Combined loss of Hey1 and HeyL causes congenital heart defects because of impaired epithelial to mesenchymal transition

Circulation Research

Volumn 100, Issue 6, 2007, Pages 856-863

  Fischer, Andreas ^a   Steidl, Christian ^a   Wagner, Toni U ^a   Lang, Esra ^a   Jakob, Peter M ^a   Friedl, Peter ^a,b   Knobeloch, Klaus Peter ^c   Gessler, Manfred ^a,b,d  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^d UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Epithelial to mesenchymal transition; Hey1; Hey2; HeyL; Notch

Indexed keywords

GELATINASE A; JAGGED1; NOTCH RECEPTOR; NOTCH1 RECEPTOR; NOTCH2 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATRIOVENTRICULAR CANAL; CELL DENSITY; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; DISEASE SEVERITY; EMBRYO; ENDOCARDIUM; EPITHELIUM; GENE EXPRESSION; HEART FAILURE; HEART VENTRICLE SEPTUM DEFECT; LETHALITY; MESENCHYME; MESENCHYME CELL; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY VALVE DISEASE; TRICUSPID VALVE DISEASE;

EID: 34147096361     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000260913.95642.3b     Document Type: Article

References (44)

1. Hoffman JI, Kaplan S. The incidence of congenital heart disease. J Am Coll Cardiol. 2002;39:1890-1900.
2. Garg V, Muth AN, Ransom JF, Schluterman MK, Barnes R, King IN, Grossfeld PD, Srivastava D. Mutations in NOTCH1 cause aortic valve disease. Nature. 2005;437:270-274.
3. Li L, Krantz ID, Deng Y, Genin A, Banta AB, Collins CC, Qi M, Trask BJ, Kuo WL, Cochran J, Costa T, Pierpont ME, Rand EB, Piccoli DA, Hood L, Spinner NB. Alagille syndrome is caused by mutations in human Jagged1, which encodes a ligand for Notch1. Nat Genet. 1997;16:243-251.
4. Oda T, Elkahloun AG, Pike BL, Okajima K, Krantz ID, Genin A, Piccoli DA, Meltzer PS, Spinner NB, Collins FS, Chandrasekharappa SC. Mutations in the human Jagged1 gene are responsible for Alagille syndrome. Nat Genet. 1997;16:235-242.
5. Eldadah ZA, Hamosh A, Biery NJ, Montgomery RA, Duke M, Elkins R, Dietz HC. Familial Tetralogy of Fallot caused by mutation in the jagged1 gene. Hum Mol Genet. 2001;10:163-169.
6. Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science. 1999;284:770-776.
7. Gridley T Notch signaling and inherited disease syndromes. Hum Mol Genet. 2003;12 Spec No 1:R9-R13.
8. Hansson EM, Lendahl U, Chapman G. Notch signaling in development and disease. Semin Cancer Biol. 2004;14:320-328.
9. Fischer A, Gessler M. Hey genes in cardiovascular development. Trends Cardiovasc Med. 2003;13:221-226.
10. Gessler M, Knobeloch KP, Helisch A, Amann K, Schumacher N, Rohde E, Fischer A, Leimeister C. Mouse gridlock: no aortic coarctation or deficiency, but fatal cardiac defects in Hey2 -/- mice. Curr Biol. 2002;12:1601-1604.
11. Donovan J, Kordylewska A, Jan YN, Utset MF. Tetralogy of fallot and other congenital heart defects in Hey2 mutant mice. Curr Biol. 2002;12:1605-1610.
12. Sakata Y, Kamei CN, Nakagami H, Bronson R, Liao JK, Chin MT. Ventricular septal defect and cardiomyopathy in mice lacking the transcription factor CHF1/Hey2. Proc Natl Acad Sci U S A. 2002;99:16197-16202.
13. Kokubo H, Miyagawa-Tomita S, Tomimatsu H, Nakashima Y, Nakazawa M, Saga Y, Johnson RL. Targeted disruption of hesr2 results in atrioventricular valve anomalies that lead to heart dysfunction. Circ Res. 2004;95:540-547.
