Notch signaling mediates TGF-β1-induced epithelial-mesenchymal transition through the induction of Snai1

International Journal of Biochemistry and Cell Biology

Volumn 44, Issue 5, 2012, Pages 776-789

  Matsuno, Yosuke ^a   Coelho, Ana Lucia ^a   Jarai, Gabor ^b   Westwick, John ^b   Hogaboam, Cory M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b Novartis Institutes of Biomedical Research   (United Kingdom)

Author keywords

A549; EMT; Notch signaling; Snai1; TGF 1

Indexed keywords

FIBRONECTIN; GAMMA SECRETASE INHIBITOR; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; JAGGED1; NERVE CELL ADHESION MOLECULE; NOTCH RECEPTOR; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA1; UVOMORULIN; VIMENTIN;

ARTICLE; CELL COMMUNICATION; CELL FATE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; HUMAN; HUMAN CELL; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

CALCIUM-BINDING PROTEINS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINE; CELL MOVEMENT; ENZYME INHIBITORS; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; PLASMIDS; RECEPTORS, NOTCH; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84859270591     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2012.01.021     Document Type: Article

References (48)

1. H. Acloque, M.S. Adams, K. Fishwick, M. Bronner-Fraser, and M.A. Nieto Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease J Clin Invest 119 2009 1438 1449
2. D. Amsen, J.M. Blander, G.R. Lee, K. Tanigaki, T. Honjo, and R.A. Flavell Instruction of distinct CD4T helper cell fates by different notch ligands on antigen-presenting cells Cell 117 2004 515 526 (Pubitemid 38610236)
3. R. Benedito, C. Roca, I. Sorensen, S. Adams, A. Gossler, and M. Fruttiger The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis Cell 137 2009 1124 1135
4. V. Bolos, J. Grego-Bessa, and J.L. de la Pompa Notch signaling in development and cancer Endocr Rev 28 2007 339 363 (Pubitemid 46984831)
5. S. Brabletz, K. Bajdak, S. Meidhof, U. Burk, G. Niedermann, and E. Firat The ZEB1/miR-200 feedback loop controls Notch signalling in cancer cells EMBO J 30 2011 770 782
6. R.M. Bremnes, R. Veve, E. Gabrielson, F.R. Hirsch, A. Baron, and L. Bemis High-throughput tissue microarray analysis used to evaluate biology and prognostic significance of the E-cadherin pathway in non-small-cell lung cancer J Clin Oncol 20 2002 2417 2428 (Pubitemid 34525727)
7. J. Chen, N. Imanaka, and J.D. Griffin Hypoxia potentiates Notch signaling in breast cancer leading to decreased E-cadherin expression and increased cell migration and invasion Br J Cancer 102 2010 351 360
8. X. Chen, A. Stoeck, S.J. Lee, M. Shih Ie, M.M. Wang, and T.L. Wang Jagged1 expression regulated by Notch3 and Wnt/beta-catenin signaling pathways in ovarian cancer Oncotarget 1 2010 210 218
9. P. Cheng, Y. Nefedova, C.A. Corzo, and D.I. Gabrilovich Regulation of dendritic-cell differentiation by bone marrow stroma via different Notch ligands Blood 109 2007 507 515 (Pubitemid 46105947)
10. T. Donnem, S. Andersen, K. Al-Shibli, S. Al-Saad, L.T. Busund, and R.M. Bremnes Prognostic impact of Notch ligands and receptors in nonsmall cell lung cancer: coexpression of Notch-1 and vascular endothelial growth factor-A predicts poor survival Cancer 116 2010 5676 5685
11. J. Foldi, A.Y. Chung, H. Xu, J. Zhu, H.H. Outtz, and J. Kitajewski Autoamplification of Notch signaling in macrophages by TLR-induced and RBP-J-dependent induction of Jagged1 J Immunol 185 2010 5023 5031
