RESEARCH PROGRESS OF PATHOLOGY OF ENDOCHONDRAL OSSIFICATION IN OSTEOARTHRITIS_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

XIAOZhifeng ^1,2 ,  LINDingkun ³

1. The Second Clinical Medical College of Guangzhou University of Chinese Medicine, Guangzhou Guangdong, 510120, P. R. China;
2. Laboratory Affiliated to National Key Discipline of Orthopaedic and Traumatology of Chinese Medicine, Guangzhou University of Chinese Medicine, Guangzhou Guangdong, 510120, P. R. China;
3. Department of Orthopaedic Surgery, Guangdong Province Hospital of Traditional Chinese Medicine, Guangzhou Guangdong, 510120, P. R. China;

Corresponding author：

LINDingkun, Email: lindingkun@126.com

Keywords：

Osteoarthritis; Endochondral ossification; Growth plate; Chondrocyte hypertrophy; Bone-cartilage remodeling

DOI：

10.7507/1002-1892.20160320

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the research progress of pathological manifestations and mechanism of endochondral ossification in osteoarthritis (OA). Methods The literature about endochondral ossification, bone-cartilage remodeling in OA, and joints development was reviewed, analyzed, and summarized. Results Chondrocyte hypertrophy and apoptosis, vascular invasion, replication of the tidemark, thickening calcified cartilage, and thinning superficial cartilage are the characteristics of cartilage degeneration in OA. Articular cartilage and growth plate are similar in structure, and cartilage degeneration in OA is similar to a process of endochondral ossification of the growth plate. Conclusion Loss of stability characterization from resting metabolic balance to a high conversion state of temporary cartilage in stimulation of abnormal mechanical stresses and cytokines would subsequently contributed to continual calcification and remodeling of articular cartilage, which may be the key link of the initiation and development of OA.

Citation： XIAOZhifeng, LINDingkun. RESEARCH PROGRESS OF PATHOLOGY OF ENDOCHONDRAL OSSIFICATION IN OSTEOARTHRITIS. Chinese Journal of Reparative and Reconstructive Surgery, 2016, 30(12): 1556-1561. doi: 10.7507/1002-1892.20160320 Copy

1.	Macias-Hernandez S. The disability associated with osteoarthritis. Rev Med Inst Mex Seguro Soc, 2014, 52(5):484-485.
2.	Ayral X, Pickering EH, Woodworth TG, et al. Synovitis:a potential predictive factor of structural progression of medial tibiofemoral knee osteoarthritis-results of a 1 year longitudinal arthroscopic study in 422 patients. Osteoarthritis Cartilage, 2005, 13(5):361-367.
3.	Thambyah A, Broom N. On new bone formation in the pre-osteoarthritic joint. Osteoarthritis and Cartilage, 2009, 17(4):456-463.
4.	Loeser RF, Goldring SR, Scanzello CR, et al. Osteoarthritis:a disease of the joint as an organ. Arthritis Rheum, 2012, 64(6):1697-1707.
5.	Zamli Z, Robson Brown K, Tarlton JF, et al. Subchondral bone plate thickening precedes chondrocyte apoptosis and cartilage degradation in spontaneous animal models of osteoarthritis. Biomed Res Int, 2014, 2014:606870.
6.	Roemer FW, Guermazi A, Felson DT, et al. Presence of MRI-detected joint effusion and synovitis increases the risk of cartilage loss in knees without osteoarthritis at 30-month follow-up:the MOST study. Ann Rheum Dis, 2011, 70(10):1804-1809.
7.	Felson DT. Osteoarthritis as a disease of mechanics. Osteoarthritis Cartilage, 2013, 21(1):10-15.
8.	Varady NH, Grodzinsky AJ. Osteoarthritis year in review 2015:mechanics. Osteoarthritis Cartilage, 2016, 24(1):27-35.
9.	Lories RJ, Luyten FP. The bone-cartilage unit in osteoarthritis. Nat Rev Rheumatol, 2011, 7(1):43-49.
10.	Spyropoulou A, Karamesinis K, Basdra EK. Mechanotransduction pathways in bone pathobiology. Biochimica et Biophysica Acta-Molecular Basis of Disease, 2015, 1852(9):1700-1708.
