Disruption of spatiotemporal hypoxic signaling causes congenital heart disease in mice

Journal of Clinical Investigation

Volumn 127, Issue 6, 2017, Pages 2235-2248

  Yuan, Xuejun ^a   Qi, Hui ^a   Li, Xiang ^a   Wu, Fan ^a   Fang, Jian ^a   Bober, Eva ^a   Dobreva, Gergana ^a   Zhou, Yonggang ^a   Braun, Thomas ^a  

^a MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 5; HOMEOBOX PROTEIN NKX-2.5; HYPOXIA INDUCIBLE FACTOR 1ALPHA; ISLET 1 PROTEIN; MESSENGER RNA; PROTEIN; SIRTUIN 1; TRANSCRIPTION FACTOR HES 1; UNCLASSIFIED DRUG; HISTONE DEACETYLASE; INSULIN GENE ENHANCER BINDING PROTEIN ISL-1; LIM HOMEODOMAIN PROTEIN; NKX2-5 PROTEIN, MOUSE; SIRT1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC MUSCLE CELL; CARDIAC STEM CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; COMPLEX FORMATION; CONGENITAL HEART DISEASE; CONTROLLED STUDY; DIFFERENTIATION; EMBRYO; GENE EXPRESSION; HEART DEVELOPMENT; HEART MUSCLE ISCHEMIA; HYPOXIC CELL; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TISSUE OXYGENATION; UPREGULATION; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; CELL HYPOXIA; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HEART DEFECTS, CONGENITAL; HEK293 CELL LINE; HUMAN; MAMMALIAN EMBRYO; METABOLISM; PATHOLOGY; PREGNANCY; SPATIOTEMPORAL ANALYSIS; TRANSGENIC MOUSE;

ANIMALS; CELL HYPOXIA; CELL PROLIFERATION; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; HEART DEFECTS, CONGENITAL; HEK293 CELLS; HISTONE DEACETYLASES; HOMEOBOX PROTEIN NKX-2.5; HUMANS; LIM-HOMEODOMAIN PROTEINS; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCARDIUM; PREGNANCY; SIGNAL TRANSDUCTION; SIRTUIN 1; SPATIO-TEMPORAL ANALYSIS; TRANSCRIPTION FACTORS;

EID: 85020182993     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI88725     Document Type: Article

References (60)

