Hairy and enhancer of split-related with YRPW motif (HEY)2 regulates bone remodeling in mice

Journal of Biological Chemistry

Volumn 288, Issue 30, 2013, Pages 21547-21557

  Zanotti, Stefano ^a,b   Canalis, Ernesto ^a,b  

^a SAINT FRANCIS HOSPITAL AND MEDICAL CENTER   (United States)

^b UNIVERSITY OF CONNECTICUT SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MASS; BONE REMODELING; BONE RESORPTION; MALE MOUSE; OVER-EXPRESSION; SKELETAL FUNCTION;

MAMMALS;

BONE;

ALKALINE PHOSPHATASE; COLLAGEN TYPE 1; COLLAGEN TYPE 1 ALPHA1; CRE RECOMBINASE; HAIRY AND ENHANCER OF SPLIT RELATED WITH YRPW MOTIF PROTEIN 2; INTERLEUKIN 6; OSTEOCALCIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR OSTERIX; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MASS; BONE REMODELING; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE INACTIVATION; GENETIC TRANSCRIPTION; HEY2 GENE; MALE; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; OSTEOLYSIS; OSTEOPENIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SPLEEN CELL; TRABECULAR BONE;

BONE; BONE REMODELING; HEY2; INTERLEUKIN; NOTCH; OSTEOBLASTS; OSTEOCLAST;

ALKALINE PHOSPHATASE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BONE DISEASES, METABOLIC; BONE REMODELING; BONE RESORPTION; CELLS, CULTURED; COCULTURE TECHNIQUES; FEMALE; GENE EXPRESSION; INTERLEUKIN-6; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OSTEOBLASTS; OSTEOCALCIN; OSTEOGENESIS; RATS; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEX FACTORS; SPLEEN;

EID: 84881245884     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.489435     Document Type: Article

References (55)

