Please wait a minute...
Shopping Cart Email List Chinese
Advanced Search Fig/Tab
Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Featured Articles  |  Most Downloaded  |  Most Reading
Online Submission Subscribe to Our RSS Content Feed
Front Biol    2010, Vol. 5 Issue (5) : 396-406    https://doi.org/10.1007/s11515-010-0930-8
REVIEW
Understanding of stem cells in bone biology and translation into clinical applications
Peng LIU1(), Zhipeng FAN2, Songlin WANG2
1. Laboratory for Skeletal Development and Regenerative Medicine, The Key Laboratory of Oral Biomedicine (Wuhan), Ministry of Education, Wuhan University School of Stomatology, Wuhan 430070, China; 2. Molecular Laboratory for Gene Therapy & Tooth Regeneration, Capital Medical University School of Stomatology, Beijing 100050, China
 Download: PDF(211 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

Developments of stem cell biology provide new approaches for understanding the mechanisms of a number of diseases, including osteoporosis. In this mini-review, we highlight two areas that related to stem cells in bone biology. Recent discovery of the role of osteoclast and their stem cells leads to developing a new approach for treatment of osteoporosis with the initial stimulation of cells in osteoclast lineage and followed by sequentially enhanced bone formation. Stimulation on both sides in bone remodeling is expected to achieve a long term effect on bone formation. For bone regeneration, multiple disciplinary collaborations among bone biologists, stem cell biologists and biomaterial scientists are necessary to successfully develop an integrated stem cell therapy that should include stem cells, suitable scaffolds and bioactive factors/small molecular compounds.
Keywords Stem cells      bone regeneration      osteoporosis      scaffolds      small molecules     
Corresponding Author(s): LIU Peng,Email:liupossible@gmail.com   
Issue Date: 01 October 2010
 Cite this article:   
Peng LIU,Zhipeng FAN,Songlin WANG. Understanding of stem cells in bone biology and translation into clinical applications[J]. Front Biol, 2010, 5(5): 396-406.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-010-0930-8
https://academic.hep.com.cn/fib/EN/Y2010/V5/I5/396
Fig.1  An integrated stem cell therapy for bone regeneration in bone and craniofacial defects. The integrated stem cell therapy for bone regeneration should include expanded stem cells from an optimal resource, ideal scaffolds that can deliver stem cells with controlled biodegradability and well interconnected pores, and bioactive factors, such as small molecules that guide implanted stem cells to adapt to an expected lineages of osteoclasts and osteoblasts.
Fig.1  An integrated stem cell therapy for bone regeneration in bone and craniofacial defects. The integrated stem cell therapy for bone regeneration should include expanded stem cells from an optimal resource, ideal scaffolds that can deliver stem cells with controlled biodegradability and well interconnected pores, and bioactive factors, such as small molecules that guide implanted stem cells to adapt to an expected lineages of osteoclasts and osteoblasts.
1 Alkhiary Y M, Gerstenfeld L C, Krall E, Westmore M, Sato M, Mitlak B H, Einhorn T A (2005). Enhancement of experimental fracture-healing by systemic administration of recombinant human parathyroid hormone (PTH 1-34). J Bone Joint Surg Am , 87(4): 731-741
doi: 10.2106/JBJS.D.02115
2 Aoi T, Yae K, Nakagawa M, Ichisaka T, Okita K, Takahashi K, Chiba T, Yamanaka S (2008). Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science (New York, N. Y) , 321: 699-702
3 Bedogni A, Bettini G, Totola A, Saia G, Nocini P F (2010). Oral bisphosphonate-associated osteonecrosis of the jaw after implant surgery: a case report and literature review. J Oral Maxillofac Surg , 68(7): 1662-1666
doi: 10.1016/j.joms.2010.02.037
