Human immunodeficiency virus type 1 enhancer-binding protein 3 is essential for the expression of asparagine-linked glycosylation 2 in the regulation of osteoblast and chondrocyte differentiation

Journal of Biological Chemistry

Volumn 289, Issue 14, 2014, Pages 9865-9879

  Imamura, Katsuyuki ^a   Maeda, Shingo ^a   Kawamura, Ichiro ^a   Matsuyama, Kanehiro ^a   Shinohara, Naohiro ^a   Yahiro, Yuhei ^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

AMINO ACIDS; BONE; CARTILAGE; CELL MEMBRANES; CYTOLOGY; DISEASES; ESTERIFICATION; GENE EXPRESSION; GLYCOSYLATION; PROTEINS; RNA; VIRUSES;

CHONDROCYTE DIFFERENTIATION; CHONDROCYTE MATURATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENHANCER-BINDING PROTEINS; HUMAN IMMUNODEFICIENCY VIRUS TYPE-1; OSTEOBLAST DIFFERENTIATION; PROTEASOMAL DEGRADATION;

OSTEOBLASTS;

ASPARAGINE LINKED GLYCOSYLATION 2; BINDING PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS TYPE 1 ENHANCER BINDING PROTEIN 1; HUMAN IMMUNODEFICIENCY VIRUS TYPE 1 ENHANCER BINDING PROTEIN 2; HUMAN IMMUNODEFICIENCY VIRUS TYPE 1 ENHANCER BINDING PROTEIN 3; MANNOSYLTRANSFERASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CALVARIA; CARTILAGE CELL; CELL DIFFERENTIATION; CELL MATURATION; CELL NUCLEUS; CELL STIMULATION; CHONDROGENESIS; CONTROLLED STUDY; CREB3L2 GENE; EMBRYO; ENDOPLASMIC RETICULUM STRESS; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENE SILENCING; GROWTH INHIBITION; IMMUNOPRECIPITATION; IN VITRO STUDY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STROMA CELL; VIRUS CELL INTERACTION;

ALG2; BONE MORPHOGENETIC PROTEIN (BMP); CHONDROGENESIS; ENDOPLASMIC RETICULUM (ER); ENDOPLASMIC RETICULUM STRESS; HIVEP3; OSTEOBLASTS; RUNX2;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL NUCLEUS; CHONDROCYTES; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE KNOCKDOWN TECHNIQUES; MANNOSYLTRANSFERASES; MICE; OSTEOBLASTS; OSTEOGENESIS;

EID: 84898063643     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.520585     Document Type: Article

References (43)

