Complex cardiac defects after ethanol exposure during discrete cardiogenic events in zebrafish: Prevention with folic acid

Developmental Dynamics

Volumn 242, Issue 10, 2013, Pages 1184-1201

  Sarmah, Swapnalee ^a   Marrs, James A ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Cardiac defects; Congenital heart defects; Ethanol exposure; Fetal alcohol spectrum disorder; Zebrafish

Indexed keywords

ALCOHOL; FOLIC ACID; RETINOIC ACID;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDOCARDIAL CUSHION; ENDOCARDIAL CUSHION DEFECT; ENDOCARDIUM; GASTRULATION; GENE EXPRESSION; GROWTH CURVE; HEART DEVELOPMENT; HEART DISEASE; LONG TERM EXPOSURE; MORPHOGENESIS; MYOCARDIAL DISEASE; NONHUMAN; PRECURSOR; PRIORITY JOURNAL; VITAMIN SUPPLEMENTATION; ZEBRA FISH;

DANIO RERIO;

CARDIAC DEFECTS; CONGENITAL HEART DEFECTS; ETHANOL EXPOSURE; FETAL ALCOHOL SPECTRUM DISORDER; ZEBRAFISH;

ALCOHOL-INDUCED DISORDERS; ANIMALS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ETHANOL; FOLIC ACID; GASTRULATION; HEART; HEART DEFECTS, CONGENITAL; ORGANOGENESIS; VITAMIN B COMPLEX; ZEBRAFISH;

EID: 84884717423     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24015     Document Type: Article

References (62)

