Biomaterials Translational ›› 2022, Vol. 3 ›› Issue (4): 280-294.doi: 10.12336/biomatertransl.2022.04.007
• REVIEW • Previous Articles
Guixin Yuan1,2,3, Zan Li4, Xixi Lin1,2,3, Na Li1,2,3,*(), Ren Xu1,2,3,*(
)
Received:
2022-11-09
Revised:
2022-11-29
Accepted:
2022-12-19
Online:
2022-12-29
Published:
2022-12-28
Contact:
Na Li, Email: xuren526@xmu.edu.cn; Ren Xu, Email: lina0924@xmu.edu.cn
About author:
Na Li, lina0924@xmu.edu.cn.;#Author Equally.
Yuan, G.; Li, Z.; Lin, X.; Li, N.; Xu, R. New perspective of skeletal stem cells. Biomater Transl. 2022, 3(4), 280-294.
PDPN | CD146 | CD73 | CD164 | THY1 | AlphaV | Thy | 6C3 | CD105 | CD200 | ||
---|---|---|---|---|---|---|---|---|---|---|---|
hSSC | + | – | + | + | mSSCs | + | – | – | – | ||
hBCSP | + | + | Pre–BCSP | + | – | – | – | – | |||
hOP–1 | – | + | hi | BCSP | + | – | – | + | |||
hOP–2 | – | + | – | – | lo | PCP | + | – | – | + | + |
hCP–1 | + | – | – | – | Thy | + | + | – | + | ||
hCP–2 | + | – | – | + | BLSP | + | + | – | – | ||
hCP–3 | + | – | + | + | 6C3 | + | – | + | + | ||
HEC | + | – | – | – |
Table 1. Differences in surface markers between hSSCs and mSSCs
PDPN | CD146 | CD73 | CD164 | THY1 | AlphaV | Thy | 6C3 | CD105 | CD200 | ||
---|---|---|---|---|---|---|---|---|---|---|---|
hSSC | + | – | + | + | mSSCs | + | – | – | – | ||
hBCSP | + | + | Pre–BCSP | + | – | – | – | – | |||
hOP–1 | – | + | hi | BCSP | + | – | – | + | |||
hOP–2 | – | + | – | – | lo | PCP | + | – | – | + | + |
hCP–1 | + | – | – | – | Thy | + | + | – | + | ||
hCP–2 | + | – | – | + | BLSP | + | + | – | – | ||
hCP–3 | + | – | + | + | 6C3 | + | – | + | + | ||
HEC | + | – | – | – |
Gene | Transgenes | Source | Function | References |
---|---|---|---|---|
Col2a1 | Col2a1a–CreER | Bone/cartilage | Contribute to osteoblasts and chondrocytes and the formation of CD31+ blood vessels | |
Gli1 | Gli1–CreERT | Bone/cartilage | Expressed in the quiescent zone of the long bone growth plate in postnatal mice | |
PTHrP | PTHrP–CreER | Bone/cartilage | Generate chondrocytes, osteoblasts, and mature cortical osteocytes during the repair of femoral fracture | |
Sox9 | Sox9–CreERT | cartilage | Differentiate into chondrocytes | |
FoxA2 | FoxA2–CreER | Bone/cartilage | Promote growth plate tissue regeneration, exhibit higher clonogenicity, and longevity | |
mTert | mTert–rtTA | Cartilage | Contribute to endochondral osteogenesis as chondrogenic osteoprogenitor cells |
Table 2. Markers of skeletal stem cells in long bone growth plates
Gene | Transgenes | Source | Function | References |
---|---|---|---|---|
Col2a1 | Col2a1a–CreER | Bone/cartilage | Contribute to osteoblasts and chondrocytes and the formation of CD31+ blood vessels | |
Gli1 | Gli1–CreERT | Bone/cartilage | Expressed in the quiescent zone of the long bone growth plate in postnatal mice | |
PTHrP | PTHrP–CreER | Bone/cartilage | Generate chondrocytes, osteoblasts, and mature cortical osteocytes during the repair of femoral fracture | |
Sox9 | Sox9–CreERT | cartilage | Differentiate into chondrocytes | |
FoxA2 | FoxA2–CreER | Bone/cartilage | Promote growth plate tissue regeneration, exhibit higher clonogenicity, and longevity | |
mTert | mTert–rtTA | Cartilage | Contribute to endochondral osteogenesis as chondrogenic osteoprogenitor cells |
