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Science 30 April 1999:
Vol. 284. no. 5415, pp. 770 - 776
DOI: 10.1126/science.284.5415.770
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Review

Notch Signaling: Cell Fate Control and Signal Integration in Development

Spyros Artavanis-Tsakonas, * Matthew D. Rand, Robert J. Lake

Notch signaling defines an evolutionarily ancient cell interaction mechanism, which plays a fundamental role in metazoan development. Signals exchanged between neighboring cells through the Notch receptor can amplify and consolidate molecular differences, which eventually dictate cell fates. Thus, Notch signals control how cells respond to intrinsic or extrinsic developmental cues that are necessary to unfold specific developmental programs. Notch activity affects the implementation of differentiation, proliferation, and apoptotic programs, providing a general developmental tool to influence organ formation and morphogenesis.

Massachusetts General Hospital Cancer Center, Department of Cell Biology, Harvard Medical School, Building 149, 13th Street, Charlestown, MA 02129, USA.
*   To whom correspondence should be addressed.

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J. Biol. Chem. 283, 35486-35495
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J. Cell Biol. 183, 1129-1143
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Circ. Res. 103, 1370-1382
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RNA target specificity of the embryonic cell fate determinant POS-1.
B. M. Farley, J. M. Pagano, and S. P. Ryder (2008)
RNA 14, 2685-2697
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A. M. Ghaleb, G. Aggarwal, A. B. Bialkowska, M. O. Nandan, and V. W. Yang (2008)
Mol. Cancer Res. 6, 1920-1927
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Impaired Notch4 Activity Elicits Endothelial Cell Activation and Apoptosis: Implication for Transplant Arteriosclerosis.
T. Quillard, S. Coupel, F. Coulon, J. Fitau, M. Chatelais, M.C. Cuturi, E. Chiffoleau, and B. Charreau (2008)
Arterioscler. Thromb. Vasc. Biol. 28, 2258-2265
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Defective Notch activation in microenvironment leads to myeloproliferative disease.
Y.-W. Kim, B.-K. Koo, H.-W. Jeong, M.-J. Yoon, R. Song, J. Shin, D.-C. Jeong, S.-H. Kim, and Y.-Y. Kong (2008)
Blood 112, 4628-4638
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Oncogenesis of T-ALL and nonmalignant consequences of overexpressing intracellular NOTCH1.
X. Li, F. Gounari, A. Protopopov, K. Khazaie, and H. von Boehmer (2008)
J. Exp. Med. 205, 2851-2861
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Artery and vein size is balanced by Notch and ephrin B2/EphB4 during angiogenesis.
Y. H. Kim, H. Hu, S. Guevara-Gallardo, M. T. Y. Lam, S.-Y. Fong, and R. A. Wang (2008)
Development 135, 3755-3764
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Signaling Pathways Controlling Neural Stem Cells Slow Progressive Brain Disease.
A. Androutsellis-Theotokis, M.A. Rueger, H. Mkhikian, E. Korb, and R.D.G. McKay (2008)
Cold Spring Harb Symp Quant Biol
   Abstract »    PDF »
Notch signaling is required for the maintenance of enteric neural crest progenitors.
Y. Okamura and Y. Saga (2008)
Development 135, 3555-3565
   Abstract »    Full Text »    PDF »
The Diversity of O-Linked Glycans Expressed during Drosophila melanogaster Development Reflects Stage- and Tissue-specific Requirements for Cell Signaling.
K. Aoki, M. Porterfield, S. S. Lee, B. Dong, K. Nguyen, K. H. McGlamry, and M. Tiemeyer (2008)
J. Biol. Chem. 283, 30385-30400
   Abstract »    Full Text »    PDF »
Mind bomb 1 in the lymphopoietic niches is essential for T and marginal zone B cell development.
R. Song, Y.-W. Kim, B.-K. Koo, H.-W. Jeong, M.-J. Yoon, K.-J. Yoon, D.-J. Jun, S.-K. Im, J. Shin, M.-P. Kong, et al. (2008)
J. Exp. Med. 205, 2525-2536
   Abstract »    Full Text »    PDF »
{gamma}-Secretase Activation of Notch Signaling Regulates the Balance of Proximal and Distal Fates in Progenitor Cells of the Developing Lung.
