Research progress in the mechanism of protein factors in regulating bone remodeling_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

LI Ju ^1,2 , GUO Xiaodong ^1,2 , LI Mingzheng ^1,2,3 ,  XIAO Yu ^1,2 ,  BAO Chongyun ^1,3

1. State Key Laboratory of Oral Diseases, Sichuan University, Chengdu Sichuan, 610041, P.R.China;
2. National Clinical Research Center of Oral Diseases, Sichuan University, Chengdu Sichuan, 610041, P.R.China;
3. Department of Oral and Maxillofacial Surgery, West China Hospital of Stomatology, Sichuan University, Chengdu Sichuan, 610041, P.R.China;

Corresponding author：

XIAO Yu, Email: xiaoyu_8528@163.com; BAO Chongyun, Email: cybao9933@sina.com

Keywords：

Bone remodeling; proteins; osteoblast; osteoclast

DOI：

10.7507/1002-1892.201808059

Video：

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Objective To review the role and mechanism of protein factors in bone remodeling, and provides theoretical basis for further elucidating the pathogenesis and clinical treatment of bone-related diseases. Methods The relevant research results at home and abroad in recent years were extensively consulted, analyzed, and summarized. Results Bone remodeling is an important physiological process to maintain bone homeostasis. Protein, as an important stimulator in bone remodeling, regulates the balance between bone resorption and bone formation. Conclusion At present, the research on the mechanism of protein in bone remodeling is insufficient. Therefore, it is necessary to further study the specific time, process, and interaction network of protein in bone remodeling, and to confirm its mechanism in bone remodeling, so as to reveal and treat the pathogenesis of bone-related diseases.

Citation： LI Ju, GUO Xiaodong, LI Mingzheng, XIAO Yu, BAO Chongyun. Research progress in the mechanism of protein factors in regulating bone remodeling. Chinese Journal of Reparative and Reconstructive Surgery, 2019, 33(1): 115-123. doi: 10.7507/1002-1892.201808059 Copy

1.	Furuya M, Kikuta J, Fujimori S, et al. Direct cell-cell contact between mature osteoblasts and osteoclasts dynamically controls their functions in vivo. Nat Commun, 2018, 9(1): 300.
2.	Montagnani A. Bone anabolics in osteoporosis: Actuality and perspectives. World J Orthop, 2014, 5(3): 247-254.
3.	Väänänen HK, Laitala-Leinonen T. Osteoclast lineage and function. Arch Biochem Biophys, 2008, 473(2): 132-138.
4.	Väänänen HK, Zhao H, Mulari M, et al. The cell biology of osteoclast function. J Cell Sci, 2000, 113(Pt 3): 377-381.
5.	Okaji M, Sakai H, Sakai E, et al. The regulation of bone resorption in tooth formation and eruption processes in mouse alveolar crest devoid of cathepsin k. J Pharmacol Sci, 2003, 91(4): 285-294.
6.	Garnero P, Borel O, Byrjalsen I, et al. The collagenolytic activity of cathepsin K is unique among mammalian proteinases. J Biol Chem, 1998, 273(48): 32347-32352.
7.	Borel O, Gineyts E, Bertholon C, et al. Cathepsin K preferentially solubilizes matured bone matrix. Calcif Tissue Int, 2012, 91(1): 32-39.
8.	Gowen M, Lazner F, Dodds R, et al. Cathepsin K knockout mice develop osteopetrosis due to a deficit in matrix degradation but not demineralization. J Bone Miner Res, 1999, 14(10): 1654-1663.
9.	Saftig P, Hunziker E, Wehmeyer O, et al. Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc Natl Acad Sci U S A, 1998, 95(23): 13453-13458.
10.	Drake MT, Clarke BL, Oursler MJ, et al. Cathepsin K inhibitors for osteoporosis: biology, potential clinical utility, and lessons learned. Endocr Rev, 2017, 38(4): 325-350.
11.	Nesbitt SA, Horton MA. Trafficking of matrix collagens through bone-resorbing osteoclasts. Science, 1997, 276(5310): 266-269.
12.	Salo J, Lehenkari P, Mulari M, et al. Removal of osteoclast bone resorption products by transcytosis. Science, 1997, 276(5310): 270-273.
13.	Vääräniemi J, Halleen JM, Kaarlonen K, et al. Intracellular machinery for matrix degradation in bone-resorbing osteoclasts. J Bone Miner Res, 2004, 19(9): 1432-1440.