1. Iso, T., Kedes, L., and Hamamori, Y. (2003) HES and HERP families: multiple effectors of the Notch signaling pathway. J. Cell Physiol. 194, 237-255
2. Kageyama, R., Ohtsuka, T., and Kobayashi, T. (2007) The Hes gene family: repressors and oscillators that orchestrate embryogenesis. Development 134, 1243-1251
3. Fischer, A., and Gessler, M. (2007) Delta-Notch-and then? Protein interactions and proposed modes of repression by Hes and Hey bHLH factors. Nucleic Acids Res. 35, 4583-4596
4. Zanotti, S., and Canalis, E. (2010) Notch and the skeleton. Mol. Cell Biol. 30, 886-896
5. Kokubo, H., Miyagawa-Tomita, S., Tomimatsu, H., Nakashima, Y., Nakazawa, M., Saga, Y., and Johnson, R. L. (2004) Targeted disruption of hesr2 results in atrioventricular valve anomalies that lead to heart dysfunction. Circ. Res. 95, 540-547
6. Xin, M., Small, E. M., van Rooij, E., Qi, X., Richardson, J. A., Srivastava, D., Nakagawa, O., and Olson, E. N. (2007) Essential roles of the bHLH transcription factor Hrt2 in repression of atrial gene expression and maintenance of postnatal cardiac function. Proc. Natl. Acad. Sci. U.S.A. 104, 7975-7980
7. Fischer, A., Steidl, C., Wagner, T. U., Lang, E., Jakob, P. M., Friedl, P., Knobeloch, K. P., and Gessler, M. (2007) Combined loss of Hey1 and HeyL causes congenital heart defects because of impaired epithelial to mesenchymal transition. Circ. Res. 100, 856-863
8. Fischer, A., Schumacher, N., Maier, M., Sendtner, M., and Gessler, M. (2004) The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev. 18, 901-911
9. Kokubo, H., Miyagawa-Tomita, S., Nakazawa, M., Saga, Y., and Johnson, R. L. (2005) Mouse hesr1 and hesr2 genes are redundantly required to mediate Notch signaling in the developing cardiovascular system. Dev. Biol. 278, 301-309
10. Bianco, P., and Gehron Robey, P. (2000) Marrow stromal stem cells. J. Clin. Invest. 105, 1663-1668
11. Canalis, E., Giustina, A., and Bilezikian, J. P. (2007) Mechanisms of anabolic therapies for osteoporosis. N. Engl. J. Med. 357, 905-916
12. Canalis, E., Economides, A. N., and Gazzerro, E. (2003) Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr. Rev. 24, 218-235
13. Westendorf, J. J., Kahler, R. A., and Schroeder, T. M. (2004) Wnt signaling in osteoblasts and bone diseases. Gene 341, 19-39
14. Engin, F., Yao, Z., Yang, T., Zhou, G., Bertin, T., Jiang, M. M., Chen, Y., Wang, L., Zheng, H., Sutton, R. E., Boyce, B. F., and Lee, B. (2008) Dimorphic effects of Notch signaling in bone homeostasis. Nat. Med. 14, 299-305
15. Hilton, M. J., Tu, X., Wu, X., Bai, S., Zhao, H., Kobayashi, T., Kronenberg, H. M., Teitelbaum, S. L., Ross, F. P., Kopan, R., and Long, F. (2008) Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation. Nat. Med. 14, 306-314
16. Zanotti, S., Smerdel-Ramoya, A., Stadmeyer, L., Durant, D., Radtke, F., and Canalis, E. (2008) Notch inhibits osteoblast differentiation and causes osteopenia. Endocrinology 149, 3890-3899
17. Lacey, D. L., Timms, E., Tan, H. L., Kelley, M. J., Dunstan, C. R., Burgess, T., Elliott, R., Colombero, A., Elliott, G., Scully, S., Hsu, H., Sullivan, J., Hawkins, N., Davy, E., Capparelli, C., Eli, A., Qian, Y. X., Kaufman, S., Sarosi, I., Shalhoub, V., Senaldi, G., Guo, J., Delaney, J., and Boyle, W. J. (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93, 165-176
18. Teitelbaum, S. L. (2007) Osteoclasts: what do they do and how do they do it? Am. J. Pathol. 170, 427-435
19. Dong, Y., Jesse, A. M., Kohn, A., Gunnell, L. M., Honjo, T., Zuscik, M. J., O'Keefe, R. J., and Hilton, M. J. (2010) RBPj-dependent Notch signaling regulates mesenchymal progenitor cell proliferation and differentiation during skeletal development. Development 137, 1461-1471
