Short-time glucose exposure of embryonic carcinoma cells impairs their function as terminally differentiated cardiomyocytes

Biochemical and Biophysical Research Communications

Volumn 420, Issue 2, 2012, Pages 230-235

  Knelangen, Julia M ^a   Kurz, Randy ^b   Schagdarsurengin, Undraga ^c   Fischer, Bernd ^a   Navarrete Santos, Anne ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Cardiac differentiation; CpG methylation; Glucose; P19 embryonic carcinoma cells

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; GLUCOSE; GLUCOSE TRANSPORTER 4; INSULIN RECEPTOR; SOMATOMEDIN C RECEPTOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL DAMAGE; CELL DIFFERENTIATION; CELL MATURATION; CELL STRUCTURE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DNA METHYLATION; EMBRYOID BODY; EMBRYONAL CARCINOMA STEM CELL; EXPOSURE; GENE EXPRESSION; GENOME IMPRINTING; HEART MUSCLE CELL; IN VITRO STUDY; MARKER GENE; METABOLIC STRESS; MOUSE; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROMOTER REGION; RNA METHYLATION; SHORT TIME GLUCOSE EXPOSURE; TRANSCRIPTION REGULATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE, TUMOR; DNA METHYLATION; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; MICE; MYOCYTES, CARDIAC; MYOSIN HEAVY CHAINS; PLURIPOTENT STEM CELLS; PROMOTER REGIONS, GENETIC; RECEPTOR, IGF TYPE 1; RECEPTOR, INSULIN; VENTRICULAR MYOSINS;

EID: 84859425016     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.02.105     Document Type: Article

References (40)

