RBPjκ-dependent Notch signaling regulates mesenchymal progenitor cell proliferation and differentiation during skeletal development

Development

Volumn 137, Issue 9, 2010, Pages 1461-1471

  Dong, Yufeng ^a   Jesse, Alana M ^a   Kohn, Anat ^a   Gunnell, Lea M ^a   Honjo, Tasuku ^b   Zuscik, Michael J ^a   O'Keefe, Regis J ^a   Hilton, Matthew J ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Hes1; Limb development; Mesenchymal progenitor cell; Mouse; Notch; RBPj

Indexed keywords

IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; NOTCH RECEPTOR; TRANSCRIPTION FACTOR HES 1; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HES1 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; PRRX1 PROTEIN, MOUSE; RBPJ PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDROGENESIS; CONTROLLED STUDY; EMBRYO; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; BONE; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIMB BUD; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

MUS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOTTING, WESTERN; BONE AND BONES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; LIMB BUDS; MESENCHYMAL STEM CELLS; MICE; MODELS, BIOLOGICAL; RECEPTORS, NOTCH; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 77951229591     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.042911     Document Type: Article

References (77)

1. 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)
2. Akiyama, H., Kim, J. E., Nakashima, K., Balmes, G., Iwai, N., Deng, J. M., Zhang, Z., Martin, J. F., Behringer, R. R., Nakamura, T. et al. (2005). Osteochondroprogenitor cells are derived from Sox9 expressing precursors. Proc. Natl. Acad. Sci. USA 102, 14665-14670. (Pubitemid 41457113)
3. Apelqvist, A., Li, H., Sommer, L., Beatus, P., Anderson, D. J., Honjo, T., Hrabe de Angelis, M., Lendahl, U. and Edlund, H. (1999). Notch signalling controls pancreatic cell differentiation. Nature 400, 877-881. (Pubitemid 29406724)
4. Artavanis-Tsakonas, S., Rand, M. D. and Lake, R. J. (1999). Notch signaling: cell fate control and signal integration in development. Science 284, 770-776. (Pubitemid 29291335)
5. Axelrod, J. D., Matsuno, K., Artavanis-Tsakonas, S. and Perrimon, N. (1996). Interaction between Wingless and Notch signaling pathways mediated by dishevelled. Science 271, 1826-1832. (Pubitemid 3040961)
6. Bellusci, S., Grindley, J., Emoto, H., Itoh, N. and Hogan, B. L. (1997). Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 124, 4867-4878. (Pubitemid 28016850)
7. 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.
8. Blokzijl, A., Dahlqvist, C., Reissmann, E., Falk, A., Moliner, A., Lendahl, U. and Ibanez, C. F. (2003). Cross-talk between the Notch and TGF-beta signaling pathways mediated by interaction of the Notch intracellular domain with Smad3. J. Cell Biol. 163, 723-728. (Pubitemid 37517880)
9. Chiba, S. (2006). Notch signaling in stem cell systems. Stem Cells 24, 2437-2447.
10. Crossley, P. H. and Martin, G. R. (1995). The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121, 439-451.
11. Dahlqvist, C., Blokzijl, A., Chapman, G., Falk, A., Dannaeus, K., Ibanez, C. F. and Lendahl, U. (2003). Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 130, 6089-6099. (Pubitemid 38008810)
12. de la Pompa, J. L., Wakeham, A., Correia, K. M., Samper, E., Brown, S., Aguilera, R. J., Nakano, T., Honjo, T., Mak, T. W., Rossant, J. et al. (1997). Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 124, 1139-1148. (Pubitemid 27142068)
13. Demehri, S., Morimoto, M., Holtzman, M. J. and Kopan, R. (2009). Skin-derived TSLP triggers progression from epidermal-barrier defects to asthma. PLoS Biol. 7, e1000067.
14. Denker, A. E., Haas, A. R., Nicoll, S. B. and Tuan, R. S. (1999). Chondrogenic differentiation of murine C3H10T1/2 multipotential mesenchymal cells: I. Stimulation by bone morphogenetic protein-2 in high-density micromass cultures. Differentiation 64, 67-76.
