Interaction of TGFβ and bmp signaling pathways during chondrogenesis

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Keller, Bettina ^a   Yang, Tao ^a   Chen, Yuqing ^a   Munivez, Elda ^a   Bertin, Terry ^a   Zabel, Bernhard ^b   Lee, Brendan ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; SMAD1 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; BMP1 PROTEIN, MOUSE; BMP2 PROTEIN, MOUSE; BONE MORPHOGENETIC PROTEIN 2; PROCOLLAGEN C PROTEINASE; SMAD PROTEIN;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CELL PROLIFERATION; CHONDROGENESIS; CONTROLLED STUDY; ENCHONDRAL OSSIFICATION; EXTRACELLULAR MATRIX; GROWTH INHIBITION; INTRACELLULAR SIGNALING; LIGAND BINDING; MOUSE; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN TARGETING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL MODEL; CARTILAGE; CELL DIFFERENTIATION; CYTOLOGY; GROWTH PLATE; METABOLISM; PHYSIOLOGY;

MUS MUSCULUS;

ANIMALS; BONE MORPHOGENETIC PROTEIN 1; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEINS; CARTILAGE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDROGENESIS; GROWTH PLATE; MICE; MODELS, ANIMAL; RECEPTOR CROSS-TALK; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA;

EID: 79551527246     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016421     Document Type: Article

References (48)