14.	Ljusberg J, Wang Y, Lång P, et al. Proteolytic excision of a repressive loop domain in tartrate-resistant acid phosphatase by cathepsin K in osteoclasts. J Biol Chem, 2005, 280(31): 28370-28381.
15.	Halleen JM, Räisänen S, Salo JJ, et al. Intracellular fragmentation of bone resorption products by reactive oxygen species generated by osteoclastic tartrate-resistant acid phosphatase. J Biol Chem, 1999, 274(33): 22907-22910.
16.	Alatalo SL, Halleen JM, Hentunen TA, et al. Rapid screening method for osteoclast differentiation in vitro that measures tartrate-resistant acid phosphatase 5b activity secreted into the culture medium. Clin Chem, 2000, 46(11): 1751-1754.
17.	Rissanen JP, Suominen MI, Peng Z, et al. Secreted tartrate-resistant acid phosphatase 5b is a marker of osteoclast number in human osteoclast cultures and the rat ovariectomy model. Calcif Tissue Int, 2008, 82(2): 108-115.
18.	Wu Y, Lee JW, Uy L, et al. Tartrate-resistant acid phosphatase (TRACP 5b): a biomarker of bone resorption rate in support of drug development: modification, validation and application of the BoneTRAP kit assay. J Pharm Biomed Anal, 2009, 49(5): 1203-1212.
19.	Hill PA, Murphy G, Docherty AJ, et al. The effects of selective inhibitors of matrix metalloproteinases (MMPs) on bone resorption and the identification of MMPs and TIMP-1 in isolated osteoclasts. J Cell Sci, 1994, 107(Pt 11): 3055-3064.
20.	Spessotto P, Rossi FM, Degan M, et al. Hyaluronan-CD44 interaction hampers migration of osteoclast-like cells by down-regulating MMP-9. J Cell Biol, 2002, 158(6): 1133-1144.
21.	Samanna V, Ma T, Mak TW, et al. Actin polymerization modulates CD44 surface expression, MMP-9 activation, and osteoclast function. J Cell Physiol, 2007, 213(3): 710-720.
22.	Engsig MT, Chen QJ, Vu TH, et al. Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones. J Cell Biol, 2000, 151(4): 879-889.
23.	Dougall WC, Glaccum M, Charrier K, et al. RANK is essential for osteoclast and lymph node development. Genes Dev, 1999, 13(18): 2412-2424.
24.	Li J, Sarosi I, Yan XQ, et al. RANK is the intrinsic hematopoietic cell surface receptor that controls osteoclastogenesis and regulation of bone mass and calcium metabolism. Proc Natl Acad Sci U S A, 2000, 97(4): 1566-1571.
25.	Boyle WJ, Simonet WS, Lacey DL. Osteoclast differentiation and activation. Nature, 2003, 423(6937): 337-342.
26.	Mizuno A, Amizuka N, Irie K, et al. Severe osteoporosis in mice lacking osteoclastogenesis inhibitory factor/osteoprotegerin. Biochem Biophys Res Commun, 1998, 247(3): 610-615.
27.	Bucay N, Sarosi I, Dunstan CR, et al. osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev, 1998, 12(9): 1260-1268.
28.	Song R, Gu J, Liu X, et al. Inhibition of osteoclast bone resorption activity through osteoprotegerin-induced damage of the sealing zone. Int J Mol Med, 2014, 34(3): 856-862.
29.	Jaffe AB, Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol, 2005, 21: 247-269.
30.	Palmqvist P, Persson E, Conaway HH, et al. IL-6, leukemia inhibitory factor, and oncostatin M stimulate bone resorption and regulate the expression of receptor activator of NF-kappa B ligand, osteoprotegerin, and receptor activator of NF-kappa B in mouse calvariae. J Immunol, 2002, 169(6): 3353-3362.
31.	Hattersley G, Chambers TJ. Calcitonin receptors as markers for osteoclastic differentiation: correlation between generation of bone-resorptive cells and cells that express calcitonin receptors in mouse bone marrow cultures. Endocrinology, 1989, 125(3): 1606-1612.
32.	Kulterer B, Friedl G, Jandrositz A, et al. Gene expression profiling of human mesenchymal stem cells derived from bone marrow during expansion and osteoblast differentiation. BMC Genomics, 2007, 8: 70.
33.	Huang Z, Nelson ER, Smith RL, et al. The sequential expression profiles of growth factors from osteoprogenitors [correction of osteroprogenitors] to osteoblasts in vitro. Tissue Eng, 2007, 13(9): 2311-2320.
