Endothelial nitric oxide synthase deficiency in mice results in reduced chondrocyte proliferation and endochondral bone growth

Arthritis and Rheumatism

Volumn 62, Issue 7, 2010, Pages 2013-2022

  Yan, Qian ^a   Feng, Qingping ^a   Beier, Frank ^a  

^a WESTERN UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; PROTEIN P57; TRANSCRIPTION FACTOR SOX9;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CELL CYCLE PROGRESSION; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; ENCHONDRAL OSSIFICATION; ENZYME INACTIVATION; EXPLANT; FATALITY; FEMALE; GENE MUTATION; GROWTH PLATE; IN VITRO STUDY; MOUSE; MOUSE MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; BODY SIZE; BONE AND BONES; BONE DEVELOPMENT; BREEDING; CELL COUNT; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHONDROCYTES; CYCLIN D1; FEMALE; HUMANS; LONGEVITY; MALE; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE III; SOX9 TRANSCRIPTION FACTOR;

EID: 77954232158     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.27486     Document Type: Article

References (44)

1. Abramson SB. Nitric oxide in inflammation and pain associated with osteoarthritis. Arthritis Res Ther 2008;10 Suppl 2:S2.
2. Abramson SB. Osteoarthritis and nitric oxide. Osteoarthritis Cartilage 2008;16 Suppl 2:S15-20.
3. Van't Hof RJ, Ralston SH. Nitric oxide and bone. Immunology 2001;103:255-61.
4. Mungrue IN, Bredt DS, Stewart DJ, Husain M. From molecules to mammals: what's NOS got to do with it? Acta Physiol Scand 2003;179:123-35.
5. Appleton CT, Pitelka V, Henry J, Beier F. Global analyses of gene expression in early experimental osteoarthritis. Arthritis Rheum 2007;56:1854-68. (Pubitemid 47110385)
6. 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: 169-79. (Pubitemid 40462025)
7. Gauci SJ, Golub SB, Tutolo L, Little CB, Sims NA, Lee ER, et al. Modulating chondrocyte hypertrophy in growth plate and osteoarthritic cartilage. J Musculoskelet Neuronal Interact 2008;8: 308-10.
8. Karsenty G, Wagner EF. Reaching a genetic and molecular understanding of skeletal development. Dev Cell 2002;2:389-406. (Pubitemid 34436569)
9. Zelzer E, Olsen BR. The genetic basis for skeletal diseases. Nature 2003;423:343-8.
10. Wagner EF, Karsenty G. Genetic control of skeletal development. Curr Opin Genet Dev 2001;11:527-32.
11. Olsen BR. Genetic regulation of skeletal patterning, differentiation, and growth. Bone 1999;25:77-9.
12. Goldring MB, Tsuchimochi K, Ijiri K. The control of chondrogenesis. J Cell Biochem 2006;97:33-44.
13. Kronenberg HM. Developmental regulation of the growth plate. Nature 2003;423:332-6.
14. Mackie EJ, Ahmed YA, Tatarczuch L, Chen KS, Mirams M. Endochondral ossification: how cartilage is converted into bone in the developing skeleton. Int J Biochem Cell Biol 2008;40:46-62. (Pubitemid 350052658)
15. Hoffman LM, Weston AD, Underhill TM. Molecular mechanisms regulating chondroblast differentiation. J Bone Joint Surg Am 2003;85-A Suppl 2:124-32.
16. Stanton LA, Underhill TM, Beier F. MAP kinases in chondrocyte differentiation. Dev Biol 2003;263:165-75.
17. Olsen BR, Reginato AM, Wang W. Bone development. Annu Rev Cell Dev Biol 2000;16:191-220.
18. Okazaki K, Iwamoto Y. Matrix gene regulation in cartilage. Clin Calcium 2006;16:1213-9. In Japanese.
19. Teixeira CC, Agoston H, Beier F. Nitric oxide, C-type natriuretic peptide and cGMP as regulators of endochondral ossification. Dev Biol 2008;319:171-8.
20. Teixeira CC, Ischiropoulos H, Leboy PS, Adams SL, Shapiro IM. Nitric oxide-nitric oxide synthase regulates key maturational events during chondrocyte terminal differentiation. Bone 2005;37: 37-45. (Pubitemid 40848416)
21. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, Laubach VE, et al. Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 1996;93:13176-81. (Pubitemid 26382789)