1. Massague J, Seoane J, Wotton D (2005) Smad transcription factors. Genes Dev 19: 2783-2810.
2. Miyazono K, Kusanagi K, Inoue H (2001) Divergence and convergence of TGF-beta/BMP signaling. J Cell Physiol 187: 265-276.
3. Denker AE, Haas AR, Nicoll SB, Tuan RS (1999) Chondrogenic differentiation of murine C3H10T1/2 multipotential mesenchymal cells: I. Stimulation by bone morphogenetic protein-2 in high-density micromass cultures. Differentiation 64: 67-76.
4. Yoon BS, Ovchinnikov DA, Yoshii I, Mishina Y, Behringer RR, et al. (2005) Bmpr1a and Bmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proc Natl Acad Sci U S A 102: 5062-5067.
5. Minina E, Wenzel HM, Kreschel C, Karp S, Gaffield W, et al. (2001) BMP and Ihh/PTHrP signaling interact to coordinate chondrocyte proliferation and differentiation. Development 128: 4523-4534.
6. Pathi S, Rutenberg JB, Johnson RL, Vortkamp A (1999) Interaction of Ihh and BMP/Noggin signaling during cartilage differentiation. Dev Biol 209: 239-253.
7. Lyons KM, Hogan BL, Robertson EJ (1995) Colocalization of BMP 7 and BMP 2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech Dev 50: 71-83.
8. Zou H, Wieser R, Massague J, Niswander L (1997) Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev 11: 2191-2203.
9. Zhang D, Schwarz EM, Rosier RN, Zuscik MJ, Puzas JE, et al. (2003) ALK2 functions as a BMP type I receptor and induces Indian hedgehog in chondrocytes during skeletal development. J Bone Miner Res 18: 1593-1604.
10. Yoon BS, Lyons KM (2004) Multiple functions of BMPs in chondrogenesis. J Cell Biochem 93: 93-103.
11. Brunet LJ, McMahon JA, McMahon AP, Harland RM (1998) Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science 280: 1455-1457.
12. Kobayashi T, Lyons KM, McMahon AP, Kronenberg HM (2005) BMP signaling stimulates cellular differentiation at multiple steps during cartilage development. Proc Natl Acad Sci U S A 102: 18023-18027.
13. Retting KN, Song B, Yoon BS, Lyons KM (2009) BMP canonical Smad signaling through Smad1 and Smad5 is required for endochondral bone formation. Development 136: 1093-1104.
14. Sandberg M, Autio-Harmainen H, Vuorio E (1988) Localization of the expression of types I, III, and IV collagen, TGF-beta 1 and c-fos genes in developing human calvarial bones. Dev Biol 130: 324-334.
15. Gatherer D, Ten Dijke P, Baird DT, Akhurst RJ (1990) Expression of TGF-beta isoforms during first trimester human embryogenesis. Development 110: 445-460.
16. Pelton RW, Dickinson ME, Moses HL, Hogan BL (1990) In situ hybridization analysis of TGF beta 3 RNA expression during mouse development: comparative studies with TGF beta 1 and beta 2. Development 110: 609-620.
17. Millan FA, Denhez F, Kondaiah P, Akhurst RJ (1991) Embryonic gene expression patterns of TGF beta 1, beta 2 and beta 3 suggest different developmental functions in vivo. Development 111: 131-143.
18. Pelton RW, Saxena B, Jones M, Moses HL, Gold LI (1991) Immunohistochemical localization of TGF beta 1, TGF beta 2, and TGF beta 3 in the mouse embryo: expression patterns suggest multiple roles during embryonic development. J Cell Biol 115: 1091-1105.
19. Serra R, Karaplis A, Sohn P (1999) Parathyroid hormone-related peptide (PTHrP)-dependent and -independent effects of transforming growth factor beta (TGF-beta) on endochondral bone formation. J Cell Biol 145: 783-794.
20. Yang X, Chen L, Xu X, Li C, Huang C, et al. (2001) TGF-beta/Smad3 signals repress chondrocyte hypertrophic differentiation and are required for maintaining articular cartilage. J Cell Biol 153: 35-46.
21. Baffi MO, Slattery E, Sohn P, Moses HL, Chytil A, et al. (2004) Conditional deletion of the TGF-beta type II receptor in Col2a expressing cells results in defects in the axial skeleton without alterations in chondrocyte differentiation or embryonic development of long bones. Dev Biol 276: 124-142.
22. Seo HS, Serra R (2007) Deletion of Tgfbr2 in Prx1-cre expressing mesenchyme results in defects in development of the long bones and joints. Dev Biol 310: 304-316.
23. Sakou T, Onishi T, Yamamoto T, Nagamine T, Sampath T, et al. (1999) Localization of Smads, the TGF-beta family intracellular signaling components during endochondral ossification. J Bone Miner Res 14: 1145-1152.
24. Tremblay KD, Dunn NR, Robertson EJ (2001) Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 128: 3609-3621.
25. Ovchinnikov DA, Deng JM, Ogunrinu G, Behringer RR (2000) Col2a1-directed expression of Cre recombinase in differentiating chondrocytes in transgenic mice. Genesis 26: 145-146.