Figure 1. The distribution of SSCs in the growth plate, periosteum, bone marrow, and peripheral circulation shows different cell surface markers. The cell surface markers of SSCs on the growth plate are CD200+, PTHrP+ Col2a1+, Gli1+, FoxA2+, and mTert+. The cell surface markers of PSCs are Ctsk+, Prx1+ Axin2+, Sox9+, Mx1+, and α–SMA+. The cell surface markers of SSCs in the bone marrow cavity are Lepr+, Nestin+, Nes+, Cxcl12+, and Grem1+. The cell surface markers of circulating osteogenic cells in the peripheral circulation are haematopoietic COP cells (CD45+, CD34+, CD14+, OCN+, AP+, and Col1+) and MSC–like COP cells (CD45–, CD34–, CD44+, CD73+, CD90+, and CD105+). Axin2: axis inhibition protein 2; AP: alkaline phosphatase; OCN: osteocalcin; Col1: type 1 collagen; Col2a1: type 2 collagen alpha 1 chain; COP: circulating osteogenic cell; Ctsk: cathepsin K; Cxcl12: chemokine (C–X–C motif) ligand 12; FoxA2: forkhead box A2; Gli1: GLI–Kruppel family member GLI1; Grem1: gremlin 1, DAN family BMP antagonist; Lepr: leptin receptor; MSC: mesenchymal stem cell; mTert: mouse Telomerase; Mx1: MX dynamin like GTPase 1; Nes: nestin; Prx1: paired related homeobox 1; PSC: periosteal stem cell; PTHrP: parathyroid–associated protein; Sox9: SRY (sex determining region Y)–box 9; SSCs: skeletal stem cells; α–SMA: α–smooth muscle actin.
Gene | Transgenes | Source | Function | References |
---|---|---|---|---|
Ctsk | Ctsk–Cre | Bone/cartilage/adipose | A marker of osteoclasts; distinguishing periosteal osteoprogenitor cell types | |
Prx1 | Prrx1–Cre | Bone/cartilage | In the repair of cranial defects | |
Sox9 | Sox9–CreERT | Bone/cartilage | Generate chondrocytes, osteoblasts, and mature cortical osteocytes during the repair of femoral fracture | |
Mx1 | Mx1–Cre αSMA–CreERT αSMA–GFP | Bone/cartilage | Repairing new periosteum | |
αSMA | ||||
Gli1 | Gli1–CreERT | Bone/cartilage | Labels skeletal stem cells of the growth plate | |
Hoxa11 | Hoxa11–CreERT2 Hoxa11–EGFP | Bone/cartilage | Regulating differentiation of Hox–expressing skeletal stem cells into the osteolineage |
Table 3. Markers of skeletal stem cells in the periosteum of long bones
Gene | Transgenes | Source | Function | References |
---|---|---|---|---|
Ctsk | Ctsk–Cre | Bone/cartilage/adipose | A marker of osteoclasts; distinguishing periosteal osteoprogenitor cell types | |
Prx1 | Prrx1–Cre | Bone/cartilage | In the repair of cranial defects | |
Sox9 | Sox9–CreERT | Bone/cartilage | Generate chondrocytes, osteoblasts, and mature cortical osteocytes during the repair of femoral fracture | |
Mx1 | Mx1–Cre αSMA–CreERT αSMA–GFP | Bone/cartilage | Repairing new periosteum | |
αSMA | ||||
Gli1 | Gli1–CreERT | Bone/cartilage | Labels skeletal stem cells of the growth plate | |
Hoxa11 | Hoxa11–CreERT2 Hoxa11–EGFP | Bone/cartilage | Regulating differentiation of Hox–expressing skeletal stem cells into the osteolineage |
Gene | Transgenes | Source | Function | References |
---|---|---|---|---|
Axin2 | Axin2–CreER | Bone/cartilage/adipose | Osteoblasts, mesenchymal cells | |
Cxcl12 | Cxcl12–CreER | Bone/cartilage | Reactivate to form osteoblasts after injury | |
Mx1 | Mx1–CreER | Bone/cartilage | Differentiate into cartilage and adipose tissue, respond to bone fractures | |
Nestin | Nestin–CreER | Bone/cartilage | Nestin+ mesenchymal stem cells can self–renew and expand in transplantation experiments | |
Lepr | Lepr–Cre | Bone/cartilage/adipose | Regulation of adipogenesis and osteogenesis | |
