Notch Signaling Promotes Osteoclast Maturation and Resorptive Activity

Journal of Cellular Biochemistry

Volumn 116, Issue 11, 2015, Pages 2598-2609

  Ashley, Jason W ^a   Ahn, Jaimo ^a   Hankenson, Kurt D ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Bone resorption; Notch signaling; Osteoclast commitment; Osteoclast fusion; Osteoclasts

Indexed keywords

GAMMA SECRETASE; JAGGED1; NOTCH RECEPTOR; OSTEOCLAST DIFFERENTIATION FACTOR; CALCIUM BINDING PROTEIN; DIPEPTIDE; IMMOBILIZED PROTEIN; JAG1 PROTEIN, MOUSE; MEMBRANE PROTEIN; N-(N-(3,5-DIFLUOROPHENACETYL)ALANYL)PHENYLGLYCINE TERT-BUTYL ESTER; PROTEIN JAGGED 1; SERRATE JAGGED PROTEIN; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL MATURATION; CONTROLLED STUDY; FUSION GENE; GENE EXPRESSION; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; PRIORITY JOURNAL; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE TECHNIQUE; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; ETIOLOGY; METABOLISM; OSTEOLYSIS; SIGNAL TRANSDUCTION;

ANIMALS; BONE RESORPTION; CALCIUM-BINDING PROTEINS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; DIPEPTIDES; IMMOBILIZED PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; JAGGED-1 PROTEIN; MEMBRANE PROTEINS; MICE; OSTEOCLASTS; RECEPTORS, NOTCH; SERRATE-JAGGED PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84941109493     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.25205     Document Type: Article

References (38)