4 Beloti M M, Bellesini L S, Rosa A L (2005a). Purmorphamine enhances osteogenic activity of human osteoblasts derived from bone marrow mesenchymal cells. Cell Biol Int , 29(7): 537-541
doi: 10.1016/j.cellbi.2005.02.007
5 Beloti M M, Bellesini L S, Rosa A L (2005b). The effect of purmorphamine on osteoblast phenotype expression of human bone marrow mesenchymal cells cultured on titanium. Biomaterials , 26(20): 4245-4248
doi: 10.1016/j.biomaterials.2004.10.039
6 Bennett J H, Joyner C J, Triffitt J T, Owen M E (1991). Adipocytic cells cultured from marrow have osteogenic potential. J Cell Sci , 99(Pt 1): 131-139
7 Blackwell K A, Raisz L G, Pilbeam C C (2010). Prostaglandins in bone: bad cop, good cop? Trends in endocrinology and metabolism: TEM , 21, 294-301
8 Bodine P V (2008). Wnt signaling control of bone cell apoptosis. Cell Res , 18(2): 248-253
doi: 10.1038/cr.2008.13
9 Bolós V, Grego-Bessa J, de la Pompa J L (2007). Notch signaling in development and cancer. Endocr Rev , 28(3): 339-363
doi: 10.1210/er.2006-0046
10 Bonyadi M, Waldman S D, Liu D, Aubin J E, Grynpas M D, Stanford W L (2003). Mesenchymal progenitor self-renewal deficiency leads to age-dependent osteoporosis in Sca-1/Ly-6A null mice. Proc Natl Acad Sci U S A , 100(10): 5840-5845
11 Brown S E, Tong W, Krebsbach P H (2009). The derivation of mesenchymal stem cells from human embryonic stem cells. Cells Tissues Organs , 189(1-4): 256-260
doi: 10.1159/000151746
12 Buckbinder L, Crawford D T, Qi H, Ke H Z, Olson L M, Long K R, Bonnette P C, Baumann A P, Hambor J E, Grasser W A 3rd, Pan L C, Owen T A, Luzzio M J, Hulford C A, Gebhard D F, Paralkar V M, Simmons H A, Kath J C, Roberts W G, Smock S L, Guzman-Perez A, Brown T A, Li M (2007). Proline-rich tyrosine kinase 2 regulates osteoprogenitor cells and bone formation, and offers an anabolic treatment approach for osteoporosis. Proc Natl Acad Sci U S A , 104(25): 10619-10624
doi: 10.1073/pnas.0701421104
13 Bueno E M, Glowacki J (2009). Cell-free and cell-based approaches for bone regeneration. Nat Rev Rheumatol , 5(12): 685-697
doi: 10.1038/nrrheum.2009.228
14 Cameron K O, Lefker B A, Chu-Moyer M Y, Crawford D T, Jardine P D, DeNinno S L, Gilbert S, Grasser W A, Ke H, Lu B, Owen T A, Paralkar V M, Qi H, Scott D O, Thompson D D, Tjoa C M, Zawistoski M P (2006). Discovery of highly selective EP4 receptor agonists that stimulate new bone formation and restore bone mass in ovariectomized rats. Bioorg Med Chem Lett , 16(7): 1799-1802
15 Canalis E (2008). Notch signaling in osteoblasts. Sci Signal , 1(17): pe17
doi: 10.1126/stke.117pe17
16 Chai G, Zhang Y, Hu X J, Wang M, Liu W, Cui L, Cao Y L (2006). Repair alveolar cleft bone defects with bone marrow stromal cells. Zhonghua Zhengxing Waike Zazhi , 22, 409-411
17 Chen Y, Alman B A (2009). Wnt pathway, an essential role in bone regeneration. J Cell Biochem , 106(3): 353-362
doi: 10.1002/jcb.22020
18 Cipriano C A, Issack P S, Shindle L, Werner C M, Helfet D L, Lane J M (2009). Recent advances toward the clinical application of PTH (1-34) in fracture healing. HSS J , 5(2): 149-153
doi: 10.1007/s11420-009-9109-8
19 Cunningham V J, D'Apice M R, Licata N, Novelli G, Cundy T (2010). Skeletal phenotype of mandibuloacral dysplasia associated with mutations in ZMPSTE24. Bone , 47(3): 591-597
20 Daley G Q (2010). Stem cells: roadmap to the clinic. J Clin Invest , 120(1): 8-10
doi: 10.1172/JCI41801
21 De Kok I J, Hicok K C, Padilla R J, Young R G, Cooper L F (2006). Effect of vitamin D pretreatment of human mesenchymal stem cells on ectopic bone formation. J Oral Implantol , 32(3): 103-109
doi: 10.1563/760.1
22 Delmas P D, Vergnaud P, Arlot M E, Pastoureau P, Meunier P J, Nilssen M H (1995). The anabolic effect of human PTH (1-34) on bone formation is blunted when bone resorption is inhibited by the bisphosphonate tiludronate—is activated resorption a prerequisite for the in vivo effect of PTH on formation in a remodeling system? Bone , 16(6): 603-610