1. Kelly RG, Buckingham ME, Moorman AF. Heart fields and cardiac morphogenesis. Cold Spring Harb Perspect Med. 2014;4(10):a015750.
2. Fahed AC, Gelb BD, Seidman JG, Seidman CE. Genetics of congenital heart disease: the glass half empty. Circ Res. 2013;112(4):707-720.
3. Patel SS, Burns TL. Nongenetic risk factors and congenital heart defects. Pediatr Cardiol. 2013;34(7):1535-1555.
4. Kenchegowda D, Liu H, Thompson K, Luo L, Martin SS, Fisher SA. Vulnerability of the developing heart to oxygen deprivation as a cause of congenital heart defects. J Am Heart Assoc. 2014;3(3):e000841.
5. Dunwoodie SL. The role of hypoxia in development of the Mammalian embryo. Dev Cell. 2009;17(6):755-773.
6. Webster WS, Abela D. The effect of hypoxia in development. Birth Defects Res C Embryo Today. 2007;81(3):215-228.
7. Miao CY, Zuberbuhler JS, Zuberbuhler JR. Prevalence of congenital cardiac anomalies at high altitude. J Am Coll Cardiol. 1988;12(1):224-228.
8. Hasan A. Relationship of high altitude and congenital heart disease. Indian Heart J. 2016;68(1):9-12.
9. Simon MC, Keith B. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol. 2008;9(4):285-296.
10. Mohyeldin A, Garzón-Muvdi T, Quiñones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell. 2010;7(2):150-161.
11. Majmundar AJ, Wong WJ, Simon MC. Hypoxiainducible factors and the response to hypoxic stress. Mol Cell. 2010;40(2):294-309.
12. Kaelin WG, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell. 2008;30(4):393-402.
13. Semenza GL. Hypoxia-inducible factors in physiology and medicine. Cell. 2012;148(3):399-408.
14. Buckingham M, Meilhac S, Zaffran S. Building the mammalian heart from two sources of myocardial cells. Nat Rev Genet. 2005;6(11):826-835.
15. Meilhac SM, Esner M, Kelly RG, Nicolas JF, Buckingham ME. The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev Cell. 2004;6(5):685-698.
16. Evans SM, Yelon D, Conlon FL, Kirby ML. Myocardial lineage development. Circ Res. 2010;107(12):1428-1444.
17. Stainier DY. Zebrafish genetics and vertebrate heart formation. Nat Rev Genet. 2001;2(1):39-48.
18. Zhou Y, Kim J, Yuan X, Braun T. Epigenetic modifications of stem cells: a paradigm for the control of cardiac progenitor cells. Circ Res. 2011;109(9):1067-1081.
19. Prall OW, et al. An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell. 2007;128(5):947-959.
20. Dyer LA, Kirby ML. The role of secondary heart field in cardiac development. Dev Biol. 2009;336(2):137-144.
21. Dorn T, et al. Direct nkx2-5 transcriptional repression of isl1 controls cardiomyocyte subtype identity. Stem Cells. 2015;33(4):1113-1129.
22. Watanabe Y, et al. Fibroblast growth factor 10 gene regulation in the second heart field by Tbx1, Nkx2-5, and Islet1 reveals a genetic switch for down-regulation in the myocardium. Proc Natl Acad Sci U S A. 2012;109(45):18273-18280.
23. Cai CL, et al. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell. 2003;5(6):877-889.
24. Kwon C, Qian L, Cheng P, Nigam V, Arnold J, Srivastava D. A regulatory pathway involving Notch1/beta-catenin/Isl1 determines cardiac progenitor cell fate. Nat Cell Biol. 2009;11(8):951-957.
25. Krishnan J, et al. Essential role of developmentally activated hypoxia-inducible factor 1alpha for cardiac morphogenesis and function. Circ Res. 2008;103(10):1139-1146.
26. Arany Z, et al. An essential role for p300/CBP in the cellular response to hypoxia. Proc Natl Acad Sci U S A. 1996;93(23):12969-12973.
27. Ema M, et al. Molecular mechanisms of transcription activation by HLF and HIF1alpha in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300. EMBO J. 1999;18(7):1905-1914.
28. Eltzschig HK, et al. HIF-1-dependent repression of equilibrative nucleoside transporter (ENT) in hypoxia. J Exp Med. 2005;202(11):1493-1505.
29. Prozorovski T, et al. Sirt1 contributes critically to the redox-dependent fate of neural progenitors. Nat Cell Biol. 2008;10(4):385-394.
30. Rochais F, Dandonneau M, Mesbah K, Jarry T, Mattei MG, Kelly RG. Hes1 is expressed in the second heart field and is required for outflow tract development. PLoS ONE. 2009;4(7):e6267.
31. Nasrin N, et al. JNK1 phosphorylates SIRT1 and promotes its enzymatic activity. PLoS ONE. 2009;4(12):e8414.
32. Cheng HL, et al. Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice. Proc Natl Acad Sci U S A. 2003;100(19):10794-10799.