14. 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. 2004;18:901-911.
15. Maier MM, Gessler M. Comparative analysis of the human and mouse Hey1 promoter: Hey genes are new Notch target genes. Biochem Biophys Res Commun. 2000;275:652-660.
16. Lin MH, Leimeister C, Gessler M, Kopan R. Activation of the Notch pathway in the hair cortex leads to aberrant differentiation of the adjacent hair-shaft layers. Development. 2000;127:2421-2432.
17. Leimeister C, Schumacher N, Steidl C, Gessler M. Analysis of HeyL expression in wild-type and Notch pathway mutant mouse embryos. Mech Dev. 2000;98:175-178.
18. Leimeister C, Schumacher N, Gessler M. Expression of Notch pathway genes in the embryonic mouse metanephros suggests a role in proximal tubule development. Gene Expr Patterns. 2003;3:595-598.
19. Nakagawa O, McFadden DG, Nakagawa M, Yanagisawa H, Hu T, Srivastava D, Olson EN. Members of the HRT family of basic helix-loop-helix proteins act as transcriptional repressors downstream of Notch signaling. Proc Natl Acad Sci U S A. 2000;97:13655-13660.
20. Steidl C, Leimeister C, Klamt B, Maier M, Nanda I, Dixon M, Clarke R, Schmid M, Gessler M. Characterization of the human and mouse HEY1, HEY2, and HEYL genes: cloning, mapping, and mutation screening of a new bHLH gene family. Genomics. 2000;66:195-203.
21. Radtke F, Wilson A, Stark G, Bauer M, van Meerwijk J, MacDonald HR, Aguet M. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity. 1999;10:547-558.
22. Leimeister C, Bach A, Gessler M. Developmental expression patterns of mouse sFRP genes encoding members of the secreted frizzled related protein family. Mech Dev. 1998;75:29-42.
23. Runyan RB, Markwald RR. Invasion of mesenchyme into threedimensional collagen gels: a regional and temporal analysis of interaction in embryonic heart tissue. Dev Biol. 1983;95:108-114.
24. Potts JD, Dagle JM, Walder JA, Weeks DL, Runyan RB. Epithelial- mesenchymal transformation of embryonic cardiac endothelial cells is inhibited by a modified antisense oligodeoxynucleotide to transforming growth factor beta 3. Proc Natl Acad Sci U S A. 1991;88:1516-1520.
25. Fischer A, Klattig J, Kneitz B, Diez H, Maier M, Holtmann B, Englert C, Gessler M. Hey Basic Helix-Loop-Helix Transcription Factors Are Repressors of GATA4 and GATA6 and Restrict Expression of the GATA Target Gene ANF in Fetal Hearts. Mol Cell Biol. 2005;25:8960-8970.
26. Wong ET, Kolman JL, Li YC, Mesner LD, Hillen W, Berens C, Wahl GM. Reproducible doxycycline-inducible transgene expression at specific loci generated by Cre-recombinase mediated cassette exchange. Nucleic Acids Res. 2005;33:e147.
27. Stegmeier F, Hu G, Rickles RJ, Hannon GJ, Elledge SJ. A lentiviral microRNA-based system for single-copy polymerase II-regulated RNA interference in mammalian cells. Proc Natl Acad Sci U S A. 2005;102:13212-13217.
28. Fischer A, Klamt B, Schumacher N, Glaeser C, Hansmann I, Fenge H, Gessler M. Phenotypic variability in Hey2 -/- mice and absence of HEY2 mutations in patients with congenital heart defects or Alagille syndrome. Mamm Genome. 2004;15:711-716.
