 386: 477-482

[187]

Lotinun S et al. Osteoclast-specific cathepsin K deletion stimulates S1P-dependent bone formation. J. Clin. Investig., 2013, 123: 666-681

[188]

Han Y et al. Lkb1 deletion in periosteal mesenchymal progenitors induces osteogenic tumors through mTORC1 activation. J. Clin. Investig., 2019, 129: 1895-1909

[189]

Yang W et al. Ptpn11 deletion in a novel progenitor causes metachondromatosis by inducing hedgehog signalling. Nature, 2013, 499: 491-495

[190]

Karlsson C, Thornemo M, Henriksson HB, Lindahl A. Identification of a stem cell niche in the zone of Ranvier within the knee joint. J. Anat., 2009, 215: 355-363

[191]

Tsukasaki M et al. Periosteal stem cells control growth plate stem cells during postnatal skeletal growth. Nat. Commun., 2022, 13

[192]

Ding Y, Mo C, Geng J, Li J, Sun Y. Identification of periosteal osteogenic progenitors in Jawbone. J. Dent. Res., 2022, 101: 1101-1109

[193]

Jones RE et al. Skeletal stem cell-schwann cell circuitry in mandibular repair. Cell Rep., 2019, 28: 2757-2766 e5

[194]

Carr MJ et al. Mesenchymal precursor cells in adult nerves contribute to mammalian tissue repair and regeneration. Cell Stem Cell, 2019, 24: 240-256.e9

[195]

Clements MP et al. The wound microenvironment reprograms schwann cells to invasive mesenchymal-like cells to drive peripheral nerve regeneration. Neuron, 2017, 96: 98-114 e7

[196]

Johnston AP et al. Dedifferentiated schwann cell precursors secreting paracrine factors are required for regeneration of the mammalian digit tip. Cell Stem Cell, 2016, 19: 433-448

[197]

Ransom RC et al. Mechanoresponsive stem cells acquire neural crest fate in jaw regeneration. Nature, 2018, 563: 514-521

[198]

Greenblatt MB, Ono N, Ayturk UM, Debnath S, Lalani S. The unmixing problem: a guide to applying single‐cell RNA sequencing to bone. J. Bone Miner. Res., 2019, 34: 1207-1219

[199]

Li X, Wang C-Y. From bulk, single-cell to spatial RNA sequencing. Int. J. Oral. Sci., 2021, 13: 36

[200]

Kelly NH, Huynh NPT, Guilak F. Single cell RNA-sequencing reveals cellular heterogeneity and trajectories of lineage specification during murine embryonic limb development. Matrix Biol. J. Int. Soc. Matrix Biol., 2020, 89: 1-10

[201]

Sivaraj KK et al. Mesenchymal stromal cell-derived septoclasts resorb cartilage during developmental ossification and fracture healing. Nat. Commun., 2022, 13

[202]

Wolock SL et al. Mapping distinct bone marrow niche populations and their differentiation paths. Cell Rep., 2019, 28: 302-311.e5

[203]

Tikhonova AN et al. The bone marrow microenvironment at single-cell resolution. Nature, 2019, 569: 222-228

[204]

Baryawno N et al. A cellular taxonomy of the bone marrow stroma in homeostasis and leukemia. Cell, 2019, 177: 1915-1932.e16

[205]

Severe N et al. Stress-induced changes in bone marrow stromal cell populations revealed through single-cell protein expression mapping. Cell Stem Cell, 2019, 25: 570-583.e7

[206]

Yianni V, Sharpe PT. Single cell RNA-seq: cell isolation and data analysis. Methods Mol. Methods Mol. Biol., 2022, 2403: 81-89

[207]

Krivanek J et al. Dental cell type atlas reveals stem and differentiated cell types in mouse and human teeth. Nat. Commun., 2020, 11

[208]

Ayturk UM et al. Single-cell RNA sequencing of calvarial and long-bone endocortical cells. J. Bone Min. Res., 2020, 35: 1981-1991

[209]

Farmer DT et al. The developing mouse coronal suture at single-cell resolution. Nat. Commun., 2021, 12

[210]

Holmes G et al. Single-cell analysis identifies a key role for Hhip in murine coronal suture development. Nat. Commun., 2021, 12

[211]

Xie M, Chagin AS. The epiphyseal secondary ossification center: evolution, development and function. Bone, 2021, 142: 115701

[212]

Matthews BG et al. Heterogeneity of murine periosteum progenitors involved in fracture healing. eLife, 2021, 10: e58534

[213]

Kenswil KJG et al. Endothelium-derived stromal cells contribute to hematopoietic bone marrow niche formation. Cell Stem Cell, 2021, 28: 653-670.e11

[214]

Isern J et al. The neural crest is a source of mesenchymal stem cells with specialized hematopoietic stem cell niche function. eLife, 2014, 3: e03696

[215]

Soleimani M, Nadri S. A protocol for isolation and culture of mesenchymal stem cells from mouse bone marrow. Nat. Protoc., 2009, 4: 102-106

[216]

Zhu H et al. A protocol for isolation and culture of mesenchymal stem cells from mouse compact bone. Nat. Protoc., 2010, 5: 550-560

[217]

van den Brink SC et al. Single-cell sequencing reveals dissociation-induced gene expression in tissue subpopulations. Nat. Methods, 2017, 14: 935-936

[218]

Park E et al. Bone marrow transplantation procedures in mice to study clonal hematopoiesis. J. Vis. Exp., 2021, 171: e61875

[219]

Coutu DL, Kokkaliaris KD, Kunz L, Schroeder T. Three-dimensional map of nonhematopoietic bone and bone-marrow cells and molecules. Nat. Biotechnol., 2017, 35: 1202-1210

[220]

Kawamoto, T. & Kawamoto, K. Preparation of thin frozen sections from nonfixed and undecalcified hard tissues using Kawamot’s Film Method (2012). Vol. 1130. In Skeletal Development and Repair (ed. Hilton, M. J.) 149–164 (Humana Press, 2014).

[221]

Li Q et al. Ubiquitin-specific protease 34 inhibits osteoclast differentiation by regulating NF-κB signaling. J. Bone Miner. Res., 2020, 35: 1597-1608

[222]

Kusumbe AP, Ramasamy SK, Starsichova A, Adams RH. Sample preparation for high-resolution 3D confocal imaging of mouse skeletal tissue. Nat. Protoc., 2015, 10: 1904-1914

[223]

Langen UH et al. Cell–matrix signals specify bone endothelial cells during developmental osteogenesis. Nat. Cell Biol., 2017, 19: 189-201

[224]

Jing D et al. Tissue clearing of both hard and soft tissue organs with the PEGASOS method. Cell Res., 2018, 28: 803-818

[225]

Zhan Y, Wu H, Liu L, Lin J, Zhang S. Organic solvent-based tissue clearing techniques and their applications. J. Biophotonics, 2021, 14: e202000413

Funding

National Natural Science Foundation of China (National Science Foundation of China)(82125006)

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