23 Derubeis A R, Mastrogiacomo M, Cancedda R, Quarto R (2003). Osteogenic potential of rat spleen stromal cells. Eur J Cell Biol , 82(4): 175-181
doi: 10.1078/0171-9335-00300
24 Ding G, Liu Y, An Y, Zhang C, Shi S, Wang W, Wang S (2010). Suppression of T cell proliferation by root apical papilla stem cells in vitro. Cells Tissues Organs , 191(5): 357-364
doi: 10.1159/000276589
25 Duailibi M T, Duailibi S E, Young C S, Bartlett J D, Vacanti J P, Yelick P C (2004). Bioengineered teeth from cultured rat tooth bud cells. J Dent Res , 83(7): 523-528
doi: 10.1177/154405910408300703
26 Duan X, Tu Q, Zhang J, Ye J, Sommer C, Mostoslavsky G, David K, Yang P, Chen J (2010). Application of induced pluripotent stem (iPS) cells in periodontal tissue regeneration. J Cellular Physiol ,
doi: 10.1002/jcp.22316
doi: 10.1002/jcp.22316
27 El?in Y M, Inan? B, El?in A E (2010). Human embryonic stem cell differentiation on periodontal ligament fibroblasts. Methods Mol Biol , 584: 269-281
28 Fang D, Seo B M, Liu Y, Sonoyama W, Yamaza T, Zhang C, Wang S, Shi S (2007). Transplantation of mesenchymal stem cells is an optimal approach for plastic surgery. Stem cells, (Dayton, Ohio) , 25, 1021-1028
29 Ferrari S (2009). [Bone remodeling: new therapeutic approaches]. Rev Med Suisse , 5(207): 1325-1328
30 Fracon R N, Teófilo J M, Satin R B, Lamano T (2008). Prostaglandins and bone: potential risks and benefits related to the use of nonsteroidal anti-inflammatory drugs in clinical dentistry. J Oral Sci , 50(3): 247-252
doi: 10.2334/josnusd.50.247
31 Friedenstein A J, Chailakhjan R K, Lalykina K S (1970). The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet , 3(4): 393-403
32 Friedenstein A J, Petrakova K V, Kurolesova A I, Frolova G P (1968). Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation , 6(2): 230-247
doi: 10.1097/00007890-196803000-00009
33 Friedenstein A J, Piatetzky-Shapiro I I, Petrakova K V (1966). Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol , 16(3): 381-390
34 Gronthos S, Mankani M, Brahim J, Robey P G, Shi S (2000). Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci U S A , 97(25): 13625-13630
doi: 10.1073/pnas.240309797
35 Heitz-Mayfield L J, Lang N P (2004). Antimicrobial treatment of peri-implant diseases. Int J Oral Maxillofac Implants , 19(Suppl): 128-139
36 Hoeppner L H, Secreto F J, Westendorf J J (2009). Wnt signaling as a therapeutic target for bone diseases. Expert Opin Ther Targets , 13(4): 485-496
doi: 10.1517/14728220902841961
37 Holmes C, Khan T S, Owen C, Ciliberti N, Grynpas M D, Stanford W L (2007). Longitudinal analysis of mesenchymal progenitors and bone quality in the stem cell antigen-1-null osteoporotic mouse. J Bone Miner Res , 22(9): 1373-1386
doi: 10.1359/jbmr.070604
38 Horwitz E M, Gordon P L, Koo W K, Marx J C, Neel M D, McNall R Y, Muul L, Hofmann T (2002). Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proc Natl Acad Sci U S A , 99(13): 8932-8937
doi: 10.1073/pnas.132252399
39 Huang K Y, Chang J K, Ling S Y, Endo N, Takahashi H E (2000). Epidemiology of cervical and trochanteric fractures of the proximal femur in 1996 in Kaohsiung City, Taiwan. J Bone Miner Metab , 18(2): 89-95
doi: 10.1007/s007740050017
40 Itasaki N, Hoppler S (2010). Crosstalk between Wnt and bone morphogenic protein signaling: a turbulent relationship. Dev Dyn , 239(1): 16-33
41 Jethva R, Otsuru S, Dominici M, Horwitz E M (2009). Cell therapy for disorders of bone. Cytotherapy , 11(1): 3-17
42 Johnson M L (2004). The high bone mass family—the role of Wnt/Lrp5 signaling in the regulation of bone mass. J Musculoskelet Neuronal Interact , 4(2): 135-138
43 Jung Y, Song J, Shiozawa Y, Wang J, Wang Z, Williams B, Havens A, Schneider A, Ge C, Franceschi R T, McCauley L K, Krebsbach P H, Taichman R S (2008). Hematopoietic stem cells regulate mesenchymal stromal cell induction into osteoblasts thereby participating in the formation of the stem cell niche. Stem Cells , 26(8): 2042-2051
