Subtilisin-like proprotein convertase paired basic amino acid-cleaving enzyme 4 is required for chondrogenic differentiation in ATDC5 cells

FEBS Journal

Volumn 279, Issue 21, 2012, Pages 3997-4009

  Yuasa, Keizo ^a   Futamatsu, Go ^a   Kawano, Tsuyoshi ^a   Muroshita, Masaki ^a   Kageyama, Yoko ^a   Taichi, Hiromi ^a   Ishikawa, Hiroshi ^a   Nagahama, Masami ^a   Matsuda, Yoshiko ^a   Tsuji, Akihiko ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

bone morphogenetic protein 6 (BMP6); chondrogenic differentiation; paired basic amino acid cleaving enzyme 4 (PACE4); processing; subtilisin like proprotein convertase (SPC)

Indexed keywords

ALPHA 1 ANTITRYPSIN; BONE MORPHOGENETIC PROTEIN 6; DECANOYL ARGINYLVALYLLYSYLARGININE CHLOROMETHYLKETONE; FURIN; MESSENGER RNA; PAIRED BASIC AMINO ACID CLEAVING ENZYME 4; SERINE PROTEINASE; SERINE PROTEINASE INHIBITOR; SUBTILISIN LIKE PROPROTEIN CONVERTASE 2; SUBTILISIN LIKE PROPROTEIN CONVERTASE 3; SUBTILISIN LIKE PROPROTEIN CONVERTASE 5; SUBTILISIN LIKE PROPROTEIN CONVERTASE 6; SUBTILISIN LIKE PROPROTEIN CONVERTASE 7; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL LINE; CELL STRAIN ATDC5; CELL STRAIN COS7; CHONDROGENIC DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYONAL CARCINOMA STEM CELL; ENZYME ACTIVITY; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; UPREGULATION;

ALPHA 1-ANTITRYPSIN; AMINO ACIDS, BASIC; ANIMALS; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEIN 6; CARCINOMA, EMBRYONAL; CELL DIFFERENTIATION; CHONDROCYTES; FURIN; HUMANS; MICE; PROPROTEIN CONVERTASES; RATS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED;

EID: 84867575958     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08758.x     Document Type: Article

References (39)