29. Schneider JE, Bamforth SD, Farthing CR, Clarke K, Neubauer S, Bhattacharya S. Rapid identification and 3D reconstruction of complex cardiac malformations in transgenic mouse embryos using fast gradient echo sequence magnetic resonance imaging. J Mol Cell Cardiol. 2003;35:217-222.
30. Leimeister C, Externbrink A, Klamt B, Gessler M. Hey genes: a novel subfamily of hairy- and Enhancer of split related genes specifically expressed during mouse embryogenesis. Mech Dev. 1999;85:173-177.
31. Iso T, Sartorelli V, Poizat C, Iezzi S, Wu HY, Chung G, Kedes L, Hamamori Y. HERP, a novel heterodimer partner of HES/E(spl) in Notch signaling. Mol Cell Biol. 2001;21:6080-6089.
32. Eisenberg LM, Markwald RR. Molecular regulation of atrioventricular valvuloseptal morphogenesis. Circ Res. 1995;77:1-6.
33. Camenisch TD, Schroeder JA, Bradley J, Klewer SE, McDonald JA. Heart-valve mesenchyme formation is dependent on hyaluronan-augmented activation of ErbB2-ErbB3 receptors. Nat Med. 2002;8:850-855.
34. Timmerman LA, Grego-Bessa J, Raya A, Bertran E, Perez-Pomares JM, Diez J, Aranda S, Palomo S, McCormick F, Izpisua-Belmonte JC, de la Pompa JL. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev. 2004;18:99-115.
35. Wolf K, Mazo I, Leung H, Engelke K, von Andrian UH, Deryugina EI, Strongin AY, Brocker EB, Friedl P. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J Cell Biol. 2003;160:267-277.
36. Song W, Jackson K, McGuire PG. Degradation of type IV collagen by matrix metalloproteinases is an important step in the epithelial-mesenchymal transformation of the endocardial cushions. Dev Biol. 2000;227:606-617.
37. Enciso JM, Gratzinger D, Camenisch TD, Canosa S, Pinter E, Madri JA. Elevated glucose inhibits VEGF-A-mediated endocardial cushion formation: modulation by PECAM-1 and MMP-2. J Cell Biol. 2003;160:605-615.
38. Yokoyama K, Kamata N, Fujimoto R, Tsutsumi S, Tomonari M, Taki M, Hosokawa H, Nagayama M. Increased invasion and matrix metalloproteinase-2 expression by Snail-induced mesenchymal transition in squamous cell carcinomas. Int J Oncol. 2003;22:891-898.
39. Swiatek PJ, Lindsell CE, del Amo FF, Weinmaster G, Gridley T. Notch1 is essential for postimplantation development in mice. Genes Dev. 1994;8:707-719.
40. Oka C, Nakano T, Wakeham A, de la Pompa JL, Mori C, Sakai T, Okazaki S, Kawaichi M, Shiota K, Mak TW, Honjo T. Disruption of the mouse RBP-J kappa gene results in early embryonic death. Development. 1995;121:3291-3301.
41. Bessho Y, Sakata R, Komatsu S, Shiota K, Yamada S, Kageyama R. Dynamic expression and essential functions of Hes7 in somite segmentation. Genes Dev. 2001;15:2642-2647.
42. Noseda M, McLean G, Niessen K, Chang L, Pollet I, Montpetit R, Shahidi R, Dorovini-Zis K, Li L, Beckstead B, Durand RE, Hoodless PA, Karsan A. Notch activation results in phenotypic and functional changes consistent with endothelial-to-mesenchymal transformation. Circ Res. 2004;94:910-917.
43. Friedl P. Prespecification and plasticity: shifting mechanisms of cell migration. Curr Opin Cell Biol. 2004;16:14-23.
44. Wang Z, Banerjee S, Li Y, Rahman KM, Zhang Y, Sarkar FH. Down-regulation of notch-1 inhibits invasion by inactivation of nuclear factor-kappaB, vascular endothelial growth factor, and matrix metalloproteinase-9 in pancreatic cancer cells. Cancer Res. 2006;66:2778-2784.