Vulnerability of the developing heart to oxygen deprivation as a cause of congenital heart defects

Journal of the American Heart Association

Volumn 3, Issue 3, 2014, Pages

  Kenchegowda, Doreswamy ^a   Liu, Hongbin ^b   Thompson, Keyata ^a   Luo, Liping ^b   Martin, Stuart S ^a   Fisher, Steven A ^a,b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Conotruncus; Hypoxia; Neural crest; Persistent truncus arteriosus

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXYGEN; HIF1A PROTEIN, MOUSE; LUCIFERASE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; AORTA ANOMALY; ARTICLE; CHICK EMBRYO; CONGENITAL HEART MALFORMATION; EMBRYO; FEMALE; GENE EXPRESSION; HEART ATRIUM SEPTUM DEFECT; HEART DEVELOPMENT; HEART RIGHT VENTRICLE DOUBLE OUTLET; HEART VENTRICLE SEPTUM DEFECT; HYPOXIA; LIVER; MOUSE; NEURAL CREST CELL; NONHUMAN; OXYGEN TRANSPORT; PATENT DUCTUS ARTERIOSUS; PRIORITY JOURNAL; ANIMAL; ANOXIA; C57BL MOUSE; CARDIAC MUSCLE; CHEMISTRY; EMBRYOLOGY; HEART; HEART DEFECTS, CONGENITAL; METABOLISM; MUTANT MOUSE STRAIN; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; ANOXIA; HEART; HEART DEFECTS, CONGENITAL; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LUCIFERASES; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MYOCARDIUM; OXYGEN; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84904760921     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.114.000841     Document Type: Article

References (46)

1. Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell. 2008;30:393-402.
2. Prabhakar NR, Semenza GL. Adaptive and maladaptive cardiorespiratory responses to continuous and intermittent hypoxia mediated by hypoxiainducible factors 1 and 2. Physiol Rev. 2012;92:967-1003.
3. Fisher SA, Burggren WW. Role of hypoxia in the evolution and development of the cardiovascular system. Antioxid Redox Signal. 2007;9:1339-1352.
4. Dunwoodie SL. The role of hypoxia in development of the mammalian embryo. Dev Cell. 2009;17:755-773.
5. Webster WS, Abela D. The effect of hypoxia in development. Birth Defects Res C. 2007;81:215-228.
6. Safran M, Kim WY, O'Connell F, Flippin L, Gunzler V, Horner JW, DePinho RA, Kaelin WG Jr. Mouse model for noninvasive imaging of HIF prolyl hydroxylase activity: assessment of an oral agent that stimulates erythropoietin production. Proc Natl Acad Sci USA. 2006;103:105-110.
7. Hutson MR, Kirby ML. Model systems for the study of heart development and disease. Cardiac neural crest and conotruncal malformations. Semin Cell Dev Biol. 2007;18:101-110.
8. Gruber PJ, Epstein JA. Development gone awry: congenital heart disease. Circ Res. 2004;94:273-283.
9. Sugishita Y, Watanabe M, Fisher SA. Role of myocardial hypoxia in the remodeling of the embryonic avian cardiac outflow tract. Dev Biol. 2004;267:294-308.
10. Barbosky L, Lawrence DK, Karunamuni G, Wikenheiser JC, Doughman YQ, Visconti RP, Burch JB, Watanabe M. Apoptosis in the developing mouse heart. Dev Dyn. 2006;235:2592-2602.
11. Xu B, Doughman Y, Turakhia M, Jiang W, Landsettle CE, Agani FH, Semenza GL, Watanabe M, Yang YC. Partial rescue of defects in Cited2-deficient embryos by HIF-1alpha heterozygosity. Dev Biol. 2007;301:130-140.
12. Safran M, Kim WY, Kung AL, Horner JW, DePinho RA, Kaelin WG Jr. Mouse reporter strain for noninvasive bioluminescent imaging of cells that have undergone Cre-mediated recombination. Mol Imaging. 2003;2:297-302.
13. Hayashi S, McMahon AP. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol. 2002;244:305-318.
14. Ryan HE, Poloni M, McNulty W, Elson D, Gassmann M, Arbeit JM, Johnson RS. Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res. 2000;60:4010-4015.
15. Jiang X, Rowitch DH, Soriano P, McMahon AP, Sucov HM. Fate of the mammalian cardiac neural crest. Development. 2000;127:1607-1616.
16. Pan Y, Mansfield KD, Bertozzi CC, Rudenko V, Chan DA, Giaccia AJ, Simon MC. Multiple factors affecting cellular redox status and energy metabolism modulate hypoxia-inducible factor prolyl hydroxylase activity in vivo and in vitro. Mol Cell Biol. 2007;27:912-925.
17. New DA, Coppola PT. Effects of different oxygen concentrations on the development of rat embryos in culture. J Reprod Fertil. 1970;21:109-118.
18. Bamforth SD, Braganca J, Eloranta JJ, Murdoch JN, Marques FI, Kranc KR, Farza H, Henderson DJ, Hurst HC, Bhattacharya S. Cardiac malformations, adrenal agenesis, neural crest defects and exencephaly in mice lacking Cited2, a new Tfap2 co-activator. Nat Genet. 2001;29:469-474.
19. Barbera JP, Rodriguez TA, Greene ND, Weninger WJ, Simeone A, Copp AJ, Beddington RS, Dunwoodie S. Folic acid prevents exencephaly in Cited2 deficient mice. Hum Mol Genet. 2002;11:283-293.
20. Bamforth SD, Braganca J, Farthing CR, Schneider JE, Broadbent C, Michell AC, Clarke K, Neubauer S, Norris D, Brown NA, Anderson RH, Bhattacharya S. Cited2 controls left-right patterning and heart development through a Nodal-Pitx2c pathway. Nat Genet. 2004;36:1189-1196.
21. Lopes Floro K, Artap ST, Preis JI, Fatkin D, Chapman G, Furtado MB, Harvey RP, Hamada H, Sparrow DB, Dunwoodie SL. Loss of Cited2 causes congenital heart disease by perturbing left-right patterning of the body axis. Hum Mol Genet. 2011;20:1097-1110.
22. Popel AS, Goldman D, Vadapalli A. Modeling of oxygen diffusion from the blood vessels to intracellular organelles. Adv Exp Med Biol. 2003;530:485-495.
23. Kelly RG. The second heart field. Curr Top Dev Biol. 2012;100:33-65.
24. Schipani E, Ryan HE, Didrickson S, Kobayashi T, Knight M, Johnson RS. Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival. Genes Dev. 2001;15:2865-2876.
25. Maes C, Carmeliet G, Schipani E. Hypoxia-driven pathways in bone development, regeneration and disease. Nat Rev Rheumatol. 2012;8:358-366.
