Differential regulation of NOTCH2 and NOTCH3 contribute to their unique functions in vascular smooth muscle cells

Journal of Biological Chemistry

Volumn 290, Issue 26, 2015, Pages 16226-16237

  Baeten, Jeremy T ^a,b   Lilly, Brenda ^a,b  

^a NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CELLS; CYTOLOGY; MUSCLE;

CELL SURVIVAL; DIFFERENTIAL REGULATION; KEY REGULATORS; MAP KINASE SIGNALING; NOTCH RECEPTOR; NOTCH SIGNALING; RECEPTOR EXPRESSION; VASCULAR SMOOTH MUSCLE CELLS;

CELL SIGNALING;

MITOGEN ACTIVATED PROTEIN KINASE; NOTCH2 RECEPTOR; NOTCH3 RECEPTOR; NOTCH RECEPTOR; NOTCH3 PROTEIN, HUMAN; NOTCH3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; C57BL MOUSE; CYTOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

ANIMALS; CELL PROLIFERATION; CELL SURVIVAL; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; RECEPTOR, NOTCH2; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84941345833     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.655548     Document Type: Article

References (61)

1. 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
2. Egan, S. E., St-Pierre, B., and Leow, C. C. (1998) Notch receptors, partners and regulators: from conserved domains to powerful functions. Curr. Topics Microbiol. Immunol. 228, 273-324
3. Bianchi, S., Dotti, M. T., and Federico, A. (2006) Physiology and pathology of notch signalling system. J. Cell. Physiol. 207, 300-308
4. Pursglove, S. E., and Mackay, J. P. (2005) CSL: a notch above the rest. Int. J. Biochem. Cell Biol. 37, 2472-2477
5. Blokzijl, A., Dahlqvist, C., Reissmann, E., Falk, A., Moliner, A., Lendahl, U., and Ibáñez, C. F. (2003) Cross-talk between the Notch and TGF-β signaling pathways mediated by interaction of the Notch intracellular domain with Smad3. J. Cell Biol. 163, 723-728
6. Hiratochi, M., Nagase, H., Kuramochi, Y., Koh, C. S., Ohkawara, T., and Nakayama, K. (2007) The Delta intracellular domain mediates TGF-β/Activin signaling through binding to Smads and has an important bidirectional function in the Notch-Delta signaling pathway. Nucleic Acids Res. 35, 912-922
7. Hayward, P., Brennan, K., Sanders, P., Balayo, T., Das Gupta, 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
8. Muñoz-Descalzo, S., Tkocz, K., Balayo, T., and Arias, A. M. (2011) Modulation of the ligand-independent traffic of Notch by Axin and Apc contributes to the activation of Armadillo in Drosophila. Development 138, 1501-1506
9. Wang, T., Holt, C. M., Xu, C., Ridley, C., R, P. O. Jones, R., Baron, M., and Trump, D. (2007) Notch3 activation modulates cell growth behaviour and cross-talk to Wnt/TCF signalling pathway. Cell. Signal. 19, 2458-2467
10. Carmena, A., Speicher, S., and Baylies, M. (2006) The PDZ protein Canoe/AF-6 links Ras-MAPK, Notch and Wingless/Wnt signaling pathways by directly interacting with Ras, Notch and Dishevelled. PloS one 1, e66
11. Wang, W., Prince, C. Z., Mou, Y., and Pollman, M. J. (2002) Notch3 signaling in vascular smooth muscle cells induces c-FLIP expression via ERK/MAPK activation. Resistance to Fas ligand-induced apoptosis. J. Biol. Chem. 277, 21723-21729
12. High, F. A., Lu, M. M., Pear, W. S., Loomes, K. M., Kaestner, K. H., and Epstein, J. A. (2008) Endothelial expression of the Notch ligand Jagged1 is required for vascular smooth muscle development. Proc. Natl. Acad. Sci. U. S. A. 105, 1955-1959