12. D. Gallahan, and R. Callahan Mammary tumorigenesis in feral mice: identification of a new int locus in mouse mammary tumor virus (Czech II)-induced mammary tumors J Virol 61 1987 66 74 (Pubitemid 17212445)
13. E. Gore-Hyer, D. Shegogue, M. Markiewicz, S. Lo, D. Hazen-Martin, and E.L. Greene TGF-beta and CTGF have overlapping and distinct fibrogenic effects on human renal cells Am J Physiol Renal Physiol 283 2002 F707 F716
14. I. Graziani, S. Eliasz, M.A. De Marco, Y. Chen, H.I. Pass, and R.M. De May Opposite effects of Notch-1 and Notch-2 on mesothelioma cell survival under hypoxia are exerted through the Akt pathway Cancer Res 68 2008 9678 9685
15. A. Jayachandran, M. Konigshoff, H. Yu, E. Rupniewska, M. Hecker, and W. Klepetko SNAI transcription factors mediate epithelial-mesenchymal transition in lung fibrosis Thorax 64 2009 1053 1061
16. D.A. Johnston, B. Dong, and C.C. Hughes TNF induction of jagged-1 in endothelial cells is NFkappaB-dependent Gene 435 2009 36 44
17. R. Kalluri, and R.A. Weinberg The basics of epithelial-mesenchymal transition J Clin Invest 119 2009 1420 1428
18. H. Kasai, J.T. Allen, R.M. Mason, T. Kamimura, and Z. Zhang TGF-beta1 induces human alveolar epithelial to mesenchymal cell transition (EMT) Respir Res 6 2005 56
19. K.K. Kim, M.C. Kugler, P.J. Wolters, L. Robillard, M.G. Galvez, and A.N. Brumwell Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix Proc Natl Acad Sci U S A 103 2006 13180 13185 (Pubitemid 44338936)
20. K.G. Leong, X. Hu, L. Li, M. Noseda, B. Larrivee, and C. Hull Activated Notch4 inhibits angiogenesis: role of beta 1-integrin activation Mol Cell Biol 22 2002 2830 2841 (Pubitemid 34263003)
21. K.G. Leong, and A. Karsan Recent insights into the role of Notch signaling in tumorigenesis Blood 107 2006 2223 2233 (Pubitemid 43345539)
22. K.G. Leong, K. Niessen, I. Kulic, A. Raouf, C. Eaves, and I. Pollet Jagged1-mediated Notch activation induces epithelial-to-mesenchymal transition through Slug-induced repression of E-cadherin J Exp Med 204 2007 2935 2948 (Pubitemid 350179562)
23. F. MacKenzie, P. Duriez, B. Larrivee, L. Chang, I. Pollet, and F. Wong Notch4-induced inhibition of endothelial sprouting requires the ankyrin repeats and involves signaling through RBP-Jkappa Blood 104 2004 1760 1768 (Pubitemid 39202285)
24. F. MacKenzie, P. Duriez, F. Wong, M. Noseda, and A. Karsan Notch4 inhibits endothelial apoptosis via RBP-Jkappa-dependent and -independent pathways J Biol Chem 279 2004 11657 11663 (Pubitemid 38401668)
25. O.G. Morali, V. Delmas, R. Moore, C. Jeanney, J.P. Thiery, and L. Larue IGF-II induces rapid beta-catenin relocation to the nucleus during epithelium to mesenchyme transition Oncogene 20 2001 4942 4950 (Pubitemid 32769784)
26. A. Moustakas, and C.H. Heldin Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression Cancer Sci 98 2007 1512 1520 (Pubitemid 47308444)
27. Y. Nefedova, P. Cheng, M. Alsina, W.S. Dalton, and D.I. Gabrilovich Involvement of Notch-1 signaling in bone marrow stroma-mediated de novo drug resistance of myeloma and other malignant lymphoid cell lines Blood 103 2004 3503 3510 (Pubitemid 38525684)
28. K. Niessen, Y. Fu, L. Chang, P.A. Hoodless, D. McFadden, and A. Karsan Slug is a direct Notch target required for initiation of cardiac cushion cellularization J Cell Biol 182 2008 315 325
29. K.C. Nyhan, N. Faherty, G. Murray, L.B. Cooey, C. Godson, and J.K. Crean Jagged/Notch signalling is required for a subset of TGFbeta1 responses in human kidney epithelial cells Biochim Biophys Acta 1803 2010 1386 1395
