Loss of Vhl in cartilage accelerated the progression of age-associated and surgically induced murine osteoarthritis

Osteoarthritis and Cartilage

Volumn 22, Issue 8, 2014, Pages 1197-1205

  Weng, T ^a   Xie, Y ^a   Yi, L ^a   Huang, J ^a   Luo, F ^a   Du, X ^a   Chen, L ^a   Liu, C ^a   Chen, D ^b  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Autophagy; Hypoxia inducible factor (HIF ); Osteoarthritis; Von hippel lindau gene (Vhl)

Indexed keywords

COLLAGENASE 3; FAS ANTIGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; PROTEOGLYCAN; TAMOXIFEN; VON HIPPEL LINDAU PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; VHLH PROTEIN, MOUSE;

ADULT; AGE; AGED; ANIMAL EXPERIMENT; ANIMAL IMAGING SYSTEM; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ARTICULAR CARTILAGE; AUTOPHAGY; BONE; CARTILAGE CELL; CARTILAGE DEGENERATION; CARTILAGE MATRIX; COMPUTED TOMOGRAPHY SCANNER; CONTROLLED STUDY; DISEASE COURSE; GENE; GENE EXPRESSION; GENE INACTIVATION; GENE LOSS; HISTOPATHOLOGY; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; KNEE; KNEE OSTEOARTHRITIS; MALE; MICRO-COMPUTED TOMOGRAPHY; MOUSE; MOUSE MODEL; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; SUBCHONDRAL BONE; UPREGULATION; VON HIPPEL LINDAU GENE; AGING; ANIMAL; EXPERIMENTAL ARTHRITIS; GENETICS; KNOCKOUT MOUSE; METABOLISM;

AGING; ANIMALS; APOPTOSIS; ARTHRITIS, EXPERIMENTAL; AUTOPHAGY; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARTILAGE, ARTICULAR; CHONDROCYTES; DISEASE PROGRESSION; KNEE JOINT; MICE; MICE, KNOCKOUT; OSTEOARTHRITIS, KNEE; UP-REGULATION; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 84905577960     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2014.06.031     Document Type: Article

References (32)

