Ah receptor activation by dioxin disrupts activin, BMP, and WNT signals during the early differentiation of mouse embryonic stem cells and inhibits cardiomyocyte functions

Toxicological Sciences

Volumn 149, Issue 2, 2016, Pages 346-357

  Wang, Qin ^a   Hisaka, Kurita ^a,b   Carreira, Vinicius ^a   Ko, Chia I ^a   Fan, Yunxia ^a   Zhang, Xiang ^a   Biesiada, Jacek ^a   Medvedovic, Mario ^a   Puga, Alvaro ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b GIFU PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

Aryl hydrocarbon receptor; cardiomyogenesis; differentiation; dioxin; embryonic stem cells; mitochondrial dysfunction

Indexed keywords

ACTIVIN A; AROMATIC HYDROCARBON RECEPTOR; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; DIOXIN; NOGGIN; TRANSFORMING GROWTH FACTOR BETA; WNT3A PROTEIN; WNT5A PROTEIN; ACTIVIN; BONE MORPHOGENETIC PROTEIN; POLYCHLORINATED DIBENZODIOXIN; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE DOSAGE; GENE EXPRESSION; HEART MUSCLE CONTRACTILITY; MOUSE EMBRYONIC STEM CELL; NONHUMAN; ONTOGENY; PHENOTYPE; PROTEIN SECRETION; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE CELL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; HEART CONTRACTION; MITOCHONDRION; MOUSE; PHYSIOLOGY;

ACTIVINS; ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MOUSE EMBRYONIC STEM CELLS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; POLYCHLORINATED DIBENZODIOXINS; RECEPTORS, ARYL HYDROCARBON; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84960099337     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfv246     Document Type: Article

References (64)