11.	Vincent TL. Targeting mechanotransduction pathways in osteoarthritis:a focus on the pericellular matrix. Curr Opin Pharmacol, 2013, 13(3):449-454.
12.	Usami Y, Gunawardena AT, Iwamoto M, et al. Wnt signaling in cartilage development and diseases:lessons from animal studies. Lab Invest, 2016, 96(2):186-196.
13.	Zhen GH, Wen C, Jia XF, et al. Inhibition of TGF-beta signaling in mesenchymal stem cells of subchondral bone attenuates osteoarthritis. Nat Med, 2013, 19(6):704-712.
14.	Tang Y, Wu X, Lei W, et al. TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med, 2009, 15(7):757-765.
15.	Tat SK, Amiable N, Pelletier J, et al. Modulation of OPG, RANK and RANKL by human chondrocytes and their implication during osteoarthritis. Rheumatology, 2009, 48(12):1482-1490.
16.	Yuan XL, Meng HY, Wang YC, et al. Bone-cartilage interface crosstalk in osteoarthritis:potential pathways and future therapeutic strategies. Osteoarthritis Cartilage, 2014, 22(8):1077-1089.
17.	Muir P, McCarthy J, Radtke CL, et al. Role of endochondral ossification of articular cartilage and functional adaptation of the subchondral plate in the development of fatigue microcracking of joints. Bone, 2006, 38(3):342-349.
18.	Pap T, Korb-Pap A. Cartilage damage in osteoarthritis and rheumatoid arthritis-two unequal siblings. Nat Rev Rheumatol, 2015, 11(10):606-615.
19.	Kawaguchi H. Endochondral ossification signals in cartilagedegradation during osteoarthritis progression in experimental mouse models. Mol Cells, 2008, 25(1):1-6.
20.	Funck-Brentano T, Cohen-Solal M. Crosstalk between cartilage and bone:When bone cytokines matter. Cytokine Growth Factor Rev, 2011, 22(2):91-97.
21.	Walsh DA. Angiogenesis in osteoarthritis and spondylosis:successful repair with undesirable outcomes. Curr Opin Rheumatol, 2004, 16(5):609-615.
22.	Suri S, Walsh DA. Osteochondral alterations in osteoarthritis. Bone, 2012, 51(2):204-211.
23.	Staines KA, Madi K, Mirczuk SM, et al. Endochondral growth defect and deployment of transient chondrocyte behaviors underlie osteoarthritis onset in a natural murine model. Arthritis & Rheumatology, 2016, 68(4):880-891.
24.	Mackie EJ, Ahmed YA, Tatarczuch L, et al. Endochondral ossification:How cartilage is converted into bone in the developing skeleton. International Journal of Biochemistry & Cell Biology, 2008, 40(1):46-62.
25.	Cox L, van Donkelaar CC, van Rietbergen B, et al. Alterations to the subchondral bone architecture during osteoarthritis:bone adaptation vs endochondral bone formation. Osteoarthritis Cartilage, 2013, 21(2):331-338.
26.	Mangiavini L, Merceron C, Schipani E. Analysis of mouse growth plate development. Curr Protoc Mouse Biol, 2016, 6(1):67-130.
27.	Kronenberg HM. Developmental regulation of the growth plate. Nature, 2003, 423(6937):332-336.
28.	Edwards CJ, Francis-West PH. Bone morphogenetic proteins in the development and healing of synovial joints. Semin Arthritis Rheum, 2001, 31(1):33-42.
29.	Longobardi L, Li T, Tagliafierro L, et al. Synovial joints:from development to homeostasis. Curr Osteoporos Rep, 2015, 13(1):41-51.
