The differentiation of cardiomyocytes from mouse embryonic stem cells is altered by dioxin

Toxicology Letters

Volumn 202, Issue 3, 2011, Pages 226-236

  Neri, Tui ^a,e   Merico, Valeria ^a,b   Fiordaliso, Fabio ^c   Salio, Monica ^c   Rebuzzini, Paola ^a   Sacchi, Lucia ^a   Bellazzi, Riccardo ^a   Redi, Carlo Alberto ^a,b   Zuccotti, Maurizio ^d   Garagna, Silvia ^a  

^a UNIVERSITY OF PAVIA   (Italy)

^b FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^c MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^d UNIVERSITY OF PARMA   (Italy)

^e Parc Scientifique de Luminy   (France)

Author keywords

Cardiomyocytes differentiation; Dioxin; Embryonic stem cells; Mouse; Myofibrils

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ADENOSINE TRIPHOSPHATE; ALPHA ACTININ; ALPHA KINASE 3; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 1B1; GLUCURONOSYLTRANSFERASE 1A6; GLUTATHIONE TRANSFERASE A1; MYOSIN HEAVY CHAIN BETA; PHOSPHOTRANSFERASE; TROPONIN C; TROPONIN I; TROPONIN T; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; EMBRYONIC STEM CELL; HEART MUSCLE CELL; IMMUNOHISTOCHEMISTRY; MESODERM; MICROARRAY ANALYSIS; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; SARCOMERE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL DIFFERENTIATION; CELL LINE; DOWN-REGULATION; EMBRYOID BODIES; EMBRYONIC STEM CELLS; ENVIRONMENTAL POLLUTANTS; ENZYMES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; METABOLIC DETOXICATION, PHASE I; METABOLIC DETOXICATION, PHASE II; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; MYOCYTES, CARDIAC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TERATOGENS; TETRACHLORODIBENZODIOXIN; TRANSCRIPTION, GENETIC;

EID: 79954572856     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2011.02.008     Document Type: Article

References (41)