1. Abbott, B. D., Birnbaum, L. S., and Perdew, G. H. (1995). Developmental expression of two members of a new class of transcription factors: I. Expression of aryl hydrocarbon receptor in the C57BL/6N mouse embryo. Dev. Dyn. 204, 133-143.
2. Aly, H. A., and Domenech, O. (2009). Cytotoxicity and mitochondrial dysfunction of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) in isolated rat hepatocytes. Toxicol. Lett. 191, 79-87.
3. Anders, S., and Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biol. 11, R106.
4. Aragon, A. C., Kopf, P. G., Campen, M. J., Huwe, J. K., and Walker, M. K. (2008). In utero and lactational 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin exposure: effects on fetal and adult cardiac gene expression and adult cardiac and renal morphology. Toxicol. Sci. 101, 321-330.
5. Barker, D. J. (2007). The origins of the developmental origins theory. J. Intern. Med. 261, 412-417.
6. Biswas, G., Srinivasan, S., Anandatheerthavarada, H. K., and Avadhani, N. G. (2008). Dioxin-mediated tumor progression through activation of mitochondria-to-nucleus stress signaling. Proc. Natl. Acad. Sci. U. S. A. 105, 186-191.
7. Chen, S. C., Liao, T. L., Wei, Y. H., Tzeng, C. R., and Kao, S. H. (2010). Endocrine disruptor, dioxin (TCDD)-induced mitochondrial dysfunction and apoptosis in human trophoblastlike JAR cells. Mol. Hum. Reprod. 16, 361-372.
8. Chien, K. R. (2000). Genomic circuits and the integrative biology of cardiac diseases. Nature 407, 227-232.
9. Cohen, E. D., Tian, Y., and Morrisey, E. E. (2008). Wnt signaling: an essential regulator of cardiovascular differentiation, morphogenesis and progenitor self-renewal. Development 135, 789-798.
10. Damstra, T. (2002). Potential effects of certain persistent organic pollutants and endocrine disrupting chemicals on the health of children. J. Toxicol. Clin. Toxicol. 40, 457-465.
11. Doetschman, T., Gregg, R. G., Maeda, N., Hooper, M. L., Melton, D. W., Thompson, S., and Smithies, O. (1987). Targetted correction of a mutant HPRT gene in mouse embryonic stem cells. Nature 330, 576-578.
12. Dummer, T. J., Dickinson, H. O., and Parker, L. (2003). Adverse pregnancy outcomes around incinerators and crematoriums in Cumbria, north west England, 1956-93. J. Epidemiol. Commun. Health 57, 456-461.
13. Fukuda, K., and Yuasa, S. (2006). Stem cells as a source of regenerative cardiomyocytes. Circ. Res. 98, 1002-1013.
14. Gessert, S., and Kuhl, M. (2010). The multiple phases and faces of wnt signaling during cardiac differentiation and development. Circ. Res. 107, 186-199.
15. Godoy, J. A., Arrazola, M. S., Ordenes, D., Silva-Alvarez, C., Braidy, N., and Inestrosa, N. C. (2014). Wnt-5a ligand modulates mitochondrial fission-fusion in rat hippocampal neurons. J. Biol. Chem. 289, 36179-36193.
16. Gonzalez, F. J., and Fernandez-Salguero, P. (1998). The aryl hydrocarbon receptor: studies using the AHR-null mice. Drug Metab. Dispos. 26, 1194-1198.
17. Gu, Y. Z., Hogenesch, J. B., and Bradfield, C. A. (2000). The PAS superfamily: Sensors of environmental and developmental signals. Annu. Rev. Pharmacol. Toxicol. 40, 519-561.
18. Guo, X. and Wang, X. F. (2009). Signaling cross-talk between TGFbeta/BMP and other pathways. Cell Res. 19, 71-88.
19. Handley-Goldstone, H. M., Grow, M. W., and Stegeman, J. J. (2005). Cardiovascular gene expression profiles of dioxin exposure in zebrafish embryos. Toxicol. Sci. 85, 683-693.
20. Hogan, B. L. (1996). Bone morphogenetic proteins in development. Curr. Opin. Genet. Dev. 6, 432-438.
21. Hogan, B. L. (1996). Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594.
22. Ivnitski-Steele, I. D., Friggens, M., Chavez, M., and Walker, M. K. (2005). 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) inhibition of coronary vasculogenesis is mediated, in part, by reduced responsiveness to endogenous angiogenic stimuli, including vascular endothelial growth factor A (VEGF-A). Birth. Defects. Res. A Clin. Mol. Teratol. 73, 440-446.
23. Kattman, S. J., Witty, A. D., Gagliardi, M., Dubois, N. C., Niapour, M., Hotta, A., Ellis, J., and Keller, G. (2011). Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell 8, 228-240.
24. Keller, G. M. (1995). In vitro differentiation of embryonic stem cells. Curr. Opin. Cell. Biol. 7, 862-869.