34.	Viguet-Carrin S, Garnero P, Delmas PD. The role of collagen in bone strength. Osteoporos Int, 2006, 17(3): 319-336.
35.	Staines KA, MacRae VE, Farquharson C. The importance of the SIBLING family of proteins on skeletal mineralisation and bone remodelling. J Endocrinol, 2012, 214(3): 241-255.
36.	Neve A, Corrado A, Cantatore FP. Osteocalcin: skeletal and extra-skeletal effects. J Cell Physiol, 2013, 228(6): 1149-1153.
37.	Fleisher GA, Eickelberg ES, Elveback LR. Alkaline phosphatase activity in the plasma of children and adolescents. Clin Chem, 1977, 23(3): 469-472.
38.	Canalis E. Effect of hormones and growth factors on alkaline phosphatase activity and collagen synthesis in cultured rat calvariae. Metabolism, 1983, 32(1): 14-20.
39.	Marie PJ, Travers R. Continuous infusion of 1,25-dihydroxyvitamin D3 stimulates bone turnover in the normal young mouse. Calcif Tissue Int, 1983, 35(4-5): 418-425.
40.	Farley JR, Baylink DJ. Skeletal alkaline phosphatase activity as a bone formation index in vitro. Metabolism, 1986, 35(6): 563-571.
41.	Fedde KN, Lane CC, Whyte MP. Alkaline phosphatase is an ectoenzyme that acts on micromolar concentrations of natural substrates at physiologic pH in human osteosarcoma (SAOS-2) cells. Arch Biochem Biophys, 1988, 264(2): 400-409.
42.	Ullrich SJ, Glaubitz C. Perspectives in enzymology of membrane proteins by solid-state NMR. Acc Chem Res, 2013, 46(9): 2164-2171.
43.	Haarhaus M, Brandenburg V, Kalantar-Zadeh K, et al. Alkaline phosphatase: a novel treatment target for cardiovascular disease in CKD. Nat Rev Nephrol, 2017, 13(7): 429-442.
44.	Jikko A, Harris SE, Chen D, et al. Collagen integrin receptors regulate early osteoblast differentiation induced by BMP-2. J Bone Miner Res, 1999, 14(7): 1075-1083.
45.	Epstein EH Jr, Munderloh NH. Isolation and characterization of CNBr peptides of human (alpha 1(III) )3 collagen and tissue distribution of (alpha 1(I) )2 alpha 2 and (alpha 1(III) )3 collagens. J Biol Chem, 1975, 250(24): 9304-9312.
46.	Jikko A, Harris SE, Chen D, et al. Collagen integrin receptors regulate early osteoblast differentiation induced by BMP-2. J Bone Miner Res, 1999, 14(7): 1075-1083.
47.	Twine NA, Chen L, Pang CN, et al. Identification of differentiation-stage specific markers that define the ex vivo osteoblastic phenotype. Bone, 2014, 67: 23-32.
48.	Franceschi RT, Iyer BS, Cui Y. Effects of ascorbic acid on collagen matrix formation and osteoblast differentiation in murine MC3T3-E1 cells. J Bone Miner Res, 1994, 9(6): 843-854.
49.	Quarles LD, Yohay DA, Lever LW, et al. Distinct proliferative and differentiated stages of murine MC3T3-E1 cells in culture: an in vitro model of osteoblast development. J Bone Miner Res, 1992, 7(6): 683-692.
50.	Mikami Y, Asano M, Honda MJ, et al. Bone morphogenetic protein 2 and dexamethasone synergistically increase alkaline phosphatase levels through JAK/STAT signaling in C3H10T1/2 cells. J Cell Physiol, 2010, 223(1): 123-133.
51.	de Vries S, Albracht SP. Intensity of highly anisotropic low-spin heme EPR signals. Biochim Biophys Acta, 1979, 546(2): 334-340.
52.	Boskey AL, Gadaleta S, Gundberg C, et al. Fourier transform infrared microspectroscopic analysis of bones of osteocalcin-deficient mice provides insight into the function of osteocalcin. Bone, 1998, 23(3): 187-196.
53.	Thurner PJ, Chen CG, Ionova-Martin S, et al. Osteopontin deficiency increases bone fragility but preserves bone mass. Bone, 2010, 46(6): 1564-1573.
54.	Hauschka PV, Carr SA. Calcium-dependent alpha-helical structure in osteocalcin. Biochemistry, 1982, 21(10): 2538-2547.