15. Diederich, R. J., Matsuno, K., Hing, H. and Artavanis-Tsakonas, S. (1994). Cytosolic interaction between deltex and Notch ankyrin repeats implicates deltex in the Notch signaling pathway. Development 120, 473-481. (Pubitemid 24071190)
16. Dong, Y., Drissi, H., Chen, M., Chen, D., Zuscik, M. J., Schwarz, E. M. and O'Keefe, R. J. (2005). Wnt-mediated regulation of chondrocyte maturation: modulation by TGF-beta. J. Cell Biochem. 95, 1057-1068. (Pubitemid 41420151)
17. Donoviel, D. B., Hadjantonakis, A. K., Ikeda, M., Zheng, H., Hyslop, P. S. and Bernstein, A. (1999). Mice lacking both presenilin genes exhibit early embryonic patterning defects. Genes Dev. 13, 2801-2810.
18. Drissi, H., Luc, Q., Shakoori, R., Chuva De Sousa Lopes, S., Choi, J. Y., Terry, A., Hu, M., Jones, S., Neil, J. C., Lian, J. B. et al. (2000). Transcriptional autoregulation of the bone related CBFA1/RUNX2 gene. J. Cell. Physiol. 184, 341-350. (Pubitemid 30625497)
19. Durland, J. L., Sferlazzo, M., Logan, M. and Burke, A. C. (2008). Visualizing the lateral somitic frontier in the Prx1Cre transgenic mouse. J. Anat. 212, 590-602.
20. Engin, F. and Lee, B. (2009). NOTCHing the bone: Insights into multi-functionality. Bone 46, 274-280.
21. Engin, F., Yao, Z., Yang, T., Zhou, G., Bertin, T., Jiang, M. M., Chen, Y., Wang, L., Zheng, H., Sutton, R. E. et al. (2008). Dimorphic effects of Notch signaling in bone homeostasis. Nat. Med. 14, 299-305. (Pubitemid 351347909)
22. Francis, J. C., Radtke, F. and Logan, M. P. (2005). Notch1 signals through Jagged2 to regulate apoptosis in the apical ectodermal ridge of the developing limb bud. Dev. Dyn. 234, 1006-1015. (Pubitemid 41741172)
23. Fre, S., Huyghe, M., Mourikis, P., Robine, S., Louvard, D. and Artavanis-Tsakonas, S. (2005). Notch signals control the fate of immature progenitor cells in the intestine. Nature 435, 964-968. (Pubitemid 40896323)
24. Fujimaki, R., Toyama, Y., Hozumi, N. and Tezuka, K. (2006). Involvement of Notch signaling in initiation of prechondrogenic condensation and nodule formation in limb bud micromass cultures. J. Bone Miner. Metab. 24, 191-198.
25. 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)
26. Hadland, B. K., Huppert, S. S., Kanungo, J., Xue, Y., Jiang, R., Gridley, T., Conlon, R. A., Cheng, A. M., Kopan, R. and Longmore, G. D. (2004). A requirement for Notch1 distinguishes 2 phases of definitive hematopoiesis during development. Blood 104, 3097-3105. (Pubitemid 39507124)
27. Hamada, Y., Kadokawa, Y., Okabe, M., Ikawa, M., Coleman, J. R. and Tsujimoto, Y. (1999). Mutation in ankyrin repeats of the mouse Notch2 gene induces early embryonic lethality. Development 126, 3415-3424. (Pubitemid 29396781)
28. Han, H., Tanigaki, K., Yamamoto, N., Kuroda, K., Yoshimoto, M., Nakahata, T., Ikuta, K. and Honjo, T. (2002). Inducible gene knockout of transcription factor recombination signal binding protein-J reveals its essential role in T versus B lineage decision. Int. Immunol. 14, 637-645. (Pubitemid 34649719)
