Current understanding on the molecular basis of chondrogenesis

Clinical Pediatric Endocrinology

Volumn 23, Issue 1, 2014, Pages 1-8

  Michigami, Toshimi ^a  

^a RESEARCH INSTITUTE FOR MATERNAL AND CHILD HEALTH   (Japan)

Author keywords

Chondrocyte; Differentiation; Extracellular matrix; Growth factors; Transcription factors

Indexed keywords

TRANSCRIPTION FACTOR;

CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CHONDROGENESIS; DISEASE ASSOCIATION; EPIGENETICS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENE MUTATION; HUMAN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION;

EID: 84893472204     PISSN: 09185739     EISSN: 13477358     Source Type: Journal    
DOI: 10.1297/cpe.23.1     Document Type: Review

References (70)

1. Wagner EF, Karsenty G. Genetic control of skeletal development. Curr Opin Genet Dev 2001;11: 527-32. [Medline] [CrossRef]
2. Kronenberg HM. Developmental regulation of the growth plate. Nature 2003;423: 332-6. [Medline] [CrossRef]
3. Michigami T. Regulatory mechanisms for the development of growth plate cartilage. Cell Mol Life Sci 2013: [CrossRef] [Medline]
4. Zelzer E, Mamluk R, Ferrara N, Johnson RS, Schipani E, Olsen BR. VEGFA is necessary for chondrocyte survival during bone development. Development 2004;131: 2161-71. [Medline] [CrossRef]
5. Stickens D, Behonick DJ, Ortega N, Heyer B, Hartenstein B, Yu Y, et al. Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development 2004;131: 5883-95. [Medline] [CrossRef]
6. Foster JW, Dominguez-Steglich MA, Guioli S, Kwok C, Weller PA, Stevanovic M, et al. Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 1994;372: 525-30. [Medline] [CrossRef]
7. Wagner T, Wirth J, Meyer J, Zabel B, Held M, Zimmer J, et al. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 1994;79: 1111-20. [Medline] [CrossRef]
8. Akiyama H, Lefebvre V. Unraveling the transcriptional regulatory machinery in chondrogenesis. J Bone Miner Metab 2011;29: 390-5. [Medline] [CrossRef]
9. 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: 2336-46. [Medline]
10. Lefebvre V, Li P, de Crombrugghe B. A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene. EMBO J 1998;17: 5718-33. [Medline] [CrossRef]
11. Akiyama H, Chaboissier MC, Martin JF, Schedl A, de Crombrugghe B. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 2002;16: 2813-28. [Medline] [CrossRef]
12. Vale-Cruz DS, Ma Q, Syme J, LuValle PA. Activating transcription factor-2 affects skeletal growth by modulating pRb gene expression. Mech Dev 2008;125: 843-56. [Medline] [CrossRef]
13. Wang ZQ, Ovitt C, Grigoriadis AE, MohleSteinlein U, Ruther U, Wagner EF. Bone and haematopoietic defects in mice lacking c-fos. Nature 1992;360: 741-5. [Medline] [CrossRef]
14. Yoshida CA, Komori T. Role of Runx proteins in chondrogenesis. Crit Rev Eukaryot Gene Expr 2005;15: 243-54. [Medline] [CrossRef]
15. Yoshida CA, Yamamoto H, Fujita T, Furuichi T, Ito K, Inoue K, et al. Runx2 and Runx3 are essential for chondrocyte maturation, and Runx2 regulates limb growth through induction of Indian hedgehog. Genes Dev 2004;18: 952-63. [Medline] [CrossRef]
16. Selvamurugan N, Kwok S, Partridge NC. Smad3 interacts with JunB and Cbfa1/Runx2 for transforming growth factor-beta1-stimulated collagenase-3 expression in human breast cancer cells. J Biol Chem 2004;279: 27764-73. [Medline] [CrossRef]
17. Zheng Q, Zhou G, Morello R, Chen Y, Garcia-Rojas X, Lee B. Type X collagen gene regulation by Runx2 contributes directly to its hypertrophic chondrocyte-specific expression in vivo. J Cell Biol 2003;162: 833-42. [Medline] [CrossRef]