55.	Rammelt S, Neumann M, Hanisch U, et al. Osteocalcin enhances bone remodeling around hydroxyapatite/collagen composites. J Biomed Mater Res A, 2005, 73(3): 284-294.
56.	Tsao YT, Huang YJ, Wu HH, et al. Osteocalcin Mediates Biomineralization during Osteogenic Maturation in Human Mesenchymal Stromal Cells. Int J Mol Sci, 2017, 18(1): pii: E159.
57.	Ducy P, Desbois C, Boyce B, et al. Increased bone formation in osteocalcin-deficient mice. Nature, 1996, 382(6590): 448-452.
58.	Bodine PV, Komm BS. Evidence that conditionally immortalized human osteoblasts express an osteocalcin receptor. Bone, 1999, 25(5): 535-543.
59.	Giachelli CM, Steitz S. Osteopontin: a versatile regulator of inflammation and biomineralization. Matrix Biol, 2000, 19(7): 615-622.
60.	Rodriguez DE, Thula-Mata T, Toro EJ, et al. Multifunctional role of osteopontin in directing intrafibrillar mineralization of collagen and activation of osteoclasts. Acta Biomater, 2014, 10(1): 494-507.
61.	Kojima H, Uede T, Uemura T. In vitro and in vivo effects of the overexpression of osteopontin on osteoblast differentiation using a recombinant adenoviral vector. J Biochem, 2004, 136(3): 377-386.
62.	Mizuno M, Imai T, Fujisawa R, et al. Bone sialoprotein (BSP) is a crucial factor for the expression of osteoblastic phenotypes of bone marrow cells cultured on type Ⅰ collagen matrix. Calcif Tissue Int, 2000, 66(5): 388-396.
63.	Gordon JA, Tye CE, Sampaio AV, et al. Bone sialoprotein expression enhances osteoblast differentiation and matrix mineralization in vitro. Bone, 2007, 41(3): 462-473.
64.	Malaval L, Wade-Guéye NM, Boudiffa M, et al. Bone sialoprotein plays a functional role in bone formation and osteoclastogenesis. J Exp Med, 2008, 205(5): 1145-1153.
65.	Cooper LF, Yliheikkilä PK, Felton DA, et al. Spatiotemporal assessment of fetal bovine osteoblast culture differentiation indicates a role for BSP in promoting differentiation. J Bone Miner Res, 1998, 13(4): 620-632.
66.	Gordon JA, Tye CE, Sampaio AV, et al. Bone sialoprotein expression enhances osteoblast differentiation and matrix mineralization in vitro. Bone, 2007, 41(3): 462-473.
67.	Hunter GK, Goldberg HA. Nucleation of hydroxyapatite by bone sialoprotein. Proc Natl Acad Sci U S A, 1993, 90(18): 8562-8565.
68.	Meredith JE Jr, Winitz S, Lewis JM, et al. The regulation of growth and intracellular signaling by integrins. Endocr Rev, 1996, 17(3): 207-220.
69.	Giusta MS, Andrade H, Santos AV, et al. Proteomic analysis of human mesenchymal stromal cells derived from adipose tissue undergoing osteoblast differentiation. Cytotherapy, 2010, 12(4): 478-490.
70.	Granéli C, Thorfve A, Ruetschi U, et al. Novel markers of osteogenic and adipogenic differentiation of human bone marrow stromal cells identified using a quantitative proteomics approach. Stem Cell Res, 2014, 12(1): 153-165.
71.	Zhang AX, Yu WH, Ma BF, et al. Proteomic identification of differently expressed proteins responsible for osteoblast differentiation from human mesenchymal stem cells. Mol Cell Biochem, 2007, 304(1-2): 167-179.
72.	William F, Mroczkowski B, Cohen S, et al. Differentiation of HL-60 cells is associated with an increase in the 35-kDa protein lipocortin I. J Cell Physiol, 1988, 137(3): 402-410.
73.	Ye NS, Chen J, Luo GA, et al. Proteomic profiling of rat bone marrow mesenchymal stem cells induced by 5-azacytidine. Stem Cells Dev, 2006, 15(5): 665-676.
74.	周颖, 侯树勋, 陈秉耀, 等. 骨髓间充质干细胞定向诱导成骨分化的蛋白质组学分析. 中国骨肿瘤骨病, 2009, 8(5): 296-299.
75.	Kim JM, Kim J, Kim YH, et al. Comparative secretome analysis of human bone marrow-derived mesenchymal stem cells during osteogenesis. J Cell Physiol, 2013, 228(1): 216-224.