1. Mcmillen I.C., Robinson J.S. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol. Rev. 2005, 85:571-633.
2. Barker D.J., Hales C.N., Fall C.H., Osmond C., Phipps K., Clark P.M. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 1993, 36:62-67.
3. Waterland R.A., Michels K.B. Epigenetic epidemiology of the developmental origins hypothesis. Annu. Rev. Nutr. 2007, 27:363-388.
4. Fleming T.P., Kwong W.Y., Porter R., Ursell E., Fesenko I., Wilkins A., Miller D.J., Watkins A.J., Eckert J.J. The embryo and its future. Biol. Reprod. 2004, 71:1046-1054.
5. Kwong W., Wild A., Roberts P., Willis A., Fleming T. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development 2000, 127:4195-4202.
6. Kwong W.Y., Miller D.J., Wilkins A.P., Dear M.S., Wright J.N., Osmond C., Zhang J., Fleming T.P. Maternal low protein diet restricted to the preimplantation period induces a gender-specific change on hepatic gene expression in rat fetuses. Mol. Reprod. Dev. 2007, 74:52-60.
7. Ramin N., Thieme R., Fischer S., Schindler M., Schmidt T., Fischer B., Santos A.N. Maternal diabetes impairs gastrulation and insulin and IGF-I receptor expression in rabbit blastocysts. Endocrinology 2010, 151:4158-4167.
8. Rüegg J., Cai W., Karimi M., Kiss N.B., Swedenborg E., Larsson C., Ekström T.J., Pongratz I. Epigenetic regulation of glucose transporter 4 by estrogen receptor β. Mol. Endocrinol. 2011, 25:2017-2028.
9. Rothermel A., Kurz R., Rüffer M., Weigel W., Jahnke H.G., Sedello A.K., Stepan H., Faber R., Schulze-Forster K., Robitzki A.A. Cells on a chip - The use of electric properties for highly sensitive monitoring of blood-derived factors involved in angiotensin II type 1 receptor signalling. Cell. Physiol. Biochem. 2005, 16:51-58.
10. Tonack S., Kind K., Thompson J.G., Wobus A.M., Fischer B., Navarrete Santos A. Dioxin affects glucose transport via the arylhydrocarbon receptor signal cascade in pluripotent embryonic carcinoma cells. Endocrinology 2007, 148:5902-5912.
11. Maltsev V.A., Wobus A.M., Rohwedel J., Bader M., Hescheler J. Cardiomyocytes differentiated in vitro from embryonic stem cells developmentally express cardiac-specific genes and ionic currents. Circ. Res. 1994, 75:233-244.
12. Banach K., Halbach M.D., Hu P., Hescheler J., Egert U. Development of electrical activity in cardiac myocyte aggregates derived from mouse embryonic stem cells. Am. J. Physiol. Heart Circ. Physiol. 2003, 287:H2114-2123.
13. Egert U., Knott T., Schwarz C., Nawrot M., Brandt A., Rotter S., Diesmann M. MEA tools: an open source tool box for the analysis of multi-electrode data with MATLAB. J. Neurosci. Methods 2002, 117:33-42.
14. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162:156-159.
15. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-[delta][delta]CT method. Methods 2001, 25:402-408.
16. Shapiro R., Braverman B., Louis J.B., Servis R.E. Nucleic acid reactivity and conformation. II. Reaction of cytosine and uracil with sodium bisulfite. J. Biol. Chem. 1973, 248:4060-4064.
17. Navarrete Santos A., Tonack S., Kirstein M., Kietz S., Fischer B. Two insulin-responsive glucose transporter isoforms and the insulin receptor are developmentally expressed in rabbit preimplantation embryos. Reproduction 2004, 128:503-516.
18. Rohwedel J., Guan K., Hegert C., Wobus A.M. Embryonic stem cells as an in vitro model for mutagenicity, cytotoxicity and embryotoxicity studies: present state and future prospects. Toxicol. In Vitro 2001, 15:741-753.
19. Skerjanc I.S. Cardiac and skeletal muscle development in P19 embryonal carcinoma cells. Trends Cardiovasc. Med. 1999, 9:139-143.
20. Fijnvandraat A.C., van Ginneken A.C.G., de Boer P.A.J., Ruijter J.M., Christoffels V.M., Moorman A.F.M., Lekanne Deprez R.H. Cardiomyocytes derived from embryonic stem cells resemble cardiomyocytes of the embryonic heart tube. Cardiovasc. Res. 2003, 58:399-409.
21. Watkins A.J., Ursell E., Panton R., Papenbrock T., Hollis L., Cunningham C., Wilkins A., Perry V.H., Sheth B., Kwong W.Y., Eckert J.J., Wild A.E., Hanson M.A., Osmond C., Fleming T.P. Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult onset disease. Biol. Reprod. 2008, 78:299-306.
22. Watkins A.J., Lucas E.S., Torrens C., Cleal J.K., Green L., Osmond C., Eckert J.J., Gray W.P., Hanson M.A., Fleming T.P. Maternal low-protein diet during mouse pre-implantation development induces vascular dysfunction and altered renin-angiotensin-system homeostasis in the offspring. Br. J. Nutr. 2010, 103:1762-1770.
23. Williams C.L., Teeling J.L., Perry V.H., Fleming T.P. Mouse maternal systemic inflammation at the zygote stage causes blunted cytokine responsiveness in lipopolysaccharide-challenged adult offspring. BMC Biol. 2011, 9:49.
24. Clausen T.D., Mathiesen E.R., Hansen T., Pedersen O., Jensen D.M., Lauenborg J., Schmidt L., Damm P. Overweight and the metabolic syndrome in adult offspring of women with diet-treated gestational diabetes mellitus or type 1 diabetes. JCEM 2009, 94:2464-2470.
25. Clausen T.D., Mathiesen E.R., Hansen T., Pedersen O., Jensen D.M., Lauenborg J., Damm P. High prevalence of type 2 diabetes and pre-diabetes in adult offspring of women with gestational diabetes mellitus or type 1 diabetes: the role of intrauterine hyperglycemia. Diabetes Care 2008, 31:340-346.
26. Aerts L., Assche F.A.V. Animal evidence for the transgenerational development of diabetes mellitus. Int. J. Biochem. Cell Biol. 2006, 38:894-903.
27. Reinking B.E., Wedemeyer E.W., Weiss R.M., Segar J.L., Scholz T.D. Cardiomyopathy in offspring of diabetic rats is associated with activation of the MAPK and apoptotic pathways. Cardiovasc. Diabetol. 2009, 8:43.
28. Jovanovic L., Knopp R.H., Kim H., Cefalu W.T., Zhu X., Lee Y.J., Simpson J.L., Mills A.J.L. Elevated pregnancy losses at high and low extremes of maternal glucose in early normal and diabetic pregnancy: evidence for a protective adaptation in diabetes. Diabetes Care 2005, 28:1113-1117.
29. Wyman A., Pinto A.B., Sheridan R., Moley K.H. One-cell zygote transfer from diabetic to nondiabetic mouse results in congenital malformations and growth retardation in offspring. Endocrinology 2008, 149:466-469.
30. Moley K., Chi M., Manchester J., McDougal D., Lowry O. Alterations of intraembryonic metabolites in preimplantation mouse embryos exposed to elevated concentrations of glucose: a metabolic explanation for the developmental retardation seen in preimplantation embryos from diabetic animals. Biol. Reprod. 1996, 54:1209-1216.
31. Fraser R.B., Waite S.L., Wood K.A., Martin K.L. Impact of hyperglycemia on early embryo development and embryopathy: in vitro experiments using a mouse model. Hum. Reprod. 2007, 22:3059-3068.
32. Leppens-Luisier G., Urner F., Sakkas D. Facilitated glucose transporters play a crucial role throughout mouse preimplantation embryo development. Hum. Reprod. 2001, 16:1229-1236.
33. Waterland R.A. Epigenetic mechanisms and gastrointestinal development. J. Pediatr. Nutr. Gastrointest. Tract Dev. Funct. 2006, 149:S137-S142.
34. Blewitt M.E., Vickaryous N.K., Paldi A., Koseki H., Whitelaw E. Dynamic reprogramming of DNA methylation at an epigenetically sensitive allele in mice. PLoS Genet. 2006, 2:e49.
35. Yokomori N., Tawata M., Onaya T. DNA demethylation during the differentiation of 3T3-L1 cells affects the expression of the mouse GLUT4 gene. Diabetes 1999, 48:685-690.
36. Nikoshkov A., Sunkari V.G., Savu O., Forsberg E., Catrina S.-B., Brismar K. Epigenetic DNA methylation in the promoters of the Igf1 receptor and insulin receptor genes in db/db mice. Epigenetics 2011, 6:405-409.
37. Moshe S. The early life environment and the epigenome. Biochim. Biophys. Acta (BBA) - General Subjects 2009, 1790:878-885.
38. Knelangen J.M., van der Hoek M.B., Kong W.-C., Owens J.A., Fischer B., Santos A.N. MicroRNA expression profile during adipogenic differentiation in mouse embryonic stem cells. Physiol. Genomics 2011, 43:611-620.
39. Loffredo C.A., Wilson P.D., Ferencz C. Maternal diabetes: an independent risk factor for major cardiovascular malformations with increased mortality of affected infants. Teratology 2001, 64:98-106.
40. Gardner D.S., Pearce S., Dandrea J., Walker R., Ramsay M.M., Stephenson T., Symonds M.E. Peri-implantation undernutrition programs blunted angiotensin II evoked baroreflex responses in young adult sheep. Hypertension 2004, 43:1290-1296.