Grem1 | Grem1–CreER | Bone/cartilage | Mark osteochondroreticular stem cells, bone repair |
Table 4. Markers of skeletal stem cells in the bone marrow
Gene | Transgenes | Source | Function | References |
---|---|---|---|---|
Axin2 | Axin2–CreER | Bone/cartilage/adipose | Osteoblasts, mesenchymal cells | |
Cxcl12 | Cxcl12–CreER | Bone/cartilage | Reactivate to form osteoblasts after injury | |
Mx1 | Mx1–CreER | Bone/cartilage | Differentiate into cartilage and adipose tissue, respond to bone fractures | |
Nestin | Nestin–CreER | Bone/cartilage | Nestin+ mesenchymal stem cells can self–renew and expand in transplantation experiments | |
Lepr | Lepr–Cre | Bone/cartilage/adipose | Regulation of adipogenesis and osteogenesis | |
Grem1 | Grem1–CreER | Bone/cartilage | Mark osteochondroreticular stem cells, bone repair |
Craniofacial bone | Gene | Transgenes | Source | Function | References |
---|---|---|---|---|---|
Periosteum of the cranium | Ctsk | Ctsk–Cre | Bone/cartilage | Intramembranous osteogenesis | |
Mx1 | Mx1–Cre | Bone/cartilage | Participate in bone healing | ||
SMA | αSMA–CreERT | Bone/cartilage | |||
Calvarial sutures | Gli1 | Gli1–CreER | Bone/cartilage | Cause premature craniosynostosis | |
Axin2 | Axin2–CreERT | Bone/cartilage | Respond to orthodontic tension force | ||
Prx1 | Prx1–Cre | Bone/cartilage | Scattered distribution in calvaria sutures | ||
Teeth and periodontal tissue | Gli1 | Gli1–CreER | Bone/cartilage | Regulated by Wnt pathway | |
Axin2 | Axin2–CreERT | Bone/cartilage | Primary progenitor cells of cementoblasts | ||
Prx1 | Prx1–Cre | Bone/cartilage | Participate in angiogenesis. | ||
Jaw bone | Ctsk | Ctsk–Cre | Bone/cartilage | Present on the periosteum of the jaw | |
Ly6a | Bone/cartilage |
Table 5. Markers of skeletal stem cells in craniofacial bone
Craniofacial bone | Gene | Transgenes | Source | Function | References |
---|---|---|---|---|---|
Periosteum of the cranium | Ctsk | Ctsk–Cre | Bone/cartilage | Intramembranous osteogenesis | |
Mx1 | Mx1–Cre | Bone/cartilage | Participate in bone healing | ||
SMA | αSMA–CreERT | Bone/cartilage | |||
Calvarial sutures | Gli1 | Gli1–CreER | Bone/cartilage | Cause premature craniosynostosis | |
Axin2 | Axin2–CreERT | Bone/cartilage | Respond to orthodontic tension force | ||
Prx1 | Prx1–Cre | Bone/cartilage | Scattered distribution in calvaria sutures | ||
Teeth and periodontal tissue | Gli1 | Gli1–CreER | Bone/cartilage | Regulated by Wnt pathway | |
Axin2 | Axin2–CreERT | Bone/cartilage | Primary progenitor cells of cementoblasts | ||
Prx1 | Prx1–Cre | Bone/cartilage | Participate in angiogenesis. | ||
Jaw bone | Ctsk | Ctsk–Cre | Bone/cartilage | Present on the periosteum of the jaw | |
Ly6a | Bone/cartilage |
Figure 2. Distribution of SSCs in craniofacial bone, with different cell surfaces shown. The cell surface markers of SSCs in the cranial periosteum are Ctsk+ and Mx1+αSMA+. The cell surface markers of SSCs in the calvarial sutures are Gli1+, Prx1+, and Axin2+. The cell surface markers of SSCs in the teeth and periodontal tissue are Gli1+, Prx1+, and Axin2+. The cell surface markers of SSCs in the jaw bone are Ctsk+ and Ly6a+. Axin2: axis inhibition protein 2; Ctsk: cathepsin K; Gli1: GLI–Kruppel family member GLI1; Ly6a: lymphocyte antigen 6 complex, locus A; Mx1: MX dynamin like GTPase 1; Prx1: paired related homeobox 1; SSC: skeletal stem cell; αSMA: α–smooth muscle actin.