76.	Alves RD, Eijken M, Swagemakers S, et al. Proteomic analysis of human osteoblastic cells: relevant proteins and functional categories for differentiation. J Proteome Res, 2010, 9(9): 4688-4700.
77.	Pan X, Peng L, Yin G. Downregulation of Annexin A1 by short hairpin RNA inhibits the osteogenic differentiation of rat bone marrow-derived mesenchymal stem cells. Int J Mol Med, 2015, 36(2): 406-414.
78.	Kim JS, Lee HK, Kim MR, et al. Differentially expressed proteins of mesenchymal stem cells derived from human cord blood (hUCB) during osteogenic differentiation. Biosci Biotechnol Biochem, 2008, 72(9): 2309-2317.
79.	Baroncelli M, van der Eerden BC, Kan YY, et al. Comparative proteomic profiling of human osteoblast-derived extracellular matrices identifies proteins involved in mesenchymal stromal cell osteogenic differentiation and mineralization. J Cell Physiol, 2018, 233(1): 387-395.

1. Furuya M, Kikuta J, Fujimori S, et al. Direct cell-cell contact between mature osteoblasts and osteoclasts dynamically controls their functions in vivo. Nat Commun, 2018, 9(1): 300.
2. Montagnani A. Bone anabolics in osteoporosis: Actuality and perspectives. World J Orthop, 2014, 5(3): 247-254.
3. Väänänen HK, Laitala-Leinonen T. Osteoclast lineage and function. Arch Biochem Biophys, 2008, 473(2): 132-138.
4. Väänänen HK, Zhao H, Mulari M, et al. The cell biology of osteoclast function. J Cell Sci, 2000, 113(Pt 3): 377-381.
5. Okaji M, Sakai H, Sakai E, et al. The regulation of bone resorption in tooth formation and eruption processes in mouse alveolar crest devoid of cathepsin k. J Pharmacol Sci, 2003, 91(4): 285-294.
6. Garnero P, Borel O, Byrjalsen I, et al. The collagenolytic activity of cathepsin K is unique among mammalian proteinases. J Biol Chem, 1998, 273(48): 32347-32352.
7. Borel O, Gineyts E, Bertholon C, et al. Cathepsin K preferentially solubilizes matured bone matrix. Calcif Tissue Int, 2012, 91(1): 32-39.
8. Gowen M, Lazner F, Dodds R, et al. Cathepsin K knockout mice develop osteopetrosis due to a deficit in matrix degradation but not demineralization. J Bone Miner Res, 1999, 14(10): 1654-1663.
9. Saftig P, Hunziker E, Wehmeyer O, et al. Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc Natl Acad Sci U S A, 1998, 95(23): 13453-13458.
10. Drake MT, Clarke BL, Oursler MJ, et al. Cathepsin K inhibitors for osteoporosis: biology, potential clinical utility, and lessons learned. Endocr Rev, 2017, 38(4): 325-350.
11. Nesbitt SA, Horton MA. Trafficking of matrix collagens through bone-resorbing osteoclasts. Science, 1997, 276(5310): 266-269.
12. Salo J, Lehenkari P, Mulari M, et al. Removal of osteoclast bone resorption products by transcytosis. Science, 1997, 276(5310): 270-273.
13. Vääräniemi J, Halleen JM, Kaarlonen K, et al. Intracellular machinery for matrix degradation in bone-resorbing osteoclasts. J Bone Miner Res, 2004, 19(9): 1432-1440.
14. Ljusberg J, Wang Y, Lång P, et al. Proteolytic excision of a repressive loop domain in tartrate-resistant acid phosphatase by cathepsin K in osteoclasts. J Biol Chem, 2005, 280(31): 28370-28381.
15. Halleen JM, Räisänen S, Salo JJ, et al. Intracellular fragmentation of bone resorption products by reactive oxygen species generated by osteoclastic tartrate-resistant acid phosphatase. J Biol Chem, 1999, 274(33): 22907-22910.
16. Alatalo SL, Halleen JM, Hentunen TA, et al. Rapid screening method for osteoclast differentiation in vitro that measures tartrate-resistant acid phosphatase 5b activity secreted into the culture medium. Clin Chem, 2000, 46(11): 1751-1754.
17. Rissanen JP, Suominen MI, Peng Z, et al. Secreted tartrate-resistant acid phosphatase 5b is a marker of osteoclast number in human osteoclast cultures and the rat ovariectomy model. Calcif Tissue Int, 2008, 82(2): 108-115.
