Ethanol exposure alters early cardiac function in the looping heart: A mechanism for congenital heart defects?

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 306, Issue 3, 2014, Pages

  Karunamuni, Ganga ^a   Gu, Shi ^b   Doughman, Yong Qiu ^a   Peterson, Lindsy M ^b   Mai, Katherine ^a   McHale, Quinn ^a   Jenkins, Michael W ^b   Linask, Kersti K ^c   Rollins, Andrew M ^b   Watanabe, Michiko ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b Case Western Reserve University   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Cardiac function; Congenital heart defects; Ethanol

Indexed keywords

ALCOHOL;

ANIMAL TISSUE; ARTICLE; BIRTH DEFECT; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; DOPPLER ECHOCARDIOGRAPHY; EMBRYO; EMBRYO DEVELOPMENT; GASTRULATION; HEART ATRIOVENTRICULAR VALVE; HEART DEVELOPMENT; HEART FUNCTION; HEART HEMODYNAMICS; HEART RATE; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; PRIORITY JOURNAL; QUAIL; STRUCTURE ANALYSIS; YOLK SAC;

CARDIAC FUNCTION; CONGENITAL HEART DEFECTS; ETHANOL;

ANIMALS; COTURNIX; ECHOCARDIOGRAPHY, DOPPLER; EMBRYO, NONMAMMALIAN; ETHANOL; GASTRULATION; HEART; HEART DEFECTS, CONGENITAL; HEMODYNAMICS; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 84893423665     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00600.2013     Document Type: Article

References (67)

