Bone Morphogenic Protein (BMP) signaling up-regulates neutral sphingomyelinase 2 to suppress chondrocyte maturation via the Akt protein signaling pathway as a negative feedback mechanism

Journal of Biological Chemistry

Volumn 289, Issue 12, 2014, Pages 8135-8150

  Kakoi, Hironori ^a   Maeda, Shingo ^a   Shinohara, Naohiro ^a   Matsuyama, Kanehiro ^a   Imamura, Katsuyuki ^a   Kawamura, Ichiro ^a   Nagano, Satoshi ^a   Setoguchi, Takao ^a   Yokouchi, Masahiro ^a   Ishidou, Yasuhiro ^a   Komiya, Setsuro ^a  

^a KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMATERIALS; BIOMINERALIZATION; BONE; CARTILAGE; CELL DEATH; CELL SIGNALING; CERAMIDES; FEEDBACK CONTROL; MAMMALS; PROTEINS;

BONE MORPHOGENIC PROTEIN; CHONDROCYTE MATURATION; ENDOCHONDRAL OSSIFICATION; HYPERTROPHIC CHONDROCYTES; MAMMALIAN TARGET; NEGATIVE FEEDBACK MECHANISM; PROTEIN SIGNALING; SPHINGOMYELINASE;

BODY FLUIDS;

3,3' (1,4 PHENYLENE)BIS[N [4 (4,5 DIHYDRO 1H IMIDAZOL 2 YL)PHENYL]ACRYLAMIDE]; 8 [4 (1 AMINOCYCLOBUTYL)PHENYL] 9 PHENYL 1,2,4 TRIAZOLO[3,4 F][1,6]NAPHTHYRIDIN 3(2H) ONE; BONE MORPHOGENETIC PROTEIN; CERAMIDE; HYALURONAN SYNTHASE 2; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN S6; SMALL INTERFERING RNA; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELINASE 2; SYNTHETASE; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIFICATION; CARTILAGE CELL; CELL DIFFERENTIATION; CELL MATURATION; CHONDROGENESIS; CONTROLLED STUDY; EMBRYO; ENZYME PHOSPHORYLATION; FEEDBACK SYSTEM; GENE; GENE OVEREXPRESSION; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SMPD3 GENE;

AKT; BONE MORPHOGENETIC PROTEIN (BMP); CERAMIDE; CHONDROGENESIS; HYALURONAN SYNTHASE 2; SPHINGOMYELIN PHOSPHODIESTERASE 3; SPHINGOMYELINASE;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; CELLS, CULTURED; CHONDROCYTES; CORE BINDING FACTOR ALPHA 1 SUBUNIT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, INBRED C57BL; ORGAN CULTURE TECHNIQUES; PROTO-ONCOGENE PROTEINS C-AKT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 84896974492     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.509331     Document Type: Article

References (69)