1. Li X, &, Cao X, (2006) BMP signaling and skeletogenesis. Ann N Y Acad Sci 1068, 26-40.
2. Xiao YT, Xiang LX, &, Shao JZ, (2007) Bone morphogenetic protein. Biochem Biophys Res Commun 362, 550-553.
3. Rider CC, &, Mulloy B, (2010) Bone morphogenetic protein and growth differentiation factor cytokine families and their protein antagonists. Biochem J 429, 1-12.
4. Lyons KM, Pelton RW, &, Hogan BL, (1989) Patterns of expression of murine Vgr-1 and BMP-2a RNA suggest that transforming growth factor-β-like genes coordinately regulate aspects of embryonic development. Genes Dev 3, 1657-1668.
5. Kugimiya F, Kawaguchi H, Kamekura S, Chikuda H, Ohba S, Yano F, Ogata N, Katagiri T, Harada Y, Azuma Y, et al,. (2005) Involvement of endogenous bone morphogenetic protein (BMP) 2 and BMP6 in bone formation. J Biol Chem 280, 35704-35712.
6. Storm EE, &, Kingsley DM, (1996) Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (BMP) family. Development 122, 3969-3979.
7. Seidah NG, Mayer G, Zaid A, Rousselet E, Nassoury N, Poirier S, Essalmani R, &, Prat A, (2008) The activation and physiological functions of the proprotein convertases. Int J Biochem Cell Biol 40, 1111-1125.
8. Cui Y, Jean F, Thomas G, &, Christian JL, (1998) BMP-4 is proteolytically activated by furin and/or PC6 during vertebrate embryonic development. EMBO J 17, 4735-4743.
9. Constam DB, &, Robertson EJ, (1999) Regulation of morphogenetic protein activity by pro-domains and proprotein convertase. J Cell Biol 144, 139-149.
10. Tsuji A, Sakurai K, Kiyokage E, Yamazaki T, Koide S, Toida K, Ishimura K, &, Matsuda Y, (2003) Secretory proprotein convertases PACE4 and PC6A are heparin-binding proteins which are localized in the extracellular matrix. Potential role of PACE4 in the activation of proproteins in the extracellular matrix. Biochim Biophys Acta 1645, 95-104.
11. Constam DB, &, Robertson EJ, (2000) SPC4/PACE4 regulates a TGFβ signaling network during axis formation. Genes Dev 14, 1146-1155.
12. Bassi DE, Zhang J, Cenna J, Litwin S, Cukierman E, &, Klein-Szanto AJ, (2010) Proprotein convertase inhibition results in decreased skin cell proliferation, tumorigenesis, and metastasis. Neoplasia 12, 516-526.
13. Yuasa K, Masuda T, Yoshikawa C, Nagahama M, Matsuda Y, &, Tsuji A, (2009) Subtilisin-like proprotein convertase PACE4 is required for skeletal muscle differentiation. J Biochem 146, 407-415.
14. Tsuji A, Yoshida S, Hasegawa S, Bando M, Yoshida I, Koide S, Mori K, &, Matsuda Y, (1999) Human subtilisin-like proprotein convertase, PACE4 (SPC4) gene expression is highly regulated through E-box elements in HepG2 and GH4C1 cells. J Biochem 126, 494-502.
15. Yoshida I, Koide S, Hasegawa S, Nakagawara A, Tsuji A, &, Matsuda Y, (2001) Proprotein convertase PACE4 is down-regulated by the basic helix-loop-helix transcription factor hASH-1 and MASH-1. Biochem J 360, 683-689.
16. Koide S, Yoshida I, Tsuji A, &, Matsuda Y, (2003) The expression of proprotein convertase PACE4 is highly regulated by Hash-2 in placenta. Possible role of placenta-specific basic helix-loop-helix transcription factor, human achaete-scute homologue-2. J Biochem 134, 433-440.
17. Yuasa K, Suzue K, Nagahama M, Matsuda Y, &, Tsuji A, (2007) Transcriptional regulation of subtilisin-like proprotein convertase PACE4 by E2F. Possible role of E2F-mediated upregulation of PACE4 in tumor progression. Gene 402, 103-110.
18. Shukunami C, Shigeno C, Atsumi T, Ishizeki K, Suzuki F, &, 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.
19. Akamatsu T, Azlina A, Purwanti N, Karabasil MR, Hasegawa T, Yao C, &, Hosoi K, (2009) Inhibition and transcriptional silencing of a subtilisin-like proprotein convertase, PACE4/SPC4, reduces the branching morphogenesis of and AQP5 expression in rat embryonic submandibular gland. Dev Biol 325, 434-443.
20. Tsuji A, Hashimoto E, Ikoma T, Taniguchi T, Mori K, Nagahama M, &, Matsuda Y, (1999) Inactivation of proprotein convertase, PACE4, by α1-antitrypsin Portland (α1-PDX), a blocker of proteolytic activation of bone morphogenetic protein during embryogenesis. Evidence that PACE4 is able to form an SDS-stable acyl intermediate with α1-PDX. J Biochem 126, 591-603.