13. High, F. A., Zhang, M., Proweller, A., Tu, L., Parmacek, M. S., Pear, W. S., and Epstein, J. A. (2007) An essential role for Notch in neural crest during cardiovascular development and smooth muscle differentiation. J. Clin. Investig. 117, 353-363
14. Li, Y., Takeshita, K., Liu, P. Y., Satoh, M., Oyama, N., Mukai, Y., Chin, M. T., Krebs, L., Kotlikoff, M. I., Radtke, F., Gridley, T., and Liao, J. K. (2009) Smooth muscle Notch1 mediates neointimal formation after vascular injury. Circulation 119, 2686-2692
15. Tang, Y., Urs, S., Boucher, J., Bernaiche, T., Venkatesh, D., Spicer, D. B., Vary, C. P., and Liaw, L. (2010) Notch and transforming growth factor-β (TGFβ) signaling pathways cooperatively regulate vascular smooth muscle cell differentiation. J. Biol. Chem. 285, 17556-17563
16. Gridley, T. (2007) Notch signaling in vascular development and physiology. Development 134, 2709-2718
17. Lawson, N. D., Scheer, N., Pham, V. N., Kim, C. H., Chitnis, A. B., Campos-Ortega, J. A., and Weinstein, B. M. (2001) Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 128, 3675-3683
18. Phng, L. K., and Gerhardt, H. (2009) Angiogenesis: a team effort coordinated by notch. Dev. Cell 16, 196-208
19. Boucher, J., Gridley, T., and Liaw, L. (2012) Molecular pathways of notch signaling in vascular smooth muscle cells. Front. Physiol. 3, 81
20. Doi, H., Iso, T., Sato, H., Yamazaki, M., Matsui, H., Tanaka, T., Manabe, I., Arai, M., Nagai, R., and Kurabayashi, M. (2006) Jagged1-selective notch signaling induces smooth muscle differentiation via a RBP-Jκ-dependent pathway. J. Biol. Chem. 281, 28555-28564
21. Liu, H., Zhang, W., Kennard, S., Caldwell, R. B., and Lilly, B. (2010) Notch3 is critical for proper angiogenesis and mural cell investment. Circulation research 107, 860-870
22. Wang, Q., Zhao, N., Kennard, S., and Lilly, B. (2012) Notch2 and Notch3 function together to regulate vascular smooth muscle development. PLoS One 7, e37365
23. Lin, C. H., and Lilly, B. (2014) Endothelial cells direct mesenchymal stem cells toward a smooth muscle cell fate. Stem Cells Dev. 23, 2581-2590
24. Lin, C. H., and Lilly, B. (2014) Notch signaling governs phenotypic modulation of smooth muscle cells. Vasc. Pharmacol. 63, 88-96
25. Sweeney, C., Morrow, D., Birney, Y. A., Coyle, S., Hennessy, C., Scheller, A., Cummins, P. M., Walls, D., Redmond, E. M., and Cahill, P. A. (2004) Notch 1 and 3 receptor signaling modulates vascular smooth muscle cell growth, apoptosis, and migration via a CBF-1/RBP-Jk dependent pathway. FASEB J. 18, 1421-1423
26. Havrda, M. C., Johnson, M. J., O'Neill, C. F., and Liaw, L. (2006) A novel mechanism of transcriptional repression of p27kip1 through Notch/HRT2 signaling in vascular smooth muscle cells. Thrombosis Haemostasis 96, 361-370
27. Boucher, J. M., Harrington, A., Rostama, B., Lindner, V., and Liaw, L. (2013) A Receptor-Specific Function for Notch2 in Mediating Vascular Smooth Muscle Cell Growth Arrest Through Cyclin-dependent Kinase Inhibitor 1B. Circulation Res. 113, 975-985
28. Cao, H., Hu, Y., Wang, P., Zhou, J., Deng, Z., and Wen, J. (2012) Downregulation of Notch receptor signaling pathway induces caspase-dependent and caspase-independent apoptosis in lung squamous cell carcinoma cells. APMIS 120, 441-450
29. Carvalho, F. L., Simons, B. W., Eberhart, C. G., and Berman, D. M. (2014) Notch signaling in prostate cancer: a moving target. The Prostate 74, 933-945