25. Kennedy, L. H., Sutter, C. H., Leon Carrion, S., Tran, Q. T., Bodreddigari, S., Kensicki, E., Mohney, R. P., and Sutter, T. R. (2013). 2, 3, 7, 8-Tetrachlorodibenzo-p-dioxin-mediated production of reactive oxygen species is an essential step in the mechanism of action to accelerate human keratinocyte differentiation. Toxicol. Sci. 132, 235-249.
26. Kim, H. Y., Kim, H. R., Kang, M. G., Trang, N. T., Baek, H. J., Moon, J. D., Shin, J. H., Suh, S. P., Ryang, D. W., Kook, H., et al. (2014). Profiling of biomarkers for the exposure of polycyclic aromatic hydrocarbons: lamin-A/C isoform 3, poly[ADP-ribose] polymerase 1, and mitochondria copy number are identified as universal biomarkers. Biomed. Res. Int. 2014, 605135.
27. Klug, M. G., Soonpaa, M. H., Koh, G. Y., and Field, L. J. (1996). Genetically selected cardiomyocytes from differentiating embronic stem cells form stable intracardiac grafts. J. Clin. Invest. 98, 216-224.
28. Kopf, P. G., and Walker, M. K. (2009). Overview of developmental heart defects by dioxins, PCBs, and pesticides. J. Environ. Sci. Health. C Environ. Carcinog. Ecotoxicol. Rev. 27, 276-285.
29. Kuehl, K. S., and Loffredo, C. A. (2006). A cluster of hypoplastic left heart malformation in Baltimore, Maryland. Pediatr. Cardiol. 27, 25-31.
30. Laflamme, M. A., and Murry, C. E. (2011). Heart regeneration. Nature 473, 326-335.
31. Lanham, K. A., Peterson, R. E., and Heideman, W. (2012). Sensitivity to dioxin decreases as zebrafish mature. Toxicol. Sci. 127, 360-370.
32. Lian, X., Zhang, J., Azarin, S. M., Zhu, K., Hazeltine, L. B., Bao, X., Hsiao, C., Kamp, T. J., and Palecek, S. P. (2013). Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/beta-catenin signaling under fully defined conditions. Nat. Protoc. 8, 162-175.
33. Liu, W., and Foley, A. C. (2011). Signaling pathways in early cardiac development. Wiley Interdiscip Rev. Syst. Biol. Med. 3, 191-205.
34. Lund, A. K., Goens, M. B., Kanagy, N. L. and Walker, M. K. (2003). Cardiac hypertrophy in aryl hydrocarbon receptor null mice is correlated with elevated angiotensin II, endothelin-1, and mean arterial blood pressure. Toxicol. Appl. Pharmacol. 193, 177-187.
35. Morgan, M., Anders, S., Lawrence, M., Aboyoun, P., Pages, H., and Gentleman, R. (2009). ShortRead: a bioconductor package for input, quality assessment and exploration of highthroughput sequence data. Bioinformatics 25, 2607-2608.
36. Park, W. H., Jun, D. W., Kim, J. T., Jeong, J. H., Park, H., Chang, Y. S., Park, K. S., Lee, H. K., and Pak, Y. K. (2013). Novel cell-based assay reveals associations of circulating serum AhR-ligands with metabolic syndrome and mitochondrial dysfunction. Biofactors 39, 494-504.
37. Pavanello, S., Dioni, L., Hoxha, M., Fedeli, U., Mielzynska-Svach, D., and Baccarelli, A. A. (2013). Mitochondrial DNA copy number and exposure to polycyclic aromatic hydrocarbons. Cancer Epidemiol. Biomarkers. Prev. 22, 1722-1729.
38. Pereira, S. P., Pereira, G. C., Pereira, C. V., Carvalho, F. S., Cordeiro, M. H., Mota, P. C., Ramalho-Santos, J., Moreno, A. J., and Oliveira, P. J. (2013). Dioxin-induced acute cardiac mitochondrial oxidative damage and increased activity of ATPsensitive potassium channels in Wistar rats. Environ. Pollut. 180, 281-290.
39. Peterson, R. E., Theobald, H. M., and Kimmel, G. L. (1993). Developmental and reproductive toxicity of dioxins and related compounds: cross-species comparisons. Crit. Rev. Toxicol. 23, 283-335.
40. Plavicki, J., Hofsteen, P., Peterson, R. E., and Heideman, W. (2013). Dioxin inhibits zebrafish epicardium and proepicardium development. Toxicol. Sci. 131, 558-567.
41. Puga, A. (2011). Perspectives on the potential involvement of the AH receptor-dioxin axis in cardiovascular disease. Toxicol. Sci. 120, 256-261.
42. Rajala, K., Pekkanen-Mattila, M., and Aalto-Setala, K. (2011). Cardiac differentiation of pluripotent stem cells. Stem Cells Int. 2011, 383709.
43. Sartor, M. A., Schnekenburger, M., Marlowe, J. L., Reichard, J. F., Wang, Y., Fan, Y., Ma, C., Karyala, S., Halbleib, D., Liu, X., et al. (2009). Genomewide analysis of aryl hydrocarbon receptor binding targets reveals an extensive array of gene clusters that control morphogenetic and developmental programs. Environ. Health. Perspect. 117, 1139-1146.
44. Schneider, A. J., Branam, A. M., and Peterson, R. E. (2014). Intersection of AHR and Wnt signaling in development, health, and disease. Int. J. Mol. Sci. 15, 17852-17885.