18. Dy P, Wang W, Bhattaram P, Wang Q, Wang L, Ballock RT, et al. Sox9 directs hypertrophic maturation and blocks osteoblast differentiation of growth plate chondrocytes. Dev Cell 2012;22: 597-609. [Medline] [CrossRef]
19. Hinoi E, Bialek P, Chen YT, Rached MT, Groner Y, Behringer RR, et al. Runx2 inhibits chondrocyte proliferation and hypertrophy through its expression in the perichondrium. Genes Dev 2006;20: 2937-42. [Medline] [CrossRef]
20. Arnold MA, Kim Y, Czubryt MP, Phan D, McAnally J, Qi X, et al. MEF2C transcription factor controls chondrocyte hypertrophy and bone development. Dev Cell 2007;12: 377-89. [Medline] [CrossRef]
21. Kozhemyakina E, Cohen T, Yao TP, Lassar AB. Parathyroid hormone-related peptide represses chondrocyte hypertrophy through a protein phosphatase 2A/histone deacetylase 4/ MEF2 pathway. Mol Cell Biol 2009;29: 5751-62. [Medline] [CrossRef]
22. Satokata I, Ma L, Ohshima H, Bei M, Woo I, Nishizawa K, et al. Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat Genet 2000;24: 391-5. [Medline] [CrossRef]
23. Amano K, Ichida F, Sugita A, Hata K, Wada M, Takigawa Y, et al. MSX2 stimulates chondrocyte maturation by controlling Ihh expression. J Biol Chem 2008;283: 29513-21. [Medline] [CrossRef]
24. Karreth F, Hoebertz A, Scheuch H, Eferl R, Wagner EF. The AP1 transcription factor Fra2 is required for efficient cartilage development. Development 2004;131: 5717-25. [Medline] [CrossRef]
25. Ionescu A, Kozhemyakina E, Nicolae C, Kaestner KH, Olsen BR, Lassar AB. FoxA family members are crucial regulators of the hypertrophic chondrocyte differentiation program. Dev Cell 2012;22: 927-39. [Medline] [CrossRef]
26. 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: 2865-76. [Medline]
27. Maes C, Araldi E, Haigh K, Khatri R, Van Looveren R, Giacia AJ, et al. VEGF-independent cell-autonomous functions of HIF-1alpha regulating oxygen consumption in fetal cartilage are critical for chondrocyte survival. J Bone Miner Res 2012;27: 596-609. [Medline] [CrossRef]
28. Ornitz DM. FGF signaling in the developing endochondral skeleton. Cytokine Growth Factor Rev 2005;16: 205-13. [Medline] [CrossRef]
29. Rousseau F, Bonaventure J, Legeai-Mallet L, Pelet A, Rozet JM, Maroteaux P, et al. Mutations in the gene encoding fibroblast growth factor receptor-3 in achondroplasia. Nature 1994;371: 252-4. [Medline] [CrossRef]
30. Bellus GA, McIntosh I, Smith EA, Aylsworth AS, Kaltlla I, Horton WA, et al. A recurrent mutation in the tyrosine kinase domain of fibroblast growth factor receptor 3 causes hypochondroplasia. Nat Genet 1995;10: 357-9. [Medline] [CrossRef]
31. Tavormina PL, Shiang R, Thompson LM, Zhu YZ, Wilkin DJ, Lachman RS, et al. Thanatophoric dysplasia (types I and II) caused by distinct mutations in fibroblast growth factor receptor 3. Nat Genet 1995;9: 321-8. [Medline] [CrossRef]
32. Deng C, Wynshaw-Boris A, Zhou F, Kuo A, Leder P. Fibroblast growth factor receptor 3 is a negative regulator of bone growth. Cell 1996;84: 911-21. [Medline] [CrossRef]
33. Peters K, Ornitz D, Werner S, Williams L. Unique expression pattern of the FGF receptor 3 gene during mouse organogenesis. Dev Biol 1993;155: 423-30. [Medline] [CrossRef]
34. Peters KG, Werner S, Chen G, Williams LT. Two FGF receptor genes are differentially expressed in epithelial and mesenchymal tissues during limb formation and organogenesis in the mouse. Development 1992;114: 233-43. [Medline]