1. Bi, W., Deng, J. M., Zhang, Z., Behringer, R. R., and de Crombrugghe, B. (1999) Sox9 is required for cartilage formation. Nat. Genet. 22, 85-89 (Pubitemid 29214811)
2. Akiyama, H., Chaboissier, M. C., Martin, J. F., Schedl, A., and de Crombrugghe, B. (2002) 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. 16, 2813-2828 (Pubitemid 35253149)
3. Provot, S., and Schipani, E. (2005) Molecular mechanisms of endochondral bone development. Biochem. Biophys. Res. Commun. 328, 658-665 (Pubitemid 40208303)
4. Enomoto, H., Enomoto-Iwamoto, M., Iwamoto, M., Nomura, S., Himeno, M., Kitamura, Y., Kishimoto, T., and Komori, T. (2000) Cbfa1 is a positive regulatory factor in chondrocyte maturation. J. Biol. Chem. 275, 8695-8702 (Pubitemid 30180221)
5. Zheng, Q., Zhou, G., Morello, R., Chen, Y., Garcia-Rojas, X., and Lee, B. (2003) Type X collagen gene regulation by Runx2 contributes directly to its hypertrophic chondrocyte-specific expression in vivo. J. Cell Biol. 162, 833-842 (Pubitemid 37087723)
6. Kronenberg, H. M. (2003) Developmental regulation of the growth plate. Nature 423, 332-336
7. Miyazono, K., Maeda, S., and Imamura, T. (2005) BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev. 16, 251-263 (Pubitemid 40910315)
8. Guo, X., and Wang, X. F. (2009) Signaling cross-talk between TGF-β/BMP and other pathways. Cell Res. 19, 71-88
9. Pogue, R., and Lyons, K. (2006) BMP signaling in the cartilage growth plate. Curr. Top. Dev. Biol. 76, 1-48 (Pubitemid 44760537)
10. Hatakeyama, Y., Tuan, R. S., and Shum, L. (2004) Distinct functions of BMP4 and GDF5 in the regulation of chondrogenesis. J. Cell. Biochem. 91, 1204-1217
11. Haas, A. R., and Tuan, R. S. (1999) Chondrogenic differentiation of murine C3H10T1/2 multipotential mesenchymal cells: II. Stimulation by bone morphogenetic protein-2 requires modulation of N-cadherin expression and function. Differentiation 64, 77-89 (Pubitemid 29077835)
12. Fujii, M., Takeda, K., Imamura, T., Aoki, H., Sampath, T. K., Enomoto, S., Kawabata, M., Kato, M., Ichijo, H., and Miyazono, K. (1999) Roles of bone morphogenetic protein type I receptors and Smad proteins in osteoblast and chondroblast differentiation. Mol. Biol. Cell 10, 3801-3813 (Pubitemid 29534026)
13. Leboy, P., Grasso-Knight, G., D'Angelo, M., Volk, S. W., Lian, J. V., Drissi, H., Stein, G. S., and Adams, S. L. (2001) Smad-Runx interactions during chondrocyte maturation. J. Bone Joint Surg. Am. 83, S15-S22
14. Valcourt, U., Gouttenoire, J., Moustakas, A., Herbage, D., and Mallein-Gerin, F. (2002) Functions of transforming growth factor-β family type I receptors and Smad proteins in the hypertrophic maturation and osteoblastic differentiation of chondrocytes. J. Biol. Chem. 277, 33545-33558
15. Tsumaki, N., Nakase, T., Miyaji, T., Kakiuchi, M., Kimura, T., Ochi, T., and Yoshikawa, H. (2002) Bone morphogenetic protein signals are required for cartilage formation and differently regulate joint development during skeletogenesis. J. Bone Miner. Res. 17, 898-906 (Pubitemid 34441907)
16. Yoon, B. S., Ovchinnikov, D. A., Yoshii, I., Mishina, Y., Behringer, R. R., and Lyons, K. M. (2005) Bmpr1a and Bmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proc. Natl. Acad. Sci. U.S.A. 102, 5062-5067
17. Retting, K. N., Song, B., Yoon, B. S., and Lyons, K. M. (2009) BMP canonical Smad signaling through Smad1 and Smad5 is required for endochondral bone formation. Development 136, 1093-1104
18. Volk, S. W., Luvalle, P., Leask, T., and Leboy, P. S. (1998) A BMP-responsive transcriptional region in the chicken type X collagen gene. J. Bone Miner. Res. 13, 1521-1529 (Pubitemid 28465292)
19. Kempf, H., Ionescu, A., Udager, A. M., and Lassar, A. B. (2007) Prochondrogenic signals induce a competence for Runx2 to activate hypertrophic chondrocyte gene expression. Dev. Dyn. 236, 1954-1962 (Pubitemid 47076023)
