Sequential Notch activation regulates ventricular chamber development

Nature Cell Biology

Volumn 18, Issue 1, 2016, Pages 7-20

  D'Amato, Gaetano ^a   Luxán, Guillermo ^a   Del Monte Nieto, Gonzalo ^a   Martínez Poveda, Beatriz ^a   Torroja, Carlos ^a   Walter, Wencke ^a   Bochter, Matthew S ^b   Benedito, Rui ^a   Cole, Susan ^b   Martinez, Fernando ^a   Hadjantonakis, Anna Katerina ^c   Uemura, Akiyoshi ^d   Jiménez Borreguero, Luis J ^a,e   De La Pompa, José Luis ^a  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^b OHIO STATE UNIVERSITY   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d NAGOYA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

^e Instituto de Investigación Sanitaria del Hospital Universitario de La Princesa   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSYLTRANSFERASE; GLYCOSYLTRANSFERASE MANIC FRINGE; JAGGED1; JAGGED2; MEMBRANE PROTEIN; NOTCH RECEPTOR; NOTCH1 RECEPTOR; UNCLASSIFIED DRUG; CALCIUM BINDING PROTEIN; DLL4 PROTEIN, HUMAN; LIGAND; MFNG PROTEIN, HUMAN; NOTCH1 PROTEIN, HUMAN; SIGNAL PEPTIDE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORONARY BLOOD VESSEL; DOWN REGULATION; EMBRYO; ENDOCARDIUM; HEART DEVELOPMENT; HEART MUSCLE; HEART VENTRICLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRABECULAR MESHWORK; CELL CULTURE; EMBRYOLOGY; HUMAN; METABOLISM; ORGANOGENESIS; PHYSIOLOGY;

CALCIUM-BINDING PROTEINS; CELLS, CULTURED; HEART VENTRICLES; HEXOSYLTRANSFERASES; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGANDS; MEMBRANE PROTEINS; ORGANOGENESIS; RECEPTOR, NOTCH1; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84951316975     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3280     Document Type: Article

References (70)