29. Hatakeyama, J., Bessho, Y., Katoh, K., Ookawara, S., Fujioka, M., Guillemot, F. and Kageyama, R. (2004). Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development 131, 5539-5550. (Pubitemid 39625198)
30. Hayward, P., Brennan, K., Sanders, P., Balayo, T., DasGupta, R., Perrimon, N. and Martinez Arias, A. (2005). Notch modulates Wnt signalling by associating with Armadillo/beta-catenin and regulating its transcriptional activity. Development 132, 1819-1830. (Pubitemid 40691772)
31. Hellstrom, M., Phng, L. K., Hofmann, J. J., Wallgard, E., Coultas, L., Lindblom, P., Alva, J., Nilsson, A. K., Karlsson, L., Gaiano, N. et al. (2007). Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445, 776-780. (Pubitemid 46279716)
32. Hilton, M. J., Tu, X., Cook, J., Hu, H. and Long, F. (2005). Ihh controls cartilage development by antagonizing Gli3, but requires additional effectors to regulate osteoblast and vascular development. Development 132, 4339-4351. (Pubitemid 41576695)
33. Hilton, M. J., Tu, X. and Long, F. (2007). Tamoxifen-inducible gene deletion reveals a distinct cell type associated with trabecular bone, and direct regulation of PTHrP expression and chondrocyte morphology by Ihh in growth region cartilage. Dev. Biol. 308, 93-105. (Pubitemid 47087782)
34. Hilton, M. J., Tu, X., Wu, X., Bai, S., Zhao, H., Kobayashi, T., Kronenberg, H. M., Teitelbaum, S. L., Ross, F. P., Kopan, R. et al. (2008). Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation. Nat. Med. 14, 306-314. (Pubitemid 351347911)
35. Hitoshi, S., Alexson, T., Tropepe, V., Donoviel, D., Elia, A. J., Nye, J. S., Conlon, R. A., Mak, T. W., Bernstein, A. and van der Kooy, D. (2002). Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev. 16, 846-858. (Pubitemid 34280108)
36. Hrabe de Angelis, M., McIntyre, J., 2nd and Gossler, A. (1997). Maintenance of somite borders in mice requires the Delta homologue DII1. Nature 386, 717-721.
37. 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. (Pubitemid 32737822)
38. 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. (Pubitemid 36176887)
39. Itoh, F., Itoh, S., Goumans, M. J., Valdimarsdottir, G., Iso, T., Dotto, G. P., Hamamori, Y., Kedes, L., Kato, M. and ten Dijke, P. (2004). Synergy and antagonism between Notch and BMP receptor signaling pathways in endothelial cells. EMBO J. 23, 541-551.
40. Jensen, J., Pedersen, E. E., Galante, P., Hald, J., Heller, R. S., Ishibashi, M., Kageyama, R., Guillemot, F., Serup, P. and Madsen, O. D. (2000). Control of endodermal endocrine development by Hes-1. Nat. Genet. 24, 36-44. (Pubitemid 30041417)
41. Kopan, R. and Ilagan, M. X. (2009). The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137, 216-233.
42. Kunisato, A., Chiba, S., Nakagami-Yamaguchi, E., Kumano, K., Saito, T., Masuda, S., Yamaguchi, T., Osawa, M., Kageyama, R., Nakauchi, H. et al. (2003). HES-1 preserves purified hematopoietic stem cells ex vivo and accumulates side population cells in vivo. Blood 101, 1777-1783. (Pubitemid 36237573)
43. Lai, E. C. (2002). Keeping a good pathway down: transcriptional repression of Notch pathway target genes by CSL proteins. EMBO Rep. 3, 840-845.