20. Tao, J., Chen, S., Yang, T., Dawson, B., Munivez, E., Bertin, T., and Lee, B. (2010) Osteosclerosis owing to Notch gain of function is solely Rbpj-dependent. J. Bone Miner Res. 25, 2175-2183
21. Zanotti, S., Smerdel-Ramoya, A., and Canalis, E. (2011) Reciprocal regulation of Notch and nuclear factor of activated T-cells (NFAT) c1 transactivation in osteoblasts. J. Biol. Chem. 286, 4576-4588
22. Zanotti, S., Smerdel-Ramoya, A., and Canalis, E. (2011) HES1 (hairy and enhancer of split 1) is a determinant of bone mass. J. Biol. Chem. 286, 2648-2657
23. Salie, R., Kneissel, M., Vukevic, M., Zamurovic, N., Kramer, I., Evans, G., Gerwin, N., Mueller, M., Kinzel, B., and Susa, M. (2010) Ubiquitous overexpression of Hey1 transcription factor leads to osteopenia and chondrocyte hypertrophy in bone. Bone 46, 680-694
24. Tu, X., Chen, J., Lim, J., Karner, C. M., Lee, S. Y., Heisig, J., Wiese, C., Surendran, K., Kopan, R., Gessler, M., and Long, F. (2012) Physiological notch signaling maintains bone homeostasis via RBPjk and Hey upstream of NFATc1. PLoS. Genet. 8, e1002577
25. Yamada, T., Yamazaki, H., Yamane, T., Yoshino, M., Okuyama, H., Tsuneto, M., Kurino, T., Hayashi, S., and Sakano, S. (2003) Regulation of osteoclast development by Notch signaling directed to osteoclast precursors and through stromal cells. Blood 101, 2227-2234
26. Bai, S., Kopan, R., Zou, W., Hilton, M. J., Ong, C. T., Long, F., Ross, F. P., and Teitelbaum, S. L. (2008) NOTCH1 regulates osteoclastogenesis directly in osteoclast precursors and indirectly via osteoblast lineage cells. J. Biol. Chem. 283, 6509-6518
27. Fukushima, H., Nakao, A., Okamoto, F., Shin, M., Kajiya, H., Sakano, S., Bigas, A., Jimi, E., and Okabe, K. (2008) The association of Notch2 and NF-κB accelerates RANKL-induced osteoclastogenesis. Mol. Cell Biol. 28, 6402-6412
28. Sethi, N., Dai, X., Winter, C. G., and Kang, Y. (2011) Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells. Cancer Cell 19, 192-205
29. Wei, W., Zeve, D., Wang, X., Du, Y., Tang, W., Dechow, P. C., Graff, J. M., and Wan, Y. (2011) Osteoclast progenitors reside in the peroxisome proliferator-activated receptor-expressing bone marrow cell population. Mol. Cell Biol. 31, 4692-4705
30. Rodda, S. J., and McMahon, A. P. (2006) Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133, 3231-3244
31. Furth, P. A., St Onge, L., Böger, H., Gruss, P., Gossen, M., Kistner, A., Bujard, H., and Hennighausen, L. (1994) Temporal control of gene expression in transgenic mice by a tetracycline-responsive promoter. Proc. Natl. Acad. Sci. U.S.A. 91, 9302-9306
32. Kalajzic, I., Kalajzic, Z., Kaliterna, M., Gronowicz, G., Clark, S. H., Lichtler, A. C., and Rowe, D. (2002) Use of type I collagen green fluorescent protein transgenes to identify subpopulations of cells at different stages of the osteoblast lineage. J. Bone Miner. Res. 17, 15-25
33. Irwin, N. (1989) in Molecular Cloning: A Laboratory Manual (Sambrook, J., Fritsch, E. F., and Maniatis, T., eds) Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
34. Garnero, P., Borel, O., and Delmas, P. D. (2001) Evaluation of a fully automated serum assay for C-terminal cross-linking telopeptide of type I collagen in osteoporosis. Clin. Chem. 47, 694-702
35. Bouxsein, M. L., Boyd, S. K., Christiansen, B. A., Guldberg, R. E., Jepsen, K. J., and Müller, R. (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J. Bone Miner Res. 25, 1468-1486
36. Gazzerro, E., Pereira, R. C., Jorgetti, V., Olson, S., Economides, A. N., and Canalis, E. (2005) Skeletal overexpression of gremlin impairs bone formation and causes osteopenia. Endocrinology 146, 655-665