1. Sedmera, D., Pexieder, T., Vuillemin, M., Thompson, R. P., Anderson, R. H. Developmental patterning of the myocardium. Anat. Rec. 258, 319-337 (2000).
2. Moorman, A. F., Christoffels, V. M. Cardiac chamber formation: development, genes, and evolution. Physiol. Rev. 83, 1223-1267 (2003).
3. Tevosian, S. G. et al. FOG-2, a cofactor for GATA transcription factors, is essential for heart morphogenesis and development of coronary vessels from epicardium. Cell 101, 729-739 (2000).
4. Wu, B. et al. Endocardial cells form the coronary arteries by angiogenesis through myocardial-endocardial VEGF signaling. Cell 151, 1083-1096 (2012).
5. Wessels, A., Sedmera, D. Developmental anatomy of the heart: a tale of mice and man. Physiol. Genomics 15, 165-176 (2003).
6. Ritter, M. et al. Isolated noncompaction of the myocardium in adults. Mayo Clin. Proc. 72, 26-31 (1997).
7. Towbin, J. A. Left ventricular noncompaction: a new form of heart failure. Heart Fail. Clin. 6, 453-469 (2010).
8. Maron, B. J. et al. Contemporary definitions and classification of the cardiomyopathies: an American Heart Association Scientific Statement from the Council on Clinical Cardiology, Heart Failure and Transplantation Committee; Quality of Care and Outcomes Research and Functional Genomics and Translational Biology Interdisciplinary Working Groups; and Council on Epidemiology and Prevention. Circulation 113, 1807-1816 (2006).
9. Captur, G., Nihoyannopoulos, P. Left ventricular non-compaction: genetic heterogeneity, diagnosis and clinical course. Int. J. Cardiol. 140, 145-153 (2010).
10. Sarma, R. J., Chana, A., Elkayam, U. Left ventricular noncompaction. Prog. Cardiovasc. Dis. 52, 264-273 (2010).
11. Arbustini, E., Weidemann, F., Hall, J. L. Left ventricular noncompaction: a distinct cardiomyopathy or a trait shared by different cardiac diseases J. Am. Coll. Cardiol. 64, 1840-1850 (2014).
12. Grego-Bessa, J. et al. Notch signaling is essential for ventricular chamber development. Dev. Cell 12, 415-429 (2007).
13. Itoh, M. et al. Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev. Cell 4, 67-82 (2003).
14. Kopan, R., Ilagan, M. X. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137, 216-233 (2009).
15. Luxan, G. et al. Mutations in the NOTCH pathway regulator MIB1 cause left ventricular noncompaction cardiomyopathy. Nat. Med. 19, 193-201 (2013).
16. Nowotschin, S., Xenopoulos, P., Schrode, N., Hadjantonakis, A. K. A bright singlecell resolution live imaging reporter of Notch signaling in the mouse. BMC Dev. Biol. 13, http://dx.doi.org/10.1186/1471-213X-13-15 (2013).
17. Koch, U. et al. Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J. Exp. Med. 205, 2515-2523 (2008).
18. Kisanuki, Y. Y. et al. Tie2-Cre transgenic mice: a new model for endothelial celllineage analysis in vivo. Dev. Biol. 230, 230-242 (2001).
19. Wang, Y. et al. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465, 483-486 (2010).
20. Bjarnadottir, T. K., Fredriksson, R., Schioth, H. B. The adhesion GPCRs: a unique family of G protein-coupled receptors with important roles in both central and peripheral tissues. Cell Mol. Life Sci. 64, 2104-2119 (2007).
21. Waller-Evans, H. et al. The orphan adhesion-GPCR GPR126 is required for embryonic development in the mouse. PLoS ONE 5, e14047 (2010).
22. Patra, C. et al. Organ-specific function of adhesion G protein-coupled receptor GPR126 is domain-dependent. Proc. Natl Acad. Sci. USA 110, 16898-16903 (2013).
23. Munch, J., Gonzalez-Rajal, A., de la Pompa, J. L. Notch regulates blastema proliferation and prevents differentiation during adult zebrafish fin regeneration. Development 140, 1402-1411 (2013).
24. Jiao, K. et al. An essential role of Bmp4 in the atrioventricular septation of the mouse heart. Genes Dev. 17, 2362-2367 (2003).
25. Captur, G. et al. Abnormal cardiac formation in hypertrophic cardiomyopathy: fractal analysis of trabeculae and preclinical gene expression. Circ. Cardiovasc. Genet. 7, 241-248 (2014).
26. Ivins, S. et al. The CXCL12/CXCR4 axis plays a critical role in coronary artery development. Dev. Cell 33, 455-468 (2015).
27. Cavallero, S. et al. CXCL12 signaling is essential for maturation of the ventricular coronary endothelial plexus and establishment of functional coronary circulation. Dev. Cell 33, 469-477 (2015).
28. Tian, X., Pu, W. T., Zhou, B. Cellular origin and developmental program of coronary angiogenesis. Circ. Res. 116, 515-530 (2015).
29. Panin, V. M., Papayannopoulos, V., Wilson, R., Irvine, K. D. Fringe modulates Notchligand interactions. Nature 387, 908-912 (1997).
30. Yang, L. T. et al. Fringe glycosyltransferases differentially modulate Notch1 proteolysis induced by Delta1 and Jagged1. Mol. Biol. Cell 16, 927-942 (2005).
31. Benedito, R. et al. The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 137, 1124-1135 (2009).
32. McKenzie, G. J. et al. Nuclear Ca2C and CaM kinase IV specify hormonal-and Notchresponsiveness. J. Neurochem. 93, 171-185 (2005).
33. Timmerman, L. A. et al. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev. 18, 99-115 (2004).
34. Moran, J. L. et al. Manic fringe is not required for embryonic development, and fringe family members do not exhibit redundant functions in the axial skeleton, limb, or hindbrain. Dev. Dynam. 238, 1803-1812 (2009).