1. Artavanis-Tsakonas S, Rand MD, Lake RJ,. 1999. Notch signaling: Cell fate control and signal integration in development. Science 284: 770-776.
2. Ashley JW, Shi Z, Zhao H, Li X, Kesterson RA, Feng X,. 2011. Genetic ablation of CD68 results in mice with increased bone and dysfunctional osteoclasts. PLoS One 6: e25838.
3. Bai S, Kopan R, Zou W, Hilton MJ, Ong CT, Long F, Ross FP, Teitelbaum SL,. 2008. NOTCH1 regulates osteoclastogenesis directly in osteoclast precursors and indirectly via osteoblast lineage cells. J Biol Chem 283: 6509-6518.
4. Besse A, Lamothe B, Campos AD, Webster WK, Maddineni U, Lin SC, Wu H, Darnay BG,. 2007. TAK1-dependent signaling requires functional interaction with TAB2/T AB3. J Biol Chem 282: 3918-3928.
5. Bradley EW, Oursler MJ,. 2008. Osteoclast culture and resorption assays. Methods Mol Biol 455: 19-35.
6. Chen S, Lee BH, Bae Y,. 2014. Notch signaling in skeletal stem cells. Calcif Tissue Int 94: 68-77.
7. Choi YH, Ann EJ, Yoon JH, Mo JS, Kim MY, Park HS,. 2013. Calcium/calmodulin-dependent protein kinase IV (CaMKIV) enhances osteoclast differentiation via the up-regulation of Notch1 protein stability. Biochim Biophys Acta 1833: 69-79.
8. Cordle J, Johnson S, Tay JZ, Roversi P, Wilkin MB, de Madrid BH, Shimizu H, Jensen S, Whiteman P, Jin B, Redfield C, Baron M, Lea SM, Handford PA,. 2008. A conserved face of the Jagged/Serrate DSL domain is involved in Notch trans-activation and cis-inhibition. Nat Struct Mol Biol 15: 849-857.
9. Duan L, de Vos P, Fan M, Ren Y,. 2008. Notch is activated in RANKL-induced osteoclast differentiation and resorption. Front Biosci 13: 7064-7071.
10. Feng X, 2005. RANKing intracellular signaling in osteoclasts. IUBMB Life 57: 389-395.
11. Fukushima H, Nakao A, Okamoto F, Shin M, Kajiya H, Sakano S, Bigas A, Jimi E, Okabe K,. 2008. The association of Notch2 and NF-kappaB accelerates RANKL-induced osteoclastogenesis. Mol Cell Biol 28: 6402-6412.
12. Groot AJ, Habets R, Yahyanejad S, Hodin CM, Reiss K, Saftig P, Theys J, Vooijs M,. 2014. Regulated proteolysis of NOTCH2 and NOTCH3 receptors by ADAM10 and presenilins. Mol Cell Biol 34: 2822-2832.
13. Henriksen K, Karsdal MA, Martin TJ,. 2014. Osteoclast-derived coupling factors in bone remodeling. Calcif Tissue Int 94: 88-97.
14. Hong H, Shi Z, Qiao P, Li H, McCoy EM, Mao P, Xu H, Feng X, Wang S,. 2013. Interleukin-3 plays dual roles in osteoclastogenesis by promoting the development of osteoclast progenitors but inhibiting the osteoclastogenic process. Biochem Biophys Res Commun 440: 545-550.
15. Izawa T, Zou W, Chappel JC, Ashley JW, Feng X, Teitelbaum SL,. 2012. C-Src links a RANK/alphavbeta3 integrin complex to the osteoclast cytoskeleton. Mol Cell Biol 32: 2943-2953.
16. Jones KA, 2009. Outsmarting a mastermind. Dev Cell 17: 750-752.
17. Jules J, Shi Z, Liu J, Xu D, Wang S, Feng X,. 2010. Receptor activator of NF-{kappa}B (RANK) cytoplasmic IVVY 535-538 motif plays an essential role in tumor necrosis factor-{alpha} (TNF)-mediated osteoclastogenesis. J Biol Chem 285: 37427-37435.
18. Jules J, Zhang P, Ashley JW, Wei S, Shi Z, Liu J, Michalek SM, Feng X,. 2012. Molecular basis of requirement of receptor activator of nuclear factor kappaB signaling for interleukin 1-mediated osteoclastogenesis. J Biol Chem 287: 15728-15738.
19. Kopan R, Ilagan MX,. 2009. The canonical Notch signaling pathway: Unfolding the activation mechanism. Cell 137: 216-233.
20. Kornilova AY, Das C, Wolfe MS,. 2003. Differential effects of inhibitors on the gamma-secretase complex. Mechanistic implications. J Biol Chem 278: 16470-16473.
21. Li C, Yang Z, Li Z, Ma Y, Zhang L, Zheng C, Qiu W, Wu X, Wang X, Li H, Tang J, Qian M, Li D, Wang P, Luo J, Liu M,. 2011. Maslinic acid suppresses osteoclastogenesis and prevents ovariectomy-induced bone loss by regulating RANKL-mediated NF-kappaB and MAPK signaling pathways. J Bone Miner Res 26: 644-656.
22. Maeda K, Kobayashi Y, Udagawa N, Uehara S, Ishihara A, Mizoguchi T, Kikuchi Y, Takada I, Kato S, Kani S, Nishita M, Marumo K, Martin TJ, Minami Y, Takahashi N,. 2012. Wnt5a-Ror2 signaling between osteoblast-lineage cells and osteoclast precursors enhances osteoclastogenesis. Nat Med 18: 405-412.
23. McCoy EM, Hong H, Pruitt HC, Feng X,. 2013. IL-11 produced by breast cancer cells augments osteoclastogenesis by sustaining the pool of osteoclast progenitor cells. BMC Cancer 13: 16.
24. Moellering RE, Cornejo M, Davis TN, Del Bianco C, Aster JC, Blacklow SC, Kung AL, Gilliland DG, Verdine GL, Bradner JE,. 2009. Direct inhibition of the NOTCH transcription factor complex. Nature 462: 182-188.
25. Morohashi Y, Kan T, Tominari Y, Fuwa H, Okamura Y, Watanabe N, Sato C, Natsugari H, Fukuyama T, Iwatsubo T, Tomita T,. 2006. C-terminal fragment of presenilin is the molecular target of a dipeptidic gamma-secretase-specific inhibitor DAPT (N-[N-(3,5-difluorophenacetyl)-L-alanyl]-S-phenylglycine t-butyl ester). J Biol Chem 281: 14670-14676.
26. Park KH, Park B, Yoon DS, Kwon SH, Shin DM, Lee JW, Lee HG, Shim JH, Park JH, Lee JM,. 2013. Zinc inhibits osteoclast differentiation by suppression of Ca2+-Calcineurin-NFATc1 signaling pathway. Cell Commun Signal 11: 74.
27. Sardi SP, Murtie J, Koirala S, Patten BA, Corfas G,. 2006. Presenilin-dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain. Cell 127: 185-197.
28. Schwarzer R, Kaiser M, Acikgoez O, Heider U, Mathas S, Preissner R, Sezer O, Doerken B, Jundt F,. 2008. Notch inhibition blocks multiple myeloma cell-induced osteoclast activation. Leukemia 22: 2273-2277.
29. Sekine C, Koyanagi A, Koyama N, Hozumi K, Chiba S, Yagita H,. 2012. Differential regulation of osteoclastogenesis by Notch2/Delta-like 1 and Notch1/Jagged1 axes. Arthritis Res Ther 14: R45.
30. Sethi N, Dai X, Winter CG, 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.
31. Teitelbaum SL, 2007. Osteoclasts: What do they do and how do they do it?. Am J Pathol 170: 427-435.
32. Tevlin R, McArdle A, Chan CK, Pluvinage J, Walmsley GG, Wearda T, Marecic O, Hu MS, Paik KJ, Senarath-Yapa K, Atashroo DA, Zielins ER, Wan DC, Weissman IL, Longaker MT,. 2014. Osteoclast derivation from mouse bone marrow. J Vis Exp e52056.
33. Wang R, Liu K, Chen L, Aihara K,. 2011. Neural fate decisions mediated by trans-activation and cis-inhibition in Notch signaling. Bioinformatics 27: 3158-3165.
34. Wang X, Ha T,. 2013. Defining single molecular forces required to activate integrin and notch signaling. Science 340: 991-994.
35. Yamada T, Yamazaki H, Yamane T, Yoshino M, Okuyama H, Tsuneto M, Kurino T, Hayashi S, Sakano S,. 2003. Regulation of osteoclast development by Notch signaling directed to osteoclast precursors and through stromal cells. Blood 101: 2227-2234.
36. Zhou J, Fujiwara T, Ye S, Li X, Zhao H,. 2014. Downregulation of Notch modulators, tetraspanin 5 and 10, inhibits osteoclastogenesis in vitro. Calcif Tissue Int 95: 209-217.
37. Zhou J, Fujiwara T, Ye S, Li X, Zhao H,. 2015. Ubiquitin E3 Ligase LNX2 is Critical for Osteoclastogenesis In Vitro by Regulating M-CSF/RANKL Signaling and Notch2. Calcif Tissue Int 2015 Feb 25. [Epub ahead of print]
38. Zhu F, Sweetwyne MT, Hankenson KD., 2013. PKCdelta is required for Jagged-1 induction of human mesenchymal stem cell osteogenic differentiation. Stem Cells 31: 1181-92.