1. Abel EL. 1995. An update on incidence of FAS: FAS is not an equal opportunity birth defect. Neurotoxicol Teratol 17:437-443.
2. Abel EL. 1998. Fetal alcohol abuse syndrome. New York: Plenum Press.
3. Abel EL, Hannigan JH. 1995. Maternal risk factors in fetal alcohol syndrome: provocative and permissive influences. Neurotoxicol Teratol 17:445-462.
4. Auman HJ, Coleman H, Riley HE, Olale F, Tsai HJ, Yelon D. 2007. Functional modulation of cardiac form through regionally confined cell shape changes. PLoS Biol 5:e53.
5. Bailey LB, Berry RJ. 2005. Folic acid supplementation and the occurrence of congenital heart defects, orofacial clefts, multiple births, and miscarriage. Am J Clin Nutrit 81:1213S-1217S.
6. Ballard MS, Sun M, Ko J. 2012. Vitamin A, folate, and choline as a possible preventive intervention to fetal alcohol syndrome. Med Hypoth 78:489-493.
7. Bartman T, Walsh EC, Wen KK, McKane M, Ren J, Alexander J, Rubenstein PA, Stainier DY. 2004. Early myocardial function affects endocardial cushion development in zebrafish. PLoS Biol 2:E129.
8. Bean LJ, Allen EG, Tinker SW, Hollis ND, Locke AE, Druschel C, Hobbs CA, O'Leary L, Romitti PA, Royle MH, Torfs CP, Dooley KJ, Freeman SB, Sherman SL. 2011. Lack of maternal folic acid supplementation is associated with heart defects in Down syndrome: a report from the National Down Syndrome Project. Birth Defects Res A 91:885-893.
9. Beis D, Bartman T, Jin SW, Scott IC, D'Amico LA, Ober EA, Verkade H, Frantsve J, Field HA, Wehman A, Baier H, Tallafuss A, Bally-Cuif L, Chen JN, Stainier DY, Jungblut B. 2005. Genetic and cellular analyses of zebrafish atrioventricular cushion and valve development. Development 132:4193-4204.
10. Bingol N, Schuster C, Fuchs M, Iosub S, Turner G, Stone RK, Gromisch DS. 1987. The influence of socioeconomic factors on the occurrence of fetal alcohol syndrome. Adv Alcohol Substance Abuse 6:105-118.
11. Blader P, Strahle U. 1998. Ethanol impairs migration of the prechordal plate in the zebrafish embryo. Dev Biol 201:185-201.
12. Bruyere HJ Jr, Stith CE. 1993. Strain-dependent effect of ethanol on ventricular septal defect frequency in White Leghorn chick embryos. Teratology 48:299-303.
13. Burd L, Deal E, Rios R, Adickes E, Wynne J, Klug MG. 2007. Congenital heart defects and fetal alcohol spectrum disorders. Congenit Heart Disease 2:250-255.
14. Cavieres MF, Smith SM. 2000. Genetic and developmental modulation of cardiac deficits in prenatal alcohol exposure. Alcoholism Clin Exp Res 24:102-109.
15. Chernyavskaya Y, Ebert AM, Milligan E, Garrity DM. 2012. Voltage-gated calcium channel CACNB2 (beta2.1) protein is required in the heart for control of cell proliferation and heart tube integrity. Dev Dyn 241:648-662.
16. Clendenon SG, Sarmah S, Shah B, Liu Q, Marrs JA. 2012. Zebrafish cadherin-11 participates in retinal differentiation and retinotectal axon projection during visual system development. Dev Dyn 241:442-454.
17. Daft PA, Johnston MC, Sulik KK. 1986. Abnormal heart and great vessel development following acute ethanol exposure in mice. Teratology 33:93-104.
18. Dlugos CA, Rabin RA. 2010. Structural and functional effects of developmental exposure to ethanol on the zebrafish heart. Alcoholism Clin Exp Res 34:1013-1021.
19. Duester G. 1991. A hypothetical mechanism for fetal alcohol syndrome involving ethanol inhibition of retinoic acid synthesis at the alcohol dehydrogenase step. Alcoholism Clin Exp Res 15:568-572.
20. Fang TT, Bruyere HJ Jr, Kargas SA, Nishikawa T, Takagi Y, Gilbert EF. 1987. Ethyl alcohol-induced cardiovascular malformations in the chick embryo. Teratology 35:95-103.
21. Garro AJ, McBeth DL, Lima V, Lieber CS. 1991. Ethanol consumption inhibits fetal DNA methylation in mice: implications for the fetal alcohol syndrome. Alcoholism Clin Exp Res 15:395-398.