1. Antkiewicz D., Burns C., Carney S., Peterson R., Heideman W. Heart malformation is an early response to TCDD in embryonic zebrafish. Toxicol. Sci. 2005, 84:368-377.
2. Arzuaga X., Reiterer G., Majkova Z., Kilgore M., Toborek M., Hennig B. PPARalpha ligands reduce PCB-induced endothelial activation: possible interactions in inflammation and atherosclerosis. Cardiovasc. Toxicol. 2007, 7:264-272.
3. Barouki R., Coumoul X., Fernandez-Salguero P.M. The aryl hydrocarbon receptor, more than a xenobiotic-interacting protein. FEBS Lett. 2007, 581:3608-3615.
4. Bock K.W., Köhle C. Ah receptor: dioxin-mediated toxic responses as hints to deregulated physiologic functions. Biochem. Pharmacol. 2006, 72:393-404.
5. Boheler K., Czyz J., Tweedie D., Yang H., Anisimov S., Wobus A. Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ. Res. 2002, 91:189-201.
6. Chung S., Dzeja P.P., Faustino R.S., Perez-Terzic C., Behfar A., Terzic A. Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat. Clin. Pract. Cardiovasc. Med. 2007, 4(Suppl. 1):S60-67.
7. Dalton T., Kerzee J., Wang B., Miller M., Dieter M., Lorenz J., Shertzer H., Nerbert D., Puga A. Dioxin exposure is an environmental risk factor for ischemic heart disease. Cardiovasc. Toxicol. 2001, 1:285-298.
8. Goldstone H., Stegeman J. Molecular mechanisms of 2,3,7,8-tetrachlorodibenzo-p-dioxin cardiovascular embryotoxicity. Drug Metab. Rev. 2006, 38:261-289.
9. Hosoda T., Monzen K., Hiroi Y., Oka T., Takimoto E., Yazaki Y., Nagai R., Komuro I. A novel myocyte-specific gene Midori promotes the differentiation of P19CL6 cells into cardiomyocytes. J. Biol. Chem. 2001, 276:35978-35989.
10. Ivnitski I., Elmaoued R., Walker M. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) inhibition of coronary development is preceded by a decrease in myocyte proliferation and an increase in cardiac apoptosis. Teratology 2001, 64:201-212.
11. Jokinen M., Walker N., Brix A., Sells D., Haseman J., Nyska A. Increase in cardiovascular pathology in female Sprague-Dawley rats following chronic treatment with 2,3,7,8-tetrachlorodibenzo-p-dioxin and 3,3',4,4',5-pentachlorobiphenyl. Cardiovasc. Toxicol. 2003, 3:299-310.
12. Kehat I., Kenyagin-Karsenti D., Snir M., Segev H., Amit M., Gepstein A., Livne E., Binah O., Itskovitz-Eldor J., Gepstein L. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J. Clin. Invest. 2001, 108:407-414.
13. Kelling C., Menahan L., Peterson R. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin treatment on mechanical function of the rat heart. Toxicol. Appl. Pharmacol. 1987, 91:497-501.
14. Kopf P., Huwe J., Walker M. Hypertension, cardiac hypertrophy, and impaired vascular relaxation induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin are associated with increased superoxide. Cardiovasc. Toxicol. 2008, 8:181-193.
15. Korashy H., El-Kadi A. The role of aryl hydrocarbon receptor in the pathogenesis of cardiovascular diseases. Drug Metab. Rev. 2006, 38:411-450.
16. Lind P., Orberg J., Edlund U., Sjöblom L., Lind L. The dioxin-like pollutant PCB 126 (3,3',4,4',5-pentachlorobiphenyl) affects risk factors for cardiovascular disease in female rats. Toxicol. Lett. 2004, 150:293-299.
17. Lund A., Goens M., Kanagy N., Walker M. Cardiac hypertrophy in aryl hydrocarbon receptor null mice is correlated with elevated angiotensin II, endothelin-1, and mean arterial blood pressure. Toxicol. Appl. Pharmacol. 2003, 193:177-187.
18. Lund A., Goens M., Nuñez B., Walker M. Characterizing the role of endothelin-1 in the progression of cardiac hypertrophy in aryl hydrocarbon receptor (AhR) null mice. Toxicol. Appl. Pharmacol. 2006, 212:127-135.
19. Lund A., Peterson S., Timmins G., Walker M. Endothelin-1-mediated increase in reactive oxygen species and NADPH oxidase activity in hearts of aryl hydrocarbon receptor (AhR) null mice. Toxicol. Sci. 2005, 88:265-273.
20. Maltsev V., Rohwedel J., Hescheler J., Wobus A. Embryonic stem cells differentiate in vitro into cardiomyocytes representing sinusnodal, atrial and ventricular cell types. Mech. Dev. 1993, 44:41-50.
21. Mandal P. Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. J. Comp. Physiol. B 2005, 175:221-230.