30.	Brunet LJ, McMahon JA, McMahon AP, et al. Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science, 1998, 280(5368):1455-1457.
31.	Wei X, Hu M, Mishina Y, et al. Developmental regulation of the growth plate and cranial synchondrosis. J Dent Res, 2016, 95(11):1221-1229.
32.	Jaroszewicz J, Kosowska A, Hutmacher D, et al. Insight into characteristic features of cartilage growth plate as a physiological template for bone formation. J Biomed Mater Res A, 2016, 104(2):357-366.
33.	Ray A, Singh PN, Sohaskey ML, et al. Precise spatial restriction of BMP signaling is essential for articular cartilage differentiation. Development, 2015, 142(6):1169-1179.
34.	Kavanagh E, Abiri M, Bland YS, et al. Division and death of cells in developing synovial joints and long bones. Cell Biol Int, 2002, 26(8):679-688.
35.	Aicher WK, Rolauffs B. The spatial organisation of joint surface chondrocytes:review of its potential roles in tissue functioning, disease and early, preclinical diagnosis of osteoarthritis. Ann Rheum Dis, 2014, 73(4):645-653.
36.	Decker RS, Koyama E, Pacifici M. Genesis and morphogenesis of limb synovial joints and articular cartilage. Matrix Biology, 2014, 39:5-10.
37.	Muldrew K. Osteoarthritis as an inevitable consequence of the structure of articular cartilage. Med Hypotheses, 2002, 59(4):389-397.
38.	O'Conor CJ, Leddy HA, Benefield HC, et al. TRPV4-mediated mechanotransduction regulates the metabolic response of chondrocytes to dynamic loading. Proc Natl Acad Sci U S A, 2014, 111(4):1316-1321.
39.	Lotz MK, Otsuki S, Grogan SP, et al. Cartilage cell clusters. Arthritis Rheum, 2010, 62(8):2206-2218.
40.	Bertrand J, Cromme C, Umlauf D, et al. Molecular mechanisms of cartilage remodelling in osteoarthritis. Int J Biochem Cell Biol, 2010, 42(10):1594-1601.
41.	Chan CK, Seo EY, Chen JY, et al. Identification and specification of the mouse skeletal stem cell. Cell, 2015, 160(1-2):285-298.
42.	Gerber HP, Vu TH, Ryan AM, et al. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med, 1999, 5(6):623-628.
43.	Harper J, Klagsbrun M. Cartilage to bone-angiogenesis leads the way. Nat Med, 1999, 5(6):617-618.
44.	Sasaki J, Matsumoto T, Egusa H, et al. In vitro reproduction of endochondral ossification using a 3D mesenchymal stem cell construct. Integrative Biology, 2012, 4(10):1207-1214.
45.	Pfander D, Cramer T, Swoboda B. Hypoxia and HIF-1alpha in osteoarthritis. Int Orthop, 2005, 29(1):6-9.
46.	Wu LH, Huang XH, Li LF, et al. Insights on biology and pathology of HIF-1 alpha/-2 alpha, TGF beta/BMP, Wnt/beta-Catenin, and NF-kappa B pathways in osteoarthritis. Curr Pharm Des, 2012, 18(22):3293-3312.
47.	Saito T, Fukai A, Mabuchi A, et al. Transcriptional regulation of endochondral ossification by HIF-2 alpha during skeletal growth and osteoarthritis development. Nat Med, 2010, 16(6):678-686.
48.	Yahara Y, Takemori H, Okada M, et al. Pterosin B prevents chondrocyte hypertrophy and osteoarthritis in mice by inhibiting Sik3. Nat Commun, 2016, 7:10959.
49.	Hwang HS, Kim HA. Chondrocyte apoptosis in the pathogenesis of osteoarthritis. Int J Mol Sci, 2015, 16(11):26035-26054.
50.	Musumeci G, Castrogiovanni P, Trovato FM, et al. Biomarkers of chondrocyte apoptosis and autophagy in osteoarthritis. Int J Mol Sci, 2015, 16(9):20560-20575.
