Role of Notch signaling in the mammalian heart

Brazilian Journal of Medical and Biological Research

Volumn 47, Issue 1, 2014, Pages 1-10

  Zhou, X L ^a   Liu, J C ^a  

^a NANCHANG UNIVERSITY   (China)

Author keywords

Angiogenesis; Cardiac fibroblast myofibroblast transformation; Cardioprotection; Congenital heart disease; Myocardial regeneration; Notch signaling

Indexed keywords

CYCLIN D1; GAMMA SECRETASE INHIBITOR; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; JAGGED1; NOTCH RECEPTOR; TRANSCRIPTION FACTOR HES 1; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ATRIOVENTRICULAR CONDUCTION; CONGENITAL HEART DISEASE; GENE MUTATION; HEART MUSCLE INJURY; HEART PROTECTION; HUMAN; REVIEW; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY; ANIMAL; APOPTOSIS; CELL DIFFERENTIATION; HEART DISEASE; HEART INFARCTION PREVENTION; HEART MUSCLE; MAMMAL; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; REGENERATION;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; HEART DISEASES; HUMANS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MAMMALS; MYOCARDIUM; RECEPTORS, NOTCH; REGENERATION; SIGNAL TRANSDUCTION;

EID: 84893013442     PISSN: 0100879X     EISSN: 1414431X     Source Type: Journal    
DOI: 10.1590/1414-431X20133177     Document Type: Review

References (60)