20. Kobayashi, T., Lyons, K. M., McMahon, A. P., and Kronenberg, H. M. (2005) BMP signaling stimulates cellular differentiation at multiple steps during cartilage development. Proc. Natl. Acad. Sci. U.S.A. 102, 18023-18027 (Pubitemid 41798495)
21. Scotti, C., Tonnarelli, B., Papadimitropoulos, A., Scherberich, A., Schaeren, S., Schauerte, A., Lopez-Rios, J., Zeller, R., Barbero, A., and Martin, I. (2010) Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc. Natl. Acad. Sci. U.S.A. 107, 7251-7256
22. Pullig, O., Weseloh, G., Ronneberger, D., Käkönen, S., and Swoboda, B. (2000) Chondrocyte differentiation in human osteoarthritis: expression of osteocalcin in normal and osteoarthritic cartilage and bone. Calcif. Tissue Int. 67, 230-240 (Pubitemid 30648786)
23. Sandell, L. J., and Aigner, T. (2001) Articular cartilage and changes in arthritis. An introduction: cell biology of osteoarthritis. Arthritis Res. 3, 107-113 (Pubitemid 32237037)
24. Dreier, R. (2010) Hypertrophic differentiation of chondrocytes in osteoarthritis: The developmental aspect of degenerative joint disorders. Arthritis Res. Ther. 12, 216
25. Nelea, V., Luo, L., Demers, C. N., Antoniou, J., Petit, A., Lerouge, S., R Wertheimer, M., and Mwale, F. (2005) Selective inhibition of type X collagen expression in human mesenchymal stem cell differentiation on polymer substrates surface-modified by glow discharge plasma. J. Biomed. Mater. Res. A 75, 216-223 (Pubitemid 41309079)
26. Sekiya, I., Vuoristo, J. T., Larson, B. L., and Prockop, D. J. (2002) In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis. Proc. Natl. Acad. Sci. U.S.A. 99, 4397-4402 (Pubitemid 34285996)
27. Imamura, T., Takase, M., Nishihara, A., Oeda, E., Hanai, J., Kawabata, M., and Miyazono, K. (1997) Smad6 inhibits signalling by the TGF-β super-family. Nature 389, 622-626 (Pubitemid 27446182)
28. Zhu, H., Kavsak, P., Abdollah, S., Wrana, J. L., and Thomsen, G. H. (1999) A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 400, 687-693
29. Murakami, G., Watabe, T., Takaoka, K., Miyazono, K., and Imamura, T. (2003) Cooperative inhibition of bone morphogenetic protein signaling by Smurf1 and inhibitory Smads. Mol. Biol. Cell 14, 2809-2817 (Pubitemid 36871523)
30. Kawamura, I., Maeda, S., Imamura, K., Setoguchi, T., Yokouchi, M., Ishidou, Y., and Komiya, S. (2012) SnoN suppresses maturation of chondrocytes by mediating signal cross-talk between transforming growth factor-β and bone morphogenetic protein pathways. J. Biol. Chem. 287, 29101-29113
31. Obeid, L. M., Linardic, C. M., Karolak, L. A., and Hannun, Y. A. (1993) Programmed cell death induced by ceramide. Science 259, 1769-1771 (Pubitemid 23114667)
32. Sjöholm, A. (1995) Ceramide inhibits pancreatic β-cell insulin production and mitogenesis and mimics the actions of interleukin-1 β. FEBS Lett. 367, 283-286
33. Mebarek, S., Komati, H., Naro, F., Zeiller, C., Alvisi, M., Lagarde, M., Prigent, A. F., and Némoz, G. (2007) Inhibition of de novo ceramide synthesis upregulates phospholipase D and enhances myogenic differentiation. J. Cell Sci. 120, 407-416 (Pubitemid 46332504)
34. Sharma, K., and Shi, Y. (1999) The yins and yangs of ceramide. Cell Res. 9, 1-10 (Pubitemid 129623864)
35. Aubin, I., Adams, C. P., Opsahl, S., Septier, D., Bishop, C. E., Auge, N., Salvayre, R., Negre-Salvayre, A., Goldberg, M., Guénet, J. L., and Poirier, C. (2005) A deletion in the gene encoding sphingomyelin phosphodiesterase 3 (Smpd3) results in osteogenesis and dentinogenesis imperfecta in the mouse. Nat. Genet. 37, 803-805 (Pubitemid 41077104)
36. Khavandgar, Z., Poirier, C., Clarke, C. J., Li, J., Wang, N., McKee, M. D., Hannun, Y. A., and Murshed, M. (2011) A cell-autonomous requirement for neutral sphingomyelinase 2 in bone mineralization. J. Cell Biol. 194, 277-289