Cell type | Markers | Function | References |
---|---|---|---|
Haematopoietic COP cells | CD45+CD34+CD14+OCN+AP+Col1+ | Maintain a stable level in the peripheral circulation | |
MSC–like COP cells | CD45–CD34–CD44+CD73+CD90+CD105+ | Possess characteristics of mesenchymal stem cells |
Table 6. Markers of circulating osteogenic cells in the peripheral circulation
Cell type | Markers | Function | References |
---|---|---|---|
Haematopoietic COP cells | CD45+CD34+CD14+OCN+AP+Col1+ | Maintain a stable level in the peripheral circulation | |
MSC–like COP cells | CD45–CD34–CD44+CD73+CD90+CD105+ | Possess characteristics of mesenchymal stem cells |
Figure 3. Circulating osteogenic cells contribute to bone formation through stem cell homing to receive IGF–1, PDGF–AB, SDF–1, and MDC. M–CSF stimulates HSCs to differentiate into monocytes and macrophages and then differentiate into osteoclasts to receive RANKL. COP: circulating osteogenic precursor cell; HSC: haematopoietic stem cell; IGF–1: insulin–like growth factor 1; M–CSF: macrophage colony–stimulating factor; MDC: macrophage–derived chemokine; MSC: mesenchymal stem cell; PDGF–AB: platelet derived growth factor AB; RANKL: receptor activator of nuclear factor kappa–Β ligand; SDF–1: stromal cell–derived factor–1.
Figure 4. (A) Wnt and BMP2 are enriched in PSCs. PDGF–BB and CCL5/CCR3/CCR5 promote the migration of SSCs, while activation of Piezo1 promotes the expression and nuclear localisation of Yap in PSCs, and forms a transcriptional Yap/β–catenin complex which promotes fracture healing. (B) The Wnt and mTORC1 signalling pathways regulate SSCs of the growth plate. PSCs control growth plate SSCs through the Ihh signalling pathway. (C) Aged mice develop a pro–inflammatory microenvironment that disrupts the osteoclast–osteoblast balance. A combination of BMP2 and CSF1 antagonists reverses this change and activates aging SSCs in mice, returning them to a younger state. BMP2: bone morphogenetic protein 2; CCL5: chemokine (C–C motif) ligand 5; CCR3: C–C motif chemokine receptor 3; CCR5: C–C motif chemokine receptor 5; CSF1: colony stimulating factor 1; mTORC1: mechanistic target of rapamycin complex; PDGF–BB: platelet derived growth factor BB; PSC: periosteal stem cell; PTHrP: parathyroid hormone–related protein; Wnt: wingless–related integration site; Yap: yes–related protein.
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[2] | Suzanne M. Watt. The long and winding road: homeostatic and disordered haematopoietic microenvironmental niches: a narrative review [J]. Biomaterials Translational, 2022, 3(1): 31-54. |
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