51.	van der Kraan PM, van den Berg WB. Chondrocyte hypertrophy and osteoarthritis:role in initiation and progression of cartilage degeneration? Osteoarthritis Cartilage, 2012, 20(3):223-232.
52.	Fuerst M, Bertrand J, Lammers L, et al. Calcification of articular cartilage in human osteoarthritis. Arthritis Rheum, 2009, 60(9):2694-2703.
53.	Bay-Jensen AC, Reker D, Kjelgaard-Petersen C, et al. Osteoarthritis year in review 2015:soluble biomarkers and the BIPED criteria. Osteoarthritis Cartilage, 2016, 24(1):9-20.
54.	Kim JS, Ali MH, Wydra F, et al. Characterization of degenerative human facet joints and facet joint capsular tissues. Osteoarthritis Cartilage, 2015, 23(12):2242-2251.
55.	Yeh TT, Wu SS, Lee CH, et al. The short-term therapeutic effect of recombinant human bone morphogenetic protein-2 on collagenase-induced lumbar facet joint osteoarthritis in rats. Osteoarthritis Cartilage, 2007, 15(12):1357-1366.
56.	Gao SG, Li KH, Zeng KB, et al. Elevated osteopontin level of synovial fluid and articular cartilage is associated with disease severity in knee osteoarthritis patients. Osteoarthritis Cartilage, 2010, 18(1):82-87.
57.	Min TU, Sheng LY, Chao C, et al. Correlation between osteopontin and caveolin-1 in the pathogenesis and progression of osteoarthritis. Exp Ther Med, 2015, 9(6):2059-2064.
58.	Cheng C, Gao SG, Lei GH. Association of osteopontin with osteoarthritis. Rheumatol Int, 2014, 34(12):1627-1631.
59.	Reynard LN, Loughlin J. The genetics and functional analysis of primary osteoarthritis susceptibility. Expert Rev Mol Med, 2013, 15:e2.
60.	Retting KN, Song BE, Yoon BS, et al. BMP canonical Smad signaling through Smad1 and Smad5 is required for endochondral bone formation. Development, 2009, 136(7):1093-1104.
61.	Krawczak DA, Westendorf JJ, Carlson CS. Influence of bone morphogenetic protein-2 on the extracellular matrix, material properties, and gene expression of long-term articular chondrocyte cultures:loss of chondrocyte stability. Tissue Eng Part A, 2009, 15(6):1247-1255.
62.	Mayan MD, Carpintero-Fernandez P, Gago-Fuentes R, et al. Human articular chondrocytes express multiple gap junction proteins:differential expression of connexins in normal and osteoarthritic cartilage. Am J Pathol, 2013, 182(4):1337-1346.
63.	Rolauffs B, Williams JM, Aurich M, et al. Proliferative re-modeling of the spatial organization of human superficial chondrocytes distant to focal early osteoarthritis (OA). Arthritis & Rheumatism, 2010, 62(2):489-498.
64.	Simkin PA. Consider the tidemark. J Rheumatol, 2012, 39(5):890-892.
65.	Gibson G. Active role of chondrocyte apoptosis in endochondral ossification. Microsc Res Tech, 1998, 43(2):191-204.
66.	Roach HI. New aspects of endochondral ossification in the chick:chondrocyte apoptosis, bone formation by former chondrocytes, and acid phosphatase activity in the endochondral bone matrix. J Bone Miner Res, 1997, 12(5):795-805.
67.	King KB, Opel CF, Rempel DM. Cyclical articular joint loading leads to cartilage thinning and osteopontin production in a novel in vivo rabbit model of repetitive finger flexion. Osteoarthritis Cartilage, 2005, 13(11):971-978.
68.	Fuerst M, Niggemeyer O, Lammers L, et al. Articular cartilage mineralization in osteoarthritis of the hip. BMC Musculoskelet Disord, 2009, 10:166.