P.-N. Tsao, F. Chen, K. I. Izvolsky, J. Walker, M. A. Kukuruzinska, J. Lu, and W. V. Cardoso (2008)
J. Biol. Chem. 283, 29532-29544
   Abstract »    Full Text »    PDF »
Brothers and Sisters: Molecular Insights Into Arterial-Venous Heterogeneity.
J. Aitsebaomo, A. L. Portbury, J. C. Schisler, and C. Patterson (2008)
Circ. Res. 103, 929-939
   Abstract »    Full Text »    PDF »
The Association of Notch2 and NF-{kappa}B Accelerates RANKL-Induced Osteoclastogenesis.
H. Fukushima, A. Nakao, F. Okamoto, M. Shin, H. Kajiya, S. Sakano, A. Bigas, E. Jimi, and K. Okabe (2008)
Mol. Cell. Biol. 28, 6402-6412
   Abstract »    Full Text »    PDF »
AP-2 factors act in concert with Notch to orchestrate terminal differentiation in skin epidermis.
X. Wang, H. A. Pasolli, T. Williams, and E. Fuchs (2008)
J. Cell Biol. 183, 37-48
   Abstract »    Full Text »    PDF »
Notch1 signaling stimulates proliferation of immature cardiomyocytes.
C. Collesi, L. Zentilin, G. Sinagra, and M. Giacca (2008)
J. Cell Biol. 183, 117-128
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Hairless induces cell death by downregulation of EGFR signalling activity.
C. E. Protzer, I. Wech, and A. C. Nagel (2008)
J. Cell Sci. 121, 3167-3176
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Ero1L, a thiol oxidase, is required for Notch signaling through cysteine bridge formation of the Lin12-Notch repeats in Drosophila melanogaster.
A.-C. Tien, A. Rajan, K. L. Schulze, H. D. Ryoo, M. Acar, H. Steller, and H. J. Bellen (2008)
J. Cell Biol. 182, 1113-1125
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NOTCH1 mutations in individuals with left ventricular outflow tract malformations reduce ligand-induced signaling.
K. L. McBride, M. F. Riley, G. A. Zender, S. M. Fitzgerald-Butt, J. A. Towbin, J. W. Belmont, and S. E. Cole (2008)
Hum. Mol. Genet. 17, 2886-2893
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Hedgehog: functions and mechanisms.
M. Varjosalo and J. Taipale (2008)
Genes & Dev. 22, 2454-2472
   Abstract »    Full Text »    PDF »
ADAM10 is essential for proteolytic activation of Notch during thymocyte development.
L. Tian, X. Wu, C. Chi, M. Han, T. Xu, and Y. Zhuang (2008)
Int. Immunol. 20, 1181-1187
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Self-modulation of Notch signaling during ommatidial development via the Roughened eye transcriptional repressor.
D. del Alamo and M. Mlodzik (2008)
Development 135, 2895-2904
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Clonal analysis of Drosophila antennal lobe neurons: diverse neuronal architectures in the lateral neuroblast lineage.
S.-L. Lai, T. Awasaki, K. Ito, and T. Lee (2008)
Development 135, 2883-2893
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Soluble Forms of the Notch Ligands Delta1 and Jagged1 Promote in Vivo Tumorigenicity in NIH3T3 Fibroblasts with Distinct Phenotypes.
S. Urs, A. Roudabush, C. F. O'Neill, I. Pinz, I. Prudovsky, D. Kacer, Y. Tang, L. Liaw, and D. Small (2008)
Am. J. Pathol. 173, 865-878
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BRI2 Inhibits Amyloid {beta}-Peptide Precursor Protein Processing by Interfering with the Docking of Secretases to the Substrate.