26. Ryan HE, Lo J, Johnson RS. HIF-1alpha is required for solid tumor formation and embryonic vascularization. EMBO J. 1998;17:3005-3015.
27. Adelman DM, Gertsenstein M, Nagy A, Simon MC, Maltepe E. Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev. 2000;14:3191-3203.
28. Withington SL, Scott AN, Saunders DN, Lopes Floro K, Preis JI, Michalicek J, Maclean K, Sparrow DB, Barbera JP, Dunwoodie SL. Loss of Cited2 affects trophoblast formation and vascularization of the mouse placenta. Dev Biol. 2006;294:67-82.
29. Takeda K, Ho VC, Takeda H, Duan LJ, Nagy A, Fong GH. Placental but not heart defects are associated with elevated hypoxia-inducible factor alpha levels in mice lacking prolyl hydroxylase domain protein 2. Mol Cell Biol. 2006;26:8336-8346.
30. Makita T, Duncan SA, Sucov HM. Retinoic acid, hypoxia, and GATA factors cooperatively control the onset of fetal liver erythropoietin expression and erythropoietic differentiation. Dev Biol. 2005;280:59-72.
31. Sugishita Y, Leifer DW, Agani F, Watanabe M, Fisher SA. Hypoxia-responsive signaling regulates the apoptosis-dependent remodeling of the embryonic avian cardiac outflow tract. Dev Biol. 2004;273:285-296.
32. Bradshaw L, Chaudhry B, Hildreth V, Webb S, Henderson DJ. Dual role for neural crest cells during outflow tract septation in the neural crest-deficient mutant Splotch(2H). J Anat. 2009;214:245-257.
33. Compernolle V, Brusselmans K, Franco D, Moorman A, Dewerchin M, Collen D, Carmeliet P. Cardia bifida, defective heart development and abnormal neural crest migration in embryos lacking hypoxia-inducible factor-1alpha. Cardiovasc Res. 2003;60:569-579.
34. Iyer NV, Kotch LE, Agani F, Leung SW, Laughner E, Wenger RH, Gassmann M, Gearhart JD, Lawler AM, Yu AY, Semenza GL. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev. 1998;12:149-162.
35. Liu H, Fisher SA. Hypoxia-inducible transcription factor-1alpha triggers an autocrine survival pathway during embryonic cardiac outflow tract remodeling. Circ Res. 2008;102:1331-1339.
36. Friedman JM. The principles of teratology: are they still true? Birth Defects Res A Clin Mol Teratol. 2010;88:766-768.
37. Krishnan J, Ahuja P, Bodenmann S, Knapik D, Perriard E, Krek W, Perriard JC. Essential role of developmentally activated hypoxia-inducible factor 1alpha for cardiac morphogenesis and function. Circ Res. 2008;103:1139-1146.
38. Lage K, Greenway SC, Rosenfeld JA, Wakimoto H, Gorham JM, Segre AV, Roberts AE, Smoot LB, Pu WT, Pereira AC, Mesquita SM, Tommerup N, Brunak S, Ballif BC, Shaffer LG, Donahoe PK, Daly MJ, Seidman JG, Seidman CE, Larsen LA. Genetic and environmental risk factors in congenital heart disease functionally converge in protein networks driving heart development. Proc Natl Acad Sci USA. 2012;109:14035-14040.
39. Kulesa PM, Bailey CM, Kasemeier-Kulesa JC, McLennan R. Cranial neural crest migration: new rules for an old road. Dev Biol. 2010;344:543-554.
40. Wolf N, Yang W, Dunk CE, Gashaw I, Lye SJ, Ring T, Schmidt M, Winterhager E, Gellhaus A. Regulation of the matricellular proteins CYR61 (CCN1) and NOV (CCN3) by hypoxia-inducible factor-1alpha and transforming-growth factor-beta3 in the human trophoblast. Endocrinology. 2010;151:2835-2845.
41. Meyuhas R, Pikarsky E, Tavor E, Klar A, Abramovitch R, Hochman J, Lago TG, Honigman A. A key role for cyclic AMP-responsive element binding protein in hypoxia-mediated activation of the angiogenesis factor CCN1 (CYR61) in tumor cells. Mol Cancer Res. 2008;6:1397-1409.
42. Xia X, Kung AL. Preferential binding of HIF-1 to transcriptionally active loci determines cell-type specific response to hypoxia. Genome Biol. 2009;10:R113.
43. Lendahl U, Lee KL, Yang H, Poellinger L. Generating specificity and diversity in the transcriptional response to hypoxia. Nat Rev Genet. 2009;10:821-832.
44. Mo FE, Lau LF. The matricellular protein CCN1 is essential for cardiac development. Circ Res. 2006;99:961-969.
45. Katsube K, Sakamoto K, Tamamura Y, Yamaguchi A. Role of CCN, a vertebrate specific gene family, in development. Dev Growth Differ. 2009;51:55-67.
46. Wright S. The results of crosses between inbred strains of guinea pigs, differing in number of digits. Genetics. 1934;19:537-551.