35. Luna-Zurita, L. et al. Integration of a Notch-dependent mesenchymal gene program and Bmp2-driven cell invasiveness regulates murine cardiac valve formation. J. Clin. Invest. 120, 3493-3507 (2010).
36. Fischer, A., Schumacher, N., Maier, M., Sendtner, M., Gessler, M. The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev. 18, 901-911 (2004).
37. Watanabe, T., Koibuchi, N., Chin, M. T. Transcription factor CHF1/Hey2 regulates coronary vascular maturation. Mech. Dev. 127, 418-427 (2010).
38. Leask, A. Getting to the heart of the matter: new insights into cardiac fibrosis. Circ. Res. 116, 1269-1276 (2015).
39. Hinz, B. The extracellular matrix and transforming growth factor-1: tale of a strained relationship. Matrix Biol. 47, 54-65 (2015).
40. Epstein, J. A., Aghajanian, H., Singh, M. K. Semaphorin signaling in cardiovascular development. Cell Metab. 21, 163-173 (2015).
41. Toyofuku, T. et al. Guidance of myocardial patterning in cardiac development by Sema6D reverse signalling. Nat. Cell Biol. 6, 1204-1211 (2004).
42. Dirkx, E. et al. Nfat and miR-25 cooperate to reactivate the transcription factor Hand2 in heart failure. Nat. Cell Biol. 15, 1282-1293 (2013).
43. Hertig, C. M., Kubalak, S. W., Wang, Y., Chien, K. R. Synergistic roles of neuregulin-1 and insulin-like growth factor-I in activation of the phosphatidylinositol 3-kinase pathway and cardiac chamber morphogenesis. J. Biol. Chem. 274, 37362-37369 (1999).
44. Kelly, R. G., Buckingham, M. E., Moorman, A. F. Heart fields and cardiac morphogenesis. Cold Spring Harb. Perspect. Med. 4, a015750 (2014).
45. Conlon, R. A., Reaume, A. G., Rossant, J. Notch1 is required for the coordinate segmentation of somites. Development 121, 1533-1545 (1995).
46. Oka, C. et al. Disruption of the mouse RBP-J kappa gene results in early embryonic death. Development 121, 3291-3301 (1995).
47. Mancini, S. J. et al. Jagged1-dependent Notch signaling is dispensable for hematopoietic stem cell self-renewal and differentiation. Blood 105, 2340-2342 (2005).
48. Xu, J., Krebs, L. T., Gridley, T. Generation of mice with a conditional null allele of the Jagged2 gene. Genesis 48, 390-393 (2010).
49. Radtke, F. et al. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 10, 547-558 (1999).
50. Koo, B. K. et al. An obligatory role of mind bomb-1 in notch signaling of mammalian development. PLoS ONE 2, e1221 (2007).
51. Zhang, C., Li, Q., Lim, C. H., Qiu, X., Jiang, Y. J. The characterization of zebrafish antimorphic mib alleles reveals that Mib and Mind bomb-2 (Mib2) function redundantly. Dev. Biol. 305, 14-27 (2007).
52. de la Pompa, J. L. et al. Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 124, 1139-1148 (1997).
53. Kanzler, B., Kuschert, S. J., Liu, Y. H., Mallo, M. Hoxa-2 restricts the chondrogenic domain and inhibits bone formation during development of the branchial area. Development 125, 2587-2597 (1998).
54. Del Monte, G., Grego-Bessa, J., Gonzalez-Rajal, A., Bolos, V., de la Pompa, J. L. Monitoring Notch1 activity in development: evidence for a feedback regulatory loop. Dev. Dynam. 236, 2594-2614 (2007).
55. Del Monte, G. et al. Differential notch signaling in the epicardium is required for cardiac inflow development and coronary vessel morphogenesis. Circ. Res. 108, 824-836 (2011).
56. Yang, J. et al. Inhibition of Notch2 by Numb/Numblike controls myocardial compaction in the heart. Cardiovasc. Res. 96, 276-285 (2012).
57. Chen, H. et al. Analysis of ventricular hypertrabeculation and noncompaction using genetically engineered mouse models. Pediatr. Cardiol. 30, 626-634 (2009).
58. Soufan, A. T. et al. Regionalized sequence of myocardial cell growth and proliferation characterizes early chamber formation. Circ. Res. 99, 545-552 (2006).
59. de Boer, B. A. et al. The interactive presentation of 3D information obtained from reconstructed datasets and 3D placement of single histological sections with the 3D portable document format. Development 138, 159-167 (2011).
60. Esteban, V. et al. Regulator of calcineurin 1 mediates pathological vascular wall remodeling. J. Exp. Med. 208, 2125-2139 (2011).
61. Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMB J. 17, 10-12 (2011).
62. Li, B., Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 12, http://dx.doi.org/10.1186/1471-2105-12-323 (2011).
63. Robinson, M. D., McCarthy, D. J., Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).
64. Johnson, W. E., Li, C., Rabinovic, A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8, 118-127 (2007).
65. Huang da, W., Sherman, B. T., Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
66. Sturn, A., Quackenbush, J., Trajanoski, Z. Genesis: cluster analysis of microarray data. Bioinformatics 18, 207-208 (2002).
67. Walter, W., Sanchez-Cabo, F., Ricote, M. GOplot: an R package for visually combining expression data with functional analysis. Bioinformatics 31, 2912-2914 (2015).
68. Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639-1645 (2009).
69. Cruz-Adalia, A. et al. CD69 limits the severity of cardiomyopathy after autoimmune myocarditis. Circulation 122, 1396-1404 (2010).
70. van de Weijer, T. et al. Geometrical models for cardiac MRI in rodents: comparison of quantification of left ventricular volumes and function by various geometrical models with a full-volume MRI data set in rodents. Am. J. Physiol. Heart Circ. Physiol. 302, H709-H715 (2012).