1. Abel. EL Fetal Alcohol Syndrome. Oradell, NJ: Medical Economics, 1990.
2. Atkins GB, Jain MK. Role of Kruppel-like transcription factors in endothelial biology. Circ Res 100: 1686-1695, 2007.
3. Bilotta J, Barnett JA, Hancock L, Saszik S. Ethanol exposure alters zebrafish development: a novel model of fetal alcohol syndrome. Neurotoxicol Teratol 26: 737-743, 2004.
4. Binkhorst M, Wortmann SB, Funke S, Kozicz T, Wevers RA, Morava E. Glycosylation defects underlying fetal alcohol spectrum disorder: a novel pathogenetic model. "When the wine goes in, strange things come out"-S. T. Coleridge, The Piccolomini. J Inherit Metab Dis 35: 399-405, 2012.
5. Brennan D, Giles S. Sonic hedgehog expression is disrupted following in ovo ethanol exposure during early chick eye development. Reprod Toxicol 41: 49-56, 2013. 5a. Bruyere HJ Jr, Stith CE. Ethyl alcohol reduces cardiac output, stroke volume, and end diastolic volume in the embryonic chick. Teratology 49: 104-112, 1994.
6. Burd L, Deal E, Rios R, Adickes E, Wynne J, Klug MG. Congenital heart defects and fetal alcohol spectrum disorders. Congenit Heart Dis 2: 250-255, 2007.
7. Cartwright MM, Smith SM. Increased cell death and reduced neural crest cell numbers in ethanol-exposed embryos: partial basis for the fetal alcohol syndrome phenotype. Alcohol Clin Exp Res 19: 378-386, 1995.
8. Cavieres MF, Smith SM. Genetic and developmental modulation of cardiac deficits in prenatal alcohol exposure. Alcohol Clin Exp Res 24: 102-109, 2000.
9. Chi NC, Bussen M, Brand-Arzamendi K, Ding C, Olgin JE, Shaw RM, Martin GR, Stainier DY. Cardiac conduction is required to preserve cardiac chamber morphology. Proc Natl Acad Sci USA 107: 14662-14667, 2010.
10. Chi NC, Shaw RM, Jungblut B, Huisken J, Ferrer T, Arnaout R, Scott I, Beis D, Xiao T, Baier H, Jan LY, Tristani-Firouzi M, Stainier DY. Genetic and physiologic dissection of the vertebrate cardiac conduction system. PLoS Biol 6: e109, 2008.
11. Clarren SK, Smith DW. The fetal alcohol syndrome. Lamp 35: 4-7, 1978.
12. Combs MD, Yutzey KE. Heart valve development: regulatory networks in development and disease. Circ Res 105: 408-421, 2009.
13. Creazzo TL, Brotto MA, Burch J. Excitation-contraction coupling in the day 15 embryonic chick heart with persistent truncus arteriosus. Pediatr Res 42: 731-737, 1997.
14. Daft PA, Johnston MC, Sulik KK. Abnormal heart and great vessel development following acute ethanol exposure in mice. Teratology 33: 93-104, 1986.
15. Dekker RJ, van Soest S, Fontijn RD, Salamanca S, de Groot PG, VanBavel E, Pannekoek H, Horrevoets AJ. Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Kruppel-like factor (KLF2). Blood 100: 1689-1698, 2002.
16. Deltour L, Ang HL, Duester G. Ethanol inhibition of retinoic acid synthesis as a potential mechanism for fetal alcohol syndrome. FASEB J 10: 1050-1057, 1996.
17. Dlugos CA, Rabin RA. Structural and functional effects of developmental exposure to ethanol on the zebrafish heart. Alcohol Clin Exp Res 34: 1013-1021, 2010.
18. Flentke GR, Garic A, Amberger E, Hernandez M, Smith SM. Calciummediated repression of beta-catenin and its transcriptional signaling mediates neural crest cell death in an avian model of fetal alcohol syndrome. Birth Defects Res A Clin Mol Teratol 91: 591-602, 2011.
19. Floyd RL, Sidhu JS. Monitoring prenatal alcohol exposure. Am J Med Genet C Semin Med Genet 127C: 3-9, 2004.
20. Flynn ME, Pikalow AS, Kimmelman RS, Searls RL. The mechanism of cervical flexure formation in the chick. Anat Embryol (Berl) 184: 411-420, 1991.
21. Godt RE, Fogaca RT, Nosek TM. Alterations of myocardial contraction associated with a structural heart defect in embryonic chicks. Adv Exp Med Biol 453: 453-458; discussion 459, 1998.
22. Granados-Riveron JT, Brook JD. The impact of mechanical forces in heart morphogenesis. Circ Cardiovasc Genet 5: 132-142, 2012.
23. Grewal J, Carmichael SL, Ma C, Lammer EJ, Shaw GM. Maternal periconceptional smoking and alcohol consumption and risk for select congenital anomalies. Birth Defects Res A Clin Mol Teratol 82: 519-526, 2008.