1. Borggrefe T, Oswald F. The Notch signaling pathway: Transcriptional regulation at Notch target genes. Cell Mol Life Sci 2009; 66: 1631-1646, doi: 10.1007/s00018-009-8668-7.
2. Tien AC, Rajan A, Bellen HJ. A Notch updated. J Cell Biol 2009; 184: 621-629, doi: 10.1083/jcb.200811141.
3. Schwanbeck R, Martini S, Bernoth K, Just U. The Notch signaling pathway: Molecular basis of cell context dependency. Eur J Cell Biol 2011; 90: 572-581, doi: 10.1016/j.ejcb.2010.10.004.
4. Penton AL, Leonard LD, Spinner NB. Notch signaling in human development and disease. Semin Cell Dev Biol 2012; 23: 450-457, doi: 10.1016/j.semcdb.2012.01.010.
5. de la Pompa JL, Epstein JA. Coordinating tissue interactions: Notch signaling in cardiac development and disease. Dev Cell 2012; 22: 244-254, doi: 10.1016/j.devcel.2012.01.014.
6. Boni A, Urbanek K, Nascimbene A, Hosoda T, Zheng H, Delucchi F, et al. Notch1 regulates the fate of cardiac progenitor cells. Proc Natl Acad Sci U S A 2008; 105: 15529-15534, doi: 10.1073/pnas.0808357105.
7. Gude N, Sussman M. Notch signaling and cardiac repair. J Mol Cell Cardiol 2012; 52: 1226-1232, doi: 10.1016/j.yjmcc.2012.03.007.
8. Fan YH, Dong H, Pan Q, Cao YJ, Li H, Wang HC. Notch signaling may negatively regulate neonatal rat cardiac fibroblast-myofibroblast transformation. Physiol Res 2011; 60: 739-748.
9. Kume T. Ligand-dependent Notch signaling in vascular formation. Adv Exp Med Biol 2012; 727: 210-222, doi: 10.1007/978-1-4614-0899-4_16.
10. Wang MM. Notch signaling and Notch signaling modifiers. Int J Biochem Cell Biol 2011; 43: 1550-1562, doi: 10.1016/j.biocel.2011.08.005.
11. D'Souza B, Miyamoto A, Weinmaster G. The many facets of Notch ligands. Oncogene 2008; 27: 5148-5167, doi: 10.1038/onc.2008.229.
12. Molle V, Campagna S, Bessin Y, Ebran N, Saint N, Molle G. First evidence of the pore-forming properties of a keratin from skin mucus of rainbow trout (Oncorhynchus mykiss, formerly Salmo gairdneri). Biochem J 2008; 411: 33-40, doi: 10.1042/BJ20070801.
13. Miazga CM, McLaughlin KA. Coordinating the timing of cardiac precursor development during gastrulation: A new role for Notch signaling. Dev Biol 2009; 333: 285-296, doi: 10.1016/j.ydbio.2009.06.040.
14. de la Pompa JL. Notch signaling in cardiac development and disease. Pediatr Cardiol 2009; 30: 643-650, doi: 10.1007/s00246-008-9368-z.
15. Rutenberg JB, Fischer A, Jia H, Gessler M, Zhong TP, Mercola M. Developmental patterning of the cardiac atrioventricular canal by Notch and Hairy-related transcription factors. Development 2006; 133: 4381-4390, doi: 10.1242/dev.02607.
16. Fischer A, Steidl C, Wagner TU, Lang E, Jakob PM, Friedl P, et al. Combined loss of Hey1 and HeyL causes congenital heart defects because of impaired epithelial to mesenchymal transition. Circ Res 2007; 100: 856-863, doi: 10.1161/01.RES.0000260913.95642.3b.
17. Niessen K, Fu Y, Chang L, Hoodless PA, McFadden D, Karsan A. Slug is a direct Notch target required for initiation of cardiac cushion cellularization. J Cell Biol 2008; 182: 315-325, doi: 10.1083/jcb.200710067.
18. Noseda M, McLean G, Niessen K, Chang L, Pollet I, Montpetit R, et al. Notch activation results in phenotypic and functional changes consistent with endothelial-tomesenchymal transformation. Circ Res 2004; 94: 910-917, doi: 10.1161/01.RES.0000124300.76171.C9.
19. Chang AC, Fu Y, Garside VC, Niessen K, Chang L, Fuller M, et al. Notch initiates the endothelial-to-mesenchymal transition in the atrioventricular canal through autocrine activation of soluble guanylyl cyclase. Dev Cell 2011; 21: 288-300, doi: 10.1016/j.devcel.2011.06.022.
20. Grego-Bessa J, Luna-Zurita L, del Monte G, Bolos V, Melgar P, Arandilla A, et al. Notch signaling is essential for ventricular chamber development. Dev Cell 2007; 12: 415-429, doi: 10.1016/j.devcel.2006.12.011.
21. Manderfield LJ, High FA, Engleka KA, Liu F, Li L, Rentschler S, et al. Notch activation of Jagged1 contributes to the assembly of the arterial wall. Circulation 2012; 125: 314-323, doi: 10.1161/CIRCULATIONAHA.111.047159.
22. High FA, Zhang M, Proweller A, Tu L, Parmacek MS, Pear WS, et al. An essential role for Notch in neural crest during cardiovascular development and smooth muscle differentiation. J Clin Invest 2007; 117: 353-363, doi: 10.1172/JCI 30070.