37. Stoffel, W., Jenke, B., Blöck, B., Zumbansen, M., and Koebke, J. (2005) Neutral sphingomyelinase 2 (smpd3) in the control of postnatal growth and development. Proc. Natl. Acad. Sci. U.S.A. 102, 4554-4559 (Pubitemid 40397150)
38. Stoffel, W., Jenke, B., Holz, B., Binczek, E., Günter, R. H., Knifka, J., Koebke, J., and Niehoff, A. (2007) Neutral sphingomyelinase (SMPD3) deficiency causes a novel form of chondrodysplasia and dwarfism that is rescued by Col2A1-driven smpd3 transgene expression. Am. J. Pathol. 171, 153-161 (Pubitemid 47339235)
39. Chae, Y. M., Heo, S. H., Kim, J. Y., Lee, J. M., Ryoo, H. M., and Cho, J. Y. (2009) Upregulation of smpd3 via BMP2 stimulation and Runx2. BMB Rep. 42, 86-90
40. Atsumi, T., Miwa, Y., Kimata, K., and Ikawa, Y. (1990) A chondrogenic cell line derived from a differentiating culture of AT805 teratocarcinoma cells. Cell Differ. Dev. 30, 109-116 (Pubitemid 20196328)
41. Goldring, M. B., Birkhead, J. R., Suen, L. F., Yamin, R., Mizuno, S., Glowacki, J., Arbiser, J. L., and Apperley, J. F. (1994) Interleukin-1 β-modulated gene expression in immortalized human chondrocytes. J. Clin. Invest. 94, 2307-2316
42. Alvarez, J., Sohn, P., Zeng, X., Doetschman, T., Robbins, D. J., and Serra, R. (2002) TGFβ2 mediates the effects of hedgehog on hypertrophic differentiation and PTHrP expression. Development 129, 1913-1924 (Pubitemid 34874206)
43. Shukunami, C., Ohta, Y., Sakuda, M., and Hiraki, Y. (1998) Sequential progression of the differentiation program by bone morphogenetic protein-2 in chondrogenic cell line ATDC5. Exp. Cell Res. 241, 1-11 (Pubitemid 28366574)
44. Yao, Y., and Wang, Y. (2013) ATDC5: an excellent in vitro model cell line for skeletal development. J. Cell. Biochem. 114, 1223-1229
45. Origuchi, N., Ishidou, Y., Nagamine, T., Onishi, T., Matsunaga, S., Yoshida, H., and Sakou, T. (1998) The spatial and temporal immunolocalization of TGF-β 1 and bone morphogenetic protein-2/-4 in phallic bone formation in inbred Sprague Dawley male rats. In Vivo 12, 473-480
46. Heinonen, J., Taipaleenmäki, H., Roering, P., Takatalo, M., Harkness, L., Sandholm, J., Uusitalo-Järvinen, H., Kassem, M., Kiviranta, I., Laitala-Leinonen, T., and Säämänen, A. M. (2011) Snorc is a novel cartilage specific small membrane proteoglycan expressed in differentiating and articular chondrocytes. Osteoarthritis Cartilage 19, 1026-1035
47. Korchynskyi, O., and ten Dijke, P. (2002) Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J. Biol. Chem. 277, 4883-4891 (Pubitemid 34968524)
48. Lefebvre, V., Li, P., and de Crombrugghe, B. (1998) 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. 17, 5718-5733 (Pubitemid 28445983)
49. Marchesini, N., Luberto, C., and Hannun, Y. A. (2003) Biochemical properties of mammalian neutral sphingomyelinase 2 and its role in sphingolipid metabolism. J. Biol. Chem. 278, 13775-13783 (Pubitemid 36799914)
50. Qin, J., Berdyshev, E., Poirer, C., Schwartz, N. B., and Dawson, G. (2012) Neutral sphingomyelinase 2 deficiency increases hyaluronan synthesis by up-regulation of hyaluronan synthase 2 through decreased ceramide production and activation of Akt. J. Biol. Chem. 287, 13620-13632
51. Rokutanda, S., Fujita, T., Kanatani, N., Yoshida, C. A., Komori, H., Liu, W., Mizuno, A., and Komori, T. (2009) Akt regulates skeletal development through GSK3, mTOR, and FoxOs. Dev. Biol. 328, 78-93
52. Shukunami, C., Shigeno, C., Atsumi, T., Ishizeki, K., Suzuki, F., and Hiraki, Y. (1996) Chondrogenic differentiation of clonal mouse embryonic cell line ATDC5 in vitro: differentiation-dependent gene expression of parathyroid hormone (PTH)/PTH-related peptide receptor. J. Cell Biol. 133, 457-468 (Pubitemid 26131617)