S. Matsuda, L. Giliberto, Y. Matsuda, E. M. McGowan, and L. D'Adamio (2008)
J. Neurosci. 28, 8668-8676
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The intracellular region of Notch ligands Dll1 and Dll3 regulates their trafficking and signaling activity.
S. F. Heuss, D. Ndiaye-Lobry, E. M. Six, A. Israel, and F. Logeat (2008)
PNAS 105, 11212-11217
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The Activated Notch1 Receptor Cooperates with {alpha}-Enolase and MBP-1 in Modulating c-myc Activity.
K.-W. Hsu, R.-H. Hsieh, Y.-H. W. Lee, C.-H. Chao, K.-J. Wu, M.-J. Tseng, and T.-S. Yeh (2008)
Mol. Cell. Biol. 28, 4829-4842
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Mind bomb-1 Is Essential for Intraembryonic Hematopoiesis in the Aortic Endothelium and the Subaortic Patches.
M.-J. Yoon, B.-K. Koo, R. Song, H.-W. Jeong, J. Shin, Y.-W. Kim, Y.-Y. Kong, and P.-G. Suh (2008)
Mol. Cell. Biol. 28, 4794-4804
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Notch Inhibits Osteoblast Differentiation and Causes Osteopenia.
S. Zanotti, A. Smerdel-Ramoya, L. Stadmeyer, D. Durant, F. Radtke, and E. Canalis (2008)
Endocrinology 149, 3890-3899
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Inhibitor of differentiation 4 drives brain tumor-initiating cell genesis through cyclin E and notch signaling.
H.-M. Jeon, X. Jin, J.-S. Lee, S.-Y. Oh, Y.-W. Sohn, H.-J. Park, K. M. Joo, W.-Y. Park, D.-H. Nam, R. A. DePinho, et al. (2008)
Genes & Dev. 22, 2028-2033
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Receptor Type Protein Tyrosine Phosphatase {zeta}-Pleiotrophin Signaling Controls Endocytic Trafficking of DNER That Regulates Neuritogenesis.
N. Fukazawa, S. Yokoyama, M. Eiraku, M. Kengaku, and N. Maeda (2008)
Mol. Cell. Biol. 28, 4494-4506
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LvNumb works synergistically with Notch signaling to specify non-skeletal mesoderm cells in the sea urchin embryo.
R. C. Range, T. D. Glenn, E. Miranda, and D. R. McClay (2008)
Development 135, 2445-2454
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Ethanol stimulates endothelial cell angiogenic activity via a Notch- and angiopoietin-1-dependent pathway.
D. Morrow, J. P. Cullen, P. A. Cahill, and E. M. Redmond (2008)
Cardiovasc Res 79, 313-321
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Biological Functions of Glycosyltransferase Genes Involved in O-fucose Glycan Synthesis.
T. Okajima, A. Matsuura, and T. Matsuda (2008)
J. Biochem. 144, 1-6
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Methylmercury Activates Enhancer-of-Split and Bearded Complex Genes Independent of the Notch Receptor.
M. D. Rand, C. E. Bland, and J. Bond (2008)
Toxicol. Sci. 104, 163-176
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NOTCH2 mutations in marginal zone lymphoma.
G. Troen, I. Wlodarska, A. Warsame, S. Hernandez Llodra, C. De Wolf-Peeters, and J. Delabie (2008)
Haematologica 93, 1107-1109
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Cancer Stem Cells and the Ontogeny of Lung Cancer.
C. D. Peacock and D. N. Watkins (2008)
J. Clin. Oncol. 26, 2883-2889
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Delta-like 1 is essential for the maintenance of marginal zone B cells in normal mice but not in autoimmune mice.
Y. Moriyama, C. Sekine, A. Koyanagi, N. Koyama, H. Ogata, S. Chiba, S. Hirose, K. Okumura, and H. Yagita (2008)
Int. Immunol. 20, 763-773
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RAM-induced Allostery Facilitates Assembly of a Notch Pathway Active Transcription Complex.
D. R. Friedmann, J. J. Wilson, and R. A. Kovall (2008)
J. Biol. Chem. 283, 14781-14791
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Notch Signaling in Cardiac Development.