69.	Mitsuyama H, Healey RM, Terkeltaub RA, et al. Calcification of human articular knee cartilage is primarily an effect of aging rather than osteoarthritis. Osteoarthritis Cartilage, 2007, 15(5):559-565.
70.	Patel N, Buckland-Wright C. Advancement in the zone of calcified cartilage in osteoarthritic hands of patients detected by high definition macroradiography. Osteoarthritis Cartilage, 1999, 7(6):520-525.
71.	Hudelmaier M, Glaser C, Hohe J, et al. Age-related changes in the morphology and deformational behavior of knee joint cartilage. Arthritis Rheum, 2001, 44(11):2556-2561.
72.	Lotz M, Loeser RF. Effects of aging on articular cartilage homeostasis. Bone, 2012, 51(2):241-248.
73.	Fawns HT, Landells JW. Histochemical studies of rheumatic conditions. Ⅰ. Observations on the fine structures of the matrix of normal bone and cartilage. Ann Rheum Dis, 1953, 12(2):105-113.
74.	Bonde HV, Talman ML, Kofoed H. The area of the tidemark in osteoarthritis-a three-dimensional stereological study in 21 patients. APMIS, 2005, 113(5):349-352.
75.	Chen R, Chen S, Chen XM, et al. Study of the tidemark in human mandibular condylar cartilage. Arch Oral Biol, 2011, 56(11):1390-1397.

1. Macias-Hernandez S. The disability associated with osteoarthritis. Rev Med Inst Mex Seguro Soc, 2014, 52(5):484-485.
2. Ayral X, Pickering EH, Woodworth TG, et al. Synovitis:a potential predictive factor of structural progression of medial tibiofemoral knee osteoarthritis-results of a 1 year longitudinal arthroscopic study in 422 patients. Osteoarthritis Cartilage, 2005, 13(5):361-367.
3. Thambyah A, Broom N. On new bone formation in the pre-osteoarthritic joint. Osteoarthritis and Cartilage, 2009, 17(4):456-463.
4. Loeser RF, Goldring SR, Scanzello CR, et al. Osteoarthritis:a disease of the joint as an organ. Arthritis Rheum, 2012, 64(6):1697-1707.
5. Zamli Z, Robson Brown K, Tarlton JF, et al. Subchondral bone plate thickening precedes chondrocyte apoptosis and cartilage degradation in spontaneous animal models of osteoarthritis. Biomed Res Int, 2014, 2014:606870.
6. Roemer FW, Guermazi A, Felson DT, et al. Presence of MRI-detected joint effusion and synovitis increases the risk of cartilage loss in knees without osteoarthritis at 30-month follow-up:the MOST study. Ann Rheum Dis, 2011, 70(10):1804-1809.
7. Felson DT. Osteoarthritis as a disease of mechanics. Osteoarthritis Cartilage, 2013, 21(1):10-15.
8. Varady NH, Grodzinsky AJ. Osteoarthritis year in review 2015:mechanics. Osteoarthritis Cartilage, 2016, 24(1):27-35.
9. Lories RJ, Luyten FP. The bone-cartilage unit in osteoarthritis. Nat Rev Rheumatol, 2011, 7(1):43-49.
10. Spyropoulou A, Karamesinis K, Basdra EK. Mechanotransduction pathways in bone pathobiology. Biochimica et Biophysica Acta-Molecular Basis of Disease, 2015, 1852(9):1700-1708.
11. Vincent TL. Targeting mechanotransduction pathways in osteoarthritis:a focus on the pericellular matrix. Curr Opin Pharmacol, 2013, 13(3):449-454.
12. Usami Y, Gunawardena AT, Iwamoto M, et al. Wnt signaling in cartilage development and diseases:lessons from animal studies. Lab Invest, 2016, 96(2):186-196.
13. Zhen GH, Wen C, Jia XF, et al. Inhibition of TGF-beta signaling in mesenchymal stem cells of subchondral bone attenuates osteoarthritis. Nat Med, 2013, 19(6):704-712.
