Role of hypoxia-inducible factor 1 alpha in the integrity of articular cartilage in murine knee joints

Arthritis Research and Therapy

Volumn 10, Issue 5, 2008, Pages

  Gelse, Kolja ^a,b   Pfander, David ^c   Obier, Simon ^a   Knaup, Karl X ^b   Wiesener, Michael ^b   Hennig, Friedrich F ^b   Swoboda, Bernd ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^c Hufeland Clinic   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2 METHOXYESTRADIOL; 2-METHOXYESTRADIOL; CYTOKINE; DICARBOXYLIC AMINO ACID; DRUG DERIVATIVE; ESTRADIOL; HIF1A PROTEIN, MOUSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXALYLGLYCINE; TUBULIN MODULATOR; UNCLASSIFIED DRUG;

ANIMAL; APOPTOSIS; ARTICLE; ARTICULAR CARTILAGE; BAGG ALBINO MOUSE; BIOSYNTHESIS; CARTILAGE CELL; CELL CULTURE; CELL HYPOXIA; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; HUMAN; IMMUNOHISTOCHEMISTRY; KNEE; KNEE OSTEOARTHRITIS; METABOLISM; MOUSE; NICK END LABELING; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AMINO ACIDS, DICARBOXYLIC; ANIMALS; APOPTOSIS; CARTILAGE, ARTICULAR; CELL HYPOXIA; CELLS, CULTURED; CHONDROCYTES; CYTOKINES; ESTRADIOL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; KNEE JOINT; MICE; MICE, INBRED BALB C; OSTEOARTHRITIS, KNEE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUBULIN MODULATORS;

EID: 54749087972     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar2508     Document Type: Article

References (40)

