Reduced chondrocyte proliferation, earlier cell cycle exit and increased apoptosis in neuronal nitric oxide synthase-deficient mice

Osteoarthritis and Cartilage

Volumn 20, Issue 2, 2012, Pages 144-151

  Yan, Q ^a,b   Feng, Q ^a   Beier, F ^a,b  

^a WESTERN UNIVERSITY   (Canada)

^b CHILDREN S HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

Nitric oxide Neuronal nitric oxide synthase Chondrocyte proliferation Endochondral bone formation

Indexed keywords

CALCIUM; CASPASE 3; CYCLIN D1; NEURONAL NITRIC OXIDE SYNTHASE; PROTEIN P57; RETINOID RELATED ORPHAN RECEPTOR ALPHA; TRANSCRIPTION FACTOR SOX;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE DEVELOPMENT; BONE MINERALIZATION; CALCIUM BONE LEVEL; CARTILAGE CELL; CELL COUNT; CELL CYCLE; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CONTROLLED STUDY; CORTICAL BONE; ENCHONDRAL OSSIFICATION; ENZYME DEFICIENCY; ENZYME INACTIVATION; GENE EXPRESSION; GENE MUTATION; GROWTH PLATE; GROWTH RETARDATION; HETEROZYGOTE; HISTOLOGY; HYPERTROPHY; IMMUNOHISTOCHEMISTRY; LONG BONE; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRABECULAR BONE;

ANIMALS; APOPTOSIS; CALCIUM; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDROCYTES; CHONDROGENESIS; FEMALE; GENE EXPRESSION; GROWTH DISORDERS; GROWTH PLATE; HUMERUS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE I; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIBIA; WEIGHT GAIN;

EID: 84855825441     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2011.11.014     Document Type: Article

References (35)