14. Tang Y, Wu X, Lei W, et al. TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med, 2009, 15(7):757-765.
15. Tat SK, Amiable N, Pelletier J, et al. Modulation of OPG, RANK and RANKL by human chondrocytes and their implication during osteoarthritis. Rheumatology, 2009, 48(12):1482-1490.
16. Yuan XL, Meng HY, Wang YC, et al. Bone-cartilage interface crosstalk in osteoarthritis:potential pathways and future therapeutic strategies. Osteoarthritis Cartilage, 2014, 22(8):1077-1089.
17. Muir P, McCarthy J, Radtke CL, et al. Role of endochondral ossification of articular cartilage and functional adaptation of the subchondral plate in the development of fatigue microcracking of joints. Bone, 2006, 38(3):342-349.
18. Pap T, Korb-Pap A. Cartilage damage in osteoarthritis and rheumatoid arthritis-two unequal siblings. Nat Rev Rheumatol, 2015, 11(10):606-615.
19. Kawaguchi H. Endochondral ossification signals in cartilagedegradation during osteoarthritis progression in experimental mouse models. Mol Cells, 2008, 25(1):1-6.
20. Funck-Brentano T, Cohen-Solal M. Crosstalk between cartilage and bone:When bone cytokines matter. Cytokine Growth Factor Rev, 2011, 22(2):91-97.
21. Walsh DA. Angiogenesis in osteoarthritis and spondylosis:successful repair with undesirable outcomes. Curr Opin Rheumatol, 2004, 16(5):609-615.
22. Suri S, Walsh DA. Osteochondral alterations in osteoarthritis. Bone, 2012, 51(2):204-211.
23. Staines KA, Madi K, Mirczuk SM, et al. Endochondral growth defect and deployment of transient chondrocyte behaviors underlie osteoarthritis onset in a natural murine model. Arthritis & Rheumatology, 2016, 68(4):880-891.
24. Mackie EJ, Ahmed YA, Tatarczuch L, et al. Endochondral ossification:How cartilage is converted into bone in the developing skeleton. International Journal of Biochemistry & Cell Biology, 2008, 40(1):46-62.
25. Cox L, van Donkelaar CC, van Rietbergen B, et al. Alterations to the subchondral bone architecture during osteoarthritis:bone adaptation vs endochondral bone formation. Osteoarthritis Cartilage, 2013, 21(2):331-338.
26. Mangiavini L, Merceron C, Schipani E. Analysis of mouse growth plate development. Curr Protoc Mouse Biol, 2016, 6(1):67-130.
27. Kronenberg HM. Developmental regulation of the growth plate. Nature, 2003, 423(6937):332-336.
28. Edwards CJ, Francis-West PH. Bone morphogenetic proteins in the development and healing of synovial joints. Semin Arthritis Rheum, 2001, 31(1):33-42.
29. Longobardi L, Li T, Tagliafierro L, et al. Synovial joints:from development to homeostasis. Curr Osteoporos Rep, 2015, 13(1):41-51.
30. Brunet LJ, McMahon JA, McMahon AP, et al. Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science, 1998, 280(5368):1455-1457.
31. Wei X, Hu M, Mishina Y, et al. Developmental regulation of the growth plate and cranial synchondrosis. J Dent Res, 2016, 95(11):1221-1229.
32. Jaroszewicz J, Kosowska A, Hutmacher D, et al. Insight into characteristic features of cartilage growth plate as a physiological template for bone formation. J Biomed Mater Res A, 2016, 104(2):357-366.
33. Ray A, Singh PN, Sohaskey ML, et al. Precise spatial restriction of BMP signaling is essential for articular cartilage differentiation. Development, 2015, 142(6):1169-1179.
34. Kavanagh E, Abiri M, Bland YS, et al. Division and death of cells in developing synovial joints and long bones. Cell Biol Int, 2002, 26(8):679-688.