24. Groenendijk BC, Hierck BP, Vrolijk J, Baiker M, Pourquie MJ, Gittenberger-de Groot AC, Poelmann RE. Changes in shear stressrelated gene expression after experimentally altered venous return in the chicken embryo. Circ Res 96: 1291-1298, 2005.
25. Groenendijk BC, Stekelenburg-de Vos S, Vennemann P, Wladimiroff JW, Nieuwstadt FT, Lindken R, Westerweel J, Hierck BP, Ursem NT, Poelmann RE. The endothelin-1 pathway and the development of cardiovascular defects in the haemodynamically challenged chicken embryo. J Vasc Res 45: 54-68, 2008.
26. Groenendijk BC, Van der Heiden K, Hierck BP, Poelmann RE. The role of shear stress on ET-1, KLF2, and NOS-3 expression in the developing cardiovascular system of chicken embryos in a venous ligation model. Physiology (Bethesda) 22: 380-389, 2007.
27. Gu S, Jenkins MW, Peterson LM, Doughman YQ, Rollins AM, Watanabe M. Optical coherence tomography captures rapid hemodynamic responses to acute hypoxia in the cardiovascular system of early embryos. Dev Dyn 241: 534-544, 2012.
28. Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. J Morphol 88: 49-92, 1951.
29. Hogers B, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE. Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal. Cardiovasc Res 41: 87-99, 1999.
30. Hove JR, Koster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, Gharib M. Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421: 172-177, 2003.
31. Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WG, Chang W, Hee MR, Flotte T, Gregory K, Puliafito CA, Fujimoto JG. Optical coherence tomography. Science 254: 1178-1181, 1991.
32. Huber R, Adler DC, Fujimoto JG. Buffered Fourier domain mode locking: Unidirectional swept laser sources for optical coherence tomography imaging at 370, 000 lines/s. Opt Lett 31: 2975-2977, 2006.
33. Huber R, Wojtkowski M, Fujimoto JG. Fourier Domain Mode Locking (FDML): A new laser operating regime and applications for optical coherence tomography. Opt Express 14: 3225-3237, 2006.
34. Jenkins MW, Watanabe M, Rollins AM. Longitudinal imaging of heart development with optical coherence tomography. IEEE J 18: 1166-1175, 2011.
35. Jenkins MW, Adler DC, Gargesha M, Huber R, Rothenberg F, Belding J, Watanabe M, Wilson DL, Fujimoto JG, Rollins AM. Ultrahigh-speed optical coherence tomography imaging and visualization of the embryonic avian heart using a buffered Fourier Domain Mode Locked laser. Opt Express 15: 6251-6267, 2007.
36. Jenkins MW, Peterson L, Gu S, Gargesha M, Wilson DL, Watanabe M, Rollins AM. Measuring hemodynamics in the developing heart tube with four-dimensional gated Doppler optical coherence tomography. J Biomed Opt 15: 066022, 2010.
37. Jones KL, Smith DW. Recognition of the fetal alcohol syndrome in early infancy. Lancet 302: 999-1001, 1973.
38. Keller BB, Liu LJ, Tinney JP, Tobita K. Cardiovascular developmental insights from embryos. Ann NY Acad Sci 1101: 377-388, 2007.
39. Kim M, Kim S, Lim JH, Lee C, Choi HC, Woo CH. Laminar flow activation of ERK5 protein in vascular endothelium leads to atheroprotective effect via NF-E2-related factor 2 (Nrf2) activation. J Biol Chem 287: 40722-40731, 2012.
40. Kot-Leibovich H, Fainsod A. Ethanol induces embryonic malformations by competing for retinaldehyde dehydrogenase activity during vertebrate gastrulation. Dis Model Mech 2: 295-305, 2009.
41. Lee JS, Yu Q, Shin JT, Sebzda E, Bertozzi C, Chen M, Mericko P, Stadtfeld M, Zhou D, Cheng L, Graf T, MacRae CA, Lepore JJ, Lo CW, Kahn ML. Klf2 is an essential regulator of vascular hemodynamic forces in vivo. Dev Cell 11: 845-857, 2006.
42. Lee TC, Zhao YD, Courtman DW, Stewart DJ. Abnormal aortic valve development in mice lacking endothelial nitric oxide synthase. Circulation 101: 2345-2348, 2000.
43. Linask KK, Vanauker M. A role for the cytoskeleton in heart looping. ScientificWorldJournal 7: 280-298, 2007.
44. Loucks EJ, Ahlgren SC. Deciphering the role of Shh signaling in axial defects produced by ethanol exposure. Birth Defects Res A Clin Mol Teratol 85: 556-567, 2009.
45. Lucitti JL, Visconti R, Novak J, Keller BB. Increased arterial load alters aortic structural and functional properties during embryogenesis. Am J Physiol Heart Circ Physiol 291: H1919-H1926, 2006.