37. Parfitt, A. M., Drezner, M. K., Glorieux, F. H., Kanis, J. A., Malluche, H., Meunier, P. J., Ott, S. M., and Recker, R. R. (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res. 2, 595-610
38. McCarthy, T. L., Centrella, M., and Canalis, E. (1990) CyclicAMPinduces insulin-like growth factor I synthesis in osteoblast-enriched cultures. J. Biol. Chem. 265, 15353-15356
39. Akazawa, C., Sasai, Y., Nakanishi, S., and Kageyama, R. (1992) Molecular characterization of a rat negative regulator with a basic helix-loop-helix structure predominantly expressed in the developing nervous system. J. Biol. Chem. 267, 21879-21885
40. Lian, J., Stewart, C., Puchacz, E., Mackowiak, S., Shalhoub, V., Collart, D., Zambetti, G., and Stein, G. (1989) Structure of the rat osteocalcin gene and regulation of vitamin D-dependent expression. Proc. Natl. Acad. Sci. U.S.A. 86, 1143-1147
41. Iso, T., Sartorelli, V., Poizat, C., Iezzi, S., Wu, H. Y., Chung, G., Kedes, L., and Hamamori, Y. (2001) HERP, a novel heterodimer partner of HES/ E(spl) in Notch signaling. Mol. Cell Biol. 21, 6080-6089
42. Kouadjo, K. E., Nishida, Y., Cadrin-Girard, J. F., Yoshioka, M., and St-Amand, J. (2007) Housekeeping and tissue-specific genes in mouse tissues. BMC. Genomics 8, 127
43. Tso, J. Y., Sun, X. H., Kao, T. H., Reece, K. S., and Wu, R. (1985) Isolation and characterization of rat and human glyceraldehyde-3-phosphate dehydrogenase cDNAs: genomic complexity and molecular evolution of the gene. Nucleic Acids Res. 13, 2485-2502
44. Takahashi, N., Akatsu, T., Udagawa, N., Sasaki, T., Yamaguchi, A., Moseley, J. M., Martin, T. J., and Suda, T. (1988) Osteoblastic cells are involved in osteoclast formation. Endocrinology 123, 2600-2602
45. Lee, S. K., Kalinowski, J., Jastrzebski, S., and Lorenzo, J. A. (2002) 1,25(OH)2 vitamin D3-stimulated osteoclast formation in spleen-osteoblast cocultures is mediated in part by enhanced IL-1 and receptor activator of NF-κB ligand production in osteoblasts. J. Immunol. 169, 2374-2380
46. Wyzga, N., Varghese, S., Wikel, S., Canalis, E., and Sylvester, F. A. (2004) Effects of activated T cells on osteoclastogenesis depend on how they are activated. Bone 35, 614-620
47. Sokal, R. R., and Rohlf, F. J. (1981) Biometry, 2nd Edition, W. H. Freeman, San Francisco, CA
48. Canalis, E., Parker, K., Feng, J. Q., and Zanotti, S. (2013) Osteoblast lineage-specific effects of notch activation in the skeleton. Endocrinology 154, 623-634
49. Hildebrand, T., and Rüegsegger, P. (1997) Quantification of bone microarchitecture with the Structure Model Index. Comput. Methods Biomech. Biomed. Engin. 1, 15-23
50. Mundy, G. R. (2007) Osteoporosis and inflammation. Nutr. Rev. 65, S147-S151
51. Boban, I., Jacquin, C., Prior, K., Barisic-Dujmovic, T., Maye, P., Clark, S. H., and Aguila, H. L. (2006) The 3.6 kb DNA fragment from the rat Col1a1 gene promoter drives the expression of genes in both osteoblast and osteoclast lineage cells. Bone 39, 1302-1312
52. Scheller, E. L., Leinninger, G. M., Hankenson, K. D., Myers, M. G., Jr., and Krebsbach, P. H. (2011) Ectopic expression of Col2.3 and Col3.6 promoters in the brain and association with leptin signaling. Cells Tissues Organs 194, 268-273
53. Manolagas, S. C., Kousteni, S., and Jilka, R. L. (2002) Sex steroids and bone. Recent Prog. Horm. Res 57, 385-409
54. O'Brien, C. A., Lin, S. C., Bellido, T., and Manolagas, S. C. (2000) Expression levels of gp130 in bone marrow stromal cells determine the magnitude of osteoclastogenic signals generated by IL-6-type cytokines. J. Cell Biochem. 79, 532-541
55. Yoshitake, F., Itoh, S., Narita, H., Ishihara, K., and Ebisu, S. (2008) Interleukin-6 directly inhibits osteoclast differentiation by suppressing receptor activator of NF-κB signaling pathways. J. Biol. Chem. 283, 11535-11540