22. Nebert D. Comparison of gene expression in cell culture to that in the intact animal: relevance to drugs and environmental toxicants. Focus on " development of a transactivator in hepatoma cells that allows expression of phase I, phase II, and chemical defense genes" Am. J. Physiol. Cell Physiol. 2006, 290:C37-41.
23. Nebert D., Roe A., Dieter M., Solis W., Yang Y., Dalton T. Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem. Pharmacol. 2000, 59:65-85.
24. Neri T., Merico V., Garagna S., Redi C., Zuccotti M. Expression of phase I and phase II genes in mouse embryonic stem cells cultured in the presence of 2,3,7,8-tetrachlorodibenzo-para-dioxin. Biochim. Biophys. Acta 2008, 1780:826-836.
25. Nishii K., Morimoto S., Minakami R., Miyano Y., Hashizume K., Ohta M., Zhan D.Y., Lu Q.W., Shibata Y. Targeted disruption of the cardiac troponin T gene causes sarcomere disassembly and defects in heartbeat within the early mouse embryo. Dev. Biol. 2008, 322:65-73.
26. Ohtsuki I., Maruyama K., Ebashi S. Regulatory and cytoskeletal proteins of vertebrate skeletal muscle. Adv. Protein Chem. 1986, 38:1-67.
27. Pucéat M. Protocols for cardiac differentiation of embryonic stem cells. Methods 2008, 45:168-171.
28. Schmidt J., Su G., Reddy J., Simon M., Bradfield C. Characterization of a murine Ahr null allele: involvement of the Ah receptor in hepatic growth and development. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:6731-6736.
29. Schuldiner M., Yanuka O., Itskovitz-Eldor J., Melton D., Benvenisty N. Effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:11307-11312.
30. Stoilov I., Akarsu A., Alozie I., Child A., Barsoum-Homsy M., Turacli M., Or M., Lewis R., Ozdemir N., Brice G., Aktan S., Chevrette L., Coca-Prados M., Sarfarazi M. Sequence analysis and homology modeling suggest that primary congenital glaucoma on 2p21 results from mutations disrupting either the hinge region or the conserved core structures of cytochrome P4501B1. Am. J. Hum. Genet. 1998, 62:573-584.
31. Stoilov I., Rezaie T., Jansson I., Schenkman J., Sarfarazi M. Expression of cytochrome P4501b1 (Cyp1b1) during early murine development. Mol. Vis. 2004, 10:629-636.
32. Thackaberry E., Gabaldon D., Walker M., Smith S. Aryl hydrocarbon receptor null mice develop cardiac hypertrophy and increased hypoxia-inducible factor-1alpha in the absence of cardiac hypoxia. Cardiovasc. Toxicol. 2002, 2:263-274.
33. Thackaberry E., Jiang Z., Johnson C., Ramos K., Walker M. Toxicogenomic profile of 2,3,7,8-tetrachlorodibenzo-p-dioxin in the murine fetal heart: modulation of cell cycle and extracellular matrix genes. Toxicol. Sci. 2005, 88:231-241.
34. Thackaberry E., Nunez B., Ivnitski-Steele I., Friggins M., Walker M. Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on murine heart development: alteration in fetal and postnatal cardiac growth, and postnatal cardiac chronotropy. Toxicol. Sci. 2005, 88:242-249.
35. Wang Y., Fan Y., Puga A. Dioxin exposure disrupts the differentiation of mouse embryonic stem cells into cardiomyocytes. Toxicol. Sci. 2010, 115:225-237.
36. Wobus A., Guan K., Yang H., Boheler K. Embryonic stem cells as a model to study cardiac, skeletal muscle, and vascular smooth muscle cell differentiation. Methods Mol. Biol. 2002, 185:127-156.
37. Xie A., Walker N., Wang D. Dioxin (2,3,7,8-tetrachlorodibenzo-p-dioxin) enhances triggered after depolarizations in rat ventricular myocytes. Cardiovasc. Toxicol. 2006, 6:99-110.
38. Xu R., Chen X., Li D., Li R., Addicks G., Glennon C., Zwaka T., Thomson J. BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat. Biotechnol. 2002, 20:1261-1264.
39. Yano S., Miake J., Mizuta E., Manabe K., Bahrudin U., Morikawa K., Arakawa K., Sasaki N., Igawa O., Shigemasa C., Yamamoto Y., Morisaki T., Hidaka K., Kurata Y., Yoshida A., Shiota G., Higaki K., Ninomiya H., Lee J.K., Shirayoshi Y., Hisatome I. Changes of HCN gene expression and I(f) currents in Nkx2.5-positive cardiomyocytes derived from murine embryonic stem cells during differentiation. Biomed. Res. 2008, 29:195-203.
40. Yeager R., Oleske D., Millsap D., Henshel D. Severe craniofacial malformations resulting from developmental exposure to dioxin. Reprod. Toxicol. 2006, 22:811-812.
41. zur Nieden N., Kempka G., Ahr H. Molecular multiple endpoint embryonic stem cell test-a possible approach to test for the teratogenic potential of compounds. Toxicol. Appl. Pharmacol. 2004, 194:257-269.