30. Mann, C. D., Bastianpillai, C., Neal, C. P., Masood, M. M., Jones, D. J., Teichert, F., Singh, R., Karpova, E., Berry, D. P., and Manson, M. M. (2012) Notch3 and HEY-1 as prognostic biomarkers in pancreatic adenocarcinoma. PloS one 7, e51119
31. O'Neill, C. F., Urs, S., Cinelli, C., Lincoln, A., Nadeau, R. J., León, R., Toher, J., Mouta-Bellum, C., Friesel, R. E., and Liaw, L. (2007) Notch2 signaling induces apoptosis and inhibits human MDA-MB-231 xenograft growth. Am. J. Pathol. 171, 1023-1036
32. Pancewicz, J., and Nicot, C. (2011) Current views on the role of Notch signaling and the pathogenesis of human leukemia. BMC cancer 11, 502
33. Konishi, J., Yi, F., Chen, X., Vo, H., Carbone, D. P., and Dang, T. P. (2010) Notch3 cooperates with the EGFR pathway to modulate apoptosis through the induction of bim. Oncogene 29, 589-596
34. Lin, L., Mernaugh, R., Yi, F., Blum, D., Carbone, D. P., and Dang, T. P. (2010) Targeting specific regions of the Notch3 ligand-binding domain induces apoptosis and inhibits tumor growth in lung cancer. Cancer Res. 70, 632-638
35. Song, G., Zhang, Y., and Wang, L. (2009) MicroRNA-206 targets notch3, activates apoptosis, and inhibits tumor cell migration and focus formation. J. Biol. Chem. 284, 31921-31927
36. Wang, X. W., Xi, X. Q., Wu, J., Wan, Y. Y., Hui, H. X., and Cao, X. F. (2015) microRNA-206 attenuates tumor proliferation and migration involving the downregulation of NOTCH3 in colorectal cancer. Oncology Reports 33, 1402-1410
37. Henshall, T. L., Keller, A., He, L., Johansson, B. R., Wallgard, E., Raschperger, E., Mäe, M. A., Jin, S., Betsholtz, C., and Lendahl, U. (2015) Notch3 is necessary for blood vessel integrity in the central nervous system. Arterioscler. Thromb. Vasc. Biol. 35, 409-420
38. Jalali, S., Ramanathan, G. K., Parthasarathy, P. T., Aljubran, S., Galam, L., Yunus, A., Garcia, S., Cox, R. R., Jr., Lockey, R. F., and Kolliputi, N. (2012) Mir-206 regulates pulmonary artery smooth muscle cell proliferation and differentiation. PloS one 7, e46808
39. Ye, Y. Z., Zhang, Z. H., Fan, X. Y., Xu, X. L., Chen, M. L., Chang, B. W., and Zhang, Y. B. (2013) Notch3 overexpression associates with poor prognosis in human non-small-cell lung cancer. Med. Oncol. 30, 595
40. Truong, M., Cook, M. R., Pinchot, S. N., Kunnimalaiyaan, M., and Chen, H. (2011) Resveratrol induces Notch2-mediated apoptosis and suppression of neuroendocrine markers in medullary thyroid cancer. Ann. Surg. Oncol. 18, 1506-1511
41. Liu, H., Kennard, S., and Lilly, B. (2009) NOT CH3 expression is induced in mural cells through an autoregulatory loop that requires endothelial-expressed JAGGED1. Circ. Res. 104, 466-475
42. Liu, H., Chen, B., and Lilly, B. (2008) Fibroblasts potentiate blood vessel formation partially through secreted factor TIMP-1. Angiogenesis 11, 223-234
43. Voss, O. H., Kim, S., Wewers, M. D., and Doseff, A. I. (2005) Regulation of monocyte apoptosis by the protein kinase CΔ-dependent phosphorylation of caspase-3. J. Biol. Chem. 280, 17371-17379
44. Krebs, L. T., Xue, Y., Norton, C. R., Sundberg, J. P., Beatus, P., Lendahl, U., Joutel, A., and Gridley, T. (2003) Characterization of Notch3-deficient mice: normal embryonic development and absence of genetic interactions with a Notch1 mutation. Genesis 37, 139-143
45. McCright, B., Lozier, J., and Gridley, T. (2006) Generation of new Notch2 mutant alleles. Genesis 44, 29-33