44. Lai, E. C. (2004). Notch signaling: control of cell communication and cell fate. Development 131, 965-973. (Pubitemid 38380451)
45. Logan, M., Martin, J. F., Nagy, A., Lobe, C., Olson, E. N. and Tabin, C. J. (2002). Expression of Cre Recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33, 77-80. (Pubitemid 34651279)
46. Martin, J. F. and Olson, E. N. (2000). Identification of a prx1 limb enhancer. Genesis 26, 225-229.
47. Martinez Arias, A., Zecchini, V. and Brennan, K. (2002). CSL-independent Notch signalling: a checkpoint in cell fate decisions during development? Curr. Opin. Genet. Dev. 12, 524-533. (Pubitemid 35013534)
48. Matsuno, K., Go, M. J., Sun, X., Eastman, D. S. and Artavanis-Tsakonas, S. (1997). Suppressor of Hairless-independent events in Notch signaling imply novel pathway elements. Development 124, 4265-4273. (Pubitemid 27496862)
49. McCright, B., Lozier, J. and Gridley, T. (2002). A mouse model of Alagille syndrome: Notch2 as a genetic modifier of Jag1 haploinsufficiency. Development 129, 1075-1082. (Pubitemid 34874130)
50. McDaniell, R., Warthen, D. M., Sanchez-Lara, P. A., Pai, A., Krantz, I. D., Piccoli, D. A. and Spinner, N. B. (2006). NOTCH2 mutations cause Alagille syndrome, a heterogeneous disorder of the notch signaling pathway. Am. J. Hum. Genet. 79, 169-173. (Pubitemid 43927389)
51. McLeod, M. J. (1980). Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 22, 299-301.
52. Mead, T. J. and Yutzey, K. E. (2009). Notch pathway regulation of chondrocyte differentiation and proliferation during appendicular and axial skeleton development. Proc. Natl. Acad. Sci. USA 106, 14420-14425.
53. Mitsiadis, T. A., Lardelli, M., Lendahl, U. and Thesleff, I. (1995). Expression of Notch 1, 2 and 3 is regulated by epithelial-mesenchymal interactions and retinoic acid in the developing mouse tooth and associated with determination of ameloblast cell fate. J. Cell Biol. 130, 407-418.
54. Murtaugh, L. C., Stanger, B. Z., Kwan, K. M. and Melton, D. A. (2003). Notch signaling controls multiple steps of pancreatic differentiation. Proc. Natl. Acad. Sci. USA 100, 14920-14925.
55. Niswander, L., Jeffrey, S., Martin, G. R. and Tickle, C. (1994). A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature 371, 609-912. (Pubitemid 24315742)
56. Ohtsuka, T., Ishibashi, M., Gradwohl, G., Nakanishi, S., Guillemot, F. and Kageyama, R. (1999). Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J. 18, 2196-2207. (Pubitemid 29179176)
57. Oka, C., Nakano, T., Wakeham, A., de la Pompa, J. L., Mori, C., Sakai, T., Okazaki, S., Kawaichi, M., Shiota, K., Mak, T. W. et al. (1995). Disruption of the mouse RBP-J kappa gene results in early embryonic death. Development 121, 3291-3301.
58. Oldershaw, R. A., Tew, S. R., Russell, A. M., Meade, K., Hawkins, R., McKay, T. R., Brennan, K. R. and Hardingham, T. E. (2008). Notch signaling through Jagged-1 is necessary to initiate chondrogenesis in human bone marrow stromal cells but must be switched off to complete chondrogenesis. Stem Cells 26, 666-674.
59. Ramain, P., Khechumian, K., Seugnet, L., Arbogast, N., Ackermann, C. and Heitzler, P. (2001). Novel Notch alleles reveal a Deltex-dependent pathway repressing neural fate. Curr. Biol. 11, 1729-1738. (Pubitemid 33092161)
60. Robert-Moreno, A., Espinosa, L., de la Pompa, J. L. and Bigas, A. (2005). RBPjkappa-dependent Notch function regulates Gata2 and is essential for the formation of intra-embryonic hematopoietic cells. Development 132, 1117-1126. (Pubitemid 40484944)
61. Ross, D. A. and Kadesch, T. (2001). The notch intracellular domain can function as a coactivator for LEF-1. Mol. Cell. Biol. 21, 7537-7544.
62. Ross, D. A., Hannenhalli, S., Tobias, J. W., Cooch, N., Shiekhattar, R. and Kadesch, T. (2006). Functional analysis of Hes-1 in preadipocytes. Mol. Endocrinol. 20, 698-705.