45. Schnekenburger, M., Peng, L., and Puga, A. (2007). HDAC1 bound to the Cyp1a1 promoter blocks histone acetylation associated with Ah receptor-mediated trans-activation. Biochim. Biophys. Acta 1769, 569-578.
46. Schott, J. J., Benson, D. W., Basson, C. T., Pease, W., Silberbach, G. M., Moak, J. P., Maron, B. J., Seidman, C. E., and Seidman, J. G. (1998). Congenital heart disease caused by mutations in the transcription factor NKX2-5. Science 281, 108-111.
47. Schultheiss, T. M., Burch, J. B., and Lassar, A. B. (1997). A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 11, 451-462.
48. Selevan, S. G., Kimmel, C. A., and Mendola, P. (2000). Identifying critical windows of exposure for children's health. Environ. Health. Perspect. 108(Suppl 3), 451-455.
49. Serrat, R., Lopez-Domenech, G., Mirra, S., Quevedo, M., Garcia-Fernandez, J., Ulloa, F., Burgaya, F., and Soriano, E. (2013). The non-canonical Wnt/PKC pathway regulates mitochondrial dynamics through degradation of the arm-like domaincontaining protein Alex3. PLoS One 8, e67773.
50. Shertzer, H. G., Genter, M. B., Shen, D., Nebert, D. W., Chen, Y., and Dalton, T. P. (2006). TCDD decreases ATP levels and increases reactive oxygen production through changes in mitochondrial F(0)F(1)-ATP synthase and ubiquinone. Toxicol. Appl. Pharmacol. 217, 363-374.
51. Smith, A. G. (2001). Embryo-derived stem cells: of mice and men. Annu. Rev. Cell Dev. Biol. 17, 435-462.
52. Spikings, E. C., Alderson, J., and St John, J. C. (2007). Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development. Biol. Reprod. 76, 327-335.
53. Srivastava, D., and Olson, E. N. (2000). A genetic blueprint for cardiac development. Nature 407, 221-226.
54. Stites, T., Storms, D., Bauerly, K., Mah, J., Harris, C., Fascetti, A., Rogers, Q., Tchaparian, E., Satre, M., and Rucker, R. B. (2006). Pyrroloquinoline quinone modulates mitochondrial quantity and function in mice. J. Nutr. 136, 390-396.
55. Ten Berge, D., Koole, W., Fuerer, C., Fish, M., Eroglu, E., and Nusse, R. (2008). Wnt signaling mediates self-organization and axis formation in embryoid bodies. Cell StemCell 3, 508-518.
56. Thackaberry, E. A., Nunez, B. A., Ivnitski-Steele, I. D., Friggins, M., and Walker, M. K. (2005). Effect of 2, 3, 7, 8-tetrachlorodibenzop-dioxin on murine heart development: alteration in fetal and postnatal cardiac growth, and postnatal cardiac chronotropy. Toxicol. Sci. 88, 242-249.
57. Thundathil, J., Filion, F., and Smith, L. C. (2005). Molecular control of mitochondrial function in preimplantation mouse embryos. Mol. Reprod. Dev. 71, 405-413.
58. Trapnell, C., Pachter, L., and Salzberg, S. L. (2009). TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111.
59. Walker, M. K., and Catron, T. F. (2000). Characterization of cardiotoxicity induced by 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin and related chemicals during early chick embryo development. Toxicol. Appl. Pharmacol. 167, 210-221.
60. Wang, Q., Chen, J., Ko, C. I., Fan, Y., Carreira, V., Chen, Y., Xia, Y., Medvedovic, M., and Puga, A. (2013). Disruption of aryl hydrocarbon receptor homeostatic levels during embryonic stem cell differentiation alters expression of homeobox transcription factors that control cardiomyogenesis. Environ. Health. Perspect. 121, 1334-1343.
61. Wang, Y., Fan, Y., and Puga, A. (2010). Dioxin exposure disrupts the differentiation of mouse embryonic stem cells into cardiomyocytes. Toxicol. Sci. 115, 225-237.
62. Wang, Z., Shu, W., Lu, M. M., and Morrisey, E. E. (2005). Wnt7b activates canonical signaling in epithelial and vascular smooth muscle cells through interactions with Fzd1, Fzd10, and LRP5. Mol. Cell Biol. 25, 5022-5030.
63. Yamashita, J. K., Takano, M., Hiraoka-Kanie, M., Shimazu, C., Peishi, Y., Yanagi, K., Nakano, A., Inoue, E., Kita, F., and Nishikawa, S. (2005). Prospective identification of cardiac progenitors by a novel single cell-based cardiomyocyte induction. FASEB J. 19, 1534-1536.
64. Zaher, H., Fernandez-Salguero, P. M., Letterio, J., Sheikh, M. S., Fornace, A. J., Jr, Roberts, A. B., and Gonzalez, F. J. (1998). The involvement of aryl hydrocarbon receptor in the activation of transforming growth factor-beta and apoptosis. Mol. Pharmacol. 54, 313-321.