1. Schipani E Ryan HE Didrickson S Kobayashi T Knight M Johnson RS Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival Genes Dev 2001, 15:2865-2876. 312800 11691837
2. Pfander D Cramer T Schipani E Johnson RS HIF-1α controls extracellular matrix synthesis by epiphyseal chondrocytes J Cell Sci 2003, 116:1819-1826. 10.1242/jcs.00385 12665562
3. Amarilio R Viukov SV Sharir A Eshkar-Oren I Johnson RS Zelzer E HIF1α regulation of Sox9 is necessary to maintain differentiation of hypoxic prechondrogenic cells during early skeletogenesis Development 2007, 134:3917-3928. 10.1242/dev.008441 17913788
4. Robins JC Akeno N Mukherjee A Dalal RR Aronow BJ Koopman P Clemens TL Hypoxia induces chondrocyte-specific gene expression in mesenchymal cells in association with transcriptional activation of Sox9 Bone 2005, 37:313-322. 10.1016/j.bone.2005.04.040 16023419
5. Pfander D Kobayashi T Knight MC Zelzer E Chan DA Olsen BR Giaccia AJ Johnson RS Haase VH Schipani E Deletion of Vhlh in chondrocytes reduces cell proliferation and increases matrix deposition during growth plate development Development 2004, 131:2497-2508. 10.1242/dev.01138 15128677
6. Semenza GL HIF-1, O(2), and the 3 PHDs: How animal cells signal hypoxia to the nucleus Cell 2001, 107:1-3. 10.1016/S0092-8674(01)00518-9 11595178
7. Maxwell PH Ratcliffe PJ Oxygen sensors and angiogenesis Semin Cell Dev Biol 2002, 13:29-37. 10.1006/scdb.2001.0287 11969369
8. Treins C Giorgetti-Peraldi S Murdaca J Monthouel-Kartmann MN Van Obberghen E Regulation of hypoxia-inducible factor (HIF)-1 activity and expression of HIF hydroxylases in response to insulin-like growth factor I Mol Endocrinol 2005, 19:1304-1317. 10.1210/me.2004-0239 15695372
9. Yudoh K Nakamura H Masuko-Hongo K Kato T Nishioka K Catabolic stress induces expression of hypoxia-inducible factor (HIF)-1 alpha in articular chondrocytes: Involvement of HIF-1 alpha in the pathogenesis of osteoarthritis Arthritis Res Ther 2005, 7:R904-R914. 1175045 15987493 10.1186/ar1765
10. Fukuda R Hirota K Fan F Jung YD Ellis LM Semenza GL Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells J Biol Chem 2002, 277:38205-38211. 10.1074/jbc.M203781200 12149254
11. Pfander D Cramer T Swoboda B Hypoxia and HIF-1α in osteoarthritis Int Orthop 2005, 29:6-9. 10.1007/s00264-004-0618-2 15611874
12. Grimmer C Pfander D Swoboda B Aigner T Mueller L Hennig FF Gelse K Hypoxia-inducible factor 1α is involved in the prostaglandin metabolism of osteoarthritic cartilage through up-regulation of microsomal prostaglandin E synthase 1 in articular chondrocytes Arthritis Rheum 2007, 56:4084-4094. 10.1002/art.23136 18050215
13. Grimmer C Balbus N Lang U Aigner T Cramer T Muller L Swoboda B Pfander D Regulation of type II collagen synthesis during osteoarthritis by prolyl-4-hydroxylases: Possible influence of low oxygen levels Am J Pathol 2006, 169:491-502. 1698781 16877351 10.2353/ajpath.2006.050738
14. Ricker JL Chen Z Yang XP Pribluda VS Swartz GM Van Waes C 2-Methoxyestradiol inhibits hypoxia-inducible factor 1α, tumor growth, and angiogenesis and augments paclitaxel efficacy in head and neck squamous cell carcinoma Clin Cancer Res 2004, 10:8665-8673. 10.1158/ 1078-0432.CCR-04-1393 15623651
15. Asikainen TM Schneider BK Waleh NS Clyman RI Ho WB Flippin LA Gunzler V White CW Activation of hypoxia-inducible factors in hyperoxia through prolyl 4-hydroxylase blockade in cells and explants of primate lung Proc Natl Acad Sci USA 2005, 102:10212-10217. 1177409 16009933 10.1073/ pnas.0504520102
16. Walton M Degenerative joint disease in the mouse knee; histological observations J Pathol 1977, 123:109-122. 10.1002/path.1711230207 592015
17. Walton M Degenerative joint disease in the mouse knee; radiological and morphological observations J Pathol 1977, 123:97-107. 10.1002/ path.1711230206 592018
18. Altman FP A metabolic dysfunction in early murine osteoarthritis Ann Rheum Dis 1981, 40:303-306. 1000767 7247474 10.1136/ard.40.3.303
19. Schunke M Tillmann B Bruck M Muller-Ruchholtz W Morphologic characteristics of developing osteoarthrotic lesions in the knee cartilage of STR/IN mice Arthritis Rheum 1988, 31:898-905. 10.1002/ art.1780310711 3395383
20. Gelse K Soder S Eger W Diemtar T Aigner T Osteophyte development - molecular characterization of differentiation stages Osteoarthr Cartil 2003, 11:141-148. 10.1053/joca.2002.0873 12554130