1. Murad F. Discovery of some of the biological effects of nitric oxide and its role in cell signaling. Biosci Rep 1999, 19(3):133-154.
2. Moncada S., Palmer R.M., Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 1991, 43(2):109-142.
3. Teixeira C.C., Agoston H., Beier F. Nitric oxide, C-type natriuretic peptide and cGMP as regulators of endochondral ossification. Dev Biol 2008, 319(2):171-178.
4. Ignarro L.J. Nitric oxide: a unique endogenous signaling molecule in vascular biology. Biosci Rep 1999, 19(2):51-71.
5. Abramson S.B. Osteoarthritis and nitric oxide. Osteoarthr Cartilage 2008, 16(Suppl 2):S15-S20.
6. Van't Hof R.J., Ralston S.H. Nitric oxide and bone. Immunology 2001, 103(3):255-261.
7. Teixeira C.C., Ischiropoulos H., Leboy P.S., Adams S.L., Shapiro I.M. Nitric oxide-nitric oxide synthase regulates key maturational events during chondrocyte terminal differentiation. Bone 2005, 37(1):37-45.
8. Collin-Osdoby P., Nickols G.A., Osdoby P. Bone cell function, regulation, and communication: a role for nitric oxide. JCell Biochem 1995, 57(3):399-408.
9. Drissi H., Zuscik M., Rosier R., O'Keefe R. Transcriptional regulation of chondrocyte maturation: potential involvement of transcription factors in OA pathogenesis. Mol Aspects Med 2005, 26(3):169-179.
10. Karsenty G., Kronenberg H.M., Settembre C. Genetic control of bone formation. Annu Rev Cell Dev Biol 2009, 25:629-648.
11. Beier F. Cell-cycle control and the cartilage growth plate. JCell Physiol 2005, 202(1):1-8.
12. Horton W.A. Skeletal development: insights from targeting the mouse genome. Lancet 2003, 362(9383):560-569.
13. Provot S., Schipani E. Molecular mechanisms of endochondral bone development. Biochem Biophys Res Commun 2005, 328(3):658-665.
14. Zelzer E., Olsen B.R. The genetic basis for skeletal diseases. Nature 2003, 423(6937):343-348.
15. Dreier R. Hypertrophic differentiation of chondrocytes in osteoarthritis: the developmental aspect of degenerative joint disorders. Arthritis Res Ther 2010, 12(5):216.
16. Pitsillides A.A., Beier F. Cartilage biology in osteoarthritis-lessons from developmental biology. Nat Rev Rheumatol 2011, 7(11):654-663.
17. Yan Q., Feng Q., Beier F. Endothelial nitric oxide synthase deficiency in mice results in reduced chondrocyte proliferation and endochondral bone growth. Arthritis Rheum 2010, 62(7):2013-2022.
18. Wang G., Yan Q., Woods A., Aubrey L.A., Feng Q., Beier F. Inducible nitric oxide synthase-nitric oxide signaling mediates the mitogenic activity of Rac1 during endochondral bone growth. JCell Sci 2011, 124(Pt 20):3405-3413.
19. Van't Hof R.J., Macphee J., Libouban H., Helfrich M.H., Ralston S.H. Regulation of bone mass and bone turnover by neuronal nitric oxide synthase. Endocrinology 2004, 145(11):5068-5074.
20. Solomon L.A., Li J.R., Berube N.G., Beier F. Loss of ATRX in chondrocytes has minimal effects on skeletal development. PLoS One 2009, 4(9):e7106.
21. Wang G., Woods A., Agoston H., Ulici V., Glogauer M., Beier F. Genetic ablation of Rac1 in cartilage results in chondrodysplasia. Dev Biol 2007, 306(2):612-623.
22. Ulici V., Hoenselaar K.D., Agoston H., McErlain D.D., Umoh J., Chakrabarti S., et al. The role of Akt1 in terminal stages of endochondral bone formation: angiogenesis and ossification. Bone 2009, 45(6):1133-1145.
23. Ulici V., Hoenselaar K.D., Gillespie J.R., Beier F. The PI3K pathway regulates endochondral bone growth through control of hypertrophic chondrocyte differentiation. BMC Dev Biol 2008, 8:40.
24. Agoston H., Khan S., James C.G., Gillespie J.R., Serra R., Stanton L.A., et al. C-type natriuretic peptide regulates endochondral bone growth through p38 MAP kinase-dependent and -independent pathways. BMC Dev Biol 2007, 7:18.
25. James C.G., Woods A., Underhill T.M., Beier F. The transcription factor ATF3 is upregulated during chondrocyte differentiation and represses cyclin D1 and A gene transcription. BMC Mol Biol 2006, 7:30.
26. Riemer S., Gebhard S., Beier F., Poschl E., von der Mark K. Role of c-fos in the regulation of type X collagen gene expression by PTH and PTHrP: localization of a PTH/PTHrP-responsive region in the human COL10A1 enhancer. JCell Biochem 2002, 86(4):688-699.
27. Chusho H., Tamura N., Ogawa Y., Yasoda A., Suda M., Miyazawa T., et al. Dwarfism and early death in mice lacking C-type natriuretic peptide. Proc Natl Acad Sci U S A 2001, 98(7):4016-4021.
28. Sabanai K., Tsutsui M., Sakai A., Hirasawa H., Tanaka S., Nakamura E., et al. Genetic disruption of all NO synthase isoforms enhances BMD and bone turnover in mice invivo: involvement of the renin-angiotensin system. JBone Miner Res 2008, 23(5):633-643.
29. Nakata S., Tsutsui M., Shimokawa H., Suda O., Morishita T., Shibata K., et al. Spontaneous myocardial infarction in mice lacking all nitric oxide synthase isoforms. Circulation 2008, 117(17):2211-2223.
30. Beier F., Lee R.J., Taylor A.C., Pestell R.G., LuValle P. Identification of the cyclin D1 gene as a target of activating transcription factor 2 in chondrocytes. Proc Natl Acad Sci USA 1999, 96(4):1433-1438.
31. Beier F., Ali Z., Mok D., Taylor A.C., Leask T., Albanese C., et al. TGFbeta and PTHrP control chondrocyte proliferation by activating cyclin D1 expression. Mol Biol Cell 2001, 12(12):3852-3863.
32. Beier F., LuValle P. The cyclin D1 and cyclin A genes are targets of activated PTH/PTHrP receptors in Jansen's metaphyseal chondrodysplasia. Mol Endocrinol 2002, 16(9):2163-2173.
33. Ionescu A.M., Schwarz E.M., Vinson C., Puzas J.E., Rosier R., Reynolds P.R., et al. PTHrP modulates chondrocyte differentiation through AP-1 and CREB signaling. JBiol Chem 2001, 276(15):11639-11647.
34. Wang J., Zhou J., Bondy C.A. Igf1 promotes longitudinal bone growth by insulin-like actions augmenting chondrocyte hypertrophy. Faseb J 1999, 13(14):1985-1990.
35. Woods A., Wang G., James C.G., Dupuis H., Beier F. Microarray analyses of chondrocyte gene expression in response to manipulation of the actin cytoskeleton: Identification of a central role of RORα signaling. J Cell Mol Med 2009, 13(9B):3497-3516.