44 Kaback L A, Soung Y, Naik A, Geneau G, Schwarz E M, Rosier R N, O’Keefe R J, Drissi H (2008). Teriparatide (1-34 human PTH) regulation of osterix during fracture repair. J Cell Biochem , 105(1): 219-226
45 K?rner E, Unger C, Cerny R, Ahrlund-Richter L, Ganss B, Dilber M S, Wendel M (2009). Differentiation of human embryonic stem cells into osteogenic or hematopoietic lineages: a dose-dependent effect of osterix over-expression. J Cell Physiol , 218(2): 323-333
46 Karsdal M A, Neutzsky-Wulff A V, Dziegiel M H, Christiansen C, Henriksen K (2008). Osteoclasts secrete non-bone derived signals that induce bone formation. Biochem Biophys Res Commun , 366(2): 483-488
47 Katoh M (2007). Networking of WNT, FGF, Notch, BMP, and Hedgehog signaling pathways during carcinogenesis. Stem Cell Rev , 3(1): 30-38
48 Khan A A, Sándor G K, Dore E, Morrison A D, Alsahli M, Amin F, Peters E, Hanley D A, Chaudry S R, Lentle B, Dempster D W, Glorieux F H, Neville A J, Talwar R M, Clokie C M, Mardini M A, Paul T, Khosla S, Josse R G, Sutherland S, Lam D K, Carmichael R P, Blanas N, Kendler D, Petak S, Ste-Marie L G, Brown J, Evans A W, Rios L, Compston J E, and the Canadian Taskforce on Osteonecrosis of the Jaw (2009). Bisphosphonate associated osteonecrosis of the jaw. J Rheumatol , 36(3): 478-490
49 Kim S, Kim S S, Lee S H, Eun Ahn S, Gwak S J, Song J H, Kim B S, Chung H M (2008). In vivo bone formation from human embryonic stem cell-derived osteogenic cells in poly(d,l-lactic-co-glycolic acid)/hydroxyapatite composite scaffolds. Biomaterials , 29(8): 1043-1053
50 Klüppel M, Wrana J L (2005). Turning it up a Notch: cross-talk between TGF beta and Notch signaling. Bioessays , 27(2): 115-118
doi: 10.1002/bies.20187
51 Koh A J, Demiralp B, Neiva K G, Hooten J, Nohutcu R M, Shim H, Datta N S, Taichman R S, McCauley L K (2005). Cells of the osteoclast lineage as mediators of the anabolic actions of parathyroid hormone in bone. Endocrinology , 146(11): 4584-4596
doi: 10.1210/en.2005-0333
52 Kubota T, Michigami T, Ozono K (2009). Wnt signaling in bone metabolism. J Bone Miner Metab , 27(3): 265-271
doi: 10.1007/s00774-009-0064-8
53 Lee K W, Yook J Y, Son M Y, Kim M J, Koo D B, Han Y M, Cho Y S (2010). Rapamycin promotes the osteoblastic differentiation of human embryonic stem cells by blocking the mTOR pathway and stimulating the BMP/Smad pathway. Stem Cells Dev , 19(4): 557-568
doi: 10.1089/scd.2009.0147
54 Li F, Bronson S, Niyibizi C (2010). Derivation of murine induced pluripotent stem cells (iPS) and assessment of their differentiation toward osteogenic lineage. J Cell Biochem , 109(4): 643-652
doi: 10.1002/jcb.22440
55 Li M, Ke H Z, Qi H, Healy D R, Li Y, Crawford D T, Paralkar V M, Owen T A, Cameron K O, Lefker B A, Brown T A, Thompson D D (2003). A novel, non-prostanoid EP2 receptor-selective prostaglandin E2 agonist stimulates local bone formation and enhances fracture healing. J Bone Miner Res , 18(11): 2033-2042
doi: 10.1359/jbmr.2003.18.11.2033
56 Li M, Thompson D D, Paralkar V M (2007). Prostaglandin E(2) receptors in bone formation. Int Orthop , 31(6): 767-772
doi: 10.1007/s00264-007-0406-x
57 Liu B, Wang J, Chan K M, Tjia W M, Deng W, Guan X, Huang J D, Li K M, Chau P Y, Chen D J, Pei D, Pendas A M, Cadi?anos J, López-Otín C, Tse H F, Hutchison C, Chen J, Cao Y, Cheah K S, Tryggvason K, Zhou Z (2005). Genomic instability in laminopathy-based premature aging. Nat Med , 11(7): 780-785
58 Liu X, Pettway G J, McCauley L K, Ma P X (2007). Pulsatile release of parathyroid hormone from an implantable delivery system. Biomaterials , 28(28): 4124-4131
doi: 10.1016/j.biomaterials.2007.05.034
59 Liu Y, Zheng Y, Ding G, Fang D, Zhang C, Bartold P M, Gronthos S, Shi S, Wang S (2008). Periodontal ligament stem cell-mediated treatment for periodontitis in miniature swine. Stem Cells , 26(4): 1065-1073
doi: 10.1634/stemcells.2007-0734
60 Luo L Z, Xu L (2005). Study on direct economic-burden and its risk factors of osteoporotic hip fracture. Zhonghua Liuxingbingxue Zazhi , 26, 669-672