1. Murphy C.L., Thoms B.L., Vaghjiani R.J., Lafont J.E. Hypoxia. HIF-mediated articular chondrocyte function: prospects for cartilage repair. Arthritis Res Ther 2009, 11:213.
2. Saito T., Fukai A., Mabuchi A., Ikeda T., Yano F., Ohba S., et al. Transcriptional regulation of endochondral ossification by HIF-2alpha during skeletal growth and osteoarthritis development. Nat Med 2010, 16:678-686.
3. Yang S., Kim J., Ryu J.H., Oh H., Chun C.H., Kim B.J., et al. Hypoxia-inducible factor-2alpha is a catabolic regulator of osteoarthritic cartilage destruction. Nat Med 2010, 16:687-693.
4. Schipani E., Ryan H.E., Didrickson S., Kobayashi T., Knight M., Johnson R.S. Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival. Genes Dev 2001, 15:2865-2876.
5. Gelse K., Pfander D., Obier S., Knaup K.X., Wiesener M., Hennig F.F., et al. Role of hypoxia-inducible factor 1 alpha in the integrity of articular cartilage in murine knee joints. Arthritis Res Ther 2008, 10:R111.
6. Ryu J.H., Shin Y., Huh Y.H., Yang S., Chun C.H., Chun J.S. Hypoxia-inducible factor-2alpha regulates Fas-mediated chondrocyte apoptosis during osteoarthritic cartilage destruction. Cell Death Differ 2012, 19:440-450.
7. Gnarra J.R., Ward J.M., Porter F.D., Wagner J.R., Devor D.E., Grinberg A., et al. Defective placental vasculogenesis causes embryonic lethality in VHL-deficient mice. Proc Natl Acad Sci U S A 1997, 94:9102-9107.
8. Wang Y., Wan C., Deng L., Liu X., Cao X., Gilbert S.R., et al. The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest 2007, 117:1616-1626.
9. Pfander D., Kobayashi T., Knight M.C., Zelzer E., Chan D.A., Olsen B.R., et al. Deletion of Vhlh in chondrocytes reduces cell proliferation and increases matrix deposition during growth plate development. Development 2004, 131:2497-2508.
10. Zhu M., Chen M., Lichtler A.C., O'Keefe R.J., Chen D. Tamoxifen-inducible Cre-recombination in articular chondrocytes of adult Col2a1-CreER(T2) transgenic mice. Osteoarthritis Cartilage 2008, 16:129-130.
11. Shen J., Li J., Wang B., Jin H., Wang M., Zhang Y., et al. Deletion of the type II TGF-beta receptor gene in articular chondrocytes leads to a progressive OA-like phenotype in mice. Arthritis Rheum 2013, 65(12):3107-3119.
12. Chen M., Lichtler A.C., Sheu T.J., Xie C., Zhang X., O'Keefe R.J., et al. Generation of a transgenic mouse model with chondrocyte-specific and tamoxifen-inducible expression of Cre recombinase. Genesis 2007, 45:44-50.
13. Weng T., Yi L., Huang J., Luo F., Wen X., Du X., et al. Genetic inhibition of FGFR1 in cartilage attenuates articular cartilage degeneration in adult mice. Arthritis Rheum 2013, 64(12):3982-3992.
14. Glasson S.S., Chambers M.G., Van Den Berg W.B., Little C.B. The OARSI histopathology initiative - recommendations for histological assessments of osteoarthritis in the mouse. Osteoarthritis Cartilage 2010, 18(Suppl 3):S17-S23.
15. Weng T., Xie Y., Huang J., Luo F., Yi L., He Q., et al. Inactivation of Vhl in osteochondral progenitor cells causes high bone mass phenotype and protects against age-related bone loss in adult mice. J Bone Miner Res 2014, 29:820-829.
16. Goldring M.B., Goldring S.R. Articular cartilage and subchondral bone in the pathogenesis of osteoarthritis. Ann N Y Acad Sci 2010, 1192:230-237.
17. Weng T., Xie Y., Huang J., Luo F., Yi L., He Q., et al. Inactivation of Vhl in osteochondral progenitor cells causes high bone mass phenotype and protects against age-related bone loss in adult mice. J Bone Miner Res 2014, 29(4):820-829.
18. Loeser R.F. Aging and osteoarthritis. Curr Opin Rheumatol 2011, 23:492-496.
19. Kim H.A., Blanco F.J. Cell death and apoptosis in osteoarthritic cartilage. Curr Drug Targets 2007, 8:333-345.
20. Gillies L.A., Kuwana T. Apoptosis regulation at the mitochondrial outer membrane. J Cell Biochem 2014, 115:632-640.
21. Carames B., Taniguchi N., Otsuki S., Blanco F.J., Lotz M. Autophagy is a protective mechanism in normal cartilage, and its aging-related loss is linked with cell death and osteoarthritis. Arthritis Rheum 2010, 62:791-801.
22. Sasaki H., Takayama K., Matsushita T., Ishida K., Kubo S., Matsumoto T., et al. Autophagy modulates osteoarthritis-related gene expressions in human chondrocytes. Arthritis Rheum 2012, 64(6):1920-1928.
23. Khan W.S., Adesida A.B., Hardingham T.E. Hypoxic conditions increase hypoxia-inducible transcription factor 2alpha and enhance chondrogenesis in stem cells from the infrapatellar fat pad of osteoarthritis patients. Arthritis Res Ther 2007, 9:R55.
24. Hickey M.M., Richardson T., Wang T., Mosqueira M., Arguiri E., Yu H., et al. The von Hippel-Lindau Chuvash mutation promotes pulmonary hypertension and fibrosis in mice. J Clin Invest 2010, 120:827-839.
25. Lotz M.K., Carames B. Autophagy and cartilage homeostasis mechanisms in joint health, aging and OA. Nat Rev Rheumatol 2011, 7:579-587.
26. Yang R.T., Zhang C., Liu Y., Zhou H.H., Li Z.B. Autophagy prior to chondrocyte cell death during the degeneration of Meckel's cartilage. Anat Rec (Hoboken) 2012, 295:734-741.
27. Aigner T., Kim H.A. Apoptosis and cellular vitality: issues in osteoarthritic cartilage degeneration. Arthritis Rheum 2002, 46:1986-1996.
28. Zamli Z., Adams M.A., Tarlton J.F., Sharif M. Increased chondrocyte apoptosis is associated with progression of osteoarthritis in spontaneous Guinea pig models of the disease. Int J Mol Sci 2013, 14:17729-17743.
29. Carames B., Hasegawa A., Taniguchi N., Miyaki S., Blanco F.J., Lotz M. Autophagy activation by rapamycin reduces severity of experimental osteoarthritis. Ann Rheum Dis 2012, 71:575-581.
30. Caramés B., Taniguchi N., Seino D., Blanco F.J., D'Lima D., Lotz M. Mechanical injury suppresses autophagy regulators and pharmacologic activation of autophagy results in chondroprotection. Arthritis Rheum 2012, 64:1182-1192.
31. Bohensky J., Terkhorn S.P., Freeman T.A., Adams C.S., Garcia J.A., Shapiro I.M., et al. Regulation of autophagy in human and murine cartilage: hypoxia-inducible factor 2 suppresses chondrocyte autophagy. Arthritis Rheum 2009, 60:1406-1415.
32. Bohensky J., Shapiro I.M., Leshinsky S., Terkhorn S.P., Adams C.S., Srinivas V. HIF-1 regulation of chondrocyte apoptosis: induction of the autophagic pathway. Autophagy 2007, 3:207-214.