K. Niessen and A. Karsan (2008)
Circ. Res. 102, 1169-1181
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ETO, but Not Leukemogenic Fusion Protein AML1/ETO, Augments RBP-J{kappa}/SHARP-Mediated Repression of Notch Target Genes.
D. Salat, R. Liefke, J. Wiedenmann, T. Borggrefe, and F. Oswald (2008)
Mol. Cell. Biol. 28, 3502-3512
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Critical Role of Notch Signaling in Osteosarcoma Invasion and Metastasis.
P. Zhang, Y. Yang, P. A. Zweidler-McKay, and D. P.M. Hughes (2008)
Clin. Cancer Res. 14, 2962-2969
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Essential role of Notch signaling in effector memory CD8+ T cell-mediated airway hyperresponsiveness and inflammation.
M. Okamoto, K. Takeda, A. Joetham, H. Ohnishi, H. Matsuda, C. H. Swasey, B. J. Swanson, K. Yasutomo, A. Dakhama, and E. W. Gelfand (2008)
J. Exp. Med. 205, 1087-1097
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Activation of Notch-Mediated Protective Signaling in the Myocardium.
N. A. Gude, G. Emmanuel, W. Wu, C. T. Cottage, K. Fischer, P. Quijada, J. A. Muraski, R. Alvarez, M. Rubio, E. Schaefer, et al. (2008)
Circ. Res. 102, 1025-1035
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Current Management of Medullary Thyroid Cancer.
R. S. Sippel, M. Kunnimalaiyaan, and H. Chen (2008)
Oncologist 13, 539-547
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Hes1 Regulates Corneal Development and the Function of Corneal Epithelial Stem/Progenitor Cells.
T. Nakamura, T. Ohtsuka, E. Sekiyama, L. J. Cooper, H. Kokubu, N. J. Fullwood, Y. Barrandon, R. Kageyama, and S. Kinoshita (2008)
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Localization of the Delta-like-1-binding Site in Human Notch-1 and Its Modulation by Calcium Affinity.
J. Cordle, C. RedfieldZ, M. Stacey, P. A. van der Merwe, A. C. Willis, B. R. Champion, S. Hambleton, and P. A. Handford (2008)
J. Biol. Chem. 283, 11785-11793
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Linking Notch signaling to ischemic stroke.
J. F. Arboleda-Velasquez, Z. Zhou, H. K. Shin, A. Louvi, H.-H. Kim, S. I. Savitz, J. K. Liao, S. Salomone, C. Ayata, M. A. Moskowitz, et al. (2008)
PNAS 105, 4856-4861
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Regulation of Lymphocyte Development by Cell-Type-Specific Interpretation of Notch Signals.
L. Nie, S. S. Perry, Y. Zhao, J. Huang, P. W. Kincade, M. A. Farrar, and X.-H. Sun (2008)
Mol. Cell. Biol. 28, 2078-2090
   Abstract »    Full Text »    PDF »
Defining Pancreatic Endocrine Precursors and Their Descendants.
P. White, C. Lee May, R. N. Lamounier, J. E. Brestelli, and K. H. Kaestner (2008)
Diabetes 57, 654-668
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Distinct Effects of the Soluble Versus Membrane-Bound Forms of the Notch Ligand Delta-4 on Human CD34+CD38low Cell Expansion and Differentiation.
M. Lahmar, C. Catelain, S. Poirault, M. Dorsch, J.-L. Villeval, W. Vainchenker, O. Albagli, and E. Lauret (2008)
Stem Cells 26, 621-629
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Notch Signaling Through Jagged-1 Is Necessary to Initiate Chondrogenesis in Human Bone Marrow Stromal Cells but Must Be Switched off to Complete Chondrogenesis.
R. A. Oldershaw, S. R. Tew, A. M. Russell, K. Meade, R. Hawkins, T. R. McKay, K. R. Brennan, and T. E. Hardingham (2008)
Stem Cells 26, 666-674
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Science. ISSN 0036-8075 (print), 1095-9203 (online)