53. Matsumoto, K., Li, Y., Jakuba, C., Sugiyama, Y., Sayo, T., Okuno, M., Dealy, C. N., Toole, B. P., Takeda, J., Yamaguchi, Y., and Kosher, R. A. (2009) Conditional inactivation of Has2 reveals a crucial role for hyaluronan in skeletal growth, patterning, chondrocyte maturation and joint formation in the developing limb. Development 136, 2825-2835
54. Ulici, V., Hoenselaar, K. D., Gillespie, J. R., and Beier, F. (2008) The PI3K pathway regulates endochondral bone growth through control of hypertrophic chondrocyte differentiation. BMC Dev. Biol. 8, 40
55. Fujita, T., Azuma, Y., Fukuyama, R., Hattori, Y., Yoshida, C., Koida, M., Ogita, K., and Komori, T. (2004) Runx2 induces osteoblast and chondrocyte differentiation and enhances their migration by coupling with PI3K-Akt signaling. J. Cell Biol. 166, 85-95 (Pubitemid 38931919)
56. Kang, M. H., Kim, J. S., Seo, J. E., Oh, S. C., and Yoo, Y. A. (2010) BMP2 accelerates the motility and invasiveness of gastric cancer cells via activation of the phosphatidylinositol 3-kinase (PI3K)/Akt pathway. Exp. Cell Res. 316, 24-37
57. Bartke, N., and Hannun, Y. A. (2009) Bioactive sphingolipids: metabolism and function. J. Lipid Res. 50, S91-S96
58. Mora, A., Sabio, G., Risco, A. M., Cuenda, A., Alonso, J. C., Soler, G., and Centeno, F. (2002) Lithium blocks the PKB and GSK3 dephosphorylation induced by ceramide through protein phosphatase-2A. Cell. Signal. 14, 557-562 (Pubitemid 34230591)
59. Kolesnick, R., and Hannun, Y. A. (1999) Ceramide and apoptosis. Trends Biochem. Sci. 24, 224-225
60. Wiesner, D. A., Kilkus, J. P., Gottschalk, A. R., Quintáns, J., and Dawson, G. (1997) Anti-immunoglobulin-induced apoptosis in WEHI 231 cells involves the slow formation of ceramide from sphingomyelin and is blocked by bcl-XL. J. Biol. Chem. 272, 9868-9876 (Pubitemid 27171654)
61. Lee, J. T., Xu, J., Lee, J. M., Ku, G., Han, X., Yang, D. I., Chen, S., and Hsu, C. Y. (2004) Amyloid-β peptide induces oligodendrocyte death by activating the neutral sphingomyelinase-ceramide pathway. J. Cell Biol. 164, 123-131 (Pubitemid 38082463)
62. Grassme, H., Jekle, A., Riehle, A., Schwarz, H., Berger, J., Sandhoff, K., Kolesnick, R., and Gulbins, E. (2001) CD95 signaling via ceramide-rich membrane rafts. J. Biol. Chem. 276, 20589-20596
63. Dumitru, C. A., and Gulbins, E. (2006) TRAIL activates acid sphingomyelinase via a redox mechanism and releases ceramide to trigger apoptosis. Oncogene 25, 5612-5625 (Pubitemid 44387617)
64. Kultti, A., Kärnä, R., Rilla, K., Nurminen, P., Koli, E., Makkonen, K. M., Si, J., Tammi, M. I., and Tammi, R. H. (2010) Methyl-β-cyclodextrin suppresses hyaluronan synthesis by down-regulation of hyaluronan synthase 2 through inhibition of Akt. J. Biol. Chem. 285, 22901-22910
65. Sabatini, M., Rolland, G., Léonce, S., Thomas, M., Lesur, C., Pérez, V., de Nanteuil, G., and Bonnet, J. (2000) Effects of ceramide on apoptosis, proteoglycan degradation, and matrix metalloproteinase expression in rabbit articular cartilage. Biochem. Biophys. Res. Commun. 267, 438-444 (Pubitemid 30072570)
66. Gilbert, S. J., Blain, E. J., Jones, P., Duance, V. C., and Mason, D. J. (2006) Exogenous sphingomyelinase increases collagen and sulphated glycosaminoglycan production by primary articular chondrocytes: an in vitro study. Arthritis Res. Ther. 8, R89
67. Ehlert, K., Frosch, M., Fehse, N., Zander, A., Roth, J., and Vormoor, J. (2007) Farber disease: clinical presentation, pathogenesis and a new approach to treatment. Pediatr. Rheumatol. Online J. 5, 15
68. Goldring, M. B. (1999) The role of cytokines as inflammatory mediators in osteoarthritis: lessons from animal models. Connect. Tissue Res. 40, 1-11
69. Wiegmann, K., Schütze, S., Machleidt, T., Witte, D., and Krönke, M. (1994) Functional dichotomy of neutral and acidic sphingomyelinases in tumor necrosis factor signaling. Cell 78, 1005-1015 (Pubitemid 24292328)