30. T.T. Onder, P.B. Gupta, S.A. Mani, J. Yang, E.S. Lander, and R.A. Weinberg Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways Cancer Res 68 2008 3645 3654
31. H. Peinado, D. Olmeda, and A. Cano Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 7 2007 415 428 (Pubitemid 46809165)
32. D.Y. Rhyu, Y. Yang, H. Ha, G.T. Lee, J.S. Song, and S.T. Uh Role of reactive oxygen species in TGF-beta1-induced mitogen-activated protein kinase activation and epithelial-mesenchymal transition in renal tubular epithelial cells J Am Soc Nephrol 16 2005 667 675 (Pubitemid 41725103)
33. C. Sahlgren, M.V. Gustafsson, S. Jin, L. Poellinger, and U. Lendahl Notch signaling mediates hypoxia-induced tumor cell migration and invasion Proc Natl Acad Sci U S A 105 2008 6392 6397 (Pubitemid 351758356)
34. R. Sanalkumar, S.B. Dhanesh, and J. James Non-canonical activation of Notch signaling/target genes in vertebrates Cell Mol Life Sci 67 2010 2957 2968
35. M.A. Santos, L.M. Sarmento, M. Rebelo, A.A. Doce, I. Maillard, and A. Dumortier Notch1 engagement by Delta-like-1 promotes differentiation of B lymphocytes to antibody-secreting cells Proc Natl Acad Sci U S A 104 2007 15454 15459 (Pubitemid 47502938)
36. M. Shih Ie, and T.L. Wang Notch signaling, gamma-secretase inhibitors, and cancer therapy Cancer Res 67 2007 1879 1882
37. T. Shirakihara, M. Saitoh, and K. Miyazono Differential regulation of epithelial and mesenchymal markers by deltaEF1 proteins in epithelial mesenchymal transition induced by TGF-beta Mol Biol Cell 18 2007 3533 3544 (Pubitemid 47378691)
38. M.A. Sulzer, M.P. Leers, J.A. van Noord, E.C. Bollen, and P.H. Theunissen Reduced E-cadherin expression is associated with increased lymph node metastasis and unfavorable prognosis in non-small cell lung cancer Am J Respir Crit Care Med 157 1998 1319 1323
39. J. Theys, B. Jutten, R. Habets, K. Paesmans, A.J. Groot, and P. Lambin E-Cadherin loss associated with EMT promotes radioresistance in human tumor cells Radiother Oncol 99 2011 392 397
40. J.P. Thiery Epithelial-mesenchymal transitions in tumour progression Nat Rev Cancer 2 2002 442 454
41. J.P. Thiery, and J.P. Sleeman Complex networks orchestrate epithelial-mesenchymal transitions Nat Rev Mol Cell Biol 7 2006 131 142 (Pubitemid 43278296)
42. L.A. Timmerman, J. Grego-Bessa, A. Raya, E. Bertran, J.M. Perez-Pomares, and J. Diez Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation Genes Dev 18 2004 99 115 (Pubitemid 38090691)
43. H. Uyttendaele, J. Ho, J. Rossant, and J. Kitajewski Vascular patterning defects associated with expression of activated Notch4 in embryonic endothelium Proc Natl Acad Sci U S A 98 2001 5643 5648 (Pubitemid 32435695)
44. H. Uyttendaele, G. Marazzi, G. Wu, Q. Yan, D. Sassoon, and J. Kitajewski Notch4/int-3, a mammary proto-oncogene, is an endothelial cell-specific mammalian Notch gene Development 122 1996 2251 2259 (Pubitemid 26235824)
45. D.M. Vallejo, E. Caparros, and M. Dominguez Targeting Notch signalling by the conserved miR-8/200 microRNA family in development and cancer cells EMBO J 30 2011 756 769
46. J. Xu, S. Lamouille, and R. Derynck TGF-beta-induced epithelial to mesenchymal transition Cell Res 19 2009 156 172
47. J. Zavadil, L. Cermak, N. Soto-Nieves, and E.P. Bottinger Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition EMBO J 23 2004 1155 1165 (Pubitemid 38436879)
48. G. Zhou, L.A. Dada, M. Wu, A. Kelly, H. Trejo, and Q. Zhou Hypoxia-induced alveolar epithelial-mesenchymal transition requires mitochondrial ROS and hypoxia-inducible factor 1 Am J Physiol Lung Cell Mol Physiol 297 2009 L1120 L1130