1. Kronenberg, H. M. (2003) Developmental regulation of the growth plate. Nature 423, 332-336
2. Boyle, W. J., Simonet, W. S., and Lacey, D. L. (2003) Osteoclast differentiation and activation. Nature 423, 337-342
3. Komori, T., Yagi, H., Nomura, S., Yamaguchi, A., Sasaki, K., Deguchi, K., Shimizu, Y., Bronson, R. T., Gao, Y. H., Inada, M., Sato, M., Okamoto, R., Kitamura, Y., Yoshiki, S., and Kishimoto, T. (1997) Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89, 755-764
4. Mundlos, S., Otto, F., Mundlos, C., Mulliken, J. B., Aylsworth, A. S., Albright, S., Lindhout, D., Cole, W. G., Henn, W., Knoll, J. H., Owen, M. J., Mertelsmann, R., Zabel, B. U., and Olsen, B. R.(1997) Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89, 773-779
5. Otto, F., Thornell, A. P., Crompton, T., Denzel, A., Gilmour, K. C., Rosewell, I. R., Stamp, G. W., Beddington, R. S., Mundlos, S., Olsen, B. R., Selby, P. B., and Owen, M. J. (1997) Cbfa1, a candidate gene for cleidocra-nial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89, 765-771
6. Gong, Y., Slee, R. B., Fukai, N., Rawadi, G., Roman-Roman, S., Reginato, A. M., Wang, H., Cundy, T., Glorieux, F. H., Lev, D., Zacharin, M., Oexle, K., Marcelino, J., Suwairi, W., Heeger, S., Sabatakos, G., Apte, S., Adkins, W. N., Allgrove, J., Arslan-Kirchner, M., Batch, J. A., Beighton, P., Black, G. C., Boles, R. G., Boon, L. M., Borrone, C., Brunner, H. G., Carle, G. F., Dallapiccola, B., De Paepe, A., Floege, B., Halfhide, M. L., Hall, B., Hennekam, R. C., Hirose, T., Jans, A., Jüppner, H., Kim, C. A., Keppler-Noreuil, K., Kohlschuetter, A., LaCombe, D., Lambert, M., Lemyre, E., Letteboer, T., Peltonen, L., Ramesar, R. S., Romanengo, M., Somer, H., Steichen-Gersdorf, E., Steinmann, B., Sullivan, B., Superti-Furga, A., Swoboda, W., van den Boogaard, M. J., Van Hul, W., Vikkula, M., Votruba, M., Zabel, B., Garcia, T., Baron, R., Olsen, B. R., and Warman, M. L. (2001) LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 107, 513-523
7. Brunkow, M. E., Gardner, J. C., Van Ness, J., Paeper, B. W., Kovacevich, B. R., Proll, S., Skonier, J. E., Zhao, L., Sabo, P. J., Fu, Y., Alisch, R. S., Gillett, L., Colbert, T., Tacconi, P., Galas, D., Hamersma, H., Beighton, P., and Mulligan, J. (2001) Bone dysplasia sclerosteosis results from loss of the SOST gene product, a novel cystine knot-containing protein. Am. J. Hum. Genet. 68, 577-589
8. Kato, M., Patel, M. S., Levasseur, R., Lobov, I., Chang, B. H., Glass, D. A., 2nd, Hartmann, C., Li, L., Hwang, T. H., Brayton, C. F., Lang, R. A., Karsenty, G., and Chan, L. (2002) Cbfa1-independent decrease in osteo-blast proliferation, osteopenia, and persistent embryonic eye vasculariza-tion in mice deficient in Lrp5, a Wnt coreceptor. J. Cell Biol. 157, 303-314
9. Li, X., Ominsky, M. S., Niu, Q. T., Sun, N., Daugherty, B., D'Agostin, D., Kurahara, C., Gao, Y., Cao, J., Gong, J., Asuncion, F., Barrero, M., Warm-ington, K., Dwyer, D., Stolina, M., Morony, S., Sarosi, I., Kostenuik, P. J., Lacey, D. L., Simonet, W. S., Ke, H. Z., and Paszty, C. (2008) Targeted deletion of the sclerostin gene in mice results in increased bone formation and bone strength. J. Bone Miner. Res. 23, 860-869
10. Jones, D. C., Wein, M. N., Oukka, M., Hofstaetter, J. G., Glimcher, M. J., and Glimcher, L. H. (2006) Regulation of adult bone mass by the zinc finger adapter protein Schnurri-3. Science 312, 1223-1227
11. Wu, L. C. (2002) ZAS: C2H2 zinc finger proteins involved in growth and development. Gene Expr. 10, 137-152
12. Jin, W., Takagi, T., Kanesashi, S. N., Kurahashi, T., Nomura, T., Harada, J., and Ishii, S. (2006) Schnurri-2 controls BMP-dependent adipogenesis via interaction with Smad proteins. Dev. Cell 10, 461-471