63. Shutter, J. R., Scully, S., Fan, W., Richards, W. G., Kitajewski, J., Deblandre, G. A., Kintner, C. R. and Stark, K. L. (2000). Dll4, a novel Notch ligand expressed in arterial endothelium. Genes Dev. 14, 1313-1318. (Pubitemid 30397075)
64. Stier, S., Cheng, T., Dombkowski, D., Carlesso, N. and Scadden, D. T. (2002). Notch1 activation increases hematopoietic stem cell self-renewal in vivo and favors lymphoid over myeloid lineage outcome. Blood 99, 2369-2378. (Pubitemid 34525422)
65. Swiatek, P. J., Lindsell, C. E., del Amo, F. F., Weinmaster, G. and Gridley, T. (1994). Notch1 is essential for postimplantation development in mice. Genes Dev. 8, 707-719. (Pubitemid 24116765)
66. Szabova, L., Yamada, S. S., Wimer, H., Chrysovergis, K., Ingvarsen, S., Behrendt, N., Engelholm, L. H. and Holmbeck, K. (2009). MT1-MMP and type II collagen specify skeletal stem cells and their bone and cartilage progeny. J. Bone Miner. Res. 24, 1905-1916.
67. Vacca, A., Felli, M. P., Palermo, R., Di Mario, G., Calce, A., Di Giovine, M., Frati, L., Gulino, A. and Screpanti, I. (2006). Notch3 and pre-TCR interaction unveils distinct NF-kappaB pathways in T-cell development and leukemia. EMBO J. 25, 1000-1008. (Pubitemid 43372114)
68. Varnum-Finney, B., Xu, L., Brashem-Stein, C., Nourigat, C., Flowers, D., Bakkour, S., Pear, W. S. and Bernstein, I. D. (2000). Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling. Nat. Med. 6, 1278-1281.
69. Vasiliauskas, D., Laufer, E. and Stern, C. D. (2003). A role for hairy1 in regulating chick limb bud growth. Dev. Biol. 262, 94-106. (Pubitemid 37153107)
70. Vilimas, T., Mascarenhas, J., Palomero, T., Mandal, M., Buonamici, S., Meng, F., Thompson, B., Spaulding, C., Macaroun, S., Alegre, M. L. et al. (2007). Targeting the NF-kappaB signaling pathway in Notch1-induced T-cell leukemia. Nat. Med. 13, 70-77. (Pubitemid 46067388)
71. Vujovic, S., Henderson, S. R., Flanagan, A. M. and Clements, M. O. (2007). Inhibition of gamma-secretases alters both proliferation and differentiation of mesenchymal stem cells. Cell Prolif. 40, 185-195. (Pubitemid 46398815)
72. Wang, J., Shelly, L., Miele, L., Boykins, R., Norcross, M. A. and Guan, E. (2001). Human Notch-1 inhibits NF-kappa B activity in the nucleus through a direct interaction involving a novel domain. J. Immunol. 167, 289-295. (Pubitemid 32567791)
73. Williams, R., Lendahl, U. and Lardelli, M. (1995). Complementary and combinatorial patterns of Notch gene family expression during early mouse development. Mech. Dev. 53, 357-368.
74. Xue, Y., Gao, X., Lindsell, C. E., Norton, C. R., Chang, B., Hicks, C., Gendron-Maguire, M., Rand, E. B., Weinmaster, G. and Gridley, T. (1999). Embryonic lethality and vascular defects in mice lacking the Notch ligand Jagged1. Hum. Mol. Genet. 8, 723-730. (Pubitemid 29189039)
75. Zanotti, S. and Canalis, E. (2009). Notch and the skeleton. Mol. Cell. Biol. 30, 886-896.
76. 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.
77. Zhang, X., Ziran, N., Goater, J. J., Schwarz, E. M., Puzas, J. E., Rosier, R. N., Zuscik, M., Drissi, H. and O'Keefe, R. J. (2004). Primary murine limb bud mesenchymal cells in long-term culture complete chondrocyte differentiation: TGF-beta delays hypertrophy and PGE2 inhibits terminal differentiation. Bone 34, 809-817. (Pubitemid 38581126)