35. Aicher WK, Rolauffs B. The spatial organisation of joint surface chondrocytes:review of its potential roles in tissue functioning, disease and early, preclinical diagnosis of osteoarthritis. Ann Rheum Dis, 2014, 73(4):645-653.
36. Decker RS, Koyama E, Pacifici M. Genesis and morphogenesis of limb synovial joints and articular cartilage. Matrix Biology, 2014, 39:5-10.
37. Muldrew K. Osteoarthritis as an inevitable consequence of the structure of articular cartilage. Med Hypotheses, 2002, 59(4):389-397.
38. O'Conor CJ, Leddy HA, Benefield HC, et al. TRPV4-mediated mechanotransduction regulates the metabolic response of chondrocytes to dynamic loading. Proc Natl Acad Sci U S A, 2014, 111(4):1316-1321.
39. Lotz MK, Otsuki S, Grogan SP, et al. Cartilage cell clusters. Arthritis Rheum, 2010, 62(8):2206-2218.
40. Bertrand J, Cromme C, Umlauf D, et al. Molecular mechanisms of cartilage remodelling in osteoarthritis. Int J Biochem Cell Biol, 2010, 42(10):1594-1601.
41. Chan CK, Seo EY, Chen JY, et al. Identification and specification of the mouse skeletal stem cell. Cell, 2015, 160(1-2):285-298.
42. Gerber HP, Vu TH, Ryan AM, et al. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med, 1999, 5(6):623-628.
43. Harper J, Klagsbrun M. Cartilage to bone-angiogenesis leads the way. Nat Med, 1999, 5(6):617-618.
44. Sasaki J, Matsumoto T, Egusa H, et al. In vitro reproduction of endochondral ossification using a 3D mesenchymal stem cell construct. Integrative Biology, 2012, 4(10):1207-1214.
45. Pfander D, Cramer T, Swoboda B. Hypoxia and HIF-1alpha in osteoarthritis. Int Orthop, 2005, 29(1):6-9.
46. Wu LH, Huang XH, Li LF, et al. Insights on biology and pathology of HIF-1 alpha/-2 alpha, TGF beta/BMP, Wnt/beta-Catenin, and NF-kappa B pathways in osteoarthritis. Curr Pharm Des, 2012, 18(22):3293-3312.
47. Saito T, Fukai A, Mabuchi A, et al. Transcriptional regulation of endochondral ossification by HIF-2 alpha during skeletal growth and osteoarthritis development. Nat Med, 2010, 16(6):678-686.
48. Yahara Y, Takemori H, Okada M, et al. Pterosin B prevents chondrocyte hypertrophy and osteoarthritis in mice by inhibiting Sik3. Nat Commun, 2016, 7:10959.
49. Hwang HS, Kim HA. Chondrocyte apoptosis in the pathogenesis of osteoarthritis. Int J Mol Sci, 2015, 16(11):26035-26054.
50. Musumeci G, Castrogiovanni P, Trovato FM, et al. Biomarkers of chondrocyte apoptosis and autophagy in osteoarthritis. Int J Mol Sci, 2015, 16(9):20560-20575.
51. van der Kraan PM, van den Berg WB. Chondrocyte hypertrophy and osteoarthritis:role in initiation and progression of cartilage degeneration? Osteoarthritis Cartilage, 2012, 20(3):223-232.
52. Fuerst M, Bertrand J, Lammers L, et al. Calcification of articular cartilage in human osteoarthritis. Arthritis Rheum, 2009, 60(9):2694-2703.
53. Bay-Jensen AC, Reker D, Kjelgaard-Petersen C, et al. Osteoarthritis year in review 2015:soluble biomarkers and the BIPED criteria. Osteoarthritis Cartilage, 2016, 24(1):9-20.
54. Kim JS, Ali MH, Wydra F, et al. Characterization of degenerative human facet joints and facet joint capsular tissues. Osteoarthritis Cartilage, 2015, 23(12):2242-2251.