46. Long, X., Creemers, E. E., Wang, D. Z., Olson, E. N., and Miano, J. M. (2007) Myocardin is a bifunctional switch for smooth versus skeletal muscle differentiation. Proc. Natl. Acad. Sci. U. S. A. 104, 16570-16575
47. Vaux, D. L., Cory, S., and Adams, J. M. (1988) Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335, 440-442
48. Ambrosini, G., Adida, C., and Altieri, D. C. (1997) A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nature Med. 3, 917-921
49. Irmler, M., Thome, M., Hahne, M., Schneider, P., Hofmann, K., Steiner, V., Bodmer, J. L., Schröter, M., Burns, K., Mattmann, C., Rimoldi, D., French, L. E., and Tschopp, J. (1997) Inhibition of death receptor signals by cellular FLIP. Nature 388, 190-195
50. Boucher, M. J., Morisset, J., Vachon, P. H., Reed, J. C., Lainé, J., and Rivard, N. (2000) MEK/ERK signaling pathway regulates the expression of Bcl-2, Bcl-X (L), and Mcl-1 and promotes survival of human pancreatic cancer cells. J. Cell. Biochem. 79, 355-369
51. Seidelin, J. B., Coskun, M., Vainer, B., Riis, L., Soendergaard, C., and Nielsen, O. H. (2013) ERK controls epithelial cell death receptor signalling and cellular FLICE-like inhibitory protein (c-FLIP) in ulcerative colitis. J. Mol. Med. 91, 839-849
52. Zhao, X., Ogunwobi, O. O., and Liu, C. (2011) Survivin inhibition is critical for Bcl-2 inhibitor-induced apoptosis in hepatocellular carcinoma cells. PloS one 6, e21980
53. Ballif, B. A., and Blenis, J. (2001) Molecular mechanisms mediating mammalian mitogen-activated protein kinase (MAPK) kinase (MEK)-MAPK cell survival signals. Cell Growth Differ. 12, 397-408
54. Bonni, A., Brunet, A., West, A. E., Datta, S. R., Takasu, M. A., and Greenberg, M. E. (1999) Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286, 1358-1362
55. Jin, S., Hansson, E. M., Tikka, S., Lanner, F., Sahlgren, C., Farnebo, F., Baumann, M., Kalimo, H., and Lendahl, U. (2008) Notch signaling regulates platelet-derived growth factor receptor-β expression in vascular smooth muscle cells. Circulation Res. 102, 1483-1491
56. Iso, T., Hamamori, Y., and Kedes, L. (2003) Notch signaling in vascular development. Arterioscler., Thromb., Vasc. Biol. 23, 543-553
57. Domenga, V., Fardoux, P., Lacombe, P., Monet, M., Maciazek, J., Krebs, L. T., Klonjkowski, B., Berrou, E., Mericskay, M., Li, Z., Tournier-Lasserve, E., Gridley, T., and Joutel, A. (2004) Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev. 18, 2730-2735
58. Li, X., Zhang, X., Leathers, R., Makino, A., Huang, C., Parsa, P., Macias, J., Yuan, J. X., Jamieson, S. W., and Thistlethwaite, P. A. (2009) Notch3 signaling promotes the development of pulmonary arterial hypertension. Nature Medicine 15, 1289-1297
59. Kok, F. O., Shin, M., Ni, C. W., Gupta, A., Grosse, A. S., Van Impel, A., Kirchmaier, B. C., Peterson-Maduro, J., Kourkoulis, G., Male, I., De Santis, D. F., Sheppard-Tindell, S., Ebarasi, L., Betsholtz, C., Schulte-Merker, S., Wolfe, S. A., and Lawson, N. D. (2015) Reverse genetic screening reveals poor correlation between morpholino-induced and mutant phenotypes in zebrafish. Dev. Cell 32, 97-108
60. Fedorov, Y., Anderson, E. M., Birmingham, A., Reynolds, A., Karpilow, J., Robinson, K., Leake, D., Marshall, W. S., and Khvorova, A. (2006) Offtarget effects by siRNA can induce toxic phenotype. Rna 12, 1188-1196
61. Jackson, A. L., and Linsley, P. S. (2004) Noise amidst the silence: off-target effects of siRNAs? Trends Genetics 20, 521-524