21. Krenn V Morawietz L Haupl T Neidel J Petersen I Konig A Grading of chronic synovitis - a histopathological grading system for molecular and diagnostic pathology Pathol Res Pract 2002, 198:317-325. 10.1078/ 0344-0338-5710261 12092767
22. Samoszuk MK Walter J Mechetner E Improved immunohistochemical method for detecting hypoxia gradients in mouse tissues and tumors J Histochem Cytochem 2004, 52:837-839. 10.1369/jhc.4B6248.2004 15150293
23. Provot S Zinyk D Gunes Y Kathri R Le Q Kronenberg HM Johnson RS Longaker MT Giaccia AJ Schipani E Hif-1α regulates differentiation of limb bud mesenchyme and joint development J Cell Biol 2007, 177:451-464. 2064828 17470636 10.1083/jcb.200612023
24. Malladi P Xu Y Chiou M Giaccia AJ Longaker MT Hypoxia inducible factor-1α deficiency affects chondrogenesis of adipose-derived adult stromal cells Tissue Eng 2007, 13:1159-1171. 10.1089/ten.2006.0265 17518738
25. Mooberry SL Mechanism of action of 2-methoxyestradiol: New developments Drug Resist Updat 2003, 6:355-361. 10.1016/j.drup.2003.10.001 14744499
26. Mabjeesh NJ Escuin D LaVallee TM Pribluda VS Swartz GM Johnson MS Willard MT Zhong H Simons JW Giannakakou P 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF Cancer Cell 2003, 3:363-375. 10.1016/S1535-6108(03)00077-1 12726862
27. Lakhani NJ Sarkar MA Venitz J Figg WD 2-Methoxyestradiol, a promising anticancer agent Pharmacotherapy 2003, 23:165-172. 10.1592/ phco.23.2.165.32088 12587805
28. Aigner T Hemmel M Neureiter D Gebhard PM Zeiler G Kirchner T McKenna L Apoptotic cell death is not a widespread phenomenon in normal aging and osteoarthritis human articular knee cartilage: A study of proliferation, programmed cell death (apoptosis), and viability of chondrocytes in normal and osteoarthritic human knee cartilage Arthritis Rheum 2001, 44:1304-1312. 10.1002/ 1529-0131(200106)44:6<1304::AID-ART222>3.0.CO;2-T 11407689
29. Coimbra IB Jimenez SA Hawkins DF Piera-Velazquez S Stokes DG Hypoxia inducible factor-1 alpha expression in human normal and osteoarthritic chondrocytes Osteoarthr Cartil 2004, 12:336-345. 10.1016/ j.joca.2003.12.005 15023385
30. Kilic M Kasperczyk H Fulda S Debatin KM Role of hypoxia inducible factor-1 alpha in modulation of apoptosis resistance Oncogene 2007, 26:2027-2038. 10.1038/sj.onc.1210008 17043658
31. Loor G Schumacker PT Role of hypoxia-inducible factor in cell survival during myocardial ischemia-reperfusion Cell Death Differ 2008, 15:686-690. 10.1038/cdd.2008.13 18259200
32. Malhotra R Tyson DW Rosevear HM Brosius FC 3rd Hypoxia-inducible factor-1α is a critical mediator of hypoxia induced apoptosis in cardiac H9c2 and kidney epithelial HK-2 cells BMC Cardiovasc Disord 2008, 8:9. 2387135 18447926 10.1186/1471-2261-8-9
33. Asikainen TM White CW HIF stabilizing agents: Shotgun or scalpel? Am J Physiol Lung Cell Mol Physiol 2007, 293:L555-L556. 10.1152/ ajplung.00251.2007 17616644
34. Jimenez S Harsch M Rosenbloom J Hydroxyproline stabilizes the triple helix of chick tendon collagen Biochem Biophys Res Commun 1973, 52:106-114. 10.1016/0006-291X(73)90960-1 4576266
35. Harsch M Murphy L Rosenbloom J Metabolism by isolated fibroblasts of abnormal collagens containing analogues of proline or lysine FEBS Lett 1972, 26:48-52. 10.1016/0014-5793(72)80539-8 4636750
36. Lefebvre V Huang W Harley VR Goodfellow PN de Crombrugghe B SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene Mol Cell Biol 1997, 17:2336-2346. 232082 9121483
37. Cramer T Yamanishi Y Clausen BE Forster I Pawlinski R Mackman N Haase VH Jaenisch R Corr M Nizet V Firestein GS Gerber HP Ferrara N Johnson RS HIF-1α is essential for myeloid cell-mediated inflammation Cell 2003, 112:645-657. 10.1016/S0092-8674(03)00154-5 12628185
38. Zhang W Petrovic JM Callaghan D Jones A Cui H Howlett C Stanimirovic D Evidence that hypoxia-inducible factor-1 (HIF-1) mediates transcriptional activation of interleukin-1beta (IL-1β) in astrocyte cultures J Neuroimmunol 2006, 174:63-73. 10.1016/ j.jneuroim.2006.01.014 16504308
39. Merrihew C Soeder S Rueger DC Kuettner KE Chubinskaya S Modulation of endogenous osteogenic protein-1 (OP-1) by interleukin-1 in adult human articular cartilage J Bone Joint Surg Am 2003, 85-A:67-74. 12925612
40. Fukui N Zhu Y Maloney WJ Clohisy J Sandell LJ Stimulation of BMP-2 expression by pro-inflammatory cytokines IL-1 and TNF-α in normal and osteoarthritic chondrocytes J Bone Joint Surg Am 2003, 85-A:59-66. 12925611