33. Karamboulas C, et al. HDAC activity regulates entry of mesoderm cells into the cardiac muscle lineage. J Cell Sci. 2006;119(Pt 20):4305-4314.
34. Breckenridge RA, et al. Hypoxic regulation of hand1 controls the fetal-neonatal switch in cardiac metabolism. PLoS Biol. 2013;11(9):e1001666.
35. Guarani V, Potente M. SIRT1 - a metabolic sensor that controls blood vessel growth. Curr Opin Pharmacol. 2010;10(2):139-145.
36. Hsu CP, et al. Silent information regulator 1 protects the heart from ischemia/reperfusion. Circulation. 2010;122(21):2170-2182.
37. Potente M, et al. SIRT1 controls endothelial angiogenic functions during vascular growth. Genes Dev. 2007;21(20):2644-2658.
38. Della-Morte D, Dave KR, DeFazio RA, Bao YC, Raval AP, Perez-Pinzon MA. Resveratrol pretreatment protects rat brain from cerebral ischemic damage via a sirtuin 1-uncoupling protein 2 pathway. Neuroscience. 2009;159(3):993-1002.
39. Sakamoto J, Miura T, Shimamoto K, Horio Y. Predominant expression of Sir2alpha, an NADdependent histone deacetylase, in the embryonic mouse heart and brain. FEBS Lett. 2004;556(1-3):281-286.
40. Nath KA. The role of Sirt1 in renal rejuvenation and resistance to stress. J Clin Invest. 2010;120(4):1026-1028.
41. Dioum EM, et al. Regulation of hypoxiainducible factor 2alpha signaling by the stress-responsive deacetylase sirtuin 1. Science. 2009;324(5932):1289-1293.
42. Yoon H, Shin SH, Shin DH, Chun YS, Park JW. Differential roles of Sirt1 in HIF-1α and HIF-2α mediated hypoxic responses. Biochem Biophys Res Commun. 2014;444(1):36-43.
43. Stevens KN, et al. Common variation in ISL1 confers genetic susceptibility for human congenital heart disease. PLoS ONE. 2010;5(5):e10855.
44. Friedrich FW, et al. A novel genetic variant in the transcription factor Islet-1 exerts gain of function on myocyte enhancer factor 2C promoter activity. Eur J Heart Fail. 2013;15(3):267-276.
45. Osoegawa K, Schultz K, Yun K, Mohammed N, Shaw GM, Lammer EJ. Haploinsufficiency of insulin gene enhancer protein 1 (ISL1) is associated with d-transposition of the great arteries. Mol Genet Genomic Med. 2014;2(4):341-351.
46. Witzel HR, Jungblut B, Choe CP, Crump JG, Braun T, Dobreva G. The LIM protein Ajuba restricts the second heart field progenitor pool by regulating Isl1 activity. Dev Cell. 2012;23(1):58-70.
47. Caputo L, et al. The Isl1/Ldb1 complex orchestrates genome-wide chromatin organization to instruct differentiation of multipotent cardiac Progenitors. Cell Stem Cell. 2015;17(3):287-299.
48. Srinivas S, et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol. 2001;1:4.
49. Eggan K, et al. Hybrid vigor, fetal overgrowth, and viability of mice derived by nuclear cloning and tetraploid embryo complementation. Proc Natl Acad Sci USA. 2001;98(11):6209-6214.
50. Yang L, et al. Isl1Cre reveals a common Bmp pathway in heart and limb development. Development. 2006;133(8):1575-1585.
51. Osterwalder M, Galli A, Rosen B, Skarnes WC, Zeller R, Lopez-Rios J. Dual RMCE for efficient re-engineering of mouse mutant alleles. Nat Methods. 2010;7(11):893-895.
52. Petrie K, et al. The histone deacetylase 9 gene encodes multiple protein isoforms. J Biol Chem. 2003;278(18):16059-16072.
53. Zhou Y, Santoro R, Grummt I. The chromatin remodeling complex NoRC targets HDAC1 to the ribosomal gene promoter and represses RNA polymerase I transcription. EMBO J. 2002;21(17):4632-4640.
54. Zhou Y, Schmitz KM, Mayer C, Yuan X, Akhtar A, Grummt I. Reversible acetylation of the chromatin remodelling complex NoRC is required for non-coding RNA-dependent silencing. Nat Cell Biol. 2009;11(8):1010-1016.
55. Wystub K, Besser J, Bachmann A, Boettger T, Braun T. miR-1/133a clusters cooperatively specify the cardiomyogenic lineage by adjustment of myocardin levels during embryonic heart development. PLoS Genet. 2013;9(9):e1003793.
56. Bu L, et al. Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature. 2009;460(7251):113-117.
57. Zhang T, et al. Prmt5 is a regulator of muscle stem cell expansion in adult mice. Nat Commun. 2015;6:7140.
58. Nelson JD, Denisenko O, Bomsztyk K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat Protoc. 2006;1(1):179-185.
59. Larionov A, Krause A, Miller W. A standard curve based method for relative real time PCR data processing. BMC Bioinformatics. 2005;6:62.
60. Domian IJ, et al. Generation of functional ventricular heart muscle from mouse ventricular progenitor cells. Science. 2009;326(5951):426-429.