35. Chen L, Adar R, Yang X, Monsonego EO, Li C, Hauschka PV, et al. Gly369Cys mutation in mouse FGFR3 causes achondroplasia by affecting both chondrogenesis and osteogenesis. J Clin Invest 1999;104: 1517-25. [Medline] [CrossRef]
36. Dailey L, Laplantine E, Priore R, Basilico C. A network of transcriptional and signaling events is activated by FGF to induce chondrocyte growth arrest and differentiation. J Cell Biol 2003;161: 1053-66. [Medline] [CrossRef]
37. Li C, Chen L, Iwata T, Kitagawa M, Fu XY, Deng CX. A Lys644Glu substitution in fibroblast growth factor receptor 3 (FGFR3) causes dwarfism in mice by activation of STATs and ink4 cell cycle inhibitors. Hum Mol Genet 1999;8: 35-44. [Medline] [CrossRef]
38. Ohbayashi N, Shibayama M, Kurotaki Y, Imanishi M, Fujimori T, Itoh N, et al. FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis. Genes Dev 2002;16: 870-9. [Medline] [CrossRef]
39. Liu Z, Xu J, Colvin JS, Ornitz DM. Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18. Genes Dev 2002;16: 859-69. [Medline] [CrossRef]
40. Kronenberg HM. PTHrP and skeletal development. Ann NY Acad Sci 2006;1068: 1-13. [Medline] [CrossRef]
41. St-Jacques B, Hammerschmidt M, McMahon AP. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 1999;13: 2072-86. [Medline] [CrossRef]
42. Kobayashi T, Soegiarto DW, Yang Y, Lanske B, Schipani E, McMahon AP, et al. Indian hedgehog stimulates periarticular chondrocyte differentiation to regulate growth plate length independently of PTHrP. J Clin Invest 2005;115: 1734-42. [Medline] [CrossRef]
43. Mak KK, Kronenberg HM, Chuang PT, Mackem S, Yang Y. Indian hedgehog signals independently of PTHrP to promote chondrocyte hypertrophy. Development 2008;135: 1947-56. [Medline] [CrossRef]
44. 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 USA 2001;98: 4016-21. [Medline] [CrossRef]
45. Yasoda A, Ogawa Y, Suda M, Tamura N, Mori K, Sakuma Y, et al. Natriuretic peptide regulation of endochondral ossification. Evidence for possible roles of the C-type natriuretic peptide/guanylyl cyclase-B pathway. J Biol Chem 1998;273: 11695-700. [Medline] [CrossRef]
46. Yasoda A, Komatsu Y, Chusho H, Miyazawa T, Ozasa A, Miura M, et al. Overexpression of CNP in chondrocytes rescues achondroplasia through a MAPK-dependent pathway. Nat Med 2004;10: 80-6. [Medline] [CrossRef]
47. Bartels CF, Bukulmez H, Padayatti P, Rhee DK, van Ravenswaaji-Arts C, Pauli RM, et al. Mutations in the transmembrane natriuretic peptide receptor NPR-B impair skeletal growth and cause acromesomelic dysplasia, type Maroteaux. Am J Hum Genet 2004;75: 27-34. [Medline] [CrossRef]
48. Hachiya R, Ohashi Y, Kamei Y, Suganami T, Mochizuki H, Mitsui N, et al. Intact kinase homology domain of natriuretic peptide receptor-B is essential for skeletal development. J Clin Endocrinol Metab 2007;92: 4009-14. [Medline] [CrossRef]
49. Miura K, Namba N, Fujiwara M, Ohata Y, Ishida H, Kitaoka T, et al. An overgrowth disorder associated with excessive production of cGMP due to a gain-of-function mutation of the natriuretic peptide receptor 2 gene. PLoS One 2012;7: e42180. [Medline] [CrossRef]
50. 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. [Medline] [CrossRef]
51. Pogue R, Lyons K. BMP signaling in the cartilage growth plate. Curr Top Dev Biol 2006;76: 1-48. [Medline] [CrossRef]
52. 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. [Medline] [CrossRef]