22. Hamid A, Kaur J. 2007. Long-term alcohol ingestion alters the folate-binding kinetics in intestinal brush border membrane in experimental alcoholism. Alcohol 41:441-446.
23. Hochgreb T, Linhares VL, Menezes DC, Sampaio AC, Yan CY, Cardoso WV, Rosenthal N, Xavier-Neto J. 2003. A caudorostral wave of RALDH2 conveys anteroposterior information to the cardiac field. Development 130:5363-5374.
24. Hutson JR, Stade B, Lehotay DC, Collier CP, Kapur BM. 2012. Folic acid transport to the human fetus is decreased in pregnancies with chronic alcohol exposure. PLoS One 7:e38057.
25. Ibrahim W, Tousson E, El-Masry T, Arafa N, Akela M. 2012. The effect of folic acid as an antioxidant on the hypothalamic monoamines in experimentally induced hypothyroid rat. Toxicol Indust Health 28:253-261.
26. Ionescu-Ittu R, Marelli AJ, Mackie AS, Pilote L. 2009. Prevalence of severe congenital heart disease after folic acid fortification of grain products: time trend analysis in Quebec, Canada. BMJ 338:b1673.
27. Johnson CS, Zucker RM, Hunter ES, Sulik KK. 2007. Perturbation of retinoic acid (RA)-mediated limb development suggests a role for diminished RA signaling in the teratogenesis of ethanol. Birth Defects Res A Clin Mol Teratol 79:631-641.
28. Joshi R, Adhikari S, Patro BS, Chattopadhyay S, Mukherjee T. 2001. Free radical scavenging behavior of folic acid: evidence for possible antioxidant activity. Free Radical Biol Med 30:1390-1399.
29. Kaminen-Ahola N, Ahola A, Maga M, Mallitt KA, Fahey P, Cox TC, Whitelaw E, Chong S. 2010. Maternal ethanol consumption alters the epigenotype and the phenotype of offspring in a mouse model. PLoS Genet 6:e1000811.
30. Kashyap B, Frey RA, Stenkamp DL. 2011. Ethanol-induced microphthalmia is not mediated by changes in retinoic acid or sonic hedgehog signaling during retinal neurogenesis. Alcohol Clin Exp Res 35:1644-1661.
31. Keegan BR, Feldman JL, Begemann G, Ingham PW, Yelon D. 2005. Retinoic acid signaling restricts the cardiac progenitor pool. Science 307:247-249.
32. Klingenberg CP, Wetherill L, Rogers J, Moore E, Ward R, Autti-Ramo I, Fagerlund A, Jacobson SW, Robinson LK, Hoyme HE, Mattson SN, Li TK, Riley EP, Foroud T. 2010. Prenatal alcohol exposure alters the patterns of facial asymmetry. Alcohol 44:649-657.
33. Lazic S, Scott IC. 2011. Mef2cb regulates late myocardial cell addition from a second heart field-like population of progenitors in zebrafish. Dev Biol 354:123-133.
34. Lee MS, Bonner JR, Barnard DJ, Sanchez EL, Sause ET, Prentice RR, Burgess SM, Brody LC. 2012. Disruption of the folate pathway in zebrafish causes developmental defects. BMC Dev Biol 12:12.
35. Lieber CS. 2003. Relationships between nutrition, alcohol use, and liver disease. Alcohol Res Health 27:220-231.
36. Lin CJ, Lin CY, Chen CH, Zhou B, Chang CP. 2012. Partitioning the heart: mechanisms of cardiac septation and valve development. Development 139:3277-3299.
37. Liu Y, Balaraman Y, Wang G, Nephew KP, Zhou FC. 2009. Alcohol exposure alters DNA methylation profiles in mouse embryos at early neurulation. Epigenetics 4:500-511.
38. Marrs JA, Clendenon SG, Ratcliffe DR, Fielding SM, Liu Q, Bosron WF. 2010. Zebrafish fetal alcohol syndrome model: effects of ethanol are rescued by retinoic acid supplement. Alcohol 44:707-715.
39. Mitchell JJ, Paiva M, Heaton MB. 1999. The antioxidants vitamin E and beta-carotene protect against ethanol-induced neurotoxicity in embryonic rat hippocampal cultures. Alcohol 17:163-168.
40. Muralidharan P, Sarmah S, Zhou FC, Marrs JA. 2013. Fetal alcohol spectrum disorder (FASD) associated neural defects: Complex mechanisms and potential therapeutic targets. Brain Sciences 3:964-991.
41. Niederreither K, Vermot J, Messaddeq N, Schuhbaur B, Chambon P, Dolle P. 2001. Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse. Development 128:1019-1031