55. Yeh TT, Wu SS, Lee CH, et al. The short-term therapeutic effect of recombinant human bone morphogenetic protein-2 on collagenase-induced lumbar facet joint osteoarthritis in rats. Osteoarthritis Cartilage, 2007, 15(12):1357-1366.
56. Gao SG, Li KH, Zeng KB, et al. Elevated osteopontin level of synovial fluid and articular cartilage is associated with disease severity in knee osteoarthritis patients. Osteoarthritis Cartilage, 2010, 18(1):82-87.
57. Min TU, Sheng LY, Chao C, et al. Correlation between osteopontin and caveolin-1 in the pathogenesis and progression of osteoarthritis. Exp Ther Med, 2015, 9(6):2059-2064.
58. Cheng C, Gao SG, Lei GH. Association of osteopontin with osteoarthritis. Rheumatol Int, 2014, 34(12):1627-1631.
59. Reynard LN, Loughlin J. The genetics and functional analysis of primary osteoarthritis susceptibility. Expert Rev Mol Med, 2013, 15:e2.
60. Retting KN, Song BE, Yoon BS, et al. BMP canonical Smad signaling through Smad1 and Smad5 is required for endochondral bone formation. Development, 2009, 136(7):1093-1104.
61. Krawczak DA, Westendorf JJ, Carlson CS. Influence of bone morphogenetic protein-2 on the extracellular matrix, material properties, and gene expression of long-term articular chondrocyte cultures:loss of chondrocyte stability. Tissue Eng Part A, 2009, 15(6):1247-1255.
62. Mayan MD, Carpintero-Fernandez P, Gago-Fuentes R, et al. Human articular chondrocytes express multiple gap junction proteins:differential expression of connexins in normal and osteoarthritic cartilage. Am J Pathol, 2013, 182(4):1337-1346.
63. Rolauffs B, Williams JM, Aurich M, et al. Proliferative re-modeling of the spatial organization of human superficial chondrocytes distant to focal early osteoarthritis (OA). Arthritis & Rheumatism, 2010, 62(2):489-498.
64. Simkin PA. Consider the tidemark. J Rheumatol, 2012, 39(5):890-892.
65. Gibson G. Active role of chondrocyte apoptosis in endochondral ossification. Microsc Res Tech, 1998, 43(2):191-204.
66. Roach HI. New aspects of endochondral ossification in the chick:chondrocyte apoptosis, bone formation by former chondrocytes, and acid phosphatase activity in the endochondral bone matrix. J Bone Miner Res, 1997, 12(5):795-805.
67. King KB, Opel CF, Rempel DM. Cyclical articular joint loading leads to cartilage thinning and osteopontin production in a novel in vivo rabbit model of repetitive finger flexion. Osteoarthritis Cartilage, 2005, 13(11):971-978.
68. Fuerst M, Niggemeyer O, Lammers L, et al. Articular cartilage mineralization in osteoarthritis of the hip. BMC Musculoskelet Disord, 2009, 10:166.
69. Mitsuyama H, Healey RM, Terkeltaub RA, et al. Calcification of human articular knee cartilage is primarily an effect of aging rather than osteoarthritis. Osteoarthritis Cartilage, 2007, 15(5):559-565.
70. Patel N, Buckland-Wright C. Advancement in the zone of calcified cartilage in osteoarthritic hands of patients detected by high definition macroradiography. Osteoarthritis Cartilage, 1999, 7(6):520-525.
71. Hudelmaier M, Glaser C, Hohe J, et al. Age-related changes in the morphology and deformational behavior of knee joint cartilage. Arthritis Rheum, 2001, 44(11):2556-2561.
72. Lotz M, Loeser RF. Effects of aging on articular cartilage homeostasis. Bone, 2012, 51(2):241-248.
73. Fawns HT, Landells JW. Histochemical studies of rheumatic conditions. Ⅰ. Observations on the fine structures of the matrix of normal bone and cartilage. Ann Rheum Dis, 1953, 12(2):105-113.
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