21. Tsuji A, Ikoma T, Hashimoto E, &, Matsuda Y, (2002) Development of selectivity of alpha1-antitrypsin variant by mutagenesis in its reactive site loop against proprotein convertase. A crucial role of the P4 arginine in PACE4 inhibition. Protein Eng 15, 123-130.
22. Constam DB, Calfon M, &, Robertson EJ, (1996) SPC4, SPC6, and the novel protease SPC7 are coexpressed with bone morphogenetic proteins at distinct sites during embryogenesis. J Cell Biol 134, 181-191.
23. Tsuji A, Kanie H, Makise H, Yuasa K, Nagahama M, &, Matsuda Y, (2007) Engineering of alpha1-antitrypsin variants selective for subtilisin-like proprotein convertases PACE4 and PC6: importance of the P2' residue in stable complex formation of the serpin with proprotein convertase. Protein Eng Des Sel 20, 163-170.
24. Galanopoulou AS, Kent G, Rabbani SN, Seidah NG, &, Patel YC, (1993) Heterologous processing of prosomatostatin in constitutive and regulated secretory pathways. Putative role of the endoproteases furin, PC1, and PC2. J Biol Chem 268, 6041-6049.
25. Peng H, Chen ST, Wergedal JE, Polo JM, Yee JK, Lau KH, &, Baylink DJ, (2001) Development of an MFG-based retroviral vector system for secretion of high levels of functionally active human BMP4. Mol Ther 4, 95-104.
26. Liu Y, Watanabe H, Nifuji A, Yamada Y, Olson EN, &, Noda M, (1997) Overexpression of a single helix-loop-helix transcription factor, scleraxis, enhances aggrecan gene expression in osteoblastic osteosarcoma ROS17/2.8 cells. J Biol Chem 272, 29880-29885.
27. Shen M, Yoshida E, Yan W, Kawamoto T, Suardita K, Koyano Y, Fujimoto K, Noshiro M, &, Kato Y, (2002) Basic helix-loop-helix protein DEC1 promotes chondrocyte differentiation at the early and terminal stages. J Biol Chem 277, 50112-50120.
28. Malfait AM, Arner EC, Song RH, Alston JT, Markosyan S, Staten N, Yang Z, Griggs DW, &, Tortorella MD, (2008) Proprotein convertase activation of aggrecanases in cartilage in situ. Arch Biochem Biophys 478, 43-51.
29. Wylie JD, Ho JC, Singh S, McCulloch DR, &, Apte SS, (2012) Adamts5 (aggrecanase-2) is widely expressed in the mouse musculoskeletal system and is induced in specific regions of knee joint explants by inflammatory cytokines. J Orthop Res 30, 226-233.
30. Essalmani R, Zaid A, Marcinkiewicz J, Chamberland A, Pasquato A, Seidah NG, &, Prat A, (2008) In vivo functions of the proprotein convertase PC5/6 during mouse development: Gdf11 is a likely substrate. Proc Natl Acad Sci USA 105, 5750-5755.
31. Iwasaki M, Le AX, &, Helms JA, (1997) Expression of indian hedgehog, bone morphogenetic protein 6 and gli during skeletal morphogenesis. Mech Dev 69, 197-202.
32. Ito H, Akiyama H, Shigeno C, &, Nakamura T, (1999) Bone morphogenetic protein-6 and parathyroid hormone-related protein coordinately regulate the hypertrophic conversion in mouse clonal chondrogenic EC cells, ATDC5. Biochim Biophys Acta 1451, 263-270.
33. Grimsrud CD, Romano PR, D'Souza M, Puzas JE, Reynolds PR, Rosier RN, &, O'Keefe RJ, (1999) BMP-6 is an autocrine stimulator of chondrocyte differentiation. J Bone Miner Res 14, 475-482.
34. Hellingman CA, Davidson EN, Koevoet W, Vitters EL, van den Berg WB, van Osch GJ, &, van der Kraan PM, (2011) Smad signaling determines chondrogenic differentiation of bone-marrow-derived mesenchymal stem cells: inhibition of Smad1/5/8P prevents terminal differentiation and calcification. Tissue Eng Part A 17, 1157-1167.
35. Sampath TK, Muthukumaran N, &, Reddi AH, (1987) Isolation of osteogenin, an extracellular matrix-associated, bone-inductive protein, by heparin affinity chromatography. Proc Natl Acad Sci USA 84, 7109-7113.
36. Solloway MJ, Dudley AT, Bikoff EK, Lyons KM, Hogan BL, &, Robertson EJ, (1998) Mice lacking Bmp6 function. Dev Genet 22, 321-339.
37. Wu C, Wu F, Pan J, Morser J, &, Wu Q, (2003) Furin-mediated processing of Pro-C-type natriuretic peptide. J Biol Chem 278, 25847-25852.
38. Jane JA Jr, Dunford BA, Kron A, Pittman DD, Sasaki T, Li JZ, Li H, Alden TD, Dayoub H, Hankins GR, et al,. (2002) Ectopic osteogenesis using adenoviral bone morphogenetic protein (BMP)-4 and BMP-6 gene transfer. Mol Ther 6, 464-470.
39. Yuasa K, Tada K, Harita G, Fujimoto T, Tsukayama M, &, Tsuji A, (2012) Sudachitin, a polymethoxyflavone from Citrus sudachi, suppresses lipopolysaccharide-induced inflammatory responses in mouse macrophage-like RAW264 cells. Biosci Biotechnol Biochem 76, 598-600.