18. Wu Y, Lee JW, Uy L, et al. Tartrate-resistant acid phosphatase (TRACP 5b): a biomarker of bone resorption rate in support of drug development: modification, validation and application of the BoneTRAP kit assay. J Pharm Biomed Anal, 2009, 49(5): 1203-1212.
19. Hill PA, Murphy G, Docherty AJ, et al. The effects of selective inhibitors of matrix metalloproteinases (MMPs) on bone resorption and the identification of MMPs and TIMP-1 in isolated osteoclasts. J Cell Sci, 1994, 107(Pt 11): 3055-3064.
20. Spessotto P, Rossi FM, Degan M, et al. Hyaluronan-CD44 interaction hampers migration of osteoclast-like cells by down-regulating MMP-9. J Cell Biol, 2002, 158(6): 1133-1144.
21. Samanna V, Ma T, Mak TW, et al. Actin polymerization modulates CD44 surface expression, MMP-9 activation, and osteoclast function. J Cell Physiol, 2007, 213(3): 710-720.
22. Engsig MT, Chen QJ, Vu TH, et al. Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones. J Cell Biol, 2000, 151(4): 879-889.
23. Dougall WC, Glaccum M, Charrier K, et al. RANK is essential for osteoclast and lymph node development. Genes Dev, 1999, 13(18): 2412-2424.
24. Li J, Sarosi I, Yan XQ, et al. RANK is the intrinsic hematopoietic cell surface receptor that controls osteoclastogenesis and regulation of bone mass and calcium metabolism. Proc Natl Acad Sci U S A, 2000, 97(4): 1566-1571.
25. Boyle WJ, Simonet WS, Lacey DL. Osteoclast differentiation and activation. Nature, 2003, 423(6937): 337-342.
26. Mizuno A, Amizuka N, Irie K, et al. Severe osteoporosis in mice lacking osteoclastogenesis inhibitory factor/osteoprotegerin. Biochem Biophys Res Commun, 1998, 247(3): 610-615.
27. Bucay N, Sarosi I, Dunstan CR, et al. osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev, 1998, 12(9): 1260-1268.
28. Song R, Gu J, Liu X, et al. Inhibition of osteoclast bone resorption activity through osteoprotegerin-induced damage of the sealing zone. Int J Mol Med, 2014, 34(3): 856-862.
29. Jaffe AB, Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol, 2005, 21: 247-269.
30. Palmqvist P, Persson E, Conaway HH, et al. IL-6, leukemia inhibitory factor, and oncostatin M stimulate bone resorption and regulate the expression of receptor activator of NF-kappa B ligand, osteoprotegerin, and receptor activator of NF-kappa B in mouse calvariae. J Immunol, 2002, 169(6): 3353-3362.
31. Hattersley G, Chambers TJ. Calcitonin receptors as markers for osteoclastic differentiation: correlation between generation of bone-resorptive cells and cells that express calcitonin receptors in mouse bone marrow cultures. Endocrinology, 1989, 125(3): 1606-1612.
32. Kulterer B, Friedl G, Jandrositz A, et al. Gene expression profiling of human mesenchymal stem cells derived from bone marrow during expansion and osteoblast differentiation. BMC Genomics, 2007, 8: 70.
33. Huang Z, Nelson ER, Smith RL, et al. The sequential expression profiles of growth factors from osteoprogenitors [correction of osteroprogenitors] to osteoblasts in vitro. Tissue Eng, 2007, 13(9): 2311-2320.
34. Viguet-Carrin S, Garnero P, Delmas PD. The role of collagen in bone strength. Osteoporos Int, 2006, 17(3): 319-336.
35. Staines KA, MacRae VE, Farquharson C. The importance of the SIBLING family of proteins on skeletal mineralisation and bone remodelling. J Endocrinol, 2012, 214(3): 241-255.
36. Neve A, Corrado A, Cantatore FP. Osteocalcin: skeletal and extra-skeletal effects. J Cell Physiol, 2013, 228(6): 1149-1153.
37. Fleisher GA, Eickelberg ES, Elveback LR. Alkaline phosphatase activity in the plasma of children and adolescents. Clin Chem, 1977, 23(3): 469-472.
38. Canalis E. Effect of hormones and growth factors on alkaline phosphatase activity and collagen synthesis in cultured rat calvariae. Metabolism, 1983, 32(1): 14-20.