23. del Monte G, Casanova JC, Guadix JA, MacGrogan D, Burch JB, Perez-Pomares JM, et al. Differential Notch signaling in the epicardium is required for cardiac inflow development and coronary vessel morphogenesis. Circ Res 2011; 108: 824-836, doi: 10.1161/CIRCRESAHA.110.229062.
24. Grieskamp T, Rudat C, Ludtke TH, Norden J, Kispert A. Notch signaling regulates smooth muscle differentiation of epicardium-derived cells. Circ Res 2011; 108: 813-823, doi: 10.1161/CIRCRESAHA.110.228809.
25. Rentschler S, Harris BS, Kuznekoff L, Jain R, Manderfield L, Lu MM, et al. Notch signaling regulates murine atrioventricular conduction and the formation of accessory pathways. J Clin Invest 2011; 121: 525-533, doi: 10.1172/JCI 44470.
26. Sciacca S, Pilato M, Mazzoccoli G, Pazienza V, Vinciguerra M. Anti-correlation between longevity gene SirT1 and Notch signaling in ascending aorta biopsies from patients with bicuspid aortic valve disease. Heart Vessels 2013; 28: 268-275, doi: 10.1007/s00380-012-0238-5.
27. Garg V, Muth AN, Ransom JF, Schluterman MK, Barnes R, King IN, et al. Mutations in Notch1 cause aortic valve disease. Nature 2005; 437: 270-274, doi: 10.1038/nature 03940.
28. Acharya A, Hans CP, Koenig SN, Nichols HA, Galindo CL, Garner HR, et al. Inhibitory role of Notch1 in calcific aortic valve disease. PloS One 2011; 6: e27743, doi: 10.1371/journal.pone.0027743.
29. Li Z, Feng L, Wang CM, Zheng QJ, Zhao BJ, Yi W, et al. Deletion of rbp-j in adult mice leads to the onset of aortic valve degenerative diseases. Mol Biol Rep 2012; 39: 3837-3845, doi: 10.1007/s11033-011-1162-y.
30. Kamath BM, Bauer RC, Loomes KM, Chao G, Gerfen J, Hutchinson A, et al. Notch2 mutations in Alagille syndrome. J Med Genet 2012; 49: 138-144, doi: 10.1136/jmedgenet-2011-100544.
31. Riley MF, McBride KL, Cole SE. Notch1 missense alleles associated with left ventricular outflow tract defects exhibit impaired receptor processing and defective emt. Biochim Biophys Acta 2011; 1812: 121-129, doi: 10.1016/j.bbadis.2010.10.002.
32. Fre S, Huyghe M, Mourikis P, Robine S, Louvard D, Artavanis-Tsakonas S. Notch signals control the fate of immature progenitor cells in the intestine. Nature 2005; 435: 964-968, doi: 10.1038/nature03589.
33. Koyanagi M, Bushoven P, Iwasaki M, Urbich C, Zeiher AM, Dimmeler S. Notch signaling contributes to the expression of cardiac markers in human circulating progenitor cells. Circ Res 2007; 101: 1139-1145, doi: 10.1161/CIRCRESAHA.107.151381.
34. Sassoli C, Pini A, Mazzanti B, Quercioli F, Nistri S, Saccardi R, et al. Mesenchymal stromal cells affect cardiomyocyte growth through juxtacrine Notch-1/Jagged-1 signaling and paracrine mechanisms: Clues for cardiac regeneration. J Mol Cell Cardiol 2011; 51: 399-408, doi: 10.1016/j.yjmcc.2011.06.004.
35. Urbanek K, Cabral-da-Silva MC, Ide-Iwata N, Maestroni S, Delucchi F, Zheng H, et al. Inhibition of Notch1-dependent cardiomyogenesis leads to a dilated myopathy in the neonatal heart. Circ Res 2010; 107: 429-441, doi: 10.1161/CIRCRESAHA.110.218487.
36. Collesi C, Zentilin L, Sinagra G, Giacca M. Notch1 signaling stimulates proliferation of immature cardiomyocytes. J Cell Biol 2008; 183: 117-128, doi: 10.1083/jcb.200806091.
37. Campa VM, Gutierrez-Lanza R, Cerignoli F, Diaz-Trelles R, Nelson B, Tsuji T, et al. Notch activates cell cycle reentry and progression in quiescent cardiomyocytes. J Cell Biol 2008; 183: 129-141, doi: 10.1083/jcb.200806104.
38. Croquelois A, Domenighetti AA, Nemir M, Lepore M, Rosenblatt-Velin N, Radtke F, et al. Control of the adaptive response of the heart to stress via the Notch1 receptor pathway. J Exp Med 2008; 205: 3173-3185, doi: 10.1084/jem.20081427.
39. Russell JL, Goetsch SC, Gaiano NR, Hill JA, Olson EN, Schneider JW. A dynamic Notch injury response activates epicardium and contributes to fibrosis repair. Circ Res 2011; 108: 51-59, doi: 10.1161/CIRCRESAHA.110.233262.
40. Ge W, Ren J. mTOR-STAT3-Notch signalling contributes to ALDH2-induced protection against cardiac contractile dysfunction and autophagy under alcoholism. J Cell Mol Med 2012; 16: 616-626, doi: 10.1111/j.1582-4934.2011.01347.x.
41. Lee JH, Suk J, Park J, Kim SB, Kwak SS, Kim JW, et al. Notch signal activates hypoxia pathway through hes1-dependent src/signal transducers and activators of transcription 3 pathway. Mol Cancer Res 2009; 7: 1663-1671, doi: 10.1158/1541-7786.MCR-09-0191.