22. Hefler LA, Reyes CA, O'Brien WE, Gregg AR. Perinatal development of endothelial nitric oxide synthase-deficient mice. Biol Reprod 2001;64:666-73.
23. Wang G, Woods A, Agoston H, Ulici V, Glogauer M, Beier F. Genetic ablation of Rac1 in cartilage results in chondrodysplasia. Dev Biol 2007;306:612-23. (Pubitemid 46873537)
24. Ulici V, Hoenselaar KD, Agoston H, McErlain DD, Umoh J, Chakrabarti S, et al. The role of Akt1 in terminal stages of endochondral bone formation: angiogenesis and ossification. Bone 2009;45:1133-45.
25. Solomon LA, Li JR, Berube NG, Beier F. Loss of ATRX in chondrocytes has minimal effects on skeletal development. PLoS One 2009;4:e7106.
26. James CG, Appleton CT, Ulici V, Underhill TM, Beier F. Microarray analyses of gene expression during chondrocyte differentiation identifies novel regulators of hypertrophy. Mol Biol Cell 2005;16:5316-33.
27. Halawani D, Mondeh R, Stanton LA, Beier F. p38 MAP kinase signaling is necessary for rat chondrosarcoma cell proliferation. Oncogene 2004;23:3726-31.
28. Wang G, Woods A, Sabari S, Pagnotta L, Stanton LA, Beier F. RhoA/ROCK signaling suppresses hypertrophic chondrocyte differentiation. J Biol Chem 2004;279:13205-14.
29. Agoston H, Khan S, James CG, Gillespie JR, Serra R, Stanton LA, et al. C-type natriuretic peptide regulates endochondral bone growth through p38 MAP kinase-dependent and -independent pathways. BMC Dev Biol 2007;7:18.
30. Ulici V, Hoenselaar KD, Gillespie JR, Beier F. The PI3K pathway regulates endochondral bone growth through control of hypertrophic chondrocyte differentiation. BMC Dev Biol 2008;8:40.
31. Woods A, Wang G, Beier F. RhoA/ROCK signaling regulates Sox9 expression and actin organization during chondrogenesis. J Biol Chem 2005;280:11626-34.
32. Beier F. Cell-cycle control and the cartilage growth plate. J Cell Physiol 2005;202:1-8. (Pubitemid 39603357)
33. Beier F, Ali Z, Mok D, Taylor AC, Leask T, Albanese C, et al. TGFβ and PTHrP control chondrocyte proliferation by activating cyclin D1 expression. Mol Biol Cell 2001;12:3852-63. (Pubitemid 34001078)
34. James CG, Woods A, Underhill TM, 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.
35. Woods A, James CG, Wang G, Dupuis H, Beier F. Control of chondrocyte gene expression by actin dynamics: a novel role of cholesterol/Rorα signaling in endochondral bone growth. J Cell Mol Med 2009;13:3497-516.
36. Hwang PM, Byrne DH, Kitos PA. Effects of molecular oxygen on chick limb bud chondrogenesis. Differentiation 1988;37:14-9.
37. Koshiji M, Huang LE. Dynamic balancing of the dual nature of HIF-1α for cell survival. Cell Cycle 2004;3:853-4. (Pubitemid 40179457)
38. Schipani E, Ryan HE, Didrickson S, Kobayashi T, Knight M, Johnson RS. Hypoxia in cartilage: HIF-1α is essential for chondrocyte growth arrest and survival. Genes Dev 2001;15:2865-76. (Pubitemid 33042056)
39. 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;98:4016-21.
40. Pfeifer A, Aszodi A, Seidler U, Ruth P, Hofmann F, Fassler R. Intestinal secretory defects and dwarfism in mice lacking cGMP-dependent protein kinase II. Science 1996;274:2082-6. (Pubitemid 27020701)
41. Foster MW, Hess DT, Stamler JS. Protein S-nitrosylation in health and disease: a current perspective. Trends Mol Med 2009;15: 391-404.
42. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 2005;6:150-66.
43. Beier F, Lee RJ, Taylor AC, Pestell RG, LuValle P. Identification of the cyclin D1 gene as a target of activating transcription factor 2 in chondrocytes. Proc Natl Acad Sci U S A 1999;96:1433-8. (Pubitemid 29098468)
44. Aguirre J, Buttery L, O'Shaughnessy M, Afzal F, Fernandez de Marticorena I, Hukkanen M, et al. Endothelial nitric oxide synthase gene-deficient mice demonstrate marked retardation in postnatal bone formation, reduced bone volume, and defects in osteoblast maturation and activity. Am J Pathol 2001;158: 247-57.