13. Shim, J. H., Greenblatt, M. B., Zou, W., Huang, Z., Wein, M. N., Brady, N., Hu, D., Charron, J., Brodkin, H. R., Petsko, G. A., Zaller, D., Zhai, B., Gygi, S., Glimcher, L. H., and Jones, D. C. (2013) Schnurri-3 regulates ERK downstream of WNT signaling in osteoblasts. J. Clin. Invest. 123, 4010-4022
14. Wein, M. N., Jones, D. C., Shim, J. H., Aliprantis, A. O., Sulyanto, R., Lazarevic, V., Poliachik, S. L., Gross, T. S., and Glimcher, L. H. (2012) Control of bone resorption in mice by Schnurri-3. Proc. Natl. Acad. Sci. U.S.A. 109, 8173-8178
15. Liu, S., Madiai, F., Hackshaw, K. V., Allen, C. E., Carl, J., Huschart, E., Karanfilov, C., Litsky, A., Hickey, C. J., Marcucci, G., Huja, S., Agarwal, S., Yu, J., Caligiuri, M. A., and Wu, L. C. (2011) The large zinc finger protein ZAS3 is a critical modulator of osteoclastogenesis. PloS One 6, e17161
16. Saita, Y., Takagi, T., Kitahara, K., Usui, M., Miyazono, K., Ezura, Y., Nakashima, K., Kurosawa, H., Ishii, S., and Noda, M. (2007) Lack of Schnurri-2 expression associates with reduced bone remodeling and osteopenia. J. Biol. Chem. 282, 12907-12915
17. Jones, D. C, Schweitzer, M. N, Wein, M., Sigrist, K., Takagi, T., Ishii, S., and Glimcher, L. H. (2010) Uncoupling of growth plate maturation and bone formation in mice lacking both Schnurri-2 and Schnurri-3. Proc. Natl. Acad. Sci. U.S.A. 107, 8254-8258
18. Saito, A., Hino, S., Murakami, T., Kanemoto, S., Kondo, S., Saitoh, M., Nishimura, R., Yoneda, T., Furuichi, T., Ikegawa, S., Ikawa, M., Okabe, M., and Imaizumi, K. (2009) Regulation of endoplasmic reticulum stress response by a BBF2H7-mediated Sec23a pathway is essential for chondro-genesis.Nat. Cell Biol. 11, 1197-1204
19. Bobick, B. E., and Kulyk, W. M. (2004) The MEK-ERK signaling pathway is a negative regulator of cartilage-specific gene expression in embryonic limb mesenchyme. J. Biol. Chem. 279, 4588-4595
20. Tominaga, H., Maeda, S., Hayashi, M., Takeda, S., Akira, S., Komiya, S., Nakamura, T., Akiyama, H., and Imamura, T. (2008) CCAAT/enhancer-binding protein/3 promotes osteoblast differentiation by enhancing Runx2 activity with ATF4. Mol. Biol. Cell 19, 5373-5386
21. Alvarez, J., Sohn, P., Zeng, X., Doetschman, T., Robbins, D. J., andSerra, R. (2002) TGF/32 mediates the effects of hedgehog on hypertrophic differentiation and PTHrP expression. Development 129, 1913-1924
22. Ducy, P., Starbuck, M., Priemel, M., Shen, J., Pinero, G., Geoffroy, V., Amling, M., and Karsenty, G. (1999) A Cbfa1-dependent genetic pathway controls bone formation beyond embryonic development. Genes Dev. 13, 1025-1036
23. Geoffroy, V., Kneissel, M., Fournier, B., Boyde, A., and Matthias, P. (2002) High bone resorption in adult aging transgenic mice overexpressing cbfa1/runx2 in cells of the osteoblastic lineage. Mol. Cell. Biol. 22, 6222-6233
24. Kelleher, D. J., and Gilmore, R. (2006) An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 16, 47R-62R
25. Thiel, C., Schwarz, M., Peng, J., Grzmil, M., Hasilik, M., Braulke, T., Kohlschütter, A., von Figura, K., Lehle, L., and Korner, C. (2003) A new type of congenital disorders of glycosylation (CDG-Ii) provides new insights into the early steps of dolichol-linked oligosaccharide biosynthesis. J. Biol. Chem. 278, 22498-22505
26. Moremen, K. W., and Molinari, M. (2006) N-Linked glycan recognition and processing: The molecular basis of endoplasmic reticulum quality control. Curr. Opin. Struct. Biol. 16, 592-599
27. Aebi, M., Bernasconi, R., Clerc, S., and Molinari, M. (2010) N-Glycan structures: Recognition and processing in the ER. Trends Biochem. Sci. 35, 74-82