61 Mahmood A, Harkness L, Schr?der H D, Abdallah B M, Kassem M (2010). Enhanced differentiation of human embryonic stem cells to mesenchymal progenitors by inhibition of TGF-beta/activin/nodal signaling using SB-431542. J Bone Miner Res , 25(6): 1216-1233
doi: 10.1002/jbmr.34
62 Marsell R, Jonsson K B, Cho T J, Einhorn T A, Ohlsson C, Schipani E (2007). Mice expressing a constitutively active PTH/PTHrP receptor in osteoblasts show reduced callus size but normal callus morphology during fracture healing. Acta Orthop , 78(1): 39-45
doi: 10.1080/17453670610013402
63 Martin T J, Seeman E (2008). Bone remodelling: its local regulation and the emergence of bone fragility. Best Prac Res , 22, 701-722
64 Martin T, Gooi J H, Sims N A (2009). Molecular mechanisms in coupling of bone formation to resorption. Crit Rev Eukaryot Gene Expr , 19(1): 73-88
65 Mendes S C, Tibbe J M, Veenhof M, Both S, Oner F C, van Blitterswijk C A, de Bruijn J D (2004). Relation between in vitro and in vivo osteogenic potential of cultured human bone marrow stromal cells. J Mater Sci Mater Med , 15(10): 1123-1128
doi: 10.1023/B:JMSM.0000046394.53153.21
66 Méndez-Ferrer S, Michurina T V, Ferraro F, Mazloom A R, Macarthur B D, Lira S A, Scadden D T, Ma’ayan A, Enikolopov G N, Frenette P S (2010). Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature , 466(7308): 829-834
doi: 10.1038/nature09262
67 Miura M, Gronthos S, Zhao M, Lu B, Fisher L W, Robey P G, Shi S (2003). SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A , 100(10): 5807-5812
doi: 10.1073/pnas.0937635100
68 Miura Y, Miura M, Gronthos S, Allen M R, Cao C, Uveges T E, Bi Y, Ehirchiou D, Kortesidis A, Shi S, Zhang L (2005). Defective osteogenesis of the stromal stem cells predisposes CD18-null mice to osteoporosis. Proc Natl Acad Sci U S A , 102(39): 14022-14027
doi: 10.1073/pnas.0409397102
69 Mizoguchi F, Izu Y, Hayata T, Hemmi H, Nakashima K, Nakamura T, Kato S, Miyasaka N, Ezura Y, Noda M (2010). Osteoclast-specific Dicer gene deficiency suppresses osteoclastic bone resorption. J Cell Biochem , 109(5): 866-875
70 Mukherjee S, Raje N, Schoonmaker J A, Liu J C, Hideshima T, Wein M N, Jones D C, Vallet S, Bouxsein M L, Pozzi S, Chhetri S, Seo Y D, Aronson J P, Patel C, Fulciniti M, Purton L E, Glimcher L H, Lian J B, Stein G, Anderson K C, Scadden D T (2008). Pharmacologic targeting of a stem/progenitor population in vivo is associated with enhanced bone regeneration in mice. J Clin Invest , 118(2): 491-504
71 Murray P E, Garcia-Godoy F (2004). Stem cell responses in tooth regeneration. Stem Cells Dev , 13(3): 255-262
doi: 10.1089/154732804323099181
72 Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, Okita K, Mochiduki Y, Takizawa N, Yamanaka S (2008). Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol , 26(1): 101-106
doi: 10.1038/nbt1374
73 Ohazama A, Courtney J M, Tucker A S, Naito A, Tanaka S, Inoue J, Sharpe P T (2004). Traf6 is essential for murine tooth cusp morphogenesis. Dev Dyn , 229(1): 131-135
doi: 10.1002/dvdy.10400
74 Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S (2008). Generation of mouse induced pluripotent stem cells without viral vectors. Science , 322(5903): 949-953
doi: 10.1126/science.1164270
75 Paralkar V M, Borovecki F, Ke H Z, Cameron K O, Lefker B, Grasser W A, Owen T A, Li M, DaSilva-Jardine P, Zhou M, Dunn R L, Dumont F, Korsmeyer R, Krasney P, Brown T A, Plowchalk D, Vukicevic S, Thompson D D (2003). An EP2 receptor-selective prostaglandin E2 agonist induces bone healing. Proc Natl Acad Sci U S A , 100(11): 6736-6740
doi: 10.1073/pnas.1037343100
76 Park S H, Wang H L (2005). Implant reversible complications: classification and treatments. Implant Dent , 14(3): 211-220
doi: 10.1097/01.id.0000173334.60107.1a