53. Olney RC, Mougey EB. Expression of the components of the insulin-like growth factor axis across the growth-plate. Mol Cell Endocrinol 1999;156: 63-71. [Medline] [CrossRef]
54. Tavella S, Raffo P, Tacchetti C, Cancedda R, Castagnola P. N-CAM and N-cadherin expression during in vitro chondrogenesis. Exp Cell Res 1994;215: 354-62. [Medline] [CrossRef]
55. Oberlender SA, Tuan RS. Expression and functional involvement of N-cadherin in embryonic limb chondrogenesis. Development 1994;120: 177-87. [Medline]
56. Ffrench-Constant C, Colognato H. Integrins: versatile integrators of extracellular signals. Trends Cell Biol 2004;14: 678-86. [Medline] [CrossRef]
57. Loeser RF. Chondrocyte integrin expression and function. Biorheology 2000;37: 109-16. [Medline]
58. Aszodi A, Hunziker EB, Brakebusch C, Fassler R. Beta1 integrins regulate chondrocyte rotation, G1 progression, and cytokinesis. Genes Dev 2003;17: 2465-79. [Medline] [CrossRef]
59. Terpstra L, Prud'homme J, Arabian A, Takeda S, Karsenty G, Dedhar S, et al. Reduced chondrocyte proliferation and chondrodysplasia in mice lacking the integrin-linked kinase in chondrocytes. J Cell Biol 2003;162: 139-48. [Medline] [CrossRef]
60. Mertz EL, Facchini M, Pham AT, Gualeni B, De Leonardis F, Rossi A, et al. Matrix disruptions, growth, and degradation of cartilage with impaired sulfation. J Biol Chem 2012;287: 22030-42. [Medline] [CrossRef]
61. Sato T, Kudo T, Ikehara Y, Ogawa H, Hirano T, Kiyohara K, et al. Chondroitin sulfate N-acetylgalactosaminyltransferase 1 is necessary for normal endochondral ossification and aggrecan metabolism. J Biol Chem 2011;286: 5803-12. [Medline] [CrossRef]
62. Settembre C, Arteaga-Solis E, McKee MD, de Pablo R, Al Awqati Q, Ballabio A, et al. Proteoglycan desulfation determines the efficiency of chondrocyte autophagy and the extent of FGF signaling during endochondral ossification. Genes Dev 2008;22: 2645-50. [Medline] [CrossRef]
63. Koshimizu T, Kawai M, Kondou H, Tachikawa K, Sakai N, Ozono K, et al. Vinculin functions as regulator of chondrogenesis. J Biol Chem 2012;287: 15760-75. [Medline] [CrossRef]
64. Vega RB, Matsuda K, Oh J, Barbosa AC, Yang X, Meadows E, et al. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 2004;119: 555-66. [Medline] [CrossRef]
65. Hong S, Derfoul A, Pereira-Mouries L, Hall DJ. A novel domain in histone deacetylase 1 and 2 mediates repression of cartilage-specific genes in human chondrocytes. FASEB J 2009;23: 3539-52. [Medline] [CrossRef]
66. Zimmermann P, Boeuf S, Dickhut A, Boehmer S, Olek S, Richter W. Correlation of COL10A1 induction during chondrogenesis of mesenchymal stem cells with demethylation of two CpG sites in the COL10A1 promoter. Arthritis Rheum 2008;58: 2743-53. [Medline] [CrossRef]
67. Kobayashi T, Lu J, Cobb BS, Rodda SJ, McMahon AP, Schipani E, et al. Dicer-dependent pathways regulate chondrocyte proliferation and differentiation. Proc Natl Acad Sci USA 2008;105: 1949-54. [Medline] [CrossRef]
68. Miyaki S, Sato T, Inoue A, Otsuki S, Ito Y, Yokoyama S, et al. MicroRNA-140 plays dual roles in both cartilage development and homeostasis. Genes Dev 2010;24: 1173-85. [Medline] [CrossRef]
69. Yang B, Guo H, Zhang Y, Chen L, Ying D, Dong S. MicroRNA-145 regulates chondrogenic differentiation of mesenchymal stem cells by targeting Sox9. PLoS One 2011;6: e21679. [Medline] [CrossRef]
70. Lin EA, Kong L, Bai XH, Luan Y, Liu CJ. miR-199a, a bone morphogenic protein 2-responsive MicroRNA, regulates chondrogenesis via direct targeting to Smad1. J Biol Chem 2009;284: 11326-35. [Medline] [CrossRef]