42. Chen J, Imanaka N, Griffin JD. Hypoxia potentiates Notch signaling in breast cancer leading to decreased e-cadherin expression and increased cell migration and invasion. Br J Cancer 2010; 102: 351-360, doi: 10.1038/sj.bjc.6605486.
43. Qiang L, Wu T, Zhang HW, Lu N, Hu R, Wang YJ, et al. Hif-1alpha is critical for hypoxia-mediated maintenance of glioblastoma stem cells by activating Notch signaling pathway. Cell Death Differ 2012; 19: 284-294, doi: 10.1038/cdd.2011.95.
44. Yu HC, Qin HY, He F, Wang L, Fu W, Liu D, et al. Canonical Notch pathway protects hepatocytes from ischemia/reperfusion injury in mice by repressing reactive oxygen species production through jak2/stat3 signaling. Hepatology 2011; 54: 979-988, doi: 10.1002/hep.24469.
45. Gude NA, Emmanuel G, Wu W, Cottage CT, Fischer K, Quijada P, et al. Activation of Notch-mediated protective signaling in the myocardium. Circ Res 2008; 102: 1025-1035, doi: 10.1161/CIRCRESAHA.107.164749.
46. Oie E, Sandberg WJ, Ahmed MS, Yndestad A, Laerum OD, Attramadal H, et al. Activation of Notch signaling in cardiomyocytes during post-infarction remodeling. Scand Cardiovasc J 2010; 44: 359-366, doi: 10.3109/14017431.2010.511256.
47. Li Y, Hiroi Y, Ngoy S, Okamoto R, Noma K, Wang CY, et al. Notch1 in bone marrow-derived cells mediates cardiac repair after myocardial infarction. Circulation 2011; 123: 866-876, doi: 10.1161/CIRCULATIONAHA.110.947531.
48. Bridges E, Oon CE, Harris A. Notch regulation of tumor angiogenesis. Future Oncol 2011; 7: 569-588, doi: 10.2217/fon.11.20.
49. Li Y, Takeshita K, Liu PY, Satoh M, Oyama N, Mukai Y, et al. Smooth muscle Notch1 mediates neointimal formation after vascular injury. Circulation 2009; 119: 2686-2692, doi: 10.1161/CIRCULATIONAHA.108.790485.
50. Al Haj Zen A, Oikawa A, Bazan-Peregrino M, Meloni M, Emanueli C, Madeddu P. Inhibition of delta-like-4-mediated signaling impairs reparative angiogenesis after ischemia. Circ Res 2010; 107: 283-293, doi: 10.1161/CIRCRESAHA.110.221663.
51. Harrington LS, Sainson RC, Williams CK, Taylor JM, ShiW, Li JL, et al. Regulation of multiple angiogenic pathways by DII4 and Notch in human umbilical vein endothelial cells. Microvasc Res 2008; 75: 144-154, doi: 10.1016/j.mvr.2007.06.006.
52. Benedito R, Roca C, Sorensen I, Adams S, Gossler A, Fruttiger M, et al. The Notch ligands DII4 and Jagged1 have opposing effects on angiogenesis. Cell 2009; 137: 1124-1135, doi: 10.1016/j.cell.2009.03.025.
53. Cao L, Arany PR, Wang YS, Mooney DJ. Promoting angiogenesis via manipulation of vegf responsiveness with Notch signaling. Biomaterials 2009; 30: 4085-4093, doi: 10.1016/j.biomaterials.2009.04.051.
54. Cao L, Arany PR, Kim J, Rivera-Feliciano J, Wang YS, He Z, et al. Modulating Notch signaling to enhance neovascularization and reperfusion in diabetic mice. Biomaterials 2010; 31: 9048-9056, doi: 10.1016/j.biomaterials.2010.08.002.
55. Takeshita K, Satoh M, Ii M, Silver M, Limbourg FP, Mukai Y, et al. Critical role of endothelial Notch1 signaling in postnatal angiogenesis. Circ Res 2007; 100: 70-78, doi: 10.1161/01.RES.0000254788.47304.6e.
56. Aoyagi-Ikeda K, Maeno T, Matsui H, Ueno M, Hara K, Aoki Y, et al. Notch induces myofibroblast differentiation of alveolar epithelial cells via transforming growth factor-{beta}-smad3 pathway. Am J Respir Cell Mol Biol 2011; 45: 136-144.
57. Dees C, Zerr P, Tomcik M, Beyer C, Horn A, Akhmetshina A, et al. Inhibition of Notch signaling prevents experimental fibrosis and induces regression of established fibrosis. Arthritis Rheum 2011; 63: 1396-1404, doi: 10.1002/art.30254.
58. Chen Y, Zheng S, Qi D, Zheng S, Guo J, Zhang S, et al. Inhibition of Notch signaling by a gamma-secretase inhibitor attenuates hepatic fibrosis in rats. PloS One 2012; 7: e46512, doi: 10.1371/journal.pone.0046512.
59. Bielesz B, Sirin Y, Si H, Niranjan T, Gruenwald A, Ahn S, et al. Epithelial Notch signaling regulates interstitial fibrosis development in the kidneys of mice and humans. J Clin Invest 2010; 120: 4040-4054, doi: 10.1172/JCI43025.
60. Liu T, Hu B, Choi YY, Chung M, Ullenbruch M, Yu H, et al. Notch1 signaling in FIZZ1 induction of myofibroblast differentiation. Am J Pathol 2009; 174: 1745-1755, doi: 10.2353/ajpath.2009.080618.