77 Raaijmakers M H, Mukherjee S, Guo S, Zhang S, Kobayashi T, Schoonmaker J A, Ebert B L, Al-Shahrour F, Hasserjian R P, Scadden E O, Aung Z, Matza M, Merkenschlager M, Lin C, Rommens J M, Scadden D T (2010). Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature , 464(7290): 852-857
doi: 10.1038/nature08851
78 Raisz L G (1999). Prostaglandins and bone: physiology and pathophysiology. Osteoarthritis and cartilage/OARS. Osteoarthritis Research Society , 7: 419-421
doi: 10.1053/joca.1998.0230
79 Raisz L G (2005). Pathogenesis of osteoporosis: concepts, conflicts, and prospects. J Clin Invest , 115(12): 3318-3325
doi: 10.1172/JCI27071
80 Rivas D, Li W, Akter R, Henderson J E, Duque G (2009). Accelerated features of age-related bone loss in zmpste24 metalloproteinase-deficient mice. J Gerontology , 64A, 1015-1024
81 Rowe D, Lichtler A (2002). A strategy for identifying osteoporosis risk genes. Endocrine , 17(1): 67-75
doi: 10.1385/ENDO:17:1:67
82 Rozen N, Lewinson D, Bick T, Jacob Z C, Stein H, Soudry M (2007). Fracture repair: modulation of fracture-callus and mechanical properties by sequential application of IL-6 following PTH 1-34 or PTH 28-48. Bone , 41(3): 437-445
83 Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I, Tagliafico E, Ferrari S, Robey P G, Riminucci M, Bianco P (2007). Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell , 131(2): 324-336
84 Sahlgren C, Lendahl U (2006). Notch signaling and its integration with other signaling mechanisms. Regen Med , 1(2): 195-205
doi: 10.2217/17460751.1.2.195
85 Secreto F J, Hoeppner L H, Westendorf J J (2009). Wnt signaling during fracture repair. Curr Osteoporos Rep , 7(2): 64-69
doi: 10.1007/s11914-009-0012-5
86 Seo B M, Miura M, Gronthos S, Bartold P M, Batouli S, Brahim J, Young M, Robey P G, Wang C Y, Shi S (2004). Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet , 364(9429): 149-155
doi: 10.1016/S0140-6736(04)16627-0
87 Shi S, Bartold P M, Miura M, Seo B M, Robey P G, Gronthos S (2005). The efficacy of mesenchymal stem cells to regenerate and repair dental structures. Orthod Craniofac Res , 8(3): 191-199
doi: 10.1111/j.1601-6343.2005.00331.x
88 Sonoyama W, Liu Y, Fang D, Yamaza T, Seo B M, Zhang C, Liu H, Gronthos S, Wang C Y, Wang S, Shi S (2006). Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS One , 1: e79
doi: 10.1371/journal.pone.0000079
89 Stevenson K, McGlynn L, Shiels P G (2009). Stem cells: outstanding potential and outstanding questions. Scott Med J , 54(4): 35-37
90 Sudo K, Kanno M, Miharada K, Ogawa S, Hiroyama T, Saijo K, Nakamura Y (2007). Mesenchymal progenitors able to differentiate into osteogenic, chondrogenic, and/or adipogenic cells in vitro are present in most primary fibroblast-like cell populations. Stem Cells , 25(7): 1610-1617
doi: 10.1634/stemcells.2006-0504
91 Takada I, Kouzmenko A P, Kato S (2009). Wnt and PPARgamma signaling in osteoblastogenesis and adipogenesis. Nat Rev Rheumatol , 5(8): 442-447
doi: 10.1038/nrrheum.2009.137
92 Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell , 131(5): 861-872
93 Takahashi K, Yamanaka S (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell , 126(4): 663-676
94 Tamaoki N, Takahashi K, Tanaka T, Ichisaka T, Aoki H, Takeda-Kawaguchi T, Iida K, Kunisada T, Shibata T, Yamanaka S, Tezuka K (2010). Dental pulp cells for induced pluripotent stem cell banking. J Dent Res , 89(8): 773-778
doi: 10.1177/0022034510366846
95 Tamura M, Nemoto E, Sato M M, Nakashima A, Shimauchi H (2010). Role of the Wnt signaling pathway in bone and tooth. Frontiers in bioscience (Elite edition) , 2: 1405-1413
96 Tanaka M, Sakai A, Uchida S, Tanaka S, Nagashima M, Katayama T, Yamaguchi K, Nakamura T (2004). Prostaglandin E2 receptor (EP4) selective agonist (ONO-4819.CD) accelerates bone repair of femoral cortex after drill-hole injury associated with local upregulation of bone turnover in mature rats. Bone , 34(6): 940-948
97 Thesleff I (2003). Developmental biology and building a tooth. Quintessence Int , 34(8): 613-620