39. Marie PJ, Travers R. Continuous infusion of 1,25-dihydroxyvitamin D3 stimulates bone turnover in the normal young mouse. Calcif Tissue Int, 1983, 35(4-5): 418-425.
40. Farley JR, Baylink DJ. Skeletal alkaline phosphatase activity as a bone formation index in vitro. Metabolism, 1986, 35(6): 563-571.
41. Fedde KN, Lane CC, Whyte MP. Alkaline phosphatase is an ectoenzyme that acts on micromolar concentrations of natural substrates at physiologic pH in human osteosarcoma (SAOS-2) cells. Arch Biochem Biophys, 1988, 264(2): 400-409.
42. Ullrich SJ, Glaubitz C. Perspectives in enzymology of membrane proteins by solid-state NMR. Acc Chem Res, 2013, 46(9): 2164-2171.
43. Haarhaus M, Brandenburg V, Kalantar-Zadeh K, et al. Alkaline phosphatase: a novel treatment target for cardiovascular disease in CKD. Nat Rev Nephrol, 2017, 13(7): 429-442.
44. Jikko A, Harris SE, Chen D, et al. Collagen integrin receptors regulate early osteoblast differentiation induced by BMP-2. J Bone Miner Res, 1999, 14(7): 1075-1083.
45. Epstein EH Jr, Munderloh NH. Isolation and characterization of CNBr peptides of human (alpha 1(III) )3 collagen and tissue distribution of (alpha 1(I) )2 alpha 2 and (alpha 1(III) )3 collagens. J Biol Chem, 1975, 250(24): 9304-9312.
46. Jikko A, Harris SE, Chen D, et al. Collagen integrin receptors regulate early osteoblast differentiation induced by BMP-2. J Bone Miner Res, 1999, 14(7): 1075-1083.
47. Twine NA, Chen L, Pang CN, et al. Identification of differentiation-stage specific markers that define the ex vivo osteoblastic phenotype. Bone, 2014, 67: 23-32.
48. Franceschi RT, Iyer BS, Cui Y. Effects of ascorbic acid on collagen matrix formation and osteoblast differentiation in murine MC3T3-E1 cells. J Bone Miner Res, 1994, 9(6): 843-854.
49. Quarles LD, Yohay DA, Lever LW, et al. Distinct proliferative and differentiated stages of murine MC3T3-E1 cells in culture: an in vitro model of osteoblast development. J Bone Miner Res, 1992, 7(6): 683-692.
50. Mikami Y, Asano M, Honda MJ, et al. Bone morphogenetic protein 2 and dexamethasone synergistically increase alkaline phosphatase levels through JAK/STAT signaling in C3H10T1/2 cells. J Cell Physiol, 2010, 223(1): 123-133.
51. de Vries S, Albracht SP. Intensity of highly anisotropic low-spin heme EPR signals. Biochim Biophys Acta, 1979, 546(2): 334-340.
52. Boskey AL, Gadaleta S, Gundberg C, et al. Fourier transform infrared microspectroscopic analysis of bones of osteocalcin-deficient mice provides insight into the function of osteocalcin. Bone, 1998, 23(3): 187-196.
53. Thurner PJ, Chen CG, Ionova-Martin S, et al. Osteopontin deficiency increases bone fragility but preserves bone mass. Bone, 2010, 46(6): 1564-1573.
54. Hauschka PV, Carr SA. Calcium-dependent alpha-helical structure in osteocalcin. Biochemistry, 1982, 21(10): 2538-2547.
55. Rammelt S, Neumann M, Hanisch U, et al. Osteocalcin enhances bone remodeling around hydroxyapatite/collagen composites. J Biomed Mater Res A, 2005, 73(3): 284-294.
56. Tsao YT, Huang YJ, Wu HH, et al. Osteocalcin Mediates Biomineralization during Osteogenic Maturation in Human Mesenchymal Stromal Cells. Int J Mol Sci, 2017, 18(1): pii: E159.
57. Ducy P, Desbois C, Boyce B, et al. Increased bone formation in osteocalcin-deficient mice. Nature, 1996, 382(6590): 448-452.
58. Bodine PV, Komm BS. Evidence that conditionally immortalized human osteoblasts express an osteocalcin receptor. Bone, 1999, 25(5): 535-543.
59. Giachelli CM, Steitz S. Osteopontin: a versatile regulator of inflammation and biomineralization. Matrix Biol, 2000, 19(7): 615-622.