42. Pullarkat RK. 1991. Hypothesis: prenatal ethanol-induced birth defects and retinoic acid. Alcoholism Clin Exp Res 15:565-567.
43. Riikonen R, Salonen I, Partanen K, Verho S. 1999. Brain perfusion SPECT and MRI in foetal alcohol syndrome. Dev Med Child Neurol 41:652-659.
44. Ryckebusch L, Wang Z, Bertrand N, Lin SC, Chi X, Schwartz R, Zaffran S, Niederreither K. 2008. Retinoic acid deficiency alters second heart field formation. Proc Natl Acad Sci USA 105:2913-2918.
45. Sarmah S, Barrallo-Gimeno A, Melville DB, Topczewski J, Solnica-Krezel L, Knapik EW. 2010. Sec24D-dependent transport of extracellular matrix proteins is required for zebrafish skeletal morphogenesis. PloS One 5:e10367.
46. Sarmah S, Muralidharan P, Curtis CL, McClintick JN, Buente BB, Holdgrafer DJ, Ogbeifun O, Olorungbounmi OC, Patino L, Lucas R, Gilbert S, Groninger ES, Arciero J, Edenberg HJ, Marrs JA. In Press. Ethanol exposure disrupts extraembryonic microtubule cytoskeleton and embryonic blastomere cell adhesion, producing epiboly and gastrulation defects. Biology Open.
47. Serrano M, Han M, Brinez P, Linask KK. 2010. Fetal alcohol syndrome: cardiac birth defects in mice and prevention with folate. Am J Obstet Gynecol 203:75e77-75e15.
48. Sirbu IO, Zhao X, Duester G. 2008. Retinoic acid controls heart anteroposterior patterning by down-regulating Isl1 through the Fgf8 pathway. Dev Dyn 237:1627-1635.
49. Stainier DY. 2001. Zebrafish genetics and vertebrate heart formation. Nature Rev Genet 2:39-48.
50. Staudt D, Stainier D. 2012. Uncovering the molecular and cellular mechanisms of heart development using the zebrafish. Annu Rev Genet.
51. Strandberg-Larsen K, Skov-Ettrup LS, Gronbaek M, Andersen AM, Olsen J, Tolstrup J. 2011. Maternal alcohol drinking pattern during pregnancy and the risk for an offspring with an isolated congenital heart defect and in particular a ventricular septal defect or an atrial septal defect. Birth Defects Res A 91:616-622.
52. Thisse CT. 2005.High throughput expression analysis of ZF-models consortium clones. ZFIN Direct Data Submission (http://zfin.org.)
53. Twal OW, Zile MH. 1997. Retinoic acid reverses ethanol-induced cardiovascular abnormalities in quail embryos. Alcohol Clin Exp Res 21:1137-1143.
54. Waxman JS, Keegan BR, Roberts RW, Poss KD, Yelon D. 2008. Hoxb5b acts downstream of retinoic acid signaling in the forelimb field to restrict heart field potential in zebrafish. Dev Cell 15:923-934.
55. Webster WS, Germain MA, Lipson A, Walsh D. 1984. Alcohol and congenital heart defects: an experimental study in mice. Cardiovasc Res 18:335-338.
56. Westerfield M. 2000. The zebrafish book. Eugene, OR: The University of Oregon Press.
57. Xavier-Neto J, Rosenthal N, Silva FA, Matos TG, Hochgreb T, Linhares VL. 2001. Retinoid signaling and cardiac anteroposterior segmentation. Genesis 31:97-104.
58. Yelin R, Schyr RB, Kot H, Zins S, Frumkin A, Pillemer G, Fainsod A. 2005. Ethanol exposure affects gene expression in the embryonic organizer and reduces retinoic acid levels. Dev Biol 279:193-204.
59. Zachman RD, Grummer MA. 1998. The interaction of ethanol and vitamin A as a potential mechanism for the pathogenesis of Fetal Alcohol syndrome. Alcoholism: Clin Exp Res 22:1544-1556.
60. Zhang Y, Shao M, Wang L, Liu Z, Gao M, Liu C, Zhang H. 2010. Ethanol exposure affects cell movement during gastrulation and induces split axes in zebrafish embryos. Int J Dev Neurosci 28:283-288.
61. Zhou FC, Balaraman Y, Teng M, Liu Y, Singh RP, Nephew KP. 2011a. Alcohol alters DNA methylation patterns and inhibits neural stem cell differentiation. Alcohol Clin Exp Res 35:735-746.
62. Zhou Y, Cashman TJ, Nevis KR, Obregon P, Carney SA, Liu Y, Gu A, Mosimann C, Sondalle S, Peterson RE, Heideman W, Burns CE, Burns CG. 2011b. Latent TGF-beta binding protein 3 identifies a second heart field in zebrafish. Nature 474:645-648.