98 Thyagarajan B, Scheyhing K, Xue H, Fontes A, Chesnut J, Rao M, Lakshmipathy U (2009). A single EBV-based vector for stable episomal maintenance and expression of GFP in human embryonic stem cells. Regen Med , 4(2): 239-250
doi: 10.2217/17460751.4.2.239
99 Tong W, Brown S E, Krebsbach P H (2007). Human Embryonic Stem Cells Undergo Osteogenic Differentiation in Human Bone Marrow Stromal Cell Microenvironments. J Stem Cells , 2, 139-147
100 Van den Wyngaert T, Huizing M T, Vermorken J B (2006). Bisphosphonates and osteonecrosis of the jaw: cause and effect or a post hoc fallacy? Ann Oncol , 17(8): 1197-1204
doi: 10.1093/annonc/mdl294
101 Vassiliou V, Tselis N, Kardamakis D (2010). Osteonecrosis of the jaws: clinicopathologic and radiologic characteristics, preventive and therapeutic strategies. Strahlenther Onkol , 186(7): 367-373
doi: 10.1007/s00066-010-2066-9
102 Walker E C, McGregor N E, Poulton I J, Pompolo S, Allan E H, Quinn J M, Gillespie M T, Martin T J, Sims N A (2008). Cardiotrophin-1 is an osteoclast-derived stimulus of bone formation required for normal bone remodeling. J Bone Miner Res , 23(12): 2025-2032
doi: 10.1359/jbmr.080706
103 Wang S, Liu Y, Fang D, Shi S (2007). The miniature pig: a useful large animal model for dental and orofacial research. Oral Dis , 13(6): 530-537
doi: 10.1111/j.1601-0825.2006.01337.x
104 Warden S J, Komatsu D E, Rydberg J, Bond J L, Hassett S M (2009). Recombinant human parathyroid hormone (PTH 1-34) and low-intensity pulsed ultrasound have contrasting additive effects during fracture healing. Bone , 44(3): 485-494
105 Wataru S, Kazuomi S, Yoshikazu N, Hiroaki I, Takaharu Y, Hideki Y (2005). Three-dimensional morphological analysis of humeral heads: a study in cadavers. Acta Orthop , 76(3): 392-396
106 Weber J M, Calvi L M (2010). Notch signaling and the bone marrow hematopoietic stem cell niche. Bone , 46(2): 281-285
107 Wei G, Pettway G J, McCauley L K, Ma P X (2004). The release profiles and bioactivity of parathyroid hormone from poly(lactic-co-glycolic acid) microspheres. Biomaterials , 25(2): 345-352
doi: 10.1016/S0142-9612(03)00528-3
108 Woo D G, Shim M S, Park J S, Yang H N, Lee D R, Park K H (2009). The effect of electrical stimulation on the differentiation of hESCs adhered onto fibronectin-coated gold nanoparticles. Biomaterials , 30(29): 5631-5638
doi: 10.1016/j.biomaterials.2009.07.026
109 Wu X, Ding S, Ding Q, Gray N S, Schultz P G (2002). A small molecule with osteogenesis-inducing activity in multipotent mesenchymal progenitor cells. J Am Chem Soc , 124(49): 14520-14521
doi: 10.1021/ja0283908
110 Xu C, Jiang J, Sottile V, McWhir J, Lebkowski J, Carpenter M K (2004). Immortalized fibroblast-like cells derived from human embryonic stem cells support undifferentiated cell growth. Stem Cells , 22(6): 972-980
doi: 10.1634/stemcells.22-6-972
111 Xu L, Lu A, Zhao X, Chen X, Cummings S R (1996). Very low rates of hip fracture in Beijing, People’s Republic of China the Beijing Osteoporosis Project. Am J Epidemiol , 144(9): 901-907
112 Yadav V K, Ducy P (2010). Lrp5 and bone formation : A serotonin-dependent pathway. Ann N Y Acad Sci , 1192(1): 103-109
doi: 10.1111/j.1749-6632.2009.05312.x
113 Yan L, Zhou B, Prentice A, Wang X, Golden M H (1999). Epidemiological study of hip fracture in Shenyang, People’s Republic of China. Bone , 24(2): 151-155
114 Yan X, Qin H, Qu C, Tuan R S, Shi S, Huang G T (2010). iPS cells reprogrammed from human mesenchymal-like stem/progenitor cells of dental tissue origin. Stem Cells Dev , 19(4): 469-480
doi: 10.1089/scd.2009.0314
115 Yin D, Wang Z, Gao Q, Sundaresan R, Parrish C, Yang Q, Krebsbach P H, Lichtler A C, Rowe D W, Hock J, Liu P (2009). Determination of the fate and contribution of ex vivo expanded human bone marrow stem and progenitor cells for bone formation by 2.3ColGFP. Mol Ther , 17(11): 1967-1978
doi: 10.1038/mt.2009.151
116 Young C S, Abukawa H, Asrican R, Ravens M, Troulis M J, Kaban L B, Vacanti J P, Yelick P C (2005). Tissue-engineered hybrid tooth and bone. Tissue Eng , 11(9-10): 1599-1610