60. Rodriguez DE, Thula-Mata T, Toro EJ, et al. Multifunctional role of osteopontin in directing intrafibrillar mineralization of collagen and activation of osteoclasts. Acta Biomater, 2014, 10(1): 494-507.
61. Kojima H, Uede T, Uemura T. In vitro and in vivo effects of the overexpression of osteopontin on osteoblast differentiation using a recombinant adenoviral vector. J Biochem, 2004, 136(3): 377-386.
62. Mizuno M, Imai T, Fujisawa R, et al. Bone sialoprotein (BSP) is a crucial factor for the expression of osteoblastic phenotypes of bone marrow cells cultured on type Ⅰ collagen matrix. Calcif Tissue Int, 2000, 66(5): 388-396.
63. Gordon JA, Tye CE, Sampaio AV, et al. Bone sialoprotein expression enhances osteoblast differentiation and matrix mineralization in vitro. Bone, 2007, 41(3): 462-473.
64. Malaval L, Wade-Guéye NM, Boudiffa M, et al. Bone sialoprotein plays a functional role in bone formation and osteoclastogenesis. J Exp Med, 2008, 205(5): 1145-1153.
65. Cooper LF, Yliheikkilä PK, Felton DA, et al. Spatiotemporal assessment of fetal bovine osteoblast culture differentiation indicates a role for BSP in promoting differentiation. J Bone Miner Res, 1998, 13(4): 620-632.
66. Gordon JA, Tye CE, Sampaio AV, et al. Bone sialoprotein expression enhances osteoblast differentiation and matrix mineralization in vitro. Bone, 2007, 41(3): 462-473.
67. Hunter GK, Goldberg HA. Nucleation of hydroxyapatite by bone sialoprotein. Proc Natl Acad Sci U S A, 1993, 90(18): 8562-8565.
68. Meredith JE Jr, Winitz S, Lewis JM, et al. The regulation of growth and intracellular signaling by integrins. Endocr Rev, 1996, 17(3): 207-220.
69. Giusta MS, Andrade H, Santos AV, et al. Proteomic analysis of human mesenchymal stromal cells derived from adipose tissue undergoing osteoblast differentiation. Cytotherapy, 2010, 12(4): 478-490.
70. Granéli C, Thorfve A, Ruetschi U, et al. Novel markers of osteogenic and adipogenic differentiation of human bone marrow stromal cells identified using a quantitative proteomics approach. Stem Cell Res, 2014, 12(1): 153-165.
71. Zhang AX, Yu WH, Ma BF, et al. Proteomic identification of differently expressed proteins responsible for osteoblast differentiation from human mesenchymal stem cells. Mol Cell Biochem, 2007, 304(1-2): 167-179.
72. William F, Mroczkowski B, Cohen S, et al. Differentiation of HL-60 cells is associated with an increase in the 35-kDa protein lipocortin I. J Cell Physiol, 1988, 137(3): 402-410.
73. Ye NS, Chen J, Luo GA, et al. Proteomic profiling of rat bone marrow mesenchymal stem cells induced by 5-azacytidine. Stem Cells Dev, 2006, 15(5): 665-676.
74. 周颖, 侯树勋, 陈秉耀, 等. 骨髓间充质干细胞定向诱导成骨分化的蛋白质组学分析. 中国骨肿瘤骨病, 2009, 8(5): 296-299.
75. Kim JM, Kim J, Kim YH, et al. Comparative secretome analysis of human bone marrow-derived mesenchymal stem cells during osteogenesis. J Cell Physiol, 2013, 228(1): 216-224.
76. Alves RD, Eijken M, Swagemakers S, et al. Proteomic analysis of human osteoblastic cells: relevant proteins and functional categories for differentiation. J Proteome Res, 2010, 9(9): 4688-4700.
77. Pan X, Peng L, Yin G. Downregulation of Annexin A1 by short hairpin RNA inhibits the osteogenic differentiation of rat bone marrow-derived mesenchymal stem cells. Int J Mol Med, 2015, 36(2): 406-414.
78. Kim JS, Lee HK, Kim MR, et al. Differentially expressed proteins of mesenchymal stem cells derived from human cord blood (hUCB) during osteogenic differentiation. Biosci Biotechnol Biochem, 2008, 72(9): 2309-2317.
79. Baroncelli M, van der Eerden BC, Kan YY, et al. Comparative proteomic profiling of human osteoblast-derived extracellular matrices identifies proteins involved in mesenchymal stromal cell osteogenic differentiation and mineralization. J Cell Physiol, 2018, 233(1): 387-395.

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