28. Yang, X., Matsuda, K., Bialek, P., Jacquot, S., Masuoka, H. C., Schinke, T., Li, L., Brancorsini, S., Sassone-Corsi, P., Townes, T. M., Hanauer, A., and Karsenty, G. (2004) ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology; implication for Coffin-Lowry syndrome. Cell 117, 387-398
29. Murakami, T., Saito, A., Hino, S., Kondo, S., Kanemoto, S., Chihara, K., Sekiya, H., Tsumagari, K., Ochiai, K., Yoshinaga, K., Saitoh, M., Nishimura, R., Yoneda, T., Kou, I., Furuichi, T., Ikegawa, S., Ikawa, M., Okabe, M., Wanaka, A., and Imaizumi, K. (2009) Signalling mediated by the endoplasmic reticulum stress transducer OASIS is involved in bone formation. Nat Cell Biol. 11, 1205-1211
30. Saito, A., Ochiai, K., Kondo, S., Tsumagari, K., Murakami, T., Cavener, D. R., and Imaizumi, K. (2011) Endoplasmic reticulum stress response mediated by the PERK-eIF2a-ATF4 pathway is involved in osteoblast differentiation induced by BMP2. J. Biol. Chem. 286, 4809-4818
31. 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
32. Ishida, W., Hamamoto, T., Kusanagi, K., Yagi, K., Kawabata, M., Takehara, K., Sampath, T. K., Kato, M., and Miyazono, K. (2000) Smad6 is a Smad1/5-induced Smad inhibitor. Characterization of bone morphogenetic protein-responsive element in the mouse Smad6 promoter. J. Biol. Chem. 275, 6075-6079
33. Garg, V., Muth, A. N, Ransom, J. F., Schluterman, M. K., Barnes, R., King, I. N, Grossfeld, P. D., and Srivastava, D. (2005) Mutations in NOTCH1 cause aortic valve disease. Nature 437, 270-274
34. McLarren, K. W., Lo, R., Grbavec, D., Thirunavukkarasu, K., Karsenty, G., and Stifani, S. (2000) The mammalian basic helix loop helix protein HES-1 binds to and modulates the transactivating function of the runt-related factor Cbfa1. J. Biol. Chem. 275, 530-538
35. Lee, J. S., Thomas, D. M., Gutierrez, G., Carty, S. A., Yanagawa, S., and Hinds, P. W. (2006) HES1 cooperates with pRb to activate RUNX2-depen-dent transcription. J. Bone Miner. Res. 21, 921-933
36. Zaidi, S.K., Javed, A., Choi, J. Y., van Wijnen, A. J., Stein, J.L., Lian, J.B., and Stein, G. S. (2001) A specific targeting signal directs Runx2/Cbfa1 to sub-nuclear domains and contributes to transactivation of the osteocalcin gene. J. Cell Sci. 114, 3093-3102
37. Kawamura, I., Maeda, S., Imamura, K., Setoguchi, T., Yokouchi, M., Ishi-dou, Y., and Komiya, S. (2012) SnoN suppresses maturation of chondrocytes by mediating signal cross-talk between transforming growth fac-tor-/3 and bone morphogenetic protein pathways. J. Biol. Chem. 287, 29101-29113
38. Dai, H., Hogan, C, Gopalakrishnan, B., Torres-Vazquez, J., Nguyen, M., Park, S., Raftery, L. A., Warrior, R., and Arora, K. (2000) The zinc finger protein schnurri acts as a Smad partner in mediating the transcriptional response to decapentaplegic. Dev. Biol. 227, 373-387
39. Udagawa, Y., Hanai, J., Tada, K., Grieder, N. C, Momoeda, M., Taketani, Y., Affolter, M., Kawabata, M., and Miyazono, K. (2000) Schnurri interacts with Mad in a Dpp-dependent manner. Genes Cells 5, 359-369
40. 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
41. Haeuptle, M. A., and Hennet, T. (2009) Congenital disorders of glycosylation: an update on defects affecting the biosynthesis of dolichol-linked oligosaccharides. Hum. Mutat. 30, 1628-1641
42. Coman, D., Irving, M., Kannu, P., Jaeken, J., and Savarirayan, R. (2008) The skeletal manifestations of the congenital disorders of glycosylation. Clin. Genet. 73, 507-515
43. Asada, R., Kanemoto, S., Kondo, S., Saito, A., and Imaizumi, K. (2011) The signalling from endoplasmic reticulum-resident bZIP transcription factors involved in diverse cellular physiology. J. Biochem. 149, 507-518