26. Yew KH, Hembree M, Prasadan K, Preuett B, McFall C, et al. (2005) Cross-talk between bone morphogenetic protein and transforming growth factor-beta signaling is essential for exendin-4-induced insulin-positive differentiation of AR42J cells. J Biol Chem 280: 32209-32217.
27. Wrighton KH, Lin X, Yu PB, Feng XH (2009) Transforming Growth Factor {beta} Can Stimulate Smad1 Phosphorylation Independently of Bone Morphogenic Protein Receptors. J Biol Chem 284: 9755-9763.
28. Giacomini D, Paez-Pereda M, Stalla J, Stalla GK, Arzt E (2009) Molecular interaction of BMP-4, TGF-beta, and estrogens in lactotrophs: impact on the PRL promoter. Mol Endocrinol 23: 1102-1114.
29. Pogue R, Lyons K (2006) BMP signaling in the cartilage growth plate. Curr Top Dev Biol 76: 1-48.
30. Song B, Estrada KD, Lyons KM (2009) Smad signaling in skeletal development and regeneration. Cytokine Growth Factor Rev 20: 379-388.
31. Goldring MB, Tsuchimochi K, Ijiri K (2006) The control of chondrogenesis. J Cell Biochem 97: 33-44.
32. Zhang Y, Feng X, We R, Derynck R (1996) Receptor-associated Mad homologues synergize as effectors of the TGF-beta response. Nature 383: 168-172.
33. Feng XH, Filvaroff EH, Derynck R (1995) Transforming growth factor-beta (TGF-beta)-induced down-regulation of cyclin A expression requires a functional TGF-beta receptor complex. Characterization of chimeric and truncated type I and type II receptors. J Biol Chem 270: 24237-24245.
34. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL (2003) Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 5: 410-421.
35. Serra R, Johnson M, Filvaroff EH, LaBorde J, Sheehan DM, et al. (1997) Expression of a truncated, kinase-defective TGF-beta type II receptor in mouse skeletal tissue promotes terminal chondrocyte differentiation and osteoarthritis. J Cell Biol 139: 541-552.
36. Yang T, Mendoza-Londono R, Lu H, Tao J, Li K, et al. (2010) E-selectin ligand-1 regulates growth plate homeostasis in mice by inhibiting the intracellular processing and secretion of mature TGF-beta. J Clin Invest 120: 2474-2485.
37. Chen Y, Dabovic B, Annes JP, Rifkin DB (2002) Latent TGF-beta binding protein-3 (LTBP-3) requires binding to TGF-beta for secretion. FEBS Lett 517: 277-280.
38. Wang S, Hirschberg R (2003) BMP7 antagonizes TGF-beta -dependent fibrogenesis in mesangial cells. Am J Physiol Renal Physiol 284: F1006-1013.
39. Izumi N, Mizuguchi S, Inagaki Y, Saika S, Kawada N, et al. (2006) BMP-7 opposes TGF-beta1-mediated collagen induction in mouse pulmonary myofibroblasts through Id2. Am J Physiol Lung Cell Mol Physiol 290: L120-126.
40. Spinella-Jaegle S, Roman-Roman S, Faucheu C, Dunn FW, Kawai S, et al. (2001) Opposite effects of bone morphogenetic protein-2 and transforming growth factor-beta1 on osteoblast differentiation. Bone 29: 323-330.
41. Faucheux C, Ulysse F, Bareille R, Reddi AH, Amedee J (1997) Opposing actions of BMP3 and TGF beta 1 in human bone marrow stromal cell growth and differentiation. Biochem Biophys Res Commun 241: 787-793.
42. Mehlhorn AT, Niemeyer P, Kaschte K, Muller L, Finkenzeller G, et al. (2007) Differential effects of BMP-2 and TGF-beta1 on chondrogenic differentiation of adipose derived stem cells. Cell Prolif 40: 809-823.
43. Chang H, Huylebroeck D, Verschueren K, Guo Q, Matzuk MM, et al. (1999) Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development 126: 1631-1642.
44. Zhou G, Garofalo S, Mukhopadhyay K, Lefebvre V, Smith CN, et al. (1995) A 182 bp fragment of the mouse pro alpha 1(II) collagen gene is sufficient to direct chondrocyte expression in transgenic mice. J Cell Sci 108: 3677-3684.
45. Hsiao YC, Chang HH, Tsai CY, Jong YJ, Horng LS, et al. (2004) Coat colortagged green mouse with EGFP expressed from the RNA polymerase II promoter. Genesis 39: 122-129.
46. Zufferey R, Donello JE, Trono D, Hope TJ (1999) Woodchuck hepatitis virus posttranscriptional regulatory element enhances expression of transgenes delivered by retroviral vectors. J Virol 73: 2886-2892.
47. Morello R, Bertin TK, Schlaubitz S, Shaw CA, Kakuru S, et al. (2008) Brachysyndactyly caused by loss of Sfrp2 function. J Cell Physiol 217: 127-137.
48. Napierala D, Sam K, Morello R, Zheng Q, Munivez E, et al. (2008) Uncoupling of chondrocyte differentiation and perichondrial mineralization underlies the skeletal dysplasia in tricho-rhino-phalangeal syndrome. Hum Mol Genet 17: 2244-2254.