doi: 10.1089/ten.2005.11.1599
117 Young C S, Terada S, Vacanti J P, Honda M, Bartlett J D, Yelick P C (2002). Tissue engineering of complex tooth structures on biodegradable polymer scaffolds. J Dent Res , 81(10): 695-700
doi: 10.1177/154405910208101008
118 Zanotti S, Canalis E (2010). Notch and the skeleton. Mol Cell Biol , 30(4): 886-896
doi: 10.1128/MCB.01285-09
119 Zhao X Y, Li W, Lv Z, Liu L, Tong M, Hai T, Hao J, Guo C L, Ma Q W, Wang L, Zeng F, Zhou Q (2009). iPS cells produce viable mice through tetraploid complementation. Nature , 461(7260): 86-90
doi: 10.1038/nature08267
120 Zhao X Y, Li W, Lv Z, Liu L, Tong M, Hai T, Hao J, Wang X, Wang L, Zeng F, Zhou Q (2010a). Viable fertile mice generated from fully pluripotent iPS cells derived from adult somatic cells. Stem Cell Rev , 6(3): 390-397
doi: 10.1007/s12015-010-9160-3
121 Zhao X Y, Lv Z, Li W, Zeng F, Zhou Q (2010b). Production of mice using iPS cells and tetraploid complementation. Nat Protoc , 5(5): 963-971
doi: 10.1038/nprot.2010.61
122 Zheng Y, Liu Y, Zhang C M, Zhang H Y, Li W H, Shi S, Le A D, Wang S L (2009). Stem cells from deciduous tooth repair mandibular defect in swine. J Dent Res , 88(3): 249-254
doi: 10.1177/0022034509333804
123 Zhu H, Zhang Y, Ge H, (2004). Investigation of milk product consuming and the prevalence of spine fracture in elderly women. Proceeding of the 3rd. Shanghai Osteoporosis Symposium , 7: 146
124 Zippel N, Schulze M, Tobiasch E (2010). Biomaterials and mesenchymal stem cells for regenerative medicine. Recent Pat Biotechnol , 4(1): 1-22
doi: 10.2174/187220810790069497
[1] Tyler Harvey, Chen-Ming Fan. Origin of tendon stem cells in situ[J]. Front. Biol., 2018, 13(4): 263-276.
[2] Thai Q. Dao, Jennifer C. Fletcher. CLE peptide-mediated signaling in shoot and vascular meristem development[J]. Front. Biol., 2017, 12(6): 406-420.
[3] Liang Hu,Edward Trope,Qi-Long Ying. Metabolism of pluripotent stem cells[J]. Front. Biol., 2016, 11(5): 355-365.
[4] Kyle R. Denton,Chongchong Xu,Harsh Shah,Xue-Jun Li. Modeling axonal defects in hereditary spastic paraplegia with human pluripotent stem cells[J]. Front. Biol., 2016, 11(5): 339-354.
[5] Gabrielle Rushing,Rebecca A. Ihrie. Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone[J]. Front. Biol., 2016, 11(4): 261-284.
[6] Paul J. Lucassen,Charlotte A. Oomen. Stress, hippocampal neurogenesis and cognition: functional correlations[J]. Front. Biol., 2016, 11(3): 182-192.
[7] Fatih Semerci,Mirjana Maletic-Savatic. Transgenic mouse models for studying adult neurogenesis[J]. Front. Biol., 2016, 11(3): 151-167.
[8] Jin He. Function of Polycomb repressive complexes in stem cells[J]. Front. Biol., 2016, 11(2): 65-74.
[9] Stuart J. Grice,Ji-Long Liu. A SteMNess perspective of survival motor neuron function: splicing factors in stem cell biology and disease[J]. Front. Biol., 2015, 10(4): 297-309.
[10] Massimo Bonora,Paolo Pinton,Keisuke Ito. Mitochondrial control of hematopoietic stem cell balance and hematopoiesis[J]. Front. Biol., 2015, 10(2): 117-124.
[11] Gary R. HIME,Nicole SIDDALL,Katja HORVAY,Helen E. ABUD. Analyzing stem cell dynamics: use of cutting edge genetic approaches in model organisms[J]. Front. Biol., 2015, 10(1): 1-10.
[12] Brandoch D. COOK. Modeling murine yolk sac hematopoiesis with embryonic stem cell culture systems[J]. Front. Biol., 2014, 9(5): 339-346.
[13] Wei Bin FANG,Min YAO,Nikki CHENG. Priming cancer cells for drug resistance: role of the fibroblast niche[J]. Front. Biol., 2014, 9(2): 114-126.
[14] Adalto PONTES, Yonggang ZHANG, Wenhui HU. Novel functions of GABA signaling in adult neurogenesis[J]. Front Biol, 2013, 8(5): 496-507.
[15] Bipasha MUKHERJEE-CLAVIN, Mark TOMISHIMA, Gabsang LEE. Current approaches for efficient genetic editing in human pluripotent stem cells[J]. Front Biol, 2013, 8(5): 461-467.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed