RESEARCH PROGRESS OF OSTEOCLASTS FUNCTION BEYOND BONE RESORPTION_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

WUChaorui ¹ , ZHANGJie ² ,  TIANJing ²

1. The Second Medical College, Southern Medical University, Guangzhou Guangdong, 510280, P. R. China;
2. Department of Orthopedics, Zhujiang Hospital Affiliated to Southern Medical University, Guangzhou Guangdong, 510280, P. R. China;

Corresponding author：

TIANJing, Email: tianjing_ortho@163.com

Keywords：

Osteoclasts; Osteoblasts; Hematopoietic stem cells; Neovascularization

DOI：

10.7507/1002-1892.20150221

Video：

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Objective To review the osteoclasts (OC) function beyond bone resorption. Methods The related literature on OC function beyond bone resorption was reviewed, analyzed, and summarized. Results OC control the bone formation through releasing of matrix-derived growth factors, bidirectional cell-to-cell signals, and secreting OC-coupling factors, and play an important role in the niche formation, hematopoietic stem cells mobilization, and maintenance of its quantity and function;besides, OCs also regulate angiogenesis. Conclusion These discoveries greatly enrich the current knowledge of OC function and open up an all-new research domain. However, the exact regulatory mechanism of OC affecting the hematopoiesis is still lack in-depth understood. Additionally, it remains to be elucidated how OC-coupling factors act on osteoblast lineage differentiation and how OC-induced angiogenesis participates in physiological and pathological processes. Unclosing the underlying mechanisms will facilitate providing scientific therapeutic strategies for treatment of many OC-related diseases.

Citation： WUChaorui, ZHANGJie, TIANJing. RESEARCH PROGRESS OF OSTEOCLASTS FUNCTION BEYOND BONE RESORPTION. Chinese Journal of Reparative and Reconstructive Surgery, 2015, 29(8): 1038-1042. doi: 10.7507/1002-1892.20150221 Copy

1.	颜艳,林欣,代晓华,等.破骨细胞形成和功能调节的研究进展.中国修复重建外科杂志,2014,28(11):1435-1440.
2.	Ota K,Quint P,Weivoda MM,et al.Transforming growth factor beta 1 induces CXCL16 and leukemia inhibitory factor expression in osteoclasts to modulate migration of osteoblast progenitors.Bone,2013,57(1):68-75.
3.	Ghosh D,Lili L,McGrail DJ,et al.Integral role of platelet-derived growth factor in mediating transforming growth factor-β1-dependent mesenchymal stem cell stiffening.Stem Cells Dev,2013,23(3):245-261.
4.	Xian L,Wu X,Pang L,et al.Matrix IGF-1 maintains bone mass by activation of mTOR in mesenchymal stem cells.Nat Med,2012,18(7):1095-1101.
5.	Zhao C,Irie N,Takada Y,et al.Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis.Cell Metab,2006,4(2):111-121.
6.	Ballanti P,Minisola S,Pacitti M,et al.Tartrate-resistant acid phosphate activity as osteoclastic marker:sensitivity of cytochemical assessment and serum assay in comparison with standardized osteoclast histomorphometry.Osteoporos Int,1997,7(1):39-43.
7.	Hayaman AR,Cox TM.Tartrate-resistant acid phosphatase knockout mice.J Bone Miner Res,2003,18(10):1905-1907.
8.	Del Fattore A,Fornari R,Van Wesnbeeck L,et al.A new heterozygous mutation (R714C) of the osteopetrosis gene,pleckstrin homolog domain containing family M (with run domain) member 1(PLEKHM1),impairs vesicular acidification and increases TRACP secretion in osteoclasts.J Bone Miner Res,2008,23(3):380-391.
9.	Pederson L,Ruan M,Westendorf JJ,et al.Regulation of bone formation by osteoclasts involves Wnt/BMP signaling and the chemokine sphingosine-1-phosphate.Proc Natl Acad Sci U S A,2008,105(52):20764-20769.
10.	Lotinun S,Kiviranta R,Matsubara T,et al.Osteoclast-specific cathepsin K deletion stimulates S1P-dependent bone formation.J Clin Invest,2013,123(2):666-681.
11.	Garimella R,Tague SE,Zhang J,et al.Expression and synthesis of bone morphogenetic proteins by osteoclasts:a possible path to anabolic bone remodeling.J Histochem Cytochem,2008,56(6):569-577.
12.	Takeshita S,Fumoto T,Matsuoka K,et al.Osteoclast-secreted CTHRC1 in the coupling of bone resorption to formation.J Clin Invest,2013,123(9):3914-3924.
13.	Chen HT,Tsou HK,Chang CH,et al.Hepatocyte growth factor increases osteopontin expression in human osteoblasts through PI3K,Akt,c-Src,and AP-1 signaling pathway.PLoS One,2012,7(6):e38378.
14.	Grano M,Galimi F,Zambonin G,et al.Hepatocyte growth factor is a coupling factor for osteoclasts and osteoblasts in vitro.Proc Natl Acad Sci U S A,1996,93(15):7644-7648.
15.	Kubota K,Sakikawa C,Katsumata M,et al.Platelet-derived growth factor BB secreted from osteoclasts acts as an osteoblastogenesis inhibitory factor.J Bone Miner Res,2002,17(2):257-265.
16.	Del Fattore A,Peruzzi B,Rucci N,et al.Clinical,genetic,and cellular analysis of 49 osteopetrotic patients:implications for diagnosis and treatment.J Med Genet,2006,43(4):315-325.
17.	Guerrini MM,Sobacchi C,Cassani B,et al.Human osteoclast-poor osteopetrosis with hypogammaglobulinemia due to TNFRSF11A (RANK) mutations.Am J Hum Genet,2008,83(1):64-76.
18.	Del Fattore A,Peruzzi B,Rucci N,et al.Clinical,genetic,and cellular analysis of 49 osteopetrotic patients:implications for diagnosis and treatment.J Med Genet,2006,43(4):315-325.
19.	Kook S,Cho J,Lee SB,et al.The nucleotide sugar UDP-glucose mobilizes long-term repopulating primitive hematopoietic cells.J Clin Invest,2013,123(8):3420-3435.
20.	Miyamoto K,Yoshida S,Kawasumi M,et al.Osteoclasts are dispensable for hematopoietic stem cell maintenance and mobilization.J Exp Med,2011,208(11):2175-2181.
21.	Flores C,Moscatelli I,Thudium CS,et al.Osteoclasts are not crucial for hematopoietic stem cell maintenance in adult mice.Haematologica,2013,98(12):1848-1855.
22.	Tagaya H,Kunisada T,Yamazaki H,et al.Intramedullary and extramedullary B lymphopoiesis in osteopetrotic mice.Blood,2000,95(11):3363-3370.
23.	Mansour A,Abou-Ezzi G,Sitnicka E,et al.Osteoclasts promote the formation of hematopoietic stem cell niches in the bone marrow.J Exp Med,2012,209(3):537-549.
24.	Coskun S,Hirschi KK.Establishment and regulation of the HSC niche:Roles of osteoblastic and vascular compartments.Birth Defects Res C Embryo Today,2010,90(4):229-242.
25.	Porter RL,Calvi LM.Communications between bone cells and hematopoietic stem cells.Arch Biochem Biophys,2008,473(2):193-200.
26.	Zhang J,Niu C,Ye L,et al.Identification of the haematopoietic stem cell niche and control of the niche size.Nature,2003,425(6960):836-841.
27.	Lymperi S,Horwood N,Marley S,et al.Strontium can increase some osteoblasts without increasing hematopoietic stem cells.Blood,2008,111(3):1173-1181.
28.	Lymperi S,Ersek A,Ferraro F,et al.Inhibition of osteoclast function reduces hematopoietic stem cell numbers in vivo.Blood,2011,117(5):1540-1549.
29.	Shivtiel S,Kollet O,Lapid K,et al.CD45 regulates retention,motility,and numbers of hematopoietic progenitors,and affects osteoclast remodeling of metaphyseal trabecules.J Exp Med,2008,205(10):2381-2395.
30.	Adams GB,Chabner KT,Alley IR,et al.Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor.Nature,2006,439(7076):599-603.
31.	Winkler I,Pettit A,Raggatt L,et al.Hematopoietic stem cell mobilizing agents G-CSF,cyclophosphamide or AMD3100 have distinct mechanisms of action on bone marrow HSC niches and bone formation.Leukemia,2012,26(7):1594-1601.
32.	Takamatsu Y,Simmons PJ,Moore RJ,et al.Osteoclast-mediated bone resorption is stimulated during short-term administration of granulocyte colony-stimulating factor but is not responsible for hematopoietic progenitor cell mobilization.Blood,1998,92(9):3465-3473.
33.	Kollet O,Dar A,Shivtiel S,et al.Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells.Nat Med,2006,12(6):657-664.
34.	Heissig B,Hattori K,Dias S,et al.Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand.Cell,2002,109(5):625-637.
35.	Wada T,Nakashima T,Hiroshi N,et al.RANKL-RANK signaling in osteoclastogenesis and bone disease.Trends Mol Med,2006,12(1):17-25.
36.	Liang X,Xu F,Li X,et al.VEGF signal system:the application of antiangiogenesis.Curr Med Chem,2014,21(7):894-910.
37.	Trebec-Reynolds DP,Voronov I,Heersche JN,et al.VEGF-A expression in osteoclasts is regulated by NF-kappaB induction of HIF-1alpha.J Cell Biochem,2010,110(2):343-351.
38.	Yeh LC,Lee JC.Osteogenic protein-1 increases gene expression of vascular endothelial growth factor in primary cultures of fetal rat calvaria cells.Mol Cell Endocrinol,1999,153(1):113-124.
39.	Yi T,Lee HL,Cha JH,et al.Epidermal growth factor receptor regulates osteoclast differentiation and survival through cross-talking with RANK signaling.J Cell Physiol,2008,217(2):409-422.
40.	Xie H,Cui Z,Wang L,et al.PDGF-BB secreted by preosteoclasts induces angiogenesis during coupling with osteogenesis.Nat Med,2014,20(11):1270-1278.
41.	Kusumbe AP,Adams RH.Osteoclast progenitors promote bone vascularization and osteogenesis.Nat Med,2014,20(11):1238-1240.
42.	Saharinen J,Hyytiäinen M,Taipale J,et al.Latent transforming growth factor-beta binding proteins (LTBPs)-structural extracellular matrix proteins for targeting TGF-beta action.Cytokine Growth Factor Rev,1999,10(2):99-117.
43.	Shin JH,Shim JW,Kim DS,et al.TGF-beta effects on airway smooth muscle cell proliferation,VEGF release and signal transduction pathways.Respirology,2009,14(3):347-353.
44.	Dallas SL,Rosser JL,Mundy GR,et al.Proteolysis of latent transforming growth factor-beta (TGF-beta)-binding protein-1 by osteoclasts.A cellular mechanism for release of TGF-beta from bone matrix.J Biol Chem,2002,277(24):21352-21360.
45.	Saijo M,Kitazawa R,Nakajima M,et al.Heparanase mRNA expression during fracture repair in mice.Histochem Cell Biol,2003,120(6):493-503.
46.	Collin-Osdoby P,Rothe L,Bekker S,et al.Basic fibroblast growth factor stimulates osteoclast recruitment,development,and bone pit resorption in association with angiogenesis in vivo on the chick chorioallantoic membrane and activates isolated avian osteoclast resorption in vitro.J Bone Miner Res,2002,17(10):1859-1871.
47.	Cackowski FC,Anderson JL,Patrene KD,et al.Osteoclasts are important for bone angiogenesis.Blood,2010,115(1):140-149.

1. 颜艳,林欣,代晓华,等.破骨细胞形成和功能调节的研究进展.中国修复重建外科杂志,2014,28(11):1435-1440.
2. Ota K,Quint P,Weivoda MM,et al.Transforming growth factor beta 1 induces CXCL16 and leukemia inhibitory factor expression in osteoclasts to modulate migration of osteoblast progenitors.Bone,2013,57(1):68-75.
3. Ghosh D,Lili L,McGrail DJ,et al.Integral role of platelet-derived growth factor in mediating transforming growth factor-β1-dependent mesenchymal stem cell stiffening.Stem Cells Dev,2013,23(3):245-261.
4. Xian L,Wu X,Pang L,et al.Matrix IGF-1 maintains bone mass by activation of mTOR in mesenchymal stem cells.Nat Med,2012,18(7):1095-1101.
5. Zhao C,Irie N,Takada Y,et al.Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis.Cell Metab,2006,4(2):111-121.
6. Ballanti P,Minisola S,Pacitti M,et al.Tartrate-resistant acid phosphate activity as osteoclastic marker:sensitivity of cytochemical assessment and serum assay in comparison with standardized osteoclast histomorphometry.Osteoporos Int,1997,7(1):39-43.
7. Hayaman AR,Cox TM.Tartrate-resistant acid phosphatase knockout mice.J Bone Miner Res,2003,18(10):1905-1907.
8. Del Fattore A,Fornari R,Van Wesnbeeck L,et al.A new heterozygous mutation (R714C) of the osteopetrosis gene,pleckstrin homolog domain containing family M (with run domain) member 1(PLEKHM1),impairs vesicular acidification and increases TRACP secretion in osteoclasts.J Bone Miner Res,2008,23(3):380-391.
9. Pederson L,Ruan M,Westendorf JJ,et al.Regulation of bone formation by osteoclasts involves Wnt/BMP signaling and the chemokine sphingosine-1-phosphate.Proc Natl Acad Sci U S A,2008,105(52):20764-20769.
10. Lotinun S,Kiviranta R,Matsubara T,et al.Osteoclast-specific cathepsin K deletion stimulates S1P-dependent bone formation.J Clin Invest,2013,123(2):666-681.
11. Garimella R,Tague SE,Zhang J,et al.Expression and synthesis of bone morphogenetic proteins by osteoclasts:a possible path to anabolic bone remodeling.J Histochem Cytochem,2008,56(6):569-577.
12. Takeshita S,Fumoto T,Matsuoka K,et al.Osteoclast-secreted CTHRC1 in the coupling of bone resorption to formation.J Clin Invest,2013,123(9):3914-3924.
13. Chen HT,Tsou HK,Chang CH,et al.Hepatocyte growth factor increases osteopontin expression in human osteoblasts through PI3K,Akt,c-Src,and AP-1 signaling pathway.PLoS One,2012,7(6):e38378.
14. Grano M,Galimi F,Zambonin G,et al.Hepatocyte growth factor is a coupling factor for osteoclasts and osteoblasts in vitro.Proc Natl Acad Sci U S A,1996,93(15):7644-7648.
15. Kubota K,Sakikawa C,Katsumata M,et al.Platelet-derived growth factor BB secreted from osteoclasts acts as an osteoblastogenesis inhibitory factor.J Bone Miner Res,2002,17(2):257-265.
16. Del Fattore A,Peruzzi B,Rucci N,et al.Clinical,genetic,and cellular analysis of 49 osteopetrotic patients:implications for diagnosis and treatment.J Med Genet,2006,43(4):315-325.
17. Guerrini MM,Sobacchi C,Cassani B,et al.Human osteoclast-poor osteopetrosis with hypogammaglobulinemia due to TNFRSF11A (RANK) mutations.Am J Hum Genet,2008,83(1):64-76.
18. Del Fattore A,Peruzzi B,Rucci N,et al.Clinical,genetic,and cellular analysis of 49 osteopetrotic patients:implications for diagnosis and treatment.J Med Genet,2006,43(4):315-325.
19. Kook S,Cho J,Lee SB,et al.The nucleotide sugar UDP-glucose mobilizes long-term repopulating primitive hematopoietic cells.J Clin Invest,2013,123(8):3420-3435.
20. Miyamoto K,Yoshida S,Kawasumi M,et al.Osteoclasts are dispensable for hematopoietic stem cell maintenance and mobilization.J Exp Med,2011,208(11):2175-2181.
21. Flores C,Moscatelli I,Thudium CS,et al.Osteoclasts are not crucial for hematopoietic stem cell maintenance in adult mice.Haematologica,2013,98(12):1848-1855.
22. Tagaya H,Kunisada T,Yamazaki H,et al.Intramedullary and extramedullary B lymphopoiesis in osteopetrotic mice.Blood,2000,95(11):3363-3370.
23. Mansour A,Abou-Ezzi G,Sitnicka E,et al.Osteoclasts promote the formation of hematopoietic stem cell niches in the bone marrow.J Exp Med,2012,209(3):537-549.
24. Coskun S,Hirschi KK.Establishment and regulation of the HSC niche:Roles of osteoblastic and vascular compartments.Birth Defects Res C Embryo Today,2010,90(4):229-242.
25. Porter RL,Calvi LM.Communications between bone cells and hematopoietic stem cells.Arch Biochem Biophys,2008,473(2):193-200.
26. Zhang J,Niu C,Ye L,et al.Identification of the haematopoietic stem cell niche and control of the niche size.Nature,2003,425(6960):836-841.
27. Lymperi S,Horwood N,Marley S,et al.Strontium can increase some osteoblasts without increasing hematopoietic stem cells.Blood,2008,111(3):1173-1181.
28. Lymperi S,Ersek A,Ferraro F,et al.Inhibition of osteoclast function reduces hematopoietic stem cell numbers in vivo.Blood,2011,117(5):1540-1549.
29. Shivtiel S,Kollet O,Lapid K,et al.CD45 regulates retention,motility,and numbers of hematopoietic progenitors,and affects osteoclast remodeling of metaphyseal trabecules.J Exp Med,2008,205(10):2381-2395.
30. Adams GB,Chabner KT,Alley IR,et al.Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor.Nature,2006,439(7076):599-603.
31. Winkler I,Pettit A,Raggatt L,et al.Hematopoietic stem cell mobilizing agents G-CSF,cyclophosphamide or AMD3100 have distinct mechanisms of action on bone marrow HSC niches and bone formation.Leukemia,2012,26(7):1594-1601.
32. Takamatsu Y,Simmons PJ,Moore RJ,et al.Osteoclast-mediated bone resorption is stimulated during short-term administration of granulocyte colony-stimulating factor but is not responsible for hematopoietic progenitor cell mobilization.Blood,1998,92(9):3465-3473.
33. Kollet O,Dar A,Shivtiel S,et al.Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells.Nat Med,2006,12(6):657-664.
34. Heissig B,Hattori K,Dias S,et al.Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand.Cell,2002,109(5):625-637.
35. Wada T,Nakashima T,Hiroshi N,et al.RANKL-RANK signaling in osteoclastogenesis and bone disease.Trends Mol Med,2006,12(1):17-25.
36. Liang X,Xu F,Li X,et al.VEGF signal system:the application of antiangiogenesis.Curr Med Chem,2014,21(7):894-910.
37. Trebec-Reynolds DP,Voronov I,Heersche JN,et al.VEGF-A expression in osteoclasts is regulated by NF-kappaB induction of HIF-1alpha.J Cell Biochem,2010,110(2):343-351.
38. Yeh LC,Lee JC.Osteogenic protein-1 increases gene expression of vascular endothelial growth factor in primary cultures of fetal rat calvaria cells.Mol Cell Endocrinol,1999,153(1):113-124.
39. Yi T,Lee HL,Cha JH,et al.Epidermal growth factor receptor regulates osteoclast differentiation and survival through cross-talking with RANK signaling.J Cell Physiol,2008,217(2):409-422.
40. Xie H,Cui Z,Wang L,et al.PDGF-BB secreted by preosteoclasts induces angiogenesis during coupling with osteogenesis.Nat Med,2014,20(11):1270-1278.
41. Kusumbe AP,Adams RH.Osteoclast progenitors promote bone vascularization and osteogenesis.Nat Med,2014,20(11):1238-1240.
42. Saharinen J,Hyytiäinen M,Taipale J,et al.Latent transforming growth factor-beta binding proteins (LTBPs)-structural extracellular matrix proteins for targeting TGF-beta action.Cytokine Growth Factor Rev,1999,10(2):99-117.
43. Shin JH,Shim JW,Kim DS,et al.TGF-beta effects on airway smooth muscle cell proliferation,VEGF release and signal transduction pathways.Respirology,2009,14(3):347-353.
44. Dallas SL,Rosser JL,Mundy GR,et al.Proteolysis of latent transforming growth factor-beta (TGF-beta)-binding protein-1 by osteoclasts.A cellular mechanism for release of TGF-beta from bone matrix.J Biol Chem,2002,277(24):21352-21360.
45. Saijo M,Kitazawa R,Nakajima M,et al.Heparanase mRNA expression during fracture repair in mice.Histochem Cell Biol,2003,120(6):493-503.
46. Collin-Osdoby P,Rothe L,Bekker S,et al.Basic fibroblast growth factor stimulates osteoclast recruitment,development,and bone pit resorption in association with angiogenesis in vivo on the chick chorioallantoic membrane and activates isolated avian osteoclast resorption in vitro.J Bone Miner Res,2002,17(10):1859-1871.
47. Cackowski FC,Anderson JL,Patrene KD,et al.Osteoclasts are important for bone angiogenesis.Blood,2010,115(1):140-149.

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RESEARCH PROGRESS OF OSTEOCLASTS FUNCTION BEYOND BONE RESORPTION

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