46. Manner J, Seidl W, Steding G. Correlation between the embryonic head flexures and cardiac development. An experimental study in chick embryos. Anat Embryol (Berl) 188: 269-285, 1993.
47. Manner J, Thrane L, Norozi K, Yelbuz TM. High-resolution in vivo imaging of the cross-sectional deformations of contracting embryonic heart loops using optical coherence tomography. Dev Dyn 237: 953-961, 2008.
48. Marrs JA, Clendenon SG, Ratcliffe DR, Fielding SM, Liu Q, Bosron WF. Zebrafish fetal alcohol syndrome model: effects of ethanol are rescued by retinoic acid supplement. Alcohol 44: 707-715, 2010.
49. Marschall S, Sander B, Mogensen M, Jorgensen TM, Andersen PE. Optical coherence tomography-current technology and applications in clinical and biomedical research. Anal Bioanal Chem 400: 2699-2720, 2011.
50. McQuinn TC, Bratoeva M, Dealmeida A, Remond M, Thompson RP, Sedmera D. High-frequency ultrasonographic imaging of avian cardiovascular development. Dev Dyn 236: 3503-3513, 2007.
51. Peterson LM, Jenkins MW, Gu S, Barwick L, Watanabe M, Rollins AM. 4D shear stress maps of the developing heart using Doppler optical coherence tomography. Biomed Opt Express 3: 3022-3032, 2012.
52. Reckova M, Rosengarten C, deAlmeida A, Stanley CP, Wessels A, Gourdie RG, Thompson RP, Sedmera D. Hemodynamics is a key epigenetic factor in development of the cardiac conduction system. Circ Res 93: 77-85, 2003.
53. Rovasio RA, Battiato NL. Role of early migratory neural crest cells in developmental anomalies induced by ethanol. Int J Dev Biol 39: 421-422, 1995.
54. Ruckman RN, Messersmith DJ, O'Brien SA, Getson PR, Boeckx RL, Morse DE. Chronic ethanol exposure in the embryonic chick heart: effect on myocardial function and structure. Teratology 37: 317-327, 1988.
55. Serrano M, Han M, Brinez P, Linask KK. Fetal alcohol syndrome: cardiac birth defects in mice and prevention with folate. Am J Obstet Gynecol 203: 75. e7-75. e15, 2010.
56. Shu X, Cheng K, Patel N, Chen F, Joseph E, Tsai HJ, Chen JN. Na, K-ATPase is essential for embryonic heart development in the zebrafish. Development 130: 6165-6173, 2003.
57. Smith SM, Flentke GR, Garic A. Avian models in teratology and developmental toxicology. Methods Mol Biol 889: 85-103, 2012.
58. Tai LK, Zheng Q, Pan S, Jin ZG, Berk BC. Flow activates ERK1/2 and endothelial nitric oxide synthase via a pathway involving PECAM1, SHP2, and Tie2. J Biol Chem 280: 29620-29624, 2005.
59. Tawakol A, Omland T, Creager MA. Direct effect of ethanol on human vascular function. Am J Physiol Heart Circ Physiol 286: H2468-H2473, 2004.
60. Twal WO, Zile MH. Retinoic acid reverses ethanol-induced cardiovascular abnormalities in quail embryos. Alcohol Clin Exp Res 21: 1137-1143, 1997.
61. Vermot J, Forouhar AS, Liebling M, Wu D, Plummer D, Gharib M, Fraser SE. Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart. PLoS Biol 7: e1000246, 2009.
62. Vittorini S, Storti S, Parri MS, Cerillo AG, Clerico A. SERCA2a, phospholamban, sarcolipin, and ryanodine receptors gene expression in children with congenital heart defects. Mol Med 13: 105-111, 2007.
63. Wang G, Bieberich E. Prenatal alcohol exposure triggers ceramideinduced apoptosis in neural crest-derived tissues concurrent with defective cranial development. Cell Death Dis 1: e46, 2010.
64. Wang N, Miao H, Li YS, Zhang P, Haga JH, Hu Y, Young A, Yuan S, Nguyen P, Wu CC, Chien S. Shear stress regulation of Kruppel-like factor 2 expression is flow pattern-specific. Biochem Biophys Res Commun 341: 1244-1251, 2006.
65. Yashiro K, Shiratori H, Hamada H. Haemodynamics determined by a genetic programme govern asymmetric development of the aortic arch. Nature 450: 285-288, 2007.
66. Yelbuz TM, Waldo KL, Kumiski DH, Stadt HA, Wolfe RR, Leatherbury L, Kirby ML. Shortened outflow tract leads to altered cardiac looping after neural crest ablation. Circulation 106: 504-510, 2002.
67. Yelin R, Yelin D, Oh WY, Yun SH, Boudoux C, Vakoc BJ, Bouma BE, Tearney GJ. Multimodality optical imaging of embryonic heart microstructure. J Biomed Opt 12: 064021, 2007.